Attrition of T-Cell functions and simultaneous upregulation of inhibitory markers correspond with the waning of BCG-induced protection against tuberculosis in mice

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Nandakumar, Subhadra ^a   Kannanganat, Sunil ^b   Posey, James E ^a   Rao Amara, Rama ^b   Sable, Suraj B ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; L SELECTIN; TUMOR NECROSIS FACTOR ALPHA; KLRG1 PROTEIN, HUMAN; LECTIN; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BCG VACCINATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOLYSIS; DRUG EFFICACY; FEMALE; IN VITRO STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTECTION; PROTEIN EXPRESSION; T LYMPHOCYTE; TUBERCULOSIS; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CYTOTOXICITY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; RADIOGRAPHY; TIME;

MUS;

ANIMALS; BCG VACCINE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CTLA-4 ANTIGEN; CYTOTOXICITY, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; HOST-PATHOGEN INTERACTIONS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-2; L-SELECTIN; LECTINS, C-TYPE; MICE, INBRED BALB C; MYCOBACTERIUM TUBERCULOSIS; TIME FACTORS; TRANS-ACTIVATORS; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84913569222     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113951     Document Type: Article

References (88)

1. World Health Organization (2013) Global Tuberculosis Report 2013 (World Health Organization, Geneva). Available: http://www.who.int/tb/publications/factsheet-global.pdf
2. Zwerling A, Behr MA, Verma A, Brewer TF, Menzies D, et al. (2011) The BCG World Atlas: a database of global BCG vaccination policies and practices. PLoS Med 8: e1001012.
3. Colditz GA, Berkey CS, Mosteller F, Brewer TF, Wilson ME, et al. (1995) The efficacy of bacillus Calmette-Guerin vaccination of newborns and infants in the prevention of tuberculosis: meta-analyses of the published literature. Pediatrics 96: 29-35.
4. Trunz BB, Fine P, Dye C (2006) Effect of BCG vaccination on childhood tuberculous meningitis and miliary tuberculosis worldwide: a meta-analysis and assessment of cost-effectiveness. Lancet 367: 1173-1180.
5. Fine PE (1995) Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346: 1339-1345.
6. Colditz GA, Brewer TF, Berkey CS, Wilson ME, Burdick E, et al. (1994) Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. JAMA 271: 698-702.
7. Brooks JV, Frank AA, Keen MA, Bellisle JT, Orme IM (2001) Boosting vaccine for tuberculosis. Infect Immun 69: 2714-2717.
8. Andersen P, Doherty TM (2005) The success and failure of BCG - implications for a novel tuberculosis vaccine. Nat Rev Microbiol 3: 656-662.
9. McShane H, Jacobs WR, Fine PE, Reed SG, McMurray DN, et al. (2012) BCG: myths, realities, and the need for alternative vaccine strategies. Tuberculosis (Edinb) 92: 283-288.
10. Brennan MJ, Clagett B, Fitzgerald H, Chen V, Williams A, et al. (2012) Preclinical evidence for implementing a prime-boost vaccine strategy for tuberculosis. Vaccine 30: 2811-2823.
11. Goonetilleke NP, McShane H, Hannan CM, Anderson RJ, Brookes RH, et al. (2003) Enhanced immunogenicity and protective efficacy against Mycobacterium tuberculosis of bacille Calmette-Guerin vaccine using mucosal administration and boosting with a recombinant modified vaccinia virus Ankara. J Immunol 171: 1602-1609.
12. Kaveh DA, Bachy VS, Hewinson RG, Hogarth PJ (2011) Systemic BCG immunization induces persistent lung mucosal multifunctional CD4 T(EM) cells which expand following virulent mycobacterial challenge. PLoS One 6: e21566.
13. Wherry EJ, Barber DL, Kaech SM, Blattman JN, Ahmed R (2004) Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc Natl Acad Sci U S A 101: 16004-16009.
14. Jelley-Gibbs DM, Dibble JP, Filipson S, Haynes L, Kemp RA, et al. (2005) Repeated stimulation of CD4 effector T cells can limit their protective function. J Exp Med 201: 1101-1112.
15. Soares AP, Kwong Chung CK, Choice T, Hughes EJ, Jacobs G, et al. (2013) Longitudinal changes in CD4(+) T-cell memory responses induced by BCG vaccination of newborns. J Infect Dis 207: 1084-1094.
16. Hawkridge A, Hatherill M, Little F, Goetz MA, Barker L, et al. (2008) Efficacy of percutaneous versus intradermal BCG in the prevention of tuberculosis in South African infants: randomised trial. BMJ 337: a2052.
17. Horvath CN, Shaler CR, Jeyanathan M, Zganiacz A, Xing Z (2012) Mechanisms of delayed antituberculosis protection in the lung of parenteral BCG-vaccinated hosts: a critical role of airway luminal T cells. Mucosal Immunol 5: 420-431.
18. Beverley PC, Sridhar S, Lalvani A, Tchilian EZ (2014) Harnessing local and systemic immunity for vaccines against tuberculosis. Mucosal Immunol 7: 20-26.
19. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR (2007) Multiple-cytokineproducing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J Virol 81: 8468-8476.
20. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, et al. (2007) Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 13: 843-850.
21. Grode L, Seiler P, Baumann S, Hess J, Brinkmann V, et al. (2005) Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guerin mutants that secrete listeriolysin. J Clin Invest 115: 2472-2479.
22. Sable SB, Cheruvu M, Nandakumar S, Sharma S, Bandyopadhyay K, et al. (2011) Cellular immune responses to nine Mycobacterium tuberculosis vaccine candidates following intranasal vaccination. PLoS One 6: e22718.
23. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, et al. (2003) Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 281: 65-78.
24. Casazza JP, Betts MR, Price DA, Precopio ML, Ruff LE, et al. (2006) Acquisition of direct antiviral effector functions by CMV-specific CD4+ T lymphocytes with cellular maturation. J Exp Med 203: 2865-2877.
25. Henao-Tamayo MI, Ordway DJ, Irwin SM, Shang S, Shanley C, et al. (2010) Phenotypic definition of effector and memory T-lymphocyte subsets in mice chronically infected with Mycobacterium tuberculosis. Clin Vaccine Immunol 17: 618-625.
26. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R (2003) Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 77: 4911-4927.
27. Wherry EJ, Ha SJ, Kaech SM, Haining WN, Sarkar S, et al. (2007) Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
28. Jurado JO, Alvarez IB, Pasquinelli V, Martinez GJ, Quiroga MF, et al. (2008) Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis. J Immunol 181: 116-125.
29. Reiley WW, Shafiani S, Wittmer ST, Tucker-Heard G, Moon JJ, et al. (2010) Distinct functions of antigen-specific CD4 T cells during murine Mycobacterium tuberculosis infection. Proc Natl Acad Sci U S A 107: 19408-19413.
30. Akbar AN, Henson SM (2011) Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Nat Rev Immunol 11: 289-295.
31. Turner J, Gonzalez-Juarrero M, Ellis DL, Basaraba RJ, Kipnis A, et al. (2002) In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice. J Immunol 169: 6343-6351.
32. Redford PS, Murray PJ, O'Garra A (2011) The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol 4: 261-270.
33. Cooper AM, Callahan JE, Griffin JP, Roberts AD, Orme IM (1995) Old Mice Are Able to Control Low-Dose Aerogenic Infections with Mycobacterium tuberculosis. Infect Immun 63: 3259-3265.
34. Vordermeier HM, Chambers MA, Cockle PJ, Whelan AO, Simmons J, et al. (2002) Correlation of ESAT-6-specific gamma interferon production with pathology in cattle following Mycobacterium bovis BCG vaccination against experimental bovine tuberculosis. Infect Immun 70: 3026-3032.
35. Tree JA, Williams A, Clark S, Hall G, Marsh PD, et al. (2004) Intranasal bacille Calmette-Guerin (BCG) vaccine dosage needs balancing between protection and lung pathology. Clin Exp Immunol 138: 405-409.
36. Olsen AW, Brandt L, Agger EM, van Pinxteren LAH, Andersen P (2004) The influence of remaining live BCG organisms in vaccinated mice on the maintenance of immunity to tuberculosis. Scand J of Immunol 60: 273-277.
37. Orme IM, Collins FM (1986) Aerogenic Vaccination of Mice with Mycobacterium Bovis BCG. Tubercle 67: 133-140.
38. Das B, Kashino SS, Pulu I, Kalita D, Swami V, et al. (2013) CD271(+) Bone Marrow Mesenchymal Stem Cells May Provide a Niche for Dormant Mycobacterium tuberculosis. Sci Transl Med 5.
39. Palendira U, Bean AG, Feng CG, Britton WJ (2002) Lymphocyte recruitment and protective efficacy against pulmonary mycobacterial infection are independent of the route of prior Mycobacterium bovis BCG immunization. Infect Immun 70: 1410-1416.
40. Mittrucker HW, Steinhoff U, Kohler A, Krause M, Lazar D, et al. (2007) Poor correlation between BCG vaccination-induced Tcell responses and protection against tuberculosis. Proc Natl Acad Sci U S A 104: 12434-12439.
41. Lindenstrom T, Aagaard C, Christensen D, Agger EM, Andersen P (2014) High-frequency vaccineinduced CD8 T cells specific for an epitope naturally processed during infection with Mycobacterium tuberculosis do not confer protection. Eur J Immunol.
42. Baldwin SL, Ching LK, Pine SO, Moutaftsi M, Lucas E, et al. (2013) Protection against Tuberculosis with Homologous or Heterologous Protein/Vector Vaccine Approaches Is Not Dependent on CD8(+) T Cells. J Immunol 191: 2514-2525.
43. Ryan A A, Nambiar J K, Wozniak T M, Roediger B, Shklovskaya E, et al. (2009) Antigen load governs the differential priming of CD8 T cells in response to the bacille Calmette Guerin vaccine or Mycobacterium tuberculosis infection. J Immunol 182: 7172-7177.
44. Chen CY, Huang D, Wang RC, Shen L, Zeng GC, et al. (2009) A Critical Role for CD8 T Cells in a Nonhuman Primate Model of Tuberculosis. PLOS Pathog 5.
45. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, et al. (1993) An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178: 2249-2254.
46. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, et al. (1995) Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2: 561-572.
47. Kagina BMN, Abel B, Scriba TJ, Hughes EJ, Keyser A, et al. (2010) Specific T Cell Frequency and Cytokine Expression Profile Do Not Correlate with Protection against Tuberculosis after Bacillus Calmette-Guerin Vaccination of Newborns. Am J Respir Crit Care Med. 182: 1073-1079.
48. Millington KA, Innes JA, Hackforth S, Hinks TS, Deeks JJ, et al. (2007) Dynamic relationship between IFN-gamma and IL-2 profile of Mycobacterium tuberculosis-specific T cells and antigen load. J Immunol 178: 5217-5226.
49. Day CL, Abrahams DA, Lerumo L, van Rensburg EJ, Stone L, et al. (2011) Functional Capacity of Mycobacterium tuberculosis-Specific T Cell Responses in Humans Is Associated with Mycobacterial Load. J Immunol 187: 2222-2232.
50. Nikolich-Zugich J (2008) Ageing and life-long maintenance of T-cell subsets in the face of latent persistent infections. Nat Rev Immunol 8: 512-522.
51. Henson SM, Akbar AN (2009) KLRG1-more than a marker for T cell senescence. Age 31: 285-291.
52. Wherry EJ (2011) T cell exhaustion. Nat Immunol 12: 492-499.
53. Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, et al. (2009) Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 10: 29-37.
54. Vesosky B, Flaherty DK, Turner J (2006) Th1 cytokines facilitate CD8-T-cell-mediated early resistance to infection with Mycobacterium tuberculosis in old mice. Infect Immun 74: 3314-3324.
55. Komine-Aizawa S, Yamazaki T, Yamazaki T, Hattori S, Miyamoto Y, et al. (2010) Influence of Advanced Age on Mycobacterium bovis BCG Vaccination in Guinea Pigs Aerogenically Infected with Mycobacterium tuberculosis. Clin Vaccine Immunol 17: 1500-1506.
56. Orme IM (2010) The Achilles heel of BCG. Tuberculosis (Edinb) 90: 329-332.
57. Lindenstrom T, Agger EM, Korsholm KS, Darrah PA, Aagaard C, et al. (2009) Tuberculosis Subunit Vaccination Provides Long-Term Protective Immunity Characterized by Multifunctional CD4 Memory T Cells. J Immunol 182: 8047-8055.
58. Kamath A, Woodworth JS, Behar SM (2006) Antigen-specific CD8+ T cells and the development of central memory during Mycobacterium tuberculosis infection. J Immunol 177: 6361-6369.
59. Sallusto F, Geginat J, Lanzavecchia A (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22: 745-763.
60. Harari A, Vallelian F, Meylan PR, Pantaleo G (2005) Functional heterogeneity of memory CD4 T cell responses in different conditions of antigen exposure and persistence. J Immunol 174: 1037-1045.
61. Soares AP, Scriba TJ, Joseph S, Harbacheuski R, Murray RA, et al. (2008) Bacillus Calmette-Guerin vaccination of human newborns induces T cells with complex cytokine and phenotypic profiles. J Immunol 180: 3569-3577.
62. Harari A, Vallelian F, Pantaleo G (2004) Phenotypic heterogeneity of antigen-specific CD4 Tcells under different conditions of antigen persistence and antigen load. Eur J Immunol 34: 3525-3533.
63. Andersen P, Smedegaard B (2000) CD4(+) T-cell subsets that mediate immunological memory to Mycobacterium tuberculosis infection in mice. Infect Immun 68: 621-629.
64. Kipnis A, Irwin S, Izzo AA, Basaraba RJ, Orme IM (2005) Memory T lymphocytes generated by Mycobacterium bovis BCG vaccination reside within a CD4 CD44(lo) CD62 ligand(hi) population. Infect Immun 73: 7759-7764.
65. Jagannath C, Lindsey DR, Dhandayuthapani S, Xu Y, Hunter RL Jr, et al. (2009) Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat Med 15: 267-276.
66. Vogelzang A, Perdomo C, Zedler U, Kuhlmann S, Hurwitz R, 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. DOI: 10.1093/infdis/jiu347
67. Hofstadler G, Schmitt K, Tulzer G, Binder L, Brandstetter B (1998) BCG lymphadenitis in an HIV-infected child 9.5 years after vaccination. AIDS Patient Care STDS 12: 677-680.
68. Hesseling AC, Rabie H, Marais BJ, Manders M, Lips M, et al. (2006) Bacille Calmette-Guerin vaccineinduced disease in HIV-infected and HIV-uninfected children. Clin Infect Dis 42: 548-558.
69. Smith E, Thybo S, Bennedsen J (1992) Infection with Mycobacterium bovis in a patient with AIDS: a late complication of BCG vaccination. Scand J Infect Dis 24: 109-110.
70. Waddell RD, Lishimpi K, von Reyn CF, Chintu C, Baboo KS, et al. (2001) Bacteremia due to Mycobacterium tuberculosis or M. bovis, Bacille Calmette-Guerin (BCG) among HIV-positive children and adults in Zambia. AIDS 15: 55-60.
71. Jouanguy E, Altare F, Lamhamedi S, Revy P, Emile JF, et al. (1996) Interferon-gamma-receptor deficiency in an infant with fatal bacille Calmette-Guerin infection. N Engl J Med 335: 1956-1961.
72. Sterne JAC, Rodrigues LC, Guedes IN (1998) Does the efficacy of BCG decline with time since vaccination? Int J Tuberc Lung Dis 2: 200-207.
73. Aronson NE, Santosham M, Comstock GW, Howard RS, Moulton LH, et al. (2004) Long-term efficacy of BCG vaccine in American Indians and Alaska natives - A 60-year follow-up study. JAMA 291: 2086-2091.
74. Singh A, Mohan A, Dey AB, Mitra DK (2013) Inhibiting the Programmed Death 1 Pathway Rescues Mycobacterium tuberculosis-Specific Interferon gamma-Producing T Cells From Apoptosis in Patients With Pulmonary Tuberculosis. J Infect Dis 208: 603-615.
75. Bucks CM, Norton JA, Boesteanu AC, Mueller YM, Katsikis PD (2009) Chronic Antigen Stimulation Alone Is Sufficient to Drive CD8(+) T Cell Exhaustion. J Immunol 182: 6697-6708.
76. Han S, Asoyan A, Rabenstein H, Nakano N, Obst R (2010) Role of antigen persistence and dose for CD4(+) T-cell exhaustion and recovery. Proc Natl Acad Sci U S A 107: 20453-20458.
77. Sakai S, Kawamura I, Okazaki T, Tsuchiya K, Uchiyama R, et al. (2010) 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 22: 915-925.
78. Adekambi T, Ibegbu CC, Kalokhe AS, Yu T, Ray SM, et al. (2012) Distinct effector memory CD4+ Tcell signatures in latent Mycobacterium tuberculosis infection, BCG vaccination and clinically resolved tuberculosis. PLoS One 7: e36046.
79. Sable SB (2013) Programmed Death 1 Lives Up to Its Reputation in Active Tuberculosis. J Infect Dis 208: 541-543.
80. Nandakumar S, Kannanganat S, Dobos KM, Lucas M, Spencer JS, et al. (2013) O-mannosylation of the Mycobacterium tuberculosis Adhesin Apa Is Crucial for T Cell Antigenicity during Infection but Is Expendable for Protection. PLoS Pathog 9: e1003705.
81. West EE, Jin HT, Rasheed AU, Penaloza-Macmaster P, Ha SJ, et al. (2013) PD-L1 blockade synergizes with IL-2 therapy in reinvigorating exhausted T cells. J Clin Invest 123: 2604-2615.
82. Lindenstrom T, Knudsen NP, Agger EM, Andersen P (2013) Control of chronic Mycobacterium tuberculosis infection by CD4 KLRG1- IL-2-secreting central memory cells. J Immunol 190: 6311-6319.
83. Sable SB, Verma I, Khuller GK (2005) Multicomponent antituberculous subunit vaccine based on immunodominant antigens of Mycobacterium tuberculosis. Vaccine 23: 4175-4184.
84. Hiraishi Y, Nandakumar S, Choi SO, Lee JW, Kim YC, et al. (2011) Bacillus Calmette-Guerin vaccination using a microneedle patch. Vaccine 29: 2626-2636.
85. Sow FB, Nandakumar S, Velu V, Kellar KL, Schlesinger LS, et al. (2011) Mycobacterium tuberculosis components stimulate production of the antimicrobial peptide hepcidin. Tuberculosis (Edinb) 91: 314-321.
86. Kirman J, McCoy K, Hook S, Prout M, Delahunt B, et al. (1999) CTLA-4 blockade enhances the immune response induced by mycobacterial infection but does not lead to increased protection. Infect Immun 67: 3786-3792.
87. Ito M, Maruyama T, Saito N, Koganei S, Yamamoto K, et al. (2006) Killer cell lectin-like receptor G1 binds three members of the classical cadherin family to inhibit NK cell cytotoxicity. J Exp Med 203: 289-295.
88. Takahashi T, Tagami T, Yamazaki S, Uede T, Shimizu J, et al. (2000) Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyteassociated antigen 4. J Exp Med 192: 303-309.