Skp, Cullin, F-box (SCF)-Met30 and SCF-Cdc4-Mediated Proteolysis of CENP-A Prevents Mislocalization of CENP-A for Chromosomal Stability in Budding Yeast
Autoři:
Wei-Chun Au aff001; Tianyi Zhang aff001; Prashant K. Mishra aff001; Jessica R. Eisenstatt aff001; Robert L. Walker aff001; Josefina Ocampo aff002; Anthony Dawson aff001; Jack Warren aff001; Michael Costanzo aff003; Anastasia Baryshnikova aff004; Karin Flick aff005; David J. Clark aff002; Paul S. Meltzer aff001; Richard E. Baker aff006; Chad Myers aff007; Charles Boone aff003; Peter Kaiser aff005; Munira A. Basrai aff001
Působiště autorů:
Genetics Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States of America
aff001; Division of Developmental Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, United States of America
aff002; Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, ON, Canada
aff003; Calico Life Sciences LLC, South San Francisco, CA, United States of America
aff004; Department of Biological Chemistry, College of Medicine, University of California, Irvine, CA, United States of America
aff005; Department of Microbiology and Physiological Systems, University of Massachusetts Medical School, Worcester, MA, United States of America
aff006; Department of Computer Science and Engineering, University of Minnesota-Twin Cities, Minneapolis, MN, United States of America
aff007
Vyšlo v časopise:
Skp, Cullin, F-box (SCF)-Met30 and SCF-Cdc4-Mediated Proteolysis of CENP-A Prevents Mislocalization of CENP-A for Chromosomal Stability in Budding Yeast. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008597
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008597
Souhrn
Restricting the localization of the histone H3 variant CENP-A (Cse4 in yeast, CID in flies) to centromeres is essential for faithful chromosome segregation. Mislocalization of CENP-A leads to chromosomal instability (CIN) in yeast, fly and human cells. Overexpression and mislocalization of CENP-A has been observed in many cancers and this correlates with increased invasiveness and poor prognosis. Yet genes that regulate CENP-A levels and localization under physiological conditions have not been defined. In this study we used a genome-wide genetic screen to identify essential genes required for Cse4 homeostasis to prevent its mislocalization for chromosomal stability. We show that two Skp, Cullin, F-box (SCF) ubiquitin ligases with the evolutionarily conserved F-box proteins Met30 and Cdc4 interact and cooperatively regulate proteolysis of endogenous Cse4 and prevent its mislocalization for faithful chromosome segregation under physiological conditions. The interaction of Met30 with Cdc4 is independent of the D domain, which is essential for their homodimerization and ubiquitination of other substrates. The requirement for both Cdc4 and Met30 for ubiquitination is specifc for Cse4; and a common substrate for Cdc4 and Met30 has not previously been described. Met30 is necessary for the interaction between Cdc4 and Cse4, and defects in this interaction lead to stabilization and mislocalization of Cse4, which in turn contributes to CIN. We provide the first direct link between Cse4 mislocalization to defects in kinetochore structure and show that SCF-mediated proteolysis of Cse4 is a major mechanism that prevents stable maintenance of Cse4 at non-centromeric regions, thus ensuring faithful chromosome segregation. In summary, we have identified essential pathways that regulate cellular levels of endogenous Cse4 and shown that proteolysis of Cse4 by SCF-Met30/Cdc4 prevents mislocalization and CIN in unperturbed cells.
Klíčová slova:
Cell cycle and cell division – Galactose – Glucose – Histones – Chromatin – Chromosomes – Proteolysis – Ubiquitination
Zdroje
1. McKinley KL, Cheeseman IM. The molecular basis for centromere identity and function. Nat Rev Mol Cell Biol. 2016;17(1):16–29. Epub 2015/11/26. doi: 10.1038/nrm.2015.5 26601620.
2. Sharma AB, Dimitrov S, Hamiche A, Van Dyck E. Centromeric and ectopic assembly of CENP-A chromatin in health and cancer: old marks and new tracks. Nucleic Acids Res. 2018. Epub 2018/12/28. doi: 10.1093/nar/gky1298 30590707.
3. Athwal RK, Walkiewicz MP, Baek S, Fu S, Bui M, Camps J, et al. CENP-A nucleosomes localize to transcription factor hotspots and subtelomeric sites in human cancer cells. Epigenetics Chromatin. 2015;8:2. Epub 2015/03/20. doi: 10.1186/1756-8935-8-2 25788983; PubMed Central PMCID: PMC4363203.
4. Au WC, Crisp MJ, DeLuca SZ, Rando OJ, Basrai MA. Altered dosage and mislocalization of histone H3 and Cse4p lead to chromosome loss in Saccharomyces cerevisiae. Genetics. 2008;179(1):263–75. Epub 2008/05/07. doi: 10.1534/genetics.108.088518 18458100; PubMed Central PMCID: PMC2390605.
5. Lacoste N, Woolfe A, Tachiwana H, Garea AV, Barth T, Cantaloube S, et al. Mislocalization of the centromeric histone variant CenH3/CENP-A in human cells depends on the chaperone DAXX. Mol Cell. 2014;53(4):631–44. Epub 2014/02/18. doi: 10.1016/j.molcel.2014.01.018 24530302.
6. Shrestha RL, Ahn GS, Staples MI, Sathyan KM, Karpova TS, Foltz DR, et al. Mislocalization of centromeric histone H3 variant CENP-A contributes to chromosomal instability (CIN) in human cells. Oncotarget. 2017;8(29):46781–800. Epub 2017/06/10. doi: 10.18632/oncotarget.18108 28596481; PubMed Central PMCID: PMC5564523.
7. Heun P, Erhardt S, Blower MD, Weiss S, Skora AD, Karpen GH. Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell. 2006;10(3):303–15. Epub 2006/03/07. doi: 10.1016/j.devcel.2006.01.014 16516834; PubMed Central PMCID: PMC3192491.
8. Mishra PK, Au WC, Choy JS, Kuich PH, Baker RE, Foltz DR, et al. Misregulation of Scm3p/HJURP causes chromosome instability in Saccharomyces cerevisiae and human cells. PLoS Genet. 2011;7(9):e1002303. Epub 2011/10/08. doi: 10.1371/journal.pgen.1002303 21980305; PubMed Central PMCID: PMC3183075.
9. McGovern SL, Qi Y, Pusztai L, Symmans WF, Buchholz TA. Centromere protein-A, an essential centromere protein, is a prognostic marker for relapse in estrogen receptor-positive breast cancer. Breast Cancer Res. 2012;14(3):R72. Epub 2012/05/09. doi: 10.1186/bcr3181 22559056; PubMed Central PMCID: PMC3446334.
10. Tomonaga T, Matsushita K, Yamaguchi S, Oohashi T, Shimada H, Ochiai T, et al. Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res. 2003;63(13):3511–6. Epub 2003/07/04. 12839935.
11. Sun X, Clermont PL, Jiao W, Helgason CD, Gout PW, Wang Y, et al. Elevated expression of the centromere protein-A(CENP-A)-encoding gene as a prognostic and predictive biomarker in human cancers. Int J Cancer. 2016;139(4):899–907. Epub 2016/04/12. doi: 10.1002/ijc.30133 27062469.
12. Zhang W, Mao JH, Zhu W, Jain AK, Liu K, Brown JB, et al. Centromere and kinetochore gene misexpression predicts cancer patient survival and response to radiotherapy and chemotherapy. Nat Commun. 2016;7:12619. Epub 2016/09/01. doi: 10.1038/ncomms12619 27577169; PubMed Central PMCID: PMC5013662 PCT/US15/31413 entitled 'Centromere/Kinetochore protein genes for cancer diagnosis, prognosis and treatment selection'. The remaining authors declare no competing financial interests.
13. Li Y, Zhu Z, Zhang S, Yu D, Yu H, Liu L, et al. ShRNA-targeted centromere protein A inhibits hepatocellular carcinoma growth. PLoS One. 2011;6(3):e17794. Epub 2011/03/23. doi: 10.1371/journal.pone.0017794 21423629; PubMed Central PMCID: PMC3058037.
14. Amato A, Schillaci T, Lentini L, Di Leonardo A. CENPA overexpression promotes genome instability in pRb-depleted human cells. Mol Cancer. 2009;8:119. Epub 2009/12/17. doi: 10.1186/1476-4598-8-119 20003272; PubMed Central PMCID: PMC2797498.
15. Collins KA, Furuyama S, Biggins S. Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol. 2004;14(21):1968–72. Epub 2004/11/09. doi: 10.1016/j.cub.2004.10.024 15530401.
16. Gonzalez M, He H, Dong Q, Sun S, Li F. Ectopic centromere nucleation by CENP—a in fission yeast. Genetics. 2014;198(4):1433–46. Epub 2014/10/10. doi: 10.1534/genetics.114.171173 25298518; PubMed Central PMCID: PMC4256763.
17. Moreno-Moreno O, Medina-Giro S, Torras-Llort M, Azorin F. The F box protein partner of paired regulates stability of Drosophila centromeric histone H3, CenH3(CID). Curr Biol. 2011;21(17):1488–93. Epub 2011/08/30. doi: 10.1016/j.cub.2011.07.041 21871803.
18. Moreno-Moreno O, Torras-Llort M, Azorin F. Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Res. 2006;34(21):6247–55. Epub 2006/11/09. doi: 10.1093/nar/gkl902 17090596; PubMed Central PMCID: PMC1693906.
19. Au WC, Dawson AR, Rawson DW, Taylor SB, Baker RE, Basrai MA. A novel role of the N terminus of budding yeast histone H3 variant Cse4 in ubiquitin-mediated proteolysis. Genetics. 2013;194(2):513–8. Epub 2013/03/26. doi: 10.1534/genetics.113.149898 23525333; PubMed Central PMCID: PMC3664860.
20. Pickart CM. Ubiquitin in chains. Trends Biochem Sci. 2000;25(11):544–8. Epub 2000/11/21. doi: 10.1016/s0968-0004(00)01681-9 11084366.
21. Deshaies RJ, Joazeiro CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem. 2009;78:399–434. Epub 2009/06/06. doi: 10.1146/annurev.biochem.78.101807.093809 19489725.
22. Finley D, Ulrich HD, Sommer T, Kaiser P. The ubiquitin-proteasome system of Saccharomyces cerevisiae. Genetics. 2012;192(2):319–60. Epub 2012/10/03. doi: 10.1534/genetics.112.140467 23028185; PubMed Central PMCID: PMC3454868.
23. Cheng H, Bao X, Rao H. The F-box Protein Rcy1 Is Involved in the Degradation of Histone H3 Variant Cse4 and Genome Maintenance. J Biol Chem. 2016;291(19):10372–7. Epub 2016/03/16. doi: 10.1074/jbc.M115.701813 26975376; PubMed Central PMCID: PMC4858983.
24. Hewawasam G, Shivaraju M, Mattingly M, Venkatesh S, Martin-Brown S, Florens L, et al. Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol Cell. 2010;40(3):444–54. Epub 2010/11/13. doi: 10.1016/j.molcel.2010.10.014 21070970; PubMed Central PMCID: PMC2998187.
25. Ranjitkar P, Press MO, Yi X, Baker R, MacCoss MJ, Biggins S. An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol Cell. 2010;40(3):455–64. Epub 2010/11/13. doi: 10.1016/j.molcel.2010.09.025 21070971; PubMed Central PMCID: PMC2995698.
26. Ohkuni K, Takahashi Y, Fulp A, Lawrimore J, Au WC, Pasupala N, et al. SUMO-Targeted Ubiquitin Ligase (STUbL) Slx5 regulates proteolysis of centromeric histone H3 variant Cse4 and prevents its mislocalization to euchromatin. Mol Biol Cell. 2016. Epub 2016/03/11. doi: 10.1091/mbc.E15-12-0827 26960795; PubMed Central PMCID: PMC4850037.
27. Ohkuni K, Levy-Myers R, Warren J, Au WC, Takahashi Y, Baker RE, et al. N-terminal Sumoylation of Centromeric Histone H3 Variant Cse4 Regulates Its Proteolysis To Prevent Mislocalization to Non-centromeric Chromatin. G3 (Bethesda). 2018;8(4):1215–23. Epub 2018/02/13. doi: 10.1534/g3.117.300419 29432128; PubMed Central PMCID: PMC5873912.
28. Hildebrand EM, Biggins S. Regulation of Budding Yeast CENP-A levels Prevents Misincorporation at Promoter Nucleosomes and Transcriptional Defects. PLoS Genet. 2016;12(3):e1005930. doi: 10.1371/journal.pgen.1005930 26982580; PubMed Central PMCID: PMC4794243.
29. Deyter GM, Biggins S. The FACT complex interacts with the E3 ubiquitin ligase Psh1 to prevent ectopic localization of CENP-A. Genes Dev. 2014;28(16):1815–26. Epub 2014/08/17. doi: 10.1101/gad.243113.114 25128498; PubMed Central PMCID: PMC4197964.
30. Hewawasam GS, Mattingly M, Venkatesh S, Zhang Y, Florens L, Workman JL, et al. Phosphorylation by casein kinase 2 facilitates Psh1 protein-assisted degradation of Cse4 protein. J Biol Chem. 2014;289(42):29297–309. Epub 2014/09/04. doi: 10.1074/jbc.M114.580589 25183013; PubMed Central PMCID: PMC4200280.
31. Gkikopoulos T, Schofield P, Singh V, Pinskaya M, Mellor J, Smolle M, et al. A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science. 2011;333(6050):1758–60. Epub 2011/09/24. doi: 10.1126/science.1206097 21940898; PubMed Central PMCID: PMC3428865.
32. Lopes da Rosa J, Holik J, Green EM, Rando OJ, Kaufman PD. Overlapping regulation of CenH3 localization and histone H3 turnover by CAF-1 and HIR proteins in Saccharomyces cerevisiae. Genetics. 2011;187(1):9–19. Epub 2010/10/15. doi: 10.1534/genetics.110.123117 20944015; PubMed Central PMCID: PMC3018296.
33. Ciftci-Yilmaz S, Au WC, Mishra PK, Eisenstatt JR, Chang J, Dawson AR, et al. A Genome-Wide Screen Reveals a Role for the HIR Histone Chaperone Complex in Preventing Mislocalization of Budding Yeast CENP-A. Genetics. 2018;210(1):203–18. Epub 2018/07/18. doi: 10.1534/genetics.118.301305 30012561; PubMed Central PMCID: PMC6116949.
34. Crotti LB, Basrai MA. Functional roles for evolutionarily conserved Spt4p at centromeres and heterochromatin in Saccharomyces cerevisiae. EMBO J. 2004;23(8):1804–14. Epub 2004/04/02. doi: 10.1038/sj.emboj.7600161 15057281; PubMed Central PMCID: PMC394231.
35. Aristizabal-Corrales D, Yang J, Li F. Cell Cycle-Regulated Transcription of CENP-A by the MBF Complex Ensures Optimal Level of CENP-A for Centromere Formation. Genetics. 2019;211(3):861–75. Epub 2019/01/13. doi: 10.1534/genetics.118.301745 30635289; PubMed Central PMCID: PMC6404251.
36. Moreno-Moreno O, Torras-Llort M, Azorin F. The E3-ligases SCFPpa and APC/CCdh1 co-operate to regulate CENP-ACID expression across the cell cycle. Nucleic Acids Res. 2019;47(7):3395–406. Epub 2019/02/13. doi: 10.1093/nar/gkz060 30753559; PubMed Central PMCID: PMC6468245.
37. Cheng H, Bao X, Gan X, Luo S, Rao H. Multiple E3s promote the degradation of histone H3 variant Cse4. Sci Rep. 2017;7(1):8565. Epub 2017/08/19. doi: 10.1038/s41598-017-08923-w 28819127; PubMed Central PMCID: PMC5561092.
38. Baryshnikova A, Costanzo M, Dixon S, Vizeacoumar FJ, Myers CL, Andrews B, et al. Synthetic genetic array (SGA) analysis in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Methods Enzymol. 2010;470:145–79. Epub 2010/10/16. doi: 10.1016/S0076-6879(10)70007-0 20946810.
39. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, et al. The genetic landscape of a cell. Science. 2010;327(5964):425–31. Epub 2010/01/23. doi: 10.1126/science.1180823 20093466; PubMed Central PMCID: PMC5600254.
40. Costanzo M, VanderSluis B, Koch EN, Baryshnikova A, Pons C, Tan G, et al. A global genetic interaction network maps a wiring diagram of cellular function. Science. 2016;353(6306). Epub 2016/10/07. doi: 10.1126/science.aaf1420 27708008; PubMed Central PMCID: PMC5661885.
41. Amin AD, Dimova DK, Ferreira ME, Vishnoi N, Hancock LC, Osley MA, et al. The mitotic Clb cyclins are required to alleviate HIR-mediated repression of the yeast histone genes at the G1/S transition. Biochim Biophys Acta. 2012;1819(1):16–27. doi: 10.1016/j.bbagrm.2011.09.003 21978826; PubMed Central PMCID: PMC3249481.
42. Petroski MD, Deshaies RJ. Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol. 2005;6(1):9–20. Epub 2005/02/03. doi: 10.1038/nrm1547 15688063.
43. Vodermaier HC. APC/C and SCF: controlling each other and the cell cycle. Curr Biol. 2004;14(18):R787–96. Epub 2004/09/24. doi: 10.1016/j.cub.2004.09.020 15380093.
44. Jonkers W, Rep M. Lessons from fungal F-box proteins. Eukaryot Cell. 2009;8(5):677–95. doi: 10.1128/EC.00386-08 19286981; PubMed Central PMCID: PMC2681605.
45. Flick K, and Kaiser P. Cellular Mechanisms to Respond to Cadmium Exposure: Ubiquitin LigasesCellular Effects of Heavy Metals. Banfalvi G, ed (Springer Netherlands)2011. p. 275–89.
46. Flick K, Ouni I, Wohlschlegel JA, Capati C, McDonald WH, Yates JR, et al. Proteolysis-independent regulation of the transcription factor Met4 by a single Lys 48-linked ubiquitin chain. Nat Cell Biol. 2004;6(7):634–41. Epub 2004/06/23. doi: 10.1038/ncb1143 15208638.
47. Kaiser P, Flick K, Wittenberg C, Reed SI. Regulation of transcription by ubiquitination without proteolysis: Cdc34/SCF(Met30)-mediated inactivation of the transcription factor Met4. Cell. 2000;102(3):303–14. Epub 2000/09/07. doi: 10.1016/s0092-8674(00)00036-2 10975521.
48. Patton EE, Peyraud C, Rouillon A, Surdin-Kerjan Y, Tyers M, Thomas D. SCF(Met30)-mediated control of the transcriptional activator Met4 is required for the G(1)-S transition. EMBO J. 2000;19(7):1613–24. Epub 2000/04/04. doi: 10.1093/emboj/19.7.1613 10747029; PubMed Central PMCID: PMC310230.
49. Ouni I, Flick K, Kaiser P. A transcriptional activator is part of an SCF ubiquitin ligase to control degradation of its cofactors. Mol Cell. 2010;40(6):954–64. Epub 2010/12/22. doi: 10.1016/j.molcel.2010.11.018 21172660; PubMed Central PMCID: PMC3026289.
50. Schwob E, Bohm T, Mendenhall MD, Nasmyth K. The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell. 1994;79(2):233–44. Epub 1994/10/21. doi: 10.1016/0092-8674(94)90193-7 7954792.
51. Meimoun A, Holtzman T, Weissman Z, McBride HJ, Stillman DJ, Fink GR, et al. Degradation of the transcription factor Gcn4 requires the kinase Pho85 and the SCF(CDC4) ubiquitin-ligase complex. Mol Biol Cell. 2000;11(3):915–27. Epub 2000/03/11. doi: 10.1091/mbc.11.3.915 10712509; PubMed Central PMCID: PMC14820.
52. Lyons NA, Fonslow BR, Diedrich JK, Yates JR 3rd, Morgan DO. Sequential primed kinases create a damage-responsive phosphodegron on Eco1. Nat Struct Mol Biol. 2013;20(2):194–201. Epub 2013/01/15. doi: 10.1038/nsmb.2478 23314252; PubMed Central PMCID: PMC3565030.
53. Delgoshaie N, Tang X, Kanshin ED, Williams EC, Rudner AD, Thibault P, et al. Regulation of the histone deacetylase Hst3 by cyclin-dependent kinases and the ubiquitin ligase SCFCdc4. J Biol Chem. 2014;289(19):13186–96. Epub 2014/03/22. doi: 10.1074/jbc.M113.523530 24648511; PubMed Central PMCID: PMC4036330.
54. Ortiz J, Stemmann O, Rank S, Lechner J. A putative protein complex consisting of Ctf19, Mcm21, and Okp1 represents a missing link in the budding yeast kinetochore. Genes Dev. 1999;13(9):1140–55. Epub 1999/05/14. doi: 10.1101/gad.13.9.1140 10323865; PubMed Central PMCID: PMC316948.
55. Chen Y, Baker RE, Keith KC, Harris K, Stoler S, Fitzgerald-Hayes M. The N terminus of the centromere H3-like protein Cse4p performs an essential function distinct from that of the histone fold domain. Mol Cell Biol. 2000;20(18):7037–48. Epub 2000/08/25. doi: 10.1128/mcb.20.18.7037-7048.2000 10958698; PubMed Central PMCID: PMC88778.
56. Morey L, Barnes K, Chen Y, Fitzgerald-Hayes M, Baker RE. The histone fold domain of Cse4 is sufficient for CEN targeting and propagation of active centromeres in budding yeast. Eukaryot Cell. 2004;3(6):1533–43. doi: 10.1128/EC.3.6.1533-1543.2004 15590827; PubMed Central PMCID: PMC539035.
57. Hornung P, Troc P, Malvezzi F, Maier M, Demianova Z, Zimniak T, et al. A cooperative mechanism drives budding yeast kinetochore assembly downstream of CENP-A. J Cell Biol. 2014;206(4):509–24. Epub 2014/08/20. doi: 10.1083/jcb.201403081 25135934; PubMed Central PMCID: PMC4137059.
58. Boeckmann L, Takahashi Y, Au WC, Mishra PK, Choy JS, Dawson AR, et al. Phosphorylation of centromeric histone H3 variant regulates chromosome segregation in Saccharomyces cerevisiae. Mol Biol Cell. 2013;24(12):2034–44. Epub 2013/05/03. doi: 10.1091/mbc.E12-12-0893 23637466; PubMed Central PMCID: PMC3681705.
59. Mishra PK, Guo J, Dittman LE, Haase J, Yeh E, Bloom K, et al. Pat1 protects centromere-specific histone H3 variant Cse4 from Psh1-mediated ubiquitination. Mol Biol Cell. 2015;26(11):2067–79. Epub 2015/04/03. doi: 10.1091/mbc.E14-08-1335 25833709; PubMed Central PMCID: PMC4472017.
60. Hoffmann G, Samel-Pommerencke A, Weber J, Cuomo A, Bonaldi T, Ehrenhofer-Murray AE. A role for CENP-A/Cse4 phosphorylation on serine 33 in deposition at the centromere. FEMS Yeast Res. 2018;18(1). Epub 2017/12/23. doi: 10.1093/femsyr/fox094 29272409.
61. Samel A, Cuomo A, Bonaldi T, Ehrenhofer-Murray AE. Methylation of CenH3 arginine 37 regulates kinetochore integrity and chromosome segregation. Proc Natl Acad Sci U S A. 2012;109(23):9029–34. Epub 2012/05/23. doi: 10.1073/pnas.1120968109 22615363; PubMed Central PMCID: PMC3384136.
62. Mishra PK, Olafsson G, Boeckmann L, Westlake TJ, Jowhar ZM, Dittman LE, et al. Cell cycle dependent association of polo kinase Cdc5 with CENP-A contributes to faithful chromosome segregation in budding yeast. Mol Biol Cell. 2019:mbcE18090584. Epub 2019/02/07. doi: 10.1091/mbc.E18-09-0584 30726152.
63. Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods. 2009;6(12):917–22. Epub 2009/11/17. doi: 10.1038/nmeth.1401 19915560.
64. Morawska M, Ulrich HD. An expanded tool kit for the auxin-inducible degron system in budding yeast. Yeast. 2013;30(9):341–51. Epub 2013/07/10. doi: 10.1002/yea.2967 23836714; PubMed Central PMCID: PMC4171812.
65. Suzuki H, Chiba T, Suzuki T, Fujita T, Ikenoue T, Omata M, et al. Homodimer of two F-box proteins betaTrCP1 or betaTrCP2 binds to IkappaBalpha for signal-dependent ubiquitination. J Biol Chem. 2000;275(4):2877–84. doi: 10.1074/jbc.275.4.2877 10644755.
66. Tang X, Orlicky S, Lin Z, Willems A, Neculai D, Ceccarelli D, et al. Suprafacial orientation of the SCFCdc4 dimer accommodates multiple geometries for substrate ubiquitination. Cell. 2007;129(6):1165–76. doi: 10.1016/j.cell.2007.04.042 17574027.
67. Welcker M, Clurman BE. Fbw7/hCDC4 dimerization regulates its substrate interactions. Cell Div. 2007;2:7. Epub 2007/02/15. doi: 10.1186/1747-1028-2-7 17298674; PubMed Central PMCID: PMC1802738.
68. Hao B, Oehlmann S, Sowa ME, Harper JW, Pavletich NP. Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases. Mol Cell. 2007;26(1):131–43. doi: 10.1016/j.molcel.2007.02.022 17434132.
69. Kitagawa T, Ishii K, Takeda K, Matsumoto T. The 19S proteasome subunit Rpt3 regulates distribution of CENP-A by associating with centromeric chromatin. Nat Commun. 2014;5:3597. Epub 2014/04/09. doi: 10.1038/ncomms4597 24710126.
70. Hieter P, Mann C, Snyder M, Davis RW. Mitotic stability of yeast chromosomes: a colony color assay that measures nondisjunction and chromosome loss. Cell. 1985;40(2):381–92. Epub 1985/02/01. doi: 10.1016/0092-8674(85)90152-7 3967296.
71. Meluh PB, Yang P, Glowczewski L, Koshland D, Smith MM. Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell. 1998;94(5):607–13. Epub 1998/09/19. doi: 10.1016/s0092-8674(00)81602-5 9741625.
72. Saunders MJ, Yeh E, Grunstein M, Bloom K. Nucleosome depletion alters the chromatin structure of Saccharomyces cerevisiae centromeres. Mol Cell Biol. 1990;10(11):5721–7. Epub 1990/11/01. doi: 10.1128/mcb.10.11.5721 2233714; PubMed Central PMCID: PMC361343.
73. Mishra PK, Ottmann AR, Basrai MA. Structural integrity of centromeric chromatin and faithful chromosome segregation requires Pat1. Genetics. 2013;195(2):369–79. Epub 2013/07/31. doi: 10.1534/genetics.113.155291 23893485; PubMed Central PMCID: PMC3781966.
74. Camahort R, Shivaraju M, Mattingly M, Li B, Nakanishi S, Zhu D, et al. Cse4 is part of an octameric nucleosome in budding yeast. Mol Cell. 2009;35(6):794–805. Epub 2009/09/29. doi: 10.1016/j.molcel.2009.07.022 19782029; PubMed Central PMCID: PMC2757638.
75. Lefrancois P, Euskirchen GM, Auerbach RK, Rozowsky J, Gibson T, Yellman CM, et al. Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genomics. 2009;10:37. Epub 2009/01/23. doi: 10.1186/1471-2164-10-37 19159457; PubMed Central PMCID: PMC2656530.
76. Choi ES, Stralfors A, Catania S, Castillo AG, Svensson JP, Pidoux AL, et al. Factors that promote H3 chromatin integrity during transcription prevent promiscuous deposition of CENP-A(Cnp1) in fission yeast. PLoS Genet. 2012;8(9):e1002985. Epub 2012/10/03. doi: 10.1371/journal.pgen.1002985 23028377; PubMed Central PMCID: PMC3447972.
77. Castillo AG, Pidoux AL, Catania S, Durand-Dubief M, Choi ES, Hamilton G, et al. Telomeric repeats facilitate CENP-A(Cnp1) incorporation via telomere binding proteins. PLoS One. 2013;8(7):e69673. Epub 2013/08/13. doi: 10.1371/journal.pone.0069673 23936074; PubMed Central PMCID: PMC3729655.
78. Kominami K, Ochotorena I, Toda T. Two F-box/WD-repeat proteins Pop1 and Pop2 form hetero- and homo-complexes together with cullin-1 in the fission yeast SCF (Skp1-Cullin-1-F-box) ubiquitin ligase. Genes Cells. 1998;3(11):721–35. doi: 10.1046/j.1365-2443.1998.00225.x 9990507.
79. Wolf DA, McKeon F, Jackson PK. F-box/WD-repeat proteins pop1p and Sud1p/Pop2p form complexes that bind and direct the proteolysis of cdc18p. Curr Biol. 1999;9(7):373–6. Epub 1999/04/21. doi: 10.1016/s0960-9822(99)80165-1 10209119.
80. Filipescu D, Naughtin M, Podsypanina K, Lejour V, Wilson L, Gurard-Levin ZA, et al. Essential role for centromeric factors following p53 loss and oncogenic transformation. Genes Dev. 2017;31(5):463–80. Epub 2017/03/31. doi: 10.1101/gad.290924.116 28356341; PubMed Central PMCID: PMC5393061.
81. He N, Li C, Zhang X, Sheng T, Chi S, Chen K, et al. Regulation of lung cancer cell growth and invasiveness by beta-TRCP. Mol Carcinog. 2005;42(1):18–28. Epub 2004/11/13. doi: 10.1002/mc.20063 15536641.
82. Wu Q, Qian YM, Zhao XL, Wang SM, Feng XJ, Chen XF, et al. Expression and prognostic significance of centromere protein A in human lung adenocarcinoma. Lung Cancer. 2012;77(2):407–14. Epub 2012/05/01. doi: 10.1016/j.lungcan.2012.04.007 22542705.
83. Akhoondi S, Sun D, von der Lehr N, Apostolidou S, Klotz K, Maljukova A, et al. FBXW7/hCDC4 is a general tumor suppressor in human cancer. Cancer Res. 2007;67(19):9006–12. Epub 2007/10/03. doi: 10.1158/0008-5472.CAN-07-1320 17909001.
84. Malyukova A, Dohda T, von der Lehr N, Akhoondi S, Corcoran M, Heyman M, et al. The tumor suppressor gene hCDC4 is frequently mutated in human T-cell acute lymphoblastic leukemia with functional consequences for Notch signaling. Cancer Res. 2007;67(12):5611–6. Epub 2007/06/19. doi: 10.1158/0008-5472.CAN-06-4381 17575125.
85. Grim JE, Knoblaugh SE, Guthrie KA, Hagar A, Swanger J, Hespelt J, et al. Fbw7 and p53 cooperatively suppress advanced and chromosomally unstable intestinal cancer. Mol Cell Biol. 2012;32(11):2160–7. Epub 2012/04/05. doi: 10.1128/MCB.00305-12 22473991; PubMed Central PMCID: PMC3372235.
86. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 1998;14(10):953–61. Epub 1998/08/26. doi: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U 9717241.
87. Li Z, Vizeacoumar FJ, Bahr S, Li J, Warringer J, Vizeacoumar FS, et al. Systematic exploration of essential yeast gene function with temperature-sensitive mutants. Nat Biotechnol. 2011;29(4):361–7. Epub 2011/03/29. doi: 10.1038/nbt.1832 21441928; PubMed Central PMCID: PMC3286520.
88. Tong AH, Lesage G, Bader GD, Ding H, Xu H, Xin X, et al. Global mapping of the yeast genetic interaction network. Science. 2004;303(5659):808–13. Epub 2004/02/07. doi: 10.1126/science.1091317 14764870.
89. Kastenmayer JP, Ni L, Chu A, Kitchen LE, Au WC, Yang H, et al. Functional genomics of genes with small open reading frames (sORFs) in S. cerevisiae. Genome Res. 2006;16(3):365–73. Epub 2006/03/03. doi: 10.1101/gr.4355406 16510898; PubMed Central PMCID: PMC1415214.
90. Mishra PK, Ciftci-Yilmaz S, Reynolds D, Au WC, Boeckmann L, Dittman LE, et al. Polo kinase Cdc5 associates with centromeres to facilitate the removal of centromeric cohesin during mitosis. Mol Biol Cell. 2016;27(14):2286–300. Epub 2016/05/27. doi: 10.1091/mbc.E16-01-0004 27226485; PubMed Central PMCID: PMC4945145.
91. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5. Epub 2012/08/30. doi: 10.1038/nmeth.2089 22930834; PubMed Central PMCID: PMC5554542.
92. Basrai MA, Kingsbury J, Koshland D, Spencer F, Hieter P. Faithful chromosome transmission requires Spt4p, a putative regulator of chromatin structure in Saccharomyces cerevisiae. Mol Cell Biol. 1996;16(6):2838–47. Epub 1996/06/01. doi: 10.1128/mcb.16.6.2838 8649393; PubMed Central PMCID: PMC231276.
93. Spencer F, Gerring SL, Connelly C, Hieter P. Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics. 1990;124(2):237–49. Epub 1990/02/01. 2407610; PubMed Central PMCID: PMC1203917.
94. Mishra PK, Baum M, Carbon J. Centromere size and position in Candida albicans are evolutionarily conserved independent of DNA sequence heterogeneity. Molecular genetics and genomics: MGG. 2007;278(4):455–65. doi: 10.1007/s00438-007-0263-8 17588175.
95. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8. Epub 2002/02/16. doi: 10.1006/meth.2001.1262 [pii]. 11846609.
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