The HCV ARFP/F/Core+1 protein: Production and functional analysis of an unconventional viral product

IUBMB Life

Volumn 61, Issue 7, 2009, Pages 739-752

  Vassilaki, Niki ^a   Mavromara, Penelope ^a  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

Author keywords

ARFP F core+1 proteins; Core; Core+1 open reading frame; Frameshift; Hepatitis C; Internal initiation

Indexed keywords

ALTERNATIVE READING FRAME PROTEIN; CORE PROTEIN; UNCLASSIFIED DRUG; HEPATITIS C ANTIGEN; HEPATITIS C PROTEIN F, HEPATITIS C VIRUS;

ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENETIC VARIABILITY; GENOME; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IN VITRO STUDY; LIVER CELL CARCINOMA; NONHUMAN; PROTEIN PROCESSING; REVIEW; RNA SEQUENCE; T LYMPHOCYTE; VIRUS ISOLATION; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; FRAMESHIFT MUTATION; GENETICS; LIVER TUMOR; MOUSE; PHYSIOLOGY; TUMOR CELL LINE;

FLAVIVIRIDAE; HEPATITIS C VIRUS; MUS; RNA VIRUSES;

ANIMALS; CELL LINE, TUMOR; FRAMESHIFT MUTATION; HEPACIVIRUS; HEPATITIS C ANTIGENS; HUMANS; LIVER NEOPLASMS; MICE; VIRAL CORE PROTEINS;

EID: 69249215471     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.201     Document Type: Review

References (121)

1. Di Bisceglie, A. M. (2000) Hepatology 31, 1014-1018.
2. Hoofnagle, J. H. (2002) Hepatology 36, S21-S29.
3. Poynard, T., Yuen, M. F., Ratziu, V., and Lai, C. L. (2003) Lancet 362, 2095-2100.
4. Houghton, M. and Abrignani, S. (2005) Nature 436, 961-966.
5. Alter, M. J. (1996) Eur. J. Gastroenterol. Hepatol. 8, 319-323.
6. Van Regenmortel, M. H. V., Fauquet, C. M., Bishop, D. H. L., Carstens, E. B., Estes, M. K., Lemon, S. M., Maniloff, J., Mayo, M. A., McGeoch, D. J., Pringle, C. R., and Wickner, R. B. (2000) Virus Taxonomy: The VIIth Report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
7. Bartenschlager, R., Frese, M., and Pietschmann, T. (2004) Adv. Virus Res. 63, 71-180.
8. Moradpour, D., Penin, F., and Rice, C. M. (2007) Nat. Rev. Microbiol. 5, 453-463.
9. Pestova, T. V., Kolupaeva, V. G., Lomakin, I. B., Pilipenko, E. V., Shatsky, I. N., Agol, V. I., and Hellen, C. U. (2001) Proc. Natl. Acad. Sci. USA 98, 7029-7036.
10. Giannini, C. and Brechot, C. (2003) Cell Death Differ. 10 (Suppl. 1), S27-S38.
11. Simmonds, P., Bukh, J., Combet, C., Deleage, G., Enomoto, N., Feinstone, S., Halfon, P., Inchauspe, G., Kuiken, C., Maertens, G., Mizokami, M., Murphy, D. G., Okamoto, H., Pawlotsky, J. M., Penin, F., Sablon, E., Shin, I. T., Stuyver, L. J., Thiel, H. J., Viazov, S., Weiner, A. J., and Widell, A. (2005) Hepatology 42, 962-973.
12. Feld, J. J. and Hoofnagle, J. H. (2005) Nature 436, 967-972.
13. Zein, N. N., Poterucha, J. J., Gross, J. B., Jr., Wiesner, R. H., Therneau, T. M., Gossard, A. A., Wendt, N. K., Mitchell, P. S., Germer, J. J., and Persing, D. H. (1996) Am. J. Gastroenterol. 91, 2560-2562.
14. Smith, D. B. and Simmonds, P. (1997) J. Mol. Evol. 45, 238-246.
15. Ina, Y., Mizokami, M., Ohba, K., and Gojobori, T. (1994) J. Mol. Evol. 38, 50-56.
16. Walewski, J. L., Stump, D. D., Keller, T. R., and Branch, A. D. (1998) Hepatology 28, 278A, Abstract 462.
17. Walewski, J. L., Keller, T. R., Stump, D. D., and Branch, A. D. (2001) RNA 7, 710-721.
18. Varaklioti, A., Vassilaki, N., Georgopoulou, U., and Mavromara, P. (2002) J. Biol. Chem. 277, 17713-17721.
19. Xu, Z., Choi, J., Yen, T. S., Lu, W., Strohecker, A., Govindarajan, S., Chien, D., Selby, M. J., and Ou, J. (2001) EMBO J. 20, 3840-3848.
20. Varaklioti, R., Georgopoulou, U., Vassilaki, N., and Mavromara, P. (2000) Molecular virology and pathogenesis. Presented at the 7th International Meeting on Hepatitis C Virus and Related Viruses. Gold coast, Queensland, Australia.
21. Baril, M. and Brakier-Gingras, L. (2005) Nucleic Acids Res. 33, 1474-1486.
22. Boulant, S., Becchi, M., Penin, F., and Lavergne, J. P. (2003) J Biol Chem 278, 45785-45792.
23. Choi, J., Xu, Z., and Ou, J. H. (2003) Mol. Cell Biol. 23, 1489-1497.
24. Vassilaki, N. and Mavromara, P. (2003) J. Biol. Chem. 278, 40503-40513.
25. Tuplin, A., Evans, D. J., and Simmonds, P. (2004) J. Gen. Virol. 85, 3037-3047.
26. Tuplin, A., Wood, J., Evans, D. J., Patel, A. H., and Simmonds, P. (2002) RNA 8, 824-841.
27. Vassilaki, N., Kalliampakou, K. I., and Mavromara, P. (2008) J. Gen. Virol. 89, 222-231.
28. Xu, Z., Choi, J., Lu, W., and Ou, J. H. (2003) J. Virol. 77, 1578-1583.
29. Vassilaki, N., Boleti, H., and Mavromara, P. (2007) FEBS J. 274, 4057-4074.
30. Vassilaki, N., Boleti, H., and Mavromara, P. (2008) Virus Res. 133, 123-135.
31. Roussel, J., Pillez, A., Montpellier, C., Duverlie, G., Cahour, A., Dubuisson, J., and Wychowski, C. (2003) J. Gen. Virol. 84, 1751-1759.
32. Ratinier, M., Boulant, S., Combet, C., Targett-Adams, P., McLauchlan, J., and Lavergne, J. P. (2008) J. Gen. Virol. 89, 1569-1578.
33. Branch, A. D., Walewski, J. L., Gutierrez, J. A., Fernandez, E. J., Im, G. Y., Dieterich, D. T., Schiano, T. D., Sigal S.H., Schilsky M. L., and Schwartz, M. E. (2003) Hepatology 38, 468A-469A.
34. Bain, C., Parroche, P., Lavergne, J. P., Duverger, B., Vieux, C., Dubois, V., Komurian-Pradel, F., Trepo, C., Gebuhrer, L., Paranhos-Baccala, G., Penin, F., and Inchauspe, G. (2004) J. Virol. 78, 10460-10469.
35. Miladi, A., Lavergne, J. P., Hezode, C., Dhumeaux, D., Penin, F., and Pawlotsky, J. M. (2004) In the 11th International Symposium on Hepatitis C Virus and Related Viruses. Heidelberg, Germany, p. 238.
36. Troesch, M., Jalbert, E., Canobio, S., Boulassel, M. R., Routy, J. P., Bernard, N. F., Bruneau, J., Lapointe, N., Boucher, M., and Soudeyns, H. (2005) AIDS 19, 775-784.
37. Cohen, M., Bachmatov, L., Ben-Ari, Z., Rotman, Y., Tur-Kaspa, R., and Zemel, R. (2007) Dig. Dis. Sci. 52, 2427-2432.
38. Chuang, W. C. and Allain, J. P. (2008) J. Gen. Virol. 89, 1890-1900.
39. Shesheer Kumar, M., Venkateswara Rao, K., Mohammed Habeebullah, C., and Dashavantha Reddy, V. (2008) Infect. Genet. Evol. 8, 374-377.
40. Pawlotsky, J. M., Morice, Y., Miladi, A., Lavergne, J. P., Germanidis, G., and Penin, F. (2005) Presented at the 12th International Symposium on Hepatitis C Virus and Related Viruses. Montreal, Canada.
41. Komurian-Pradel, F., Rajoharison, A., Berland, J. L., Khouri, V., Perret, M., Van Roosmalen, M., Pol, S., Negro, F., and Paranhos-Baccala, G. (2004) Hepatology 40, 900-909.
42. Basu, A., Steele, R., Ray, R., and Ray, R. B. (2004) J. Gen. Virol. 85, 2299-2306.
43. Ulsenheimer, A., Gerlach, J. T., Gruener, N. H., Jung, M. C., Schirren, C. A., Schraut, W., Zachoval, R., Pape, G. R., and Diepolder, H. M. (2003) Hepatology 37, 1189-1198.
44. Wedemeyer, H., He, X. S., Nascimbeni, M., Davis, A. R., Greenberg, H. B., Hoofnagle, J. H., Liang, T. J., Alter, H., and Rehermann, B. (2002) J. Immunol. 169, 3447-3458.
45. Sobesky, R., Feray, C., Rimlinger, F., Derian, N., Dos Santos, A., Roque-Afonso, A. M., Samuel, D., Brechot, C., and Thiers, V. (2007) Hepatology 46, 1704-1712.
46. Ruster, B., Zeuzem, S., and Roth, W. K. (1996) Biochem. Biophys. Res. Commun. 219, 911-915.
47. Yeh, C. T., Lu, S. C., Chu, C. M., and Liaw, Y. F. (1997) J. Gen. Virol. 78 (Part 11), 2761-2770.
48. Yeh, C. T., Lo, S. Y., Dai, D. I., Tang, J. H., Chu, C. M., and Liaw, Y. F. (2000) J. Gastroenterol. Hepatol. 15, 182-191.
49. Hayashi, J., Furusyo, N., Ariyama, I., Sawayama, Y., Etoh, Y., and Kashiwagi, S. (2000) J. Infect. Dis. 181, 1523-1527.
50. Ogata, S., Nagano-Fujii, M., Ku, Y., Yoon, S., and Hotta, H. (2002) J. Clin. Microbiol. 40, 3625-3630.
51. Alam, S. S., Nakamura, T., Naganuma, A., Nozaki, A., Nouso, K., Shimomura, H., and Kato, N. (2002) Acta Med. Okayama 56, 141-147.
52. Ruggli, N., Tratschin, J. D., Schweizer, M., McCullough, K. C., Hofmann, M. A., and Summerfield, A. (2003) J. Virol. 77, 7645-7654.
53. Rumenapf, T., Stark, R., Heimann, M., and Thiel, H. J. (1998) J. Virol. 72, 2544-2547.
54. Cristina, J., Lopez, F., Moratorio, G., Lopez, L., Vasquez, S., Garcia-Aguirre, L., and Chunga, A. (2005) J. Gen. Virol. 86, 115-120.
55. Walewski, J. L., Gutierrez, J. A., Branch-Elliman, W., Stump, D. D., Keller, T. R., Rodriguez, A., Benson, G., and Branch, A. D. (2002) RNA 8, 557-571.
56. Sander, C. and Schneider, R. (1991) Proteins 9, 56-68.
57. Efferth, T. (2003) Ageing Res. Rev. 2, 11-24.
58. Zhong, J., Gastaminza, P., Cheng, G., Kapadia, S., Kato, T., Burton, D. R., Wieland, S. F., Uprichard, S. L., Wakita, T., and Chisari, F. V. (2005) Proc. Natl. Acad. Sci. USA 102, 9294-9299.
59. Guruprasad, K., Reddy, B. V., and Pandit, M. W. (1990) Protein Eng. 4, 155-161.
60. Wolf, M., Dimitrova, M., Baumert, T. F., and Schuster, C. (2008) Nucleic Acids Res. 36, 3054-3064.
61. Hagglund, R. and Roizman, B. (2004) J. Virol. 78, 2169-2178.
62. Huang, J., Huang, Q., Zhou, X., Shen, M. M., Yen, A., Yu, S. X., Dong, G., Qu, K., Huang, P., Anderson, E. M., Daniel-Issakani, S., Buller, R. M., Payan, D. G., and Lu, H. H. (2004) J. Biol. Chem. 279, 54110-54116.
63. Mansouri, M., Bartee, E., Gouveia, K., Hovey Nerenberg, B. T., Barrett, J., Thomas, L., Thomas, G., McFadden, G., and Fruh, K. (2003) J. Virol. 77, 1427-1440.
64. Coadou, G., Gharbi-Benarous, J., Megy, S., Bertho, G., Evrard-Todeschi, N., Segeral, E., Benarous, R., and Girault, J. P. (2003) Biochemistry 42, 14741-14751.
65. Kehn, K., Fuente Cde, L., Strouss, K., Berro, R., Jiang, H., Brady, J., Mahieux, R., Pumfery, A., Bottazzi, M. E., and Kashanchi, F. (2005) Oncogene 24, 525-540.
66. Eom, C. Y., Heo, W. D., Craske, M. L., Meyer, T., and Lehman, I. R. (2004) Proc. Natl. Acad. Sci. USA 101, 4036-4040.
67. Thomas, M., Pim, D., and Banks, L. (1999) Oncogene 18, 7690-7700.
68. Choi, B. H., Park, G. T., and Rho, H. M. (1999) J. Biol. Chem. 274, 2858-2865.
69. Kim, J. H., Kang, S., Kim, J., and Ahn, B. Y. (2003) J. Virol. 77, 7166-7173.
70. Spandau, D. F. and Lee, C. H. (1988) J. Virol. 62, 427-434.
71. Twu, J. S. and Schloemer, R. H. (1987) J. Virol. 61, 3448-3453.
72. Yen, T. S. (1996) J. Biomed. Sci. 3, 20-30.
73. Moriishi, K., Okabayashi, T., Nakai, K., Moriya, K., Koike, K., Murata, S., Chiba, T., Tanaka, K., Suzuki, R., Suzuki, T., Miyamura, T., and Matsuura, Y. (2003) J. Virol. 77, 10237-10249.
74. Ma, H. C., Lin, T. W., Li, H., Iguchi-Ariga, S. M., Ariga, H., Chuang, Y. L., Ou, J. H., and Lo, S. Y. (2008) J. Biomed. Sci. 15, 417-425.
75. Gorlich, D. and Kutay, U. (1999) Annu. Rev. Cell. Dev. Biol. 15, 607-660.
76. Lyman, S. K., Guan, T., Bednenko, J., Wodrich, H., and Gerace, L. (2002) J. Cell Biol. 159, 55-67.
77. Nachury, M. V. and Weis, K. (1999) Proc. Natl. Acad. Sci. USA 96, 9622-9627.
78. Ratinier, M., Boulant, S., Crussard, S., McLauchlan, J., and Lavergne, J. P. (2009) Virus Res. 139, 106-110.
79. Wakita, T., Pietschmann, T., Kato, T., Date, T., Miyamoto, M., Zhao, Z., Murthy, K., Habermann, A., Krausslich, H. G., Mizokami, M., Bartenschlager, R., and Liang, T. J. (2005) Nat. Med. 11, 791-796.
80. Bartenschlager, R. and Pietschmann, T. (2005) Proc. Natl. Acad. Sci. USA 102, 9739-9740.
81. Lindenbach, B. D., Evans, M. J., Syder, A. J., Wolk, B., Tellinghuisen, T. L., Liu, C. C., Maruyama, T., Hynes, R. O., Burton, D. R., McKeating, J. A., and Rice, C. M. (2005) Science 309, 623-626.
82. Lohmann, V., Korner, F., Koch, J., Herian, U., Theilmann, L., and Bartenschlager, R. (1999) Science 285, 110-113.
83. Blight, K. J., Kolykhalov, A. A., and Rice, C. M. (2000) Science 290, 1972-1974.
84. Vassilaki, N., Friebe, P., Meuleman, P., Kallis, S., Kaul, A., Paranhos-Baccalà, G., Leroux-Roels, G., Mavromara, P., and Bartenschlager, R. (2008) J. Virol. 82, 11503-11515.
85. McMullan, L. K., Grakoui, A., Evans, M. J., Mihalik, K., Puig, M., Branch, A. D., Feinstone, S. M., and Rice, C. M. (2007) Proc. Natl. Acad. Sci. USA 104, 2879-2884.
86. Blight, K. J., McKeating, J. A., and Rice, C. M. (2002) J. Virol. 76, 13001-13014.
87. Friebe, P., Boudet, J., Simorre, J. P., and Bartenschlager, R. (2005) J. Virol. 79, 380-392.
88. Bartenschlager, R. and Sparacio, S. (2007) Virus Res. 127, 195-207.
89. Delgrange, D., Pillez, A., Castelain, S., Cocquerel, L., Rouille, Y., Dubuisson, J., Wakita, T., Duverlie, G., and Wychowski, C. (2007) J. Gen. Virol. 88, 2495-2503.
90. McLauchlan, J. (2000) J. Viral. Hepat. 7, 2-14.
91. Ray, R. B. and Ray, R. (2001) FEMS Microbiol. Lett. 202, 149-156.
92. Spengler, U. and Nattermann, J. (2007) Clin. Sci. (Lond) 112, 141-155.
93. Moriya, K., Fujie, H., Shintani, Y., Yotsuyanagi, H., Tsutsumi, T., Ishibashi, K., Matsuura, Y., Kimura, S., Miyamura, T., and Koike, K. (1998) Nat. Med. 4, 1065-1067.
94. Wu, W.B., Shao, S.W., Zhao L.J., Luan, J., Cao, J., Gao, J., Zhu, S.Y., Qi, Z.T. (2007). Intervirology 50, 341-346.
95. Fiorucci, M., Boulant, S., Fournillier, A., Abraham, J. D., Lavergne, J. P., Paranhos-Baccala, G., Inchauspe, G., and Bain, C. (2007) J. Gen. Virol. 88, 1149-1162.
96. Tsao, M. L., Chao, C. H., and Yeh, C. T. (2006) Biochem. Biophys. Res. Commun. 348, 271-277.
97. Huang, Y. P., Cheng, J., Zhang, S. L., Wang, L., Guo, J., Liu, Y., Yang, Y., Zhang, L. Y., Bai, G. Q., Gao, X. S., Ji, D., Lin, S. M., and Shao, Q. (2005) World J. Gastroenterol. 11, 5659-5665.
98. Dou, J., Liu, P., Wang, J., and Zhang, X. (2006) J. Gastroenterol. Hepatol. 21, 1794-1800.
99. Ray, R. B., Steele, R., Meyer, K., and Ray, R. (1998) Gene 208, 331-336.
100. Mori, K., Maeda, Y., Kitaura, H., Taira, T., Iguchi-Ariga, S. M., and Ariga, H. (1998) J. Biol. Chem. 273, 29794-29800.
101. Satou, A., Hagio, Y., Taira, T., Iguchi-Ariga, S. M., and Ariga, H. (2004) FEBS Lett. 572, 211-215.
102. Martin-Benito, J., Boskovic, J., Gomez-Puertas, P., Carrascosa, J. L., Simons, C. T., Lewis, S. A., Bartolini, F., Cowan, N. J., and Valpuesta, J. M. (2002) EMBO J. 21, 6377-6386.
103. Okochi, M., Nomura, T., Zako, T., Arakawa, T., Iizuka, R., Ueda, H., Funatsu, T., Leroux, M., and Yohda, M. (2004) J. Biol. Chem. 279, 31788-31795.
104. Bost, A. G., Venable, D., Liu, L., and Heinz, B. A. (2003) J. Virol. 77, 4401-4408.
105. Strebel, K. and Beck, E. (1986) J. Virol. 58, 893-899.
106. Yamasaki, L. and Pagano, M. (2004) Curr. Opin. Cell. Biol. 16, 623-628.
107. La Rocca, S. A., Herbert, R. J., Crooke, H., Drew, T. W., Wileman, T. E., and Powell, P. P. (2005) J. Virol. 79, 7239-7247.
108. Mayer, D., Hofmann, M. A., and Tratschin, J. D. (2004) Vaccine 22, 317-328.
109. Devaney, M. A., Vakharia, V. N., Lloyd, R. E., Ehrenfeld, E., and Grubman, M. J. (1988) J. Virol. 62, 4407-4409.
110. Medina, M., Domingo, E., Brangwyn, J. K., and Belsham, G. J. (1993) Virology 194, 355-359.
111. Chen, H. H., Kong, W. P., Zhang, L., Ward, P. L., and Roos, R. P. (1995) Nat. Med. 1, 927-931.
112. Ghadge, G. D., Ma, L., Sato, S., Kim, J., and Roos, R. P. (1998) J. Virol. 72, 8605-8612.
113. Himeda, T., Ohara, Y., Asakura, K., Kontani, Y., and Sawada, M. (2005) Microb. Pathog. 38, 201-207.
114. Soussan, P., Garreau, F., Zylberberg, H., Ferray, C., Brechot, C., and Kremsdorf, D. (2000) J. Clin. Invest. 105, 55-60.
115. Soussan, P., Tuveri, R., Nalpas, B., Garreau, F., Zavala, F., Masson, A., Pol, S., Brechot, C., and Kremsdorf, D. (2003) J. Hepatol. 38, 343-348.
116. Franck, N., Le Seyec, J., Guguen-Guillouzo, C., and Erdtmann, L. (2005) J. Virol. 79, 2700-2708.
117. Fujita, M., Akari, H., Sakurai, A., Yoshida, A., Chiba, T., Tanaka, K., Strebel, K., and Adachi, A. (2004) Microbes Infect. 6, 791-798.
118. Gao, L., Tu, H., Shi, S. T., Lee, K. J., Asanaka, M., Hwang, S. B., and Lai, M. M. (2003) J. Virol. 77, 4149-4159.
119. Lehto, K., Bubrick, P., and Dawson, W. O. (1990) Virology 174, 290-293.
120. Maule, A. (1991) Plant Sci. 9, 457-473.
121. Pavio, N., Taylor, D. R., and Lai, M. M. (2002) J. Virol. 76, 1265-1272.