The Mechanism of Interferon Refractoriness during Hepatitis C Virus Infection and Its Reversal with a Peroxisome Proliferator-Activated Receptor α Agonist

Journal of Interferon and Cytokine Research

Volumn 35, Issue 6, 2015, Pages 488-497

  Read, Scott A ^a   Tay, Enoch S ^a   Shahidi, Mahsa ^a   McLauchlan, John ^b   George, Jacob ^a   Douglas, Mark W ^a,b,c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^c University of Sydney   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA ACTIN; INTERFERON REGULATORY FACTOR; METFORMIN; PIOGLITAZONE; PIRINIXIC ACID; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE AXL; SMALL INTERFERING RNA; STAT1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG; 2,4 THIAZOLIDINEDIONE DERIVATIVE; AXL RECEPTOR TYROSINE KINASE; HYBRID PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LUCIFERASE; ONCOPROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PYRIMIDINE DERIVATIVE; SOCS1 PROTEIN, HUMAN; SOCS3 PROTEIN, HUMAN; STAT1 PROTEIN, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING;

ADJUVANT THERAPY; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG POTENTIATION; ENZYME ACTIVATION; GENE EXPRESSION; HEPATITIS C; HUMAN; IN VITRO STUDY; LIPID METABOLISM; LIVER CELL; LIVER CELL CARCINOMA; LOW DRUG DOSE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REFRACTORY PERIOD; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; UPREGULATION; VIRAL CLEARANCE; VIRUS REPLICATION; WESTERN BLOTTING; AGONISTS; ANTIVIRAL RESISTANCE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEPACIVIRUS; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; REPORTER GENE; TUMOR CELL LINE; VIROLOGY;

HEPATITIS C VIRUS;

AMP-ACTIVATED PROTEIN KINASES; CELL LINE, TUMOR; DRUG RESISTANCE, VIRAL; GENE EXPRESSION REGULATION; GENES, REPORTER; HEPACIVIRUS; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-ALPHA; LUCIFERASES; METFORMIN; PPAR ALPHA; PPAR GAMMA; PROTO-ONCOGENE PROTEINS; PYRIMIDINES; RECEPTOR PROTEIN-TYROSINE KINASES; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING 1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; THIAZOLIDINEDIONES;

EID: 84931059231     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2014.0209     Document Type: Article

References (30)

1. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, Wilkinson KA, Banchereau R, Skinner J, Wilkinson RJ, Quinn C, Blankenship D, Dhawan R, Cush JJ, Mejias A, Ramilo O, Kon OM, Pascual V, Banchereau J, Chaussabel D, O'Garra A. 2010. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466(7309):973-977.
2. Camma C, Bruno S, Di Marco V, Di Bona D, Rumi M, Vinci M, Rebucci C, Cividini A, Pizzolanti G, Minola E, Mondelli MU, Colombo M, Pinzello G, Craxi A. 2006. Insulin resistance is associated with steatosis in nondiabetic patients with genotype 1 chronic hepatitis C. Hepatology 43(1):64-71.
3. Chu TW, Kulkarni R, Gane EJ, Roberts SK, Stedman C, Angus PW, Ritchie B, Lu XY, Ipe D, Lopatin U, Germer S, Iglesias VA, Elston R, Smith PF, Shulman NS. 2012. Effect of IL28B genotype on early viral kinetics during interferon-free treatment of patients with chronic hepatitis C. Gastroenterology 142(4):790-795.
4. D'Souza R, Sabin CA, Foster GR. 2005. Insulin resistance plays a significant role in liver fibrosis in chronic hepatitis C and in the response to antiviral therapy. Am J Gastroenterol 100(7):1509-1515.
5. Francois-Newton V, Magno de Freitas Almeida G, Payelle-Brogard B, Monneron D, Pichard-Garcia L, Piehler J, Pellegrini S, Uze G. 2011. USP18-based negative feedback control is induced by type I and type III interferons and specifically inactivates interferon alpha response. PLoS One 6(7):e22200.
6. Fujita N, KaitoM,KaiM,Sugimoto R, Tanaka H, HoriikeS,Konishi M, IwasaM,Watanabe S, Adachi Y. 2006. Effects of bezafibrate in patients with chronic hepatitis C virus infection: combination with interferon and ribavirin. J Viral Hepat 13(7):441-448.
7. Gorzin AA, Ramsland PA, Tachedjian G, Gowans EJ. 2012. Identification of residues involved in NS2 homodimerization and elucidation of their impact on the HCV life cycle. J Viral Hepat 19(3):189-198.
8. Herbeuval JP, Nilsson J, Boasso A, Hardy AW, Kruhlak MJ, Anderson SA, Dolan MJ, Dy M, Andersson J, Shearer GM. 2006. Differential expression of IFN-alpha and TRAIL/DR5 in lymphoid tissue of progressor versus nonprogressor HIV-1-infected patients. Proc Natl Acad Sci U S A 103(18):7000-7005.
9. Hill A, Khoo S, Fortunak J, Simmons B, Ford N. 2014. Minimum costs for producing hepatitis C direct-acting antivirals for use in large-scale treatment access programs in developing countries. Clin Infect Dis 58(7):928-936.
10. Huang Y, Feld JJ, Sapp RK, Nanda S, Lin JH, Blatt LM, Fried MW, Murthy K, Liang TJ. 2007. Defective hepatic response to interferon and activation of suppressor of cytokine signaling 3 in chronic hepatitis C. Gastroenterology 132(2):733-744.
11. Jones DM, Domingues P, Targett-Adams P, McLauchlan J. 2010. Comparison of U2OS and Huh-7 cells for identifying host factors that affect hepatitis C virus RNA replication. J Gen Virol 91(Pt 9):2238-2248.
12. Kawaguchi T, Ide T, Taniguchi E, Hirano E, Itou M, Sumie S, Nagao Y, Yanagimoto C, Hanada S, Koga H, Sata M. 2007. Clearance of HCV improves insulin resistance, beta-cell function, and hepatic expression of insulin receptor substrate 1 and 2. Am J Gastroenterol 102(3):570-576.
13. Kawaguchi T, Yoshida T, Harada M, Hisamoto T, Nagao Y, Ide T, Taniguchi E, Kumemura H, Hanada S, Maeyama M, Baba S, Koga H, Kumashiro R, Ueno T, Ogata H, Yoshimura A, Sata M. 2004. Hepatitis C virus down-regulates insulin receptor substrates 1 and 2 through up-regulation of suppressor of cytokine signaling 3. Am J Pathol 165(5):1499-1508.
14. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12(6):996-1006.
15. Lanford RE, Guerra B, Bigger CB, Lee H, Chavez D, Brasky KM. 2007. Lack of response to exogenous interferon-alpha in the liver of chimpanzees chronically infected with hepatitis C virus. Hepatology 46(4):999-1008.
16. Lawitz E, Sulkowski MS, Ghalib R, Rodriguez-Torres M, Younossi ZM, Corregidor A, DeJesus E, Pearlman B, Rabinovitz M, Gitlin N, Lim JK, Pockros PJ, Scott JD, Fevery B, Lambrecht T, Ouwerkerk-Mahadevan S, Callewaert K, Symonds WT, Picchio G, Lindsay KL, Beumont M, Jacobson IM. 2014. Simeprevir plus sofosbuvir, with or without ribavirin, to treat chronic infection with hepatitis C virus genotype 1 in non-responders to pegylated interferon and ribavirin and treatment-naive patients: The COSMOS randomised study. Lancet 384(9956):1756-1765.
17. Lee JH, Joe EH, Jou I. 2005. PPAR-alpha activators suppress STAT1 inflammatory signaling in lipopolysaccharide-activated rat glia. Neuroreport 16(8):829-833.
18. Michalik L, Wahli W. 2008. PPARs mediate lipid signaling in inflammation and cancer. PPAR Res 2008:134059.
19. Odorizzi PM, Wherry EJ. 2013. Immunology. An interferon paradox. Science 340(6129):155-156.
20. Persico M, Capasso M, Persico E, Svelto M, Russo R, Spano D, Croce L, La Mura V, Moschella F, Masutti F, Torella R, Tiribelli C, Iolascon A. 2007. Suppressor of cytokine signaling 3 (SOCS3) expression and hepatitis C virus-related chronic hepatitis: Insulin resistance and response to antiviral therapy. Hepatology 46(4):1009-1015.
21. Poordad F, McCone J, Jr., Bacon BR, Bruno S, Manns MP, Sulkowski MS, Jacobson IM, Reddy KR, Goodman ZD, Boparai N, DiNubile MJ, Sniukiene V, Brass CA, Albrecht JK, Bronowicki JP. 2011. Boceprevir for untreated chronic HCV genotype 1 infection. N Engl J Med 364(13):1195-1206.
22. Reich NC. 2007. STAT dynamics. Cytokine Growth Factor Rev 18(5-6):511-518.
23. Romero-Gomez M, Del Mar Viloria M, Andrade RJ, Salmeron J, Diago M, Fernandez-Rodriguez CM, Corpas R, Cruz M, Grande L, Vazquez L, Munoz-De-Rueda P, Lopez-Serrano P, Gila A, Gutierrez ML, Perez C, Ruiz-Extremera A, Suarez E, Castillo J. 2005. Insulin resistance impairs sustained response rate to peginterferon plus ribavirin in chronic hepatitis C patients. Gastroenterology 128(3):636-641.
24. Rothlin CV, Ghosh S, Zuniga EI, Oldstone MB, Lemke G. 2007. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131(6):1124-1136.
25. Sarasin-Filipowicz M, Oakeley EJ, Duong FH, Christen V, Terracciano L, Filipowicz W, Heim MH. 2008. Interferon signaling and treatment outcome in chronic hepatitis C. Proc Natl Acad Sci U S A 105(19):7034-7039.
26. Sarasin-Filipowicz M, Wang X, Yan M, Duong FH, Poli V, Hilton DJ, Zhang DE, Heim MH. 2009. Alpha interferon induces long-lasting refractoriness of JAK-STAT signaling in the mouse liver through induction of USP18/UBP43. Mol Cell Biol 29(17):4841-4851.
27. Sumpter R, Jr., Loo YM, Foy E, Li K, Yoneyama M, Fujita T, Lemon SM, Gale M, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellularRNAhelicase, RIG-I. JVirol 79(5):2689-2699.
28. van der Meer DL, Degenhardt T, Vaisanen S, de Groot PJ, Heinaniemi M, de Vries SC, Muller M, Carlberg C, Kersten S. 2010. Profiling of promoter occupancy by PPARalpha in human hepatoma cells via ChIP-chip analysis. Nucleic Acids Res 38(9):2839-2850.
29. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11(7):791-796.
30. Yoo SH, Park O, Henderson LE, Abdelmegeed MA, Moon KH, Song BJ. 2011. Lack of PPARalpha exacerbates lipopolysaccharide-induced liver toxicity through STAT1 inflammatory signaling and increased oxidative/nitrosative stress. Toxicol Lett 202(1):23-29.