A coordinated interdependent protein circuitry stabilizes the kinetochore ensemble to protect CENP-A in the human pathogenic yeast Candida albicans

PLoS Genetics

Volumn 8, Issue 4, 2012, Pages

  Thakur, Jitendra ^a   Sanyal, Kaustuv ^a  

^a JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; CENTROMERE PROTEIN C; FUNGAL PROTEIN; PROTEIN DAM1; UNCLASSIFIED DRUG; AUTOANTIGEN; CELL CYCLE PROTEIN; DAM1 PROTEIN, S CEREVISIAE; HISTONE; MICROTUBULE ASSOCIATED PROTEIN; NONHISTONE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BINDING AFFINITY; CANDIDA ALBICANS; CELL LEVEL; CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FUNCTIONAL PROTEOMICS; GENETIC CONSERVATION; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STRUCTURE ANALYSIS; WESTERN BLOTTING; CHROMATIN; CHROMOSOME; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; SACCHAROMYCES CEREVISIAE; ULTRASTRUCTURE;

CANDIDA ALBICANS; EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

AUTOANTIGENS; CANDIDA ALBICANS; CELL CYCLE PROTEINS; CENTROMERE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; EPIGENESIS, GENETIC; HISTONES; HUMANS; KINETOCHORES; MICROTUBULE-ASSOCIATED PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84860555258     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002661     Document Type: Article

References (63)

1. Allshire RC, Karpen GH, (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9: 923-937.
2. Clarke L, Carbon J, (1980) ISOLATION OF A YEAST CENTROMERE AND CONSTRUCTION OF FUNCTIONAL SMALL CIRCULAR CHROMOSOMES. Nature 287: 504-509.
3. Clarke L, (1990) Centromeres of budding and fission yeasts. Trends Genet 6: 150-154.
4. Fishel B, Amstutz H, Baum M, Carbon J, Clarke L, (1988) Structural organization and functional analysis of centromeric DNA in the fission yeast Schizosaccharomyces pombe. Mol Cell Biol 8: 754-763.
5. Sun X, Wahlstrom J, Karpen G, (1997) Molecular structure of a functional Drosophila centromere. Cell 91: 1007-1019.
6. 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.
7. 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.
8. Dimitriadis EK, Weber C, Gill RK, Diekmann S, Dalal Y, (2010) Tetrameric organization of vertebrate centromeric nucleosomes. Proc Natl Acad Sci U S A 107: 20317-20322.
9. 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.
10. Foltz DR, Jansen LE, Bailey AO, Yates JR, Bassett EA, et al. (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137: 472-484.
11. Ekwall K, (2007) Epigenetic control of centromere behavior. Annu Rev Genet 41: 63-81.
12. 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.
13. Desai A, Rybina S, Müller-Reichert T, Shevchenko A, Hyman A, et al. (2003) KNL-1 directs assembly of the microtubule-binding interface of the kinetochore in C. elegans. Genes Dev 17: 2421-2435.
14. Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA, (2001) Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol 153: 1209-1226.
15. Goshima G, Kiyomitsu T, Yoda K, Yanagida M, (2003) Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J Cell Biol 160: 25-39.
16. Hajra S, Ghosh SK, Jayaram M, (2006) The centromere-specific histone variant Cse4p (CENP-A) is essential for functional chromatin architecture at the yeast 2-microm circle partitioning locus and promotes equal plasmid segregation. J Cell Biol 174: 779-790.
17. Roy B, Burrack LS, Lone MA, Berman J, Sanyal K, (2011) CaMtw1, a member of the evolutionarily conserved Mis12 kinetochore protein family, is required for efficient inner kinetochore assembly in the pathogenic yeast Candida albicans. Mol Microbiol.
18. Hayashi T, Fujita Y, Iwasaki O, Adachi Y, Takahashi K, et al. (2004) Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118: 715-729.
19. Takahashi K, Takayama Y, Masuda F, Kobayashi Y, Saitoh S, (2005) Two distinct pathways responsible for the loading of CENP-A to centromeres in the fission yeast cell cycle. Philos Trans R Soc Lond B Biol Sci 360: 595-606; discussion 606-597.
20. 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.
21. Cleveland DW, Mao Y, Sullivan KF, (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112: 407-421.
22. Lechner J, Carbon J, (1991) A 240 kd multisubunit protein complex, CBF3, is a major component of the budding yeast centromere. Cell 64: 717-725.
23. De Wulf P, McAinsh AD, Sorger PK, (2003) Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev 17: 2902-2921.
24. Cheeseman IM, Desai A, (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9: 33-46.
25. McAinsh AD, Tytell JD, Sorger PK, (2003) Structure, function, and regulation of budding yeast kinetochores. Annu Rev Cell Dev Biol 19: 519-539.
26. Welburn JP, Grishchuk EL, Backer CB, Wilson-Kubalek EM, Yates JR, et al. (2009) The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev Cell 16: 374-385.
27. Bharadwaj R, Qi W, Yu H, (2004) Identification of two novel components of the human NDC80 kinetochore complex. J Biol Chem 279: 13076-13085.
28. Cheeseman IM, Brew C, Wolyniak M, Desai A, Anderson S, et al. (2001) Implication of a novel multiprotein Dam1p complex in outer kinetochore function. J Cell Biol 155: 1137-1145.
29. 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.
30. Janke C, Ortiz J, Tanaka TU, Lechner J, Schiebel E, (2002) Four new subunits of the Dam1-Duo1 complex reveal novel functions in sister kinetochore biorientation. Embo Journal 21: 181-193.
31. Jin QW, Fuchs J, Loidl J, (2000) Centromere clustering is a major determinant of yeast interphase nuclear organization. J Cell Sci 113 (Pt 11): 1903-1912.
32. Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, et al. (2010) A three-dimensional model of the yeast genome. Nature 465: 363-367.
33. Anderson M, Haase J, Yeh E, Bloom K, (2009) Function and assembly of DNA looping, clustering, and microtubule attachment complexes within a eukaryotic kinetochore. Mol Biol Cell 20: 4131-4139.
34. Funabiki H, Hagan I, Uzawa S, Yanagida M, (1993) Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J Cell Biol 121: 961-976.
35. Brenner S, Pepper D, Berns MW, Tan E, Brinkley BR, (1981) Kinetochore structure, duplication, and distribution in mammalian cells: analysis by human autoantibodies from scleroderma patients. J Cell Biol 91: 95-102.
36. Monen J, Maddox PS, Hyndman F, Oegema K, Desai A, (2005) Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7: 1248-1255.
37. Ketel C, Wang HS, McClellan M, Bouchonville K, Selmecki A, et al. (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5: e1000400 doi:10.1371/journal.pgen.1000400.
38. Marshall OJ, Chueh AC, Wong LH, Choo KH, (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82: 261-282.
39. Ishii K, Ogiyama Y, Chikashige Y, Soejima S, Masuda F, et al. (2008) Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science 321: 1088-1091.
40. Williams BC, Murphy TD, Goldberg ML, Karpen GH, (1998) Neocentromere activity of structurally acentric mini-chromosomes in Drosophila. Nat Genet 18: 30-37.
41. Moreno-Moreno O, Torras-Llort M, Azorín F, (2006) Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Res 34: 6247-6255.
42. 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.
43. Collins KA, Castillo AR, Tatsutani SY, Biggins S, (2005) De novo kinetochore assembly requires the centromeric histone H3 variant. Mol Biol Cell 16: 5649-5660.
44. Joglekar AP, Bouck D, Finley K, Liu X, Wan Y, et al. (2008) Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J Cell Biol 181: 587-594.
45. Baum M, Sanyal K, Mishra PK, Thaler N, Carbon J, (2006) Formation of functional centromeric chromatin is specified epigenetically in Candida albicans. Proc Natl Acad Sci U S A 103: 14877-14882.
46. Sanyal K, Baum M, Carbon J, (2004) Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc Natl Acad Sci U S A 101: 11374-11379.
47. Padmanabhan S, Thakur J, Siddharthan R, Sanyal K, (2008) Rapid evolution of Cse4p-rich centromeric DNA sequences in closely related pathogenic yeasts, Candida albicans and Candida dubliniensis. Proc Natl Acad Sci U S A 105: 19797-19802.
48. Sanyal K, Carbon J, (2002) The CENP-A homolog CaCse4p in the pathogenic yeast Candida albicans is a centromere protein essential for chromosome transmission. Proc Natl Acad Sci U S A 99: 12969-12974.
49. Thakur J, Sanyal K, (2011) The essentiality of the fungus-specific Dam1 complex is correlated with a one-kinetochore-one-microtubule interaction present throughout the cell cycle, independent of the nature of a centromere. Eukaryot Cell 10: 1295-1305.
50. Care RS, Trevethick J, Binley KM, Sudbery PE, (1999) The MET3 promoter: a new tool for Candida albicans molecular genetics. Mol Microbiol 34: 792-798.
51. Leuker CE, Sonneborn A, Delbrück S, Ernst JF, (1997) Sequence and promoter regulation of the PCK1 gene encoding phosphoenolpyruvate carboxykinase of the fungal pathogen Candida albicans. Gene 192: 235-240.
52. Tanaka TU, (2010) Kinetochore-microtubule interactions: steps towards bi-orientation. EMBO J 29: 4070-4082.
53. Tanaka K, Kitamura E, Tanaka TU, (2010) Live-cell analysis of kinetochore-microtubule interaction in budding yeast. Methods 51: 206-213.
54. Liu X, McLeod I, Anderson S, Yates JR, He X, (2005) Molecular analysis of kinetochore architecture in fission yeast. EMBO J 24: 2919-2930.
55. Liu ST, Rattner JB, Jablonski SA, Yen TJ, (2006) Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J Cell Biol 175: 41-53.
56. Régnier V, Vagnarelli P, Fukagawa T, Zerjal T, Burns E, et al. (2005) CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol Cell Biol 25: 3967-3981.
57. Westermann S, Cheeseman IM, Anderson S, Yates JR, Drubin DG, et al. (2003) Architecture of the budding yeast kinetochore reveals a conserved molecular core. J Cell Biol 163: 215-222.
58. Przewloka MR, Zhang W, Costa P, Archambault V, D'Avino PP, et al. (2007) Molecular analysis of core kinetochore composition and assembly in Drosophila melanogaster. PLoS ONE 2: e478 doi:10.1371/journal.pone.0000478.
59. Takahashi K, Chen ES, Yanagida M, (2000) Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science 288: 2215-2219.
60. Straight AF, Marshall WF, Sedat JW, Murray AW, (1997) Mitosis in living budding yeast: anaphase A but no metaphase plate. Science 277: 574-578.
61. Dekker J, Rippe K, Dekker M, Kleckner N, (2002) Capturing chromosome conformation. Science 295: 1306-1311.
62. Gerami-Nejad M, Berman J, Gale CA, (2001) Cassettes for PCR-mediated construction of green, yellow, and cyan fluorescent protein fusions in Candida albicans. Yeast 18: 859-864.
63. Reuss O, Vik A, Kolter R, Morschhäuser J, (2004) The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119-127.