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Zebrafish as a Model to Study Cohesin and Cohesinopathies

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Cohesin and Condensin

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1515))

Abstract

The cohesin protein complex regulates multiple cellular events including sister chromatid cohesion and gene expression. Several distinct human diseases called cohesinopathies have been associated with genetic mutations in cohesin subunit genes or genes encoding regulators of cohesin function. Studies in different model systems, from yeast to mouse have provided insights into the molecular mechanisms of action of cohesin/cohesin regulators and their implications in the pathogenesis of cohesinopathies. The zebrafish has unique advantages for embryonic analyses and quantitative gene knockdown with morpholinos during the first few days of development, in contrast to knockouts of cohesin regulators in flies or mammals, which are either lethal as homozygotes or dramatically compensated for in heterozygotes. This has been particularly informative for Rad21, where a role in gene expression was first shown in zebrafish, and Nipbl, where the fish work revealed tissue-specific functions in heart, gut, and limbs, and long-range enhancer–promoter interactions that control Hox gene expression in vivo. Here we discuss the utility of the zebrafish in studying the developmental and pathogenic roles of cohesin.

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References

  1. Michaelis C, Ciosk R, Nasmyth K (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91(1):35–45, doi:S0092-8674(01)80007-6 [pii]

    Article  CAS  PubMed  Google Scholar 

  2. Ball AR Jr, Chen YY, Yokomori K (2014) Mechanisms of cohesin-mediated gene regulation and lessons learned from cohesinopathies. Biochim Biophys Acta 1839(3):191–202. doi:10.1016/j.bbagrm.2013.11.002

    Article  CAS  PubMed  Google Scholar 

  3. Watrin E, Peters JM (2006) Cohesin and DNA damage repair. Exp Cell Res 312(14):2687–2693. doi:10.1016/j.yexcr.2006.06.024

    Article  CAS  PubMed  Google Scholar 

  4. Lu S, Goering M, Gard S, Xiong B, McNairn AJ, Jaspersen SL, Gerton JL (2010) Eco1 is important for DNA damage repair in S. cerevisiae. Cell Cycle 9(16):3315–3327. doi:10.4161/cc.9.16.12673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Lee J (2013) Roles of cohesin and condensin in chromosome dynamics during mammalian meiosis. J Reprod Dev 59(5):431–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400(6743):461–464. doi:10.1038/22774

    Article  CAS  PubMed  Google Scholar 

  7. Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, Yaeger D, Jukofsky L, Wasserman N, Bottani A, Morris CA, Nowaczyk MJM, Toriello H, Bamshad MJ, Carey JC, Rappaport E, Kawauchi S, Lander AD, Calof AL, H-h L, Devoto M, Jackson LG (2004) Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped-B. Nat Genet 36(6):631–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Tonkin ET, Wang T-J, 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(6):636–641

    Article  CAS  PubMed  Google Scholar 

  9. Borck G, Zarhrate M, Cluzeau C, Bal E, Bonnefont J-P, Munnich A, Cormier-Daire V, Colleaux L (2006) Father-to-daughter transmission of Cornelia de Lange syndrome caused by a mutation in the 5′ untranslated region of the NIPBL gene. Hum Mutat 27(8):731–735

    Article  CAS  PubMed  Google Scholar 

  10. Deardorff MA, Kaur M, Yaeger D, Rampuria A, Korolev S, Pie J, Gil-Rodríguez C, Arnedo M, Loeys B, Kline AD, Wilson M, Lillquist K, Siu V, Ramos FJ, Musio A, Jackson LS, Dorsett D, Krantz ID (2007) Mutations in Cohesin complex members SMC3 and SMC1A cause a mild variant of Cornelia de Lange syndrome with predominant mental retardation. Am J Hum Genet 80:485–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. Deardorff MA, Wilde JJ, Albrecht M, Dickinson E, Tennstedt S, Braunholz D, Monnich M, Yan Y, Xu W, Gil-Rodriguez MC, Clark D, Hakonarson H, Halbach S, Michelis LD, Rampuria A, Rossier E, Spranger S, Van Maldergem L, Lynch SA, Gillessen-Kaesbach G, Ludecke HJ, Ramsay RG, McKay MJ, Krantz ID, Xu H, Horsfield JA, Kaiser FJ (2012) RAD21 mutations cause a human cohesinopathy. Am J Hum Genet 90(6):1014–1027. doi:10.1016/j.ajhg.2012.04.019, S0002-9297(12)00252-2 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, Minamino M, Saitoh K, Komata M, Katou Y, Clark D, Cole KE, De Baere E, Decroos C, Di Donato N, Ernst S, Francey LJ, Gyftodimou Y, Hirashima K, Hullings M, Ishikawa Y, Jaulin C, Kaur M, Kiyono T, Lombardi PM, Magnaghi-Jaulin L, Mortier GR, Nozaki N, Petersen MB, Seimiya H, Siu VM, Suzuki Y, Takagaki K, Wilde JJ, Willems PJ, Prigent C, Gillessen-Kaesbach G, Christianson DW, Kaiser FJ, Jackson LG, Hirota T, Krantz ID, Shirahige K (2012) HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature 489(7415):313–317. doi:10.1038/nature11316, nature11316 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Vega H, Waisfisz Q, Gordillo M, Sakai N, Yanagihara I, Yamada M, van Gosliga D, Kayserili H, Xu C, Ozono K, Jabs EW, 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(5):468–470. doi:10.1038/ng1548, ng1548 [pii]

    Article  CAS  PubMed  Google Scholar 

  15. 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. Development 132:4743–4753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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(8):3100–3111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kawauchi S, Calof AL, Santos R, Lopez-Burks ME, Young CM, Hoang MP, Chua A, Lao T, Lechner MS, Daniel JA, Nussenzweig A, Kitzes L, Yokomori K, Hallgrimsson B, Lander AD (2009) Multiple organ system defects and transcriptional dysregulation in the Nipbl +/2 mouse, a model of Cornelia de Lange syndrome. PLoS Genet 5(9):e1000650

    Article  PubMed  PubMed Central  Google Scholar 

  18. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters J-M (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796–801

    Article  CAS  PubMed  Google Scholar 

  19. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, Cobb BS, Yokomori K, Dillon N, Aragon L, Fisher AG, Merkenschlager M (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422–433

    Article  CAS  PubMed  Google Scholar 

  20. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467(7314):430–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ing-Simmons E, Seitan VC, Faure AJ, Flicek P, Carroll T, Dekker J, Fisher AG, Lenhard B, Merkenschlager M (2015) Spatial enhancer clustering and regulation of enhancer-proximal genes by cohesin. Genome Res 25(4):504–513. doi:10.1101/gr.184986.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Mizuguchi T, Fudenberg G, Mehta S, Belton JM, Taneja N, Folco HD, FitzGerald P, Dekker J, Mirny L, Barrowman J, Grewal SI (2014) Cohesin-dependent globules and heterochromatin shape 3D genome architecture in S. pombe. Nature 516(7531):432–435. doi:10.1038/nature13833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Losada A, Yokochi T, Kobayashi R, Hirano T (2000) Identification and characterization of SA/Scc3p subunits in the Xenopus and human cohesin complexes. J Cell Biol 150(3):405–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Vass S, Cotterill S, Valdeolmillos AM, Barbero JL, Lin E, Warren WD, Heck MM (2003) Depletion of Drad21/Scc1 in Drosophila cells leads to instability of the cohesin complex and disruption of mitotic progression. Curr Biol 13(3):208–218

    Article  CAS  PubMed  Google Scholar 

  25. Gruber S, Haering CH, Nasmyth K (2003) Chromosomal cohesin forms a ring. Cell 112(6):765–777

    Article  CAS  PubMed  Google Scholar 

  26. Anderson DE, Losada A, Erickson HP, Hirano T (2002) Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol 156(3):419–424. doi:10.1083/jcb.200111002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  29. Woodman J, Fara T, Dzieciatkowska M, Trejo M, Luong N, Hansen KC, Megee PC (2014) Cell cycle-specific cleavage of Scc2 regulates its cohesin deposition activity. Proc Natl Acad Sci U S A 111(19):7060–7065. doi:10.1073/pnas.1321722111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. Lopez-Serra L, Kelly G, Patel H, Stewart A, Uhlmann F (2014) The Scc2-Scc4 complex acts in sister chromatid cohesion and transcriptional regulation by maintaining nucleosome-free regions. Nat Genet 46(10):1147–1151. doi:10.1038/ng.3080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Shintomi K, Hirano T (2009) Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes Dev 23(18):2224–2236. doi:10.1101/gad.1844309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, Mechtler K, Peters JM (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127(5):955–967. doi:10.1016/j.cell.2006.09.040

    Article  CAS  PubMed  Google Scholar 

  34. 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(24):2406–2417. doi:10.1016/j.cub.2006.10.061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhang J, Shi X, Li Y, Kim BJ, Jia J, Huang Z, Yang T, Fu X, Jung SY, Wang Y, Zhang P, Kim ST, Pan X, Qin J (2008) Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol Cell 31(1):143–151. doi:10.1016/j.molcel.2008.06.006, S1097-2765(08)00420-6 [pii]

    Article  CAS  PubMed  Google Scholar 

  36. Unal E, Heidinger-Pauli JM, Kim W, Guacci V, Onn I, Gygi SP, Koshland DE (2008) A molecular determinant for the establishment of sister chromatid cohesion. Science 321(5888):566–569

    Article  PubMed  Google Scholar 

  37. Ben-Shahar TR, Heeger S, Lehane C, East P, Flynn H, Skehel M, Uhlmann F (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321(5888):563–566

    Article  CAS  Google Scholar 

  38. Higashi TL, Ikeda M, Tanaka H, Nakagawa T, Bando M, Shirahige K, Kubota Y, Takisawa H, Masukata H, Takahashi TS (2012) The prereplication complex recruits XEco2 to chromatin to promote cohesin acetylation in Xenopus egg extracts. Curr Biol 22(11):977–988. doi:10.1016/j.cub.2012.04.013

    Article  CAS  PubMed  Google Scholar 

  39. 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(8):2999–3007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Rankin S, Ayad NG, Kirschner MW (2005) Sororin, a substrate of the anaphase-promoting complex, is required for sister chromatid cohesion in vertebrates. Mol Cell 18(2):185–200. doi:10.1016/j.molcel.2005.03.017

    Article  CAS  PubMed  Google Scholar 

  41. Schmitz J, Watrin E, Lenart P, Mechtler K, Peters JM (2007) Sororin is required for stable binding of cohesin to chromatin and for sister chromatid cohesion in interphase. Curr Biol 17(7):630–636. doi:10.1016/j.cub.2007.02.029

    Article  CAS  PubMed  Google Scholar 

  42. Nishiyama T, Ladurner R, Schmitz J, Kreidl E, Schleiffer A, Bhaskara V, Bando M, Shirahige K, Hyman AA, Mechtler K, Peters JM (2010) Sororin mediates sister chromatid cohesion by antagonizing Wapl. Cell 143(5):737–749. doi:10.1016/j.cell.2010.10.031

    Article  CAS  PubMed  Google Scholar 

  43. Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters JM (2005) Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol 3(3), e69. doi:10.1371/journal.pbio.0030069, 04-PLBI-RA-0677R1 [pii]

    Article  PubMed  PubMed Central  Google Scholar 

  44. Sumara I, Vorlaufer E, Stukenberg PT, Kelm O, Redemann N, Nigg EA, Peters JM (2002) The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell 9(3):515–525

    Article  CAS  PubMed  Google Scholar 

  45. Zhang N, Panigrahi AK, Mao Q, Pati D (2011) Interaction of Sororin protein with polo-like kinase 1 mediates resolution of chromosomal arm cohesion. J Biol Chem 286(48):41826–41837. doi:10.1074/jbc.M111.305888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Wang X, Dai W (2005) Shugoshin, a guardian for sister chromatid segregation. Exp Cell Res 310(1):1–9. doi:10.1016/j.yexcr.2005.07.018

    Article  CAS  PubMed  Google Scholar 

  47. Salah SM, Nasmyth K (2000) Destruction of the securin Pds1p occurs at the onset of anaphase during both meiotic divisions in yeast. Chromosoma 109(1-2):27–34

    Article  CAS  PubMed  Google Scholar 

  48. Borges V, Lehane C, Lopez-Serra L, Flynn H, Skehel M, Rolef Ben-Shahar T, Uhlmann F (2010) Hos1 deacetylates Smc3 to close the cohesin acetylation cycle. Mol Cell 39(5):677–688. doi:10.1016/j.molcel.2010.08.009

    Article  CAS  PubMed  Google Scholar 

  49. Xiong B, Lu S, Gerton JL (2010) Hos1 is a lysine deacetylase for the Smc3 subunit of cohesin. Curr Biol 20(18):1660–1665. doi:10.1016/j.cub.2010.08.019

    Article  CAS  PubMed  Google Scholar 

  50. Bose T, Gerton JL (2010) Cohesinopathies, gene expression, and chromatin organization. J Cell Biol 189(2):201–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ireland M, Donnai D, Burn J (1993) Brachmann–de Lange syndrome. Delineation of the clinical phenotype. Am J Med Genet 47:959–964

    Article  CAS  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  Google Scholar 

  53. Boyle MI, Jespersgaard C, Brondum-Nielsen K, Bisgaard AM, Tumer Z (2015) Cornelia de Lange syndrome. Clin Genet 88(1):1–12. doi:10.1111/cge.12499

    Article  CAS  PubMed  Google Scholar 

  54. Hoppman-Chaney N, Jang JS, Jen J, Babovic-Vuksanovic D, Hodge JC (2011) In-frame multi-exon deletion of SMC1A in a severely affected female with Cornelia de Lange syndrome. Am J Med Genet A 158A(1):193–198. doi:10.1002/ajmg.a.34360

    Article  PubMed  Google Scholar 

  55. Gil-Rodriguez MC, Deardorff MA, Ansari M, Tan CA, Parenti I, Baquero-Montoya C, Ousager LB, Puisac B, Hernandez-Marcos M, Teresa-Rodrigo ME, Marcos-Alcalde I, Wesselink JJ, Lusa-Bernal S, Bijlsma EK, Braunholz D, Bueno-Martinez I, Clark D, Cooper NS, Curry CJ, Fisher R, Fryer A, Ganesh J, Gervasini C, Gillessen-Kaesbach G, Guo Y, Hakonarson H, Hopkin RJ, Kaur M, Keating BJ, Kibaek M, Kinning E, Kleefstra T, Kline AD, Kuchinskaya E, Larizza L, Li YR, Liu X, Mariani M, Picker JD, Pie A, Pozojevic J, Queralt E, Richer J, Roeder E, Sinha A, Scott RH, So J, Wusik KA, Wilson L, Zhang J, Gomez-Puertas P, Casale CH, Strom L, Selicorni A, Ramos FJ, Jackson LG, Krantz ID, Das S, Hennekam RC, Kaiser FJ, FitzPatrick DR, Pie J (2015) De novo heterozygous mutations in SMC3 cause a range of Cornelia de Lange syndrome-overlapping phenotypes. Hum Mutat 36(4):454–462. doi:10.1002/humu.22761

    Article  CAS  PubMed  Google Scholar 

  56. Castronovo P, Gervasini C, Cereda A, Masciadri M, Milani D, Russo S, Selicorni A, Larizza L (2009) Premature chromatid separation is not a useful diagnostic marker for Cornelia de Lange syndrome. Chromosome Res 17(6):763–771. doi:10.1007/s10577-009-9066-6

    Article  CAS  PubMed  Google Scholar 

  57. Xu B, Lu S, Gerton JL (2014) Roberts syndrome: a deficit in acetylated cohesin leads to nucleolar dysfunction. Rare Dis 2:e27743. doi:10.4161/rdis.27743

    Article  PubMed  PubMed Central  Google Scholar 

  58. Dupont C, Bucourt M, Guimiot F, Kraoua L, Smiljkovski D, Le Tessier D, Lebugle C, Gerard B, Spaggiari E, Bourdoncle P, Tabet AC, Benzacken B, Dupont JM (2014) 3D-FISH analysis reveals chromatid cohesion defect during interphase in Roberts syndrome. Mol Cytogenet 7(1):59. doi:10.1186/s13039-014-0059-6

    Article  PubMed  PubMed Central  Google Scholar 

  59. Lu S, Lee KK, Harris B, Xiong B, Bose T, Saraf A, Hattem G, Florens L, Seidel C, Gerton JL (2014) The cohesin acetyltransferase Eco1 coordinates rDNA replication and transcription. EMBO Rep 15(5):609–617. doi:10.1002/embr.201337974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Bose T, Lee KK, Lu S, Xu B, Harris B, Slaughter B, Unruh J, Garrett A, McDowell W, Box A, Li H, Peak A, Ramachandran S, Seidel C, Gerton JL (2012) Cohesin proteins promote ribosomal RNA production and protein translation in yeast and human cells. PLoS Genet 8(6), e1002749. doi:10.1371/journal.pgen.1002749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Losada A, Hirano M, Hirano T (1998) Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev 12(13):1986–1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Darwiche N, Freeman LA, Strunnikov A (1999) Characterization of the components of the putative mammalian sister chromatid cohesion complex. Gene 233(1-2):39–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Chien R, Zeng W, Kawauchi S, Bender MA, Santos R, Gregson HC, Schmiesing JA, Newkirk DA, Kong X, Ball AR Jr, Calof AL, Lander AD, Groudine MT, Yokomori K (2011) Cohesin mediates chromatin interactions that regulate mammalian beta-globin expression. J Biol Chem 286(20):17870–17878. doi:10.1074/jbc.M110.207365, M110.207365 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T, Fraser P, Fisher AG, Merkenschlager M (2009) Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460(7253):410–413. doi:10.1038/nature08079, nature08079 [pii]

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Guo Y, Monahan K, Wu H, Gertz J, Varley KE, Li W, Myers RM, Maniatis T, Wu Q (2012) CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice. Proc Natl Acad Sci U S A 109(51):21081–21086. doi:10.1073/pnas.1219280110, 1219280110 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Misulovin Z, Schwartz YB, Li X-Y, Kahn TG, Gause M, MacArthur S, Fay JC, Eisen MB, Pirrotta V, Biggin MD, Dorsett D (2008) Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome. Chromosoma 117(1):89–102

    Article  CAS  PubMed  Google Scholar 

  67. Stedman W, Kang H, Lin S, Kissil JL, Bartolomei SM, Lieberman PM (2008) Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J 27:654–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN, Baliga NS, Aebersold R, Ranish JA, Krumm A (2008) CTCF physically links cohesin to chromatin. Proc Natl Acad Sci U S A 105:8309–8314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Muto A, Ikeda S, Lopez-Burks ME, Kikuchi Y, Calof AL, Lander AD, Schilling TF (2014) Nipbl and mediator cooperatively regulate gene expression to control limb development. PLoS Genet 10(9), e1004671. doi:10.1371/journal.pgen.1004671

    Article  PubMed  PubMed Central  Google Scholar 

  70. Fay A, Misulovin Z, Li J, Schaaf CA, Gause M, Gilmour DS, Dorsett D (2011) Cohesin selectively binds and regulates genes with paused RNA polymerase. Curr Biol 21(19):1624–1634. doi:10.1016/j.cub.2011.08.036, S0960-9822(11)00942-0 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Schaaf CA, Kwak H, Koenig A, Misulovin Z, Gohara DW, Watson A, Zhou Y, Lis JT, Dorsett D (2013) Genome-wide control of RNA polymerase II activity by cohesin. PLoS Genet 9(3), e1003382. doi:10.1371/journal.pgen.1003382, PGENETICS-D-12-02409 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assuncao JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G, Whitehead S, Kay M, Brown J, Murnane C, Gray E, Humphries M, Sycamore N, Barker D, Saunders D, Wallis J, Babbage A, Hammond S, Mashreghi-Mohammadi M, Barr L, Martin S, Wray P, Ellington A, Matthews N, Ellwood M, Woodmansey R, Clark G, Cooper J, Tromans A, Grafham D, Skuce C, Pandian R, Andrews R, Harrison E, Kimberley A, Garnett J, Fosker N, Hall R, Garner P, Kelly D, Bird C, Palmer S, Gehring I, Berger A, Dooley CM, Ersan-Urun Z, Eser C, Geiger H, Geisler M, Karotki L, Kirn A, Konantz J, Konantz M, Oberlander M, Rudolph-Geiger S, Teucke M, Lanz C, Raddatz G, Osoegawa K, Zhu B, Rapp A, Widaa S, Langford C, Yang F, Schuster SC, Carter NP, Harrow J, Ning Z, Herrero J, Searle SM, Enright A, Geisler R, Plasterk RH, Lee C, Westerfield M, de Jong PJ, Zon LI, Postlethwait JH, Nusslein-Volhard C, Hubbard TJ, Roest Crollius H, Rogers J, Stemple DL (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496(7446):498–503. doi:10.1038/nature12111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Eisen JS, Smith JC (2008) Controlling morpholino experiments: don't stop making antisense. Development 135(10):1735–1743. doi:10.1242/dev.001115

    Article  CAS  PubMed  Google Scholar 

  74. Muto A, Calof AL, Lander AD, Schilling TF (2011) Multifactorial origins of heart and gut defects in nipbl-deficient zebrafish, a model of Cornelia de Lange syndrome. PLoS Biol 9(10), e1001181. doi:10.1371/journal.pbio.1001181, PBIOLOGY-D-10-01312 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Westerfield M (1995) The Zebrafish book. A guide for the laboratory use of Zebrafish (Danio rerio). University of Oregon Press, Eugene, OR

    Google Scholar 

  76. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203(3):253–310. doi:10.1002/aja.1002030302

    Article  CAS  PubMed  Google Scholar 

  77. Bedell VM, Ekker SC (2015) Using engineered endonucleases to create knockout and knockin zebrafish models. Methods Mol Biol 1239:291–305. doi:10.1007/978-1-4939-1862-1_17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, Stainier DY, Zwartkruis F, Abdelilah S, Rangini Z, Belak J, Boggs C (1996) A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123:37–46

    CAS  PubMed  Google Scholar 

  79. Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang YJ, Heisenberg CP, Kelsh RN, Furutani-Seiki M, Vogelsang E, Beuchle D, Schach U, Fabian C, Nusslein-Volhard C (1996) The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123:1–36

    CAS  PubMed  Google Scholar 

  80. Horsfield JA, Anagnostou SH, Hu JK-H, Cho KHY, Geisler R, Lieschke G, Crosier KE, Crosier PS (2007) Cohesin-dependent regulation of Runx genes. Development 134:2639–2649

    Article  CAS  PubMed  Google Scholar 

  81. Gaiano N, Amsterdam A, Kawakami K, Allende M, Becker T, Hopkins N (1996) Insertional mutagenesis and rapid cloning of essential genes in zebrafish. Nature 383(6603):829–832. doi:10.1038/383829a0

    Article  CAS  PubMed  Google Scholar 

  82. Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, Mishina M (2004) A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 7(1):133–144. doi:10.1016/j.devcel.2004.06.005

    Article  CAS  PubMed  Google Scholar 

  83. Ghiselli G (2006) SMC3 knockdown triggers genomic instability and p53-dependent apoptosis in human and zebrafish cells. Mol Cancer 5:52–64

    Article  PubMed  PubMed Central  Google Scholar 

  84. Pistocchi A, Fazio G, Cereda A, Ferrari L, Bettini LR, Messina G, Cotelli F, Biondi A, Selicorni A, Massa V (2013) Cornelia de Lange syndrome: NIPBL haploinsufficiency downregulates canonical Wnt pathway in zebrafish embryos and patients fibroblasts. Cell Death Dis 4, e866. doi:10.1038/cddis.2013.371, cddis2013371 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Marsman J, O'Neill AC, Kao BR, Rhodes JM, Meier M, Antony J, Monnich M, Horsfield JA (2014) Cohesin and CTCF differentially regulate spatiotemporal runx1 expression during zebrafish development. Biochim Biophys Acta 1839(1):50–61. doi:10.1016/j.bbagrm.2013.11.007

    Article  CAS  PubMed  Google Scholar 

  86. Mönnich M, Kuriger Z, Print CG, Horsfield JA (2011) A zebrafish model of Roberts syndrome reveals that esco2 depletion interferes with development by disrupting the cell cycle. PLoS One 6(5), e20051. doi:10.1371/journal.pone.0020051, PONE-D-11-03789 [pii]

    Article  PubMed  PubMed Central  Google Scholar 

  87. Rhodes JM, Bentley FK, Print CG, Dorsett D, Misulovin Z, Dickinson EJ, Crosier KE, Crosier PS, Horsfield JA (2010) Positive regulation of c-Myc by cohesin is direct, and evolutionarily conserved. Dev Biol 344:637–649. doi:10.1016/j.ydbio.2010.05.493, S0012-1606(10)00779-7 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Liu J, Krantz ID (2009) Cornelia de Lange syndrome, cohesin, and beyond. Clin Genet 76:303–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Xu B, Lee KK, Zhang L, Gerton JL (2013) Stimulation of mTORC1 with L-leucine rescues defects associated with Roberts syndrome. PLoS Genet 9(10), e1003857. doi:10.1371/journal.pgen.1003857

    Article  PubMed  PubMed Central  Google Scholar 

  90. Auer TO, Del Bene F (2014) CRISPR/Cas9 and TALEN-mediated knock-in approaches in zebrafish. Methods 69(2):142–150. doi:10.1016/j.ymeth.2014.03.027

    Article  CAS  PubMed  Google Scholar 

  91. Lemaitre C, Bickmore WA (2015) Chromatin at the nuclear periphery and the regulation of genome functions. Histochem Cell Biol. doi:10.1007/s00418-015-1346-y

    PubMed  Google Scholar 

  92. Gomez-Diaz E, Corces VG (2014) Architectural proteins: regulators of 3D genome organization in cell fate. Trends Cell Biol 24(11):703–711. doi:10.1016/j.tcb.2014.08.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Barutcu AR, Fritz AJ, Zaidi SK, vanWijnen AJ, Lian JB, Stein JL, Nickerson JA, Imbalzano AN, Stein GS (2015) C-ing the genome: a compendium of chromosome conformation capture methods to study higher-order chromatin organization. J Cell Physiol. doi:10.1002/jcp.25062

    Google Scholar 

  94. Lindeman LC, Vogt-Kielland LT, Alestrom P, Collas P (2009) Fish’n ChIPs: chromatin immunoprecipitation in the zebrafish embryo. Methods Mol Biol 567:75–86. doi:10.1007/978-1-60327-414-2_5

    Article  CAS  PubMed  Google Scholar 

  95. Klonisch T, Wark L, Hombach-Klonisch S, Mai S (2010) Nuclear imaging in three dimensions: a unique tool in cancer research. Ann Anat 192(5):292–301. doi:10.1016/j.aanat.2010.07.007

    Article  CAS  PubMed  Google Scholar 

  96. Tschopp P, Duboule D (2011) A genetic approach to the transcriptional regulation of Hox gene clusters. Annu Rev Genet 45:145–166. doi:10.1146/annurev-genet-102209-163429

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The work in the Lander and Schilling laboratories at the University of California, Irvine was supported by funds from the National Institutes of Health (P01-HD052860 and P50-GM76516) and the Cornelia de Lange Syndrome Foundation, and in the Kikuchi laboratory at Hiroshima University was supported by research funds from the University. We thank members of the Lander, Calof, Schilling, and Kikuchi Labs.

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Authors and Affiliations

  1. Department of Biological Science, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima, 739-8526, Japan

    Akihiko Muto

  2. Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA, 92697, USA

    Thomas F. Schilling

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  1. Akihiko Muto
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  2. Thomas F. Schilling
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Correspondence to Akihiko Muto .

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  1. Department of Biological Chemistry, School of Medicine University of California— Irvine, Irvine, California, USA

    Kyoko Yokomori

  2. Laboratory of Genome Structure and Function Research Center for Epigenetic Disease, Institute of Molecular and Cellular Biosciences The University of Tokyo, Tokyo, Japan

    Katsuhiko Shirahige

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Muto, A., Schilling, T.F. (2017). Zebrafish as a Model to Study Cohesin and Cohesinopathies. In: Yokomori, K., Shirahige, K. (eds) Cohesin and Condensin. Methods in Molecular Biology, vol 1515. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6545-8_11

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