The Mub1/Ubr2 Ubiquitin Ligase Complex Regulates the Conserved Dsn1 Kinetochore Protein

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Akiyoshi, Bungo ^a,b,d   Nelson, Christian R ^a   Duggan, Nicole ^a   Ceto, Steven ^a   Ranish, Jeffrey A ^c   Biggins, Sue ^a  

^a USA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE ANTIBODY; CENTROMERE PROTEIN A; DSN1 PROTEIN; MUB1 PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UBR2 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ENZYME PURIFICATION; ENZYME REGULATION; IMMUNOBLOTTING; MASS SPECTROMETRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STABILITY; QUALITY CONTROL; UBIQUITINATION;

CARRIER PROTEINS; CELL SURVIVAL; CENTROMERE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; KINETOCHORES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84874787781     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003216     Document Type: Article

References (79)

1. Holland AJ, Cleveland DW, (2012) Losing balance: the origin and impact of aneuploidy in cancer. EMBO Rep 13: 501-514.
2. Westermann S, Drubin DG, Barnes G, (2007) Structures and functions of yeast kinetochore complexes. Annu Rev Biochem 76: 563-591.
3. Cheeseman IM, Desai A, (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9: 33-46.
4. Santaguida S, Musacchio A, (2009) The life and miracles of kinetochores. EMBO J 28: 2511-2531.
5. Bloom K, Joglekar A, (2010) Towards building a chromosome segregation machine. Nature 463: 446-456.
6. Lampert F, Westermann S, (2011) A blueprint for kinetochores- new insights into the molecular mechanics of cell division. Nat Rev Mol Cell Biol 12: 407-412.
7. Allshire RC, Karpen GH, (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9: 923-937.
8. Black BE, Cleveland DW, (2011) Epigenetic Centromere Propagation and the Nature of CENP-A Nucleosomes. Cell 144: 471-479.
9. McAinsh AD, Tytell JD, Sorger PK, (2003) Structure, function, and regulation of budding yeast kinetochores. Annu Rev Cell Dev Biol 19: 519-539.
10. Takeuchi K, Fukagawa T, (2012) Molecular architecture of vertebrate kinetochores. Exp Cell Res 318: 1367-1374.
11. Tanaka K, Chang HL, Kagami A, Watanabe Y, (2009) CENP-C functions as a scaffold for effectors with essential kinetochore functions in mitosis and meiosis. Dev Cell 17: 334-343.
12. Okada M, Cheeseman IM, Hori T, Okawa K, McLeod IX, et al. (2006) The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat Cell Biol 8: 446-457.
13. Carroll CW, Straight AF, (2006) Centromere formation: from epigenetics to self-assembly. Trends Cell Biol 16: 70-78.
14. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A, (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127: 983-997.
15. Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, et al. (2010) Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468: 576-579.
16. Kline SL, Cheeseman IM, Hori T, Fukagawa T, Desai A, (2006) The human Mis12 complex is required for kinetochore assembly and proper chromosome segregation. J Cell Biol 173: 9-17.
17. Cheeseman IM, Hori T, Fukagawa T, Desai A, (2008) KNL1 and the CENP-H/I/K complex coordinately direct kinetochore assembly in vertebrates. Mol Biol Cell 19: 587-594.
18. Davies AE, Kaplan KB, (2010) Hsp90-Sgt1 and Skp1 target human Mis12 complexes to ensure efficient formation of kinetochore-microtubule binding sites. J Cell Biol 189: 261-274.
19. Maskell DP, Hu XW, Singleton MR, (2010) Molecular architecture and assembly of the yeast kinetochore MIND complex. J Cell Biol 190: 823-834.
20. Petrovic A, Pasqualato S, Dube P, Krenn V, Santaguida S, et al. (2010) The MIS12 complex is a protein interaction hub for outer kinetochore assembly. J Cell Biol 190: 835-852.
21. Przewloka MR, Venkei Z, Bolanos-Garcia VM, Debski J, Dadlez M, et al. (2011) CENP-C is a structural platform for kinetochore assembly. Curr Biol 21: 399-405.
22. Screpanti E, De Antoni A, Alushin GM, Petrovic A, Melis T, et al. (2011) Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr Biol 21: 391-398.
23. Deshaies RJ, Joazeiro CA, (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78: 399-434.
24. Hershko A, (2005) The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle. Cell Death Differ 12: 1191-1197.
25. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, et al. (2000) Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol Cell 6: 1365-1375.
26. Ju D, Wang X, Xu H, Xie Y, (2008) Genome-wide analysis identifies MYND-domain protein Mub1 as an essential factor for Rpn4 ubiquitylation. Mol Cell Biol 28: 1404-1412.
27. Moreno-Moreno O, Torras-Llort M, Azorin F, (2006) Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Res 34: 6247-6255.
28. Collins KA, Furuyama S, Biggins S, (2004) Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol 14: 1968-1972.
29. Kaplan KB, Hyman AA, Sorger PK, (1997) Regulating the yeast kinetochore by ubiquitin-dependent degradation and Skp1p-mediated phosphorylation. Cell 91: 491-500.
30. Kopski KM, Huffaker TC, (1997) Suppressors of the ndc10-2 mutation: a role for the ubiquitin system in Saccharomyces cerevisiae kinetochore function. Genetics 147: 409-420.
31. Wang L, Mao X, Ju D, Xie Y, (2004) Rpn4 is a physiological substrate of the Ubr2 ubiquitin ligase. J Biol Chem 279: 55218-55223.
32. Ju D, Wang L, Mao X, Xie Y, (2004) Homeostatic regulation of the proteasome via an Rpn4-dependent feedback circuit. Biochem Biophys Res Commun 321: 51-57.
33. Andreson BL, Gupta A, Georgieva BP, Rothstein R, (2010) The ribonucleotide reductase inhibitor, Sml1, is sequentially phosphorylated, ubiquitylated and degraded in response to DNA damage. Nucleic Acids Res 38: 6490-6501.
34. Nillegoda NB, Theodoraki MA, Mandal AK, Mayo KJ, Ren HY, et al. (2010) Ubr1 and Ubr2 function in a quality control pathway for degradation of unfolded cytosolic proteins. Mol Biol Cell 21: 2102-2116.
35. Akiyoshi B, Nelson CR, Ranish JA, Biggins S, (2009) Quantitative proteomic analysis of purified yeast kinetochores identifies a PP1 regulatory subunit. Genes Dev 23: 2887-2899.
36. Everett RD, Earnshaw WC, Findlay J, Lomonte P, (1999) Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J 18: 1526-1538.
37. Westermann S, Cheeseman IM, Anderson S, Yates JR 3rd, Drubin DG, et al. (2003) Architecture of the budding yeast kinetochore reveals a conserved molecular core. J Cell Biol 163: 215-222.
38. Welburn JP, Vleugel M, Liu D, Yates JR 3rd, Lampson MA, et al. (2010) Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol Cell 38: 383-392.
39. Ranjitkar P, Press MO, Yi X, Baker R, MacCoss MJ, Biggins S, (2010) An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol Cell 40: 455-464.
40. Goshima G, Yanagida M, (2000) Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell 100: 619-633.
41. Straight AF, Belmont AS, Robinett CC, Murray AW, (1996) GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol 6: 1599-1608.
42. Goh PY, Kilmartin JV, (1993) NDC10: a gene involved in chromosome segregation in Saccharomyces cerevisiae. J Cell Biol 121: 503-512.
43. Wigge PA, Jensen ON, Holmes S, Soues S, Mann M, et al. (1998) Analysis of the Saccharomyces spindle pole by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry. J Cell Biol 141: 967-977.
44. He X, Asthana S, Sorger PK, (2000) Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 101: 763-775.
45. Pearson CG, Yeh E, Gardner M, Odde D, Salmon ED, et al. (2004) Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase. Curr Biol 14: 1962-1967.
46. Pinsky BA, Kung C, Shokat KM, Biggins S, (2006) The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat Cell Biol 8: 78-83.
47. Peng Y, Wong CC, Nakajima Y, Tyers RG, Sarkeshik AS, et al. (2011) Overlapping kinetochore targets of CK2 and Aurora B kinases in mitotic regulation. Mol Biol Cell 22: 2680-2689.
48. Li R, Murray AW, (1991) Feedback control of mitosis in budding yeast. Cell 66: 519-531.
49. Hoyt MA, Totis L, Roberts BT, (1991) S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66: 507-517.
50. Marston AL, Tham WH, Shah H, Amon A, (2004) A genome-wide screen identifies genes required for centromeric cohesion. Science 303: 1367-1370.
51. Corbett KD, Yip CK, Ee LS, Walz T, Amon A, et al. (2010) The monopolin complex crosslinks kinetochore components to regulate chromosome-microtubule attachments. Cell 142: 556-567.
52. Betting J, Seufert W, (1996) A yeast Ubc9 mutant protein with temperature-sensitive in vivo function is subject to conditional proteolysis by a ubiquitin- and proteasome-dependent pathway. J Biol Chem 271: 25790-25796.
53. Bordallo J, Plemper RK, Finger A, Wolf DH, (1998) Der3p/Hrd1p is required for endoplasmic reticulum-associated degradation of misfolded lumenal and integral membrane proteins. Mol Biol Cell 9: 209-222.
54. Bays NW, Gardner RG, Seelig LP, Joazeiro CA, Hampton RY, (2001) Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat Cell Biol 3: 24-29.
55. Brew CT, Huffaker TC, (2002) The yeast ubiquitin protease, Ubp3p, promotes protein stability. Genetics 162: 1079-1089.
56. Gardner RG, Nelson ZW, Gottschling DE, (2005) Degradation-mediated protein quality control in the nucleus. Cell 120: 803-815.
57. Emanuele MJ, Lan W, Jwa M, Miller SA, Chan CS, et al. (2008) Aurora B kinase and protein phosphatase 1 have opposing roles in modulating kinetochore assembly. J Cell Biol 181: 241-254.
58. Yang Y, Wu F, Ward T, Yan F, Wu Q, et al. (2008) Phosphorylation of HsMis13 by Aurora B kinase is essential for assembly of functional kinetochore. J Biol Chem 283: 26726-26736.
59. Kiyomitsu T, Murakami H, Yanagida M, (2011) Protein interaction domain mapping of human kinetochore protein Blinkin reveals a consensus motif for binding of spindle assembly checkpoint proteins Bub1 and BubR1. Mol Cell Biol 31: 998-1011.
60. Amann JM, Nip J, Strom DK, Lutterbach B, Harada H, et al. (2001) ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain. Mol Cell Biol 21: 6470-6483.
61. Isobe T, Uchida C, Hattori T, Kitagawa K, Oda T, et al. (2006) Ubiquitin-dependent degradation of adenovirus E1A protein is inhibited by BS69. Biochem Biophys Res Commun 339: 367-374.
62. Choi KO, Lee T, Lee N, Kim JH, Yang EG, et al. (2005) Inhibition of the catalytic activity of hypoxia-inducible factor-1alpha-prolyl-hydroxylase 2 by a MYND-type zinc finger. Mol Pharmacol 68: 1803-1809.
63. Hesson LB, Cooper WN, Latif F, (2007) Evaluation of the 3p21.3 tumour-suppressor gene cluster. Oncogene 26: 7283-7301.
64. Rose MD, Winston F, Heiter P (1990) Methods in yeast genetics. Cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory Press. p. 198 p.
65. Brown MT, Goetsch L, Hartwell LH, (1993) MIF2 is required for mitotic spindle integrity during anaphase spindle elongation in Saccharomyces cerevisiae. J Cell Biol 123: 387-403.
66. Ghislain M, Udvardy A, Mann C, (1993) S. cerevisiae 26S protease mutants arrest cell division in G2/metaphase. Nature 366: 358-362.
67. Nekrasov VS, Smith MA, Peak-Chew S, Kilmartin JV, (2003) Interactions between centromere complexes in Saccharomyces cerevisiae. Mol Biol Cell 14: 4931-4946.
68. Ortiz J, Stemmann O, Rank S, Lechner J, (1999) A putative protein complex consisting of Ctf19, Mcm21, and Okp1 represents a missing link in the budding yeast kinetochore. Genes Dev 13: 1140-1155.
69. Enquist-Newman M, Cheeseman IM, Van Goor D, Drubin DG, Meluh PB, et al. (2001) Dad1p, third component of the Duo1p/Dam1p complex involved in kinetochore function and mitotic spindle integrity. Mol Biol Cell 12: 2601-2613.
70. Li Y, Bachant J, Alcasabas AA, Wang Y, Qin J, et al. (2002) The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev 16: 183-197.
71. Biggins S, Bhalla N, Chang A, Smith DL, Murray AW, (2001) Genes Involved in Sister Chromatid Separation and Segregation in the Budding Yeast Saccharomyces cerevisiae. Genetics 159: 453-470.
72. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
73. Gelbart ME, Rechsteiner T, Richmond TJ, Tsukiyama T, (2001) Interactions of Isw2 chromatin remodeling complex with nucleosomal arrays: analyses using recombinant yeast histones and immobilized templates. Mol Cell Biol 21: 2098-2106.
74. Goldstein AL, McCusker JH, (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
75. Pinsky BA, Tatsutani SY, Collins KA, Biggins S, (2003) An Mtw1 complex promotes kinetochore biorientation that is monitored by the Ipl1/Aurora protein kinase. Dev Cell 5: 735-745.
76. Sikorski RS, Hieter P, (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
77. Akiyoshi B, Biggins S, (2010) Cdc14-dependent dephosphorylation of a kinetochore protein prior to anaphase in Saccharomyces cerevisiae. Genetics 186: 1487-1491.
78. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, et al. (1999) The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev 13: 532-544.
79. Swerdlow PS, Finley D, Varshavsky A, (1986) Enhancement of immunoblot sensitivity by heating of hydrated filters. Anal Biochem 156: 147-153.