Ribavirin induced hemolysis: A novel mechanism of action against chronic hepatitis C virus infection

World Journal of Gastroenterology

Volumn 20, Issue 43, 2014, Pages 16184-16190

  Soota, Kaartik ^a   Maliakkal, Benedict ^b  

^a UNITY HEALTH SYSTEM   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Chronic hepatitis C; Heme oxygenase 1; Hemolysis; Ribavirin; Therapy

Indexed keywords

HEME OXYGENASE 1; INTERFERON; RIBAVIRIN; ANTIVIRUS AGENT; AUTACOID;

ANTIINFLAMMATORY ACTIVITY; ANTIVIRAL THERAPY; DRUG MECHANISM; DRUG POTENTIATION; ENZYME METABOLISM; ERYTHROCYTE; HEMOLYSIS; HEMOLYTIC ANEMIA; HEPATITIS C; HUMAN; IMMUNOLOGICAL TOLERANCE; KUPFFER CELL; LIVER CELL; MACROPHAGE; MONOTHERAPY; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PERIPHERAL BLOOD MONONUCLEAR CELL; REVIEW; ANIMAL; BLOOD; CHEMICALLY INDUCED; DRUG COMBINATION; DRUG EFFECTS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; TREATMENT OUTCOME; VIROLOGY;

ANEMIA, HEMOLYTIC; ANIMALS; ANTIVIRAL AGENTS; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; HEME OXYGENASE-1; HEMOLYSIS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION MEDIATORS; RIBAVIRIN; TREATMENT OUTCOME;

EID: 84912520348     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i43.16184     Document Type: Review

References (45)

1. Lauer GM, Walker BD. Hepatitis C virus infection. N Engl J Med 2001; 345: 41-52 [PMID: 11439948 DOI: 10.1056/NEJM200107053450107].
2. Asselah T, Marcellin P. Direct acting antivirals for the treatment of chronic hepatitis C: one pill a day for tomorrow. Liver Int 2012; 32 Suppl 1: 88-102 [PMID: 22212578 DOI: 10.1111/j.1478-3231.2011.02699.x].
3. Crespo G, Mariño Z, Navasa M, Forns X. Viral hepatitis in liver transplantation. Gastroenterology 2012; 142: 1373-1383. e1 [PMID: 22537446 DOI: 10.1053/j.gastro.2012.02.011].
4. Neuman MG, Benhamou JP, Malkiewicz IM, Ibrahim A, Valla DC, Martinot-Peignoux M, Asselah T, Bourliere M, Katz GG, Shear NH, Marcellin P. Kinetics of serum cytokines reflect changes in the severity of chronic hepatitis C presenting minimal fibrosis. J Viral Hepat 2002; 9: 134-140 [PMID: 11876796 DOI: 10.1046/j.1365-2893.2002.00343].
5. Dobrovolskaia MA, Medvedev AE, Thomas KE, Cuesta N, Toshchakov V, Ren T, Cody MJ, Michalek SM, Rice NR, Vogel SN. Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" versus "heterotolerance" on NF-kappa B signaling pathway components. J Immunol 2003; 170: 508-519 [PMID: 12496438].
6. Dolganiuc A, Norkina O, Kodys K, Catalano D, Bakis G, Marshall C, Mandrekar P, Szabo G. Viral and host factors induce macrophage activation and loss of toll-like receptor tolerance in chronic HCV infection. Gastroenterology 2007; 133: 1627-1636 [PMID: 17916356 DOI: 10.1053/j.gastro.2007.08.003].
7. Kazankov K, Barrera F, Møller HJ, Bibby BM, Vilstrup H, George J, Grønbaek H. Soluble CD163, a macrophage activation marker, is independently associated with fibrosis in patients with chronic viral hepatitis B and C. Hepatology 2014; 60: 521-530 [PMID: 24623375 DOI: 10.1002/hep.27129].
8. Abdalla MY, Britigan BE, Wen F, Icardi M, McCormick ML, LaBrecque DR, Voigt M, Brown KE, Schmidt WN. Downregulation of heme oxygenase-1 by hepatitis C virus infection in vivo and by the in vitro expression of hepatitis C core protein. J Infect Dis 2004; 190: 1109-1118 [PMID: 15319861 DOI: 10.1086/423488].
9. Lau DT, Negash A, Chen J, Crochet N, Sinha M, Zhang Y, Guedj J, Holder S, Saito T, Lemon SM, Luxon BA, Perelson AS, Gale M. Innate immune tolerance and the role of kupffer cells in differential responses to interferon therapy among patients with HCV genotype 1 infection. Gastroenterology 2013; 144: 402-413.e12 [PMID: 23123437 DOI: 10.1053/j.gastro.2012.10.044].
10. Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, Gonçales FL, Häussinger D, Diago M, Carosi G, Dhumeaux D, Craxi A, Lin A, Hoffman J, Yu J. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 2002; 347: 975-982 [PMID: 12324553 DOI: 10.1056/NEJMoa020047].
11. Chung RT, Gale M, Polyak SJ, Lemon SM, Liang TJ, Hoofnagle JH. Mechanisms of action of interferon and ribavirin in chronic hepatitis C: Summary of a workshop. Hepatology 2008; 47: 306-320 [PMID: 18161743 DOI: 10.1002/hep.22070].
12. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011; 472: 481-485 [PMID: 21478870 DOI: 10.1038/nature09907].
13. Chen L, Borozan I, Feld J, Sun J, Tannis LL, Coltescu C, Heathcote J, Edwards AM, McGilvray ID. Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005; 128: 1437-1444 [PMID: 15887125].
14. Brok J, Gluud LL, Gluud C. Ribavirin monotherapy for chronic hepatitis C. Cochrane Database Syst Rev 2009; (4): CD005527 [PMID: 19821346 DOI: 10.1002/14651858.CD005527.pub2].
15. Tong MJ, Hwang SJ, Lefkowitz M, Lee SD, Co RL, Conrad A, Schmid P, Lo KJ. Correlation of serum HCV RNA and alanine aminotransferase levels in chronic hepatitis C patients during treatment with ribavirin. J Gastroenterol Hepatol 1994; 9: 587-591 [PMID: 7865717 DOI: 10.1111/j.1440-1746.1994. tb01566].
16. Rotman Y, Noureddin M, Feld JJ, Guedj J, Witthaus M, Han H, Park YJ, Park SH, Heller T, Ghany MG, Doo E, Koh C, Abdalla A, Gara N, Sarkar S, Thomas E, Ahlenstiel G, Edlich B, Titerence R, Hogdal L, Rehermann B, Dahari H, Perelson AS, Hoofnagle JH, Liang TJ. Effect of ribavirin on viral kinetics and liver gene expression in chronic hepatitis C. Gut 2014; 63: 161-169 [PMID: 23396509 DOI: 10.1136/gutjnl-2012-303852].
17. Wright H, Alex P, Nguyen T, Bader T, Gurakar A, Sebastian A, Gonzales L, Wallis G, Naylor M, Dozmorov I, Centola M, Nour B. Multiplex cytokine profiling of initial therapeutic response in patients with chronic hepatitis C virus infection. Dig Dis Sci 2005; 50: 1793-1803 [PMID: 16187176 DOI: 10.1007/s10620-005-2940-y].
18. Neuman MG, Benhamou JP, Malkiewicz IM, Akremi R, Shear NH, Asselah T, Ibrahim A, Boyer N, Martinot-Peignoux M, Jacobson-Brown P, Katz GG, Le Breton V, Le Guludec G, Suneja A, Marcellin P. Cytokines as predictors for sustained response and as markers for immunomodulation in patients with chronic hepatitis C. Clin Biochem 2001; 34: 173-182 [PMID: 11408014 DOI: 10.1016/S0009-9120(01)00212-0].
19. Sulkowski MS, Shiffman ML, Afdhal NH, Reddy KR, McCone J, Lee WM, Herrine SK, Harrison SA, Poordad FF, Koury K, Deng W, Noviello S, Pedicone LD, Brass CA, Albrecht JK, McHutchison JG. Hepatitis C virus treatment-related anemia is associated with higher sustained virologic response rate. Gastroenterology 2010; 139: 1602-1611, 1611.e1 [PMID: 20723545 DOI: 10.1053/j.gastro.2010.07.059].
20. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 1968; 61: 748-755 [PMID: 4386763 DOI: 10.1073/pnas.61.2.748].
21. McCoubrey WK, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 1997; 247: 725-732 [PMID: 9266719 DOI: 10.1111/j.1432-1033.1997.00725].
22. Guo X, Shin VY, Cho CH. Modulation of heme oxygenase in tissue injury and its implication in protection against gastrointestinal diseases. Life Sci 2001; 69: 3113-3119 [PMID: 11758836 DOI: 10.1016/S0024-3205(01)01417-5].
23. Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase- 1: unleashing the protective properties of heme. Trends Immunol 2003; 24: 449-455 [PMID: 12909459 DOI: 10.1016/S1471-4906(03)00181-9].
24. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA, Agarwal A. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 2004; 165: 1045-1053 [PMID: 15331427 DOI: 10.1016/S0002-9440(10)63365-2].
25. Dubuisson J. Hepatitis C virus proteins. World J Gastroenterol 2007; 13: 2406-2415 [PMID: 17552023].
26. Okuda M, Li K, Beard MR, Showalter LA, Scholle F, Lemon SM, Weinman SA. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology 2002; 122: 366-375 [PMID: 11832451 DOI: 10.1053/gast.2002.30983].
27. Li K, Prow T, Lemon SM, Beard MR. Cellular response to conditional expression of hepatitis C virus core protein in Huh7 cultured human hepatoma cells. Hepatology 2002; 35: 1237-1246 [PMID: 11981774 DOI: 10.1053/jhep.2002.32968].
28. Paracha UZ, Fatima K, Alqahtani M, Chaudhary A, Abuzenadah A, Damanhouri G, Qadri I. Oxidative stress and hepatitis C virus. Virol J 2013; 10: 251 [PMID: 23923986 DOI: 10.1186/1 743-422X-10-251].
29. Li N, Karin M. Is NF-kappaB the sensor of oxidative stress? FASEB J 1999; 13: 1137-1143 [PMID: 10385605].
30. Svinka J, Mikulits W, Eferl R. STAT3 in hepatocellular carcinoma: new perspectives. Hepatic Oncol 2013; 1: 107-120 [DOI: 10.2217/hep.13.7].
31. Karin M. NF-kappaB and cancer: mechanisms and targets. Mol Carcinog 2006; 45: 355-361 [PMID: 16673382 DOI: 10.1002/mc.20217].
32. Melhem A, Stern M, Shibolet O, Israeli E, Ackerman Z, Pappo O, Hemed N, Rowe M, Ohana H, Zabrecky G, Cohen R, Ilan Y. Treatment of chronic hepatitis C virus infection via antioxidants: results of a phase I clinical trial. J Clin Gastroenterol 2005; 39: 737-742 [PMID: 16082287 DOI: 10.1097/01. mcg.0000174023.73472.29].
33. Wen F, Brown KE, Britigan BE, Schmidt WN. Hepatitis C core protein inhibits induction of heme oxygenase-1 and sensitizes hepatocytes to cytotoxicity. Cell Biol Toxicol 2008; 24: 175-188 [PMID: 17721824 DOI: 10.1007/s10565-007-9027-9].
34. Schmidt WN, Mathahs MM, Zhu Z. Heme and HO-1 Inhibition of HCV, HBV, and HIV. Front Pharmacol 2012; 3: 129 [PMID: 23060790 DOI: 10.3389/fphar.2012.00129].
35. Zhu Z, Wilson AT, Mathahs MM, Wen F, Brown KE, Luxon BA, Schmidt WN. Heme oxygenase-1 suppresses hepatitis C virus replication and increases resistance of hepatocytes to oxidant injury. Hepatology 2008; 48: 1430-1439 [PMID: 18972446 DOI: 10.1002/hep.22491].
36. Shan Y, Zheng J, Lambrecht RW, Bonkovsky HL. Reciprocal effects of micro-RNA-122 on expression of heme oxygenase- 1 and hepatitis C virus genes in human hepatocytes. Gastroenterology 2007; 133: 1166-1174 [PMID: 17919492 DOI: 10.1053/j.gastro.2007.08.002].
37. Hou W, Tian Q, Zheng J, Bonkovsky HL. MicroRNA-196 represses Bach1 protein and hepatitis C virus gene expression in human hepatoma cells expressing hepatitis C viral proteins. Hepatology 2010; 51: 1494-1504 [PMID: 20127796 DOI: 10.1002/hep.23401].
38. Chen WC, Wang SY, Chiu CC, Tseng CK, Lin CK, Wang HC, Lee JC. Lucidone suppresses hepatitis C virus replication by Nrf2-mediated heme oxygenase-1 induction. Antimicrob Agents Chemother 2013; 57: 1180-1191 [PMID: 23254429 DOI: 10.1128/AAC.02053-12].
39. Zhu Z, Wilson AT, Luxon BA, Brown KE, Mathahs MM, Bandyopadhyay S, McCaffrey AP, Schmidt WN. Biliverdin inhibits hepatitis C virus nonstructural 3/4A protease activity: mechanism for the antiviral effects of heme oxygenase? Hepatology 2010; 52: 1897-1905 [PMID: 21105106 DOI: 10.1002/hep.23921].
40. Sulkowski MS, Poordad F, Manns MP, Bronowicki JP, Rajender Reddy K, Harrison SA, Afdhal NH, Sings HL, Pedicone LD, Koury KJ, Sniukiene V, Burroughs MH, Albrecht JK, Brass CA, Jacobson IM. Anemia during treatment with peginterferon Alfa-2b/ribavirin and boceprevir: Analysis from the serine protease inhibitor therapy 2 (SPRINT-2) trial. Hepatology 2013; 57: 974-984 [PMID: 23081753 DOI: 10.1002/hep.26096].
41. Lindahl K, Stahle L, Bruchfeld A, Schvarcz R. High-dose ribavirin in combination with standard dose peginterferon for treatment of patients with chronic hepatitis C. Hepatology 2005; 41: 275-279 [PMID: 15660393 DOI: 10.1002/hep.20563].
42. Vafiadis I, Trilianos P, Vlachogiannakos J, Karagiorga M, Hatziliami A, Voskaridou E, Ladas SD. Efficacy and safety of interferon-based therapy in the treatment of adult thalassemic patients with chronic hepatitis C: A 12 years audit. Ann Hepatol 2013; 12: 532-538 [PMID: 23813130].
43. Benhamou Y, Afdhal NH, Nelson DR, Shiffman ML, Halliman DG, Heise J, Chun E, Pockros PJ. A phase III study of the safety and efficacy of viramidine versus ribavirin in treatment-naïve patients with chronic hepatitis C: ViSER1 results. Hepatology 2009; 50: 717-726 [PMID: 19585653 DOI: 10.1002/hep.23073].
44. Shields WW, Pockros PJ. Ribavirin analogs. Clin Liver Dis 2009; 13: 419-427 [PMID: 19628158 DOI: 10.1016/j.cld.2009.05.006].
45. Ochi H, Maekawa T, Abe H, Hayashida Y, Nakano R, Kubo M, Tsunoda T, Hayes CN, Kumada H, Nakamura Y, Chayama K. ITPA polymorphism affects ribavirin-induced anemia and outcomes of therapy- A genome-wide study of Japanese HCV virus patients. Gastroenterology 2010; 139: 1190-1197 [PMID: 20637204 DOI: 10.1053/j.gastro.2010.06.071].