Hepatitis C virus-induced furin and thrombospondin-1 activate TGF-β1: Role of TGF-β1 in HCV replication

Virology

Volumn 412, Issue 2, 2011, Pages 284-296

  Presser, Lance D ^a   Haskett, Adam ^a   Waris, Gulam ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Calcium; Furin; HCV replication; Hepatitis C virus; ROS; TGF 1; Thrombospondin 1

Indexed keywords

ANGIOGENIN; CALCIUM CHELATING AGENT; CORE PROTEIN; FURIN; MESSENGER RNA; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5A; PLATELET DERIVED GROWTH FACTOR BB; REACTIVE OXYGEN METABOLITE; SERINE PROTEINASE; SMALL INTERFERING RNA; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ARTICLE; CALCIUM SIGNALING; CELL CULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE MUTATION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

CARRIER PROTEINS; CELL LINE; DNA MUTATIONAL ANALYSIS; FURIN; GENE SILENCING; GENES, REPORTER; HEPACIVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; LUCIFERASES; MUTAGENESIS, SITE-DIRECTED; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 79952616582     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.12.051     Document Type: Article

References (60)

1. Abe M., Harpel J.G., Metz C.N., Nunes I., Loskutoff D.J., Rifkin D.B. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal. Biochem. 1994, 216(2):276-284.
2. Adinolfi L.E., Utili R., Andreana A., Tripodi M.F., Marracino M., Gambardella M., Giordano M., Ruggiero G. Serum HCV RNA levels correlate with histological liver damage and concur with steatosis in progression of chronic hepatitis C. Dig. Dis. Sci. 2001, 46(8):1677-1683.
3. Annes J.P., Munger J.S., Rifkin D.B. Making sense of latent TGF beta activation. J. Cell Sci. 2003, 116(2):217-224.
4. Bartenschlager R., Lohmann V. Replication of hepatitis C virus. J. Gen. Virol. 2000, 81(7):1631-1648.
5. Bataller R., Paik Y.H., Lindquist J.N., Lemasters J.J., Brenner D.A. Hepatitis C virus core and nonstructural proteins induce fibrogenic effects in hepatic stellate cells. Gastroenterology 2004, 126(2):529-540.
6. Benali-Furet N.L., Chami M., Houel L., De Giorgi F., Vernejoul F., Lagorce D., Buscail L., Bartenschlager R., Ichas F., Rizzuto R., Paterlini-Brechot P. Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion. Oncogene 2005, 24(31):4921-4933.
7. Bissell D.M., Roulot D., George J. Transforming growth factor beta and the liver. Hepatology 2001, 34(5):859-867.
8. Blackard J.T., Kemmer N., Sherman K.E. Extrahepatic replication of HCV: insights into clinical manifestations and biological consequences. Hepatology 2006, 44(1):15-22.
9. Blight K.J., McKeating J.A., Rice C.M. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 2002, 76:13001-13014.
10. Brass V., Bieck E., Montserret R., Wolk B., Hellings J.A., Blum H.E., Penin F., Moradpour D. An amino-terminal amphipathic alpha-helix mediates membrane association of the hepatitis C virus nonstructural protein 5A. J. Biol. Chem. 2002, 277(10):8130-8139.
11. Burdette D., Olivarez M., Waris G. Activation of transcription factor Nrf2 by hepatitis C virus induces the cell-survival pathway. J. Gen. Virol. 2010, 91(3):681-690.
12. Bureau C., Bernad J., Chaouche N., Orfila C., Beraud M., Gonindard C., Alric L., Vinel J.P., Pipy B. Nonstructural 3 protein of hepatitis C virus triggers an oxidative burst in human monocytes via activation of NADPH oxidase. J. Biol. Chem. 2001, 276(25):23077-23083.
13. Calzada M.J., Kuznetsova S.A., Sipes J.M., Rodrigues R.G., Cashel J.A., Annis D.S., Mosher D.F., Roberts D.D. Calcium indirectly regulates immunochemical reactivity and functional activities of the N-domain of thrombospondin-1. Matrix Biol. 2008, 27(4):339-351.
14. Canbay A., Friedman S., Gores G.J. Apoptosis: the nexus of liver injury and fibrosis. Hepatology 2004, 39(2):273-278.
15. Di Bisceglie A.M. Hepatitis C and hepatocellular carcinoma. Hepatology 1997, 26(3):34S-38S.
16. Dubois C.M., Laprise M.H., Blanchette F., Gentry L.E., Leduc R. Processing of transforming growth factor beta 1 precursor by human furin convertase. J. Biol. Chem. 1995, 270(18):10618-10624.
17. Gao C., Gressner G., Zoremba M., Gressner A.M. Transforming growth factor beta (TGF-beta) expression in isolated and cultured rat hepatocytes. J. Cell. Physiol. 1996, 167(3):394-405.
18. Gong G., Waris G., Tanveer R., Siddiqui A. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-kappa B. Proc. Natl Acad. Sci. 2001, 98(17):9599-9604.
19. Gouttenoire J., Penin F., Moradpour D. Hepatitis C virus nonstructural protein 4B: a journey into unexplored territory. Rev. Med. Virol. 2001, 20(2):117-129.
20. Grakoui A., Wychowski C., Lin C., Feinstone S.M., Rice C.M. Expression and identification of hepatitis C virus polyprotein cleavage products. J. Virol. 1993, 67(3):1385-1395.
21. Grungreiff K., Reinhold D., Ansorge S. Serum concentrations of sIL-2R, IL-6, TGF-beta1, neopterin, and zinc in chronic hepatitis C patients treated with interferon-alpha. Cytokine 1999, 11(12):1076-1080.
22. Hosui A., Kimura A., Yamaji D., Zhu B.M., Na R., Hennighausen L. Loss of STAT5 causes liver fibrosis and cancer development through increased TGF-{beta} and STAT3 activation. J. Exp. Med. 2009, 206(4):819-831.
23. Jennings M.T., Pietenpol J.A. The role of transforming growth factor beta in glioma progression. J. Neurooncol. 1998, 36(2):123-140.
24. Jeong W.I., Do S.H., Yun H.S., Song B.J., Kim S.J., Kwak W.J., Yoo S.E., Park H.Y., Jeong K.S. Hypoxia potentiates transforming growth factor-beta expression of hepatocyte during the cirrhotic condition in rat liver. Liver Int. 2004, 24(6):658-668.
25. Johnson C.L., Owen D.M., Gale M. Functional and therapeutic analysis of hepatitis C virus NS3.4A protease control of antiviral immune defense. J. Biol. Chem. 2007, 282(14):10792-10803.
26. Kaminska B., Wesolowska A., Danilkiewicz M. TGF beta signalling and its role in tumour pathogenesis. Acta Biochim. Pol. 2005, 52(2):329-337.
27. Kasprzak A., Adamek A. Role of hepatitis C virus proteins (C, NS3, NS5A) in hepatic oncogenesis. Hepatol. Res. 2008, 38(1):1-26.
28. Kazerounian S., Yee K.O., Lawler J. Thrombospondins in cancer. Cell. Mol. Life Sci. 2008, 65(5):700-712.
29. Li K., Foy E., Ferreon J.C., Nakamura M., Ferreon A.C., Ikeda M., Ray S.C., Gale M., Lemon S.M. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl Acad. Sci. 2005, 102(8):2992-2997.
30. Li S., Ye L., Yu X., Xu B., Li K., Zhu X., Liu H., Wu X., Kong L. Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulum overload response-dependent NF-kappaB activation. Virology 2009, 391(2):257-264.
31. Lin W., Weinberg E.M., Tai A.W., Peng L.F., Brockman M.A., Kim K.A., Kim S.S., Borges C.B., Shao R.X., Chung R.T. HIV increases HCV replication in a TGF-beta1-dependent manner. Gastroenterology 2008, 134(3):803-811.
32. Lin W., Tsai W.L., Shao R.X., Wu G., Peng L.F., Barlow L.L., Chung W.J., Zhang L., Zhao H., Jang J.Y., Chung R.T. Hepatitis C virus regulates transforming growth factor beta1 production through the generation of reactive oxygen species in a nuclear factor kappaB-dependent manner. Gastroenterology 2010, 138(7):2509-2518. 2518 e1.
33. Lindenbach B.D., Evans M.J., Syder A.J., Wolk B., Tellinghuisen T.L., Liu C.C., Maruyama T., Hynes R.O., Burton D.R., McKeating J.A., Rice C.M. Complete replication of hepatitis C virus in cell culture. Science 2005, 309(5734):623-626.
34. Lohmann V., Koch J.O., Bartenschlager R. Processing pathways of the hepatitis C virus proteins. J. Hepatol. 1996, 24(2):11-19.
35. Macdonald A., Harris M. Hepatitis C virus NS5A: tales of a promiscuous protein. J. Gen. Virol. 2004, 85(9):2485-2502.
36. Machida K., Cheng K.T., Lai C.K., Jeng K.S., Sung V.M., Lai M.M. Hepatitis C virus triggers mitochondrial permeability transition with production of reactive oxygen species, leading to DNA damage and STAT3 activation. J. Virol. 2006, 80(14):7199-7207.
37. McCann K.L., Imani F. Transforming growth factor beta enhances respiratory syncytial virus replication and tumor necrosis factor alpha induction in human epithelial cells. J. Virol. 2007, 81(6):2880-2886.
38. McMahon S., Charbonneau M., Grandmont S., Richard D.E., Dubois C.M. Transforming growth factor beta1 induces hypoxia-inducible factor-1 stabilization through selective inhibition of PHD2 expression. J. Biol. Chem. 2006, 281(34):24171-24181.
39. Murata T., Ohshima T., Yamaji M., Hosaka M., Miyanari Y., Hijikata M., Shimotohno K. Suppression of hepatitis C virus replicon by TGF-beta. Virology 2005, 331(2):407-417.
40. Nelson D.R., Gonzalez-Peralta R.P., Qian K., Xu Y., Marousis C.G., Davis G.L., Lau J.Y. Transforming growth factor-beta 1 in chronic hepatitis C. J. Viral Hepat. 1997, 4(1):29-35.
41. Okuda M., Li K., Beard M.R., Showalter L.A., Scholle F., Lemon S.M., Weinman S.A. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology 2002, 122(2):366-375.
42. Pal S., Polyak S.J., Bano N., Qiu W.C., Carithers R.L., Shuhart M., Gretch D.R., Das A. Hepatitis C virus induces oxidative stress, DNA damage and modulates the DNA repair enzyme NEIL1. J. Gastroenterol. Hepatol. 2010, 25(3):627-634.
43. Paradis V., Degos F., Dargere D., Pham N., Belghiti J., Degott C., Janeau J.L., Bezeaud A., Delforge D., Cubizolles M., Laurendeau I., Bedossa P. Identification of a new marker of hepatocellular carcinoma by serum protein profiling of patients with chronic liver diseases. Hepatology 2005, 41(1):40-47.
44. Piccoli C., Scrima R., Quarato G., D'Aprile A., Ripoli M., Lecce L., Boffoli D., Moradpour D., Capitanio N. Hepatitis C virus protein expression causes calcium-mediated mitochondrial bioenergetic dysfunction and nitro-oxidative stress. Hepatology 2007, 46(1):58-65.
45. Ravichandran V., Jensen P.N., Major E.O. MEK1/2 inhibitors block basal and transforming growth factor 1beta1-stimulated JC virus multiplication. J. Virol. 2007, 81(12):6412-6418.
46. Rizzuto R., Pozzan T. Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol. Rev. 2006, 86(1):369-408.
47. Rossmanith W., Schulte-Hermann R. Biology of transforming growth factor beta in hepatocarcinogenesis. Microsc. Res. Tech. 2001, 52(4):430-436.
48. Schulze-Krebs A., Preimel D., Popov Y., Bartenschlager R., Lohmann V., Pinzani M., Schuppan D. Hepatitis C virus-replicating hepatocytes induce fibrogenic activation of hepatic stellate cells. Gastroenterology 2005, 129(1):246-258.
49. Schuppan D., Krebs A., Bauer M., Hahn E.G. Hepatitis C and liver fibrosis. Cell Death Differ. 2003, 10(1):S59-S67.
50. Takehara T., Tatsumi T., Suzuki T., Rucker E.B., Hennighausen L., Jinushi M., Miyagi T., Kanazawa Y., Hayashi N. Hepatocyte-specific disruption of Bcl-xL leads to continuous hepatocyte apoptosis and liver fibrotic responses. Gastroenterology 2004, 127(4):1189-1197.
51. Taniguchi H., Kato N., Otsuka M., Goto T., Yoshida H., Shiratori Y., Omata M. Hepatitis C virus core protein upregulates transforming growth factor-beta 1 transcription. J. Med. Virol. 2004, 72(1):52-59.
52. Tardif K.D., Mori K., Kaufman R.J., Siddiqui A. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J. Biol. Chem. 2004, 279(17):17158-17164.
53. Tardif K.D., Waris G., Siddiqui A. Hepatitis C virus, ER stress, and oxidative stress. Trends Microbiol. 2005, 13(4):159-163.
54. Wakita T., Pietschmann T., Kato T., Date T., Miyamoto M., Zhao Z., Murthy K., Habermann A., Krausslich H.G., Mizokami M., Bartenschlager R., Liang T.J. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 2005, 11(7):791-796.
55. Waris G., Tardif K.D., Siddiqui A. Endoplasmic reticulum (ER) stress: hepatitis C virus induces an ER-nucleus signal transduction pathway and activates NF-kappaB and STAT-3. Biochem. Pharmacol. 2002, 64(10):1425-1430.
56. Waris G., Livolsi A., Imbert V., Peyron J.F., Siddiqui A. Hepatitis C virus NS5A and subgenomic replicon activate NF-kappaB via tyrosine phosphorylation of IkappaBalpha and its degradation by calpain protease. J. Biol. Chem. 2003, 278(42):40778-40787.
57. Waris G., Turkson J., Hassanein T., Siddiqui A. Hepatitis C virus (HCV) constitutively activates STAT-3 via oxidative stress: role of STAT-3 in HCV replication. J. Virol. 2005, 79(3):1569-1580.
58. Waris G., Felmlee D.J., Negro F., Siddiqui A. Hepatitis C virus induces proteolytic cleavage of sterol regulatory element binding proteins and stimulates their phosphorylation via oxidative stress. J. Virol. 2007, 81(15):8122-8130.
59. Wilson L.E., Torbenson M., Astemborski J., Faruki H., Spoler C., Rai R., Mehta S., Kirk G.D., Nelson K., Afdhal N., Thomas D.L. Progression of liver fibrosis among injection drug users with chronic hepatitis C. Hepatology 2006, 43(4):788-795.
60. Zhong J., Gastaminza P., Cheng G., Kapadia S., Kato T., Burton D.R., Wieland S.F., Uprichard S.L., Wakita T., Chisari F.V. Robust hepatitis C virus infection in vitro. Proc. Natl Acad. Sci. 2005, 102(26):9294-9299.