Ume6 Acts as a Stable Platform To Coordinate Repression and Activation of Early Meiosis-Specific Genes in Saccharomyces cerevisiae

REFERENCES

• Silveira MAD, Bilodeau S. 2018. Defining the transcriptional ecosystem. Mol Cell 72:920–924. https://doi.org/10.1016/j.molcel.2018.11.022.
   PubMed Web of Science ®Google Scholar
• Neiman AM. 2011. Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 189:737–765. https://doi.org/10.1534/genetics.111.127126.
   PubMed Web of Science ®Google Scholar
• Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I. 1998. The transcriptional program of sporulation in budding yeast. Science 282:699–705. https://doi.org/10.1126/science.282.5389.699.
   PubMed Web of Science ®Google Scholar
• Chu S, Herskowitz I. 1998. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol Cell 1:685–696. https://doi.org/10.1016/S1097-2765(00)80068-4.
   PubMed Web of Science ®Google Scholar
• Primig M, Williams RM, Winzeler EA, Tevzadze GG, Conway AR, Hwang SY, Davis RW, Esposito RE. 2000. The core meiotic transcriptome in budding yeasts. Nat Genet 26:415–423. https://doi.org/10.1038/82539.
   PubMed Web of Science ®Google Scholar
• Chia M, van Werven FJ. 2016. Temporal expression of a master regulator drives synchronous sporulation in budding yeast. G3 (Bethesda) 6:3553–3560. https://doi.org/10.1534/g3.116.034983.
   PubMedGoogle Scholar
• Kassir Y, Granot D, Simchen G. 1988. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell 52:853–862. https://doi.org/10.1016/0092-8674(88)90427-8.
   PubMed Web of Science ®Google Scholar
• Smith HE, Su SS, Neigeborn L, Driscoll SE, Mitchell AP. 1990. Role of IME1 expression in regulation of meiosis in Saccharomyces cerevisiae. Mol Cell Biol 10:6103–6113. https://doi.org/10.1128/MCB.10.12.6103.
   PubMed Web of Science ®Google Scholar
• Mandel S, Robzyk K, Kassir Y. 1994. IME1 gene encodes a transcription factor which is required to induce meiosis in Saccharomyces cerevisiae. Dev Genet 15:139–147. https://doi.org/10.1002/dvg.1020150204.
   PubMedGoogle Scholar
• Williams RM, Primig M, Washburn BK, Winzeler EA, Bellis M, Sarrauste de Menthiere C, Davis RW, Esposito RE. 2002. The Ume6 regulon coordinates metabolic and meiotic gene expression in yeast. Proc Natl Acad Sci U S A 99:13431–13436. https://doi.org/10.1073/pnas.202495299.
   PubMed Web of Science ®Google Scholar
• Anderson SF, Steber CM, Esposito RE, Coleman JE. 1995. UME6, a negative regulator of meiosis in Saccharomyces cerevisiae, contains a C-terminal Zn2Cys6 binuclear cluster that binds the URS1 DNA sequence in a zinc-dependent manner. Protein Sci 4:1832–1843. https://doi.org/10.1002/pro.5560040918.
   PubMed Web of Science ®Google Scholar
• Kadosh D, Struhl K. 1997. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89:365–371. https://doi.org/10.1016/S0092-8674(00)80217-2.
   PubMed Web of Science ®Google Scholar
• Fazzio TG, Kooperberg C, Goldmark JP, Neal C, Basom R, Delrow J, Tsukiyama T. 2001. Widespread collaboration of Isw2 and Sin3-Rpd3 chromatin remodeling complexes in transcriptional repression. Mol Cell Biol 21:6450–6460. https://doi.org/10.1128/MCB.21.19.6450-6460.2001.
   PubMed Web of Science ®Google Scholar
• Kadosh D, Struhl K. 1998. Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo. Mol Cell Biol 18:5121–5127. https://doi.org/10.1128/MCB.18.9.5121.
   PubMed Web of Science ®Google Scholar
• Rundlett SE, Carmen AA, Suka N, Turner BM, Grunstein M. 1998. Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3. Nature 392:831–835. https://doi.org/10.1038/33952.
   PubMed Web of Science ®Google Scholar
• Goldmark JP, Fazzio TG, Estep PW, Church GM, Tsukiyama T. 2000. The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103:423–433. https://doi.org/10.1016/S0092-8674(00)00134-3.
   PubMed Web of Science ®Google Scholar
• Bowdish KS, Mitchell AP. 1993. Bipartite structure of an early meiotic upstream activation sequence from Saccharomyces cerevisiae. Mol Cell Biol 13:2172–2181. https://doi.org/10.1128/MCB.13.4.2172.
   PubMed Web of Science ®Google Scholar
• Strich R, Surosky RT, Steber C, Dubois E, Messenguy F, Esposito RE. 1994. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev 8:796–810. https://doi.org/10.1101/gad.8.7.796.
   PubMed Web of Science ®Google Scholar
• Vidan S, Mitchell AP. 1997. Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p. Mol Cell Biol 17:2688–2697. https://doi.org/10.1128/MCB.17.5.2688.
   PubMed Web of Science ®Google Scholar
• Colomina N, Gari E, Gallego C, Herrero E, Aldea M. 1999. G1 cyclins block the Ime1 pathway to make mitosis and meiosis incompatible in budding yeast. EMBO J 18:320–329. https://doi.org/10.1093/emboj/18.2.320.
   PubMed Web of Science ®Google Scholar
• Smith HE, Driscoll SE, Sia RA, Yuan HE, Mitchell AP. 1993. Genetic evidence for transcriptional activation by the yeast IME1 gene product. Genetics 133:775–784. https://doi.org/10.1093/genetics/133.4.775.
   PubMed Web of Science ®Google Scholar
• Bowdish KS, Yuan HE, Mitchell AP. 1995. Positive control of yeast meiotic genes by the negative regulator UME6. Mol Cell Biol 15:2955–2961. https://doi.org/10.1128/MCB.15.6.2955.
   PubMed Web of Science ®Google Scholar
• Pnueli L, Edry I, Cohen M, Kassir Y. 2004. Glucose and nitrogen regulate the switch from histone deacetylation to acetylation for expression of early meiosis-specific genes in budding yeast. Mol Cell Biol 24:5197–5208. https://doi.org/10.1128/MCB.24.12.5197-5208.2004.
   PubMed Web of Science ®Google Scholar
• Rubin-Bejerano I, Mandel S, Robzyk K, Kassir Y. 1996. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional repressor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol Cell Biol 16:2518–2526. https://doi.org/10.1128/MCB.16.5.2518.
   PubMed Web of Science ®Google Scholar
• Mallory MJ, Cooper KF, Strich R. 2007. Meiosis-specific destruction of the Ume6p repressor by the Cdc20-directed APC/C. Mol Cell 27:951–961. https://doi.org/10.1016/j.molcel.2007.08.019.
   PubMed Web of Science ®Google Scholar
• Lee BH, Amon A. 2003. Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science 300:482–486. https://doi.org/10.1126/science.1081846.
   PubMed Web of Science ®Google Scholar
• Oelschlaegel T, Schwickart M, Matos J, Bogdanova A, Camasses A, Havlis J, Shevchenko A, Zachariae W. 2005. The yeast APC/C subunit Mnd2 prevents premature sister chromatid separation triggered by the meiosis-specific APC/C-Ama1. Cell 120:773–788. https://doi.org/10.1016/j.cell.2005.01.032.
   PubMed Web of Science ®Google Scholar
• Okaz E, Arguello-Miranda O, Bogdanova A, Vinod PK, Lipp JJ, Markova Z, Zagoriy I, Novak B, Zachariae W. 2012. Meiotic prophase requires proteolysis of M phase regulators mediated by the meiosis-specific APC/CAma1. Cell 151:603–618. https://doi.org/10.1016/j.cell.2012.08.044.
   PubMed Web of Science ®Google Scholar
• Tan GS, Lewandowski R, Mallory MJ, Strich R, Cooper KF. 2013. Mutually dependent degradation of Ama1p and Cdc20p terminates APC/C ubiquitin ligase activity at the completion of meiotic development in yeast. Cell Div 8:9. https://doi.org/10.1186/1747-1028-8-9.
   PubMed Web of Science ®Google Scholar
• Marston AL, Tham WH, Shah H, Amon A. 2004. A genome-wide screen identifies genes required for centromeric cohesion. Science 303:1367–1370. https://doi.org/10.1126/science.1094220.
   PubMed Web of Science ®Google Scholar
• Cooper KF, Mallory MJ, Egeland DB, Jarnik M, Strich R. 2000. Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast. Proc Natl Acad Sci U S A 97:14548–14553. https://doi.org/10.1073/pnas.250351297.
   PubMed Web of Science ®Google Scholar
• Diamond AE, Park JS, Inoue I, Tachikawa H, Neiman AM. 2009. The anaphase promoting complex targeting subunit Ama1 links meiotic exit to cytokinesis during sporulation in Saccharomyces cerevisiae. Mol Biol Cell 20:134–145. https://doi.org/10.1091/mbc.e08-06-0615.
   PubMed Web of Science ®Google Scholar
• Penkner AM, Prinz S, Ferscha S, Klein F. 2005. Mnd2, an essential antagonist of the anaphase-promoting complex during meiotic prophase. Cell 120:789–801. https://doi.org/10.1016/j.cell.2005.01.017.
   PubMed Web of Science ®Google Scholar
• Tan GS, Magurno J, Cooper KF. 2011. Ama1p-activated anaphase-promoting complex regulates the destruction of Cdc20p during meiosis II. Mol Biol Cell 22:315–326. https://doi.org/10.1091/mbc.e10-04-0360.
   PubMed Web of Science ®Google Scholar
• Coluccio A, Bogengruber E, Conrad MN, Dresser ME, Briza P, Neiman AM. 2004. Morphogenetic pathway of spore wall assembly in Saccharomyces cerevisiae. Eukaryot Cell 3:1464–1475. https://doi.org/10.1128/EC.3.6.1464-1475.2004.
   PubMedGoogle Scholar
• Bartholomew CR, Suzuki T, Du Z, Backues SK, Jin M, Lynch-Day MA, Umekawa M, Kamath A, Zhao M, Xie Z, Inoki K, Klionsky DJ. 2012. Ume6 transcription factor is part of a signaling cascade that regulates autophagy. Proc Natl Acad Sci U S A 109:11206–11210. https://doi.org/10.1073/pnas.1200313109.
   PubMed Web of Science ®Google Scholar
• Wen FP, Guo YS, Hu Y, Liu WX, Wang Q, Wang YT, Yu HY, Tang CM, Yang J, Zhou T, Xie ZP, Sha JH, Guo X, Li W. 2016. Distinct temporal requirements for autophagy and the proteasome in yeast meiosis. Autophagy 12:671–688. https://doi.org/10.1080/15548627.2016.1149659.
   PubMed Web of Science ®Google Scholar
• Bhaumik SR, Green MR. 2001. SAGA is an essential in vivo target of the yeast acidic activator Gal4p. Genes Dev 15:1935–1945. https://doi.org/10.1101/gad.911401.
   PubMed Web of Science ®Google Scholar
• Qiu H, Hu C, Zhang F, Hwang GJ, Swanson MJ, Boonchird C, Hinnebusch AG. 2005. Interdependent recruitment of SAGA and Srb mediator by transcriptional activator Gcn4p. Mol Cell Biol 25:3461–3474. https://doi.org/10.1128/MCB.25.9.3461-3474.2005.
   PubMed Web of Science ®Google Scholar
• Burgess SM, Ajimura M, Kleckner N. 1999. GCN5-dependent histone H3 acetylation and RPD3-dependent histone H4 deacetylation have distinct, opposing effects on IME2 transcription, during meiosis and during vegetative growth, in budding yeast. Proc Natl Acad Sci U S A 96:6835–6840. https://doi.org/10.1073/pnas.96.12.6835.
   PubMed Web of Science ®Google Scholar
• Mallory MJ, Law MJ, Sterner DE, Berger SL, Strich R. 2012. Gcn5p-dependent acetylation induces degradation of the meiotic transcriptional repressor Ume6p. Mol Biol Cell 23:1609–1617. https://doi.org/10.1091/mbc.e11-06-0536.
   PubMed Web of Science ®Google Scholar
• Steber CM, Esposito RE. 1995. UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression. Proc Natl Acad Sci U S A 92:12490–12494. https://doi.org/10.1073/pnas.92.26.12490.
   PubMed Web of Science ®Google Scholar
• Xiao Y, Mitchell AP. 2000. Shared roles of yeast glycogen synthase kinase 3 family members in nitrogen-responsive phosphorylation of meiotic regulator Ume6p. Mol Cell Biol 20:5447–5453. https://doi.org/10.1128/MCB.20.15.5447-5453.2000.
   PubMed Web of Science ®Google Scholar
• Bryant JM, Govin J, Zhang L, Donahue G, Pugh BF, Berger SL. 2012. The linker histone plays a dual role during gametogenesis in Saccharomyces cerevisiae. Mol Cell Biol 32:2771–2783. https://doi.org/10.1128/MCB.00282-12.
   PubMed Web of Science ®Google Scholar
• Knop M, Siegers K, Pereira G, Zachariae W, Winsor B, Nasmyth K, Schiebel E. 1999. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15:963–972. https://doi.org/10.1002/(SICI)1097-0061(199907)15:10B<963::AID-YEA399>3.0.CO;2-W.
   PubMed Web of Science ®Google Scholar
• Kurdistani SK, Robyr D, Tavazoie S, Grunstein M. 2002. Genome-wide binding map of the histone deacetylase Rpd3 in yeast. Nat Genet 31:248–254. https://doi.org/10.1038/ng907.
   PubMed Web of Science ®Google Scholar
• Inai T, Yukawa M, Tsuchiya E. 2007. Interplay between chromatin and trans-acting factors on the IME2 promoter upon induction of the gene at the onset of meiosis. Mol Cell Biol 27:1254–1263. https://doi.org/10.1128/MCB.01661-06.
   PubMed Web of Science ®Google Scholar
• Sharov G, Voltz K, Durand A, Kolesnikova O, Papai G, Myasnikov AG, Dejaegere A, Ben Shem A, Schultz P. 2017. Structure of the transcription activator target Tra1 within the chromatin modifying complex SAGA. Nat Commun 8:1556. https://doi.org/10.1038/s41467-017-01564-7.
   PubMed Web of Science ®Google Scholar
• Lin L, Chamberlain L, Zhu LJ, Green MR. 2012. Analysis of Gal4-directed transcription activation using Tra1 mutants selectively defective for interaction with Gal4. Proc Natl Acad Sci U S A 109:1997–2002. https://doi.org/10.1073/pnas.1116340109.
   PubMed Web of Science ®Google Scholar
• Herbig E, Warfield L, Fish L, Fishburn J, Knutson BA, Moorefield B, Pacheco D, Hahn S. 2010. Mechanism of mediator recruitment by tandem Gcn4 activation domains and three Gal11 activator-binding domains. Mol Cell Biol 30:2376–2390. https://doi.org/10.1128/MCB.01046-09.
   PubMed Web of Science ®Google Scholar
• Washburn BK, Esposito RE. 2001. Identification of the Sin3-binding site in Ume6 defines a two-step process for conversion of Ume6 from a transcriptional repressor to an activator in yeast. Mol Cell Biol 21:2057–2069. https://doi.org/10.1128/MCB.21.6.2057-2069.2001.
   PubMed Web of Science ®Google Scholar
• Horvath A, Riezman H. 1994. Rapid protein extraction from Saccharomyces cerevisiae. Yeast 10:1305–1310. https://doi.org/10.1002/yea.320101007.
   PubMed Web of Science ®Google Scholar
• Byers B, Goetsch L. 1982. Reversible pachytene arrest of Saccharomyces cerevisiae at elevated temperature. Mol Gen Genet 187:47–53. https://doi.org/10.1007/BF00384382.
   PubMedGoogle Scholar
• Lardenois A, Becker E, Walther T, Law MJ, Xie B, Demougin P, Strich R, Primig M. 2015. Global alterations of the transcriptional landscape during yeast growth and development in the absence of Ume6-dependent chromatin modification. Mol Genet Genomics 290:2031–2046. https://doi.org/10.1007/s00438-015-1051-5.
   PubMed Web of Science ®Google Scholar
• Mendelsohn S, Pinsky M, Weissman Z, Kornitzer D. 2017. Regulation of the Candida albicans hypha-inducing transcription factor Ume6 by the CDK1 cyclins Cln3 and Hgc1. mSphere 2:e00248-16. https://doi.org/10.1128/mSphere.00248-16.
   Google Scholar
• Lu Y, Su C, Ray S, Yuan Y, Liu H. 2019. Signaling through the Ptc2-Ssn3 axis governs sustained hyphal development of Candida albicans by reducing Ume6 phosphorylation and degradation. mBio 10:e02320-18. https://doi.org/10.1128/mBio.02320-18.
   Google Scholar
• Zhu Z, Bani Ismail M, Shinohara M, Shinohara A. 2021. SCFCdc4 ubiquitin ligase regulates synaptonemal complex formation during meiosis. Life Sci Alliance 4:e202000933. https://doi.org/10.26508/lsa.202000933.
   Google Scholar
• Lamb TM, Mitchell AP. 2001. Coupling of Saccharomyces cerevisiae early meiotic gene expression to DNA replication depends upon RPD3 and SIN3. Genetics 157:545–556. https://doi.org/10.1093/genetics/157.2.545.
   PubMed Web of Science ®Google Scholar
• Mallory MJ, Strich R. 2003. Ume1p represses meiotic gene transcription in Saccharomyces cerevisiae through interaction with the histone deacetylase Rpd3p. J Biol Chem 278:44727–44734. https://doi.org/10.1074/jbc.M308632200.
   PubMed Web of Science ®Google Scholar
• Yukawa M, Yo K, Hasegawa H, Ueno M, Tsuchiya E. 2009. The Rpd3/HDAC complex is present at the URS1 cis-element with hyperacetylated histone H3. Biosci Biotechnol Biochem 73:378–384. https://doi.org/10.1271/bbb.80621.
   PubMed Web of Science ®Google Scholar
• Deckert J, Struhl K. 2002. Targeted recruitment of Rpd3 histone deacetylase represses transcription by inhibiting recruitment of Swi/Snf, SAGA, and TATA binding protein. Mol Cell Biol 22:6458–6470. https://doi.org/10.1128/MCB.22.18.6458-6470.2002.
   PubMed Web of Science ®Google Scholar
• Shimizu M, Takahashi K, Lamb TM, Shindo H, Mitchell AP. 2003. Yeast Ume6p repressor permits activator binding but restricts TBP binding at the HOP1 promoter. Nucleic Acids Res 31:3033–3037. https://doi.org/10.1093/nar/gkg425.
   PubMed Web of Science ®Google Scholar
• Papai G, Frechard A, Kolesnikova O, Crucifix C, Schultz P, Ben-Shem A. 2020. Structure of SAGA and mechanism of TBP deposition on gene promoters. Nature 577:711–716. https://doi.org/10.1038/s41586-020-1944-2.
   PubMed Web of Science ®Google Scholar
• Wang L, Liu L, Berger SL. 1998. Critical residues for histone acetylation by Gcn5, functioning in Ada and SAGA complexes, are also required for transcriptional function in vivo. Genes Dev 12:640–653. https://doi.org/10.1101/gad.12.5.640.
   PubMed Web of Science ®Google Scholar
• Pray-Grant MG, Schieltz D, McMahon SJ, Wood JM, Kennedy EL, Cook RG, Workman JL, Yates JR, III, Grant PA. 2002. The novel SLIK histone acetyltransferase complex functions in the yeast retrograde response pathway. Mol Cell Biol 22:8774–8786. https://doi.org/10.1128/MCB.22.24.8774-8786.2002.
   PubMed Web of Science ®Google Scholar
• Yadon AN, Singh BN, Hampsey M, Tsukiyama T. 2013. DNA looping facilitates targeting of a chromatin remodeling enzyme. Mol Cell 50:93–103. https://doi.org/10.1016/j.molcel.2013.02.005.
   PubMed Web of Science ®Google Scholar
• Strich R, Khakhina S, Mallory MJ. 2011. Ume6p is required for germination and early colony development of yeast ascospores. FEMS Yeast Res 11:104–113. https://doi.org/10.1111/j.1567-1364.2010.00696.x.
   PubMed Web of Science ®Google Scholar
• Estojak J, Brent R, Golemis E. 1995. Correlation of two-hybrid affinity data with in vitro measurements. Mol Cell Biol 15:5820–5829. https://doi.org/10.1128/MCB.15.10.5820.
   PubMed Web of Science ®Google Scholar
• Kane SM, Roth R. 1974. Carbohydrate metabolism during ascospore development in yeast. J Bacteriol 118:8–14. https://doi.org/10.1128/JB.118.1.8-14.1974.
   PubMed Web of Science ®Google Scholar
• Sherman F. 2002. Getting started with yeast. Methods Enzymol 350:3–41. https://doi.org/10.1016/s0076-6879(02)50954-x.
   PubMed Web of Science ®Google Scholar
• Stuart D, Wittenberg C. 1998. CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint. Genes Dev 12:2698–2710. https://doi.org/10.1101/gad.12.17.2698.
   PubMed Web of Science ®Google Scholar
• Scherer S, Davis RW. 1979. Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proc Natl Acad Sci U S A 76:4951–4955. https://doi.org/10.1073/pnas.76.10.4951.
   PubMed Web of Science ®Google Scholar
• Longtine MS, McKenzie A, III, 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. https://doi.org/10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U.
   PubMed Web of Science ®Google Scholar
• Wach A, Brachat A, Pohlmann R, Philippsen P. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793–1808. https://doi.org/10.1002/yea.320101310.
   PubMed Web of Science ®Google Scholar
• Foiani M, Marini F, Gamba D, Lucchini G, Plevani P. 1994. The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol Cell Biol 14:923–933. https://doi.org/10.1128/MCB.14.2.923.
   PubMed Web of Science ®Google Scholar
• Raithatha SA, Stuart DT. 2005. Meiosis-specific regulation of the Saccharomyces cerevisiae S-phase cyclin CLB5 is dependent on MluI cell cycle box (MCB) elements in its promoter but is independent of MCB-binding factor activity. Genetics 169:1329–1342. https://doi.org/10.1534/genetics.104.036103.
   PubMed Web of Science ®Google Scholar
• Rupp S. 2002. LacZ assays in yeast. Methods Enzymol 350:112–131. https://doi.org/10.1016/s0076-6879(02)50959-9.
   PubMed Web of Science ®Google Scholar
• Kurdistani SK, Grunstein M. 2003. In vivo protein-protein and protein-DNA crosslinking for genomewide binding microarray. Methods 31:90–95. https://doi.org/10.1016/S1046-2023(03)00092-6.
   PubMed Web of Science ®Google Scholar
• Ahmed NT, Bungard D, Shin ME, Moore M, Winter E. 2009. The Ime2 protein kinase enhances the disassociation of the Sum1 repressor from middle meiotic promoters. Mol Cell Biol 29:4352–4362. https://doi.org/10.1128/MCB.00305-09.
   PubMed Web of Science ®Google Scholar
• Gyuris J, Golemis E, Chertkov H, Brent R. 1993. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75:791–803. https://doi.org/10.1016/0092-8674(93)90498-F.
   PubMed Web of Science ®Google Scholar