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Sex Differences in Susceptibility to Viral Infection

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Sex Hormones and Immunity to Infection

Abstract

Males and females differ in their susceptibility to a variety of viral pathogens. Although behavioral factors can influence exposure to viruses, several studies illustrate that physiological differences between males and females cause dimorphic responses to infection. Females often exhibit reduced susceptibility to viral infections because they typically mount stronger immune responses than males. Innate recognition and response to viruses as well as downstream adaptive immune responses differ between males and females during viral infections. This often results in sex differences in cytokine responses to infection that play a critical role in determining susceptibility to viruses. Immune responses to viruses can vary with changes in hormone concentrations naturally observed over the menstrual or estrous cycle, from contraception use, and during pregnancy.

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References

  • Aaby P, Ariyoshi K, Buckner M, Jensen H, Berry N, Wilkins A, Richard D, Larsen O, Dias F, Melbye M, Whittle H (1996) Age of wife as a major determinant of male-to-female transmission of HIV-2 infection: a community study from rural West Africa. Aids 10:1585–1590

    Article  PubMed  CAS  Google Scholar 

  • Ahlm C, Linderholm M, Juto P, Stegmayr B, Settergren B (1994) Prevalence of serum IgG antibodies to Puumala virus (haemorrhagic fever with renal syndrome) in northern Sweden. Epidemiol Infect 113:129–136

    Article  PubMed  CAS  Google Scholar 

  • Al-Harthi L, Kovacs A, Coombs RW, Reichelderfer PS, Wright DJ, Cohen MH, Cohn J, Cu-Uvin S, Watts H, Lewis S, Beckner S, Landay A (2001) A menstrual cycle pattern for cytokine levels exists in HIV-positive women: implication for HIV vaginal and plasma shedding. Aids 15:1535–1543

    Article  PubMed  CAS  Google Scholar 

  • Anderson D, Wilson J, Carthy C, Yang D, Kandolf R, McManus B (1996) Direct interactions of coxsackievirus B3 with immune cells in the splenic compartment of mice susceptible or resistant to myocarditis. J Virol 70:4632–4645

    PubMed  CAS  Google Scholar 

  • Araneo BA, Dowell T, Diegel M, Daynes RA (1991) 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 78:688–699

    PubMed  CAS  Google Scholar 

  • Armien B, Pascale JM, Bayard V, Munoz C, Mosca I, Guerrero G, Armien A, Quiroz E, Castillo Z, Zaldivar Y, Gracia F, Hjelle B, Koster F (2004) High seroprevalence of hantavirus infection on the Azuero peninsula of Panama. Am J Trop Med Hyg 70:682–687

    PubMed  Google Scholar 

  • Baeten JM, Benki S, Chohan V, Lavreys L, McClelland RS, Mandaliya K, Ndinya-Achola JO, Jaoko W, Overbaugh J (2007) Hormonal contraceptive use, herpes simplex virus infection, and risk of HIV-1 acquisition among Kenyan women. Aids 21:1771–1777

    Article  PubMed  Google Scholar 

  • Barna M, Komatsu T, Bi Z, Reiss CS (1996) Sex differences in susceptibility to viral infection of the central nervous system. J Neuroimmunol 67:31–39

    PubMed  Google Scholar 

  • Barrat F, Lesourd B, Boulouis HJ, Thibault D, Vincent-Naulleau S, Gjata B, Louise A, Neway T, Pilet C (1997) Sex and parity modulate cytokine production during murine ageing. Clin Exp Immunol 109:562–568

    Article  PubMed  CAS  Google Scholar 

  • Bazzoni G (2006) Endothelial tight junctions: permeable barriers of the vessel wall. Thromb Haemost 95:36–42

    PubMed  CAS  Google Scholar 

  • Benki S, Mostad SB, Richardson BA, Mandaliya K, Kreiss JK, Overbaugh J (2004) Cyclic shedding of HIV-1 RNA in cervical secretions during the menstrual cycle. J Infect Dis 189:2192–2201

    Article  PubMed  CAS  Google Scholar 

  • Benki S, Mostad SB, Richardson BA, Mandaliya K, Kreiss JK, Overbaugh J (2008) Increased Levels of HIV-1-Infected Cells in Endocervical Secretions After the Luteinizing Hormone Surge. J Acquir Immune Defic Syndr 47:529–534

    Article  PubMed  CAS  Google Scholar 

  • Bergelson JM, Mohanty JG, Crowell RL, St John NF, Lublin DM, Finberg RW (1995) Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55). J Virol 69:1903–1906

    PubMed  CAS  Google Scholar 

  • Berghofer B, Frommer T, Haley G, Fink L, Bein G, Hackstein H (2006) TLR7 ligands induce higher IFN-alpha production in females. J Immunol 177:2088–2096

    PubMed  Google Scholar 

  • Bernshtein AD, Apekina NS, Mikhailova TV, Myasnikov YA, Khlyap LA, Korotkov YS, Gavrilovskaya IN (1999) Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrinomys glareolus). Arch Virol 144:2415–2428

    Article  PubMed  CAS  Google Scholar 

  • Bihl F, Brahic M, Bureau JF (1999) Two loci, Tmevp2 and Tmevp3, located on the telomeric region of chromosome 10, control the persistence of Theiler’s virus in the central nervous system of mice. Genetics 152:385–392

    PubMed  CAS  Google Scholar 

  • Bijlsma JW, Cutolo M, Masi AT, Chikanza IC (1999) The neuroendocrine immune basis of rheumatic diseases. Immunol Today 20:298–301

    Article  PubMed  CAS  Google Scholar 

  • Bowles NE, Ni J, Kearney DL, Pauschinger M, Schultheiss HP, McCarthy R, Hare J, Bricker JT, Bowles KR, Towbin JA (2003) 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 42:466–472

    Article  PubMed  Google Scholar 

  • Brabin L (2002) Interactions of the female hormonal environment, susceptibility to viral infections, and disease progression. AIDS Patient Care STDS 16:211–221

    Article  PubMed  Google Scholar 

  • Brahmachary M, Schonbach C, Yang L, Huang E, Tan SL, Chowdhary R, Krishnan SP, Lin CY, Hume DA, Kai C, Kawai J, Carninci P, Hayashizaki Y, Bajic VB (2006) Computational promoter analysis of mouse, rat and human antimicrobial peptide-coding genes. BMC Bioinformatics 7(Suppl 5):S8

    Article  PubMed  CAS  Google Scholar 

  • Brownstein DG, Gras L (1995) Chromosome mapping of Rmp-4, a gonad-dependent gene encoding host resistance to mousepox. J Virol 69:6958–6964

    PubMed  CAS  Google Scholar 

  • Brownstein DG, Bhatt PN, Gras L, Jacoby RO (1991) Chromosomal locations and gonadal dependence of genes that mediate resistance to ectromelia (mousepox) virus-induced mortality. J Virol 65:1946–1951

    PubMed  CAS  Google Scholar 

  • Bruland T, Lavik LA, Dai HY, Dalen A (2003) A glucocorticoid response element in the LTR U3 region of Friend murine leukaemia virus variant FIS-2 enhances virus production in vitro and is a major determinant for sex differences in susceptibility to FIS-2 infection in vivo. J Gen Virol 84:907–916

    Article  CAS  Google Scholar 

  • Burgoyne PS, Lovell-Badge R, Rattigan A (2001) Evidence that the testis determination pathway interacts with a non-dosage compensated, X-linked gene. Int J Dev Biol 45:509–512

    PubMed  CAS  Google Scholar 

  • Butterfield RJ, Roper RJ, Rhein DM, Melvold RW, Haynes L, Ma RZ, Doerge RW, Teuscher C (2003) Sex-specific quantitative trait loci govern susceptibility to Theiler’s murine encephalomyelitis virus-induced demyelination. Genetics 163:1041–1046

    PubMed  CAS  Google Scholar 

  • Canning CA, Lovell-Badge R (2002) Sry and sex determination: how lazy can it be? Trends Genet 18:111–113

    Article  PubMed  CAS  Google Scholar 

  • Caramalho I, Lopes-Carvalho T, Ostler D, Zelenay S, Haury M, Demengeot J (2003) Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide. J Exp Med 197:403–411

    Article  PubMed  CAS  Google Scholar 

  • Carson SD (2001) Receptor for the group B coxsackieviruses and adenoviruses: CAR. Rev Med Virol 11:219–226

    Article  PubMed  CAS  Google Scholar 

  • Carson SD, Chapman NM (2001) Coxsackievirus and adenovirus receptor (CAR) binds immunoglobulins. Biochemistry 40:14324–14329

    Article  PubMed  CAS  Google Scholar 

  • Cato AC, Miksicek R, Schutz G, Arnemann J, Beato M (1986) The hormone regulatory element of mouse mammary tumour virus mediates progesterone induction. Embo J 5:2237–2240

    PubMed  CAS  Google Scholar 

  • Chang TH, Liao CL, Lin YL (2006) Flavivirus induces interferon-beta gene expression through a pathway involving RIG-I-dependent IRF-3 and PI3K-dependent NF-kappaB activation. Microbes Infect 8:157–171

    Article  PubMed  CAS  Google Scholar 

  • Chellappan S, Kraus VB, Kroger B, Munger K, Howley PM, Phelps WC, Nevins JR (1992) Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc Natl Acad Sci USA 89:4549–4553

    Article  PubMed  CAS  Google Scholar 

  • Cheung TC, Humphreys IR, Potter KG, Norris PS, Shumway HM, Tran BR, Patterson G, Jean-Jacques R, Yoon M, Spear PG, Murphy KM, Lurain NS, Benedict CA, Ware CF (2005) Evolutionarily divergent herpesviruses modulate T cell activation by targeting the herpesvirus entry mediator cosignaling pathway. Proc Natl Acad Sci USA 102:13218–13223

    Article  PubMed  CAS  Google Scholar 

  • Childs JE, Glass GE, Korch GW, LeDuc JW (1988) The ecology and epizootiology of hantaviral infections in small mammal communities of Baltimore: A review and synthesis. Bulletin of the Society of Vector Biology 13:113–122

    Google Scholar 

  • Childs JE, Ksiazek TG, Spiropoulou CF, Krebs JW, Morzunov S, Maupin GO, Gage KL, Rollin PE, Sarisky J, Enscore RE et al (1994) Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States. J Infect Dis 169:1271–1280

    PubMed  CAS  Google Scholar 

  • Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, Ponath PD, Wu L, Mackay CR, LaRosa G, Newman W, Gerard N, Gerard C, Sodroski J (1996) The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135–1148

    Article  PubMed  CAS  Google Scholar 

  • Clemetson DB, Moss GB, Willerford DM, Hensel M, Emonyi W, Holmes KK, Plummer F, Ndinya-Achola J, Roberts PL, Hillier S et al (1993) Detection of HIV DNA in cervical and vaginal secretions. Prevalence and correlates among women in Nairobi, Kenya. Jama 269:2860–2864

    Article  PubMed  CAS  Google Scholar 

  • Collman RG, Yi Y, Liu QH, Freedman BD (2000) Chemokine signaling and HIV-1 fusion mediated by macrophage CXCR4: implications for target cell tropism. J Leukoc Biol 68:318–323

    PubMed  CAS  Google Scholar 

  • D’Addario M, Ahmad A, Xu JW, Menezes J (1999) Epstein-Barr virus envelope glycoprotein gp350 induces NF-kappaB activation and IL-1beta synthesis in human monocytes-macrophages involving PKC and PI3-K. Faseb J 13:2203–2213

    PubMed  Google Scholar 

  • D’Addario M, Ahmad A, Morgan A, Menezes J (2000) Binding of the Epstein-Barr virus major envelope glycoprotein gp350 results in the upregulation of the TNF-alpha gene expression in monocytic cells via NF-kappaB involving PKC, PI3-K and tyrosine kinases. J Mol Biol 298:765–778

    Article  PubMed  CAS  Google Scholar 

  • D’Addario M, Libermann TA, Xu J, Ahmad A, Menezes J (2001) Epstein-Barr Virus and its glycoprotein-350 upregulate IL-6 in human B-lymphocytes via CD21, involving activation of NF-kappaB and different signaling pathways. J Mol Biol 308:501–514

    Article  PubMed  CAS  Google Scholar 

  • Darbre P, Page M, King RJ (1986) Androgen regulation by the long terminal repeat of mouse mammary tumor virus. Mol Cell Biol 6:2847–2854

    PubMed  CAS  Google Scholar 

  • Daughaday CC, Brandt WE, McCown JM, Russell PK (1981) Evidence for two mechanisms of dengue virus infection of adherent human monocytes: trypsin-sensitive virus receptors and trypsin-resistant immune complex receptors. Infect Immun 32:469–473

    PubMed  CAS  Google Scholar 

  • Del Corno M, Liu QH, Schols D, de Clercq E, Gessani S, Freedman BD, Collman RG (2001) HIV-1 gp120 and chemokine activation of Pyk2 and mitogen-activated protein kinases in primary macrophages mediated by calcium-dependent, pertussis toxin-insensitive chemokine receptor signaling. Blood 98:2909–2916

    Article  PubMed  Google Scholar 

  • DiMaio D, Lai CC, Klein O (1998) Virocrine transformation: the intersection between viral transforming proteins and cellular signal transduction pathways. Annu Rev Microbiol 52:397–421

    Article  PubMed  CAS  Google Scholar 

  • Dobner T, Horikoshi N, Rubenwolf S, Shenk T (1996) Blockage by adenovirus E4orf6 of transcriptional activation by the p53 tumor suppressor. Science 272:1470–1473

    Article  PubMed  CAS  Google Scholar 

  • Domingo E (2000) Viruses at the edge of adaptation. Virology 270:251–253

    Article  PubMed  CAS  Google Scholar 

  • Domingo E, Holland J (1997) RNA virus mutations and fitness for survival. Am Rev Microbiol 51:151–178

    Article  CAS  Google Scholar 

  • Donaldson DD, Whitters MJ, Fitz LJ, Neben TY, Finnerty H, Henderson SL, O′Hara RM Jr, Beier DR, Turner KJ, Wood CR, Collins M (1998) The murine IL-13 receptor alpha 2: molecular cloning, characterization, and comparison with murine IL-13 receptor alpha 1. J Immunol 161:2317–2324

    PubMed  CAS  Google Scholar 

  • Douglass RJ, Calisher CH, Wagoner KD, Mills JN (2007) Sin nombre virus infection of deer mice in montana: characteristics of newly infected mice, incidence, and temporal pattern of infection. J Wildl Dis 43:12–22

    PubMed  Google Scholar 

  • Easterbrook JD, Klein SL (2008) Corticosteroids modulate Seoul virus infection, regulatory T-cell responses and matrix metalloprotease 9 expression in male, but not female, Norway rats. J Gen Virol 89:2723–2730

    Article  PubMed  CAS  Google Scholar 

  • Easterbrook JD, Kaplan JB, Glass GE, Pletnikov MV, Klein SL (2007) Elevated testosterone and reduced 5-HIAA concentrations are associated with wounding and hantavirus infection in male Norway rats. Horm Behav 52(4):474–481

    Article  PubMed  CAS  Google Scholar 

  • Eigen M (1993) Viral quasispecies. Sci Am 269:42–49

    Article  PubMed  CAS  Google Scholar 

  • Epp T, Waldner C, West K, Townsend H (2007) Factors associated with West Nile virus disease fatalities in horses. Can Vet J 48:1137–1145

    PubMed  Google Scholar 

  • Falter H, Persinger MA, Reid K (1991) Sex differences in primary humoral responses of albino rats to human serum albumin. Immunol Lett 28:143–145

    Article  PubMed  CAS  Google Scholar 

  • Farzadegan H, Hoover DR, Astemborski J, Lyles CM, Margolick JB, Markham RB, Quinn TC, Vlahov D (1998) Sex differences in HIV-1 viral load and progression to AIDS. Lancet 352:1510–1514

    Article  PubMed  CAS  Google Scholar 

  • Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872–877

    Article  PubMed  CAS  Google Scholar 

  • Ferrer JF, Jonsson CB, Esteban E, Galligan D, Basombrio MA, Peralta-Ramos M, Bharadwaj M, Torrez-Martinez N, Callahan J, Segovia A, Hjelle B (1998) High prevalence of hantavirus infection in Indian communities of the Paraguayan and Argentinean Gran Chaco. Am J Trop Med Hyg 59:438–444

    PubMed  CAS  Google Scholar 

  • Fitzgerald-Bocarsly P, Dai J, Singh S (2008) Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev 19:3–19

    Article  PubMed  CAS  Google Scholar 

  • Fleming DT, McQuillan GM, Johnson RE, Nahmias AJ, Aral SO, Lee FK, St Louis ME (1997) Herpes simplex virus type 2 in the United States, 1976 to 1994. N Engl J Med 337:1105–1111

    Article  PubMed  CAS  Google Scholar 

  • Fox HS, Bond BL, Parslow TG (1991) Estrogen regulates the IFN-gamma promoter. J Immunol 146:4362–4367

    PubMed  CAS  Google Scholar 

  • Friedman SB, Grota LJ, Glasgow LA (1972) Differential susceptibility of male and female mice to encephalomyocarditis virus: effects of castration, adrenalectomy, and the administration of sex hormones. Infect Immun 5:637–644

    PubMed  CAS  Google Scholar 

  • Frisancho-Kiss S, Davis SE, Nyland JF, Frisancho JA, Cihakova D, Barrett MA, Rose NR, Fairweather D (2007) Cutting edge: cross-regulation by TLR4 and T cell Ig mucin-3 determines sex differences in inflammatory heart disease. J Immunol 178:6710–6714

    PubMed  CAS  Google Scholar 

  • Fuller A, Yahikozawa H, So EY, Dal Canto M, Koh CS, Welsh CJ, Kim BS (2007) Castration of male C57L/J mice increases susceptibility and estrogen treatment restores resistance to Theiler’s virus-induced demyelinating disease. J Neurosci Res 85:871–881

    Article  PubMed  CAS  Google Scholar 

  • Gallichan WS, Rosenthal KL (1996) Effects of the estrous cycle on local humoral immune responses and protection of intranasally immunized female mice against herpes simplex virus type 2 infection in the genital tract. Virology 224:487–497

    Article  PubMed  CAS  Google Scholar 

  • Garenne M (1994) Sex differences in measles mortality: a world review. Int J Epidemiol 23:632–642

    Article  PubMed  CAS  Google Scholar 

  • Gavrilovskaya IN, Shepley M, Shaw R, Ginsberg MH, Mackow ER (1998) beta3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci USA 95:7074–7079

    Article  PubMed  CAS  Google Scholar 

  • Gillgrass AE, Ashkar AA, Rosenthal KL, Kaushic C (2003) Prolonged exposure to progesterone prevents induction of protective mucosal responses following intravaginal immunization with attenuated herpes simplex virus type 2. J Virol 77:9845–9851

    Article  PubMed  CAS  Google Scholar 

  • Giron DJ, Patterson RR (1982) Effect of steroid hormones on virus-induced diabetes mellitus. Infect Immun 37:820–822

    PubMed  CAS  Google Scholar 

  • Giron DJ, Allen PT, Pindak FF, Schmidt JP (1973) Further studies on the influence of steroids on viral infection in mice. Infect Immun 8:151–155

    PubMed  CAS  Google Scholar 

  • Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, Flavell RA, Diamond MS, Colonna M (2006) Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci USA 103:8459–8464

    Article  PubMed  CAS  Google Scholar 

  • Glass GE, Childs JE, Korch GW, LeDuc JW (1988) Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol Infect 101:459–472

    Article  PubMed  CAS  Google Scholar 

  • Glass GE, Livingstone W, Mills JN, Hlady WG, Fine JB, Biggler W, Coke T, Frazier D, Atherley S, Rollin PE, Ksiazek TG, Peters CJ, Childs JE (1998) Black Creek Canal Virus infection in Sigmodon hispidus in southern Florida. Am J Trop Med Hyg 59:699–703

    PubMed  CAS  Google Scholar 

  • Gomez E, Ortiz V, Saint-Martin B, Boeck L, Diaz-Sanchez V, Bourges H (1993) Hormonal regulation of the secretory IgA (sIgA) system: estradiol- and progesterone-induced changes in sIgA in parotid saliva along the menstrual cycle. Am J Reprod Immunol 29:219–223

    PubMed  CAS  Google Scholar 

  • Groschel S, Piggott KD, Vaglio A, Ma-Krupa W, Singh K, Goronzy JJ, Weyand CM (2008) TLR-mediated induction of negative regulatory ligands on dendritic cells. J Mol Med 86:443–455

    Article  PubMed  CAS  Google Scholar 

  • Haeryfar SM (2005) The importance of being a pDC in antiviral immunity: the IFN mission versus Ag presentation? Trends Immunol 26:311–317

    Article  PubMed  CAS  Google Scholar 

  • Han X, Lundberg P, Tanamachi B, Openshaw H, Longmate J, Cantin E (2001) Gender influences herpes simplex virus type 1 infection in normal and gamma interferon-mutant mice. J Virol 75:3048–3052

    Article  PubMed  CAS  Google Scholar 

  • Hanna L (1999) The menstrual cycle and viral load. Beta 12:18

    Google Scholar 

  • Hannah MF, Bajic VB, Klein SL (2008) Sex differences in the recognition of and innate antiviral responses to Seoul virus in Norway rats. Brain Behav Immun 22(4):503–516

    Article  PubMed  CAS  Google Scholar 

  • Hardarson HS, Baker JS, Yang Z, Purevjav E, Huang CH, Alexopoulou L, Li N, Flavell RA, Bowles NE, Vallejo JG (2007) Toll-like receptor 3 is an essential component of the innate stress response in virus-induced cardiac injury. Am J Physiol Heart Circ Physiol 292:H251–H258

    Article  PubMed  CAS  Google Scholar 

  • Hinson ER, Shone SM, Zink MC, Glass GE, Klein SL (2004) Wounding: the primary mode of Seoul virus transmission among male Norway rats. Am J Trop Med Hyg 70:310–317

    PubMed  Google Scholar 

  • Hornung V, Schlender J, Guenthner-Biller M, Rothenfusser S, Endres S, Conzelmann KK, Hartmann G (2004) Replication-dependent potent IFN-alpha induction in human plasmacytoid dendritic cells by a single-stranded RNA virus. J Immunol 173:5935–5943

    PubMed  CAS  Google Scholar 

  • Howell AL, Asin SN, Yeaman GR, Wira CR (2005) HIV-1 infection of the female reproductive tract. Curr HIV/AIDS Rep 2:35–38

    Article  PubMed  Google Scholar 

  • Huber S, Job L, Auld K (1982) Influence of sex hormones on coxsackie B3 virus infection in Balb/c mice. Cell Immunol 67:173–179

    Article  PubMed  CAS  Google Scholar 

  • Huber S, Kupperman J, Newell M (1999) Hormonal regulation of CD4+ T-cell responses in coxsackievirus B3-induced myocarditis in mice. J Virol 73:4689–4695

    PubMed  CAS  Google Scholar 

  • Huber S, Shi C, Budd RC (2002a) Gammadelta T cells promote a Th1 response during coxsackievirus B3 infection in vivo: role of Fas and Fas ligand. J Virol 76:6487–6494

    Article  PubMed  CAS  Google Scholar 

  • Huber SA, Sartini D, Exley M (2002b) Vgamma4(+) T cells promote autoimmune CD8(+) cytolytic T-lymphocyte activation in coxsackievirus B3-induced myocarditis in mice: role for CD4(+) Th1 cells. J Virol 76:10785–10790

    Article  PubMed  CAS  Google Scholar 

  • Jean CM, Honarmand S, Louie JK, Glaser CA (2007) Risk factors for West Nile virus neuroinvasive disease, California, 2005. Emerg Infect Dis 13:1918–1920

    PubMed  Google Scholar 

  • Jung JU, Stager M, Desrosiers RC (1994) Virus-encoded cyclin. Mol Cell Biol 14:7235–7244

    PubMed  CAS  Google Scholar 

  • Katagiri D, Hayashi H, Victoriano AF, Okamoto T, Onozaki K (2006) Estrogen stimulates transcription of human immunodeficiency virus type 1 (HIV-1). Int Immunopharmacol 6:170–181

    Article  PubMed  CAS  Google Scholar 

  • Kawai T, Akira S (2006) Innate immune recognition of viral infection. Nat Immunol 7:131–137

    Article  PubMed  CAS  Google Scholar 

  • Klein SL (2000) The effects of hormones on sex differences in infection: from genes to behavior. Neurosci Biobehav Rev 24:627–638

    Article  PubMed  CAS  Google Scholar 

  • Klein SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 79:441–449

    Article  PubMed  CAS  Google Scholar 

  • Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264

    Article  PubMed  CAS  Google Scholar 

  • Klein SL, Calisher CH (2007) Emergence and persistence of hantaviruses. Curr Top Microbiol Immunol 315:217–252

    Article  PubMed  CAS  Google Scholar 

  • Klein SL, Bird BH, Glass GE (2000) Sex differences in Seoul virus infection are not related to adult sex steroid concentrations in Norway rats. J Virol 74:8213–8217

    Article  PubMed  CAS  Google Scholar 

  • Klein SL, Bird BH, Glass GE (2001) Sex differences in immune responses and viral shedding following Seoul virus infection in Norway rats. Am J Trop Med Hyg 65:57–63

    PubMed  CAS  Google Scholar 

  • Klein SL, Marson AL, Scott AL, Ketner G, Glass GE (2002) Neonatal sex steroids affect responses to Seoul virus infection in male but not female Norway rats. Brain Behav Immun 16:736–746

    Article  PubMed  CAS  Google Scholar 

  • Klein SL, Cernetich A, Hilmer S, Hoffman EP, Scott AL, Glass GE (2004) Differential expression of immunoregulatory genes in male and female Norway rats following infection with Seoul virus. J Med Virol 74:180–190

    Article  PubMed  CAS  Google Scholar 

  • Klingstrom J, Lindgren T, Ahlm C (2008) Hantavirus infection induces higher plasma levels of IL-9, FGF-2 and GM-CSF, and lower levels of IL-8 and IP-10, in females compared to males. Clin Vaccine Immunol doi:10.1128/CVI.00035-08

    Google Scholar 

  • Knudsen KM, Aaby P, Whittle H, Rowe M, Samb B, Simondon F, Sterne J, Fine P (1996) Child mortality following standard, medium or high titre measles immunization in West Africa. Int J Epidemiol 25:665–673

    Article  PubMed  CAS  Google Scholar 

  • Kolesnitchenko V, Snart RS (1992) Regulatory elements in the human immunodeficiency virus type 1 long terminal repeat LTR (HIV-1) responsive to steroid hormone stimulation. AIDS Res Hum Retroviruses 8:1977–1980

    Article  PubMed  CAS  Google Scholar 

  • Kubarek L, Jagodzinski PP (2007) Epigenetic up-regulation of CXCR4 and CXCL12 expression by 17 beta-estradiol and tamoxifen is associated with formation of DNA methyltransferase 3B4 splice variant in Ishikawa endometrial adenocarcinoma cells. FEBS Lett 581:1441–1448

    Article  PubMed  CAS  Google Scholar 

  • Kumar H, Kawai T, Kato H, Sato S, Takahashi K, Coban C, Yamamoto M, Uematsu S, Ishii KJ, Takeuchi O, Akira S (2006) Essential role of IPS-1 in innate immune responses against RNA viruses. J Exp Med 203:1795–1803

    Article  PubMed  CAS  Google Scholar 

  • Lamey PJ, Ferguson MM, Marshall W (1985) Sex hormone involvement in the development of experimental virally induced murine salivary gland tumors. J Oral Pathol 14:414–421

    Article  PubMed  CAS  Google Scholar 

  • Langenberg AG, Corey L, Ashley RL, Leong WP, Straus SE (1999) A prospective study of new infections with herpes simplex virus type 1 and type 2. Chiron HSV Vaccine Study Group. N Engl J Med 341:1432–1438

    CAS  Google Scholar 

  • Leclerc PM, Dubois-Colas N, Garenne M (2008) Hormonal contraception and HIV prevalence in four African countries. Contraception 77:371–376

    Article  PubMed  Google Scholar 

  • Lehmer EM, Clay CA, Wilson E, St Jeor S, Dearing MD (2007) Differential resource allocation in deer mice exposed to sin nombre virus. Physiol Biochem Zool 80:514–521

    Article  PubMed  Google Scholar 

  • Lenz F (1931) Morbidic hereditary factors. Macmillan Press, New York

    Google Scholar 

  • Leopold PL, Crystal RG (2007) Intracellular trafficking of adenovirus: many means to many ends. Adv Drug Deliv Rev 59:810–821

    Article  PubMed  CAS  Google Scholar 

  • Li CF, Ross FP, Cao X, Teitelbaum SL (1995) Estrogen enhances alpha v beta 3 integrin expression by avian osteoclast precursors via stabilization of beta 3 integrin mRNA. Mol Endocrinol 9:805–813

    Article  PubMed  CAS  Google Scholar 

  • Li SH, Huang HL, Chen YH (2002) Ovarian steroid-regulated synthesis and secretion of complement C3 and factor B in mouse endometrium during the natural estrous cycle and pregnancy period. Biol Reprod 66:322–332

    Article  PubMed  CAS  Google Scholar 

  • Little TV, Holyoak GR, McCollum WH, Timoney PJ (1992) Output of equine arteritis virus from persistently infected stallions is testosterone-dependent. In:Proceedings of the sixth international conference on equine infectious diseases pp 225–229

    Google Scholar 

  • Liu P, Aitken K, Kong YY, Opavsky MA, Martino T, Dawood F, Wen WH, Kozieradzki I, Bachmaier K, Straus D, Mak TW, Penninger JM (2000a) The tyrosine kinase p56lck is essential in coxsackievirus B3-mediated heart disease. Nat Med 6:429–434

    Article  PubMed  CAS  Google Scholar 

  • Liu QH, Williams DA, McManus C, Baribaud F, Doms RW, Schols D, De Clercq E, Kotlikoff MI, Collman RG, Freedman BD (2000b) HIV-1 gp120 and chemokines activate ion channels in primary macrophages through CCR5 and CXCR4 stimulation. Proc Natl Acad Sci USA 97:4832–4837

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Miwa T, Hilliard B, Chen Y, Lambris JD, Wells AD, Song WC (2005) The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J Exp Med 201:567–577

    Article  PubMed  CAS  Google Scholar 

  • Lyden D, Huber S (1984) Aggrevation of coxsackievirus group B type 3-induced myocarditis and increase in cellular immunity to myocyte antigens in pregnant BALB/c mice and animals treated with progesterone. Cell Immunol 87:462–472

    Article  PubMed  CAS  Google Scholar 

  • Lyden DC, Olszewski J, Feran M, Job LP, Huber SA (1987) Coxsackievirus B-3-induced myocarditis. Effect of sex steroids on viremia and infectivity of cardiocytes. Am J Pathol 126:432–438

    CAS  Google Scholar 

  • Maddon PJ, Dalgleish AG, McDougal JS, Clapham PR, Weiss RA, Axel R (1986) The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 47:333–348

    Article  PubMed  CAS  Google Scholar 

  • Marx PA, Spira AI, Gettie A, Dailey PJ, Veazey RS, Lackner AA, Mahoney CJ, Miller CJ, Claypool LE, Ho DD, Alexander NJ (1996) Progesterone implants enhance SIV vaginal transmission and early virus load. Nat Med 2:1084–1089

    Article  PubMed  CAS  Google Scholar 

  • McCollum WH, Little TV, Timoney PJ, Swerczek TW (1994) Resistance of castrated male horses to attempted establishment of the carrier state with equine arteritis virus. J Comp Pathol 111:383–388

    Article  PubMed  CAS  Google Scholar 

  • McIntyre NE, Chu YK, Owen RD, Abuzeineh A, De la Sancha N, Dick CW, Holsomback T, Nisbett RA, Jonsson C (2005) A longitudinal study of Bayou virus, hosts, and habitat. Am J Trop Med Hyg 73:1043–1049

    PubMed  Google Scholar 

  • Medof ME, Walter EI, Rutgers JL, Knowles DM, Nussenzweig V (1987) Identification of the complement decay-accelerating factor (DAF) on epithelium and glandular cells and in body fluids. J Exp Med 165:848–864

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R, Janeway CA Jr (2002) Decoding the patterns of self and nonself by the innate immune system. Science 296:298–300

    Article  PubMed  CAS  Google Scholar 

  • Melchjorsen J, Jensen SB, Malmgaard L, Rasmussen SB, Weber F, Bowie AG, Matikainen S, Paludan SR (2005) Activation of innate defense against a paramyxovirus is mediated by RIG-I and TLR7 and TLR8 in a cell-type-specific manner. J Virol 79:12944–12951

    Article  PubMed  CAS  Google Scholar 

  • Mertz GJ, Benedetti J, Ashley R, Selke SA, Corey L (1992) Risk factors for the sexual transmission of genital herpes. Ann Intern Med 116:197–202

    PubMed  CAS  Google Scholar 

  • Mills JN, Ellis BA, McKee KT Jr, Calderon GE, Maiztegui JI, Nelson GO, Ksiazek TG, Peters CJ, Childs JE (1992) A longitudinal study of Junin virus activity in the rodent reservoir of Argentine hemorrhagic fever. Am J Trop Med Hyg 47:749–763

    PubMed  CAS  Google Scholar 

  • Mills JN, Ellis BA, Childs JE, McKee KT Jr, Maiztegui JI, Peters CJ, Ksiazek TG, Jahrling PB (1994) Prevalence of infection with Junin virus in rodent populations in the epidemic area of Argentine hemorrhagic fever. Am J Trop Med Hyg 51:554–562

    PubMed  CAS  Google Scholar 

  • Mills JN, Ksiazek TG, Ellis BA, Rollin PE, Nichol ST, Yates TL, Gannon WL, Levy CE, Engelthaler DM, Davis T, Tanda DT, Frampton JW, Nichols CR, Peters CJ, Childs JE (1997) Patterns of association with host and habitat: antibody reactive with Sin Nombre virus in small mammals in the major biotic communities of the southwestern United States. Am J Trop Med Hyg 56:273–284

    PubMed  CAS  Google Scholar 

  • Mills JN, Johnson JM, Ksiazek TG, Ellis BA, Rollin PE, Yates TL, Mann MO, Johnson MR, Campbell ML, Miyashiro J, Patrick M, Zyzak M, Lavender D, Novak MG, Schmidt K, Peters CJ, Childs JE (1998) A survey of hantavirus antibody in small-mammal populations in selected United States National Parks. Am J Trop Med Hyg 58:525–532

    PubMed  CAS  Google Scholar 

  • Mirand EA, Back N, Grace JT Jr, Buffet R (1967) Effect of pituitary and gonadal hormones on Friend Virus Disease in mice. Proc Soc Exp Biol Med 124:1055–1059

    Google Scholar 

  • Misse D, Esteve PO, Renneboog B, Vidal M, Cerutti M, St Pierre Y, Yssel H, Parmentier M, Veas F (2001) HIV-1 glycoprotein 120 induces the MMP-9 cytopathogenic factor production that is abolished by inhibition of the p38 mitogen-activated protein kinase signaling pathway. Blood 98:541–547

    Article  PubMed  CAS  Google Scholar 

  • Mo R, Chen J, Grolleau-Julius A, Murphy HS, Richardson BC, Yung RL (2005) Estrogen regulates CCR gene expression and function in T lymphocytes. J Immunol 174:6023–6029

    PubMed  CAS  Google Scholar 

  • Morrow PL, Freedman A, Craighead JE (1980) Testosterone effect on experimental diabetes mellitus in encephalomyocarditis (EMC) virus infected mice. Diabetologia 18:247–249

    Article  PubMed  CAS  Google Scholar 

  • Mostad SB, Overbaugh J, DeVange DM, Welch MJ, Chohan B, Mandaliya K, Nyange P, Martin HL Jr, Ndinya-Achola J, Bwayo JJ, Kreiss JK (1997) Hormonal contraception, vitamin A deficiency, and other risk factors for shedding of HIV-1 infected cells from the cervix and vagina. Lancet 350:922–927

    Article  PubMed  CAS  Google Scholar 

  • Mostad SB, Kreiss JK, Ryncarz A, Chohan B, Mandaliya K, Ndinya-Achola J, Bwayo JJ, Corey L (2000a) Cervical shedding of herpes simplex virus and cytomegalovirus throughout the menstrual cycle in women infected with human immunodeficiency virus type 1. Am J Obstet Gynecol 183:948–955

    Article  PubMed  CAS  Google Scholar 

  • Mostad SB, Kreiss JK, Ryncarz AJ, Mandaliya K, Chohan B, Ndinya-Achola J, Bwayo JJ, Corey L (2000b) Cervical shedding of herpes simplex virus in human immunodeficiency virus-infected women: effects of hormonal contraception, pregnancy, and vitamin A deficiency. J Infect Dis 181:58–63

    Article  PubMed  CAS  Google Scholar 

  • Muller D, Chen M, Vikingsson A, Hildeman D, Pederson K (1995) Oestrogen influences CD4+ T-lymphocyte activity in vivo and in vitro in beta 2-microglobulin-deficient mice. Immunology 86:162–167

    PubMed  CAS  Google Scholar 

  • Munk C, Zielonka J, Constabel H, Kloke BP, Rengstl B, Battenberg M, Bonci F, Pistello M, Lochelt M, Cichutek K (2007) Multiple restrictions of human immunodeficiency virus type 1 in feline cells. J Virol 81:7048–7060

    Article  PubMed  CAS  Google Scholar 

  • Napravnik S, Poole C, Thomas JC, Eron JJ Jr (2002) Gender difference in HIV RNA levels: a meta-analysis of published studies. J Acquir Immune Defic Syndr 31:11–19

    PubMed  CAS  Google Scholar 

  • Nassal M (2008) Hepatitis B viruses: Reverse transcription a different way. Virus Res 134(1–2):235–249

    Article  PubMed  CAS  Google Scholar 

  • Nie CQ, Bernard NJ, Schofield L, Hansen DS (2007) CD4+ CD25+ regulatory T cells suppress CD4+ T-cell function and inhibit the development of Plasmodium berghei-specific TH1 responses involved in cerebral malaria pathogenesis. Infect Immun 75:2275–2282

    Article  PubMed  CAS  Google Scholar 

  • Niermann GL, Buehring GC (1997) Hormone regulation of bovine leukemia virus via the long terminal repeat. Virology 239:249–258

    Article  PubMed  CAS  Google Scholar 

  • Nieva JL, Agirre A (2003) Are fusion peptides a good model to study viral cell fusion? Biochim Biophys Acta 1614:104–115

    Article  PubMed  CAS  Google Scholar 

  • Nohara K, Izumi H, Tamura S, Nagata R, Tohyama C (2002) Effect of low-dose 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) on influenza A virus-induced mortality in mice. Toxicology 170:131–138

    Article  PubMed  CAS  Google Scholar 

  • Obasi A, Mosha F, Quigley M, Sekirassa Z, Gibbs T, Munguti K, Todd J, Grosskurth H, Mayaud P, Changalucha J, Brown D, Mabey D, Hayes R (1999) Antibody to herpes simplex virus type 2 as a marker of sexual risk behavior in rural Tanzania. J Infect Dis 179:16–24

    Article  PubMed  CAS  Google Scholar 

  • O’Leary DR, Marfin AA, Montgomery SP, Kipp AM, Lehman JA, Biggerstaff BJ, Elko VL, Collins PD, Jones JE, Campbell GL (2004) The epidemic of West Nile virus in the United States, 2002. Vector Borne Zoonotic Dis 4:61–70

    Article  PubMed  Google Scholar 

  • Olsson GE, White N, Ahlm C, Elgh F, Verlemyr AC, Juto P, Palo RT (2002) Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 8:924–929

    PubMed  Google Scholar 

  • Otten AD, Sanders MM, McKnight GS (1988) The MMTV LTR promoter is induced by progesterone and dihydrotestosterone but not by estrogen. Mol Endocrinol 2:143–147

    Article  PubMed  CAS  Google Scholar 

  • Palaszynski KM, Smith DL, Kamrava S, Burgoyne PS, Arnold AP, Voskuhl RR (2005) A yin-yang effect between sex chromosome complement and sex hormones on the immune response. Endocrinology 146:3280–3285

    Article  PubMed  CAS  Google Scholar 

  • Parr MB, Kepple L, McDermott MR, Drew MD, Bozzola JJ, Parr EL (1994) A mouse model for studies of mucosal immunity to vaginal infection by herpes simplex virus type 2. Lab Invest 70:369–380

    PubMed  CAS  Google Scholar 

  • Pearce-Duvet JM, St Jeor SC, Boone JD, Dearing MD (2006) Changes in sin nombre virus antibody prevalence in deer mice across seasons: the interaction between habitat, sex, and infection in deer mice. J Wildl Dis 42:819–824

    PubMed  Google Scholar 

  • Peng G, Guo Z, Kiniwa Y, Voo KS, Peng W, Fu T, Wang DY, Li Y, Wang HY, Wang RF (2005) Toll-like receptor 8-mediated reversal of CD4+ regulatory T cell function. Science 309: 1380–1384

    Article  PubMed  CAS  Google Scholar 

  • Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, Bolland S (2006) Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 312:1669–1672

    Article  PubMed  CAS  Google Scholar 

  • Polanczyk MJ, Hopke C, Huan J, Vandenbark AA, Offner H (2005) Enhanced FoxP3 expression and Treg cell function in pregnant and estrogen-treated mice. J Neuroimmunol 170:85–92

    Article  PubMed  CAS  Google Scholar 

  • Pong RC, Roark R, Ou JY, Fan J, Stanfield J, Frenkel E, Sagalowsky A, Hsieh JT (2006) Mechanism of increased coxsackie and adenovirus receptor gene expression and adenovirus uptake by phytoestrogen and histone deacetylase inhibitor in human bladder cancer cells and the potential clinical application. Cancer Res 66:8822–8828

    Article  PubMed  CAS  Google Scholar 

  • Poonia B, Walter L, Dufour J, Harrison R, Marx PA, Veazey RS (2006) Cyclic changes in the vaginal epithelium of normal rhesus macaques. J Endocrinol 190:829–835

    Article  PubMed  CAS  Google Scholar 

  • Porter MB, Long MT, Getman LM, Giguere S, MacKay RJ, Lester GD, Alleman AR, Wamsley HL, Franklin RP, Jacks S, Buergelt CD, Detrisac CJ (2003) West Nile virus encephalomyelitis in horses: 46 cases (2001). J Am Vet Med Assoc 222:1241–1247

    Article  PubMed  Google Scholar 

  • Purtilo DT, Sullivan JL (1979) Immunological bases for superior survival of females. Am J Dis Child 133:1251–1253

    PubMed  CAS  Google Scholar 

  • Quinn TC, Overbaugh J (2005) HIV/AIDS in women: an expanding epidemic. Science 308: 1582–1583

    Article  PubMed  CAS  Google Scholar 

  • Roberts CW, Walker W, Alexander J (2001) Sex-associated hormones and immunity to protozoan parasites. Clin Microbiol Rev 14:476–488

    Article  PubMed  CAS  Google Scholar 

  • Roivainen M, Piirainen L, Hovi T, Virtanen I, Riikonen T, Heino J, Hyypia T (1994) Entry of coxsackievirus A9 into host cells: specific interactions with alpha v beta 3 integrin, the vitronectin receptor. Virology 203:357–365

    Article  PubMed  CAS  Google Scholar 

  • Root JJ, Calisher CH, Beaty BJ (1999) Relationships of deer mouse movement, vegetative structure, and prevalence of infection with Sin Nombre virus. J Wildl Dis 35:311–318

    PubMed  CAS  Google Scholar 

  • Sartini D, Moussawi M, Sallam R, Bernstein I, Huber S (2004) Correlation between serum estradiol in the follicular phase of the ovarian cycle and decay acceleration factor (DAF) expression on red blood cells and coxsackiervirus B-3 induced hemagglutination in young cycling women. Am J Reprod Immunol 51:180–187

    Article  PubMed  Google Scholar 

  • Schwartz J, Sartini D, Huber S (2004) Myocarditis susceptibility in female mice depends upon ovarian cycle phase at infection. Virology 330:16–23

    Article  PubMed  CAS  Google Scholar 

  • Seth RB, Sun L, Chen ZJ (2006) Antiviral innate immunity pathways. Cell Res 16:141–147

    Article  PubMed  CAS  Google Scholar 

  • Smith SM, Baskin GB, Marx PA (2000) Estrogen protects against vaginal transmission of simian immunodeficiency virus. J Infect Dis 182:708–715

    Article  PubMed  CAS  Google Scholar 

  • Smith-Bouvier DL, Divekar AA, Sasidhar M, Du S, Tiwari-Woodruff SK, King JK, Arnold AP, Singh RR, Voskuhl RR (2008) A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med 205(5):1099–1108

    Article  PubMed  CAS  Google Scholar 

  • Sodora DL, Gettie A, Miller CJ, Marx PA (1998) Vaginal transmission of SIV: assessing infectivity and hormonal influences in macaques inoculated with cell-free and cell-associated viral stocks. AIDS Res Hum Retroviruses 14(Suppl 1):S119–S123

    PubMed  Google Scholar 

  • Song WC, Deng C, Raszmann K, Moore R, Newbold R, McLachlan JA, Negishi M (1996) Mouse decay-accelerating factor: selective and tissue-specific induction by estrogen of the gene encoding the glycosylphosphatidylinositol-anchored form. J Immunol 157:4166–4172

    PubMed  CAS  Google Scholar 

  • Sterling TR, Vlahov D, Astemborski J, Hoover DR, Margolick JB, Quinn TC (2001) Initial plasma HIV-1 RNA levels and progression to AIDS in women and men. N Engl J Med 344:720–725

    Article  PubMed  CAS  Google Scholar 

  • Stringer EM, Kaseba C, Levy J, Sinkala M, Goldenberg RL, Chi BH, Matongo I, Vermund SH, Mwanahamuntu M, Stringer JS (2007) A randomized trial of the intrauterine contraceptive device vs hormonal contraception in women who are infected with the human immunodeficiency virus. Am J Obstet Gynecol 197(144):e141–e148

    Google Scholar 

  • Sun X, Funk CD, Deng C, Sahu A, Lambris JD, Song WC (1999) Role of decay-accelerating factor in regulating complement activation on the erythrocyte surface as revealed by gene targeting. Proc Natl Acad Sci USA 96:628–633

    Article  PubMed  CAS  Google Scholar 

  • Sun Q, Sun L, Liu HH, Chen X, Seth RB, Forman J, Chen ZJ (2006) The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24:633–642

    Article  PubMed  CAS  Google Scholar 

  • 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 (2008) Induction of regulatory T cells by physiological level estrogen. J Cell Physiol 214:456–464

    Article  PubMed  CAS  Google Scholar 

  • Teepe AG, Allen LB, Wordinger RJ, Harris EF (1990) Effect of the estrous cycle on susceptibility of female mice to intravaginal inoculation of herpes simplex virus type 2 (HSV-2). Antiviral Res 14:227–235

    Article  PubMed  CAS  Google Scholar 

  • Theofilopoulos AN, Baccala R, Beutler B, Kono DH (2005) Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 23:307–336

    Article  PubMed  CAS  Google Scholar 

  • Tolou H, Nicoli J, Chastel C (2002) Viral evolution and emerging viral infections: what future for the viruses? A theoretical evaluation based on informational spaces and quasispecies. Virus Genes 24:267–274

    Article  PubMed  CAS  Google Scholar 

  • Tsan MF, Gao B (2004) Endogenous ligands of Toll-like receptors. J Leukoc Biol 76:514–519

    Article  PubMed  CAS  Google Scholar 

  • Vapalahti O, Mustonen J, Lundkvist A, Henttonen H, Plyusnin A, Vaheri A (2003) Hantavirus infections in Europe. Lancet Infect Dis 3:653–661

    Article  PubMed  Google Scholar 

  • Varani S, Cederarv M, Feld S, Tammik C, Frascaroli G, Landini MP, Soderberg-Naucler C (2007) Human cytomegalovirus differentially controls B cell and T cell responses through effects on plasmacytoid dendritic cells. J Immunol 179:7767–7776

    PubMed  CAS  Google Scholar 

  • Vik DP, Amiguet P, Moffat GJ, Fey M, Amiguet-Barras F, Wetsel RA, Tack BF (1991) Structural features of the human C3 gene: intron/exon organization, transcriptional start site, and promoter region sequence. Biochemistry 30:1080–1085

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Kato N, Hoshida Y, Yoshida H, Taniguchi H, Goto T, Moriyama M, Otsuka M, Shiina S, Shiratori Y, Ito Y, Omata M (2003) Interleukin-1beta gene polymorphisms associated with hepatocellular carcinoma in hepatitis C virus infection. Hepatology 37:65–71

    Article  PubMed  CAS  Google Scholar 

  • Weber F, Kochs G, Haller O (2004) Inverse interference: how viruses fight the interferon system. Viral Immunol 17:498–515

    Article  PubMed  CAS  Google Scholar 

  • Weigler BJ, Ksiazek TG, Vandenbergh JG, Levin M, Sullivan WT (1996) Serological evidence for zoonotic hantaviruses in North Carolina rodents. J Wildl Dis 32:354–357

    PubMed  CAS  Google Scholar 

  • Westbury HA, Sinkovic B (1978) The pathogenesis of infectious avian encephalomyelitis. 3. The relationship between viraemia, invasion of the brain by the virus, and the development of specific serum neutralising antibody. Aust Vet J 54:76–80

    Article  PubMed  CAS  Google Scholar 

  • White DJ, Means RG, Birkhead GS, Bosler EM, Grady LJ, Chatterjee N, Woodall J, Hjelle B, Rollin PE, Ksiazek TG, Morse DL (1996) Human and rodent hantavirus infection in New York State: public health significance of an emerging infectious disease. Arch Intern Med 156: 722–726

    Article  PubMed  CAS  Google Scholar 

  • Wickham TJ, Mathias P, Cheresh DA, Nemerow GR (1993) Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73:309–319

    Article  PubMed  CAS  Google Scholar 

  • Wickham TJ, Filardo EJ, Cheresh DA, Nemerow GR (1994) Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization. J Cell Biol 127:257–264

    Article  PubMed  CAS  Google Scholar 

  • Williams RJ, Bryan RT, Mills JN, Palma RE, Vera I, De Velasquez F, Baez E, Schmidt WE, Figueroa RE, Peters CJ, Zaki SR, Khan AS, Ksiazek TG (1997) An outbreak of hantavirus pulmonary syndrome in western Paraguay. Am J Trop Med Hyg 57:274–282

    PubMed  CAS  Google Scholar 

  • Woodruff J (1980) Viral myocarditis. Am J Pathol 101:425–483

    PubMed  CAS  Google Scholar 

  • Woodward TL, Mienaltowski AS, Modi RR, Bennett JM, Haslam SZ (2001) Fibronectin and the alpha(5)beta(1) integrin are under developmental and ovarian steroid regulation in the normal mouse mammary gland. Endocrinology 142:3214–3222

    Article  PubMed  CAS  Google Scholar 

  • Yeaman GR, Howell AL, Weldon S, Demian DJ, Collins JE, O’Connell DM, Asin SN, Wira CR, Fanger MW (2003) Human immunodeficiency virus receptor and coreceptor expression on human uterine epithelial cells: regulation of expression during the menstrual cycle and implications for human immunodeficiency virus infection. Immunology 109:137–146

    Article  PubMed  CAS  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023

    Article  PubMed  CAS  Google Scholar 

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    Sabra L. Klein

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    Sabra L. Klein

  2. Institute for Biomedical Sciences, University of Strathclyde, Taylor Street 27, Glasgow, G4 0NR, United Kingdom

    Craig Roberts

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Klein, S.L., Huber, S. (2010). Sex Differences in Susceptibility to Viral Infection. In: Klein, S., Roberts, C. (eds) Sex Hormones and Immunity to Infection. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02155-8_4

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