Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN

Journal of Virology

Volumn 82, Issue 22, 2008, Pages 11283-11293

  Harb, Maya ^a   Becker, Michelle M ^a,d   Vitour, Damien ^a,e   Baron, Carolina H ^a   Vende, Patrice ^a   Brown, Spencer C ^b   Bolte, Susanne ^b   Arold, Stefan T ^c   Poncet, Didier ^a  

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

^b INSTITUT DES SCIENCES DU VÉGÉTAL   (France)

^c CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; INITIATION FACTOR 4G; MESSENGER RNA; NONSTRUCTURAL PROTEIN 3; POLYADENYLIC ACID BINDING PROTEIN; POLYADENYLIC ACID BINDING PROTEIN C1; PROTEIN ROXAN; UNCLASSIFIED DRUG; MUTANT PROTEIN; NSP3 PROTEIN, ROTAVIRUS; RNA BINDING PROTEIN; VIRUS PROTEIN; ZC3H7B PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; ROTAVIRUS; TRANSLATION INITIATION; VIRUS INFECTION; AMINO ACID SUBSTITUTION; ANIMAL; BINDING SITE; CELL LINE; GENE DELETION; GENETICS; HAPLORHINI; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN TRANSPORT; SITE DIRECTED MUTAGENESIS;

EUKARYOTA; ROTAVIRUS;

AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CELL LINE; EUKARYOTIC INITIATION FACTOR-4G; HAPLORHINI; HUMANS; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; POLY(A)-BINDING PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RNA-BINDING PROTEINS; ROTAVIRUS; SEQUENCE DELETION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 55549116341     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00872-08     Document Type: Article

References (53)

1. Afonina, E., R. Stauber, and G. N. Pavlakis. 1998. The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J. Biol. Chem. 273:13015-13021.
2. Angel, J., M. A. Franco, and H. B. Greenberg. 2007. Rotavirus vaccines: recent developments and future considerations. Nat. Rev. Microbiol. 5:529-539.
3. Aponte, C., D. Poncet, and J. Cohen. 1996. Recovery and characterization of a replicase complex in rotavirus-infected cells by using a monoclonal antibody against NSP2. J. Virol. 70:985-991.
4. Arold, S. T., M. K. Hoellerer, and M. E. Noble. 2002. The structural basis of localization and signaling by the focal adhesion targeting domain. Structure 10:319-327.
5. Boehmer, T., J. Enninga, S. Dales, G. Blobel, and H. Zhong. 2003. Depletion of a single nucleoporin, Nup107, prevents the assembly of a subset of nucleoporins into the nuclear pore complex. Proc. Natl. Acad. Sci. USA 100:981-985.
6. Borman, A. M., Y. M. Michel, and K. M. Kean. 2000. Biochemical characterisation of cap-poly(A) synergy in rabbit reticulocyte lysates: the eIF4GPABP interaction increases the functional affinity of eIF4E for the capped mRNA 5′-end. Nucleic Acids Res. 28:4068-4075.
7. Bushell, M., D. Poncet, W. E. Marissen, H. Flotow, R. E. Lloyd, M. J. Clemens, and S. J. Morley. 2000. Cleavage of polypeptide chain initiation factor eIF4GI during apoptosis in lymphoma cells: characterisation of an internal fragment generated by caspase-3-mediated cleavage. Cell Death Differ. 7:628-636.
8. Catherinot, V., and G. Labesse. 2004. ViTO: tool for refinement of protein sequence-structure alignments. Bioinformatics 20:3694-3696.
9. Chekanova, J. A., and D. A. Belostotsky. 2003. Evidence that poly(A) binding protein has an evolutionarily conserved function in facilitating mRNA biogenesis and export. RNA 9:1476-1490.
10. Cosson, B., N. Berkova, A. Couturier, S. Chabelskaya, M. Philippe, and G. Zhouravleva. 2002. Poly(A)-binding protein and eRF3 are associated in vivo in human and Xenopus cells. Biol. Cell 94:205-216.
11. Craig, A. W., A. Haghighat, A. T. Yu, and N. Sonenberg. 1998. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 392:520-523.
12. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60:2126-2132.
13. Fiser, A., and A. Sali. 2003. Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol. 374:461-491.
14. Gorlach, M., C. G. Burd, and G. Dreyfuss. 1994. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell. Res. 211:400-407.
15. Groft, C. M., and S. K. Burley. 2002. Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol. Cell 9:1273-1283.
16. Hoellerer, M. K., M. E. Noble, G. Labesse, I. D. Campbell, J. M. Werner, and S. T. Arold. 2003. Molecular recognition of paxillin LD motifs by the focal adhesion targeting domain. Structure 11:1207-1217.
17. Hosoda, N., F. Lejeune, and L. E. Maquat. 2006. Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol. Cell. Biol. 26:3085-3097.
18. Hutten, S., and R. H. Kehlenbach. 2007. CRM1-mediated nuclear export: to the pore and beyond. Trends Cell. Biol. 17:193-201.
19. Imataka, H., A. Gradi, and N. Sonenberg. 1998. A newly identified Nterminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 17:7480-7489.
20. Kahvejian, A., Y. V. Svitkin, R. Sukarieh, M. N. M'Boutchou, and N. Sonenberg. 2005. Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev. 19:104-113.
21. Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30:963-969.
22. Kedersha, N., M. R. Cho, W. Li, P. W. Yacono, S. Chen, N. Gilks, D. E. Golan, and P. Anderson. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151:1257-1268.
23. Khaleghpour, K., Y. V. Svitkin, A. W. Craig, C. T. DeMaria, R. C. Deo, S. K. Burley, and N. Sonenberg. 2001. Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol. Cell 7:205-216.
24. Kobayashi, T., A. A. Antar, K. W. Boehme, P. Danthi, E. A. Eby, K. M. Guglielmi, G. H. Holm, E. M. Johnson, M. S. Maginnis, S. Naik, W. B. Skelton, J. D. Wetzel, G. J. Wilson, J. D. Chappell, and T. S. Dermody. 2007. A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host Microbe 1:147-157.
25. Kohler, A., and E. Hurt. 2007. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 8:761-773.
26. Komoto, S., J. Sasaki, and K. Taniguchi. 2006. Reverse genetics system for introduction of site-specific mutations into the double-stranded RNA genome of infectious rotavirus. Proc. Natl. Acad. Sci. USA 103:4646-4651.
27. Kuhn, U., and E. Wahle. 2004. Structure and function of poly(A) binding proteins. Biochim. Biophys. Acta 1678:67-84.
28. Luo, Y., and D. J. Goss. 2001. Homeostasis in mRNA initiation: wheat germ poly(A)-binding protein lowers the activation energy barrier to initiation complex formation. J. Biol. Chem. 276:43083-43086.
29. Mangus, D. A., M. C. Evans, and A. Jacobson. 2003. Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4:223.
30. Michel, Y. M., D. Poncet, M. Piron, K. M. Kean, and A. M. Borman. 2000. Cap-poly(A) synergy in mammalian cell-free extracts: investigation of the requirements for poly(A)-mediated stimulation of translation initiation. J. Biol. Chem. 275:32268-32276.
31. Montero, H., M. Rojas, C. F. Arias, and S. Lopez. 2008. Rotavirus infection induces the phosphorylation of eIF2α but prevents the formation of stress granules. J. Virol. 82:1496-1504.
32. Murshudov, G. N., A. A. Vagin, and E. J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53:240-255.
33. Padilla-Noriega, L., O. Paniagua, and S. Guzman-Leon. 2002. Rotavirus protein NSP3 shuts off host cell protein synthesis. Virology 298:1-7.
34. Parashar, U. D., C. J. Gibson, J. S. Bresse, and R. I. Glass. 2006. Rotavirus and severe childhood diarrhea. Emerg. Infect. Dis. 12:304-306.
35. Pasdeloup, D., N. Poisson, H. Raux, Y. Gaudin, R. W. Ruigrok, and D. Blondel. 2005. Nucleocytoplasmic shuttling of the rabies virus P protein requires a nuclear localization signal and a CRM1-dependent nuclear export signal. Virology 334:284-293.
36. Patel, G. P., S. Ma, and J. Bag. 2005. The autoregulatory translational control element of poly(A)-binding protein mRNA forms a heteromeric ribonucleoprotein complex. Nucleic Acids Res. 33:7074-7089.
37. Pestova, T. V., V. G. Kolupaeva, I. B. Lomakin, E. V. Pilipenko, I. N. Shatsky, V. I. Agol, and C. U. Hellen. 2001. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA 98:7029-7036.
38. Piron, M., T. Delaunay, J. Grosclaude, and D. Poncet. 1999. Identification of the RNA-binding, dimerization, and eIF4GI-binding domains of rotavirus nonstructural protein NSP3. J. Virol. 73:5411-5421.
39. Piron, M., P. Vende, J. Cohen, and D. Poncet. 1998. Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J. 17:5811-5821.
40. Poncet, D., C. Aponte, and J. Cohen. 1993. Rotavirus protein NSP3 (NS34) is bound to the 3′ end consensus sequence of viral mRNAs in infected cells. J. Virol. 67:3159-3165.
41. Poncet, D., P. Lindenbaum, R. L'Haridon, and J. Cohen. 1997. In vivo and in vitro phosphorylation of rotavirus NSP5 correlates with its localization in viroplasms. J. Virol. 71:34-41.
42. Siddiqui, N., D. A. Mangus, T. C. Chang, J. M. Palermino, A. B. Shyu, and K. Gehring. 2007. Poly(A) nuclease interacts with the C-terminal domain of polyadenylate-binding protein domain from poly(A)-binding protein. J. Biol. Chem. 282:25067-25075.
43. Simon, E., and B. Seraphin. 2007. A specific role for the C-terminal region of the Poly(A)-binding protein in mRNA decay. Nucleic Acids Res. 35:6017-6028.
44. Siomi, H., and G. Dreyfuss. 1995. A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 129:551-560.
45. Tumbarello, D. A., M. C. Brown, and C. E. Turner. 2002. The paxillin LD motifs. FEBS Lett. 513:114-118.
46. Turner, C. E. 2000. Paxillin interactions. J. Cell Sci. 113:4139-4140.
47. Uchida, N., S. Hoshino, H. Imataka, N. Sonenberg, and T. Katada. 2002. A novel role of the mammalian GSPT/eRF3 associating with poly(A)-binding protein in Cap/Poly(A)-dependent translation. J. Biol. Chem. 277:50286-50292.
48. Vende, P., M. Piron, N. Castagne, and D. Poncet. 2000. Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA 3′ end. J. Virol. 74:7064-7071.
49. Vitour, D., P. Lindenbaum, P. Vende, M. M. Becker, and D. Poncet. 2004. RoXaN, a novel cellular protein containing TPR, LD, and zinc finger motifs, forms a ternary complex with eukaryotic initiation factor 4G and rotavirus NSP3. J. Virol. 78:3851-3862.
50. Woods, A. J., T. Kantidakis, H. Sabe, D. R. Critchley, and J. C. Norman. 2005. Interaction of paxillin with poly(A)-binding protein 1 and its role in focal adhesion turnover and cell migration. Mol. Cell. Biol. 25:3763-3773.
51. Woods, A. J., M. S. Roberts, J. Choudhary, S. T. Barry, Y. Mazaki, H. Sabe, S. J. Morley, D. R. Critchley, and J. C. Norman. 2002. Paxillin associates with poly(A)-binding protein 1 at the dense endoplasmic reticulum and the leading edge of migrating cells. J. Biol. Chem. 277:6428-6437.
52. Xu, A., A. R. Bellamy, and J. A. Taylor. 1998. BiP (GRP78) and endoplasmin (GRP94) are induced following rotavirus infection and bind transiently to an endoplasmic reticulum-localized virion component. J. Virol. 72:9865-9872.
53. Yoshida, M., K. Yoshida, G. Kozlov, N. S. Lim, G. De Crescenzo, Z. Pang, J. J. Berlanga, A. Kahvejian, K. Gehring, S. S. Wing, and N. Sonenberg. 2006. Poly(A) binding protein (PABP) homeostasis is mediated by the stability of its inhibitor, Paip2. EMBO J. 25:1934-1944.