An ATPase activity associated with the rotavirus phosphoprotein NSP5

Virology

Volumn 369, Issue 2, 2007, Pages 389-399

  Bar Magen, Tamara ^a,b   Spencer, Eugenio ^a   Patton, John T ^b  

^a UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

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

Author keywords

ATPase; NSP5; Phosphoprotein; Rotavirus

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; CASEIN KINASE; MAGNESIUM; PHOSPHOPROTEIN; PROTEIN NSP2; PROTEIN NSP5; SERINE; THREONINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; ENZYME ACTIVITY; GENE REPLICATION; HYDROLYSIS; ISOMER; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ROTAVIRUS; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CA(2+) MG(2+)-ATPASE; DNA PRIMERS; DNA, VIRAL; HUMANS; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; RECOMBINANT PROTEINS; RNA, VIRAL; RNA-BINDING PROTEINS; ROTAVIRUS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; VIRAL NONSTRUCTURAL PROTEINS;

ROTAVIRUS;

EID: 36148956609     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.07.029     Document Type: Article

References (45)

1. Afrikanova I., Miozzo M., Giambiagi S., and Burrone O. Phosphorylation generates different forms of rotavirus NSP5. J. Gen. Virol. 77 (1996) 2059-2065
2. Afrikanova I., Fabbretti E., Miozzo M., and Burrone O. Rotavirus NSP5 phosphorylation is up-regulated by interaction with NSP2. J. Gen. Virol. 79 (1998) 2679-2686
3. Arnoldi F., Campagna M., Eichwald C., Desselberger U., and Burrone O.R. Interaction of rotavirus polymerase VP1 with nonstructural protein NSP5 is stronger than that with NSP2. J. Virol. 81 (2007) 2128-2137
4. Berois M., Sapin C., Erk I., Poncet D., and Cohen J. Rotavirus nonstructural protein NSP5 interacts with major core protein VP2. J. Virol. 77 (2003) 1757-1763
5. Blackhall J., Fuentes A., Hansen K., and Magnusson G. Serine protein kinase activity associated with rotavirus phosphoprotein NSP5. J. Virol. 71 (1997) 138-144
6. Blackhall J., Munoz M., Fuentes A., and Magnusson G. Analysis of rotavirus nonstructural protein NSP5 phosphorylation. J. Virol. 72 (1998) 6398-6405
7. Carpio R.V., Gonzalez-Nilo F.D., Jayaram H., Spencer E., Prasad B.V., Patton J.T., and Taraporewala Z.F. Role of the histidine triad-like motif in nucleotide hydrolysis by the rotavirus RNA-packaging protein NSP2. J. Biol. Chem. 279 (2004) 10624-10633
8. Clari G., and Moret V. Phosphorylation of membrane proteins by cytosolic casein kinases in human erythrocytes. Effect of monovalent ions, 2,3-bisphosphoglycerate and spermine. Mol. Cell. Biochem. 68 (1985) 181-187
9. de la Cruz J., Kressler D., and Linder P. Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem. Sci. 24 (1999) 192-198
10. Eichwald C., Vascotto F., Fabbretti E., and Burrone O.R. Rotavirus NSP5: mapping phosphorylation sites and kinase activation and viroplasm localization domains. J. Virol. 76 (2002) 3461-3470
11. Eichwald C., Jacob G., Muszynski B., Allende J.E., and Burrone O.R. Uncoupling substrate and activation functions of rotavirus NSP5: phosphorylation of Ser-67 by casein kinase 1 is essential for hyperphosphorylation. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 16304-16309
12. Estes M.K. Rotaviruses and their replication. In: Howley P.M. (Ed). Fields Fundamental Virology. 4th ed. vol. 2 (2001), Lippincott Williams & Wilkins Press, Philadelphia 1747-1785
13. Fabbretti E., Afrikanova I., Vascotto F., and Burrone O. Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J. Gen. Virol. 80 (1999) 333-339
14. Gonzalez S., and Burrone O. Rotavirus NS26 is modified by addition of single O-linked residues of N-acetylglucosamine. Virology 182 (1991) 8-16
15. Gonzalez R., Espinosa R., Romero P., Lopez S., and Arias C. Relative localization of viroplasmic and endoplasmic reticulum-resident rotavirus proteins in infected cells. Arch. Virol. 145 (2000) 1963-1973
16. Gwack Y., Yoo H., Song I., Choe J., and Han J.H. RNA-stimulated ATPase and RNA helicase activities and RNA binding domain of hepatitis G virus nonstructural protein 3. J. Virol. 73 (1999) 2909-2915
17. Imai M., Akatani K., Ikegami N., and Furuichi Y. Capped and conserved terminal structures in human rotavirus genome double-stranded RNA segments. J. Virol. 47 (1983) 125-136
18. Jayaram H., Taraporewala Z., Patton J., and Prasad B. Rotavirus protein involved in genome replication and packaging exhibits a HIT-like fold. Nature 417 (2002) 311-315
19. Jiang X., Jayaram H., Kumar M., Ludtke S.J., Estes M.K., and Prasad B.V.V. Cryoelectron microscopy structures of rotavirus NSP2-NSP5 and NSP2-RNA complexes: implications for genome replication. J. Virol. 80 (2006) 10829-10835
20. Kainov D.E., Tuma R., and Mancini E.J. Hexameric molecular motors: P4 packaging ATPase unravels the mechanism. Cell. Mol. Life Sci. 63 (2006) 1095-1105
21. Kuang W.F., Lin Y.C., Jean F., Huang Y.W., Tai C.L., Chen D.S., Chen P.J., and Hwang L.H. Hepatitis C virus NS3 RNA helicase activity is modulated by the two domains of NS3 and NS4A. Biochem. Biophys. Res. Commun. 317 (2004) 211-217
22. Kumar, M., Jayaram, H., Vasquez del Carpio, R., Jiang, X., Jacobson, R.H., Patton, J.T., Prasad, B.V.V., in press. Crystallographic and biochemical analysis of rotavirus NSP2 with nucleotides reveals NDP kinase like activity. J. Virol.
23. Mohan K.V.K., Miller J., and Atreya C.D. The N- and C-terminal regions of rotavirus NSP5 are the critical determinants for the formation of viroplasm-like structures independent of NSP2. J. Virol. 77 (2003) 12184-12192
24. Noble S., and Nibert M. Core protein mu2 is a second determinant of nucleoside triphosphatase activities by reovirus cores. J. Virol. 71 (1997) 7728-7735
25. Parashar U., Hummelman E., Bresee J., Miller M., and Glass R. Global illness and deaths caused by rotavirus disease in children. Emerg. Infect. Dis. 9 (2003) 565-572
26. Patel S.S., and Donmez I. Mechanisms of helicases. J. Biol. Chem. 281 (2006) 18265-18268
27. Patton J.T. Rotavirus VP1 alone specifically binds to the 3′ end of viral mRNA, but the interaction is not sufficient to initiate minus-strand synthesis. J. Virol. 70 (1996) 7940-7947
28. Prasad B., Wang G., Clerx J., and Chiu W. Three-dimensional structure of rotavirus. J. Mol. Biol 199 (1988) 269-275
29. Rubin H. The logic of the membrane, magnesium, mitosis (MMM) model for the regulation of animal cell proliferation. Arch. Biochem. Biophys. 458 (2007) 16-23
30. Schapiro F.B., and Grinstein S. Determinants of the pH of the Golgi complex. J. Biol. Chem. 275 (2000) 21025-21032
31. Silvestri L.S., Taraporewala Z.F., and Patton J.T. Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 78 (2004) 7763-7774
32. Suzuki H., Kutsuzawa T., Konno T., Ebina T., and Ishida N. Morphogenesis of human rotavirus type 2 Wa strain in MA104 cells. Arch. Virol. 70 (1981) 33-41
33. Taraporewala Z.F., and Patton J.T. Identification and characterization of the helix-destabilizing activity of rotavirus nonstructural protein NSP2. J. Virol. 75 (2001) 4519-4527
34. Taraporewala Z., and Patton J. Nonstructural proteins involved in genome packaging and replication of rotaviruses and other members of the Reoviridae. Virus Res. 101 (2004) 57-66
35. Taraporewala Z., Chen D., and Patton J.T. Multimers formed by the rotavirus nonstructural protein NSP2 bind to RNA and have nucleoside triphosphatase activity. J. Virol. 73 (1999) 9934-9943
36. Taraporewala Z., Chen D., and Patton J. Multimers of the bluetongue virus nonstructural protein, NS2, possess nucleotidyl phosphatase activity: similarities between NS2 and rotavirus NSP2. Virology 280 (2001) 221-231
37. Taraporewala Z.F., Schuck P., Ramig R.F., Silvestri L., and Patton J.T. Analysis of a temperature-sensitive mutant rotavirus indicates that NSP2 octamers are the functional form of the protein. J. Virol. 76 (2002) 7082-7093
38. Taraporewala Z.F., Jiang X., Vasquez-Del Carpio R., Jayaram H., Prasad B.V., and Patton J.T. Structure-function analysis of rotavirus NSP2 octamer by using a novel complementation system. J. Virol. 80 (2006) 7984-7994
39. Taylor J., O'Brien J., and Yeager M. The cytoplasmic tail of NSP4, the endoplasmic reticulum-localized non-structural glycoprotein of rotavirus, contains distinct virus binding and coiled coil domains. EMBO J. 15 (1996) 4469-4476
40. 2+ from the endoplasmic reticulum. J. Virol. 69 (1995) 5763-5772
41. Torres-Vega M.A., Gonzalez R.A., Duarte M., Poncet D., Lopez S., and Aria C.F. The C-terminal domain of rotavirus NSP5 is essential for its multimerization, hyperphosphorylation and interaction with NSP6. J. Gen. Virol. 81 (2000) 821-830
42. Vasquez-Del Carpio R., Gonzalez-Nilo F., Riadi G., Taraporewala Z., and Patton J. Histidine triad-like motif of the rotavirus NSP2 octamer mediates both RTPase and NTPase activities. J. Mol. Biol. 362 (2006) 539-554
43. Vende P., Taraporewala Z.F., and Patton J.T. RNA-binding activity of the rotavirus phosphoprotein NSP5 includes affinity for double-stranded RNA. J. Virol. 76 (2002) 5291-5299
44. Yeager M., Dryden K., Olson N., Greenberg H., and Baker T. Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J. Cell Biol. 110 (1990) 2133-2144
45. Yon C., Teramoto T., Mueller N., Phelan J., Ganesh V.K., Murthy K.H., and Padmanabhan R. Modulation of the nucleoside triphosphatase/RNA helicase and 5′-RNA triphosphatase activities of Dengue virus type 2 nonstructural protein 3 (NS3) by interaction with NS5, the RNA-dependent RNA polymerase. J. Biol. Chem. 280 (2005) 27412-27419