CAMP (C13orf8, ZNF828) is a novel regulator of kinetochore-microtubule attachment

EMBO Journal

Volumn 30, Issue 1, 2011, Pages 130-144

  Itoh, Go ^a   Kanno, Shin Ichiro ^a   Uchida, Kazuhiko S K ^b   Chiba, Shuhei ^a   Sugino, Shiro ^a   Watanabe, Kana ^a   Mizuno, Kensaku ^a   Yasui, Akira ^a   Hirota, Toru ^b   Tanaka, Kozo ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b CANCER INSTITUTE   (Japan)

Author keywords

chromosome; kinetochore; metaphase; microtubule; spindle

Indexed keywords

CENTROMERE PROTEIN E; CENTROMERE PROTEIN F; CHROMOSOME ALIGNMENT MAINTAINING PHOSPHOPROTEIN; CYCLIN DEPENDENT KINASE 1; NUCLEAR PROTEIN; PHOSPHOPROTEIN; PROTEIN C13ORF8; PROTEIN ZNF 828; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL MIGRATION; CELLULAR DISTRIBUTION; CENTROMERE; CHROMOSOME; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; HUMAN; HUMAN CELL; MICROTUBULE; MITOSIS; MUTANT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SHORT TANDEM REPEAT; SPINDLE CELL; ZINC FINGER MOTIF;

CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, HUMAN; HELA CELLS; HUMANS; KINETOCHORES; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; PHOSPHOPROTEINS; PROTEINS; RNA INTERFERENCE;

EID: 78650889802     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.276     Document Type: Article

References (70)

1. Asbury CL, Gestaut DR, Powers AF, Franck AD, Davis TN (2006) The Dam1 kinetochore complex harnesses microtubule dynamics to produce force and movement. Proc Natl Acad Sci USA 103: 9873-9878
2. Ashar HR, James L, Gray K, Carr D, Black S, Armstrong L, Bishop WR, Kirschmeier P (2000) Farnesyl transferase inhibitors block the farnesylation of CENP-E and CENP-F and alter the association of CENP-E with the microtubules. J Biol Chem 275: 30451-30457
3. Baker DJ, Dawlaty MM, Galardy P, van Deursen JM (2007) Mitotic regulation of the anaphase-promoting complex. Cell Mol Life Sci 64: 589-600
4. Bomont P, Maddox P, Shah JV, Desai AB, Cleveland DW (2005) Unstable microtubule capture at kinetochores depleted of the centromere-associated protein CENP-F. EMBO J 24: 3927-3939
5. Cahill DP, da Costa LT, Carson-Walter EB, Kinzler KW, Vogelstein B, Lengauer C (1999) Characterization of MAD2B and other mitotic spindle checkpoint genes. Genomics 58: 181-187
6. Cassimeris L, Morabito J (2004) TOGp, the human homolog of XMAP215/Dis1, is required for centrosome integrity, spindle pole organization, and bipolar spindle assembly. Mol Biol Cell 15: 1580-1590
7. Chan GK, Schaar BT, Yen TJ (1998) Characterization of the kine-tochore binding domain of CENP-E reveals interactions with the kinetochore proteins CENP-F and hBUBR1. J Cell Biol 143: 49-63
8. 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
9. Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9: 33-46
10. Chen J, Fang G (2001) MAD2B is an inhibitor of the anaphase-promoting complex. Genes Dev 15: 1765-1770
11. Cheung HW, Chun AC, Wang Q, Deng W, Hu L, Guan XY, Nicholls JM, Ling MT, Chuan Wong Y, Tsao SW, Jin DY, Wang X (2006) Inactivation of human MAD2B in nasopharyngeal carcinoma cells leads to chemosensitization to DNA-damaging agents. Cancer Res 66: 4357-4367
12. Dai J, Sultan S, Taylor SS, Higgins JM (2005) The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev 19: 472-488
13. Daum JR, Wren JD, Daniel JJ, Sivakumar S, McAvoy JN, Potapova TA, Gorbsky GJ (2009) Ska3 is required for spindle checkpoint silencing and the maintenance of chromosome cohesion in mitosis. Curr Biol 19: 1467-1472
14. De Luca M, Brunetto L, Asteriti IA, Giubettini M, Lavia P, Guarguaglini G (2008) Aurora-A and ch-TOG act in a common pathway in control of spindle pole integrity. Oncogene 27: 6539-6549
15. Draviam VM, Shapiro I, Aldridge B, Sorger PK (2006) Misorientation and reduced stretching of aligned sister kineto-chores promote chromosome missegregation in EB1- or APC-depleted cells. EMBO J 25: 2814-2827
16. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208
17. Feng J, Huang H, Yen TJ (2006) CENP-F is a novel microtubule-binding protein that is essential for kinetochore attachments and affects the duration of the mitotic checkpoint delay. Chromosoma 115: 320-329
18. Gaitanos TN, Santamaria A, Jeyaprakash AA, Wang B, Conti E, Nigg EA (2009) Stable kinetochore-microtubule interactions depend on the Ska complex and its new component Ska3/C13Orf3. EMBO J 28: 1442-1452
19. Gan GN, Wittschieben JP, Wittschieben BO, Wood RD (2008) DNA polymerase zeta (pol zeta) in higher eukaryotes. Cell Res 18: 174-183
20. Ganem NJ, Storchova Z, Pellman D (2007) Tetraploidy, aneuploidy and cancer. Curr Opin Genet Dev 17: 157-162
21. Gimenez-Abian JF, Sumara I, Hirota T, Hauf S, Gerlich D, de la Torre C, Ellenberg J, Peters JM (2004) Regulation of sister chromatid cohesion between chromosome arms. Curr Biol 14: 1187-1193
22. Green RA, Wollman R, Kaplan KB (2005) APC and EB1 function together in mitosis to regulate spindle dynamics and chromosome alignment. Mol Biol Cell 16: 4609-4622
23. Hanisch A, Sillje HH, Nigg EA (2006) Timely anaphase onset requires a novel spindle and kinetochore complex comprising Ska1 and Ska2. EMBO J 25: 5504-5515
24. Hoffman DB, Pearson CG, Yen TJ, Howell BJ, Salmon ED (2001) Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol Biol Cell 12: 1995-2009
25. Holt SV, Vergnolle MA, Hussein D, Wozniak MJ, Allan VJ, Taylor SS (2005) Silencing Cenp-F weakens centromeric cohesion, prevents chromosome alignment and activates the spindle checkpoint. J Cell Sci 118: 4889-4900
26. Howell BJ, Moree B, Farrar EM, Stewart S, Fang G, Salmon ED (2004) Spindle checkpoint protein dynamics at kinetochores in living cells. Curr Biol 14: 953-964
27. Hussein D, Taylor SS (2002) Farnesylation of Cenp-F is required for G2/M progression and degradation after mitosis. J Cell Sci 115: 3403-3414
28. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32: 1037-1049
29. Ishida T, Kinoshita K (2007) PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Res 35: W460-W464
30. Iwai H, Kim M, Yoshikawa Y, Ashida H, Ogawa M, Fujita Y, Muller D, Kirikae T, Jackson PK, Kotani S, Sasakawa C (2007) A bacterial effector targets Mad2L2, an APC inhibitor, to modulate host cell cycling. Cell 130: 611-623
31. Johnson VL, Scott MI, Holt SV, Hussein D, Taylor SS (2004) Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression. J Cell Sci 117: 1577-1589
32. Khodjakov A, Copenagle L, Gordon MB, Compton DA, Kapoor TM (2003) Minus-end capture of preformed kinetochore fibers contributes to spindle morphogenesis. J Cell Biol 160: 671-683
33. Kiyomitsu T, Iwasaki O, Obuse C, Yanagida M (2010) Inner centromere formation requires hMis14, a trident kinetochore protein that specifically recruits HP1 to human chromosomes. J Cell Biol 188: 791-807
34. Laoukili J, Kooistra MR, Bras A, Kauw J, Kerkhoven RM, Morrison A, Clevers H, Medema RH (2005) FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol 7: 126-136
35. Lawo S, Bashkurov M, Mullin M, Ferreria MG, Kittler R, Habermann B, Tagliaferro A, Poser I, Hutchins JR, Hegemann B, Pinchev D, Buchholz F, Peters JM, Hyman AA, Gingras AC, Pelletier L (2009) HAUS, the 8-subunit human Augmin complex, regulates centro-some and spindle integrity. Curr Biol 19: 816-826
36. Liu D, Ding X, Du J, Cai X, Huang Y, Ward T, Shaw A, Yang Y, Hu R, Jin C, Yao X (2007) Human NUF2 interacts with centromere-associated protein E and is essential for a stable spindle micro-tubule-kinetochore attachment. J Biol Chem 282: 21415-21424
37. Maiato H, Rieder CL, Khodjakov A (2004) Kinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis. J Cell Biol 167: 831-840
38. McEwen BF, Chan GK, Zubrowski B, Savoian MS, Sauer MT, Yen TJ (2001) CENP-E is essential for reliable bioriented spindle attachment, but chromosome alignment can be achieved via redundant mechanisms in mammalian cells. Mol Biol Cell 12: 2776-2789
39. Medendorp K, van Groningen JJ, Vreede L, Hetterschijt L, van den Hurk WH, de Bruijn DR, Brugmans L, van Kessel AG (2009) The mitotic arrest deficient protein MAD2B interacts with the small GTPase RAN throughout the cell cycle. PLoS One 4: e7020
40. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393
41. Nakajima M, Kumada K, Hatakeyama K, Noda T, Peters JM, Hirota T (2007) The complete removal of cohesin from chromosome arms depends on separase. J Cell Sci 120: 4188-4196
42. Okada T, Sonoda E, Yoshimura M, Kawano Y, Saya H, Kohzaki M, Takeda S (2005) Multiple roles of vertebrate REV genes in DNA repair and recombination. Mol Cell Biol 25: 6103-6111
43. Pfleger CM, Salic A, Lee E, Kirschner MW (2001) Inhibition of Cdh1-APC by the MAD2-related protein MAD2L2: a novel mechanism for regulating Cdh1. Genes Dev 15: 1759-1764
44. Putkey FR, Cramer T, Morphew MK, Silk AD, Johnson RS, McIntosh JR, Cleveland DW (2002) Unstable kinetochore-microtubule capture and chromosomal instability following deletion of CENP-E. Dev Cell 3: 351-365
45. Raaijmakers JA, Tanenbaum ME, Maia AF, Medema RH (2009) RAMA1 is a novel kinetochore protein involved in kinetochore-microtubule attachment. J Cell Sci 122: 2436-2445
46. Ricke RM, van Ree JH, van Deursen JM (2008) Whole chromosome instability and cancer: a complex relationship. Trends Genet 24: 457-466
47. Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812
48. Savoian MS, Earnshaw WC, Khodjakov A, Rieder CL (1999) Cleavage furrows formed between centrosomes lacking an intervening spindle and chromosomes contain microtubule bundles, INCENP, and CHO1 but not CENP-E. Mol Biol Cell 10: 297-311
49. Schaar BT, Chan GK, Maddox P, Salmon ED, Yen TJ (1997) CENP-E function at kinetochores is essential for chromosome alignment. J Cell Biol 139: 1373-1382
50. Schafer-Hales K, Iaconelli J, Snyder JP, Prussia A, Nettles JH, El-Naggar A, Khuri FR, Giannakakou P, Marcus AI (2007) Farnesyl transferase inhibitors impair chromosomal maintenance in cell lines and human tumors by compromising CENP-E and CENP-F function. Mol Cancer Ther 6: 1317-1328
51. Tanaka K, Hirota T (2009) Chromosome segregation machinery and cancer. Cancer Sci 100: 1158-1165
52. Tanaka K, Kitamura E, Kitamura Y, Tanaka TU (2007) Molecular mechanisms of microtubule-dependent kinetochore transport toward spindle poles. J Cell Biol 178: 269-281
53. Tanaka TU (2008) Bi-orienting chromosomes: acrobatics on the mitotic spindle. Chromosoma 117: 521-533
54. Tanaka TU, Desai A (2008) Kinetochore-microtubule interactions: the means to the end. Curr Opin Cell Biol 20: 53-63
55. Tanaka TU, Stark MJ, Tanaka K (2005) Kinetochore capture and bi-orientation on the mitotic spindle. Nat Rev Mol Cell Biol 6: 929-942 (Pubitemid 41778712)
56. Tanenbaum ME, Galjart N, van Vugt MA, Medema RH (2006) CLIP-170 facilitates the formation of kinetochore-microtubule attachments. EMBO J 25: 45-57
57. Theis M, Slabicki M, Junqueira M, Paszkowski-Rogacz M, Sontheimer J, Kittler R, Heninger AK, Glatter T, Kruusmaa K, Poser I, Hyman AA, Pisabarro MT, Gstaiger M, Aebersold R, Shevchenko A, Buchholz F (2009) Comparative profiling identifies C13orf3 as a component of the Ska complex required for mammalian cell division. EMBO J 28: 1453-1465
58. Tokai-Nishizumi N, Ohsugi M, Suzuki E, Yamamoto T (2005) The chromokinesin Kid is required for maintenance of proper meta-phase spindle size. Mol Biol Cell 16: 5455-5463
59. Tulu US, Fagerstrom C, Ferenz NP, Wadsworth P (2006) Molecular requirements for kinetochore-associated microtubule formation in mammalian cells. Curr Biol 16: 536-541
60. Uehara R, Nozawa RS, Tomioka A, Petry S, Vale RD, Obuse C, Goshima G (2009) The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc Natl Acad Sci USA 106: 6998-7003
61. Vergnolle MA, Taylor SS (2007) Cenp-F links kinetochores to Ndel1/ Nde1/Lis1/dynein microtubule motor complexes. Curr Biol 17: 1173-1179
62. Walczak CE, Cai S, Khodjakov A (2010) Mechanisms of chromosome behaviour during mitosis. Nat Rev Mol Cell Biol 11 : 91-102
63. Weaver BA, Cleveland DW (2005) Decoding the links between mitosis, cancer, and chemotherapy: The mitotic checkpoint, adaptation, and cell death. Cancer Cell 8: 7-12
64. Welburn JP, Grishchuk EL, Backer CB, Wilson-Kubalek EM, Yates III JR, Cheeseman IM (2009) The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev Cell 16: 374-385
65. Westermann S, Wang HW, Avila-Sakar A, Drubin DG, Nogales E, Barnes G (2006) The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends. Nature 440: 565-569
66. Wong J, Fang G (2006) HURP controls spindle dynamics to promote proper interkinetochore tension and efficient kinetochore capture. J Cell Biol 173: 879-891
67. Yang Z, Guo J, Chen Q, Ding C, Du J, Zhu X (2005) Silencing mitosin induces misaligned chromosomes, premature chromosome de-condensation before anaphase onset, and mitotic cell death. Mol Cell Biol 25: 4062-4074
68. Yao X, Abrieu A, Zheng Y, Sullivan KF, Cleveland DW (2000) CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint. Nat Cell Biol 2: 484-491
69. Yokoyama H, Rybina S, Santarella-Mellwig R, Mattaj IW, Karsenti E (2009) ISWI is a RanGTP-dependent MAP required for chromosome segregation. J Cell Biol 187: 813-829
70. Zhang XD, Goeres J, Zhang H, Yen TJ, Porter AC, Matunis MJ (2008) SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol Cell 29: 729-741