Distinct poly(rC) binding protein KH domain determinants for poliovirus translation initiation and viral RNA replication

Journal of Virology

Volumn 76, Issue 23, 2002, Pages 12008-12022

  Walter, Brandon L ^a   Parsley, Todd B ^a   Ehrenfeld, Ellie ^a   Semler, Bert L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; POLYCYTIDYLIC ACID BINDING PROTEIN 2; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA REPLICATION; TRANSLATION INITIATION; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; DNA-BINDING PROTEINS; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; POLIOVIRUS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; REPLICON; RNA, VIRAL; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS; VIRUS REPLICATION;

EID: 0036889353     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.76.23.12008-12022.2002     Document Type: Article

References (63)

1. Aasheim, H. C., T. Loukianova, A. Deggerdal, and E. B. Smeland. 1994. Tissue specific expression and cDNA structure of a human transcript encoding a nucleic acid binding [oligo(dC)] protein related to the pre-mRNA binding protein K. Nucleic Acids Res. 22:959-964.
2. Adinolfi, S., C. Bagni, M. A. Castiglione Morelli, F. Fraternali, G. Musco, and A. Pastore. 1999. Novel RNA-binding motif: The KH module. Biopolymers 51:153-164.
3. Andino, R., N. Boddeker, D. Silvera, and A. V. Gamarnik. 1999. Intracellular determinants of picornavirus replication. Trends Microbiol. 7:76-82.
4. Andino, R., G. E. Rieckhof, P. L. Achacoso, and D. Baltimore. 1993. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA. EMBO J. 12:3587-3598.
5. Andino, R., G. E. Rieckhof. and D. Baltimore. 1990. A functional ribonucleoprotein complex forms around the 5′ end of poliovirus RNA. Cell 63:369-380.
6. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 2000. Current Protocols in Molecular Biology. John Wiley & Sons, New York, N.Y.
7. Barton, D. J., and J. B. Flanegan. 1993. Coupled translation and replication of poliovirus RNA in vitro: Synthesis of functional 3D polymerase and infectious virus. J. Virol. 67:822-831.
8. Barton, D. J., and J. B. Flanegan. 1997. Synchronous replication of poliovirus RNA: Initiation of negative-strand RNA synthesis requires the guanidine-inhibited activity of protein 2C. J. Virol. 71:8482-8489.
9. Barton, D. J., B. J. Morasco, and J. B. Flanegan. 1999. Translating ribosomes inhibit poliovirus negative-strand RNA synthesis. J. Virol. 73:10104-10112.
10. Barton, D. J., B. J. O'Donnell, and J. B. Flanegan. 2001. 5′ cloverleaf in poliovirus RNA is a cis-acting replication element required for negativestrand synthesis. EMBO J. 20:1439-1448.
11. Bass, S. H., M. G. Mulkerrin, and J. A. Wells. 1991. A systematic mutational analysis of hormone-binding determinants in the human growth hormone receptor. Proc. Natl. Acad. Sci. USA 88:4498-4502.
12. Birikh, K. R., P. A. Heaton, and F. Eckstein. 1997. The structure, function and application of the hammerhead ribozyme. Eur. J. Biochem. 245:1-16.
13. Blair, W. S., J. H. Nguyen, T. B. Parsley, and B. L. Semler. 1996. Mutations in the poliovirus 3CD proteinase S1-specificity pocket affect substrate recognition and RNA binding. Virology 218:1-13.
14. Blyn, L. B., R. Chen, B. L. Semler, and E. Ehrenfeld. 1995. Host cell proteins binding to domain IV of the 5′ noncoding region of poliovirus RNA. J. Virol. 69:4381-4389.
15. Blyn, L. B., K. M. Swiderek, O. Richards, D. C. Stahl, B. L. Semler, and E. Ehrenfeld. 1996. Poly(rC) binding protein 2 binds to stem-loop IV of the poliovirus RNA 5′ noncoding region: Identification by automated liquid chromatography-tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 93:11115-11120.
16. Blyn, L. B., J. S. Towner, B. L. Semler, and E. Ehrenfeld. 1997. Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA. J. Virol. 71:6243-6246.
17. Brown, B. A., and E. Ehrenfeld. 1979. Translation of poliovirus RNA in vitro: Changes in cleavage pattern and initiation sites by ribosomal salt wash. Virology 97:396-405.
18. Charini, W. A., C. C. Burns, E. Ehrenfeld, and B. L. Semler. 1991. Trans rescue of a mutant poliovirus RNA polymerase function. J. Virol. 65:2655-2665.
19. Chkheidze, A. N., D. L. Lyakhov, A. V. Makeyev, J. Morales, J. Kong, and S. A. Liebhaber. 1999. Assembly of the a-globin mRNA stability complex reflects binary interaction between the pyrimidine-rich 3′ untranslated region determinant and poly(C) binding protein αCP. Mol. Cell. Biol. 19:4572-4581.
20. Collier, B., L. Goobar-Larsson, M. Sokolowski, and S. Schwartz. 1998. Translational inhibition in vitro of human papillomavirus type 16 L2 mRNA mediated through interaction with heterogenous ribonucleoprotein K and poly(rC)-binding proteins 1 and 2. J. Biol. Chem. 273:22648-22656.
21. Czyzyk-Krzeska, M. F., and A. C. Bendixen. 1999. Identification of the poly(C) binding protein in the complex associated with the 3′ untranslated region of erythropoietin messenger RNA. Blood 93:2111-2120.
22. Dejgaard, K., and H. Leffers. 1996. Characterisation of the nucleic-acid-binding activity of KH domains. Different properties of different domains. Eur. J. Biochem. 241:425-431.
23. Dildine, S. L., and B. L. Semler. 1992. Conservation of RNA-protein interactions among picornaviruses. J. Virol. 66:4364-4376.
24. Gamarnik, A. V., and R. Andino. 1997. Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3:882-892.
25. Gamarnik, A. V., and R. Andino. 1998. Switch from translation to RNA replication in a positive-stranded RNA virus. Genes Dev. 12:2293-2304.
26. Gamarnik, A. V., and R. Andino. 2000. Interactions of viral protein 3CD and poly(rC) binding protein with the 5′ untranslated region of the poliovirus genome. J. Virol. 74:2219-2226.
27. Graff, J., J. Cha, L. B. Blyn, and E. Ehrenfeld. 1998. Interaction of poly(rC) binding protein 2 with the 5′ noncoding region of hepatitis A virus RNA and its effects on translation. J. Virol. 72:9668-9675.
28. Haller, A. A., and B. L. Semler. 1992. Linker scanning mutagenesis of the internal ribosome entry site of poliovirus RNA. J. Virol. 66:5075-5086.
29. pro with the 5′ and 3′ termini of the poliovirus genome. Identification of viral and cellular cofactors needed for efficient binding. J. Biol. Chem. 269:27004-27014.
30. Herold, J., and R. Andino. 2000. Poliovirus requires a precise 5′ end for efficient positive-strand RNA synthesis. J. Virol. 74:6394-6400.
31. Herold, J., and R. Andino. 2001. Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol. Cell 7:581-591.
32. Holcik, M., and S. A. Liebhaber. 1997. Four highly stable eukaryotic mRNAs assemble 3′ untranslated region RNA-protein complexes sharing cis and trans components. Proc. Natl. Acad. Sci. USA 94:2410-2414.
33. Kiledjian, M., X. Wang, and S. A. Liebhaber. 1995. Identification of two KH domain proteins in the alpha-globin mRNP stability complex. EMBO J. 14:4357-4364.
34. Kim, J. H., B. Hahm, Y. K. Kim, M. Choi, and S. K. Jang. 2000. Proteinprotein interaction among hnRNPs shuttling between nucleus and cytoplasm. J. Mol. Biol. 298:395-405.
35. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82:488-492.
36. Leffers, H., K. Dejgaard, and J. E. Cells. 1995. Characterisation of two major cellular poly(rC)-binding human proteins, each containing three K-homologous (KH) domains. Eur. J. Biochem. 230:447-453.
37. Lewis, H. A., H. Chen, C. Edo, R. J. Buckanovich, Y. Y. Yang, K. Musunuru, R. Zhong, R. B. Darnell, and S. K. Burley. 1999. Crystal structures of Nova-1 and Nova-2 K-homology RNA-binding domains. Structure Fold. Des. 7:191-203.
38. 2 and the 3′-untranslated region of collagen α1(I) mRNA. Nucleic Acids Res. 28:4306-4316.
39. Makeyev, A. V., A. N. Chkheidze, and S. A. Liebhaber. 1999. A set of highly conserved RNA-binding proteins, αCP-1 and αCP-2, implicated in mRNA stabilization, are coexpressed from an intronless gene and its intron-containing paralog. J. Biol. Chem. 274:24849-24857.
40. Makeyev, A. V., and S. A. Liebhaber. 2000. Identification of two novel mammalian genes establishes a subfamily of KH-domain RNA-binding proteins. Genomics 67:301-316.
41. Makeyev, A. V., and S. A. Liebhaber. 2002. The poly(C)-binding proteins: A multiplicity of functions and a search for mechanisms. RNA 8:265-278.
42. Molla, A., S. K. Jang, A. V. Paul, Q. Reuer, and E. Wimmer. 1992. Cardioviral internal ribosomal entry site is functional in a genetically engineered dicistronic poliovirus. Nature 356:255-257.
43. Molla, A., A. V. Paul, and E. Wimmer. 1991. Cell-free, de novo synthesis of poliovirus. Science 254:1647-1651.
44. Murray, K. E., A. W. Roberts, and D. J. Barton. 2001. Poly(rC) binding proteins mediate poliovirus mRNA stability. RNA 7:1126-1141.
45. Musco, G., A. Kharrat, G. Stier, F. Fraternali, T. J. Gibson, M. Nilges, and A. Pastore. 1997. The solution structure of the first KH domain of FMR1, the protein responsible for the fragile X syndrome. Nat. Struct. Biol. 4:712-716.
46. Musco, G., G. Stier, C. Joseph, M. A. Castiglione Morelli, M. Nilges, T. J. Gibson, and A. Pastore. 1996. Three-dimensional structure and stability of the KH domain: Molecular insights into the fragile X syndrome. Cell 85:237-245.
47. Nelson, M., and M. McClelland. 1992. Use of DNA methyltransferase/ endonuclease enzyme combinations for megabase mapping of chromosomes. Methods Enzymol. 216:279-303.
48. Ostareck, D. H., A. Ostareck-Lederer, I. N. Shatsky, and M. W. Hentze. 2001. Lipoxygenase mRNA silencing in erythroid differentiation: The 3′UTR regulatory complex controls 60S ribosomal subunit joining. Cell 104:281-290.
49. Ostareck, D. H., A. Ostareck-Lederer, M. Wilm, B. J. Thiele, M. Mann, and M. W. Hentze. 1997. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89:597-606.
50. Parsley, T. B., J. S. Towner, L. B. Blyn, E. Ehrenfeld, and B. L. Semler. 1997. Poly(rC) binding protein 2 forms a ternary complex with the 5′-terminal sequences of poliovirus RNA and the viral 3CD proteinase. RNA 3:1124-1134.
51. Paulding, W. R., and M. F. Czyzyk-Krzeska. 1999. Regulation of tyrosine hydroxylase mRNA stability by protein-binding, pyrimidine-rich sequence in the 3′-untranslated region. J. Biol. Chem. 274:2532-2538.
52. Scott, W. G. 1997. Crystallographic analyses of chemically synthesized modified hammerhead RNA sequences as a general approach toward understanding ribozyme structure and function. Methods Mol. Biol. 74:387-391.
53. Silvera, D., A. V. Gamarnik, and R. Andino. 1999. The N-terminal K homology domain of the poly(rC)-binding protein is a major determinant for binding to the poliovirus 5′-untranslated region and acts as an inhibitor of viral translation. J. Biol. Chem. 274:38163-38170.
54. Stefanovic, B., C. Hellerbrand, M. Holcik, M. Breindl, S. Liebhaber, and D. A. Brenner. 1997. Posttranscriptional regulation of collagen α1(I) mRNA in hepatic stellate cells. Mol. Cell. Biol. 17:5201-5209.
55. Stewart, S. R., and B. L. Semler. 1997. RNA determinants of picornavirus cap-independent translation initiation. Semin. Virol. 8:242-255.
56. Todd, S., J. S. Towner, and B. L. Semler. 1997. Translation and replication properties of the human rhinovirus genome in vivo and in vitro. Virology 229:90-97.
57. Urlaub, H., V. Kruft, O. Bischof, E. C. Muller, and B. Wittmann-Liebold. 1995. Protein-rRNA binding features and their structural and functional implications in ribosomes as determined by cross-linking studies. EMBO J. 14:4578-4588.
58. Walter, B. L., J. H. Nguyen, E. Ehrenfeld, and B. L. Semler. 1999. Differential utilization of poly(rC) binding protein 2 in translation directed by picornavirus IRES elements. RNA 5:1570-1585.
59. Wang, Z., N. Day, P. Trifillis, and M. Kiledjian. 1999. An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Mol. Cell. Biol. 19:4552-4560.
60. Weiss, I. M., and S. A. Liebhaber. 1994. Erythroid cell-specific determinants of alpha-globin mRNA stability. Mol. Cell. Biol. 14:8123-8132.
61. Weiss, I. M., and S. A. Liebhaber. 1995. Erythroid cell-specific mRNA stability elements in the α2-globin 3′ nontranslated region. Mol. Cell. Biol. 15:2457-2465.
62. Wimmer, E., C. U. Hellen, and X. Cao. 1993. Genetics of poliovirus. Annu. Rev. Genet. 27:353-436.
63. Yu, J., and J. E. Russell. 2001. Structural and functional analysis of an mRNP complex that mediates the high stability of human β-globin mRNA. Mol. Cell. Biol. 21:5879-5888.