Identification and characterization of a novel bipartite nuclear localization signal in the hepatitis B virus polymerase

World Journal of Gastroenterology

Volumn 19, Issue 44, 2013, Pages 8000-8010

  Lupberger, Joachim ^a,b   Schaedler, Stephanie ^a   Peiran, Alexander ^c   Hildt, Eberhard ^a,d  

^a UNIVERSITY OF FREIBURG   (Germany)

^b INSERM   (France)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d PAUL EHRLICH INSTITUT   (Germany)

Author keywords

Casein Kinase II; Hepatitis B virus; Nuclear localization signal; Replication; Trafficking

Indexed keywords

CASEIN KINASE II; COMPLEMENTARY DNA; HEPATITIS B VIRUS POLYMERASE; KARYOPHERIN; UNCLASSIFIED DRUG; VIRUS ENZYME;

ARTICLE; CELL CULTURE; CELL FRACTIONATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENDOGENOUS POLYMERASE REACTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE AMPLIFICATION; GENOME ANALYSIS; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; LIFE CYCLE ASSESSMENT; NUCLEAR LOCALIZATION SIGNAL; POLYMERASE CHAIN REACTION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; VIRUS CHARACTERIZATION; VIRUS IDENTIFICATION;

CASEIN KINASE II; HEPATITIS B VIRUS; NUCLEAR LOCALIZATION SIGNAL; REPLICATION; TRAFFICKING;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; AMINO ACID SEQUENCE; ANIMALS; CASEIN KINASE II; CELL NUCLEUS; CONSERVED SEQUENCE; GENE PRODUCTS, POL; HEP G2 CELLS; HEPATITIS B VIRUS; HEPATOCYTES; HUMANS; MUTATION; NUCLEAR LOCALIZATION SIGNALS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TIME FACTORS; TUPAIA; VIRUS REPLICATION;

EID: 84888625030     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v19.i44.8000     Document Type: Article

References (56)

1. Buendia MA. Hepatitis B viruses and cancerogenesis. Biomed Pharmacother 1998; 52: 34-43. [PMID: 9755793 DOI: 10.1016/ S0753-3322(97)86239-7]
2. Lupberger J, Hildt E. Hepatitis B virus-induced oncogenesis. World J Gastroenterol 2007; 13: 74-81. [PMID: 17206756]
3. Prange AN, Bartsch M, Meiners J, Serek M, Winkelmann T. Interspecific somatic hybrids between Cyclamen persicum and C. coum, two sexually incompatible species. Plant Cell Rep 2012; 31: 723-735. [PMID: 22108718 DOI: 10.1007/s00299-011-1190-z]
4. Rehermann B. Pathogenesis of chronic viral hepatitis: differential roles of T cells and NK cells. Nat Med 2013; 19: 859-868. [PMID: 23836236 DOI: 10.1038/nm.3251]
5. Tan YJ. Hepatitis B virus infection and the risk of hepatocellular carcinoma. World J Gastroenterol 2011; 17: 4853-4857. [PMID: 22171125 DOI: 10.3748/wjg.v17.i44.4853]
6. Rivière L, Ducroux A, Buendia MA. The oncogenic role of hepatitis B virus. Recent Results Cancer Res 2014; 193: 59-74. [PMID: 24008293 DOI: 10.1007/978-3-642-38965-8_4]
7. Shin YC, Ko C, Ryu WS. Hydrophobic residues of terminal protein domain of hepatitis B virus polymerase contribute to distinct steps in viral genome replication. FEBS Lett 2011; 585: 3964-3968. [PMID: 22079666 DOI: 10.1016/ j.febslet.2011.11.003]
8. Wang YX, Xu X, Luo C, Ma ZM, Jiang HL, Ding JP, Wen YM. A putative new domain target for anti-hepatitis B virus: residues flanking hepatitis B virus reverse transcriptase residue 306 (rtP306). J Med Virol 2007; 79: 676-682. [PMID: 17457904 DOI: 10.1002/jmv.20835]
9. Beck J, Nassal M. A Tyr residue in the reverse transcriptase domain can mimic the protein-priming Tyr residue in the terminal protein domain of a hepadnavirus P protein. J Virol 2011; 85: 7742-7753. [PMID: 21593158 DOI: 10.1128/ JVI.00482-11]
10. Lin CG, Yang SJ, Hwang WL, Su TS, Lo SJ. Demonstration of the presence of protease-cutting site in the spacer of hepatitis B viral Pol protein. J Virol Methods 1995; 51: 61-73. [PMID: 7730438 DOI: 10.1016/0166-0934(94)00118-Z]
11. Köck J, Theilmann L, Galle P, Schlicht HJ. Hepatitis B virus nucleic acids associated with human peripheral blood mononuclear cells do not originate from replicating virus. Hepatology 1996; 23: 405-413. [PMID: 8617418]
12. Stoeckl L, Funk A, Kopitzki A, Brandenburg B, Oess S, Will H, Sirma H, Hildt E. Identification of a structural motif crucial for infectivity of hepatitis B viruses. Proc Natl Acad Sci USA 2006; 103: 6730-6734. [PMID: 16618937 DOI: 10.1073/ pnas.0509765103]
13. Brandenburg B, Stockl L, Gutzeit C, Roos M, Lupberger J, Schwartlander R, Gelderblom H, Sauer IM, Hofschneider PH, Hildt E. A novel system for efficient gene transfer into primary human hepatocytes via cell-permeable hepatitis B virus-like particle. Hepatology 2005; 42: 1300-1309. [PMID: 16317706 DOI: 10.1002/hep.20950]
14. Rabe B, Glebe D, Kann M. Lipid-mediated introduction of hepatitis B virus capsids into nonsusceptible cells allows highly efficient replication and facilitates the study of early infection events. J Virol 2006; 80: 5465-5473. [PMID: 16699026 DOI: 10.1128/JVI.02303-05]
15. Nassal M. Hepatitis B virus replication: novel roles for virus-host interactions. Intervirology 1999; 42: 100-116. [PMID: 10516465 DOI: 10.1159/000024970]
16. Rabe B, Vlachou A, Panté N, Helenius A, Kann M. Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc Natl Acad Sci USA 2003; 100: 9849-9854. [PMID: 12909718 DOI: 10.1073/pnas.1730940100]
17. Panté N, Kann M. Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol Biol Cell 2002; 13: 425-434. [PMID: 11854401 DOI: 10.1091/ mbc.01-06-0308]
18. Schädler S, Hildt E. HBV life cycle: entry and morphogenesis. Viruses 2009; 1: 185-209. [PMID: 21994545 DOI: 10.3390/ v1020185]
19. Kann M, Sodeik B, Vlachou A, Gerlich WH, Helenius A. Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex. J Cell Biol 1999; 145: 45-55. [PMID: 10189367 DOI: 10.1083/jcb.145.1.45]
20. Rabe B, Delaleau M, Bischof A, Foss M, Sominskaya I, Pumpens P, Cazenave C, Castroviejo M, Kann M. Nuclear entry of hepatitis B virus capsids involves disintegration to protein dimers followed by nuclear reassociation to capsids. PLoS Pathog 2009; 5: e1000563. [PMID: 19714236 DOI:10.1371/journal.ppat.1000563]
21. Schmitz A, Schwarz A, Foss M, Zhou L, Rabe B, Hoellenriegel J, Stoeber M, Panté N, Kann M. Nucleoporin 153 arrests the nuclear import of hepatitis B virus capsids in the nuclear basket. PLoS Pathog 2010; 6: e1000741. [PMID: 20126445 DOI:10.1371/journal.ppat.1000741]
22. Choi J, Chang JS, Song MS, Ahn BY, Park Y, Lim DS, Han YS. Association of hepatitis B virus polymerase with promyelocytic leukemia nuclear bodies mediated by the S100 family protein p11. Biochem Biophys Res Commun 2003; 305: 1049-1056. [PMID: 12767936 DOI: 10.1016/S0006-291X(03)00881-7]
23. Kann M, Bischof A, Gerlich WH. In vitro model for the nuclear transport of the hepadnavirus genome. J Virol 1997; 71: 1310-1316. [PMID: 8995655]
24. Yao E, Gong Y, Chen N, Tavis JE. The majority of duck hepatitis B virus reverse transcriptase in cells is nonencapsidated and is bound to a cytoplasmic structure. J Virol 2000; 74: 8648-8657. [PMID: 10954566 DOI: 10.1128/JVI.74.18.8648-8657.2000]
25. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 1982; 42: 3858-3863. [PMID: 6286115]
26. Sells MA, Chen ML, 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; 84: 1005-1009. [PMID: 3029758 DOI: 10.1073/pnas.84.4.1005]
27. Ladner SK, Otto MJ, Barker CS, Zaifert K, Wang GH, Guo JT, Seeger C, King RW. Inducible expression of human hepaa novel system for screening potential inhibitors of HBV replication. Antimicrob Agents Chemother 1997; 41: 1715-1720. [PMID: 9257747]
28. Hafner A, Brandenburg B, Hildt E. Reconstitution of gene expression from a regulatory-protein-deficient hepatitis B virus genome by cell-permeable HBx protein. EMBO Rep 2003; 4: 767-773. [PMID: 12872136 DOI: 10.1038/sj.embor.embor903]
29. Ploen D, Hafirassou ML, Himmelsbach K, Sauter D, Biniossek ML, Weiss TS, Baumert TF, Schuster C, Hildt E. TIP47 plays a crucial role in the life cycle of hepatitis C virus. J Hepatol 2013; 58: 1081-1088. [PMID: 23354285 DOI: 10.1016/ j.jhep.2013.01.022]
30. Lupberger J, Mund A, Kock J, Hildt E. Cultivation of HepG2.2.15 on Cytodex-3: higher yield of hepatitis B virus and less subviral particles compared to conventional culture methods. J Hepatol 2006; 45: 547-552. [PMID: 16879893 DOI:10.1016/j.jhep.2006.05.012]
31. Köck J, Nassal M, MacNelly S, Baumert TF, Blum HE, von Weizsäcker F. Efficient infection of primary tupaia hepatocytes with purified human and woolly monkey hepatitis B virus. J Virol 2001; 75: 5084-5089. [PMID: 11333889 DOI:10.1128/JVI.75.11.5084-5089.2001]
32. Funk A, Mhamdi M, Lin L, Will H, Sirma H. Itinerary of hepatitis B viruses: delineation of restriction points critical for infectious entry. J Virol 2004; 78: 8289-8300. [PMID: 15254201 DOI: 10.1128/JVI.78.15.8289-8300.2004]
33. Funk A, Mhamdi M, Hohenberg H, Will H, Sirma H. pH-independent entry and sequential endosomal sorting are major determinants of hepadnaviral infection in primary hepatocytes. Hepatology 2006; 44: 685-693. [PMID: 16941679 DOI: 10.1002/hep.21297]
34. Kozak M. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 1987; 15: 8125-8148. [PMID: 3313277 DOI: 10.1093/nar/15.20.8125]
35. Fisher CL, Pei GK. Modification of a PCR-based site-directed mutagenesis method. Biotechniques 1997; 23: 570-571+574. [PMID: 9343663]
36. Bleifuss E, Kammertoens T, Hutloff A, Quarcoo D, Dorner M, Straub P, Uckert W, Hildt E. The translocation motif of hepatitis B virus improves protein vaccination. Cell Mol Life Sci 2006; 63: 627-635. [PMID: 16482397 DOI: 10.1007/ s00018-005-5548-7]
37. Oess S, Hildt E. Novel cell permeable motif derived from the PreS2-domain of hepatitis-B virus surface antigens. Gene Ther 2000; 7: 750-758. [PMID: 10822301 DOI: 10.1038/sj.gt.3301154]
38. Stöckl L, Berting A, Malkowski B, Foerste R, Hofschneider PH, Hildt E. Integrity of c-Raf-1/MEK signal transduction cascade is essential for hepatitis B virus gene expression. Oncogene 2003; 22: 2604-2610. [PMID: 12730674 DOI: 10.1038/ sj.onc.1206320]
39. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. Current protocols of molecular biology. New York: John Wiley & Sons, 2004
40. Koschel M, Oed D, Gerelsaikhan T, Thomssen R, Bruss V. Hepatitis B virus core gene mutations which block nucleocapsid envelopment. J Virol 2000; 74: 1-7. [PMID: 10590084 DOI: 10.1128/JVI.74.1.1-7.2000]
41. Schaedler S, Krause J, Himmelsbach K, Carvajal-Yepes M, Lieder F, Klingel K, Nassal M, Weiss TS, Werner S, Hildt E. Hepatitis B virus induces expression of antioxidant response element-regulated genes by activation of Nrf2. J Biol Chem 2010; 285: 41074-41086. [PMID: 20956535 DOI: 10.1074/jbc. M110.145862]
42. Carvajal-Yepes M, Himmelsbach K, Schaedler S, Ploen D, Krause J, Ludwig L, Weiss T, Klingel K, Hildt E. Hepatitis C virus impairs the induction of cytoprotective Nrf2 target genes by delocalization of small Maf proteins. J Biol Chem 2011; 286: 8941-8951. [PMID: 21216956 DOI: 10.1074/jbc. M110.186684]
43. Nassal M. Hepatitis B viruses: reverse transcription a different way. Virus Res 2008; 134: 235-249. [PMID: 18339439 DOI:10.1016/j.virusres.2007.12.024]
44. Prange R. Host factors involved in hepatitis B virus maturation, assembly, and egress. Med Microbiol Immunol 2012; 201: 449-461. [PMID: 22965171 DOI: 10.1007/s00430-012-0267-9]
45. Wittkop L, Schwarz A, Cassany A, Grün-Bernhard S, Delaleau M, Rabe B, Cazenave C, Gerlich W, Glebe D, Kann M. Inhibition of protein kinase C phosphorylation of hepatitis B virus capsids inhibits virion formation and causes intracellular capsid accumulation. Cell Microbiol 2010; 12: 962-975. [PMID: 20109160]
46. Kantelhardt VC, Schwarz A, Wend U, Schüttler CG, Willems WR, Trimoulet P, Fleury H, Gerlich WH, Kann M. Reevaluation of anti-HBc non-reactive serum samples from patients with persistent hepatitis B infection by immune precipitation with labelled HBV core antigen. J Clin Virol 2009; 46: 124-128. [PMID: 19631583 DOI: 10.1016/j.jcv.2009.06.018]
47. Kann M, Schmitz A, Rabe B. Intracellular transport of hepatitis B virus. World J Gastroenterol 2007; 13: 39-47. [PMID: 17206753]
48. Guo H, Mao R, Block TM, Guo JT. Production and function of the cytoplasmic deproteinized relaxed circular DNA of hepadnaviruses. J Virol 2010; 84: 387-396. [PMID: 19864387 DOI: 10.1128/JVI.01921-09]
49. Stahl M, Beck J, Nassal M. Chaperones activate hepadnavirus reverse transcriptase by transiently exposing a C-proximal region in the terminal protein domain that contributes to epsilon RNA binding. J Virol 2007; 81: 13354-13364. [PMID: 17913810 DOI: 10.1128/JVI.01196-07]
50. Litchfield DW. Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem J 2003; 369: 1-15. [PMID: 12396231 DOI: 10.1042/BJ20021469]
51. Meggio F, Pinna LA. One-thousand-and-one substrates of protein kinase CK2? FASEB J 2003; 17: 349-368. [PMID: 12631575 DOI: 10.1096/fj.02-0473rev]
52. Jans DA, Hübner S. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol Rev 1996; 76: 651-685. [PMID: 8757785]
53. Jans DA, Jans P. Negative charge at the casein kinase II site flanking the nuclear localization signal of the SV40 large T-antigen is mechanistically important for enhanced nuclear import. Oncogene 1994; 9: 2961-2968. [PMID: 8084599]
54. Harreman MT, Kline TM, Milford HG, Harben MB, Hodel AE, Corbett AH. Regulation of nuclear import by phosphorylation adjacent to nuclear localization signals. J Biol Chem 2004; 279: 20613-20621. [PMID: 14998990 DOI: 10.1074/jbc. M401720200]
55. Howard EA, Zupan JR, Citovsky V, Zambryski PC. The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell 1992; 68: 109-118. [PMID: 1732061 DOI: 10.1016/0092-8674(92)90210-4]
56. Robbins J, Dilworth SM, Laskey RA, Dingwall C. Two inter-dependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 1991; 64: 615-623. [PMID: 1991323 DOI:10.1016/0092-8674(91)90245-T]