Allele-Specific Induction of IL-1β Expression by C/EBPβ and PU.1 Contributes to Increased Tuberculosis Susceptibility

English version České info

IL-1β is important for the initial establishment of antimicrobial adaptive immunity, but prolonged IL-1β expression can also cause progressive immunopathology during M. tuberculosis infection. The paradoxical activities of IL-1β in promoting both antimycobacterial immunity and chronic tissue damage have left the ultimate contribution of this cytokine to TB progression in human populations unclear. In this work, we address the role of IL-1β-mediated inflammation using a combination of human genetics and molecular biology, and suggest that exuberant IL-1β responses are causatively associated with TB progression and poor treatment outcome in humans. This work furthers our understanding of the immunological factors that underlie TB disease and provide a strong rationale for the development of specific anti-inflammatory adjunctive therapies that could improve the long-term outcome of TB treatment. In addition, these insights inform the design of future TB control efforts that include the rational design of disease-preventing vaccines and genotype-targeted delivery of TB chemotherapy.

Vyšlo v časopise: Allele-Specific Induction of IL-1β Expression by C/EBPβ and PU.1 Contributes to Increased Tuberculosis Susceptibility. PLoS Pathog 10(10): e32767. doi:10.1371/journal.ppat.1004426
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004426

Souhrn

Zdroje

1. AhmadS (2011) Pathogenesis, immunology, and diagnosis of latent Mycobacterium tuberculosis infection. Clin Dev Immunol 2011: 814943.

2. SiaIG, WielandML (2011) Current concepts in the management of tuberculosis. Mayo Clin Proc 86: 348–361.

3. El BaghdadiJ, GrantAV, SabriA, El AzbaouiS, ZaidiH, et al. (2013) [Human genetics of tuberculosis]. Pathol Biol (Paris) 61: 11–16.

4. CottleLE (2011) Mendelian susceptibility to mycobacterial disease. Clin Genet 79: 17–22.

5. MischEA, MacdonaldM, RanjitC, SapkotaBR, WellsRD, et al. (2008) Human TLR1 deficiency is associated with impaired mycobacterial signaling and protection from leprosy reversal reaction. PLoS Negl Trop Dis 2: e231.

6. CawsM, ThwaitesG, DunstanS, HawnTR, LanNT, et al. (2008) The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog 4: e1000034.

7. ThuongNT, HawnTR, ThwaitesGE, ChauTT, LanNT, et al. (2007) A polymorphism in human TLR2 is associated with increased susceptibility to tuberculous meningitis. Genes Immun 8: 422–428.

8. TobinDM, VaryJCJr, RayJP, WalshGS, DunstanSJ, et al. (2010) The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 140: 717–730.

9. ZhangG, ChenX, ChanL, ZhangM, ZhuB, et al. (2011) An SNP selection strategy identified IL-22 associating with susceptibility to tuberculosis in Chinese. Sci Rep 1: 20.

10. ZhangG, ZhouB, WangW, ZhangM, ZhaoY, et al. (2012) A functional single-nucleotide polymorphism in the promoter of the gene encoding interleukin 6 is associated with susceptibility to tuberculosis. J Infect Dis 205: 1697–1704.

11. HayashiF, WatanabeM, NanbaT, InoueN, AkamizuT, et al. (2009) Association of the -31C/T functional polymorphism in the interleukin-1beta gene with the intractability of Graves' disease and the proportion of T helper type 17 cells. Clin Exp Immunol 158: 281–286.

12. LiC, WangC (2013) Current evidences on IL1B polymorphisms and lung cancer susceptibility: a meta-analysis. Tumour Biol 34: 3477–3482.

13. ChenML, LiaoN, ZhaoH, HuangJ, XieZF (2014) Association between the IL1B (−511), IL1B (+3954), IL1RN (VNTR) polymorphisms and Graves' disease risk: a meta-analysis of 11 case-control studies. PLoS One 9: e86077.

14. El-OmarEM, CarringtonM, ChowWH, McCollKE, BreamJH, et al. (2000) Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 404: 398–402.

15. MishraBB, RathinamVA, MartensGW, MartinotAJ, KornfeldH, et al. (2013) Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1beta. Nat Immunol 14: 52–60.

16. AwomoyiAA, CharuratM, MarchantA, MillerEN, BlackwellJM, et al. (2005) Polymorphism in IL1B: IL1B-511 association with tuberculosis and decreased lipopolysaccharide-induced IL-1beta in IFN-gamma primed ex-vivo whole blood assay. J Endotoxin Res 11: 281–286.

17. KusuharaK, YamamotoK, OkadaK, MizunoY, HaraT (2007) Association of IL12RB1 polymorphisms with susceptibility to and severity of tuberculosis in Japanese: a gene-based association analysis of 21 candidate genes. Int J Immunogenet 34: 35–44.

18. NaslednikovaIO, UrazovaOI, VoronkovaOV, StrelisAK, NovitskyVV, et al. (2009) Allelic polymorphism of cytokine genes during pulmonary tuberculosis. Bull Exp Biol Med 148: 175–180.

19. SunH, WangY, MaX, PeiF, ZhangY, et al. (2007) A method of oligochip for single nucleotide polymorphism genotyping in the promoter region of the interleukin-1 beta gene and its clinical application. Oligonucleotides 17: 336–344.

20. GomezLM, CamargoJF, CastiblancoJ, Ruiz-NarvaezEA, CadenaJ, et al. (2006) Analysis of IL1B, TAP1, TAP2 and IKBL polymorphisms on susceptibility to tuberculosis. Tissue Antigens 67: 290–296.

21. MishraBB, RathinamVA, MartensGW, MartinotAJ, KornfeldH, et al. (2012) Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1beta. Nat Immunol 14: 52–60.

22. DorhoiA, DeselC, YeremeevV, PradlL, BrinkmannV, et al. (2010) The adaptor molecule CARD9 is essential for tuberculosis control. J Exp Med 207: 777–792.

23. DorhoiA, IannacconeM, FarinacciM, FaeKC, SchreiberJ, et al. (2013) MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment. J Clin Invest.

24. GabayC, LamacchiaC, PalmerG (2010) IL-1 pathways in inflammation and human diseases. Nat Rev Rheumatol 6: 232–241.

25. JuffermansNP, FlorquinS, CamoglioL, VerbonA, KolkAH, et al. (2000) Interleukin-1 signaling is essential for host defense during murine pulmonary tuberculosis. J Infect Dis 182: 902–908.

26. YamadaH, MizumoS, HoraiR, IwakuraY, SugawaraI (2000) Protective role of interleukin-1 in mycobacterial infection in IL-1 alpha/beta double-knockout mice. Lab Invest 80: 759–767.

27. O'KaneCM, ElkingtonPT, JonesMD, CaviedesL, TovarM, et al. (2010) STAT3, p38 MAPK, and NF-kappaB drive unopposed monocyte-dependent fibroblast MMP-1 secretion in tuberculosis. Am J Respir Cell Mol Biol 43: 465–474.

28. HarrisJE, Fernandez-VilasecaM, ElkingtonPT, HorncastleDE, GraeberMB, et al. (2007) IFNgamma synergizes with IL-1beta to up-regulate MMP-9 secretion in a cellular model of central nervous system tuberculosis. Faseb J 21: 356–365.

29. LyadovaIV, TsiganovEN, KapinaMA, ShepelkovaGS, SosunovVV, et al. (2010) In mice, tuberculosis progression is associated with intensive inflammatory response and the accumulation of Gr-1 cells in the lungs. PLoS One 5: e10469.

30. ChensueSW, DaveyMP, RemickDG, KunkelSL (1986) Release of interleukin-1 by peripheral blood mononuclear cells in patients with tuberculosis and active inflammation. Infect Immun 52: 341–343.

31. TsaoTC, LiL, HsiehM, LiaoS, ChangKS (1999) Soluble TNF-alpha receptor and IL-1 receptor antagonist elevation in BAL in active pulmonary TB. Eur Respir J 14: 490–495.

32. HarrisonP, PointonJJ, ChapmanK, RoddamA, WordsworthBP (2008) Interleukin-1 promoter region polymorphism role in rheumatoid arthritis: a meta-analysis of IL-1B-511A/G variant reveals association with rheumatoid arthritis. Rheumatology (Oxford) 47: 1768–1770.

33. MigitaK, MaedaY, AbiruS, NakamuraM, KomoriA, et al. (2007) Polymorphisms of interleukin-1beta in Japanese patients with hepatitis B virus infection. J Hepatol 46: 381–386.

34. Martinez-CarrilloDN, Garza-GonzalezE, Betancourt-LinaresR, Monico-ManzanoT, Antunez-RiveraC, et al. (2010) Association of IL1B -511C/-31T haplotype and Helicobacter pylori vacA genotypes with gastric ulcer and chronic gastritis. BMC Gastroenterol 10: 126.

35. SunH, WangY, MaX, PeiF, SunH, et al. (2007) A method of oligochip for single nucleotide polymorphism genotyping in the promoter region of the interleukin-1 beta gene and its clinical application. Oligonucleotides 17: 336–344.

36. QiuZ, ZhangM, ZhuY, ZhengF, LuP, et al. (2012) Multifunctional CD4 T cell responses in patients with active tuberculosis. Sci Rep 2: 216.

37. OrsF, DenizO, BozlarU, GumusS, TasarM, et al. (2007) High-resolution CT findings in patients with pulmonary tuberculosis: correlation with the degree of smear positivity. J Thorac Imaging 22: 154–159.

38. WenAQ, WangJ, FengK, ZhuPF, WangZG, et al. (2006) Effects of haplotypes in the interleukin 1beta promoter on lipopolysaccharide-induced interleukin 1beta expression. Shock 26: 25–30.

39. ZielinskiCE, MeleF, AschenbrennerD, JarrossayD, RonchiF, et al. (2012) Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 484: 514–518.

40. LasiglieD, TraggiaiE, FedericiS, AlessioM, BuoncompagniA, et al. (2012) Role of IL-1 beta in the development of human T(H)17 cells: lesson from NLPR3 mutated patients. PLoS One 6: e20014.

41. ChenX, YangQ, ZhangM, GranerM, ZhuX, et al. (2009) Diagnosis of active tuberculosis in China using an in-house gamma interferon enzyme-linked immunospot assay. Clin Vaccine Immunol 16: 879–884.

42. ZhangM, WangH, LiaoM, ChenX, GranerM, et al. (2010) Diagnosis of latent tuberculosis infection in bacille Calmette-Guerin vaccinated subjects in China by interferon-gamma ELISpot assay. Int J Tuberc Lung Dis 14: 1556–1563.

43. LindH, HaugenA, ZienolddinyS (2007) Differential binding of proteins to the IL1B -31 T/C polymorphism in lung epithelial cells. Cytokine 38: 43–48.

44. KominatoY, GalsonD, WatermanWR, WebbAC, AuronPE (1995) Monocyte expression of the human prointerleukin 1 beta gene (IL1B) is dependent on promoter sequences which bind the hematopoietic transcription factor Spi-1/PU.1. Mol Cell Biol 15: 58–68.

45. FremondCM, TogbeD, DozE, RoseS, VasseurV, et al. (2007) IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J Immunol 179: 1178–1189.

46. VerwayM, BouttierM, WangTT, CarrierM, CalderonM, et al. (2013) Vitamin D Induces Interleukin-1beta Expression: Paracrine Macrophage Epithelial Signaling Controls M. tuberculosis Infection. PLoS Pathog 9: e1003407.

47. BhowmickR, Tin MaungNH, HurleyBP, GhanemEB, GronertK, et al. (2013) Systemic Disease during Streptococcus pneumoniae Acute Lung Infection Requires 12-Lipoxygenase-Dependent Inflammation. J Immunol.

48. LitvakV, RatushnyAV, LampanoAE, SchmitzF, HuangAC, et al. (2012) A FOXO3-IRF7 gene regulatory circuit limits inflammatory sequelae of antiviral responses. Nature 490: 421–425.

49. CillonizC, ShinyaK, PengX, KorthMJ, ProllSC, et al. (2009) Lethal influenza virus infection in macaques is associated with early dysregulation of inflammatory related genes. PLoS Pathog 5: e1000604.

50. TrajkovD, TrajchevskaM, ArsovT, PetlichkovskiA, StrezovaA, et al. (2009) Association of 22 cytokine gene polymorphisms with tuberculosis in Macedonians. Indian J Tuberc 56: 117–131.

51. Motsinger-ReifAA, AntasPR, OkiNO, LevyS, HollandSM, et al. (2010) Polymorphisms in IL-1beta, vitamin D receptor Fok1, and Toll-like receptor 2 are associated with extrapulmonary tuberculosis. BMC Med Genet 11: 37.

52. WilkinsonRJ, PatelP, LlewelynM, HirschCS, PasvolG, et al. (1999) Influence of polymorphism in the genes for the interleukin (IL)-1 receptor antagonist and IL-1beta on tuberculosis. J Exp Med 189: 1863–1874.

53. LiuY, LiS, ZhangG, NieG, MengZ, et al. (2013) Genetic variants in IL1A and IL1B contribute to the susceptibility to 2009 pandemic H1N1 influenza A virus. BMC Immunol 14: 37.

54. MikamiT, MeguroA, TeshigawaraT, TakeuchiM, UemotoR, et al. (2013) Interleukin 1 beta promoter polymorphism is associated with keratoconus in a Japanese population. Mol Vis 19: 845–851.

55. KimSH, MokJW, KimHS, JooCK (2008) Association of -31T>C and -511 C>T polymorphisms in the interleukin 1 beta (IL1B) promoter in Korean keratoconus patients. Mol Vis 14: 2109–2116.

56. RechcinskiT, GrebowskaA, KurpesaM, SztybrychM, PerugaJZ, et al. (2009) Interleukin-1b and interleukin-1 receptor inhibitor gene cluster polymorphisms in patients with coronary artery disease after percutaneous angioplasty or coronary artery bypass grafting. Kardiol Pol 67: 601–610.

57. LaiosaCV, StadtfeldM, XieH, de Andres-AguayoL, GrafT (2006) Reprogramming of committed T cell progenitors to macrophages and dendritic cells by C/EBP alpha and PU.1 transcription factors. Immunity 25: 731–744.

58. MaoK, ChenS, ChenM, MaY, WangY, et al. (2013) Nitric oxide suppresses NLRP3 inflammasome activation and protects against LPS-induced septic shock. Cell Res 23: 201–212.

59. GallegosAM, van HeijstJW, SamsteinM, SuX, PamerEG, et al. (2011) A gamma interferon independent mechanism of CD4 T cell mediated control of M. tuberculosis infection in vivo. PLoS Pathog 7: e1002052.

60. CaccamoN, GugginoG, JoostenSA, GelsominoG, Di CarloP, et al. (2010) Multifunctional CD4(+) T cells correlate with active Mycobacterium tuberculosis infection. Eur J Immunol 40: 2211–2220.

61. 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.

62. NandiB, BeharSM (2011) Regulation of neutrophils by interferon-gamma limits lung inflammation during tuberculosis infection. J Exp Med 208: 2251–2262.

63. KellerC, HoffmannR, LangR, BrandauS, HermannC, et al. (2006) Genetically determined susceptibility to tuberculosis in mice causally involves accelerated and enhanced recruitment of granulocytes. Infect Immun 74: 4295–4309.

64. EumSY, KongJH, HongMS, LeeYJ, KimJH, et al. (2010) Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 137: 122–128.

65. HnizdoE, SinghT, ChurchyardG (2000) Chronic pulmonary function impairment caused by initial and recurrent pulmonary tuberculosis following treatment. Thorax 55: 32–38.

66. PengR, YueJ, HanM, ZhaoY, LiuL, et al. (2013) The IL-17F sequence variant is associated with susceptibility to tuberculosis. Gene 515: 229–232.

67. 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.

68. ChenX, ZhouB, LiM, DengQ, WuX, et al. (2007) CD4(+)CD25(+)FoxP3(+) regulatory T cells suppress Mycobacterium tuberculosis immunity in patients with active disease. Clin Immunol 123: 50–59.

69. NovikovA, CardoneM, ThompsonR, ShenderovK, KirschmanKD, et al. (2011) Mycobacterium tuberculosis triggers host type I IFN signaling to regulate IL-1beta production in human macrophages. J Immunol 187: 2540–2547.

70. TodaY, TsukadaJ, MisagoM, KominatoY, AuronPE, et al. (2002) Autocrine induction of the human pro-IL-1beta gene promoter by IL-1beta in monocytes. J Immunol 168: 1984–1991.

71. YuLL, ChangK, LuLS, ZhaoD, HanJ, et al. (2013) Lentivirus-mediated RNA interference targeting the H19 gene inhibits cell proliferation and apoptosis in human choriocarcinoma cell line JAR. BMC Cell Biol 14: 26.