Slam haplotype 2 promotes NKT but suppresses Vγ4+ T-cell activation in coxsackievirus b3 infection leading to increased liver damage but reduced myocarditis

American Journal of Pathology

Volumn 182, Issue 2, 2013, Pages 401-409

  Huber, Sally Ann ^a   Roberts, Brian ^a   Moussawi, Mohamad ^a   Boyson, Jonathan E ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALPHA GALACTOSYLCERAMIDE; CD150 ANTIGEN; DIMETHYL SULFOXIDE; GAMMA INTERFERON; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; TETRAMER; TRANSCRIPTION FACTOR FOXP3;

ADAPTIVE IMMUNITY; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELL SPECIFICITY; CONTROLLED STUDY; COXSACKIE VIRUS B3; COXSACKIE VIRUS INFECTION; DISEASE PREDISPOSITION; GAMMA DELTA T LYMPHOCYTE; GENE EXPRESSION; GENE LOCUS; HAPLOTYPE; HEART PROTECTION; HEPATITIS; HISTOPATHOLOGY; IMMUNE RESPONSE; INNATE IMMUNITY; LIGAND BINDING; LIVER INJURY; MALE; MOUSE; MOUSE STRAIN; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; VIRUS LOAD; VIRUS MYOCARDITIS;

ADAPTIVE IMMUNITY; ALANINE TRANSAMINASE; ANIMALS; ANTIGENS, CD; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; GALACTOSYLCERAMIDES; HAPLOTYPES; HEPATITIS; LIVER; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MALE; MICE; MICE, INBRED C57BL; MYOCARDITIS; NATURAL KILLER T-CELLS; POLYMORPHISM, GENETIC; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, CELL SURFACE; TROPONIN I; VIRAL LOAD;

EID: 84872704753     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.10.019     Document Type: Article

References (57)

1. S. Huber Host immune responses to coxsackievirus B3 Curr Top Microbiol Immunol 323 2008 199 221
2. N.E. Bowles, J. Ni, D.L. Kearney, M. Pauschinger, H.P. Schultheiss, R. McCarthy, J. Hare, J.T. Bricker, K.R. Bowles, and J.A. Towbin Detection of viruses in myocardial tissues by polymerase chain reaction. Evidence of adenovirus as a common cause of myocarditis in children and adults J Am Coll Cardiol 42 2003 466 472
3. N.E. Bowles, J. Ni, F. Marcus, and J.A. Towbin The detection of cardiotropic viruses in the myocardium of patients with arrhythmogenic right ventricular dysplasia/cardiomyopathy J Am Coll Cardiol 39 2002 892 895
4. C. Badorff, G.H. Lee, B.J. Lamphear, M.E. Martone, K.P. Campbell, R.E. Rhoads, and K.U. Knowlton Enteroviral protease 2A cleaves dystrophin: evidence of cytoskeletal disruption in an acquired cardiomyopathy Nat Med 5 1999 320 326
5. R. Rueckert Picronaviruses B.N. Fields, D.M. Knipe, P.M. Howley, 1996 Lippincott-Raven Philadelphia 477 522
6. G. Freeman, J. Colston, M. Zabalgoitia, and B. Chandrasekar Contractile depression and expression of proinflammatory cytokines and iNOS in viral myocarditis Am J Physiol 274 1998 H249 H258
7. N.R. Rose The adjuvant effect in infection and autoimmunity Clin Rev Allergy Immunol 34 2008 279 282
8. C.Y. Wu, Y. Feng, G.C. Qian, J.H. Wu, J. Luo, Y. Wang, G.J. Chen, X.K. Guo, and Z.J. Wang α-Galactosylceramide protects mice from lethal Coxsackievirus B3 infection and subsequent myocarditis Clin Exp Immunol 162 2010 178 187
9. M.A. Jordan, J.M. Fletcher, D. Pellicci, and A.G. Baxter Slamf1, the NKT cell control gene Nkt1 J Immunol 178 2007 1618 1627
10. K.E. Nichols, J. Hom, S.Y. Gong, A. Ganguly, C.S. Ma, J.L. Cannons, S.G. Tangye, P.L. Schwartzberg, G.A. Koretzky, and P.L. Stein Regulation of NKT cell development by SAP, the protein defective in XLP Nat Med 11 2005 340 345
11. K. Griewank, C. Borowski, S. Rietdijk, N. Wang, A. Julien, D.G. Wei, A.A. Mamchak, C. Terhorst, and A. Bendelac Homotypic interactions mediated by Slamf1 and Slamf6 receptors control NKT cell lineage development Immunity 27 2007 751 762
12. I. Aktan, A. Chant, Z.D. Borg, D.E. Damby, P.C. Leenstra, G.W. Lilley, J. Petty, B.T. Suratt, C. Teuscher, E.K. Wakeland, M.E. Poynter, and J.E. Boyson Slam haplotypes modulate the response to lipopolysaccharide in vivo through control of NKT cell number and function J Immunol 185 2010 144 156
13. A.E. Wandstrat, C. Nguyen, N. Limaye, A.Y. Chan, S. Subramanian, X.H. Tian, Y.S. Yim, A. Pertsemlidis, H.R. Garner Jr., L. Morel, and E.K. Wakeland Association of extensive polymorphisms in the SLAM/CD2 gene cluster with murine lupus Immunity 21 2004 769 780
14. N. Limaye, K.A. Belobrajdic, A.E. Wandstrat, F. Bonhomme, S.V. Edwards, and E.K. Wakeland Prevalence and evolutionary origins of autoimmune susceptibility alleles in natural mouse populations Genes Immun 9 2008 61 68
15. S. Mehrle, C. Watzl, M. von Lilienfeld-Toal, A. Amoroso, J. Schmidt, and A. Marten Comparison of phenotype of gammadelta T cells generated using various cultivation methods Immunol Lett 125 2009 53 58
16. S. Huber, D. Graveline, M. Newell, W. Born, and R. O'Brien V gamma1+ T cells suppress and V gamma4+ T cells promote susceptibility to coxsackievirus B3-induced myocarditis in mice J Immunol 165 2000 4174 4181
17. S. Huber T cells expressing the gamma-delta T cell receptor induce apoptosis in cardiac myocytes Cardiovasc Res 45 2000 579 587
18. P. Lapierre, K. Beland, I. Djilali-Saiah, and F. Alvarez Type 2 autoimmune hepatitis murine model: the influence of genetic background in disease development J Autoimmun 26 2006 82 89
19. A. Pellegrini, E.A. Carrera-Silva, A. Arocena, R.C. Cano, M.P. Aoki, and S. Gea Trypanosoma cruzi antigen immunization induces a higher B cell survival in BALB/c mice, a susceptible strain, compared to C57BL/6 B lymphocytes, a resistant strain to cardiac autoimmunity Med Microbiol Immunol 200 2011 209 218
20. J.C. Lenzo, D. Fairweather, V. Cull, G.R. Shellam, and C.M. James Lawson Characterisation of murine cytomegalovirus myocarditis: cellular infiltration of the heart and virus persistence J Mol Cell Cardiol 34 2002 629 640
21. D. Fairweather, C.M. Lawson, A.J. Chapman, C.M. Brown, T.W. Booth, J.M. Papadimitriou, and G.R. Shellam Wild isolates of murine cytomegalovirus induce myocarditis and antibodies that cross-react with virus and cardiac myosin Immunology 94 1998 263 270
22. C.M. Lawson, H. O'Donoghue, W.N. Bartholomaeus, and W.D. Reed Genetic control of mouse cytomegalovirus-induced myocarditis Immunology 69 1990 20 26
23. K.U. Knowlton, E.S. Jeon, N. Berkley, R. Wessely, and S. Huber A mutation in the puff region of VP2 attenuates the myocarditic phenotype of an infectious cDNA of the Woodruff variant of coxsackievirus B3 J Virol 70 1996 7811 7818
24. N. Van Houten, P. Bouchard, A. Moraska, and S. Huber Selection of an attenuated coxsackievirus B3 variant using a monoclonal antibody reactive to myocyte antigen J Virol 65 1991 1286 1290
25. S. Huber, D. Graveline, W. Born, and R. O'Brien Cytokine production by Vgamma+ T cell subsets is an important factor determining CD4+ Th cell phenotype and susceptibility of BALB/c mice to coxsackievirus B3-induced myocarditis J Virol 75 2001 5860 5868
26. S. Huber, and A.I. Ramsingh Coxsackievirus-induced pancreatitis Viral Immunol 17 2004 358 369
27. R. Gu, A. Shampang, A. Reilly, D. Fisher, W. Glass, and A.I. Ramsingh IL-10 is pathogenic during the development of coxsackievirus B4-induced chronic pancreatitis Virology 395 2009 77 86
28. R. Gu, A. Shampang, A. Reilly, D. Fisher, W. Glass, and A.I. Ramsingh Dynamics of molecular responses to coxsackievirus B4 infection differentiate between resolution and progression of acute pancreatitis Virology 427 2012 135 143
29. W. Liu, S. Li, W. Tian, W. Li, and Z. Zhang Immunoregulatory effects of alpha-GalCer in a murine model of autoimmune myocarditis Exp Mol Pathol 91 2011 636 642
30. C.M. Olson Jr., T.C. Bates, H. Izadi, J.D. Radolf, S.A. Huber, J.E. Boyson, and J. Anguita Local production of IFN-gamma by invariant NKT cells modulates acute Lyme carditis J Immunol 182 2009 3728 3734
31. K. Takeda, Y. Hayakawa, L. Van Kaer, H. Matsuda, H. Yagita, and K. Okumura Critical contribution of liver natural killer T cells to a murine model of hepatitis Proc Natl Acad Sci U S A 97 2000 5498 5503
32. Y. Kaneko, M. Harada, T. Kawano, M. Yamashita, Y. Shibata, F. Gejyo, T. Nakayama, and M. Taniguchi Augmentation of Valpha14 NKT cell-mediated cytotoxicity by interleukin 4 in an autocrine mechanism resulting in the development of concanavalin A-induced hepatitis J Exp Med 191 2000 105 114
33. H. Diao, S. Kon, K. Iwabuchi, C. Kimura, J. Morimoto, D. Ito, T. Segawa, M. Maeda, J. Hamuro, T. Nakayama, M. Taniguchi, H. Yagita, L. Van Kaer, K. Onoe, D. Denhardt, S. Rittling, and T. Uede Osteopontin as a mediator of NKT cell function in T cell-mediated liver diseases Immunity 21 2004 539 550
34. Y.H. Chuang, Z.X. Lian, G.X. Yang, S.A. Shu, Y. Moritoki, W.M. Ridgway, A.A. Ansari, M. Kronenberg, R.A. Flavell, B. Gao, and M.E. Gershwin Natural killer T cells exacerbate liver injury in a transforming growth factor beta receptor II dominant-negative mouse model of primary biliary cirrhosis Hepatology 47 2008 571 580
35. J. Mattner, P.B. Savage, P. Leung, S.S. Oertelt, V. Wang, O. Trivedi, S.T. Scanlon, K. Pendem, L. Teyton, J. Hart, W.M. Ridgway, L.S. Wicker, M.E. Gershwin, and A. Bendelac Liver autoimmunity triggered by microbial activation of natural killer T cells Cell Host Microbe 3 2008 304 315
36. H.N.O. Kita, M. Kronenberg, A.A. Ansari, P. Rogers, X.S. He, F. Koning, T. Mikayama, J. Van De Water, R.L. Coppel, M. Kaplan, and M.E. Gershwin Quantitation and phenotypic analysis of natural killer T cells in primary biliary cirrhosis using a human CD1d tetramer Gastroenterology 123 2002 1031 1043
37. I. Locatelli, S. Sutti, M. Vacchiano, C. Bozzola, and E. Albano Nf-Kappab1 deficiency stimulates the progression of nonalcoholic steatohepatitis (Nash) in mice by promoting Nkt-mediated responses Clin Sci (Lond) 124 2013 279 287
38. W.K. Syn, K.M. Agboola, M. Swiderska, G.A. Michelotti, E. Liaskou, H. Pang, G. Xie, G. Philips, I.S. Chan, G.F. Karaca, A. Pereira Tde, Y. Chen, Z. Mi, P.C. Kuo, S.S. Choi, C.D. Guy, M.F. Abdelmalek, and A.M. Diehl NKT-associated hedgehog and osteopontin drive fibrogenesis in non-alcoholic fatty liver disease Gut 61 2012 1323 1329
39. Z. Li, J.A. Oben, S. Yang, H. Lin, E.A. Stafford, M.J. Soloski, S.A. Thomas, and A.M. Diehl Norepinephrine regulates hepatic innate immune system in leptin-deficient mice with nonalcoholic steatohepatitis Hepatology 40 2004 434 441
40. W.K. Syn, Y.H. Oo, T.A. Pereira, G.F. Karaca, Y. Jung, A. Omenetti, R.P. Witek, S.S. Choi, C.D. Guy, C.M. Fearing, V. Teaberry, F.E. Pereira, D.H. Adams, and A.M. Diehl Accumulation of natural killer T cells in progressive nonalcoholic fatty liver disease Hepatology 51 2010 1998 2007
41. S.L. Rymarchyk, H. Lowenstein, J. Mayette, S.R. Foster, D.E. Damby, I.W. Howe, I. Aktan, R.E. Meyer, M.E. Poynter, and J.E. Boyson Widespread natural variation in murine natural killer T-cell number and function Immunology 125 2008 331 343
42. S. Frisancho-Kiss, M.J. Coronado, J.A. Frisancho, V.M. Lau, N.R. Rose, S.L. Klein, and D. Fairweather Gonadectomy of male BALB/c mice increases Tim-3(+) alternatively activated M2 macrophages. Tim-3(+) T cells, Th2 cells and Treg in the heart during acute coxsackievirus-induced myocarditis Brain Behav Immun 23 2009 649 657
43. C. Elamm, D. Fairweather, and L.T. Cooper Pathogenesis and diagnosis of myocarditis Heart 98 2012 835 840
44. M.J. Coronado, J.E. Brandt, E. Kim, A. Bucek, D. Bedja, E.D. Abston, J. Shin, K.L. Gabrielson, W. Mitzner, and D. Fairweather Testosterone and interleukin-1beta increase cardiac remodeling during coxsackievirus B3 myocarditis via serpin A 3n Am J Physiol 302 2012 H1726 H1736
45. S.A. Huber Coxsackievirus B3-induced myocarditis: infection of females during the estrus phase of the ovarian cycle leads to activation of T regulatory cells Virology 378 2008 292 298
46. S.A. Huber, A.M. Feldman, and D. Sartini Coxsackievirus B3 induces T regulatory cells, which inhibit cardiomyopathy in tumor necrosis factor-alpha transgenic mice Circ Res 99 2006 1109 1116
47. S. Huber γδ T lymphocytes kill T regulatory cells through CD1d Immunology 131 2010 202 209
48. S.A. Huber Depletion of gammadelta+ T cells increases CD4+ FoxP3 (T regulatory) cell response in coxsackievirus B3-induced myocarditis Immunology 127 2009 567 576
49. W. Liu, and S.A. Huber Cross-talk between cd1d-restricted nkt cells and γδ cells in t regulatory cell response Virol J 8 2011 32
50. A. La Cava, L. Van Kaer, and S. Fu Dong CD4+CD25+ Tregs and NKT cells: regulators regulating regulators Trends Immunol 27 2006 322 327
51. K.H. Sonoda, M. Exley, S. Snapper, S.P. Balk, and J. Stein-Streilein CD1-reactive natural killer T cells are required for development of systemic tolerance through an immune-privileged site J Exp Med 190 1999 1215 1226
52. K.H. Sonoda, D.E. Faunce, M. Taniguchi, M. Exley, S. Balk, and J. Stein-Streilein NK T cell-derived IL-10 is essential for the differentiation of antigen-specific T regulatory cells in systemic tolerance J Immunol 166 2001 42 50
53. S. Calpe, N. Wang, X. Romero, S.B. Berger, A. Lanyi, P. Engel, and C. Terhorst The SLAM and SAP gene families control innate and adaptive immune responses Adv Immunol 97 2008 177 250
54. N. Nagy, L. Matskova, U. Hellman, G. Klein, and E. Klein The apoptosis modulating role of SAP (SLAM associated protein) contributes to the symptomatology of the X linked lymphoproliferative disease Cell Cycle 8 2009 3086 3090
55. B.G. Cocks, C.C. Chang, J.M. Carballido, H. Yssel, J.E. de Vries, and G. Aversa A novel receptor involved in T-cell activation Nature 376 1995 260 263
56. A.L. Snow, R.A. Marsh, S.M. Krummey, P. Roehrs, L.R. Young, K. Zhang, J. van Hoff, D. Dhar, K.E. Nichols, A.H. Filipovich, H.C. Su, J.J. Bleesing, and M.J. Lenardo Restimulation-induced apoptosis of T cells is impaired in patients with X-linked lymphoproliferative disease caused by SAP deficiency J Clin Invest 119 2009 2976 2989
57. R. Kageyama, J.L. Cannons, F. Zhao, I. Yusuf, C. Lao, M. Locci, P.L. Schwartzberg, and S. Crotty The receptor Ly108 functions as a SAP adaptor-dependent on-off switch for T cell help to B cells and NKT cell development Immunity 36 2012 986 1002