Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails

Molecular and Cellular Biology

Volumn 26, Issue 8, 2006, Pages 3085-3097

  Hosoda, Nao ^a   Lejeune, Fabrice ^a,b   Maquat, Lynne E ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; MESSENGER RNA; MESSENGER RNA PRECURSOR; NUCLEAR PROTEIN; POLYADENYLIC ACID; POLYADENYLIC ACID BINDING PROTEIN; POLYADENYLIC ACID BINDING PROTEIN C1; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; INTRON; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN RNA BINDING; RNA DEGRADATION; RNA PROCESSING; RNA STABILITY; RNA TRANSLATION; RNA TRANSPORT;

ANIMALS; BLOTTING, WESTERN; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; CROSS-LINKING REAGENTS; HELA CELLS; HUMANS; INTRONS; POLY A; POLY(A)-BINDING PROTEIN I; POLYADENYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; ULTRAVIOLET RAYS;

ANIMALIA; MAMMALIA;

EID: 33645824089     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.8.3085-3097.2006     Document Type: Article

References (61)

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. Bear, D. G., N. Fomproix, T. Soop, B. Bjorkroth, S. Masich, and B. Daneholt. 2003. Nuclear poly(A)-binding protein PABPN1 is associated with RNA polymerase II during transcription and accompanies the released transcript to the nuclear pore. Exp. Cell Res. 286:332-344.
3. Belgrader, P., J. Cheng, X. Zhou, L. S. Stephenson, and L. E. Maquat. 1994. Mammalian nonsense codons can be cis effectors of nuclear mRNA half-life. Mol. Cell. Biol. 14:8219-8228.
4. Belgrader, P., and L. E. Maquat. 1994. Nonsense but not missense mutations can decrease the abundance of nuclear mRNA for the mouse major urinary protein, while both types of mutations can facilitate exon skipping. Mol. Cell. Biol. 14:6326-6336.
5. Bienroth, S., W. Keller, and E. Wahle. 1993. Assembly of a processive messenger RNA polyadenylation complex. EMBO J. 12:585-594.
6. Bird, G., N. Fong, J. C. Gatlin, S. Farabaugh, and D. L. Bentley. 2005. Ribozyme cleavage reveals connections between mRNA release from the site of transcription and pre-mRNA processing. Mol. Cell 20:747-758.
7. Brune, C., S. E. Munchel, N. Fischer, A. V. Podtelejnikov, and K. Weis. 2005. Yeast poly(A)-binding protein Pabl shuttles between the nucleus and the cytoplasm and functions in mRNA export. RNA 11:517-531.
8. Calado, A., and M. Carmo-Fonseca. 2000. Localization of poly(A)-binding protein 2 (PABP2) in nuclear speckles is independent of import into the nucleus and requires binding to poly(A) RNA. J. Cell Sci. 113:2309-2318.
9. Calado, A., U. Kutay, U. Kuhn, E. Wahle, and M. Carmo-Fonseca. 2000. Deciphering the cellular pathway for transport of poly(A)-binding protein II. RNA 6:245-256.
10. Chen, Z., Y. Li, and R. M. Krug. 1999. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′-end processing machinery. EMBO J. 18:2273-2283.
11. Chiu, S. Y., F. Lejeune, A. C. Ranganathan, and L. E. Maquat. 2004. The pioneer translation initiation complex is functionally distinct from but structurally overlaps with the steady-state translation initiation complex. Genes Dev. 18:745-754.
12. Chiu, S. Y., G. Serin, O. Ohara, and L. E. Maquat. 2003. Characterization of human Smg5/7a: a protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1. RNA 9:77-87.
13. Daneholt, B. 2001. Assembly and transport of a premessenger RNP particle. Proc. Natl. Acad. Sci. USA 98:7012-7017.
14. Davis, L. I., and G. Blobel. 1986. Identification and characterization of a nuclear pore complex protein. Cell 45:699-709.
15. Dominski, Z., and W. F. Marzluff. 1999. Formation of the 3′ end of histone mRNA. Gene 239:1-14.
16. Fan, X., P. Dion, J. Laganiere, B. Brais, and G. A. Rouleau. 2001. Oligomerization of polyalanine expanded PABPN1 facilitates nuclear protein aggregation that is associated with cell death. Hum. Mol. Genet. 10:2341-2351.
17. Feral, C., G. Guellaen, and A. Pawlak. 2001. Human testis expresses a specific poly(A)-binding protein. Nucleic Acids Res. 29:1872-1883.
18. 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.
19. Grange, T., C. M. de Sa, J. Oddos, and R. Pictet. 1987. Human mRNA polyadenylate binding protein: evolutionary conservation of a nucleic acid binding motif. Nucleic Acids Res. 15:4771-4787.
20. Grosset, C., C. Y. Chen, N. Xu, N. Sonenberg, H. Jacquemin-Sablon, and A. B. Shyu. 2000. A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell 103:29-40.
21. Hoshino, S., M. Imai, T. Kobayashi, N. Uchida, and T. Katada. 1999. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3′-poly(A) tail of mRNA. Direct association of eRF3/GSPT with polyadenylate-binding protein. J. Biol. Chem. 274:16677-16680.
22. Hosoda, N., Y. K. Kim, F. Lejeune, and L. E. Maquat. 2005. CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat. Struct. Mol. Biol. 12:893-901.
23. Imataka, H., A. Gradi, and N. Sonenberg. 1998. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 17:7480-7489.
24. Ishigaki, Y., X. Li, G. Serin, and L. E. Maquat. 2001. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106:607-617.
25. Izaurralde, E., J. Lewis, C. McGuigan, M. Jankowska, E. Darzynkiewicz, and I. W. Mattaj. 1994. A nuclear cap binding protein complex involved in pre-mRNA splicing. Cell 78:657-668.
26. Johnson, C., D. Primorac, M. McKinstry, J. McNeil, D. Rowe, and J. B. Lawrence. 2000. Tracking COL1A1 RNA in osteogenesis imperfecta: splice-defective transcripts initiate transport from the gene but are retained within the SC35 domain. J. Cell Biol. 150:417-432.
27. 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.
28. Kerwitz, Y., U. Kuhn, H. Lilie, A. Knoth, T. Scheuermann, H. Friedrich, E. Schwarz, and E. Wahle. 2003. Stimulation of poly(A) polymerase through a direct interaction with the nuclear poly(A) binding protein allosterically regulated by RNA. EMBO J. 22:3705-3714.
29. Khaleghpour, K., A. Kahvejian, G. De Crescenzo, G. Roy, Y. V. Svitkin, H. Imataka, M. O'Connor-McCourt, and N. Sonenberg. 2001. Dual interactions of the translational repressor Paip2 with poly(A) binding protein. Mol. Cell. Biol. 21:5200-5213.
30. Khanna, R., and M. Kiledjian. 2004. Poly(A)-binding-protein-mediated regulation of hDcp2 decapping in vitro. EMBO J. 23:1968-1976.
31. Krause, S., S. Fakan, K. Weis, and E. Wahle. 1994. Immunodetection of poly(A) binding protein II in the cell nucleus. Exp. Cell Res. 214:75-82.
32. Kuhn, U., and E. Wahle. 2004. Structure and function of poly(A) binding proteins. Biochim. Biophys. Acta 1678:67-84.
33. Kuyumcu-Martinez, M., G. Belliot, S. V. Sosnovtsev, K. O. Chang, K. Y. Green, and R. E. Lloyd. 2004. Calicivirus 3C-like proteinase inhibits cellular translation by cleavage of poly(A)-binding protein. J. Virol. 78:8172-8182.
34. Kyriakopoulou, C. B., H. Nordvarg, and A. Virtanen. 2001. A novel nuclear human poly(A) polymerase (PAP), PAPγ. J. Biol. Chem. 276:33504-33511.
35. Lejeune, F., Y. Ishigaki, X. Li, and L. E. Maquat. 2002. The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: dynamics of mRNP remodeling. EMBO J. 21:3536-3545.
36. Lejeune, F., X. Li, and L. E. Maquat. 2003. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12:675-687.
37. Lejeune, F., A. C. Ranganathan, and L. E. Maquat. 2004. eIF4G is required for the pioneer round of translation in mammalian cells. Nat. Struct. Mol. Biol. 11:992-1000.
38. Lewis, J. D., and E. Izaurralde. 1997. The role of the cap structure in RNA processing and nuclear export. Eur. J. Biochem. 247:461-469.
39. Mangus, D. A., M. C. Evans, N. S. Agrin, M. Smith, P. Gongidi, and A. Jacobson. 2004. Positive and negative regulation of poly(A) nuclease. Mol. Cell. Biol. 24:5521-5533.
40. 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.
41. Mangus, D. A., M. M. Smith, J. M. McSweeney, and A. Jacobson. 2004. Identification of factors regulating poly(A) tail synthesis and maturation. Mol. Cell. Biol. 24:4196-4206.
42. +- thalassemia. Proc. Natl. Acad. Sci. USA 77:4287-4291.
43. Maquat, L. E., A. J. Kinniburgh, E. A. Rachmilewitz, and J. Ross. 1981. Unstable beta-globin mRNA in mRNA-deficient beta°-thalassemia. Cell 27:543-553.
44. Maquat, L. E., and X. Li. 2001. Mammalian heat shock p70 and histone H4 transcripts, which derive from naturally intronless genes, are immune to nonsense-mediated decay. RNA 7:445-456.
45. Mili, S., and J. A. Steitz. 2004. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 10:1692-1694.
46. Nemeth, A., S. Krause, D. Blank, A. Jenny, P. Jene, A. Lustig, and E. Wahle. 1995. Isolation of genomic and cDNA clones encoding bovine poly(A) binding protein II. Nucleic Acids Res. 23:4034-4041.
47. Penalva, L. O., and J. D. Keene. 2004. Biotinylated tags for recovery and characterization of ribonucleoprotein complexes. BioTechniques 37:604, 606, 608-610.
48. Siomi, H., and G. Dreyfuss. 1995. A nuclear localization domain in the hnRNP Al protein. J. Cell Biol. 129:551-560.
49. Thomas, M. G., L. J. Martinez Tosar, M. Loschi, J. M. Pasquini, J. Correale, S. Kindler, and G. L. Boccaccio. 2005. Staufen recruitment into stress granules does not affect early mRNA transport in oligodendrocytes. Mol. Biol. Cell 16:405-420.
50. 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.
51. Uchida, N., S. Hoshino, and T. Katada. 2004. Identification of a human cytoplasmic poly(A) nuclease complex stimulated by poly(A)-binding protein. J. Biol. Chem. 279:1383-1391.
52. Visa, N., E. Izaurralde, J. Ferreira, B. Daneholt, and I. W. Mattaj. 1996. A nuclear cap-binding complex binds Balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export. J. Cell Biol. 133:5-14.
53. Wahle, E. 1991. A novel poly(A)-binding protein acts as a specificity factor in the second phase of messenger RNA polyadenylation. Cell 66:759-768.
54. 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.
55. Wang, Z., X. Jiao, A. Carr-Schmid, and M. Kiledjian. 2002. The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc. Natl. Acad. Sci. USA 99:12663-12668.
56. Wilusz, C. J., M. Gao, C. L. Jones, J. Wilusz, and S. W. Peltz. 2001. Poly(A)-binding proteins regulate both mRNA deadenylation and decapping in yeast cytoplasmic extracts. RNA 7:1416-1424.
57. 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.
58. 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.
59. Yamashita, A., T. C. Chang, Y. Yamashita, W. Zhu, Z. Zhong, C. Y. Chen, and A. B. Shyu. 2005. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat. Struct. Mol. Biol. 12:1054-1063.
60. Zhang, J., X. Sun, Y. Qian, J. P. LaDuca, and L. E. Maquat. 1998. At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol. Cell. Biol. 18:5272-5283.
61. Zhang, J., X. Sun, Y. Qian, and L. E. Maquat. 1998. Intron function in the nonsense-mediated decay of beta-globin mRNA: indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 4:801-815.