RNA chaperoning and intrinsic disorder in the core proteins of Flaviviridae

Nucleic Acids Research

Volumn 36, Issue 3, 2008, Pages 712-725

  Ivanyi Nagy, Roland ^a   Lavergne, Jean Pierre ^b   Gabus, Caroline ^a   Ficheux, Damien ^b   Darlix, Jean Luc ^a  

^a University Lyon i   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CORE PROTEIN; NUCLEIC ACID; RNA; VIRUS RNA;

ARTICLE; BOVINE DIARRHEA VIRUS; CIRCULAR DICHROISM; CONTROLLED STUDY; ENTROPY; FLAVIVIRUS; GENE REARRANGEMENT; HEAT TOLERANCE; HEPATITIS C VIRUS; HEPATITIS GB VIRUS B; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE; RNA STRUCTURE; SEQUENCE HOMOLOGY; ULTRAVIOLET SPECTROSCOPY; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; WEST NILE FLAVIVIRUS;

CIRCULAR DICHROISM; DNA; FLAVIVIRIDAE; MOLECULAR CHAPERONES; PROTEIN DENATURATION; PROTEIN STRUCTURE, SECONDARY; RNA; RNA, CATALYTIC; RNA-BINDING PROTEINS; VIRAL CORE PROTEINS;

BOVINAE; BOVINE VIRAL DIARRHEA VIRUS 1; FLAVIVIRIDAE; HEPATITIS C VIRUS; HEPATITIS GB VIRUS B; WEST NILE VIRUS;

EID: 39449097872     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm1051     Document Type: Article

References (64)

1. Shepard,C.W., Finelli,L. and Alter,M.J. (2005) Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis., 5, 558-567.
2. Brown,R.S. (2005) Hepatitis C and liver transplantation. Nature, 436, 973-978.
3. Lindenbach,B.D., Thiel,H.J. and Rice,C.M. (2007) Flaviviridae: The viruses and their replication. In Knipe,D.M., Howley,P.M., Griffin,D.E., Lamb,R.A., Martin,M.A., Roizman,B. and Straus,S.E. (eds), Fields Virology, Lippincott Williams & Wilkins, Philadelphia, pp. 1101-1152.
4. Hijikata,M., Kato.N., Ootsuyama.Y., Nakagawa,M. and Shimotohno,K. (1991) Gene mapping of the putative structural region of the hepatitis C virus genome by in vitro processing analysis. Proc. Natl Acad. Sci. USA, 88, 5547-5551.
5. Santolini,E., Migliaccio,G. and La Monica,N. (1994) Biosynthesis and biochemical properties of the hepatitis C virus core protein. J. Virol., 68, 3631-3641.
6. Lemberg,M.K. and Martoglio,B. (2002) Requirements for signal peptide peptidase-catalyzed intramembrane proteolysis. Mol. Cell, 10 735-744.
7. 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.
8. 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.
9. Hope,R.G., Murphy,D.J. and McLauchlan,J. (2002) The domains required to direct core proteins of hepatitis C virus and GB virus-B to lipid droplets share common features with plant oleosin proteins. J. Biol. Chem., 277, 4261-4270.
10. Lobigs,M. (1993) Flavivirus premembrane protein cleavage and spike heterodimer secretion require the function of the viral proteinase NS3. Proc. Natl Acad. Sci. USA, 90, 6218-6222.
11. Amberg,S.M., Nestorowicz,A., McCourt,D.W. and Rice,C.M. (1994) NS2B-3 proteinase-mediated processing in the yellow fever virus structural region: in vitro and in vivo studies. J. Virol., 68 3794-3802.
12. Yamshchikov,V.F. and Compans,R.W. (1994) Processing of the intracellular form of the West Nile virus capsid protein by the viral NS2B-NS3 protease: An in vitro study. J. Virol., 68, 5765-5771.
13. l3 Rümenapf,T., Unger,G., Strauss.J.H. and Thiel,H.J. (1993) Processing of the envelope glycoproteins of pestiviruses. J. Virol. 67, 3288-3294.
14. Stark,R., Meyers,G., Rümenapf,T. and Thiel,H.J. (1993) Processing of pestivirus polyprotein: Cleavage site between autoprotease and nucleocapsid protein of classical swine fever virus. J. Virol., 67, 7088-7095.
15. Rümenapf,T., Stark,R., Heimann,M. and Thiel,H.J. (1998) N-terminal protease of pestiviruses: Identification of putative catalytic residues by site-directed mutagenesis. J. Virol., 72, 2544-2547.
16. Heimann,M., Roman-Sosa,G., Martoglio,B., Thiel,H.J. and Rümenapf,T. (2006) Core protein of pestiviruses is processed at the C terminus by signal peptide peptidase. J. Virol., 90, 1915-1921.
17. Herschlag,D. (1995) RNA chaperones and the RNA folding problem. J. Biol. Chem., 270, 20871-20874.
18. Cristofari,G. and Darlix,J.L. (2002) The ubiquitous nature of RNA chaperone proteins. Prog. Nucleic Acid Res. Mol. Biol., 72, 223-268.
19. Schroeder,R., Barta,A. and Semrad,K. (2004) Strategies for RNA folding and assembly. Nat. Rev. Mol. Cell Biol., 5, 908-919.
20. 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.
21. Bertrand,E.L. and Rossi,J.J. (1994) Facilitation of hammerhead ribozyme catalysis by the nucleocapsid protein of HIV-1 and the heterogeneous nuclear ribonucleoprotein A1. EMBO J., 13, 2904-2912.
22. Darlix,J.L., Lapadat-Tapolsky,M., de Rocquigny,H. and Roques,B.P. (1995) First glimpses at structure-function relationships of the nucleocapsid protein of retroviruses. J. Mol. Biol., 254, 523-537.
23. Rein,A., Henderson,L.E. and Levin,J.G. (1998) Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: Significance for viral replication. Trends Biochem. Sci., 23, 297-301.
24. Tompa,P. and Csermely,P. (2004) The role of structural disorder in the function of RNA and protein chaperones. FASEB J., 18, 1169-1175.
25. 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.
26. Ivanyi-Nagy,R., Kanevsky, I., Gabus,C., Lavergne,J.P., Ficheux,D., Penin,F., Fossé,P. and Darlix,J.L. (2006) Analysis of hepatitis C virus RNA dimerization and core-RNA interactions. Nucleic Acids Res. 34, 2618-2633.
27. Boulant,S., Becchi,M., Penin,F. and Lavergne,J.P. (2003) Unusual multiple recoding events leading to alternative forms of hepatitis C virus core protein from genotype 1b. J. Biol. Chem., 278, 45785-45792.
28. Boni,S., Lavergne,J.P., Boulant,S. and Cahour,A. (2005) Hepatitis C virus core protein acts as a trans-modulating factor on internal translation initiation of the viral RNA. J. Biol. Chem., 280 17737-17748.
29. Tsuchihashi,Z. and Brown,P.O. (1994) DNA strand exchange and selective DNA annealing promoted by the human immunodeficiency virus type 1 nucleocapsid protein. J. Virol., 68, 5863-5870.
30. Lys,2 binding sites in the endogenous retrovirus Gypsy. Nucleic Acids Res., 34, 5764-5777.
31. Obradovic,Z., Peng,K., Vucetic,S., Radivojac,P., Brown,C.J. and Dunker,A.K. (2003) Predicting intrinsic disorder from amino acid sequence. Proteins, 53(Suppl. 6), 566-572.
32. Dosztányi,Z., Csizmók,V., Tompa,P. and Simon,I. (2005) IUPred: Web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics, 21 3433-3434.
33. Prilusky,J., Felder,C.E., Zeev-Ben-Mordehai,T., Rydberg,E.H., Man,O., Beckmann,J.S., Silman,I. and Sussman,J.L. (2005) FoldIndex: A simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics, 21, 3435-3438.
34. Dosztányi,Z., Csizmók,V., Tompa,P. and Simon,I. (2005) The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J. Mol. Biol., 347, 827-839.
35. Uversky,V.N., Gillespie,J.R. and Fink,A.L. (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins, 41, 415-427.
36. 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.
37. 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.
38. Klein,K.C., Polyak,S.J. and Lingappa,J.R. (2004) Unique features of hepatitis C virus capsid formation revealed by de novo cell-free assembly. J. Virol., 78, 9257-9269.
39. Majeau,N., Gagne,V., Boivin,A., Bolduc,M., Majeau,J.A., Ouellet,D., and Leclerc,D. (2004) The N-terminal half of the core protein of hepatitis C virus is sufficient for nucleocapsid formation. J. Gen. Virol., 85, 971-981.
40. Dokland,T., Walsh,M., Mackenzie,J.M., Khromykh,A.A., Ee,K.H. and Wang,S. (2004) West Nile virus core protein; tetramer structure and ribbon formation. Structure, 12, 1157-1163.
41. Ma,L., Jones,C.T., Groesch,T,D., Kuhn,R.J. and Post,C.B. (2004) Solution structure of dengue virus capsid protein reveals another fold. Proc. Natl Acad. Sci. USA, 101, 3414-3419.
42. Jones,C.T., Ma,L., Burgner,J.W., Groesch,T.D., Post,C.B. and Kuhn,R.J. (2003) Flavivirus capsid is a dimeric alpha-helical protein. J. Virol., 77, 7143-7149.
43. Khromykh,A.A. and Westaway,E.G. (1996) RNA binding properties of core protein of the flavivirus Kunjin. Arch. Virol., 141, 685-699.
44. Waldsich,C., Grossberger,R. and Schroeder,R. (2002) RNA chaperone StpA loosens interactions of the tertiary structure in the td group I intron in vivo. Genes Dev., 16, 2300-2312.
45. Tsuchihashi,Z., Khosla,M. and Herschlag,D. (1993) Protein enhancement of hammerhead ribozyme catalysis. Science, 262, 99-102.
46. Herschlag,D., Khosla,M., Tsuchihashi,Z. and Karpel,R.L. (1994) An RNA chaperone activity of non-spepific RNA binding proteins in hammerhead ribozyme catalysis. EMBO J., 13, 2913-2924.
47. Gabus,C., Mazroui,R., Tremblay,S., Khandjian,E.W. and Darlix,J.L. (2004) The fragile X mental retardation protein has nucleic acid chaperone properties. Nucleic Acids Res., 32, 2129-2137.
48. Weinreb,P.H., Zhen,W., Poon,A.W., Conway,K.A. and Lansbury,P.T. Jr (1996) NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry, 35, 13709-13715.
49. Receveur-Bréchot,V., Bourhis,J.M., Uversky,V.N., Canard,B. and Longhi,S. (2006) Assessing protein disorder and induced folding. Proteins, 62, 24-45.
50. Kalthoff,C. (2003) A novel strategy for the purification of recombinantly expressed unstructured protein domains. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 786, 247-254.
51. Csizmók,V., Szollosi,E., Friedrich,P. and Tompa,P. (2006) A novel two-dimensional electrophoresis technique for the identification of intrinsically unstructured proteins. Mol. Cell. Proteomics, 5 265-273.
52. Csizmók,V., Dosztányi,Z., Simon,I. and Tompa,P. (2007) Towards proteomic approaches for the identification of structural disorder. Curr. Protein Pept. Sci., 8, 173-179.
53. Kunkel,M. and Watowich,S.J. (2004) Biophysical characterization of hepatitis C virus core protein: Implications for interactions within the virus and host. FEBS Lett., 557, 174-180.
54. Kim,T.D., Ryu,H.J., Cho,H.I., Yang,C.H. and Kim,J. (2000) Thermal behavior of proteins: Heat-resistant proteins and their heat-induced secondary structural changes. Biochemistry, 39, 14839-14846.
55. Uversky,V.N. (2002) What does it mean to be natively unfolded? Eur. J. Biochem., 269, 2-12.
56. Darlix,J.L., Garrido,J.L., Morellet,N., Mély,Y. and Rocquigny,H. (2007) Properties, functions, and drug targeting of the multifunctional nucleocapsid protein of the human immunodeficiency virus. Adv. Pharmacol., 55, 299-346.
57. Moradpour,D., Penin,F. and Rice,C.M. (2007) Replication of hepatitis C virus. Nat. Rev. Microbiol., 5, 453-463.
58. Negroni,M. and Buc,H. (2000) Copy-choice recombination by reverse transcriptases: Reshuffling of genetic markers mediated by RNA chaperones. Proc. Natl Acad. Sci. USA, 97, 6385-6390.
59. Bukh,J., Apgar,C.L., Govindarajan,S. and Purcell,R.H. (2001) Host range studies of GB virus-B hepatitis agent, the closest relative of hepatitis C virus, in New World monkeys and chimpanzees. J. Med. Virol., 65, 694-697.
60. Muerhoff,A.S., Leary,T.P, Simons,J.N., Pilot-Matias,T.J., Dawson,G.J., Erker,J.C., Chalmers,M.L., Schlauder,G.G., Desai,S.M. et al. (1995) Genomic organization of GB viruses A and B: Two new members of the Flaviviridae associated with GB agent hepatitis. J. Virol., 69, 5621-5630.
61. Khromykh,A.A., Meka,H., Guyatt,K.J. and Westaway,E.G. (2001) Essential role of cyclization sequences in flavivirus RNA replication. J. Virol., 75, 6719-6728.
62. Lo,M.K., Tilgner,M., Bernard,K.A. and Shi,P.Y. (2003) Functional analysis of mosquito-borne flavivirus conserved sequence elements within 3′ untranslated region of West Nile virus by use of a reporting replicon that differentiates between viral translation and RNA replication. J. Virol., 77, 10004-10014.
63. Alvarez,D.E., Lodeiro,M.F., Luduena,S.J., Pietrasanta,L.I. and Gamarnik,A.V. (2005) Long-range RNA-RNA interactions circularize the dengue virus genome. J. Virol., 79, 6631-6643.
64. Filomatori,C.V., Lodeiro,M.F., Alvarez,D.E., Samsa,M.M., Pietrasanta,L. and Gamarnik,A.V. (2006) A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome Genes Dev., 20, 2238-2249.