Crystallographic analysis reveals Octamerization of viroplasm matrix protein P9-1 of rice black streaked dwarf virus

Journal of Virology

Volumn 86, Issue 2, 2012, Pages 746-756

  Akita, Fusamichi ^a   Higashiura, Akifumi ^b   Shimizu, Takumi ^a   Pu, Yingying ^a,c   Suzuki, Mamoru ^b   Uehara Ichiki, Tamaki ^a   Sasaya, Takahide ^a   Kanamaru, Shuji ^d   Arisaka, Fumio ^d   Tsukihara, Tomitake ^b,e   Nakagawa, Atsushi ^b   Omura, Toshihiro ^a  

^a NATIONAL AGRICULTURAL RESEARCH CENTER   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c PEKING UNIVERSITY   (China)

^d TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^e UNIVERSITY OF HYOGO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; P9 1 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; OCTAMERIZATION; OLIGOMERIZATION; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; REOVIRUS; RICE BLACK STREAKED DWARF VIRUS; STRUCTURE ANALYSIS; VIROPLASM; VIRUS MORPHOLOGY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PLANT DISEASES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; REOVIRIDAE; SEQUENCE ALIGNMENT; VIRAL MATRIX PROTEINS;

REOVIRIDAE; RICE BLACK STREAKED DWARF VIRUS; ROTAVIRUS;

EID: 84863115713     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00826-11     Document Type: Article

References (54)

1. Adams P, et al. 2002. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58:1948-1954.
2. Afonine PV, et al. 2010. Joint X-ray and neutron refinement with phenix. refine. Acta Crystallogr. D Biol. Crystallogr. 66:1153-1163.
3. Azuhata F, Uyeda I, Kimura I, Shikata E. 1993. Close similarity between genome structures of rice black-streaked dwarf and maize rough dwarf viruses. J. Gen. Virol. 74:1227-1232.
4. Baker N, Sept D, Joseph S, Holst M, McCammon J. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U. S. A. 98:10037-10041.
5. Broering T, Parker J, Joyce P, Kim J, Nibert M. 2002. Mammalian reovirus nonstructural protein microNS forms large inclusions and colocalizes with reovirus microtubule-associated protein micro2 in transfected cells. J. Virol. 76:8285-8297.
6. Brookes SM, Hyatt AD, Eaton BT. 1993. Characterization of virus inclusion bodies in bluetongue virus-infected cells. J. Gen. Virol. 74: 525-530.
7. Butan C, Van Der Zandt H, Tucker P. 2004. Structure and assembly of the RNA binding domain of bluetongue virus non-structural protein 2. J. Biol. Chem. 279:37613-37621.
8. Collaborative Computational Project N. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
9. Davis IW, Murray LW, Richardson JS, Richardson DC. 2004. MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32:W615-W619.
10. DeLano WL. 2008. The PyMOL molecular graphics system. DeLano Scientific LLC, San Carlos, CA. http://www.pmol.org.
11. Eaton B, Hyatt A, White J. 1987. Association of bluetongue virus with the cytoskeleton. Virology 157:107-116.
12. Eichwald C, Rodriguez JF, Burrone OR. 2004. Characterization of rotavirus NSP2/NSP5 interactions and the dynamics of viroplasm formation. J. Gen. Virol. 85:625-634.
13. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
14. Fabbretti E, Afrikanova I, Vascotto F, Burrone OR. 1999. Two nonstructural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J. Gen. Virol. 80:333-339.
15. Gouet P, Robert X, Courcelle E. 2003. ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31:3320-3323.
16. Hartley J. 2003. Use of the gateway system for protein expression in multiple hosts. Curr. Protoc. Protein Sci. Chapter 5:Unit 5.17.
17. Isogai M, Uyeda I, Lee BC. 1998. Detection and assignment of proteins encoded by rice black streaked dwarf fijivirus S7, S8, S9 and S10. J. Gen. Virol. 79:1487-1494.
18. Jayaram H, Taraporewala Z, Patton JT, Prasad BVV. 2002. Rotavirus protein involved in genome replication and packaging exhibits a HIT-like fold. Nature 417:311-315.
19. Jiang XF, et al. 2006. Cryoelectron microscopy structures of rotavirus NSP2-NSP5 and NSP2-RNA complexes: implications for genome replication. J. Virol. 80:10829-10835.
20. Kattoura MD, Chen X, Patton JT. 1994. The rotavirus RNA-binding protein NS35 (NSP2) forms 10S multimers and interacts with the viral RNA polymerase. Virology 202:803-813.
21. Kobayashi T, Chappell JD, Danthi P, Dermody TS. 2006. Gene-specific inhibition of reovirus replication by RNA interference. J. Virol. 80: 9053-9063.
22. Kumar M, et al. 2007. Crystallographic and biochemical analysis of rotavirus NSP2 with nucleotides reveals a nucleoside diphosphate kinaselike activity. J. Virol. 81:12272-12284.
23. Liu HJ, Wei CH, Zhong YW, Li Y. 2007. Rice black-streaked dwarf virus outer capsid protein P10 has self-interactions and forms oligomeric complexes in solution. Virus Res. 127:34-42.
24. López T, Rojas M, Ayala-Breton C, López S, Arias CF. 2005. Reduced expression of the rotavirus NSP5 gene has a pleiotropic effect on virus replication. J. Gen. Virol. 86:1609-1617.
25. Maroniche GA, et al. 2010. Functional and biochemical properties of Mal de Río Cuarto virus (Fijivirus, Reoviridae) P9-1 viroplasm protein show further similarities to animal reovirus counterparts. Virus Res. 152: 96-103.
26. McNulty M, Curran W, McFerran J. 1976. The morphogenesis of a cytopathic bovine rotavirus in Madin-Darby bovine kidney cells. J. Gen. Virol. 33:503-508.
27. Mertens PPC, Attoui H, Duncan R, Dermody TS. 2005. Reoviridae, p 447-454. In Fauquest CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (ed), Virus taxonomy: eighth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, United Kingdom.
28. Miller C, Arnold M, Broering T, Hastings C, Nibert M. 2010. Localization of mammalian orthoreovirus proteins to cytoplasmic factory-like structures via nonoverlapping regions of microNS. J. Virol. 84:867-882.
29. Miyazaki N, et al. 2005. Transcapsidation and the conserved interactions of two major structural proteins of a pair of phytoreoviruses confirm the mechanism of assembly of the outer capsid layer. J. Mol. Biol. 345: 229-237.
30. Murshudov G, Vagin A, Dodson E. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
31. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
32. Pettersen E, et al. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
33. Prasad BVV, et al. 1996. Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus. Nature 382: 471-473.
34. Sharpe A, Chen L, Fields B. 1982. The interaction of mammalian reoviruses with the cytoskeleton of monkey kidney CV-1 cells. Virology 120: 399-411.
35. Shimizu T, Yoshii M, Wei T, Hirochika H, Omura T. 2009. Silencing by RNAi of the gene for Pns12, a viroplasm matrix protein of rice dwarf virus, results in strong resistance of transgenic rice plants to the virus. Plant Biotechnol. J. 7:24-32.
36. Silvestri LS, Taraporewala ZF, Patton JT. 2004. Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 78:7763-7774.
37. Supyani S, Hillman B, Suzuki N. 2007. Baculovirus expression of the 11 mycoreovirus-1 genome segments and identification of the guanylyltransferase-encoding segment. J. Gen. Virol. 88:342-350.
38. Suzuki N, Hosokawa D, Matsuura Y, Kikuchi A, Omura T. 1999. In vivo and in vitro phosphorylation of rice dwarf phytoreovirus Pns12 cytoplasmic nonstructural protein. Arch. Virol. 144:1371-1380.
39. Suzuki N, Sugawara M, Kusano T, Mori H, Matsuura Y. 1994. Immunodetection of rice dwarf phytoreoviral proteins in both insect and plant hosts. Virology 202:41-48.
40. Taraporewala ZF, Chen D, Patton JT. 1999. Multimers formed by the rotavirus nonstructural protein NSP2 bind to RNA and have nucleoside triphosphatase activity. J. Virol. 73:9934-9943.
41. Taraporewala ZF, Kumar M, Prasad BVV, Patton JT. 2008. Structure and function of the rotavirus NSP2 octamer, an essential component of the viroplasm, p 273-289. In Patton JT (ed), Segmented double-stranded RNA viruses: structure and molecular biology. Caister Academic Press, Norfolk, United Kingdom.
42. Taraporewala ZF, Patton JT. 2001. Identification and characterization of the helix-destabilizing activity of rotavirus nonstructural protein NSP2. J. Virol. 75:4519-4527.
43. Terwilliger T. 2003. Improving macromolecular atomic models at moderate resolution by automated iterative model building, statistical density modification and refinement. Acta Crystallogr. D Biol. Crystallogr. 59:1174-1182.
44. Terwilliger T, Berendzen J. 1999. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55:849-861.
45. Theron J, Huismans H, Nel LH. 1996. Site-specific mutations in the NS2 protein of epizootic haemorrhagic disease virus markedly affect the formation of cytoplasmic inclusion bodies. Arch. Virol. 141:1143-1151.
46. Thomas CP, Booth TF, Roy P. 1990. Synthesis of bluetongue virusencoded phosphoprotein and formation of inclusion bodies by recombinant baculovirus in insect cells: it binds the single-stranded RNA species. J. Gen. Virol. 71:2073-2083.
47. Touris-Otero F, Martínez-Costas J, Vakharia V, Benavente J. 2004. Avian reovirus nonstructural protein microNS forms viroplasm-like inclusions and recruits protein sigmaNS to these structures. Virology 319: 94-106.
48. Vasquez-Del Carpio R, Gonzalez-Nilo FD, Riadi G, Taraporewala ZF, Patton JT. 2006. Histidine triad-like motif of the rotavirus NSP2 octamer mediates both RTPase and NTPase activities. J. Mol. Biol. 362:539-554.
49. Wei T, et al. 2006. Pns12 protein of rice dwarf virus is essential for formation of viroplasms and nucleation of viral-assembly complexes. J. Gen. Virol. 87:429-438.
50. Wei T, Shimizu T, Omura T. 2008. Endomembranes and myosin mediate assembly into tubules of Pns10 of rice dwarf virus and intercellular spreading of the virus in cultured insect vector cells. Virology 372:349-356.
51. Zhang C, et al. 2008. Rice black streaked dwarf virus P9-1, an alphahelical protein, self-interacts and forms viroplasms in vivo. J. Gen. Virol. 89:1770-1776.
52. Zhang H, Chen J, Adams M. 2001. Molecular characterisation of segments 1 to 6 of rice black-streaked dwarf virus from China provides the complete genome. Arch. Virol. 146:2331-2339.
53. Zhang LD, et al. 2005. Two virus-encoded RNA silencing suppressors, P14 of beet necrotic yellow vein virus and S6 of rice black streak dwarf virus. Chin. Sci. Bull. 50:305-310.
54. Zhong B, et al. 2003. A minor outer capsid protein, P9, of rice dwarf virus. Arch. Virol. 148:2275-2280.