HIV Infection Disrupts the Sympatric Host–Pathogen Relationship in Human Tuberculosis

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The phylogeographic population structure of Mycobacterium tuberculosis suggests local adaptation to sympatric human populations. We hypothesized that HIV infection, which induces immunodeficiency, will alter the sympatric relationship between M. tuberculosis and its human host. To test this hypothesis, we performed a nine-year nation-wide molecular-epidemiological study of HIV–infected and HIV–negative patients with tuberculosis (TB) between 2000 and 2008 in Switzerland. We analyzed 518 TB patients of whom 112 (21.6%) were HIV–infected and 233 (45.0%) were born in Europe. We found that among European-born TB patients, recent transmission was more likely to occur in sympatric compared to allopatric host–pathogen combinations (adjusted odds ratio [OR] 7.5, 95% confidence interval [95% CI] 1.21–infinity, p = 0.03). HIV infection was significantly associated with TB caused by an allopatric (as opposed to sympatric) M. tuberculosis lineage (OR 7.0, 95% CI 2.5–19.1, p<0.0001). This association remained when adjusting for frequent travelling, contact with foreigners, age, sex, and country of birth (adjusted OR 5.6, 95% CI 1.5–20.8, p = 0.01). Moreover, it became stronger with greater immunosuppression as defined by CD4 T-cell depletion and was not the result of increased social mixing in HIV–infected patients. Our observation was replicated in a second independent panel of 440 M. tuberculosis strains collected during a population-based study in the Canton of Bern between 1991 and 2011. In summary, these findings support a model for TB in which the stable relationship between the human host and its locally adapted M. tuberculosis is disrupted by HIV infection.

Vyšlo v časopise: HIV Infection Disrupts the Sympatric Host–Pathogen Relationship in Human Tuberculosis. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003318
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003318

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Zdroje

1. WoolhouseME, WebsterJP, DomingoE, CharlesworthB, LevinBR (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet 32: 569–577.

2. GandonS, Van ZandtPA (1998) Local adaptation and host-parasite interactions. Trends Ecol Evol 13: 214–216.

3. KaweckiTJ, EbertD (2004) Conceptual issues in local adaptation. Ecology Letters 7: 1225–1241.

4. SchulteRD, MakusC, HasertB, MichielsNK, SchulenburgH (2011) Host-parasite local adaptation after experimental coevolution of Caenorhabditis elegans and its microparasite Bacillus thuringiensis. Proc Biol Sci 278: 2832–2839.

5. AgnewP, KoellaC, MichalakisY (2000) Host life history responses to parasitism. Microbes Infect 2: 891–896.

6. GandonS, AgnewP, MichalakisY (2002) Coevolution between parasite virulence and host life-history traits. Am Nat 160: 374–388.

7. LivelyCM, DybdahlMF (2000) Parasite adaptation to locally common host genotypes. Nature 405: 679–681.

8. BroschR, GordonSV, MarmiesseM, BrodinP, BuchrieserC, et al. (2002) A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A 99: 3684–3689.

9. GagneuxS, DeRiemerK, VanT, Kato-MaedaM, de JongBC, et al. (2006) Variable host–pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 103: 2869–2873.

10. GutierrezMC, BrisseS, BroschR, FabreM, OmaisB, et al. (2005) Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Pathog 1: e5 doi:10.1371/journal.ppat.0010005.

11. HirshAE, TsolakiAG, DeRiemerK, FeldmanMW, SmallPM (2004) Stable association between strains of Mycobacterium tuberculosis and their human host populations. Proc Natl Acad Sci U S A 101: 4871–4876.

12. HershbergR, LipatovM, SmallPM, ShefferH, NiemannS, et al. (2008) High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 6: e311 doi:10.1371/journal.pbio.0060311.

13. WirthT, HildebrandF, Allix-BeguecC, WolbelingF, KubicaT, et al. (2008) Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog 4: e1000160 doi:10.1371/journal.ppat.1000160.

14. Pearce-DuvetJM (2006) The origin of human pathogens: evaluating the role of agriculture and domestic animals in the evolution of human disease. Biol Rev Camb Philos Soc 81: 369–382.

15. VinaMA, HollenbachJA, LykeKE, SzteinMB, MaiersM, et al. (2012) Tracking human migrations by the analysis of the distribution of HLA alleles, lineages and haplotypes in closed and open populations. Philos Trans R Soc Lond B Biol Sci 367: 820–829.

16. BrudeyK, DriscollJR, RigoutsL, ProdingerWM, GoriA, et al. (2006) Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol 6: 23.

17. FilliolI, MotiwalaAS, CavatoreM, QiW, HazbonMH, et al. (2006) Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol 188: 759–772.

18. BakerL, BrownT, MaidenMC, DrobniewskiF (2004) Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis. Emerg Infect Dis 10: 1568–1577.

19. ReedMB, PichlerVK, McIntoshF, MattiaA, FallowA, et al. (2009) Major Mycobacterium tuberculosis lineages associate with patient country of origin. J Clin Microbiol 47: 1119–1128.

20. GutackerMM, MathemaB, SoiniH, ShashkinaE, KreiswirthBN, et al. (2006) Single-nucleotide polymorphism-based population genetic analysis of Mycobacterium tuberculosis strains from 4 geographic sites. J Infect Dis 193: 121–128.

21. GagneuxS (2012) Host–pathogen coevolution in human tuberculosis. Philos Trans R Soc Lond B Biol Sci 367: 850–859.

22. BritesD, GagneuxS (2012) Old and new selective pressures on Mycobacterium tuberculosis. Infect Genet Evol 12: 678–85.

23. Wicker HR, Fibbi R, Haug W (2004) “Ergebnisse des Nationalen Forschungsprogramms ‘Migration und interkulturelle Beziehungen’”. Seismo publishing, Zürich, Switzerland.

24. de JongBC, AntonioM, GagneuxS (2010) Mycobacterium africanum–review of an important cause of human tuberculosis in West Africa. PLoS Negl Trop Dis 4: e744 doi:10.1371/journal.pntd.0000744.

25. GagneuxS, SmallPM (2007) Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis 7: 328–337.

26. Federal Office of Public Health (2011) Tuberkulose in der Schweiz 2005–2009. [Erratum appears in Bull Bundesamt für Gesundheit (Switzerland) 2011;(no 13):277]. Bull BAG (no 10) 205–213.

27. BorgdorffMW, NagelkerkeN, Van SoolingenD, de HaasPE, VeenJ, et al. (1998) Analysis of tuberculosis transmission between nationalities in the Netherlands in the period 1993–1995 using DNA fingerprinting. Am J Epidemiol 147: 187–195.

28. LillebaekT, AndersenÅB, BauerJ, DirksenA, GlismannS, et al. (2001) Risk of Mycobacterium tuberculosis transmission in a low-incidence country due to immigration from high-incidence areas. J Clin Microbiol 39: 855–861.

29. FennerL, GagneuxS, HelblingP, BattegayM, RiederHL, et al. (2012) Mycobacterium tuberculosis transmission in a country with low tuberculosis incidence: role of immigration and HIV infection. J Clin Microbiol 50: 388–395.

30. SpiegelhalterDJ, MylesJP, JonesDR, AbramsKR (1999) Methods in health service research. An introduction to bayesian methods in health technology assessment. BMJ 319: 508–512.

31. LawnSD, ZumlaAI (2011) Tuberculosis. Lancet 378: 57–72.

32. RodrigoT, CaylàJA, Garcia de OlallaP, Galdós-TangüisH, JansàJM, et al. (1997) Characteristics of tuberculosis patients who generate secondary cases. Int J Tuberc Lung Dis 1: 352–357.

33. ComstockGW, LivesayVT, WoolpertSF (1974) The prognosis of a positive tuberculin reaction in childhood and adolescence. Am J Epidemiol 99: 131–138.

34. VynnyckyE, FinePEM (2000) Life time risks, incubation period, and serial interval of tuberculosis. Am J Epidemiol 152: 247–263.

35. HorsburghCRJr (2004) Priorities for the treatment of latent tuberculosis infection in the United States. N Engl J Med 350: 2060–2067.

36. FennerL, EggerM, GagneuxS (2009) Annie Darwin's death, the evolution of tuberculosis and the need for systems epidemiology. Int J Epidemiol 38: 1425–1428.

37. RiederHL (1999) Epidemiologic basis of tuberculosis control. International Union Against Tuberculosis and Lung Disease, Paris 1999.

38. FennerL, WeberR, SteffenR, SchlagenhaufP (2007) Imported infectious disease and purpose of travel, Switzerland. Emerg Infect Dis 13: 217–222.

39. NegredoE, MassanellaM, PuigJ, Perez-AlvarezN, Gallego-EscuredoJM, et al. (2010) Nadir CD4 T cell count as predictor and high CD4 T cell intrinsic apoptosis as final mechanism of poor CD4 T cell recovery in virologically suppressed HIV–infected patients: clinical implications. Clin Infect Dis 50: 1300–1308.

40. KelleyCF, KitchenCM, HuntPW, RodriguezB, HechtFM, et al. (2009) Incomplete peripheral CD4+ cell count restoration in HIV–infected patients receiving long-term antiretroviral treatment. Clin Infect Dis 48: 787–794.

41. LangeCG, LedermanMM, MedvikK, AsaadR, WildM, et al. (2003) Nadir CD4+ T-cell count and numbers of CD28+ CD4+ T-cells predict functional responses to immunizations in chronic HIV–1 infection. AIDS 17: 2015–2023.

42. DiedrichCR, FlynnJL (2011) HIV–1/Mycobacterium tuberculosis coinfection immunology: how does HIV–1 exacerbate tuberculosis? Infect Immun 79: 1407–1417.

43. FalvoJV, RanjbarS, JasenoskyLD, GoldfeldAE (2011) Arc of a vicious circle: pathways activated by Mycobacterium tuberculosis that target the HIV–1 LTR. Am J Respir Cell Mol Biol 45: 1116–24.

44. HoshinoY, NakataK, HoshinoS, HondaY, TseDB, et al. (2002) Maximal HIV–1 replication in alveolar macrophages during tuberculosis requires both lymphocyte contact and cytokines. J Exp Med 195: 495–505.

45. PatelNR, ZhuJ, TachadoSD, ZhangJ, WanZ, et al. (2007) HIV impairs TNF-alpha mediated macrophage apoptotic response to Mycobacterium tuberculosis. J Immunol 179: 6973–6980.

46. GeldmacherC, SchuetzA, NgwenyamaN, CasazzaJP, SangaE, et al. (2008) Early depletion of Mycobacterium tuberculosis-specific T helper 1 cell responses after HIV–1 infection. J Infect Dis 198: 1590–1598.

47. PortevinD, GagneuxS, ComasI, YoungD (2011) Human macrophage responses to clinical isolates from the Mycobacterium tuberculosis complex discriminate between ancient and modern lineages. PLoS Pathog 7: e1001307 doi:10.1371/journal.ppat.1001307.

48. MusserJM, KrollJS, GranoffDM, MoxonER, BrodeurBR, et al. (1990) Global genetic structure and molecular epidemiology of encapsulated Haemophilus influenzae. Rev Infect Dis 12: 75–111.

49. CaufieldPW (2009) Tracking human migration patterns through the oral bacterial flora. Clin Microbiol Infect 15 Suppl 1: 37–39.

50. MonotM, HonoreN, GarnierT, ZidaneN, SherafiD, et al. (2009) Comparative genomic and phylogeographic analysis of Mycobacterium leprae. Nat Genet 41: 1282–1289.

51. FalushD, WirthT, LinzB, PritchardJK, StephensM, et al. (2003) Traces of human migrations in Helicobacter pylori populations. Science 299: 1582–1585.

52. LinzB, BallouxF, MoodleyY, ManicaA, LiuH, et al. (2007) An African origin for the intimate association between humans and Helicobacter pylori. Nature 445: 915–918.

53. Aspholm-HurtigM, DailideG, LahmannM, KaliaA, IlverD, et al. (2004) Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305: 519–522.

54. ZdziarskiJ, BrzuszkiewiczE, WulltB, LiesegangH, BiranD, et al. (2010) Host imprints on bacterial genomes – rapid, divergent evolution in individual patients. PLoS Pathog 6: e1001078 doi:10.1371/journal.ppat.1001078.

55. 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 doi:10.1371/journal.ppat.1000034.

56. van CrevelR, ParwatiI, SahiratmadjaE, MarzukiS, OttenhoffTHM, et al. (2009) Infection with Mycobacterium tuberculosis Beijing genotype strains is associated with polymorphisms in SLC11A1/NRAMP1 in Indonesian patients with tuberculosis. J Infect Dis 200: 1671–1674.

57. HerbF, ThyeT, NiemannS, BrowneEN, ChinbuahMA, et al. (2008) ALOX5 variants associated with susceptibility to human pulmonary tuberculosis. Hum Mol Genet 17: 1052–1060.

58. IntemannCD, ThyeT, NiemannS, BrowneEN, AmanuaCM, et al. (2009) Autophagy gene variant IRGM −261T contributes to protection from tuberculosis caused by Mycobacterium tuberculosis but not by M. africanum strains. PLoS Pathog 5: e1000577 doi:10.1371/journal.ppat.1000577.

59. ThyeT, NiemannS, WalterK, HomolkaS, IntemannCD, et al. (2011) Variant G57E of mannose binding lectin associated with protection against tuberculosis caused by Mycobacterium africanum but not by M. tuberculosis. PLoS ONE 6: e20908 doi:10.1371/journal.pone.0020908.

60. KwanCK, ErnstJD (2011) HIV and tuberculosis: a deadly human syndemic. Clin Microbiol Rev 24: 351–376.

61. FennerL, GagneuxS, JanssensJP, FehrJ, CavassiniM, et al. (2012) Tuberculosis in HIV–negative and HIV–infected patients in a low-incidence country: clinical characteristics and treatment outcomes. PLoS ONE 7: e34186 doi:10.1371/journal.pone.0034186.

62. FennerL, EggerM, BodmerT, AltpeterE, ZwahlenM, et al. (2012) Effect of mutation and genetic background on drug resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 56: 3047–3053.

63. Schoeni-AffolterF, LedergerberB, RickenbachM, RudinC, GunthardHF, et al. (2010) Cohort profile: the Swiss HIV Cohort study. Int J Epidemiol 39: 1179–1189.

64. Allix-BeguecC, Fauville-DufauxM, SupplyP (2008) Three-year population-based evaluation of standardized mycobacterial interspersed repetitive-unit-variable-number tandem-repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 46: 1398–1406.

65. SupplyP, AllixC, LesjeanS, Cardoso-OelemannM, Rusch-GerdesS, et al. (2006) Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 44: 4498–4510.

66. OelemannMC, DielR, VatinV, HaasW, Rusch-GerdesS, et al. (2007) Assessment of an optimized mycobacterial interspersed repetitive- unit-variable-number tandem-repeat typing system combined with spoligotyping for population-based molecular epidemiology studies of tuberculosis. J Clin Microbiol 45: 691–697.

67. StuckiD, MallaB, HostettlerS, HunaT, FeldmannJ, et al. (2012) Two new rapid SNP-typing methods for classifying Mycobacterium tuberculosis complex into the main phylogenetic lineages. PLoS ONE 7: e41253 doi:10.1371/journal.pone.0041253.

68. FennerL, MallaB, NinetB, DubuisO, StuckiD, et al. (2011) “Pseudo-Beijing”: Evidence for convergent evolution in the direct repeat region of Mycobacterium tuberculosis. PLoS ONE 6: e24737 doi:10.1371/journal.pone.0024737.

69. SreevatsanS, PanX, StockbauerKE, ConnellND, KreiswirthBN, et al. (1997) Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci U S A 94: 9869–9874.

70. PearlJ (2010) An Introduction to Causal Inference. Int J Biostat 6: Article 7.

71. GelmanA, JakulinA, PittauMG, SuYS (2008) A weakly informative default prior distribution for logistic and other regression models. Ann Appl Stat 2: 1360–1383.

72. BentleySD, ComasI, BryantJM, WalkerD, SmithNH, et al. (2012) The genome of Mycobacterium africanum West African 2 reveals a lineage-specific locus and genome erosion common to the M. tuberculosis complex. PLoS Negl Trop Dis 6: e1552 doi:10.1371/journal.pntd.0001552.