T cell responses to mycobacterial catalase-peroxidase profile a pathogenic antigen in systemic sarcoidosis

Journal of Immunology

Volumn 181, Issue 12, 2008, Pages 8784-8796

  Chen, Edward S ^a   Wahlström, Jan ^b   Song, Zhimin ^a   Willett, Matthew H ^a   Wikén, Maria ^b   Yung, Rex C ^a   West, Erin E ^a   McDyer, John F ^a   Zhang, Ying ^c   Eklund, Anders ^b   Grunewald, Johan ^b   Moller, David R ^a,d  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; KATG PROTEIN; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; BCG VACCINE; CATALASE; KATG PROTEIN, MYCOBACTERIUM TUBERCULOSIS; TUBERCULIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD; CD4+ T LYMPHOCYTE; FEMALE; HUMAN; HUMAN CELL; LUNG; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SARCOIDOSIS; TH1 CELL; BIOSYNTHESIS; CLINICAL TRIAL; COHORT ANALYSIS; COMPARATIVE STUDY; ENZYMOLOGY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; MIDDLE AGED; MULTICENTER STUDY; MYCOBACTERIUM TUBERCULOSIS; PATHOGENICITY; PATHOLOGY; SWEDEN; UNITED STATES;

ADULT; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BCG VACCINE; CATALASE; CD4-POSITIVE T-LYMPHOCYTES; COHORT STUDIES; FEMALE; HUMANS; INTERFERON-GAMMA; LUNG; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; SARCOIDOSIS; SWEDEN; TH1 CELLS; TUBERCULIN; UNITED STATES;

EID: 58849109438     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.12.8784     Document Type: Article

References (80)

1. Joint Statement of the American Thoracic Society (ATS), the European Respiratory Society (ERS) and the World Association of Sarcoidosis and Other Granulomatous Disorders (WASOG) adopted by the ATS Board of Directors and by the ERS Executive Committee, February 1999. Statement on sarcoidosis. Am. J. Respir. Crit. Care Med. 160: 736-755.
2. Grunewald, J., and A. Eklund. 2007. Sex-specific manifestations of Lofgren's syndrome. Am. J. Respir. Crit. Care Med. 175: 40-44.
3. Rybicki, B. A., and M. C. Iannuzzi. 2007. Epidemiology of sarcoidosis: recent advances and future prospects. Semin. Respir. Crit. Care Med. 28: 22-35. (Pubitemid 46371213)
4. Baughman, R. P., A. S. Teirstein, M. A. Judson, M. D. Rossman, H. Yeager, Jr., E. A. Bresnitz, L. DePalo, G. Hunninghake, M. C. Iannuzzi, C. J. Johns, et al. 2001. Clinical characteristics of patients in a case control study of sarcoidosis. Am. J. Respir. Crit. Care Med. 164: 1885-1889. (Pubitemid 33152325)
5. Zissel, G., A. Prasse, and J. Muller-Quernheim. 2007. Sarcoidosis: immunopathogenetic concepts. Semin. Respir. Crit. Care Med. 28: 3-14.
6. Hunninghake, G. W., and R. G. Crystal. 1981. Pulmonary sarcoidosis: a disorder mediated by excess helper T-lymphocyte activity at sites of disease activity. N. Engl. J. Med. 305: 429-434.
7. Robinson, B. W., T. L. McLemore, and R. G. Crystal. 1985. γ interferon is spontaneously released by alveolar macrophages and lung T lymphocytes in patients with pulmonary sarcoidosis. J. Clin. Invest. 75: 1488-1495.
8. Moller, D. R., J. D. Forman, M. C. Liu, P. W. Noble, B. M. Greenlee, P. Vyas, D. A. Holden, J. M. Forrester, A. Lazarus, M. Wysocka, et al. 1996. Enhanced expression of IL-12 associated with Th1 cytokine profiles in active pulmonary sarcoidosis. J. Immunol. 156: 4952-4960.
9. Rogge, L., A. Papi, D. H. Presky, M. Biffi, L. J. Minetti, D. Miotto, C. Agostini, G. Semenzato, L. M. Fabbri, and F. Sinigaglia. 1999. Antibodies to the IL-12 receptor β 2 chain mark human Th1 but not Th2 cells in vitro and in vivo. J. Immunol. 162: 3926-3932. (Pubitemid 29314771)
10. +T lymphocyte activation in sarcoidosis. J. Immunol. 165: 4718-4724.
11. Katchar, K., A. Eklund, and J. Grunewald. 2003. Expression of Th1 markers by lung accumulated T cells in pulmonary sarcoidosis. J. Intern. Med. 254: 564-571.
12. Chiu, B. C., C. M. Freeman, V. R. Stolberg, E. Komuniecki, P. M. Lincoln, S. L. Kunkel, and S. W. Chensue. 2003. Cytokine-chemokine networks in experimental mycobacterial and schistosomal pulmonary granuloma formation. Am. J. Respir. Cell Mol. Biol. 29: 106-116.
13. Nakajima, M., Y. Kubota, N. Miyashita, Y. Niki, T. Matsushima, and T. Manabe. 1996. Recurrence of sarcoidosis following interferon α therapy for chronic hepatitis C. Intern. Med. 35: 376-379.
14. Naccache, J. M., M. Antoine, M. Wislez, J. Fleury-Feith, E. Oksenhendler, C. Mayaud, and J. Cadranel. 1999. Sarcoid-like pulmonary disorder in human immunodeficiency virus-infected patients receiving antiretroviral therapy. Am. J. Respir. Crit. Care Med. 159: 2009-2013.
15. Chen, E. S., and D. R. Moller. 2008. Etiology of sarcoidosis. Clin. Chest Med. 29: 365-377.
16. Moller, D. R. 1998. Involvement of T cells and alterations in T cell receptors in sarcoidosis. Semin. Respir. Infect. 13: 174-183. (Pubitemid 28440836)
17. Moller, D. R., K. Konishi, M. Kirby, B. Balbi, and R. G. Crystal. 1988. Bias toward use of a specific T cell receptor β-chain variable region in a subgroup of individuals with sarcoidosis. J. Clin. Invest. 82: 1183-1191.
18. +T lymphocytes in bronchoalveolar lavage fluid from sarcoidosis patients correlates with HLA-DR3. Eur. J. Immunol. 22: 129-135.
19. Forrester, J. M., Y. Wang, N. Ricalton, J. E. Fitzgerald, J. Loveless, L. S. Newman, T. E. King, and B. L. Kotzin. 1994. TCR expression of activated T cell clones in the lungs of patients with pulmonary sarcoidosis. J. Immunol. 153: 4291-4302.
20. +sarcoidosis patients. Mol. Med. 1: 287-296.
21. Silver, R. F., R. G. Crystal, and D. R. Moller. 1996. Limited heterogeneity of biased T-cell receptor Vβ gene usage in lung but not blood T cells in active pulmonary sarcoidosis. Immunology 88: 516-523.
22. Song, Z., L. Marzilli, B. M. Greenlee, E. S. Chen, R. F. Silver, F. B. Askin, A. S. Teirstein, Y. Zhang, R. J. Cotter, and D. R. Moller. 2005. Mycobacterial catalase-peroxidase is a tissue antigen and target of the adaptive immune response in systemic sarcoidosis. J. Exp. Med. 201: 755-767.
23. Gupta, D., R. Agarwal, A. N. Aggarwal, and S. K. Jindal. 2007. Molecular evidence for the role of mycobacteria in sarcoidosis: a meta-analysis. Eur. Respir. J. 30: 508-516. (Pubitemid 351182075)
24. Hance, A. J. 1998. The role of mycobacteria in the pathogenesis of sarcoidosis. Semin. Respir. Infect. 13: 197-205.
25. Drake, W. P., M. S. Dhason, M. Nadaf, B. E. Shepherd, S. Vadivelu, R. Hajizadeh, L. S. Newman, and S. A. Kalams. 2007. Cellular recognition of Mycobacterium tuberculosis ESAT-6 and KatG peptides in systemic sarcoidosis. Infect. Immun. 75: 527-530.
26. Hajizadeh, R., H. Sato, J. Carlisle, M. T. Nadaf, W. Evans, B. E. Shepherd, R. F. Miller, S. A. Kalams, and W. P. Drake. 2007. Mycobacterium tuberculosis Antigen 85A induces Th-1 immune responses in systemic sarcoidosis. J. Clin. Immunol. 27: 445-454. (Pubitemid 46906652)
27. Dubaniewicz, A., P. Trzonkowski, M. Dubaniewicz-Wybieralska, M. Singh, and A. Mysliwski. 2007. Mycobacterial heat shock protein-induced blood T lymphocytes subsets and cytokine pattern: comparison of sarcoidosis with tuberculosis and healthy controls. Respirology 12: 346-354.
28. 1994. Consensus conference: activity of sarcoidosis. Third WASOG meeting, Los Angeles, USA, September 8-11, 1993. Eur. Respir. J. 7: 624-627.
29. 2000. Targeted tuberculin testing and treatment of latent tuberculosis infection. American Thoracic Society. MMWR Recomm. Rep. 49: 1-51.
30. Idali, F., M. Wiken, J. Wahlstrom, H. Mellstedt, A. Eklund, H. Rabbani, and J. Grunewald. 2006. Reduced Th1 response in the lungs of HLA-DRB1*0301 patients with pulmonary sarcoidosis. Eur. Respir. J. 27: 451-459.
31. Zhang, Y., B. Heym, B. Allen, D. Young, and S. Cole. 1992. The catalaseperoxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature 358: 591-593.
32. Johnsson, K., W. A. Froland, and P. G. Schultz. 1997. Overexpression, purifi- cation, and characterization of the catalase-peroxidase KatG from Mycobacterium tuberculosis. J. Biol. Chem. 272: 2834-2840. (Pubitemid 27053330)
33. + T cells in bronchoalveolar lavage fluid and peripheral blood of sarcoidosis patients. Proc. Natl. Acad. Sci. USA 91: 4965-4969.
34. Forman, J. D., J. T. Klein, R. F. Silver, M. C. Liu, B. M. Greenlee, and D. R. Moller. 1994. Selective activation and accumulation of oligoclonal Vβ-specific T cells in active pulmonary sarcoidosis. J. Clin. Invest. 94: 1533-1542.
35. Eklund, A., and E. Blaschke. 1986. Relationship between changed alveolar-capillary permeability and angiotensin converting enzyme activity in serum in sarcoidosis. Thorax 41: 629-634. (Pubitemid 16039655)
36. Lalvani, A., A. A. Pathan, H. Durkan, K. A. Wilkinson, A. Whelan, J. J. Deeks, W. H. Reece, M. Latif, G. Pasvol, and A. V. Hill. 2001. Enhanced contact tracing and spatial tracking of Mycobacterium tuberculosis infection by enumeration of antigen-specific T cells. Lancet 357: 2017-2021. (Pubitemid 32592390)
37. Shlobin, O. A., E. E. West, N. Lechtzin, S. M. Miller, M. Borja, J. B. Orens, L. K. Dropulic, and J. F. McDyer. 2006. Persistent cytomegalovirus- specific memory responses in the lung allograft and blood following primary infection in lung transplant recipients. J. Immunol. 176: 2625-2634.
38. Holmes, K. L., G. Otten, and W. M. Yokoyama. 2002. Flow cytometry analysis using the Becton Dickinson FACS Calibur. In Current Protocols in Immunology. J. E. Coligan, B. E. Bierer, D. H. Margulies, E. M. Shevach, and W. Strober, eds. John Wiley & Sons, Inc., Hoboken, NJ. 5.4.1-5.4.22.
39. Lecossier, D., D. Valeyre, A. Loiseau, J. Cadranel, A. Tazi, J. P. Battesti, and A. J. Hance. 1991. Antigen-induced proliferative response of lavage and blood T lymphocytes: comparison of cells from normal subjects and patients with sarcoidosis. Am. Rev. Respir. Dis. 144: 861-868.
40. Dominique, S., F. Bouchonnet, J. M. Smiejan, and A. J. Hance. 1990. Expression of surface antigens distinguishing "naive" and previously activated lymphocytes in bronchoalveolar lavage fluid. Thorax 45: 391-396. (Pubitemid 20184899)
41. Grunewald, J., M. Berlin, O. Olerup, and A. Eklund. 2000. Lung T-helper cells expressing T-cell receptor AV2S3 associate with clinical features of pulmonary sarcoidosis. Am. J. Respir. Crit. Care Med. 161: 814-818. (Pubitemid 30171736)
42. Nishino, K., H. Yoshida, O. Yoshida, M. Watanabe, A. Fukushima, and H. Ueno. 2000. Analysis of responses of peripheral blood lymphocytes from sarcoidosis patients to purified protein derivative. Jpn. J. Ophthalmol. 44: 165-170. (Pubitemid 30133201)
43. Mustafa, A. S., H. A. Amoudy, H. G. Wiker, A. T. Abal, P. Ravn, F. Oftung, and P. Andersen. 1998. Comparison of antigen-specific T-cell responses of tuberculosis patients using complex or single antigens of Mycobacterium tuberculosis. Scand. J. Immunol. 48: 535-543.
44. Bergeron, A., M. Bonay, M. Kambouchner, D. Lecossier, M. Riquet, P. Soler, A. Hance, and A. Tazi. 1997. Cytokine patterns in tuberculous and sarcoid granulomas: correlations with histopathologic features of the granulomatous response. J. Immunol. 159: 3034-3043.
45. Zhang, Y., and D. Young. 1994. Strain variation in the katG region of Mycobacterium tuberculosis. Mol. Microbiol. 14: 301-308. (Pubitemid 24325807)
46. Mackay, I. R., N. V. Leskovsek, and N. R. Rose. 2008. Cell damage and autoimmunity: a critical appraisal. J. Autoimmun. 30: 5-11.
47. Silver, R. F., L. Zukowski, S. Kotake, Q. Li, F. Pozuelo, A. Krywiak, and R. Larkin. 2003. Recruitment of antigen-specific Th1-like responses to the human lung following bronchoscopic segmental challenge with purified protein derivative of Mycobacterium tuberculosis. Am. J. Respir. Cell Mol. Biol. 29: 117-123.
48. Palendira, U., A. G. Bean, C. G. Feng, and W. J. Britton. 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.
49. Rose, N. R. 1998. The role of infection in the pathogenesis of autoimmune disease. Semin. Immunol. 10: 5-13. (Pubitemid 28108126)
50. Pathan, A. A., K. A. Wilkinson, P. Klenerman, H. McShane, R. N. Davidson, G. Pasvol, A. V. Hill, and A. Lalvani. 2001. Direct ex vivo analysis of antigenspecific IFN-γ-secreting CD4 T cells in Mycobacterium tuberculosis-infected individuals: associations with clinical disease state and effect of treatment. J. Immunol. 167: 5217-5225.
51. Flanagan, K. L., E. A. Lee, M. B. Gravenor, W. H. Reece, B. C. Urban, T. Doherty, K. A. Bojang, M. Pinder, A. V. Hill, and M. Plebanski. 2001. Unique T cell effector functions elicited by Plasmodium falciparum epitopes in malariaexposed Africans tested by three T cell assays. J. Immunol. 167: 4729-4737.
52. + T cells after clearance of hepatitis C virus. J. Immunol. 169: 2210-2214.
53. Lanzavecchia, A., and F. Sallusto. 2005. Understanding the generation and function of memory T cell subsets. Curr. Opin. Immunol. 17: 326-332. (Pubitemid 40692670)
54. Fazel, S. B., S. E. Howie, A. S. Krajewski, and D. Lamb. 1994. Increased CD45RO expression on T lymphocytes in mediastinal lymph node and pulmonary lesions of patients with pulmonary sarcoidosis. Clin. Exp. Immunol. 95: 509-513.
55. + T cells in blood determines proliferative response. J. Clin. Invest. 115: 2886-2893.
56. Modlin, R. L., F. M. Hofman, P. R. Meyer, O. P. Sharma, C. R. Taylor, and T. H. Rea. 1983. In situ demonstration of T lymphocyte subsets in granulomatous inflammation: leprosy, rhinoscleroma and sarcoidosis. Clin. Exp. Immunol. 51: 430-438.
57. Gonzalez-Juarrero, M., O. C. Turner, J. Turner, P. Marietta, J. V. Brooks, and I. M. Orme. 2001. Temporal and spatial arrangement of lymphocytes within lung granulomas induced by aerosol infection with Mycobacterium tuberculosis. Infect. Immun. 69: 1722-1728.
58. Orme, I. M. 1987. The kinetics of emergence and loss of mediator T lymphocytes acquired in response to infection with Mycobacterium tuberculosis. J. Immunol. 138: 293-298.
59. + T cells. Infect. Immun. 55: 2037-2041.
60. + cytotoxic T cells and relative resistance of alveolar macrophages to lysis. J. Immunol. 159: 290-297.
61. +-T-cell epitopes from antigen 85A. Infect. Immun. 70: 1623-1626.
62. + T cells in patients with chronic beryllium disease. J. Clin. Invest. 110: 1473-1482.
63. Saunders, B. M., and A. M. Cooper. 2000. Restraining mycobacteria: role of granulomas in mycobacterial infections. Immunol. Cell Biol. 78: 334-341.
64. Staton, J. M., J. E. Dench, B. Currie, D. R. Fitzpatrick, R. P. Himbeck, R. Allen, J. Bruce, B. W. Robinson, and H. Bielefeldt-Ohmann. 1995. Expression and immune recognition of stress proteins in sarcoidosis and other chronic interstitial lung diseases. Immunol. Cell Biol. 73: 23-32.
65. Cosma, C. L., O. Humbert, and L. Ramakrishnan. 2004. Superinfecting mycobacteria home to established tuberculous granulomas. Nat. Immunol. 5: 828-835.
66. Jamieson, B. D., and R. Ahmed. 1989. T cell memory. Long-term persistence of virus-specific cytotoxic T cells. J. Exp. Med. 169: 1993-2005.
67. Swain, S. L. 2000. CD4 T-cell memory can persist in the absence of class II. Philos. Trans. R. Soc. London B 355: 407-411.
68. Zhu, Y., G. Zhu, L. Luo, A. S. Flies, and L. Chen. 2007. CD137 stimulation delivers an antigen-independent growth signal for T lymphocytes with memory phenotype. Blood 109: 4882-4889. (Pubitemid 46827785)
69. Iannuzzi, M. C. 2007. Genetics of sarcoidosis. Semin. Respir. Crit. Care Med. 28: 15-21.
70. Khomenko, A. G., V. I. Litvinov, V. P. Chukanova, and L. E. Pospelov. 1990. Tuberculosis in patients with various HLA phenotypes. Tubercle 71: 187-192. (Pubitemid 20287008)
71. + individuals upon stimulation with Mycobacterium tuberculosis. Infect. Immun. 67: 3800-3809.
72. Wahlstrom, J., J. Dengjel, B. Persson, H. Duyar, H. G. Rammensee, S. Stevanovic, A. Eklund, R. Weissert, and J. Grunewald. 2007. Identification of HLA-DR-bound peptides presented by human bronchoalveolar lavage cells in sarcoidosis. J. Clin. Invest. 117: 3576-3582.
73. Ziegenhagen, M. W., U. K. Benner, G. Zissel, P. Zabel, M. Schlaak, and J. Muller-Quernheim. 1997. Sarcoidosis: TNF-α release from alveolar macrophages and serum level of sIL-2R are prognostic markers. Am. J. Respir. Crit. Care Med. 156: 1586-1592.
74. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol. 6: 1123-1132.
75. Bettelli, E., T. Korn, M. Oukka, and V. K. Kuchroo. 2008. Induction and effector functions of TH17 cells. Nature 453: 1051-1057. (Pubitemid 351871737)
76. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, and M. Toda. 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155: 1151-1164.
77. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389: 737-742.
78. Zhang, Z. X., L. Yang, K. J. Young, B. DuTemple, and L. Zhang. 2000. Identification of a previously unknown antigen-specific regulatory T cell and its mechanism of suppression. Nat. Med. 6: 782-789.
79. Miyara, M., Z. Amoura, C. Parizot, C. Badoual, K. Dorgham, S. Trad, M. Kambouchner, D. Valeyre, C. Chapelon-Abric, P. Debre, et al. 2006. The immune paradox of sarcoidosis and regulatory T cells. J. Exp. Med. 203: 359-370.
80. Idali, F., J. Wahlstrom, C. Muller-Suur, A. Eklund, and J. Grunewald. 2008. Analysis of regulatory T cell associated forkhead box P3 expression in the lungs of patients with sarcoidosis. Clin. Exp. Immunol. 152: 127-137. (Pubitemid 351347561)