Neutrophil granulocytes: participation in homeostatic and reparative processes. Part II

Cover Page


Cite item

Full Text

Abstract

A supportive homeostatic function of neutrophilic granulocytes is accomplished in the physiology of diverse tissues and body systems. Neutrophils are found along the entire female reproductive tract (FRT), gradually declining in numbers from the upper parts towards the vagina. At the same time, both quantity and activity of FRT mucosal neutrophils are controlled by hormonal changes at different phases of menstrual cycle. Tissue neutrophils serve as an important source of broad-spectrum proteolytic enzymes such as matrix metalloproteinases and elastase necessary for extracellular matrix remodeling as well as vascular endothelial growth factor (VEGF) required for physiological FRT angiogenesis. During pregnancy, decidual neutrophils play a prominent role in vascular remodeling in pregnant uterus as well as development of maternal-fetal immune tolerance. The influx of neutrophils into the intestinal mucosa due to its trauma or infection not only ensures defense against pathogens, but also leads to increased proliferation of intestinal epithelial cells. Neutrophilic granulocytes elicit signals and events protective for the epithelium by marking them with a “hypoxic signature” to trigger transcription of the gene set responsible for production of mucins, mucin-modifying peptides, antimicrobial proteins, в-defensins, ultimately contributing to lesion healing and recovery of epithelial barrier function. “Inflammatory hypoxia” initiated by neutrophils and subsequent stabilization of the transcription factor hypoxia-induced factor (HIF) in intestinal epithelial cells trigger mechanisms of self-limited and resolved inflammation, which prevent excessive accumulation of neutrophils in the intestinal lumen and development of chronic inflammatory process. Neutrophilic granulocytes dominate in the oral cavity mucosa and comprise more than 95% of total leukocyte population recruited into the gingival sulcus and gingival fluid. Neutrophils maintain physiological amount and stability of symbiotic microflora composition in dental and gingival biofilms, counteracting pathogenic bacteria via phagocytosis, degranulation and extracellular trap formation, thereby ensuring healthy state in periodontal structures. Finally, similar to some other congenital disorders affecting neutrophil quantity and functions it was shown that in case of leukocyte adhesion deficiency type 1 (LAD-1) pathogenesis of periodontitis may not only be associated with a defect in their protective effector activity, but also with altered immunoregulatory function of tissue neutrophils.

About the authors

I. I. Dolgushin

South-Ural State Medical University

Email: alena_mez_75@mail.ru

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

Chelyabinsk

Россия

E. A. Mezentseva

South-Ural State Medical University

Author for correspondence.
Email: alena_mez_75@mail.ru

Elena A. Mezentseva - PhD (Medicine), Associate Professor, Department of Microbiology, Virology, Immunology and Clinical Laboratory Diagnostics.

454092, Chelyabinsk, Vorovskogo str., 64, Phone: +7 902 892-28-43 Россия

References

  1. Алиева М.С., Расулов И.М., Магомедов М.А., Мейланова Р.Д. Современные аспекты этиологии и патогенеза пародонтита // Известия Дагестанского государственного университета. Естественные и точные науки. 2013. № 1 (22). С. 25—29.
  2. Вольф Г.Ф., Хэссел Т.М. Пародонтология. Гигиенические аспекты. Пер. с англ.; под ред. Г.И. Ронь. М.: Медпресс-информ, 2014. 360 с.
  3. Долгушин И.И., Андреева Ю.С., Савочкина А.Ю. Нейтрофильные внеклеточные ловушки и методы оценки функционального статуса нейтрофилов. М.: Издательство РАМН, 2009. 208 с.
  4. Долгушин И.И., Бухарин О.В. Нейтрофилы и гомеостаз. Екатеринбург: УрО РАН, 2001. 288 с.
  5. Долгушин И.И., Мезенцева Е.А. Нейтрофильные гранулоциты: участие в гомеостатических и репаративных процессах. Часть I // Инфекция и иммунитет. 2020. Т. 10, № 4. С. 609—624.
  6. Лебедева О.П., Рудых Н.А., Полякова И.С., Пахомов С.П., Чурносов М.И., Самборская Н.И. Антимикробные пептиды первая линия антиинфекционной защиты женских половых путей // Научные ведомости Белгородского Государственного Университета. Серия: Медицина. Фармация. 2010. № 22 (93), вып. 12. С. 25—30.
  7. Степанова Т.Ю., Тимофеева А.В. Микробиом ротовой полости человека // Современные проблемы науки и образования. 2016. № 5. URL: http://www.science-education.ru/ru/article/view?id=25212 (In Russ.)]
  8. Хабибуллина А.Р., Тимофеева А.В. Микробиом дентальной бляшки человека // Современные проблемы науки и образования. 2017. № 3. URL: http://www.science-education.ru/ru/article/view?id=26539
  9. Aas J.A. Paster B.J., Stokes L.N., Olsen I., Dewhirst F.E. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol., 2005, vol. 43, no. 11,pp. 5721-5732. doi: 10.1128/JCM.43.11.5721-5732.2005
  10. Akiyama I., Yoshino O., Osuga Y., Shi J., Takamura M., Harada M., Koga K., Hirota Y., Hirata T., Fujii T., Saito S., Kozuma S. The role of bone morphogenetic protein 6 in accumulation and regulation of neutrophils in the human ovary. Reprod. Sci., 2014, vol. 21, iss. 6, pp. 772-777. doi: 10.1177/1933719113518988
  11. Amin M., Ho A.C., Lin J.Y., Batista da Silva A.P., Glogauer M., Ellen R.P. Induction of de novo subcortical actin filament assembly by Treponema denticola major outer sheath protein. Infect. Immun., 2004, vol. 72, no. 6, pp. 3650-3654. doi: 10.1128/IAI.72.6.3650-3654.2004
  12. Amsalem H., Kwan M., Hazan A., Zhang J., Jones R.L., Whittle W., Kingdom J.C., Croy B.A., Lye S.J., Dunk C.E. Identification of a novel neutrophil population: proangiogenic granulocytes in second-trimester human decidua. J. Immunol., 2014, vol. 193, iss. 6, pp. 3070-3079. doi: 10.4049/jimmunol.1303117
  13. Arck P.C., Hecher K. Fetomaternal immune cross-talk and its consequences for maternal and offspring’s health. Nat. Med., 2013, vol. 19, iss. 5, pp. 548-556. doi: 10.1038/nm.3160
  14. Armstrong G.M., Maybin J.A., Murray A.A., Nicol M., Walker C., Saunders P.T.K., Rossi A.G., Critchley H.O.D. Endometrial apoptosis and neutrophil infiltration during menstruation exhibits spatial and temporal dynamics that are recapitulated in a mouse model. Sci. Rep., 2017, vol. 7: 17416. doi: 10.1038/s41598-017-17565-x
  15. Berezow A.B., Darveau R.P. Microbial shift and periodontitis. Periodontology 2000, 2011, vol. 55, iss. 1, pp. 36-47. doi: 10.1111/j.1600-0757.2010.00350.x
  16. Bollapragada S., Youssef R., Jordan F., Greer I., Norman J., Nelson S. Term labor is associated with a core inflammatory response in human fetal membranes, myometrium, and cervix. Am. J. Obstet. Gynecol., 2009, vol. 200, iss. 1, pp. 104.e1-104.e11. doi: 10.1016/j.ajog.2008.08.032
  17. Brannstrom M., Enskog A. Leukocyte networks and ovulation. J. Reprod. Immunol., 2002, vol. 57, iss. 1-2, pp. 47-60. doi: 10.1016/S0165-0378(02)00009-8
  18. Brissette C.A., Pham T.T., Coats S.R., Darveau R.P., Lukehart S.A. Treponema denticola does not induce production of common innate immune mediators from primary gingival epithelial cells. Oral Microbiol. Immunol., 2008, vol. 23, iss. 6, pp. 474-481. doi: 10.1111/j.1399-302X.2008.00452.x
  19. Brown L.F., Detmar M., Claffey K., Nagy J.A., Feng D., Dvorak A.M., Dvorak H.F. Vascular permeability factor/vascular endothelial growth factor: a multifunctional angiogenic cytokine. EXS, 1997, vol. 79, pp. 233-269. doi: 10.1007/978-3-0348-9006-9_10
  20. Bukulmez O., Arici A. Leukocytes in ovarian functio. Hum. Reprod. Update, 2000, vol. 6, iss. 1, 15 p. doi: 10.1093/humupd/6.1.1
  21. Campbell E.L., Bruyninckx W.J., Kelly C.J., Glover L.E., McNamee E.N., Bowers B.E., Bayless A.J., Scully M., Saeedi B.J., Golden-Mason L., Ehrentraut S.F., Curtis V.F., Burgess A., Garvey J.F., Sorensen A., Nemenoff R., Jedlicka P., Taylor C.T., Kominsky D.J., Colgan S.P. Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation. Immunity, 2014, vol. 40, iss. 1, pp. 66-77. doi: 10.1016/j.immuni.2013.11.020
  22. Cortes-Vieyra R., Rosales C., Uribe-Querol E. Neutrophil functions in periodontal homeostasis. J. Immunol. Res., 2016, vol. 2016, 9 p. doi: 10.1155/2016/1396106
  23. Curtis M.A., Zenobia C., Darveau R.P. The relationship of the oral microbiota to periodontal health and disease. Cell. Host Microbe, 2011, vol. 10, iss. 4, pp. 302-306. doi: 10.1016/j.chom.2011.09.008
  24. Dababneh R., Al-Wahadneh A.M., Hamadneh S., Khouri A., Bissada N.F. Periodontal manifestation of leukocyte adhesion deficiency type I. J. Periodontol., 2008, vol. 79, iss. 4, pp. 764-768. doi: 10.1902/jop.2008.070323
  25. Darveau R.P. Periodontitis: a polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol., 2010, vol. 8, iss. 7, pp. 481-490. doi: 10.1038/nrmicro2337
  26. Darveau R.P., Belton C.M., Reife R.A., Lamont R.J. Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infect. Immun., 1998, vol. 66, no. 4, pp. 1660-1665.
  27. Dashper S.G., Seers C.A., Tan K.H., Reynolds E.C. Virulence factors of the oral spirochete Treponema denticola. J. Dental Res., 2011, vol. 90, iss. 6, pp. 691-703. doi: 10.1177%2F0022034510385242
  28. Deas D.E., Mackey S.A., McDonnell H.T. Systemic disease and periodontitis: manifestations of neutrophil dysfunction. Periodontology 2000, 2003, vol. 32, iss. 1, pp. 82-104. doi: 10.1046/j.0906-6713.2003.03207.x
  29. Delima A.J., Van Dyke T.E. Origin and function of the cellular components in gingival crevice fluid. Periodontology 2000, 2003, vol. 31, iss. 1, pp. 55-76. doi: 10.1034/j.1600-0757.2003.03105.x
  30. Dewhirst F.E., Chen T., Izard J., Paster B.J., Tanner A.C., Yu W.H., Lakshmanan A., Wade W.G. The human oral microbiome. J. Bacteriol., 2010, vol. 192, no. 19, pp. 5002-5017. doi: 10.1128/JB.00542-10
  31. Dixon D.R., Bainbridge B.W., Darveau R.P. Modulation of the innate immune response within the periodontium. Periodontology 2000, 2004, vol. 35, iss. 1, pp. 53-74. doi: 10.1111/j.0906-6713.2004.003556.x
  32. Dunbar B., Patel M., Fahey J., Wira C. Endocrine control of mucosal immunity in the female reproductive tract: impact of environmental disruptors. Mol. Cell. Endocrinol., 2012, vol. 354, iss. 1-2, pp. 85-93. doi: 10.1016/j.mce.2012.01.002
  33. Dvorak H.F., Brown L.F., Detmar M., Dvorak A.M. Vascular permeability factor/vascular endothelial growth factor, microvas-cular hyperpermeability, and angiogenesis. Am. J. Pathol., 1995, vol. 146, no. 5, pp. 1029-1039.
  34. Ferrara N., Davis-Smyth T. The biology of vascular endothelial growth factor. Endocrine Rev., 1997, vol. 18, iss. 1, pp. 4-25. doi: 10.1210/edrv.18.1.0287
  35. Fine N., Hassanpour S., Borenstein A., Sima C., Oveisi M., Scholey J., Cherney D., Glogauer M. Distinct oral neutrophil subsets define health and periodontal disease states. J. Dental Res., 2016, vol. 95, iss. 8, pp. 931-938. doi: 10.1177/0022034516645564
  36. Fischbach M.A., Sonnenburg J.L. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe, 2011, vol. 10, iss. 4, pp. 336-347. doi: 10.1016/j.chom.2011.10.002
  37. Flannigan K.L., Ngo V.L., Geem D., Harusato A., Hirota S.A., Parkos C.A., Lukacs N.W., Nusrat A., Gaboriau-Routhiau V., Cerf-Bensussan N., Gewirtz A.T., Denning T.L. IL-17A-mediated neutrophil recruitment limits expansion of segmented filamentous bacteria. Mucosal Immunol., 2017, vol. 10, iss. 3, pp. 673-684. doi: 10.1038/mi.2016.80
  38. Fournier B.M., Parkos C.A. The role of neutrophils during intestinal inflammation. Mucosal Immunol., 2012, vol. 5, pp. 354-366. doi: 10.1038/mi.2012.24
  39. 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, iss. 3, pp. 183-194. doi: 10.1016%2Fj.ccr.2009.06.017
  40. Fujioka M., Sasa R., Inoue M., Nakamura M. Immunological characterization of junctional epithelium: an immunohistochemical study. Dental Med. Res., 2009, vol. 29, iss. 3, pp. 253-258. doi: 10.7881/dentalmedres.29.253
  41. Gargett C.E., Lederman F., Heryanto B., Gambino L.S., Rogers P.A. Focal vascular endothelial growth factor correlates with angiogenesis in human endometrium. Role of intravascular neutrophils. Hum. Reprod., 2001, vol. 16, iss. 6, pp. 1065-1075. doi: 10.1093/humrep/16.6.1065
  42. Gasparoto T.H., Vieira N.A., Porto V.C., Campanelli A.P., Lara V.S. Differences between salivary and blood neutrophils from elderly and young denture wearers. J. Oral. Rehabil., 2011, vol. 38, iss. 1, pp. 41-51. doi: 10.1111/j.1365-2842.2010.02126.x
  43. Giaglis S., Stoikou M., Grimolizzi F., Subramanian B.Y., van Breda S.V., Hoesli I., Lapaire O., Hasler P., Than N.G., Hahn S. Neutrophil migration into the placenta: good, bad or deadly? Cell Adh. Migr., 2016, vol. 10, iss. 1-2, pp. 208-225. doi: 10.1080/19336918.2016.1148866
  44. Giaglis S., Stoikou M., Sur Chowdhury C., Schaefer G., Grimolizzi F., Rossi S.W., Hoesli I.M., Lapaire O., Hasler P., Hahn S. Multimodal regulation of NET formation in pregnancy: Progesterone antagonizes the Pro-NETotic effect of estrogen and G-CSF. Front. Immunol., 2016, vol. 7: 565. doi: 10.3389/fimmu.2016.00565
  45. Gomez-Lopez N., StLouis D., Lehr M.A., Sanchez-Rodriguez E.N., Arenas-Hernandez M. Immune cells in term and preterm labor. Cell. Mol. Immunol., 2014, vol. 11, iss. 6, pp. 571-581. doi: 10.1038/cmi.2014.46
  46. Gonzalez J.M., Xu H., Chai J., Ofori E., Elovitz M.A. Preterm and term cervical ripening in CD1 mice (Mus musculus): similar or divergent molecular mechanisms? Biol. Reprod., 2009, vol. 81, iss. 6, pp. 1226-1232. doi: 10.1095/biolreprod.108.075309
  47. Greer A., Irie K., Hashim A., Leroux B.G., Chang A.M., Curtis M.A., Darveau R.P. Site-specific neutrophil migration and CXCL2 expression in periodontal tissue. J. Dental Res., 2016, vol. 95, iss. 8, pp. 946-952. doi: 10.1177%2F0022034516641036
  48. Groeger S., Meyle J. Oral Mucosal Epithelial Cells. Front. Immunol., 2019, vol. 10: 208. doi: 10.3389/fimmu.2019.00208
  49. Hahn S., Giaglis S., Hoesli I., Hasler P. Neutrophil NETs in reproduction: from infertility to preeclampsia and the possibility of fetal loss. Front. Immunol., 2012, vol. 3: 362. doi: 10.3389/fimmu.2012.00362
  50. Hahn S., Hasler P., Vokalova L., van Breda S.V., Lapaire O., Than G.N., Hoesli I., Rossi S.W. The role of neutrophil activation in determining the outcome of pregnancy and modulation by hormones and/or cytokines. Clin. Exp. Immunol., 2019. doi: 10.1111/cei.13278
  51. Hajishengallis E., Hajishengallis G. Neutrophil homeostasis and periodontal health in children and adults. J. Dental Res., 2014, vol. 93, iss. 3, pp. 231-237. doi: 10.1177/0022034513507956
  52. Hajishengallis G., Darveau R.P., Curtis M.A. The keystone-pathogen hypothesis. Nat. Rev. Microbiol., 2012, vol. 10, pp. 717-725. doi: 10.1038/nrmicro2873
  53. Hajishengallis G., Chavakis T., Hajishengallis E., Lambris J.D. Neutrophil homeostasis and inflammation: novel paradigms from studying periodontitis. J. Leukoc. Biol., 2015, vol. 98, iss. 4, pp. 539-548. doi: 10.1189/jlb.3VMR1014-468R
  54. Hall C.H.T., Campbell E.L., Colgan S.P. Neutrophils as components of mucosal homeostasis. Cell. Mol. Gastroenterol. Hepatol., 2017, vol. 4, iss. 3, pp. 329-337. doi: 10.1016/j.jcmgh.2017.07.001
  55. Horne A.W., Stock S.J., King A.E. Innate immunity and disorders of the female reproductive tract. Reproduction, 2008, vol. 135, iss. 6, pp. 739-749. doi: 10.1530/REP-07-0564
  56. Ji S., Choi Y. Innate immune response to oral bacteria and the immune evasive characteristics of periodontal pathogens. J. Periodontal. Implant. Sci., 2013, vol. 43, iss. 1, pp. 3-11. doi: 10.5051/jpis.2013.43.1.3
  57. Jiemtaweeboon S., Shirasuna K., Nitta A., Kobayashi A., Schuberth H., Shimizu T., Miyamoto A. Evidence that polymorphonuclear neutrophils infiltrate into the developing corpus luteum and promote angiogenesis with interleukin-8 in the cow. Reprod. Biol. Endocrinol., 2011, vol. 9: 79. doi: 10.1186/1477-7827-9-79
  58. Junqueira L.C., Zugaib M., Montes G.S., Toledo O.M., Krisztan R.M., Shigihara K.M. Morphologic and histochemical evidence for the occurrence of collagenolysis and for the role of neutrophilic polymorphonuclear leukocytes during cervical dilation. Am. J. Obstet. Gynecol., 1980, vol. 138, iss. 3, pp. 273-281. doi: 10.1016/0002-9378(80)90248-3
  59. Kaitu’u T.J., Shen J., Zhang J., Morison N.B., Salamonsen L.A. Matrix metalloproteinases in endometrial breakdown and repair: functional significance in a mouse model. Biol. Reprod., 2005, vol. 73, iss. 4, pp. 672-680. doi: 10.1095/biolreprod.105.042473
  60. Kaitu’u-Lino T.J., Morison N.B., Salamonsen L.A. Neutrophil depletion retards endometrial repair in a mouse model. Cell Tissue Res., 2007, vol. 328, iss. 1, pp. 197-206. doi: 10.1007/s00441-006-0358-2
  61. Kelly C.J., Zheng L., Campbell E.L., Saeedi B., Scholz C.C., Bayless A.J., Wilson K.E., Glover L.E., Kominsky D.J., Magnuson A., Weir T.L., Ehrentraut S.F., Pickel C., Kuhn K.A., Lanis J.M., Nguyen V., Taylor C.T., Colgan S.P. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe, 2015, vol. 17, iss. 5, pp. 662-671. doi: 10.1016/j.chom.2015.03.005
  62. Khajan M. Role of neutrophils in disease pathogenesis. InTechOpen, 2017. 178 p. doi: 10.5772/65581
  63. Kinane D.F., Hart T.C. Genes and gene polymorphisms associated with periodontal disease. Crit. Rev. Oral Biol. Med., 2003, vol. 14, iss. 6, pp. 430-449. doi: 10.1177%2F154411130301400605
  64. King A.E., Critchley H.O., Sallenave J.M., Kelly R.W. Elafin in human endometrium: an antiprotease and antimicrobial molecule expressed during menstruation. J. Clin. Endocrinol. Metab., 2003, vol. 88, iss. 9, pp. 4426-4431. doi: 10.1210/jc.2003-030239
  65. Koch S., Capaldo C.T., Hilgarth R.S., Fournier B., Parkos C.A., Nusrat A. Protein kinase CK2 is a critical regulator of epithelial homeostasis in chronic intestinal inflammation. Mucosal Immunol., 2013, vol. 6, pp. 136-145. doi: 10.1038/mi.2012.57
  66. 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., Muller I. Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur. J. Immunol., 2007, vol. 37, iss. 4, pp. 935-945. doi: 10.1002/eji.200636542
  67. Landzberg M., Doering H., Aboodi G.M., Tenenbaum H.C., Glogauer M. Quantifying oral inflammatory load: oral neutrophil counts in periodontal health and disease. J. Periodontal. Res., 2015, vol. 50, iss. 3, pp. 330-336. doi: 10.1111/jre.12211
  68. Lasarte S., Samaniego R., Salinas-Munoz L., Guia-Gonzalez M.A., Weiss L.A., Mercader E., Ceballos-Garcia E., Navarro-Gonzalez T., Moreno-Ochoa L., Perez-Millan F., Pion M., Sanchez-Mateos P., Hidalgo A., Munoz-Fernandez M.A., Relloso M. Sex hormones coordinate neutrophil immunity in the vagina by controlling chemokine gradients. J. Infect. Dis., 2016, vol. 213, iss. 3, pp. 476—484. doi: 10.1093/infdis/jiv402
  69. Lathbury L.J., Salamonsen L.A. In vitro studies of the potential role of neutrophils in the process of menstruation. Mol. Hum. Reprod., 2000, vol. 6, iss. 10, pp. 899—906. doi: 10.1093/molehr/6.10.899
  70. Lee S.K., Kim C.J., Kim D.J., Kang J.H. Immune cells in the female reproductive tract. Immune Network, 2015, vol. 15, iss. 1, pp. 16-26. doi: 10.4110/in.2015.15.1.16
  71. Leiding J.W. Neutrophil evolution and their diseases in humans. Front. Immunol., 2017, vol. 8: 1009. doi: 10.3389/fimmu.2017.01009
  72. Li S., Herrera G.G., Tam K.K., Lizarraga J.S., Beedle M.T., Winuthayanon W. Estrogen action in the epithelial cells of the mouse vagina regulates neutrophil infiltration and vaginal tissue integrity. Sci. Rep., 2018, vol. 8: 11247. doi: 10.1038/s41598-018-29423-5
  73. Louis N.A., Hamilton K.E., Kong T., Colgan S.P. HIF-dependent induction of apical CD55 coordinates epithelial clearance of neutrophils. FASEB J., 2005, vol. 19, no. 8, pp. 950-959. doi: 10.1096/fj.04-3251com
  74. Luissint A.C., Parkos C.A., Nusrat A. Inflammation and the intestinal barrier: leukocyte-epithelial cell interactions, cell junction remodeling, and mucosal repair. Gastroenterology, 2016, vol. 151, iss. 4, pp. 616-632. doi: 10.1053/j.gastro.2016.07.008
  75. Magalhaes M.A., Sun C.X., Glogauer M., Ellen R.P. The major outer sheath protein of Treponema denticola selectively inhibits Rac1 activation in murine neutrophils. Cell. Microbiol., 2008, vol. 10, iss. 2, pp. 344-354. doi: 10.1111/j.1462-5822.2007.01045.x
  76. Mager D.L., Ximenez-Fyvie L.A., Haffajee A.D., Socransky S.S. Distribution of selected bacterial species on intraoral surfaces. J. Clin. Periodontol., 2003, vol. 30, iss. 7, pp. 644-654. doi: 10.1034/j.1600-051X.2003.00376.x
  77. Manresa M.C., Taylor C.T. Hypoxia inducible factor (HIF) hydroxylases as regulators of intestinal epithelial barrier function. Cell. Mol. Gastroenterol. Hepatol., 2017, vol. 3, iss. 3, pp. 303-315. doi: 10.1016/j.jcmgh.2017.02.004
  78. Marder W., Knight J.S., Kaplan M.J., Somers E.C., Zhang X., O’Dell A.A., Padmanabhan V., Lieberman R.W. Placental histology and neutrophil extracellular traps in lupus and pre-eclampsia pregnancies. Lupus Sci. Med., 2016, vol. 3, iss. 1: e000134. doi: 10.1136/lupus-2015-000134
  79. Matthews J.D., Weight C.M., Parkos C.A. Leukocyte-epithelial interactions and mucosal homeostasis. Toxicol Pathol., 2014, vol. 42, iss. 1, pp. 91-98. doi: 10.1177%2F0192623313511336
  80. Menning A., Walter A., Rudolph M., Gashaw I., Fritzemeier K.H., Roese L. Granulocytes and vascularization regulate uterine bleeding and tissue remodeling in a mouse menstruation model. PLoS One, 2012, vol. 7, iss. 8: e41800. doi: 10.1371/journal.pone.0041800
  81. Mittal P., Romero R., Tarca A.L., Gonzalez J., Draghici S., Xu Y., Dong Z., Nhan-Chang C.L., Chaiworapongsa T., Lye S., Kusanovic J.P., Lipovich L., Mazaki-Tovi S., Hassan S.S., Mesiano S., Kim C.J. Characterization of the myometrial transcriptome and biological pathways of spontaneous human labor at term. J. Perinat. Med., 2010, vol. 38, iss. 6, pp. 617-643. doi: 10.1515/jpm.2010.097
  82. Mohanty T., Sjogren J., Kahn F., Abu-Humaidan A.H., Fisker N., Assing K., Morgelin M., Bengtsson A.A., Borregaard N., S0rensen O.E. A novel mechanism for NETosis provides antimicrobial defense at the oral mucosa. Blood, 2015, vol. 126, iss. 18, pp. 2128-2137. doi: 10.1182/blood-2015-04-641142
  83. Moutsopoulos N.M., Konkel J.E. Tissue-specific immunity at the oral mucosal barrier. Trends Immunol., 2018, vol. 39, iss. 4, pp. 276-287. doi: 10.1016/j.it.2017.08.005
  84. Moutsopoulos N.M., Lionakis M.S., Hajishengallis G. Inborn errors in immunity: unique natural models to dissect oral immunity. J. Dental Res., 2015, vol. 94, iss. 6, pp. 753-758. doi: 10.1177%2F0022034515583533
  85. Moutsopoulos N.M., Konkel J., Sarmadi M., Eskan M.A., Wild T., Dutzan N., Abusleme L., Zenobia C., Hosur K.B., Abe T., Uzel G., Chen W., Chavakis T., Holland S.M., Hajishengallis G. Defective neutrophil recruitment in leukocyte adhesion deficiency Type I disease causes local IL-17-driven Inflammatory bone loss. Sci. Transl. Med., 2014, vol. 6, iss. 229, pp. 229ra40. doi: 10.1126/scitranslmed.3007696
  86. Nakamura M. Histological and immunological characteristics of the junctional epithelium. Jpn. Dent. Sci. Rev., 2018, vol. 54, iss. 2, pp. 59-65. doi: 10.1016/j.jdsr.2017.11.004
  87. Nicolas-Avila J.A., Adrover J.M., Hidalgo A. Neutrophils in homeostasis, immunity, and cancer. Immunity, 2017, vol. 46, iss. 1, pp. 15-28. doi: 10.1016/j.immuni.2016.12.012
  88. Nicu E.A., Rijkschroeff P., Wartewig E., Nazmi K., Loos B.G. Characterization of oral polymorphonuclear neutrophils in periodontitis patients: a case-control study. BMC Oral Health, 2018, vol. 18: 149. doi: 10.1186/s12903-018-0615-2
  89. Nussbaum G., Shapira L. How has neutrophil research improved our understanding of periodontal pathogenesis? J. Clin. Periodontol., 2011, vol. 38, iss. s11, Special Issue: Proceedings of the 7th European Workshop on Periodontology, pp. 49-59. doi: 10.1111/j.1600-051X.2010.01678.x
  90. Ochiel D.O., Fahey J.V., Ghosh M., Haddad S.N., Wira C.R. Innate immunity in the female reproductive tract: role of sex hormones in regulating uterine epithelial cell protection against pathogens. Curr. Womens Health Rev., 2008, vol. 4, iss. 2, pp. 102117. doi: 10.2174/157340408784246395
  91. Olsen I., Hajishengallis G. Major neutrophil functions subverted by Porphyromonas gingivalis. J. Oral. Microbiol., 2016, vol. 8: 30936. doi: 10.3402/jom.v8.30936
  92. Osmers R., Rath W., Adelmann-Grill B.C., Fittkow C., Kuloczik M., Szeverenyi M., Tschesche H., Kuhn W. Origin of cervical collagenase during parturition. Am. J. Obstet. Gynecol., 1992, vol. 166, iss. 5, pp. 1455-1460. doi: 10.1016/0002-9378(92)91619-L
  93. Parkos C.A. Neutrophil-epithelial interactions: a double-edged sword. Am. J. Pathol., 2016, vol. 186, iss. 6, pp. 1404-1416. doi: 10.1016/j.ajpath.2016.02.001
  94. Paster B.J., Olsen I., Aas J.A., Dewhirst F.E. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontology, 2006, vol. 42, iss. 1, pp. 80-87. doi: 10.1111/j.1600-0757.2006.00174.x
  95. Puthengady Thomas B., Sun C.X., Bajenova E., Ellen R.P., Glogauer M. Modulation of human neutrophil functions in vitro by Treponema denticola major outer sheath protein. Infect. Immun., 2006, vol. 74, no. 3, pp. 1954-1957. doi: 10.1128/IAI.74.3.1954-1957.2006
  96. Reis Machado J., da Silva M.V., Cavellani C.L., dos Reis M.A., Monteiro M.L., Teixeira Vde P., Miranda Correa R.R. Mucosal immunity in the female genital tract, HIV/AIDS. BioMed Res. Int., 2014, vol. 2014, 20 p. doi: 10.1155/2014/350195
  97. Rijkschroeff P., Loos B.G., Nicu E.A. Impaired polymorphonuclear neutrophils in the oral cavity of edentulous individuals. Eur. J. Oral Sci., 2017, vol. 125, iss. 5, pp. 371-378. doi: 10.1111/eos.12367
  98. Rijkschroeff P., Loos B.G., Nicu E.A. Oral polymorphonuclear neutrophil contributes to oral health. Curr. Oral Health Rep., 2018, vol. 5, pp. 211-220. doi: 10.1007/s40496-018-0199-6
  99. Rijkschroeff P., Jansen I.D., van der Weijden F.A., Keijser B.J., Loos B.G., Nicu E.A. Oral polymorphonuclear neutrophil characteristics in relation to oral health: a cross-sectional, observational clinical study. Int. J. Oral Sci., 2016, vol. 8, iss. 3, pp. 191-198. doi: 10.1038/ijos.2016.23
  100. Ryder M.I. Comparison of neutrophil functions in aggressive and chronic periodontitis. Periodontology 2000, 2010, vol. 53, iss. 1, pp. 124-137. doi: 10.1111/j.1600-0757.2009.00327.x
  101. Sakamoto Y., Moran P., Bulmer J.N., Searle R.F., Robson S.C. Macrophages and not granulocytes are involved in cervical ripening. J. Reprod. Immunol., 2005, vol. 66, iss. 2, pp. 161-173. doi: 10.1016/j.jri.2005.04.005
  102. Sakamoto Y., Moran P., Searle R.F., Bulmer J.N., Robson S.C. Interleukin-8 is involved in cervical dilatation but not in prelabour cervical ripening. Clin. Exp. Immunol., 2004, vol. 138, iss. 1, pp. 151-157. doi: 10.1111/j.1365-2249.2004.02584.x
  103. Salamonsen L.A., Woolley D.E. Menstruation: induction by matrix metalloproteinases and inflammatory cells. J. Reprod. Immunol., 1999, vol. 44, iss. 1-2, 27 p. doi: 10.1016/S0165-0378(99)00002-9
  104. Salinas-Munoz L., Campos-Fernandez R., Mercader E., Olivera-Valle I., Fernandez-Pacheco C., Matilla L., Garcia-Bordas J., Brazil J.C., Parkos C.A., Asensio F., Munoz-Fernandez M.A., Hidalgo A., Sanchez-Mateos P., Samaniego R., Relloso M. Estrogen receptor-alpha (ESR1) governs the lower female reproductive tract vulnerability to Candida albicans. Front. Immunol., 2018, vol. 9: 1033. doi: 10.3389/fimmu.2018.01033
  105. Schmidt S., Moser M., Sperandio M. The molecular basis of leukocyte recruitment and its deficiencies. Mol. Immunol., 2012, vol. 55, iss. 1, pp. 49-58. doi: 10.1016/j.molimm.2012.11.006
  106. Sela M.N. Role of Treponema denticola in periodontal diseases. Crit. Rev. Oral Biol. Med., 2001, vol. 12, iss. 5, pp. 399-413. doi: 10.1177/10454411010120050301
  107. Shaul M.E., Fridlender Z.G. Cancer related circulating and tumor-associated neutrophils — subtypes, sources and function. FEBS J., 2018, vol. 285, iss. 23, pp. 4316-4342. doi: 10.1111/febs.14524
  108. Shirasuna K., Jiemtaweeboon S., Raddatz S., Nitta A., Schuberth H.J., Bollwein H., Shimizu T., Miyamoto A. Rapid accumulation of polymorphonuclear neutrophils in the Corpus luteum during prostaglandin F(2a)-induced luteolysis in the cow. PLoS One, 2012, vol. 7, iss. 1: e29054. doi: 10.1371/journal.pone.0029054
  109. Shynlova O., Nedd-Roderique T., Li Y., Dorogin A., Nguyen T., Lye S.J. Infiltration of myeloid cells into decidua is a critical early event in the labour cascade and post-partum uterine remodelling. J. Cell. Mol. Med., 2013, vol. 17, iss. 2, pp. 311-324. doi: 10.1111/jcmm.12012
  110. Singh N., Herbert B., Sooranna G.R., Orsi N.M., Edey L., Dasgupta T., Sooranna S.R., Yellon S.M., Johnson M.R. Is myometrial inflammation a cause or a consequence of term human labour? J. Endocrinol., 2017, vol. 235, iss. 1, pp. 69-83. doi: 10.1530/JOE-17-0318
  111. Ssemaganda A., Kindinger L., Bergin P., Nielsen L., Mpendo J., Ssetaala A., Kiwanuka N., Munder M., Teoh T.G., Kropf P., Muller I. Characterization ofneutrophil subsets in healthy human pregnancies. PLoS One, 2014, vol. 9, iss. 2: e85696. doi: 10.1371/journal.pone.0085696
  112. Stanley R.L., Ohashi T., Gordon J., Mowa C.N. A proteomic profile of postpartum cervical repair in mice. J. Mol. Endocrinol., 2018, vol. 60, iss. 1, pp. 17-28. doi: 10.1530/JME-17-0179
  113. 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, iss. 3, pp. 285-294. doi: 10.1016/j.immuni.2005.01.011
  114. Stocco C., Telleria C., Gibori G. The molecular control of corpus luteum formation, function, and regression. Endocr. Rev., 2007, vol. 28, iss. 1, pp. 117-149. doi: 10.1210/er.2006-0022
  115. Sugino N., Okuda K. Species-related differences in the mechanism of apoptosis during structural luteolysis. J. Reprod. Dev., 2007, vol. 53, iss. 5, pp. 977-986. doi: 10.1262/jrd.19047
  116. Sumagin R., Brazil J.C., Nava P., Nishio H., Alam A., Luissint A.C., Weber D.A., Neish A.S., Nusrat A., Parkos C.A. Neutrophil interactions with epithelial expressed ICAM-1 enhances intestinal mucosal wound healing. Mucosal Immunol., 2016, vol. 9, iss. 5, pp. 1151-1162. doi: 10.1038/mi.2015.135
  117. Sumagin R., Parkos C.A. Epithelial adhesion molecules and the regulation of intestinal homeostasis during neutrophil transepi-thelial migration. Tissue Barriers, 2015, vol. 3, iss. 1-2: e969100. doi: 10.4161/21688362.2014.969100
  118. Sumagin R., Robin A.Z., Nusrat A., Parkos C.A. Transmigrated neutrophils in the intestinal lumen engage ICAM 1 to regulate the epithelial barrier and neutrophil recruitment. Mucosal Immunol., 2014, vol. 7, iss. 4, pp. 905-915. doi: 10.1038/mi.2013.106
  119. Talbott H., Delaney A., Zhang P., Yu Y., Cushman R.A., Cupp A.S., Hou X., Davis J.D. Effects of IL8 and immune cells on the regulation of luteal progesterone secretion. Reproduction, 2014, vol. 148, iss. 1, pp. 21-31. doi: 10.1530/REP-13-0602
  120. Tawara F., Tamura N., Suganuma N., Kanayama N. Changes in cervical neutrophil elastase levels during the menstrual cycle. Reprod. Med. Biol., 2012, vol. 11, iss. 1, pp. 65-68. doi: 10.1007/s12522-011-0104-7
  121. Thomson A.J., Telfer J.F., Young A., Campbell S., Stewart C.J., Cameron I.T., Greer I.A., Norman J.E. Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Human Reprod., 1999, vol. 14, iss. 1, pp. 229-236. doi: 10.1093/humrep/15.1.229
  122. Timmons B., Akins M., Mahendroo M. Cervical remodeling during pregnancy and parturition. Trends Endocrinol. Metab., 2010, vol. 21, iss. 6, pp. 353-361. doi: 10.1016/j.tem.2010.01.011
  123. Timmons B.C., Fairhurst A.M., Mahendroo M.S. Temporal changes in myeloid cells in the cervix during pregnancy and parturition. J. Immunol., 2009, vol. 182, iss. 5, pp. 2700-2707. doi: 10.4049/jimmunol.0803138
  124. Timmons B.C., Mahendroo M.S. Timing of neutrophil activation and expression of proinflammatory markers do not support a role for neutrophils in cervical ripening in the mouse. Biol. Reprod., 2006, vol. 74, iss. 2, pp. 236-245. doi: 10.1095/biolreprod.105.044891
  125. Tinsley J.H., Wu M.H., Ma W.Y., Taulman A.C., Yuan S.Y. Activated neutrophils induce hyperpermeability and phosphorylation of adherens junction proteins in coronary venular endothelial cells. J. Biol. Chem., 1999, vol. 274, no. 35, pp. 24930—24934. doi: 10.1074/jbc.274.35.24930
  126. Tsukamoto Y., Usui M., Yamamoto G., Takagi Y., Tachikawa T., Yamamoto M., Nakamura M. Role of the junctional epithelium in periodontal innate defense and homeostasis. J. Periodontal. Res., 2012, vol. 47, iss. 6, pp. 750—757. doi: 10.1111/j.1600-0765.2012.01490.x
  127. Uriarte S.M., Edmisson J.S., Jimenez-Flores E. Human neutrophils and oral microbiota: a constant tug-of-war between a harmonious and a discordant coexistence. Immunol. Rev., 2016, vol. 273, iss. 1, special iss.: Neutrophils, pp. 282—298. doi: 10.1111/imr.12451
  128. Vincent A.J., Malakooti N., Zhang J., Rogers P.A.W., Affandi B., Salamonsen L.A. Endometrial breakdown in women using Norplant is associated with migratory cells expressing matrix metalloproteinase-9 (gelatinase B). Hum. Reprod., 1999, vol. 14, iss. 3, pp. 807-815. doi: 10.1093/humrep/14.3.807
  129. Wade W.G. The oral microbiome in health and disease. Pharmacol. Res., 2013, vol. 69, iss. 1, pp. 137-143. doi: 10.1016/j.phrs.2012.11.006
  130. Webb C.R., Koboziev I., Furr K.L., Grisham M.B. Protective and pro-inflammatory roles of intestinal bacteria. Pathophysiology, 2016, vol. 23, iss. 2, pp. 67-80. doi: 10.1016/j.pathophys.2016.02.002
  131. Winkler M., Fischer D.C., Ruck P., Marx T., Kaiserling E., Oberpichler A., Tschesche H., Rath W. Parturition at term: parallel increases in interleukin-8 and proteinase concentrations and neutrophil count in the lower uterine segment. Hum. Reprod., 1999, vol. 14, iss. 4, pp. 1096-1000. doi: 10.1093/humrep/14.4.1096
  132. Winter S.E., Winter M.G., Xavier M.N., Thiennimitr P., Poon V., Keestra A.M., Laughlin R.C., Gomez G., Wu J., Lawhon S.D., Popova I.E., Parikh S.J., Adams L.G., Tsolis R.M., Stewart V.J., Baumler A.J. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science, 2013, vol. 339, iss. 6120, pp. 708-711. doi: 10.1126/science.1232467
  133. Wira C.R., Fahey J.V., Sentman C.L., Pioli P.A., Shen L. Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunol. Rev., 2005, vol. 206, iss. 1, pp. 306-335. doi: 10.1111/j.0105-2896.2005.00287.x
  134. Wira C.R., Rodriguez-Garcia M., Patel M.V. The role of sex hormones in immune protection of the female reproductive tract. Nat. Rev. Immunol., 2015, vol. 15, iss. 4, pp. 217-230. doi: 10.1038/nri3819
  135. Yamazaki T., Miyamoto M., Yamada S., Okuda K., Ishihara K. Surface protease of Treponema denticola hydrolyzes C3 and influences function of polymorphonuclear leukocytes. Microbes Infect., 2006, vol. 8, iss. 7, pp. 1758-1763. doi: 10.1016/j.micinf.2006.02.013
  136. Yeaman G.R., Collins J.E., Currie J.K., Guyre P.M., Wira C.R., Fanger M.W. IFN-y is produced by polymorphonuclear neutrophils in human uterine endometrium and by cultured peripheral blood polymorphonuclear neutrophils. J. Immunol., vol. 160, iss. 10, pp. 5145-5153.
  137. Yellon S.M. Contributions to the dynamics of cervix remodeling prior to term and preterm birth. Biol. Reprod., 2017, vol. 96, iss. 1, pp. 13-23. doi: 10.1095/biolreprod.116.142844
  138. Yoon M.Y., Yoon S.S. Disruption of the gut ecosystem by antibiotics. Yonsei Med. J., 2018, vol. 59, iss. 1, pp. 4-12. doi: 10.3349/ymj.2018.59.1.4
  139. Zaura E., Keijser B.J.F., Huse S.M., Crialaard W. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol., 2009, vol. 9: 259. doi: 10.1186/1471-2180-9-259
  140. Zenobia C., Luo X.L., Hashim A., Abe T., Jin L., Chang Y., Jin Z.C., Sun J.X., Hajishengallis G., Curtis M.A., Darveau R.P. Commensal bacteria-dependent select expression of CXCL2 contributes to periodontal tissue homeostasis. Cell. Microbiol., 2013, vol. 15, iss. 8, pp. 1419-1426. doi: 10.1111/cmi.12127
  141. Zhao H., Kalish F., Wong R.J., Stevenson D.K. Infiltration of myeloid cells in the pregnant uterus is affected by heme oxyge-nase-1. J. Leukoc. Biol., 2017, vol. 101, iss. 1, pp. 217-226. doi: 10.1189/jlb.1A0116-020RR
  142. Zindl C.L., Lai J.F., Lee Y.K., Maynard C.L., Harbour S.N., Ouyang W., Chaplin D.D., Weaver C.T. IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc. Natl. Acad. Sci. USA, 2013, vol. 110, iss. 31, pp. 12768-12773. doi: 10.1073/pnas.1300318110

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2021 Dolgushin I.I., Mezentseva E.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies