Interferon-α suppresses hepatitis B virus enhancer II activity via the protein kinase C pathway

Virology

Volumn 432, Issue 2, 2012, Pages 452-459

  Nawa, Takatoshi ^a   Ishida, Hisashi ^a   Tatsumi, Tomohide ^a   Li, Wei ^a   Shimizu, Satoshi ^a   Kodama, Takahiro ^a   Hikita, Hayato ^a   Hosui, Atsushi ^a   Miyagi, Takuya ^a   Kanto, Tatsuya ^a   Hiramatsu, Naoki ^a   Hayashi, Norio ^b   Takehara, Tetsuo ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KANSAI ROSAI HOSPITAL   (Japan)

Author keywords

Enhancer II; HBV; Interferon ; Protein kinase C

Indexed keywords

ALPHA INTERFERON; MYXOVIRUS RESISTANCE PROTEIN; PROTEIN KINASE C; STAT1 PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; ENHANCER II REGION; ENHANCER REGION; GENE DELETION; GENE MUTATION; GENE REPRESSION; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTIVIRAL AGENTS; BASE SEQUENCE; CELL LINE, TUMOR; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, VIRAL; HEPATITIS B VIRUS; HUMANS; INTERFERON-ALPHA; MOLECULAR SEQUENCE DATA; PROTEIN KINASE C; TRANSFECTION; VIRUS REPLICATION;

HEPATITIS B VIRUS;

EID: 84865277717     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.07.002     Document Type: Article

References (55)

1. Antonucci T.K., Rutter W.J. Hepatitis B virus (HBV) promoters are regulated by the HBV enhancer in a tissue-specific manner. J. Virol. 1989, 63:579-583.
2. Azzi A., Boscoboinik D., Hensey C. The protein kinase C family. Eur. J. Biochem. 1992, 208:547-557.
3. Beck J., Nassal M. Hepatitis B virus replication. World J. Gastroenterol. 2007, 13:48-64.
4. Breitkreutz D., Braiman-Wiksman L., Daum N., Denning M.F., Tennenbaum T. Protein kinase C family: on the crossroads of cell signaling in skin and tumor epithelium. J. Cancer Res. Clin. Oncol. 2007, 133:793-808.
5. Bruss V., Ganem D. The role of envelope proteins in hepatitis B virus assembly. Proc. Nat. Acad. Sci. U.S.A. 1991, 88:1059-1063.
6. Caraglia M., Abbruzzese A., Leardi A., Pepe S., Budillon A., Baldassare G., Selleri C., Lorenzo S.D., Fabbrocini A., Giuberti G., Vitale G., Lupoli G., Bianco A.R., Tagliaferri P. Interferon-alpha induces apoptosis in human KB cells through a stress-dependent mitogen activated protein kinase pathway that is antagonized by epidermal growth factor. Cell Death Differ. 1999, 6:773-780.
7. Castagna M., Takai Y., Kaibuchi K., Sano K., Kikkawa U., Nishizuka Y. Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J. Biol. Chem. 1982, 257:7847-7851.
8. Darnell J.E., Kerr I.M., Stark G.R. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994, 264:1415-1421.
9. David M., Petricoin E., Benjamin C., Pine R., Weber M.J., Larner A.C. Requirement for MAP kinase (ERK2) activity in interferon alpha- and interferon beta-stimulated gene expression through STAT proteins. Science 1995, 269:1721-1723.
10. Delmotte M.H., Tahayato A., Formstecher P., Lefebvre P. Serine 157, a retinoic acid receptor alpha residue phosphorylated by protein kinase C in vitro, is involved in RXR. RARalpha heterodimerization and transcriptional activity. J. Biol. Chem. 1999, 274:38225-38231.
11. Der S.D., Zhou A., Williams B.R., Silverman R.H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Nat. Acad. Sci. U.S.A. 1998, 95:15623-15628.
12. Goh K.C., Haque S.J., Williams B.R. p38 MAP kinase is required for STAT1 serine phosphorylation and transcriptional activation induced by interferons. EMBO J. 1999, 18:5601-5608.
13. Griner E.M., Kazanietz M.G. Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer 2007, 7:281-294.
14. Gschwendt M., Müller H.J., Kielbassa K., Zang R., Kittstein W., Rincke G., Marks F. Rottlerin, a novel protein kinase inhibitor. Biochem. Biophys. Res. Commun. 1994, 199:93-98.
15. Guo W., Chen M., Yen T.S., Ou J.H. Hepatocyte-specific expression of the hepatitis B virus core promoter depends on both positive and negative regulation. Mol. Cell. Biol. 1993, 13:443-448.
16. Ishida H., Ueda K., Ohkawa K., Kanazawa Y., Hosui A., Nakanishi F., Mita E., Kasahara A., Sasaki Y., Hori M., Hayashi N. Identification of multiple transcription factors, HLF, FTF, and E4BP4, controlling hepatitis B virus enhancer II. J. Virol. 2000, 74:1241-1251.
17. Johnson J.L., Raney A.K., McLachlan A. Characterization of a functional hepatocyte nuclear factor 3 binding site in the hepatitis B virus nucleocapsid promoter. Virology 1995, 208:147-158.
18. Jonas M.M., Block J.M., Haber B.A., Karpen S.J., London W.T., Murray K.F., Narkewicz M.R., Rosenthal P., Schwarz K.B., McMahon B.J., Foundation H.B. Treatment of children with chronic hepatitis B virus infection in the United States: patient selection and therapeutic options. Hepatology 2010, 52:2192-2205.
19. Kang H., Yu J., Jung G. Phosphorylation of hepatitis B virus core C-terminally truncated protein (Cp149) by PKC increases capsid assembly and stability. Biochem. J. 2008, 416:47-54.
20. Kaur S., Parmar S., Smith J., Katsoulidis E., Li Y., Sassano A., Majchrzak B., Uddin S., Tallman M.S., Fish E.N., Platanias L.C. Role of protein kinase C-delta (PKC-delta) in the generation of the effects of IFN-alpha in chronic myelogenous leukemia cells. Exp. Hematol. 2005, 33:550-557.
21. Kikkawa U., Kishimoto A., Nishizuka Y. The protein kinase C family: heterogeneity and its implications. Annu. Rev. Biochem. 1989, 58:31-44.
22. Laras A., Koskinas J., Hadziyannis S.J. In vivo suppression of precore mRNA synthesis is associated with mutations in the hepatitis B virus core promoter. Virology 2002, 295:86-96.
23. Li M., Xie Y., Wu X., Kong Y., Wang Y. HNF3 binds and activates the second enhancer, ENII, of hepatitis B virus. Virology 1995, 214:371-378.
24. Li M., Xie Y.H., Kong Y.Y., Wu X., Zhu L., Wang Y. Cloning and characterization of a novel human hepatocyte transcription factor, hB1F, which binds and activates enhancer II of hepatitis B virus. J. Biol. Chem. 1998, 273:29022-29031.
25. Liaw Y.F. HBeAg seroconversion as an important end point in the treatment of chronic hepatitis B. Hepatol. Int 2009.
26. Lok A.S., McMahon B.J. Chronic hepatitis B: update 2009. Hepatology 2009, 50:661-662.
27. López-Cabrera M., Letovsky J., Hu K.Q., Siddiqui A. Multiple liver-specific factors bind to the hepatitis B virus core/pregenomic promoter: trans-activation and repression by CCAAT/enhancer binding protein. Proc. Nat. Acad. Sci. U.S.A. 1990, 87:5069-5073.
28. López-Cabrera M., Letovsky J., Hu K.Q., Siddiqui A. Transcriptional factor C/EBP binds to and transactivates the enhancer element II of the hepatitis B virus. Virology 1991, 183:825-829.
29. Mahoney C.W., Shuman J., McKnight S.L., Chen H.C., Huang K.P. Phosphorylation of CCAAT-enhancer binding protein by protein kinase C attenuates site-selective DNA binding. J. Biol. Chem. 1992, 267:19396-19403.
30. Marte B.M., Meyer T., Stabel S., Standke G.J., Jaken S., Fabbro D., Hynes N.E. Protein kinase C and mammary cell differentiation: involvement of protein kinase C alpha in the induction of beta-casein expression. Cell Growth Differ. 1994, 5:239-247.
31. Martiny-Baron G., Kazanietz M.G., Mischak H., Blumberg P.M., Kochs G., Hug H., Marmé D., Schächtele C. Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. J. Biol. Chem. 1993, 268:9194-9197.
32. Moolla N., Kew M., Arbuthnot P. Regulatory elements of hepatitis B virus transcription. J. Viral. Hepat. 2002, 9:323-331.
33. Nakao K., Nakata K., Yamashita M., Tamada Y., Hamasaki K., Ishikawa H., Kato Y., Eguchi K., Ishii N. p48 (ISGF-3gamma) is involved in interferon-alpha-induced suppression of hepatitis B virus enhancer-1 activity. J. Biol. Chem. 1999, 274:28075-28078.
34. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 1988, 334:661-665.
35. Pal S., Claffey K.P., Cohen H.T., Mukhopadhyay D. Activation of Sp1-mediated vascular permeability factor/vascular endothelial growth factor transcription requires specific interaction with protein kinase C zeta. J. Biol. Chem. 1998, 273:26277-26280.
36. Pfeffer L.M., Eisenkraft B.L., Reich N.C., Improta T., Baxter G., Daniel-Issakani S., Strulovici B. Transmembrane signaling by interferon alpha involves diacylglycerol production and activation of the epsilon isoform of protein kinase C in Daudi cells. Proc. Nat. Acad. Sci. U.S.A. 1991, 88:7988-7992.
37. Pfeffer L.M., Strulovici B., Saltiel A.R. Interferon-alpha selectively activates the beta isoform of protein kinase C through phosphatidylcholine hydrolysis. Proc. Nat. Acad. Sci. U.S.A. 1990, 87:6537-6541.
38. Rafty L.A., Khachigian L.M. Sp1 phosphorylation regulates inducible expression of platelet-derived growth factor B-chain gene via atypical protein kinase C-zeta. Nucleic Acids Res. 2001, 29:1027-1033.
39. Raney A.K., Johnson J.L., Palmer C.N., McLachlan A. Members of the nuclear receptor superfamily regulate transcription from the hepatitis B virus nucleocapsid promoter. J. Virol. 1997, 71:1058-1071.
40. Rang A., Heise T., Will H. Lack of a role of the interferon-stimulated response element-like region in interferon alpha -induced suppression of Hepatitis B virus in vitro. J. Biol. Chem. 2001, 276:3531-3535.
41. Romero R., Lavine J.E. Cytokine inhibition of the hepatitis B virus core promoter. Hepatology 1996, 23:17-23.
42. Schulte-Frohlinde E., Seidler B., Burkard I., Freilinger T., Lersch C., Erfle V., Foster G.R., Classen M. Different activities of type I interferons on hepatitis B virus core promoter regulated transcription. Cytokine 2002, 17:214-220.
43. Srivastava K.K., Batra S., Sassano A., Li Y., Majchrzak B., Kiyokawa H., Altman A., Fish E.N., Platanias L.C. Engagement of protein kinase C-theta in interferon signaling in T-cells. J. Biol. Chem. 2004, 279:29911-29920.
44. Su H., Yee J.K. Regulation of hepatitis B virus gene expression by its two enhancers. Proc. Nat. Acad. Sci. U.S.A. 1992, 89:2708-2712.
45. Sureau C., Romet-Lemonne J.L., Mullins J.I., Essex M. Production of hepatitis B virus by a differentiated human hepatoma cell line after transfection with cloned circular HBV DNA. Cell 1986, 47:37-47.
46. Tur-Kaspa R., Teicher L., Laub O., Itin A., Dagan D., Bloom B.R., Shafritz D.A. Alpha interferon suppresses hepatitis B virus enhancer activity and reduces viral gene transcription. J. Virol. 1990, 64:1821-1824.
47. Uddin S., Sassano A., Deb D.K., Verma A., Majchrzak B., Rahman A., Malik A.B., Fish E.N., Platanias L.C. Protein kinase C-delta (PKC-delta) is activated by type I interferons and mediates phosphorylation of Stat1 on serine 727. J. Biol. Chem. 2002, 277:14408-14416.
48. Uddin S., Yenush L., Sun X.J., Sweet M.E., White M.F., Platanias L.C. Interferon-alpha engages the insulin receptor substrate-1 to associate with the phosphatidylinositol 3'-kinase. J. Biol. Chem. 1995, 270:15938-15941.
49. Vannice J.L., Levinson A.D. Properties of the human hepatitis B virus enhancer: position effects and cell-type nonspecificity. J. Virol. 1988, 62:1305-1313.
50. von Hahn, T., Schulze, A., Chicano Wust, I., Heidrich, B., Becker, T., Steinmann, E., Helfritz, F.A., Rohrmann, K., Urban, S., Manns, M.P., Pietschmann, T., Ciesek, S., 2011. The novel immunosuppressive protein kinase C inhibitor sotrastaurin has no pro-viral effects on the replication cycle of hepatitis B or C virus. PLoS One 6, e24142.
51. Wang W.X., Li M., Wu X., Wang Y., Li Z.P. HNF1 is critical for the liver-specific function of HBV enhancer II. Res. Virol. 1998, 149:99-108.
52. Wang Y., Chen P., Wu X., Sun A.L., Wang H., Zhu Y.A., Li Z.P. A new enhancer element, ENII, identified in the X gene of hepatitis B virus. J. Virol. 1990, 64:3977-3981.
53. Yee J.K. A liver-specific enhancer in the core promoter region of human hepatitis B virus. Science 1989, 246:658-661.
54. Yuh C.H., Ting L.P. The genome of hepatitis B virus contains a second enhancer: cooperation of two elements within this enhancer is required for its function. J. Virol. 1990, 64:4281-4287.
55. Yuh C.H., Ting L.P. C/EBP-like proteins binding to the functional box-alpha and box-beta of the second enhancer of hepatitis B virus. Mol. Cell. Biol. 1991, 11:5044-5052.