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Roles of the sister chromatid cohesion apparatus in gene expression, development, and human syndromes

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Abstract

The sister chromatid cohesion apparatus mediates physical pairing of duplicated chromosomes. This pairing is essential for appropriate distribution of chromosomes into the daughter cells upon cell division. Recent evidence shows that the cohesion apparatus, which is a significant structural component of chromosomes during interphase, also affects gene expression and development. The Cornelia de Lange (CdLS) and Roberts/SC phocomelia (RBS/SC) genetic syndromes in humans are caused by mutations affecting components of the cohesion apparatus. Studies in Drosophila suggest that effects on gene expression are most likely responsible for developmental alterations in CdLS. Effects on chromatid cohesion are apparent in RBS/SC syndrome, but data from yeast and Drosophila point to the likelihood that changes in expression of genes located in heterochromatin could contribute to the developmental deficits.

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References

  • Anderson DE, Losada A, Erickson HP, Hirano T (2002) Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol 156:419–424

    PubMed  CAS  Google Scholar 

  • Arumugam P, Gruber S, Tanaka K, Haering CH, Mechtler K, Nasmyth K (2003) ATP hydrolysis is required for cohesin’s association with chromosomes. Curr Biol 13:1941–1953

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542

    PubMed  CAS  Google Scholar 

  • Bénard CY, Kébir H, Takagi S, Hekimi S (2004) mau-2 acts cell-autonomously to guide axonal migrations in Caenorhabditis elegans. Development 131:5947–5958

    PubMed  Google Scholar 

  • Bhuiyan Z, Klein M, Hammond P, Mannens MM, Van Haeringen A, Van Berckelaer-Onnes I, Hennekam RC (2005) Genotype-Phenotype correlations of 39 patients with Cornelia de Lange syndrome: the Dutch experience. J Med Genet (online publication), Oct 19

  • Blat Y, Kleckner N (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98:249–259

    PubMed  CAS  Google Scholar 

  • Borck G, Redon R, Sanlaville D, Rio M, Prieur M, Lyonnet S, Vekemans M, Carter NP, Munnich A, Colleaux L, Cormier-Daire V (2004) NIPBL mutations and genetic heterogeneity in Cornelia de Lange syndrome. J Med Genet 41:e128

    PubMed  CAS  Google Scholar 

  • Brands A, Skibbens RV (2005) Ctf7/Eco1p exhibits acetyltransferase activity—but does it matter? Curr Biol 15:R50–R51

    PubMed  CAS  Google Scholar 

  • Brown CJ, Miller AP, Carrel L, Rupert JL, Davies KE, Williard HF (1995) The DXS423E gene in Xp 11.21 escapes X chromosome inactivation. Hum Mol Genet 4:251–255

    PubMed  CAS  Google Scholar 

  • Chang CR, Wu CS, Hom Y, Gartenberg MR (2005) Targeting of cohesin by transcriptionally silent chromatin. Genes Dev 19:3031–3042

    PubMed  CAS  Google Scholar 

  • Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, Nasmyth K (2000) Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5:243–254

    PubMed  CAS  Google Scholar 

  • de Lange C (1933) Sur un type nouveau de dégénération (typus Amstelodamensis). Arch Méd Enfants 36:713–719

    Google Scholar 

  • Dimitri P, Corradini N, Rossi F, Verni F (2005) The paradox of functional heterochromatin. Bioessays 27:29–41

    PubMed  CAS  Google Scholar 

  • Donze D, Adams CR, Rine J, Kamakaka RT (1999) The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev 13:698–708

    PubMed  CAS  Google Scholar 

  • Dorsett D (1999) Distant liaisons: long range enhancer–promoter interactions in Drosophila. Curr Opin Genet Dev 9:505–514

    PubMed  CAS  Google Scholar 

  • Dorsett D (2004) Adherin: key to the cohesin ring and Cornelia de Lange syndrome. Curr Biol 14:R834–R836

    PubMed  CAS  Google Scholar 

  • Dorsett D, Eissenberg JC, Misulovin Z, Martens A, Redding B, McKim K (2005) Effects of sister chromatid cohesion proteins on cut gene expression during wing development in Drosophila. 132:4743–4753

  • Freeman MV, Williams DW, Schimke RN, Temtamy SA, Vachier E, German J (1974) The Roberts syndrome. Clin Genet 5:1–16

    Article  PubMed  CAS  Google Scholar 

  • Furuya K, Takahashi K, Yanagida M (1998) Faithful anaphase is ensured by Mis4, a sister chromatid cohesion molecule required in S phase and not destroyed in G1 phase. Genes Dev 12:3408–3418

    PubMed  CAS  Google Scholar 

  • Gause M, Morcillo P, Dorsett D (2001) Insulation of enhancer–promoter communication by a gypsy transposon insert in the Drosophila cut gene: cooperation between suppressor of hairy-wing and modifier of mdg4 proteins. Mol Cell Biol 21:4807–4817

    PubMed  CAS  Google Scholar 

  • German J (1979) Roberts’ syndrome. I. Cytological evidence for a disturbance in chromatid pairing. Clin Genet 16:441–447

    Article  PubMed  CAS  Google Scholar 

  • Gillespie PJ, Hirano T (2004) Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr Biol 14:1598–1603

    PubMed  CAS  Google Scholar 

  • Gillis LA, McCallum J, Kaur M, DeScipio C, Yaeger D, Mariani A, Kline A, Li H, Devoto M, Jackson LG, Krantz ID (2004) NIPBL mutational analysis in 120 individuals with Cornelia de Lange syndrome and evalutation of genotype–phenotype analysis in CdLS. Am J Hum Genet 75:610–623

    PubMed  CAS  Google Scholar 

  • Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, Li Y, Hao YL, Ooi CE, Godwin B, Vitols E, Vijayadamodar G, Pochart P, Machineni H, Welsh M, Kong Y, Zerhusen B, Malcolm R, Varrone Z, Collis A, Minto M, Burgess S, McDaniel L, Stimpson E, Spriggs F, Williams J, Neurath K, Ioime N, Agee M, Voss E, Furtak K, Renzulli R, Aanensen N, Carrolla S, Bickelhaupt E, Lazovatsky Y, DaSilva A, Zhong J, Stanyon CA, Finley RL Jr, White KP, Braverman M, Jarvie T, Gold S, Leach M, Knight J, Shimkets RA, McKenna MP, Chant J, Rothberg JM (2003) A protein interaction map of Drosophila melanogaster. Science 302:1727–1736

    PubMed  CAS  Google Scholar 

  • Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, Koshland DE, DeRisi JL, Gerton JL (2004) Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol 2:E259

    PubMed  Google Scholar 

  • Haering CH, Lowe J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9:773–788

    PubMed  CAS  Google Scholar 

  • Hagstrom KA, Meyer BJ (2003) Condensin and cohesin: more than chromosome compactor and glue. Nat Rev Genet 4:520–534

    PubMed  CAS  Google Scholar 

  • Haldar D, Kamakaka RT (2006) tRNA genes as chromatin barriers. Nat Struct Mol Biol 13:192–193

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hauf S, Waizenegger IC, Peters JM (2001) Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293:1320–1323

    PubMed  CAS  Google Scholar 

  • Herrmann J, Opitz JM (1977) The SC phocomelia and the Roberts syndrome: nosologic aspects. Eur J Pediatr 125:117–134

    PubMed  CAS  Google Scholar 

  • Herrmann J, Feingold M, Tuffli GA, Opitz, JM (1969) A familial dysmorphogenetic syndrome of limb deformities, characteristic facial appearance and associated anomalies: the ‘pseudothalidomide’ or ‘SC-syndrome’. Birth Defects Orig Artic Ser V(3): 81–89

    Google Scholar 

  • Hirano T (2005) SMC proteins and chromosome mechanics: from bacteria to humans. Philos Trans R Soc Lond B Biol Sci 360:507–514

    PubMed  CAS  Google Scholar 

  • Hirano M, Hirano T (2002) Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J 21:5733–5744

    PubMed  CAS  Google Scholar 

  • Hirano M, Hirano T (2006) Opening closed arms: long-distance activation of SMC ATPase by hinge–DNA interactions. Mol Cell 21:175–186

    PubMed  CAS  Google Scholar 

  • Hou F, Zou H (2005) Two human orthologs of Eco1/Ctf7 acetyltransferases are both required for proper sister-chromatid cohesion. Mol Biol Cell 16:3908–3918

    PubMed  CAS  Google Scholar 

  • Huang CE, Milutinovich M, Koshland D (2005) Rings, bracelet or snaps: fashionable alternatives for Smc complexes. Philos Trans R Soc Lond B Biol Sci 360:537–542

    PubMed  CAS  Google Scholar 

  • Hulinsky R, Winesette H, Dent KM, Silver R, King J, Lowichik A, Chen Z, Viskochil DH (2003) Prenatal diagnosis dilemma: fetus with del(5)(p13.1p14.2) diagnosed postnatally with Cornelia de Lange syndrome. Am J Hum Genet 73:602 (Suppl)

    Google Scholar 

  • Ireland M, Donnai D, Burn J (1993) Brachmann–de Lange syndrome. Delineation of the clinical phenotype. Am J Med Genet 47:959–963

    PubMed  CAS  Google Scholar 

  • Ivanov D, Nasmyth K (2005) A topological interaction between cohesin rings and a circular minichromosome. Cell 122:849–860

    PubMed  CAS  Google Scholar 

  • Ivanov D, Schleiffer A, Eisenhaber F, Mechtler K, Haering CH, Nasmyth K (2002) Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr Biol 12:323–328

    PubMed  CAS  Google Scholar 

  • Jabs EW, Tuck-Muller CM, Cusano R, Rattner JB (1991) Studies of mitotic and centromeric abnormalities in Roberts syndrome: implications for a defect in the mitotic mechanisms. Chromosoma 100:251–261

    PubMed  CAS  Google Scholar 

  • Jackson L, Kline AD, Barr MA, Koch S (1993) de Lange syndrome: a clinical review of 310 individuals. Am J Med Genet 47:940–946

    PubMed  CAS  Google Scholar 

  • Judge C (1973) A sibship with the pseudothalidomide syndrome and an association with Rh incompatibility. Med J Aust 2:280–281

    PubMed  CAS  Google Scholar 

  • Kaur M, DeScipio C, McCallum J, Yaeger D, Devoto M, Jackson LG, Spinner NB, Krantz ID (2005) Precocious sister chromatid separation (PSCS) in Cornelia de Lange syndrome. Am J Med Genet A 138:27–31

    PubMed  Google Scholar 

  • Kenna MA, Skibbens RV (2003) Mechanical link between cohesion establishment and DNA replication: Ctf7p/Eco1p, a cohesion establishment factor, associates with three different replication factor C complexes. Mol Cell Biol 23:2999–3007

    PubMed  CAS  Google Scholar 

  • Kobayashi T, Ganley AR (2005) Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309:1581–1584

    PubMed  CAS  Google Scholar 

  • Kobayashi T, Horiuchi T, Tongaonkar P, Vu L, Nomura M (2004) SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell 117:441–453

    PubMed  CAS  Google Scholar 

  • Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, Yaeger D, Jukovsky L, Wassarman N, Bottani A, Morris CA, Nowaczyk MJM, Toriello H, Bamshad MJ, Carey JC, Rappaport E, Kawauchi S, Lander AD, Calof AL, Li H, Devoto M, Jackson LG (2004) Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of the Drosophila Nipped-B gene. Nat Genet 36:631–635

    PubMed  CAS  Google Scholar 

  • Laloraya S, Guacci V, Koshland D (2000) Chromosomal addresses of the cohesin component Mcd1p. J Cell Biol. 151:1047–1056

    PubMed  CAS  Google Scholar 

  • Lau A, Blitzbau H, Bell SP (2002) Cell-cycle control of the estabilishment of mating-type silencing in S. cerevisiae. Genes Dev 16:2935–2945

    PubMed  CAS  Google Scholar 

  • Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F (2004) Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430:573–578

    PubMed  CAS  Google Scholar 

  • Losada A, Hirano T (2005) Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev 19:1269–1287

    PubMed  CAS  Google Scholar 

  • Losada A, Hirano M, Hirano T (1998) Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev 12:1986–1997

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Louie E, German J (1981) Roberts’s syndrome. II. Aberrant Y-chromosome behavior. Clin Genet 19:71–74

    Article  PubMed  CAS  Google Scholar 

  • McDaniel LD, Prueitt R, Probst LC, Wilson KS, Tomkins D, Wilson GN, Schultz RA (2000) Novel assay for Roberts syndrome assigns variable phenotypes to one complementation group. Am J Med Genet 93:223–229

    PubMed  CAS  Google Scholar 

  • McDaniel LD, Tomkins DJ, Stanbridge EJ, Somerville MJ, Friedberg EC, Schultz RA (2005) Mapping of a single locus capable of complementing the defective heterochromatin phenotype of Roberts syndrome cells. Am J Hum Genet 77:132–139

    PubMed  CAS  Google Scholar 

  • McGuinness BE, Hirota T, Kudo NR, Peters JM, Nasmyth K (2005) Shugoshin prevents dissociation of cohesin from centromeres during mitosis in vertebrate cells. PLoS Biol 3:e86

    PubMed  Google Scholar 

  • Megee PC, Mistrot C, Guacci V, Koshland D (1999) The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences. Mol Cell 4:445–450

    PubMed  CAS  Google Scholar 

  • Michaelis C, Ciosk R, Nasmyth K (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91:35–45

    PubMed  CAS  Google Scholar 

  • Milutinovich M, Koshland DE (2003) Molecular biology. SMC complexes—wrapped up in controversy. Science 300:1101–1102

    PubMed  CAS  Google Scholar 

  • Miyake N, Visser R, Kinoshita A, Yoshiura K, Niikawa N, Kondoh T, Matsumoto N, Harada N, Okamoto N, Sonoda T, Naritomi K, Kaname T, Chinen Y, Tonoki H, Kurosawa K (2005) Four novel NIPBL mutations in Japanese patients with Cornelia de Lange syndrome. Am J Med Genet A 135:103–105

    PubMed  Google Scholar 

  • Morcillo P, Rosen C, Dorsett D (1996) Genes regulating the remote wing margin enhancer in the Drosophila cut locus. Genetics 144:1143–1154

    PubMed  CAS  Google Scholar 

  • Musio A, Selicorni A, Focarelli ML, Gervasini C, Milani D, Russo S, Vezzoni P, Larizza L (2006) X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Genet 38(5):528–530

    PubMed  CAS  Google Scholar 

  • Nasmyth K (2005) How might cohesin hold sister chromatids together? Philos Trans R Soc Lond B Biol Sci 360:483–496

    PubMed  CAS  Google Scholar 

  • Nasmyth K, Haering CH (2005) The structure and function of SMC and kleisin complexes. Ann Rev Biochem 74:595–648

    PubMed  CAS  Google Scholar 

  • Neuwald AF, Hirano T (2000) HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions. Genome Res 10:1445–1452

    PubMed  CAS  Google Scholar 

  • Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, Grewal SI, Watanabe Y (2002) Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 4:89–93

    PubMed  CAS  Google Scholar 

  • Opitz JM (1985) The Brachmann–de Lange syndrome. Am J Med Genet 22:89–102

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Partridge JF, Scott KS, Bannister AJ, Kouzarides T, Allshire RC (2002) cis-acting DNA from fission yeast centromeres mediates histone H3 methylation and recruitment of silencing factors and cohesin to an ectopic site. Curr Biol 12:1652–1660

    PubMed  CAS  Google Scholar 

  • Roberts JB (1919) A child with double cleft of lip and palate, protrusion of the intermaxillary portion of the upper jaw and imperfect development of the bones of the four extremities. Ann Surg 70:252–254

    Google Scholar 

  • Rollins RA, Morcillo P, Dorsett D (1999) Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 152:577–593

    PubMed  CAS  Google Scholar 

  • Rollins RA, Korom M, Aulner N, Martens A, Dorsett D (2004) Drosophila Nipped-B protein supports sister chromatid cohesion and opposes the Stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Mol Cell Biol 24:3100–3111

    PubMed  CAS  Google Scholar 

  • Romke C, Froster-Iskenius U, Heyne K, Hohn W, Hof M, Grzejszczyk G, Rauskolb R, Rehder H, Schwinger E (1987) Roberts syndrome and SC phocomelia: a single genetic entity. Clin Genet 31:170–177

    Article  PubMed  CAS  Google Scholar 

  • Sakai A, Hizume K, Sutani T, Takeyasu K, Yanagida M (2003) Condensin but not cohesin SMC heterodimer induces DNA reannealing through protein–protein assembly. EMBO J 22:2764–2775

    PubMed  CAS  Google Scholar 

  • Salic A, Waters JC, Mitchison TJ (2004) Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis. Cell 118:567-578

    PubMed  CAS  Google Scholar 

  • Schüle B, Oviedo A, Johnston K, Pai S, Francke U (2005). Inactivating mutations in ESCO2 cause SC phocomelia and Roberts syndrome: no phenotype-genotype correlation. Am J Hum Genet 77:1117–1128

    PubMed  Google Scholar 

  • Seitan VC, Banks P, Laval S, Majid NA, Dorsett D, Rana A, Smith J, Bateman A, Krpic S, Hostert A, Rollins RA, Erdjument-Bromage H, Tempst P, Benard CY, Hekimi S, Newbury SF, Strachan T (2006) Metazoan Scc4 homologues link sister chromatid cohesion to cell and axon migration. PLOS Biol (in press)

  • Selicorni A, Sforzini C, Milani D, Cagnoli G, Fossali E, Bianchetti MG (2005) Anomalies of the kidney and urinary tract are common in de Lange syndrome. Am J Med Genet A132(4):395–397

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Spitz F, Gonzalez F, Duboule D (2003) A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 113:405–417

    PubMed  CAS  Google Scholar 

  • Stead K, Aguilar C, Hartman T, Drexel M, Meluh P, Guacci V (2003) Pds5p regulates the maintenance of sister chromatid cohesion and is sumoylated to promote the dissolution of cohesion. J Cell Biol 163:729–741

    PubMed  CAS  Google Scholar 

  • Strachan T (2005) Cornelia de Lange Syndrome and the link between chromosomal function, DNA repair and developmental gene regulation. Curr Opin Genet Dev 15:258–264

    PubMed  CAS  Google Scholar 

  • Sumara I, Vorlaufer E, Gieffers C, Peters, BH, Peters JM (2000) Characterization of vertebrate cohesin complexes and their regulation in prophase. J Cell Biol 151:749–762

    PubMed  CAS  Google Scholar 

  • Suter B, Tong A, Chang M, Yu L, Brown GW, Boone C, Rine J (2004) The origin recognition complex links replication, sister chromatid cohesion and transcriptional silencing in Saccharomyces cerevisiae. Genetics 167:579–591

    PubMed  CAS  Google Scholar 

  • Takagi S, Bénard C, Pak J, Livingstone D, Hekimi S (1997) Cellular and axonal migrations are misguided along both body axes in the maternal-effect mau-2 mutants of Caenorhabditis elegans. Development 124:5115–5126

    PubMed  CAS  Google Scholar 

  • Takahashi TS, Yiu P, Chou MF, Gygi S, Walter JC (2004) Recruitment of Xenopus Scc2 and cohesin to chromatin requires the pre-replication complex. Nat Cell Biol 6:991–996

    PubMed  CAS  Google Scholar 

  • Tanaka T, Cosma MP, Wirth K, Nasmyth K (1999) Identification of cohesin association sites at centromeres and along chromosome arms. Cell 98:847–858

    PubMed  CAS  Google Scholar 

  • Tanaka K, Yonekawa T, Kawasaki Y, Kai M, Furuya K, Iwasaki M, Murakami H, Yanagida M, Okayama H (2000) Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase. Mol Cell Biol 20:3459–3469

    PubMed  CAS  Google Scholar 

  • Tanaka K, Hao Z, Kai M, Okayama H (2001) Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J 20:5779–5790

    PubMed  CAS  Google Scholar 

  • Tomkins DJ, Sisken JE (1984) Abnormalities in the cell-division cycle in Roberts syndrome fibroblasts: a cellular basis for the phenotypic characteristics? Am J Hum Genet 36:1332–1340

    PubMed  CAS  Google Scholar 

  • Tomkins D, Hunter A, Roberts M (1979) Cytogenetic findings in Roberts-SC phocomelia syndrome(s). Am J Med Genet 4:17–26

    PubMed  CAS  Google Scholar 

  • Tomonaga T, Nagao K, Kawasaki Y, Furuya K, Murakami A, Morishita J, Yuasa T, Sutani T, Kearsey SE, Uhlmann F, Nasmyth K, Yanagida M (2000) Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. Genes Dev 14:2757–2770

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Torigoi E, Bennani-Baiti IM, Rosen C, Gonzalez K, Morcillo P, Ptashne M, Dorsett D (2000) Chip interacts with diverse homeodomain proteins and potentiates bicoid activity in vivo. Proc Natl Acad Sci USA 97:2686–2691

    PubMed  CAS  Google Scholar 

  • Toth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A, Nasmyth K (1999) Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7) to establish cohesion between sister chromatids during DNA replication. Genes Dev 13:320–333

    PubMed  CAS  Google Scholar 

  • Uhlmann F, Lottspeich F, Nasmyth K (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400:37–42

    PubMed  CAS  Google Scholar 

  • Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K (2000) Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103:375-386

    PubMed  CAS  Google Scholar 

  • Van den Berg DJ, Francke U (1993) Roberts syndrome: a review of 100 cases and a new rating system for severity. Am J Med Genet 47:1104–1123

    Google Scholar 

  • Vega H, Waisfisz Q, Gordillo M, Sakai N, Yanagihara I, Yamada M, van Gosliga D, Kayserili H, Xu C, Ozono K, Wang Jabs E, Inui K, Joenje H (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

    PubMed  CAS  Google Scholar 

  • Waizenegger IC, Hauf S, Meinke A, Peters JM (2000) Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103:399–410

    PubMed  CAS  Google Scholar 

  • Watanabe Y (2005) Shugoshin: guardian spirit at the centromere. Curr Opin Cell Biol 17:590–595

    PubMed  CAS  Google Scholar 

  • Weitzer S, Lehane C, Uhlmann F (2003) A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr Biol 13:1930–1940

    PubMed  CAS  Google Scholar 

  • Williams BC, Garrett-Engele CM, Li Z, Williams EV, Rosenman ED, Goldberg ML (2003) Two putative acetyltransferases, san and deco, are required for establishing sister chromatid cohesion in Drosophila. Curr Biol 13:2025–2036

    PubMed  CAS  Google Scholar 

  • Yanagida M (2005) Basic mechanism of eukaryotic chromosome segregation. Philos Trans R Soc Lond B Biol Sci 360:609–621

    PubMed  CAS  Google Scholar 

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Acknowledgements

The author thanks Ian Krantz, Laird Jackson, Uta Francke, Joel Eissenberg, and Tom Strachan for interesting discussions and comments on the manuscript, and Sergey Korolev for help with structural analysis of the Smc1L1 mutations. Work in the author’s laboratory is supported by grants from the NIH, March of Dimes and CdLS Foundation (USA).

Note added in proof

While this review was in proof, papers describing S. pombe and human homologues of the Scc4 adherin subunit were published:

Bernard P, Drogat J, Maure JF, Dheur S, Vaur S, Genier S, Javerzat JP (2006) A screen for cohesion mutants uncovers Ssl3, the fission yeast counterpart of the cohesin loading factor Scc4. Curr Biol 16:875–881.

Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, Peters JM (2006) Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr Biol 16:863–874.

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  1. Edward A. Doisy Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, Saint Louis, MO, 63104, USA

    Dale Dorsett

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Dorsett, D. Roles of the sister chromatid cohesion apparatus in gene expression, development, and human syndromes. Chromosoma 116, 1–13 (2007). https://doi.org/10.1007/s00412-006-0072-6

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