Hepatocystin/80K-H inhibits replication of hepatitis B virus through interaction with HBx protein in hepatoma cell

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 10, 2013, Pages 1569-1581

  Shin, Gu Choul ^a   Ahn, Sung Hyun ^a   Choi, Hyo Sun ^a   Lim, Keo Heun ^a   Choi, Do Young ^b   Kim, Kwang Pyo ^b   Kim, Kyun Hwan ^a,b  

^a Konkuk University School of Medicine   (South Korea)

^b Konkuk University   (South Korea)

Author keywords

HBx; Hepatitis B virus replication; Hepatocystin 80K H; Molecular chaperon; Protein interaction

Indexed keywords

AMINO ACID; HEPATITIS B VIRUS X PROTEIN; HEPATOCYSTIN; PROTEASOME; PROTEASOME INHIBITOR; PROTEIN KINASE C; SOMATOMEDIN B RECEPTOR; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA REPLICATION; HEPATITIS B VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PURIFICATION; VIRUS REPLICATION; WESTERN BLOTTING;

HBX; HEPATITIS B VIRUS REPLICATION; HEPATOCYSTIN/80K-H; MOLECULAR CHAPERON; PROTEIN INTERACTION;

AMINO ACID SEQUENCE; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; GLUCOSIDASES; HEPATITIS B VIRUS; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER NEOPLASMS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; TRANS-ACTIVATORS; VIRUS REPLICATION;

HEPATITIS B VIRUS;

EID: 84879566216     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.04.026     Document Type: Article

References (59)

1. Torres H.A., Davila M. Reactivation of hepatitis B virus and hepatitis C virus in patients with cancer. Nat. Rev. Clin. Oncol. 2012, 9:156-166.
2. Lai C.L., Ratziu V., Yuen M.F., Poynard T. Viral hepatitis B. Lancet 2003, 362:2089-2094.
3. Centers for Disease Control, Prevention (CDC) Surveillance for chronic hepatitis B virus infection-New York City, June 2008-November 2009. MMWR Morb. Mortal. Wkly Rep 2012, 61:6-9.
4. Lucifora J., Arzberger S., Durantel D., Belloni L., Strubin M., Levrero M., Zoulim F., Hantz O., Protzer U. Hepatitis B virus X protein is essential to initiate and maintain virus replication after infection. J. Hepatol. 2011, 55:996-1003.
5. Keasler V.V., Hodgson A.J., Madden C.R., Slagle B.L. Enhancement of hepatitis B virus replication by the regulatory X protein in vitro and in vivo. J. Virol. 2007, 81:2656-2662.
6. Kremsdorf D., Soussan P., Paterlini-Brechot P., Brechot C. Hepatitis B virus-related hepatocellular carcinoma: paradigms for viral-related human carcinogenesis. Oncogene 2006, 25:3823-3833.
7. Hong A., Han D.D., Wright C.J., Burch T., Piper J., Osiowy C., Gao C., Chiang S., Magill T., Dick K., Booth T.F., Li X., He R. The interaction between hepatitis B virus X protein and AIB1 oncogene is required for the activation of NFκB signal transduction. Biochem. Biophys. Res. Commun. 2012, 423:6-12.
8. Kim J.Y., Song E.H., Lee H.J., Oh Y.K., Choi K.H., Yu D.Y., Park S.I., Seong J.K., Kim W.H. HBx-induced hepatic steatosis and apoptosis are regulated by TNFR1- and NF-kappaB-dependent pathways. J. Mol. Biol. 2010, 397:917-931.
9. Lee Y.H., Yun Y. HBx protein of hepatitis B virus activates Jak1-STAT signaling. J. Biol. Chem. 1998, 273:25510-25515.
10. Tanaka Y., Kanai F., Ichimura T., Tateishi K., Asaoka Y., Guleng B., Jazag A., Ohta M., Imamura J., Ikenoue T., Ijichi H., Kawabe T., Isobe T., Omata M. The hepatitis B virus X protein enhances AP-1 activation through interaction with Jab1. Oncogene 2006, 25:633-642.
11. Cong Y.S., Yao Y.L., Yang W.M., Kuzhandaivelu N., Seto E. The hepatitis B virus X-associated protein, XAP3, is a protein kinase C-binding protein. J. Biol. Chem. 1997, 272:16482-16489.
12. Cheong J.H., Yi M., Lin Y., Murakami S. Human RPB5, a subunit shared by eukaryotic nuclear RNA polymerases, binds human hepatitis B virus X protein and may play a role in X transactivation. EMBO J. 1995, 14:143-150.
13. Lin Y., Nomura T., Cheong J., Dorjsuren D., Iida K., Murakami S. Hepatitis B virus X protein is a transcriptional modulator that communicates with transcription factor IIB and the RNA polymerase II subunit 5. J. Biol. Chem. 1997, 272:7132-7139.
14. Qadri I., Maguire H.F., Siddiqui A. Hepatitis B virus transactivator protein X interacts with the TATA-binding protein. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:1003-1007.
15. Maguire H.F., Hoeffler J.P., Siddiqui A. HBV X protein alters the DNA binding specificity of CREB and ATF-2 by protein-protein interactions. Science 1991, 252:842-844.
16. Kim K.H., Seong B.L. Pro-apoptotic function of HBV X protein is mediated by interaction with c-FLIP and enhancement of death-inducing signal. EMBO J. 2003, 22:2104-2116.
17. Sohn S.Y., Kim S.B., Kim J., Ahn B.Y. Negative regulation of hepatitis B virus replication by cellular Hsp40/DnaJ proteins through destabilization of viral core and X proteins. J. Gen. Virol. 2006, 87:1883-1891.
18. Tanaka Y., Kanai F., Kawakami T., Tateishi K., Ijichi H., Kawabe T., Arakawa Y., Kawakami T., Nishimura T., Shirakata Y., Koike K., Omata M. Interaction of the hepatitis B virus X protein (HBx) with heat shock protein 60 enhances HBx-mediated apoptosis. Biochem. Biophys. Res. Commun. 2004, 318:461-469.
19. Hirai M., Shimizu N. Purification of two distinct proteins of approximate Mr 80,000 from human epithelial cells and identification as proper substrates for protein kinase C. Biochem. J. 1990, 270:583-589.
20. Trombetta E.S., Simons J.F., Helenius A. Endoplasmic reticulum glucosidase II is composed of a catalytic subunit, conserved from yeast to mammals, and a tightly bound noncatalytic HDEL-containing subunit. J. Biol. Chem. 1996, 271:27509-27516.
21. Kanai M., Göke M., Tsunekawa S., Podolsky D.K. Signal transduction pathway of human fibroblast growth factor receptor 3. Identification of a novel 66-kDa phosphoprotein. J. Biol. Chem. 1997, 272:6621-6628.
22. Hodgkinson C.P., Mander A., Sale G.J. Identification of 80K-H as a protein involved in GLUT4 vesicle trafficking. Biochem. J. 2005, 388:785-793.
23. 2+ sensor regulating the activity of the epithelial Ca2+ channel transient receptor potential cation channel V5 (TRPV5). J. Biol. Chem. 2004, 279:26351-26357.
24. Gao H., Wang Y., Wegierski T., Skouloudaki K., Pütz M., Fu X., Engel C., Boehlke C., Peng H., Kuehn E.W., Kim E., Kramer-Zucker A., Walz G. PRKCSH/80K-H, the protein mutated in polycystic liver disease, protects polycystin-2/TRPP2 against HERP-mediated degradation. Hum. Mol. Genet. 2010, 19:16-24.
25. Kawaai K., Hisatsune C., Kuroda Y., Mizutani A., Tashiro T., Mikoshiba K. 80K-H interacts with inositol 1,4,5-trisphosphate (IP3) receptors and regulates IP3-induced calcium release activity. J. Biol. Chem. 2009, 284:372-380.
26. Drenth J.P., te Morsche R.H., Smink R., Bonifacino J.S., Jansen J.B. Germline mutations in PRKCSH are associated with autosomal dominant polycystic liver disease. Nat. Genet. 2003, 33:345-347.
27. Ma Y., Yu J., Chan H.L., Chen Y.C., Wang H., Chen Y., Chan C.Y., Go M.Y., Tsai S.N., Ngai S.M., To K.F., Tong J.H., He Q.Y., Sung J.J., Kung H.F., Cheng C.H., He M.L. Glucose-regulated protein 78 is an intracellular antiviral factor against hepatitis B virus. Mol. Cell. Proteomics 2009, 8:2582-2594.
28. Tong S.W., Yang Y.X., Hu H.D., An X., Ye F., Ren H., Li S.L., Zhang D.Z. HSPB1 is an intracellular antiviral factor against hepatitis B virus. J. Cell. Biochem. 2013, 114:162-173.
29. Lim K.H., Kim K.H., Choi S.I., Park E.S., Park S.H., Ryu K., Park Y.K., Kwon S.Y., Yang S.I., Lee H.C., Sung I.K., Seong B.L. RPS3a over-expressed in HBV-associated hepatocellular carcinoma enhances the HBx-induced NF-κB signaling via its novel chaperoning function. PLoS One 2011, 6:e22258.
30. Cha M.Y., Ryu D.K., Jung H.S., Chang H.E., Ryu W.S. Stimulation of hepatitis B virus genome replication by HBx is linked to both nuclear and cytoplasmic HBx expression. J. Gen. Virol. 2009, 90:978-986.
31. Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 2006, 1:2856-2860.
32. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74:5383-5392.
33. Khan N., Guarnieri M., Ahn S.H., Li J., Zhou Y., Bang G., Kim K.H., Wands J.R., Tong S. Modulation of hepatitis B virus secretion by naturally occurring mutations in the S gene. J. Virol. 2004, 78:3262-3270.
34. Zhang S.M., Sun D.C., Lou S., Bo X.C., Lu Z., Qian X.H., Wang S.Q. HBx protein of hepatitis B virus (HBV) can form complex with mitochondrial HSP60 and HSP70. Arch. Virol. 2005, 150:1579-1590.
35. Gray P.C., Vale W. Cripto/GRP78 modulation of the TGF-β pathway in development and oncogenesis. FEBS Lett. 2012, 586:1836-1845.
36. Henkler F., Hoare J., Waseem N., Goldin R.D., McGarvey M.J., Koshy R., King I.A. Intracellular localization of the hepatitis B virus HBx protein. J. Gen. Virol. 2001, 82:871-882.
37. Yang Y., Kitagaki J., Dai R.M., Tsai Y.C., Lorick K.L., Ludwig R.L., Pierre S.A., Jensen J.P., Davydov I.V., Oberoi P., Li C.C., Kenten J.H., Beutler J.A., Vousden K.H., Weissman A.M. Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics. Cancer Res. 2007, 67:9472-9481.
38. Blum H.E., Zhang Z.S., Galun E., von Weizsäcker F., Garner B., Liang T.J., Wands J.R. Hepatitis B virus X protein is not central to the viral life cycle in vitro. J. Virol. 1992, 66:1223-1227.
39. Park S.G., Min J.Y., Chung C., Hsieh A., Jung G. Tumor suppressor protein p53 induces degradation of the oncogenic protein HBx. Cancer Lett. 2009, 282:229-237.
40. Kido T., Ou J.H., Lau Y.F. The X-linked tumor suppressor TSPX interacts and promotes degradation of the hepatitis B viral protein HBx via the proteasome pathway. PLoS One 2011, 6:e22979.
41. Xian L., Zhao J., Wang J., Fang Z., Peng B., Wang W., Ji X., Yu L. p53 Promotes proteasome-dependent degradation of oncogenic protein HBx by transcription of MDM2. Mol. Biol. Rep. 2010, 37:2935-2940.
42. Ling M.T., Chiu Y.T., Lee T.K., Leung S.C., Fung M.K., Wang X., Wong K.F., Wong Y.C. Id-1 induces proteasome-dependent degradation of the HBX protein. J. Mol. Biol. 2008, 382:34-43.
43. Hu Z., Zhang Z., Doo E., Coux O., Goldberg A.L., Liang T.J. Hepatitis B virus X protein is both a substrate and a potential inhibitor of the proteasome complex. J. Virol. 1999, 73:7231-7240.
44. Huang J., Kwong J., Sun E.C., Liang T.J. Proteasome complex as a potential cellular target of hepatitis B virus X protein. J. Virol. 1996, 70:5582-5591.
45. Zhang Z., Torii N., Furusaka A., Malayaman N., Hu Z., Liang T.J. Structural and functional characterization of interaction between hepatitis B virus X protein and the proteasome complex. J. Biol. Chem. 2000, 275:15157-15165.
46. Lizzano R.A., Yang B., Clippinger A.J., Bouchard M.J. The C-terminal region of the hepatitis B virus X protein is essential for its stability and function. Virus Res. 2011, 155:231-239.
47. Luo N., Cai Y., Zhang J., Tang W., Slagle B.L., Wu X., He S. The C-terminal region of the hepatitis B virus X protein is required for its stimulation of HBV replication in primary mouse hepatocytes. Virus Res. 2012, 165:170-178.
48. Melegari M., Scaglioni P.P., Wands J.R. Cloning and characterization of a novel hepatitis B virus x binding protein that inhibits viral replication. J. Virol. 1998, 72:1737-1743.
49. Zhao Z., Hong W., Zeng Z., Wu Y., Hu K., Tian X., Li W., Cao Z. Mucroporin-M1 inhibits hepatitis B virus replication by activating the mitogen-activated protein kinase (MAPK) pathway and down-regulating HNF4α in vitro and in vivo. J. Biol. Chem. 2012, 287:30181-30190.
50. Han Q., Zhang C., Zhang J., Tian Z. Involvement of activation of PKR in HBx-siRNA-mediated innate immune effects on HBV inhibition. PLoS One 2011, 6:e27931.
51. Han Q., Zhang C., Zhang J., Tian Z. Reversal of hepatitis B virus-induced immune tolerance by an immunostimulatory 3p-HBx-siRNAs in a retinoic acid inducible gene I-dependent manner. Hepatology 2011, 54:1179-1189.
52. Reddi H., Kumar R., Jain S.K., Kumar V. A carboxy-terminal region of the hepatitis B virus X protein promotes DNA interaction of CREB and mimics the native protein for transactivation function. Virus Genes. 2003, 26:227-238.
53. Ma N.F., Lau S.H., Hu L., Xie D., Wu J., Yang J., Wang Y., Wu M.C., Fung J., Bai X., Tzang C.H., Fu L., Yang M., Su Y.A., Guan X.Y. COOH-terminal truncated HBV X protein plays key role in hepatocarcinogenesis. Clin. Cancer Res. 2008, 14:5061-5068.
54. Tu H., Bonura C., Giannini C., Mouly H., Soussan P., Kew M., Paterlini-Bréchot P., Bréchot C., Kremsdorf D. Biological impact of natural COOH-terminal deletions of hepatitis B virus X protein in hepatocellular carcinoma tissues. Cancer Res. 2001, 61:7803-7810.
55. Forough R., Lindner L., Partridge C., Jones B., Guy G., Clark G. Elevated 80K-H protein in breast cancer: a role for FGF-1 stimulation of 80K-H. Int. J. Biol. Markers 2003, 18:89-98.
56. Shen J., Behrens C., Wistuba I.I., Feng L., Lee J.J., Hong W.K., Lotan R. Identification and validation of differences in protein levels in normal, premalignant, and malignant lung cells and tissues using high-throughput Western Array and immunohistochemistry. Cancer Res. 2006, 66:11194-11206.
57. Seimiya M., Tomonaga T., Matsushita K., Sunaga M., Oh-Ishi M., Kodera Y., Maeda T., Takano S., Togawa A., Yoshitomi H., Otsuka M., Yamamoto M., Nakano M., Miyazaki M., Nomura F. Identification of novel immunohistochemical tumor markers for primary hepatocellular carcinoma; clathrin heavy chain and formiminotransferase cyclodeaminase. Hepatology 2008, 48:519-530.
58. Höhfeld J., Cyr D.M., Patterson C. From the cradle to the grave: molecular chaperones that may choose between folding and degradation. EMBO Rep. 2001, 2:885-890.
59. Park E.S., Park Y.K., Shin C., Park S.H., Ahn S.H., Kim D.H., Kim K.M., Kwon S.Y., Kim K.P., Yang S.I., Seong B.L., Kim K.H. Hepatitis B virus inhibits liver regeneration via epigenetic regulation of urokinase-type plasminogen activator. Hepatology 2013, 10.1002/hep.26379.