Expression studies of the core+1 protein of the hepatitis C virus 1a in mammalian cells: The influence of the core protein and proteasomes on the intracellular levels of core+1

FEBS Journal

Volumn 274, Issue 16, 2007, Pages 4057-4074

  Vassilaki, Niki ^a   Boleti, Haralabia ^a   Mavromara, Penelope ^a  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

Author keywords

Core+1 ORF; Core+1 F protein; Core+1 S protein; Frameshift; Hepatitis C

Indexed keywords

CORE PROTEIN; PROTEASOME;

ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTERPHASE; MAMMAL CELL; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; VIRUS ISOLATION;

CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOBLOTTING; INTRACELLULAR FLUID; MICROSCOPY, FLUORESCENCE; PROTEASOME ENDOPEPTIDASE COMPLEX; RECOMBINANT FUSION PROTEINS; TRANSFECTION; VIRAL CORE PROTEINS;

HEPATITIS C VIRUS; HEPATITIS C VIRUS GENOTYPE 1; MAMMALIA;

EID: 34547795201     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05929.x     Document Type: Article

References (81)

1. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW Houghton M (1989) Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244, 359 362.
2. Di Bisceglie AM (2000) Natural history of hepatitis C: its impact on clinical management. Hepatology 31, 1014 1018.
3. Hoofnagle JH (2002) Course and outcome of hepatitis C. Hepatology 36, S21 S29.
4. Zoulim F, Chevallier M, Maynard M Trepo C (2003) Clinical consequences of hepatitis C virus infection. Rev Med Virol 13, 57 68.
5. Houghton M Abrignani S (2005) Prospects for a vaccine against the hepatitis C virus. Nature 436, 961 966.
6. Feld JJ Hoofnagle JH (2005) Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436, 967 972.
7. Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA Summers MD (1995) Virus Taxonomy. Sixth Report of the International Committee on Taxonomy of Viruses. Springer- Verlag, Vienna.
8. Reed KE Rice CM (2000) Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr Top Microbiol Immunol 242, 55 84.
9. Rice CM (2003) Hcv life cycle and targets for drug development. Hepatitis Annual Update, 123 142.
10. Penin F, Dubuisson J, Rey FA, Moradpour D Pawlotsky JM (2004) Structural biology of hepatitis C virus. Hepatology 39, 5 19.
11. Lindenbach BD Rice CM (2005) Unravelling hepatitis C virus replication from genome to function. Nature 436, 933 938.
12. Hellen CU Pestova TV (1999) Translation of hepatitis C virus RNA. J Viral Hepat 6, 79 87.
13. Rijnbrand RC Lemon SM (2000) Internal ribosome entry site-mediated translation in hepatitis C virus replication. Curr Top Microbiol Immunol 242, 85 116.
14. Walewski JL, Keller TR, Stump DD Branch AD (2001) Evidence for a new hepatitis C virus antigen encoded in an overlapping reading frame. RNA 7, 710 721.
15. Xu Z, Choi J, Yen TS, Lu W, Strohecker A, Govindarajan S, Chien D, Selby MJ Ou J (2001) Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J 20, 3840 3848.
16. Varaklioti A, Vassilaki N, Georgopoulou U Mavromara P (2002) Alternate translation occurs within the core coding region of the hepatitis C viral genome. J Biol Chem 277, 17713 17721.
17. Varaklioti R, Georgopoulou U, Vassilaki N Mavromara P (2000) Evidence for Alternate Translation within the Core Coding Region of the Hepatitis C Virus. 7th International Meeting on Hepatitis C Virus and Related Viruses. Molecular Virology and Pathogenesis, Gold Coast, Australia.
18. Branch AD, Walewski JL, Gutierrez JA, Fernandez EJ, Im GY, Dieterich DT, Schiano TD, Sigal SH, Schilsky ML Schwartz ME (2003) HCV alternate reading frame proteins (ARFPs) may be virulence factors that help the virus survive adverse conditions. Hepatology 38, 468A 469A.
19. Komurian-Pradel F, Rajoharison A, Berland JL, Khouri V, Perret M, Van Roosmalen M, Pol S, Negro F Paranhos-Baccala G (2004) Antigenic relevance of F protein in chronic hepatitis C virus infection. Hepatology 40, 900 909.
20. Bain C, Parroche P, Lavergne JP, Duverger B, Vieux C, Dubois V, Komurian-Pradel F, Trepo C, Gebuhrer L, Paranhos-Baccala G, Penin F Inchauspe G (2004) Memory T-cell-mediated immune responses specific to an alternative core protein in hepatitis C virus infection. J Virol 78, 10460 10469.
21. Vassilaki N Mavromara P (2003) Two alternative translation mechanisms are responsible for the expression of the HCV ARFP/F/core+1 coding open reading frame. J Biol Chem 278, 40503 40513.
22. Baril M Brakier-Gingras L (2005) Translation of the F protein of hepatitis C virus is initiated at a non-AUG codon in a +1 reading frame relative to the polyprotein. Nucleic Acids Res 33, 1474 1486.
23. Roussel J, Pillez A, Montpellier C, Duverlie G, Cahour A, Dubuisson J Wychowski C (2003) Characterization of the expression of the hepatitis C virus F protein. J Gen Virol 84, 1751 1759.
24. Choi J, Xu Z Ou JH (2003) Triple decoding of hepatitis C virus RNA by programmed translational frameshifting. Mol Cell Biol 23, 1489 1497.
25. Xu Z, Choi J, Lu W Ou JH (2003) Hepatitis C virus f protein is a short-lived protein associated with the endoplasmic reticulum. J Virol 77, 1578 1583.
26. Kozak M (1987) At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J Mol Biol 196, 947 950.
27. Scherrer K, Imaizumi-Scherrer MT, Reynaud CA Therwath A (1979) On pre-messenger RNA and transcriptions. A review. Mol Biol Rep 5, 5 28.
28. Flint SJ (1981) Splicing and the regulation of viral gene expression. Curr Top Microbiol Immunol 93, 47 79.
29. Boris-Lawrie K, Roberts TM Hull S (2001) Retroviral RNA elements integrate components of post-transcriptional gene expression. Life Sci 69, 2697 2709.
30. Zheng ZM Baker CC (2006) Papillomavirus genome structure, expression, and post-transcriptional regulation. Front Biosci 11, 2286 2302.
31. Goncalves MA de Vries AA (2006) Adenovirus: from foe to friend. Rev Med Virol 16, 167 186.
32. Hiscox JA (2003) The interaction of animal cytoplasmic RNA viruses with the nucleus to facilitate replication. Virus Res 95, 13 22.
33. Gorlich D Kutay U (1999) Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15, 607 660.
34. Nachury MV Weis K (1999) The direction of transport through the nuclear pore can be inverted. Proc Natl Acad Sci USA 96, 9622 9627.
35. Lyman SK, Guan T, Bednenko J, Wodrich H Gerace L (2002) Influence of cargo size on Ran and energy requirements for nuclear protein import. J Cell Biol 159, 55 67.
36. Bordier C (1981) Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 256, 1604 1607.
37. Branch AD, Stump DD, Gutierrez JA, Eng F Walewski JL (2005) The hepatitis C virus alternate reading frame (ARF) and its family of novel products: the alternate reading frame protein/F-protein, the double-frameshift protein, and others. Semin Liver Dis 25, 105 117.
38. Guruprasad K, Reddy BV Pandit MW (1990) Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Eng 4, 155 161.
39. Hagglund R Roizman B (2004) Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J Virol 78, 2169 2178.
40. Huang J, Huang Q, Zhou X, Shen MM, Yen A, Yu SX, Dong G, Qu K, Huang P, Anderson EM et al. (2004) The poxvirus p28 virulence factor is an E3 ubiquitin ligase. J Biol Chem 279, 54110 54116.
41. Mansouri M, Bartee E, Gouveia K, Hovey Nerenberg BT, Barrett J, Thomas L, Thomas G, McFadden G Fruh K (2003) The PHD/LAP-domain protein M153R of myxomavirus is a ubiquitin ligase that induces the rapid internalization and lysosomal destruction of CD4. J Virol 77, 1427 1440.
42. Coadou G, Gharbi-Benarous J, Megy S, Bertho G, Evrard-Todeschi N, Segeral E, Benarous R Girault JP (2003) NMR studies of the phosphorylation motif of the HIV-1 protein Vpu bound to the F-box protein beta-TrCP. Biochemistry 42, 14741 14751.
43. Kehn K, Fuente Cde L, Strouss K, Berro R, Jiang H, Brady J, Mahieux R, Pumfery A, Bottazzi ME Kashanchi F (2005) The HTLV-I Tax oncoprotein targets the retinoblastoma protein for proteasomal degradation. Oncogene 24, 525 540.
44. Thomas M, Pim D Banks L (1999) The role of the E6-p53 interaction in the molecular pathogenesis of HPV. Oncogene 18, 7690 7700.
45. Eom CY, Heo WD, Craske ML, Meyer T Lehman IR (2004) The neural F-box protein NFB42 mediates the nuclear export of the herpes simplex virus type 1 replication initiator protein (UL9 protein) after viral infection. Proc Natl Acad Sci USA 101, 4036 4040.
46. Twu JS Schloemer RH (1987) Transcriptional trans-activating function of hepatitis B virus. J Virol 61, 3448 3453.
47. Spandau DF Lee CH (1988) Trans-activation of viral enhancers by the hepatitis B virus X protein. J Virol 62, 427 434.
48. Yen TS (1996) Hepadnaviral X protein: review of recent progress. J Biomed Sci 3, 20 30.
49. Choi BH, Park GT Rho HM (1999) Interaction of hepatitis B viral X protein and CCAAT/enhancer-binding protein alpha synergistically activates the hepatitis B viral enhancer II/pregenomic promoter. J Biol Chem 274, 2858 2865.
50. Kim JH, Kang S, Kim J Ahn BY (2003) Hepatitis B virus core protein stimulates the proteasome-mediated degradation of viral X protein. J Virol 77, 7166 7173.
51. Moriishi K, Okabayashi T, Nakai K, Moriya K, Koike K, Murata S, Chiba T, Tanaka K, Suzuki R, Suzuki T et al. (2003) Proteasome activator PA28gamma-dependent nuclear retention and degradation of hepatitis C virus core protein. J Virol 77, 10237 10249.
52. Rullier A, Trimoulet P, Urbaniak R, Winnock M, Zauli D, Ballardini G, Rosenbaum J, Balabaud C, Bioulac-Sage P Le Bail B (2001) Immunohistochemical detection of hcv in cirrhosis, dysplastic nodules, and hepatocellular carcinomas with parallel-tissue quantitative RT-PCR. Mod Pathol 14, 496 505.
53. Ruster B, Zeuzem S Roth WK (1996) Hepatitis C virus sequences encoding truncated core proteins detected in a hepatocellular carcinoma. Biochem Biophys Res Commun 219, 911 915.
54. Yeh CT, Lu SC, Chu CM Liaw YF (1997) Molecular cloning of a defective hepatitis C virus genome from the ascitic fluid of a patient with hepatocellular carcinoma. J Gen Virol 78, 2761 2770.
55. Yeh CT, Lo SY, Dai DI, Tang JH, Chu CM Liaw YF (2000) Amino acid substitutions in codons 9-11 of hepatitis C virus core protein lead to the synthesis of a short core protein product. J Gastroenterol Hepatol 15, 182 191.
56. Hayashi J, Furusyo N, Ariyama I, Sawayama Y, Etoh Y Kashiwagi S (2000) A relationship between the evolution of hepatitis C virus variants, liver damage, and hepatocellular carcinoma in patients with hepatitis C viremia. J Infect Dis 181, 1523 1527.
57. Ruster B, Zeuzem S, Krump-Konvalinkova V, Berg T, Jonas S, Severin K Roth WK (2001) Comparative sequence analysis of the core- and NS5-region of hepatitis C virus from tumor and adjacent non-tumor tissue. J Med Virol 63, 128 134.
58. Alam SS, Nakamura T, Naganuma A, Nozaki A, Nouso K, Shimomura H Kato N (2002) Hepatitis C virus quasispecies in cancerous and noncancerous hepatic lesions: the core protein-encoding region. Acta Med Okayama 56, 141 147.
59. Ogata S, Nagano-Fujii M, Ku Y, Yoon S Hotta H (2002) Comparative sequence analysis of the core protein and its frameshift product, the F protein, of hepatitis C virus subtype 1b strains obtained from patients with and without hepatocellular carcinoma. J Clin Microbiol 40, 3625 3630.
60. Miladi A, Lavergne J, Hezode C, Dhumeaux D, Penin F MPJ (2004) Prevalence of Anti-HCV F (Frameshift) Protein Antibodies in Patients with Various Forms of HCV Infection and the Putative Physiological Role of F Protein. 11th International Symposium on Hepatitis C Virus and Related Viruses, 3-7 October, Heidelberg, Germany.
61. Tusnady GE Simon I (1998) Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol 283, 489 506.
62. Tusnady GE Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849 850.
63. Egger D, Wolk B, Gosert R, Bianchi L, Blum HE, Moradpour D Bienz K (2002) Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 76, 5974 5984.
64. Mottola G, Cardinali G, Ceccacci A, Trozzi C, Bartholomew L, Torrisi MR, Pedrazzini E, Bonatti S Migliaccio G (2002) Hepatitis C virus nonstructural proteins are localized in a modified endoplasmic reticulum of cells expressing viral subgenomic replicons. Virology 293, 31 43.
65. Gosert R, Egger D, Lohmann V, Bartenschlager R, Blum HE, Bienz K Moradpour D (2003) Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J Virol 77, 5487 5492.
66. Walewski JL, Gutierrez JA, Branch-Elliman W, Stump DD, Keller TR, Rodriguez A, Benson G Branch AD (2002) Mutation master: profiles of substitutions in hepatitis C virus RNA of the core, alternate reading frame, and NS2 coding regions. RNA 8, 557 571.
67. Sander C Schneider R (1991) Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 9, 56 68.
68. Efferth T (2003) Adenosine triphosphate-binding cassette transporter genes in ageing and age-related diseases. Ageing Res Rev 2, 11 24.
69. Kapadia SB Chisari FV (2005) Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc Natl Acad Sci USA 102, 2561 2566.
70. Gao L, Tu H, Shi ST, Lee KJ, Asanaka M, Hwang SB Lai MM (2003) Interaction with a ubiquitin-like protein enhances the ubiquitination and degradation of hepatitis C virus RNA-dependent RNA polymerase. J Virol 77, 4149 4159.
71. Pavio N, Taylor DR Lai MM (2002) Detection of a novel unglycosylated form of hepatitis C virus E2 envelope protein that is located in the cytosol and interacts with PKR. J Virol 76, 1265 1272.
72. Franck N, Le Seyec J, Guguen-Guillouzo C Erdtmann L (2005) Hepatitis C virus NS2 protein is phosphorylated by the protein kinase CK2 and targeted for degradation to the proteasome. J Virol 79, 2700 2708.
73. Fujita M, Akari H, Sakurai A, Yoshida A, Chiba T, Tanaka K, Strebel K Adachi A (2004) Expression of HIV-1 accessory protein Vif is controlled uniquely to be low and optimal by proteasome degradation. Microbes Infect 6, 791 798.
74. Reichel C Beachy RN (2000) Degradation of tobacco mosaic virus movement protein by the 26S proteasome. J Virol 74, 3330 3337.
75. Drugeon G Jupin I (2002) Stability in vitro of the 69K movement protein of turnip yellow mosaic virus is regulated by the ubiquitin-mediated proteasome pathway. J Gen Virol 83, 3187 3197.
76. Rumenapf T, Stark R, Heimann M Thiel HJ (1998) N-Terminal protease of pestiviruses: identification of putative catalytic residues by site-directed mutagenesis. J Virol 72, 2544 2547.
77. Strebel K Beck E (1986) A second protease of foot-and-mouth disease virus. J Virol 58, 893 899.
78. Yamasaki K, Weihl CC Roos RP (1999) Alternative translation initiation of Theiler's murine encephalomyelitis virus. J Virol 73, 8519 8526.
79. Sambrook J, Fritsch EF Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
80. Kalamvoki M Mavromara P (2004) Calcium-dependent calpain proteases are implicated in processing of the hepatitis C virus NS5A protein. J Virol 78, 11865 11878.
81. Harlow E Lane D (1988) Antibodies. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.