Biomarkers of CD4+ T-cell activation as risk factors for tuberculosis-associated immune reconstitution inflammatory syndrome

AIDS

Volumn 28, Issue 11, 2014, Pages 1593-1602

  Chakrabarti, Lisa A ^a   Boucherie, Céline ^b,c   Bugault, Florence ^a   Cumont, Marie Christine ^a   Roussillon, Caroline ^b,c   Breton, Guillaume ^d   Patey, Olivier ^e   Chêne, Geneviève ^b,c,f   Richert, Laura ^b,c   Lortholary, Olivier ^g  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c INSERM   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^e Hôpital Villeneuve St Georges   (France)

^f BORDEAUX UNIVERSITY HOSPITAL   (France)

^g UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Biomarker; HIV; Immune reconstitution inflammatory syndrome; Interleukin 7; Soluble interleukin 2 receptor; Tuberculosis

Indexed keywords

BIOLOGICAL MARKER; CYTOKINE; EFAVIRENZ; EMTRICITABINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; RIFAMPICIN; TENOFOVIR; TUMOR NECROSIS FACTOR ALPHA; ADENINE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; BENZOXAZINE DERIVATIVE; DEOXYCYTIDINE; PHOSPHONIC ACID DERIVATIVE;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FOLLOW UP; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; INFECTION RISK; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MIXED INFECTION; MULTICENTER STUDY (TOPIC); MYCOBACTERIUM TUBERCULOSIS; PHASE 2 CLINICAL TRIAL (TOPIC); PREDICTION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; T LYMPHOCYTE ACTIVATION; TUBERCULOSIS; TUBERCULOSIS ASSOCIATED IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; VIRUS LOAD; ANALOGS AND DERIVATIVES; BLOOD; CLINICAL TRIAL; COMPLICATION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MIDDLE AGED; MULTICENTER STUDY; RISK FACTOR;

ADENINE; ADULT; ANTI-HIV AGENTS; BENZOXAZINES; BIOLOGICAL MARKERS; CD4-POSITIVE T-LYMPHOCYTES; DEOXYCYTIDINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HIV INFECTIONS; HUMANS; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; ORGANOPHOSPHONATES; RISK FACTORS; TUBERCULOSIS;

EID: 84904749527     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000311     Document Type: Article

References (60)

1. Zumla A, Raviglione M, Hafner R, von Reyn CF. Tuberculosis. N Engl J Med 2013; 368: 745-755.
2. Ackah AN, Coulibaly D, Digbeu H, Diallo K, Vetter KM, Coulibaly IM, et al. Response to treatment, mortality, and CD4 lymphocyte counts in HIV-infected persons with tuberculosis in Abidjan, Cote d'Ivoire. Lancet 1995; 345: 607-610.
3. Aaron L, Saadoun D, Calatroni I, Launay O, Memain N, Vincent V, et al. Tuberculosis in HIV-infected patients: a comprehensive review. Clin Microbiol Infect 2004; 10: 388-398.
4. Gandhi NR, Moll A, Sturm AW, Pawinski R, Govender T, Lalloo U, et al. Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet 2006; 368: 1575-1580.
5. Muller M, Wandel S, Colebunders R, Attia S, Furrer H, Egger M, et al. Immune reconstitution inflammatory syndrome in patients starting antiretroviral therapy for HIV infection: a systematic review and meta-Analysis. Lancet Infect Dis 2010; 10: 251-261.
6. Breton G, Duval X, Estellat C, Poaletti X, Bonnet D, Mvondo Mvondo D, et al. Determinants of immune reconstitution inflammatory syndrome in HIV type 1-infected patients with tuberculosis after initiation of antiretroviral therapy. Clin Infect Dis 2004; 39: 1709-1712.
7. Meintjes G, Lawn SD, Scano F, Maartens G, French MA, Worodria W, et al. Tuberculosis-Associated immune reconstitution inflammatory syndrome: case definitions for use in resource-limited settings. Lancet Infect Dis 2008; 8: 516-523.
8. Marais S, Meintjes G, Pepper DJ, Dodd LE, Schutz C, Ismail Z, et al. Frequency, severity, and prediction of tuberculous meningitis immune reconstitution inflammatory syndrome. Clin Infect Dis 2013; 56: 450-460.
9. Agarwal U, Kumar A, Behera D, French MA, Price P. Tuberculosis associated immune reconstitution inflammatory syndrome in patients infected with HIV: meningitis a potentially life threatening manifestation. AIDS Res Ther 2012; 9: 17.
10. French MA. The immunopathogenesis of mycobacterial immune restoration disease. Lancet Infect Dis 2006; 6: 461-462.
11. Pean P, Nerrienet E, Madec Y, Borand L, Laureillard D, Fernandez M, et al. Natural killer cell degranulation capacity predicts early onset of the immune reconstitution inflammatory syndrome (IRIS) in HIV-infected patients with tuberculosis. Blood 2012; 119: 3315-3320.
12. Bourgarit A, Carcelain G, Martinez V, Lascoux C, Delcey V, Gicquel B, et al. Explosion of tuberculin-specific Th1-responses induces immune restoration syndrome in tuberculosis and HIV co-infected patients. AIDS 2006; 20: F1-F7.
13. Mahnke YD, Greenwald JH, DerSimonian R, Roby G, Antonelli LR, Sher A, et al. Selective expansion of polyfunctional pathogen-specific CD4(+) T cells in HIV-1-infected patients with immune reconstitution inflammatory syndrome. Blood 2012; 119: 3105-3112.
14. Bourgarit A, Carcelain G, Samri A, Parizot C, Lafaurie M, Abgrall S, et al. Tuberculosis-Associated immune restoration syndrome in HIV-1-infected patients involves tuberculinspecific CD4 Th1 cells and KIR-negative gammadelta T cells. J Immunol 2009; 183: 3915-3923.
15. Elliott JH, Vohith K, Saramony S, Savuth C, Dara C, Sarim C, et al. Immunopathogenesis and diagnosis of tuberculosis and tuberculosis-Associated immune reconstitution inflammatory syndrome during early antiretroviral therapy. J Infect Dis 2009; 200: 1736-1745.
16. Sereti I, Rodger AJ, French MA. Biomarkers in immune reconstitution inflammatory syndrome: signals from pathogenesis. Curr Opin HIV AIDS 2010; 5: 504-510.
17. Barber DL, Andrade BB, Sereti I, Sher A. Immune reconstitution inflammatory syndrome: the trouble with immunity when you had none. Nat Rev Microbiol 2012; 10: 150-156.
18. Tadokera R, Meintjes G, Skolimowska KH, Wilkinson KA, Matthews K, Seldon R, et al. Hypercytokinaemia accompanies HIV-Tuberculosis immune reconstitution inflammatory syndrome. Eur Respir J 2011; 37: 1248-1259.
19. Lortholary O, Fontanet A, Memain N, Martin A, Sitbon K, Dromer F. Incidence and risk factors of immune reconstitution inflammatory syndrome complicating HIV-Associated cryptococcosis in France. AIDS 2005; 19: 1043-1049.
20. Lawn SD, Wainwright H, Orrell C. Fatal unmasking tuberculosis immune reconstitution disease with bronchiolitis obliterans organizing pneumonia: the role of macrophages. AIDS 2009; 23: 143-145.
21. Tadokera R, Wilkinson KA, Meintjes GA, Skolimowska KH, Matthews K, Seldon R, et al. Role of the interleukin 10 family of cytokines in patients with immune reconstitution inflammatory syndrome associated with HIV infection and tuberculosis. J Infect Dis 2013; 207: 1148-1156.
22. Tan DB, Lim A, Yong YK, Ponnampalavanar S, Omar S, Kamarulzaman A, et al. TLR2-induced cytokine responses may characterize HIV-infected patients experiencing mycobacterial immune restoration disease. AIDS 2011; 25: 1455-1460.
23. Breton G. Immune reconstitution inflammatory syndrome. In: Schaaf HS, Zumla A,editors. Tuberculosis: a comprehensive clinical reference Philadelphia: Saunders, Elsevier; 2009. pp. 689-700.
24. Meintjes G, Scriven J, Marais S. Management of the immune reconstitution inflammatory syndrome. Curr HIV/AIDS Rep 2012; 9: 238-250.
25. Oliver BG, Elliott JH, Price P, Phillips M, Saphonn V, Vun MC, et al. Mediators of innate and adaptive immune responses differentially affect immune restoration disease associated with Mycobacterium tuberculosis in HIV patients beginning antiretroviral therapy. J Infect Dis 2010; 202: 1728-1737.
26. Porter BO, Ouedraogo GL, Hodge JN, Smith MA, Pau A, Roby G, et al. d-Dimer and CRP levels are elevated prior to antiretroviral treatment in patients who develop IRIS. Clin Immunol 2010; 136: 42-50.
27. Narendran G, Andrade BB, Porter BO, Chandrasekhar C, Venkatesan P, Menon PA, et al. 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 2013; 8: e63541.
28. Haddow LJ, Dibben O, Moosa MY, Borrow P, Easterbrook PJ. Circulating inflammatory biomarkers can predict and characterize tuberculosis-Associated immune reconstitution inflammatory syndrome. AIDS 2011; 25: 1163-1174.
29. French MA, Price P, Stone SF. Immune restoration disease after antiretroviral therapy. AIDS 2004; 18: 1615-1627.
30. Benjamini Y, Hochberg Y. On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Educ Behav Stat 2000; 25: 60-83.
31. Richert L, Hue S, Hocini H, Raimbault M, Lacabaratz C, Surenaud M, et al. Cytokine and gene transcription profiles of immune responses elicited by HIV lipopeptide vaccine in HIV-negative volunteers. AIDS 2013; 27: 1421-1431.
32. Lundstrom W, Fewkes NM, Mackall CL. IL-7 in human health and disease. Semin Immunol 2012; 24: 218-224.
33. Rubin LA, Nelson DL. The soluble interleukin-2 receptor: biology, function, and clinical application. Ann Intern Med 1990; 113: 619-627.
34. Brusko TM, Wasserfall CH, Hulme MA, Cabrera R, Schatz D, Atkinson MA. Influence of membrane CD25 stability on T lymphocyte activity: implications for immunoregulation. PLoS One 2009; 4: e7980.
35. Mackall CL, Fry TJ, Gress RE. Harnessing the biology of IL-7 for therapeutic application. Nat Rev Immunol 2011; 11: 330-342.
36. Prince HE, Kleinman S, Williams AE. Soluble IL-2 receptor levels in serum from blood donors seropositive for HIV. J Immunol 1988; 140: 1139-1141.
37. Maier LM, Anderson DE, Severson CA, Baecher-Allan C, Healy B, Liu DV, et al. Soluble IL-2RA levels in multiple sclerosis subjects and the effect of soluble IL-2RA on immune responses. J Immunol 2009; 182: 1541-1547.
38. Deeks SG. HIV infection, inflammation, immunosenescence, and aging. Annu Rev Med 2011; 62: 141-155.
39. Antonelli LR, Mahnke Y, Hodge JN, Porter BO, Barber DL, DerSimonian R, et al. Elevated frequencies of highly activated CD4+ T cells in HIV+ patients developing immune reconstitution inflammatory syndrome. Blood 2010; 116: 3818-3827.
40. Chahroudi A, Silvestri G. Interleukin-7 in HIV pathogenesis and therapy. Eur Cytokine Netw 2010; 21: 202-207.
41. Juffroy O, Bugault F, Lambotte O, Landires I, Viard JP, Niel L, et al. Dual mechanism of impairment of interleukin-7 (IL-7) responses in human immunodeficiency virus infection: decreased IL-7 binding and abnormal activation of the JAK/STAT5 pathway. J Virol 2010; 84: 96-108.
42. Landires I, Bugault F, Lambotte O, de Truchis P, Slama L, Danckaert A, et al. HIV infection perturbs interleukin-7 signaling at the step of STAT5 nuclear relocalization. AIDS 2011; 25: 1843-1853.
43. Seddiki N, Sasson SC, Santner-Nanan B, Munier M, van Bockel D, Ip S, et al. Proliferation of weakly suppressive regulatory CD4+ T cells is associated with over-Active CD4+ T-cell responses in HIV-positive patients with mycobacterial immune restoration disease. Eur J Immunol 2009; 39: 391-403.
44. Napolitano LA, Grant RM, Deeks SG, Schmidt D, De Rosa SC, Herzenberg LA, et al. Increased production of IL-7 accompanies HIV-1-mediated T-cell depletion: implications for T-cell homeostasis. Nat Med 2001; 7: 73-79.
45. Sawa Y, Arima Y, Ogura H, Kitabayashi C, Jiang JJ, Fukushima T, et al. Hepatic interleukin-7 expression regulates T-cell responses. Immunity 2009; 30: 447-457.
46. Alves NL, Huntington ND, Mention JJ, Richard-Le Goff O, Di Santo JP. Cutting edge: a thymocyte-Thymic epithelial cell cross-Talk dynamically regulates intrathymic IL-7 expression in vivo. J Immunol 2010; 184: 5949-5953.
47. Miller CN, Hartigan-O'Connor DJ, Lee MS, Laidlaw G, Cornelissen IP, Matloubian M, et al. IL-7 production in murine lymphatic endothelial cells and induction in the setting of peripheral lymphopenia. Int Immunol 2013; 25: 471-483.
48. Grant PM, Komarow L, Lederman MM, Pahwa S, Zolopa AR, Andersen J, et al. Elevated interleukin 8 and T-helper 1 and T-helper 17 cytokine levels prior to antiretroviral therapy in participants who developed immune reconstitution inflammatory syndrome during ACTG A5164. J Infect Dis 2012; 206: 1715-1723.
49. Boulware DR, Meya DB, Bergemann TL, Wiesner DL, Rhein J, Musubire A, et al. Clinical features and serum biomarkers in HIV immune reconstitution inflammatory syndrome after cryptococcal meningitis: a prospective cohort study. PLoS Med 2010; 7: e1000384.
50. Swain SL, McKinstry KK, Strutt TM. Expanding roles for CD4(+) T cells in immunity to viruses. Nat Rev Immunol 2012; 12: 136-148.
51. Barber DL, Mayer-Barber KD, Antonelli LR, Wilson MS, White S, Caspar P, et al. Th1-driven immune reconstitution disease in Mycobacterium avium-infected mice. Blood 2010; 116: 3485-3493.
52. Liovat AS, Rey-Cuille MA, Lecuroux C, Jacquelin B, Girault I, Petitjean G, et al. Acute plasma biomarkers of T-cell activation set-point levels and of disease progression in HIV-1 infection. PLoS One 2012; 7: e46143.
53. Groom JR, Luster AD. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol Cell Biol 2011; 89: 207-215.
54. Crane M, Oliver B, Matthews G, Avihingsanon A, Ubolyam S, Markovska V, et al. Immunopathogenesis of hepatic flare in HIV/hepatitis B virus (HBV)-coinfected individuals after the initiation of HBV-Active antiretroviral therapy. J Infect Dis 2009; 199: 974-981.
55. Tan DB, Yong YK, Tan HY, Kamarulzaman A, Tan LH, Lim A, et al. Immunological profiles of immune restoration disease presenting as mycobacterial lymphadenitis and cryptococcal meningitis. HIV Med 2008; 9: 307-316.
56. Groom JR, Richmond J, Murooka TT, Sorensen EW, Sung JH, Bankert K, et al. CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity 2012; 37: 1091-1103.
57. Kitaura H, Ohara N, Kobayashi K, Yamada T. TNF-Alphamediated multiplication of human immunodeficiency virus in chronically infected monocytoid cells by mycobacterial infection. APMIS 2001; 109: 533-540.
58. Blanc FX, Sok T, Laureillard D, Borand L, Rekacewicz C, Nerrienet E, et al. Earlier versus later start of antiretroviral therapy in HIV-infected adults with tuberculosis. N Engl J Med 2011; 365: 1471-1481.
59. Abdool Karim SS, Naidoo K, Grobler A, Padayatchi N, Baxter C, Gray AL, et al. Integration of antiretroviral therapy with tuberculosis treatment. N Engl J Med 2011; 365: 1492-1501.
60. Havlir DV, Kendall MA, Ive P, Kumwenda J, Swindells S, Qasba SS, et al. Timing of antiretroviral therapy for HIV-1 infection and tuberculosis. N Engl J Med 2011; 365: 1482-1491.