The structural and functional role of RNA in icosahedral virus assembly

Annual Review of Microbiology

Volumn 60, Issue , 2006, Pages 51-67

  Schneemann, Anette ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

(+)ssRNA; RNA folding; RNA packaging; Virus structure

Indexed keywords

COAT PROTEIN; RNA; SINGLE STRANDED RNA;

BEAN POD MOTTLE VIRUS; BROMOVIRUS; NODAVIRUS; NONHUMAN; PARIACOTO VIRUS; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN RNA BINDING; RED CLOVER NECROTIC MOSAIC VIRUS; REVIEW; RNA CONFORMATION; SATELLITE TOBACCO MOSAIC VIRUS; TOBACCO MOSAIC VIRUS; TOMBUSVIRUS; VIRION; VIRUS ASSEMBLY; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS PARTICLE; X RAY CRYSTALLOGRAPHY;

COMOVIRIDAE; MODELS, MOLECULAR; NODAVIRIDAE; NUCLEIC ACID CONFORMATION; RNA, VIRAL; TOBACCO MOSAIC SATELLITE VIRUS; VIRION; VIRUS ASSEMBLY;

EID: 33749462736     PISSN: 00664227     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.micro.60.080805.142304     Document Type: Review

References (53)

1. Abad-Zapatero C, Abdel-Meguid SS, Johnson JE, Leslie AGW, Rayment I, et al. 1980. Structure of southern bean mosaic virus at 2.8 Å resolution. Nature 286:33-39
2. Basnayake VR, Sit TL, Lommel SA. 2006. The genomic RNA packaging scheme of Red clover necrotic mosaic virus. Virology 345:532-39
3. Bertolotti-Ciarlet A, White LJ, Chen R, Prasad BV, Estes MK. 2002. Structural requirements for the assembly of Norwalk virus-like particles. J. Virol. 76:4044-55
4. Bothner B, Schneemann A, Marshall D, Reddy V, Johnson JE, Siuzdak G. 1999. Crystallographically identical virus capsids display different properties in solution. Nat. Struct. Biol. 6:114-16
5. Chen ZG, Stauffacher C, Li Y, Schmidt T, Bomu W, et al. 1989. Protein-RNA interactions in an icosahedral virus at 3.0 A resolution. Science 245:154-59
6. Choi YG, Rao AL. 2000. Packaging of tobacco mosaic virus subgenomic RNAs by Brome mosaic virus coat protein exhibits RNA controlled polymorphism. Virology 275:249-57
7. Dong XF, Natarajan P, Tihova M, Johnson JE, Schneemann A. 1998. Particle polymorphism caused by deletion of a peptide molecular switch in a quasi-equivalent virus. J. Virol. 72:6024-33
8. Felden B, Florentz C, McPherson A, Giege R. 1994. A histidine accepting tRNA-like fold at the 3′-end of satellite tobacco mosaic virus RNA. Nucleic Acids Res. 22:2882-86
9. Fisher AJ, Johnson JE. 1993. Ordered duplex RNA controls capsid architecture in an icosahedral animal virus. Nature 361:176-79
10. Frolova E, Frolov I, Schlesinger S. 1997. Packaging signals in alphaviruses. J. Virol. 71:248-58
11. Gallagher T, Rueckert RR. 1988. Assembly-dependent maturation cleavage in provirions of a small icosahedral insect ribovirus. J. Virol. 62:3399-406
12. Harrison SC, Olson AJ, Schutt CE, Winkler FK, Bricogne G. 1978. Tomato bushy stunt virus at 2.9 Å resolution. Nature 276:368-73
13. Herschlag D. 1995. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270:20871-74
14. Hogle JM, Chow M, Filman DJ. 1985. Three-dimensional structure of poliovirus at 2.9 Å resolution. Science 229:1358-65
15. Huang ZS, Wu HN. 1998. Identification and characterization of the RNA chaperone activity of hepatitis delta antigen peptides. J. Biol. Chem. 273:26455-61
16. Johnson JE, Rueckert RR. 1997. Packaging and release of the viral genome. In Structural Biology of Viruses, ed. W Chiu, RM Burnett, R Garcea, pp. 269-87. New York: Oxford Univ. Press
17. Johnson JM, Willits DA, Young MJ, Zlotnick A. 2004. Interaction with capsid protein alters RNA structure and the pathway for in vitro assembly of cowpea chlorotic mottle virus. J. Mol. Biol. 335:455-64
18. Johnson KN, Tang L, Johnson JE, Ball LA. 2004. Heterologous RNA encapsidated in Pariacoto virus-like particles forms a dodecahedral cage similar to genomic RNA in wild-type virions. J. Virol. 78:11371-78
19. Koning R, van den Worm S, Plaisier JR, van Duin J, Pieter Abrahams J, Koerten H. 2003. Visualization by cryo-electron microscopy of genomic RNA that binds to the protein capsid inside bacteriophage MS2. J. Mol. Biol. 332:415-22
20. Kramvis A, Kew MC. 1998. Structure and function of the encapsidation signal of hepadnaviridae. J. Viral. Hepat. 5:357-67
21. Krishna NK, Schneemann A. 1999. Formation of an RNA heterodimer upon heating of nodavirus particles. J. Virol. 73:1699-703
22. Krol MA, Olson NH, Tate J, Johnson JE, Baker TS, Ahlquist P. 1999. RNA-controlled polymorphism in the in vivo assembly of 180-subunit and 120-subunit virions from a single capsid protein. Proc. Natl. Acad. Sci. USA 96:13650-55
23. Larson SB, Day J, Greenwood A, McPherson A. 1998. Refined structure of satellite tobacco mosaic virus at 1.8 A resolution. J. Mol. Biol. 277:37-59
24. Larson SB, Koszelak S, Day J, Greenwood A, Dodds JA, McPherson A. 1993. Double helical RNA in satellite tobacco mosaic virus. Nature 361:179-82
25. Larson SB, Koszelak S, Day J, Greenwood A, Dodds JA, McPherson A. 1993. Three-dimensional structure of satellite tobacco mosaic virus at 2.9 A resolution. J. Mol. Biol. 231:375-91
26. Larson SB, Lucas RW, Greenwood A, McPherson A. 2005. The RNA of turnip yellow mosaic virus exhibits icosahedral order. Virology 334:245-54
27. Larson SB, McPherson A. 2001. Satellite tobacco mosaic virus RNA: structure and implications for assembly. Curr. Opin. Struct. Biol. 11:59-65
28. Li T, Chen Z, Johnson JE, Thomas GJJ. 1992. Conformations, interactions, and thermostabilities of RNA and proteins in bean pod mottle virus: investigation of solution and crystal structures by laser Raman spectroscopy. Biochemistry 31:6673-82
29. Li TS, Chen ZG, Johnson JE, Thomas GJJ. 1990. Structural studies of bean pod mottle virus in crystal and solution states by laser Raman spectroscopy. Biochemistry 29:5018-26
30. Lin T, Cavarelli J, Johnson JE. 2003. Evidence for assembly-dependent folding of protein and RNA in an icosahedral virus. Virology 314:26-33
31. Marshall D, Schneemann A. 2001. Specific packaging of nodaviral RNA2 requires the N-terminus of the capsid protein. Virology 285:165-75
32. Molenkamp R, Spaan WJM. 1997. Identification of a specific interaction between the coronavirus mouse hepatitis virus A59 nucleocapsid protein and packaging signal. Virology 239:78-86
33. Owen KE, Kuhn RJ. 1996. Identification of a region in the Sindbis virus nucleocapsid protein that is involved in specificity of RNA encapsidation. J. Virol. 70:2757-63
34. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. 2004. UCSF chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-12
35. Qu F, Morris TJ. 1997. Encapsidation of turnip crinkle virus is defined by a specific packaging signal and RNA size. J. Virol. 71:1428-35
36. Rein A, Henderson LE, Levin JG. 1998. Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem. Sci. 23:297-301
37. Rossmann MG, Arnold E, Erickson JW, Frankenberger EA, Griffith JP, et al. 1985. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317:145-53
38. Schmidt T, Johnson JE, Phillips WE. 1983. The spherically averaged structures of cowpea mosaic virus components by X-ray solution scattering. Virology 127:65-73
39. Schneemann A. 1992. Studies on assembly and maturation of flock house virus, a small insect ribovirus. PhD thesis. Univ. Wisconsin, Madison. 164 pp.
40. Schneemann A, Marshall D. 1998. Specific encapsidation of nodavirus RNA is mediated through the C terminus of capsid precursor protein alpha. J. Virol. 72:8738-46
41. Seifer M, Standring DN. 1995. Assembly and antigenicity of hepatitis B virus core particles. Intervirology 38:47-62
42. Tang L, Johnson KN, Ball LA, Lin T, Yeager M, Johnson JE. 2001. The structure of pariacoto virus reveals a dodecahedral cage of duplex RNA. Nat. Struct. Biol. 8:77-83
43. Tellinghuisen TL, Kuhn RJ. 2000. Nucleic acid-dependent cross-linking of the nucleocapsid protein of Sindbis virus. J. Virol. 74:4302-9
44. Tihova M, Dryden KA, Le TV, Harvey SC, Johnson JE, et al. 2004. Nodavirus coat protein imposes dodecahedral RNA structure independent of nucleotide sequence and length. J. Virol. 78:2897-905
45. Timmins PA, Wild D, Witz J. 1994. The three-dimensional distribution of RNA and protein in the interior of tomato bushy stunt virus: a neutron low-resolution single-crystal diffraction study. Structure 2:1191-201
46. Tompa P, Csermely P. 2004. The role of structural disorder in the function of RNA and protein chaperones. FASEB J. 18:1169-75
47. Valegard K, Murray JB, Stockley PG, Stonehouse NJ, Liljas L. 1994. Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature 371:623-26
48. Venter PA, Krishna NK, Schneemann A. 2005. Capsid protein synthesis from replicating RNA directs specific packaging of the genome of a multipartite, positive-strand RNA virus. J. Virol. 79:6239-48
49. Wery JP, Reddy VS, Hosur MV, Johnson JE. 1994. The refined three-dimensional structure of an insect virus at 2.8 A resolution. J. Mol. Biol. 235:565-86
50. Woodson SA. 2000. Compact but disordered states of RNA. Nat. Struct. Biol. 7:349-52
51. Zhao X, Fox JM, Olson NH, Baker TS, Young MJ. 1995. In vitro assembly of cowpea chlorotic mottle virus from coat protein expressed in Escherichia coli and in vitro-transcribed viral cDNA. Virology 207:486-94
52. Bink HHJ, Pleij CWA. 2002. RNA-protein interactions in spherical viruses. Arch. Virol. 147:2261-79
53. Prasad BV, Prevelige PE Jr. 2003. Viral genome organization. Adv. Protein Chem. 64:219-58