The Ccr4-Not complex interacts with the mRNA Export Machinery

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Kerr, Shana C ^a   Azzouz, Nowel ^b   Fuchs, Stephen M ^c   Collart, Martine A ^b   Strahl, Brian D ^c   Corbett, Anita H ^a   Laribee, R Nicholas ^d  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR4; HEPATOMA DERIVED GROWTH FACTOR; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA; NOT PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN HRP1; PROTEIN NAB2; REGULATOR PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; CCR4 PROTEIN, S CEREVISIAE; HMT1 PROTEIN, S CEREVISIAE; MULTIPROTEIN COMPLEX; MUTANT PROTEIN; POLYADENYLIC ACID; PROTEIN SUBUNIT; REPRESSOR PROTEIN; RIBONUCLEASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BIOGENESIS; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE OVEREXPRESSION; IMMUNOPRECIPITATION; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR PORE COMPLEX; ORTHOLOGY; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN RNA BINDING; RNA PROCESSING; RNA TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; YEAST; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MUTATION; NUCLEAR PORE; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; SACCHAROMYCETALES;

HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; MULTIPROTEIN COMPLEXES; MUTANT PROTEINS; MUTATION; NUCLEAR PORE; POLY A; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN-ARGININE N-METHYLTRANSFERASES; REPRESSOR PROTEINS; RIBONUCLEASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA TRANSPORT; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 79953152192     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018302     Document Type: Article

References (91)

1. Aguilera A, (2005) Cotranscriptional mRNP assembly: from the DNA to the nuclear pore. Current Opinion in Cell Biology 17: 242.
2. Vinciguerra P, Stutz F, (2004) mRNA export: an assembly line from genes to nuclear pores. Current Opinion in Cell Biology 16: 285.
3. Erkmann JA, Kutay U, (2004) Nuclear export of mRNA: from the site of transcription to the cytoplasm. Experimental Cell Research 296: 12.
4. Kohler A, Hurt E, (2007) Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 8: 761.
5. Carmody SR, Wente SR, (2009) mRNA nuclear export at a glance. J Cell Sci 122: 1933-1937.
6. Rodriguez MS, Dargemont C, Stutz F, (2004) Nuclear export of RNA. Biology of the Cell 96: 639.
7. Dreyfuss G, Kim VN, Kataoka N, (2002) Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3: 195.
8. Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG, (1993) hnRNP Proteins and the Biogenesis of mRNA. Annual Review of Biochemistry 62: 289-321.
9. Kessler MM, Henry MF, Shen E, Zhao J, Gross S, et al. (1997) Hrp1, a sequence-specific RNA-binding protein that shuttles between the nucleus and the cytoplasm, is required for mRNA 3′-end formation in yeast. Genes & Development 11: 2545-2556.
10. Kelly SM, Pabit SA, Kitchen CM, Guo P, Marfatia KA, et al. (2007) Recognition of polyadenosine RNA by zinc finger proteins. Proceedings of the National Academy of Sciences 104: 12306-12311.
11. Hector RE, Nykamp KR, Dheur S, Anderson JT, Non PJ, et al. (2002) Dual requirement for yeast hnRNP Nab2p in mRNA poly(A) tail length control and nuclear export. EMBO J 21: 1800.
12. Marfatia KA, Crafton EB, Green DM, Corbett AH, (2003) Domain Analysis of the Saccharomyces cerevisiae Heterogeneous Nuclear Ribonucleoprotein, Nab2p. DISSECTING THE REQUIREMENTS FOR Nab2p-FACILITATED POLY(A) RNA EXPORT. J Biol Chem 278: 6731-6740.
13. Dermody JL, Dreyfuss JM, Villén J, Ogundipe B, Gygi SP, et al. (2008) Unphosphorylated SR-Like Protein Npl3 Stimulates RNA Polymerase II Elongation. PLoS ONE 3: e3273.
14. Kress TL, Krogan NJ, Guthrie C, (2008) A Single SR-like Protein, Npl3, Promotes Pre-mRNA Splicing in Budding Yeast. Molecular Cell 32: 727.
15. Lim R, Aebi U, Fahrenkrog B, (2008) Towards reconciling structure and function in the nuclear pore complex. Histochemistry and Cell Biology 129: 105.
16. Suntharalingam M, Wente SR, (2003) Peering through the Pore: Nuclear Pore Complex Structure, Assembly, and Function. Developmental Cell 4: 775.
17. Terry LJ, Wente SR, (2007) Nuclear mRNA export requires specific FG nucleoporins for translocation through the nuclear pore complex. J Cell Biol 178: 1121-1132.
18. Sträßer K, Hurt E, (1999) Nuclear RNA export in yeast. FEBS Letters 452: 77.
19. Doye V, Wepf R, Hurt E, (1994) A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution. The EMBO Journal 13: 6062-6075.
20. Aitchison JD, Blobel G, Rout MP, (1995) Nup120p: a yeast nucleoporin required for NPC distribution and mRNA transport. J Cell Biol 131: 1659-1675.
21. Bogerd AM, Hoffman JA, Amberg DC, Fink GR, Davis LI, (1994) nup1 mutants exhibit pleiotropic defects in nuclear pore complex function. J Cell Biol 127: 319-332.
22. Wente SR, Blobel G, (1993) A temperature-sensitive NUP116 null mutant forms a nuclear envelope seal over the yeast nuclear pore complex thereby blocking nucleocytoplasmic traffic. J Cell Biol 123: 275-284.
23. Fabre E, Boelens WC, Wimmer C, Mattaj IW, Hurt EC, (1994) Nup145p is required for nuclear export of mRNA and binds homopolymeric RNA in vitro via a novel conserved motif. Cell 78: 275.
24. Ahmed S, Brickner JH, (2007) Regulation and epigenetic control of transcription at the nuclear periphery. Trends in Genetics 23: 396.
25. Blobel G, (1985) Gene gating: a hypothesis. Proceedings of the National Academy of Sciences of the United States of America 82: 8527-8529.
26. Collart MA, (2003) Global control of gene expression in yeast by the Ccr4-Not complex. Gene 313: 1.
27. Collart MA, Timmers HTM, Kivie M, (2004) The Eukaryotic Ccr4-Not Complex: A Regulatory Platform Integrating mRNA Metabolism with Cellular Signaling Pathways? Progress in Nucleic Acid Research and Molecular Biology Academic Press.
28. Tucker M, Valencia-Sanchez MA, Staples RR, Chen J, Denis CL, et al. (2001) The Transcription Factor Associated Ccr4 and Caf1 Proteins Are Components of the Major Cytoplasmic mRNA Deadenylase in Saccharomyces cerevisiae. Cell 104: 377.
29. Viswanathan P, Ohn T, Chiang Y-C, Chen J, Denis CL, (2004) Mouse CAF1 Can Function As a Processive Deadenylase/3′-5′-Exonuclease in Vitro but in Yeast the Deadenylase Function of CAF1 Is Not Required for mRNA Poly(A) Removal. Journal of Biological Chemistry 279: 23988-23995.
30. Chen J, Chiang Y-C, Denis CL, (2002) CCR4, a 3[prime]-5[prime] poly(A) RNA and ssDNA exonuclease, is the catalytic component of the cytoplasmic deadenylase. EMBO J 21: 1414.
31. Albert TK, Hanzawa H, Legtenberg YIA, de Ruwe MJ, van den Heuvel FAJ, et al. (2002) Identification of a ubiquitin-protein ligase subunit within the CCR4-NOT transcription repressor complex. EMBO J 21: 355.
32. Panasenko O, Landrieux E, Feuermann M, Finka A, Paquet N, et al. (2006) The Yeast Ccr4-Not Complex Controls Ubiquitination of the Nascent-associated Polypeptide (NAC-EGD) Complex. Journal of Biological Chemistry 281: 31389-31398.
33. Mersman DP, Du H-N, Fingerman IM, South PF, Briggs SD, (2009) Polyubiquitination of the demethylase Jhd2 controls histone methylation and gene expression. Genes & Development 23: 951-962.
34. Cui Y, Ramnarain D, Chiang Y-C, Ding L-H, McMahon J, et al. (2008) Genome wide expression analysis of the CCR4-NOT complex indicates that it consists of three modules with the NOT module controlling SAGA-responsive genes. Molecular Genetics and Genomics 279: 323.
35. Azzouz N, Panasenko OO, Deluen Cc, Hsieh J, Theiler Gg, et al. (2009) Specific roles for the Ccr4-Not complex subunits in expression of the genome. RNA 15: 377-383.
36. Benson JD, Benson M, Howley PM, Struhl K, (1998) Association of distinct yeast Not2 functional domains with components of Gcn5 histone acetylase and Ccr4 transcriptional regulatory complexes. EMBO J 17: 6714.
37. Laribee RN, Shibata Y, Mersman DP, Collins SR, Kemmeren P, et al. (2007) CCR4/NOT complex associates with the proteasome and regulates histone methylation. Proceedings of the National Academy of Sciences 104: 5836-5841.
38. Chang M, French-Cornay D, Fan H-y, Klein H, Denis CL, et al. (1999) A Complex Containing RNA Polymerase II, Paf1p, Cdc73p, Hpr1p, and Ccr4p Plays a Role in Protein Kinase C Signaling. Mol Cell Biol 19: 1056-1067.
39. Deluen C, James N, Maillet L, Molinete M, Theiler G, et al. (2002) The Ccr4-Not Complex and yTAF1 (yTafII130p/yTafII145p) Show Physical and Functional Interactions. Mol Cell Biol 22: 6735-6749.
40. Lemaire M, Collart MA, (2000) The TATA-binding Protein-associated Factor yTafII19p Functionally Interacts with Components of the Global Transcriptional Regulator Ccr4-Not Complex and Physically Interacts with the Not5 Subunit. Journal of Biological Chemistry 275: 26925-26934.
41. Azzouz N, Panasenko OO, Colau G, Collart MA, (2009) The CCR4-NOT Complex Physically and Functionally Interacts with TRAMP and the Nuclear Exosome. PLoS ONE 4: e6760.
42. Robin-Lespinasse Y, Sentis S, Kolytcheff C, Rostan M-C, Corbo L, et al. (2007) hCAF1, a new regulator of PRMT1-dependent arginine methylation. J Cell Sci 120: 638-647.
43. Henry MF, Silver PA, (1996) A novel methyltransferase (Hmt1p) modifies poly(A)+-RNA-binding proteins. Mol Cell Biol 16: 3668-3678.
44. Shen EC, Henry MF, Weiss VH, Valentini SR, Silver PA, et al. (1998) Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes & Development 12: 679-691.
45. Green DM, Marfatia KA, Crafton EB, Zhang X, Cheng X, et al. (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.
46. McBride AE, Weiss VH, Kim HK, Hogle JM, Silver PA, (2000) Analysis of the Yeast Arginine Methyltransferase Hmt1p/Rmt1p and Its in Vivo Function. Journal of Biological Chemistry 275: 3128-3136.
47. Siebel CW, Guthrie C, (1996) The essential yeast RNA binding protein Npl3p is methylated. Proceedings of the National Academy of Sciences of the United States of America 93: 13641-13646.
48. Wilson SM, Datar KV, Paddy MR, Swedlow JR, Swanson MS, (1994) Characterization of nuclear polyadenylated RNA-binding proteins in Saccharomyces cerevisiae. J Cell Biol 127: 1173-1184.
49. Lenssen E, Azzouz N, Michel A, Landrieux E, Collart MA, (2007) The Ccr4-Not Complex Regulates Skn7 through Srb10 Kinase. Eukaryotic Cell 6: 2251-2259.
50. Thomas D, Surdin-Kerjan Y, (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 61: 503-532.
51. Strambio-de-Castillia C, Blobel G, Rout MP, (1999) Proteins Connecting the Nuclear Pore Complex with the Nuclear Interior. J Cell Biol 144: 839-855.
52. Feuerbach F, Galy V, Trelles-Sticken E, Fromont-Racine M, Jacquier A, et al. (2002) Nuclear architecture and spatial positioning help establish transcriptional states of telomeres in yeast. Nature Cell Biology 4: 214-221.
53. Dilworth DJ, Suprapto A, Padovan JC, Chait BT, Wozniak RW, et al. (2001) Nup2p Dynamically Associates with the Distal Regions of the Yeast Nuclear Pore Complex. The Journal of Cell Biology 153: 1465-1478.
54. Chavez S, Beilharz T, Rondon AG, Erdjument-Bromage H, Tempst P, et al. (2000) A protein complex containing Tho2, Hpr1, Mft1 and a novel protein, Thp2, connects transcription elongation with mitotic recombination in Saccharomyces cerevisiae. EMBO J 19: 5824.
55. Straszer K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, et al. (2002) TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417: 304.
56. Snay-Hodge CA, Colot HV, Goldstein AL, Cole CN, (1998) Dbp5p/Rat8p is a yeast nuclear pore-associated DEAD-box protein essential for RNA export. EMBO J 17: 2663.
57. Tseng SSI, Weaver PL, Liu Y, Hitomi M, Tartakoff AM, et al. (1998) Dbp5p, a cytosolic RNA helicase, is required for poly(A)+ RNA export. EMBO J 17: 2651.
58. Strasser K, Hurt E, (2000) Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J 19: 410.
59. Galy V, Gadal O, Fromont-Racine M, Romano A, Jacquier A, et al. (2004) Nuclear Retention of Unspliced mRNAs in Yeast Is Mediated by Perinuclear Mlp1. Cell 116: 63-73.
60. Vinciguerra P, Iglesias N, Camblong J, Zenklusen D, Stutz F, (2005) Perinuclear Mlp proteins downregulate gene expression in response to a defect in mRNA export. The EMBO Journal 24: 813-823.
61. Green DM, Johnson CP, Hagan H, Corbett AH, (2003) The C-terminal domain of myosin-like protein 1 (Mlp1p) is a docking site for heterogeneous nuclear ribonucleoproteins that are required for mRNA export. PNAS 100: 1010-1015.
62. Strawn LA, Shen T, Wente SR, (2001) The GLFG Regions of Nup116p and Nup100p Serve as Binding Sites for Both Kap95p and Mex67p at the Nuclear Pore Complex. Journal of Biological Chemistry 276: 6445-6452.
63. Mulder KW, Inagaki A, Cameroni E, Mousson F, Winkler GS, et al. (2007) Modulation of Ubc4p/Ubc5p-Mediated Stress Responses by the RING-Finger-Dependent Ubiquitin-Protein Ligase Not4p in Saccharomyces cerevisiae. Genetics 176: 181-192.
64. Xu C, Henry PA, Setya A, Henry MF, (2003) In vivo analysis of nucleolar proteins modified by the yeast arginine methyltransferase Hmt1/Rmt1p. RNA 9: 746-759.
65. Taura T, Krebber H, Silver PA, (1998) A member of the Ran-binding protein family, Yrb2p, is involved in nuclear protein export. Proceedings of the National Academy of Sciences of the United States of America 95: 7427-7432.
66. Yan C, Lee LH, Davis LI, (1998) Crm1p mediates regulated nuclear export of a yeast AP-1-like transcription factor. EMBO J 17: 7416.
67. Loeb JD, Schlenstedt G, Pellman D, Kornitzer D, Silver PA, et al. (1995) The yeast nuclear import receptor is required for mitosis. Proceedings of the National Academy of Sciences of the United States of America 92: 7647-7651.
68. Pulliam KF, Fasken MB, McLane LM, Pulliam JV, Corbett AH, (2009) The Classical Nuclear Localization Signal Receptor, Importin-{alpha}, Is Required for Efficient Transition Through the G1/S Stage of the Cell Cycle in Saccharomyces cerevisiae. Genetics 181: 105-118.
69. Gavin A-C, Bosche M, Krause R, Grandi P, Marzioch M, et al. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141.
70. Wilmes GM, Bergkessel M, Bandyopadhyay S, Shales M, Braberg H, et al. (2008) A Genetic Interaction Map of RNA-Processing Factors Reveals Links between Sem1/Dss1-Containing Complexes and mRNA Export and Splicing. Molecular Cell 32: 735.
71. Lau NC, Kolkman A, van Schaik FMA, Mulder KW, Pijnappel WWMP, et al. (2009) Human Ccr4â€"Not complexes contain variable deadenylase subunits. Biochemical Journal 422: 443-453.
72. Singleton DR, Chen S, Hitomi M, Kumagai C, Tartakoff AM, (1995) A yeast protein that bidirectionally affects nucleocytoplasmic transport. J Cell Sci 108: 265-272.
73. Lee MS, Henry M, Silver PA, (1996) A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes & Development 10: 1233-1246.
74. Duncan K, Umen JG, Guthrie C, (2000) A putative ubiquitin ligase required for efficient mRNA export differentially affects hnRNP transport. Current Biology 10: 687.
75. Rodriguez MS, Gwizdek C, Haguenauer-Tsapis R, Dargemont C, (2003) The HECT Ubiquitin Ligase Rsp5p Is Required for Proper Nuclear Export of mRNA in Saccharomyces cerevisiae. Traffic 4: 566-575.
76. Gwizdek C, Iglesias N, Rodriguez MS, Ossareh-Nazari B, Hobeika M, et al. (2006) Ubiquitin-associated domain of Mex67 synchronizes recruitment of the mRNA export machinery with transcription. Proceedings of the National Academy of Sciences 103: 16376-16381.
77. Singh RK, Kabbaj M-HM, Paik J, Gunjan A, (2009) Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat Cell Biol 11: 925.
78. Cléry A, Blatter M, Allain FHT, (2008) RNA recognition motifs: boring? Not quite. Current Opinion in Structural Biology 18: 290.
79. Sambrook J, Fritsch E, T M, (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
80. Adams A, Gottschling DE, Kaiser CA, Stearns T, (1997) Methods in yeast genetics Cold Spring Harbor Laboratory Press.
81. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical Statistical Model To Estimate the Accuracy of Peptide Identifications Made by MS/MS and Database Search. Analytical Chemistry 74: 5383-5392.
82. Nesvizhskii AI, Keller A, Kolker E, Aebersold R, (2003) A Statistical Model for Identifying Proteins by Tandem Mass Spectrometry. Analytical Chemistry 75: 4646-4658.
83. Wong DH, Corbett AH, Kent HM, Stewart M, Silver PA, (1997) Interaction between the small GTPase Ran/Gsp1p and Ntf2p is required for nuclear transport. Mol Cell Biol 17: 3755-3767.
84. Winston F, Dollard C, Ricupero-Hovasse S, (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11: 53-55.
85. Belanger KD, Gupta A, MacDonald KM, Ott CM, Hodge CA, et al. (2005) Nuclear Pore Complex Function in Saccharomyces cerevisiae Is Influenced by Glycosylation of the Transmembrane Nucleoporin Pom152p. Genetics 171: 935-947.
86. Heath CV, Copeland CS, Amberg DC, Del Priore V, Snyder M, et al. (1995) Nuclear pore complex clustering and nuclear accumulation of poly(A)+ RNA associated with mutation of the Saccharomyces cerevisiae RAT2/NUP120 gene. J Cell Biol 131: 1677-1697.
87. Lange A, Mills RE, Devine SE, Corbett AH, (2008) A PY-NLS Nuclear Targeting Signal Is Required for Nuclear Localization and Function of the Saccharomyces cerevisiae mRNA-binding Protein Hrp1. Journal of Biological Chemistry 283: 12926-12934.
88. Swanson MJ, Qiu H, Sumibcay L, Krueger A, Kim S-j, et al. (2003) A Multiplicity of Coactivators Is Required by Gcn4p at Individual Promoters In Vivo. Mol Cell Biol 23: 2800-2820.
89. Mumberg D, Müller R, Funk M, (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156: 119.
90. Tran EJ, Zhou Y, Corbett AH, Wente SR, (2007) The DEAD-Box Protein Dbp5 Controls mRNA Export by Triggering Specific RNA:Protein Remodeling Events. Molecular Cell 28: 850.
91. Sikorski RS, Hieter P, (1989) A System of Shuttle Vectors and Yeast Host Strains Designed for Efficient Manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.