A zebrafish model of roberts syndrome reveals that esco2 depletion interferes with development by disrupting the cell cycle

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Mönnich, Maren ^a   Kuriger, Zoë ^a   Print, Cristin G ^b   Horsfield, Julia A ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; MEMBRANE PROTEIN; PROTEIN ESCO2; RAD21 PROTEIN; UNCLASSIFIED DRUG; ACYLTRANSFERASE; ANTISENSE OLIGONUCLEOTIDE; CASPASE; CELL CYCLE PROTEIN; COHESINS; ESCO2 PROTEIN, ZEBRAFISH; NONHISTONE PROTEIN; PROTEIN P53; ZEBRAFISH PROTEIN;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL ADHESION; CELL CYCLE; CELL DISRUPTION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; HOMOZYGOSITY; INTRON; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN DEPLETION; ROBERTS SYNDROME; TRANSCRIPTION REGULATION; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; CELL CYCLE G2 PHASE; CRANIOFACIAL MALFORMATION; DISEASE MODEL; DRUG EFFECT; ENZYME ACTIVATION; FIN (ORGAN); GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; HYPERTELORISM; LARVA; METABOLISM; MITOSIS; PATHOLOGY; PHOCOMELIA; PRENATAL DEVELOPMENT;

DANIO RERIO;

ACETYLTRANSFERASES; ANIMAL FINS; ANIMALS; APOPTOSIS; CASPASES; CELL CYCLE; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CRANIOFACIAL ABNORMALITIES; DISEASE MODELS, ANIMAL; ECTROMELIA; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; ENZYME ACTIVATION; G2 PHASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; HYPERTELORISM; LARVA; MITOSIS; OLIGONUCLEOTIDES, ANTISENSE; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 79957542842     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020051     Document Type: Article

References (70)

1. Nasmyth K, Haering CH, (2009) Cohesin: Its Roles and Mechanisms. Annu Rev Genet 43: 525-58.
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.
3. Seitan VC, Banks P, Laval S, Majid NA, Dorsett D, et al. (2006) Metazoan Scc4 Homologs Link Sister Chromatid Cohesion to Cell and Axon Migration Guidance. PLoS Biol 4: e242.
4. 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.
5. 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.
6. Gerlich D, Koch B, Dupeux F, Peters J-M, Ellenberg J, (2006) Live-cell imaging reveals a stable cohesin-chromatin interaction after but not before DNA replication. Curr Biol 16: 1571-1578.
7. Moldovan GL, Pfander B, Jentsch S, (2006) PCNA controls establishment of sister chromatid cohesion during S phase. Mol Cell 23: 723-732.
8. 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.
9. 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.
10. Ivanov D, Schleiffer A, Eisenhaber F, Mechtler K, Haering CH, et al. (2002) Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr Biol 12: 323-328.
11. Hou F, Zou H, (2005) Two human orthologues of Eco1/Ctf7 acetyltransferases are both required for proper sister-chromatid cohesion. Mol Biol Cell 16: 3908-3918.
12. Ben-Shahar TR, 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. Craig JM, Choo KH, (2005) Kiss and break up-a safe passage to anaphase in mitosis and meiosis. Chromosoma 114: 252-262.
18. 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.
19. 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.
20. Xiong B, Lu S, Gerton JL, (2010) Hos1 Is a Lysine Deacetylase for the Smc3 Subunit of Cohesin. Curr Biol 18: 1660-5.
21. Ball AR Jr, Yokomori K, (2008) Damage-induced reactivation of cohesin in postreplicative DNA repair. Bioessays 30: 5-9.
22. 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.
23. 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.
24. Gordillo M, Vega H, Trainer AH, Hou F, Sakai N, et al. (2008) The molecular mechanism underlying Roberts syndrome involves loss of ESCO2 acetyltransferase activity. Hum Mol Genet 17: 2172-2180.
25. Schule 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.
26. Vega H, Trainer AH, Gordillo M, Crosier M, Kayserili H, et al. (2010) Phenotypic variability in 49 cases of ESCO2 mutations, including novel missense and codon deletion in the acetyltransferase domain, correlates with ESCO2 expression and establishes the clinical criteria for Roberts syndrome. J Med Genet 47: 30-37.
27. Liu J, Baynam G, (2010) Cornelia de Lange syndrome. Adv Exp Med Biol 685: 111-123.
28. Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, et al. (2004) Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped-B. Nat Genet 36: 631-635.
29. Deardorff MA, Kaur M, Yaeger D, Rampuria A, Korolev S, et al. (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.
30. 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.
31. Musio A, Selicorni A, Focarelli ML, Gervasini C, Milani D, et al. (2006) X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Genet 38: 528-530.
32. Liu J, Krantz ID, (2008) Cohesin and Human Disease. Annu Rev Genomics Hum Genet 9: 303-320.
33. 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.
34. Dorsett D, (2009) Cohesin, gene expression and development: lessons from Drosophila. Chromosome Res 17: 185-200.
35. Kawauchi S, Calof AL, Santos R, Lopez-Burks ME, Young CM, et al. (2009) Multiple organ system defects and transcriptional dysregulation in the Nipbl(+/-) mouse, a model of Cornelia de Lange Syndrome. PLoS Genet 5: e1000650.
36. Horsfield J, Anagnostou S, Hu JKH, Cho KH-Y, Geisler R, et al. (2007) Cohesin-dependent regulation of runx genes. Development 134: 2639-2649.
37. Rhodes JM, Bentley FK, Print CG, Dorsett D, Misulovin Z, et al. (2010) Positive regulation of c-Myc by cohesin is direct, and evolutionarily conserved. Dev Biol 344: 637-649.
38. Liu J, Zhang Z, Bando M, Itoh T, Deardorff MA, et al. (2009) Transcriptional dysregulation in NIPBL and cohesin mutant human cells. PLoS Biol 7: e1000119.
39. Gause M, Webber HA, Misulovin Z, Haller G, Rollins RA, et al. (2008) Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells. Chromosoma 117: 51-66.
40. 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.
41. Pauli A, van Bemmel JG, Oliveira RA, Itoh T, Shirahige K, et al. (2010) A direct role for cohesin in gene regulation and ecdysone response in Drosophila salivary glands. Curr Biol 20: 1787-1798.
42. 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.
43. Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN, et al. (2008) CTCF physically links cohesin to chromatin. Proc Natl Acad Sci U S A 105: 8309-8314.
44. Stedman W, Kang H, Lin S, Kissil JL, Bartolomei MS, et al. (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.
45. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, et al. (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451: 796-801.
46. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-5.
47. Schmidt D, Schwalie P, Ross-Innes CS, Hurtado A, Brown G, et al. (2010) A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20: 578-88.
48. Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T, et al. (2009) Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460: 410-413.
49. Monnich M, Banks S, Eccles M, Dickinson E, Horsfield J, (2009) Expression of cohesin and condensin genes during zebrafish development supports a non-proliferative role for cohesin. Gene Expr Patterns 9: 586-594.
50. Dorsett D, Krantz ID, (2009) On the molecular etiology of Cornelia de Lange syndrome. Ann N Y Acad Sci 1151: 22-37.
51. Berghmans S, Murphey RD, Wienholds E, Neuberg D, Kutok JL, et al. (2005) tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci U S A 102: 407-412.
52. Lee KC, Goh WL, Xu M, Kua N, Lunny D, et al. (2008) Detection of the p53 response in zebrafish embryos using new monoclonal antibodies. Oncogene 27: 629-640.
53. Dorsett D, (2010) Gene regulation: the cohesin ring connects developmental highways. Curr Biol 20: R886-888.
54. Bose T, Gerton JL, (2010) Cohesinopathies, gene expression, and chromatin organization. J Cell Biol 189: 201-210.
55. Dorsett D, (2011) Cohesin: genomic insights into controlling gene transcription and development. Curr Opin Genet Dev 21: 199-206.
56. 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.
57. 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.
58. Schulz S, Gerloff C, Ledig S, Langer D, Volleth M, et al. (2008) Prenatal diagnosis of Roberts syndrome and detection of an ESCO2 frameshift mutation in a Pakistani family. Prenat Diagn 28: 42-45.
59. Herrmann J, Opitz JM, (1977) The SC phocomelia and the Roberts syndrome: nosologic aspects. Eur J Pediatr 125: 117-134.
60. 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.
61. Knight RD, Schilling TF, (2006) Cranial neural crest and development of the head skeleton. Adv Exp Med Biol 589: 120-133.
62. Qi HH, Sarkissian M, Hu GQ, Wang Z, Bhattacharjee A, et al. (2010) Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 466: 503-507.
63. Galloway JL, Delgado I, Ros MA, Tabin CJ, (2009) A reevaluation of X-irradiation-induced phocomelia and proximodistal limb patterning. Nature 460: 400-404.
64. Schaaf CA, Misulovin Z, Sahota G, Siddiqui AM, Schwartz YB, et al. (2009) Regulation of the Drosophila Enhancer of split and invected-engrailed gene complexes by sister chromatid cohesion proteins. PLoS One 4: e6202.
65. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R, (2005) Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306: 343-348.
66. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Sudhof TC, et al. (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463: 1035-1041.
67. Westerfield M, (1995) The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR University of Oregon Press.
68. Thisse B, Pflumio S, Fürthauer M, Loppin B, Heyer V, et al. (2001) Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN Direct Data Submission. Available: https://wikizfinorg/display/prot/ThisseLab-InSituHybridizationProtocol-2010update Accessed 2011 Apr 26.
69. Walker MB, Kimmel CB, (2007) A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem 82: 23-28.
70. Shepard J, Stern HM, Pfaff KL, Amatruda JF, (2004) Analysis of the Cell Cycle in Zebrafish Embryos. In: Detrich HW, Westerfield M, Zon L, editors. The Zebrafish: 2nd Edition Cellular and Developmental Biology 2nd ed. San Diego Elsevier pp. 109-125.