CENP-A K124Ubiquitylation Is Required for CENP-A Deposition at the Centromere

Developmental Cell

Volumn 32, Issue 5, 2015, Pages 589-603

  Niikura, Yohei ^a   Kitagawa, Risa ^a   Ogi, Hiroo ^a   Abdulle, Rashid ^a   Pagala, Vishwajeeth ^b   Kitagawa, Katsumi ^a,c  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; CHAPERONE; COPS8 E3 LIGASE; CULLIN; CULLIN 4A; HOLLIDAY JUNCTION RECOGNITION PROTEIN; LIGASE; LYSINE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; AUTOANTIGEN; CARRIER PROTEIN; COPS8 PROTEIN, HUMAN; CUL4A PROTEIN, HUMAN; HISTONE; LUCIFERASE; MESSENGER RNA; NONHISTONE PROTEIN; NUCLEOSOME; PROTEIN; PROTEIN BINDING; RBX1 PROTEIN, HUMAN; UBIQUITIN;

ARTICLE; CELLULAR DISTRIBUTION; CENTROMERE; CONTROLLED STUDY; ENZYME ACTIVITY; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UBIQUITINATION; AMINO ACID SEQUENCE; CELL CULTURE; CHEMISTRY; CHROMOSOME SEGREGATION; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOSOME; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; AUTOANTIGENS; BLOTTING, WESTERN; CARRIER PROTEINS; CELLS, CULTURED; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; CULLIN PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HISTONES; HUMANS; IMMUNOENZYME TECHNIQUES; LUCIFERASES; LYSINE; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; PROTEIN BINDING; PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITIN; UBIQUITINATION;

EID: 84924444021     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.01.024     Document Type: Article

References (65)

1. Ando S., Yang H., Nozaki N., Okazaki T., Yoda K. CENP-A, -B, and -C chromatin complex that contains the I-type alpha-satellite array constitutes the prekinetochore in HeLa cells. Mol. Cell. Biol. 2002, 22:2229-2241.
2. Angers S., Li T., Yi X., MacCoss M.J., Moon R.T., Zheng N. Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 2006, 443:590-593.
3. Antonelli A., Crinelli R., Bianchi M., Cerasi A., Gentilini L., Serafini G., Magnani M. Efficient inhibition of macrophage TNF-alpha production upon targeted delivery of K48R ubiquitin. Br. J. Haematol. 1999, 104:475-481.
4. Bade D., Pauleau A.L., Wendler A., Erhardt S. The E3 ligase CUL3/RDX controls centromere maintenance by ubiquitylating and stabilizing CENP-A in a CAL1-dependent manner. Dev. Cell 2014, 28:508-519.
5. Bailey A.O., Panchenko T., Sathyan K.M., Petkowski J.J., Pai P.J., Bai D.L., Russell D.H., Macara I.G., Shabanowitz J., Hunt D.F., et al. Posttranslational modification of CENP-A influences the conformation of centromeric chromatin. Proc. Natl. Acad. Sci. USA 2013, 110:11827-11832.
6. Barnhart M.C., Kuich P.H., Stellfox M.E., Ward J.A., Bassett E.A., Black B.E., Foltz D.R. HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J.Cell Biol. 2011, 194:229-243.
7. Bennett E.J., Rush J., Gygi S.P., Harper J.W. Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 2010, 143:951-965.
8. Bernad R., Sánchez P., Rivera T., Rodríguez-Corsino M., Boyarchuk E., Vassias I., Ray-Gallet D., Arnaoutov A., Dasso M., Almouzni G., Losada A. Xenopus HJURP and condensin II are required for CENP-A assembly. J.Cell Biol. 2011, 192:569-582.
9. Black B.E., Cleveland D.W. Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell 2011, 144:471-479.
10. Black B.E., Foltz D.R., Chakravarthy S., Luger K., Woods V.L., Cleveland D.W. Structural determinants for generating centromeric chromatin. Nature 2004, 430:578-582.
11. Black B.E., Jansen L.E., Maddox P.S., Foltz D.R., Desai A.B., Shah J.V., Cleveland D.W. Centromere identity maintained by nucleosomes assembled with histone H3 containing the CENP-A targeting domain. Mol. Cell 2007, 25:309-322.
12. Bui M., Dimitriadis E.K., Hoischen C., An E., Quénet D., Giebe S., Nita-Lazar A., Diekmann S., Dalal Y. Cell-cycle-dependent structural transitions in the human CENP-A nucleosome invivo. Cell 2012, 150:317-326.
13. Carroll C.W., Silva M.C., Godek K.M., Jansen L.E., Straight A.F. Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 2009, 11:896-902.
14. Chen C.C., Dechassa M.L., Bettini E., Ledoux M.B., Belisario C., Heun P., Luger K., Mellone B.G. CAL1 is the Drosophila CENP-A assembly factor. J.Cell Biol. 2014, 204:313-329.
15. Codomo C.A., Furuyama T., Henikoff S. CENP-A octamers do not confer a reduction in nucleosome height by AFM. Nat. Struct. Mol. Biol. 2014, 21:4-5.
16. Collins K.A., Furuyama S., Biggins S. Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr. Biol. 2004, 14:1968-1972.
17. Dunleavy E.M., Roche D., Tagami H., Lacoste N., Ray-Gallet D., Nakamura Y., Daigo Y., Nakatani Y., Almouzni-Pettinotti G. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 2009, 137:485-497.
18. Erhardt S., Mellone B.G., Betts C.M., Zhang W., Karpen G.H., Straight A.F. Genome-wide analysis reveals a cell cycle-dependent mechanism controlling centromere propagation. J.Cell Biol. 2008, 183:805-818.
19. Fachinetti D., Folco H.D., Nechemia-Arbely Y., Valente L.P., Nguyen K., Wong A.J., Zhu Q., Holland A.J., Desai A., Jansen L.E., Cleveland D.W. A two-step mechanism for epigenetic specification of centromere identity and function. Nat. Cell Biol. 2013, 15:1056-1066.
20. Folco H.D., Desai A. A PSHaver for centromeric histones. Mol. Cell 2010, 40:351-352.
21. Foltz D.R., Jansen L.E., Bailey A.O., Yates J.R., Bassett E.A., Wood S., Black B.E., Cleveland D.W. Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 2009, 137:472-484.
22. Fujita Y., Hayashi T., Kiyomitsu T., Toyoda Y., Kokubu A., Obuse C., Yanagida M. Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev. Cell 2007, 12:17-30.
23. Glickman M.H., Rubin D.M., Coux O., Wefes I., Pfeifer G., Cjeka Z., Baumeister W., Fried V.A., Finley D. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 1998, 94:615-623.
24. Goshima G., Wollman R., Goodwin S.S., Zhang N., Scholey J.M., Vale R.D., Stuurman N. Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 2007, 316:417-421.
25. Goutte-Gattat D., Shuaib M., Ouararhni K., Gautier T., Skoufias D.A., Hamiche A., Dimitrov S. Phosphorylation of the CENP-A amino-terminus in mitotic centromeric chromatin is required for kinetochore function. Proc. Natl. Acad. Sci. USA 2013, 110:8579-8584.
26. Han J., Zhang H., Zhang H., Wang Z., Zhou H., Zhang Z. A Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly. Cell 2013, 155:817-829.
27. He Y.J., McCall C.M., Hu J., Zeng Y., Xiong Y. DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev. 2006, 20:2949-2954.
28. Hemmerich P., Weidtkamp-Peters S., Hoischen C., Schmiedeberg L., Erliandri I., Diekmann S. Dynamics of inner kinetochore assembly and maintenance in living cells. J.Cell Biol. 2008, 180:1101-1114.
29. Hewawasam G., Shivaraju M., Mattingly M., Venkatesh S., Martin-Brown S., Florens L., Workman J.L., Gerton J.L. Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol. Cell 2010, 40:444-454.
30. Higa L.A., Wu M., Ye T., Kobayashi R., Sun H., Zhang H. CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 2006, 8:1277-1283.
31. Izuta H., Ikeno M., Suzuki N., Tomonaga T., Nozaki N., Obuse C., Kisu Y., Goshima N., Nomura F., Nomura N., et al. Comprehensive analysis of the ICEN (Interphase Centromere Complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 2006, 11:673-684.
32. Jackson S., Xiong Y. CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem. Sci. 2009, 34:562-570.
33. Jansen L.E., Black B.E., Foltz D.R., Cleveland D.W. Propagation of centromeric chromatin requires exit from mitosis. J.Cell Biol. 2007, 176:795-805.
34. Jin J., Arias E.E., Chen J., Harper J.W., Walter J.C. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 2006, 23:709-721.
35. Karpen G.H., Allshire R.C. The case for epigenetic effects on centromere identity and function. Trends Genet. 1997, 13:489-496.
36. Keppler A., Gendreizig S., Gronemeyer T., Pick H., Vogel H., Johnsson K. A general method for the covalent labeling of fusion proteins with small molecules invivo. Nat. Biotechnol. 2003, 21:86-89.
37. Kim I.S., Lee M., Park K.C., Jeon Y., Park J.H., Hwang E.J., Jeon T.I., Ko S., Lee H., Baek S.H., Kim K.I. Roles of Mis18α in epigenetic regulation of centromeric chromatin and CENP-A loading. Mol. Cell 2012, 46:260-273.
38. Lagana A., Dorn J.F., De Rop V., Ladouceur A.M., Maddox A.S., Maddox P.S. A small GTPase molecular switch regulates epigenetic centromere maintenance by stabilizing newly incorporated CENP-A. Nat. Cell Biol. 2010, 12:1186-1193.
39. Lorick K.L., Yang Y., Jensen J.P., Iwai K., Weissman A.M. Detection of E3 Activity in Immunoprecipitated Protein. Current Protocols in Cell Biology 2006, 15.19.25-15.19.26. John Wiley & Sons, Somerset.
40. Maddox P.S., Hyndman F., Monen J., Oegema K., Desai A. Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J.Cell Biol. 2007, 176:757-763.
41. McKinley K.L., Cheeseman I.M. Polo-like kinase 1 licenses CENP-A deposition at centromeres. Cell 2014, 158:397-411.
42. Merlet J., Burger J., Gomes J.E., Pintard L. Regulation of cullin-RING E3 ubiquitin-ligases by neddylation and dimerization. Cell. Mol. Life Sci. 2009, 66:1924-1938.
43. Moree B., Meyer C.B., Fuller C.J., Straight A.F. CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J.Cell Biol. 2011, 194:855-871.
44. Niikura Y., Ohta S., Vandenbeldt K.J., Abdulle R., McEwen B.F., Kitagawa K. 17-AAG, an Hsp90 inhibitor, causes kinetochore defects: a novel mechanism by which 17-AAG inhibits cell proliferation. Oncogene 2006, 25:4133-4146.
45. Niikura Y., Dixit A., Scott R., Perkins G., Kitagawa K. BUB1 mediation of caspase-independent mitotic death determines cell fate. J.Cell Biol. 2007, 178:283-296.
46. Niikura Y., Ogi H., Kikuchi K., Kitagawa K. BUB3 that dissociates from BUB1 activates caspase-independent mitotic death (CIMD). Cell Death Differ. 2010, 17:1011-1024.
47. Obuse C., Yang H., Nozaki N., Goto S., Okazaki T., Yoda K. Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNA binding protein 1 (DDB-1) is a component of the CEN-complex, while BMI-1 is transiently co-localized with the centromeric region in interphase. Genes Cells 2004, 9:105-120.
48. Perpelescu M., Nozaki N., Obuse C., Yang H., Yoda K. Active establishment of centromeric CENP-A chromatin by RSF complex. J.Cell Biol. 2009, 185:397-407.
49. Pierce N.W., Lee J.E., Liu X., Sweredoski M.J., Graham R.L., Larimore E.A., Rome M., Zheng N., Clurman B.E., Hess S., et al. Cand1 promotes assembly of new SCF complexes through dynamic exchange of F box proteins. Cell 2013, 153:206-215.
50. Prendergast L., Sullivan K.F. A GTPase switch maintains CENP-A at centromeric chromatin. Nat. Cell Biol. 2010, 12:1128-1130.
51. Ranjitkar P., Press M.O., Yi X., Baker R., MacCoss M.J., Biggins S. An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol. Cell 2010, 40:455-464.
52. Samel A., Cuomo A., Bonaldi T., Ehrenhofer-Murray A.E. Methylation of CenH3 arginine 37 regulates kinetochore integrity and chromosome segregation. Proc. Natl. Acad. Sci. USA 2012, 109:9029-9034.
53. Sanchez-Pulido L., Pidoux A.L., Ponting C.P., Allshire R.C. Common ancestry of the CENP-A chaperones Scm3 and HJURP. Cell 2009, 137:1173-1174.
54. Schuh M., Lehner C.F., Heidmann S. Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 2007, 17:237-243.
55. Sekulic N., Bassett E.A., Rogers D.J., Black B.E. The structure of (CENP-A-H4)(2) reveals physical features that mark centromeres. Nature 2010, 467:347-351.
56. Shuaib M., Ouararhni K., Dimitrov S., Hamiche A. HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres. Proc. Natl. Acad. Sci. USA 2010, 107:1349-1354.
57. Sigismund S., Polo S., Di Fiore P.P. Signaling through monoubiquitination. Curr. Top. Microbiol. Immunol. 2004, 286:149-185.
58. Tachiwana H., Kagawa W., Shiga T., Osakabe A., Miya Y., Saito K., Hayashi-Takanaka Y., Oda T., Sato M., Park S.Y., et al. Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 2011, 476:232-235.
59. Tatsumi Y., Ohta S., Kimura H., Tsurimoto T., Obuse C. The ORC1 cycle in human cells: I. cell cycle-regulated oscillation of human ORC1. J.Biol. Chem. 2003, 278:41528-41534.
60. Thrower J.S., Hoffman L., Rechsteiner M., Pickart C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19:94-102.
61. Wang H., Zhai L., Xu J., Joo H.Y., Jackson S., Erdjument-Bromage H., Tempst P., Xiong Y., Zhang Y. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 2006, 22:383-394.
62. Warburton P.E., Cooke C.A., Bourassa S., Vafa O., Sullivan B.A., Stetten G., Gimelli G., Warburton D., Tyler-Smith C., Sullivan K.F., et al. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr. Biol. 1997, 7:901-904.
63. Wei N., Deng X.W. The COP9 signalosome. Annu. Rev. Cell Dev. Biol. 2003, 19:261-286.
64. Zeitlin S.G., Shelby R.D., Sullivan K.F. CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J.Cell Biol. 2001, 155:1147-1157.
65. Zhang X., Li X., Marshall J.B., Zhong C.X., Dawe R.K. Phosphoserines on maize CENTROMERIC HISTONE H3 and histone H3 demarcate the centromere and pericentromere during chromosome segregation. Plant Cell 2005, 17:572-583.