Removal of divalent cations induces structural transitions in Red clover necrotic mosaic virus, revealing a potential mechanism for RNA release

Journal of Virology

Volumn 80, Issue 21, 2006, Pages 10395-10406

  Sherman, Michael B ^a,f   Guenther, Richard H ^b   Tama, Florence ^c   Sit, Tim L ^b   Brooks, Charles L ^c   Mikhailov, Albert M ^d   Orlova, Elena V ^e   Baker, Timothy S ^a,g   Lommel, Steven A ^b  

^a PURDUE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d SHUBNIKOV INSTITUTE OF CRYSTALLOGRAPHY   (Russian Federation)

^e UNIVERSITY OF LONDON   (United Kingdom)

^f University of Texas Medical Branch School of Medicine   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; DIVALENT CATION; MAGNESIUM ION; NUCLEASE; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATION TRANSPORT; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; MOSAIC VIRUS; NONHUMAN; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN STRUCTURE; RED CLOVER; RED CLOVER NECROTIC MOSAIC VIRUS; RNA ANALYSIS; SENSITIVITY ANALYSIS; TOMBUSVIRUS; VIRUS CAPSID; VIRUS MORPHOLOGY;

AMINO ACID SEQUENCE; CALCIUM; CAPSID; CAPSID PROTEINS; CATIONS, DIVALENT; CRYOELECTRON MICROSCOPY; ELECTROSTATICS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNESIUM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; RNA, VIRAL; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; TOMBUSVIRIDAE;

MIRIDAE; RED CLOVER NECROTIC MOSAIC VIRUS; TOMBUSVIRIDAE;

EID: 33750318283     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01137-06     Document Type: Article

References (55)

1. Aramayo, R., C. Merigoux, E. Larquet, P. Bron, J. Perez, C. Dumas, P. Vachette, and N. Boisset. 2005. Divalent ion-dependent swelling of Tomato Bushy Stunt Virus: a multi-approach study. Biochim. Biophys. Acta 1724:345-354.
2. Atkinson, M. M., L. D. Keppler, E. W. Orlandi, C. J. Baker, and C. F. Mischke. 1990. Involvement of plasma membrane calcium influx in bacterial induction of the K/H and hypersensitive responses in tobacco. Plant Physiol. 92:215-221.
3. Barber, S. A. 1995. Soil nutrient bioavailability, p. 271. Wiley-Interscience, New York, N.Y.
4. Basnayake, V. R., T. L. Sit, and S. A. Lommel. 2006. The genomic RNA packaging scheme of Red clover necrotic mosaic virus. Virology 345:532-539.
5. Bowman, V. D., E. S. Chase, A. W. Franz, P. R. Chipman, X. Zhang, K. L. Perry, T. S. Baker, and T. J. Smith. 2002. An antibody to the putative aphid recognition site on cucumber mosaic virus recognizes pentons but not hexons. J. Virol. 76:12250-12258.
6. Briggs, J. C., and J. F. Ficke. 1977. Quality of rivers of the United States, 1975 water year-based on the National Stream Quality Accounting Network (NASQAN). U.S. Geological Survey water-supply paper 1540-C.
7. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
8. Caldwell, P. C. 1970. Calcium chelation and buffers, p. 10-16. In A. W. Cuthbert (ed.), Calcium and cellular function. Macmillan, London, United Kingdom.
9. Caspar, D. L., and A. Klug. 1962. Physical principles in the construction of regular viruses. Cold Spring Harbor Symp. Quant. Biol. 27:1-24.
10. Clough, S. J., K. A. Fengler, I. C. Yu, B. Lippok, R. K. Smith, Jr., and A. F. Bent. 2000. The Arabidopsis dndl "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc. Natl. Acad. Sci. USA 97:9323-9328.
11. Desvoyes, B., and H. B. Scholthof. 2002. Host-dependent recombination of a Tomato bushy stunt virus coat protein mutant yields truncated capsid subunits that form virus-like complexes which benefit systemic spread. Virology 304:434-442.
12. Doan, D. N., K. C. Lee, P. Laurinmaki, S. Butcher, S. M. Wong, and T. Dokland. 2003. Three-dimensional reconstruction of hibiscus chlorotic ring-spot virus. J. Struct. Biol. 144:253-261.
13. Durham, A. C., D. A. Hendry, and M. B. Von Wechmar. 1977. Does calcium ion binding control plant virus disassembly? Virology 77:524-533.
14. Fishman, M. J., and S. C. Downs. 1966. Methods for analysis of selected metals in water by atomic absorption: U.S. Geological Survey water-supply paper 1540-C, p. C26-C28.
15. Hallett, F. R., J. Watton, and P. Krygsman. 1991. Vesicle sizing: number distributions by dynamic light scattering. Biophys. J. 59:357-362.
16. Hsu, C., P. Singh, W. Ochoa, D. J. Manayani, M. Manchester, A. Schneemann, and V. S. Reddy. 2006. Characterization of polymorphism displayed by the coat protein mutants of tomato bushy stunt virus. Virology 349:222-229.
17. Isea, R., C. Aponte, and R. Cipriani. 2004. Can the RNA of the cowpea chlorotic mottle virus be released through a channel by means of free diffusion? A test in silico. Biophys. Chem. 107:101-106.
18. Jones, T. A., J. Y. Zou, S. W. Cowan, and Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47(Pt. 2):110-119.
19. Larson, S. B., J. Day, A. Greenwood, and A. McPherson. 1998. Refined structure of satellite tobacco mosaic virus at 1.8 Å resolution. J. Mol. Biol. 277:37-59.
20. Larson, S. B., and A. McPherson. 2001. Satellite tobacco mosaic virus RNA: structure and implications for assembly. Curr. Opin. Struct. Biol. 11:59-65.
21. Lommel, S. A. 1983. Ph.D. dissertation. University California, Berkeley.
22. Luan, S., J. Kudla, M. Rodriguez-Concepcion, S. Yalovsky, and W. Gruissem. 2002. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14(Suppl.):S389-S400.
23. Lucas, R. W., S. B. Larson, M. A. Canady, and A. McPherson. 2002. The structure of tomato aspermy virus by X-ray crystallography. J. Struct. Biol. 139:90-102.
24. Montelius, I., L. Liljas, and T. Unge. 1988. Structure of EDTA-treated satellite tobacco necrosis virus at pH 6.5. J. Mol. Biol. 201:353-363.
25. Morgunova, E. Y., Z. Dauter, E. Fry, D. I. Stuart, V. Y. Stel'mashchuk, A. M. Mikhailov, K. S. Wilson, and B. K. Vainshtein. 1994. The atomic structure of Carnation Mottle Virus capsid protein. FEBS Lett. 338:267-271.
26. Musil, M., and J. Gallo. 1982. Serotypes of red clover necrotic mosaic virus. I. Characterization of three serotypes. Acta Virol. 26:497-501.
27. Oda, Y., K. Saeki, Y. Takahashi, T. Maeda, H. Naitow, T. Tsukihara, and K. Fukuyama. 2000. Crystal structure of tobacco necrosis virus at 2.25 Å resolution. J. Mol. Biol. 300:153-169.
28. Olson, A. J., G. Bricogne, and S. C. Harrison. 1983. Structure of tomato busy stunt virus. IV. The virus particle at 2.9 Å resolution. J. Mol. Biol. 171:61-93.
29. Opalka, N., M. Tihova, C. Brugidou, A. Kumar, R. N. Beachy, C. M. Fauquet, and M. Yeager. 2000. Structure of native and expanded sobemo-viruses by electron cryo-microscopy and image reconstruction. J. Mol. Biol. 303:197-211.
30. Orlova, E. V., M. B. Sherman, W. Chiu, H. Mowri, L. C. Smith, and A. M. Gotto. 1999. Three-dimensional structure of low density lipoproteins by electron cryomicroscopy. Proc. Natl. Acad. Sci. USA 96:8420-8425.
31. 2+ levels. Curr. Opin. Plant Biol. 6:257-262.
32. Poirot, O., K. Suhre, C. Abergel, E. O'Toole, and C. Notredame. 2004. 3DCoffee@igs: a web server for combining sequences and structures into a multiple sequence alignment. Nucleic Acids Res. 32:W37-W40.
33. Robinson, I. K., and S. C. Harrison. 1982. Structure of the expanded state of tomato bushy stunt virus. Nature 297:563-568.
34. Rochon, D., K. Kakani, M. Robbins, and R. Reade. 2004. Molecular aspects of plant virus transmission by olpidium and plasmodiophorid vectors. Annu. Rev. Phytopathol. 42:211-241.
35. Rosenthal, P. B., and R. Henderson. 2003. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333:721-745.
36. Rossmann, M. G., C. Abad-Zapatero, J. W. Erickson, and H. S. Savithri. 1983. RNA-protein interactions in some small plant viruses. J. Biomol. Struct. Dyn. 1:565-579.
37. Saxton, W. O., and W. Baumeister. 1982. The correlation averaging of a regularly arranged bacterial cell envelope protein. J. Microsc. 127:127-138.
38. Schwede, T., J. Kopp, N. Guex, and M. C. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
39. Serysheva, I. I., E. V. Orlova, W. Chiu, M. B. Sherman, S. L. Hamilton, and M. van Heel. 1995. Electron cryomicroscopy and angular reconstitution used to visualize the skeletal muscle calcium release channel. Nat. Struct. Biol. 2:18-24.
40. Speir, J. A., S. Munshi, G. Wang, T. S. Baker, and J. E. Johnson. 1995. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure 3:63-78.
41. Tama, F., F. X. Gadea, O. Marques, and Y. H. Sanejouand. 2000. Building-block approach for determining low-frequency normal modes of macromolecules. Proteins 41:1-7.
42. Tama, F., O. Miyashita, and C. L. Brooks III. 2004. Flexible multi-scale fitting of atomic structures into low-resolution electron density maps with elastic network normal mode analysis. J. Mol. Biol. 337:985-999.
43. Tama, F., and Y. H. Sanejouand. 2001. Conformational change of proteins arising from normal mode calculations. Protein Eng. 14:1-6.
44. Tang, L., K. N. Johnson, L. A. Ball, T. Lin, M. Yeager, and J. E. Johnson. 2001. The structure of pariacoto virus reveals a dodecahedral cage of duplex RNA. Nat. Struct. Biol. 8:77-83.
45. Tihova, M., K. A. Dryden, T. V. Le, S. C. Harvey, J. E. Johnson, M. Yeager, and A. Schneemann. 2004. Nodavirus coat protein imposes dodecahedral RNA structure independent of nucleotide sequence and length. J. Virol. 78:2897-2905.
46. van Heel, M. 1987. Angular reconstitution: a posteriori assignment of projection directions for 3D reconstruction. Ultramicroscopy 21:111-124.
47. van Heel, M., and J. Frank. 1981. Use of multivariate statistics in analysing the images of biological macromolecules. Ultramicroscopy 6:187-194.
48. van Heel, M., and G. Harauz. 1986. Resolution criteria for three dimensional reconstructions. Optik 73:119-122.
49. van Heel, M., G. Harauz, and E. V. Orlova. 1996. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116:17-24.
50. Wei, N., L. A. Heaton, T. J. Morris, and S. C. Harrison. 1990. Structure and assembly of turnip crinkle virus. VI. Identification of coat protein binding sites on the RNA. J. Mol. Biol. 214:85-95.
51. Wiener, N. 1949. Extrapolation, interpolation, and smoothing of stationary time series with engineering applications. The MIT Press, Cambridge, Mass.
52. Wriggers, W., and S. Birmanns. 2001. Using Situs for flexible and rigid-body fitting of multiresolution single-molecule data. J. Struct. Biol. 133:193-202.
53. Xiong, Z. G., and S. A. Lommel. 1991. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro. Virology 182:388-392.
54. Zhang, X., S. B. Walker, P. R. Chipman, M. L. Nibert, and T. S. Baker. 2003. Reovirus polymerase lambda 3 localized by cryo-electron microscopy of virions at a resolution of 7.6 Å. Nat. Struct. Biol. 10:1011-1018.
55. Zhou, Z. H., S. Hardt, B. Wang, M. B. Sherman, J. Jakana, and W. Chiu. 1996. CTF determination of images of ice-embedded single particles using a graphics interface. J. Struct. Biol. 116:216-222.