Cotranscriptional recruitment of the nuclear poly(A)-binding protein Pab2 to nascent transcripts and association with translating mRNPs

Nucleic Acids Research

Volumn 37, Issue 10, 2009, Pages 3418-3430

  Lemieux, Caroline ^a   Bachand, François ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; POLYADENYLIC ACID BINDING PROTEIN 2; RIBONUCLEASE; RIBONUCLEOPROTEIN; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; MASS SPECTROMETRY; NONHUMAN; POLYADENYLATION; POLYSOME; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; RNA TRANSLATION; YEAST;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; GENE EXPRESSION REGULATION, FUNGAL; POLY(A)-BINDING PROTEIN II; POLYADENYLATION; PROTEIN BIOSYNTHESIS; RIBONUCLEOPROTEINS; RNA 3' END PROCESSING; RNA, MESSENGER; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION, GENETIC;

EUKARYOTA; MAMMALIA; SCHIZOSACCHAROMYCETACEAE;

EID: 67249129775     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp207     Document Type: Article

References (74)

1. Kuhn,U. and Wahle,E. (2004) Structure and function of poly(A) binding proteins. Biochim. Biophys. Acta, 1678, 67-84.
2. Mangus,D.A., Evans,M.C. and Jacobson,A. (2003) Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol., 4, 223.
3. Amrani,N., Ghosh,S., Mangus,D.A. and Jacobson,A. (2008) Translation factors promote the formation of two states of the closed-loop mRNP. Nature, 453, 1276-1280.
4. Wells,S.E., Hillner,P.E., Vale,R.D. and Sachs,A.B. (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell, 2, 135-140.
5. Amrani,N., Ganesan,R., Kervestin,S., Mangus,D.A., Ghosh,S. and Jacobson,A. (2004) A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature, 432, 112-118.
6. Behm-Ansmant,I., Gatfield,D., Rehwinkel,J., Hilgers,V. and Izaurralde,E. (2007) A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J., 26, 1591-1601.
7. Eberle,A.B., Stalder,L., Mathys,H., Orozco,R.Z. and Muhlemann,O. (2008) Posttranscriptional gene regulation by spatial rearrangement of the 3′ untranslated region. PLoS Biol., 6, e92.
8. Afonina,E., Stauber,R. and Pavlakis,G.N. (1998) The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J. Biol. Chem., 273, 13015-13021.
9. Brune,C., Munchel,S.E., Fischer,N., Podtelejnikov,A.V. and Weis,K. (2005) Yeast poly(A)-binding protein Pab1 shuttles between the nucleus and the cytoplasm and functions in mRNA export. RNA, 11, 517-531.
10. Dunn,E.F., Hammell,C.M., Hodge,C.A. and Cole,C.N. (2005) Yeast poly(A)-binding protein, Pab1, and PAN, a poly(A) nuclease complex recruited by Pab1, connect mRNA biogenesis to export. Genes Dev., 19, 90-103.
11. Chekanova,J.A. and Belostotsky,D.A. (2003) Evidence that poly(A) binding protein has an evolutionarily conserved function in facilitating mRNA biogenesis and export. RNA, 9, 1476-1490.
12. Hosoda,N., Lejeune,F. and Maquat,L.E. (2006) Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol. Cell Biol., 26, 3085-3097.
13. Buratowski,S. (2005) Connections between mRNA 3′ end processing and transcription termination. Curr. Opin. Cell Biol., 17, 257-261.
14. Proudfoot,N. and O'Sullivan,J. (2002) Polyadenylation: A tail of two complexes. Curr. Biol., 12, R855-R857.
15. Rosonina,E., Kaneko,S. and Manley,J.L. (2006) Terminating the transcript: Breaking up is hard to do. Genes Dev., 20, 1050-1056.
16. Hirose,Y. and Manley,J.L. (2000) RNA polymerase II and the integration of nuclear events. Genes Dev., 14, 1415-1429.
17. Moore,M.J. (2005) From birth to death: The complex lives of eukaryotic mRNAs. Science, 309, 1514-1518.
18. Phatnani,H.P. and Greenleaf,A.L. (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev., 20, 2922-2936.
19. Ahn,S.H., Kim,M. and Buratowski,S. (2004) Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing. Mol. Cell, 13, 67-76.
20. Kim,M., Ahn,S.H., Krogan,N.J., Greenblatt,J.F. and Buratowski,S. (2004) Transitions in RNA polymerase II elongation complexes at the 3′ ends of genes. EMBO J., 23, 354-364.
21. Runner,V.M., Podolny,V. and Buratowski,S. (2008) The Rpb4 subunit of RNA polymerase II contributes to cotranscriptional recruitment of 3′ processing factors. Mol. Cell Biol., 28, 1883-1891.
22. Glover-Cutter,K., Kim,S., Espinosa,J. and Bentley,D.L. (2008) RNA polymerase II pauses and associates with pre-mRNA processing factors at both ends of genes. Nat. Struct. Mol. Biol., 15, 71-78.
23. Swinburne,I.A., Meyer,C.A., Liu,X.S., Silver,P.A. and Brodsky,A.S. (2006) Genomic localization of RNA binding proteins reveals links between pre-mRNA processing and transcription. Genome Res., 16 912-921.
24. Edmonds,M. (2002) A history of poly A sequences: From formation to factors to function. Prog. Nucleic Acid Res. Mol. Biol., 71, 285-389.
25. Kerwitz,Y., Kuhn,U., Lilie,H., Knoth,A., Scheuermann,T., Friedrich,H., Schwarz,E. and Wahle,E. (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.
26. Wahle,E. (1995) Poly(A) tail length control is caused by termination of processive synthesis. J. Biol. Chem., 270, 2800-2808.
27. Perreault,A., Lemieux,C. and Bachand,F. (2007) Regulation of the nuclear poly(A)-binding protein by arginine methylation in fission yeast. J. Biol. Chem., 282, 7552-7562.
28. Cole,C.N. and Scarcelli,J.J. (2006) Transport of messenger RNA from the nucleus to the cytoplasm. Curr. Opin. Cell Biol., 18, 299-306.
29. Stewart,M. (2007) Ratcheting mRNA out of the nucleus. Mol. Cell, 25, 327-330.
30. Calado,A., Kutay,U., Kuhn,U., Wahle,E. and Carmo-Fonseca,M. (2000) Deciphering the cellular pathway for transport of poly(A)-binding protein II. RNA, 6, 245-256.
31. Ishigaki,Y., Li,X., Serin,G. and Maquat,L.E. (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.
32. Bahler,J., Wu,J.Q., Longtine,M.S., Shah,N.G., McKenzie,A. 3rd, Steever,A.B., Wach,A., Philippsen,P. and Pringle,J.R. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast, 14, 943-951.
33. Tasto,J.J., Carnahan,R.H., McDonald,W.H. and Gould,K.L. (2001) Vectors and gene targeting modules for tandem affinity purification in Schizosaccharomyces pombe. Yeast, 18, 657-662.
34. Mumberg,D., Muller,R. and Funk,M. (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene, 156, 119-122.
35. Forsburg,S.L. (1993) Comparison of Schizosaccharomyces pombe expression systems. Nucleic Acids Res., 21, 2955-2956.
36. Yu,M.C., Bachand,F., McBride,A.E., Komili,S., Casolari,J.M. and Silver,P.A. (2004) Arginine methyltransferase affects interactions and recruitment of mRNA processing and export factors. Genes Dev., 18, 2024-2035.
37. Abruzzi,K.C., Lacadie,S. and Rosbash,M. (2004) Biochemical analysis of TREX complex recruitment to intronless and introncontaining yeast genes. EMBO J., 23, 2620-2631.
38. Lei,E.P., Krebber,H. and Silver,P.A. (2001) Messenger RNAs are recruited for nuclear export during transcription. Genes Dev., 15, 1771-1782.
39. Bachand,F. and Silver,P.A. (2004) PRMT3 is a ribosomal protein methyltransferase that affects the cellular levels of ribosomal subunits. EMBO J., 23, 2641-2650.
40. Green,D.M., Marfatia,K.A., Crafton,E.B., Zhang,X., Cheng,X. and Corbett,A.H. (2002) Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p. J. Biol. Chem., 277, 7752-7760.
41. Nielsen,K.H., Szamecz,B., Valasek,L., Jivotovskaya,A., Shin,B.S. and Hinnebusch,A.G. (2004) Functions of eIF3 downstream of 48S assembly impact AUG recognition and GCN4 translational control. EMBO J., 23, 1166-1177.
42. Bear,D.G., Fomproix,N., Soop,T., Bjorkroth,B., Masich,S. and Daneholt,B. (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.
43. Lackner,D.H., Beilharz,T.H., Marguerat,S., Mata,J., Watt,S., Schubert,F., Preiss,T. and Bahler,J. (2007) A network of multiple regulatory layers shapes gene expression in fission yeast. Mol. Cell 26, 145-155.
44. Zenklusen,D., Vinciguerra,P., Wyss,J.C. and Stutz,F. (2002) Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Mol. Cell Biol., 22 8241-8253.
45. Maundrell,K. (1990) nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. J. Biol. Chem., 265, 10857-10864.
46. Krause,S., Fakan,S., Weis,K. and Wahle,E. (1994) Immunodetection of poly(A) binding protein II in the cell nucleus. Exp. Cell Res., 214, 75-82.
47. Lee,M.S., Henry,M. and Silver,P.A. (1996) A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes Dev., 10, 1233-1246.
48. Doye,V., Wepf,R. and Hurt,E.C. (1994) A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution. EMBO J., 13, 6062-6075.
49. Shen,E.C., Henry,M.F., Weiss,V.H., Valentini,S.R., Silver,P.A. and Lee,M.S. (1998) Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev., 12, 679-691.
50. Duncan,K., Umen,J.G. and Guthrie,C. (2000) A putative ubiquitin ligase required for efficient mRNA export differentially affects hnRNP transport. Curr. Biol., 10, 687-696.
51. Anderson,J.T., Paddy,M.R. and Swanson,M.S. (1993) PUB1 is a major nuclear and cytoplasmic polyadenylated RNA-binding protein in Saccharomyces cerevisiae. Mol. Cell Biol., 13, 6102-6113.
52. Mangus,D.A., Amrani,N. and Jacobson,A. (1998) Pbp1p, a factor interacting with Saccharomyces cerevisiae poly(A)-binding protein, regulates polyadenylation. Mol. Cell Biol., 18, 7383-7396.
53. Windgassen,M., Sturm,D., Cajigas,I.J., Gonzalez,C.I., Seedorf,M., Bastians,H. and Krebber,H. (2004) Yeast shuttling SR proteins Npl3p, Gbp2p, and Hrb1p are part of the translating mRNPs, and Npl3p can function as a translational repressor. Mol. Cell Biol., 24, 10479-10491.
54. Azzam,M.E. and Algranati,I.D. (1973) Mechanism of puromycin action: Fate of ribosomes after release of nascent protein chains from polysomes. Proc. Natl Acad. Sci. USA, 70, 3866-3869.
55. Daneholt,B. (2001) Assembly and transport of a premessenger RNP particle. Proc. Natl Acad. Sci. USA, 98, 7012-7017.
56. Benoit,B., Nemeth,A., Aulner,N., Kuhn,U., Simonelig,M., Wahle,E. and Bourbon,H.M. (1999) The Drosophila poly(A)-binding protein II is ubiquitous throughout Drosophila development and has the same function in mRNA polyadenylation as its bovine homolog in vitro. Nucleic Acids Res., 27, 3771-3778.
57. Wahle,E., Lustig,A., Jeno,P. and Maurer,P. (1993) Mammalian poly(A)-binding protein II. Physical properties and binding to polynucleotides. J. Biol. Chem., 268, 2937-2945.
58. Hurt,E., Luo,M.J., Rother,S., Reed,R. and Strasser,K. (2004) Cotranscriptional recruitment of the serine-arginine-rich (SR)-like proteins Gbp2 and Hrb1 to nascent mRNA via the TREX complex. Proc. Natl Acad. Sci. USA, 101, 1858-1862.
59. Calvo,O. and Manley,J.L. (2005) The transcriptional coactivator PC4/Sub1 has multiple functions in RNA polymerase II transcription. EMBO J. 24, 1009-1020.
60. Komarnitsky,P., Cho,E.J. and Buratowski,S. (2000) Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev., 14, 2452-2460.
61. Farny,N.G., Hurt,J.A. and Silver,P.A. (2008) Definition of global and transcript-specific mRNA export pathways in metazoans. Genes Dev., 22, 66-78.
62. Lei,E.P. and Silver,P.A. (2002) Intron status and 3′-end formation control cotranscriptional export of mRNA. Genes Dev., 16, 2761-2766.
63. Strasser,K., Masuda,S., Mason,P., Pfannstiel,J., Oppizzi,M., Rodriguez-Navarro,S., Rondon,A.G., Aguilera,A., Struhl,K., Reed,R. et al. (2002) TREX is a conserved complex coupling transcription with messenger RNA export. Nature, 417, 304-308.
64. Cheng,H., Dufu,K., Lee,C.S., Hsu,J.L., Dias,A. and Reed,R. (2006) Human mRNA export machinery recruited to the 5′ end of mRNA. Cell, 127, 1389-1400.
65. Masuda,S., Das,R., Cheng,H., Hurt,E., Dorman,N. and Reed,R. (2005) Recruitment of the human TREX complex to mRNA during splicing. Genes Dev., 19, 1512-1517.
66. Hilleren,P., McCarthy,T., Rosbash,M., Parker,R. and Jensen,T.H. (2001) Quality control of mRNA 30-end processing is linked to the nuclear exosome. Nature, 413, 538-542.
67. Benoit,B., Mitou,G., Chartier,A., Temme,C., Zaessinger,S., Wahle,E., Busseau,I. and Simonelig,M. (2005) An essential cytoplasmic function for the nuclear poly(A) binding protein, PABP2, in poly(A) tail length control and early development in Drosophila. Dev. Cell, 9, 511-522.
68. Chiu,S.Y., Lejeune,F., Ranganathan,A.C. and Maquat,L.E. (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.
69. Bolger,T.A., Folkmann,A.W., Tran,E.J. and Wente,S.R. (2008) The mRNA export factor Gle1 and inositol hexakisphosphate regulate distinct stages of translation. Cell, 134, 624-633.
70. Gross,T., Siepmann,A., Sturm,D., Windgassen,M., Scarcelli,J.J., Seedorf,M., Cole,C.N. and Krebber,H. (2007) The DEAD-box RNA helicase Dbp5 functions in translation termination. Science, 315, 646-649.
71. Michlewski,G., Sanford,J.R. and Caceres,J.F. (2008) The splicing factor SF2/ASF regulates translation initiation by enhancing phosphorylation of 4E-BP1. Mol. Cell, 30, 179-189.
72. Sanford,J.R., Gray,N.K., Beckmann,K. and Caceres,J.F. (2004) A novel role for shuttling SR proteins in mRNA translation. Genes Dev., 18, 755-768.
73. Sato,H., Hosoda,N. and Maquat,L.E. (2008) Efficiency of the pioneer round of translation affects the cellular site of nonsense-mediated mRNA decay. Mol. Cell, 29, 255-262.
74. Wilhelm,B.T., Marguerat,S., Watt,S., Schubert,F., Wood,V., Goodhead,I., Penkett,C.J., Rogers,J. and Bahler,J. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature, 453, 1239-1243.