Inhibiting the programmed death 1 pathway rescues Mycobacterium tuberculosis-specific interferon γ-producing T cells from apoptosis in patients with pulmonary tuberculosis

Journal of Infectious Diseases

Volumn 208, Issue 4, 2013, Pages 603-615

  Singh, Amar ^a   Mohan, Anant ^a   Dey, Aparajit B ^a   Mitra, Dipendra K ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

APCs and apoptosis; Programmed death 1; T cells; Tuberculosis

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; PROGRAMMED DEATH 1 RECEPTOR;

ADULT; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL STIMULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNE STATUS; IN VITRO STUDY; LUNG TUBERCULOSIS; MAJOR CLINICAL STUDY; MALE; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

APCS AND APOPTOSIS; PROGRAMMED DEATH-1; T CELLS; TUBERCULOSIS;

ADOLESCENT; ADULT; APOPTOSIS; B-LYMPHOCYTES; CYTOKINES; FEMALE; FLOW CYTOMETRY; HUMANS; INTERFERON-GAMMA; MALE; MIDDLE AGED; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; PROGRAMMED CELL DEATH 1 RECEPTOR; T-LYMPHOCYTES; TUBERCULOSIS, PULMONARY; YOUNG ADULT;

EID: 84880944556     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jit206     Document Type: Article

References (33)

1. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, et al. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 1993; 178:2243-7.
2. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, et al. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 1993; 178:2249-54.
3. O'Garra A, Vieira PL, Vieira P, Goldfeld AE. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J Clin Invest 2004; 114:1372-8.
4. Von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol 2004; 6:338-44.
5. Sharma PK, Saha PK, Singh A, Sharma SK, Ghosh B, et al. FoxP3+ regulatory T cells suppress effector T-cell function at pathologic site in miliary tuberculosis. Am J Respir Crit Care Med 2009; 179:1061-70.
6. Urbani S, Amadei B, Tola D, Massari M, Schivazappa S, et al. PD-1 expression in acute hepatitis C virus (HCV) infection is associated with HCV-specific CD8 exhaustion. J Virol 2006; 80:11398-403.
7. Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006; 443:350-4.
8. Trautmann L, Janbazian L, Chomont N, Said EA, Gimmig S, et al. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat Med 2006; 12:1198-202.
9. Sharpe AH, Wherry EJ, Ahmed R, Freeman GJ. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol 2007; 8:239-45.
10. Das S, Suarez G, Beswick EJ, Sierra JC, Graham DY, et al. Expression of B7-H1 on gastric epithelial cells: its potential role in regulating T cells during Helicobacter pylori infection. J Immunol 2006; 176:3000-9.
11. Smith P, Walsh CM, Mangan NE, Fallon RE, Sayers JR, et al. Schistosoma mansoni worms induce anergy of T cells via selective up-regulation of programmed death ligand 1 on macrophages. J Immunol 2004; 173:1240-8.
12. Lazar-Molnar E, Chen B, Sweeney KA, Wang EJ, Liu W, et al. Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis. Proc Natl Acad Sci 2010; 107:13402-7.
13. Singh A, Dey AB, Sharma PK, Mohan A, Mitra DK. Foxp3+ regulatory T cells among tuberculosis patients: impact on prognosis and restoration of antigen specific IFN-γ producing T cells. PLoS ONE 2012; 9:e44728.
14. Chattopadhyay PK, Yu J, Roederer M. A live-cell assay to detect antigen-specific CD4+ T cells with diverse cytokine profiles. Nat Med 2005; 11:1113-7.
15. Li L, Qiao D, Fu X, Lao S, Zhang X, et al. Identification of Mycobacterium tuberculosis-specific Th1, Th17 and Th22 cells using the expression of CD40L in tuberculous pleurisy. PLoS One 2011; 6:e20165.
16. Liu Y, Janeway CA Jr. Microbial induction of co-stimulatory activity for CD4 T-cell growth. Int Immunol 1991; 3:323-32.
17. Jurado JO, Alvarez IB, Pasquinelli V, Martinez GJ, Quiroga MF, et al. Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis. J Immunol 2008; 181:116-25.
18. Alvarez IB, Pasquinelli V, Jurado JO, Abbate E, Musella RM, et al. Role played by the programmed death-1-programmed death ligand pathway during innate immunity against Mycobacterium tuberculosis. J Infect Dis 2010; 202:524-32.
19. Evans A, Riva A, Cooksley H, Phillips S, Puranik S, et al. Programmed death 1 expression during antiviral treatment of chronic hepatitis B: impact of hepatitis B e-antigen seroconversion. Hepatology 2008; 48:759-69.
20. Sharma SK, Mitra DK, Balamurugan A, Pandey RM, Mehra NK. Cytokine polarization in miliary and pleural tuberculosis. J Clin Immunol 2002; 22:345-52.
21. Mitra DK, Joshi B, Dinda AK, Rai AK, Girdhar BK, et al. Induction of lepromin reactivity in cured lepromatous leprosy patients: impaired chemokine response dissociates protective immunity from delayed-type hypersensitivity. Microbes and Infection 2009; 11:1122-30.
22. Kaufmann SH. How can immunology contribute to the control of tuberculosis? Nat Rev Immunol 2001; 1:20-30.
23. de la Barrera S, Aleman M, Musella R, Schierloh P, Pasquinelli V, et al. IL-10 down-regulates costimulatory molecules on Mycobacterium tuberculosis- pulsed macrophages and impairs the lytic activity of CD4 and CD8 CTL in tuberculosis patients. Clin Exp Immunol 2004; 138:128-38.
24. Pieters J. Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 2008; 3:399-407.
25. Rohde K, Yates RM, Purdy GE, Russell DG. Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 2007; 219:37-54.
26. Sakai S, Kawamura I, Okazaki T, Tsuchiya K, Uchiyama R, et al. PD-1- PD-L1 pathway impairs T(h)1 immune response in the late stage of infection with Mycobacterium bovis bacillus Calmette-Guerin. Int Immunol 2010; 22:915-25.
27. Mendoza-Coronel E, Camacho-Sandoval R, Bonifaz LC, Lopez-Vidal Y. PD-L2 induction on dendritic cells exposed to Mycobacterium avium downregulates BCG-specific T cell response. Tuberculosis 2011; 91:36-46.
28. Dulos J, Carven GJ, van Boxtel SJ, Evers S, Driessen-Engels LJ, et al. PD-1 blockade augments Th1 and Th17 and suppresses Th2 responses in peripheral blood from patients with prostate and advanced melanoma cancer. J Immunother 2012; 35:169-78.
29. Barber DL, Mayer-Barber KD, Feng CG, Sharpe AH, Sher A. CD4 T cells promote rather than control tuberculosis in the absence of PD-1- mediated inhibition. J Immunol 2011; 186:1598-607.
30. Tousif S, Singh Y, Prasad DV, Sharma P, Van Kaer L, et al. T cells from Programmed Death-1 deficient mice respond poorly to Mycobacterium tuberculosis infection. PLoS One 2011; 6:e19864.
31. Golden-Mason L, Klarquist J, Wahed AS, Rosen HR. Cutting edge: programmed death-1 expression is increased on immunocytes in chronic hepatitis C virus and predicts failure of response to antiviral therapy: race-dependent differences. J Immunol 2008; 180:3637-41.
32. Henao-Tamayo M, Irwin SM, Shang S, Ordway D, Orme IM. T lymphocyte surface expression of exhaustion markers as biomarkers of the efficacy of chemotherapy for tuberculosis. Tuberculosis 2011; 91:308-13.
33. Ha SJ, Mueller SN, Wherry EJ, Barber DL, Aubert RD, et al. Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. J Exp Med 2008; 205:543-55.