Rad51-Rad52 Mediated Maintenance of Centromeric Chromatin in Candida albicans

PLoS Genetics

Volumn 10, Issue 4, 2014, Pages

  Mitra, Sreyoshi ^a   Gómez Raja, Jonathan ^b   Larriba, Germán ^b   Dubey, Dharani Dhar ^c   Sanyal, Kaustuv ^a  

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

^b UNIVERSITY OF EXTREMADURA   (Spain)

^c VEER BAHADUR SINGH PURVANCHAL UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; RAD51 PROTEIN; RAD52 PROTEIN; CHROMATIN; FUNGAL PROTEIN; HISTONE; NONHISTONE PROTEIN;

ARTICLE; BINDING SITE; CANDIDA ALBICANS; CENTROMERE; CHROMOSOME 5; CHROMOSOME 7; CHROMOSOME DELETION; CHROMOSOME LOSS; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA RECOMBINATION; DNA REPLICATION; G2 PHASE CELL CYCLE CHECKPOINT; HETEROZYGOSITY LOSS; HOMOLOGOUS RECOMBINATION; M PHASE CELL CYCLE CHECKPOINT; NONHUMAN; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; S PHASE CELL CYCLE CHECKPOINT; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA REPLICATION ORIGIN; GENETICS; METABOLISM; PROCEDURES;

CANDIDA ALBICANS; CENTROMERE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA REPLICATION; FUNGAL PROTEINS; HISTONES; HOMOLOGOUS RECOMBINATION; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; REPLICATION ORIGIN;

EID: 84901306855     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004344     Document Type: Article

References (73)

1. Earnshaw WC, Migeon BR, (1985) Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 92: 290-296.
2. Allshire RC, Karpen GH, (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9: 923-937.
3. Yamazaki S, Hayano M, Masai H, (2013) Replication timing regulation of eukaryotic replicons: Rif1 as a global regulator of replication timing. Trends Genet 29: 449-460.
4. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, et al. (2001) Replication dynamics of the yeast genome. Science 294: 115-121.
5. Koren A, Tsai HJ, Tirosh I, Burrack LS, Barkai N, et al. (2010) Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet 6: e1001068.
6. Kim SM, Dubey DD, Huberman JA, (2003) Early-replicating heterochromatin. Genes Dev 17: 330-335.
7. Tiengwe C, Marcello L, Farr H, Dickens N, Kelly S, et al. (2012) Genome-wide analysis reveals extensive functional interaction between DNA replication initiation and transcription in the genome of Trypanosoma brucei. Cell Rep 2: 185-197.
8. Aravamudhan P, Felzer-Kim I, Joglekar AP, (2013) The Budding Yeast Point Centromere Associates with Two Cse4 Molecules during Mitosis. Curr Biol 23: 770-774.
9. 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.
10. Takayama Y, Sato H, Saitoh S, Ogiyama Y, Masuda F, et al. (2008) Biphasic incorporation of centromeric histone CENP-A in fission yeast. Mol Biol Cell 19: 682-690.
11. Lando D, Endesfelder U, Berger H, Subramanian L, Dunne PD, et al. (2012) Quantitative single-molecule microscopy reveals that CENP-A(Cnp1) deposition occurs during G2 in fission yeast. Open Biol 2: 120078.
12. Gonzalez M, He H, Sun S, Li C, Li F, (2013) Cell cycle-dependent deposition of CENP-A requires the Dos1/2-Cdc20 complex. Proc Natl Acad Sci U S A 110: 606-611.
13. Livny J, Yamaichi Y, Waldor MK, (2007) Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol 189: 8693-8703.
14. Vernis L, Abbas A, Chasles M, Gaillardin CM, Brun C, et al. (1997) An origin of replication and a centromere are both needed to establish a replicative plasmid in the yeast Yarrowia lipolytica. Mol Cell Biol 17: 1995-2004.
15. Smith JG, Caddle MS, Bulboaca GH, Wohlgemuth JG, Baum M, et al. (1995) Replication of centromere II of Schizosaccharomyces pombe. Mol Cell Biol 15: 5165-5172.
16. Hayashi MT, Takahashi TS, Nakagawa T, Nakayama J, Masukata H, (2009) The heterochromatin protein Swi6/HP1 activates replication origins at the pericentromeric region and silent mating-type locus. Nat Cell Biol 11: 357-362.
17. Gruber S, Errington J, (2009) Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137: 685-696.
18. Kitamura E, Tanaka K, Kitamura Y, Tanaka TU, (2007) Kinetochore microtubule interaction during S phase in Saccharomyces cerevisiae. Genes Dev 21: 3319-3330.
19. Pohl TJ, Brewer BJ, Raghuraman MK, (2012) Functional centromeres determine the activation time of pericentric origins of DNA replication in Saccharomyces cerevisiae. PLoS Genet 8: e1002677.
20. Natsume T, Muller CA, Katou Y, Retkute R, Gierlinski M, et al. (2013) Kinetochores coordinate pericentromeric cohesion and early DNA replication by cdc7-dbf4 kinase recruitment. Mol Cell 50: 661-674.
21. Greenfeder SA, Newlon CS, (1992) Replication forks pause at yeast centromeres. Mol Cell Biol 12: 4056-4066.
22. Greenfeder SA, Newlon CS, (1992) A replication map of a 61-kb circular derivative of Saccharomyces cerevisiae chromosome III. Mol Biol Cell 3: 999-1013.
23. Ivessa AS, Lenzmeier BA, Bessler JB, Goudsouzian LK, Schnakenberg SL, et al. (2003) The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell 12: 1525-1536.
24. Khakhar RR, Cobb JA, Bjergbaek L, Hickson ID, Gasser SM, (2003) RecQ helicases: multiple roles in genome maintenance. Trends Cell Biol 13: 493-501.
25. Lambert S, Mizuno K, Blaisonneau J, Martineau S, Chanet R, et al. (2010) Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol Cell 39: 346-359.
26. Lambert S, Watson A, Sheedy DM, Martin B, Carr AM, (2005) Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 121: 689-702.
27. Labib K, Hodgson B, (2007) Replication fork barriers: pausing for a break or stalling for time? EMBO Rep 8: 346-353.
28. Gonzalez-Prieto R, Munoz-Cabello AM, Cabello-Lobato MJ, Prado F, (2013) Rad51 replication fork recruitment is required for DNA damage tolerance. Embo J 32: 1307-1321.
29. Irmisch A, Ampatzidou E, Mizuno K, O'Connell MJ, Murray JM, (2009) Smc5/6 maintains stalled replication forks in a recombination-competent conformation. Embo J 28: 144-155.
30. Perpelescu M, Fukagawa T, (2011) The ABCs of CENPs. Chromosoma 120: 425-446.
31. Bhattacharjee S, Osman F, Feeney L, Lorenz A, Bryer C, et al. (2013) MHF1-2/CENP-S-X performs distinct roles in centromere metabolism and genetic recombination. Open Biol 3: 130102.
32. Nakamura K, Okamoto A, Katou Y, Yadani C, Shitanda T, et al. (2008) Rad51 suppresses gross chromosomal rearrangement at centromere in Schizosaccharomyces pombe. Embo J 27: 3036-3046.
33. 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.
34. Roy B, Sanyal K, (2011) Diversity in requirement of genetic and epigenetic factors for centromere function in fungi. Eukaryot Cell 10: 1384-1395.
35. 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.
36. 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.
37. Mishra PK, Baum M, Carbon J, (2007) Centromere size and position in Candida albicans are evolutionarily conserved independent of DNA sequence heterogeneity. Mol Genet Genomics 278: 455-465.
38. Thakur J, Sanyal K, (2013) Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in Candida albicans. Genome Res 23: 638-652.
39. 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.
40. Hicks WM, Kim M, Haber JE, (2010) Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329: 82-85.
41. Lopes M, Cotta-Ramusino C, Pellicioli A, Liberi G, Plevani P, et al. (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561.
42. Fachinetti D, Bermejo R, Cocito A, Minardi S, Katou Y, et al. (2010) Replication termination at eukaryotic chromosomes is mediated by Top2 and occurs at genomic loci containing pausing elements. Mol Cell 39: 595-605.
43. Wang Y, Vujcic M, Kowalski D, (2001) DNA replication forks pause at silent origins near the HML locus in budding yeast. Mol Cell Biol 21: 4938-4948.
44. Thakur J, Sanyal K, (2012) A coordinated interdependent protein circuitry stabilizes the kinetochore ensemble to protect CENP-A in the human pathogenic yeast Candida albicans. PLoS Genet 8: e1002661.
45. Andaluz E, Ciudad T, Gomez-Raja J, Calderone R, Larriba G, (2006) Rad52 depletion in Candida albicans triggers both the DNA-damage checkpoint and filamentation accompanied by but independent of expression of hypha-specific genes. Mol Microbiol 59: 1452-1472.
46. Garcia-Prieto F, Gomez-Raja J, Andaluz E, Calderone R, Larriba G, (2011) Role of the homologous recombination genes RAD51 and RAD59 in the resistance of Candida albicans to UV light, radiomimetic and anti-tumor compounds and oxidizing agents. Fungal Genet Biol 47: 433-445.
47. Andaluz E, Bellido A, Gomez-Raja J, Selmecki A, Bouchonville K, et al. (2011) Rad52 function prevents chromosome loss and truncation in Candida albicans. Mol Microbiol 79: 1462-1482.
48. 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.
49. 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.
50. 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 80: 14-32.
51. Zeitlin SG, Baker NM, Chapados BR, Soutoglou E, Wang JY, et al. (2009) Double-strand DNA breaks recruit the centromeric histone CENP-A. Proc Natl Acad Sci U S A 106: 15762-15767.
52. Zeitlin SG, Patel S, Kavli B, Slupphaug G, (2005) Xenopus CENP-A assembly into chromatin requires base excision repair proteins. DNA Repair (Amst) 4: 760-772.
53. Fisher JK, Bourniquel A, Witz G, Weiner B, Prentiss M, et al. (2013) Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells. Cell 153: 882-895.
54. Shang WH, Hori T, Martins NM, Toyoda A, Misu S, et al. (2013) Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 24: 635-648.
55. Scott KC, (2014) Neocentromeres: a place for everything and everything in its place. Trends in Genetics 30: 66-74.
56. Catania S, (2014) Anarchic centromeres: deciphering order from apparent chaos. Current Opinion in Cell Biology 26: 41-50.
57. 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.
58. Osman F, Whitby MC, (2013) Emerging roles for centromere-associated proteins in DNA repair and genetic recombination. Biochem Soc Trans 41: 1726-1730.
59. Li PC, Petreaca RC, Jensen A, Yuan JP, Green MD, et al. (2013) Replication fork stability is essential for the maintenance of centromere integrity in the absence of heterochromatin. Cell Rep 3: 638-645.
60. 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.
61. Sanchez-Pulido L, Pidoux AL, Ponting CP, Allshire RC, (2009) Common ancestry of the CENP-A chaperones Scm3 and HJURP. Cell 137: 1173-1174.
62. Matsumoto S, Ogino K, Noguchi E, Russell P, Masai H, (2005) Hsk1-Dfp1/Him1, the Cdc7-Dbf4 kinase in Schizosaccharomyces pombe, associates with Swi1, a component of the replication fork protection complex. J Biol Chem 280: 42536-42542.
63. Noguchi E, Noguchi C, McDonald WH, Yates JR 3rd, Russell P, (2004) Swi1 and Swi3 are components of a replication fork protection complex in fission yeast. Mol Cell Biol 24: 8342-8355.
64. 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.
65. Wilson RB, Davis D, Mitchell AP, (1999) Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J Bacteriol 181: 1868-1874.
66. Murad AM, Lee PR, Broadbent ID, Barelle CJ, Brown AJ, (2000) CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16: 325-327.
67. Gomez-Raja J, Davis DA, (2012) The beta-arrestin-like protein Rim8 is hyperphosphorylated and complexes with Rim21 and Rim101 to promote adaptation to neutral-alkaline pH. Eukaryot Cell 11: 683-693.
68. Dubey DD, Davis LR, Greenfeder SA, Ong LY, Zhu JG, et al. (1991) Evidence suggesting that the ARS elements associated with silencers of the yeast mating-type locus HML do not function as chromosomal DNA replication origins. Mol Cell Biol 11: 5346-5355.
69. Kurtz MB, Cortelyou MW, Miller SM, Lai M, Kirsch DR, (1987) Development of autonomously replicating plasmids for Candida albicans. Mol Cell Biol 7: 209-217.
70. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
71. Tamura K, Nei M, Kumar S, (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101: 11030-11035.
72. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
73. Takayama Y, Mamnun YM, Trickey M, Dhut S, Masuda F, et al. (2010) Hsk1- and SCF(Pof3)-dependent proteolysis of S. pombe Ams2 ensures histone homeostasis and centromere function. Dev Cell 18: 385-396.