Neutrophil as a multifunctional relay in immune system

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Over the last two or three decades, a concept regarding functional capacities of neutrophilic granulocytes has been remarkably extended owing to new technologies. Neutrophil-related effector potential against infectious agents, including phagocytosis, production of reactive oxygen and nitrogen species, degranulation coupled with the released multiple enzymes and antimicrobial peptides, and the extracellular trap formation have been studied in detail. In particular, it was found that many of the factors used by neutrophils to directly destroy pathogens also exert regulatory effects on other immune cells as well as on neutrophils in an autocrine manner. In addition, activated neutrophils are able to de novo synthesize a range of biologically active molecules. Neutrophil-related immunoregulatory effects on macrophages, dendritic cells, T-lymphocytes and B-lymphocytes may be mediated both via direct intercellular contacts and indirectly through production of cytokines and other biologically active mediators. Ambiguous proactive and suppressive neutrophil-related effects on immune cells evidence about their important role played both in homeostasis and diverse pathologies, particularly in developing malignant tumors. Diverse, even opposing impact exhibited by neutrophilic granulocytes on immune cells and cells in non-lymphoid tissues, point at their functional plasticity and, probably, heterogeneity. Upon that, modality of effects elicited by neutrophils largely depends on surrounding microenvironment while they exit from the circulation. Widely considered as an inf lammatory response inducer, neutrophils are able to simultaneously trigger mechanisms facilitating restriction and resolution of inf lammatory reaction. Using intravital microscopy in animal models, it allowed to discover that neutrophils are able to re-enter circulation after exiting into the extravascular space, thereby challenging a classical concept about a unidirectional neutrophil migration from the blood vessels to body tissue. In addition, evidence that neutrophils can serve as antigen-presenting cells for T cells under certain conditions and are recruited from inf lammatory sites to draining lymph nodes were also obtained. Although a body of the data were obtained in vitro or in animal models, which therefore require to be further examined and verified, it may be unequivocally acknowledged that a neutrophil-related impact is not only limited to innate immunity.

About the authors

I. I. Dolgushin

South-Ural State Medical University of the Ministry of Healthcare of the Russian Federation


PhD, MD (Medicine), Professor, President of South-Ural State Medical University, Head of the Department of Microbiology, Virology, Immunology and Clinical Laboratory Diagnostics, South-Ural State Medical University.

454092, Chelyabinsk, Vorovskogo str., 64.

Russian Federation

E A Mezentseva

South-Ural State Medical University of the Ministry of Healthcare of the Russian Federation


PhD (Medicine), Associate Professor, Department of Microbiology, Virology, Immunology and Clinical Laboratory Diagnostics, South-Ural State Medical University.

454092, Chelyabinsk, Vorovskogo str., 64.

Russian Federation

A Yu Savochkina

South-Ural State Medical University of the Ministry of Healthcare of the Russian Federation


Albina Yu. Savochkina - PhD, MD (Medicine), Associate Professor, Professor of the Department of Microbiology, Virology, Immunology and Clinical Laboratory Diagnostics, South-Ural State Medical University.

454092, Chelyabinsk, Vorovskogo str., 64.

Phone: +7 (912) 772-58-06.

Russian Federation, 454092, Челябинск, ул. Воровского, 64.

E K Kuznetsova

Orenburg State Medical University of the Ministry of Healthcare of the Russian Federation

Author for correspondence.

PhD (Medicine), Assistant Professor, Department of Skin and Sexually Transmitted Diseases, Orenburg State Medical University.

Russian Federation


  1. Долгушин И.И., Андреева Ю.С., Савочкина А.Ю. Нейтрофильные внек леточные ловушки и методы оценки функционального статуса нейтрофилов. М.: Издательство РАМН. 2009. 208 с.
  2. Куликов В.А., Гребенников И.Н. Резольвины, протектины и марезины: новые медиаторы воспаления // Вестник Витебского государственного медицинского университета. 2012. Т. 11, № 1. С. 25–30. State Medical University, 2012, vol. 11, no. 1, pp. 25–30. (In Russ.)]
  3. Кунц Т.А., Михайлова Е.С., Маринкин И.О., Вараксин Н.А., Аутеншлюс А.И. Сравнительная оценка продукции цитокинов иммунокомпетентными к летками крови и опухоли в различных возрастных группах больных инвазивным протоковым раком молочной железы // Медицинская иммунология. 2017. Т. 19, № 5. С. 567–576.
  4. Недоспасов С.А. Врож денный иммунитет и его значение для биологии и медицины // Вестник Российской академии наук. 2013. Т. 83, № 9. С. 771–783.
  5. Нестерова И.В., Колесникова Н.В., Чудилова Г.А., Ломтатидзе Л.В., Ковалева С.В., Евглевский А.А. Нейтрофильные гранулоциты: новый взгляд на «старых игроков» на иммунологическом поле // Иммунология. 2015. Т. 36, № 4. С. 257–265.
  6. Нестерова И.В., Колесникова Н.В., Чудилова Г.А., Ломтатидзе Л.В., Ковалева С.В., Евглевский А.А., Нгуен Т.З.Л. Новый взгляд на нейтрофильные гранулоциты: переосмысление старых догм. Часть 1 // Инфекция и иммунитет. 2017. Т. 7, № 3. C. 219–230.
  7. Нестерова И.В., Колесникова Н.В., Чудилова Г.А., Ломтатидзе Л.В., Ковалева С.В., Евглевский А.А., Нгуен Т.З.Л. Новый взгляд на нейтрофильные гранулоциты: переосмысление старых догм. Часть 2 // Инфекция и иммунитет. 2018. Т. 8, № 1. C. 7–18.
  8. Пономарев А.В. Миелоидные супрессорные к летки: общая характеристика // Иммунология. 2016. Т. 37, № 1. С. 47–50.
  9. Потапнев М.П. Молекулярные аспекты распознавания в иммунном и воспалительном ответе // Здравоохранение (Минск). 2014. № 5. С. 18–27.
  10. Сахаров В.Н., Литвицкий П.Ф. Роль различных фенотипов макрофагов в развитии заболеваний человека // Вестник Российской академии медицинских наук. 2015. Т. 70, № 1. С. 26–31.
  11. Сенников С.В., Куликова Е.В., Кнауэр Н.Ю., Хантакова Ю.Н. Молекулярно-к леточные механизмы, опосредуемые дендритными к летками, участвующие в индукции толерантности // Медицинская иммунология. 2017. Т. 19, № 4. С. 359–374.
  12. Талаев В.Ю., Плеханова М.В., Матвеичев А.В. Экспериментальные модели, пригодные для оценки влияния компонентом новых разрабатываемых вакцин на дифференцировку дендритных к леток // Журнал МедиА ль. 2014. № 2 (12). С. 135–153.
  13. Хаитов P.M., Пащенков М.В., Пинегин Б.В. Роль паттерн-распознающих рецепторов во врож дённом и адаптивном иммунитете // Иммунология. 2009. Т. 30, № 1. С. 66–76.
  14. Abadie V., Badell E., Douillard P., Ensergueix D., Leenen P.J., Tanguy M., Fiette L., Saeland S., Gicquel B., Winter N. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood, 2005, vol. 106, no. 5, pp. 1843–1850.
  15. Aldinucci D., Colombatti A. The inf lammatory chemokine CCL5 and cancer progression. Mediators Inflamm., 2014, vol. 2014: 292376, 12 p. doi: 10.1155/2014/292376
  16. Anderson R., Tintinger G.R., Feldman C. Inf lammation and cancer: the role of the human neutrophil. South Africa J. Science, 2014, vol. 110, no. 1/2, 6 p.
  17. Andzinski L., Kasnitz N., Stahnke S., Wu C.F., Gereke M., von Kockritz-Blickwede M., Schilling B., Brandau S., Weiss S., Jablonska J. Type I IFNs induce anti-tumor polarization of tumor associated neutrophils in mice and human. Int. J. Cancer, 2016, vol. 138, no. 8, pp. 1982–1993. doi: 10.1002/ijc.29945
  18. Avondt K.V., Hartl D. Mechanisms and disease relevance of neutrophil extracellular trap formation. Eur. J. Clin. Invest., 2018, e12919. doi: 10.1111/eci.12919
  19. Bank U., Reinhold D., Schneemilch C., Kunz D., Synowitz H.J., Ansorge S. Selective proteolytic cleavage of IL-2 receptor and IL-6 receptor ligand binding chains by neutrophil-derived serine proteases at foci of inf lammation. J. Interferon Cytokine Res., 1999, vol. 19, no. 11, pp. 1277–1287.
  20. Bankey P.E., Banerjee S., Zucchiatti A., De M., Sleem R.W., Lin C.F., Miller-Graziano C.L., De A.K. Cytokine induced expression of programmed death ligands in human neutrophils. Immunol. Lett., 2010, vol. 129, no. 2, pp. 100 –107. doi: 10.1016/j.imlet.2010.01.006
  21. Barrientos L., Bignon A., Gueguen C., de Chaisemartin L., Gorges R., Sandré C., Mascarell L., Balabanian K., Kerdine-Römer S., Pallardy M., Marin-Esteban V., Chollet-Martin S. Neutrophil extracellular traps downregulate lipopolysaccharide-induced activation of monocyte-derived dendritic cells. J. Immunol., 2014, vol. 193, no. 11, pp. 5689–5698. doi: 10.4049/jimmunol.1400586
  22. Basil M.C., Levy B.D. Specialized pro-resolving mediators: endogenous regulators of infection and inf lammation. Nat. Rev. Immunol., 2016, vol. 16, no. 1, pp. 51–67. doi: 10.1038/nri.2015.4
  23. Beauvillain C., Cunin P., Doni A., Scotet M., Jaillon S., Loiry M.L., Magistrelli G., Masternak K., Chevailler A., Delneste Y., Jeannin P. CCR7 is involved in the migration of neutrophils to lymph nodes. Blood, 2011, vol. 117, no. 4, pp. 1196–1204. doi: 10.1182/blood-2009-11-254490
  24. Bekes E.M., Schweighofer B., Kupriyanova T.A., Zajac E., Ardi V.C., Quigley J.P., Deryugina E.I. Tumor-recruited neutrophils and neutrophil TIMP-free MMP-9 regulate coordinately the levels of tumor angiogenesis and efficiency of malignant cell intravasation. Am. J. Pathol., 2011, vol. 179, no. 3, pp.1455–1470. doi: 10.1016/j.ajpath.2011.05.031
  25. Bennouna S., Bliss S.K., Curiel T.J., Denkers E.Y. Cross-talk in the innate immune system: neutrophils instruct recruitment and activation of dendritic cells during microbial infection. J. Immunol., 2003, vol. 171, no. 11, pp. 6052–6058.
  26. Bennouna S., Denkers E.Y. Microbial antigen triggers rapid mobilization of TNF-α to the surface of mouse neutrophils transforming them into inducers of high-level dendritic cell TNF-α production. J. Immunol., 2005, vol. 174, no. 8, pp. 4845–4851.
  27. Berger-Achituv S., Brinkmann V., Abu Abed U., Kühn L.I., Ben-Ezra J., Elhasid R., Zychlinsky A. A proposed role for neutrophil extracellular traps in cancer immunoediting. Front. Immunol., 2013, vol. 4: 48. doi: 10.3389/fimmu.2013.00048
  28. Beyer M., Schultze J.L. Regulatory T cells: major players in the tumor microenvironment. Curr. Pharm. Des., 2009, vol. 15, no. 16, pp. 1879–1892.
  29. Blomgran R., Desvignes L., Briken V., Ernst J.D. Mycobacterium tuberculosis inhibits neutrophil apoptosis, leading to delayed activation of naive CD4 T cells. Cell Host Microbe, 2012, vol. 11, no. 1, pp. 81–90. doi: 10.1016/j.chom.2011.11.012
  30. Blomgran R., Ernst J.D. Lung neutrophils facilitate activation of naive antigen-specific CD4+ T cells during Mycobacterium tuberculosis infection. J. Immunol., 2011, vol. 186, no. 12, pp. 7110 –7119. doi: 10.4049/jimmunol.1100001
  31. Bosurgi L., Cao Y.G., Cabeza-Cabrerizo M., Tucci A., Hughes L.D., Kong Y., Weinstein J.S., Licona-Limon P., Schmid E.T., Pelorosso F., Gagliani N., Craft J.E., Flavell R.A., Ghosh S., Rothlin C.V. Macrophage function in tissue repair and remodeling requires IL-4 or IL-13 with apoptotic cells. Science, 2017, vol. 356, no. 6342, pp. 1072–1076. doi: 10.1126/science.aai8132.
  32. Bronte V., Brandau S., Chen S.H., Colombo M.P., Frey A.B., Greten T.F., Mandruzzato S., Murray P.J., Ochoa A., Ostrand-Rosenberg S., Rodriguez P.C., Sica A., Umansky V., Vonderheide R.H., Gabrilovich D.I. Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat. Commun., 2016, vol. 7: 12150. doi: 10.1038/ncomms12150
  33. Buckley C.D., Ross E.A., McGettrick H.M., Osborne C.E., Haworth O., Schmutz C., Stone P.C., Salmon M., Matharu N.M., Vohra R.K., Nash G.B., Rainger G.E. Identification of a phenotypically and functionally distinct population of longlived neutrophils in a model of reverse endothelial migration. J. Leukoc. Biol., 2006, vol. 79, no. 2, pp. 303–311.
  34. Candido J., Hagemann T. Cancer-related inf lammation. J. Clin. Immunol., 2013, vol. 33, suppl. 1, pp. 79–84. doi: 10.1007/s10875-012-9847-0
  35. Cerutti A., Cols M., Puga I. Marginal zone B cells: virtues of innate-like antibody producing lymphocytes. Nat. Rev. Immunol., 2013, vol. 13, no. 2, pp. 118–132. doi: 10.1038/nri3383
  36. Charmoy M., Brunner-Agten S., Aebischer D., Auderset F., Launois P., Milon G., Proudfoot A.E., Tacchini-Cottier F. Neutrophil derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice. PLoS Pathog., 2010, vol. 6, no. 2:e1000755. doi: 10.1371/journal.ppat.1000755
  37. Chertov O., Ueda H., Xu L.L., Tani K., Murphy W.J., Wang J.M., Howard O.M.Z., Sayers T.J., Oppenheim J.J. Identification of human neutrophil-derived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. J. Exp. Med., 1997, vol. 186, no. 5, pp. 739–747.
  38. Chopin M., Allan R.S., Belz G.T. Transcriptional regulation of dendritic cell diversity. Front. Immunol., 2012, vol. 3: 26. doi: 10.3389/fimmu.2012.00026
  39. Christoffersson G., Phillipson M. The neutrophil: one cell on many missions or many cells with different agendas? Cell Tissue Res., 2018, vol. 371, no. 3, pp. 415–423.
  40. Chtanova T., Schaeffer M., Han S.J., van Dooren G.G., Nollmann M., Herzmark P., Chan S.W., Satija H., Camfield K., Aaron H., Striepen B., Robey E.A. Dynamics of neutrophil migration in lymph nodes during infection. Immunity, 2008, vol. 29, no. 3, pp. 487–496. doi: 10.1016/j.immuni.2008.07.012
  41. Clayton A.R., Prue R.L., Harper L., Drayson M.T., Savage C.O. Dendritic cell uptake of human apoptotic and necrotic neutrophils inhibits CD40, CD80, and CD86 expression and reduces allogeneic T cell responses: relevance to systemic vasculitis. Arthritis Rheumatol., 2003, vol. 48, no. 8, pp. 2362–2374.
  42. Clynes R.A., Towers T.L., Presta L.G., Ravetch J.V. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat. Med., 2000, vol. 6, no. 4, pp. 443–446.
  43. Collin M., McGovern N., Haniffa M. Human dendritic cell subsets. Immunology, 2013, vol. 140, no. 1, pp. 22–30. doi: 10.1111/imm.12117
  44. Colom B., Bodkin J.V., Beyrau M., Woodfin A., Ody C., Rourke C., Chavakis T., Brohi K., Imhof B.A., Nourshargh S. Leukotriene B4-neutrophil elastase axis drives neutrophil reverse transendothelial cell migration in vivo. Immunity, 2015, vol. 42, no. 6, pp. 1075–1086. doi: 10.1016/j.immuni.2015.05.010
  45. Condamine T., Dominguez G.A., Youn J.I., Kossenkov A.V., Mony S., Alicea-Torres K., Tcyganov E., Hashimoto A., Nefedova Y., Lin C., Partlova S., Garfall A., Vogl D.T., Xu X., Knight S.C., Malietzis G., Lee G.H., Eruslanov E., Albelda S.M., Wang X., Mehta J.L., Bewtra M., Rustgi A., Hockstein N., Witt R., Masters G., Nam B., Smirnov D., Sepulveda M.A., Gabrilovich D.I. Lectin-type oxidized LDL receptor-1 distinguishes population of human polymorphonuclear myeloid-derived suppressor cells in cancer patients. Sci. Immunol., 2016, vol. 1, no. 2, pp. aaf8943. doi: 10.1126/sciimmunol.aaf8943
  46. Cools-Lartigue J., Spicer J., Najmeh S., Ferri L. Neutrophil extracellular traps in cancer progression. Cell. Mol. Life Sci., 2014, vol. 71, no. 21, pp. 4179–4194. doi: 10.1007/s00018-014-1683-3
  47. Cools-Lartigue J., Spicer J., McDonald B., Gowing S., Chow S., Giannias B., Bourdeau F., Kubes P., Ferri L. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J. Clin. Invest., 2013, vol. 123, no. 8, pp. 3446–3458. doi: 10.1172/JCI67484
  48. Cross A., Bucknall R.C., Cassatella M.A., Edwards S.W., Moots R.J. Synovial f luid neutrophils transcribe and express class II major histocompatibility complex molecules in rheumatoid arthritis. Arthritis Rheumatol., 2003, vol. 48, no. 10, pp. 2796–2806.
  49. Culter C.W., Jotwani R. Dendritic cells at the oral mucosal interface. J. Dent. Res., 2006, vol. 85, no. 8, pp. 678–689.
  50. Dallegri F., Ottonello L., Ballestrero A., Dapino P., Ferrando F., Patrone F., Sacchetti C. Tumor cell lysis by activated human neutrophils: analysis of neutrophil-delivered oxidative attack and role of leukocyte function-associated antigen 1. Inflammation, 1991, vol. 15, no. 1, pp. 15–30.
  51. Dalli J., Serhan C.N. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood, 2012, vol. 120, no. 15, pp. e60-e72. doi: 10.1182/blood-2012-04-423525
  52. De Filippo K., Henderson R.B., Laschinger M., Hogg N. Neutrophil chemokines KC and macrophage-inf lammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways. J. Immunol., 2008, vol. 180, no. 6, pp. 4308–4315.
  53. De Kleijn S., Langereis J.D., Leentjens J., Kox M., Netea M.G., Koenderman L., Ferwerda G., Pickkers P., Hermans P.W. IFNγ-stimulated neutrophils suppress lymphocyte proliferation through expression of PD-L1. PLoS ONE, 2013, vol. 8, no. 8: e72249. doi: 10.1371/journal.pone.0072249
  54. De Lorenzo B.H., Godoy L.C., Novaes e Brito R.R., Pagano R.L., Amorim-Dias M.A., Grosso D.M., Lopes J.D., Mariano M. Macrophage suppression following phagocytosis of apoptotic neutrophils is mediated by the S100A9 calcium-binding protein. Immunobiology, 2010, vol. 215, no. 5, pp. 341–347. doi: 10.1016/j.imbio.2009.05.013
  55. Deryugina E.I., Zajac E., Juncker-Jensen A., Kupriyanova T.A., Welter L., Quigley J.P. Tissue-infiltrating neutrophils constitute the major in vivo source of angiogenesis-inducing MMP-9 in the tumor microenvironment. Neoplasia, 2014, vol. 16, no. 10, pp. 771–788. doi: 10.1016/j.neo.2014.08.013
  56. Doherty T.M., Kastelein R., Menon S., Andrade S., Coffman R.L. Modulation of murine macrophage function by IL-13. J. Immunol., 1993, vol. 151, no. 12, pp. 7151–7160.
  57. Doyle A.G., Herbein G., Montaner L.J., Minty A.J., Caput D., Ferrara P, Gordon S. Interleukin-13 alters the activation state of murine macrophages in vitro: comparison with interleukin-4 and interferon-gamma. Eur. J. Immunol., 1994, vol. 24, no. 6, pp. 1441–1445.
  58. Dvorak H.F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. New Engl. J. Med., 1986, vol. 315, pp. 1650 –1659.
  59. Eken C., Gasser O., Zenhaeusern G., Oehri I., Hess C., Schifferli J.A. Polymorphonuclear neutrophil-derived ectosomes interfere with the maturation of monocyte-derived dendritic cells. J. Immunol., 2008, vol. 180, no. 2, pp. 817–824.
  60. Erler J.T., Bennewith K.L., Cox T.R., Lang G., Bird D., Koong A., Le Q.T., Giaccia A.J. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell, 2009, vol. 15, no. 1, pp. 35–44. doi: 10.1016/j.ccr.2008.11.012
  61. Erpenbeck L., Schön M.P. Neutrophil extracellular traps: protagonists of cancer progression? Oncogene, 2017, vol. 36, no. 18, pp. 2483–2490. doi: 10.1038/onc.2016.406
  62. Eruslanov E.B., Bhojnagarwala P.S., Quatromoni J.G., Stephen T.L., Ranganathan A., Deshpande C., Akimova T., Vachani A., Litzky L., Hancock W.W., Conejo-Garcia J.R., Feldman M., Albelda S.M., Singhal S. Tumor-associated neutrophils stimulate T cell responses in early-stage human lung cancer. J. Clin. Invest., 2014, vol. 124, no. 12, pp. 5466–5480. doi: 10.1172/JCI77053
  63. Eruslanov E.B., Singhal S., Albelda S.M. Mouse versus human neutrophils in cancer: a major knowledge gap. Trends Cancer, 2017, vol. 3, no. 2, pp. 149–160. doi: 10.1016/j.trecan.2016.12.006
  64. Escors D., Kochan G. Myeloid-derived suppressor cells and their “inconvenient” plasticity. J. Immunol. Sci., 2018, vol. 2, no. 2, pp. 42–47.
  65. Ethuin F., Gerard B., Benna J.E., Boutten A., Gougereot-Pocidalo M.A., Jacob L., Chollet-Martin S. Human neutrophils produce interferon gamma upon stimulation by interleukin-12. Lab. Invest., 2004, vol. 84, no. 10, pp. 1363–1371.
  66. Fadok V.A., Bratton D.L., Konowal A., Freed P.W., Westcott J.Y., Henson P.M. Macrophages that have ingested apoptotic cells in vitro inhibit proinf lammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest., 1998, vol. 101, no. 4, pp. 890 –898.
  67. Fanger N.A., Liu C., Guyre P.M., Wardwell K., O’Neil J., Guo T.L., Christian T.P., Mudzinski S.P., Gosselin E.J. Activation of human T cells by major histocompatability complex class II expressing neutrophils: proliferation in the presence of superantigen, but not tetanus toxoid. Blood, 1997, vol. 89, no. 11, pp. 4128–4135.
  68. Farrera C., Fadeel B. Macrophage clearance of neutrophil extracellular traps is a silent process. J. Immunol., 2013, vol. 191, no. 5, pp. 2647–2656. doi: 10.4049/jimmunol.1300436
  69. Feldmeyer N., Wabnitz G., Leicht S., Luckner-Minden C., Schiller M., Franz T., Conradi R., Kropf P., Müller I., Ho A.D., Samstag Y., Munder M. Arginine deficiency leads to impaired cofilin dephosphorylation in activated human T lymphocytes. Int. Immun., 2012, vol. 24, no. 5, pp. 303–313. doi: 10.1093/intimm/dxs004
  70. Fletcher M., Ramirez M.E., Sierra R.A., Raber P., Thevenot P., Al-Khami A.A., Sanchez-Pino D., Hernandez C., Wyczechowska D.D., Ochoa A.C., Rodriguez P.C. L-arginine depletion blunts antitumor T-cell responses by inducing myeloid-derived suppressor cells. Cancer Res., 2015, vol. 75, no. 2, pp. 275–283. doi: 10.1158/0008-5472.CAN-14-1491
  71. Fridlender Z.G., Albelda S.M. Tumor-associated neutrophils: friend or foe? Carcinogenesis, 2012, vol. 33, no. 5, pp. 949–955. doi: 10.1093/carcin/bgs123
  72. Fridlender Z.G., Sun J., Kim S., Kapoor V., Cheng G., Ling L., Worthen G.S., Albelda S.M. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell, 2009, vol. 16, no. 3, pp. 183–194. doi: 10.1016/j.ccr.2009.06.017
  73. Gabrilovich D. I., Bronte V., Chen S.H., Colombo M. P., Ochoa A., Ostrand-Rosenberg S., Schreiber H. The terminology issue for myeloid-derived suppressor cells. Cancer Res., 2007, vol. 67, no. 1, pp. 425–426.
  74. Gabrilovich D. I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol., 2009, vol. 9, no. 3, pp. 162–174. doi: 10.1038/nri2506
  75. Garcia-Romo G.S., Caielli S., Vega B., Connolly J., Allantaz F., Xu Z., Punaro M., Baisch J., Guiducci C., Coffman R.L., Barrat F.J., Banchereau J., Pascual V. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med., 2011, vol. 3, no. 73, pp. 73ra20. doi: 10.1126/scitranslmed.3001201
  76. Gasser O., Schifferli J.A. Activated polymorphonuclear neutrophils disseminate anti-inf lammatory microparticles by ectocytosis. Blood, 2004, vol. 104, no. 8, pp. 2543–2548.
  77. Gaudry M., Brégerie O., Andrieu V., El Benna J., Pocidalo M.A., Hakim J. Intracellular pool of vascular endothelial growth factor in human neutrophils. Blood, 1997, vol. 90, no. 10, pp. 4153–4161.
  78. Gautam N., Olofsson A.M., Herwald H., Iversen L.F., Lundgren-Akerlund E., Hedqvist P., Arfors K.E., Flodgaard H., Lindbom L. Heparin-binding protein (HBP/CAP37): a missing link in neutrophil-evoked alteration of vascular permeability. Nat. Med., 2001, vol. 7, pp. 1123–1127.
  79. Gershkovitz M., Caspi Y., Fainsod-Levi T., Katz B., Michaeli J., Khawaled S., Lev S., Polyansky L., Shaul M.E., Sionov R.V., Cohen-Daniel L., Aqeilan R.I., Shaul Y.D., Mori Y., Karni R., Fridlender Z.G., Binshtok A.M., Granot Z. TRPM2 mediates neutrophil killing of disseminated tumor cells. Cancer Res., 2018, vol. 78, no. 10, pp. 2680 –2690. doi: 10.1158/0008-5472.CAN-17-3614
  80. Gestermann N., Di Domizio J., Lande R., Demaria O., Frasca L., Feldmeyer L., Di Lucca J., Gilliet M. Netting neutrophils activate autoreactive B cells in lupus. J. Immunol., 2018, vol. 200, no. 10, pp. 3364–3371. doi: 10.4049/jimmunol.1700778
  81. Gosselin E.J., Wardwell K., Rigby W.F., Guyre P.M. Induction of MHC class II on human polymorphonuclear neutrophils by granulocyte/macrophage colony-stimulating factor, IFN-gamma, and IL-3. J. Immunol., 1993, vol. 151, no. 3, pp. 1482–1490.
  82. Granot Z., Henke E., Comen E.A., King T.A., Norton L., Benezra R. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell, 2011, vol. 20, no. 3, pp. 300 –314. doi: 10.1016/j.ccr.2011.08.012
  83. Grigg J.M., Savill J.S., Sarraf C., Haslett C., Silverman M. Neutrophil apoptosis and clearance from neonatal lungs. Lancet, 1991, vol. 338, no. 8769, pp. 720 –722.
  84. Grohmann U., Bronte V. Control of immune response by amino acid metabolism. Immunol. Rev., 2010, vol. 236, no. 1, pp. 236–243. doi: 10.1111/j.1600-065X.2010.00915.x
  85. Grosse-Steffen T., Giese T., Giese N., Longerich T., Schirmacher P., Hänsch G.M., Gaida M.M. Epithelial-to-mesenchymal transition in pancreatic ductal adenocarcinoma and pancreatic tumor cell lines: the role of neutrophils and neutrophil-derived elastase. Clin. Dev. Immunol., 2012, vol. 2012: 720768, 12 p. doi: 10.1155/2012/720768
  86. Halverson T.W., Wilton M., Poon K.K., Petri B., Lewenza S. DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathog., 2015, vol. 11, no. 1: e1004593. doi: 10.1371/journal.ppat.1004593
  87. Hamilton T.A., Zhao C., Pavicic P.G. Jr, Datta S. Myeloid colony-stimulating factors as regulators of macrophage polarization. Front. Immunol., 2014, vol. 5:554. doi: 10.3389/fimmu.2014.00554
  88. Hampton H.R., Chtanova T. The lymph node neutrophil. Semin. Immunol., 2016, vol. 28, no. 2, pp. 129–136. doi: 10.1016/j.smim.2016.03.008
  89. Hampton H.R., Bailey J., Tomura M., Brink R., Chtanova T. Microbe-dependent lymphatic migration of neutrophils modulates lymphocyte proliferation in lymph nodes. Nat. Commun., 2015, vol. 6: 7139. doi: 10.1038/ncomms8139
  90. Hamza B., Wong E., Patel S., Cho H., Martel J., Irimia D. Retrotaxis of human neutrophils during mechanical confinement inside microf luidic channels. Integr. Biol., 2014, vol. 6, no. 2, pp. 175–183. doi: 10.1039/c3ib40175h
  91. Hänsch G.M., Radsak M., Wagner C., Reis B., Koch A., Breitbart A., Andrassy K. Expression of major histocompatibility class II antigens on polymorphonuclear neutrophils in patients with Wegener’s granulomatosis. Kidney Int., 1999, vol. 55, no. 5, pp. 1811–1818.
  92. Himmel M.E., Crome S.Q., Ivison S., Piccirillo C., Steiner T.S., Levings M.K. Human CD4+FOXP3+ regulatory T cells produce CXCL8 and recruit neutrophils. Eur. J. Immunol., 2011, vol. 41, no. 2, pp. 306–312. doi: 10.1002/eji.201040459
  93. Hock B.D., Taylor K.G., Cross N.B., Kettle A.J., Hampton M.B., McKenzie J.L. Effect of activated human polymorphonuclear leucocytes on T lymphocyte proliferation and viability. Immunology, 2012, vol. 137, no. 3, pp. 249–258. doi: 10.1111/imm.12004
  94. Honda M., Takeichi T., Hashimoto S., Yoshii D., Isono K., Hayashida S., Ohya Y., Yamamoto H., Sugawara Y., Inomata Y. Intravital imaging of neutrophil recruitment reveals the efficacy of FPR1 blockade in hepatic ischemia-reperfusion injury. J. Immunol., 2017, vol. 198, no. 4, pp. 1718–1728. doi: 10.4049/jimmunol.1601773
  95. Hong CW. Current understanding in neutrophil differentiation and heterogeneity. Immune Netw., 2017, vol. 17, no. 5, pp. 298–306. doi: 10.4110/in.2017.17.5.298
  96. Houghton A.M., Rzymkiewicz D.M., Ji H., Gregory A.D., Egea E.E., Metz H.E., Stolz D.B., Land S.R., Marconcini L.A., Kliment C.R., Jenkins K.M., Beaulieu K.A., Mouded M., Frank S.J., Wong K.K., Shapiro S.D. Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat. Med., 2010, vol. 16, no. 2, pp. 219–223. doi: 10.1038/nm.2084
  97. Hu P., Shen M., Zhang P., Zheng C., Pang Z., Zhu L., Du J. Intratumoral neutrophil granulocytes contribute to epithelial-mesenchymal transition in lung adenocarcinoma cells. Tumor Biology, 2015, vol. 36, no. 10, pp. 7789–7796. doi: 10.1007/s13277-015-3484-1
  98. Huang A., Zhang B., Wang B., Zhang F., Fan K.X., Guo Y.J. Increased CD14(+)HLA-DR (-/low) myeloid-derived suppressor cells correlate with extrathoracic metastasis and poor response to chemotherapy in non-small cell lung cancer patients. Cancer Immunol. Immunother., 2013, vol. 62, no. 9, pp. 1439–1451. doi: 10.1007/s00262-013-1450-6
  99. Huh S.J., Liang S., Sharma A., Dong C., Robertson G.P. Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res., 2010, vol. 70, no. 14, pp. 6071–6082. doi: 10.1158/0008-5472.CAN-09-4442
  100. Iking-Konert C., Vogt S., Radsak M., Wagner C., Hänsch G.M., Andrassy K. Polymorphonuclear neutrophils in Wegener’s granulomatosis acquire characteristics of antigen presenting cells. Kidney Int., 2001, vol. 60, no. 6, pp. 2247–2262.
  101. Jablonska J., Leschner S., Westphal K., Lienenklaus S., Weiss S. Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J. Clin. Invest., 2010, vol. 120, no. 4, pp. 1151–1164. doi: 10.1172/JCI37223
  102. Jenne C.N., Liao S., Singh B. Neutrophils: multitasking first responders of immunity and tissue homeostasis. Cell Tissue Res., 2018, vol. 371, no. 3, pp. 395–397. doi: 10.1007/s00441-018-2802-5
  103. Jensen H.K., Donskov F., Marcussen N., Nordsmark M., Lundbeck F., von der Maase H. Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma. J. Clin. Oncol., 2009, vol. 27, no. 28, pp. 4709–4717. doi: 10.1200/JCO.2008.18.9498
  104. Jensen T.O., Schmidt H., Møller H.J., Donskov F., Høyer M., Sjoegren P., Christensen I.J., Steiniche T. Intratumoral neutrophils and plasmacytoid dendritic cells indicate poor prognosis and are associated with pSTAT3 expression in AJCC stage I/II melanoma. Cancer, 2012, vol. 118, no. 9, pp. 2476–2485. doi: 10.1002/cncr.26511
  105. Joyce J.A., Pollard J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer, 2009, vol. 9, no. 4, pp. 239–252. doi: 10.1038/nrc2618
  106. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest., 2009, vol. 119, no. 6, pp. 1420 –1428. doi: 10.1172/JCI39104
  107. Kalyan S., Kabelitz D. When neutrophils meet T cells: beginnings of a tumultuous relationship with underappreciated potential. Eur. J. Immunol., 2014, vol. 44, no. 3, pp. 627–633. doi: 10.1002/eji.201344195
  108. Kamenyeva O., Boularan C., Kabat J., Cheung G.Y., Cicala C., Yeh A.J., Chan J.L., Periasamy S., Otto M., Kehrl J.H. Neutrophil recruitment to lymph nodes limits local humoral response to Staphylococcus aureus. PLoS patogens, 2015, vol. 11, no. 4: e1004827. doi: 10.1371/journal.ppat.1004827
  109. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., Zhu Z., Hicklin D., Wu Y., Port J.L., Altorki N., Port E.R., Ruggero D., Shmelkov S.V., Jensen K.K., Rafii S., Lyden D. VEGFR1-positive haematopoietic bone marrow progenitors initiate the premetastatic niche. Nature, 2005, vol. 438, no. 7069, pp. 820 –827.
  110. Kindzelskii A.L., Petty H.R. Early membrane rupture events during neutrophil-mediated antibody-dependent tumor cell cytolysis. J. Immunol., 1999, vol. 162, no. 6, pp. 3188–3192.
  111. Klemke M., Wabnitz G.H., Funke F., Funk B., Kirchgessner H., Samstag Y. Oxidation of cofilin mediates T cell hyporesponsiveness under oxidative stress conditions. Immunity, 2008, vol. 29, no. 3, pp. 404–413. doi: 10.1016/j.immuni.2008.06.016
  112. Knaapen A.M., Güngör N., Schins R.P., Borm P.J., Van Schooten F.J. Neutrophils and respiratory tract DNA damage and mutagenesis: a review. Mutagenesis, 2006, vol. 21, no. 4, pp. 225–236.
  113. Koga Y., Matsuzaki A., Suminoe A., Hattori H., Hara T. Neutrophil-derived related apoptosis-inducing ligand (TR AIL): a novel mechanism of antitumor effect by neutrophils. Cancer Res., 2004, vol. 64, no. 3, pp. 1037–1043.
  114. Kolaczkowska E., Jenne C.N., Surewaard B.G., Thanabalasuriar A., Lee W.Y., Sanz M.J., Mowen K., Opdenakker G., Kubes P. Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature. Nat. Commun., 2015, vol. 6: 6673. doi: 10.1038/ncomms7673
  115. Kowanetz M., Wu X., Lee J., Tan M., Hagenbeek T., Qu X., Yu L., Ross J., Korsisaari N., Cao T., Bou-Reslan H., Kallop D., Weimer R., Ludlam M.J., Kaminker J.S., Modrusan Z., van Bruggen N., Peale F.V., Carano R., Meng Y.G., Ferrara N. Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C+ granulocytes. PNAS, 2010, vol. 107, no. 50, pp. 21248–21255. doi: 10.1073/pnas.1015855107
  116. Kropf P., Baud D., Marshall S.E., Munder M., Mosley A., Fuentes J.M., Bangham C.R., Taylor G.P., Herath S., Choi B.S., Soler G., Teoh T., Modolell M., Müller I. Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur. J. Immunol., 2007, vol. 37, iss 4, pp. 935–945.
  117. Kruger P., Saffarzadeh M., Weber A.N., Rieber N., Radsak M., von Bernuth H., Benarafa C., Roos D., Skokowa J., Hartl D. Neutrophils: Between Host Defence, Immune Modulation, and Tissue Injury. PLoS Pathog., 2015, vol. 11, no. 3: e1004651. doi: 10.1371/journal.ppat.1004651
  118. Kubes P. The enigmatic neutrophil: what we do not know. Cell Tissue Res., 2018, vol. 371, no. 3, pp. 399–406.
  119. Lande R., Ganguly D., Facchinetti V., Frasca L., Conrad C., Gregorio J., Meller S., Chamilos G., Sebasigari R., Riccieri V., Bassett R., Amuro H., Fukuhara S., Ito T., Liu Y.J., Gilliet M. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transl. Med., 2011, vol. 3, no. 73, pp. 73ra19. doi: 10.1126/scitranslmed.3001180
  120. Lande R., Gregorio J., Facchinetti V., Chatterjee B., Wang Y.H., Homey B., Cao W., Wang Y.H., Su B., Nestle F.O., Zal T., Mellman I., Schröder J.M., Liu Y.J., Gilliet M. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature, 2007, vol. 449, no. 7162, pp. 564–569.
  121. Lechner M.G., Liebertz D.J., Epstein A.L. Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J. Immunol., 2010, vol. 185, no. 4, pp. 2273–2284. doi: 10.4049/jimmunol.1000901
  122. Levy B.D., Clish C.B., Schmidt B., Gronert K., Serhan C.N. Lipid mediator class switching during acute inf lammation: signals in resolution. Nat. Immunol., 2001, vol. 2, pp. 612–619.
  123. Li X., Dai D., Chen B., Tang H., Xie X., Wei W. The value of neutrophil-to-lymphocyte ratio for response and prognostic effect of neoadjuvant chemotherapy in solid tumors: a systematic review and meta-analysis. J. Cancer, 2018, vol. 9, no. 5, pp. 861–871. doi: 10.7150/jca.23367
  124. Li Y.W., Qiu S.J., Fan J., Zhou J., Gao Q., Xiao Y.S., Xu Y.F. Intratumoral neutrophils: a poor prognostic factor for hepatocellular carcinoma following resection. J. Hepatol., 2011, vol. 54, no. 3, pp. 497–505. doi: 10.1016/j.jhep.2010.07.044
  125. Liang F., Lindgren G., Sandgren K.J., Thompson E.A., Francica J.R., Seubert A., De Gregorio E., Barnett S., O’Hagan D.T., Sullivan N.J., Koup R.A., Seder R.A., Loré K. Vaccine priming is restricted to draining lymph nodes and controlled by adjuvant-mediated antigen uptake. Sci. Transl. Med., 2017, vol. 9, no. 393: eaal2094. doi: 10.1126/scitranslmed.aal2094
  126. Liang W., Ferrara N. The complex role of neutrophils in tumor angiogenesis and metastasis. Cancer Immunol. Res., 2016, vol. 4, no. 2, pp. 83–91. doi: 10.1158/2326-6066.CIR-15-0313
  127. Lichtenstein A., Seelig M., Berek J., Zighelboim J. Human neutrophil-mediated lysis of ovarian cancer cells. Blood, 1989, vol. 74, no. 2, pp. 805–809.
  128. Lin A., Loré K. Granulocytes: new members of the antigen-presenting cell family. Front. Immunol., 2017, vol. 8: 1781. doi: 10.3389/fimmu.2017.01781
  129. Liu C., Li Y., Yu J., Feng L., Hou S., Liu Y., Guo M., Xie Y., Meng J., Zhang H., Xiao B., Ma C. Targeting the shift from M1 to M2 macrophages in experimental autoimmune encephalomyelitis mice treated with fasudil. PLoS One, 2013, vol. 8, no. 2:e54841. doi: 10.1371/journal.pone.0054841
  130. Liu Y.J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol., 2005, vol. 23, pp. 275–306.
  131. Lopez-Lago M.A., Posner S., Thodima V.J., Molina A.M., Motzer R.J., Chaganti R.S. Neutrophil chemokines secreted by tumor cells mount a lung antimetastatic response during renal cell carcinoma progression. Oncogene, 2013, vol. 32, no. 14, pp. 1752–1760. doi: 10.1038/onc.2012.201
  132. Loynes C.A., Lee J.A., Robertson A.L., Steel M.J.G., Ellett F., Feng Y., Levy B.D., Whyte M.K., Renshaw S.A. PGE2 production at sites of tissue injury promotes an anti-inf lammatory neutrophil phenotype and determines the outcome of inf lammation resolution in vivo. BioR xiv, 2017.
  133. Luckner-Minden C., Fischer I., Langhans C.D., Schiller M., Kropf P., Muller I., Hohlfeld J.M., Ho A.D., Munder M. Human eosinophil granulocytes do not express the enzyme arginase. J. Leukoc. Biol., 2010, vol. 87, no. 6, pp. 1125–1132. doi: 10.1189/jlb.1109741
  134. Mader J.S., Ewen C., Hancock R.E., Bleackley R.C. The human cathelicidin, LL-37, induces granzyme-mediated apoptosis in regulatory T cells. J. Immunother., 2011, vol. 34, no. 3, pp. 229–235. doi: 10.1097/CJI.0b013e318207ecdf
  135. Mader J.S., Marcet-Palacios M., Hancock R.E., Bleackley R.C. The human cathelicidin, LL-37, induces granzyme-mediated apoptosis in cytotoxic T lymphocytes. Exp. Cell Res., 2011, vol. 317, no. 4, pp. 531–538. doi: 10.1016/j.yexcr.2010.11.015
  136. Maffia P.C., Zittermann S.E., Scimone M.L., Tateosian N., Amiano N., Guerrieri D., Lutzky V., Rosso D., Romeo H.E., Garcia V.E., Issekutz A.C., Chuluyan H.E. Neutrophil elastase converts human immature dendritic cells into transforming growth factor-β1-secreting cells and reduces allostimulatory ability. Am. J. Pathol., 2007, vol. 171, no. 3, pp. 928–937.
  137. Malcolm K.C., Arndt P.G., Manos E.J., Jones D.A., Worthen G.S. Microarray analysis of lipopolysaccharide-treated human neutrophils. Am. J. Physiol. Lung Cell. Mol. Physiol., 2003, vol. 284, no. 4, pp. L663–L670.
  138. Maletto B.A., Ropolo A.S., Alignani D.O., Liscovsky M.V., Ranocchia R.P., Moron V.G., Pistoresi-Palencia M.C. Presence of neutrophil-bearing antigen in lymphoid organs of immune mice. Blood, 2006, vol. 108, no. 9, pp. 3094–3102.
  139. Malmberg K.J., Arulampalam V., Ichihara F., Petersson M., Seki K., Andersson T., Lenkei R., Masucci G., Pettersson S., Kiessling R. Inhibition of activated/memory (CD45RO(+)) T cells by oxidative stress associated with block of NF-kappaB activation. J. Immunol., 2001, vol. 167, no. 5, pp. 2595–2601.
  140. Mandruzzato S., Brandau S., Britten C.M., Bronte V., Damuzzo V., Gouttefangeas C., Maurer D., Ottensmeier C., van der Burg S.H., Welters M.J., Walter S. Toward harmonized phenotyping of human myeloid-derived suppressor cells by f low cytometry: results from an interim study. Cancer Immunol. Immunother., 2016, vol. 65, no. 2, pp. 161–169. doi: 10.1007/s00262-015-1782-5
  141. Mantovani A., Cassatella M.A., Costantini C., Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol., 2011, vol. 11, no. 8, pp. 519–531. doi: 10.1038/nri3024
  142. Martinez F.O., Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep., 2014, vol. 6: 13. doi: 10.12703/P6-13
  143. Masedunskas A., Milberg O., Porat-Shliom N., Sramkova M., Wigand T., Amornphimoltham P., Weigert R. Intravital microscopy: a practical guide on imaging intracellular structures in live animals. BioArchitecture, 2012, vol. 2, no. 5, pp. 143–157. doi: 10.4161/bioa.21758
  144. Mathias J.R., Perrin B.J., Liu T.X., Kanki J., Look A.T., Huttenlocher A. Resolution of inf lammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol., 2006, vol. 80, no. 6, pp. 1281–1288.
  145. Matsushima H., Geng S., Lu R., Okamoto T., Yao Y., Mayuzumi N., Kotol P.F., Chojnacki B.J., Miyazaki T., Gallo R.L., Takashima A. Neutrophil differentiation into a unique hybrid population exhibiting dual phenotype and functionality of neutrophils and dendritic cells. Blood, 2013, vol. 121, no. 10, pp. 1677–1689. doi: 10.1182/blood-2012-07-445189
  146. McDonald B., Pittman K., Menezes G.B., Hirota S.A., Slaba I., Waterhouse C.C., Beck P.L., Muruve D.A., Kubes P. Intravascular danger signals guide neutrophils to sites of sterile inf lammation. Science, 2010, vol. 330, no. 6002, pp. 362–366. doi: 10.1126/science.1195491
  147. McNulty S., Fonfria E. The role of TRPM channels in cell death. Pflügers Arch., 2005, vol. 451, no. 1, pp. 235–242. doi: 10.1007/s00424-005-1440-4
  148. Means T.K., Latz E., Hayashi F., Murali M.R., Golenbock D.T., Luster A.D. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J. Clin. Invest., 2005, vol. 115, no. 2, pp. 407–417.
  149. Merad M., Manz M.G. Dendritic cell homeostasis. Blood, 2009, vol. 113, no. 15, pp. 3418–3427. doi: 10.1182/blood-2008-12-180646
  150. Mishalian I., Bayuh R., Eruslanov E., Michaeli J., Levy L., Zolotarov L., Singhal S., Albelda S.M., Granot Z., Fridlender Z.G. Neutrophils recruit regulatory T-cells into tumors via secretion of CCL17 – a new mechanism of impaired antitumor immunity. Int. J. Cancer, 2014, vol. 135, no. 5, pp.1178–1186. doi: 10.1002/ijc.28770
  151. Mougiakakos D., Johansson C.C., Kiessling R. Naturally occurring regulatory T cells show reduced sensitivity toward oxidative stress-induced cell death. Blood, 2009, vol. 113, no. 15, pp. 3542–3545. doi: 10.1182/blood-2008-09-181040
  152. Munder M., Mollinedo F., Calafat J., Canchado J., Gil-Lamaignere C., Fuentes J.M., Luckner C., Doschko G., Soler G., Eichmann K., Muller F.M., Ho A.D., Goerner M., Modolell M. Arginase I is constitutively expressed in human granulocytes and participates in fungicidal activity. Blood, 2005, vol. 105, no. 6, pp. 2549–2556.
  153. Munder M., Schneider H., Luckner C., Giese T., Langhans C.D., Fuentes J.M., Kropf P., Mueller I., Kolb A., Modolell M., Ho A.D. Suppression of T-cell functions by human granulocyte arginase. Blood, 2006, vol. 108, no. 5, pp. 1627–1634.
  154. Nakazawa D., Shida H., Kusunoki Y., Miyoshi A., Nishio S., Tomaru U., Atsumi T., Ishizu A. The responses of macrophages in interaction with neutrophils that undergo NETosis. J. Autoimmun., 2016, vol. 67, pp. 19–28. doi: 10.1016/j.jaut.2015.08.018
  155. Nicolás-Ávila J.Á., Adrover J.M., Hidalgo A. Neutrophils in homeostasis, immunity, and cancer. Immunity, 2017, vol. 46, no. 1, pp. 15–28. doi: 10.1016/j.immuni.2016.12.012
  156. Ocana A., Nieto-Jiménez C., Pandiella A., Templeton A.J. Neutrophils in cancer: prognostic role and therapeutic strategies. Mol. Cancer., 2017, vol. 16, no. 1: 137. doi: 10.1186/s12943-017-0707-7
  157. Odobasic D., Kitching A.R., Yang Y., O’Sullivan K.M., Muljadi R.C., Edgtton K.L., Tan D.S., Summers S.A., Morand E.F., Holdsworth S.R. Neutrophil myeloperoxidase regulates T-cell-driven tissue inf lammation in mice by inhibiting dendritic cell function. Blood, 2013 vol. 121, no. 20, pp. 4195–4204. doi: 10.1182/blood-2012-09-456483
  158. Ostrand-Rosenberg S., Sinha P. Myeloid-derived suppressor cells: linking inf lammation and cancer. J. Immunol., 2009, vol. 182, no. 8, pp. 4499–4506. doi: 10.4049/jimmunol.0802740
  159. Ouyang W., Kolls J.K., Zheng Y. The biological functions of T helper 17 cell effector cytokines in inf lammation. Immunity, 2008, vol. 28, no. 4, pp. 454–467. doi: 10.1016/j.immuni.2008.03.004
  160. Påhlman L.I., Mörgelin M., Eckert J., Johansson L., Russell W., Riesbeck K., Soehnlein O., Lindbom L., Norrby-Teglund A., Schumann R.R., Björck L., Herwald H. Streptococcal M-protein: a multipotent and powerful inducer of inf lammation. J. Immunol., 2006, vol. 177, no. 2, pp. 1221–1228.
  161. Park S.A., Hyun YM. Neutrophil extravasation cascade: what can we learn from two-photon intravital imaging? Immune Netw., 2016, vol. 16, no. 6, pp. 317–321. doi: 10.4110/in.2016.16.6.317
  162. Pelletier M., Maggi L., Micheletti A., Lazzeri E., Tamassia N., Costantini C., Cosmi L., Lunardi C., Annunziato F., Romagnani S., Cassatella M.A. Evidence for a cross-talk between human neutrophils and Th17 cells. Blood, 2010, vol. 115, no. 2, pp. 335–343. doi: 10.1182/blood-2009-04-216085
  163. Perobelli S.M., Silva T.G., Bonomo A. Neutrophils plasticity: the regulatory interface in various pathological conditions. In: Role of neutrophils in disease pathogenesis. Ed. Maitham Khajah. Chapter 7. Published by InTechOpen, 2017, 178 p.
  164. Perobelli S.M., Galvani R.G., Gonçalves-Silva T., Xavier C.R., Nóbrega A., Bonomo A. Plasticity of neutrophils reveals modulatory capacity. Braz. J. Med. Biol. Res., 2015, vol. 48, no. 8, pp. 665–675. doi: 10.1590/1414-431X20154524
  165. Piccard H., Muschel R.J., Opdenakker G. On the dual roles and polarized phenotypes of neutrophils in tumor development and progression. Crit. Rev. Oncol. Hematol., 2012, vol. 82, no. 3, pp. 296–309. doi: 10.1016/j.critrevonc.2011.06.004
  166. Pillay J., Kamp V.M., van Hoffen E., Visser T., Tak T., Lammers J.W., Ulfman L.H., Leenen L.P., Pickkers P., Koenderman L. A subset of neutrophils in human systemic inf lammation inhibits T cell responses through Mac-1. J. Clin. Invest., 2012, vol. 122, no. 1, pp. 327–336. doi: 10.1172/JCI57990
  167. Pillay J., Tak T., Kamp V.M., Koenderman L. Immune suppression by neutrophils and granulocytic myeloid-derived suppressor cells: similarities and differences. Cell. Mol. Life Sci., 2013, vol. 70, no. 20, pp. 3813–3827. doi: 10.1007/s00018-013-1286-4
  168. Pittman K., Kubes P. Damage-associated molecular patterns control neutrophil recruitment. J. Innate. Immun., 2013, vol. 5, no. 4, pp. 315–323. doi: 10.1159/000347132
  169. Poon I.K., Lucas C.D., Rossi A.G., Ravichandran K.S. Apoptotic cell clearance: basic biology and therapeutic potential. Nat. Rev. Immunol., 2014, vol. 14, no. 3, pp. 166–180. doi: 10.1038/nri3607
  170. Powell D.R., Huttenlocher A. Neutrophils in the tumor microenvironment. Trends Immunol., 2016, vol. 37, no. 1, pp. 41–52. doi: 10.1016/
  171. Prame Kumar K., Nicholls A.J., Wong C.H.Y. Partners in crime: neutrophils and monocytes/macrophages in inf lammation and disease. Cell Tissue Res., 2018, vol. 371, no. 3, pp. 551–565. doi: 10.1007/s00441-017-2753-2
  172. Psaila B., Lyden D. The metastatic niche: adapting the foreign soil. Nat. Rev. Cancer, 2009, vol. 9, no. 4, pp. 285–293. doi: 10.1038/nrc2621
  173. Puga I., Cols M., Barra C.M., He B., Cassis L., Gentile M., Comerma L., Chorny A., Shan M., Xu W., Magri G., Knowles D.M., Tam W., Chiu A., Bussel J.B., Serrano S., Lorente J.A., Bellosillo B., Lloreta J., Juanpere N., Alameda F., Baró T., de Heredia C.D., Torán N., Català A., Torrebadell M., Fortuny C., Cusí V., Carreras C., Diaz G.A., Blander J.M., Farber C.M., Silvestri G., Cunningham-Rundles C., Calvillo M., Dufour C., Notarangelo L.D., Lougaris V., Plebani A., Casanova J.L., Ganal S.C., Diefenbach A., Aróstegui J.I., Juan M., Yagüe J., Mahlaoui N., Donadieu J., Chen K., Cerutti A. B cell-helper neutrophils stimulate immunoglobulin diversification and production in the marginal zone of the spleen. Nat. Immunol., 2011, vol. 13, no. 2, pp. 170 –180. doi: 10.1038/ni.2194
  174. Queen M.M., Ryan R.E., Holzer R.G., Keller-Peck C.R., Jorcyk C.L. Breast cancer cells stimulate neutrophils to produce oncostatin M: potential implications for tumor progression. Cancer Res., 2005, vol. 65, no. 19, pp. 8896–8904.
  175. Radsak M., Iking-Konert C., Stegmaier S., Andrassy K., Hänsch G.M. Polymorphonuclear neutrophils as accessory cells for T-cell activation: major histocompatibility complex class II restricted antigen-dependent induction of T-cell proliferation. Immunology, 2000, vol. 101, no. 4, pp. 521–530.
  176. Rafii S., Lyden D. S100 chemokines mediate bookmarking of premetastatic niches. Nat. Cell Biol., 2006, vol. 8, no. 12, pp. 1321–1323.
  177. Rahman A.H., Taylor D.K., Turka L.A. The contribution of direct TLR signaling to T cell responses. Immunol. Res., 2009, vol. 45, no. 1, pp. 25–36. doi: 10.1007/s12026-009-8113-x
  178. Randolph G.J., Ochando J., Patrida-Sanchez S. Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol., 2008, vol. 26, pp. 293–316.
  179. Rao H.L., Chen J.W., Li M., Xiao Y.B., Fu J., Zeng Y.X., Cai M.Y., Xie D. Increased intratumoral neutrophil in colorectal carcinomas correlates closely with malignant phenotype and predicts patients’ adverse prognosis. PLoS One, 2012, vol. 7, no. 1: e30806. doi: 10.1371/journal.pone.0030806
  180. Ribeiro-Gomes F.L., Peters N.C., Debrabant A., Sacks D.L. Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog., 2012, vol. 8, no. 2:e1002536. doi: 10.1371/journal.ppat.1002536
  181. Ribeiro-Gomes F.L., Romano A., Lee S., Roffê E., Peters N.C., Debrabant A., Sacks D. Apoptotic cell clearance of Leishmania major-infected neutrophils by dendritic cells inhibits CD8+ T-cell priming in vitro by Mer tyrosine kinase-dependent signaling. Cell Death Dis., 2015, vol. 6: e2018. doi: 10.1038/cddis.2015.351
  182. Rodriguez F.M., Novak I.T.C. Costimulatory molecules CD80 and CD86 colocalized in neutrophil extracellular traps (NETs). J. Immunol. Inf. Dis., 2016, vol. 3, no. 1: 103.
  183. Rodriguez P.C., Quiceno D.G., Ochoa A.C. L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood, 2007, vol. 109, no. 4, pp. 1568–1573.
  184. Rodriguez P.C., Zea A.H., Culotta K.S., Zabaleta J., Ochoa J.B., Ochoa A.C. Regulation of T cell receptor CD3zeta chain expression by L-arginine. J. Biol. Chem., 2002, vol. 277, no. 24, pp. 21123–21129.
  185. Rosales C. Neutrophil: a cell with many roles in inf lammation or several cell types? Front. Physiol., 2018, vol. 9: 113. doi: 10.3389/fphys.2018.00113
  186. Rotondo R., Bertolotto M., Barisione G., Astigiano S., Mandruzzato S., Ottonello L., Dallegri F., Bronte V., Ferrini S., Barbieri O. Exocytosis of azurophil and arginase 1-containing granules by activated polymorphonuclear neutrophils is required to inhibit T lymphocyte proliferation. J. Leukoc. Biol., 2011, vol. 89, no. 5, pp. 721–727. doi: 10.1189/jlb.1109737
  187. Sagiv J.Y., Michaeli J., Assi S., Mishalian I., Kisos H., Levy L., Damti P., Lumbroso D., Polyansky L., Sionov R.V., Ariel A., Hovav A.H., Henke E., Fridlender Z.G., Granot Z. Phenotypic diversity and plasticity in circulating neutrophil subpopulations in cancer. Cell Rep., 2015, vol. 10, no. 4, pp. 562–573. doi: 10.1016/j.celrep.2014.12.039
  188. Sandilands G.P., Ahmed Z., Perry N., Davison M., Lupton A., Young B. Cross-linking of neutrophil CD11b results in rapid cell surface expression of molecules required for antigen presentation and T-cell activation. Immunology, 2005, vol. 114, no. 3, pp. 354–368.
  189. Sandilands G.P., McCrae J., Hill K., Perry M., Baxter D. Major histocompatibility complex class II (DR) antigen and costimulatory molecules on in vitro and in vivo activated human polymorphonuclear neutrophils. Immunology, 2006, vol. 119, no. 4, pp. 562–571.
  190. Sato T., Takahashi S., Mizumoto T., Harao M., Akizuki M., Takasugi M., Fukutomi T., Yamashita J. Neutrophil elastase and cancer. Surg. Oncol., 2006, vol. 15, no. 4, pp. 217–222.
  191. Scannell M., Flanagan M.B., deStefani A., Wynne K.J., Cagney G., Godson C., Maderna P. Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J. Immunol., 2007, vol. 178, no. 7, pp. 4595–4605.
  192. Scapini P., Cassatella M.A. Social networking of human neutrophils within the immune system. Blood, 2014, vol. 124, no. 5, pp. 710 –719. doi: 10.1182/blood-2014-03-453217
  193. Schmielau J., Finn O.J. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res., 2001, vol. 61, no. 12, pp. 4756–4760.
  194. Schuster S., Hurrell B., Tacchini-Cottier F. Crosstalk between neutrophils and dendritic cells: a context-dependent process. J. Leukoc. Biol., 2013, vol. 94, no. 4, pp. 671–675. doi: 10.1189/jlb.1012540
  195. Schwab J.M., Chiang N., Arita M., Serhan C.N. Resolvin E1 and protectin D1 activate inf lammation resolution programmes. Nature, 2007, vol. 447, no. 7146, pp. 869–874.
  196. Secklehner J., Lo Celso C., Carlin L.M. Intravital microscopy in historic and contemporary immunology. Immunol. Cell Biol., 2017, vol. 95, no. 6, pp. 506–513. doi: 10.1038/icb.2017.25
  197. Serafini P., Borrello I., Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin. Cancer Biol., 2006, vol. 16, no. 1, pp. 53–65.
  198. Serhan C.N., Chiang N., Van Dyke T.E. Resolving inf lammation: dual anti-inf lammatory and pro-resolution lipid mediators. Nat. Rev. Immunol., 2008, vol. 8, no. 5, pp. 349–361. doi: 10.1038/nri2294
  199. Serhan C.N., Clish C.B., Brannon J., Colgan S.P., Chiang N., Gronert K. Novel functional sets of lipid derived mediators with antiinf lammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinf lammatory drugs and transcellular processing. J. Exp. Med., 2000, vol. 192, no. 8, pp. 1197–1204.
  200. Sharpe A.H., Freeman G.J. The B7-CD28 superfamily. Nat. Rev. Immunol., 2002, vol. 2, no. 2, pp. 116–126.
  201. Shaul M.E., Fridlender Z.G. Cancer related circulating and tumor-associated neutrophils — subtypes, sources and function. FEBS J., 2018.
  202. Silva M.T. Macrophage phagocytosis of neutrophils at inf lammatory/infectious foci: a cooperative mechanism in the control of infection and infectious inf lammation. J. Leukoc. Biol., 2011, vol. 89, no. 5, pp. 675–683. doi: 10.1189/jlb.0910536
  203. Silvestre-Roig C., Hidalgo A., Soehnlein O. Neutrophil heterogeneity: implications for homeostasis and pathogenesis. Blood, 2016, vol. 127, no. 18, pp. 2173–81. doi: 10.1182/blood-2016-01-688887
  204. Singhal S., Bhojnagarwala P.S., O’Brien S., Moon E.K., Garfall A.L., Rao A.S., Quatromoni J.G., Stephen T.L., Litzky L., Deshpande C., Feldman M.D., Hancock W.W., Conejo-Garcia J.R., Albelda S.M., Eruslanov E.B. Origin and role of a subset of tumor-associated neutrophils with antigen-presenting cell features in early-stage human lung cancer. Cancer Cell, 2016, vol. 30, no. 1, pp. 120 –135. doi: 10.1016/j.ccell.2016.06.001
  205. Skrzeczynska-Moncznik J., Wlodarczyk A., Banas M., Kwitniewski M., Zabieglo K., Kapinska-Mrowiecka M., Dubin A., Cichy J. DNA structures decorated with cathepsin G/secretory leukocyte proteinase inhibitor stimulate IFNI production by plasmacytoid dendritic cells. Am. J. Clin. Exp. Immunol., 2013, vol. 2, no. 2, pp. 186–194.
  206. Smith D.A., Kiba A., Zong Y., Witte O.N. Interleukin-6 and oncostatin-M synergize with the PI3K/AKT pathway to promote aggressive prostate malignancy in mouse and human tissues. Mol. Cancer Res., 2013, vol. 11, no. 10, pp. 1159–1165. doi: 10.1158/1541-7786.MCR-13-0238
  207. Soehnlein O., Kai-Larsen Y., Frithiof R., Sorensen O.E., Kenne E., Scharffetter-Kochanek K., Eriksson E.E., Herwald H., Agerberth B., Lindbom L. Neutrophil primary granule proteins HBP and HNP1–3 boost bacterial phagocytosis by human and murine macrophages. J. Clin. Invest., 2008, vol. 118, no. 10, pp. 3491–3502. doi: 10.1172/JCI35740
  208. Soehnlein O., Lindbom L. Phagocyte partnership during the onset and resolution of inf lammation. Nat. Rev. Immunol., 2010, vol. 10, no. 6, pp. 427–439. doi: 10.1038/nri2779
  209. Solito E., Kamal A., Russo-Marie F., Buckingham J.C., Marullo S., Perretti M. A novel calcium-dependent proapoptotic effect of annexin 1 on human neutrophils. FASEB J., 2003, vol. 17, no. 11, pp. 1544–1546.
  210. Solito S., Falisi E., Diaz-Montero C.M., Doni A., Pinton L., Rosato A., Francescato S., Basso G., Zanovello P., Onicescu G., Garrett-Mayer E., Montero A.J., Bronte V., Mandruzzato S. A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood, 2011, vol. 118, no. 8, pp. 2254–2265. doi: 10.1182/blood-2010-12-325753
  211. Solito S., Marigo I., Pinton L., Damuzzo V., Mandruzzato S., Bronte V. Myeloid-derived suppressor cell heterogeneity in human cancers. Ann. N.Y. Acad. Sci., 2014, vol. 1319, no. 1, pp. 47–65. doi: 10.1111/nyas.12469
  212. Spiegel A., Brooks M.W., Houshyar S., Reinhardt F., Ardolino M., Fessler E., Chen M.B., Krall J.A., DeCock J., Zervantonakis I.K., Iannello A., Iwamoto Y., Cortez-Retamozo V., Kamm R.D., Pittet M.J., Raulet D.H., Weinberg R.A. Neutrophils suppress intraluminal NK cell-mediated tumor cell clearance and enhance extravasation of disseminated carcinoma cells. Cancer Discov., 2016, vol. 6, no. 6, pp. 630 –649. doi: 10.1158/2159-8290.CD-15-1157
  213. Stagg A.J., Hart A.L., Knight C.S., Kamm M.A. The dendritic cell: its role in intestional inf lammation and relationship with gut bacteria. Gut, 2003, vol. 52, pp. 1522–1529.
  214. Stark M.A., Huo Y., Burcin T.L., Morris M.A., Olson T.S., Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity, 2005, vol. 22, no. 3, pp. 285–294.
  215. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med., 1992, vol. 176, no. 1, pp. 287–292.
  216. Steinman, R.M. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol., 2012, vol. 30, pp. 1–22. doi: 10.1146/annurev-immunol-100311-102839
  217. Takano T., Azuma N., Satoh M., Toda A., Hashida Y., Satoh R., Hohdatsu T. Neutrophil survival factors (TNF-alpha, GM-CSF, and GCSF) produced by macrophages in cats infected with feline infectious peritonitis virus contribute to the pathogenesis of granulomatous lesions. Arch. Virol., 2009, vol. 154, no. 5, pp. 775–781. doi: 10.1007/s00705-009-0371-3
  218. Tateosian N.L., Reiteri R.M., Amiano N.O., Costa M.J., Villalonga X., Guerrieri D., Maffía P.C. Neutrophil elastase treated dendritic cells promote the generation of CD4(+)FOXP3(+) regulatory T cells in vitro. Cell. Immunol., 2011, vol. 269, no. 2, pp. 128–134. doi: 10.1016/j.cellimm.2011.03.013
  219. Templeton A.J., McNamara M.G., Šeruga B., Vera-Badillo F.E., Aneja P., Ocaña A., Leibowitz-Amit R., Sonpavde G., Knox J.J., Tran B., Tannock I.F., Amir E. Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and metaanalysis. J. Natl. Cancer Inst., 2014, vol. 106, no. 6: dju124. doi: 10.1093/jnci/dju124
  220. Tesmer L.A., Lundy S.K., Sarkar S., Fox D.A. Th17 cells in human disease. Immunol. Rev., 2008, vol. 223, no. 1, pp. 87–113. doi: 10.1111/j.1600-065X.2008.00628.x
  221. Tillack K., Breiden P., Martin R., Sospedra M. T lymphocyte priming by neutrophil extracellular traps links innate and adaptive immune responses. J. Immunol., 2012, vol. 188, no. 7, pp. 3150 –3159. doi: 10.4049/jimmunol.1103414
  222. Tohme S., Yazdani H.O., Al-Khafaji A.B., Chidi A.P., Loughran P., Mowen K., Wang Y., Simmons R.L., Huang H., Tsung A. Neutrophil extracellular traps promote the development and progression of liver metastases after surgical stress. Cancer Res., 2016, vol. 76, no. 6, pp. 1367–1380. doi: 10.1158/0008-5472.CAN-15-1591
  223. Trellakis S., Bruderek K., Dumitru C.A., Gholaman H., Gu X., Bankfalvi A., Scherag A., Hütte J., Dominas N., Lehnerdt G.F., Hoffmann T.K., Lang S., Brandau S. Polymorphonuclear granulocytes in human head and neck cancer: enhanced inf lammatory activity, modulation by cancer cells and expansion in advanced disease. Int. J. Cancer, 2011, vol. 129, no. 9, pp. 2183–2193. doi: 10.1002/ijc.25892
  224. Trellakis S., Farjah H., Bruderek K., Dumitru C.A., Hoffmann T.K., Lang S., Brandau S. Peripheral blood neutrophil granulocytes from patients with head and neck squamous cell carcinoma functionally differ from their counterparts in healthy donors. Int. J. Immunopathol. Pharmacol., 2011, vol. 24, no. 3, pp. 683–693.
  225. Valladeau J., Saeland S. Cutaneous dendritic cells. Semin. Immunol., 2005, vol. 17, no. 4, pp. 273–283.
  226. Van Dyken S.J., Locksley R.M. Interleukin-4-and interleukin-13-mediated alternatively activated macrophages: roles in homeostasis and disease. Annu. Rev. Immunol., 2013, vol. 31, pp. 317–343. doi: 10.1146/annurev-immunol-032712-095906
  227. Van Gisbergen K.P., Sanchez-Hernandez M., Geijtenbeek T.B., van Kooyk Y. Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med., 2005, vol. 201, no. 8, pp. 1281–1292.
  228. Veglia F., Perego M., Gabrilovich D. Myeloid-derived suppressor cells coming of age. Nat. Immunol., 2018, vol. 19, no. 2, pp. 108–119. doi: 10.1038/s41590-017-0022-x
  229. Vono M., Lin A., Norrby-Teglund A., Koup R.A., Liang F., Loré K. Neutrophils acquire the capacity for antigen presentation to memory CD4+ T cells in vitro and ex vivo. Blood, 2017, vol. 129, no. 14, pp. 1991–2001. doi: 10.1182/blood-2016-10-744441
  230. Walter S., Weinschenk T., Stenzl A., Zdrojowy R., Pluzanska A., Szczylik C., Staehler M., Brugger W., Dietrich P.Y., Mendrzyk R., Hilf N., Schoor O., Fritsche J., Mahr A., Maurer D., Vass V., Trautwein C., Lewandrowski P., Flohr C., Pohla H., Stanczak J.J., Bronte V., Mandruzzato S., Biedermann T., Pawelec G., Derhovanessian E., Yamagishi H., Miki T., Hongo F., Takaha N., Hirakawa K., Tanaka H., Stevanovic S., Frisch J., Mayer-Mokler A., Kirner A., Rammensee H.G., Reinhardt C., Singh-Jasuja H. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat. Med., 2012, vol. 18, no. 8, pp. 1254–1261. doi: 10.1038/nm.2883
  231. Wang J. Neutrophils in tissue injury and repair. Cell Tissue Res., 2018, vol. 371, no. 3, pp. 531–539.
  232. Wang J.F., Li J.B., Zhao Y.J., Yi W.J., Bian J.J., Wan X.J., Zhu K.M., Deng X.M. Up-regulation of programmed cell death 1 ligand 1 on neutrophils may be involved in sepsis-induced immunosuppression: an animal study and a prospective case-control study. Anesthesiology, 2015, vol. 122, no. 4, pp. 852–863. doi: 10.1097/ALN.0000000000000525
  233. Wang L., Chang E.W., Wong S.C., Ong S.M., Chong D.Q., Ling K.L. Increased myeloid-derived suppressor cells in gastric cancer correlate with cancer stage and plasma S100A8/A9 proinf lammatory proteins. J. Immunol., 2013, vol. 190, no. 2, pp. 794–804. doi: 10.4049/jimmunol.1202088
  234. Wang T.T., Zhao Y.L., Peng L.S., Chen N., Chen W., Lv Y.P, Mao F.Y., Zhang J.Y., Cheng P., Teng Y.S., Fu X.L., Yu P.W., Guo G., Luo P., Zhuang Y., Zou Q.M. Tumour-activated neutrophils in gastric cancer foster immune suppression and disease progression through GM-CSF-PD-L1 pathway. Gut, 2017, vol. 66, no. 11, pp. 1900 –1911. doi: 10.1136/gutjnl-2016-313075
  235. Webb N.J., Myers C.R., Watson C.J., Bottomley M.J., Brenchley P.E. Activated human neutrophils express vascular endothelial growth factor (VEGF). Cytokine, 1998, vol. 10, no. 4, pp. 254–257.
  236. Wels J., Kaplan R.N., Rafii S., Lyden D. Migratory neighbors and distant invaders: tumor-associated niche cells. Genes Dev., 2008, vol. 22, no. 5, pp. 559–574. doi: 10.1101/gad.1636908
  237. Wislez M., Fleury-Feith J., Rabbe N., Moreau J., Cesari D., Milleron B., Mayaud C., A ntoine M., Soler P., Cadranel J. Tumor-derived granulocyte-macrophage colony-stimulating factor and granulocyte colony-stimulating factor prolong the sur vival of neutrophils inf iltrating bronchoalveolar subtype pulmonary adenocarcinoma. Am. J. Pathol., 2001, vol. 159, no. 4, pp. 1423–1433.
  238. Wittamer V., Bondue B., Guillabert A., Vassart G., Parmentier M., Communi D. Neutrophil-mediated maturation of chemerin: a link between innate and adaptive immunity. J. Immunol., 2005, vol. 175, no. 1, pp. 487–493.
  239. Woodfin A., Voisin M.B., Beyrau M., Colom B., Caille D., Diapouli F.M., Nash G.B., Chavakis T., Albelda S.M., Rainger G.E., Meda P., Imhof B.A., Nourshargh S. The junctional adhesion molecule (JAM-C) regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol., 2011, vol. 12, no. 8, pp. 761–769. doi: 10.1038/ni.2062
  240. Wu D., Zeng Y., Fan Y., Wu J., Mulatibieke T., Ni J., Yu G., Wan R., Wang X., Hu G. Reverse-migrated neutrophils regulated by JAM-C are involved in acute pancreatitis-associated lung injury. Sci. Rep., 2016, vol. 6, article number: 20545. doi: 10.1038/srep20545
  241. Wynn T.A., Vannella K.M. Macrophages in tissue repair, regeneration, and fibrosis. Immunity, 2016, vol. 44, no. 3, pp. 450 –462. doi: 10.1016/j.immuni.2016.02.015
  242. Xu N., Lei X., Liu L. Tracking neutrophil intraluminal crawling, transendothelial migration and chemotaxis in tissue by intravital video microscopy. J. Vis. Exp., 2011, vol. 55: e3296. doi: 10.3791/3296
  243. Yang C.W., Strong B.S., Miller M.J., Unanue E.R. Neutrophils inf luence the level of antigen presentation during the immune response to protein antigens in adjuvants. J. Immunol., 2010, vol. 185, no. 5, pp. 2927–2934. doi: 10.4049/jimmunol.1001289
  244. Youn J.I., Kumar V., Collazo M., Nefedova Y., Condamine T., Cheng P., Villagra A., Antonia S., McCaffrey J.C., Fishman M., Sarnaik A., Horna P., Sotomayor E., Gabrilovich D.I. Epigenetic silencing of retinoblastoma gene regulates pathologic differentiation of myeloid cells in cancer. Nat. Immunol., 2013, vol. 14, no. 3, pp. 211–220. doi: 10.1038/ni.2526.
  245. Youn J.I., Nagaraj S., Collazo M., Gabrilovich D.I. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol., 2008, vol. 181, no. 8, pp. 5791–5802.
  246. Zivkovic M., Poljak-Blazi M., Egger G., Sunjic S.B., Schaur R.J., Zarkovic N. Oxidative burst and anticancer activities of rat neutrophils. BioFactors, 2005, vol. 24, no. 1–4, pp. 305–312.
  247. Zivkovic M., Poljak-Blazi M., Zarkovic K., Mihaljevic D., Schaur R.J., Zarkovic N. Oxidative burst of neutrophils against melanoma B16-F10. Cancer Lett., 2007, vol. 246, no. 1–2, pp. 100 –108.

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