Preview

Инфекция и иммунитет

Расширенный поиск

Нейтрофилы: неоднозначная роль в патогенезе туберкулеза

https://doi.org/10.15789/2220-7619-ACR-1670

Полный текст:

Аннотация

Туберкулез (ТБ) до сих пор является важной нерешенной медицинской проблемой. Примерно четверть человечества заражена Mycobacterium tuberculosis, и у 5–10% рано или поздно развивается ТБ. Макрофаги и Т-лимфоциты CD4+ являются основными иммунными клетками, противостоящими ТБ-инфекции. Гораздо меньше известно о роли нейтрофилов при ТБ. Нейтрофилы, короткоживущие лейкоциты, в числе первых реагируют на проникновение инфекции, мигрируют в очаг воспаления и поглощают микобактерии в легких. С одной стороны, есть свидетельства защитной роли нейтрофилов за счет продукции пептидов, подавляющих рост микобактерий, усиления активации Т-лимфоцитов CD4+ и миграции дендритных клеток в лимфоузлы. С другой стороны, инфицирование генетически чувствительных к ТБ животных приводит к избыточному притоку нейтрофилов в легкие, формированию некротических гранулем и быстрой гибели. Нейтрофилы напрямую или опосредованно воздействуют на микобактерии, используя различные окислительные и неокислительные реакции, а также образуя нейтрофильные внеклеточные ловушки (NETs). Фагоцитоз микобактерий нейтрофилами стимулирует выделение ими множества провоспалительных медиаторов, поэтому нейтрофилы являются активными участниками воспаления на всех стадиях развития инфекционного процесса. В конечном итоге нейтрофилы погибают путем апоптоза или некроза. Гибель нейтрофилов путем некроза, инициируемого активными формами кислорода, в свою очередь также провоцирует излишнее воспаление. В связи с этим велика вероятность того, что именно нейтрофилы способствуют переходу ТБ в терминальную стадию, участвуя в распаде легочной ткани. Кроме того, несмотря на то что эволюционно нейтрофилы имеют достаточно возможностей воздействия на патоген, по-видимому, сами по себе они не обладают достаточной бактерицидной активностью в отношении микобактерий вследствие формирования у последних механизмов защиты, позволяющих выживать внутри клеток. Таким образом, нейтрофилы фагоцитируют, но не убивают микобактерии и могут выступать в роли «троянского коня», экранируя бактерии от более эффективных защитных действий макрофагов. В этом обзоре мы обобщаем данные последних лет об участии нейтрофилов в туберкулезном воспалении. Мы обсуждаем неоднозначность их роли в патогенезе в зависимости от вирулентости микобактерий и генетических особенностей хозяина, динамику притока нейтрофилов в очаг воспаления и персистирование в начальной и хронической стадиях инфекции.

Об авторах

И. А. Линге
ФГБНУ Центральный НИИ туберкулеза
Россия

Линге Ирина Андреевна,  к.б.н., старший научный сотрудник лаборатории иммуногенетики отдела иммунологии 

107564, Москва, Яузская аллея, 2,

Тел.: 8 499 785-90-72



А. С. Апт
ФГБНУ Центральный НИИ туберкулеза
Россия

д.б.н., профессор, зав. лабораторией иммуногенетики отдела иммунологии 

Москва



Список литературы

1. Abadie V., Badell E., Douillard P., Ensergueix D., Leenen P.J.M., 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, pp. 1843–1850. doi: 10.1182/blood-2005-03-1281

2. Bazzoni F., Cassatella M.A., Rossi F., Ceska M., Dewald B., Baggiolini M. Phagocytosing neutrophils produce and release high amounts of the neutrophil-activating peptide 1/interleukin 8. J. Exp. Med., 1991, vol. 173, pp. 771–774. doi: 10.1084/jem.173.3.771

3. Berry M.P.R., Graham C.M., McNab F.W., Xu Z., Bloch S.A.A., Oni T., Wilkinson K.A., Banchereau R., Skinner J., Wilkinson R.J., Quinn C., Blankenship D., Dhawan R., Cush J.J., Mejias A., Ramilo O., Kon O.M., Pascual V., Banchereau J., Chaussabel D., O’Garra A. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature, 2010, vol. 466, pp. 973–977. doi: 10.1038/nature09247

4. 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, pp. 81–90. doi: 10.1016/j.chom.2011.11.012

5. 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, pp. 7110–7119. doi: 10.4049/jimmunol.1100001

6. Bober L.A., Grace M.J., Pugliese-Sivo C., Rojas-Triana A., Waters T., Sullivan L.M., Narula S.K. The effect of GM-CSF and G-CSF on human neutrophil function. Immunopharmacology, 1995, vol. 29, pp. 111–119. doi: 10.1016/0162-3109(94)00050-P

7. Braian C., Hogea V., Stendahl O. Mycobacterium tuberculosis-induced neutrophil extracellular traps activate human macrophages. J. Innate Immun., 2013, vol. 5, pp. 591–602. doi: 10.1159/000348676

8. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science, 2004, vol. 303, pp. 1532–1535. doi: 10.1126/science.1092385

9. Castillo E.F., Dekonenko A., Arko-Mensah J., Mandell M.A., Dupont N., Jiang S., Delgado-Vargas M., Timmins G.S., Bhattacharya D., Yang H., Hutt J., Lyons C.R., Dobos K.M., Deretic V. Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc. Natl. Acad. Sci. USA, 2012, vol. 109, no. 46, pp. E3168– E3176. doi: 10.1073/pnas.1210500109

10. Choi H., Chon H.R., Kim K., Kim S., Oh K.J., Jeong S.H., Jung W.J., Shin B., Jhun B.W., Lee H., Park H.Y., Koh W.J. Clinical and laboratory differences between lymphocyte- and neutrophil-predominant pleural tuberculosis. PLoS One, 2016, vol. 11, no. 10: e0165428. doi: 10.1371/journal.pone.0165428

11. Choreño-Parra J.A., Bobba S., Rangel-Moreno J., Ahmed M., Mehra S., Rosa B., Martin J., Mitreva M., Kaushal D., Zúñiga J., Khader S.A. Mycobacterium tuberculosis HN878 infection induces human-like B-cell follicles in mice. J. Infect. Dis., 2020, vol. 221, pp. 1636–1646. doi: 10.1093/infdis/jiz663

12. Cohen S.B., Gern B.H., Delahaye J.L., Adams K.N., Plumlee C.R., Winkler J.K., Sherman D.R., Gerner M.Y., Urdahl K.B. Alveolar macrophages provide an early Mycobacterium tuberculosis niche and initiate dissemination. Cell Host Microbe, 2018, vol. 24, pp. 439–446. doi: 10.1016/j.chom.2018.08.001

13. Condliffe A.M., Chilvers E.R., Haslett C., Dransfield I. Priming differentially regulates neutrophil adhesion molecule expression/function. Immunology, 1996, vol. 89, pp. 105–111. doi: 10.1046/j.1365-2567.1996.d01-711.x

14. Corleis B., Korbel D., Wilson R., Bylund J., Chee R., Schaible U.E. Escape of Mycobacterium tuberculosis from oxidative killing by neutrophils. Cell Microbiol., 2012, vol. 14, pp. 1109–1121. doi: 10.1111/j.1462-5822.2012.01783.x

15. Dallenga T., Repnik U., Corleis B., Eich J., Reimer R., Griffiths G.W., Schaible U.E. M. tuberculosis-induced necrosis of infected neutrophils promotes bacterial growth following phagocytosis by macrophages. Cell Host Microbe, 2017, vol. 22, pp. 519.e3–530.e3. doi: 10.1016/j.chom.2017.09.003

16. Dapino P., Dallegri F., Ottonello L., Sacchetti C. Induction of neutrophil respiratory burst by tumour necrosis factor-alpha; priming effect of solid-phase fibronectin and intervention of CD llb-CD18 integrins. Clin. Exp. Immunol., 2008, vol. 94, pp. 533–538. doi: 10.1111/j.1365-2249.1993.tb08230.x

17. Das R., Koo M.S., Kim B.H., Jacob S.T., Subbian S., Yao J., Leng L., Levy R., Murchison C., Burman W.J., Moore C.C., Michael Scheld W., David J.R., Kaplan G., MacMicking J.D., Bucala R. Macrophage migration inhibitory factor (MIF) is a critical mediator of the innate immune response to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA, 2013, vol. 110: E2997. doi: 10.1073/pnas.1301128110

18. Deffert C., Cachat J., Krause K.H. Phagocyte NADPH oxidase, chronic granulomatous disease and mycobacterial infections. Cell Microbiol., 2014, vol. 16, pp. 1168–1178. doi: 10.1111/cmi.12322

19. DeLeo F.R. Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis, 2004, vol. 9, pp. 399–413. doi: 10.1023/B:APP T.0000031448.64969.fa

20. Desvignes L., Ernst J.D. Interferon-γ-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity, 2009, vol. 31, pp. 974–985. doi: 10.1016/j.immuni.2009.10.007

21. Dorhoi A., Desel C., Yeremeev V., Pradl L., Brinkmann V., Mollenkopf H.J., Hanke K., Gross O., Ruland J., Kaufmann S.H.E. The adaptor molecule CARD9 is essential for tuberculosis control. J. Exp. Med., 2010, vol. 207, pp. 777–792. doi: 10.1084/jem.20090067

22. Dorhoi A., Iannaccone M., Farinacci M., Faé K.C., Schreiber J., Moura-Alves P., Nouailles G., Mollenkopf H.J., OberbeckMüller D., Jörg S., Heinemann E., Hahnke K., Löwe D., Del Nonno F., Goletti D., Capparelli R., Kaufmann S.H.E. MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment. J. Clin. Invest., 2013, vol. 123, pp. 4836–4848. doi: 10.1172/JCI67604

23. Ellison M.A., Gearheart C.M., Porter C.C., Ambruso D.R. IFN-γ alters the expression of diverse immunity related genes in a cell culture model designed to represent maturing neutrophils. PLoS One, 2017, vol. 12: e0185956. doi: 10.1371/journal.pone.0185956

24. Eruslanov E.B., Lyadova I.V., Kondratieva T.H., Majorov K.B., Scheglov I.V., Orlova M.O., Apt A.S. Neutrophil responses to Mycobacterium tuberculosis infection in genetically susceptible and resistant mice neutrophil responses to Mycobacterium tuberculosis infection in genetically susceptible and resistant mice. Infect. Immun., 2005, vol. 73, pp. 1744–1753. doi: 10.1128/IAI.73.3.1744

25. Ethuin F., Gérard 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. Investig., 2004, vol. 84, pp. 1363–1371. doi: 10.1038/labinvest.3700148

26. Eum S.Y., Kong J.H., Hong M.S., Lee Y.J., Kim J.H., Hwang S.H., Cho S.H., Via S.N., Laura E., Clifton B.E. Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest, 2010, vol. 137, pp. 122–128. doi: 10.1378/chest.09-0903

27. Francis R.J., Butler R.E., Stewart G.R. Mycobacterium tuberculosis ESAT-6 is a leukocidin causing Ca2+ influx, necrosis and neutrophil extracellular trap formation. Cell Death Dis., 2014, vol. 5: e1474. doi: 10.1038/cddis.2014.394

28. Futosi K., Fodor S., Mócsai A. Reprint of neutrophil cell surface receptors and their intracellular signal transduction pathways. Int. Immunopharmacology, 2013, vol. 17, pp. 1185–1197. doi: 10.1016/j.intimp.2013.11.010

29. Ganz T. Defensins: Antimicrobial peptides of innate immunity. Nat. Rev. Immunol., 2003, vol. 3, pp. 710–720. doi: 10.1038/nri1180

30. Gopal R., Monin L., Torres D., Slight S., Mehra S., McKenna K.C., Junecko B.A.F., Reinhart T.A., Kolls J., Báez-Saldańa R., Cruz-Lagunas A., Rodríguez-Reyna T.S., Kumar N.P., Tessier P., Roth J., Selman M., Becerril-Villanueva E., BaqueraHeredia J., Cumming B., Kasprowicz V.O., Steyn A.J.C., Babu S., Kaushal D., Zúñiga J., Vogl T., Rangel-Moreno J., Khader Sh.A. S100A8/A9 proteins mediate neutrophilic inflammation and lung pathology during tuberculosis. Am. J. Respir. Crit. Care Med., 2013, vol. 188, pp. 1137–1146. doi: 10.1164/rccm.201304-0803OC

31. Alvarez-Jiménez V.D., Leyva-Paredes K., Campillo-Navarro M., Romo-Cruz I., Hugo Rosales-García V., CastañedaCasimiro J., González-Pozos S., Manuel Hernández J., Wong-Baeza C., Estela García-Pérez B., Ortiz-Navarrete V., EstradaParra S., Serafín-López J., Wong-Baeza I., Estrada-García I. Extracellular vesicles released from Mycobacterium tuberculosisinfected neutrophils promote macrophage autophagy and decrease intracellular mycobacterial survival. Front. Immunol., 2018, vol. 9: 272. doi: 10.3389/fimmu.2018.00272

32. Hilda J.N., Das S., Tripathy S.P., Hanna L.E. Role of neutrophils in tuberculosis: a bird’s eye view. Innate Immun., 2020, vol. 26, no. 4, pp. 240–247. doi: 10.1177/1753425919881176

33. Jena P., Mohanty S., Mohanty T., Kallert S., Morgelin M., Lindstrøm T., Borregaard N., Stenger S., Sonawane A., Sørensen O.E. Azurophil granule proteins constitute the major mycobactericidal proteins in human neutrophils and enhance the killing of mycobacteria in macrophages. PLoS One, 2012, vol. 7: e50345. doi: 10.1371/journal.pone.0050345

34. Jin L., Batra S., Douda D.N., Palaniyar N., Jeyaseelan S. CXCL1 contributes to host defense in polymicrobial sepsis via modulating T cell and neutrophil functions. J. Immunol., 2014, vol. 193, pp. 3549–3558. doi: 10.4049/jimmunol.1401138

35. Keller C., Hoffmann R., Lang R., Brandau S., Hermann C., Ehlers S. Genetically determined susceptibility to tuberculosis in mice causally involves accelerated and enhanced recruitment of granulocytes. Infect. Immun., 2006, vol. 74, pp. 4295–4309. doi: 10.1128/IAI.00057-06

36. Kimmey J.M., Huynh J.P., Weiss L.A., Park S., Kambal A., Debnath J., Virgin H.W., Stallings C.L. Unique role for ATG5 in neutrophil-mediated immunopathology during M. tuberculosis infection. Nature, 2015, vol. 528, pp. 565–569. doi: 10.1038/nature16451

37. Kondratieva T.K., Rubakova E.I., Linge I.A., Evstifeev V.V., Majorov K.B., Apt A.S. B cells delay neutrophil migration toward the site of stimulus: tardiness critical for effective Bacillus Calmette–Guerin vaccination against tuberculosis infection in mice. J. Immunol., 2010, vol. 184, pp. 1227–1234. doi: 10.4049/jimmunol.0902011

38. Kroon E.E., Coussens A.K., Kinnear C., Orlova M., Möller M., Seeger A., Wilkinson R.J., Hoal E.G., Schurr E. Neutrophils: innate effectors of TB resistance? Front. Immunol., 2018, vol. 9: 2637. doi: 10.3389/fimmu.2018.02637

39. Law K., Weiden M., Harkin T., Tchou-Wong K., Chi C., Rom W.N. Increased release of interleukin-1β, interleukin-6, and tumor necrosis factor-α by bronchoalveolar cells lavaged from involved sites in pulmonary tuberculosis. Am. J. Respir. Crit. Care Med., 1996, vol. 153, pp. 799–804. doi: 10.1164/ajrccm.153.2.8564135

40. Liles W.C., Ledbetter J.A., Waltersdorph A.W., Klebanoff S.J. Cross-linking of CD18 primes human neutrophils for activation of the respiratory burst in response to specific stimuli: Implications for adhesion-dependent physiological responses in neutrophils. J. Leukoc. Biol., 1995, vol. 58, pp. 690–697. doi: 10.1002/jlb.58.6.690

41. Lovewell R.R., Baer C.E., Mishra B.B., Smith C.M., Sassetti C.M. Granulocytes act as a niche for Mycobacterium tuberculosis growth. Mucosal Immunol., 2020, vol. 14, pp. 229–241. doi: 10.1038/s41385-020-0300-z

42. Lowe D.M., Bandara A.K., Packe G.E., Barker R.D., Wilkinson R.J., Griffiths C.J., Martineau A.R. Neutrophilia independently predicts death in tuberculosis. Eur. Respir. J., 2013, vol. 42, pp. 1752–1757. doi: 10.1183/09031936.00140913

43. Lowe D.M., Demaret J., Bangani N., Nakiwala J.K., Goliath R., Wilkinson K.A., Wilkinson R.J., Martineau A.R. Differential effect of viable versus necrotic neutrophils on mycobacterium tuberculosis growth and cytokine induction in whole blood. Front. Immunol., 2018, vol. 9: 27. doi: 10.3389/fimmu.2018.00903

44. Lyadova I.V. Review article neutrophils in tuberculosis: heterogeneity shapes the way? Mediators Inflamm., 2017, vol. 2017: 8619307. doi: 10.1155/2017/8619307

45. Martineau A.R., Newton S.M., Wilkinson K.A., Kampmann B., Hall B.M., Nawroly N., Packe G., Davidson R.N., Griffiths C.J., Wilkinson R.J. Neutrophil-mediated innate immune resistance to mycobacteria. J. Clin. Invest., 2007, vol. 117, pp. 1988–1994. doi: 10.1172/JCI31097

46. Marzo E., Vilaplana C., Tapia G., Diaz J., Garcia V., Cardona P.-J. Damaging role of neutrophilic infiltration in a mouse model of progressive tuberculosis. Tuberculosis, 2014, vol. 94, pp. 55–64. doi: 10.1016/j.tube.2013.09.004

47. Mayadas T.N., Cullere X., Lowell C.A. The Multifaceted functions of neutrophils. Annu. Rev. Pathol., 2014, vol. 9, pp. 181–218. doi: 10.1146/annurev-pathol-020712-164023

48. McCracken J.M., Allen L.A.H. Regulation of human neutrophil apoptosis and lifespan in health and disease. J. Cell Death, 2014, vol. 7, pp. 15–23. doi: 10.4137/JCD.S11038

49. Miralda I., Uriarte S.M., McLeish K.R. Multiple phenotypic changes define neutrophil priming. Front. Cell. Infect. Microbiol., 2017, vol. 7: 217. doi: 10.3389/fcimb.2017.00217

50. Mitra S., Abraham E. Participation of superoxide in neutrophil activation and cytokine production. Biochim. Biophys. Acta-Mol. Basis. Dis., 2006, vol. 1762, pp. 732–741. doi: 10.1016/j.bbadis.2006.06.011

51. Muefong C.N., Sutherland J.S. Neutrophils in tuberculosis-associated inflammation and lung pathology. Front. Immunol., 2020, vol. 11: 962. doi: 10.3389/fimmu.2020.00962

52. N’Diaye E.-N., Darzacq X., Astarie-Dequeker C., Daffé M., Calafat J., Maridonneau-Parini I. Fusion of azurophil granules with phagosomes and activation of the tyrosine kinase hck are specifically inhibited during phagocytosis of mycobacteria by human neutrophils. J. Immunol., 1998, vol. 161, pp. 4983–4991.

53. Nandi B., Behar S.M. Regulation of neutrophils by interferon-γ limits lung inflammation during tuberculosis infection. J. Exp. Med., 2011, vol. 208, pp. 2251–2262. doi: 10.1084/jem.20110919

54. Nathan C. Points of control in inflammation. Nature, 2002, vol. 420, pp. 846–852. doi: 10.1038/nature01320

55. Nathan C., Cunningham-Bussel A. Beyond oxidative stress: an immunologist’s guide to reactive oxygen species. Nat. Rev. Immunol., 2013, vol. 13, pp. 349–361. doi: 10.1038/nri3423

56. Neufert C., Pai R.K., Noss E.H., Berger M., Boom W.H., Harding C.V. Mycobacterium tuberculosis 19-kDa lipoprotein promotes neutrophil activation. J. Immunol., 2001, vol. 167, pp. 1542–1549. doi: 10.4049/jimmunol.167.3.1542

57. Niazi M.K.K., Dhulekar N., Schmidt D., Major S., Cooper R., Abeijon C., Gatti D.M., Kramnik I., Yener B., Gurcan M., Beamer G. Lung necrosis and neutrophils reflect common pathways of susceptibility to Mycobacterium tuberculosis in genetically diverse, immune-competent mice. Dis. Model. Mech., 2015, vol. 8, pp. 1141–1153. doi: 10.1242/dmm.020867

58. Nouailles G., Dorhoi A., Koch M., Zerrahn J., Weiner J., Faé K.C., Arrey F., Kuhlmann S., Bandermann S., Loewe D., Mollen kopf H.J., Vogelzang A., Meyer-Schwesinger C., Mittrücker H.W., McEwen G., Kaufmann S.H.E. CXCL5-secreting pulmonary epithelial cells drive destructive neutrophilic inflammation in tuberculosis. J. Clin. Invest., 2014, vol. 124, pp. 1268–1282. doi: 10.1172/JCI72030

59. O’Garra A., Redford P.S., McNab F.W., Bloom C.I., Wilkinson R.J., Berry M.P.R. The immune response in tuberculosis. Annu. Rev. Immunol., 2013, vol. 31, pp. 475–527. doi: 10.1146/annurev-immunol-032712-095939

60. Papayannopoulos V., Zychlinsky A. NETs: a new strategy for using old weapons. Trends Immunol., 2009, vol. 30, pp. 513–521. doi: 10.1016/j.it.2009.07.011

61. Petrofsky M., Bermudez L.E. Neutrophils from Mycobacterium avium-infected mice produce TNFα, IL-12, and IL-1β and have a putative role in early host response. Clin. Immunol., 1999, vol. 91, pp. 354–358. doi: 10.1006/clim.1999.4709

62. Riedel D.D., Kaufmann S.H.E. Chemokine secretion by human polymorphonuclear granulocytes after stimulation with mycobacterium tuberculosis and lipoarabinomannan. Infect. Immun., 1997, vol. 65, pp. 4620–4623. doi: 10.1128/IAI.65.11.4620-4623.1997

63. Rivas-Santiago B., Hernandez-Pando R., Carranza C., Juarez E., Contreras J.L., Aguilar-Leon D., Torres M., Sada E. Expression of cathelicidin LL-37 during Mycobacterium tuberculosis infection in human alveolar macrophages, monocytes, neutrophils, and epithelial cells. Infect. Immun., 2008, vol. 76, pp. 935–941. doi: 10.1128/IAI.01218-07

64. Russell D.G. Mycobacterium tuberculosis: here today, and here tomorrow. Nat. Rev. Mol. Cell Biol., 2001, vol. 2, pp. 569–577. doi: 10.1038/35085034

65. Russell D.G. Who puts the tubercle in tuberculosis? Nat. Rev. Microbiol., 2007, vol. 5, pp. 39–47. doi: 10.1038/nrmicro1538

66. Ryckman C., McColl S.R., Vandal K., De Médicis R., Lussier A., Poubelle P.E., Tessier P.A. Role of S100A8 and S100A9 in neutrophil recruitment in response to monosodium urate monohydrate crystals in the air-pouch model of acute gouty arthritis. Arthritis Rheum., 2003, vol. 48, pp. 2310–2320. doi: 10.1002/art.11079

67. Sakai S., Kauffman K.D., Sallin M.A., Sharpe A.H., Young H.A., Ganusov V.V., Barber V.V., Daniel L. CD4 T cell-derived IFN-γ plays a minimal role in control of pulmonary Mycobacterium tuberculosis infection and must be actively repressed by PD-1 to prevent lethal disease. PLoS Pathog., 2016, vol. 12, no. 5: e1005667. doi: 10.1371/journal.ppat.1005667

68. Sawant K.V., McMurray D.N. Guinea pig neutrophils infected with Mycobacterium tuberculosis produce cytokines which activate alveolar macrophages in noncontact cultures. Infect. Immun., 2007, vol. 75, pp. 1870–1877. doi: 10.1128/IAI.00858-06

69. Schneider B.E., Korbel D., Hagens K., Koch M., Raupach B., Enders J., Kaufmann S.H.E., Mittrücker H.W., Schaible U.E. A role for IL-18 in protective immunity against Mycobacterium tuberculosis. Eur. J. Immunol., 2010, vol. 40, pp. 396–405. doi: 10.1002/eji.200939583

70. Scott N.R., Swanson R.V., Al-Hammadi N., Domingo-Gonzalez R., Rangel-Moreno J., Kriel B.A., Domingo-Gonzalez R., Rangel-Moreno J., Kriel B.A., Bucsan A.N., Das S., Ahmed M., Mehra S., Treerat P., Cruz-Lagunas A., Jimenez-Alvarez L., Muñoz-Torrico M., Bobadilla-Lozoya K., Vogl T., Walzl G., du Plessis N., Kaushal D., Scriba T., Zuñiga J., Khader S. S100A8/ A9 regulates CD11b expression and neutrophil recruitment during chronic tuberculosis. J. Clin. Invest., 2020, vol. 130, no. 6, pp. 3098–3112. doi: 10.1172/JCI130546

71. Seiler P., Aichele P., Raupach B., Odermatt B., Steinhoff U., Kaufmann S.H.E. Rapid neutrophil response controls fast-replicating intracellular bacteria but not slow-replicating Mycobacterium tuberculosis. J. Infect. Dis., 2000, vol. 181, pp. 671–680. doi: 10.1086/315278

72. Sharma S., Verma I., Khuller G.K. Therapeutic potential of human neutrophil peptide 1 against experimental tuberculosis. Antimicrob. Agents Chemother., 2001, vol. 45, pp. 639–640. doi: 10.1128/AAC.45.2.639-640.2001

73. Shea-Donohue T., Thomas K., Cody M.J., Zhao A., Detolla L.J., Kopydlowski K.M., Fukata M., Lira S.A., Vogel S.N. Mice deficient in the CXCR2 ligand, CXCL1 (KC/GRO-α), exhibit increased susceptibility to dextran sodium sulfate (DSS)-induced colitis. Innate Immun., 2008, vol. 14, pp. 117–124. doi: 10.1177/1753425908088724

74. Spiekermann K., Roesler J., Emmendoerffer A., Elsner J., Welte K. Functional features of neutrophils induced by G-CSF and GMCSF treatment: Differential effects and clinical implications. Leukemia, 1997, vol. 11, pp. 466–478. doi: 10.1038/sj.leu.2400607

75. Stamm C.E., Collins A.C., Shiloh M.U. Sensing of Mycobacterium tuberculosis and consequences to both host and bacillus. Immunol. Rev., 2015, vol. 264, pp. 204–219. doi: 10.1111/imr.12263

76. Steinwede K., Maus R., Bohling J., Voedisch S., Braun A., Ochs M., Schmiedl A., Länger F., Gauthier F., Roes J., Welte T., Bange F.C., Niederweis M., Bühling F., Maus U.A. Cathepsin G and neutrophil elastase contribute to lung-protective immunity against mycobacterial infections in mice. J. Immunol., 2012, vol. 188, pp. 4476–4487. doi: 10.4049/jimmunol.1103346

77. Stek C., Allwood B., Walker N.F., Wilkinson R.J., Lynen L., Meintjes G. The immune mechanisms of lung parenchymal damage in tuberculosis and the role of host-directed therapy. Front. Microbiol., 2018, vol. 9: 2603. doi: 10.3389/fmicb.2018.02603

78. Strieter R.M., Kasahara K., Allen R.M., Standiford T.J., Rolfe M.W., Becker F.S., Chensue S.W., Kunkel S.L. Cytokine-induced neutrophil-derived interleukin-8. Am. J. Pathol., 1992, vol. 141, pp. 397–407. URL: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1886610

79. Sugawara I., Udagawa T., Yamada H. Rat neutrophils prevent the development of tuberculosis. Infect. Immun., 2004, vol. 72, pp. 1804–1806. doi: 10.1128/IAI.72.3.1804-1806.2004

80. Summers C., Rankin S.M., Condliffe A.M., Singh N., Peters A.M., Chilvers E.R. Neutrophil kinetics in health and disease. Trends Immunol., 2010, vol. 31, pp. 318–324. doi: 10.1016/j.it.2010.05.006

81. Sunahori K., Yamamura M., Yamana J., Takasugi K., Kawashima M., Yamamoto H., Chazin W.J., Nakatani Y., Yui S., Makino H. The S100A8/A9 heterodimer amplifies proinflammatory cytokine production by macrophages via activation of nuclear factor kappa B and p38 mitogen-activated protein kinase in rheumatoid arthritis. Arthritis Res. Ther., 2006, vol. 8: 69. doi: 10.1186/ar1939

82. Sutherland J.S., Jeffries D.J., Donkor S., Walther B., Hill P.C., Adetifa I.M.O., Adegbola I.M.O., Ota R.A., Martin O.C. High granulocyte/lymphocyte ratio and paucity of NKT cells defines TB disease in a TB-endemic setting. Tuberculosis, 2009, vol. 89, pp. 398–404. doi: 10.1016/j.tube.2009.07.004

83. Tan B.H., Meinken C., Bastian M., Bruns H., Legaspi A., Ochoa M.T., Krutzik S.R., Bloom B.R., Ganz T., Modlin R.L., Stenger S. Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens. J. Immunol., 2006, vol. 177, pp. 1864–1871. doi: 10.4049/jimmunol.177.3.1864

84. Trentini M.M., de Oliveira F.M., Kipnis A., Junqueira-Kipnis A.P. The role of neutrophils in the induction of specific Th1 and Th17 during vaccination against tuberculosis. Front. Microbiol., 2016, vol. 7: 898. doi: 10.3389/fmicb.2016.00898

85. Ueda Y., Cain D.W., Kuraoka M., Kondo M., Kelsoe G. IL-1R type I-dependent hemopoietic stem cell proliferation is necessary for inflammatory granulopoiesis and reactive neutrophilia. J. Immunol., 2009, vol. 182, pp. 6477–6484. doi: 10.4049/jimmunol.0803961

86. Velmurugan K., Chen B., Miller J.L., Azogue S., Gurses S., Hsu T., Glickman M., Jacobs W.R., Porcelli S.A., Briken V. Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog., 2007, vol. 3, no. 7: e110. doi: 10.1371/journal.ppat.0030110

87. Voskuil M.I., Bartek I.L., Visconti K., Schoolnik G.K. The response of Mycobacterium tuberculosis to reactive oxygen and nitrogen species. Front. Microbiol., 2011, vol. 2: 105. doi: 10.3389/fmicb.2011.00105

88. Vyas S.P., Goswami R. Striking the right immunological balance prevents progression of tuberculosis. Inflamm. Res., 2017, vol. 66, pp. 1031–1056. doi: 10.1007/s00011-017-1081-z

89. Warnatsch A., Tsourouktsoglou T.D., Branzk N., Wang Q., Reincke S., Herbst S., Gutierrez M., Papayannopoulos V. Reactive oxygen species localization programs inflammation to clear microbes of different size. Immunity, 2017, vol. 46, pp. 421–432. doi: 10.1016/j.immuni.2017.02.013

90. Weisbart R.H., Golde D.W., Clark S.C., Wong G.G., Gasson J.C. Human granulocyte-macrophage colony-stimulating factor is a neutrophil activator. Nature, 1985, vol. 314, pp. 361–363. doi: 10.1038/314361a0

91. Wengner A.M., Pitchford S.C., Furze R.C., Rankin S.M. The coordinated action of G-CSF and ELR CXC chemokines in neutrophil mobilization during acute inflammation. Blood, 2008, vol. 111, no. 1, pp. 42–49. doi: 10.1182/blood-2007-07-099648

92. Witko-Sarsat V., Rieu P., Descamps-Latscha B., Lesavre P., Halbwachs-Mecarelli L. Neutrophils: molecules, functions and pathophysiological aspects. Lab. Investig., 2000, vol. 80, pp. 617–654. doi: 10.1038/labinvest.3780067

93. Wolf A.J., Linas B., Trevejo-Nuñez G.J., Kincaid E., Tamura T., Takatsu K., Ernst J.D. Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J. Immunol., 2007, vol. 179, pp. 2509–2519. doi: 10.4049/jimmunol.179.4.2509

94. Yang C.T., Cambier C.J., Davis J.M., Hall C.J., Crosier P.S., Ramakrishnan L. Neutrophils exert protection in the early tuberculous granuloma by oxida tive killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe, 2012, vol. 12, pp. 301–312. doi: 10.1016/j.chom.2012.07.009

95. Yeremeev V., Linge I., Kondratieva T., Apt A. Neutrophils exacerbate tuberculosis infection in genetically susceptible mice. Tuberculosis, 2015, vol. 95, pp. 447–451. doi: 10.1016/j.tube.2015.03.007

96. Zanetti M. Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol., 2004, vol. 75, pp. 39–48. doi: 10.1189/jlb.0403147


Дополнительные файлы

Для цитирования:


Линге И.А., Апт А.С. Нейтрофилы: неоднозначная роль в патогенезе туберкулеза. Инфекция и иммунитет. 2021;11(5):809-819. https://doi.org/10.15789/2220-7619-ACR-1670

For citation:


Linge I.A., Apt A.S. A controversial role of neutrophils in tuberculosis infection pathogenesis. Russian Journal of Infection and Immunity. 2021;11(5):809-819. (In Russ.) https://doi.org/10.15789/2220-7619-ACR-1670

Просмотров: 142


Creative Commons License
Контент доступен под лицензией Creative Commons Attribution 4.0 License.


ISSN 2220-7619 (Print)
ISSN 2313-7398 (Online)