A new regulatory pathway of mRNA export by an F-box protein, Mdm30

RNA

Volumn 20, Issue 2, 2014, Pages 133-142

  Durairaj, Geetha ^a   Lahudkar, Shweta ^a   Bhaumik, Sukesh R ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mdm30; MRNA export; Sub2; Transcription; TREX; Yra1

Indexed keywords

F BOX PROTEIN; MDM30 PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; FUNGAL STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; REGULATORY MECHANISM; UBIQUITINATION; YEAST;

MDM30; MRNA EXPORT; SUB2; TRANSCRIPTION; TREX; YRA1;

ADENOSINE TRIPHOSPHATASES; ALCOHOL DEHYDROGENASE; F-BOX PROTEINS; GENE KNOCKOUT TECHNIQUES; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; PROTEOLYSIS; RNA SPLICING; RNA TRANSPORT; RNA, FUNGAL; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC; UBIQUITINATION;

EID: 84892687939     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.042325.113     Document Type: Article

References (60)

1. Ang K, Ee G, Ang E, Koh E, Siew WL, Chan YM, Nur S, Tan YS, Lehming N. 2012. Mediator acts upstream of the transcriptional activator Gal4. PLoS Biol 10:e1001290.
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Struhl K. 2001. Current protocols in molecular biology. Wiley, New York.
3. Bai C, Richman R, Elledge SJ. 1994. Human cyclin F. EMBO J 13:6087-6098.
4. Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge SJ. 1996. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263-274.
5. Bhaumik SR, Green MR. 2002. Differential requirement of SAGA components for recruitment of TATA-box-binding protein to promoters in vivo. Mol Cell Biol 22:7365-7371.
6. Bhaumik SR, Green MR. 2003. Interaction of Gal4p with components of transcription machinery in vivo. Methods Enzymol 370:445-454.
7. Bhaumik SR, Malik S. 2008. Diverse regulatory mechanisms of eukaryotic transcriptional activation by the proteasome complex. Crit Rev Biochem Mol Biol 43:419-433.
8. Bhaumik SR, Raha T, Aiello DP, Green MR. 2004. In vivo target of a transcriptional activator revealed by fluorescence resonance energy transfer. Genes Dev 18:333-343.
9. Carmody SR, Wente SR. 2009. mRNA nuclear export at a glance. J Cell Sci 122:1933-1937.
10. Chavez S, Beilharz T, Rondon AG, Erdjument-Bromage H, Tempst P, Svejstrup JQ, Lithgow T, Aguilera A. 2000. A protein complex containing Tho2, Hpr1, Mft1 and a novel protein, Thp2, connects transcription elongation with mitotic recombination in Saccharomyces cerevisiae. EMBO J 19:5824-5834.
11. Cohen MM, Leboucher GP, Livnat-Levanon N, Glickman MH, Weissman AM. 2008. Ubiquitin-proteasome-dependent degradation of a mitofusin, a critical regulator of mitochondrial fusion. Mol Biol Cell 19:2457-2464.
12. Dieppois G, Stutz F. 2010. Connecting the transcription site to the nuclear pore: A multi-tether process that regulates gene expression. J Cell Sci 15:1989-1999.
13. Duncan K, Umen JG, Guthrie C. 2000. A putative ubiquitin ligase required for efficient mRNA export differentially affects hnRNP transport. Curr Biol 10:687-696.
14. Durairaj G, Garg P, Bhaumik SR. 2009. Nuclear export of mRNA and its regulation by ubiquitylation. RNA Biol 6:531-535.
15. Fischer T, Strasser K, Racz A, Rodriguez-Navarro S, Oppizzi M, Ihrig P, Lechner J, Hurt E. 2002. The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J 21:5843-5852.
16. Fritz S, Weinbach N, Westermann B. 2003. Mdm30 is an F-box protein required for maintenance of fusion competent mitochondria in yeast. Mol Biol Cell 14:2303-2313.
17. Gwizdek C, Hobeika M, Kus B, Ossareh-Nazari B, Dargemont C, Rodriguez MS. 2005. The mRNA nuclear export factor Hpr1 is regulated by Rsp5-mediated ubiquitylation. J Biol Chem 280:13401-13405.
18. Hammell CM, Gross S, Zenklusen D, Heath CV, Stutz F, Moore C, Cole CN. 2002. Coupling of termination, 3' processing, and mRNA export. Mol Cell Biol 22:6441-6457.
19. Hurt E, Luo MJ, Röther S, Reed R, Strässer 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 101:1858-1862.
20. 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.
21. Jimeno S, Rondón AG, Luna R, Aguilera A. 2002. The yeast THO complex and mRNA export factors link RNA metabolism with transcription and genome instability. EMBO J 21:3526-3535.
22. Johnson SA, Cubberley G, Bentley DL. 2009. Cotranscriptional recruitment of the mRNA export factor Yra1 by direct interaction with the 3' end processing factor Pcf11. Mol Cell 33:215-226.
23. Johnson SA, Kim H, Erickson B, Bentley DL. 2011. The export factor Yra1 modulates mRNA 3' end processing. Nat Struct Mol Biol 18:1164-1171.
24. Jonkers W, Rep M. 2009. Lessons from fungal F-box proteins. Eukaryot Cell 8:677-695.
25. Kashyap AK, Schieltz D, Yates J III, Kellogg DR. 2005. Biochemical and genetic characterization of Yra1p in budding yeast. Yeast 22:43-56.
26. Kim M, Ahn SH, Krogan NJ, Greenblatt JF, Buratowski S. 2004. Transitions in RNA polymerase II elongation complexes at the 3' ends of genes. EMBO J 23:354-364.
27. Kistler AL, Guthrie C. 2001. Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for sub2, an essential spliceosomal ATPase. Genes Dev 15:42-49.
28. Kus BM, Caldon CE, Andorn-Broza R, Edwards AM. 2004. Functional interaction of 13 yeast SCF complexes with a set of yeast E2 enzymes in vitro. Proteins 54:455-467.
29. Lackner LL, Nunnari JM. 2009. The molecular mechanism and cellular functions of mitochondrial division. Biochim Biophys Acta 1792:1138-1144.
30. Lahudkar S, Shukla A, Bajwa P, Durairaj G, Stanojevic N, Bhaumik SR. 2011. The mRNA cap-binding complex stimulates the formation of pre-initiation complex at the promoter via its interaction with Mot1p in vivo. Nucleic Acids Res 39:2188-2209.
31. Libri D, Graziani N, Saguez C, Boulay J. 2001. Multiple roles for the yeast SUB2/yUAP56 gene in splicing. Genes Dev 15:36-41.
32. Livnat-Levanon N, Glickman MH. 2011. Ubiquitin-proteasome system and mitochondria - reciprocity. Biochim Biophys Acta 1809:80-87.
33. Luo ML, Zhou Z, Magni K, Christoforides C, Rappsilber J, Mann M, Reed R. 2001. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature 413:644-647.
34. MacKellar AL, Greenleaf AL. 2011. Cotranscriptional association of mRNA export factor Yra1 with C-terminal domain of RNA polymerase II. J Biol Chem 286:36385-36395.
35. Malik S, Chaurasia P, Lahudkar S, Durairaj G, Shukla A, Bhaumik SR. 2010. Rad26p, a transcription-coupled repair factor, is recruited to the site of DNA lesion in an elongating RNA polymerase II-dependent manner in vivo. Nucleic Acids Res 38:1461-1477.
36. Malik S, Chaurasia P, Lahudkar S, Uprety B, Bhaumik SR. 2012. Rad26p regulates the occupancy of histone H2A-H2B dimer at the active genes in vivo. Nucleic Acids Res 40:3348-3363.
37. Malik S, Durairaj G, Bhaumik SR. 2013. Mechanisms of antisense transcription initiation from the 3' end of the GAL10 coding sequence in vivo. Mol Cell Biol 33:3549-3567.
38. Meeusen SL, Nunnari J. 2005. How mitochondria fuse. Curr Opin Cell Biol 17:389-394.
39. Muratani M, Kung C, Shokat KM, Tansey WP. 2005. The F box protein Dsg1/Mdm30 is a transcriptional coactivator that stimulates Gal4 turnover and cotranscriptional mRNA processing. Cell 120:887-899.
40. Neumann S, Petfalski E, Brugger B, Grosshans H, Wieland F, Tollervey D, Hurt E. 2003. Formation and nuclear export of tRNA, rRNA and mRNA is regulated by the ubiquitin ligase Rsp5p. EMBO Rep 4:1156-1162.
41. Ota K, Kito K, Okada S, Ito T. 2008. A proteomic screen reveals the mitochondrial outer membrane protein Mdm34p as an essential target of the F-box protein Mdm30p. Genes Cells 13:1075-1085.
42. Peterson CL, Kruger W, Herskowitz I. 1991. A functional interaction between the C-terminal domain of RNA polymerase II and the negative regulator SIN1. Cell 64:1135-1143.
43. Reed SI. 2003. Ratchets and clocks: The cell cycle, ubiquitylation and protein turnover. Nat Rev Mol Cell Biol 4:855-864.
44. Rehwinkel J, Herold A, Gari K, Kocher T, Rode M, Ciccarelli FL, Wilm M, Izaurralde E. 2004. Genome-wide analysis of mRNAs regulated by the THO complex in Drosophila melanogaster. Nat Struct Mol Biol 11:558-566.
45. 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.
46. Rondón AG, Jimeno S, García-Rubio M, Aguilera A. 2003. Molecular evidence that the eukaryotic THO/TREX complex is required for efficient transcription elongation. J Biol Chem 278:39037-39043.
47. Rubin DM, Glickman MH, Larsen CN, Dhruvakumar S, Finley D. 1998. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J 17:4909-4919.
48. Russell SJ, Gonzalez F, Joshua-Tor L, Johnston SA. 2001. Selective chemical inactivation of AAA proteins reveals distinct functions of proteasomal ATPases. Chem Biol 8:941-950.
49. Shukla A, Stanojevic N, Duan Z, Sen P, Bhaumik SR. 2006. Ubp8p, a histone deubiquitinase whose association with SAGA is mediated by Sgf11p, differentially regulates lysine 4 methylation of histone H3 in vivo. Mol Cell Biol 26:3339-3352.
50. Shukla A, Durairaj G, Schneider J, Duan Z, Shadle T, Bhaumik SR. 2009. Stimulation of mRNA export by an F-box protein, Mdm30p, in vivo. J Mol Biol 389:238-247.
51. Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209-219.
52. Strässer K, Hurt E. 2000. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J 19:410-420.
53. Strässer K, Hurt E. 2001. Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p. Nature 413:648-652.
54. Strässer K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, Rodriguez-Navarro S, Rondón AG, Aguilera A, Struhl K, Reed R, et al. 2002. TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417:304-308.
55. Stutz F, Bachi A, Doerks T, Braun IC, Séraphin B, Wilm M, Bork P, Izaurralde E. 2000. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 6:638-650.
56. Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, Knight JR, Lockshon D, Narayan V, Srinivasan M, Pochart P, et al. 2000. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403:623-627.
57. Xiong F, Lin Y, Han Z, Shi G, Tian L, Wu X, Zeng Q, Zhou Y, Deng J, Chen H. 2012. Plk1-mediated phosphorylation of UAP56 regulates the stability of UAP56. Mol Biol Rep 39:1935-1942.
58. Yen HC, Elledge SJ. 2008. Identification of SCF ubiquitin ligase substrates by global protein stability profiling. Science 322:923-929.
59. Zenklusen D, Vinciguerra P, Wyss JC, 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.
60. Zhang M, Green MR. 2001. Identification and characterization of yUAP/Sub2p, a yeast homolog of the essential human pre-mRNA splicing factor hUAP56. Genes Dev 15:30-35.