THE NEW LOOK AT NEUTROPHILIC GRANULOCYTES: RETHINKING OLD DOGMAS. PART 1

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Abstract

Numerous modern basic research done undeniable fact that neutrophilic granulocytes (NG) are key effector and regulatory circuits both innate and adaptive immunity, and play a crucial role in the pathogenesis of a wide range of diseases. NG have potent receptor repertoire, providing a connection between them, cells of the immune system, as well as communication with endothelial cells, epithelial and other tissues. NG inducing stimuli activate and promote the translocation of cytoplasmic granules and vesicles surface molecules on the cytoplasmic membrane the secretion of a large spectrum of pro-and anti-inf lammatory, immunoregulatory cytokines, colony, angiogenic factors and fibrogenic, TNF superfamily members, chemokines, regulatory protein, etc. Chromatin nuclei NG capable of restructuring under the influence of inducing stimuli, which is associated with the expression of multiple cytokine genes. NG receiving complex cytokine inf luence not only acquire new features, but also in various stages of activation and differentiation processes involved in intracellular intraphagosomalis degranulation and killing of implementing elimination microorganisms and extracellular neutrophil degranulation in the formation neutrophil extracellular traps (NET), while this dying through NETosis. Features NG phenotype and their functional properties, demonstrate the existence of subpopulations of NG with different capabilities: equipment of different receptor, the ability to restructure chromatin expressing cytokine genes and secrete cytokines to implement the contents of the granular system, produce reactive oxygen species, implement cytotoxicity form NET. In our opinion, there subpopulation NG: regulatory; suppressor; proinf lammatory — initiating an inf lammatory response; inf lammation with a positive potential microbicidal (antibacterial, antiviral, antifungal); inf lammatory cytotoxic potential of the negative  — “aggressive”; anti-inf lammation regulating regression; antitumoral — TAN1; pro-tumoral — TAN2; hybrid, combining the characteristics of NG and dendritic cells. The absence of adequate response, or hyperactivation blockade NG functions leads to the development of low-intensity infectious and inf lammatory diseases, do not respond to conventional therapy of autoimmune diseases/chronic immune-dependent processes. Remodeling dysfunctions NG — the key to new immunotherapeutic strategies.

About the authors

I. V. Nesterova

Peoples’ Friendship University of Russia; Kuban State Medical University of Ministry of Health Development of Russia

Author for correspondence.
Email: inesterova1@yandex.ru

Irina V. Nesterova - PhD, MD (Medicine), Professor, Professor of the Department of Allergology and Immunology FAT MW of the MI PFUR; Chief Researcher, Department of Clinical and Experimental Immunology and Molecular Biology CSRL KSMU.

117513, Moscow, Leninsky pr., 123-1. Phone: +7 916 187-73-41 (mobile)

Russian Federation

N. V. Kolesnikova

Kuban State Medical University of Ministry of Health Development of Russia

Email: fake@neicon.ru

PhD, MD (Biology), Professor, Head of the CSRL KSMU

Krasnodar

Russian Federation

G. A. Chudilova

Kuban State Medical University of Ministry of Health Development of Russia

Email: fake@neicon.ru

PhD (Biology), Associate Professor, Head of the Department of Clinical and Experimental Immunology and Molecular Biology of the CSRL, KSMU.

Krasnodar

Russian Federation

L. V. Lomtatidze

Kuban State Medical University of Ministry of Health Development of Russia

Email: fake@neicon.ru

PhD (Biology), Senior Researcher, Department of Clinical and Experimental Immunology and Molecular Biology of the CSRL KSMU.

Krasnodar

Russian Federation

S. V. Kovaleva

Kuban State Medical University of Ministry of Health Development of Russia

Email: fake@neicon.ru

PhD (Medicine), Senior Researcher, Department of Clinical and Experimental Immunology and Molecular Biology of the CSRL KSMU.

Krasnodar

Russian Federation

A. A. Evglevsky

Kuban State Medical University of Ministry of Health Development of Russia

Email: fake@neicon.ru

PhD (Medicine), Associate Professor, Senior Researcher, Department of Clinical and Experimental Immunology and Molecular Biology of the CSRL KSMU.

Krasnodar

Russian Federation

T.D. L. Nguyen

Peoples’ Friendship University of Russia

Email: fake@neicon.ru

Postgraduate Student of the Department of Allergology and Immunology FAT MW of the Medical Institute.

Moscow

Russian Federation

References

  1. Бережная Н.М. Нейтрофилы и иммунологический гомеостаз. Киев: Наукова думка, 1988. 205 c. [Berezhnaja N.M. Neitrofily i immunologicheskii gomeostaz [Neutrophils and immunological homeostasis]. Kiev: Naukova dumka, 1988, 205 p.]
  2. Бойко А.А., Ветчинин С.С., Сапожников А.М., Коваленко Е.И. Изменение уровня белков теплового шока семейства 70 кДа в нейтрофилах человека под действием теплового шока // Биоорганическая химия. 2014. Т. 40, № 5. С. 528–540. [Boyko A.A., Vetchinin S.S., Sapozhnikov A.M., Kovalenko E.I. Changes in the heat shock 70 kDa protein level in human neutrophils induced by heat shock. Bioorganicheskaya khimiya = Bioorganic Chemistry, 2014, vol. 40, no. 5, pp. 528–540. doi: 10.7868/S0132342314050042 (In Russ.)]
  3. Долгушин И.И., Шишков Ю.С., Савочкина А.Ю. Нейтрофильные ловушки и методы оценки функционального статуса нейтрофилов. Москва: РАМН, 2009. 208 c. [Dolgushin I.I., Shishkov Ju.S., Savochkina A.Ju. Neitrofil’nye lovushki i metody otsenki funktsional’nogo statusa neitrofilov [Neutrophil traps and methods for assessing the functional status of neutrophils]. Moscow: R AMN, 2009, 208 p.]
  4. Евглевский А.А., Нестерова И.В., Ковалева С.В. Особенности реструктуризации хроматина нейтрофильных гранулоцитов при хроническом миелолейкозе // Российский иммунологический журнал. 2012. T. 6, № 4. С. 384–381. [Evglevskij A.A., Nesterova I.V., Kovaleva S.V. Features chromatin restructuring of neutrophilic granulocytes in chronic myeloid leukemia. Rossiiskii immunologicheskii zhurnal = Russian Journal of Immunology, 2012, vol. 6, no. 4, pp. 384–381. (In Russ.)]
  5. Киселева Е.П. Новые представления о противоинфекционном иммунитете // Инфекция и иммунитет. 2011. Т. 1, № 1. С. 9–14. [Kiseleva E.P. New ideas about anti-infective immunity. Infektsiya i immunitet = Russian Journal of Infection and Immunity, 2011, vol. 1, no. 1, рр. 9–14. doi: 10.15789/2220-7619-2011-1-9-14 (In Russ.)]
  6. Кравцов А.Л., Шмелькова Т.П. Секреторная дегрануляция нейтрофилов как триггер воспаления и регулятор иммунного ответа: роль сериновых лейкоцитарных протеаз и протеолитически-активных рецепторов // Эпидемиология и вакцинопрофилактика. 2011. № 1. С. 79–87. [Kravcov A.L., Shmel’kova T.P. Secretory degranulation of neutrophils as a trigger inf lammation and control the immune response: the role of serine proteases and proteolytic leukocytereceptor activity. Epidemiologiya i vaktsinoprofilaktika = Epidemiology and Vaccinal Prevention, 2011, no. 1, pp. 79–87. (In Russ.)]
  7. Нестерова И.В. Нейтрофильные экстрацеллюлярные сети: протекция и защита // International Journal on Immunorehabilitation. 2009. Т. 1, № 1. С. 25–26. [Nesterova I.V. Neutrophil extracellular network: patronage and protection. International Journal on Immunorehabilitation, 2009, vol. 11, no. 1, pp. 25–26. (In Russ.)]
  8. Нестерова И.В., Евглевский А.А., Фомичева Е.В., Колесникова Н.В., Ковалева С.В., Чудилова Г.А., Ломтатидзе Л.В., Коков Е.А., Кокова Л.Н. Особенности спонтанной и индуцированной реструктуризации хроматина и функционирования кислород-зависимых цитотоксических механизмов нейтрофильных гранулоцитов при колоректальном раке // Российский иммунологический журнал. 2011. Т. 5(14), № 3–4. С. 254–261. [Nesterova I.V., Evglevskij A.A., Fomicheva E.V., Kolesnikova N.V., Kovaleva S.V., Chudilova G.A., Lomtatidze L.V., Kokov E.A., Kokova L.N. Features of spontaneous and induced chromatin restructuring and functioning of the oxygen-dependent cytotoxic mechanisms of neutrophil granulocytes in colorectal cancer. Rossiiskii immunologicheskii zhurnal = Russian Journal of Immunology, 2011, vol. 5(14), no. 3–4, pp. 254–261. (In Russ.)]
  9. Нестерова И.В., Евглевский А.А., Чудилова Г.А., Ломтатидзе Л.В., Ковалева С.В., Калашников А.Е. Особенности реструктуризации хроматина и изменение уровня относительной экспрессии генов IL-8, IL-1β и TNFα нейтрофильных гранулоцитов под влиянием глюкозаминилмурамилдипептида и интерферона-γ у больных хроническим гайморитом в системе in vitro // Иммунология. 2015. Т. 36, № 6. С. 363–367. [Nesterova I.V., Evglevskij A.A., Chudilova G.A., Lomtatidze L.V., Kovaleva S.V., Kalashnikov A.E. Features of chromatin restructuring and changes in the level of relative expression of IL-8, IL-1β and TNFα genes of neutrophilic granulocytes under the inf luence of glucosaminylmuramyl dipeptide and interferon-γ in patients with chronic sinusitis in an in vitro system. Immunologiya = Immunology, 2015, vol. 36, no. 6, pp. 363–367. (In Russ.)]
  10. Нестерова И.В., Ковалева С.В., Чудилова Г.А., Ломтатидзе Л.В., Евглевский А.А. Двойственная роль нейтрофильных гранулоцитов в реализации противоопухолевой защиты // Иммунология. 2012. Т. 33, № 5. С. 281–288. [Nesterova I.V., Kovaleva S.V., Chudilova G.A., Lomtatidze L.V., Evglevskij A.A. The dual role of neutrophils in the implementation of the antitumor protection. Immunologiya = Immunology, 2012, vol. 33, no. 5, pp. 281–288.(In Russ.)]
  11. Нестерова И.В., Колесникова Н.В., К лещенко Е.И., Тараканов В.А., Смерчинская Т.В., Сапун О.И., Чудилова Г.А., Ломтатидзе Л.В., Фомичева Е.В., Кокова Л.Н., Стрюковский А.Е. Различные варианты дефектов функционирования нейтрофильных гранулоцитов при врож денных пневмониях у новорож денных // Российский иммунологический журнал. 2012. Т. 6, № 2. С. 170–176. [Nesterova I.V., Kolesnikova N.V., Kleshhenko E.I., Tarakanov V.A., Smerchinskaja T.V., Sapun O.I., Chudilova G.A., Lomtatidze L.V., Fomicheva E.V., Kokova L.N., Stryukovskij A.E. Different variants of functioning defects of neutrophil granulocytes in patients with congenital pneumonia in newborns. Rossiiskii immunologicheskii zhurnal = Russian Journal of Immunology, 2012, vol. 6, no. 2, pp. 170 –176. (In Russ.)]
  12. Нестерова И.В., Швыдченко И.Н., Роменская В.А., Фомичева Е.В., Быковская Е.Ю. Нейтрофильные гранулоциты — к лючевые к летки иммунной системы // А ллергология и иммунология. 2008. Т. 9, № 4. С. 432–435. [Nesterova I.V., Shvydchenko I.N., Romenskaya V.A., Fomicheva E.V., Bykovskaya E.Yu. Granulocytes — key cells of the immune system. Allergologiya i immunologiya = Allergy and Immunology, 2008, vol. 9, no. 4, pp. 432–435. (In Russ.)]
  13. Хаитов Р.М., Игнатьева Г.А., Сидорович И.Г. Иммунология. Норма и патология. 3-e изд. М.: Медицина. 2010. 752 с. [Haitov R.M., Ignat’eva G.A., Sidorovich I.G. Immunologiya. Norma i patologiya [Immunology. Health and disease]. 3rd ed. Moscow: Meditsina, 2010, 752 p.]
  14. Beyrau M., Bodkin J.V., Nourshargh S. Neutrophil heterogeneity in health and disease: a revitalized avenue in inf lammation and immunity. Open Biol., 2012, vol. 2, no. 11, pp. 120 –134. doi: 10.1098/rsob.120134
  15. Brinkmann V., Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin? J. Cell Biol, 2012, vol. 198, pp. 773–783. doi: 10.1083/jcb.201203170
  16. Buckley C.D., Ross E.A., McGettrick H.M., Osborne C.E., Haworth O., Schmutz C., Stone P.C.W., Salmon M., Matharu N.M., Vohra R.K., Nash G.B., Rainger G.E. Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration. J. Leukoc. Biol., 2006, vol. 79, pp. 303–311. doi: 10.1189/jlb.0905496
  17. Cassatella M.A. On the production of TNF-related apoptosis inducing ligand (TR AIL/Apo-2L) by human neutrophils. J. Leukoc. Biol., 2006, vol. 79, pp. 1140 –1149. doi: 10.1189/jlb.1005558
  18. Cheng O.Z., Palaniyar N. NET balancing: a problem in inf lammatory lung diseases. Front. Immunol., 2013, vol. 24, pp. 4. doi: 10.3389/fimmu.2013.00001
  19. Courtney Frasch S., Fernandez-Boyanapalli R.F., Zemski Berry K.A., Murphy R.C., Leslie C.C., Nick J.A., Henson P.M., Bratton D.L. Neutrophils regulate tissue neutrophilia in inf lammation via the oxidant-modified lipid lysophosphatidylserine. J. Biol. Chem., 2013, vol. 288, no. 7, pp. 4583–4593. doi: 10.1074/jbc.M112.438507
  20. De Oliveira-Junior E.B., Bustamante J., Newburger P.E., Condino-Neto A. The human NADPH oxidase: primary and secondary defects impairing the respiratory burst function and the microbicidal ability of phagocytes. Scand. J. Immunol., 2011, vol. 73, no. 5, pp. 420-427. doi: 10.1111/j.1365-3083.2010.02501.x
  21. Dragon S., Saffar A.S., Shan L., Gounni A.S. IL-17 attenuates the anti-apoptotic effects of GM-CSF in human neutrophils. Mol. Immunol., 2008, vol. 45, no. 1, pp. 160 –168. doi: 10.1016/j.molimm.2007.04.027
  22. Elghetany M.T. Surface antigen changes during normal neutrophilic development: a critical review. Blood Cells Mol. Dis. 2002, vol. 28, no. 2, pp. 260 –274.
  23. Fadeel B. Babies born without safety NET. Blood, 2009, vol. 113, no. 25, pp. 6270 –6271. doi: 10.1182/blood-2009-03-210328
  24. Fuchs T.A., Brill A., Duerschmied D., Schatzberg D., Monestier M., Myers D.D. Jr, Wrobleski S.K., Wakefield T.W., Hartwig J.H., Wagner D.D. Extracellular DNA traps promote thrombosis. Proc. Natl. Acad. Sci. USA, 2010, vol. 107, no. 36, pp. 15880 –15885. doi: 10.1073/pnas.1005743107.
  25. Fuchs T., Püellmann K., Scharfenstein O., Eichner R., Stobe E., Becker A., Pechlivanidou I., Kzhyshkowska J., Gratchev A., Ganser A., Neumaier M., Beham A.W., Kaminski W.E. The neutrophil recombinatorial TCR-like immune receptor is expressed across the entire human life span but repertoire diversity declines in old age. Biochem. Biophys. Res. Commun., 2012, vol. 419, no. 2, pp. 309–315. doi: 10.1016/j.bbrc.2012.02.017
  26. 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, pp. 73ra20. doi: 10.1126/scitranslmed.3001201
  27. Gougerot-Pocidalo M.A., El Benna J., Elbim C., Chollet-Martin S., Dang M.C. Regulation of human neutrophil oxidative burst by proand anti-inf lammatory cytokines. J. Soc. Biol., 2002, vol. 196, no. 1, pp. 37–46.
  28. Gupta A.K., Hasler P., Holzgreve W., Gebhardt S., Hahn S. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Human Immunol., 2005, vol. 66, no. 11, pp. 1146–1154. doi: 10.1016/ j.humimm.2005.11.003
  29. Hamon V.F., Cossart P. Histone modifications and chromatin remodeling during bacterial infections. Cell Host Microbe., 2008, vol. 4, no. 2, pp. 100 –109. doi: 10.1016/j.chom.2008.07.009
  30. Heyworth P.G., Cross A.R., Curnutte J.T. Chronic granulomatous disease. Curr. Opin. Immunol., 2003, vol. 15, pp. 578–584.
  31. Hofman P. Molecular regulation of neutrophil apoptosis and potential targets for therapeutic strategy against the inf lammatory process. Curr. Drug Targets Inflamm. Allergy, 2004, vol. 3, no. 1, pp. 1–9.
  32. Hung S.L., Chiang H.H., Wu C.Y., Hsu M.J., Chen Y.T. Effects of herpes simplex virus type 1 infection on immune functions of human neutrophils. J. Periodontal Res., 2012, vol. 47, no. 5, pp. 635-644. doi: 10.1111/j.1600-0765.2012.01476.x
  33. Hurtado-Nedelec M., Makni-Maalej K., Gougerot-Pocidalo M.A., Dang P.M., El-Benna J. Assessment of priming of the human neutrophil respiratory burst. Methods Mol. Biol., 2014, vol. 1124, pp. 405–412. doi: 10.1007/978-1-62703-845-4_ 23
  34. Iking-Konert C., Wagner C., Denef leh B., Hug F., Schneider M., Andrassy K., Hansch G.M. Up-regulation of the dendritic cell marker CD83 on polymorphonuclear neutrophils (PMN): divergent expression in acute bacterial infections and chronic inf lammatory disease. Clin. Exp. Immunol., 2002, vol. 130, no. 3, pp. 501–508. doi: 10.1046/j.1365-2249.2002.02008.x
  35. Jack R.M., Fearon D.T. Selective synthesis of mRNA and proteins by human peripheral blood neutrophils. J. Immunol., 1988, vol. 140, no. 12, pp. 4286–4293.
  36. Kaplan M. J., Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J. Immunol., 2012, vol. 189, no. 6, pp. 2689–2695. doi: 10.4049/jimmunol.1201719
  37. Klebanoff S.J., Kettle A.J., Rosen H. Winterbourn C.C., Nauseef W.M. Myeloperoxidase: a front-line defender against phagocytosed microorganisms. J. Leukoc. Biol., 2013, vol. 93, no. 2, pp. 185–198. doi: 10.1189/jlb.0712349
  38. Kobayashi S.D., De Leo F.R. Role of neutrophils in innate immunity: a systems biology-level approach. Wiley Interdiscip. Rev. Syst. Biol. Med., 2009, vol. 1, no. 3, pp. 309–333. doi: 10.1002/wsbm.32
  39. Kobayashi S.D., Voyich J.M., Buhl C.L., Stahl R.M., Deleo F.R. Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: cell fate is regulated at the level of gene expression. Proc. Nat. Acad. Sci. USA, 2002, vol. 99, pp. 6901–6906. doi: 10.1073/pnas.092148299
  40. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell, 2007, vol. 128, no. 4, pp. 707–719. doi: 10.1016/j.cell.2007.01.015
  41. Mantovani А., Cassatella M.C., 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
  42. Marcos V., Zou Z., Yildrim A.O., Bohla A., Hector A., Vitkov L., Wiedenbauer E.M., Krautgartner W.D., Stoiber W., Belohradsky B.H., Rieber N., Kormann M., Koller B., Roscher A., Roos D., Griese M., Eickelberg O., Döring G., Mall M.A., Hartl D. CXCR2 mediates NADPH oxidase-independent neutrophil extracellular trap formation in cystic fibrosis airway inf lammation. Nat Med., 2010, vol. 16, no. 9, pp. 1018–1023. doi: 10.1038/nm.2209
  43. Massberg S., Grahl L., Von Bruehl M.L., Manukyan D., Pfeiler S., Goosmann C., Brinkmann V., Lorenz M., Bidzhekov K., Khandagale A.B., Konrad I., Kennerknecht E., Reges K., Holdenrieder S., Braun S., Reinhardt C., Spannagl M., Preissner K.T., Engelmann B. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat. Med., 2010, vol. 16, no. 8, pp. 887–896. doi: 10.1038/nm.2184
  44. Matzinger P. Friendly and dangerous signals: is the tissue control? Nature Immunol. 2007, vol. 8, pp. 11–13. doi: 10.1038/ni0107-11
  45. Metelitsa L.S., Gillies S.D., Super M., Shimada H., Reynolds C.P., Seeger R.C. Antidisialogangliosid/granulocyte macrophagecolony-stimulating factor fusion protein facilitates neutrophil antibody-dependent cellular cytotoxicity and depends on FcγRII(CD32) and Mac-1 (CD11b/CD18) for enhanced effector cell adhesion and azurophil granule exocytosis. Blood, 2002, vol. 99, no. 11, pp. 4166–4173.
  46. Mócsai A. Diverse novel functions of neutrophils in immunity, inf lammation, and beyond. J. Exp. Med., 2013, vol. 210, no. 7, pp. 1283–1290. doi: 10.1084/jem.20122220
  47. Morrison A. J., Shen X. Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat. Rev. Mol. Cell Biol., 2009, no. 10, pp. 373–384. doi: 10.1038/nrm2693
  48. Ottonello L., Epstein A.L., Mancini M., Dapino P., Dallegri F. Monoclonal LYM-1 antibody-dependent cytotocsis by human neutrophils exposed to GM-CSF: auto-regulation of target cell attack by catepsin G. J. Leukoc. Biol., 2003, vol. 75, no. 1, pp. 99–105. doi: 10.1189/jlb.0403133
  49. 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
  50. Remijsen Q., Kuijpers T.W., Wirawan E., Lippens S., Vandenabeele P., Vanden Berghe T. NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ., 2011, vol. 18, pp. 581–588. doi: 10.1038/cdd.2011.1
  51. Smale S.T., Fisher A.G. Chromatin structure and gene regulation in the immune system. Annu. Rev. Immunol., 2002, vol. 20, pp. 427–462. doi: 10.1146/annurev.immunol.20.100301.064739
  52. Smuda C., Wechsler J.B., Bruce P.J. TLR-induced activation of neutrophils promotes histamine production via a P13 kinase dependent mechanism. J. Immunol. Lett., 2011, vol. 141, no. 1, pp. 102–108. doi: 10.1016/j.imlet.2011.08.002
  53. Tamassia N., Cassatella M.A. Cytoplasmic receptors recognizing nucleic acids and mediating immune functions in neutrophils. Curr. Opin. Pharmacol., 2013, vol. 13, no. 4, pp. 547–554. doi: 10.1016/j.coph.2013.05.003
  54. Tamassia N., Cassatella M.A., Bazzoni F. Fast and accurate quantitative analysis of cytokine gene expression in human neutrophils. Methods Mol. Biol., 2014, vol. 1124, pp. 451–467. doi: 10.1007/978-1-62703-845-4_ 27
  55. Vercauteren D., Piest M., Van der Aa L.J., Al Soraj M., Jones A.T., Engbersen J.F., De Smedt S.C., Braeckmans K. Flotillindependent endocytosis and a phagocytosis-like mechanism for cellular internalization of disulfide-based poly(amido amine)/ DNA polyplexes. Biomaterials, 2011, vol. 32, no. 11, pp. 3072–3084. doi: 10.1016/j.biomaterials.2010.12.045
  56. Wartha F., Beiter K., Albiger B., Fernebro J., Zychlinsky A., Normark S., Henriques-Normark B. Capsule and D-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell. Microbiol., 2007, vol. 9, no. 5, pp. 1162–1171. doi: 10.1111/j.1462-5822.2006.00857.x
  57. Winterbourn C.C., Kettle A.J. Redox reactions and microbial killing in the neutrophil phagosome. Antioxid. Redox Signal., 2013, vol. 18, no. 6, pp. 642–660. doi: 10.1089/ars.2012.4827
  58. 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
  59. Zhang X., Kluger Y., Nakayama Y., Poddar R., Whitney C., De Tora A., Weissman S.M., Newburger P.E. Gene expiession in mature neutrophils: early responses to inf lammatory stimuli. J. Leukoc. Biol., 2004, vol. 75, no. 2, pp. 358–372. doi: 10.1189/jlb.0903412

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