Skip to main content

Functions of the Rotavirus RNA Polymerase in Virus Replication

  • Chapter
  • First Online:
National Institute of Allergy and Infectious Diseases, NIH

Part of the book series: Infectious Disease ((ID))

  • 735 Accesses

Abstract

To achieve productive infection of a target cell, a virus must express viral proteins, replicate its genome, and assemble infectious particles. For many viruses with RNA genomes, all stages of RNA synthesis are mediated by a virus-encoded RNA-dependent RNA polymerase (RdRP). Viruses with a segmented, double-stranded (ds) RNA genome rely on the encoded RdRP to perform both transcription (dsRNA ® +RNA) and replication (+RNA ® dsRNA). For dsRNA viruses, the RdRP also plays an important role in recognizing and packaging the correct number and constellation of viral RNAs into progeny particles.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

–:

negative-sense

+:

positive-sense

3¢CS-:

3¢ CS of –RNA, 5¢-(A/U)7GCC-3¢

3¢CS+:

3¢ CS of +RNA, 5¢-UGUGACC-3¢

CS:

consensus sequence

DLP:

double-layered particle

ds:

double-stranded

N:

incoming nucleotide

NSP:

viral nonstructural protein

NTP:

nucleoside triphosphate

P:

priming

r:

recombinant

RdRP:

RNA-dependent RNA polymerase

RI:

replication intermediate

RV:

rotavirus

TLP:

triple-layered particle

UTR:

untranslated region

VP:

viral structural protein

References

  1. Blacklow N R & Greenberg H B (1991). Viral gastroenteritis, N Engl J Med, 325, 252–264

    Article  PubMed  CAS  Google Scholar 

  2. Kapikian A Z (1996). Overview of viral gastroenteritis, Arch Virol Suppl, 12, 7–19

    PubMed  CAS  Google Scholar 

  3. Parashar U D, Gibson C J, Bresee J S & et al (2006). Rotavirus and severe childhood diarrhea, Emerg Infect Dis, 12, 304–306

    Article  PubMed  Google Scholar 

  4. Kapikian A Z (2001). A rotavirus vaccine for prevention of severe diarrhoea of infants and young children: development, utilization and withdrawal, Novartis Found. Symp, 238, 153–171;discussion 171–159

    Article  PubMed  CAS  Google Scholar 

  5. Jiang S, Ji S, Tang Q & et al (2008) Molecular characterization of a novel adult diarrhoea rotavirus strain J19 isolated in China and its significance for the evolution and origin of group B rotaviruses, J Gen Virol, 89, 2622–2629

    Article  PubMed  CAS  Google Scholar 

  6. Nagashima S, Kobayashi N, Ishino M & et al (2008). Whole genomic characterization of a human rotavirus strain B219 belonging to a novel group of the genus Rotavirus, J Med Virol, 80, 2023–2033

    Article  PubMed  CAS  Google Scholar 

  7. Jayaram H, Estes M K & Prasad B V (2004). Emerging tshemes in rotavirus cell entry, genome organization, transcription and replication, Virus Res, 101, 67–81

    Article  PubMed  CAS  Google Scholar 

  8. Prasad B V, Wang G J, Clerx J P & et al (1988). Three- dimensional structure of rotavirus, J Mol Biol, 199, 269–275

    Article  PubMed  CAS  Google Scholar 

  9. Yeager M, Dryden K A, Olson N H & et al (1990). Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction, J Cell Biol, 110, 2133–2144

    Article  PubMed  CAS  Google Scholar 

  10. Estes M K (2001). Rotaviruses and Their Replication, (what is the title of the book or the chapter?) Lippincott, Williams and Wilkins, Philadelphia

    Google Scholar 

  11. Labbe M, Baudoux P, Charpilienne A & et al (1994). Identification of the nucleic acid binding domain of the rotavirus VP2 protein, J Gen Virol, 75 (Part 12), 3423–3430

    Article  PubMed  CAS  Google Scholar 

  12. Cohen J, Charpilienne A, Chilmonczyk S & et al (1989). Nucleotide sequence of bovine rotavirus gene 1 and expression of the gene product in baculovirus, Virology, 171, 131–140

    Article  PubMed  CAS  Google Scholar 

  13. Fukuhara N, Nishikawa K, Gorziglia M & et al (1989). Nucleotide sequence of gene segment 1 of a porcine rotavirus strain, Virology, 173, 743–749

    Article  PubMed  CAS  Google Scholar 

  14. Mitchell D B & Both G W (1990). Completion of the genomic sequence of the simian rotavirus SA11: nucleotide sequences of segments 1, 2, and 3, Virology, 177, 324–331

    Article  PubMed  CAS  Google Scholar 

  15. Valenzuela S, Pizarro J, Sandino A M & et al (1991). Photoaffinity labeling of rotavirus VP1 with 8-azido-ATP: identification of the viral RNA polymerase, J Virol., 65, 3964–3967

    PubMed  CAS  Google Scholar 

  16. Liu M, Mattion N M & Estes M K (1992). Rotavirus VP3 expressed in insect cells possesses guanylyltransferase activity, Virology, 188, 77–84

    Article  PubMed  CAS  Google Scholar 

  17. Pizarro J L, Sandino A M, Pizarro J M & et al (1991). Characterization of rotavirus guanylyltransferase activity associated with polypeptide VP3, J Gen Virol, 72 (Part 2), 325–332

    Article  PubMed  CAS  Google Scholar 

  18. Chen D, Luongo C L, Nibert M L & et al (1999). Rotavirus open cores catalyze 5′-capping and methylation of exogenous RNA: evidence that VP3 is a methyltransferase, Virology, 265, 120–130

    Article  PubMed  CAS  Google Scholar 

  19. Prasad B V, Rothnagel R, Zeng C Q & et al (1996). Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus, Nature, 382, 471– 473

    Article  PubMed  CAS  Google Scholar 

  20. Lawton J A, Zeng C Q, Mukherjee S K & et al (1997). Three-dimensional structural analysis of recombinant rotavirus-like particles with intact and amino-terminal-deleted VP2: implications for the architecture of the VP2 capsid layer, J Virol., 71, 7353–7360

    PubMed  CAS  Google Scholar 

  21. Shaw A L, Rothnagel R, Chen D & et al (1993). Three-dimensional visualization of the rotavirus hemagglutinin structure, Cell, 74, 693–701

    Article  PubMed  CAS  Google Scholar 

  22. Estes M K, Graham D Y & Mason B B (1981). Proteolytic enhancement of rotavirus infectivity: molecular mechanisms, J Virol, 39, 879–888

    PubMed  CAS  Google Scholar 

  23. Kalica A R, Flores J & Greenberg H B (1983). Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation, Virology, 125, 194–205

    Article  PubMed  CAS  Google Scholar 

  24. Dormitzer P R, Nason E B, Prasad B V & et al (2004). Structural rearrangements in the membrane penetration protein of a non- enveloped virus, Nature, 430, 1053–1058

    Article  PubMed  CAS  Google Scholar 

  25. Pesavento J B, Crawford S E, Roberts E & et al (2005). pH-induced conformational change of the rotavirus VP4 spike: implications for cell entry and antibody neutralization, J Virol, 79, 8572–8580

    Article  PubMed  CAS  Google Scholar 

  26. Desselberger U & McCrae M A (1994). The rotavirus genome, Curr. Top Microbiol Immunol, 185, 31–66

    Article  PubMed  CAS  Google Scholar 

  27. Patton J T, Wentz M, Xiaobo J & et al (1996). cis-Acting signals that promote genome replication in rotavirus mRNA, J Virol, 70, 3961–3971

    PubMed  CAS  Google Scholar 

  28. Tortorici M A, Broering T J, Nibert M L & et al (2003). Template recognition and formation of initiation complexes by the replicase of a segmented double-stranded RNA virus, J Biol Chem, 278, 32673– 32682

    Article  PubMed  CAS  Google Scholar 

  29. Chen D, Zeng C Q, Wentz M J & et al (1994). Template-dependent, in vitro replication of rotavirus RNA, J Virol, 68, 7030–7039

    PubMed  CAS  Google Scholar 

  30. Patton J T, Jones M T, Kalbach A N & et al (1997). Rotavirus RNA polymerase requires the core shell protein to synthesize the double-stranded RNA genome, J Virol, 71, 9618–9626

    PubMed  CAS  Google Scholar 

  31. Imai M, Akatani K, Ikegami N & et al (1983). Capped and conserved terminal structures in human rotavirus genome double-stranded RNA segments, J Virol, 47, 125–136

    PubMed  CAS  Google Scholar 

  32. McCrae M A & McCorquodale J G (1983). Molecular biology of rotaviruses. V. Terminal structure of viral RNA species, Virology, 126, 204–212

    Article  PubMed  CAS  Google Scholar 

  33. Patton J T (1986). Synthesis of simian rotavirus SA11 double-stranded RNA in a cell-free system, Virus Res, 6, 217–233

    Article  PubMed  CAS  Google Scholar 

  34. Patton J T (1994). Rotavirus replication, Curr Top Microbiol Immunol, 185, 107–127

    Article  PubMed  CAS  Google Scholar 

  35. Petrie B L, Greenberg H B, Graham D Y & et al (1984). Ultrastructural localization of rotavirus antigens using colloidal gold, Virus Res, 1, 133–152

    Article  PubMed  CAS  Google Scholar 

  36. Altenburg B C, Graham D Y & Estes M K (1980). Ultrastructural study of rotavirus replication in cultured cells, J Gen Virol, 46, 75–85

    Article  PubMed  CAS  Google Scholar 

  37. Berois M, Sapin C, Erk I & et al (2003). Rotavirus nonstructural protein NSP5 interacts with major core protein VP2, J Virol, 77, 1757–1763

    Article  PubMed  CAS  Google Scholar 

  38. Fabbretti E, Afrikanova I, Vascotto F & et al (1999). Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo, J Gen Virol, 80 (Part 2), 333–339

    PubMed  CAS  Google Scholar 

  39. Kattoura M D, Chen X & Patton J T (1994). The rotavirus RNA- binding protein NS35 (NSP2) forms 10S multimers and interacts with the viral RNA polymerase, Virology, 202, 803–813

    Article  PubMed  CAS  Google Scholar 

  40. Patton J T & Gallegos C O (1990). Rotavirus RNA replication: single- stranded RNA extends from the replicase particle, J Gen Virol, 71 (Part 5), 1087–1094

    Article  PubMed  CAS  Google Scholar 

  41. Suzuki H, Sato T, Konno T & et al (1984). Effect of tunicamycin on human rotavirus morphogenesis and infectivity. Brief report, Arch Virol, 81, 363–369

    Article  PubMed  CAS  Google Scholar 

  42. Maass D R & Atkinson P H (1990). Rotavirus proteins VP7, NS28, and VP4 form oligomeric structures, J Virol, 64, 2632–2641

    PubMed  CAS  Google Scholar 

  43. Tian P, Ball J M, Zeng C Q & et al (1996). Rotavirus protein expression is important for virus assembly and pathogenesis, Arch Virol Suppl, 12, 69–77

    PubMed  CAS  Google Scholar 

  44. Patton J T & Stacy-Phipps S (1986). Electrophoretic separation of the plus and minus strands of rotavirus SA11 double-stranded RNAs, J Virol Methods, 13, 185–190

    CAS  Google Scholar 

  45. Stacy-Phipps S & Patton J T (1987). Synthesis of plus- and minus- strand RNA in rotavirus-infected cells, J Virol, 61, 3479–3484

    PubMed  CAS  Google Scholar 

  46. Tortorici M A, Shapiro B A & Patton J T (2006). A base-specific recognition signal in the 5( consensus sequence of rotavirus plus-strand RNAs promotes replication of the double-stranded RNA genome segments, RNA (New York), 12, 133–146

    Article  CAS  Google Scholar 

  47. Wentz M J, Patton J T & Ramig R F (1996). The 3(-terminal consensus sequence of rotavirus mRNA is the minimal promoter of negative-strand RNA synthesis, J Virol, 70, 7833–7841

    PubMed  CAS  Google Scholar 

  48. Wentz M J, Zeng C Q, Patton J T & et al (1996). Identification of the minimal replicase and the minimal promoter of (-)-strand synthesis, functional in rotavirus RNA replication in vitro, Arch Virol Suppl, 12, 59–67

    PubMed  CAS  Google Scholar 

  49. Zeng C Q, Wentz M J, Cohen J & et al (1996). Characterization and replicase activity of double-layered and single-layered rotavirus-like particles expressed from baculovirus recombinants, J Virol, 70, 2736–2742

    PubMed  CAS  Google Scholar 

  50. Lu X, McDonald S M, Tortorici M A & et al (2008). Mechanism for coordinated RNA packaging and genome replication by rotavirus polymerase VP1, Structure, 16, 1678–1688

    Article  PubMed  CAS  Google Scholar 

  51. Zeng C Q, Estes M K, Charpilienne A & et al (1998). The N terminus of rotavirus VP2 is necessary for encapsidation of VP1 and VP3, J Virol, 72, 201–208

    PubMed  CAS  Google Scholar 

  52. Gombold J L & Ramig R F (1987). Assignment of simian rotavirus SA11 temperature-sensitive mutant groups A, C, F, and G to genome segments, Virology, 161, 463–473

    Article  PubMed  CAS  Google Scholar 

  53. Mansell E A & Patton JT (1990). Rotavirus RNA replication: VP2, but not VP6, is necessary for viral replicase activity, J Virol, 64, 4988– 4996

    PubMed  CAS  Google Scholar 

  54. Patton J T (1996). 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, 7940–7947

    PubMed  CAS  Google Scholar 

  55. Bruenn J A (2003). A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases, Nucleic Acids Res, 31, 1821– 1829

    Article  PubMed  CAS  Google Scholar 

  56. Hansen J L, Long A M & Schultz S C (1997). Structure of the RNA- dependent RNA polymerase of poliovirus, Structure, 5, 1109–1122

    Article  PubMed  CAS  Google Scholar 

  57. Kamer G & Argos P (1984). Primary structural comparison of RNA- dependent polymerases from plant, animal and bacterial viruses, Nucleic Acids Res, 12, 7269–7282

    Article  PubMed  CAS  Google Scholar 

  58. O’Reilly E K & Kao C C (1998). Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure, Virology, 252, 287–303

    Article  PubMed  Google Scholar 

  59. Joyce C M & Steitz T A (1994). Function and structure relationships in DNA polymerases, Annu Rev Biochem, 63, 777–822

    Article  PubMed  CAS  Google Scholar 

  60. Doublie S & Ellenberger T (1998). The mechanism of action of T7 DNA polymerase, Curr Opin Struct Biol, 8, 704–712

    Article  PubMed  CAS  Google Scholar 

  61. Tao Y, Farsetta D L, Nibert M L & et al (2002). RNA synthesis in a cage--structural studies of reovirus polymerase lambda3, Cell, 111, 733–745

    Article  PubMed  CAS  Google Scholar 

  62. Labbe M, Charpilienne A, Crawford S E & et al (1991). Expression of rotavirus VP2 produces empty corelike particles, J Virol, 65, 2946–2952

    PubMed  CAS  Google Scholar 

  63. McDonald S M & Patton J T (2008). Molecular characterization of a subgroup specificity associated with the rotavirus inner capsid protein VP2, J Virol, 82, 2752–2764

    Article  PubMed  CAS  Google Scholar 

  64. Hua J, Mansell E A & Patton J T (1993). Comparative analysis of the rotavirus NS53 gene: conservation of basic and cysteine-rich regions in the protein and possible stem-loop structures in the RNA, Virology, 196, 372– 378

    Article  PubMed  CAS  Google Scholar 

  65. Patton J T, Salter-Cid L, Kalbach A & et al (1993). Nucleotide and amino acid sequence analysis of the rotavirus nonstructural RNA-binding protein NS35, Virology, 192, 438–446

    Article  PubMed  CAS  Google Scholar 

  66. Chen D & Patton J T (1998). Rotavirus RNA replication requires a single-stranded 3( end for efficient minus-strand synthesis, J Virol, 72, 7387–7396

    PubMed  CAS  Google Scholar 

  67. Chen D & Patton J T (2000). De novo synthesis of minus strand RNA by the rotavirus RNA polymerase in a cell-free system involves a novel mechanism of initiation, RNA (New York), 6, 1455–1467

    Article  CAS  Google Scholar 

  68. Hsu L M, Vo N V, Kane C M & et al (2003). In vitro studies of transcript initiation by Escherichia coli RNA polymerase. 1. RNA chain initiation, abortive initiation, and promoter escape at three bacteriophage promoters, Biochemistry, 42, 3777–3786

    Article  PubMed  CAS  Google Scholar 

  69. Yin Y W & Steitz T A (2002). Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase, Science, 298, 1387–1395

    Article  PubMed  CAS  Google Scholar 

  70. Ng K K, Arnold J J & Cameron C E (2008). Structure-function relationships among RNA-dependent RNA polymerases, Curr Top Microbiol Immunol, 320, 137–156

    Article  PubMed  CAS  Google Scholar 

  71. Gallegos C O & Patton J T (1989). Characterization of rotavirus replication intermediates: a model for the assembly of single-shelled particles, Virology, 172, 616–627

    Article  PubMed  CAS  Google Scholar 

  72. Patton J T & Spencer E (2000). Genome replication and packaging of segmented double-stranded RNA viruses, Virology, 277, 217–225

    Article  PubMed  CAS  Google Scholar 

  73. Bican, P., Cohen, J., Charpilienne, A., and Scherrer, R. (1982) Purification and characterization of bovine rotavirus cores, J. Virol., 43, 1113–1117.

    PubMed  CAS  Google Scholar 

  74. Patton J T (1995). Structure and function of the rotavirus RNA-binding proteins, J Gen Virol, 76 (Part 11), 2633–2644

    Article  PubMed  CAS  Google Scholar 

  75. Sandino A M, Jashes M, Faundez G & et al (1986). Role of the inner protein capsid on in vitro human rotavirus transcription, J Virol, 60, 797–802

    PubMed  CAS  Google Scholar 

  76. Patton J T, Vasquez-Del Carpio R, Tortorici M A & et al (2007). Coupling of rotavirus genome replication and capsid assembly, Adv Virus Res, 69, 167–201

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Michelle Arnold, Sarah McDonald, and Shane Trask for helpful discussions and critical reading of the manuscript. We acknowledge the Intramural Research Program of the NIH, National Institutes of Allergy and Infectious Diseases for funding.

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Guglielmi, K.M., Patton, J.T. (2010). Functions of the Rotavirus RNA Polymerase in Virus Replication. In: Georgiev, V. (eds) National Institute of Allergy and Infectious Diseases, NIH. Infectious Disease. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-60761-512-5_4

Download citation

  • DOI: https://doi.org/10.1007/978-1-60761-512-5_4

  • Published:

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-60761-511-8

  • Online ISBN: 978-1-60761-512-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics