THE ROLE OF INNATE IMMUNITY RECEPTORS (TLRs) IN MAINTAINING THE HOMEOSTASIS OF THE FEMALE GENITAL TRACT IN DEVELOPING PREGNANCY AND INTRAUTERINE INFECTION

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Abstract

The aim of the present systematic literature review is to summarize data on the role of TLRs in maintaining homeostasis of the female genitals, in maintaining the physiological development of pregnancy, provision of anti-infective resistance in pregnant women with intrauterine infection. The review substantiates the importance of TLRs of female genitals as a necessary and determining factor in the reaction to various changes in the environment, and also responsible for changes in metabolic, structural, or energy, in the maintenance of anti-infective resistance and homeostasis. As universal regulators of vital activity of organism TLRs in conjunction with other receptors of innate immunity provide maintaining the general reactivity and anti-infective resistance at the physiological level. In physiologically developing pregnancy in a background of immunosuppression in response to pregnancy TLRs during contact with infectious and non-infectious pathogens stimulate the production of nonspecific adaptive immunity factors (defensins, cathelicidins, histatines, etc.), which together with the non-specific innate factors lysozyme, complement, properdin, etc. support antiinfective resistance of the female genitals at a high level at the beginning of the infectious process. Possible violations of the development of pregnancy may be accompanied by changes in the response of TLRs to infectious and non-infectious factors until hyper-reaction, excessive inflammation or apoptosis, which requires adequate management of pregnancy. Was established the significance of the influence of pathogens of infectious and noninfectious origin in intrauterine infection indirectly through TLRs in the homeostasis of the organism, on the formation of breaches in anti-infective resistance at the organism and community level the identification of new pathophysiological and immunological pathogenetic mechanisms of development of pathological processes. IUI is a penetration of microorganisms into the tissues of fetus and it’s infection. The inhibition of the functional activity of TLRs is accompanied by the direct effect of the pathogen on the tissues, and during hyper-reaction of TLRs to pathogens revealed a pronounced inflammatory response in the fetus. The level of expression of TLRs correlates directly with the severity of the process that can be considered as early markers of infection. Depending on the nature of the pathogen an increased expression of one or the other TLRs is observed. Explained the lack of symptoms, the possibility of atypical manifestations, the asymptomatic course of infection.

About the authors

A. V. Karaulov

I.M. Sechenov Moscow State Medical University.

Email: fake@neicon.ru

RAS Full Member, PhD, MD (Medicine), Professor, Head of the Department of Clinical Allergology and Immunology.

Moscow. Russian Federation

S. S. Afanasiev

G.N. Gabrichevsky Research Institute of Epidemiology and Microbiology.

Email: fake@neicon.ru

PhD, MD (Medicine), Professor, Head Researcher.

Moscow.

Russian Federation

V. A. Aleshkin

G.N. Gabrichevsky Research Institute of Epidemiology and Microbiology.

Email: fake@neicon.ru

hD, MD (Biology), Professor, Director.

Moscow.

Russian Federation

N. L. Bondarenko

I.M. Sechenov Moscow State Medical University.

Email: fake@neicon.ru

PhD (Medicine), Associate Professor, Department of Clinical Allergology and Immunology.

Moscow. Russian Federation

E. A. Voropaeva

G.N. Gabrichevsky Research Institute of Epidemiology and Microbiology.

Email: fake@neicon.ru

PhD, MD (Biology), Deputy Director.

Moscow.

Russian Federation

M. S. Afanasiev

I.M. Sechenov Moscow State Medical University.

Email: fake@neicon.ru

PhD, MD (Medicine), Professor of the Department of Clinical Allergology and Immunology.

Moscow. Russian Federation

Yu. V. Nesvizhsky

I.M. Sechenov Moscow State Medical University.

Email: fake@neicon.ru

PhD, MD (Medicine), Professor, Dean of the Faculty for Preventive Medicine.

Moscow. Russian Federation

O. Yu. Borisova

G.N. Gabrichevsky Research Institute of Epidemiology and Microbiology.

Author for correspondence.
Email: olgborisova@mail.ru

PhD, MD (Medicine), Associate Professor, Head of the Laboratory of Diagnostic of Diphtheria and Pertussis Infections.

125212, Russian Federation, Moscow, Admiral Makarov str., 10.

Phone: +7 (499) 747-64-84 (office); +7 916 147-19-60 (mobile). 

Fax: +7 (495) 452-18-30.

Russian Federation

A. V. Aleshkin

G.N. Gabrichevsky Research Institute of Epidemiology and Microbiology.

Email: fake@neicon.ru

PhD, MD (Biology), MBA, Head of Laboratory of Clinical Microbiology and Biotechnology for Bacteriophages.

Moscow. Russian Federation

Yu. N. Urban

G.N. Gabrichevsky Research Institute of Epidemiology and Microbiology.

Email: fake@neicon.ru

PhD (Biology), Researcher, Laboratory of Clinical Microbiology and Biotechnology.

Moscow. Russian Federation

A. B. Borisova

G.N. Gabrichevsky Research Institute of Epidemiology and Microbiology.

Email: fake@neicon.ru

Junior Researcher, Laboratory of Diagnostic of Diphtheria and Pertussis Infections.

Moscow. Russian Federation

A. D. Voropaev

G.N. Gabrichevsky Research Institute of Epidemiology and Microbiology.

Email: fake@neicon.ru

Junior Researcher, Laboratory of Clinical Microbiology and Biotechnology.

Moscow. Russian Federation

References

  1. Абрамченко В.В. Классическое акушерство. Книга вторая. СПб.: Нордмедиздат, 2008. 879 с.
  2. Алешкин В.А., Ложкина А.Н., Загородняя Э.Д. Иммунология репродукции: пособие для врачей, ординаторов и научных работников. Чита: 2004. 79 с.
  3. Аллергология. Федеральные клинические рекомендации. Под ред. Р.М. Хаитова, Н.И. Ильиной. М.: Фармарус Принт Медиа, 2014. 126 с.
  4. Бочарова И.И., Новикова С.В., Дмитриева Е.В., Паршина О.В., Гусева Т.С. Интерферонотерапия при урогенитальных инфекциях // Вестник «Ферона». 2013. № 1. С. 13–16.
  5. Буданов П.В., Стрижаков А.Н. Этиология, патогенез, диагностика и лечение внутриутробной инфекции // Вопросы гинекологии, акушерства и перинатологии. 2010. Т. 9, № 3. С. 61–71.
  6. Ванько Л.В., Сафронова В.Г., Матвеева Н.К., Сухих Г.Т. Оксидативный стресс в генезе акушерских осложнений. М.: ГЭОТАР-Медиа, 2010. 264 с.
  7. Ганковская О.А., Ковальчук Л.В., Ганковская Л.В., Лавров В.Ф., Романовская В.В., Карташов Д.Д., Фензелева В.А. Роль Толл-подобных рецепторов и дефенсинов в противомикробной защите урогенитального тракта женщин // Журнал микробиологии, эпидемиологии и иммунобиологии. 2008. № 1. С. 46–50.
  8. Ганковская Л.В., Ковальчук Л.В., Макаров О.В., Ганковская О.А., Акимова Е.А. Роль экспрессии генов Toll-подобного рецептора 2, каспаз и их ингибиторов в ткани плаценты в норме и при преждевременных родах инфекционного генеза // Российский иммунологический журнал. 2010. Т. 4, № 1 (13). С. 48–53.
  9. Джобава Э.М., Степанян А.В., Артизанова Д.П., Бояр Е.А., Хейдар Л.Х., Доброхотова Ю.Э. Современное обоснование к возможности терапии вагинальных дисбиозов во время беременности // Гинекология. 2009. Т. 11, № 1. С. 79–82.
  10. Инфекции в акушерстве и гинекологии. Под ред. Макарова О.В., Алешкина В.А., Савченко Т.Н. М.: МЕДпресс-информ, 2009. 464 с.
  11. Ковальчук Л.В., Ганковская Л.В., Мешкова Р.Я. Клиническая иммунология и аллергология с основами общей иммунологии. М.: ГЭОТАР-Медиа, 2011. 639 с.
  12. Крыжановская М.В. Роль инфекционного фактора в развитии преждевременных родов // Медико-соціальні проблеми сім’ї. 2011. Т. 16, № 1. С. 104–107.
  13. Макаров О.В., Бахарева И.В., Ковальчук Л.В., Ганковская Л.В., Романовская В.В., Ганковская О.А. Toll-подобные рецепторы как маркеры осложнений беременности // Аллергология и иммунология. 2007. Т. 8, № 3. С. 236.
  14. Макаров О.В., Ковальчук Л.В., Ганковская Л.В., Бахарева И.В., Ганковская О.А. Невынашивание беременности, инфекция, врожденный иммунитет. М.: ГЭОТАР-Медиа, 2007. 176 c.
  15. Макаров О.В., Ганковская Л.В., Ковальчук Л.В., Бахарева И.В., Романовская В.В., Ганковская О.А. Прогностическое значение компонентов врожденного иммунитета у беременных с высоким риском реализации внутриутробной инфекции // Вестник Российского государственного медицинского университета. 2009. № 4. C. 27–33.
  16. Макацария А.Д., Бицадзе В.О., Акиньшина С.В. Синдром системного воспалительного ответа в акушерстве. М.: Медицинское информационное агентство, 2006. 442 с.
  17. Микробиоценозы и здоровье человека. Под ред. Алешкина В.А., Афанасьева С.С., Караулова А.В. М.: Издательство «Династия», 2015. 548 с.
  18. Новое в физиологии мукозального иммунитета. Под ред. Караулова А.В., Алешкина В.А., Афанасьева С.С., Несвижского Ю.В. М.: Издательство Первого Московского государственного медицинского университета им. И.М. Сеченова, 2015. 168 с.
  19. Рюмина И.И., Зубков В.В., Евтеева Н.В. Профилактика, диагностика и лечение омфалита у новорожденных // Акушерство и гинекология. 2012. № 5. С. 68–74.
  20. Селихова М.С., Кузнецова О.А., Вдовин С.В., Дмитриенко Г.В. Роль эндотоксемии и механизмов врожденного иммунитета в патогенезе неразвивающейся беременности // Вестник Волгоградского государственного медицинского университета. 2012. № 1. С. 18–20.
  21. Серебренникова С.Н., Семинский И.Ж. Роль цитокинов в воспалительном процессе (сообщение 2) // Сибирский медицинский журнал (Иркутск). 2008. Т. 83, № 8. С. 5–8.
  22. Тирская Ю.И., Белкова Т.Н., Рудакова Е.Б., Долгих Т.И., Шакина И.А. Врачебная тактика при внутриутробных инфекциях // Акушерство и гинекология. 2011. № 8. С. 42–47.
  23. Щебляков Д.В., Логунов Д.Ю., Тухватулин А.И., Шмаров М.М., Народицкий Б.С., Гинцбург А.Л. Тoлл-подобные рецепторы (TLR) и их значение в опухолевой прогрессии // Acta Naturae (русскоязычная версия). 2010. Т. 2, № 3 (6). С. 28–37.
  24. Aboussahoud W., Bruce C., Elliott S., Fazeli A. Activation of Toll-like receptor 5 decreases the attachment of human trophoblast cells to endometrial cells in vitro. Hum. Reprod., 2010, vol. 25, no. 9, pp. 2217–2228. doi: 10.1093/humrep/deq185
  25. Abrahams V.M., Aldo P.B., Murphy S.P., Visintin I., Koga K., Wilson G., Romero R., Sharma S., Mor G. TLR6 modulates first trimester trophoblast responses to peptidoglycan. J. Immunol., 2008, vol. 180, no. 9, pp. 6035–6043. doi: 10.4049/jimmunol.180.9.6035
  26. Abrahams V.M., Bole Aldo P., Kim Y.M., Straszewski-Chavez S.L., Chaiworapongsa T., Romero R., Mor G. Divergent trophoblast responses to bacterial products mediated by TLRs. J. Immunol., 2004, vol. 173, no. 7, pp. 4286–4296. doi: 10.4049/jimmunol.173.7.4286
  27. Abrahams V.M., Mor G. Toll-like receptors and their role in the trophoblast. Placenta, 2005, vol. 26, no. 7, pp. 540–547. doi: 10.1016/j.placenta.2004.08.010
  28. Boldenow E., Jones S., Lieberman R.W., Chames M.C., Aronoff D.M., Xi C., Loch-Caruso R. Antimicrobial peptide response to group B Streptococcus in human extraplacental membranes in culture. Placenta, 2013, vol. 34, no. 6, pp. 480–485. doi: 10.1016/j.placenta.2013.02.010
  29. Caballero I., Al Ghareeb S., Basatvat S., Sanchez-Lopez J.A., Montazeri M., Maslehat N., Elliott S., Chapman N.R., Fazeli A. Human trophoblast cells modulate endometrial cells nuclear factor kB response to flagellin in vitro. PLoS One, 2013, vol. 8, no. 1: e39441. doi: 10.1371/journal.pone.0039441
  30. Canavan T.P., Simhan H.N. Innate immune function of the human decidual cell at the maternal-fetal interface. J. Reprod. Immunol., 2007, vol. 74, no. 1–2, pp. 46–52. doi: 10.1016/jjri.2006.10.004
  31. Chen Y.P., Pfab Т., Slowinski Т., Richter C.M., Godes M., Hocher B. Impact of genetic variation of tumor necrosis factor-alpha on gestational hypertention. Clin. Med. J. (Engl.), 2006, vol. 119, no. 9, pp. 719–724.
  32. Crocker I.P., Baker P.N., Fletcher J. Neutrophil function in pregnancy and rheumatoid arthritis. Ann. Rheum. Dis., 2000, vol. 59, no. 7, pp. 555–564.
  33. Darville T., O’Neill J.M., Andrews C.W. Jr., Nagarajan U.M., Stahl L., Ojcius D.M. Toll-like receptor-2, but not toll-like receptor- 4, is essential for development of oviduct pathology in chlamydial genital tract infection. J. Immunol., 2003, vol. 171, no. 11, pp. 6187–6197. doi: 10.4049/jimmunol.171.11.6187
  34. Den Hartog J.E., Morre S.A., Land J.A. Chlamydia trachomatis-associated tubal factor subfertility: immunogenetic aspects and serological screening. Hum. Reprod. Update, 2006, vol. 12, no. 6, pp. 719–730. doi: 10.1093/humupd/dml030
  35. Den Hartog J.E., Ouburg S., Land J.A., Lyons J.M., Ito J.I., Pena A.S., Morre S.A. Do host genetic traits in the bacterial sensing system play a role in the development of Chlamydia trachomatis-associated tubal pathology in subfertile women? BMC Infect. Dis., 2006, vol. 6, no. 1, pp. 122. doi: 10.1186/1471-2334-6-122
  36. Dusio G.F., Cardani D., Zanobbio L., Mantovani M., Luchini P., Battini L., Galli V., Diana A., Balsari A., Rumio C. Stimulation of TLRs by LMW-HA induces self-defense mechanisms in vaginal epithelium. Immunol. Cell. Biol., 2010, vol. 89, no. 5, pp. 630– 639. doi: 10.1038/icb.2010.140
  37. Fahey J.V., Schaefer T.M., Wira C.R. Sex hormones modulation of human uterine epithelial cells immune response. Integr. Comp. Biol., 2006, vol. 46, no 6, pp. 1082–1087. doi: 10.1093/icb/icl036
  38. Fichorova R.N., Tifonova R.T., Gilbert R.O., Costello C.E., Hayes G.R., Lucas J.J., Singh B.N. Trichomonas vaginalis lipophosphoglycan triggers a selective upregulation of cytokines by human female reproductive tract epithelial cells. Infect. Immun., 2006, vol. 74, no. 10, pp. 5773–5779. doi: 10.1128/iai.00631-06
  39. Fisette P.L., Ram S., Andersen J.M., Guo W., Ingalls R.R. The Lip lipoprotein from Neisseria gonorrhoeae stimulates cytokine release and NF_kB activation in epithelial cells in a Toll_like receptor 2 dependent manner. J. Biol. Chem., 2003, vol. 278, no. 47, pp. 46252–46260. doi: 10.1074/jbc.m306587200
  40. Gargo A., Tominac M., Krsulovic-Hresic V., Bace A., Matic M., Drazenovic V., Mlinaric-Galinovic G., Kosor E., Gotovac K., Bolanca I., BatinicaS., Rabatic S. Increased Toll-like receptors 4 expression in infants with respiratory syncytial virus bronchiolitis. J. Clin. Exp. Immunol., 2004, vol. 135, no. 2, pp. 267–272. doi: 10.1111/j.1365-2249.2004.02364.x
  41. Gomez-Lopez N., Guilbert L.J., Olson D.M. Invasion of the leukocytes into the fetal-maternal interface during pregnancy. J. Leukoc. Biol., 2010, vol. 88, no. 4, pp. 625–633. doi: 10.1189/jlb.1209796
  42. Gomez-Lopez N., Tanaka S., Zaeem Z., Metz G.A., Olson D.M. Maternal circulating leukocytes display early chemotactic responsiveness during late gestation. BMC Pregnancy Childbirth, 2013, vol. 13, no. 1, pp. S8. doi: 10.1186/1471-2393-13-S1-S8
  43. Grigsby P.L., Novy M.J, Adams Waldorf K.M, Sadowsky D.W, Gravett M.G. Choriodecidual inflammation: a harbinger of the preterm labor syndrome. Reprod. Sci., 2010, vol. 17, no. 1, pp. 85–94. doi: 10.1177/1933719109348025
  44. Hagberg H., Peebles D., Mallard C. Models of white matter injury: comparison of infectious, hypoxicischemic, and excitotoxic insults. Ment. Retard. Dev. Disabil. Res. Rev., 2002, vol. 8, no. 1, pp. 30–38. doi: 10.1002/mrdd.10007
  45. Hart O.M., Athie-Morales V., O’Connor G.M., Gardiner C.M. TLR7/8 mediated activation of human NK-cells results in accessory cell-dependent IFN-gamma production. J. Immunol., 2005, vol. 175, no. 3, pp. 1636–1642. doi: 10.4049/jimmunol.175.3.1636
  46. Helminen M., Nuolivirta K., Virta M., Halkosalo A., Korppi M., Vesikari T., Hurme M. IL-10 gene polymorphism at –1082 A/G is associated with severe rhinovirus bronchiolitis in infants. Pediatr. Pulmonol., 2008, vol. 43, no. 4, pp. 391–395. doi: 10.1002/ppul.20793
  47. Hemmi H.A., Takeushi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., Akira S. Toll-like receptor recognizes bacterial DNA. Nature, 2000, vol. 408, no. 6813, pp. 740–745. doi: 10.1038/35047123
  48. Hickey D.K., Fahey J.V., Wira C.R. Mouse estrous cycle regulation of vaginal versus uterine cytokines, chemokines, α-/β- defensins and TLRs. Innate Immunity, 2013, vol. 19, no. 2, pp. 121–131. doi: 10.1177/1753425912454026
  49. Holmlund U., Wahamaa H., Bachmayer N., Bremme K., Sverremark-Ekstrom E., Palmblad K. The novel inflammatory cytokine high mobility group box protein 1 (HMGB1) is expressed by human term placenta. Immunology, 2007, vol. 122, no. 3, pp. 430–437. doi: 10.1111/j.1365-2567.2007.02662.x
  50. Jarchum I., Liu M., Lipuma L., Pamer E.G. Toll-like receptor 5 stimulation protects mice from acute Clostridium difficile colitis. Infect. Immun. 2011, vol. 79, no. 4, pp. 1498–1503. doi: 10.1128/iai.01196-10
  51. Janeway C., Travers P., Walport M., Shlomchik M. Immunobiology: the immune system in health and disease. 5th ed. New York: Garland Publishing, 2001. 884 р.
  52. Kawai Т., Akira S. Toll-like receptors and their crosstalk’with other innate receptors in infection and immunity. Immunity, 2011, vol. 34, no. 5, pp. 637–650. doi: 10.1016/j.immuni.2011.05.006
  53. Khan K.N., Kitajima N., Imamura T., Hiraki K., Fujishita A., Sekine I., Ishimaru T., Masuzaki H. Toll-like receptor 4-mediated growth of endometriosis by human heat-shock protein 70. Hum. Reprod., 2008, vol. 23, no. 10, pp. 2210–2219. doi: 10.1093/humrep/den195
  54. Khan K.N., Kitajima M., Hiraki K., Fujishita A., Sekine I., Ishimaru T., Masuzaki H. Toll-like receptors receptors in innate immunity: role of bacterial edndotoxin and Toll-like receptor 4 in endometrium and endometriosis. Gynecol. Obstet. Invest., 2009, vol. 68, no. 1, pp. 40–52. doi: 10.1159/000212061
  55. Kim W.Y., Lee J.W., Choi J.-J., Choi C.H., Kim T.-J., Kim B.-J., Song S.Y., Bae D.-S. Increased expression of Toll-like receptor 5 during progression of cervical neoplasia. Int. J. Gynecol. Cancer, 2008, vol. 18, no. 2, pp. 300–305. doi: 10.1111/j.1525-1438.2007.01008.x
  56. Koga K., Aldo P.B., Mor G. Toll-like receptors and pregnancy: trophoblast as modulators of the immune response. J. Obstet. Gynaecol. Res., 2009, vol. 35, no. 2, pp. 191–202. doi: 10.1111/j.1447-0756.2008.00963.x
  57. Koga K., Cardenas I., Aldo P., Abrahams V.M., Peng B., Fill S., Romero R., Mor G. Activation of TLR3 in the trophoblast is associated with preterm delivery. Am. J. Reprod. Immunol., 2009, vol. 61, no. 3, pp. 196–212. doi: 10.1111/j.1600-0897.2008.00682.x
  58. Koga K., Izumi G., Mor G., Fujii T., Osuga Y. Toll-like receptors at the maternal-fetal Interface in normal pregnancy and pregnancy complications. Am. J. Reprod. Immunol., 2014, vol. 72, no. 2, pp. 192–205. doi: 10.1111/aji.12258
  59. Koga K., Mor G. Toll-like R at the maternal-fetal interface in normal pregnancy and pregnancy disorders. Am. J. Reprod. Immunol., 2010, vol. 63, no. 6, pp. 587–600. doi: 10.1111/j.1600-0897.2010.00848.x
  60. Kramer B.W., Ikegami M., Moss T.J., Nitsos I., Newnham J.P., Jobe A.H. Endotoxin-induced chorioamnionitis modulates innate immunity of monocytes in preterm sheep. Am. J. Respir. Crit. Care. Med., 2005, vol. 171, no. 1, pp. 73–77. doi: 10.1164/rccm.200406-745oc
  61. Krikun G., Lockwood C.J., Abrahams V.M., Mor G., Paidas M., Guller S. Expression of Toll-like receptors in the human decidua. Histol. Histopathol., 2007, vol. 22, no. 8, pp. 847–854. doi: 10.14670/HH-22.847
  62. Lekkerkerker A.N., van Kooyk Y., Geijtenbeek T.B. Viral piracy: HIV-1 targets dendriticcells for transmission. Curr. HIV Res., 2006, vol. 4, no. 2, pp. 169–176. doi: 10.2174/157016206776055020
  63. MacDonald E.M., Savoy A., Gillgrass A., Fernandez S., Smieja M., Rosenthal K.L., Ashkar A.A., Kaushic C. Susceptibility of human female primary genital epithelial cells to herpes simplex virus, type-2 and the effect of TLR3 ligand and sex hormones on infection. Biol. Reprod., 2007, vol. 77, no. 6, pp. 1049–1059. doi: 10.1095/biolreprod.107.063933
  64. Magnus M., Clark R., Myers L., Farley T., Kissinger P.J. Trichomonas vaginalis among HIV-infected women: are immune status or protease inhibitor use associated with subsequent T. vaginalis positivity? Sex. Transm. Dis., 2003, vol. 30, no. 11, pp. 839–843. doi: 10.1097/01.olq.0000086609.95617.8d
  65. Mangoni M.L. Host-defense peptides: from biology to therapeutic strategies. Cell. Mol. Life Sci., 2011, vol. 68, no. 13, pp. 2157– 2159. doi: 10.1007/s00018-011-0709-3
  66. Mitchell C., Gottsch M.L., Liu С., Fredricks D.N., Nelson D.B. Associations between vaginal bacteria and levels of vaginal defensins in pregnant women. Am. J. Obstet. Gynecol., 2013, vol. 208, no. 2, pp. 132.e1–132.e7. doi: 10.1016/j.ajog.2012.11.019
  67. Monif G.R., Martens M.G. A guest editorial: antibiotic selection in obstetrics and gynecology. Obstet. Gynecol. Surv., 2002, vol. 57, no. 8, pp. 479–480. doi: 10.1097/01.OGX.0000024258.34252.68
  68. Muthukuru M., Jotwani R., Cutler C.W. Oral mucosal endotoxin tolerance induction in chronic periodontitis. Infect. Immun., 2005, vol. 73, no. 2, pp. 687–694. doi: 10.1128/iai.73.2.687-694.2005
  69. Nasu K., Itoh H., Yuge A., Nishida M., Narahara H. Human oviductal epithelial cells express Toll-like receptor 3 and respond to double-stranded RNA: Fallopian tube-specific mucosal immunity against viral infection. Hum. Reprod., 2006, vol. 22, no. 2, pp. 356–361. doi: 10.1093/humrep/del385
  70. Netea M.G., Gow N.A., Munro CA, Bates S., Collins C., Ferwerda G., Hobson R.P., Bertram G., Hughes H.B., Jansen T., Jacobs L., Buurman E.T., Gijzen K., Williams D.L., Torensma R., McKinnon A., MacCallum D.M., Odds F.C., Van der Meer J.W., Brown A.J., Kullberg B.J. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J. Clin. Invest., 2006, vol. 116, no. 6, pp. 1642–1650. doi: 10.1172/jci27114
  71. Ochiel D.O., Fahey J.V., Ghosh M., Haddad S.N., Wira C. 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, no. 2, pp. 102–117. doi: 10.2174/157340408784246395
  72. Orihara K., Nagata K., Hamasaki S., Oba R., Hirai H., Ishida S., Kataoka T., Oketani N., Ogawa M., Mizoguchi E., Ichiki H., Tei C. Time-course of Toll-like receptor 2 expression, as a predictor of recurrence in patients with bacterial infectious diseases. Clin. Exp. Immunol., 2007, vol. 148, no. 2, pp. 260–270. doi: 10.1111/j.1365-2249.2007.03352.x
  73. Patel M.V., Ghosh M., Fahey J.V., Wira C.R. Uterine epithelial cells specifically induce interferon-stimulated genes in response to polyinosinic-polycytidylic acid independently of estradiol. PLoS One, 2012, vol. 7, no. 4, pp. e35654. doi: 10.1371/journal.pone.0035654
  74. Patni S., Wynen L.P., Seager A.L., Morgan G., White J.O., Thornton C.A. Expression and activity of Toll-like receptors 1-9 in the human term placenta and changes associated with labor at term. Biol. Reprod., 2009, vol. 80, no. 2, pp. 243–248. doi: 10.1095/biolreprod.108.069252
  75. Patterson P.H. Neuroscience. Maternal effects on schizophrenia risk. Science, 2007, vol. 318, no. 5850, pp. 576–577. doi: 10.1126/science.1150196
  76. Sampedro M., Aliaga M., Mazuelas T., Rodriquez-Grander J. Diagnosis of congenital infection. Enferm. Infect. Microbiol. Clin., 2011, vol. 29, no. 5, pp. 15–20. doi: 10.1016/S0213-005X(11)70039-8
  77. Sanchez-Lopez J.A., Caballero I., Montazeri M., Maslehat N., Elliott S., Fernandez-Gonzalez R., Calle A., Gutierrez-Adan A., Fazeli A. Local activation of uterine Toll-like receptor 2 and 2/6 decreases embryo implantation and affects uterine receptivity in mice. Biol. Reprod., 2014, vol. 90, no. 4, p. 87. doi: 10.1095/biolreprod.113.115253
  78. Saphronova V.G., Sukhikh T., Van’ko L.V. Modern concept on the role of phagocytes in the pathogenesis of complications during pregnancy. Bull. Experim. Biol. Med., 2002, vol. 134, no. 2, pp. 107–116. doi: 10.1023/A:1021117826014
  79. Shi L., Fatemi S.H., Sidwell R.W., Patterson P.H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci., 2003, vol. 23, no. 1, pp. 297–302.
  80. Sonoda Y., Abdel Mageed A.M., Isobe N., Yoshimura Y. Induction of avian β-defensins by CpG oligodeoxynucleotides and proinflammatory cytokines in hen vaginal cells in vitro. Reproduction, 2013, vol. 145, no. 6, pp. 621–631. doi: 10.1530/rep-12-0518
  81. Suzuki Y., Yamamoto T., Kojima K., Tanemura M., Tateyama H., Suzumori K. Evaluation levels of cytokines in amniotic fluid of women with intrauterine infection in the early second trimester. Fetal. Diagn. Ther., 2005, vol. 21, no. 1, pp. 45–50. doi: 10.1159/000089047
  82. Taylor B.D., Darville T., Ferrell R.E., Kammerer C.M., Roberta B., Ness R.B., Haggerty C.L. Variants in Toll-like receptor 1 and 4 genes are associated with Chlamydia trachomatis among women with pelvic inflammatory disease. J. Infect. Dis., 2012, vol. 205, no. 4, pp. 603–609. doi: 10.1093/infdis/jir822
  83. Tse D.B., Young B.K. Coordinate expression of Th1/Th2 phenotypes in maternal and fetal blood: evidence for a transplacental nexus. J. Perinat. Med., 2012, vol. 40, no. 2, pp. 165–170. doi: 10.1515/jpm.2011.131
  84. Vega-Sanchez R., Gomez-Lopez N., Flores-Pliego A., Clemente-Galvan S., Estrada-Gutierrez G., Zentella-Dehesa A., Maida-Claros R., Beltran-Montoya J., Vadillo-Ortega F. Placental blood leukocytes are functional and phenotypically different than peripheral leukocytes during human labor. J. Reprod. Immunol., 2010, vol. 84, no. 1, pp. 100–110. doi: 10.1016/j.jri.2009.08.002
  85. Viemann D., Dubbel G., Schleifenbaum S., Harms E., Sorg C., Roth J. Expression of Toll-like receptors in neonatal sepsis. J. Pediatr. Res., 2005, vol. 58, no. 4, pp. 654–659. doi: 10.1203/01.pdr.0000180544.02537.fd
  86. Von Bernuth H., Picard C., Puel A., Casanova J.-L. Experimental and natural infections in MyD88- and IRAK-4-deficient mice and humans. Eur. J. Immunol., 2012, vol. 42, no. 12, pp. 3126–3135. doi: 10.1002/eji.201242683
  87. Wang H., Ogawa M., Wood J.R., Bartolomei M.S., Sammel M.D., Kusanovic J.P., Walsh S.W., Romero R., Strauss J.F. Genetic and epigenetic mechanisms combine to control MMP1 expression and its association with preterm premature rupture of membranes. Hum. Mol. Genet., 2008, vol. 17, no. 8, pp. 1087–1096. doi: 10.1093/hmg/ddm381
  88. Weiss K., Christiaansen A.F., Fulton R.B., Meyerholz D.K., Varga S.M. Multiple CD4+ T cell subsets produce immunomodulatory IL-10 during respiratory syncytial virus infection. J. Immunol., 2011, vol. 187, no. 6, pp. 3145–3154. doi: 10.4049/jimmunol.1100764
  89. Wiechuła B., Cholewa K., Ekiel A., Romanik M., Dolezych H., Martirosian G. HBD-1 and hBD-2 are expressed in cervicovaginal lavage in female genital tract due to microbial infections. Ginekol. Pol., 2010, vol. 81, no. 4, pp. 268–271.
  90. Xu J., Yang Y., Sun J., Ding Y., Su L., Shao C., Jiang B. Expression of TLR and their association with cytokine responses in peripheral blood mononuclear cells of children with acute rotavirus diarrhea. J. Clin. Exp. Immunol., 2006, vol. 144, no. 3, pp. 376–381. doi: 10.1111/j.1365-2249.2006.03079.x
  91. Zhang C. The role of inflammatory cytokines in endothelial dysfunction. Basic. Res. Cardiol., 2008, vol. 103, no. 5, pp. 398–406. doi: 10.1007/s00395-008-0733-0
  92. Zhang D.M., Li Y.W., Mao B.L., Qian G.S. Down-regulation of Toll-like receptor 4 is related to the tolerance to lipopolysaccharide in rat alveolar macrophages. Zhonghua Jie He He Hu Xi Za Zhi., 2003, vol. 26, no. 7. pp. 411–414.
  93. Zhang J.P., Chen C., Yang Y. Changes and clinical significance of Toll-like receptor 2 and 4 expression in neonatal infections. Zhonghua Er Ke Za Zhi., 2007, vol. 45, no. 2, pp. 130–133.

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