Forkhead box transcription factor regulation and lipid accumulation by hepatitis C virus

Journal of Virology

Volumn 88, Issue 8, 2014, Pages 4195-4203

  Bose, Sandip K ^a   Kim, Hangeun ^a   Meyer, Keith ^a   Wolins, Nathan ^b   Davidson, Nicholas O ^b   Ray, Ranjit ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRYL COENZYME A DEHYDROGENASE; CORE PROTEIN; FATTY ACID SYNTHASE; FORKHEAD TRANSCRIPTION FACTOR; HEPATOCYTE NUCLEAR FACTOR 3BETA; HORMONE SENSITIVE LIPASE; MEDIUM CHAIN ACYL COENZYME A DEHYDROGENASE; PERILIPIN; PERILIPIN 2; SMALL INTERFERING RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FATTY ACID OXIDATION; HEPATITIS C; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; LIPID STORAGE; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VIRUS REPLICATION;

ACYL-COA DEHYDROGENASE; CELL LINE; FATTY ACID SYNTHASES; FATTY ACIDS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEPACIVIRUS; HEPATITIS C; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HUMANS; LIPID METABOLISM; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; VIRAL CORE PROTEINS; VIRUS REPLICATION;

EID: 84897002580     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03327-13     Document Type: Article

References (48)

1. Shepard CW, Finelli L, Alter MJ. 2005. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 5:558-567. http://dx.doi.org/10.1016/S1473-3099(05)70216-4.
2. Negro F, Alaei M. 2009. Hepatitis C virus and type 2 diabetes. World J. Gastroenterol. 15:1537-1547. http://dx.doi.org/10.3748/wjg.15.1537.
3. Negro F. 2010. Abnormalities of lipid metabolism in hepatitis C virus infection. Gut 59:1279-1287. http://dx.doi.org/10.1136/gut.2009.192732.
4. Thomas DL. 2013. Global control of hepatitis C: where challenge meets opportunity. Nat. Med. 19:850-858. http://dx.doi.org/10.1038/nm.3184.
5. Levrero M. 2006. Viral hepatitis and liver cancer. Oncogene 25:3834-3847. http://dx.doi.org/10.1038/sj.onc.1209562.
6. Banerjee S, Saito K, Ait-Goughoulte M, Meyer K, Ray RB, Ray R. 2008. Hepatitis C virus core protein upregulates serine phosphorylation of IRS-1 and impairs downstream AKT/PKB signaling pathway for insulin resistance. J. Virol. 82:2606-2612. http://dx.doi.org/10.1128/JVI.01672-07.
7. Bose SK, Shrivastava S, Meyer K, Ray RB, Ray R. 2012. Hepatitis C virus activates the mTOR/S6K1 signaling pathway in inhibiting IRS-1 function for insulin resistance. J. Virol. 86:6315-6322. http://dx.doi.org/10.1128/JVI.00050-12.
8. Puigserver PJ, Donovan RJ, Walkey CJ, Yoon JC, Oriente F, Kitamura Y, Altomonte J, Dong H, Accili D, Spiegelman BM. 2003. Insulinregulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature 423:550-555. http://dx.doi.org/10.1038/nature01667.
9. Matsumoto MS, Kitamura HT, Accili D. 2006. Dual role of transcription factor FoxO1 in controlling hepatic insulin sensitivity and lipid metabolism. J. Clin. Invest. 116:2464-2472. http://dx.doi.org/10.1172/JCI27047.
10. Nakae J, Kitamura T, Silver DL, Accili D. 2001. The forkhead transcription factor Foxo1 (Fkhr) confers insulin sensitivity onto glucose-6-phosphatase expression. J. Clin. Invest. 108:1359-1367. http://dx.doi.org/10.1172/JCI200112876.
11. Wolfrum C, Asilmaz E, Luca E, Friedman JM, Stoffel M. 2004. Foxa2 regulates lipid metabolism and ketogenesis in the liver during fasting and in diabetes. Nature 432:1027-1032. http://dx.doi.org/10.1038/nature03047.
12. Wolfrum C, Stoffel M. 2006. Coactivation of Foxa2 through Pgc-1bet promotes liver fatty acid oxidation and triglyceride/VLDL secretion. Cell Metab. 3:99-110. http://dx.doi.org/10.1016/j.cmet.2006.01.001.
13. Horton JD, Shah NA, Warrington JA, Anderson NN, Park SW, Brown MS, Goldstein JL. 2003. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. U. S. A. 100:12027-12032. http://dx.doi.org/10.1073/pnas.1534923100.
14. Brasaemle DL. 2007. Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J. Lipid Res. 48:2547-2559. http://dx.doi.org/10.1194/jlr. R700014-JLR200.
15. Imai Y, Varela GM, Jackson MB, Graham MJ, Crooke RM, Ahima RS. 2007. Reduction of hepatosteatosis and lipid levels by an adipose differentiation-related protein antisense oligonucleotide. Gastroenterology 132: 1947-1954. http://dx.doi.org/10.1053/j.gastro.2007.02.046.
16. Kanda T, Basu A, Steele R, Wakita T, Ryerse JS, Ray R, Ray RB. 2006. Generation of infectious hepatitis C virus in immortalized human hepatocytes. J. Virol. 80:4633-4639. http://dx.doi.org/10.1128/JVI.80.9.4633-4639.2006.
17. Wolins NE, Quaynor BK, Skinner JR, Schoenfish MJ, Tzekov A, Bickel PE. 2005. S3-12, adipophilin, and TIP47 package lipid in adipocytes. J. Biol. Chem. 280:19146-19155. http://dx.doi.org/10.1074/jbc. M500978200.
18. Oem JK, Jackel-Cram C, Li YP, Zhou Y, Zhong J, Shimano H, Babiuk LA, Liu Q. 2008. Activation of sterol regulatory element-binding protein 1c and fatty acid synthase transcription by hepatitis C virus non-structural protein 2. J. Gen. Virol. 89:1225-1230. http://dx.doi.org/10.1099/vir.0.83491-0.
19. Xiang Z, Qiao L, Zhou Y, Babiuk LA, Liu Q. 2010. Hepatitis C virus nonstructural protein-5A activates sterol regulatory element-binding protein-1c through transcription factor Sp1. Biochem. Biophys. Res. Commun. 402:549-553. http://dx.doi.org/10.1016/j.bbrc.2010.10.081.
20. Banerjee A, Meyer K, Mazumdar B, Ray RB, Ray R. 2010. Hepatitis C virus differentially modulates activation of forkhead transcription factors and insulin-induced metabolic gene expression. J. Virol. 84:5936-5946. http://dx.doi.org/10.1128/JVI.02344-09.
21. Weickert MO, Pfeiffer AF. 2006. Signaling mechanisms linking hepatic glucose and lipid metabolism. Diabetologia 49:1732-1741. http://dx.doi.org/10.1007/s00125-006-0295-3.
22. Wu JM, Skill NJ, Maluccio MA. 2010. Evidence of aberrant lipid metabolism in hepatitis C and hepatocellular carcinoma. HPB (Oxford) 12:625-636. http://dx.doi.org/10.1111/j.1477-2574.2010.00207.x.
23. Yeaman SJ. 1990. Hormone-sensitive lipase-a multipurpose enzyme in lipid metabolism. Biochim. Biophys. Acta 1052:128-132. http://dx.doi.org/10.1016/0167-4889(90)90067-N.
24. Yeaman SJ. 2004. Hormone-sensitive lipase-new roles for an old enzyme. Biochem. J. 379:11-22. http://dx.doi.org/10.1042/BJ20031811.
25. Lerat H, Kammoun HL, Hainault I, Mérour E, Higgs MR, Callens C, Lemon SM, Foufelle F, Pawlotsky JM. 2009. Hepatitis C virus proteins induce lipogenesis and defective triglyceride secretion in transgenic mice. J. Biol. Chem. 284:33466-33474. http://dx.doi.org/10.1074/jbc. M109.019810.
26. Yang W, Hood BL, Chadwick SL, Liu S, Watkins SC, Luo G, Conrads TP, Wang T. 2008. Fatty acid synthase is up-regulated during hepatitis C virus infection and regulates hepatitis C virus entry and production. Hepatology 48:1396-1403. http://dx.doi.org/10.1002/hep.22508.
27. Nasheri N, Joyce M, Rouleau Y, Yang P, Yao S, Tyrrell DL, Pezacki JP. 2013. Modulation of fatty acid synthase enzyme activity and expression during hepatitis C virus replication. Chem. Biol. 20:570-582. http://dx.doi.org/10.1016/j.chembiol.2013.03.014.
28. Sun LJ, Li SC, Zhao YH, Yu JW, Kang P, Yan BZ. 2013. Silent information regulator 1 inhibition induces lipid metabolism disorders of hepatocytes and enhances hepatitis C virus replication. Hepatol. Res. 43:1343-1351. http://dx.doi.org/10.1111/hepr.12089.
29. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, Zayas M, Bartenschlager R, Wakita T, Hijikata M, Shimotohno K. 2007. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9:1089-1097. http://dx.doi.org/10.1038/ncb1631.
30. Ogawa K, Hishiki T, Shimizu Y, Funami K, Sugiyama K, Miyanari Y, Shimotohno K. 2009. Hepatitis C virus utilizes lipid droplet for production of infectious virus. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 85:217-228. http://dx.doi.org/10.2183/pjab.85.217.
31. Mankouri J, Tedbury PR, Gretton S, Hughes ME, Griffin SD, Dallas ML, Green KA, Hardie DG, Peers C, Harris M. 2010. Enhanced hepatitis C virus genome replication and lipid accumulation mediated by inhibition of AMP-activated protein kinase. Proc. Natl. Acad. Sci. U. S. A. 107: 11549-11554. http://dx.doi.org/10.1073/pnas.0912426107.
32. Egger D, Wölk B, Gosert R, Bianchi L, Blum HE, Moradpour D, Bienz K. 2002. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 76:5974-5984. http://dx.doi.org/10.1128/JVI.76.12.5974-5984.2002.
33. Moradpour D, Englert C, Wakita T, Wands JR. 1996. Characterization of cell lines allowing tightly regulated expression of hepatitis C virus core protein. Virology 222:51-63. http://dx.doi.org/10.1006/viro.1996.0397.
34. Deleersnyder V, Pillez A, Wychowski C, Blight K, Xu J, Hahn YS, Rice CM, Dubuisson J. 1997. Formation of native hepatitis C virus glycoprotein complexes. J. Virol. 71:697-704.
35. Tanaka T, Kuroda K, Ikeda M, Wakita T, Kato N, Makishima M. 2013. Hepatitis C virus NS4B targets lipid droplets through hydrophobic residues in the amphipathic helices. J. Lipid Res. 54:881-892. http://dx.doi.org/10.1194/jlr. M026443.
36. Vogt DA, Camus G, Herker E, Webster BR, Tsou CL, Greene WC, Yen TS, Ott M. 2013. Lipid droplet-binding protein TIP47 regulates hepatitis C virus RNA replication through interaction with the viral NS5A protein. PLoS Pathog. 9:e1003302. http://dx.doi.org/10.1371/journal.ppat.1003302.
37. Salloum S, Wang H, Ferguson C, Parton RG, Tai AW. 2013. Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets. PLoS Pathog. 9:e1003513. http://dx.doi.org/10.1371/journal.ppat.1003513.
38. Moriya K, Yotsuyanagi H, Shintani Y, Fujie H, Ishibashi K, Matsuura Y, Miyamura T, Koike K. 1997. Hepatitis C virus core protein induces hepatic steatosis in transgenic mice. J. Gen. Virol. 78:1527-1531.
39. Cheung W, Gill M, Esposito A, Kaminski CF, Courousse N, ChwetzoffS, Trugnan G, Keshavan N, Lever A, Desselberger U. 2010. Rotaviruses associate with cellular lipid droplet components to replicate in viroplasms, and compounds disrupting or blocking lipid droplets inhibit viroplasm formation and viral replication. J. Virol. 84:6782-6798. http://dx.doi.org/10.1128/JVI.01757-09.
40. Martín-Acebes MA, Blázquez AB, Jiménez de Oya N, Escribano-Romero E, Saiz JC. 2011. West Nile virus replication requires fatty acid synthesis but is independent on phosphatidylinositol-4-phosphate lipids. PLoS One 6:e24970. http://dx.doi.org/10.1371/journal.pone.0024970.
41. Wang RY, Li K. 2012. Host factors in the replication of positive-strand RNA viruses. Chang Gung Med. J. 35:111-124.
42. Ahola T, Lampio A, Auvinen P, Kaariainen L. 1999. Semliki Forest virus mRNA capping enzyme requires association with anionic membrane phospholipids for activity. EMBO J. 18:3164-3172. http://dx.doi.org/10.1093/emboj/18.11.3164.
43. Saito K, Nishijima M, Kuge O. 2006. Phosphatidylserine is involved in gene expression from Sindbis virus subgenomic promoter. Biochem. Biophys. Res. Commun. 345:878-885. http://dx.doi.org/10.1016/j.bbrc.2006.04.138.
44. Jeong SW, Jang JY, Chung RT. 2012. Hepatitis C virus and hepatocarcinogenesis. Clin. Mol. Hepatol. 18:347-356. http://dx.doi.org/10.3350/cmh.2012.18.4.347.
45. Oben JA, Paulon E. 2007. Fatty liver in chronic hepatitis C infection: unravelling the mechanisms. Gut 56:1186-1188. http://dx.doi.org/10.1136/gut.2006.118422.
46. Qadri I, Choudhury M, Rahman SM, Knotts TA, Janssen RC, Schaack J, Iwahashi M, Puljak L, Simon FR, Kilic G, Fitz JG, Friedman JE. 2012. Increased phosphoenolpyruvate carboxykinase gene expression and steatosis during hepatitis C virus subgenome replication: role of nonstructural component 5A and CCAAT/enhancer-binding protein β. J. Biol. Chem. 287:37340-37351. http://dx.doi.org/10.1074/jbc. M112.384743.
47. Syed GH, Amako Y, Siddiqui A. 2010. Hepatitis C virus hijacks host lipid metabolism. Trends Endocrinol. Metab. 21:33-40. http://dx.doi.org/10.1016/j.tem.2009.07.005.
48. Hui JM, Sud A, Farrell GC, Bandara P, Byth K, Kench JG, McCaughan GW, George J. 2003. Insulin resistance is associated with chronic hepatitis C virus infection and fibrosis progression. Gastroenterology 125:1695-1704. http://dx.doi.org/10.1053/j.gastro.2003.08.032.