Persistent hepatitis C virus infection impairs ribavirin antiviral activity through clathrin-mediated trafficking of equilibrative nucleoside transporter 1

Journal of Virology

Volumn 89, Issue 1, 2015, Pages 626-642

  Panigrahi, Rajesh ^a   Chandra, Partha K ^a   Ferraris, Pauline ^a   Kurt, Ramazan ^a   Song, Kyoungsub ^a   Garry, Robert F ^a   Reiss, Krzysztof ^b   Coe, Imogen R ^c   Furihata, Tomomi ^d   Balart, Luis A ^a   Wu, Tong ^a   Dash, Srikanta ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c RYERSON UNIVERSITY   (Canada)

^d CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; BAFILOMYCIN A1; CLATHRIN; CLATHRIN HEAVY CHAIN; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; HYDROXYCHLOROQUINE; INTERLEUKIN 29; PROTEIN SERINE THREONINE KINASE INHIBITOR; RIBAVIRIN; TORIN 1; UNCLASSIFIED DRUG; ANTIVIRUS AGENT;

ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ARTICLE; AUTOPHAGY; CELL MEMBRANE; DOWN REGULATION; HEPATITIS C; HEPATITIS C VIRUS; HEPATOCELLULAR CARCINOMA CELL LINE; HUH 7.5 CELL LINE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LYSOSOME; PERSISTENT INFECTION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN TRANSPORT; VIRAL CLEARANCE; VIRUS ENTRY; VIRUS REPLICATION; CELL LINE; DRUG EFFECTS; DRUG RESISTANCE; HEPACIVIRUS; LIVER CELL; METABOLISM; VIROLOGY;

HEPATITIS C VIRUS;

ANTIVIRAL AGENTS; CELL LINE; CLATHRIN; DRUG RESISTANCE; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; HEPACIVIRUS; HEPATOCYTES; HUMANS; PROTEIN TRANSPORT; RIBAVIRIN;

EID: 84919427415     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02492-14     Document Type: Article

References (36)

1. Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. 2013. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology 57:1333-1342. http://dx.doi.org/10.1002/hep.26141.
2. Shiffman ML. 2014. Hepatitis C therapy in the direct acting antiviral era. Curr Opin Gastroenterol 30:217-222. http://dx.doi.org/10.1097/MOG.0000000000000062.
3. Casey LC, Lee WM. 2013. Hepatitis C virus therapy update 2013. Curr Opin Gastroenterol 29:243-249. http://dx.doi.org/10.1097/MOG.0b013e32835ff972.
4. Clark V, Nelson DR. 2012. The role of ribavirin in direct acting antiviral drug regimens for chronic hepatitis C. Liver Int 32:103-107. http://dx.doi.org/10.1111/j.1478-3231.2011.02711.x.
5. Casey J, Morris K, Narayana M, Nakagaki M, Kennedy GA. 2013. Oral ribavirin for the treatment of respiratory syncytial virus and parainfluenza 3 virus infections post-allogenic hematopoietic stem cell transplantation. Bone Marrow Transplant 48:1558-1561. http://dx.doi.org/10.1038/bmt.2013.112.
6. McCormick JB, King IJ, Webb PA, Scribner CL, Craven RB, Johnson KM, Elliott LH, Belmont-Williams R. 1986. Lassa fever. Effective therapy with ribavirin. N Engl J Med 314:20-26.
7. Dixit NM, Perelson AS. 2006. The metabolism, pharmacokinetics and mechanisms of antiviral activity of ribavirin against hepatitis C virus. Cell Mol Life Sci 63:832-842. http://dx.doi.org/10.1007/s00018-005-5455-y.
8. Lanford RE, Chavez D, Guerra B, Lau JY, Hong Z, Brasky KM, Beames B. 2001. Ribavirin induces error-prone replication of GB virus B in primary tamarin hepatocytes. J Virol 75:8074-8081. http://dx.doi.org/10.1128/JVI.75.17.8074-8081.2001.
9. Paeshuyse J, Dallmeier K, Neyts J. 2011. Ribavirin for the treatment of chronic hepatitisCvirus infection: a review of the proposed mechanism of action. Curr Opin Virol 1:590-598. http://dx.doi.org/10.1016/j.coviro.2011.10.030.
10. Kong W, Engel K, Wang J. 2004. Mammalian nucleoside transporters. Curr Drug Metab 5:63-84. http://dx.doi.org/10.2174/1389200043489162.
11. Feld JJ, Hoofnagle JH. 2005. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436:967-972. http://dx.doi.org/10.1038/nature04082.
12. Panigrahi R, Hazari S, Chandra S, Chandra PK, Datta S, Kurt R, Cameron CE, Huang Z, Zhang H, Garry RF, Balart LA, Dash S. 2013. Interferon and ribavirin combination treatment synergistically inhibit HCVinternal ribosome entry site mediated translation at the level of polyribosome formation. PLoS One 8:e72791. http://dx.doi.org/10.1371/journal.pone.0072791.
13. Pfeiffer JK, Kirkegaard K. 2005. Ribavirin resistance in hepatitis C virus replicon-containing cell lines conferred by changes in the cell line or mutations in the replicon RNA. J Virol 79:2346-2355. http://dx.doi.org/10.1128/JVI.79.4.2346-2355.2005.
14. Hmwe SS, Aizaki H, Date T, Murakam K, Ishii K, Miyamura T, Koike K, Wakita T, Suzuki T. 2010. Identification of hepatitis C virus genotype 2a replicon variants with reduced susceptibility to ribavirin. Antiviral Res 85:520-524. http://dx.doi.org/10.1016/j.antiviral.2009.12.008.
15. Ibarra KD, Jain MK, Pfeiffer JK. 2011. Host-based ribavirin resistance influences hepatitis C virus replication and treatment response. J Virol 85:7273-7273. http://dx.doi.org/10.1128/JVI.00629-11.
16. Ibarra KD, Pfeiffer JK. 2009. Reduced ribavirin antiviral efficacy via nucleoside transporter-mediated drug resistance. J Virol 83:4538-4547. http://dx.doi.org/10.1128/JVI.02280-08.
17. Iikura M, Furihata T, Mizuguchi M, Nagai M, Ikeda M, Kato N, Tsubota A, Chiba K. 2012. ENT1, a ribavirin transporter, plays a pivotal role in antiviral efficacy of ribavirin in a hepatitis C virus replication cell system. Antimicrob Agents Chemother 56:1407-1413. http://dx.doi.org/10.1128/AAC.05762-11.
18. Mori K, Hiraoka O, Ikeda M, Ariumi Y, Horamoto A, Wataya Y, Kato N. 2013. Adenosine kinase is a key determinant for anti-HCV activity of ribavirin. Hepatology 58:1236-1244. http://dx.doi.org/10.1002/hep.26421.
19. Shah NR, Sunderland A, Grdzelishvili VZ. 2010. Cell type mediated resistance of vesicular stomatitis virus and Sendai virus to ribavirin. PLoS One 5:e11265. http://dx.doi.org/10.1371/journal.pone.0011265.
20. Chandra PK, Bao L, Song K, Aboulnasr FM, Baker DP, Shores N, Wimley WC, Liu S, Hagedorn CH, Fuchs SY, Wu T, Balart LA, Dash S. 2014. HCV infection selectively impairs type I but not type III IFN signaling. AmJ Pathol 184:214-229. http://dx.doi.org/10.1016/j.ajpath.2013.10.005.
21. Datta S, Hazari S, Chandra PK, Samara M, Poat B, Gunduz F, Wimley WC, Hauser H, Koster M, Lamaze C, Balart LA, Garry RF, Dash S. 2011. Mechanisms of HCV's resistance to IFN-alpha in cell culture involve expression of functional IFN-alpha receptor 1. Virol J 8:351. http://dx.doi.org/10.1186/1743-422X-8-351.
22. Liu S, Nelson CA, Xiao L, Lu L, Seth PP, Davis DR, Hagedorn CH. 2011. Measuring antiviral activity of benzimidazole molecules that alters IRES RNA structure with an infectious hepatitis C virus chimera expressing Renilla luciferase. Antiviral Res 89:54-63. http://dx.doi.org/10.1016/j.antiviral.2010.11.004.
23. Nivillac NM, Bacani J, Coe IR. 2011. The life cycle of human equilibrative nucleoside transporter 1: from ER export to degradation. Exp Cell Res 317:1567-1579. http://dx.doi.org/10.1016/j.yexcr.2011.03.008.
24. Skrypek N, Duchene B, Hebbar M, Leteurtre E, van Seuningen I, Jonckheere N. 2013. The MUC4 mucin mediates gemcitabine resistance of human pancreatic cancer cells via the concentrative nucleoside transporter family. Oncogene 32:1714-1723. http://dx.doi.org/10.1038/onc.2012.179.
25. Dreux M, Chisari FV. 2011. Impact of the autophagy machinery on hepatitis C virus infection. Viruses 3:1342-1352. http://dx.doi.org/10.3390/v3081342.
26. Klionsky DJ, Codogno P, Cuervo AM, Deretic V, Elazar Z, Fueyo-Margareto J, Gewirtz DA, Kroemer G, Levine B, Mizushima N, Rubinsztein DC, Thumm M, Tooze SA. 2010. A comprehensive glossary of autophagy-related molecules and processes. Autophagy 6:438-448. http://dx.doi.org/10.4161/auto.6.4.12244.
27. Tanida I, Ueno T, Kominami E. 2008. LC3 and autophagy. Methods Mol Biol 445:77-88. http://dx.doi.org/10.1007/978-1-59745-157-4_4.
28. Bao L, Chandra PK, Moroz K, Zhang X, Thung SN, Wu T, Dash S. 2014. Impaired autophagy response in human hepatocellular carcinoma. Exp Mol Pathol 96:149-154. http://dx.doi.org/10.1016/j.yexmp.2013.12.002.
29. Yang YP, Hu LF, Zheng HF, Mao CJ, Hu WD, Xiong KP, Wang F, Liu CF. 2013. Application and interpretation of current autophagy inhibitors and activators. Acta Pharmacol Sin 34:625-635. http://dx.doi.org/10.1038/aps.2013.5.
30. Rong Y, Liu M, Ma L, Du W, Zhang H, Tian Y, Cao Z, Li Y, Ren H, Zhang C, Li L, Chen S, Xi J, Yu L. 2012. Clathrin and phosphatidylinositol-4,5-bisphate regulate autophagic lysosome reformation. Nat Cell Biol 14:924-934. http://dx.doi.org/10.1038/ncb2557.
31. Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC. 2010. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12:747-757. http://dx.doi.org/10.1038/ncb2078.
32. Chandra PK, Gunduz F, Hazari S, Ramazan K, Panigrahi R, Poat B, Bruce D, Cohen AJ, Behorquez HE, Carmody I, Loss G, Balart LA, Wu T, Dash S. 2014. Impaired expression of type I and type II interferon receptors in HCV-associated chronic liver disease and liver cirrhosis. PLoS One 9:e108616. http://dx.doi.org/10.1371/journal.pone.0108616.
33. Hoofnagle JH, Lau D, Conjeevaram H, Kleiner D, Di Bisceglie AM. 1996. Prolonged therapy of chronic hepatitis C with ribavirin. J Viral Hepat 3:247-252. http://dx.doi.org/10.1111/j.1365-2893.1996.tb00050.x.
34. Reddy KR, Shiffman ML, Rodriguez-Torres M, Cheinquer H, Abdurakhmanov D, Bakulin I, Morozov V, Silva GF, Geyvandova N, Stanciu C, Rabbia M, McKenna M, Thommes JA, Harrison SA, PROGRESS Study Investigators. 2010. Induction pegylated interferon alfa-2a and high dose ribavirin do not increase SVR in healthy patients with genotype 1a and high viral loads. Gastroenterology 139:1972-1983. http://dx.doi.org/10.1053/j.gastro.2010.08.051.
35. Rautou PE, Cazals-Hatem D, Feldmann G, Mansouri A, Grodet A, Barge S, Martinot-Peignoux M, Duces A, Bièche I, Lebrec D, Bedossa P, Paradis V, Marcellin P, Valla D, Asselah T, Moreau R. 2011. Changes in autophagic response in patients with chronic hepatitis C virus infection. Am J Pathol 178:2708-2715. http://dx.doi.org/10.1016/j.ajpath.2011.02.021.
36. Lamb CA, Yoshimori T, Tooze SA. 2013. The autophagosome; origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 14:759-774. http://dx.doi.org/10.1038/nrm3696.