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Unexpected Role for IL-17 in Protective Immunity against Hypervirulent HN878 Infection
Mycobacterium tuberculosis (Mtb), the causative agent of tuberculosis (TB), infects one third of the world's population. Among these infections, clinical isolates belonging to the W-Beijing are emerging, representing about 50% of Mtb isolates in East Asia, and about 13% of all Mtb isolates worldwide. In animal models, infection with W-Beijing strain, Mtb HN878, is considered “hypervirulent” resulting in increased mortality. The proinflammatory cytokine Interleukin (IL)-17 is thought to be dispensable for primary immunity against Mtb infection. We report here that while IL-17 is dispensable for protection against infection with lab adapted Mtb strains such as H37Rv, or less virulent Mtb clinical isolates such as Mtb CDC1551, IL-17 is required for early protective immunity against Mtb HN878 infection. The dependence on IL-17 to drive protective immunity against Mtb HN878 is due to the differential ability to induce high levels of IL-1β through a TLR-2-dependent mechanism, driving potent IL-17 responses, induction of the chemokine CXCL-13 and localization of T cells within lung lymphoid follicles for maximal macrophage activation and Mtb control. Together, our data change the existing paradigm that IL-17 is dispensable for primary immunity against Mtb infection, and suggests a differential requirement for IL-17 in protective immunity against some emerging Mtb strains.
Vyšlo v časopise: Unexpected Role for IL-17 in Protective Immunity against Hypervirulent HN878 Infection. PLoS Pathog 10(5): e32767. doi:10.1371/journal.ppat.1004099
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004099Souhrn
Mycobacterium tuberculosis (Mtb), the causative agent of tuberculosis (TB), infects one third of the world's population. Among these infections, clinical isolates belonging to the W-Beijing are emerging, representing about 50% of Mtb isolates in East Asia, and about 13% of all Mtb isolates worldwide. In animal models, infection with W-Beijing strain, Mtb HN878, is considered “hypervirulent” resulting in increased mortality. The proinflammatory cytokine Interleukin (IL)-17 is thought to be dispensable for primary immunity against Mtb infection. We report here that while IL-17 is dispensable for protection against infection with lab adapted Mtb strains such as H37Rv, or less virulent Mtb clinical isolates such as Mtb CDC1551, IL-17 is required for early protective immunity against Mtb HN878 infection. The dependence on IL-17 to drive protective immunity against Mtb HN878 is due to the differential ability to induce high levels of IL-1β through a TLR-2-dependent mechanism, driving potent IL-17 responses, induction of the chemokine CXCL-13 and localization of T cells within lung lymphoid follicles for maximal macrophage activation and Mtb control. Together, our data change the existing paradigm that IL-17 is dispensable for primary immunity against Mtb infection, and suggests a differential requirement for IL-17 in protective immunity against some emerging Mtb strains.
Zdroje
1. BifaniPJ, MathemaB, KurepinaNE, KreiswirthBN (2002) Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains. Trends Microbiol 10 : 45–52.
2. KremerK, GlynnJR, LillebaekT, NiemannS, KurepinaNE, et al. (2004) Definition of the Beijing/W lineage of Mycobacterium tuberculosis on the basis of genetic markers. J Clin Microbiol 42 : 4040–4049.
3. van SoolingenD, QianL, de HaasPE, DouglasJT, TraoreH, et al. (1995) Predominance of a single genotype of Mycobacterium tuberculosis in countries of east Asia. J Clin Microbiol 33 : 3234–3238.
4. OrdwayDJ, ShangS, Henao-TamayoM, Obregon-HenaoA, NoldL, et al. (2011) Mycobacterium bovis BCG-mediated protection against W-Beijing strains of Mycobacterium tuberculosis is diminished concomitant with the emergence of regulatory T cells. Clin Vaccine Immunol 18 : 1527–1535.
5. KruunerA, HoffnerSE, SillastuH, DanilovitsM, LevinaK, et al. (2001) Spread of drug-resistant pulmonary tuberculosis in Estonia. J Clin Microbiol 39 : 3339–3345.
6. GlynnJR, WhiteleyJ, BifaniPJ, KremerK, van SoolingenD (2002) Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review. Emerg Infect Dis 8 : 843–849.
7. CawsM, ThwaitesG, StepniewskaK, NguyenTN, NguyenTH, et al. (2006) Beijing genotype of Mycobacterium tuberculosis is significantly associated with human immunodeficiency virus infection and multidrug resistance in cases of tuberculous meningitis. J Clin Microbiol 44 : 3934–3939.
8. MancaC, TsenovaL, BergtoldA, FreemanS, ToveyM, et al. (2001) Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha/beta. Proc Natl Acad Sci U S A 98 : 5752–5757.
9. OrdwayD, Henao-TamayoM, HartonM, PalanisamyG, TroudtJ, et al. (2007) The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol 179 : 522–531.
10. MancaC, TsenovaL, FreemanS, BarczakAK, ToveyM, et al. (2005) Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J Interferon Cytokine Res 25 : 694–701.
11. ReedMB, DomenechP, MancaC, SuH, BarczakAK, et al. (2004) A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431 : 84–87.
12. KollsJK, KhaderSA (2010) The role of Th17 cytokines in primary mucosal immunity. Cytokine Growth Factor Rev 21 : 443–448.
13. KhaderSA, PearlJE, SakamotoK, GilmartinL, BellGK, et al. (2005) IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J Immunol 175 : 788–795.
14. AujlaSJ, ChanYR, ZhengM, FeiM, AskewDJ, et al. (2008) IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 14 : 275–281.
15. KhaderSA, GuglaniL, Rangel-MorenoJ, GopalR, Fallert JuneckoBA, et al. (2011) IL-23 Is Required for Long-Term Control of Mycobacterium tuberculosis and B Cell Follicle Formation in the Infected Lung. J Immunol 187 : 5402–5407.
16. KhaderSA, BellGK, PearlJE, FountainJJ, Rangel-MorenoJ, et al. (2007) IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 8 : 369–377.
17. GopalR, Rangel-MorenoJ, SlightS, LinY, NawarHF, et al. (2013) Interleukin-17-dependent CXCL13 mediates mucosal vaccine-induced immunity against tuberculosis. Mucosal Immunol 6 : 972–984.
18. NakaeS, KomiyamaY, NambuA, SudoK, IwaseM, et al. (2002) Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17 : 375–387.
19. ZhengM, ShellitoJE, MarreroL, ZhongQ, JulianS, et al. (2001) CD4+ T cell-independent vaccination against Pneumocystis carinii in mice. J Clin Invest 108 : 1469–1474.
20. SlightSR, Rangel-MorenoJ, GopalR, LinY, Fallert JuneckoBA, et al. (2013) CXCR5+ T helper cells mediate protective immunity against tuberculosis. J Clin Invest 123 : 712–26.
21. ReileyWW, CalayagMD, WittmerST, HuntingtonJL, PearlJE, et al. (2008) ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc Natl Acad Sci U S A 105 : 10961–10966.
22. KhaderSA, Partida-SanchezS, BellG, Jelley-GibbsDM, SwainS, et al. (2006) Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J Exp Med 203 : 1805–1815.
23. KhaderSA, Rangel-MorenoJ, FountainJJ, MartinoCA, ReileyWW, et al. (2009) In a murine tuberculosis model, the absence of homeostatic chemokines delays granuloma formation and protective immunity. J Immunol 183 : 8004–8014.
24. NurievaRI, ChungY, HwangD, YangXO, KangHS, et al. (2008) Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29 : 138–149.
25. SuttonC, BreretonC, KeoghB, MillsKH, LavelleEC (2006) A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J Exp Med 203 : 1685–1691.
26. YoshidaA, InagawaH, KohchiC, NishizawaT, SomaG (2009) The role of toll-like receptor 2 in survival strategies of Mycobacterium tuberculosis in macrophage phagosomes. Anticancer Res 29 : 907–910.
27. KleinnijenhuisJ, JoostenLA, van de VeerdonkFL, SavageN, van CrevelR, et al. (2009) Transcriptional and inflammasome-mediated pathways for the induction of IL-1beta production by Mycobacterium tuberculosis. Eur J Immunol 39 : 1914–1922.
28. LinY, RitcheaS, LogarA, SlightS, MessmerM, et al. (2009) Interleukin-17 Is Required for T Helper 1 Cell Immunity and Host Resistance to the Intracellular Pathogen Francisella tularensis. Immunity 31 : 799–810.
29. BaiH, ChengJ, GaoX, JoyeeAG, FanY, et al. (2009) IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J Immunol 183 : 5886–5895.
30. GopalR, Rangel-MorenoJ, SlightS, LinY, NawarHF, et al. (2013) Interleukin-17-dependent CXCL13 mediates mucosal vaccine-induced immunity against tuberculosis. Mucosal Immunol 6 : 972–84.
31. AgertonTB, ValwaySE, BlinkhornRJ, ShilkretKL, RevesR, et al. (1999) Spread of strain W, a highly drug-resistant strain of Mycobacterium tuberculosis, across the United States. Clin Infect Dis 29 : 85–92 discussion 93–85.
32. SinsimerD, HuetG, MancaC, TsenovaL, KooMS, et al. (2008) The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect Immun 76 : 3027–3036.
33. CambierCJ, TakakiKK, LarsonRP, HernandezRE, TobinDM, et al. (2014) Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 505 : 218–222.
34. Rangel-MorenoJ, CarragherDM, de la Luz Garcia-HernandezM, HwangJY, KusserK, et al. (2011) The development of inducible bronchus-associated lymphoid tissue depends on IL-17. Nat Immunol 12 : 639–646.
35. UmemuraM, YahagiA, HamadaS, BegumMD, WatanabeH, et al. (2007) IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol 178 : 3786–3796.
36. SchulzSM, KohlerG, SchutzeN, KnauerJ, StraubingerRK, et al. (2008) Protective immunity to systemic infection with attenuated Salmonella enterica serovar enteritidis in the absence of IL-12 is associated with IL-23-dependent IL-22, but not IL-17. J Immunol 181 : 7891–7901.
37. GopalR, KhaderSA (2013) Vaccines against tuberculosis: moving forward with new concepts. Expert Rev Vaccines 12 : 829–831.
38. JuradoJO, PasquinelliV, AlvarezIB, PenaD, RovettaAI, et al. (2012) IL-17 and IFN-gamma expression in lymphocytes from patients with active tuberculosis correlates with the severity of the disease. J Leukoc Biol 91 : 991–1002.
39. PengMY, WangZH, YaoCY, JiangLN, JinQL, et al. (2008) Interleukin 17-producing gamma delta T cells increased in patients with active pulmonary tuberculosis. Cell Mol Immunol 5 : 203–208.
40. SternJN, KeskinDB, RomeroV, ZunigaJ, EncinalesL, et al. (2009) Molecular signatures distinguishing active from latent tuberculosis in peripheral blood mononuclear cells, after in vitro antigenic stimulation with purified protein derivative of tuberculin (PPD) or Candida: a preliminary report. Immunol Res 45 : 1–12.
41. ChenX, ZhangM, LiaoM, GranerMW, WuC, et al. (2010) Reduced Th17 response in patients with tuberculosis correlates with IL-6R expression on CD4+ T Cells. Am J Respir Crit Care Med 181 : 734–742.
42. ScribaTJ, KalsdorfB, AbrahamsDA, IsaacsF, HofmeisterJ, et al. (2008) Distinct, Specific IL-17 - and IL-22-Producing CD4+ T Cell Subsets Contribute to the Human Anti-Mycobacterial Immune Response. J Immunol 180 : 1962–1970.
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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium
Článek Combined Systems Approaches Reveal Highly Plastic Responses to Antimicrobial Peptide Challenge inČlánek Two Novel Human Cytomegalovirus NK Cell Evasion Functions Target MICA for Lysosomal Degradation
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