LAG3 expression in active mycobacterium tuberculosis infections

American Journal of Pathology

Volumn 185, Issue 3, 2015, Pages 820-833

  Phillips, Bonnie L ^a,b,c   Mehra, Smriti ^a   Ahsan, Muhammad H ^a,d   Selman, Moises ^c   Khader, Shabaana A ^e   Kaushal, Deepak ^a,f  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b Biomedical Sciences Graduate Stud Program   (United States)

^c INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

^d Training in Lung Molecular and Cell Pathobiology Program   (United States)

^e WASHINGTON UNIVERSITY   (United States)

^f TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; CELL PROTEIN; GRANZYME B; INTERLEUKIN 10; LYMPHOCYTE ACTIVATION GENE 3; RNA; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; CD223 ANTIGEN; LEUKOCYTE ANTIGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; GRANULOMATOUS INFLAMMATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG GRANULOMA; LUNG TUBERCULOSIS; MALE; MYCOBACTERIUM TUBERCULOSIS; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIMATE MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; SURVIVAL; T LYMPHOCYTE; UPREGULATION; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; LATENT TUBERCULOSIS; LUNG; METABOLISM; PATHOLOGY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TUBERCULOSIS;

ANIMALS; ANTIGENS, CD; GENE EXPRESSION REGULATION; HUMANS; LATENT TUBERCULOSIS; LUNG; MACACA MULATTA; MYCOBACTERIUM TUBERCULOSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TUBERCULOSIS;

EID: 84925063774     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.11.003     Document Type: Article

References (65)

1. WHO: Global Tuberculosis Report 2013 2013 World Health Organization Geneva, Switzerland
2. M.C. Raviglione The new Stop TB Strategy and the Global Plan to Stop TB, 2006-2015 Bull World Health Organ 85 2007 327
3. J.A. Philips, and J.D. Ernst Tuberculosis pathogenesis and immunity Annu Rev Pathol 7 2012 353 384
4. C. Dye, S. Scheele, P. Dolin, V. Pathania, and M.C. Raviglione Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project JAMA 282 1999 677 686
5. B.R. Bloom, and C.J. Murray Tuberculosis: commentary on a reemergent killer Science 257 1992 1055 1064
6. D.G. Russell Who puts the tubercle in tuberculosis? Nat Rev Microbiol 5 2007 39 47
7. L. Ramakrishnan Revisiting the role of the granuloma in tuberculosis Nat Rev Immunol 12 2012 352 366
8. S. Ehlers, and U.E. Schaible The granuloma in tuberculosis: dynamics of a host-pathogen collusion Front Immunol 3 2012 411
9. E. Guirado, and L.S. Schlesinger Modeling the Mycobacterium tuberculosis granuloma: the critical battlefield in host immunity and disease Front Immunol 4 2013 98
10. P.L. Lin, A. Myers, L. Smith, C. Bigbee, M. Bigbee, C. Fuhrman, H. Grieser, I. Chiosea, N.N. Voitenek, S.V. Capuano, E. Klein, and J.L. Flynn Tumor necrosis factor neutralization results in disseminated disease in acute and latent Mycobacterium tuberculosis infection with normal granuloma structure in a cynomolgus macaque model Arthritis Rheum 62 2010 340 350
11. G. Fenhalls, L. Stevens, J. Bezuidenhout, G.E. Amphlett, K. Duncan, P. Bardin, and P.T. Lukey Distribution of IFN-gamma, IL-4 and TNF-alpha protein and CD8 T cells producing IL-12p40 mRNA in human lung tuberculous granulomas Immunology 105 2002 325 335
12. P.S. Redford, P.J. Murray, and A. O'Garra The role of IL-10 in immune regulation during M. tuberculosis infection Mucosal Immunol 4 2011 261 270
13. A.M. Cooper Cell-mediated immune responses in tuberculosis Annu Rev Immunol 27 2009 393 422
14. S. Mehra, X. Alvarez, P.J. Didier, L.A. Doyle, J.L. Blanchard, A.A. Lackner, and D. Kaushal Granuloma correlates of protection against tuberculosis and mechanisms of immune modulation by Mycobacterium tuberculosis J Infect Dis 207 2013 1115 1127
15. E. Giacomini, E. Iona, L. Ferroni, M. Miettinen, L. Fattorini, G. Orefici, I. Julkunen, and E.M. Coccia Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response J Immunol 166 2001 7033 7041
16. T.B. Geijtenbeek, S.J. Van Vliet, E.A. Koppel, M. Sanchez-Hernandez, C.M. Vandenbroucke-Grauls, B. Appelmelk, and Y. Van Kooyk Mycobacteria target DC-SIGN to suppress dendritic cell function J Exp Med 197 2003 7 17
17. N. Poirier, T. Haudebourg, C. Brignone, N. Dilek, J. Hervouet, D. Minault, F. Coulon, R.V. de Silly, F. Triebel, G. Blancho, and B. Vanhove Antibody-mediated depletion of lymphocyte-activation gene-3 (LAG-3(+))-activated T lymphocytes prevents delayed-type hypersensitivity in non-human primates Clin Exp Immunol 164 2011 265 274
18. L. Macon-Lemaitre, and F. Triebel The negative regulatory function of the lymphocyte-activation gene-3 co-receptor (CD223) on human T cells Immunology 115 2005 170 178
19. N. Li, Y. Wang, K. Forbes, K.M. Vignali, B.S. Heale, P. Saftig, D. Hartmann, R.A. Black, J.J. Rossi, C.P. Blobel, P.J. Dempsey, C.J. Workman, and D.A. Vignali Metalloproteases regulate T-cell proliferation and effector function via LAG-3 EMBO J 26 2007 494 504
20. C.J. Workman, Y. Wang, K.C. El Kasmi, D.M. Pardoll, P.J. Murray, C.G. Drake, and D.A. Vignali LAG-3 regulates plasmacytoid dendritic cell homeostasis J Immunol 182 2009 1885 1891
21. F.J. Li, Y. Zhang, G.X. Jin, L. Yao, and D.Q. Wu Expression of LAG-3 is coincident with the impaired effector function of HBV-specific CD8(+) T cell in HCC patients Immunol Lett 150 2013 116 122
22. J. Illingworth, N.S. Butler, S. Roetynck, J. Mwacharo, S.K. Pierce, P. Bejon, P.D. Crompton, K. Marsh, and F.M. Ndungu Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion J Immunol 190 2013 1038 1047
23. S. Andreae, F. Piras, N. Burdin, and F. Triebel Maturation and activation of dendritic cells induced by lymphocyte activation gene-3 (CD223) J Immunol 168 2002 3874 3880
24. S. Mehra, N.A. Golden, N.K. Dutta, C.C. Midkiff, X. Alvarez, L.A. Doyle, M. Asher, K. Russell-Lodrigue, C. Monjure, C.J. Roy, J.L. Blanchard, P.J. Didier, R.S. Veazey, A.A. Lackner, and D. Kaushal Reactivation of latent tuberculosis in rhesus macaques by coinfection with simian immunodeficiency virus J Med Primatol 40 2011 233 243
25. D. Kaushal, S. Mehra, P.J. Didier, and A.A. Lackner The non-human primate model of tuberculosis J Med Primatol 41 2012 191 201
26. S. Mehra, N.A. Golden, K. Stuckey, P.J. Didier, L.A. Doyle, K.E. Russell-Lodrigue, C. Sugimoto, A. Hasegawa, S.K. Sivasubramani, C.J. Roy, X. Alvarez, M.J. Kuroda, J.L. Blanchard, A.A. Lackner, and D. Kaushal The Mycobacterium tuberculosis stress response factor SigH is required for bacterial burden as well as immunopathology in primate lungs J Infect Dis 205 2012 1203 1213
27. S.R. Slight, J. Rangel-Moreno, R. Gopal, Y. Lin, B.A. Fallert Junecko, S. Mehra, M. Selman, E. Becerril-Villanueva, J. Baquera-Heredia, L. Pavon, D. Kaushal, T.A. Reinhart, T.D. Randall, and S.A. Khader CXCR5(+) T helper cells mediate protective immunity against tuberculosis J Clin Invest 123 2013 712 726
28. N.K. Dutta, S. Mehra, P.J. Didier, C.J. Roy, L.A. Doyle, X. Alvarez, M. Ratterree, N.A. Be, G. Lamichhane, S.K. Jain, M.R. Lacey, A.A. Lackner, and D. Kaushal Genetic requirements for the survival of tubercle bacilli in primates J Infect Dis 201 2010 1743 1752
29. B.J. Gormus, J.L. Blanchard, X.H. Alvarez, and P.J. Didier Evidence for a rhesus monkey model of asymptomatic tuberculosis J Med Primatol 33 2004 134 145
30. K.M. Lee, K.B. Chiu, H.A. Sansing, P.J. Didier, T.A. Ficht, A.M. Arenas-Gamboa, C.J. Roy, and A.G. Maclean Aerosol-induced brucellosis increases TLR-2 expression and increased complexity in the microanatomy of astroglia in rhesus macaques Front Cell Infect Microbiol 3 2013 86
31. E.Z. Kincaid, and J.D. Ernst Mycobacterium tuberculosis exerts gene-selective inhibition of transcriptional responses to IFN-gamma without inhibiting STAT1 function J Immunol 171 2003 2042 2049
32. Y. Cai, C. Sugimoto, M. Arainga, X. Alvarez, E.S. Didier, and M.J. Kuroda In vivo characterization of alveolar and interstitial lung macrophages in rhesus macaques: implications for understanding lung disease in humans J Immunol 192 2014 2821 2829
33. C. Anderson, N. Inhaber, and D. Menzies Comparison of sputum induction with fiber-optic bronchoscopy in the diagnosis of tuberculosis Am J Respir Crit Care Med 152 1995 1570 1574
34. T. Okamura, K. Fujio, M. Shibuya, S. Sumitomo, H. Shoda, S. Sakaguchi, and K. Yamamoto CD4+CD25-LAG3+ regulatory T cells controlled by the transcription factor Egr-2 Proc Natl Acad Sci U S A 106 2009 13974 13979
35. S. Sumitomo, and K. Yamamoto CD4+CD25-LAG-3+ T cells in mouse and human Nihon Rinsho Meneki Gakkai Kaishi 33 2010 92 98
36. C.W. Adams, and R.N. Poston Macrophage histology in paraffin-embedded multiple sclerosis plaques is demonstrated by the monoclonal pan-macrophage marker HAM-56: correlation with chronicity of the lesion Acta Neuropathol 80 1990 208 211
37. R. Hershberg, M. Lipatov, P.M. Small, H. Sheffer, S. Niemann, S. Homolka, J.C. Roach, K. Kremer, D.A. Petrov, M.W. Feldman, and S. Gagneux High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography PLoS Biol 6 2008 e311
38. D.G. Russell The evolutionary pressures that have molded Mycobacterium tuberculosis into an infectious adjuvant Curr Opin Microbiol 16 2013 78 84
39. C. Paige, and W.R. Bishai Penitentiary or penthouse condo: the tuberculous granuloma from the microbe's point of view Cell Microbiol 12 2010 301 309
40. J.L. Flynn, J. Chan, K.J. Triebold, D.K. Dalton, T.A. Stewart, and B.R. Bloom An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection J Exp Med 178 1993 2249 2254
41. A.M. Cooper, D.K. Dalton, T.A. Stewart, J.P. Griffin, D.G. Russell, and I.M. Orme Disseminated tuberculosis in interferon gamma gene-disrupted mice J Exp Med 178 1993 2243 2247
42. S.M. Fortune, A. Solache, A. Jaeger, P.J. Hill, J.T. Belisle, B.R. Bloom, E.J. Rubin, and J.D. Ernst Mycobacterium tuberculosis inhibits macrophage responses to IFN-gamma through myeloid differentiation factor 88-dependent and -independent mechanisms J Immunol 172 2004 6272 6280
43. V. Nagabhushanam, A. Solache, L.M. Ting, C.J. Escaron, J.Y. Zhang, and J.D. Ernst Innate inhibition of adaptive immunity: mycobacterium tuberculosis-induced IL-6 inhibits macrophage responses to IFN-gamma J Immunol 171 2003 4750 4757
44. A.N. Martinez, S. Mehra, and D. Kaushal Role of interleukin 6 in innate immunity to Mycobacterium tuberculosis infection J Infect Dis 207 2013 1253 1261
45. J.E. Graham, and J.E. Clark-Curtiss Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS) Proc Natl Acad Sci U S A 96 1999 11554 11559
46. S. Mehra, and D. Kaushal Functional genomics reveals extended roles of the Mycobacterium tuberculosis stress response factor sigmaH J Bacteriol 191 2009 3965 3980
47. T.R. Rustad, M.I. Harrell, R. Liao, and D.R. Sherman The enduring hypoxic response of Mycobacterium tuberculosis PLoS One 3 2008 e1502
48. D. Kaushal, B.G. Schroeder, S. Tyagi, T. Yoshimatsu, C. Scott, C. Ko, L. Carpenter, J. Mehrotra, Y.C. Manabe, R.D. Fleischmann, and W.R. Bishai Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH Proc Natl Acad Sci U S A 99 2002 8330 8335
49. R. Manganelli, M.I. Voskuil, G.K. Schoolnik, E. Dubnau, M. Gomez, and I. Smith Role of the extracytoplasmic-function sigma factor sigma(H) in Mycobacterium tuberculosis global gene expression Mol Microbiol 45 2002 365 374
50. P.A. Fontan, V. Aris, M.E. Alvarez, S. Ghanny, J. Cheng, P. Soteropoulos, A. Trevani, R. Pine, and I. Smith Mycobacterium tuberculosis sigma factor E regulon modulates the host inflammatory response J Infect Dis 198 2008 877 885
51. N.K. Dutta, S. Mehra, A.N. Martinez, X. Alvarez, N.A. Renner, L.A. Morici, B. Pahar, A.G. Maclean, A.A. Lackner, and D. Kaushal The stress-response factor SigH modulates the interaction between Mycobacterium tuberculosis and host phagocytes PLoS One 7 2012 e28958
52. H.E. Volkman, T.C. Pozos, J. Zheng, J.M. Davis, J.F. Rawls, and L. Ramakrishnan Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium Science 327 2010 466 469
53. P.T. Elkington, C.A. Ugarte-Gil, and J.S. Friedland Matrix metalloproteinases in tuberculosis Eur Respir J 38 2011 456 464
54. N. Agarwal, and W.R. Bishai cAMP signaling in Mycobacterium tuberculosis Indian J Exp Biol 47 2009 393 400
55. S. Subbian, L. Tsenova, G. Yang, P. O'Brien, S. Parsons, B. Peixoto, L. Taylor, D. Fallows, and G. Kaplan Chronic pulmonary cavitary tuberculosis in rabbits: a failed host immune response Open Biol 1 2011 110016
56. J.E. Korf, G. Pynaert, K. Tournoy, T. Boonefaes, A. Van Oosterhout, D. Ginneberge, A. Haegeman, J.A. Verschoor, P. De Baetselier, and J. Grooten Macrophage reprogramming by mycolic acid promotes a tolerogenic response in experimental asthma Am J Respir Crit Care Med 174 2006 152 160
57. N. Cools, P. Ponsaerts, V.F. Van Tendeloo, and Z.N. Berneman Regulatory T cells and human disease Clin Dev Immunol 2007 2007 89195
58. X. Chen, B. Zhou, M. Li, Q. Deng, X. Wu, X. Le, C. Wu, N. Larmonier, W. Zhang, H. Zhang, H. Wang, and E. Katsanis CD4(+)CD25(+)FoxP3(+) regulatory T cells suppress Mycobacterium tuberculosis immunity in patients with active disease Clin Immunol 123 2007 50 59
59. J.M. Hougardy, S. Place, M. Hildebrand, A. Drowart, A.S. Debrie, C. Locht, and F. Mascart Regulatory T cells depress immune responses to protective antigens in active tuberculosis Am J Respir Crit Care Med 176 2007 409 416
60. L. Majlessi, P. Brodin, R. Brosch, M.J. Rojas, H. Khun, M. Huerre, S.T. Cole, and C. Leclerc Influence of ESAT-6 secretion system 1 (RD1) of Mycobacterium tuberculosis on the interaction between mycobacteria and the host immune system J Immunol 174 2005 3570 3579
61. L. Geffner, J.I. Basile, N. Yokobori, Y.G.C. Sabio, R. Musella, J. Castagnino, M.C. Sasiain, and S. de la Barrera CD4(+) CD25(high) forkhead box protein 3(+) regulatory T lymphocytes suppress interferon-gamma and CD107 expression in CD4(+) and CD8(+) T cells from tuberculous pleural effusions Clin Exp Immunol 175 2014 235 245
62. A.M. Green, J.T. Mattila, C.L. Bigbee, K.S. Bongers, P.L. Lin, and J.L. Flynn CD4(+) regulatory T cells in a cynomolgus macaque model of Mycobacterium tuberculosis infection J Infect Dis 202 2010 533 541
63. M. Kisielow, J. Kisielow, G. Capoferri-Sollami, and K. Karjalainen Expression of lymphocyte activation gene 3 (LAG-3) on B cells is induced by T cells Eur J Immunol 35 2005 2081 2088
64. T. Okamura, K. Fujio, S. Sumitomo, and K. Yamamoto Roles of LAG3 and EGR2 in regulatory T cells Ann Rheum Dis 71 Suppl 2 2012 i96 i100
65. C.J. Workman, and D.A. Vignali Negative regulation of T cell homeostasis by lymphocyte activation gene-3 (CD223) J Immunol 174 2005 688 695