Sex chromosome complement contributes to sex differences in coxsackievirus B3 but not influenza A virus pathogenesis

Biology of Sex Differences

Volumn 2, Issue 1, 2011, Pages

  Robinson, Dionne P ^a   Huber, Sally A ^b   Moussawi, Mohamad ^b   Roberts, Brian ^b   Teuscher, Cory ^c   Watkins, Rebecca ^d   Arnold, Arthur P ^d   Klein, Sabra L ^a  

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

^b UNIVERSITY OF VERMONT   (United States)

^c UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 82555202871     PISSN: None     EISSN: 20426410     Source Type: Journal    
DOI: 10.1186/2042-6410-2-8     Document Type: Article

References (63)

1. Klein SL, Huber S: Sex differences in susceptibility to viral infection. In Sex Hormones and Immunity to Infection. Edited by: Klein SL, Roberts CW. Berlin, Germany: Springer-Verlag; 2010:93-122.
2. Roberts CW, Walker W, Alexander J: Sex-associated hormones and immunity to protozoan parasites. Clin Microbiol Rev 2001, 14:476-488. (Pubitemid 32642746)
3. Araneo BA, Dowell T, Diegel M, Daynes RA: Dihydrotestosterone exerts a depressive influence on the production of interleukin-4 (IL-4), IL-5, and gamma-interferon, but not IL-2 by activated murine T cells. Blood 1991, 78:688-699.
4. Barrat F, Lesourd B, Boulouis HJ, Thibault D, Vincent-Naulleau S, Gjata B, Louise A, Neway T, Pilet C: Sex and parity modulate cytokine production during murine ageing. Clin Exp Immunol 1997, 109:562-568. (Pubitemid 27402328)
5. Brabin L: Interactions of the female hormonal environment, susceptibility to viral infections, and disease progression. AIDS Patient Care STDS 2002, 16:211-221. (Pubitemid 34478161)
6. Paharkova-Vatchkova V, Maldonado R, Kovats S: Estrogen preferentially promotes the differentiation of CD11c+ CD11b(intermediate) dendritic cells from bone marrow precursors. J Immunol 2004, 172:1426-1436. (Pubitemid 38116784)
7. Ito A, Bebo BF Jr, Matejuk A, Zamora A, Silverman M, Fyfe-Johnson A, Offner H: Estrogen treatment down-regulates TNF-alpha production and reduces the severity of experimental autoimmune encephalomyelitis in cytokine knockout mice. J Immunol 2001, 167:542-552. (Pubitemid 32567822)
8. Li J, McMurray RW: Effects of estrogen receptor subtype-selective agonists on immune functions in ovariectomized mice. Int Immunopharmacol 2006, 6:1413-1423. (Pubitemid 44038682)
9. Karpuzoglu-Sahin E, Hissong BD, Ansar Ahmed S: Interferon-gamma levels are upregulated by 17-beta-estradiol and diethylstilbestrol. J Reprod Immunol 2001, 52:113-127. (Pubitemid 32923020)
10. Karpuzoglu-Sahin E, Zhi-Jun Y, Lengi A, Sriranganathan N, Ansar Ahmed S: Effects of long-term estrogen treatment on IFN-gamma, IL-2 and IL-4 gene expression and protein synthesis in spleen and thymus of normal C57BL/6 mice. Cytokine 2001, 14:208-217. (Pubitemid 32619901)
11. Lambert KC, Curran EM, Judy BM, Milligan GN, Lubahn DB, Estes DM: Estrogen receptor alpha (ERalpha) deficiency in macrophages results in increased stimulation of CD4+ T cells while 17beta-estradiol acts through ERalpha to increase IL-4 and GATA-3 expression in CD4+ T cells independent of antigen presentation. J Immunol 2005, 175:5716-5723. (Pubitemid 41508054)
12. Smithson G, Couse J, Lubahn D, Korach K, Kincade P: The role of estrogen receptors and androgen receptors in sex steroid regulation of B lymphocytes. J Immunol 1998, 161:27-34. (Pubitemid 28285502)
13. Grimaldi CM, Cleary J, Dagtas AS, Moussai D, Diamond B: Estrogen alters thresholds for B cell apoptosis and activation. J Clin Invest 2002, 109:1625-1633. (Pubitemid 34663525)
14. Islander U, Erlandsson MC, Hasseus B, Jonsson CA, Ohlsson C, Gustafsson JA, Dahlgren U, Carlsten H: Influence of oestrogen receptor alpha and beta on the immune system in aged female mice. Immunology 2003, 110:149-157. (Pubitemid 37059683)
15. Polanczyk MJ, Hopke C, Huan J, Vandenbark AA, Offner H: Enhanced FoxP3 expression and Treg cell function in pregnant and estrogen-treated mice. J Neuroimmunol 2005, 170:85-92. (Pubitemid 41740909)
16. Polanczyk M, Yellayi S, Zamora A, Subramanian S, Tovey M, Vandenbark AA, Offner H, Zachary JF, Fillmore PD, Blankenhorn EP, Gustafsson JA, Teuscher C: Estrogen receptor-1 (Esr1) and-2 (Esr2) regulate the severity of clinical experimental allergic encephalomyelitis in male mice. Am J Pathol 2004, 164:1915-1924. (Pubitemid 38669341)
17. Tai P, Wang J, Jin H, Song X, Yan J, Kang Y, Zhao L, An X, Du X, Chen X, Wang S, Xia G, Wang B: Induction of regulatory T cells by physiological level estrogen. J Cell Physiol 2008, 214:456-464. (Pubitemid 350309002)
18. Tanriverdi F, Silveira LF, MacColl GS, Bouloux PM: The hypothalamicpituitary-gonadal axis: immune function and autoimmunity. J Endocrinol 2003, 176:293-304. (Pubitemid 36410413)
19. Szekeres-Bartho J: Immunological relationship between the mother and the fetus. Int Rev Immunol 2002, 21:471-495. (Pubitemid 35399954)
20. Lenz F: Morbidic Hereditary Factors New York, USA: Macmillan Press; 1931.
21. Purtilo DT, Sullivan JL: Immunological bases for superior survival of females. Am J Dis Child 1979, 133:1251-1253. (Pubitemid 10205403)
22. Arnold AP, Chen X: What does the "four core genotypes" mouse model tell us about sex differences in the brain and other tissues? Front Neuroendocrinol 2009, 30:1-9.
23. Libert C, Dejager L, Pinheiro I: The X chromosome in immune functions: when a chromosome makes the difference. Nat Rev Immunol 2010, 10:594-604.
24. Fish EN: The X-files in immunity: sex-based differences predispose immune responses. Nat Rev Immunol 2008, 8:737-744.
25. Voskuhl R: Sex differences in autoimmune diseases. Biol Sex Differ 2011, 2:1.
26. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R: Male development of chromosomally female mice transgenic for Sry. Nature 1991, 351:117-121. (Pubitemid 21896542)
27. Smith-Bouvier DL, Divekar AA, Sasidhar M, Du S, Tiwari-Woodruff SK, King JK, Arnold AP, Singh RR, Voskuhl RR: A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med 2008, 205:1099-1108. (Pubitemid 351679685)
28. Fuller A, Yahikozawa H, So EY, Dal Canto M, Koh CS, Welsh CJ, Kim BS: Castration of male C57L/J mice increases susceptibility and estrogen treatment restores resistance to Theiler's virus-induced demyelinating disease. J Neurosci Res 2007, 85:871-881. (Pubitemid 46426087)
29. Fuller AC, Kang B, Kang HK, Yahikozowa H, Dal Canto MC, Kim BS: Gender bias in Theiler's virus-induced demyelinating disease correlates with the level of antiviral immune responses. J Immunol 2005, 175:3955-3963. (Pubitemid 41292057)
30. Huber S, Job L, Auld K: Influence of sex hormones on coxsackie B3 virus infection in Balb/c mice. Cell Immunol 1982, 67:173-179.
31. Klein SL, Pekosz A, Passaretti C, Anker M, Olukoya P: Sex, Gender and Influenza Geneva, Switzerland: World Health Organization; 2010, 1-58.
32. Robinson DP, Lorenzo ME, Jian W, Klein SL: Elevated 17β-estradiol protects females from influenza A virus pathogenesis by suppressing inflammatory responses. PLoS Pathog 2011, 7:e1002149.
33. Palaszynski KM, Smith DL, Kamrava S, Burgoyne PS, Arnold AP, Voskuhl RR: A yin-yang effect between sex chromosome complement and sex hormones on the immune response. Endocrinology 2005, 146:3280-3285. (Pubitemid 41058098)
34. Siracusa MC, Overstreet MG, Housseau F, Scott AL, Klein SL: 17{beta}-estradiol alters the activity of conventional and IFN-producing killer dendritic cells. J Immunol 2008, 180:1423-1431.
35. Cernetich A, Garver LS, Jedlicka AE, Klein PW, Kumar N, Scott AL, Klein SL: Involvement of gonadal steroids and gamma interferon in sex differences in response to blood-stage malaria infection. Infect Immun 2006, 74:3190-3203. (Pubitemid 43794507)
36. Klein SL, Bird BH, Glass GE: Sex differences in Seoul virus infection are not related to adult sex steroid concentrations in Norway rats. J Virol 2000, 74:8213-8217. (Pubitemid 30641670)
37. Knowlton KU, Jeon ES, Berkley N, Wessely R, Huber S: 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 1996, 70:7811-7818. (Pubitemid 26339087)
38. Van Houten N, Bouchard P, Moraska A, Huber S: Selection of an attenuated coxsackievirus B3 variant using a monoclonal antibody reactive to myocyte antigen. J Virol 1991, 65:1286-1290.
39. Huber SA: Coxsackievirus B3-induced myocarditis: infection of females during the estrus phase of the ovarian cycle leads to activation of T regulatory cells. Virology 2008, 378:292-298.
40. Woodruff J, Woodruff J: Involvement of T lymphocytes in the pathogenesis of coxsackievirus B3 heart disease. J Immunol 1974, 113:1726-1734.
41. Larcombe AN, Foong RE, Bozanich EM, Berry LJ, Garratt LW, Gualano RC, Jones JE, Dousha LF, Zosky GR, Sly PD: Sexual dimorphism in lung function responses to acute influenza A infection. Influenza Other Respi Viruses 2011.
42. Huber S: T cells expressing the gamma-delta T cell receptor induce apoptosis in cardiac myocytes. Cardiovasc Res 2000, 45:579-587. (Pubitemid 30047124)
43. Miller S, Vanderlugt C, Begolka W, Pao W, Yauch R, Neville K, Katz-Levy Y, Carrizosa A, Kim B: Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat Med 1997, 3:1133-1136. (Pubitemid 27444456)
44. Kawagishi A, Kubosaki A, Takeyama N, Sakudo A, Saeki K, Matsumoto Y, Hayashi T, Onodera T: Analysis of T-cell receptor Vbeta gene from infiltrating T cells in insulitis and myocarditis in encephalomyocarditis virus-infected BALB/C mice. Biochem Biophys Res Commun 2003, 310:791-795. (Pubitemid 37188691)
45. Huber SA, Feldman AM, Sartini D: Coxsackievirus B3 induces T regulatory cells, which inhibit cardiomyopathy in tumor necrosis factor-alpha transgenic mice. Circ Res 2006, 99:1109-1116. (Pubitemid 44729935)
46. Juleff N, Windsor M, Lefevre EA, Gubbins S, Hamblin P, Reid E, McLaughlin K, Beverley PC, Morrison IW, Charleston B: Foot-and-mouth disease virus can induce a specific and rapid CD4+ T-cell-independent neutralizing and isotype class-switched antibody response in naive cattle. J Virol 2009, 83:3626-3636.
47. Woodruff J: Lack of correlation between neutralizing antibody production and suppression of coxsackievirus B-3 replication in target organs: evidence for involvement of mononuclear inflammatory cells in defense. J Immunol 1979, 123:31-36. (Pubitemid 9213541)
48. La Gruta NL, Kedzierska K, Stambas J, Doherty PC: A question of selfpreservation: immunopathology in influenza virus infection. Immunol Cell Biol 2007, 85:85-92. (Pubitemid 46398724)
49. Ahmed R, Oldstone MB, Palese P: Protective immunity and susceptibility to infectious diseases: lessons from the 1918 influenza pandemic. Nat Immunol 2007, 8:1188-1193. (Pubitemid 350011755)
50. Fernandez-Sesma A, Marukian S, Ebersole BJ, Kaminski D, Park MS, Yuen T, Sealfon SC, Garcia-Sastre A, Moran TM: Influenza virus evades innate and adaptive immunity via the NS1 protein. J Virol 2006, 80:6295-6304. (Pubitemid 43927432)
51. Lee DC, Cheung CY, Law AH, Mok CK, Peiris M, Lau AS: p38 mitogenactivated protein kinase-dependent hyperinduction of tumor necrosis factor alpha expression in response to avian influenza virus H5N1. J Virol 2005, 79:10147-10154. (Pubitemid 41098555)
52. Ramirez F, Mason D: Induction of resistance to active experimental allergic encephalomyelitis by myelin basic protein-specific Th2 cell lines generated in the presence of glucocorticoids and IL-4. Eur J Immunol 2000, 30:747-758. (Pubitemid 30216246)
53. Yang Y, Weiner J, Liu Y, Smith AJ, Huss DJ, Winger R, Peng H, Cravens PD, Racke MK, Lovett-Racke AE: T-bet is essential for encephalitogenicity of both Th1 and Th17 cells. J Exp Med 2009, 206:1549-1564.
54. Cools N, Ponsaerts P, Van Tendeloo VF, Berneman ZN: Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells. J Leukoc Biol 2007, 82:1365-1374. (Pubitemid 350276946)
55. Niederkorn JY: Emerging concepts in CD8(+) T regulatory cells. Curr Opin Immunol 2008, 20:327-331.
56. Nakamura H, Kato T, Yamamura T, Yamamoto T, Umemoto S, Sekine T, Nishioka K, Matsuzaki M: Characterization of T cell receptor beta chains of accumulating T cells in chronic ongoing myocarditis demonstrated by heterotopic cardiac transplantation in mice. Jpn Circ J 2001, 65:106-110.
57. Kohm AP, Carpentier PA, Miller SD: Regulation of experimental autoimmune encephalomyelitis (EAE) by CD4+CD25+ regulatory T cells. Novartis Found Symp 2003, 252:45-52.
58. Knudsen GP: Gender bias in autoimmune diseases: X chromosome inactivation in women with multiple sclerosis. J Neurol Sci 2009, 286:43-46.
59. Disteche CM, Filippova GN, Tsuchiya KD: Escape from X inactivation. Cytogenet Genome Res 2002, 99:36-43. (Pubitemid 37467822)
60. Wijchers PJ, Festenstein RJ: Epigenetic regulation of autosomal gene expression by sex chromosomes. Trends Genet 2011.
61. Arnold AP: The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm Behav 2009, 55:570-578.
62. Martin JT: Sexual dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur J Pharmacol 2000, 405:251-261.
63. Huber SA, Kupperman J, Newell MK: Estradiol prevents and testosterone promotes Fas-dependent apoptosis in CD4+ Th2 cells by altering Bcl 2 expression. Lupus 1999, 8:384-387. (Pubitemid 29378019)