TB-IRIS, T-cell activation, and remodeling of the T-cell compartment in highly immunosuppressed HIV-infected patients with TB

AIDS

Volumn 29, Issue 3, 2014, Pages 263-273

  Haridas, Viraga ^a   Pean, Polidy ^b   Jasenosky, Luke D ^a   Madec, Yoann ^c   Laureillard, Didier ^d,g   Sok, Thim ^d   Sath, Sun ^d   Borand, Laurence ^b   Marcy, Olivier ^d,h   Chan, Sarin ^d,i   Tsitsikov, Erdyni ^a   Delfraissy, Jean François ^e,f   Blanc, François Xavier ^f,j   Goldfeld, Anne E ^a,d  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

^c INSTITUT PASTEUR   (France)

^d Cambodian Health Committee   (Cambodia)

^e French National Agency for AIDS and Viral Hepatitis Research (ANRS)   (France)

^f BICÊTRE HOSPITAL   (France)

^g NÎMES UNIVERSITY HOSPITAL   (France)

^h UNIVERSITÉ DE BORDEAUX   (France)

ⁱ Calmette Hospital   (Cambodia)

^j L INSTITUT DU THORAX   (France)

more..

Author keywords

Activated T cells; Antiretroviral therapy; CAMELIA trial; CCR5+CD4+; Effector memory; HIV; Immunosuppression; T cells; TB; TB IRIS

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; CD134 ANTIGEN; CD4 ANTIGEN; CD45RO ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR5; FAS ANTIGEN; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; TUBERCULOSTATIC AGENT; ANTIRETROVIRUS AGENT; CYTOKINE;

ADULT; ANTIVIRAL THERAPY; ARTICLE; CAMBODIA; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNOPATHOGENESIS; IMMUNOPHENOTYPING; MAJOR CLINICAL STUDY; MEMORY T LYMPHOCYTE; MIXED INFECTION; MULTICENTER STUDY (TOPIC); PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL (TOPIC); T LYMPHOCYTE ACTIVATION; TUBERCULOSIS; TUBERCULOSIS ASSOCIATED IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; VIRUS LOAD; CLINICAL TRIAL; COMPLICATION; FEMALE; HIV INFECTIONS; IMMUNOLOGY; MALE; MULTICENTER STUDY; PATHOLOGY; RANDOMIZED CONTROLLED TRIAL; SECRETION (PROCESS); T LYMPHOCYTE; TREATMENT OUTCOME;

ADULT; ANTI-RETROVIRAL AGENTS; ANTITUBERCULAR AGENTS; CAMBODIA; CYTOKINES; FEMALE; FLOW CYTOMETRY; HIV INFECTIONS; HUMANS; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNOPHENOTYPING; MALE; PROSPECTIVE STUDIES; T-LYMPHOCYTES; TREATMENT OUTCOME; TUBERCULOSIS;

EID: 84923178349     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000546     Document Type: Article

References (49)

1. 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.
2. 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.
3. 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.
4. Luetkemeyer AF, Kendall MA, Nyirenda M, Wu X, Ive P, Benson CA, et al. Tuberculosis immune reconstitution inflammatory syndrome in A5221 STRIDE: timing, severity and implications for HIV-TB programs. J Acquir Immune Defic Syndr 2014; 65:423-428.
5. 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.
6. Meintjes G, Rabie H, Wilkinson RJ, Cotton MF. Tuberculosisassociated immune reconstitution inflammatory syndrome and unmasking of tuberculosis by antiretroviral therapy. Clin Chest Med 2009; 30:797-810x.
7. Laureillard D, Marcy O, Madec Y, Chea S, Chan S, Borand L, et al. Paradoxical tuberculosis-associated immune reconstitution inflammatory syndrome after early initiation of antiretroviral therapy in a randomized clinical trial. AIDS 2013; 27:2577-2586.
8. Loken MR, Brosnan JM, Bach BA, Ault KA. Establishing optimal lymphocyte gates for immunophenotyping by flow cytometry. Cytometry 1990; 11:453-459.
9. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc B 1995; 57:289-300.
10. Liu W, Putnam AL, Xu-Yu Z, Szot GL, Lee MR, Zhu S, et al. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4R T reg cells. J Exp Med 2006; 203:1701-1711.
11. Seddiki N, Santner-Nanan B, Martinson J, Zaunders J, Sasson S, Landay A, et al. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J Exp Med 2006; 203:1693-1700.
12. Saison J, Demaret J, Venet F, Chidiac C, Malcus C, Poitevin- Later F, et al. CD4RCD25RCD127- assessment as a surrogate phenotype for FOXP3R regulatory T cells in HIV-1 infected viremic and aviremic subjects. Cytometry B Clin Cytom 2013; 84:50-54.
13. Romero P, Zippelius A, Kurth I, Pittet MJ, Touvrey C, Iancu EM, et al. Four functionally distinct populations of human effectormemory CD8R T lymphocytes. J Immunol 2007; 178:4112-4119.
14. Tomiyama H, Takata H, Matsuda T, Takiguchi M. Phenotypic classification of human CD8R T cells reflecting their function: inverse correlation between quantitative expression of CD27 and cytotoxic effector function. Eur J Immunol 2004; 34:999-1010.
15. Takata H, Takiguchi M. Three memory subsets of human CD8R T cells differently expressing three cytolytic effector molecules. J Immunol 2006; 177:4330-4340.
16. 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.
17. Meintjes G, Wilkinson KA, Rangaka MX, Skolimowska K, van Veen K, Abrahams M, et al. Type 1 helper T cells and FoxP3- positive T cells in HIV-tuberculosis-associated immune reconstitution inflammatory syndrome. Am J Respir Crit Care Med 2008; 178:1083-1089.
18. Antonelli LR, Mahnke Y, Hodge JN, Porter BO, Barber DL, DerSimonian R, et al. Elevated frequencies of highly activated CD4R T cells in HIVR patients developing immune reconstitution inflammatory syndrome. Blood 2010; 116:3818-3827.
19. Seddiki N, Sasson SC, Santner-Nanan B, Munier M, van Bockel D, Ip S, et al. Proliferation of weakly suppressive regulatory CD4R T cells is associated with over-active CD4R T-cell responses in HIV-positive patients with mycobacterial immune restoration disease. Eur J Immunol 2009; 39:391-403.
20. Zaidi I, Peterson K, Jeffries D, Whittle H, de Silva T, Rowland- Jones S, et al. Immune reconstitution inflammatory syndrome and the influence of T regulatory cells: a cohort study in The Gambia. PLoS One 2012; 7:e39213.
21. Vignesh R, Kumarasamy N, Lim A, Solomon S, Murugavel KG, Balakrishnan P, et al. TB-IRIS after initiation of antiretroviral therapy is associated with expansion of preexistent Th1 responses against Mycobacterium tuberculosis antigens. J Acquir Immune Defic Syndr 2013; 64:241-248.
22. Qin S, Rottman JB, Myers P, Kassam N, Weinblatt M, Loetscher M, et al. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J Clin Invest 1998; 101:746-754.
23. Sallusto F, Kremmer E, Palermo B, Hoy A, Ponath P, Qin S, et al. Switch in chemokine receptor expression upon TCR stimulation reveals novel homing potential for recently activated T cells. Eur J Immunol 1999; 29:2037-2045.
24. Bleul CC, Wu L, Hoxie JA, Springer TA, Mackay CR. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc Natl Acad Sci USA 1997; 94:1925-1930.
25. Giunti D, Borsellino G, Benelli R, Marchese M, Capello E, Valle MT, et al. Phenotypic and functional analysis of T cells homing into the CSF of subjects with inflammatory diseases of the CNS. J Leukoc Biol 2003; 73:584-590.
26. Pepper DJ, Marais S, Maartens G, Rebe K, Morroni C, Rangaka MX, et al. Neurologic manifestations of paradoxical tuberculosis- associated immune reconstitution inflammatory syndrome: a case series. Clin Infect Dis 2009; 48:e96-e107.
27. Leone S, Nicastri E, Giglio S, Narciso P, Ippolito G, Acone N. Immune reconstitution inflammatory syndrome associated with Mycobacterium tuberculosis infection: a systematic review. Int J Infect Dis 2010; 14:e283-e291.
28. Verhofstede C, Nijhuis M, Vandekerckhove L. Correlation of coreceptor usage and disease progression. Curr Opin HIV AIDS 2012; 7:432-439.
29. 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.
30. Tran HT, Van den Bergh R, Vu TN, Laukens K, Worodria W, Loembe MM, et al. The role of monocytes in the development of tuberculosis-associated immune reconstitution inflammatory syndrome. Immunobiology 2014; 219:37-44.
31. Goldfeld AE, Strominger JL, Doyle C. Human tumor necrosis factor a gene regulation in phorbol ester stimulated T and B cell lines. J Exp Med 1991; 174:73-81.
32. 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.
33. Goovaerts O, Jennes W, Massinga-Loembe M, Ceulemans A, Worodria W, Mayanja-Kizza H, et al. LPS-binding protein and IL-6 mark paradoxical tuberculosis immune reconstitution inflammatory syndrome in HIV patients. PLoS One 2013; 8:e81856.
34. Chakrabarti LA, Boucherie C, Bugault F, Cumont MC, Roussillon C, Breton G, et al. Biomarkers of CD4R T cell activation as risk factors for tuberculosis-associated immune reconstitution inflammatory syndrome. AIDS 2014; 28:1593-1602.
35. Conesa-Botella A, Meintjes G, Coussens AK, van der Plas H, Goliath R, Schutz C, et al. Corticosteroid therapy, vitamin D status, and inflammatory cytokine profile in the HIV-tuberculosis immune reconstitution inflammatory syndrome. Clin Infect Dis 2012; 55:1004-1011.
36. Morlese JF, Orkin CM, Abbas R, Burton C, Qazi NA, Nelson MR, et al. Plasma IL-6 as a marker of mycobacterial immune restoration disease in HIV-1 infection. AIDS 2003; 17:1411-1413.
37. Stone SF, Price P, Keane NM, Murray RJ, French MA. Levels of IL-6 and soluble IL-6 receptor are increased in HIV patients with a history of immune restoration disease after HAART. HIV Med 2002; 3:21-27.
38. Boulware DR, Hullsiek KH, Puronen CE, Rupert A, Baker JV, French MA, et al. Higher levels of CRP, D-dimer, IL-6, and hyaluronic acid before initiation of antiretroviral therapy (ART) are associated with increased risk of AIDS or death. J Infect Dis 2011; 203:1637-1646.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. Tadokera R, Wilkinson KA, Meintjes GA, Skolimowska KH, Mathews 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.
45. Sierra-Madero J, Ellenberg SS, Rassool MS, Tierney A, Belaunzaran- Zamudio PF, Lopez-Martinez A, et al. Effect of the CCR5 antagonist maraviroc on the occurrence of immune reconstitution inflammatory syndrome in HIV (CADIRIS): a doubleblind, randomised, placebo-controlled trial. Lancet HIV 2014; 1:e60-e67.
46. Choy EH, Kavanaugh AF, Jones SA. The problem of choice: current biologic agents and future prospects in RA. Nat Rev Rheumatol 2013; 9:154-163.
47. Croft M, Benedict CA, Ware CF. Clinical targeting of the TNF and TNFR superfamilies. Nat Rev Drug Discov 2013; 12:147-168.
48. Adekambi T, Ibegbu CC, Kalokhe AS, Yu T, Ray SM, Rengarajan J. Distinct effector memory CD4R T cell signatures in latent Mycobacterium tuberculosis infection, BCG vaccination and clinically resolved tuberculosis. PLoS One 2012; 7:e36046.
49. Masopust D, Picker LJ. Hidden memories: frontline memory T cells and early pathogen interception. J Immunol 2012; 188:5811-5817.