Kinetic analysis of the nucleic acid chaperone activity of the hepatitis C virus core protein

Nucleic Acids Research

Volumn 38, Issue 11, 2010, Pages 3632-3642

  Sharma, Kamal Kant ^a   Didier, Pascal ^a   Darlix, Jean Luc ^b   de Rocquigny, Hugues ^a   Bensikaddour, Hayet ^a   Lavergne, Jean Pierre ^c   Pénin, François ^a   Lessinger, Jean Marc ^a   Mély, Yves ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ DE LYON   (France)

^c University Lyon i   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; NUCLEIC ACID; OLIGONUCLEOTIDE; VIRUS DNA;

ARTICLE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; DNA SEQUENCE; FLUORESCENCE SPECTROSCOPY; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE;

HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77954357650     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq094     Document Type: Article

References (63)

1. Choo,Q.L., Kuo,G., Weiner,A.J., Overby,L.R., Bradley,D.W. and 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. Recommendations from the National Institutes of Health consensus development conference statement: management of hepatitis C: 2002, Hepatology, 36, 1039
3. Lauer,G.M. and Walker,B.D. 2001, Hepatitis C virus infection. N. Eng. J. Med., 345, 41-52
4. Moradpour,D., Penin,F. and Rice,C.M. 2007, Replication of hepatitis C virus. Nat. Rev., 5, 453-463
5. Honda,M., Beard,M.R., Ping,L.H. and Lemon,S.M. 1999, A phylogenetically conserved stem-loop structure at the 5′ border of the internal ribosome entry site of hepatitis C virus is required for cap-independent viral translation. J. Virol., 73, 1165-1174
6. Blight,K.J. and Rice,C.M. 1997, Secondary structure determination of the conserved 98-base sequence at the 3′ terminus of hepatitis C virus genome RNA. Journal of virology, 71, 7345-7352
7. Kolykhalov,A.A., Feinstone,S.M. and Rice,C.M. 1996, Identification of a highly conserved sequence element at the 3′ terminus of hepatitis C virus genome RNA. Journal of virology, 70, 3363-3371
8. Friebe,P. and Bartenschlager,R. 2002, Genetic analysis of sequences in the 3' nontranslated region of hepatitis C virus that are important for RNA replication. Journal of virology, 76, 5326-5338
9. Penin,F., Dubuisson,J., Rey,F.A., Moradpour,D. and Pawlotsky,J.M. 2004, Structural biology of hepatitis C virus. Hepatology, 39, 5-19
10. Ray,R.B. and Ray,R. 2001, Hepatitis C virus core protein: intriguing properties and functional relevance. FEMS Microbiol. Lett., 202, 149-156
11. McLauchlan,J. 2000, Properties of the hepatitis C virus core protein: a structural protein that modulates cellular processes. J. Viral Hepat., 7, 2-14
12. Hijikata,M., Kato,N., Mori,S., Ootsuyama,Y., Nakagawa,M., Sugimura,T., Ohkoshi,S., Kojima,H., Meguro,T., Taki,M. et al. 1990, Frequent detection of hepatitis C virus US strain in Japanese hemophiliacs. Jpn J Cancer Res, 81, 1195-1197
13. Lemberg,M.K. and Martoglio,B. 2002, Requirements for signal peptide peptidase-catalyzed intramembrane proteolysis. Mol. Cell, 10, 735-744
14. McLauchlan,J., Lemberg,M.K., Hope,G. and Martoglio,B. 2002, Intramembrane proteolysis promotes trafficking of hepatitis C virus core protein to lipid droplets. EMBO J., 21, 3980-3988
15. Moradpour,D., Englert,C., Wakita,T. and Wands,J.R. 1996, Characterization of cell lines allowing tightly regulated expression of hepatitis C virus core protein. Virology, 222, 51-63
16. Barba,G., Harper,F., Harada,T., Kohara,M., Goulinet,S., Matsuura,Y., Eder,G., Schaff,Z., Chapman,M.J., Miyamura,T. et al. 1997, Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc. Natl Acad. Sci. USA, 94, 1200-1205
17. Hope,R.G. and McLauchlan,J. 2000, Sequence motifs required for lipid droplet association and protein stability are unique to the hepatitis C virus core protein. J. Gen. Virol., 81, 1913-1925
18. Schwer,B., Ren,S., Pietschmann,T., Kartenbeck,J., Kaehlcke,K., Bartenschlager,R., Yen,T.S. and Ott,M. 2004, Targeting of hepatitis C virus core protein to mitochondria through a novel C-terminal localization motif. J. Virol., 78, 7958-7968
19. Boulant,S., Vanbelle,C., Ebel,C., Penin,F. and Lavergne,J.P. 2005, Hepatitis C virus core protein is a dimeric alpha-helical protein exhibiting membrane protein features. J. Virol., 79, 11353-11365
20. Ivanyi-Nagy,R., Kanevsky,I., Gabus,C., Lavergne,J.P., Ficheux,D., Penin,F., Fosse,P. and Darlix,J.L. 2006, Analysis of hepatitis C virus RNA dimerization and core-RNA interactions. Nucleic Acids Res., 34, 2618-2633
21. Boulant,S., Montserret,R., Hope,R.G., Ratinier,M., Targett-Adams,P., Lavergne,J.P., Penin,F. and McLauchlan,J. 2006, Structural determinants that target the hepatitis C virus core protein to lipid droplets. J. Biol. Chem., 281, 22236-22247
22. Shavinskaya,A., Boulant,S., Penin,F., McLauchlan,J. and Bartenschlager,R. 2007, The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly. J. Biol. Chem., 282, 37158-37169
23. Giannini,C. and Brechot,C. 2003, Hepatitis C virus biology. Cell Death Differ., 10 (Suppl. 1), S27-S38
24. Lerat,H., Honda,M., Beard,M.R., Loesch,K., Sun,J., Yang,Y., Okuda,M., Gosert,R., Xiao,S.Y., Weinman,S.A. et al. 2002, Steatosis and liver cancer in transgenic mice expressing the structural and nonstructural proteins of hepatitis C virus. Gastroenterology, 122, 352-365
25. Kunkel,M., Lorinczi,M., Rijnbrand,R., Lemon,S.M. and Watowich,S.J. 2001, Self-assembly of nucleocapsid-like particles from recombinant hepatitis C virus core protein. J. Virol., 75, 2119-2129
26. Baumert,T.F., Ito,S., Wong,D.T. and Liang,T.J. 1998, Hepatitis C virus structural proteins assemble into viruslike particles in insect cells. J. Virol., 72, 3827-3836
27. Shimoike,T., Mimori,S., Tani,H., Matsuura,Y. and Miyamura,T. 1999, Interaction of hepatitis C virus core protein with viral sense RNA and suppression of its translation. J. Virol., 73, 9718-9725
28. Cristofari,G., Ivanyi-Nagy,R., Gabus,C., Boulant,S., Lavergne,J.P., Penin,F. and Darlix,J.L. 2004, The hepatitis C virus Core protein is a potent nucleic acid chaperone that directs dimerization of the viral (+) strand RNA in vitro. Nucleic Acids Res., 32, 2623-2631
29. Bernacchi,S., Stoylov,S., Piemont,E., Ficheux,D., Roques,B.P., Darlix,J.L. and Mely,Y. 2002, HIV-1 nucleocapsid protein activates transient melting of least stable parts of the secondary structure of TAR and its complementary sequence. J. Mol. Biol., 317, 385-399
30. Godet,J., de Rocquigny,H., Raja,C., Glasser,N., Ficheux,D., Darlix,J.L. and Mely,Y. 2006, During the early phase of HIV-1 DNA synthesis, nucleocapsid protein directs hybridization of the TAR complementary sequences via the ends of their double-stranded stem. J. Mol. Biol., 356, 1180-1192
31. Ramalanjaona,N., de Rocquigny,H., Millet,A., Ficheux,D., Darlix,J.L. and Mely,Y. 2007, Investigating the mechanism of the nucleocapsid protein chaperoning of the second strand transfer during HIV-1 DNA synthesis. J. Mol. Biol., 374, 1041-1053
32. Egele,C., Piemont,E., Didier,P., Ficheux,D., Roques,B., Darlix,J.L., de Rocquigny,H. and Mely,Y. 2007, The single-finger nucleocapsid protein of moloney murine leukemia virus binds and destabilizes the TAR sequences of HIV-1 but does not promote efficiently their annealing. Biochemistry, 46, 14650-14662
33. Liu,H.W., Cosa,G., Landes,C.F., Zeng,Y., Kovaleski,B.J., Mullen,D.G., Barany,G., Musier-Forsyth,K. and Barbara,P.F. 2005, Single-molecule FRET studies of important intermediates in the nucleocapsid-protein-chaperoned minus-strand transfer step in HIV-1 reverse transcription. Biophys. J., 89, 3470-3479
34. Stewart-Maynard,K.M., Cruceanu,M., Wang,F., Vo,M.N., Gorelick,R.J., Williams,M.C., Rouzina,I. and Musier-Forsyth,K. 2008, Retroviral nucleocapsid proteins display nonequivalent levels of nucleic acid chaperone activity. J. Virol., 82, 10129-10142
35. Vo,M.N., Barany,G., Rouzina,I. and Musier-Forsyth,K. 2009, HIV-1 nucleocapsid protein switches the pathway of transactivation response element RNA/DNA annealing from loop-loop "kissing" to "zipper". J. Mol. Biol., 386, 789-801
36. Baudin,F., Marquet,R., Isel,C., Darlix,J.L., Ehresmann,B. and Ehresmann,C. 1993, Functional sites in the 5' region of human immunodeficiency virus type 1 RNA form defined structural domains. J. Mol. Biol., 229, 382-397
37. Azoulay,J., Clamme,J.P., Darlix,J.L., Roques,B.P. and Mely,Y. 2003, Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations. J. Mol. Biol., 326, 691-700
38. Beltz,H., Clauss,C., Piemont,E., Ficheux,D., Gorelick,R.J., Roques,B., Gabus,C., Darlix,J.L., de Rocquigny,H. and Mely,Y. 2005, Structural determinants of HIV-1 nucleocapsid protein for cTAR DNA binding and destabilization, and correlation with inhibition of self-primed DNA synthesis. J. Mol. Biol., 348, 1113-1126.
39. Clamme,J.P., Azoulay,J. and Mely,Y. 2003, Monitoring of the formation and dissociation of polyethylenimine/DNA complexes by two photon fluorescence correlation spectroscopy. Biophys. J., 84, 1960-1968
40. Thompson,N.L. 1991, Fluorescence Correlation Spectroscopy, in Topics in Fluorescence Spectroscopy. Plenum Publishers, NY
41. Cristofari,G. and Darlix,J.L. 2002, The ubiquitous nature of RNA chaperone proteins. Prog. Nucleic Acid Res. Mol. Biol., 72, 223-268
42. Stoylov,S.P., Vuilleumier,C., Stoylova,E., De Rocquigny,H., Roques,B.P., Gerard,D. and Mely,Y. 1997, Ordered aggregation of ribonucleic acids by the human immunodeficiency virus type 1 nucleocapsid protein. Biopolymers, 41, 301-312
43. Bloomfield,V.A., He,S., Li,A.Z. and Arscott,P.B. 1991, Light scattering studies on DNA condensation. Biochem. Soc. Transact., 19, 496
44. Beltz,H., Azoulay,J., Bernacchi,S., Clamme,J.P., Ficheux,D., Roques,B., Darlix,J.L. and Mely,Y. 2003, Impact of the terminal bulges of HIV-1 cTAR DNA on its stability and the destabilizing activity of the nucleocapsid protein NCp7. J. Mol. Biol., 328, 95-108.
45. Bombarda,E., Grell,E., Roques,B.P. and Mely,Y. 2007, Molecular mechanism of the Zn2+-induced folding of the distal CCHC finger motif of the HIV-1 nucleocapsid protein. Biophys. J., 93, 208-217.
46. Rouzina,I. and Bloomfield,V.A. 1999, Heat capacity effects on the melting of DNA. 1. General aspects. Biophys. J., 77, 3242-3251
47. Cantor,C. and Schimmel,P. 1980, Biophysical Chemistry Part 2: Techniques for the Study of Biological Structure and Function. Academic Press, NY
48. Cosa,G., Zeng,Y., Liu,H.W., Landes,C.F., Makarov,D.E., Musier-Forsyth,K. and Barbara,P.F. 2006, Evidence for non-two-state kinetics in the nucleocapsid protein chaperoned opening of DNA hairpins. J. Phys. Chem., 110, 2419-2426
49. Vo,M.N., Barany,G., Rouzina,I. and Musier-Forsyth,K. 2009, Effect of Mg(2+) and Na(+) on the nucleic acid chaperone activity of HIV-1 nucleocapsid protein: implications for reverse transcription. J. Mol. Biol., 386, 773-788
50. Beltz,H., Piemont,E., Schaub,E., Ficheux,D., Roques,B., Darlix,J.L. and Mely,Y. 2004, Role of the structure of the top half of HIV-1 cTAR DNA on the nucleic acid destabilizing activity of the nucleocapsid protein NCp7. J. Mol. Biol., 338, 711-723
51. Vo,M.N., Barany,G., Rouzina,I. and Musier-Forsyth,K. 2006, Mechanistic studies of mini-TAR RNA/DNA annealing in the absence and presence of HIV-1 nucleocapsid protein. J. Mol. Biol., 363, 244-261
52. Le Cam,E., Coulaud,D., Delain,E., Petitjean,P., Roques,B.P., Gerard,D., Stoylova,E., Vuilleumier,C., Stoylov,S.P. and Mely,Y. 1998, Properties and growth mechanism of the ordered aggregation of a model RNA by the HIV-1 nucleocapsid protein: an electron microscopy investigation. Biopolymers, 45, 217-229
53. Grohmann,D., Godet,J., Mely,Y., Darlix,J.L. and Restle,T. 2008, HIV-1 nucleocapsid traps reverse transcriptase on nucleic acid substrates. Biochemistry, 47, 12230-12240
54. Chen,Y., Balakrishnan,M., Roques,B.P. and Bambara,R.A. 2003, Steps of the acceptor invasion mechanism for HIV-1 minus strand strong stop transfer. J.Biol. Chem., 278, 38368-38375
55. Kim,J.K., Palaniappan,C., Wu,W., Fay,P.J. and Bambara,R.A. 1997, Evidence for a unique mechanism of strand transfer from the transactivation response region of HIV-1. J. Biol. Chem., 272, 16769-16777
56. Roda,R.H., Balakrishnan,M., Kim,J.K., Roques,B.P., Fay,P.J. and Bambara,R.A. 2002, Strand transfer occurs in retroviruses by a pause-initiated two-step mechanism. J. Biol. Chem., 277, 46900-46911
57. Ivanyi-Nagy,R., Davidovic,L., Khandjian,E.W. and Darlix,J.L. 2005, Disordered RNA chaperone proteins: from functions to disease. Cell. Mol. Life Sci., 62, 1409-1417
58. Morellet,N., de Rocquigny,H., Mely,Y., Jullian,N., Demene,H., Ottmann,M., Gerard,D., Darlix,J.L., Fournie-Zaluski,M.C. and Roques,B.P. 1994, Conformational behaviour of the active and inactive forms of the nucleocapsid NCp7 of HIV-1 studied by 1H NMR. J. Mol. Biol., 235, 287-301
59. Summers,M.F., Henderson,L.E., Chance,M.R., Bess,J.W. Jr, South,T.L., Blake,P.R., Sagi,I., Perez-Alvarado,G., Sowder,R.C. III, Hare,D.R. et al. 1992, Nucleocapsid zinc fingers detected in retroviruses: EXAFS studies of intact viruses and the solution-state structure of the nucleocapsid protein from HIV-1. Protein Sci., 1, 563-574
60. Ivanyi-Nagy,R., Lavergne,J.P., Gabus,C., Ficheux,D. and Darlix,J.L. 2008, RNA chaperoning and intrinsic disorder in the core proteins of Flaviviridae. Nucleic Acids Res., 36, 712-725
61. Colina,R., Casane,D., Vasquez,S., Garcia-Aguirre,L., Chunga,A., Romero,H., Khan,B. and Cristina,J. 2004, Evidence of intratypic recombination in natural populations of hepatitis C virus. J. Gen. Virol., 85, 31-37
62. Kalinina,O., Norder,H. and Magnius,L.O. 2004, Full-length open reading frame of a recombinant hepatitis C virus strain from St Petersburg: proposed mechanism for its formation. J. Gen. Virol., 85, 1853-1857
63. Kalinina,O., Norder,H., Mukomolov,S. and Magnius,L.O. 2002, A natural intergenotypic recombinant of hepatitis C virus identified in St. Petersburg. J. Virol., 76, 4034-4043