Crystallographic analysis of rotavirus NSP2-RNA complex reveals specific recognition of 5' GG sequence for RTPase activity

Journal of Virology

Volumn 86, Issue 19, 2012, Pages 10547-10557

  Hu, Liya ^a   Chow, Dar Chone ^a   Patton, John T ^b   Palzkill, Timothy ^a,b   Estes, Mary K ^a   Prasada, B V Venkataram ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA PHOSPHATE; NONSTRUCTURAL PROTEIN 2; NUCLEOSIDE TRIPHOSPHATASE; OLIGORIBONUCLEOTIDE; PHOSPHATE; UNCLASSIFIED DRUG; VIRUS RNA;

5' UNTRANSLATED REGION; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; CRYSTALLOGRAPHY; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SUBSTRATE; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN RNA BINDING; RNA SEQUENCE; ROTAVIRUS; SURFACE PLASMON RESONANCE;

BASE SEQUENCE; CATALYTIC DOMAIN; COMPUTER SIMULATION; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; GENE DELETION; GENOME, VIRAL; HYDROGEN BONDING; HYDROLYSIS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NUCLEOSIDE-TRIPHOSPHATASE; OPEN READING FRAMES; PROTEIN STRUCTURE, TERTIARY; RNA; RNA-BINDING PROTEINS; ROTAVIRUS; VIRAL NONSTRUCTURAL PROTEINS;

ROTAVIRUS; ROTAVIRUS A;

EID: 84867848667     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01201-12     Document Type: Article

References (42)

1. Adams PD, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221.
2. Aponte C, Poncet D, Cohen J. 1996. Recovery and characterization of a replicase complex in rotavirus-infected cells by using a monoclonal antibody against NSP2. J. Virol. 70:985-991.
3. Arnoldi F, Campagna M, Eichwald C, Desselberger U, Burrone OR. 2007. Interaction of rotavirus polymerase VP1 with nonstructural protein NSP5 is stronger than that with NSP2. J. Virol. 81:2128-2137.
4. Brunger AT, et al. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
5. Chen D, Luongo CL, Nibert ML, Patton JT. 1999. Rotavirus open cores catalyze 5'-capping and methylation of exogenous RNA: evidence that VP3 is a methyltransferase. Virology 265:120-130.
6. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501.
7. Estes MK, Greenberg HB. Rotaviruses. In Knipe DM, et al. (ed), Fields virology, 6th ed, in press. Lippincott/The Williams & Wilkins Co, Philadelphia, PA.
8. Fukuhara N, Nishikawa K, Gorziglia M, Kapikian AZ. 1989. Nucleotide sequence of gene segment 1 of a porcine rotavirus strain. Virology 173: 743-749.
9. Imai M, Akatani K, Ikegami N, Furuichi Y. 1983. Capped and conserved terminal structures in human rotavirus genome double-stranded RNA segments. J. Virol. 47:125-136.
10. Jayaram H, Taraporewala Z, Patton JT, Prasad BV. 2002. Rotavirus protein involved in genome replication and packaging exhibits a HIT-like fold. Nature 417:311-315.
11. Jiang X, et al. 2006. Cryoelectron microscopy structures of rotavirus NSP2-NSP5 and NSP2-RNA complexes: implications for genome replication. J. Virol. 80:10829-10835.
12. 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.
13. Kattoura MD, Clapp LL, Patton JT. 1992. The rotavirus nonstructural protein, NS35, possesses RNA-binding activity in vitro and in vivo. Virology 191:698-708.
14. 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.
15. Lawton JA, Estes MK, Prasad BV. 1997. Three-dimensional visualization of mRNA release from actively transcribing rotavirus particles. Nat. Struct. Biol. 4:118-121.
16. Li Z, Baker ML, Jiang W, Estes MK, Prasad BV. 2009. Rotavirus architecture at subnanometer resolution. J. Virol. 83:1754-1766.
17. Liu M, Mattion NM, Estes MK. 1992. Rotavirus VP3 expressed in insect cells possesses guanylyltransferase activity. Virology 188:77-84.
18. Lu X, et al. 2008. Mechanism for coordinated RNA packaging and genome replication by rotavirus polymerase VP1. Structure 16:1678-1688.
19. McCoy AJ, et al. 2007. PHASER crystallographic software. J. Appl. Crystallogr. 40:658-674.
20. McCrae MA, McCorquodale JG. 1983. Molecular biology of rotaviruses. V. Terminal structure of viral RNA species. Virology 126:204-212.
21. Miller KH, Karr JR, Marqusee S. 2010. A hinge region cis-proline in ribonuclease A acts as a conformational gatekeeper for C-terminal domain swapping. J. Mol. Biol. 400:567-578.
22. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode, In Carter CW, Jr, Sweet RM (ed), Methods in enzymology, vol 276, p 307-326. Academic Press, New York, NY.
23. Patton JT, Silvestri LS, Tortorici MA, Vasquez-Del Carpio R, Taraporewala ZF. 2006. Rotavirus genome replication and morphogenesis: role of the viroplasm. Curr. Top. Microbiol. Immunol. 309:169-187.
24. Pettersen EF, et al. 2004. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
25. Pflugrath JW. 1999. The finer things in X-ray diffraction data collection. Acta Crystallogr. D Biol. Crystallogr. 55:1718-1725.
26. Prasad BV, et al. 1996. Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus. Nature 382:471-473.
27. Rousseau F, Schymkowitz JW, Wilkinson HR, Itzhaki LS. 2001. Threedimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues. Proc. Natl. Acad. Sci. U. S. A. 98:5596-5601.
28. Schmidt A, et al. 2009. 5'-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc. Natl. Acad. Sci. U. S. A. 106:12067-12072.
29. Schrödinger. 2010. The PyMOL molecular graphics system, v1.3. Schrödinger, LLC, Munich, Germany.
30. Schuck P, Taraporewala Z, McPhie P, Patton JT. 2001. Rotavirus nonstructural protein NSP2 self-assembles into octamers that undergo ligandinduced conformational changes. J. Biol. Chem. 276:9679-9687.
31. Settembre EC, Chen JZ, Dormitzer PR, Grigorieff N, Harrison SC. 2011. Atomic model of an infectious rotavirus particle. EMBO J. 30:408-416.
32. Taraporewala Z, 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.
33. Taraporewala ZF, et al. 2006. Structure-function analysis of rotavirus NSP2 octamer by using a novel complementation system. J. Virol. 80: 7984-7994.
34. Taraporewala ZF, Patton JT. 2001. Identification and characterization of the helix-destabilizing activity of rotavirus nonstructural protein NSP2. J. Virol. 75:4519-4527.
35. Tortorici MA, Broering TJ, Nibert ML, Patton JT. 2003. Template recognition and formation of initiation complexes by the replicase of a segmented double-stranded RNA virus. J. Biol. Chem. 278:32673-32682.
36. Trask SD, Ogden KM, Patton JT. Interactions among capsid proteins orchestrate rotavirus particle functions. Curr. Opin. Virol. in press.
37. 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.
38. Wallace AC, Laskowski RA, Thornton JM. 1995. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8:127-134.
39. Wentz MJ, Patton JT, Ramig RF. 1996. The 3'-terminal consensus sequence of rotavirus mRNA is the minimal promoter of negative-strand RNA synthesis. J. Virol. 70:7833-7841.
40. Wentz MJ, Zeng CQ, Patton JT, Estes MK, Ramig RF. 1996. Identification of the minimal replicase and the minimal promoter of negativestrand synthesis, functional in rotavirus RNA replication in vitro. Arch. Virol. Suppl. 12:59-67.
41. Winn MD, et al. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67:235-242.
42. Yoneyama M, Fujita T. 2009. RNA recognition and signal transduction by RIG-I-like receptors. Immunol. Rev. 227:54-65.