Cks1 enhances transcription efficiency at the GAL1 locus by linking the Paf1 complex to the 19S proteasome

Eukaryotic Cell

Volumn 12, Issue 9, 2013, Pages 1192-1201

  Pan, Yen Ru ^a   Sun, Michael ^a   Wohlschlegel, James ^a,b   Reed, Steven I ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CKS1 PROTEIN, S CEREVISIAE; GAL1 PROTEIN, S CEREVISIAE; GALACTOKINASE; NUCLEAR PROTEIN; PAF1 PROTEIN, S CEREVISIAE; PROTEASOME; PROTEOME; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; CHROMATIN; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE PROTEINS; CHROMATIN; GALACTOKINASE; GENE EXPRESSION REGULATION, FUNGAL; GENETIC LOCI; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEOME; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84883208951     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00151-13     Document Type: Article

References (78)

1. Hadwiger JA, Wittenberg C, Mendenhall MD, Reed SI. 1989. The Saccharomyces cerevisiae CKS1 gene, a homolog of the Schizosaccharomyces pombe suc1+gene, encodes a subunit of the Cdc28 protein kinase complex. Mol. Cell. Biol. 9:2034-2041.
2. Hayles J, Beach D, Durkacz B, Nurse P. 1986. The fission yeast cell cycle control gene cdc2: isolation of a sequence suc1 that suppresses cdc2 mutant function. Mol. Gen. Genet. 202:291-293.
3. Morris MC, Kaiser P, Rudyak S, Baskerville C, Watson MH, Reed SI. 2003. Cks1-dependent proteasome recruitment and activation of CDC20 transcription in budding yeast. Nature 423:1009-1013.
4. Kaiser P, Moncollin V, Clarke DJ, Watson MH, Bertolaet BL, Reed SI, Bailly E. 1999. Cyclin-dependent kinase and Cks/Suc1 interact with the proteasome in yeast to control proteolysis of M-phase targets. Genes Dev. 13:1190-1202.
5. Sauer RT, Baker TA. 2011. AAA+ proteases: ATP-fueled machines of protein destruction. Annu. Rev. Biochem. 80:587-612.
6. Lonard DM, O'Malley BW. 2009. Emerging roles of the ubiquitin proteasome system in nuclear hormone receptor signaling. Prog. Mol. Biol. Transl. Sci. 87:117-135.
7. Wilson MD, Harreman M, Svejstrup JQ. 2013. Ubiquitylation and degradation of elongating RNA polymerase II: the last resort. Biochim. Biophys. Acta 1829:151-157.
8. Bhat KP, Greer SF. 2011. Proteolytic and non-proteolytic roles of ubiquitin and the ubiquitin proteasome system in transcriptional regulation. Biochim. Biophys. Acta 1809:150-155.
9. Geng F, Wenzel S, Tansey WP. 2012. Ubiquitin and proteasomes in transcription. Annu. Rev. Biochem. 81:177-201.
10. Gonzalez F, Delahodde A, Kodadek T, Johnston SA. 2002. Recruitment of a 19S proteasome subcomplex to an activated promoter. Science 296: 548-550.
11. Geng F, Tansey WP. 2012. Similar temporal and spatial recruitment of native 19S and 20S proteasome subunits to transcriptionally active chromatin. Proc. Natl. Acad. Sci. U. S. A. 109:6060-6065.
12. Archer CT, Delahodde A, Gonzalez F, Johnston SA, Kodadek T. 2008. Activation domain-dependent monoubiquitylation of Gal4 protein is essential for promoter binding in vivo. J. Biol. Chem. 283:12614-12623.
13. Ostendorff HP, Peirano RI, Peters MA, Schluter A, Bossenz M, Scheffner M, Bach I. 2002. Ubiquitination-dependent cofactor exchange on LIM homeodomain transcription factors. Nature 416:99-103.
14. Zhang H, Sun L, Liang J, Yu W, Zhang Y, Wang Y, Chen Y, Li R, Sun X, Shang Y. 2006. The catalytic subunit of the proteasome is engaged in the entire process of estrogen receptor-regulated transcription. EMBO J. 25:4223-4233.
15. Lee D, Ezhkova E, Li B, Pattenden SG, Tansey WP, Workman JL. 2005. The proteasome regulatory particle alters the SAGA coactivator to enhance its interactions with transcriptional activators. Cell 123:423-436.
16. Malik S, Shukla A, Sen P, Bhaumik SR. 2009. The 19 S proteasome subcomplex establishes a specific protein interaction network at the promoter for stimulated transcriptional initiation in vivo. J. Biol. Chem. 284: 35714-35724.
17. Ezhkova E, Tansey WP. 2004. Proteasomal ATPases link ubiquitylation of histone H2B to methylation of histone H3. Mol. Cell 13:435-442.
18. Koues OI, Dudley RK, Mehta NT, Greer SF. 2009. The 19S proteasome positively regulates histone methylation at cytokine inducible genes. Biochim. Biophys. Acta 1789:691-701.
19. Koues OI, Dudley RK, Truax AD, Gerhardt D, Bhat KP, McNeal S, Greer SF. 2008. Regulation of acetylation at the major histocompatibility complex class II proximal promoter by the 19S proteasomal ATPase Sug1. Mol. Cell. Biol. 28:5837-5850.
20. Koues OI, Mehta NT, Truax AD, Dudley RK, Brooks JK, Greer SF. 2010. Roles for common MLL/COMPASS subunits and the 19S proteasome in regulating CIITA pIV and MHC class II gene expression and promoter methylation. Epigenetics Chromatin 3:5. doi:10.1186/1756-8935-3-5.
21. Truax AD, Koues OI, Mentel MK, Greer SF. 2010. The 19S ATPase S6a (S6=/TBP1) regulates the transcription initiation of class II transactivator. J. Mol. Biol. 395:254-269.
22. Ferdous A, Gonzalez F, Sun L, Kodadek T, Johnston SA. 2001. The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol. Cell 7:981-991.
23. Ferdous A, Kodadek T, Johnston SA. 2002. A nonproteolytic function of the 19S regulatory subunit of the 26S proteasome is required for efficient activated transcription by human RNA polymerase II. Biochemistry 41: 12798-12805.
24. Ottosen S, Herrera FJ, Triezenberg SJ. 2002. Transcription. Proteasome parts at gene promoters. Science 296:479-481.
25. Yu VP, Baskerville C, Grunenfelder B, Reed SI. 2005. A kinaseindependent function of Cks1 and Cdk1 in regulation of transcription. Mol. Cell 17:145-151.
26. Chaves S, Baskerville C, Yu V, Reed SI. 2010. Cks1, Cdk1, and the 19S proteasome collaborate to regulate gene induction-dependent nucleosome eviction in yeast. Mol. Cell. Biol. 30:5284-5294.
27. Jaehning JA. 2010. The Paf1 complex: platform or player in RNA polymerase II transcription? Biochim. Biophys. Acta 1799:379-388.
28. Tomson BN, Arndt KM. 2013. The many roles of the conserved eukaryotic Paf1 complex in regulating transcription, histone modifications, and disease states. Biochim. Biophys. Acta 1829:116-126.
29. Ng HH, Dole S, Struhl K. 2003. The Rtf1 component of the Paf1 tran-scriptional elongation complex is required for ubiquitination of histone H2B. J. Biol. Chem. 278:33625-33628.
30. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A. 2003. The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J. Biol. Chem. 278:34739-34742.
31. Reed SI, Hadwiger JA, Lorincz AT. 1985. Protein kinase activity associated with the product of the yeast cell division cycle gene CDC28. Proc. Natl. Acad. Sci. U. S. A. 82:4055-4059.
32. Longtine MS, McKenzie A, 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
33. de Bruin RA, Kalashnikova TI, Chahwan C, McDonald WH, Wohlschlegel J, Yates J, III, Russell P, Wittenberg C. 2006. Constraining G1-specific transcription to late G1 phase: the MBF-associated corepressor Nrm1 acts via negative feedback. Mol. Cell 23:483-496.
34. Mendenhall MD, Jones CA, Reed SI. 1987. Dual regulation of the yeast CDC28-p40 protein kinase complex: cell cycle, pheromone, and nutrient limitation effects. Cell 50:927-935.
35. Olson BL, Hock MB, Ekholm-Reed S, Wohlschlegel JA, Dev KK, Kralli A, Reed SI. 2008. SCFCdc4 acts antagonistically to the PGC-1alpha transcriptional coactivator by targeting it for ubiquitin-mediated proteolysis. Genes Dev. 22:252-264.
36. Vashisht AA, Zumbrennen KB, Huang X, Powers DN, Durazo A, Sun D, Bhaskaran N, Persson A, Uhlen M, Sangfelt O, Spruck C, Leibold EA, Wohlschlegel JA. 2009. Control of iron homeostasis by an ironregulated ubiquitin ligase. Science 326:718-721.
37. de Bruin RA, Kalashnikova TI, Aslanian A, Wohlschlegel J, Chahwan C, Yates JR, III, Russell P, Wittenberg C. 2008. DNA replication checkpoint promotes G1-S transcription by inactivating the MBF repressor Nrm1. Proc. Natl. Acad. Sci. U. S. A. 105:11230-11235.
38. Ezhkova E, Tansey WP. 2006. Chromatin immunoprecipitation to study protein-DNA interactions in budding yeast. Methods Mol. Biol. 313:225-244.
39. Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, Adams SL, Millar A, Taylor P, Bennett K, Boutilier K, Yang L, Wolting C, Donaldson I, Schandorff S, Shewnarane J, Vo M, Taggart J, Goudreault M, Muskat B, Alfarano C, Dewar D, Lin Z, Michalickova K, Willems AR, Sassi H, Nielsen PA, Rasmussen KJ, Andersen JR, Johansen LE, Hansen LH, Jespersen H, Podtelejnikov A, Nielsen E, Crawford J, Poulsen V, Sorensen BD, Matthiesen J, Hendrickson RC, Gleeson F, Pawson T, Moran MF, Durocher D, Mann M, Hogue CW, Figeys D, Tyers M. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183.
40. Marton HA, Desiderio S. 2008. The Paf1 complex promotes displacement of histones upon rapid induction of transcription by RNA polymerase II. BMC Mol. Biol. 9:4. doi:10.1186/1471-2199-9-4.
41. Kaplan CD, Holland MJ, Winston F. 2005. Interaction between transcription elongation factors and mRNA 3=-end formation at the Saccharomyces cerevisiae GAL10-GAL7 locus. J. Biol. Chem. 280:913-922.
42. Warner MH, Roinick KL, Arndt KM. 2007. Rtf1 is a multifunctional component of the Paf1 complex that regulates gene expression by directing cotranscriptional histone modification. Mol. Cell. Biol. 27:6103-6115.
43. Zhou Q, Li T, Price DH. 2012. RNA polymerase II elongation control. Annu. Rev. Biochem. 81:119-143.
44. Shi X, Finkelstein A, Wolf AJ, Wade PA, Burton ZF, Jaehning JA. 1996. Paf1p, an RNA polymerase II-associated factor in Saccharomyces cerevisiae, may have both positive and negative roles in transcription. Mol. Cell. Biol. 16:669-676.
45. Betz JL, Chang M, Washburn TM, Porter SE, Mueller CL, Jaehning JA. 2002. Phenotypic analysis of Paf1/RNA polymerase II complex mutations reveals connections to cell cycle regulation, protein synthesis, and lipid and nucleic acid metabolism. Mol. Genet. Genomics 268:272-285.
46. Porter SE, Washburn TM, Chang M, Jaehning JA. 2002. The yeast pafl-rNA polymerase II complex is required for full expression of a subset of cell cycle-regulated genes. Eukaryot. Cell 1:830-842.
47. Carvin CD, Kladde MP. 2004. Effectors of lysine 4 methylation of histone H3 in Saccharomyces cerevisiae are negative regulators of PHO5 and GAL1-10. J. Biol. Chem. 279:33057-33062.
48. Piro AS, Mayekar MK, Warner MH, Davis CP, Arndt KM. 2012. Small region of Rtf1 protein can substitute for complete Paf1 complex in facilitating global histone H2B ubiquitylation in yeast. Proc. Natl. Acad. Sci. U. S. A. 109:10837-10842.
49. Mueller CL, Porter SE, Hoffman MG, Jaehning JA. 2004. The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Mol. Cell 14:447-456.
50. Richardson HE, Stueland CS, Thomas J, Russell P, Reed SI. 1990. Human cDNAs encoding homologs of the small p34Cdc28/Cdc2-associated protein of Saccharomyces cerevisiae and Schizosaccharomyces pombe. Genes Dev. 4:1332-1344.
51. Martinsson-Ahlzén HS, Liberal V, Grunenfelder B, Chaves SR, Spruck CH, Reed SI. 2008. Cyclin-dependent kinase-associated proteins Cks1 and Cks2 are essential during early embryogenesis and for cell cycle progression in somatic cells. Mol. Cell. Biol. 28:5698-5709.
52. Westbrook L, Manuvakhova M, Kern FG, Estes NR, II, Ramanathan HN, Thottassery JV. 2007. Cks1 regulates cdk1 expression: a novel role during mitotic entry in breast cancer cells. Cancer Res. 67:11393-11401.
53. Moniaux N, Nemos C, Deb S, Zhu B, Dornreiter I, Hollingsworth MA, Batra SK. 2009. The human RNA polymerase II-associated factor 1 (hPaf1): a new regulator of cell-cycle progression. PLoS One 4:e7077. doi: 10.1371/journal.pone.0007077.
54. Richardson AL, Wang ZC, De Nicolo A, Lu X, Brown M, Miron A, Liao X, Iglehart JD, Livingston DM, Ganesan S. 2006. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9:121-132.
55. Chow LS, Lam CW, Chan SY, Tsao SW, To KF, Tong SF, Hung WK, Dammann R, Huang DP, Lo KW. 2006. Identification of RASSF1A modulated genes in nasopharyngeal carcinoma. Oncogene 25:310-316.
56. de Vos S, Krug U, Hofmann WK, Pinkus GS, Swerdlow SH, Wachsman W, Grogan TM, Said JW, Koeffler HP. 2003. Cell cycle alterations in the blastoid variant of mantle cell lymphoma (MCL-BV) as detected by gene expression profiling of mantle cell lymphoma (MCL) and MCL-BV. Diagn. Mol. Pathol. 12:35-43.
57. de Wit NJ, Rijntjes J, Diepstra JH, van Kuppevelt TH, Weidle UH, Ruiter DJ, van Muijen GN. 2005. Analysis of differential gene expression in human melanocytic tumour lesions by custom made oligonucleotide arrays. Br. J. Cancer 92:2249-2261.
58. Inui N, Kitagawa K, Miwa S, Hattori T, Chida K, Nakamura H, Kitagawa M. 2003. High expression of Cks1 in human non-small cell lung carcinomas. Biochem. Biophys. Res. Commun. 303:978-984.
59. Kawakami K, Enokida H, Tachiwada T, Gotanda T, Tsuneyoshi K, Kubo H, Nishiyama K, Takiguchi M, Nakagawa M, Seki N. 2006. Identification of differentially expressed genes in human bladder cancer through genome-wide gene expression profiling. Oncol. Rep. 16:521-531.
60. Kitajima S, Kudo Y, Ogawa I, Bashir T, Kitagawa M, Miyauchi M, Pagano M, Takata T. 2004. Role of Cks1 overexpression in oral squamous cell carcinomas: cooperation with Skp2 in promoting p27 degradation. Am. J. Pathol. 165:2147-2155.
61. Li M, Lin YM, Hasegawa S, Shimokawa T, Murata K, Kameyama M, Ishikawa O, Katagiri T, Tsunoda T, Nakamura Y, Furukawa Y. 2004. Genes associated with liver metastasis of colon cancer, identified by genome-wide cDNA microarray. Int. J. Oncol. 24:305-312.
62. Masuda TA, Inoue H, Nishida K, Sonoda H, Yoshikawa Y, Kakeji Y, Utsunomiya T, Mori M. 2003. Cyclin-dependent kinase 1 gene expression is associated with poor prognosis in gastric carcinoma. Clin. Cancer Res. 9:5693-5698.
63. Ouellet V, Guyot MC, Le Page C, Filali-Mouhim A, Lussier C, Tonin PN, Provencher DM, Mes-Masson AM. 2006. Tissue array analysis of expression microarray candidates identifies markers associated with tumor grade and outcome in serous epithelial ovarian cancer. Int. J. Cancer 119:599-607.
64. Ouellet V, Provencher DM, Maugard CM, Le Page C, Ren F, Lussier C, Novak J, Ge B, Hudson TJ, Tonin PN, Mes-Masson AM. 2005. Discrimination between serous low malignant potential and invasive epithelial ovarian tumors using molecular profiling. Oncogene 24:4672-4687.
65. Shapira M, Ben-Izhak O, Bishara B, Futerman B, Minkov I, Krausz MM, Pagano M, Hershko DD. 2004. Alterations in the expression of the cell cycle regulatory protein cyclin kinase subunit 1 in colorectal carcinoma. Cancer 100:1615-1621.
66. Slotky M, Shapira M, Ben-Izhak O, Linn S, Futerman B, Tsalic M, Hershko DD. 2005. The expression of the ubiquitin ligase subunit Cks1 in human breast cancer. Breast Cancer Res. 7:R737-R744. doi:10.1186 /bcr1278.
67. Stanbrough M, Bubley GJ, Ross K, Golub TR, Rubin MA, Penning TM, Febbo PG, Balk SP. 2006. Increased expression of genes converting ad-renal androgens to testosterone in androgen-independent prostate cancer. Cancer Res. 66:2815-2825.
68. Urbanowicz-Kachnowicz I, Baghdassarian N, Nakache C, Gracia D, Mekki Y, Bryon PA, Ffrench M. 1999. ckshs expression is linked to cell proliferation in normal and malignant human lymphoid cells. Int. J. Cancer 82:98-104.
69. Wong YF, Cheung TH, Tsao GS, Lo KW, Yim SF, Wang VW, Heung MM, Chan SC, Chan LK, Ho TW, Wong KW, Li C, Guo Y, Chung TK, Smith DI. 2006. Genome-wide gene expression profiling of cervical cancer in Hong Kong women by oligonucleotide microarray. Int. J. Cancer 118:2461-2469.
70. van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. 2002. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:530-536.
71. Shapira M, Ben-Izhak O, Linn S, Futerman B, Minkov I, Hershko DD. 2005. The prognostic impact of the ubiquitin ligase subunits Skp2 and Cks1 in colorectal carcinoma. Cancer 103:1336-1346.
72. Kawakami K, Enokida H, Tachiwada T, Nishiyama K, Seki N, Nakagawa M. 2007. Increased SKP2 and CKS1 gene expression contributes to the progression of human urothelial carcinoma. J. Urol. 178:301-307.
73. Lan Y, Zhang Y, Wang J, Lin C, Ittmann MM, Wang F. 2008. Aberrant expression of Cks1 and Cks2 contributes to prostate tumorigenesis by promoting proliferation and inhibiting programmed cell death. Int. J. Cancer 123:543-551.
74. Keller UB, Old JB, Dorsey FC, Nilsson JA, Nilsson L, MacLean KH, Chung L, Yang C, Spruck C, Boyd K, Reed SI, Cleveland JL. 2007. Myc targets Cks1 to provoke the suppression of p27Kip1, proliferation and lymphomagenesis. EMBO J. 26:2562-2574.
75. Lee EK, Kim DG, Kim JS, Yoon Y. 2011. Cell-cycle regulator Cks1 promotes hepatocellular carcinoma by supporting NF-kappaBdependent expression of interleukin-8. Cancer Res. 71:6827-6835.
76. Liberal V, Martinsson-Ahlzen HS, Liberal J, Spruck CH, Widschwendter M, McGowan CH, Reed SI. 2012. Cyclin-dependent kinase subunit (Cks) 1 or Cks2 overexpression overrides the DNA damage response barrier triggered by activated oncoproteins. Proc. Natl. Acad. Sci. U. S. A. 109:2754-2759.
77. Harper JW. 2001. Protein destruction: adapting roles for Cks proteins. Curr. Biol. 11:R431-R435. doi:10.1016/S0960-9822(01)00253-6.
78. Old JB, Kratzat S, Hoellein A, Graf S, Nilsson JA, Nilsson L, Nakayama KI, Peschel C, Cleveland JL, Keller UB. 2010. Skp2 directs Myc-mediated suppression of p27Kip1 yet has modest effects on Myc-driven lymphomagenesis. Mol. Cancer Res. 8:353-362.