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Abstract

Globally, about 36.7 million people were living with HIV infection at the end of 2015. The most frequent infection co-occurring with HIV-1 is —374,000 deaths per annum are attributable to HIV-tuberculosis, 75% of those occurring in Africa. HIV-1 infection increases the risk of tuberculosis by a factor of up to 26 and alters its clinical presentation, complicates diagnosis and treatment, and worsens outcome. Although HIV-1-induced depletion of CD4+ T cells underlies all these effects, more widespread immune deficits also contribute to susceptibility and pathogenesis. These defects present a challenge to understand and ameliorate, but also an opportunity to learn and optimize mechanisms that normally protect people against tuberculosis. The most effective means to prevent and ameliorate tuberculosis in HIV-1-infected people is antiretroviral therapy, but this may be complicated by pathological immune deterioration that in turn requires more effective host-directed anti-inflammatory therapies to be derived.

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2018-04-26
2024-04-14
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Literature Cited

  1. 1. World Health Organ. 2017. Global Tuberculosis Report Geneva: World Health Organ, 22nd ed..
  2. Gupta RK, Lucas SB, Fielding KL, Lawn SD. 2.  2015. Prevalence of tuberculosis in post-mortem studies of HIV-infected adults and children in resource-limited settings: a systematic review and meta-analysis. AIDS 29:1987–2002 [Google Scholar]
  3. Lawn SD, Harries AD, Williams BG, Chaisson RE, Losina E. 3.  et al. 2011. Antiretroviral therapy and the control of HIV-associated tuberculosis: Will ART do it?. Int. J. Tuberc. Lung Dis. 15:571–81 [Google Scholar]
  4. Akolo C, Adetifa I, Shepperd S, Volmink J. 4.  2010. Treatment of latent tuberculosis infection in HIV infected persons. Cochrane Database Syst. Rev. 20:CD000171 [Google Scholar]
  5. Rangaka MX, Wilkinson RJ, Boulle A, Glynn JR, Fielding K. 5.  et al. 2014. Isoniazid plus antiretroviral therapy to prevent tuberculosis: a randomised double-blind, placebo-controlled trial. Lancet 384:682–90 [Google Scholar]
  6. Gupta A, Wood R, Kaplan R, Bekker LG, Lawn SD. 6.  2012. Tuberculosis incidence rates during 8 years of follow-up of an antiretroviral treatment cohort in South Africa: comparison with rates in the community. PLOS ONE 7:e34156 [Google Scholar]
  7. Lawn SD, Myer L, Edwards D, Bekker LG, Wood R. 7.  2009. Short-term and long-term risk of tuberculosis associated with CD4 cell recovery during antiretroviral therapy in South Africa. AIDS 23:1717–25 [Google Scholar]
  8. Fox GJ, Menzies D. 8.  2013. Epidemiology of tuberculosis immunology. Adv. Exp. Med. Biol 783:1–32 [Google Scholar]
  9. Mwandumba HC, Russell DG, Nyirenda MH, Anderson J, White SA. 9.  et al. 2004. Mycobacterium tuberculosis resides in nonacidified vacuoles in endocytically competent alveolar macrophages from patients with tuberculosis and HIV infection. J. Immunol. 172:4592–98 [Google Scholar]
  10. Esmail H, Barry CE, Young DB, Wilkinson RJ. 10.  2014. The ongoing challenge of latent tuberculosis. Philos. Trans. R. Soc. Lond. B 369:20130437 [Google Scholar]
  11. Selwyn PA, Hartel D, Lewis VA, Schoenbaum EE, Vermund SH. 11.  et al. 1989. A prospective study of the risk of tuberculosis among intravenous drug users with human immunodeficiency virus infection. N. Engl. J. Med. 320:545–50 [Google Scholar]
  12. Badri M, Wilson D, Wood R. 12.  2002. Effect of highly active antiretroviral therapy on incidence of tuberculosis in South Africa: a cohort study. Lancet 359:2059–64First clinical demonstration of efficacy of ART to reduce risk of TB in HIV-1 infection in Africa. [Google Scholar]
  13. Sonnenberg P, Glynn JR, Fielding K, Murray J, Godfrey-Faussett P, Shearer S. 13.  2005. How soon after infection with HIV does the risk of tuberculosis start to increase? A retrospective cohort study in South African gold miners. J. Infect. Dis. 191:150–58An important study clearly demonstrating increased risk of TB in HIV-1 infection soon after viral infection. [Google Scholar]
  14. Chamie G, Luetkemeyer A, Charlebois E, Havlir DV. 14.  2010. Tuberculosis as part of the natural history of HIV infection in developing countries. Clin. Infect. Dis. 50:Suppl. 3S245–54 [Google Scholar]
  15. Lucas SB, De Cock KM, Hounnou A, Peacock C, Diomande M. 15.  et al. 1994. Contribution of tuberculosis to slim disease in Africa. BMJ 308:1531–33A classic autopsy study that highlighted HIV-TB and described its microscopic pathology. [Google Scholar]
  16. Feng F, Shi YX, Xia GL, Zhu Y, Lu HZ, Zhang ZY. 16.  2013. Computed tomography in predicting smear-negative pulmonary tuberculosis in AIDS patients. Chin. Med. J. (Engl.) 126:3228–33 [Google Scholar]
  17. Janssen S, Schutz C, Ward A, Nemes E, Wilkinson KA. 17.  et al. 2017. Mortality in severe human immunodeficiency virus-tuberculosis associates with innate immune activation and dysfunction of monocytes. Clin. Infect. Dis. 65:73–82 [Google Scholar]
  18. Cruciani M, Malena M, Bosco O, Gatti G, Serpelloni G. 18.  2001. The impact of human immunodeficiency virus type 1 on infectiousness of tuberculosis: a meta-analysis. Clin. Infect. Dis. 33:1922–30 [Google Scholar]
  19. Reid MJ, Shah NS. 19.  2009. Approaches to tuberculosis screening and diagnosis in people with HIV in resource-limited settings. Lancet Infect. Dis. 9:173–84 [Google Scholar]
  20. Monkongdee P, McCarthy KD, Cain KP, Tasaneeyapan T, Nguyen HD. 20.  et al. 2009. Yield of acid-fast smear and mycobacterial culture for tuberculosis diagnosis in people with human immunodeficiency virus. Am. J. Respir. Crit. Care Med. 180:903–8 [Google Scholar]
  21. Boehme CC, Nabeta P, Hillemann D, Nicol MP, Shenai S. 21.  et al. 2010. Rapid molecular detection of tuberculosis and rifampin resistance. N. Engl. J. Med. 363:1005–15 [Google Scholar]
  22. Lawn SD, Mwaba P, Bates M, Piatek A, Alexander H. 22.  et al. 2013. Advances in tuberculosis diagnostics: the Xpert MTB/RIF assay and future prospects for a point-of-care test. Lancet Infect. Dis. 13:349–61 [Google Scholar]
  23. Boehme CC, Nicol MP, Nabeta P, Michael JS, Gotuzzo E. 23.  et al. 2011. Feasibility, diagnostic accuracy, and effectiveness of decentralised use of the Xpert MTB/RIF test for diagnosis of tuberculosis and multidrug resistance: a multicentre implementation study. Lancet 377:1495–505 [Google Scholar]
  24. Kerkhoff A, Barr DA, Schutz C, Burton R, Nicol M. 24.  et al. 2017. Disseminated tuberculosis among hospitalised HIV patients in South Africa: a common condition that can be rapidly diagnosed using urine-based assays. Sci. Rep. 7:110931 [Google Scholar]
  25. Rangaka MX, Wilkinson KA, Seldon R, Van Cutsem G Meintjes GA. 25.  et al. 2007. Effect of HIV-1 infection on T-cell-based and skin test detection of tuberculosis infection. Am. J. Respir. Crit. Care Med. 175:514–20 [Google Scholar]
  26. Luetkemeyer AF, Charlebois ED, Flores LL, Bangsberg DR, Deeks SG. 26.  et al. 2007. Comparison of an interferon-gamma release assay with tuberculin skin testing in HIV-infected individuals. Am. J. Respir. Crit. Care Med. 175:737–42 [Google Scholar]
  27. Esmail H, Thienemann F, Oni T, Goliath R, Wilkinson KA, Wilkinson RJ. 27.  2016. QuantiFERON conversion following tuberculin administration is common in HIV infection and relates to baseline response. BMC Infect. Dis. 16:1545 [Google Scholar]
  28. Rangaka MX, Wilkinson KA, Glynn JR, Ling D, Menzies D. 28.  et al. 2012. Predictive value of interferon-gamma release assays for incident active tuberculosis: a systematic review and meta-analysis. Lancet Infect. Dis. 12:45–55 [Google Scholar]
  29. Harari A, Rozot V, Bellutti Enders F, Perreau M, Stalder JM. 29.  et al. 2011. Dominant TNF-α+Mycobacterium tuberculosis-specific CD4+ T cell responses discriminate between latent infection and active disease. Nat. Med. 17:372–76 [Google Scholar]
  30. Pollock KM, Whitworth HS, Montamat-Sicotte DJ, Grass L, Cooke GS. 30.  et al. 2013. T-cell immunophenotyping distinguishes active from latent tuberculosis. J. Infect. Dis. 208:952–68 [Google Scholar]
  31. Caccamo N, Guggino G, Joosten SA, Gelsomino G, Di Carlo P. 31.  et al. 2010. Multifunctional CD4+ T cells correlate with active Mycobacterium tuberculosis infection. Eur. J. Immunol. 40:2211–20 [Google Scholar]
  32. Wilkinson KA, Oni T, Gideon HP, Goliath R, Wilkinson RJ, Riou C. 32.  2016. Activation profile of Mycobacterium tuberculosis-specific CD4+ T cells reflects disease activity irrespective of HIV status. Am. J. Respir. Crit. Care Med. 193:1307–10 [Google Scholar]
  33. Schuetz A, Haule A, Reither K, Ngwenyama N, Rachow A. 33.  et al. 2011. Monitoring CD27 expression to evaluate Mycobacterium tuberculosis activity in HIV-1 infected individuals in vivo. PLOS ONE 6:e27284 [Google Scholar]
  34. Portevin D, Moukambi F, Clowes P, Bauer A, Chachage M. 34.  et al. 2014. Assessment of the novel T-cell activation marker–tuberculosis assay for diagnosis of active tuberculosis in children: a prospective proof-of-concept study. Lancet Infect. Dis. 14:931–38 [Google Scholar]
  35. Adekambi T, Ibegbu CC, Cagle S, Kalokhe AS, Wang YF. 35.  et al. 2015. Biomarkers on patient T cells diagnose active tuberculosis and monitor treatment response. J. Clin. Investig. 125:3723 [Google Scholar]
  36. Riley RL, Wells WF, Mills CC, Nyka W, McLean RL. 36.  1957. Air hygiene in tuberculosis: quantitative studies of infectivity and control in a pilot ward. Am. Rev. Tuberc. 75:420–31 [Google Scholar]
  37. Dannenberg AM Jr. 37.  1989. Immune mechanisms in the pathogenesis of pulmonary tuberculosis. Rev. Infect. Dis. 11:Suppl. 2S369–78 [Google Scholar]
  38. O'Garra A, Redford PS, McNab FW, Bloom CI, Wilkinson RJ, Berry MP. 38.  2013. The immune response in tuberculosis. Annu. Rev. Immunol. 31:475–527 [Google Scholar]
  39. Smith DW, McMurray DN, Wiegeshaus EH, Grover AA, Harding GE. 39.  1970. Host-parasite relationships in experimental airborne tuberculosis: IV. Early events in the course of infection in vaccinated and nonvaccinated guinea pigs. Am. Rev. Respir. Dis. 102:937–49 [Google Scholar]
  40. Nusbaum RJ, Calderon VE, Huante MB, Sutjita P, Vijayakumar S. 40.  et al. 2016. Pulmonary tuberculosis in humanized mice infected with HIV-1. Sci. Rep. 6:21522 [Google Scholar]
  41. Marais BJ, Gie RP, Schaaf HS, Hesseling AC, Obihara CC. 41.  et al. 2004. The natural history of childhood intra-thoracic tuberculosis: a critical review of literature from the pre-chemotherapy era. Int. J. Tuberc. Lung Dis. 8:392–402 [Google Scholar]
  42. Lin PL, Ford CB, Coleman MT, Myers AJ, Gawande R. 42.  et al. 2014. Sterilization of granulomas is common in active and latent tuberculosis despite within-host variability in bacterial killing. Nat. Med. 20:75–79 [Google Scholar]
  43. Smith S, Jacobs RF, Wilson CB. 43.  1997. Immunobiology of childhood tuberculosis: a window on the ontogeny of cellular immunity. J. Pediatr. 131:16–26 [Google Scholar]
  44. Diedrich CR, O'Hern J, Gutierrez MG, Allie N, Papier P. 44.  et al. 2016. Relationship between HIV coinfection, interleukin 10 production, and Mycobacterium tuberculosis in human lymph node granulomas. J. Infect. Dis. 214:1309–18 [Google Scholar]
  45. Diedrich CR, O'Hern J, Wilkinson RJ. 45.  2016. HIV-1 and the Mycobacterium tuberculosis granuloma: a systematic review and meta-analysis. Tuberculosis 98:62–76 [Google Scholar]
  46. Hunter RL. 46.  2016. Tuberculosis as a three-act play: a new paradigm for the pathogenesis of pulmonary tuberculosis. Tuberculosis 97:8–17 [Google Scholar]
  47. Steinbruck P, Dankova D, Edwards LB, Doster B, Livesay VT. 47.  1972. Tuberculosis risk in persons with “fibrotic” X-ray lesions. Bull. Int. Union Tuberc. 47:135–59 [Google Scholar]
  48. Esmail H, Lai RP, Lesosky M, Wilkinson KA, Graham CM. 48.  et al. 2016. Characterization of progressive HIV-associated tuberculosis using 2-deoxy-2-[18F]fluoro-d-glucose positron emission and computed tomography. Nat. Med. 22:1090–93Delineated the nature of subclinical TB in HIV-1-infected persons by high-resolution imaging. [Google Scholar]
  49. Ong CW, Elkington PT, Friedland JS. 49.  2014. Tuberculosis, pulmonary cavitation, and matrix metalloproteinases. Am. J. Respir. Crit. Care Med. 190:9–18 [Google Scholar]
  50. Kaplan G, Post FA, Moreira AL, Wainwright H, Kreiswirth BN. 50.  et al. 2003. Mycobacterium tuberculosis growth at the cavity surface: a microenvironment with failed immunity. Infect. Immun. 71:7099–108 [Google Scholar]
  51. Donald PR, Marais BJ, Barry CE 3rd. 51.  2010. Age and the epidemiology and pathogenesis of tuberculosis. Lancet 375:1852–54 [Google Scholar]
  52. Walker NF, Clark SO, Oni T, Andreu N, Tezera L. 52.  et al. 2012. Doxycycline and HIV infection suppress tuberculosis-induced matrix metalloproteinases. Am. J. Respir. Crit. Care Med. 185:989–97 [Google Scholar]
  53. Lillebaek T, Dirksen A, Baess I, Strunge B, Thomsen VO, Andersen AB. 53.  2002. Molecular evidence of endogenous reactivation of Mycobacterium tuberculosis after 33 years of latent infection. J. Infect. Dis. 185:401–4 [Google Scholar]
  54. Diedrich CR, Flynn JL. 54.  2011. HIV-1/Mycobacterium tuberculosis coinfection immunology: How does HIV-1 exacerbate tuberculosis?. Infect. Immun. 79:1407–17 [Google Scholar]
  55. Martineau AR, Newton SM, Wilkinson KA, Kampmann B, Hall BM. 55.  et al. 2007. Neutrophil-mediated innate immune resistance to mycobacteria. J. Clin. Investig. 117:1988–94 [Google Scholar]
  56. Lowe DM, Redford PS, Wilkinson RJ, O'Garra A, Martineau AR. 56.  2012. Neutrophils in tuberculosis: friend or foe?. Trends Immunol 33:14–25 [Google Scholar]
  57. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA. 57.  et al. 2010. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466:973–77 [Google Scholar]
  58. Lowe DM, Bandara AK, Packe GE, Barker RD, Wilkinson RJ. 58.  et al. 2013. Neutrophilia independently predicts death in tuberculosis. Eur. Respir. J. 42:1752–57 [Google Scholar]
  59. Eum SY, Kong JH, Hong MS, Lee YJ, Kim JH. 59.  et al. 2010. Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 137:122–28 [Google Scholar]
  60. Lowe DM, Bangani N, Goliath R, Kampmann B, Wilkinson KA. 60.  et al. 2015. Effect of antiretroviral therapy on HIV-mediated impairment of the neutrophil antimycobacterial response. Ann. Am. Thorac. Soc. 12:1627–37 [Google Scholar]
  61. Bangani N, Nakiwala J, Martineau AR, Wilkinson RJ, Wilkinson KA, Lowe DM. 61.  2016. Brief Report: HIV-1 infection impairs CD16 and CD35 mediated opsonophagocytosis of Mycobacterium tuberculosis by human neutrophils. J. Acquir. Immune Defic. Syndr. 73:263–67 [Google Scholar]
  62. Walker NF, Wilkinson KA, Meintjes G, Tezera LB, Goliath R. 62.  et al. 2017. Matrix degradation in human immunodeficiency virus type 1-associated tuberculosis and tuberculosis immune reconstitution inflammatory syndrome: a prospective observational study. Clin. Infect. Dis. 65:121–32 [Google Scholar]
  63. Brilha S, Sathyamoorthy T, Stuttaford LH, Walker NF, Wilkinson RJ. 63.  et al. 2017. Early secretory antigenic target-6 drives matrix metalloproteinase-10 gene expression and secretion in tuberculosis. Am. J. Respir. Cell Mol. Biol. 56:223–32 [Google Scholar]
  64. Francis RJ, Butler RE, Stewart GR. 64.  2014. Mycobacterium tuberculosis ESAT-6 is a leukocidin causing Ca2+ influx, necrosis and neutrophil extracellular trap formation. Cell Death Dis 5:e1474 [Google Scholar]
  65. Marais S, Wilkinson KA, Lesosky M, Coussens AK, Deffur A. 65.  et al. 2014. Neutrophil-associated central nervous system inflammation in tuberculous meningitis immune reconstitution inflammatory syndrome. Clin. Infect. Dis. 59:163847Clearly linked neutrophils to CNS tissue damage in TB-IRIS. [Google Scholar]
  66. Jambo KC, Banda DH, Afran L, Kankwatira AM, Malamba RD. 66.  et al. 2014. Asymptomatic HIV-infected individuals on antiretroviral therapy exhibit impaired lung CD4+ T-cell responses to mycobacteria. Am. J. Respir. Crit. Care Med. 190:938–47 [Google Scholar]
  67. Pathak S, Wentzel-Larsen T, Asjo B. 67.  2010. Effects of in vitro HIV-1 infection on mycobacterial growth in peripheral blood monocyte-derived macrophages. Infect. Immun. 78:4022–32 [Google Scholar]
  68. Kalsdorf B, Scriba TJ, Wood K, Day CL, Dheda K. 68.  et al. 2009. HIV-1 infection impairs the bronchoalveolar T-cell response to mycobacteria. Am. J. Respir. Crit. Care Med. 180:1262–70 [Google Scholar]
  69. Singh SK, Andersson AM, Ellegard R, Lindestam Arlehamn CS, Sette A. 69.  et al. 2016. HIV interferes with Mycobacterium tuberculosis antigen presentation in human dendritic cells. Am. J. Pathol. 186:3083–93 [Google Scholar]
  70. da Silva RC, Segat L, Crovella S. 70.  2011. Role of DC-SIGN and L-SIGN receptors in HIV-1 vertical transmission. Hum. Immunol. 72:305–11 [Google Scholar]
  71. Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M. 71.  et al. 2003. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 197:121–27 [Google Scholar]
  72. Raghavan S, Alagarasu K, Selvaraj P. 72.  2012. Immunogenetics of HIV and HIV associated tuberculosis. Tuberculosis 92:18–30 [Google Scholar]
  73. Van Rhijn I, Moody DB. 73.  2015. Donor unrestricted T cells: a shared human T cell response. J. Immunol. 195:1927–32 [Google Scholar]
  74. Huang S, Moody DB. 74.  2016. Donor-unrestricted T cells in the human CD1 system. Immunogenetics 68:577–96 [Google Scholar]
  75. Dellabona P, Padovan E, Casorati G, Brockhaus M, Lanzavecchia A. 75.  1994. An invariant Vα24-JαQ/Vβ11 T cell receptor is expressed in all individuals by clonally expanded CD48 T cells. J. Exp. Med. 180:1171–76 [Google Scholar]
  76. Brennan PJ, Tatituri RV, Brigl M, Kim EY, Tuli A. 76.  et al. 2011. Invariant natural killer T cells recognize lipid self antigen induced by microbial danger signals. Nat. Immunol. 12:1202–11 [Google Scholar]
  77. Kim CH, Butcher EC, Johnston B. 77.  2002. Distinct subsets of human Vα24-invariant NKT cells: cytokine responses and chemokine receptor expression. Trends Immunol 23:516–19 [Google Scholar]
  78. Montoya CJ, Catano JC, Ramirez Z, Rugeles MT, Wilson SB, Landay AL. 78.  2008. Invariant NKT cells from HIV-1 or Mycobacterium tuberculosis-infected patients express an activated phenotype. Clin. Immunol. 127:1–6 [Google Scholar]
  79. Motsinger A, Haas DW, Stanic AK, Van Kaer L, Joyce S, Unutmaz D. 79.  2002. CD1d-restricted human natural killer T cells are highly susceptible to human immunodeficiency virus 1 infection. J. Exp. Med. 195:869–79 [Google Scholar]
  80. van der Vliet HJ, Balk SP, Exley MA. 80.  2006. Natural killer T cell-based cancer immunotherapy. Clin. Cancer Res. 12:5921–23 [Google Scholar]
  81. Wong EB, Ndung'u T, Kasprowicz VO. 81.  2017. The role of mucosal-associated invariant T cells in infectious diseases. Immunology 150:45–54 [Google Scholar]
  82. Wong EB, Akilimali NA, Govender P, Sullivan ZA, Cosgrove C. 82.  et al. 2013. Low levels of peripheral CD161++CD8+ mucosal associated invariant T (MAIT) cells are found in HIV and HIV/TB co-infection. PLOS ONE 8:e83474 [Google Scholar]
  83. Wilkinson RJ, Wilkinson KA, De Smet KAL, Haslov K, Pasvol G. 83.  et al. 1998. Human T and B cell reactivity to the 16 kDa α-crystallin protein of Mycobacterium tuberculosis. . Scand. J. Immunol. 48:403–9 [Google Scholar]
  84. Wilkinson RJ, Hasløv K, Rappuoli R, Giovannoni F, Narayanan PR. 84.  et al. 1997. Evaluation of the recombinant 38-kilodalton antigen of Mycobacterium tuberculosis as a potential immunodiagnostic reagent. J. Clin. Microbiol. 35:553–57 [Google Scholar]
  85. Jacobs AJ, Mongkolsapaya J, Screaton GR, McShane H, Wilkinson RJ. 85.  2016. Antibodies and tuberculosis. Tuberculosis 101:102–13 [Google Scholar]
  86. Blankley S, Graham CM, Levin J, Turner J, Berry MP. 86.  et al. 2016. A 380-gene meta-signature of active tuberculosis compared with healthy controls. Eur. Respir. J. 47:1873–76 [Google Scholar]
  87. Esmail H, Lai RP, Lesosky M, Wilkinson KA, Graham CM. 87.  et al. 2018. Complement pathway gene activation and rising circulating immune complexes characterize early disease in HIV-associated tuberculosis. PNAS 115:5E964–73 [Google Scholar]
  88. Fletcher HA, Snowden MA, Landry B, Rida W, Satti I. 88.  et al. 2016. T-cell activation is an immune correlate of risk in BCG vaccinated infants. Nat. Commun. 7:11290 [Google Scholar]
  89. Lu LL, Chung AW, Rosebrock TR, Ghebremichael M, Yu WH. 89.  et al. 2016. A functional role for antibodies in tuberculosis. Cell 167:433–43.e14 [Google Scholar]
  90. Casadevall A. 90.  2017. Antibodies to Mycobacterium tuberculosis. . N. Engl. J. Med. 376:283–85 [Google Scholar]
  91. Zimmermann N, Thormann V, Hu B, Kohler AB, Imai-Matsushima A. 91.  et al. 2016. Human isotype-dependent inhibitory antibody responses against Mycobacterium tuberculosis. . EMBO Mol. Med. 8:1325–39 [Google Scholar]
  92. Lawn SD, Bekker LG, Wood R. 92.  2005. How effectively does HAART restore immune responses to Mycobacterium tuberculosis? Implications for tuberculosis control. AIDS 19:1113–24 [Google Scholar]
  93. Geldmacher C, Schuetz A, Ngwenyama N, Casazza JP, Sanga E. 93.  et al. 2008. Early depletion of Mycobacterium tuberculosis-specific T helper 1 cell responses after HIV-1 infection. J. Infect. Dis. 198:1590–98 [Google Scholar]
  94. Riou C, Bunjun R, Muller TL, Kiravu A, Ginbot Z. 94.  et al. 2016. Selective reduction of IFN-γ single positive mycobacteria-specific CD4+ T cells in HIV-1 infected individuals with latent tuberculosis infection. Tuberculosis 101:25–30 [Google Scholar]
  95. Rangaka MX, Diwakar L, Seldon R, van Cutsem G, Meintjes GA. 95.  et al. 2007. Clinical, immunological, and epidemiological importance of antituberculosis T cell responses in HIV-infected Africans. Clin. Infect. Dis. 44:1639–46 [Google Scholar]
  96. Serbina NV, Lazarevic V, Flynn JL. 96.  2001. CD4+ T cells are required for the development of cytotoxic CD8+ T cells during Mycobacterium tuberculosis infection. J. Immunol. 167:6991–7000 [Google Scholar]
  97. Hammond AS, McConkey SJ, Hill PC, Crozier S, Klein MR. 97.  et al. 2008. Mycobacterial T cell responses in HIV-infected patients with advanced immunosuppression. J. Infect. Dis. 197:295–99 [Google Scholar]
  98. Geldmacher C, Ngwenyama N, Schuetz A, Petrovas C, Reither K. 98.  et al. 2010. Preferential infection and depletion of Mycobacterium tuberculosis–specific CD4 T cells after HIV-1 infection. J. Exp. Med. 207:2869–81Showed selective loss of Mtb-specific CD4+ T cells in HIV-1 infection. [Google Scholar]
  99. Kalsdorf B, Skolimowska KH, Scriba TJ, Dawson R, Dheda K. 99.  et al. 2013. Relationship between chemokine receptor expression, chemokine levels and HIV-1 replication in the lungs of persons exposed to Mycobacterium tuberculosis. . Eur. J. Immunol. 43:540–49 [Google Scholar]
  100. Juffermans NP, Speelman P, Verbon A, Veenstra J, Jie C. 100.  et al. 2001. Patients with active tuberculosis have increased expression of HIV coreceptors CXCR4 and CCR5 on CD4+ T cells. Clin. Infect. Dis. 32:650–52 [Google Scholar]
  101. Rosas-Taraco AG, Arce-Mendoza AY, Caballero-Olin G, Salinas-Carmona MC. 101.  2006. Mycobacterium tuberculosis upregulates coreceptors CCR5 and CXCR4 while HIV modulates CD14 favoring concurrent infection. AIDS Res. Hum. Retrovir. 22:45–51 [Google Scholar]
  102. Desvignes L, Wolf AJ, Ernst JD. 102.  2012. Dynamic roles of type I and type II IFNs in early infection with Mycobacterium tuberculosis. . J. Immunol. 188:6205–15 [Google Scholar]
  103. Orme IM, Robinson RT, Cooper AM. 103.  2015. The balance between protective and pathogenic immune responses in the TB-infected lung. Nat. Immunol. 16:57–63 [Google Scholar]
  104. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA. 104.  et al. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107:4781–89 [Google Scholar]
  105. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR. 105.  2007. Multiple-cytokine-producing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J. Virol. 81:8468–76 [Google Scholar]
  106. Wilkinson KA, Wilkinson RJ. 106.  2010. Polyfunctional T cells in human tuberculosis. Eur. J. Immunol. 40:2139–42 [Google Scholar]
  107. Wozniak TM, Saunders BM, Ryan AA, Britton WJ. 107.  2010. Mycobacterium bovis BCG-specific Th17 cells confer partial protection against Mycobacterium tuberculosis infection in the absence of gamma interferon. Infect. Immun. 78:4187–94 [Google Scholar]
  108. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J. 108.  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. 8:369–77 [Google Scholar]
  109. Cruz A, Fraga AG, Fountain JJ, Rangel-Moreno J, Torrado E. 109.  et al. 2010. Pathological role of interleukin 17 in mice subjected to repeated BCG vaccination after infection with Mycobacterium tuberculosis. . J. Exp. Med. 207:1609–16 [Google Scholar]
  110. Nandi B, Behar SM. 110.  2011. Regulation of neutrophils by interferon-gamma limits lung inflammation during tuberculosis infection. J. Exp. Med. 208:2251–62 [Google Scholar]
  111. Scott-Browne JP, Shafiani S, Tucker-Heard G, Ishida-Tsubota K, Fontenot JD. 111.  et al. 2007. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J. Exp. Med. 204:2159–69 [Google Scholar]
  112. Shafiani S, Dinh C, Ertelt JM, Moguche AO, Siddiqui I. 112.  et al. 2013. Pathogen-specific Treg cells expand early during Mycobacterium tuberculosis infection but are later eliminated in response to interleukin-12. Immunity 38:1261–70 [Google Scholar]
  113. McBride A, Konowich J, Salgame P. 113.  2013. Host defense and recruitment of Foxp3+ T regulatory cells to the lungs in chronic Mycobacterium tuberculosis infection requires Toll-like receptor 2. PLOS Pathog 9:e1003397 [Google Scholar]
  114. Salgame P. 114.  2005. Host innate and Th1 responses and the bacterial factors that control Mycobacterium tuberculosis infection. Curr. Opin. Immunol. 17:374–80 [Google Scholar]
  115. Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J. 115.  et al. 2001. Tuberculosis associated with infliximab, a tumor necrosis factor α–neutralizing agent. N. Engl. J. Med. 345:1098–104 [Google Scholar]
  116. Newport MJ, Huxley CM, Huston S, Hawrylowicz CM, Oostra BA. 116.  et al. 1996. A mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection. N. Engl. J. Med. 335:1941–49 [Google Scholar]
  117. Cooper A, Dalton D, Stewart T, Griffin J, Russell D, Orme I. 117.  1993. Disseminated tuberculosis in interferon-gamma gene-disrupted mice. J. Exp. Med. 178:2243–47 [Google Scholar]
  118. Flynn J, Chan J, Triebold K, Dalton D, Stewart T, Bloom B. 118.  1993. An essential role for interferon-gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249–54 [Google Scholar]
  119. Sakai S, Kauffman KD, Sallin MA, Sharpe AH, Young HA. 119.  et al. 2016. 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 12:e1005667 [Google Scholar]
  120. Barber DL, Mayer-Barber KD, Feng CG, Sharpe AH, Sher A. 120.  2011. CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition. J. Immunol. 186:1598–607 [Google Scholar]
  121. Reungwetwattana T, Adjei AA. 121.  2016. Anti-PD-1 antibody treatment and the development of acute pulmonary tuberculosis. J. Thorac. Oncol. 11:2048–50 [Google Scholar]
  122. Sasindran SJ, Torrelles JB. 122.  2011. Mycobacterium tuberculosis infection and inflammation: What is beneficial for the host and for the bacterium?. Front. Microbiol. 2:2 [Google Scholar]
  123. Day CL, Mkhwanazi N, Reddy S, Mncube Z, van der Stok M. 123.  et al. 2008. Detection of polyfunctional Mycobacterium tuberculosis–specific T cells and association with viral load in HIV-1–infected persons. J. Infect. Dis. 197:990–99 [Google Scholar]
  124. Zhang M, Gong J, Iyer DV, Jones BE, Modlin RL, Barnes PF. 124.  1994. T cell cytokine responses in persons with tuberculosis and human immunodeficiency virus infection. J. Clin. Investig. 94:2435–42 [Google Scholar]
  125. Moir S, Chun TW, Fauci AS. 125.  2011. Pathogenic mechanisms of HIV disease. Annu. Rev. Pathol. 6:223–48 [Google Scholar]
  126. Liu Z, Cumberland WG, Hultin LE, Prince HE, Detels R, Giorgi JV. 126.  1997. Elevated CD38 antigen expression on CD8+ T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and death in the Multicenter AIDS Cohort Study than CD4+ cell count, soluble immune activation markers, or combinations of HLA-DR and CD38 expression. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 16:83–92 [Google Scholar]
  127. Papagno L, Spina CA, Marchant A, Salio M, Rufer N. 127.  et al. 2004. Immune activation and CD8+ T-cell differentiation towards senescence in HIV-1 infection. PLOS Biol 2:E20 [Google Scholar]
  128. Pollock KM, Montamat-Sicotte DJ, Grass L, Cooke GS, Kapembwa MS. 128.  et al. 2016. PD-1 expression and cytokine secretion profiles of Mycobacterium tuberculosis-specific CD4+ T-cell subsets; potential correlates of containment in HIV-TB co-infection. PLOS ONE 11:e0146905 [Google Scholar]
  129. Shen L, Gao Y, Liu Y, Zhang B, Liu Q. 129.  et al. 2016. PD-1/PD-L pathway inhibits M.tb-specific CD4+ T-cell functions and phagocytosis of macrophages in active tuberculosis. Sci. Rep. 6:38362 [Google Scholar]
  130. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B. 130.  et al. 2008. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112:2826–35 [Google Scholar]
  131. Clark S, Page E, Ford T, Metcalf R, Pozniak A. 131.  et al. 2011. Reduced TH1/TH17 CD4 T-cell numbers are associated with impaired purified protein derivative-specific cytokine responses in patients with HIV-1 infection. J. Allergy Clin. Immunol. 128:838–46.e5 [Google Scholar]
  132. Korb VC, Phulukdaree A, Lalloo UG, Chuturgoon AA, Moodley D. 132.  2016. TB/HIV pleurisy reduces Th17 lymphocyte proportion independent of the cytokine microenvironment. Tuberculosis 99:92–99 [Google Scholar]
  133. Riou C, Strickland N, Soares AP, Corleis B, Kwon DS. 133.  et al. 2016. HIV skews the lineage-defining transcriptional profile of Mycobacterium tuberculosis-specific CD4+ T cells. J. Immunol. 196:3006–18 [Google Scholar]
  134. Bell LC, Pollara G, Pascoe M, Tomlinson GS, Lehloenya RJ. 134.  et al. 2016. In vivo molecular dissection of the effects of HIV-1 in active tuberculosis. PLOS Pathog 12:e1005469 [Google Scholar]
  135. Sarrazin H, Wilkinson KA, Andersson J, Rangaka MX, Radler L. 135.  et al. 2009. Association between tuberculin skin test reactivity, the memory CD4 cell subset, and circulating FoxP3-expressing cells in HIV-infected persons. J. Infect. Dis. 199:702–10 [Google Scholar]
  136. Lewinsohn DM, Grotzke JE, Heinzel AS, Zhu L, Ovendale PJ. 136.  et al. 2006. Secreted proteins from Mycobacterium tuberculosis gain access to the cytosolic MHC class-I antigen-processing pathway. J. Immunol. 177:437–42 [Google Scholar]
  137. Lalvani A, Brookes R, Wilkinson RJ, Malin AS, Pathan AA. 137.  et al. 1998. Human cytolytic and interferon γ-secreting CD8+ T lymphocytes specific for Mycobacterium tuberculosis. . PNAS 95:270–75 [Google Scholar]
  138. Silva BD, Trentini MM, da Costa AC, Kipnis A, Junqueira-Kipnis AP. 138.  2014. Different phenotypes of CD8+ T cells associated with bacterial load in active tuberculosis. Immunol. Lett. 160:23–32 [Google Scholar]
  139. Stenger S, Mazzacarro RJ, Uyemura K, Cho S, Barnes PF. 139.  et al. 1997. Differential effects of cytolytic T cell subsets on intracellular infection. Science 276:1684–87 [Google Scholar]
  140. Canaday DH, Wilkinson RJ, Li Q, Harding CV, Silver RF, Boom WH. 140.  2001. CD4+ and CD8+ T cells kill intracellular Mycobacterium tuberculosis by a perforin and Fas/Fas ligand-independent mechanism. J. Immunol. 167:2734–42 [Google Scholar]
  141. Lewinsohn DA, Heinzel AS, Gardner JM, Zhu L, Alderson MR, Lewinsohn DM. 141.  2003. Mycobacterium tuberculosis-specific CD8+ T cells preferentially recognize heavily infected cells. Am. J. Respir. Crit. Care Med. 168:1346–52 [Google Scholar]
  142. Woodworth JS, Behar SM. 142.  2006. Mycobacterium tuberculosis-specific CD8+ T cells and their role in immunity. Crit. Rev. Immunol. 26:317–52 [Google Scholar]
  143. Foreman TW, Mehra S, LoBato DN, Malek A, Alvarez X. 143.  et al. 2016. CD4+ T-cell-independent mechanisms suppress reactivation of latent tuberculosis in a macaque model of HIV coinfection. PNAS 113:E5636–44 [Google Scholar]
  144. Bruns H, Meinken C, Schauenberg P, Harter G, Kern P. 144.  et al. 2009. Anti-TNF immunotherapy reduces CD8+ T cell-mediated antimicrobial activity against Mycobacterium tuberculosis in humans. J. Clin. Investig. 119:1167–77 [Google Scholar]
  145. Kalokhe AS, Adekambi T, Ibegbu CC, Ray SM, Day CL, Rengarajan J. 145.  2015. Impaired degranulation and proliferative capacity of Mycobacterium tuberculosis-specific CD8+ T cells in HIV-infected individuals with latent tuberculosis. J. Infect. Dis. 211:635–40 [Google Scholar]
  146. Breton G, Chomont N, Takata H, Fromentin R, Ahlers J. 146.  et al. 2013. Programmed death-1 is a marker for abnormal distribution of naive/memory T cell subsets in HIV-1 infection. J. Immunol. 191:2194–204 [Google Scholar]
  147. Autran B, Carcelain G, Li TS, Blanc C, Mathez D. 147.  et al. 1997. Positive effects of combined antiretroviral therapy on CD4+ T cell homeostasis and function in advanced HIV disease. Science 277:112–16 [Google Scholar]
  148. Wilkinson KA, Seldon R, Meintjes G, Rangaka MX, Hanekom WA. 148.  et al. 2009. Dissection of regenerating T-cell responses against tuberculosis in HIV-infected adults sensitized by Mycobacterium tuberculosis. . Am. J. Respir. Crit. Care Med. 180:674–83 [Google Scholar]
  149. Lindenstrom T, Knudsen NP, Agger EM, Andersen P. 149.  2013. Control of chronic Mycobacterium tuberculosis infection by CD4 KLRG1 IL-2–secreting central memory cells. J. Immunol. 190:6311–19 [Google Scholar]
  150. Vogelzang A, Perdomo C, Zedler U, Kuhlmann S, Hurwitz R. 150.  et al. 2014. Central memory CD4+ T cells are responsible for the recombinant Bacillus Calmette-Guérin ΔureC::hly vaccine's superior protection against tuberculosis. J. Infect. Dis. 210:1928–37 [Google Scholar]
  151. Schnittman SM, Lane HC, Higgins SE, Folks T, Fauci AS. 151.  1986. Direct polyclonal activation of human B lymphocytes by the acquired immune deficiency syndrome virus. Science 233:1084–86 [Google Scholar]
  152. Moir S, Malaspina A, Ogwaro KM, Donoghue ET, Hallahan CW. 152.  et al. 2001. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. PNAS 98:10362–67 [Google Scholar]
  153. Moir S, Malaspina A, Ho J, Wang W, Dipoto AC. 153.  et al. 2008. Normalization of B cell counts and subpopulations after antiretroviral therapy in chronic HIV disease. J. Infect. Dis. 197:572–79 [Google Scholar]
  154. Malaspina A, Moir S, Kottilil S, Hallahan CW, Ehler LA. 154.  et al. 2003. Deleterious effect of HIV-1 plasma viremia on B cell costimulatory function. J. Immunol. 170:5965–72 [Google Scholar]
  155. Morris L, Binley JM, Clas BA, Bonhoeffer S, Astill TP. 155.  et al. 1998. HIV-1 antigen-specific and -nonspecific B cell responses are sensitive to combination antiretroviral therapy. J. Exp. Med. 188:233–45 [Google Scholar]
  156. Malaspina A, Moir S, Orsega SM, Vasquez J, Miller NJ. 156.  et al. 2005. Compromised B cell responses to influenza vaccination in HIV-infected individuals. J. Infect. Dis. 191:1442–50 [Google Scholar]
  157. Muller M, Wandel S, Colebunders R, Attia S, Furrer H, Egger M. 157.  2010. Immune reconstitution inflammatory syndrome in patients starting antiretroviral therapy for HIV infection: a systematic review and meta-analysis. Lancet Infect. Dis. 10:251–61 [Google Scholar]
  158. Namale PE, Abdullahi LH, Fine S, Kamkuemah M, Wilkinson RJ, Meintjes G. 158.  2015. Paradoxical TB-IRIS in HIV-infected adults: a systematic review and meta-analysis. Future Microbiol 10:1077–99 [Google Scholar]
  159. Marais S, Meintjes G, Pepper DJ, Dodd LE, Schutz C. 159.  et al. 2013. Frequency, severity, and prediction of tuberculous meningitis immune reconstitution inflammatory syndrome. Clin. Infect. Dis. 56:450–60 [Google Scholar]
  160. Murdoch DM, Venter WD, Feldman C, Van Rie A. 160.  2008. Incidence and risk factors for the immune reconstitution inflammatory syndrome in HIV patients in South Africa: a prospective study. AIDS 22:601–10 [Google Scholar]
  161. Blanc FX, Sok T, Laureillard D, Borand L, Rekacewicz C. 161.  et al. 2011. Earlier versus later start of antiretroviral therapy in HIV-infected adults with tuberculosis. N. Engl. J. Med. 365:1471–81 [Google Scholar]
  162. Manosuthi W, Kiertiburanakul S, Phoorisri T, Sungkanuparph S. 162.  2006. Immune reconstitution inflammatory syndrome of tuberculosis among HIV-infected patients receiving antituberculous and antiretroviral therapy. J. Infect. 53:357–63 [Google Scholar]
  163. Meintjes G, Lawn SD, Scano F, Maartens G, French MA. 163.  et al. 2008. Tuberculosis-associated immune reconstitution inflammatory syndrome: case definitions for use in resource-limited settings. Lancet Infect. Dis. 8:516–23 [Google Scholar]
  164. Meintjes G, Wilkinson RJ, Morroni C, Pepper DJ, Rebe K. 164.  et al. 2010. Randomized placebo-controlled trial of prednisone for paradoxical tuberculosis-associated immune reconstitution inflammatory syndrome. AIDS 24:2381–90Showed efficacy of corticosteroid treatment of TB-IRIS and that such therapy decreases proinflammatory cytokines. [Google Scholar]
  165. Lai RP, Meintjes G, Wilkinson RJ. 165.  2016. HIV-1 tuberculosis-associated immune reconstitution inflammatory syndrome. Semin. Immunopathol. 38:185–98 [Google Scholar]
  166. Bourgarit A, Carcelain G, Martinez V, Lascoux C, Delcey V. 166.  et al. 2006. Explosion of tuberculin-specific Th1-responses induces immune restoration syndrome in tuberculosis and HIV co-infected patients. AIDS 20:F1–7 [Google Scholar]
  167. Morlese JF, Orkin CM, Abbas R, Burton C, Qazi NA. 167.  et al. 2003. Plasma IL-6 as a marker of mycobacterial immune restoration disease in HIV-1 infection. AIDS 17:1411–13 [Google Scholar]
  168. Narendran G, Andrade BB, Porter BO, Chandrasekhar C, Venkatesan P. 168.  et al. 2013. Paradoxical tuberculosis immune reconstitution inflammatory syndrome (TB-IRIS) in HIV patients with culture confirmed pulmonary tuberculosis in India and the potential role of IL-6 in prediction. PLOS ONE 8:e63541 [Google Scholar]
  169. Ravimohan S, Tamuhla N, Steenhoff AP, Letlhogile R, Nfanyana K. 169.  et al. 2015. Immunological profiling of tuberculosis-associated immune reconstitution inflammatory syndrome and non-immune reconstitution inflammatory syndrome death in HIV-infected adults with pulmonary tuberculosis starting antiretroviral therapy: a prospective observational cohort study. Lancet Infect. Dis. 15:429–38 [Google Scholar]
  170. Meintjes G, Wilkinson KA, Rangaka MX, Skolimowska K, van Veen K. 170.  et al. 2008. Type 1 helper T cells and FoxP3-positive T cells in HIV-tuberculosis-associated immune reconstitution inflammatory syndrome. Am. J. Respir. Crit. Care Med. 178:1083–89Showed efficacy of corticosteroid treatment of TB-IRIS and that such therapy decreases proinflammatory cytokines. [Google Scholar]
  171. Antonelli LR, Mahnke Y, Hodge JN, Porter BO, Barber DL. 171.  et al. 2010. Elevated frequencies of highly activated CD4+ T cells in HIV+ patients developing immune reconstitution inflammatory syndrome. Blood 116:3818–27 [Google Scholar]
  172. Bourgarit A, Carcelain G, Samri A, Parizot C, Lafaurie M. 172.  et al. 2009. Tuberculosis-associated immune restoration syndrome in HIV-1-infected patients involves tuberculin-specific CD4 Th1 cells and KIR-negative γδ T cells. J. Immunol. 183:3915–23 [Google Scholar]
  173. Wilkinson KA, Walker NF, Meintjes G, Deffur A, Nicol MP. 173.  et al. 2015. Cytotoxic mediators in paradoxical HIV-tuberculosis immune reconstitution inflammatory syndrome. J. Immunol. 194:1748–54 [Google Scholar]
  174. Espinosa E, Romero-Rodriguez DP, Cantoral-Diaz MT, Reyes-Teran G. 174.  2013. Transient expansion of activated CD8+ T cells characterizes tuberculosis-associated immune reconstitution inflammatory syndrome in patients with HIV: a case control study. J. Inflamm. 10:21 [Google Scholar]
  175. Goovaerts O, Jennes W, Massinga-Loembé M, Ondoa P, Ceulemans A. 175.  et al.; TB-IRIS Study Group. 2015. Lower pre-treatment T cell activation in early- and late-onset tuberculosis-associated immune reconstitution inflammatory syndrome. PLOS ONE 10:e0133924 [Google Scholar]
  176. Vignesh R, Kumarasamy N, Lim A, Solomon S, Murugavel KG. 176.  et al. 2013. TB-IRIS after initiation of antiretroviral therapy is associated with expansion of preexistent Th1 responses against Mycobacterium tuberculosis antigens. J. Acquir. Immune Defic. Syndr. 64:241–48 [Google Scholar]
  177. Simonney N, Dewulf G, Herrmann JL, Gutierrez MC, Vicaut E. 177.  et al. 2008. Anti-PGL-Tb1 responses as an indicator of the immune restoration syndrome in HIV-TB patients. Tuberculosis 88:453–61 [Google Scholar]
  178. Sumatoh HR, Oliver BG, Kumar M, Elliott JH, Vonthanak S. 178.  et al. 2011. Mycobacterial antibody levels and immune restoration disease in HIV patients treated in South East Asia. Biomark. Med. 5:847–53 [Google Scholar]
  179. Pean P, Nerrienet E, Madec Y, Borand L, Laureillard D. 179.  et al. 2012. Natural killer cell degranulation capacity predicts early onset of the immune reconstitution inflammatory syndrome (IRIS) in HIV-infected patients with tuberculosis. Blood 119:3315–20 [Google Scholar]
  180. Conradie F, Foulkes AS, Ive P, Yin X, Roussos K. 180.  et al. 2011. Natural killer cell activation distinguishes Mycobacterium tuberculosis-mediated immune reconstitution syndrome from chronic HIV and HIV/MTB coinfection. J. Acquir. Immune Defic. Syndr. 58:309–18 [Google Scholar]
  181. Marais S, Lai RPJ, Wilkinson KA, Meintjes G, O'Garra A, Wilkinson RJ. 181.  2017. Inflammasome activation underlying central nervous system deterioration in HIV-associated tuberculosis. J. Infect. Dis. 215:677–86 [Google Scholar]
  182. Lawn SD, Wainwright H, Orrell C. 182.  2009. Fatal unmasking tuberculosis immune reconstitution disease with bronchiolitis obliterans organizing pneumonia: the role of macrophages. AIDS 23:143–45 [Google Scholar]
  183. Andrade BB, Singh A, Narendran G, Schechter ME, Nayak K. 183.  et al. 2014. Mycobacterial antigen driven activation of CD14++CD16 monocytes is a predictor of tuberculosis-associated immune reconstitution inflammatory syndrome. PLOS Pathog 10:e1004433 [Google Scholar]
  184. Tran HT, Van den Bergh R, Vu TN, Laukens K, Worodria W. 184.  et al.; TB-IRIS Study Group. 2014. The role of monocytes in the development of tuberculosis-associated immune reconstitution inflammatory syndrome. Immunobiology 219:37–44 [Google Scholar]
  185. Tran HT, Van den Bergh R, Loembe MM, Worodria W, Mayanja-Kizza H. 185.  et al.; TB-IRIS Study Group. 2013. Modulation of the complement system in monocytes contributes to tuberculosis-associated immune reconstitution inflammatory syndrome. AIDS 27:1725–34 [Google Scholar]
  186. Lai RP, Meintjes G, Wilkinson KA, Graham CM, Marais S. 186.  et al. 2015. HIV-tuberculosis-associated immune reconstitution inflammatory syndrome is characterized by Toll-like receptor and inflammasome signalling. Nat. Commun. 6:8451 [Google Scholar]
  187. Tan HY, Yong YK, Shankar EM, Paukovics G, Ellegard R. 187.  et al. 2016. Aberrant inflammasome activation characterizes tuberculosis-associated immune reconstitution inflammatory syndrome. J. Immunol. 196:4052–63 [Google Scholar]
  188. Wilkinson RJ. 188.  2014. Host-directed therapies against tuberculosis. Lancet Respir. Med. 2:85–87 [Google Scholar]
  189. Tenforde MW, Yadav A, Dowdy DW, Gupte N, Shivakoti R. 189.  et al. 2017. Vitamin A and D deficiencies associated with incident tuberculosis in HIV-infected patients initiating antiretroviral therapy in multinational case-cohort study. J. Acquir. Immune Defic. Syndr. 75:e71–79 [Google Scholar]
  190. Martineau AR, Nhamoyebonde S, Oni T, Rangaka MX, Marais S. 190.  et al. 2011. Reciprocal seasonal variation in vitamin D status and tuberculosis notifications in Cape Town, South Africa. PNAS 108:19013–17 [Google Scholar]
  191. Rook GA, Steele J, Ainsworth M, Champion BR. 191.  1986. Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant gamma-interferon on human monocytes and murine peritoneal macrophages. Immunology 59:333–38 [Google Scholar]
  192. Liu PT, Stenger S, Li H, Wenzel L, Tan BH. 192.  et al. 2006. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311:1770–73 [Google Scholar]
  193. Martineau AR, Wilkinson KA, Newton SM, Floto RA, Norman AW. 193.  et al. 2007. IFN-gamma- and TNF-independent vitamin D-inducible human suppression of mycobacteria: the role of cathelicidin LL-37. J. Immunol. 178:7190–98 [Google Scholar]
  194. Campbell GR, Spector SA. 194.  2012. Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLOS Pathog 8:e1002689 [Google Scholar]
  195. Campbell GR, Spector SA. 195.  2012. Toll-like receptor 8 ligands activate a vitamin D mediated autophagic response that inhibits human immunodeficiency virus type 1. PLOS Pathog 8:e1003017 [Google Scholar]
  196. Bruns H, Stegelmann F, Fabri M, Dohner K, van Zandbergen G. 196.  et al. 2012. Abelson tyrosine kinase controls phagosomal acidification required for killing of Mycobacterium tuberculosis in human macrophages. J. Immunol. 189:4069–78 [Google Scholar]
  197. Napier RJ, Rafi W, Cheruvu M, Powell KR, Zaunbrecher MA. 197.  et al. 2011. Imatinib-sensitive tyrosine kinases regulate mycobacterial pathogenesis and represent therapeutic targets against tuberculosis. Cell Host Microbe 10:475–85 [Google Scholar]
  198. Napier RJ, Norris BA, Swimm A, Giver CR, Harris WA. 198.  et al. 2015. Low doses of imatinib induce myelopoiesis and enhance host anti-microbial immunity. PLOS Pathog 11:e1004770 [Google Scholar]
  199. Swingler S, Mann AM, Zhou J, Swingler C, Stevenson M. 199.  2007. Apoptotic killing of HIV-1-infected macrophages is subverted by the viral envelope glycoprotein. PLOS Pathog 3:1281–90 [Google Scholar]
  200. Koon HB, Krown SE, Lee JY, Honda K, Rapisuwon S. 200.  et al. 2014. Phase II trial of imatinib in AIDS-associated Kaposi's sarcoma: AIDS Malignancy Consortium Protocol 042. J. Clin. Oncol. 32:402–8 [Google Scholar]
  201. Thwaites GE, Nguyen DB, Nguyen HD, Hoang TQ, Do TT. 201.  et al. 2004. Dexamethasone for the treatment of tuberculous meningitis in adolescents and adults. N. Engl. J. Med. 351:1741–51 [Google Scholar]
  202. Mayosi BM, Ntsekhe M, Bosch J, Pandie S, Jung H. 202.  et al.; for IMPI Trial Investig. 2014. Prednisolone and Mycobacterium indicus pranii in tuberculous pericarditis. N. Engl. J. Med. 371:1121–30 [Google Scholar]
  203. Meintjes G, Skolimowska KH, Wilkinson KA, Matthews K, Tadokera R. 203.  et al. 2012. Corticosteroid-modulated immune activation in the tuberculosis immune reconstitution inflammatory syndrome. Am. J. Respir. Crit. Care Med. 186:369–77 [Google Scholar]
  204. Elliott AM, Luzze H, Quigley MA, Nakiyingi JS, Kyaligonza S. 204.  et al. 2004. A randomized, double-blind, placebo-controlled trial of the use of prednisolone as an adjunct to treatment in HIV-1-associated pleural tuberculosis. J. Infect. Dis. 190:869–78 [Google Scholar]
  205. Klausner JD, Makonkawkeyoon S, Akarasewi P, Nakata K, Kasinrerk W. 205.  et al. 1996. The effect of thalidomide on the pathogenesis of human immunodeficiency virus type 1 and M. tuberculosis infection. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 11:247–57 [Google Scholar]
  206. Payvandi F, Wu L, Haley M, Schafer PH, Zhang LH. 206.  et al. 2004. Immunomodulatory drugs inhibit expression of cyclooxygenase-2 from TNF-alpha, IL-1beta, and LPS-stimulated human PBMC in a partially IL-10-dependent manner. Cell Immunol 230:81–88 [Google Scholar]
  207. Brunel AS, Reynes J, Tuaillon E, Rubbo PA, Lortholary O. 207.  et al. 2012. Thalidomide for steroid-dependent immune reconstitution inflammatory syndromes during AIDS. AIDS 26:2110–12 [Google Scholar]
  208. Schoeman JF, Springer P, van Rensburg AJ, Swanevelder S, Hanekom WA. 208.  et al. 2004. Adjunctive thalidomide therapy for childhood tuberculous meningitis: results of a randomized study. J. Child Neurol. 19:250–57 [Google Scholar]
  209. Kubler A, Luna B, Larsson C, Ammerman NC, Andrade BB. 209.  et al. 2015. Mycobacterium tuberculosis dysregulates MMP/TIMP balance to drive rapid cavitation and unrestrained bacterial proliferation. J. Pathol. 235:431–44 [Google Scholar]
  210. Green JA, Tran CT, Farrar JJ, Nguyen MT, Nguyen PH. 210.  et al. 2009. Dexamethasone, cerebrospinal fluid matrix metalloproteinase concentrations and clinical outcomes in tuberculous meningitis. PLOS ONE 4:e7277 [Google Scholar]
  211. Ravimohan S, Tamuhla N, Kung SJ, Nfanyana K, Steenhoff AP. 211.  et al. 2016. Matrix metalloproteinases in tuberculosis-immune reconstitution inflammatory syndrome and impaired lung function among advanced HIV/TB co-infected patients initiating antiretroviral therapy. EBioMedicine 3:100–7 [Google Scholar]
  212. Mahajan S, Dkhar HK, Chandra V, Dave S, Nanduri R. 212.  et al. 2012. Mycobacterium tuberculosis modulates macrophage lipid-sensing nuclear receptors PPARγ and TR4 for survival. J. Immunol. 188:5593–603 [Google Scholar]
  213. Liu L, Liu J, Niu G, Xu Q, Chen Q. 213.  2015. Mycobacterium tuberculosis 19-kDa lipoprotein induces Toll-like receptor 2-dependent peroxisome proliferator-activated receptor gamma expression and promotes inflammatory responses in human macrophages. Mol. Med. Rep. 11:2921–26 [Google Scholar]
  214. Rajaram MV, Brooks MN, Morris JD, Torrelles JB, Azad AK, Schlesinger LS. 214.  2010. Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor gamma linking mannose receptor recognition to regulation of immune responses. J. Immunol. 185:929–42 [Google Scholar]
  215. Almeida PE, Silva AR, Maya-Monteiro CM, Torocsik D, D'Avila H. 215.  et al. 2009. Mycobacterium bovis bacillus Calmette-Guérin infection induces TLR2-dependent peroxisome proliferator-activated receptor γ expression and activation: functions in inflammation, lipid metabolism, and pathogenesis. J. Immunol. 183:1337–45 [Google Scholar]
  216. Bernier A, Cleret-Buhot A, Zhang Y, Goulet JP, Monteiro P. 216.  et al. 2013. Transcriptional profiling reveals molecular signatures associated with HIV permissiveness in Th1Th17 cells and identifies peroxisome proliferator-activated receptor gamma as an intrinsic negative regulator of viral replication. Retrovirology 10:160 [Google Scholar]
  217. Okada S, Markle JG, Deenick EK, Mele F, Averbuch D. 217.  et al. 2015. Impairment of immunity to Candida and Mycobacterium in humans with bi-allelic RORC mutations. Science 349:606–13 [Google Scholar]
  218. Ryndak MB, Singh KK, Peng Z, Zolla-Pazner S, Li H. 218.  et al. 2014. Transcriptional profiling of Mycobacterium tuberculosis replicating ex vivo in blood from HIV and HIV+ subjects. PLOS ONE 9:e94939 [Google Scholar]
  219. Toossi Z, Wu M, Liu S, Hirsch CS, Walrath J. 219.  et al. 2014. Role of protease inhibitor 9 in survival and replication of Mycobacterium tuberculosis in mononuclear phagocytes from HIV-1-infected patients. AIDS 28:679–87 [Google Scholar]
  220. Ranjbar S, Boshoff HI, Mulder A, Siddiqi N, Rubin EJ, Goldfeld AE. 220.  2009. HIV-1 replication is differentially regulated by distinct clinical strains of Mycobacterium tuberculosis. . PLOS ONE 4:e6116 [Google Scholar]
  221. Mancino G, Placido R, Bach S, Mariani F, Montesano C. 221.  et al. 1997. Infection of human monocytes with Mycobacterium tuberculosis enhances human immunodeficiency virus type 1 replication and transmission to T cells. J. Infect. Dis. 175:1531–35 [Google Scholar]
  222. Zhang Y, Nakata K, Weiden M, Rom WN. 222.  1995. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication by transcriptional activation at the long terminal repeat. J. Clin. Investig. 95:2324–31 [Google Scholar]
  223. Honda Y, Rogers L, Nakata K, Zhao BY, Pine R. 223.  et al. 1998. Type I interferon induces inhibitory 16-kD CCAAT/enhancer binding protein (C/EBP)β, repressing the HIV-1 long terminal repeat in macrophages: Pulmonary tuberculosis alters C/EBP expression, enhancing HIV-1 replication. J. Exp. Med. 188:1255–65 [Google Scholar]
  224. Hoshino Y, Nakata K, Hoshino S, Honda Y, Tse DB. 224.  et al. 2002. Maximal HIV-1 replication in alveolar macrophages during tuberculosis requires both lymphocyte contact and cytokines. J. Exp. Med. 195:495–505 [Google Scholar]
  225. Lawn SD, Pisell TL, Hirsch CS, Wu M, Butera ST, Toossi Z. 225.  2001. Anatomically compartmentalized human immunodeficiency virus replication in HLA-DR+ cells and CD14+ macrophages at the site of pleural tuberculosis coinfection. J. Infect. Dis. 184:1127–33 [Google Scholar]
  226. Toossi Z, Wu M, Hirsch CS, Mayanja-Kizza H, Baseke J. 226.  et al. 2012. Activation of P-TEFb at sites of dual HIV/TB infection, and inhibition of MTB-induced HIV transcriptional activation by the inhibitor of CDK9, Indirubin-3′-monoxime. AIDS Res. Hum. Retrovir. 28:182–87 [Google Scholar]
  227. Marais S, Meintjes G, Lesosky M, Wilkinson KA, Wilkinson RJ. 227.  2016. Interleukin-17 mediated differences in the pathogenesis of HIV-1-associated tuberculous and cryptococcal meningitis. AIDS 30:395–404 [Google Scholar]
  228. Falvo JV, Ranjbar S, Jasenosky LD, Goldfeld AE. 228.  2011. Arc of a vicious circle: pathways activated by Mycobacterium tuberculosis that target the HIV-1 long terminal repeat. Am. J. Respir. Cell Mol. Biol. 45:1116–24 [Google Scholar]
  229. Hoshino Y, Tse DB, Rochford G, Prabhakar S, Hoshino S. 229.  et al. 2004. Mycobacterium tuberculosis-induced CXCR4 and chemokine expression leads to preferential X4 HIV-1 replication in human macrophages. J. Immunol. 172:6251–58 [Google Scholar]
  230. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D. 230.  et al. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661–66 [Google Scholar]
  231. Toossi Z, Johnson JL, Kanost RA, Wu M, Luzze H. 231.  et al. 2001. Increased replication of HIV-1 at sites of Mycobacterium tuberculosis infection: potential mechanisms of viral activation. J. Acquir. Immune Defic. Syndr. 28:1–8 [Google Scholar]
  232. Danaviah S, Sacks JA, Kumar KP, Taylor LM, Fallows DA. 232.  et al. 2013. Immunohistological characterization of spinal TB granulomas from HIV-negative and -positive patients. Tuberculosis 93:432–41 [Google Scholar]
  233. Danaviah S, de Oliveira T, Gordon M, Govender S, Chelule P. 233.  et al. 2016. Analysis of dominant HIV quasispecies suggests independent viral evolution within spinal granulomas coinfected with Mycobacterium tuberculosis and HIV-1 subtype C. AIDS Res. Hum. Retrovir. 32:262–70 [Google Scholar]
  234. Nakata K, Rom WN, Honda Y, Condos R, Kanegasaki S. 234.  et al. 1997. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. Am. J. Respir. Crit. Care Med. 155:996–1003 [Google Scholar]
  235. Collins KR, Mayanja-Kizza H, Sullivan BA, Quinones-Mateu ME, Toossi Z, Arts EJ. 235.  2000. Greater diversity of HIV-1 quasispecies in HIV-infected individuals with active tuberculosis. J. Acquir. Immune Defic. Syndr. 24:408–17 [Google Scholar]
  236. Collins KR, Quinones-Mateu ME, Wu M, Luzze H, Johnson JL. 236.  et al. 2002. Human immunodeficiency virus type 1 (HIV-1) quasispecies at the sites of Mycobacterium tuberculosis infection contribute to systemic HIV-1 heterogeneity. J. Virol. 76:1697–706 [Google Scholar]
  237. Biru T, Lennemann T, Sturmer M, Stephan C, Nisius G. 237.  et al. 2010. Human immunodeficiency virus type-1 group M quasispecies evolution: diversity and divergence in patients co-infected with active tuberculosis. Med. Microbiol. Immunol. 199:323–32 [Google Scholar]
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