Inhibition of Hepatitis B virus replication by Phospholipid scramblase 1 in vitro and in vivo

Antiviral Research

Volumn 94, Issue 1, 2012, Pages 9-17

  Yang, Jing ^a   Zhu, Xiangqian ^a,b   Liu, Juan ^a   Ding, Xiaoran ^a   Han, Mingming ^a   Hu, Wei ^a   Wang, Xuejun ^a   Zhou, Zhe ^a   Wang, Shengqi ^a  

^a BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^b HENAN UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Antiviral activity; Hepatitis B virus (HBV); Interferon (IFN); Phospholipid scramblase 1 (PLSCR1)

Indexed keywords

ANTIVIRUS AGENT; HEPATITIS B CORE ANTIGEN; INTERFERON; MESSENGER RNA; PHOSPHOLIPID SCRAMBLASE 1; PLASMID DNA; SCRAMBLASE; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN DETECTION; ANTIVIRAL ACTIVITY; ARTICLE; CELL STRAIN HEPG2; CONTROLLED STUDY; HEPATITIS B; HEPATITIS B VIRUS; HYDRODYNAMICS BASED TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; LIVER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; VESICULAR STOMATITIS VIRUS; VIRUS EXPRESSION; VIRUS REPLICATION;

ANIMALS; DOWN-REGULATION; GENE EXPRESSION REGULATION, VIRAL; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; MALE; MICE; MICE, INBRED BALB C; PHOSPHOLIPID TRANSFER PROTEINS; RNA, VIRAL; VIRUS REPLICATION;

ENCEPHALOMYOCARDITIS VIRUS; HEPATITIS B VIRUS; MUS; RNA VIRUSES; VESICULAR STOMATITIS VIRUS;

EID: 84862795095     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2012.01.010     Document Type: Article

References (46)

1. Ben-Efraim I., Zhou Q., Wiedmer T., Gerace L., Sims P.J. Phospholipid scramblase 1 is imported into the nucleus by a receptor-mediated pathway and interacts with DNA. Biochemistry 2004, 43:3518-3526.
2. Bonvin M., Achermann F., Greeve I., Stroka D., Keogh A., Inderbitzin D., Candinas D., Sommer P., Wain-Hobson S., Vartanian J.P., Greeve J. Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 2006, 43:1364-1374.
3. Caselmann W.H., Meyer M., Scholz S., Hofschneider P.H., Koshy R. Type I interferons inhibit hepatitis B virus replication and induce hepatocellular gene expression in cultured liver cells. J. Infect. Dis. 1992, 166:966-971.
4. Chen M.H., Ben-Efraim I., Mitrousis G., Walker-Kopp N., Sims P.J., Cingolani G. Phospholipid scramblase 1 contains a nonclassical nuclear localization signal with unique binding site in importin alpha. J. Biol. Chem. 2005, 280:10599-10606.
5. Chou Y.C., Jeng K.S., Chen M.L., Liu H.H., Liu T.L., Chen Y.L., Liu Y.C., Hu C.P., Chang C. Evaluation of transcriptional efficiency of hepatitis B virus covalently closed circular DNA by reverse transcription-PCR combined with the restriction enzyme digestion method. J. Virol. 2005, 79:1813-1823.
6. 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. Natl. Acad. Sci. USA 1998, A95:15623-15628.
7. Dienstag J.L. Hepatitis B virus infection. N. Engl. J. Med. 2008, 359:1486-1500.
8. Dong B., Zhou Q., Zhao J., Zhou A., Harty R.N., Bose S., Banerjee A., Slee R., Guenther J., Williams B.R., Wiedmer T., Sims P.J., Silverman R.H. Phospholipid scramblase 1 potentiates the antiviral activity of interferon. J. Virol. 2004, 78:8983-8993.
9. Gao B., Duan Z., Xu W., Xiong S. Tripartite motif-containing 22 inhibits the activity of hepatitis B virus core promoter, which is dependent on nuclear-located RING domain. Hepatology 2009, 50:424-433.
10. Gordien E., Rosmorduc O., Peltekian C., Garreau F., Brechot C., Kremsdorf D. Inhibition of hepatitis B virus replication by the interferon-inducible MxA protein. J. Virol. 2001, 75:2684-2691.
11. Hayashi Y., Koike K. Interferon inhibits hepatitis B virus replication in a stable expression system of transfected viral DNA. J. Virol. 1989, 63:2936-2940.
12. Huang Y., Zhao Q., Zhou C.X., Gu Z.M., Li D., Xu H.Z., Wiedmer T., Sims P.J., Zhao K.W., Chen G.Q. Antileukemic roles of human phospholipid scramblase 1 gene, evidence from inducible PLSCR1-expressing leukemic cells. Oncogene 2006, 25:6618-6627.
13. Kuo Y.B., Chan C.C., Chang C.A., Fan C.W., Hung R.P., Hung Y.S., Chen K.T., Yu J.S., Chang Y.S., Chan E.C. Identification of phospholipid scramblase 1 as a biomarker and determination of its prognostic value for colorectal cancer. Mol. Med. 2011, 17:41-47.
14. Li J., Lin S., Chen Q., Peng L., Zhai J., Liu Y., Yuan Z. Inhibition of hepatitis B virus replication by MyD88 involves accelerated degradation of pregenomic RNA and nuclear retention of pre-S/S RNAs. J. Virol. 2010, 84:6387-6399.
15. Lin S., Wu M., Xu Y., Xiong W., Yi Z., Zhang X., Zhenghong Y. Inhibition of hepatitis B virus replication by MyD88 is mediated by nuclear factor-kappaB activation. Biochim. Biophys. Acta 2007, 1772:1150-1157.
16. Lu B., Sims P.J., Wiedmer T., Moser A.H., Shigenaga J.K., Grunfeld C., Feingold K.R. Expression of the phospholipid scramblase (PLSCR) gene family during the acute phase response. Biochim. Biophys. Acta 2007, 1771:1177-1185.
17. Merregaert J., Van Langen J., Hansen U., Ponsaerts P., El Ghalbzouri A., Steenackers E., Van Ostade X., Sercu S. Phospholipid scramblase 1 is secreted by a lipid raft-dependent pathway and interacts with the extracellular matrix protein 1 in the dermal epidermal junction zone of human skin. J. Biol. Chem. 2010, 285:37823-37837.
18. Nanjundan M., Sun J., Zhao J., Zhou Q., Sims P.J., Wiedmer T. Plasma membrane phospholipid scramblase 1 promotes EGF-dependent activation of c-Src through the epidermal growth factor receptor. J. Biol. Chem. 2003, 278:37413-37418.
19. Nguyen D.H., Hu J. Reverse transcriptase- and RNA packaging signal-dependent incorporation of APOBEC3G into hepatitis B virus nucleocapsids. J. Virol. 2008, 82:6852-6861.
20. Nguyen D.H., Gummuluru S., Hu J. Deamination-independent inhibition of hepatitis B virus reverse transcription by APOBEC3G. J. Virol. 2007, 81:4465-4472.
21. Papatheodoridis G.V., Manolakopoulos S., Dusheiko G., Archimandritis A.J. Therapeutic strategies in the management of patients with chronic hepatitis B virus infection. Lancet Infect. Dis. 2008, 8:167-178.
22. Pastorelli C., Veiga J., Charles N., Voignier E., Moussu H., Monteiro R.C., Benhamou M. IgE receptor type I-dependent tyrosine phosphorylation of phospholipid scramblase. J. Biol. Chem. 2001, 276:20407-20412.
23. Peltekian C., Gordien E., Garreau F., Meas-Yedid V., Soussan P., Willams V., Chaix M.L., Olivo-Marin J.C., Brechot C., Kremsdorf D. Human MxA protein participates to the interferon-related inhibition of hepatitis B virus replication in female transgenic mice. J. Hepatol. 2005, 43:965-972.
24. Pugh J.C., Yaginuma K., Koike K., Summers J. Duck hepatitis B virus (DHBV) particles produced by transient expression of DHBV DNA in a human hepatoma cell line are infectious in vitro. J. Virol. 1988, 62:3513-3516.
25. Py B., Basmaciogullari S., Bouchet J., Zarka M., Moura I.C., Benhamou M., Monteiro R.C., Hocini H., Madrid R., Benichou S. The phospholipid scramblases 1 and 4 are cellular receptors for the secretory leukocyte protease inhibitor and interact with CD4 at the plasma membrane. PLoS One 2009, 4:e5006.
26. Qin J., Zhai J., Hong R., Shan S., Kong Y., Wen Y., Wang Y., Liu J., Xie Y. Prospero-related homeobox protein (Prox1) inhibits hepatitis B virus replication through repressing multiple cis regulatory elements. J. Gen. Virol. 2009, 90:1246-1255.
27. Rang A., Gunther S., Will H. Effect of interferon alpha on hepatitis B virus replication and gene expression in transiently transfected human hepatoma cells. J. Hepatol. 1999, 31:791-799.
28. Romero R., Lavine J.E. Cytokine inhibition of the hepatitis B virus core promoter. Hepatology 1996, 23:17-23.
29. Rosler C., Kock J., Kann M., Malim M.H., Blum H.E., Baumert T.F., von Weizsacker F. APOBEC-mediated interference with hepadnavirus production. Hepatology 2005, 42:301-309.
30. Sahu S.K., Gummadi S.N., Manoj N., Aradhyam G.K. Phospholipid scramblases: an overview. Arch. Biochem. Biophys. 2007, 462:103-114.
31. Sells M.A., Chen M.L., Acs G. Production of hepatitis B virus particles in Hep G2 cells transfected with cloned hepatitis B virus DNA. Proc. Natl. Acad. Sci. USA 1987, A84:1005-1009.
32. Sells M.A., Zelent A.Z., Shvartsman M., Acs G. Replicative intermediates of hepatitis B virus in HepG2 cells that produce infectious virions. J. Virol. 1988, 62:2836-2844.
33. Silverman R.H., Halloum A., Zhou A., Dong B., Al-Zoghaibi F., Kushner D., Zhou Q., Zhao J., Wiedmer T., Sims P.J. Suppression of ovarian carcinoma cell growth in vivo by the interferon-inducible plasma membrane protein, phospholipid scramblase 1. Cancer Res. 2002, 62:397-402.
34. Sun J., Zhao J., Schwartz M.A., Wang J.Y., Wiedmer T., Sims P.J. C-Abl tyrosine kinase binds and phosphorylates phospholipid scramblase 1. J. Biol. Chem. 2001, 276:28984-28990.
35. Suzuki E., Amengual O., Atsumi T., Oku K., Hashimoto T., Kataoka H., Horita T., Yasuda S., Ieko M., Fukushima K., Koike T. Increased expression of phospholipid scramblase 1 in monocytes from patients with systemic lupus erythematosus. J. Rheumatol. 2010, 37:1639-1645.
36. Turelli P., Mangeat B., Jost S., Vianin S., Trono D. Inhibition of hepatitis B virus replication by APOBEC3G. Science 2004, 303:1829.
37. Uprichard S.L., Wieland S.F., Althage A., Chisari F.V. Transcriptional and posttranscriptional control of hepatitis B virus gene expression. Proc. Natl. Acad. Sci. USA 2003, A100:1310-1315.
38. Wieland S.F., Guidotti L.G., Chisari F.V. Intrahepatic induction of alpha/beta interferon eliminates viral RNA-containing capsids in hepatitis B virus transgenic mice. J. Virol. 2000, 74:4165-4173.
39. Wieland S.F., Eustaquio A., Whitten-Bauer C., Boyd B., Chisari F.V. Interferon prevents formation of replication-competent hepatitis B virus RNA-containing nucleocapsids. Proc. Natl. Acad. Sci. USA 2005, A102:9913-9917.
40. Xiong W., Wang X., Liu X., Xiang L., Zheng L., Yuan Z. Interferon-inducible MyD88 protein inhibits hepatitis B virus replication. Virology 2004, 319:306-314.
41. Yang P.L., Althage A., Chung J., Chisari F.V. Hydrodynamic injection of viral DNA: a mouse model of acute hepatitis B virus infection. Proc. Natl. Acad. Sci. USA 2002, A99:13825-13830.
42. Yokoyama A., Yamashita T., Shiozawa E., Nagasawa A., Okabe-Kado J., Nakamaki T., Tomoyasu S., Kimura F., Motoyoshi K., Honma Y., Kasukabe T. MmTRA1b/phospholipid scramblase 1 gene expression is a new prognostic factor for acute myelogenous leukemia. Leuk. Res. 2004, 28:149-157.
43. Zhao K.W., Li X., Zhao Q., Huang Y., Li D., Peng Z.G., Shen W.Z., Zhao J., Zhou Q., Chen Z., Sims P.J., Wiedmer T., Chen G.Q. Protein kinase Cdelta mediates retinoic acid and phorbol myristate acetate-induced phospholipid scramblase 1 gene expression: its role in leukemic cell differentiation. Blood 2004, 104:3731-3738.
44. Zhou Q., Zhao J., Al-Zoghaibi F., Zhou A., Wiedmer T., Silverman R.H., Sims P.J. Transcriptional control of the human plasma membrane phospholipid scramblase 1 gene is mediated by interferon-alpha. Blood 2000, 95:2593-2599.
45. Zhou Q., Zhao J., Wiedmer T., Sims P.J. Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1. Blood 2002, 99:4030-4038.
46. Zhou Q., Ben-Efraim I., Bigcas J.L., Junqueira D., Wiedmer T., Sims P.J. Phospholipid scramblase 1 binds to the promoter region of the inositol 1,4,5-triphosphate receptor type 1 gene to enhance its expression. J. Biol. Chem. 2005, 280:35062-35068.