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, Behavior, and Immunity

Volumn 23, Issue 5, 2009, Pages 649-657

  Frisancho Kiss, Sylvia ^a   Coronado, Michael J ^a   Frisancho, J Augusto ^a   Lau, Vivian M ^a   Rose, Noel R ^a,b   Klein, Sabra L ^a   Fairweather, DeLisa ^a,b  

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

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

Author keywords

Autoimmunity; Cytokines; Macrophages; Myocarditis; Sex differences; Th2; Tim 3; Tolerance; Treg; Virus

Indexed keywords

CD11B ANTIGEN; CD4 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4 RECEPTOR; T CELL IMMUNOGLOBULIN MUCIN 3; TESTOSTERONE; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COXSACKIE VIRUS B3; COXSACKIE VIRUS INFECTION; DISEASE SEVERITY; FLUORESCENCE ACTIVATED CELL SORTING; GONADECTOMY; HORMONE ACTION; HORMONE RELEASE; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TESTOSTERONE BLOOD LEVEL; TH2 CELL; UPREGULATION; VIRUS MYOCARDITIS; VIRUS REPLICATION;

ACUTE DISEASE; ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD45; COXSACKIEVIRUS INFECTIONS; CYTOKINES; ENTEROVIRUS B, HUMAN; MACROPHAGE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MYOCARDITIS; MYOCARDIUM; ORCHIECTOMY; RECEPTORS, VIRUS; T-LYMPHOCYTES, REGULATORY; TESTOSTERONE; TH2 CELLS; VIRUS REPLICATION;

EID: 68649115262     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2008.12.002     Document Type: Article

References (71)

1. Anthony R.M., Rutitzky L., Urban Jr. J.F., Stadecker M.J., and Gause W.C. Protective immune mechanisms in helminth infection. Nature Rev. Immunol. 7 (2007) 975-987
2. Cernetich A., Garver L.S., Jedlicka A.E., Klein P.W., Kumar N., Scott A.L., and Klein S.L. Involvement of gonadal steroids and gamma interferon in sex differences in response to blood-stage malaria infection. Infect. Immun. 74 (2006) 3190-3203
3. Chang H., Hanawa H., Yoshida T., Hayashi M., Liu H., Ding L., Otaki K., Hao K., Yoshida K., Kato K., Toba K., Kodama M., Maruyama H., Miyazaki J., and Aizawa Y. Alteration of IL-17 related protein expressions in experimental autoimmune myocarditis and inhibition of IL-17 by IL-10-Ig fusion gene transfer. Circ. J. 72 (2008) 813-819
4. Cihakova, D., Sharma, R., Fairweather, D., Afanasyeva, M., Rose N.R., 2004. Animal models for autoimmune myocarditis and autoimmune thyroiditis. In: Perl, A. (Ed.), Methods in Molecular Medicine Autoimmunity: Methods and Protocols, vol. 102. pp. 175-194.
5. Cihakova D., Barin J.G., Afanasyeva M., Kimura M., Fairweather D., Berg M., Talor M.V., Baldeviano G.C., Frisancho-Kiss S., Gabrielson K., Bedja D., and Rose N.R. Interleukin-13 protects against experimental autoimmune myocarditis by regulating macrophage differentiation. Am. J. Pathol. 172 (2008) 1195-1208
6. Cutolo M., Accardo S., Villaggio B., Barone A., Coviello D.A., Carabbio C., Felli L., Miceli D., Farruggio R., Carruba G., and Castagnetta L. Androgen and estrogen receptors are present in primary cultures of human synovial macrophages. J. Clin. Endocrinol. Metab. 81 (1996) 820-827
7. Dardalhon V., Korn T., Kuchroo V.J., and Anderson A.C. Role of Th1 and Th17 cells in organ-specific autoimmunity. J. Autoimmun. 31 (2008) 252-256
8. De Bosscher K., Vanden Berghe W., and Haegeman G. Cross-talk between nuclear receptors and nuclear factor κB. Oncogene 25 (2006) 6868-6886
9. Dec G.W. Introduction to clinical myocarditis. In: Cooper Jr. L.T. (Ed). Myocarditis: From Bench to Bedside (2003), Humana Press, Totowa, New Jersey 157-281
10. Dechkum N., Pangsawan Y., Jayavasu C., and Saguanwongse S. Coxsackie B virus infection and myopericarditis in Thailand, 1987-1989. Southeast Asian J. Trop. Med. Public Health 29 (1998) 273-276
11. Demyanets S., Pfaffenberger S., Kaun C., Rega G., Speidl W.S., Kastl S.P., Weiss T.W., Hohensinner P.J., Dietrich W., Tschugguel W., Bochkov V.N., Awad E.M., Maurer G., Huber K., and Wojta J. The estrogen metabolite 17b-dihydroequilenin counteracts interleukin-1α induced expression of inflammatory mediators in human endothelial cells in vitro via NF-κB pathway. Thromb. Haemost. 95 (2006) 107-116
12. Ehirchiou D., Xiong Y., Xu G., Chen W., Shi Y., and Zhang L. CD11b facilitates the development of peripheral tolerance by suppressing Th17 differentiation. J. Exp. Med. 204 (2007) 1519-1524
13. Evans M.J., Eckert A., Lai K., Adelman S.J., and Harnish D.C. Reciprocal antagonism between estrogen receptor and NF-κB activity in vivo. Circ. Res. 89 (2001) 823-830
14. Fairweather D., and Frisancho-Kiss S. Mast cells and inflammatory heart disease: potential drug targets. Cardiovasc. Hematol. Disord. Drug Targets 8 (2008) 80-90
15. Fairweather D., and Rose N.R. Immunopathogenesis of autoimmune disease. In: Luebke R., House R., and Kimber I. (Eds). Immunotoxicology and Immunopharmacology. third ed. (2007), CRC Press, Boca Raton 423-436
16. Fairweather D., and Rose N.R. Coxsackievirus-induced myocarditis in mice. A model of autoimmune disease for studying immunotoxicity. Methods 41 (2007) 118-122
17. Fairweather D., Yusung S., Frisancho(-Kiss) S., Barrett M., Gatewood S., Steele R., and Rose N.R. IL-12Rβ1 and TLR4 increase IL-1β and IL-18-associated myocarditis and coxsackievirus replication. J. Immunol. 170 (2003) 4731-4737
18. 1, IL-1β, and IL-4 in the heart. Am. J. Pathol. 165 (2004) 1883-1894
19. Fairweather D., Frisancho-Kiss S., Gatewood S., Njoku D., Steele R., Barrett M., and Rose N.R. Mast cells and innate cytokines are associated with susceptibility to autoimmune heart disease following coxsackievirus B3 infection. Autoimmunity 37 (2004) 131-145
20. Fairweather D., Frisancho-Kiss S., and Rose N.R. Viruses as adjuvants for autoimmunity: evidence from coxsackievirus-induced myocarditis. Rev. Med. Virol. 15 (2005) 17-27
21. Fairweather D., Frisancho-Kiss S., Yusung S.A., Barrett M.A., Davis S.E., Steele R.A., Gatewood S.J., and Rose N.R. IL-12 protects against coxsackievirus B3-induced myocarditis by increasing IFN-γ and macrophage and neutrophil populations in the heart. J. Immunol. 174 (2005) 261-269
22. Fairweather D., Frisancho-Kiss S., Njoku D.B., Nyland J.F., Kaya Z., Yusung S.A., Davis S.E., Frisancho J.A., Barrett M.A., and Rose N.R. Complement receptor 1 and 2 deficiency increases coxsackievirus B3-induced myocarditis and heart failure by increasing macrophages, IL-1β and immune complex deposition in the heart. J. Immunol. 176 (2006) 3516-3524
23. Fairweather D., Frisancho-Kiss S., and Rose N.R. Sex differences in autoimmune disease from a pathologic perspective. Am. J. Pathol. 173 (2008) 600-609
24. Feldman A.M., and McNamara D. Myocarditis. N. Engl. J. Med. 343 (2000) 1388-1398
25. Feldman I., Feldman G.M., Mobarak C., Dunkelberg J.C., and Leslie K.K. Identification of proteins within the nuclear factor-kappa B transcriptional complex including estrogen receptor-alpha. Am. J. Obstet. Gynecol. 196 (2007) 394.e1-394.e11
26. Frisancho-Kiss S., Nyland J.F., Davis S.E., Frisancho J.A., Barrett M.A., Rose N.R., and Fairweather D. Sex differences in coxsackievirus B3-induced myocarditis: IL-12Rβ1 signaling and IFN-γ increase inflammation in males independent from STAT4. Brain Res. 1126 (2006) 139-147
27. Frisancho-Kiss S., Nyland J.F., Davis S.E., Barrett M.A., Gatewood S.J.L., Njoku D.B., Cihakova D., Silbergeld E.K., Rose N.R., and Fairweather D. Cutting edge: T cell Ig mucin-3 reduces inflammatory heart disease by increasing CTLA-4 during innate immunity. J. Immunol. 176 (2006) 6411-6415
28. Frisancho-Kiss S., Davis S.E., Nyland J.F., Frisancho J.A., Cihakova D., Rose N.R., and Fairweather D. Cutting edge: Cross-regulation by TLR4 and T cell Ig mucin-3 determines sex differences in inflammatory heart disease. J. Immunol. 178 (2007) 6710-6714
29. Galli S.J., Nakae S., and Tsai M. Mast cells in the development of adaptive immune responses. Nat. Immunol. 6 (2005) 135-142
30. Godeny E.K., Sprague E.A., Schwartz C.J., and Gauntt C.J. Coxsackievirus group B replication in cultured fetal baboon aortic smooth muscle cells. J. Med. Virol. 20 (1986) 135-149
31. Hannah M.F., Bajic V.B., and Klein S.L. Sex differences in the recognition of and innate antiviral responses to Seoul virus in Norway rats. Brain Behav. Immun. 22 (2008) 503-516
32. Huber S.A. Increased susceptibility of male BALB/c mice to coxsackievirus B3-induced myocarditis: role for CD1d. Med. Microbiol. Immunol. 194 (2005) 121-127
33. Huber S.A. 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
34. Huber S.A., and Pfaeffle B. Differential Th1 and Th2 cell responses in male and female BALB/c mice infected with coxsackievirus group B type 3. J. Virol. 68 (1994) 5126-5132
35. Huber S.A., Kupperman J., and Newell M.K. Estradiol prevents and testosterone promotes Fas-dependent apoptosis in CD4+ Th2 cells by altering Bcl 2 expression. Lupus 8 (1999) 384-387
36. Kaya Z., Afanasyeva M., Wang Y., Dohmen K.M., Schlichting J., Tretter T., Fairweather D., Holers V.M., and Rose N.R. Contribution of the innate immune system to autoimmune myocarditis: a role for complement. Nature Immunol. 2 (2001) 739-745
37. Kher A., Wang M., Tsai B.M., Pitcher J.M., Greenbaum E.S., Nagy R.D., Patel K.M., Wairiuko G.M., Markel T.A., and Meldrum D.R. Sex differences in the myocardial inflammatory response to acute injury. Shock 23 (2005) 1-10
38. Khetsuriani N., LaMonte-Fowlkes A., Oberste M.S., and Pallansch M.A. Enterovirus surveillance-United States, 1970-2005. MMWR Surveill. Summ. 55 SS08 (2006) 1-20
39. Krieg M., Smith K., and Bartsch W. Demonstration of a specific androgen receptor in rat heart muscle: relationship between binding, metabolism, and tissue levels of androgens. Endocrinology 103 (1978) 1686-1694
40. Kwon T.W., do Kim K., Ye J.S., Lee W.J., Moon M.S., Joo C.H., Lee H., and Kim Y.K. Detection of enterovirus, cytomegalovirus, and Chlamydia pneumoniae in atheromas. J. Microbiol. 42 (2004) 299-304
41. Lang T.J. Estrogen as an immunomodulator. Clin. Immunol. 113 (2004) 224-230
42. Lenzo J.C., Fairweather D., Cull V., Shellam G.R., and Lawson C.M. Characterisation of murine cytomegalovirus myocarditis: cellular infiltration of the heart and virus persistence. J. Mol. Cell. Cardiol. 34 (2002) 629-640
43. Lima A.P., Lunardi L.O., and Rosa e Silva A.A.M. Effects of castration and testosterone replacement on peritoneal histamine concentration and lung histamine concentration in pubertal male rats. J. Endocrin. 167 (2000) 71-75
44. Mahoney P.M., Hurst P.R., McLeod B.J., McConnell M.A., and Thompson E.G. Effect of estradiol treatment on mast cell populations and microflora in the vaginal cul-de-sac of seasonally anestrous brushtail possums (Trichosurus vulpecula). Reprod. 125 (2003) 733-741
45. Martinez F.O., Sica A., Mantovani A., and Locati M. Macrophage activation and polarization. Front. Biosci. 13 (2008) 453-461
46. Mayo J.C., Sainz R.M., Antolin I., Uria H., Menendez-Pelaez A., and Rodriguez C. Androgen-dependent mast cell degranulation in the Harderian gland of female Syrian hamsters: in vivo and organ culture evidence. Anat. Embryol. 196 (1997) 133-140
47. Melchert R.B., Kennedy R.H., and Acosta Jr. D. Cardiovascular effects of steroidal agents. In: Acosta Jr. D. (Ed). Cardiovascular Toxicology (2001), Taylor & Francis, London 425-475
48. Meyers J.H., Sabatos C.A., Chakravarti S., and Kuchroo V.K. The TIM gene family regulates autoimmune and allergic diseases. Trends Mol. Med. 11 (2005) 362-369
49. Monney L., Sabatos C.A., Gaglia J.L., Ryu A., Waldner H., Chernova T., Manning S., Greenfield E.A., Coyle A.J., Sobel R.A., Freeman G.J., and Kuchroo V.K. Th1-specific cell surface protein Tim-3 regulates macrophage activation and the severity of autoimmune disease. Nature 415 (2002) 536-541
50. Nahrendorf M., Swirski F.K., Aikawa E., Stangenberg L., Wurdinger T., Figueiredo J.-L., Libby P., Weissleder R., and Pittet M.J. The healing myocardium sequentially mobilized two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204 (2007) 3037-3047
51. Nakae S., Iikura M., Suto H., Akiba H., Umetsu D.T., Dekruyff R.H., Saito H., and Galli S.J. TIM-1 and TIM-3 enhancement of Th2 cytokine production by mast cells. Blood 110 (2007) 2565-2568
52. Paimela T., Ryhanen T., Mannermaa E., Ojala J., Kalesnykas G., Salminen A., and Kaarniranta K. The effect of 17beta-estradiol on IL-6 secretion and NF-kappaB DNA-binding activity in human retinal pigment epithelial cells. Immunol. Lett. 110 (2007) 139-144
53. Rangachari M., Mauermann N., Marty R.R., Dirnhofer S., Kurrer M.O., Komnenovic V., Penninger J.M., and Eriksson U. T-bet negatively regulates autoimmune myocarditis by suppressing local production of interleukin 17. J. Exp. Med. 203 (2006) 2009-2019
54. Roivainen M. Enteroviruses and myocardial infarction. Am. Heart J. 138 (1999) S479-S483
55. Rosamond W., Flegal K., Furie K., Go A., Greenlund K., Haase N., Hailpern S.M., Ho M., Howard V., Kissela B., Kittner S., Lloyd-Jones D., McDermott M., Meigs J., Moy C., Nichol G., O'Donnell C., Roger V., Sorlie P., Steinberger J., Thom T., Wilson M., and Hong Y. American Heart Association Statistics Committee and Stroke Statistics Subcommittee, 2008. Heart disease and stroke statistics-2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 117 (2008) e25-e146
56. Rossouw J.E., Anderson G.L., Prentice R.L., LaCroix A.Z., Kooperberg C., Stefanick M.L., Jackson R.D., Beresford S.A., Howard B.V., Johnson K.C., Kotchen J.M., and Ockene J. Writing Group for the Women's Health Initiative Investigators, 2002. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. J. Am. Med. Assoc. 288 (2002) 321-333
57. Schoub B.D., Johnson S., McAnerney J.M., Dos Santos I.L., and Klaassen K.I. Epidemic Coxsackie B virus infection in Johannesburg, South Africa. J. Hyg. (Lond.) 95 (1985) 447-455
58. Sica A., and Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest. 117 (2007) 1155-1166
59. Sonderegger I., Rohn T.A., Kurrer M.O., Iezzi G., Zou Y., Kastelein R.A., Bachmann M.F., and Kopf M. Neutralization of IL-17 by active vaccination inhibits IL-23-dependent autoimmune myocarditis. Eur. J. Immunol. 36 (2006) 2849-2856
60. Steinman L. A rush to judgment on Th17. J. Exp. Med. 205 (2008) 1517-1522
61. Stockinger B., Veldhoen M., and Martin B. Th17 T cells: linking innate and adaptive immunity. Semin. Immunol. 19 (2007) 353-361
62. Straub R.H. The complex role of estrogens in inflammation. Endocrine Rev. 28 (2007) 521-574
63. Styrt B., and Sugarman B. Estrogens and infection. Rev. Infect. Dis. 13 (1991) 1139-1150
64. Su E.W., Lin J.Y., and Kane L.P. TIM-1 and TIM-3 proteins in immune regulation. Cytokine 44 (2008) 9-13
65. Terrazas L.I., Walsh K.L., Piskorska D., McGuire E., and Harn Jr. D.A. The schistosome oligosaccharide lacto-N-neotetraose expands Gr1+ cells that secret anti-inflammatory cytokines and inhibit proliferation of naive CD4+ cells: A potential mechanism for immune polarization in helminth infections. J. Immunol. 167 (2001) 5294-5303
66. Valaperti A., Marty R.R., Kania G., Germano D., Mauermann N., Dirnhofer S., Leimenstoll B., Blyszczuk P., Dong C., Mueller C., Hunziker L., and Eriksson U. CD11b+ monocytes abrogate Th17 CD4+ T cell-mediated experimental autoimmune myocarditis. J. Immunol. 180 (2008) 2686-2695
67. Van Ginderachter J.A., Movahedi K., Hassanzadeh G., Meerschaut S., Beschin A., Raes G., and de Baetselier P. Classical and alternative activation of mononuclear phagocytes: picking the best of both worlds for tumor promotion. Immunobiology 211 (2006) 487-501
68. Wang X., Belguise K., Kersual N., Kirsch K.H., Mineva N.D., Galtier F., Chalbos D., and Sonenshein G.E. Oestrogen signaling inhibits invasive phenotype by repressing RelB and its target BCL2. Nature Cell Biol. 9 (2007) 470-478
69. Woodruff J.F. Viral myocarditis: a review. Am. J. Pathol. 101 (1980) 425-484
70. Zhao X.J., McKerr G., Dong Z., Higgins C.A., Carson J., Yang Z.Q., and Hannigan B.M. Expression of estrogen and progesterone receptors by mast cells alone, but not lymphocytes, macrophages or other immune cells in human upper airways. Thorax 56 (2001) 205-211
71. hi suppressive monocytes in experimental autoimmune encephalomyelitis. J. Immunol. 179 (2007) 5228-5237