Cohesin without cohesion: A novel role for Pds5 in Saccharomyces cerevisiae

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Tong, Kevin ^a   Skibbens, Robert V ^a  

^a LEHIGH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; DNA; PEPTIDES AND PROTEINS; PROTEIN PDS5; PROTEIN RAD61; PROTEIN SMC3; PROTEIN WAPL; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; FUNGAL DNA; NONHISTONE PROTEIN; PDS5 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ACETYLATION; ALLELE; ARTICLE; BINDING SITE; CELL ADHESION; CELL CYCLE S PHASE; CELL MUTANT; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONTROLLED STUDY; DEACETYLATION; DISSOCIATION; MITOSIS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID; CELL SURVIVAL; CYTOLOGY; GENETICS; METABOLISM; MUTATION; PROTEIN TRANSPORT;

ACETYLATION; ALLELES; CELL CYCLE PROTEINS; CELL SURVIVAL; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA, FUNGAL; MITOSIS; MUTATION; PROTEIN TRANSPORT; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84903519283     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100470     Document Type: Article

References (73)

1. Rudra S, Skibbens RV (2013) Cohesin codes - interpreting chromatin architecture and the many facets of cohesin function. J Cell Sci 126: 31-41.
2. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, et al. (2000) Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5: 243-254. (Pubitemid 30628083)
3. Tonkin ET, Wang TJ, Lisgo S, Bamshad MJ, Strachan T (2004) NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat Genet 36: 636-641. (Pubitemid 38715993)
4. Braunholz D, Hullings M, Gil-Rodriguez MC, Fincher CT, Mallozzi MB, et al. (2012) Isolated NIBPL missense mutations that cause Cornelia de Lange syndrome alter MAU2 interaction. Eur J Hum Genet 20: 271-276.
5. Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, et al. (2004) Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol 2: E259.
6. Laloraya S, Guacci V, Koshland D (2000) Chromosomal addresses of the cohesin component Mcd1p. J Cell Biol 151: 1047-1056.
7. Rudra S, Skibbens RV (2012) Sister chromatid cohesion establishment occurs in concert with lagging strand synthesis. Cell Cycle 11: 2114-2121.
8. Rudra S, Skibbens RV (2013) Chl1 DNA Helicase Regulates Scc2 Deposition Specifically during DNA Replication in Saccharomyces cerevisiae. PLoS One 8: e75435.
9. Bellows AM, Kenna MA, Cassimeris L, Skibbens RV (2003) Human EFO1p exhibits acetyltransferase activity and is a unique combination of linker histone and Ctf7p/Eco1p chromatid cohesion establishment domains. Nucleic Acids Res 31: 6334-6343. (Pubitemid 37442361)
10. Milutinovich M, Unal E, Ward C, Skibbens RV, Koshland D (2007) A multi-step pathway for the establishment of sister chromatid cohesion. PLoS Genet 3: e12.
11. Rolef Ben-Shahar T, Heeger S, Lehane C, East P, Flynn H, et al. (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321: 563-566.
12. Skibbens RV, Corson LB, Koshland D, Hieter P (1999) Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev 13: 307-319. (Pubitemid 29095802)
13. Toth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A, et al. (1999) Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev 13: 320-333. (Pubitemid 29095803)
14. Unal E, Heidinger-Pauli JM, Kim W, Guacci V, Onn I, et al. (2008) A molecular determinant for the establishment of sister chromatid cohesion. Science 321: 566-569.
15. Vega H, Waisfisz Q, Gordillo M, Sakai N, Yanagihara I, et al. (2005) Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat Genet 37: 468-470. (Pubitemid 40617273)
16. Zhang J, Shi X, Li Y, Kim BJ, Jia J, et al. (2008) Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol Cell 31: 143-151. (Pubitemid 351905926)
17. Skibbens RV (2005) Unzipped and loaded: the role of DNA helicases and RFC clamp-loading complexes in sister chromatid cohesion. J Cell Biol 169: 841-846.
18. Sharma U, Stefanova D, Holmes SG (2013) Histone variant H2A.Z functions in sister chromatid cohesion in Saccharomyces cerevisiae. Mol Cell Biol 33: 3473-3481.
19. Skibbens RV (2000) Holding your own: establishing sister chromatid cohesion. Genome Research 10: 1664-1671.
20. Gandhi R, Gillespie PJ, Hirano T (2006) Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Curr Biol 16: 2406-2417. (Pubitemid 44894912)
21. Gause M, Misulovin Z, Bilyeu A, Dorsett D (2010) Dosage-sensitive regulation of cohesin chromosome binding and dynamics by Nipped-B, Pds5, and Wapl. Mol Cell Biol 30: 4940-4951.
22. Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, et al. (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127: 955-967. (Pubitemid 44792249)
23. Lopez-Serra L, Lengronne A, Borges V, Kelly G, Uhlmann F (2013) Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Curr Biol 23: 64-69.
24. Rowland BD, Roig MB, Nishino T, Kurze A, Uluocak P, et al. (2009) Building sister chromatid cohesion: Smc3 acetylation counteracts an antiestablishment activity. Mol Cell 33: 763-774.
25. Sutani T, Kawaguchi T, Kanno R, Itoh T, Shirahige K (2009) Budding yeast Wpl1(Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr Biol 19: 492-497.
26. Guacci V, Koshland D (2012) Cohesin-independent segregation of sister chromatids in budding yeast. Mol Biol Cell 23: 729-739.
27. Beckouet F, Hu B, Roig MB, Sutani T, Komata M, et al. (2010) An Smc3 acetylation cycle is essential for establishment of sister chromatid cohesion. Mol Cell 39: 689-699.
28. Borges V, Lehane C, Lopez-Serra L, Flynn H, Skehel M, et al. (2010) Hos1 deacetylates Smc3 to close the cohesin acetylation cycle. Mol Cell 39: 677-688.
29. Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, et al. (2012) HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature 489: 313-317.
30. Xiong B, Lu S, Gerton JL (2010) Hos1 is a lysine deacetylase for the Smc3 subunit of cohesin. Curr Biol 20: 1660-1665.
31. Hartman T, Stead K, Koshland D, Guacci V (2000) Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae. J Cell Biol 151: 613-626.
32. Panizza S, Tanaka T, Hochwagen A, Eisenhaber F, Nasmyth K (2000) Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr Biol 10: 1557-1564. (Pubitemid 32062656)
33. Stead K, Aguilar C, Hartman T, Drexel M, Meluh P, et al. (2003) Pds5p regulates the maintenance of sister chromatid cohesion and is sumoylated to promote the dissolution of cohesion. J Cell Biol 163: 729-741. (Pubitemid 37517881)
34. Kulemzina I, Schumacher MR, Verma V, Reiter J, Metzler J, et al. (2012) Cohesin rings devoid of Scc3 and Pds5 maintain their stable association with the DNA. PLoS Genet 8: e1002856.
35. Guacci V, Koshland D, Strunnikov A (1997) A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91: 47-57 (Pubitemid 27431312)
36. Chan KL, Gligoris T, Upcher W, Kato Y, Shirahige K, et al. (2013) Pds5 promotes and protects cohesin acetylation. Proc Natl Acad Sci U S A 110: 13020-13025.
37. Noble D, Kenna MA, Dix M, Skibbens RV, Unal E, et al. (2006) Intersection between the regulators of sister chromatid cohesion establishment and maintenance in budding yeast indicates a multi-step mechanism. Cell Cycle 5: 2528-2536. (Pubitemid 44785832)
38. Vaur S, Feytout A, Vazquez S, Javerzat JP (2012) Pds5 promotes cohesin acetylation and stable cohesin-chromosome interaction. EMBO Rep 13: 645-652.
39. Denes V, Pilichowska M, Makarovskiy A, Carpinito G, Geck P (2010) Loss of a cohesin-linked suppressor APRIN (Pds5b) disrupts stem cell programs in embryonal carcinoma: an emerging cohesin role in tumor suppression. Oncogene 29: 3446-3452.
40. Zhang B, Chang J, Fu M, Huang J, Kashyap R, et al. (2009) Dosage effects of cohesin regulatory factor PDS5 on mammalian development: implications for cohesinopathies. PLoS One 4: e5232.
41. Zhang B, Jain S, Song H, Fu M, Heuckeroth RO, et al. (2007) Mice lacking sister chromatid cohesion protein PDS5B exhibit developmental abnormalities reminiscent of Cornelia de Lange syndrome. Development 134: 3191-3201. (Pubitemid 47506157)
42. Maffini M, Denes V, Sonnenschein C, Soto A, Geck P (2008) APRIN is a unique Pds5 paralog with features of a chromatin regulator in hormonal differentiation. J Steroid Biochem Mol Biol 108: 32-43. (Pubitemid 351173821)
43. Mayer ML, Gygi SP, Aebersold R, Hieter P (2001) Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol Cell 7: 959-970. (Pubitemid 32525743)
44. Antoniacci LM, Skibbens RV (2006) Sister-chromatid telomere cohesion is nonredundant and resists both spindle forces and telomere motility. Curr Biol 16: 902-906.
45. Cohen-Fix O, Peters JM, Kirschner MW, Koshland D (1996) Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev 10: 3081-3093. (Pubitemid 27020537)
46. Lyons NA, Morgan DO (2011) Cdk1-dependent destruction of Eco1 prevents cohesion establishment after S phase. Mol Cell 42: 378-389.
47. Heidinger-Pauli JM, Unal E, Koshland D (2009) Distinct targets of the Eco1 acetyltransferase modulate cohesion in S phase and in response to DNA damage. Mol Cell 34: 311-321.
48. Lyons NA, Fonslow BR, Diedrich JK, Yates JR, 3rd, Morgan DO (2013) Sequential primed kinases create a damage-responsive phosphodegron on Eco1. Nat Struct Mol Biol 20: 194-201.
49. Unal E, Heidinger-Pauli JM, Koshland D (2007) DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317: 245-248. (Pubitemid 47076200)
50. Machin F, Torres-Rosell J, Jarmuz A, Aragon L (2005) Spindle-independent condensation-mediated segregation of yeast ribosomal DNA in late anaphase. J Cell Biol 168: 209-219. (Pubitemid 40248219)
51. Tanaka K, Hao Z, Kai M, Okayama H (2001) Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO 20: 5779-5790. (Pubitemid 33010053)
52. Skibbens RV, Maradeo M, Eastman L (2007) Fork it over: the cohesion establishment factor Ctf7p and DNA replication. J Cell Sci 120: 2471-2477. (Pubitemid 47323856)
53. Losada A, Yokochi T, Hirano T (2005) Functional contribution of Pds5 to cohesin-mediated cohesion in human cells and Xenopus egg extracts. J Cell Sci 118: 2133-2141. (Pubitemid 40872836)
54. Shintomi K, Hirano T (2009) Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes Dev 23: 2224-2236.
55. Wang SW, Read RL, Norbury CJ (2002) Fission yeast Pds5 is required for accurate chromosome segregation and for survival after DNA damage or metaphase arrest. J Cell Sci 115: 587-598. (Pubitemid 34182985)
56. Zhang N, Jiang Y, Mao Q, Demeler B, Tao YJ, et al. (2013) Characterization of the interaction between the cohesin subunits Rad21 and SA1/2. PLoS One 8: e69458.
57. Schiller CB, Lammens K, Guerini I, Coordes B, Feldmann H, et al. (2012) Structure of Mre11-Nbs1 complex yields insights into Ataxia-Telangiectasia-like disease mutations and DNA damage signaling. Nat Struct Mol Biol 19: 693-700.
58. Mockel C, Lammens K, Schele A, Hopfner KP (2012) ATP driven structural changes of the bacterial Mre11:Rad50 catalytic head complex. Nucleic Acids Res 40: 914-927.
59. Chang CR, Wu CS, Hom Y, Gartenberg MR (2005) Targeting of cohesin by transcriptionally silent chromatin. Genes Dev 19: 3031-3042. (Pubitemid 41798118)
60. Nasmyth K, Haering CH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43: 525-558.
61. Lengronne A, McIntyre J, Katou Y, Kanoh Y, Hopfner KP, et al. (2006) Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol Cell 23: 787-799. (Pubitemid 44344523)
62. Kogut I, Wang J, Guacci V, Mistry RK, Megee PC (2009) The Scc2/Scc4 cohesin loader determines the distribution of cohesin on budding yeast chromosomes. Genes Dev 23: 2345-2357.
63. Misulovin Z, Schwartz YB, Li XY, Kahn TG, Gause M, et al. (2008) Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome. Chromosoma 117: 89-102.
64. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, et al. (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132: 422-433.
65. Dorsett D (2011) Cohesin: genomic insights into controlling gene transcription and development. Curr Opin Genet Dev 21: 199-206.
66. Gartenberg M (2009) Heterochromatin and the cohesion of sister chromatids. Chromosome Res 17: 229-238.
67. D'Ambrosio LM, Lavoie BD (2014) Pds5 prevents the PolySUMO-dependent separation of sister chromatids. Curr Biol 24: 1-11.
68. Zhang Z, Ren Q, Yang H, Conrad MN, Guacci V, Kateveva A, Dresser ME (2005) Budding yeast PDS5 plays an important role in meiosis and is required for sister chromatid cohesion. Mol Microbiol 56: 670-680. (Pubitemid 40562361)
69. Maradeo ME, Skibbens RV (2009) The Elg1-RFC clamp-loading complex performs a role in sister chromatid cohesion. PLoS One 4: e4707.
70. 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. (Pubitemid 28328001)
71. Maradeo ME, Skibbens RV (2010) Replication factor C complexes play unique pro- and anti-establishment roles in sister chromatid cohesion. PLoS One 5: e15381.
72. Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, Koshland D (2004) DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 16: 991-1002. (Pubitemid 40018408)
73. Pfaffl MW (2001) A new mathematical model for relative quanitfication in real-time RT-PCR. Nucleic Acids Res 1: e45.