Poly(A) tail-mediated gene regulation by opposing roles of Nab2 and Pab2 nuclear poly(A)-binding proteins in pre-mRNA decay

Molecular and Cellular Biology

Volumn 33, Issue 23, 2013, Pages 4718-4731

  St Sauveur, Valérie Grenier ^a   Soucek, Sharon ^b   Corbett, Anita H ^b   Bachand, François ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; MESSENGER RNA; MESSENGER RNA PRECURSOR; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN NAB2; PROTEIN PAB2; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; PAB2 PROTEIN, S POMBE; RIBOSOME PROTEIN; RIBOSOME PROTEIN L3; RNA BINDING PROTEIN; RNA PRECURSOR; SCHIZOSACCHAROMYCES POMBE PROTEIN; SPNAB2 PROTEIN, S POMBE; NAB2 PROTEIN, S POMBE; RIBOSOMAL PROTEIN L3;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA SEQUENCE; EUKARYOTE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA DEGRADATION; SCHIZOSACCHAROMYCES POMBE; AMINO ACID SEQUENCE; CHEMISTRY; GENE INACTIVATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYADENYLATION; RNA STABILITY; SCHIZOSACCHAROMYCES;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; MOLECULAR SEQUENCE DATA; POLY(A)-BINDING PROTEINS; POLYADENYLATION; RIBOSOMAL PROTEINS; RNA PRECURSORS; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84891681546     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00887-13     Document Type: Article

References (63)

1. LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, Tollervey D. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121:713-724.
2. Lemay JF, D'Amours A, Lemieux C, Lackner DH, St-Sauveur VG, Bahler J, Bachand F. 2010. The nuclear poly(A)-binding protein interacts with the exosome to promote synthesis of noncoding small nucleolar RNAs. Mol. Cell 37:34-45.
3. St-Andre O, Lemieux C, Perreault A, Lackner DH, Bahler J, Bachand F. 2010. Negative regulation of meiotic gene expression by the nuclear poly(A)-binding protein in fission yeast. J. Biol. Chem. 285:27859-27868.
4. Vanacova S, Wolf J, Martin G, Blank D, Dettwiler S, Friedlein A, Langen H, Keith G, Keller W. 2005. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3:e189. doi:10.1371/journal.pbio.0030189.
5. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, Regnault B, Devaux F, Namane A, Seraphin B, Libri D, Jacquier A. 2005. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121:725-737.
6. Lemay JF, Lemieux C, St-Andre O, Bachand F. 2010. Crossing the borders: poly(A)-binding proteins working on both sides of the fence. RNA Biol. 7:291-295.
7. Kuhn U, Gundel M, Knoth A, Kerwitz Y, Rudel S, Wahle E. 2009. Poly(A) tail length is controlled by the nuclear poly(A)-binding protein regulating the interaction between poly(A) polymerase and the cleavage and polyadenylation specificity factor. J. Biol. Chem. 284:22803-22814.
8. Apponi LH, Leung SW, Williams KR, Valentini SR, Corbett AH, Pavlath GK. 2010. Loss of nuclear poly(A)-binding protein 1 causes defects in myogenesis and mRNA biogenesis. Hum. Mol. Genet. 19:1058-1065.
9. de Klerk E, Venema A, Anvar SY, Goeman JJ, Hu O, Trollet C, Dickson G, den Dunnen JT, van der Maarel SM, Raz V, t'Hoen PA. 2012. Poly(A) binding protein nuclear 1 levels affect alternative polyadenylation. Nucleic Acids Res. 40:9089-9101.
10. Jenal M, Elkon R, Loayza-Puch F, van Haaften G, Kuhn U, Menzies FM, Oude Vrielink JA, Bos AJ, Drost J, Rooijers K, Rubinsztein DC, Agami R. 2012. The poly(A)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites. Cell 149:538-553.
11. Beaulieu YB, Kleinman CL, Landry-Voyer AM, Majewski J, Bachand F. 2012. Polyadenylation-dependent control of long noncoding RNA expression by the poly(A)-binding protein nuclear 1. PLoS Genet. 8:e1003078. doi:10.1371/journal.pgen.1003078.
12. Januszyk K, Lima CD. 2010. Structural components and architectures of RNA exosomes. Adv. Exp. Med. Biol. 702:9-28.
13. Schmid M, Jensen TH. 2008. The exosome: a multipurpose RNA-decay machine. Trends Biochem. Sci. 33:501-510.
14. Lemieux C, Marguerat S, Lafontaine J, Barbezier N, Bahler J, Bachand F. 2011. A pre-mRNA degradation pathway that selectively targets introncontaining genes requires the nuclear poly(A)-binding protein. Mol. Cell 44:108-119.
15. Kuhn U, Wahle E. 2004. Structure and function of poly(A) binding proteins. Biochim. Biophys. Acta 1678:67-84.
16. Mangus DA, Evans MC, Jacobson A. 2003. Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4:223.
17. Kelly SM, Pabit SA, Kitchen CM, Guo P, Marfatia KA, Murphy TJ, Corbett AH, Berland KM. 2007. Recognition of polyadenosine RNA by zinc finger proteins. Proc. Natl. Acad. Sci. U. S. A. 104:12306-12311.
18. Leung SW, Apponi LH, Cornejo OE, Kitchen CM, Valentini SR, Pavlath GK, Dunham CM, Corbett AH. 2009. Splice variants of the human ZC3H14 gene generate multiple isoforms of a zinc finger polyadenosine RNA binding protein. Gene 439:71-78.
19. Brockmann C, Soucek S, Kuhlmann SI, Mills-Lujan K, Kelly SM, Yang JC, Iglesias N, Stutz F, Corbett AH, Neuhaus D, Stewart M. 2012. Structural basis for polyadenosine-RNA binding by Nab2 Zn fingers and its function in mRNA nuclear export. Structure 20:1007-1018.
20. Kelly SM, Leung SW, Apponi LH, Bramley AM, Tran EJ, Chekanova JA, Wente SR, Corbett AH. 2010. Recognition of polyadenosine RNA by the zinc finger domain of nuclear poly(A) RNA-binding protein 2 (Nab2) is required for correct mRNA 3'-end formation. J. Biol. Chem. 285:26022-26032.
21. Soucek S, Corbett AH, Fasken MB. 2012. The long and the short of it: the role of the zinc finger polyadenosine RNA binding protein, Nab2, in control of poly(A) tail length. Biochim. Biophys. Acta 1819:546-554.
22. Iglesias N, Tutucci E, Gwizdek C, Vinciguerra P, Von Dach E, Corbett AH, Dargemont C, Stutz F. 2010. Ubiquitin-mediated mRNP dynamics and surveillance prior to budding yeast mRNA export. Genes Dev. 24:1927-1938.
23. Green DM, Marfatia KA, Crafton EB, Zhang X, Cheng X, Corbett AH. 2002. Nab2p is required for poly(A)RNAexport in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p. J. Biol. Chem. 277:7752-7760.
24. Grant RP, Marshall NJ, Yang JC, Fasken MB, Kelly SM, Harreman MT, Neuhaus D, Corbett AH, Stewart M. 2008. Structure of the N-terminal Mlp1-binding domain of the Saccharomyces cerevisiae mRNA-binding protein, Nab2. J. Mol. Biol. 376:1048-1059.
25. Hector RE, Nykamp KR, Dheur S, Anderson JT, Non PJ, Urbinati CR, Wilson SM, Minvielle-Sebastia L, Swanson MS. 2002. Dual requirement for yeast hnRNP Nab2p in mRNA poly(A) tail length control and nuclear export. EMBO J. 21:1800-1810.
26. Batisse J, Batisse C, Budd A, Bottcher B, Hurt E. 2009. Purification of nuclear poly(A)-binding protein Nab2 reveals association with the yeast transcriptome and a messenger ribonucleoprotein core structure. J. Biol. Chem. 284:34911-34917.
27. Schmid M, Poulsen MB, Olszewski P, Pelechano V, Saguez C, Gupta I, Steinmetz LM, Moore C, Jensen TH. 2012. Rrp6p controls mRNA poly(A) tail length and its decoration with poly(A) binding proteins. Mol. Cell 47:267-280.
28. Kelly S, Pak C, Garshasbi M, Kuss A, Corbett AH, Moberg K. 2012. New kid on the ID block: neural functions of the Nab2/ZC3H14 class of Cys(3)His tandem zinc-finger polyadenosineRNAbinding proteins.RNA Biol. 9:555-562.
29. Pak C, Garshasbi M, Kahrizi K, Gross C, Apponi LH, Noto JJ, Kelly SM, Leung SW, Tzschach A, Behjati F, Abedini SS, Mohseni M, Jensen LR, Hu H, Huang B, Stahley SN, Liu G, Williams KR, Burdick S, Feng Y, Sanyal S, Bassell GJ, Ropers HH, Najmabadi H, Corbett AH, Moberg KH, Kuss AW. 2011. Mutation of the conserved polyadenosine RNA binding protein, ZC3H14/dNab2, impairs neural function in Drosophila and humans. Proc. Natl. Acad. Sci. U. S. A. 108:12390-12395.
30. Guthrie CR, Schellenberg GD, Kraemer BC. 2009. SUT-2 potentiates tau-induced neurotoxicity in Caenorhabditis elegans. Hum. Mol. Genet. 18:1825-1838.
31. Bahler J, Wu JQ, Longtine MS, Shah NG, McKenzie A, III, Steever AB, Wach A, Philippsen P, Pringle JR. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14:943-951.
32. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201.
33. Brunger AT. 2007. Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2:2728-2733.
34. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
35. Beaudoin J, Labbe S. 2006. Copper induces cytoplasmic retention of fission yeast transcription factor cuf1. Eukaryot. Cell 5:277-292.
36. Craven RA, Griffiths DJ, Sheldrick KS, Randall RE, Hagan IM, Carr AM. 1998. Vectors for the expression of tagged proteins in Schizosaccharomyces pombe. Gene 221:59-68.
37. Mallet PL, Bachand F. 2013. A proline-tyrosine nuclear localization signal (PY-NLS) is required for the nuclear import of fission yeast PAB2, but not of human PABPN1. Traffic 14:282-294.
38. Perreault A, Lemieux C, Bachand F. 2007. Regulation of the nuclear poly(A)-binding protein by arginine methylation in fission yeast. J. Biol. Chem. 282:7552-7562.
39. Oeffinger M. 2012. Two steps forward-one step back: advances in affinity purification mass spectrometry of macromolecular complexes. Proteomics 12:1591-1608.
40. Lackner DH, Beilharz TH, Marguerat S, Mata J, Watt S, Schubert F, Preiss T, Bahler J. 2007. A network of multiple regulatory layers shapes gene expression in fission yeast. Mol. Cell 26:145-155.
41. Larochelle M, Lemay JF, Bachand F. 2012. The THO complex cooperates with the nuclear RNA surveillance machinery to control small nucleolar RNA expression. Nucleic Acids Res. 40:10240-10253.
42. Berriz GF, King OD, Bryant B, Sander C, Roth FP. 2003. Characterizing gene sets with FuncAssociate. Bioinformatics 19:2502-2504.
43. Grigull J, Mnaimneh S, Pootoolal J, Robinson MD, Hughes TR. 2004. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24:5534-5547.
44. Habara Y, Urushiyama S, Shibuya T, Ohshima Y, Tani T. 2001. Mutation in the prp12+ gene encoding a homolog of SAP130/SF3b130 causes differential inhibition of pre-mRNA splicing and arrest of cell-cycle progression in Schizosaccharomyces pombe. RNA 7:671-681.
45. Midtgaard SF, Assenholt J, Jonstrup AT, Van LB, Jensen TH, Brodersen DE. 2006. Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain. Proc. Natl. Acad. Sci. U. S. A. 103:11898-11903.
46. Phillips S, Butler JS. 2003. Contribution of domain structure to the RNA 3' end processing and degradation functions of the nuclear exosome subunit Rrp6p. RNA 9:1098-1107.
47. Banerjee A, Apponi LH, Pavlath GK, Corbett AH. 2013. PABPN1: molecular function and muscle disease. FEBS J. 280:4230-4250.
48. Winstall E, Sadowski M, Kuhn U, Wahle E, Sachs AB. 2000. The Saccharomyces cerevisiae RNA-binding protein Rbp29 functions in cytoplasmic mRNA metabolism. J. Biol. Chem. 275:21817-21826.
49. Marguerat S, Schmidt A, Codlin S, Chen W, Aebersold R, Bahler J. 2012. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151:671-683.
50. Eckmann CR, Rammelt C, Wahle E. 2011. Control of poly(A) tail length. Wiley Interdiscip. Rev. RNA 2:348-361.
51. Viphakone N, Voisinet-Hakil F, Minvielle-Sebastia L. 2008. Molecular dissection of mRNApoly(A) tail length control in yeast. Nucleic Acids Res. 36:2418-2433.
52. Chen HM, Futcher B, Leatherwood J. 2011. The fission yeast RNA binding protein Mmi1 regulates meiotic genes by controlling intron specific splicing and polyadenylation coupled RNA turnover. PLoS One 6:e26804. doi:10.1371/journal.pone.0026804.
53. Yamanaka S, Yamashita A, Harigaya Y, Iwata R, Yamamoto M. 2010. Importance of polyadenylation in the selective elimination of meiotic mRNAs in growing S. pombe cells. EMBO J. 29:2173-2181.
54. Bhattacharjee RB, Bag J. 2012. Depletion of nuclear poly(A) binding protein PABPN1 produces a compensatory response by cytoplasmic PABP4 and PABP5 in cultured human cells. PLoS One 7:e53036. doi:10.1371/journal.pone.0053036.
55. Hosoda N, Lejeune F, Maquat LE. 2006. Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol. Cell. Biol. 26:3085-3097.
56. Shi Y, Di Giammartino DC, Taylor D, Sarkeshik A, Rice WJ, Yates JR, III, Frank J, Manley JL. 2009. Molecular architecture of the human pre-mRNA 3' processing complex. Mol. Cell 33:365-376.
57. Dunn EF, Hammell CM, Hodge CA, Cole CN. 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.
58. Le H, Browning KS, Gallie DR. 2000. The phosphorylation state of poly(A)-binding protein specifies its binding to poly(A) RNA and its interaction with eukaryotic initiation factor (eIF) 4F, eIFiso4F, and eIF4B. J. Biol. Chem. 275:17452-17462.
59. Lee J, Bedford MT. 2002. PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays.EMBORep. 3:268-273.
60. Sipiczki M. 2000. Where does fission yeast sit on the tree of life? Genome Biol. 1:REVIEWS1011. doi:10.1186/gb-2000-1-2-reviews1011.
61. de Almeida SF, Garcia-Sacristan A, Custodio N, Carmo-Fonseca M. 2010. A link between nuclear RNA surveillance, the human exosome and RNA polymerase II transcriptional termination. Nucleic Acids Res. 38:8015-8026.
62. Eberle AB, Hessle V, Helbig R, Dantoft W, Gimber N, Visa N. 2010. Splice-site mutations cause Rrp6-mediated nuclear retention of the unspliced RNAs and transcriptional down-regulation of the splicingdefective genes. PLoS One 5:e11540. doi:10.1371/journal.pone.0011540.
63. Brais B, Bouchard JP, Xie YG, Rochefort DL, Chretien N, Tome FM, Lafreniere RG, Rommens JM, Uyama E, Nohira O, Blumen S, Korczyn AD, Heutink P, Mathieu J, Duranceau A, Codere F, Fardeau M, Rouleau GA. 1998. Short GCG expansions in the PABP2 gene cause oculopharyngeal muscular dystrophy. Nat. Genet. 18:164-167.