How tumour necrosis factor blockers interfere with tuberculosis immunity

Clinical and Experimental Immunology

Volumn 161, Issue 1, 2010, Pages 1-9

  Harris, J ^a   Keane, J ^b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ST JAMES S HOSPITAL   (Ireland)

Author keywords

Adalimumab; Certolizumab; Etanercept; Golimumab; Infliximab; Mycobacteria

Indexed keywords

ADALIMUMAB; CERTOLIZUMAB PEGOL; ETANERCEPT; GAMMA INTERFERON; GOLIMUMAB; INFLIXIMAB; INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR INHIBITOR;

ADVERSE OUTCOME; ANKYLOSING SPONDYLITIS; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; APOPTOSIS; AUTOPHAGY; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELL MATURATION; CELLULAR IMMUNITY; CLINICAL TRIAL; COMPLEMENT DEPENDENT CYTOTOXICITY; CROHN DISEASE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DRUG EFFECT; DRUG PROTEIN BINDING; DRUG SAFETY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOCOMPETENT CELL; INFLAMMATORY DISEASE; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MEMORY T LYMPHOCYTE; MOLECULAR MECHANICS; MONOCYTE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOSOME; PHENOTYPE; POSTPRIMARY TUBERCULOSIS; PRIORITY JOURNAL; PSORIASIS; PSORIATIC ARTHRITIS; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TUBERCULOSIS; ULCERATIVE COLITIS;

ANIMALS; ANTIBODIES, MONOCLONAL; APOPTOSIS; AUTOIMMUNE DISEASES; AUTOPHAGY; DENDRITIC CELLS; DISEASE SUSCEPTIBILITY; HUMANS; IMMUNITY, CELLULAR; IMMUNOGLOBULIN G; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATION; LYMPHOCYTE ACTIVATION; MACROPHAGE ACTIVATION; MICE; MYCOBACTERIUM TUBERCULOSIS; PHAGOSOMES; RECEPTORS, TUMOR NECROSIS FACTOR; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77953274576     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2010.04146.x     Document Type: Review

References (87)

1. Black RA, Rauch CT, Kozlosky CJ et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 1997 385 : 729 733.
2. Wajant H, Pfizenmaier K, Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 2003 10 : 45 65.
3. Grell M, Douni E, Wajant H et al. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 1995 83 : 793 802.
4. Keane J, Gershon S, Wise RP et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med 2001 345 : 1098 1104.
5. Nunez Martinez O, Ripoll Noiseux C, Carneros Martin JA, Gonzalez Lara V, Gregorio Maranon HG. Reactivation tuberculosis in a patient with anti-TNF-alpha treatment. Am J Gastroenterol 2001 96 : 1665 1666.
6. Flynn JL, Goldstein MM, Chan J et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 1995 2 : 561 572.
7. Champsi J, Young LS, Bermudez LE. Production of TNF-alpha, IL-6 and TGF-beta, and expression of receptors for TNF-alpha and IL-6, during murine Mycobacterium avium infection. Immunology 1995 84 : 549 554.
8. Bean AG, Roach DR, Briscoe H et al. Structural deficiencies in granuloma formation in TNF gene-targeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin. J Immunol 1999 162 : 3504 3511.
9. Senaldi G, Yin S, Shaklee CL, Piguet PF, Mak TW, Ulich TR. Corynebacterium parvum- and Mycobacterium bovis bacillus Calmette-Guerin-induced granuloma formation is inhibited in TNF receptor I (TNF-RI) knockout mice and by treatment with soluble TNF-RI. J Immunol 1996 157 : 5022 5026.
10. Olleros ML, Guler R, Corazza N et al. Transmembrane TNF induces an efficient cell-mediated immunity and resistance to Mycobacterium bovis bacillus Calmette-Guerin infection in the absence of secreted TNF and lymphotoxin-alpha. J Immunol 2002 168 : 3394 3401.
11. Olleros ML, Guler R, Vesin D et al. Contribution of transmembrane tumor necrosis factor to host defense against Mycobacterium bovis bacillus Calmette-Guerin and Mycobacterium tuberculosis infections. Am J Pathol 2005 166 : 1109 1120.
12. Roach DR, Bean AG, Demangel C, France MP, Briscoe H, Britton WJ. TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection. J Immunol 2002 168 : 4620 4627.
13. Lopez Ramirez GM, Rom WN, Ciotoli C et al. Mycobacterium tuberculosis alters expression of adhesion molecules on monocytic cells. Infect Immun 1994 62 : 2515 2520.
14. Keane J, Balcewicz-Sablinska MK, Remold HG et al. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 1997 65 : 298 304.
15. Agnholt J, Kaltoft K. Infliximab downregulates interferon-gamma production in activated gut T-lymphocytes from patients with Crohn's disease. Cytokine 2001 15 : 212 222.
16. Baeten D, Van Damme N, Van den Bosch F et al. Impaired Th1 cytokine production in spondyloarthropathy is restored by anti-TNFalpha. Ann Rheum Dis 2001 60 : 750 755.
17. Agnholt J, Dahlerup JF, Kaltoft K. The effect of etanercept and infliximab on the production of tumour necrosis factor alpha, interferon-gamma and GM-CSF in in vivo activated intestinal T lymphocyte cultures. Cytokine 2003 23 : 76 85.
18. Netea MG, Radstake T, Joosten LA, van der Meer JW, Barrera P, Kullberg BJ. Salmonella septicemia in rheumatoid arthritis patients receiving anti-tumor necrosis factor therapy: Association with decreased interferon-gamma production and Toll-like receptor 4 expression. Arthritis Rheum 2003 48 : 1853 1857.
19. Popa C, Barrera P, Joosten LA et al. Cytokine production from stimulated whole blood cultures in rheumatoid arthritis patients treated with various TNF blocking agents. Eur Cytokine Netw 2009 20 : 88 93.
20. Lugering A, Schmidt M, Lugering N, Pauels HG, Domschke W, Kucharzik T. Infliximab induces apoptosis in monocytes from patients with chronic active Crohn's disease by using a caspase-dependent pathway. Gastroenterology 2001 121 : 1145 1157.
21. van den Brande J, Hommes DW, Peppelenbosch MP. Infliximab induced T lymphocyte apoptosis in Crohn's disease. J Rheumatol Suppl 2005 74 : 26 30.
22. Bruns H, Meinken C, Schauenberg P et al. Anti-TNF immunotherapy reduces CD8+ T cell-mediated antimicrobial activity against Mycobacterium tuberculosis in humans. J Clin Invest 2009 119 : 1167 1177.
23. Nadkarni S, Mauri C, Ehrenstein MR. Anti-TNF-alpha therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-beta. J Exp Med 2007 204 : 33 9.
24. Ehrenstein MR, Evans JG, Singh A et al. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med 2004 200 : 277 285.
25. Scott-Browne JP, Shafiani S, Tucker-Heard G et al. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J Exp Med 2007 204 : 2159 2169.
26. Wallis RS. Tumour necrosis factor antagonists: Structure, function, and tuberculosis risks. Lancet Infect Dis 2008 8 : 601 611.
27. Scallon B, Cai A, Solowski N et al. Binding and functional comparisons of two types of tumor necrosis factor antagonists. J Pharmacol Exp Ther 2002 301 : 418 426.
28. Tubach F, Salmon D, Ravaud P et al. Risk of tuberculosis is higher with anti-tumor necrosis factor monoclonal antibody therapy than with soluble tumor necrosis factor receptor therapy: The three-year prospective French Research Axed on Tolerance of Biotherapies registry. Arthritis Rheum 2009 60 : 1884 1894.
29. Keystone E, Heijde D, Mason D et al. Certolizumab pegol plus methotrexate is significantly more effective than placebo plus methotrexate in active rheumatoid arthritis: findings of a fifty-two-week, phase III, multicenter, randomized, double-blind, placebo-controlled, parallel-group study. Arthritis Rheum 2008 58 : 3319 3329.
30. Smolen J, Landewe RB, Mease P et al. Efficacy and safety of certolizumab pegol plus methotrexate in active rheumatoid arthritis: The RAPID 2 study. A randomised controlled trial. Ann Rheum Dis 2009 68 : 797 804.
31. Wallis RS, Broder MS, Wong JY, Hanson ME, Beenhouwer DO. Granulomatous infectious diseases associated with tumor necrosis factor antagonists. Clin Infect Dis 2004 38 : 1261 1265.
32. Tufariello JM, Chan J, Flynn JL. Latent tuberculosis: mechanisms of host and bacillus that contribute to persistent infection. Lancet Infect Dis 2003 3 : 578 590.
33. Ray JC, Flynn JL, Kirschner DE. Synergy between individual TNF-dependent functions determines granuloma performance for controlling Mycobacterium tuberculosis infection. J Immunol 2009 182 : 3706 3717.
34. Chakravarty SD, Zhu G, Tsai MC et al. Tumor necrosis factor blockade in chronic murine tuberculosis enhances granulomatous inflammation and disorganizes granulomas in the lungs. Infect Immun 2008 76 : 916 926.
35. Mohan VP, Scanga CA, Yu K et al. Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: Possible role for limiting pathology. Infect Immun 2001 69 : 1847 1855.
36. Lawn SD, Butera ST, Shinnick TM. Tuberculosis unleashed: The impact of human immunodeficiency virus infection on the host granulomatous response to Mycobacterium tuberculosis. Microbes Infect 2002 4 : 635 646.
37. Rohde K, Yates RM, Purdy GE, Russell DG. Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 2007 219 : 37 54.
38. Deretic V, Singh S, Master S et al. Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell Microbiol 2006 8 : 719 727.
39. Kang PB, Azad AK, Torrelles JB et al. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 2005 202 : 987 999.
40. 2+/calmodulin-PI3K hVPS34 cascade. J Exp Med 2003 198 : 653 659.
41. Vergne I, Chua J, Deretic V. Mycobacterium tuberculosis phagosome maturation arrest: Selective targeting of PI3P-dependent membrane trafficking. Traffic 2003 4 : 600 606.
42. Vergne I, Fratti RA, Hill PJ, Chua J, Belisle J, Deretic V. Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol Biol Cell 2004 15 : 751 760.
43. Vergne I, Chua J, Lee HH, Lucas M, Belisle J, Deretic V. Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis. Proc Natl Acad Sci USA 2005 102 : 4033 4038.
44. Schaible UE, Sturgill-Koszycki S, Schlesinger PH, Russell DG. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J Immunol 1998 160 : 1290 1296.
45. Via LE, Fratti RA, McFalone M, Pagan-Ramos E, Deretic D, Deretic V. Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 1998 111 : 897 905.
46. Harris J, Hope JC, Keane J. Tumor necrosis factor blockers influence macrophage responses to Mycobacterium tuberculosis. J Infect Dis 2008 198 : 1842 1850.
47. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004 119 : 753 766.
48. Harris J, De Haro SA, Master SS et al. T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity 2007 27 : 505 517.
49. Singh SB, Davis AS, Taylor GA, Deretic V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 2006 313 : 1438 1441.
50. Kuma A, Hatano M, Matsui M et al. The role of autophagy during the early neonatal starvation period. Nature 2004 432 : 1032 1036.
51. Shintani T, Klionsky DJ. Autophagy in health and disease: A double-edged sword. Science 2004 306 : 990 995.
52. Andrade RM, Wessendarp M, Gubbels MJ, Striepen B, Subauste CS. CD40 induces macrophage anti-Toxoplasma gondii activity by triggering autophagy-dependent fusion of pathogen-containing vacuoles and lysosomes. J Clin Invest 2006 116 : 2366 2377.
53. Djavaheri-Mergny M, Amelotti M, Mathieu J et al. NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J Biol Chem 2006 281 : 30373 30382.
54. Jia G, Cheng G, Gangahar DM, Agrawal DK. Insulin-like growth factor-1 and TNF-alpha regulate autophagy through c-jun N-terminal kinase and Akt pathways in human atherosclerotic vascular smooth cells. Immunol Cell Biol 2006 84 : 448 454.
55. Jia L, Dourmashkin RR, Allen PD, Gray AB, Newland AC, Kelsey SM. Inhibition of autophagy abrogates tumour necrosis factor alpha induced apoptosis in human T-lymphoblastic leukaemic cells. Br J Haematol 1997 98 : 673 685.
56. Ling YM, Shaw MH, Ayala C et al. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med 2006 203 : 2063 2071.
57. Sivaprasad U, Basu A. Inhibition of ERK attenuates autophagy and potentiates tumour necrosis factor-alpha-induced cell death in MCF-7 cells. J Cell Mol Med 2008 12 : 1265 1271.
58. Harris J, Hope JC, Lavelle EC. Autophagy and the immune response to TB. Transbound Emerg Dis 2009 56 : 248 254.
59. Keane J, Remold HG, Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 2000 164 : 2016 2020.
60. Leemans JC, Juffermans NP, Florquin S et al. Depletion of alveolar macrophages exerts protective effects in pulmonary tuberculosis in mice. J Immunol 2001 166 : 4604 4611.
61. Keane J, Shurtleff B, Kornfeld H. TNF-dependent BALB/c murine macrophage apoptosis following Mycobacterium tuberculosis infection inhibits bacillary growth in an IFN-gamma independent manner. Tuberculosis (Edinb) 2002 82 : 55 61.
62. Laochumroonvorapong P, Paul S, Elkon KB, Kaplan G. H2O2 induces monocyte apoptosis and reduces viability of Mycobacterium avium-M. intracellulare within cultured human monocytes. Infect Immun 1996 64 : 452 459.
63. Schaible UE, Winau F, Sieling PA et al. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 2003 9 : 1039 1046.
64. Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol 1998 161 : 2636 2641.
65. ten Hove T, van Montfrans C, Peppelenbosch MP, van Deventer SJ. Infliximab treatment induces apoptosis of lamina propria T lymphocytes in Crohn's disease. Gut 2002 50 : 206 211.
66. Di Sabatino A, Ciccocioppo R, Cinque B et al. Defective mucosal T cell death is sustainably reverted by infliximab in a caspase dependent pathway in Crohn's disease. Gut 2004 53 : 70 7.
67. Saliu OY, Sofer C, Stein DS, Schwander SK, Wallis RS. Tumor-necrosis-factor blockers: differential effects on mycobacterial immunity. J Infect Dis 2006 194 : 486 492.
68. Stegelmann F, Bastian M, Swoboda K et al. Coordinate expression of CC chemokine ligand 5, granulysin, and perforin in CD8(+) T cells provides a host defense mechanism against Mycobacterium tuberculosis. J Immunol 2005 175 : 7474 7483.
69. Stenger S, Hanson DA, Teitelbaum R et al. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 1998 282 : 121 125. (Pubitemid 28471143)
70. Mitoma H, Horiuchi T, Hatta N et al. Infliximab induces potent anti-inflammatory responses by outside-to-inside signals through transmembrane TNF-alpha. Gastroenterology 2005 128 : 376 392.
71. Mitoma H, Horiuchi T, Tsukamoto H et al. Mechanisms for cytotoxic effects of anti-tumor necrosis factor agents on transmembrane tumor necrosis factor alpha-expressing cells: comparison among infliximab, etanercept, and adalimumab. Arthritis Rheum 2008 58 : 1248 1257.
72. Malaviya R, Sun Y, Tan JK et al. Etanercept induces apoptosis of dermal dendritic cells in psoriatic plaques of responding patients. J Am Acad Dermatol 2006 55 : 590 597.
73. Shen C, Assche GV, Colpaert S et al. Adalimumab induces apoptosis of human monocytes: A comparative study with infliximab and etanercept. Aliment Pharmacol Ther 2005 21 : 251 258.
74. Shen C, Maerten P, Geboes K, Van Assche G, Rutgeerts P, Ceuppens JL. Infliximab induces apoptosis of monocytes and T lymphocytes in a human-mouse chimeric model. Clin Immunol 2005 115 : 250 259.
75. Shen C, Van Assche G, Rutgeerts P, Ceuppens JL. Caspase activation and apoptosis induction by adalimumab: demonstration in vitro and in vivo in a chimeric mouse model. Inflamm Bowel Dis 2006 12 : 22 8.
76. Salgame P. Host innate and Th1 responses and the bacterial factors that control Mycobacterium tuberculosis infection. Curr Opin Immunol 2005 17 : 374 380.
77. Haider AS, Cardinale IR, Whynot JA, Krueger JG. Effects of etanercept are distinct from infliximab in modulating proinflammatory genes in activated human leukocytes. J Invest Dermatol Symp Proc 2007 12 : 9 15.
78. Hamdi H, Mariette X, Godot V et al. Inhibition of anti-tuberculosis T-lymphocyte function with tumour necrosis factor antagonists. Arthritis Res Ther 2006 8 : R114.
79. Kawashima M, Miossec P. Effect of treatment of rheumatoid arthritis with infliximab on IFN gamma, IL4, T-bet, and GATA-3 expression: link with improvement of systemic inflammation and disease activity. Ann Rheum Dis 2005 64 : 415 418.
80. Nissinen R, Leirisalo-Repo M, Peltomaa R, Palosuo T, Vaarala O. Cytokine and chemokine receptor profile of peripheral blood mononuclear cells during treatment with infliximab in patients with active rheumatoid arthritis. Ann Rheum Dis 2004 63 : 681 687.
81. Dieli F, Troye-Blomberg M, Ivanyi J et al. Vgamma9/Vdelta2 T lymphocytes reduce the viability of intracellular Mycobacterium tuberculosis. Eur J Immunol 2000 30 : 1512 1519.
82. Tastan Y, Arvas A, Demir G, Alikasifoglu M, Gur E, Kiray E. Influence of bacillus Calmette-Guerin vaccination at birth and 2 months of age on the peripheral blood T-cell subpopulations [gamma/delta and alpha-beta T cell]. Pediatr Allergy Immunol 2005 16 : 624 629.
83. Giardina AR, Accardo-Palumbo A, Ciccia F et al. Blocking TNF in vitro with infliximab determines the inhibition of expansion and interferon gamma production of Vgamma9/Vdelta2 T lymphocytes from patients with active rheumatoid arthritis. A role in the susceptibility to tuberculosis? Reumatismo 2009 61 : 21 6.
84. Chen X, Zhou B, Li M et al. CD4(+)CD25(+)FoxP3(+) regulatory T cells suppress Mycobacterium tuberculosis immunity in patients with active disease. Clin Immunol 2007 123 : 50 9.
85. Guyot-Revol V, Innes JA, Hackforth S, Hinks T, Lalvani A. Regulatory T cells are expanded in blood and disease sites in patients with tuberculosis. Am J Respir Crit Care Med 2006 173 : 803 810.
86. Ribeiro-Rodrigues R, Resende Co T, Rojas R et al. A role for CD4+CD25+ T cells in regulation of the immune response during human tuberculosis. Clin Exp Immunol 2006 144 : 25 34.
87. Harris J, Hanrahan O, De Haro SA. Measuring autophagy in macrophages. Curr Protoc Immunol 2009 chapter 14: unit 14.