Further characterisation of rotavirus cores: Ss(+)RNAs can be packaged in vitro but packaging lacks sequence specificity

Virus Research

Volumn 178, Issue 2, 2013, Pages 252-263

  Desselberger, Ulrich ^a,b,c   Richards, James ^c,d   Tchertanov, Luba ^a,e   Lepault, Jean ^a   Lever, Andrew ^c   Burrone, Oscar ^b   Cohen, Jean ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e Ecole Normale Superieure de Cachan   (France)

Author keywords

RNA packaging in vitro; Rotavirus; Rotavirus cores

Indexed keywords

CALCIUM ION; COBALT; COBALTHEXAMINE; EGTAZIC ACID; GENOMIC RNA; MAGNESIUM ION; PROTEIN VP6; SPERMIDINE; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; BACULOVIRUS; CONTROLLED STUDY; IN VITRO STUDY; ISOTOPE LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA PACKAGING; RNA SEQUENCE; ROTAVIRUS; VIROGENESIS; VIRUS CORE; VIRUS INFECTION; VIRUS MORPHOLOGY; VIRUS PARTICLE;

HUMAN IMMUNODEFICIENCY VIRUS 2; ROTAVIRUS;

RNA PACKAGING IN VITRO; ROTAVIRUS; ROTAVIRUS CORES;

ANIMALS; CELL LINE; HAPLORHINI; RECOMBINANT PROTEINS; RNA, VIRAL; ROTAVIRUS; VIRAL PROTEINS; VIRUS ASSEMBLY;

EID: 84888203788     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2013.09.034     Document Type: Article

References (90)

1. Afrikanova I., Fabbretti E., Miozzo M.C., Burrone O.R. Rotavirus NSP5 phosphorylation is up-regulated by interaction with NSP2. J. Gen. Virol. 1998, 79:2679-2686.
2. Arnoldi F., Campagna M., Eichwald C., Desselberger U., Burrone O.R. Interaction of rotavirus polymerase VP1 with nonstructural protein NSP5 is stronger than that with NSP2. J. Virol. 2007, 81:2128-2137.
3. Bass D.M., Baylor M.R., Chen C., Mackow E.M., Brémont M., Greenberg H.B. Liposome-mediated transfection of intact viral particles reveals that plasma membrane penetration determines permissivity of tissue culture cells to rotavirus. J. Clin. Invest. 1992, 90:2313-2320.
4. Berois M., Sapin C., Erk I., Poncet D., Cohen J. Rotavirus non-structural protein NSP5 interacts with the major core protein VP2. J. Virol. 2003, 77:1757-1763.
5. Bican P., Cohen J., Charpilienne A., Scherrer R. Purification and characterization of bovine rotavirus cores. J. Virol. 1982, 43:1113-1117.
6. Campagna M., Eichwald C., Vascotto F., Burrone O.R. RNA interference of rotavirus segment 11 mRNA reveals the essential role of NSP5 in the virus replicative cycle. J. Gen. Virol. 2005, 86:1483-1489.
7. Charpilienne A., Nejmeddine M., Berois M., Parez N., Neumann E., Hewat E., Trugnan G., Cohen J. Individual rotavirus-like particles containing 120 molecules of fluorescent protein are visible in living cells. J. Biol. Chem. 2001, 276:29361-29367.
8. Charpilienne A., Lepault J., Rey F., Cohen J. Identification of rotavirus VP6 residues located at the interphase with VP2 that are essential for capsid assembly and transcriptase activity. J. Virol. 2002, 76:7822-7831.
9. Chen D., Ramig R.F. Rescue of infectivity by in vitro transcapsidation of rotavirus single-shelled particles. Virology 1993, 192:422-429.
10. Chen D., Ramig R.F. Rescue of infectivity by sequential in vitro transcapsidation of rotavirus core particles with inner capsid and outer capsid proteins. Virology 1993, 194:743-751.
11. Chen D.Y., Patton J.T. Rotavirus RNA replication requires a single-stranded 3' end for efficient minus-strand synthesis. J. Virol. 1998, 72:7387-7396.
12. Chen D.Y., Patton J.T. De novo synthesis of minus-strand RNA by the rotavirus RNA polymerase in a cell-free system involves a novel mechanism of initiation. RNA 2000, 6:1455-1467.
13. Chen D., Zeng C.Q.Y., Wentz M.J., Gorziglia M., Estes M.K., Ramig R.F. Template-dependent, in vitro replication of rotavirus RNA. J. Virol. 1994, 68:7030-7039.
14. Chen D.Y., Luongo C.L., Nibert M.L., Patton J.T. Rotavirus open cores catalyze 5'-capping and methylation of exogenous RNA: evidence that VP3 is a methyltransferase. Virology 1999, 265:120-130.
15. Cheung W., Gill M., Esposito A., Kaminski C.F., Courousse N., Chwetzoff S., Trugnan G., Keshavan N., Lever A., Desselberger U. Rotaviruses associate with cellular lipid droplet components to replicate in viroplasms, and compounds disrupting or blocking lipid droplets inhibit viroplasm formation and viral replication. J. Virol. 2010, 84:6782-6798.
16. Cohen J., Charpilienne A., Chilmonczyk S., Estes M.K. Nucleotide sequence of bovine rotavirus gene 1 and expression of the gene product in baculovirus. Virology 1989, 171:131-140.
17. Desselberger U., Manktelow E., Li W., Cheung W., Iturriza-Gómara M., Gray J. Rotaviruses and rotavirus vaccines. Br. Med. Bull. 2009, 90:37-51.
18. Eichwald C., Vascotto F., Fabbretti E., Burrone O.R. Rotavirus NSP5: Mapping phosphorylation sites and kinase activation and viroplasm localization domains. J. Virol. 2002, 76:3461-3470.
19. Eichwald C., Rodriguez J.F., Burrone O.R. Characterization of rotavirus NSP2/NSP5 interactions and the dynamics of viroplasm formation. J. Gen. Virol. 2004, 85:625-634.
20. Erk I., Huet J.C., Duarte M., Duquerroy S., Rey F., Cohen J., Lepault J. A zincion controls assembly and stability of the major capsid protein of rotavirus. J. Virol. 2003, 77:3595-3601.
21. Estes M.K., Greenberg H.B. Rotaviruses. Fields' Virology 2013, Lippincott, Williams and Wilkins, Philadelphia. 6th ed. D.M. Knipe, P.M. Howley, et al (Eds.).
22. Estes M.K., Graham D.Y., Smith E.M., Gerba C.P. Rotavirus stability and inactivation. J. Gen. Virol. 1979, 43:403-409.
23. Estrozi L.F., Settembre E.C., Goret G., McClain B., Zhang X., Chen J.Z., Grigorieff N., Harrison S.C. Location of the dsRNA-dependent polymerase, VP1, in rotavirus particles. J. Mol. Biol. 2013, 425:124-132.
24. Fabbretti E., Afrikanova I., Vascotto F., Burrone O.E. Two nonstructural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structure in vivo. J. Gen. Virol. 1999, 80:333-339.
25. Gallegos C.O., Patton J.T. Characterization of rotavirus replication intermediates: a model for the assembly of single-shelled particles. Virology 1989, 172:616-627.
26. Gastañaduy P.A., Sánchez-Uribe E., Esparza-Aguilar M., Desai R., Parashar U.D., Patel M., Richardson V. Effect of rotavirus vaccine on diarrhea mortality in different socioeconomic regions of Mexico. Pediatrics 2013, 131:e1115-e1120.
27. Gorziglia M.I., Collins P.L. Intracellular amplification and expression of a synthetic analog of rotavirus genomic RNA bearing a foreign marker gene: mapping cis-acting nucleotides in the 3'-noncoding region. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:5784-5788.
28. Gottlieb M., Chavko M. Silver staining of native and denatured eukaryotic DNA in agarose gels. Anal. Biochem. 1987, 165:33-37.
29. Graham A., Kudesia G., Allen A.M., Desselberger U. Reassortment of human rotavirus possessing genome rearrangements with bovine rotavirus: evidence for host cell selection. J. Gen.Virol. 1987, 68:115-122.
30. Kapahnke R., Rappold W., Desselberger U., Riesner D. The stiffness of dsRNA: hydrodynamic studies on fluorescence-labelled RNA segments of bovine rotavirus. Nucleic Acids Res. 1986, 14:3215-3228.
31. Kohli E., Pothier P., Tosser G., Cohen J., Sandino A.M., Spencer E. In vitro reconstitution of rotavirus transcriptional activity using viral cores and recombinant baculovirus expressed VP6. Arch. Virol. 1993, 133:451-458.
32. Kohli E., Pothier P., Tosser G., Cohen J., Sandino A.M., Spencer E. Inhibition of in vitro reconstitution of rotavirus transcriptionally active particles by anti-VP6 monoclonal antibodies. Arch. Virol. 1994, 135:193-200.
33. Komoto S., Sasaki J., Taniguchi K. Reverse genetics system for introduction of site-specific mutations into the double-stranded RNA genome of infectious rotavirus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(12):4646-4651.
34. Labbé M., Charpilienne A., Crawford S.E., Estes M.K., Cohen J. Expression of rotavirus VP2 produces empty corelike particles. J. Virol. 1991, 65:2946-2952.
35. Lawton J.A., Zeng C.Q., Mukherjee S.K., Cohen J., Estes M.K., Prasad B.V. Three-dimensional analysis of recombinant rotavirus-like particles with intact and amino-terminal-deleted VP2: implications for the architecture of the VP2 capsid layer. J. Virol. 1997, 71:7353-7360.
36. Lee L.A., Franzel L., Atwel, l J., Datta S.D., Friberg I.K., Goldie S.J., Reef S.E., Schwalbe N., Simons E., Strebel P.M., Sweet S., Suraratdecha C., Tam Y., Vynnycky E., Walker N., Walker D.G., Hansen P.M. The estimated mortality impact of vaccinations forecast to be administered during 2011-2020 in 73 countries supported by the GAVI Alliance. Vaccine 2013, 31(Suppl. 2):B61-B72.
37. Lepault J., Petitpas I., Erk I., Navaza J., Bigot D., Dona M., Vachette P., Cohen J., Rey F.A. Structural polymorphism of the major capsid protein of rotavirus. EMBO J. 2001, 20:1498-1507.
38. Loudon P.T., Roy P. Interaction of nucleic acids with core-like and subcore-like particles of bluetongue virus. Virology 1992, 191:231-236.
39. Lourenco S., Roy P. In vitro reconstitution of Bluetongue virus infectious cores. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:13746-13751.
40. Lu X., McDonald S.M., Tortorici M.A., Tao Y.J., Vasquez-Del Carpio R., Nibert M.L., Patton J.T., Harrison S.C. Mechanism for coordinated RNA packaging and genome replication by rotavirus polymerase VP1. Structure 2008, 16:1678-1688.
41. Matsuo E., Roy P. Bluetongue virus VP6 acts early in the replication cycle and can form the basis of chimeric virus formation. J. Virol. 2009, 83:8842-8848.
42. McClain B., Settembre E., Temple B.R., Bellamy A.R., Harrison S.C. X-ray crystal structure of the rotavirus inner capsid particle at 3.8Å resolution. J. Mol. Biol. 2010, 397:587-599.
43. McDonald S.M., Patton J.T. Assortment and packaging of the segmented rotavirus genome. Trends Microbiol. 2011, 19:136-144.
44. Mindich L. Precise packaging of the three genomic segments of the double-stranded-RNA bacteriophage phi6. Microbiol. Mol. Biol. Rev. 1999, 63:149-160.
45. Molla A., Paul A.V., Wimmer E. Cell-free, de novo synthesis of poliovirus. Science 1991, 254:1647-1651.
46. Naitow H., Canady M.A., Lin T., Wickner R.B., Johnson J.E. Purification, crystallization, and preliminary X-ray analysis of L-A: a dsRNA yeast virus. J. Struct. Biol. 2001, 135:1-7.
47. Ogden K.M., Ramanathan H.N., Patton J.T. Mutational analysis of residues involved in nucleotide and divalent cation stabilization in the rotavirus RNA-dependent RNA polymerase catalytic pocket. Virology 2012, 431:12-20.
48. Olkkonen V.M., Gottlieb P., Strassman J., Qiao X., Bamford D.H., Mindich L. In vitro assembly of infectious nucleocapsids of bacteriophage phi6: formation of a recombinant double-stranded RNA virus. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:9173-9177.
49. Parashar U.D., Hummelman E.G., Bresee J.S., Miller M.A., Glass R.I. Global illness and death caused by rotavirus disease in children. Emerg. Infect. Dis. 2003, 9:565-572.
50. Parashar U.D., Burton A., Lanata C., Boschi-Pinto C., Shibuya K., Steele D. Global mortality associated with rotavirus disease among children in 2004. J. Infect. Dis. 2009, 200(Suppl. 1):S9-S15.
51. Patel M.M., Glass R., Desai R., Tate J.E., Parashar U.D. Fulfilling the promise of rotavirus vaccines: how far have we come since licensure?. Lancet Infect Dis. 2012, 12:561-570.
52. Patton J.T. Rotavirus RNA replication and gene expression. Novartis Found. Symp. 2001, 238:64-81.
53. Patton J.T., Chen D.Y. RNA-binding and capping activities of proteins in rotavirus open cores. J. Virol. 1990, 73:1382-1390.
54. Patton J.T., Gallegos C.O. Rotavirus RNA replication: single-strand RNA extends from the replicase particle. J. Gen. Virol. 1990, 71:1087-1094.
55. Patton J.T., Wentz M., Xiaobo J., Ramig R.F. Cis-acting signals that promote genome replication in rotavirus mRNA. J. Virol. 1996, 70:3961-3971.
56. Patton J.T., Jones M.T., Kalbach A.N., He Y.W., Xiaobo J. Rotavirus RNA polymerase requires the core shell protein to synthesize the double-stranded RNA genome. J. Virol. 1997, 71:9618-9626.
57. Patton J.T., Chnaiderman J., Spencer E. Open reading frame in rotavirus mRNA specifically promotes synthesis of double-stranded RNA: template size also affects replication efficiency. Virology 1999, 264:167-180.
58. Patton J.T., Chizhikov V., Taraporewala Z., Chen D.Y. Virus replication. Rotaviruses. Methods and Protocols 2000, 33-66. Humana Press, Totowa, New Jersey. J. Gray, U. Desselberger (Eds.).
59. Patton J.T., Kearney K., Taraporewala Z. Rotavirus genome replication: role of RNA-binding proteins. Viral Gastroenteritis 2003, 165-183. Elsevier Science, Amsterdam. U. Desselberger, J. Gray (Eds.).
60. Pesavento J.B., Estes M.K., Prasad B.V.V. Structural organisation of the genome in rotavirus. Viral Gastroenteritis 2003, 115-127. Elsevier Science B.V, Amsterdam. U. Desselberger, J. Gray (Eds.).
61. Poranen M.M., Tuma R. Self-assembly of double-stranded RNA bacteriophages. Virus Res. 2004, 101:93-100.
62. Poranen M.M., Paatero A.O., Tuma R., Bamford D.H. Self-assembly of a viral molecular machine from purified protein and RNA constituents. Mol. Cell 2001, 7:845-854.
63. Prasad B.V., Wang G.J., Clerx J.P., Chiu W. Three-dimensional structure of rotavirus. J. Mol. Biol. 1988, 199:269-275.
64. Prasad B.V.V., Rothnagel R., Zeng C.Q.Y., Jakana J., Lawton J.A., Chiu W., Estes M.K. Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus. Nature 1996, 382:471-473.
65. Qiao X., Casini G., Qiao J., Mindich L. In vitro packaging of individual genomic segments of bacteriophage phi 6 RNA: serial dependence relationships. J. Virol. 1995, 169:2926-2931.
66. Qiao X., Qiao J., Mindich L. Stoichiometric packaging of the three genome segments of double-stranded RNA bacteriophage phi6. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:4074-4079.
67. Richards J.E., Desselberger U., Lever A.M. Experimental pathways towards developing a rotavirus reverse genetics system: synthetic full length rotavirus ssRNAs are neither infectious nor translated in permissive cells. PLoS One 2013, 8(9):e74328.
68. Schuck P., Taraporewala Z., McPhie P., Patton J.T. Rotavirus nonstructural protein NSP2 self-assembles into octamers that undergo ligand-induced conformational changes. J. Biol. Chem. 2001, 276:9679-9687.
69. Settembre E.C., Chen J.Z., Dormitzer P.R., Grigorieff N., Harrison S.C. Atomic model of an infectious rotavirus particle. EMBO J. 2011, 30:408-416.
70. Silvestri L.S., Taraporewala Z.F., Patton J.T. Rotavirus replication: Plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 2004, 78:7763-7774.
71. Soares-Weiser K., Maclehose H., Bergman H., Ben-Aharon I., Nagpal S., Goldberg E., Pitan F., Cunliffe N. Vaccines for preventing rotavirus diarrhoea: vaccines in use. Cochrane Database Syst. Rev. 2012, 11:CD008521.
72. Taraporewala Z., Patton J.T. Identification and characterization of the helix-destabilizing activity of the rotavirus nonstructural protein NSP2. J. Virol. 2001, 75:4519-4527.
73. Taraporewala Z., Chen D., Patton J.T. Multimers formed by the rotavirus nonstructural protein NSP2 bind to RNA and have nucleoside triphosphatase activity. J. Virol. 1999, 73:9934-9943.
74. Tate J.E., Burton A.H., Boschi-Pinto C., Steele A.D., Duque J., Parashar U.D. WHO-coordinated Global Rotavirus Surveillance Network 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 2012, 12(2):136-141.
75. Thouvenin E., Schoehn G., Rey F., Petitpas I., Mathieu M., Vaney M.C., Cohen J., Kohli E., Pothier P., Hewat E. Antibody inhibition of the transcriptase activity of the rotavirus DLP: a structural view. J. Mol. Biol. 2001, 307:161-172.
76. Torres-Vega M.A., Gonzalez R.A., Duarte M., Poncet D., Lopez S., Arias C.F. The C-terminal domain of rotavirus NSP5 is essential for its multimerization, hyperphosphorylation and interaction with NSP6. J. Gen. Virol. 2000, 81:821-830.
77. Tortorici M.A., Broering T.J., Nibert M.L., Patton J.T. Template recognition and formation of initiation complexes by the replicase of a segmented double-stranded RNA virus. J. Biol. Chem. 2003, 278:32673-32682.
78. Trask S.D., Dormitzer P.R. Assembly of highly infectious rotavirus particles recoated with recombinant outer capsid proteins. J. Virol. 2006, 80:11293-11304.
79. Trask S.D., Taraporewala Z.F., Boehme K.W., Dermody T.S., Patton J.T. Dual selection mechanisms drive efficient single-gene reverse genetics for rotavirus. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18652-18657.
80. Trask S.D., Ogden K.M., Patton J.T. Interactions among capsid proteins orchestrate rotavirus particle functions. Curr. Opin. Virol. 2012, 2:373-379.
81. Trask S.D., McDonald S.M., Patton J.T. Structural insights into the coupling of virion assembly and rotavirus replication. Nat. Rev. Microbiol. 2012, 10:165-177.
82. Troupin C., Dehée A., Schnuriger A., Vende P., Poncet D., Garbarg-Chenon A. Rearranged genomic RNA segments offer a new approach to the reverse genetics of rotaviruses. J. Virol. 2010, 84:6711-6719.
83. Vascotto F., Campagna M., Visintin M., Cattaneo A., Burrone O.R. Effects of intrabodies specific for rotavirus NSP5 during the virus replicative cycle. J. Gen. Virol. 2004, 85:3285-3290.
84. Vasquez-Del Carpio R., Gonzalez-Nilo F.D., Jayaram H., Spencer E., Prasad B.V.V., Patton J.T., Taraporewala Z.F. Role of the histidine triad-like motif in nucleotide hydrolysis by the rotavirus RNA-packaging protein NSP2. J. Biol. Chem. 2004, 279:10624-10630.
85. Wentz M.J., Patton J.T., Ramig R.F. The 3'-terminal consensus sequence of rotavirus mRNA is the minimal promoter of negative-strand RNA synthesis. J. Virol. 1996, 70:7833-7841.
86. Yeager M., Dryden K.A., Olson N.H., Greenberg H.B., Baker T.S. Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J. Cell Biol. 1990, 110:2133-2144.
87. Yen C., Tate J.E., Patel M.M., Cortese M.M., Lopman B., Fleming J., Lewis K., Jiang B., Gentsch J., Steele D., Parashar U.D. Rotavirus vaccines: update on global impact and future priorities. Hum. Vaccin. 2011, 7:1282-1290.
88. Young D.F., Andrejeva L., Livingstone A., Goodbourn S., Lamb R.A., Collins P.L., Elliott R.M., Randall R.E. Virus replication in engineered human cells that do not respond to interferons. J. Virol. 2003, 77:2174-2181.
89. Zeng C.Q., Labbe M., Cohen J., Prasad B.V., Chen D., Ramig R.F., Estes M.K. Characterization of rotavirus VP2 particles. Virology 1994, 201:55-65.
90. Zeng C.Q., Wentz M.J., Cohen J., Estes M.K., Ramig R.F. Characterization and replicase activity of double-layered and single-layered rotavirus-like particles expressed from baculovirus recombinants. J. Virol. 1996, 70:2736-2742.