Sex hormones and HCV: An unresolved mystery

Expert Review of Gastroenterology and Hepatology

Volumn 7, Issue 1, 2013, Pages 69-75

  Mekky, Radwa Y ^a   Abdelaziz, Ahmed I ^a  

^a German University in Cairo   (Egypt)

Author keywords

gender; HCV; IFN; sex hormones

Indexed keywords

ADIPONECTIN; ALPHA INTERFERON; BOCEPREVIR; CYTOKINE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; HOST FACTOR; INTERFERON; JANUS KINASE; NONSTRUCTURAL PROTEIN 5B; PHYTOESTROGEN; SEX HORMONE; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TELAPREVIR; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8;

ANTIINFLAMMATORY ACTIVITY; ANTIVIRAL ACTIVITY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG RECEPTOR BINDING; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNOMODULATION; IMMUNOREGULATION; NONHUMAN; REVIEW; SEX DIFFERENCE; TREATMENT RESPONSE; VIRAL CLEARANCE; VIRUS ENTRY; VIRUS IMMUNITY; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; FEMALE; GONADAL STEROID HORMONES; HEALTH STATUS DISPARITIES; HEPACIVIRUS; HEPATITIS C; HUMANS; INTERFERONS; MALE; SEX FACTORS; TREATMENT OUTCOME;

EID: 84871589439     PISSN: 17474124     EISSN: 17474132     Source Type: Journal    
DOI: 10.1586/egh.12.69     Document Type: Review

References (60)

1. El-Zanaty FWA. Egypt Demographic and Health Survey 2008. Minstry of Health, Egypt 431 (2009).
2. Farci P, Bukh J, Purcell RH. The quasispecies of hepatitis C virus and the host immune response. Springer Semin. Immunopathol. 19(1), 5-26 (1997).
3. Fedorchenko SV, Martynovich TL, Liashok OV, Kariuk ZhA, Ianchenko VI. Spontaneous HCV clearance: an association with gender, age, viral genotypes, infection transmission routes, and markers of HBV and HIV. Ter. Arkh. 82(3), 52-56 (2010).
4. Bakr I, Rekacewicz C, El Hosseiny M et al. Higher clearance of hepatitis C virus infection in females compared with males. Gut 55(8), 1183-1187 (2006).
5. Spada E, Mele A, Berton A et al. Multispecific T cell response and negative HCV RNA tests during acute HCV infection are early prognostic factors of spontaneous clearance. Gut 53(11), 1673-1681 (2004).
6. Conjeevaram HS, Fried MW, Jeffers LJ et al. ; Virahep-C Study Group. Peginterferon and ribavirin treatment in African American and Caucasian American patients with hepatitis C genotype 1. Gastroenterology 131(2), 470-477 (2006).
7. de Bruijne J, Buster EH, Gelderblom HC et al. ; Netherlands Association of Gastroenterologists and Hepatologists. Treatment of chronic hepatitis C virus infection-Dutch national guidelines. Neth. J. Med. 66(7), 311-322 (2008).
8. Akram M, Idrees M, Zafar S et al. Effects of host and virus related factors on interferon-α+ribavirin and pegylatedinterferon+ ribavirin treatment outcomes in chronic hepatitis C patients. Virol. J. 8, 234 (2011).
9. Akuta N, Suzuki F, Kawamura Y et al. Predictive factors of early and sustained responses to peginterferon plus ribavirin combination therapy in Japanese patients infected with hepatitis C virus genotype 1b: amino acid substitutions in the core region and low-density lipoprotein cholesterol levels. J. Hepatol. 46(3), 403-410 (2007).
10. Kryczka W, Zarebska-Michaluk D, Chrapek M. Assessment of selected clinical factors as predictors of response to combined interferon-α plus ribavirin therapy among patients with chronic hepatitis C. Med. Sci. Monit. 9(Suppl. 3), 32-35 (2003).
11. Poynard T, McHutchison J, Goodman Z, Ling MH, Albrecht J. Is an "a la carte" combination interferon-α-2b plus ribavirin regimen possible for the first line treatment in patients with chronic hepatitis C? The ALGOVIRC Project Group. Hepatology 31(1), 211-218 (2000).
12. Husa P, Slesinger P, Stroblová H, Svobodník A. The effect of patient's body weight, gender and baseline viral load on the efficacy of hepatitis C therapy. Vnitr. Lek. 52(6), 590-595 (2006).
13. Qureshi S, Batool U, Iqbal M, Burki UF, Khan NU. Pre-treatment predictors of response for assessing outcomes to standard treatment in infection with HCV genotype 3. J. Coll. Physicians Surg. Pak. 21(2), 64-68 (2011).
14. Di Bisceglie AM, Fan X, Chambers T, Strinko J. Pharmacokinetics, pharmacodynamics, and hepatitis C viral kinetics during antiviral therapy: the null responder. J. Med. Virol. 78(4), 446-451 (2006).
15. Narciso-Schiavon JL, Schiavon Lde L, Carvalho-Filho RJ et al. Gender influence on treatment of chronic hepatitis C genotype 1. Rev. Soc. Bras. Med. Trop. 43(3), 217-223 (2010).
16. Jiménez-Pérez M, Sáez-Gómez AB, Pérez-Daga JA, Lozano-Rey JM, de la Cruz-Lombardo J, Rodrigo-López JM. Hepatitis C virus recurrence after liver transplantation: analysis of factors related to sustained viral response. Transplant. Proc. 42(2), 666-668 (2010).
17. Barrett S, Goh J, Coughlan B et al. The natural course of hepatitis C virus infection after 22 years in a unique homogenous cohort: spontaneous viral clearance and chronic HCV infection. Gut 49(3), 423-430 (2001).
18. Hayashida K, Shoji I, Deng L, Jiang DP, Ide YH, Hotta H. 17β-estradiol inhibits the production of infectious particles of hepatitis C virus. Microbiol. Immunol. 54(11), 684-690 (2010).
19. Kaushik-Basu N, Bopda-Waffo A, Talele TT et al. Identification and characterization of coumestans as novel HCV NS5B polymerase inhibitors. Nucleic Acids Res. 36(5), 1482-1496 (2008).
20. Latt NC, Spencer JD, Beeby PJ et al. Hepatitis C in injecting drug-using women during and after pregnancy. J. Gastroenterol. Hepatol. 15(2), 175-181 (2000).
21. Watashi K, Inoue D, Hijikata M, Goto K, Aly HH, Shimotohno K. Anti-hepatitis C virus activity of tamoxifen reveals the functional association of estrogen receptor with viral RNA polymerase NS5B. J. Biol. Chem. 282(45), 32765-32772 (2007).
22. Langer C, Gansz B, Goepfert C et al. Testosterone up-regulates scavenger receptor BI and stimulates cholesterol efflux from macrophages. Biochem. Biophys. Res. Commun. 296(5), 1051-1057 (2002).
23. Scarselli E, Ansuini H, Cerino R et al. The human scavenger receptor class B type 1 is a novel candidate receptor for the hepatitis C virus. EMBO J. 21(19), 5017-5025 (2002).
24. Srivastava RA. Scavenger receptor class B type I expression in murine brain and regulation by estrogen and dietary cholesterol. J. Neurol. Sci. 210(1-2), 11-18 (2003).
25. Meng J, Mostaghel EA, Vakar-Lopez F, Montgomery B, True L, Nelson PS. Testosterone regulates tight junction proteins and influences prostatic autoimmune responses. Horm. Cancer 2(3), 145-156 (2011).
26. Evans MJ, von Hahn T, Tscherne DM et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446(7137), 801-805 (2007).
27. Gibson SJ, Lindh JM, Riter TR et al. Plasmacytoid dendritic cells produce cytokines and mature in response to the TLR7 agonists, imiquimod and resiquimod. Cell Immunol. 218(1-2), 74-86 (2002).
28. Gorski KS, Waller EL, Bjornton-Severson J et al. Distinct indirect pathways govern human NK-cell activation by TLR-7 and TLR-8 agonists. Int. Immunol. 18(7), 1115-1126 (2006).
29. Berghöfer B, Frommer T, Haley G, Fink L, Bein G, Hackstein H. TLR7 ligands induce higher IFN-α production in females. J. Immunol. 177(4), 2088-2096 (2006).
30. Escribese MM, Kraus T, Rhee E, Fernandez-Sesma A, López CB, Moran TM. Estrogen inhibits dendritic cell maturation to RNA viruses. Blood 112(12), 4574-4584 (2008).
31. Ghisletti S, Meda C, Maggi A, Vegeto E. 17β-estradiol inhibits inflammatory gene expression by controlling NF-κB intracellular localization. Mol. Cell. Biol. 25(8), 2957-2968 (2005).
32. Hughes GC, Thomas S, Li C, Kaja MK, Clark EA. Cutting edge: progesterone regulates IFN-α production by plasmacytoid dendritic cells. J. Immunol. 180(4), 2029-2033 (2008).
33. Meier A, Chang JJ, Chan ES et al. Sex differences in the Toll-like receptor-mediated response of plasmacytoid dendritic cells to HIV-1. Nat. Med. 15(8), 955-959 (2009).
34. Young NA, Friedman A, Kaffenberger B, Jarjour WN. Estrogen stimulation of endosomal toll-like receptor expression lowers the threshold of activation in peripheral blood mononuclear cells and contributes to the gender bias of systemic lupus erythematosus. Arthritis Rheum. 63(Suppl. 10), 1425 (2011).
35. Paladino N, Fainboim H, Theiler G et al. Gender susceptibility to chronic hepatitis C virus infection associated with interleukin 10 promoter polymorphism. J. Virol. 80(18), 9144-9150 (2006).
36. Ito S, Ansari P, Sakatsume M et al. Interleukin-10 inhibits expression of both interferon α-and interferon γ-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 93(5), 1456-1463 (1999).
37. Kurosaki M, Tanaka Y, Nishida N et al. Genetic polymorphism in IL28B predicts null virological response to pegylatedinterferon plus ribavirin therapy for chronic hepatitis. J. Hepatol. 52, 451-452 (2010).
38. van den Berg CH, Grady BP, Schinkel J et al. Female sex and IL28B, a synergism for spontaneous viral clearance in hepatitis C virus (HCV) seroconverters from a community-based cohort. PLoS ONE 6(11), e27555 (2011).
39. Mekky RY, Hamdi N, El-Akel W, Esmat G, Abdelaziz AI. Estrogen-related MxA transcriptional variation in hepatitis C virus-infected patients. Transl. Res. 159(3), 190-196 (2012).
40. Hayashi J, Kishihara Y, Ueno K et al. Age-related response to interferon-α treatment in women vs men with chronic hepatitis C virus infection. Arch. Intern. Med. 158(2), 177-181 (1998).
41. Bressler BL, Guindi M, Tomlinson G, Heathcote J. High body mass index is an independent risk factor for nonresponse to antiviral treatment in chronic hepatitis C. Hepatology 38(3), 639-644 (2003).
42. Floreani A, Cazzagon N, Boemo DG et al. Female patients in fertile age with chronic hepatitis C, easy genotype, and persistently normal transaminases have a 100% chance to reach a sustained virological response. Eur. J. Gastroenterol. Hepatol. 23(11), 997-1003 (2011).
43. Villa E, Karampatou A, Cammà C et al. Early menopause is associated with lack of response to antiviral therapy in women with chronic hepatitis C. Gastroenterology 140(3), 818-829 (2011).
44. Shimizu I, Omoya T, Kondo Y et al. Estrogen therapy in a male patient with chronic hepatitis C and irradiation-induced testicular dysfunction. Intern. Med. 40(2), 100-104 (2001).
45. Fujita N, Sugimoto R, Urawa N et al. Hepatic iron accumulation is associated with disease progression and resistance to interferon/ribavirin combination therapy in chronic hepatitis C. J. Gastroenterol. Hepatol. 22(11), 1886-1893 (2007).
46. Rachon D, Mysliwska J, Suchecka-Rachon K, Wieckiewicz J, Mysliwski A. Effects of oestrogen deprivation on interleukin-6 production by peripheral blood mononuclear cells of postmenopausal women. J. Endocrinol. 172(2), 387-395 (2002).
47. Taliani G, Badolato MC, Nigro G et al. Serum concentration of gGT is a surrogate marker of hepatic TNF-α mRNA expression in chronic hepatitis C. Clin. Immunol. 105(3), 279-285 (2002).
48. Mlisorn NMN, Sanvarinda Y, Wanikiat P. β-estradiol attenuates LPS-induced interleukin-8 production by human peripheral blood monocytes through estrogen receptor-α activation. Afr. J. Pharm. Pharmacol. 4(11), 806-810 (2010).
49. Polyak SJ, Khabar KS, Paschal DM et al. Hepatitis C virus nonstructural 5A protein induces interleukin-8, leading to partial inhibition of the interferon-induced antiviral response. J. Virol. 75(13), 6095-6106 (2001).
50. Leong GM, Moverare S, Brce J et al. Estrogen up-regulates hepatic expression of suppressors of cytokine signaling-2 and-3 in vivo and in vitro. Endocrinology 145(12), 5525-5531 (2004).
51. Steyn FJ, Anderson GM, Grattan DR. Hormonal regulation of suppressors of cytokine signaling (SOCS) messenger ribonucleic acid in the arcuate nucleus during late pregnancy. Endocrinology 149(6), 3206-3214 (2008).
52. Posma E, Moes H, Heineman MJ, Faas MM. The effect of testosterone on cytokine production in the specific and non-specific immune response. Am. J. Reprod. Immunol. 52(4), 237-243 (2004).
53. Kishihara Y, Hayashi J, Yoshimura E, Yamaji K, Nakashima K, Kashiwagi S. IL-1 β and TNF-α produced by peripheral blood mononuclear cells before and during interferon therapy in patients with chronic hepatitis C. Dig. Dis. Sci. 41(2), 315-321 (1996).
54. Zografos TA, Liaskos C, Rigopoulou EI et al. Adiponectin: a new independent predictor of liver steatosis and response to IFN-α treatment in chronic hepatitis C. Am. J. Gastroenterol. 103(3), 605-614 (2008).
55. Martos-Moreno GA, Barrios V, Argente J. Normative data for adiponectin, resistin, interleukin 6, and leptin/receptor ratio in a healthy Spanish pediatric population: relationship with sex steroids. Eur. J. Endocrinol. 155(3), 429-434 (2006).
56. Rodger AJ, Roberts S, Lanigan A, Bowden S, Brown T, Crofts N. Assessment of long-term outcomes of communityacquired hepatitis C infection in a cohort with sera stored from 1971 to 1975. Hepatology 32(3), 582-587 (2000).
57. Bandyopadhyay SK, Moulick A, Saha M, Dutta A, Bandyopadhyay R, Basu AK. A study on endocrine dysfunction in adult males with liver cirrhosis. J. Indian Med. Assoc. 107(12), 866, 868-869 (2009).
58. Pignata S, Daniele B, Galati MG et al. Oestradiol and testosterone blood levels in patients with viral cirrhosis and hepatocellular carcinoma. Eur. J. Gastroenterol. Hepatol. 9(3), 283-286 (1997).
59. Gordon GG, Olivo J, Rafil F, Southren AL. Conversion of androgens to estrogens in cirrhosis of the liver. J. Clin. Endocrinol. Metab. 40(6), 1018-1026 (1975).
60. Garg V, van Heeswijk R, Yang Y, Kauffman R, Smith F, Adda N. The pharmacokinetic interaction between an oral contraceptive containing ethinyl estradiol and norethindrone and the HCV protease inhibitor telaprevir. J. Clin. Pharmacol. 52(10), 1574-1583 (2012).