An Essential Role of Variant Histone H3.3 for Ectomesenchyme Potential of the Cranial Neural Crest

PLoS Genetics

Volumn 8, Issue 9, 2012, Pages

  Cox, Samuel G ^a   Kim, Hyunjung ^b   Garnett, Aaron Timothy ^c   Medeiros, Daniel Meulemans ^c   An, Woojin ^b   Crump, J Gage ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN; CHROMOSOME CONDENSATION; CONTROLLED STUDY; DNA POLYMORPHISM; DNA REPLICATION; ECTODERM; ECTOMESENCHYME; EMBRYO; GENE EXPRESSION; GENE MUTATION; GENETIC SCREENING; GENOTYPE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN CELL; MESENCHYME; MESODERM; MICROSATELLITE MARKER; NEURAL CREST; NEURAL CREST CELL; NONHUMAN; NUCLEOSOME; PIGMENT CELL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROCESSING; SKELETON; ZEBRA FISH;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; CHROMATIN; ECTODERM; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HISTONES; HUMANS; MESODERM; MUTATION; NEURAL CREST; NEURAL PLATE; NUCLEOSOMES; SKULL; ZEBRAFISH;

DANIO RERIO; VERTEBRATA;

EID: 84866948612     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002938     Document Type: Article

References (69)

1. Gans C, Northcutt RG, (1983) Neural Crest and the Origin of Vertebrates: A New Head. Science 220: 268-273.
2. Baroffio A, Dupin E, Le Douarin NM, (1991) Common precursors for neural and mesectodermal derivatives in the cephalic neural crest. Development 112: 301-305.
3. Bronner-Fraser M, Fraser SE, (1988) Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335: 161-164.
4. Platt JB, (1893) Ectodermic origin of the cartilages of the head. Anat Anz 8: 506-509.
5. Schilling TF, Kimmel CB, (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120: 483-494.
6. Breau MA, Pietri T, Stemmler MP, Thiery JP, Weston JA, (2008) A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme. Proc Natl Acad Sci U S A 105: 7750-7755.
7. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
8. Vastenhouw NL, Zhang Y, Woods IG, Imam F, Regev A, et al. (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464: 922-926.
9. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, et al. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
10. Gargiulo G, Levy S, Bucci G, Romanenghi M, Fornasari L, et al. (2009) NA-Seq: a discovery tool for the analysis of chromatin structure and dynamics during differentiation. Dev Cell 16: 466-481.
11. Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, et al. (2010) CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463: 958-962.
12. Eroglu B, Wang G, Tu N, Sun X, Mivechi NF, (2006) Critical role of Brg1 member of the SWI/SNF chromatin remodeling complex during neurogenesis and neural crest induction in zebrafish. Dev Dyn 235: 2722-2735.
13. Strobl-Mazzulla PH, Sauka-Spengler T, Bronner-Fraser M, (2010) Histone demethylase JmjD2A regulates neural crest specification. Dev Cell 19: 460-468.
14. Takeuchi T, Watanabe Y, Takano-Shimizu T, Kondo S, (2006) Roles of jumonji and jumonji family genes in chromatin regulation and development. Dev Dyn 235: 2449-2459.
15. Patten SA, Jacobs-McDaniels NL, Zaouter C, Drapeau P, Albertson RC, et al. (2012) Role of Chd7 in zebrafish: a model for CHARGE syndrome. PLoS ONE 7: e31650 doi:10.1371/journal.pone.0031650.
16. Ahmad K, Henikoff S, (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9: 1191-1200.
17. Hajkova P, Ancelin K, Waldmann T, Lacoste N, Lange UC, et al. (2008) Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452: 877-881.
18. van der Heijden GW, Derijck AA, Posfai E, Giele M, Pelczar P, et al. (2007) Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat Genet 39: 251-258.
19. Hodl M, Basler K, (2009) Transcription in the absence of histone H3.3. Curr Biol 19: 1221-1226.
20. Sakai A, Schwartz BE, Goldstein S, Ahmad K, (2009) Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr Biol 19: 1816-1820.
21. Couldrey C, Carlton MB, Nolan PM, Colledge WH, Evans MJ, (1999) A retroviral gene trap insertion into the histone 3.3A gene causes partial neonatal lethality, stunted growth, neuromuscular deficits and male sub-fertility in transgenic mice. Hum Mol Genet 8: 2489-2495.
22. Lawson ND, Weinstein BM, (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248: 307-318.
23. Couly GF, Coltey PM, Le Douarin NM, (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117: 409-429.
24. Kimmel CB, Miller CT, Moens CB, (2001) Specification and morphogenesis of the zebrafish larval head skeleton. Dev Biol 233: 239-257.
25. Arduini BL, Bosse KM, Henion PD, (2009) Genetic ablation of neural crest cell diversification. Development 136: 1987-1994.
26. Li YX, Zdanowicz M, Young L, Kumiski D, Leatherbury L, et al. (2003) Cardiac neural crest in zebrafish embryos contributes to myocardial cell lineage and early heart function. Dev Dyn 226: 540-550.
27. Thisse B, Heyer V, Lux A, Alunni V, Degrave A, et al. (2004) Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol 77: 505-519.
28. Pauls S, Geldmacher-Voss B, Campos-Ortega JA, (2001) A zebrafish histone variant H2A.F/Z and a transgenic H2A.F/Z:GFP fusion protein for in vivo studies of embryonic development. Dev Genes Evol 211: 603-610.
29. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ, (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
30. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, et al. (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140: 678-691.
31. Meulemans D, Bronner-Fraser M, (2004) Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7: 291-299.
32. Ng RK, Gurdon JB, (2008) Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol 10: 102-109.
33. McKittrick E, Gafken PR, Ahmad K, Henikoff S, (2004) Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci U S A 101: 1525-1530.
34. Mito Y, Henikoff JG, Henikoff S, (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37: 1090-1097.
35. Ray-Gallet D, Quivy JP, Scamps C, Martini EM, Lipinski M, et al. (2002) HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell 9: 1091-1100.
36. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y, (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51-61.
37. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD, (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Natl Acad Sci U S A 107: 14075-14080.
38. Sawatsubashi S, Murata T, Lim J, Fujiki R, Ito S, et al. (2010) A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev 24: 159-170.
39. Roberts C, Sutherland HF, Farmer H, Kimber W, Halford S, et al. (2002) Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnormalities of mesoendodermal derivatives prior to early embryonic lethality. Mol Cell Biol 22: 2318-2328.
40. Wise-Draper TM, Mintz-Cole RA, Morris TA, Simpson DS, Wikenheiser-Brokamp KA, et al. (2009) Overexpression of the cellular DEK protein promotes epithelial transformation in vitro and in vivo. Cancer research 69: 1792-1799.
41. Michaelson JS, Bader D, Kuo F, Kozak C, Leder P, (1999) Loss of Daxx, a promiscuously interacting protein, results in extensive apoptosis in early mouse development. Genes & development 13: 1918-1923.
42. Schnetz MP, Bartels CF, Shastri K, Balasubramanian D, Zentner GE, et al. (2009) Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res 19: 590-601.
43. Baker CV, Bronner-Fraser M, Le Douarin NM, Teillet MA, (1997) Early- and late-migrating cranial neural crest cell populations have equivalent developmental potential in vivo. Development 124: 3077-3087.
44. Weston JA, Yoshida H, Robinson V, Nishikawa S, Fraser ST, (2004) Neural crest and the origin of ectomesenchyme: Neural fold heterogeneity suggests an alternative hypothesis. Dev Dyn 229: 118-130.
45. Dorsky RI, Moon RT, Raible DW, (1998) Control of neural crest cell fate by the Wnt signalling pathway. Nature 396: 370-373.
46. Streisinger G, Walker C, Dower N, Knauber D, Singer F, (1981) Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291: 293-296.
47. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
48. Walker MB, Kimmel CB, (2007) A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem 82: 23-28.
49. Zuniga E, Rippen M, Alexander C, Schilling TF, Crump JG, (2011) Gremlin 2 regulates distinct roles of BMP and Endothelin 1 signaling in dorsoventral patterning of the facial skeleton. Development 138: 5147-5156.
50. Phillips BT, Kwon HJ, Melton C, Houghtaling P, Fritz A, et al. (2006) Zebrafish msxB, msxC and msxE function together to refine the neural-nonneural border and regulate cranial placodes and neural crest development. Dev Biol 294: 376-390.
51. Seo HC, Saetre BO, Havik B, Ellingsen S, Fjose A, (1998) The zebrafish Pax3 and Pax7 homologues are highly conserved, encode multiple isoforms and show dynamic segment-like expression in the developing brain. Mech Dev 70: 49-63.
52. Toyama R, Gomez DM, Mana MD, Dawid IB, (2004) Sequence relationships and expression patterns of zebrafish zic2 and zic5 genes. Gene Expr Patterns 4: 345-350.
53. Thisse C, Thisse B, Schilling TF, Postlethwait JH, (1993) Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119: 1203-1215.
54. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, et al. (2001) Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128: 4113-4125.
55. Furthauer M, Thisse C, Thisse B, (1997) A role for FGF-8 in the dorsoventral patterning of the zebrafish gastrula. Development 124: 4253-4264.
56. Yan YL, Willoughby J, Liu D, Crump JG, Wilson C, et al. (2005) A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development 132: 1069-1083.
57. Akimenko MA, Ekker M, Wegner J, Lin W, Westerfield M, (1994) Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J Neurosci 14: 3475-3486.
58. Krauss S, Johansen T, Korzh V, Fjose A, (1991) Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development 113: 1193-1206.
59. Oxtoby E, Jowett T, (1993) Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res 21: 1087-1095.
60. Luo R, An M, Arduini BL, Henion PD, (2001) Specific pan-neural crest expression of zebrafish Crestin throughout embryonic development. Dev Dyn 220: 169-174.
61. Germanguz I, Lev D, Waisman T, Kim CH, Gitelman I, (2007) Four twist genes in zebrafish, four expression patterns. Dev Dyn 236: 2615-2626.
62. Ignatius MS, Moose HE, El-Hodiri HM, Henion PD, (2008) colgate/hdac1 Repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev Biol 313: 568-583.
63. Maves L, Jackman W, Kimmel CB, (2002) FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 129: 3825-3837.
64. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, et al. (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236: 3088-3099.
65. Heckman KL, Pease LR, (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2: 924-932.
66. Ooi SL, Priess JR, Henikoff S, (2006) Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLoS Genet 2: e97 doi:10.1371/journal.pgen.0020097.
67. Sarcinella E, Zuzarte PC, Lau PN, Draker R, Cheung P, (2007) Monoubiquitylation of H2A.Z distinguishes its association with euchromatin or facultative heterochromatin. Mol Cell Biol 27: 6457-6468.
68. Jung SY, Malovannaya A, Wei J, O'Malley BW, Qin J, (2005) Proteomic analysis of steady-state nuclear hormone receptor coactivator complexes. Mol Endocrinol 19: 2451-2465.
69. Crump JG, Swartz ME, Kimmel CB, (2004) An Integrin-Dependent Role of Pouch Endoderm in Hyoid Cartilage Development. PLoS Biol 2: e244 doi:10.1371/journal.pbio.0020244.