Functional role of the 5′ terminal cloverleaf in Coxsackievirus RNA replication

Virology

Volumn 393, Issue 2, 2009, Pages 238-249

  Sharma, Nidhi ^a   Ogram, Sushma A ^a   Morasco, B Joan ^a   Spear, Allyn ^a   Chapman, Nora M ^b   Flanegan, James B ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

5 cloverleaf; Coxsackievirus; Poly(C) binding protein; RNA replication; Viral persistence

Indexed keywords

BINDING PROTEIN; CIS ACTING ELEMENT; POLYCYTIDYLIC ACID; VIRUS RNA;

ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; COXSACKIE VIRUS; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RNA REPLICATION; RNA STABILITY; RNA STRUCTURE; RNA SYNTHESIS;

ENTEROVIRUS; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; RNA STABILITY; RNA, VIRAL; VIRUS REPLICATION;

COXSACKIEVIRUS;

EID: 70349835379     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.07.039     Document Type: Article

References (48)

1. Andino R., Rieckhof G.E., and Baltimore D. A functional ribonucleoprotein complex forms around the 5′ end of poliovirus RNA. Cell 63 (1990) 369-380
2. Andino R., Rieckhof G.E., Trono D., and Baltimore D. Substitutions in the protease (3Cpro) gene of poliovirus can suppress a mutation in the 5′ noncoding region. J. Virol. 64 (1990) 607-612
3. Andino R., Rieckhof G.E., Achacoso P.L., and Baltimore D. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA. EMBO J. 12 (1993) 3587-3598
4. Andreoletti L., Hober D., Becquart P., Belaich S., Copin M.C., Lambert V., and Wattre P. Experimental CVB3-induced chronic myocarditis in two murine strains: evidence of interrelationships between virus replication and myocardial damage in persistent cardiac infection. J. Med. Virol. 52 (1997) 206-214
5. Barton D.J., Black E.P., and Flanegan J.B. Complete replication of poliovirus in vitro: preinitiation RNA replication complexes require soluble cellular factors for the synthesis of VPg-linked RNA. J. Virol. 69 (1995) 5516-5527
6. pol, and authentic RNA replication in HeLa S10 extracts. Methods Enzymol. 275 (1996) 35-57
7. Barton D.J., O'Donnell B.J., and Flanegan J.B. 5′ cloverleaf in poliovirus RNA is a cis-acting replication element required for negative-strand synthesis. EMBO J. 20 (2001) 1439-1448
8. Chapman N.M., and Kim K.S. Persistent coxsackievirus infection: enterovirus persistence in chronic myocarditis and dilated cardiomyopathy. Curr. Top. Microbiol. Immunol. 323 (2008) 275-292
9. Chapman N.M., Kim K.S., Drescher K.M., Oka K., and Tracy S. 5′ terminal deletions in the genome of a coxsackievirus B2 strain occurred naturally in human heart. Virology 375 (2008) 480-491
10. Du Z., Yu J., Ulyanov N.B., Andino R., and James T.L. Solution structure of a consensus stem-loop D RNA domain that plays important roles in regulating translation and replication in enteroviruses and rhinoviruses. Biochemistry 43 (2004) 11959-11972
11. Gamarnik A.V., and Andino R. Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3 (1997) 882-892
12. Gamarnik A.V., and Andino R. Switch from translation to RNA replication in a positive-stranded RNA virus. Genes Dev. 12 (1998) 2293-2304
13. Gamarnik A.V., and Andino R. Interactions of viral protein 3CD and poly(rC) binding protein with the 5′ untranslated region of the poliovirus genome. J. Virol. 74 (2000) 2219-2226
14. Herold J., and Andino R. Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol. Cell 7 (2001) 581-591
15. Hunziker I.P., Cornell C.T., and Whitton J.L. Deletions within the 5′UTR of coxsackievirus B3: consequences for virus translation and replication. Virology 360 (2007) 120-128
16. Jurgens C.K., Barton D.J., Sharma N., Morasco B.J., Ogram S.A., and Flanegan J.B. 2Apro is a multifunctional protein that regulates the stability, translation and replication of poliovirus RNA. Virology 345 (2006) 346-357
17. Kandolf R. Molecular biology of viral heart disease. Herz. 18 (1993) 238-244
18. Kandolf R., Klingel K., Zell R., Selinka H.C., Raab U., Schneider-Brachert W., and Bultmann B. Molecular pathogenesis of enterovirus-induced myocarditis: virus persistence and chronic inflammation. [Review] [27 refs]. Intervirology 35 (1993) 140-151
19. Kandolf R., Sauter M., Aepinus C., Schnorr J.J., Selinka H.C., and Klingel K. Mechanisms and consequences of enterovirus persistence in cardiac myocytes and cells of the immune system. Virus Res. 62 (1999) 149-158
20. Kim K.S., Hufnagel G., Chapman N.M., and Tracy S. The group B coxsackieviruses and myocarditis. Rev. Med. Virol. 11 (2001) 355-368
21. Kim K.S., Tracy S., Tapprich W., Bailey J., Lee C.K., Kim K., Barry W.H., and Chapman N.M. 5′-Terminal deletions occur in coxsackievirus B3 during replication in murine hearts and cardiac myocyte cultures and correlate with encapsidation of negative-strand viral RNA. J. Virol. 79 (2005) 7024-7041
22. Kim K.S., Chapman N.M., and Tracy S. Replication of coxsackievirus B3 in primary cell cultures generates novel viral genome deletions. J. Virol. 82 (2008) 2033-2037
23. Klingel K., Hohenadl C., Canu A., Albrecht M., Seemann M., Mall G., and Kandolf R. Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 314-318
24. Klingel K., Stephan S., Sauter M., Zell R., McManus B.M., Bultmann B., and Kandolf R. Pathogenesis of murine enterovirus myocarditis: virus dissemination and immune cell targets. J. Virol. 70 (1996) 8888-8895
25. Lyons T., Murray K.E., Roberts A.W., and Barton D.J. Poliovirus 5′-terminal cloverleaf RNA is required in cis for VPg uridylylation and the initiation of negative-strand RNA synthesis. J. Virol. 75 (2001) 10696-10708
26. Martino T.A., Liu P., and Sole M.J. Viral infection and the pathogenesis of dilated cardiomyopathy. Circ. Res. 74 (1994) 182-188
27. Molla A., Paul A.V., and Wimmer E. Cell-free, de novo synthesis of poliovirus. Science 254 (1991) 1647-1651
28. Morasco B.J., Sharma N., Parilla J., and Flanegan J.B. Poliovirus cre(2C)-dependent synthesis of VPgpUpU is required for positive-but not negative-strand RNA synthesis. J. Virol. 77 (2003) 5136-5144
29. Muir P., Nicholson F., Illavia S.J., McNeil T.S., Ajetunmobi J.F., Dunn H., Starkey W.G., Reetoo K.N., Cary N.R., Parameshwar J., and Banatvala J.E. Serological and molecular evidence of enterovirus infection in patients with end-stage dilated cardiomyopathy. Heart 76 (1996) 243-249
30. Murray K.E., Roberts A.W., and Barton D.J. Poly(rC) binding proteins mediate poliovirus mRNA stability. RNA 7 (2001) 1126-1141
31. Ohlenschlager O., Wohnert J., Bucci E., Seitz S., Hafner S., Ramachandran R., Zell R., and Gorlach M. The structure of the stemloop D subdomain of coxsackievirus B3 cloverleaf RNA and its interaction with the proteinase 3C. Structure. (Camb.) 12 (2004) 237-248
32. Parsley T.B., Towner J.S., Blyn L.B., Ehrenfeld E., and Semler B.L. Poly (rC) binding protein 2 forms a ternary complex with the 5′-terminal sequences of poliovirus RNA and the viral 3CD proteinase. RNA 3 (1997) 1124-1134
33. Racaniello V. Picornaviridae: the viruses and their replication. In: Knipe D. (Ed). Fundamental Virology (2001), Lippincott Williams and Wilkins, Philadelphia, US 529-566
34. Reyes M.P., and Lerner A.M. Coxsackievirus myocarditis-with special reference to acute and chronic effects. Prog. Cardiovasc. Dis. 27 (1985) 373-394
35. Rieder E., Xiang W., Paul A., and Wimmer E. Analysis of the cloverleaf element in a human rhinovirus type 14/poliovirus chimera: correlation of subdomain D structure, ternary protein complex formation and virus replication. J. Gen. Virol. 84 (2003) 2203-2216
36. Sean P., and Semler B.L. Coxsackievirus B RNA replication: lessons from poliovirus. Curr. Top. Microbiol. Immunol. 323 (2008) 89-121
37. Sharma N., O'Donnell B.J., and Flanegan J.B. 3′-Terminal sequence in poliovirus negative-strand templates is the primary cis-acting element required for VPgpUpU-primed positive-strand initiation. J. Virol. 79 (2005) 3565-3577
38. Silvestri L.S., Parilla J.M., Morasco B.J., Ogram S.A., and Flanegan J.B. Relationship between poliovirus negative-strand RNA synthesis and the length of the 3′ poly(A) tail. Virology 345 (2006) 509-519
39. Spear A., Sharma N., and Flanegan J.B. Protein-RNA tethering: the role of poly(C) binding protein 2 in poliovirus RNA replication. Virology 374 (2008) 280-291
40. Tam P.E., and Messner R.P. Molecular mechanisms of coxsackievirus persistence in chronic inflammatory myopathy: viral RNA persists through formation of a double-stranded complex without associated genomic mutations or evolution. J. Virol. 73 (1999) 10113-10121
41. Teterina N.L., Egger D., Bienz K., Brown D.M., Semler B.L., and Ehrenfeld E. Requirements for assembly of poliovirus replication complexes and negative-strand RNA synthesis. J. Virol. 75 (2001) 3841-3850
42. Toyoda H., Franco D., Fujita K., Paul A.V., and Wimmer E. Replication of poliovirus requires binding of the poly(rC) binding protein to the cloverleaf as well as to the adjacent C-rich spacer sequence between the cloverleaf and the internal ribosomal entry site. J. Virol. 81 (2007) 10017-10028
43. Tracy S., Drescher K.M., Chapman N.M., Kim K.S., Carson S.D., Pirruccello S., Lane P.H., Romero J.R., and Leser J.S. Toward testing the hypothesis that group B coxsackieviruses (CVB) trigger insulin-dependent diabetes: inoculating nonobese diabetic mice with CVB markedly lowers diabetes incidence. J. Virol. 76 (2002) 12097-12111
44. Tyler K.L., and Nathanson N. Pathogenesis of viral infections. In: Knipe D., and Howley P.M. (Eds). Fundamental Virology (2001), Lippincott Williams and Wilkins 199-243
45. Walter B.L., Parsley T.B., Ehrenfeld E., and Semler B.L. Distinct poly(rC) binding protein KH domain determinants for poliovirus translation initiation and viral RNA replication. J. Virol. 76 (2002) 12008-12022
46. Zell R., Sidigi K., Bucci E., Stelzner A., and Gorlach M. Determinants of the recognition of enteroviral cloverleaf RNA by coxsackievirus B3 proteinase 3C. RNA 8 (2002) 188-201
47. Zell R., Ihle Y., Seitz S., Gundel U., Wutzler P., and Gorlach M. Poly(rC)-binding protein 2 interacts with the oligo(rC) tract of coxsackievirus B3. Biochem. Biophys. Res. Commun. 366 (2008) 917-921
48. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31 (2003) 3406-3415