A controversial role of neutrophils in tuberculosis infection pathogenesis
- Authors: Linge I.A.1, Apt A.S.1
-
Affiliations:
- Central Tuberculosis Research Institute
- Issue: Vol 11, No 5 (2021)
- Pages: 809-819
- Section: REVIEWS
- Submitted: 22.01.2021
- Accepted: 16.08.2021
- Published: 31.08.2021
- URL: https://iimmun.ru/iimm/article/view/1670
- DOI: https://doi.org/10.15789/2220-7619-ACR-1670
- ID: 1670
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Full Text
Abstract
Tuberculosis (TB) continues to be an important and unresolved medical problem. About a quarter of mankind is infected with Mycobacterium tuberculosis, and about 5–10% of these people eventually develop TB. Macrophages and CD4+ T cells are considered the key cells providing defense against TB infection. The role of neutrophils in TB is less well defined. Neutrophils are short-lived granulocytes among first migrate into the infectious lung tissue and phagocy tose mycobacteria. On the one hand, there is evidence for protective role of neutrophils in TB released via anti-microbial peptides inhibiting mycobacterial growth, up-regulation of CD4+ T-cell activation, and dendritic cell migration in the lymph nodes. On the other hand, infection of genetically TB susceptible animals leads to an overwhelming lung neutrophil inflammation, development of necrotic granulomata, and a rapid death. Neutrophils act directly or indirectly on mycobacteria by different oxidative or other reactions including neutrophil extracellular traps (NETs) formation. Phagocytosis of mycobacteria by neutrophils is accompanied by the production of pro-inflammatory factors, thus making neutrophils active participants of inflammation in all stages of the infectious process. Finally, neutrophils die by apoptosis or necrosis. Necrosis of neutrophils, which is activated by reactive oxygen species, also prolongs the inflammation. In this way, there is strong evidence that neutrophils are the cells involved in the transition of infection to the terminal stage, participating in lung tissue destruction. Although neutrophils evolutionary developed many ways to resist pathogens, it is likely, that neutrophils do not possess sufficient anti-mycobactericidal capacities due to the development of many adaptations allowing mycobacteria to survive inside the neutrophils. Neutrophils effectively phagocytose but poorly kill mycobacteria, thus hiding bacilli from more efficient killers, macrophages, and playing the role of the “Trojan Horse”. In this review, we summarize the data on the involvement of neutrophils in TB inflammation. We discuss their ambiguous role in pathogenesis which depends upon mycobacterial virulence, host genetics, dynamics of migration to inflammatory foci, and persistence during initial and chronic stages of the infectious process.
About the authors
I. A. Linge
Central Tuberculosis Research Institute
Author for correspondence.
Email: iralinge@gmail.com
ORCID iD: 0000-0003-1535-5800
Irina A. Linge, PhD (Biology), Senior Researcher, Laboratory of Immunogenetics, Immunology Department
107564, Moscow, Yauzskaya alley, 2
Phone: +7 499 785-90-72
РоссияA. S. Apt
Central Tuberculosis Research Institute
Email: alexapt0151@gmail.com
ORCID iD: 0000-0002-3683-3085
PhD, MD (Biology), Professor, Head of the Laboratory of Immunogenetics, Immunology Department
Moscow
РоссияReferences
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Ganz T. Defensins: Antimicrobial peptides of innate immunity. Nat. Rev. Immunol., 2003, vol. 3, pp. 710–720. doi: 10.1038/nri1180
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Lyadova I.V. Review article neutrophils in tuberculosis: heterogeneity shapes the way? Mediators Inflamm., 2017, vol. 2017: 8619307. doi: 10.1155/2017/8619307
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- Nathan C. Points of control in inflammation. Nature, 2002, vol. 420, pp. 846–852. doi: 10.1038/nature01320
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Russell D.G. Who puts the tubercle in tuberculosis? Nat. Rev. Microbiol., 2007, vol. 5, pp. 39–47. doi: 10.1038/nrmicro1538
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Zanetti M. Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol., 2004, vol. 75, pp. 39–48. doi: 10.1189/jlb.0403147