Misregulation of Scm3p/HJURP causes chromosome instability in saccharomyces cerevisiae and human cells

PLoS Genetics

Volumn 7, Issue 9, 2011, Pages

  Mishra, Prashant K ^a   Au, Wei Chun ^a   Choy, John S ^a   Kuich, P Henning ^b   Baker, Richard E ^c   Foltz, Daniel R ^b   Basrai, Munira A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H4; HOLLIDAY JUNCTION RECOGNITION PROTEIN; NUCLEAR PROTEIN; SUPPRESSOR OF CHROMOSOME MISSEGREGATION 3P PROTEIN; UNCLASSIFIED DRUG; CSE4 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; HISTONE; HOLLIDAY JUNCTION RECOGNIZING PROTEIN, HUMAN; NONHISTONE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SCM3 PROTEIN, S CEREVISIAE;

ARTICLE; CELL CYCLE REGULATION; CENTROMERE; CHROMOSOMAL INSTABILITY; CHROMOSOME LOSS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID; STOICHIOMETRY; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; GENE EXPRESSION; GENETICS; METABOLISM;

MAMMALIA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCETACEAE;

CENTROMERE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL INSTABILITY; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; DNA-BINDING PROTEINS; GENE EXPRESSION; HISTONES; HUMANS; KINETOCHORES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 80053435885     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002303     Document Type: Article

References (62)

1. Lengauer C, Kinzler KW, Vogelstein B, (1998) Genetic instabilities in human cancers. Nature 396: 643-649.
2. Skibbens RV, Hieter P, (1998) Kinetochores and the checkpoint mechanism that monitors for defects in the chromosome segregation machinery. Annu Rev Genet 32: 307-337.
3. Ekwall K, (2007) Epigenetic control of centromere behavior. Annu Rev Genet 41: 63-81.
4. Buscaino A, Allshire R, Pidoux A, (2010) Building centromeres: home sweet home or a nomadic existence? Curr Opin Genet Dev 20: 118-126.
5. Cheeseman IM, Drubin DG, Barnes G, (2002) Simple centromere, complex kinetochore: linking spindle microtubules and centromeric DNA in budding yeast. J Cell Biol 157: 199-203.
6. Cleveland DW, Mao Y, Sullivan KF, (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112: 407-421.
7. Hyman AA, Sorger PK, (1995) Structure and function of kinetochores in budding yeast. Annu Rev Cell Dev Biol 11: 471-495.
8. Blower MD, Karpen GH, (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat Cell Biol 3: 730-739.
9. Buchwitz BJ, Ahmad K, Moore LL, Roth MB, Henikoff S, (1999) A histone-H3-like protein in C. elegans. Nature 401: 547-548.
10. Chen ES, Saitoh S, Yanagida M, Takahashi K, (2003) A cell cycle-regulated GATA factor promotes centromeric localization of CENP-A in fission yeast. Mol Cell 11: 175-187.
11. Meluh PB, Yang P, Glowczewski L, Koshland D, Smith MM, (1998) Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94: 607-613.
12. Smith MM, Yang P, Santisteban MS, Boone PW, Goldstein AT, et al. (1996) A novel histone H4 mutant defective in nuclear division and mitotic chromosome transmission. Mol Cell Biol 16: 1017-1026.
13. Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M, (1995) A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev 9: 573-586.
14. Karpen GH, Allshire RC, (1997) The case for epigenetic effects on centromere identity and function. Trends Genet 13: 489-496.
15. 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.
16. Measday V, Hailey DW, Pot I, Givan SA, Hyland KM, et al. (2002) Ctf3p, the Mis6 budding yeast homolog, interacts with Mcm22p and Mcm16p at the yeast outer kinetochore. Genes Dev 16: 101-113.
17. Furuyama S, Biggins S, (2007) Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci U S A 104: 14706-14711.
18. Camahort R, Li B, Florens L, Swanson SK, Washburn MP, et al. (2007) Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol Cell 26: 853-865.
19. Mizuguchi G, Xiao H, Wisniewski J, Smith MM, Wu C, (2007) Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129: 1153-1164.
20. Stoler S, Rogers K, Weitze S, Morey L, Fitzgerald-Hayes M, et al. (2007) Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc Natl Acad Sci U S A 104: 10571-10576.
21. Zhang W, Mellone BG, Karpen GH, (2007) A specialized nucleosome has a "point" to make. Cell 129: 1047-1049.
22. Zhou Z, Feng H, Zhou BR, Ghirlando R, Hu K, et al. (2011) Structural basis for recognition of centromere histone variant CenH3 by the chaperone Scm3. Nature 472: 234-237.
23. Cho US, Harrison SC, (2011) Recognition of the centromere-specific histone Cse4 by the chaperone Scm3. Proc Natl Acad Sci U S A.
24. Sanchez-Pulido L, Pidoux AL, Ponting CP, Allshire RC, (2009) Common ancestry of the CENP-A chaperones Scm3 and HJURP. Cell 137: 1173-1174.
25. Hu H, Liu Y, Wang M, Fang J, Huang H, et al. (2011) Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes Dev 25: 901-906.
26. Foltz DR, Jansen LE, Bailey AO, Yates JR, 3rd, Bassett EA, et al. (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137: 472-484.
27. Shuaib M, Ouararhni K, Dimitrov S, Hamiche A, (2010) HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres. Proc Natl Acad Sci U S A 107: 1349-1354.
28. Camahort R, Shivaraju M, Mattingly M, Li B, Nakanishi S, et al. (2009) Cse4 is part of an octameric nucleosome in budding yeast. Mol Cell 35: 794-805.
29. Shivaraju M, Camahort R, Mattingly M, Gerton JL, (2011) Scm3 is a centromeric nucleosome assembly factor. J Biol Chem 286: 12016-12023.
30. Pidoux AL, Choi ES, Abbott JK, Liu X, Kagansky A, et al. (2009) Fission yeast Scm3: A CENP-A receptor required for integrity of subkinetochore chromatin. Mol Cell 33: 299-311.
31. Williams JS, Hayashi T, Yanagida M, Russell P, (2009) Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol Cell 33: 287-298.
32. Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray-Gallet D, et al. (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137: 485-497.
33. Bernad R, Sanchez P, Rivera T, Rodriguez-Corsino M, Boyarchuk E, et al. (2011) Xenopus HJURP and condensin II are required for CENP-A assembly. J Cell Biol 192: 569-582.
34. Castillo AG, Mellone BG, Partridge JF, Richardson W, Hamilton GL, et al. (2007) Plasticity of fission yeast CENP-A chromatin driven by relative levels of histone H3 and H4. PLoS Genet 3: e121 doi:10.1371/journal.pgen.0030121.
35. Au WC, Crisp MJ, DeLuca SZ, Rando OJ, Basrai MA, (2008) Altered dosage and mislocalization of histone H3 and Cse4p lead to chromosome loss in Saccharomyces cerevisiae. Genetics 179: 263-275.
36. Heun P, Erhardt S, Blower MD, Weiss S, Skora AD, et al. (2006) Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 10: 303-315.
37. Tomonaga T, Matsushita K, Yamaguchi S, Oohashi T, Shimada H, et al. (2003) Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res 63: 3511-3516.
38. Kato T, Sato N, Hayama S, Yamabuki T, Ito T, et al. (2007) Activation of Holliday junction recognizing protein involved in the chromosomal stability and immortality of cancer cells. Cancer Res 67: 8544-8553.
39. Hu Z, Huang G, Sadanandam A, Gu S, Lenburg ME, et al. (2010) The expression level of HJURP has an independent prognostic impact and predicts the sensitivity to radiotherapy in breast cancer. Breast Cancer Res 12: R18.
40. Glowczewski L, Yang P, Kalashnikova T, Santisteban MS, Smith MM, (2000) Histone-histone interactions and centromere function. Mol Cell Biol 20: 5700-5711.
41. Hewawasam G, Shivaraju M, Mattingly M, Venkatesh S, Martin-Brown S, et al. (2010) Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol Cell 40: 444-454.
42. Calvert ME, Lannigan J, (2010) Yeast cell cycle analysis: combining DNA staining with cell and nuclear morphology. Curr Protoc Cytom Chapter 9 Unit 9 32 31-16.
43. 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.
44. Ng TM, Waples WG, Lavoie BD, Biggins S, (2009) Pericentromeric sister chromatid cohesion promotes kinetochore biorientation. Mol Biol Cell 20: 3818-3827.
45. Wang L, Yang MQ, Yang JY, (2009) Prediction of DNA-binding residues from protein sequence information using random forests. BMC Genomics 10 (Suppl 1): S1.
46. Bailey TL, Elkan C, (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
47. Ranjitkar P, Press MO, Yi X, Baker R, MacCoss MJ, et al. (2010) An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol Cell 40: 455-464.
48. 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.
49. Eckert CA, Gravdahl DJ, Megee PC, (2007) The enhancement of pericentromeric cohesin association by conserved kinetochore components promotes high-fidelity chromosome segregation and is sensitive to microtubule-based tension. Genes Dev 21: 278-291.
50. McCarroll RM, Fangman WL, (1988) Time of replication of yeast centromeres and telomeres. Cell 54: 505-513.
51. Kitamura E, Tanaka K, Kitamura Y, Tanaka TU, (2007) Kinetochore microtubule interaction during S phase in Saccharomyces cerevisiae. Genes Dev 21: 3319-3330.
52. Jansen LE, Black BE, Foltz DR, Cleveland DW, (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176: 795-805.
53. Barnhart MC, Kuich PH, Stellfox ME, Ward JA, Bassett EA, et al. (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 194: 229-243.
54. Amato A, Schillaci T, Lentini L, Di Leonardo A, (2009) CENPA overexpression promotes genome instability in pRb-depleted human cells. Mol Cancer 8: 119.
55. Spencer F, Gerring SL, Connelly C, Hieter P, (1990) Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124: 237-249.
56. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
57. Kastenmayer JP, Lee MS, Hong AL, Spencer FA, Basrai MA, (2005) The C-terminal half of Saccharomyces cerevisiae Mad1p mediates spindle checkpoint function, chromosome transmission fidelity and CEN association. Genetics 170: 509-517.
58. Collins KA, Camahort R, Seidel C, Gerton JL, Biggins S, (2007) The overexpression of a Saccharomyces cerevisiae centromeric histone H3 variant mutant protein leads to a defect in kinetochore biorientation. Genetics 175: 513-525.
59. Tong AH, Boone C, (2006) Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol Biol 313: 171-192.
60. Pot I, Knockleby J, Aneliunas V, Nguyen T, Ah-Kye S, et al. (2005) Spindle checkpoint maintenance requires Ame1 and Okp1. Cell Cycle 4: 1448-1456.
61. Mumberg D, Muller R, Funk M, (1994) Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res 22: 5767-5768.
62. Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, et al. (2005) Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev 19: 2816-2826.