A homologue of snail is expressed transiently in subsets of mesenchyme cells in the sea urchin embryo and is down-regulated in axis-deficient embryos

Developmental Dynamics

Volumn 235, Issue 11, 2006, Pages 3121-3131

  Hardin, Jeff ^a   Illingworth, Charles A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Gastrulation; Sea urchin; Secondary mesenchyme; Snail

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR SNAIL; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; CELL SUBPOPULATION; CONTROLLED STUDY; DROSOPHILA; ECHINODERM; EMBRYO; EMBRYO AXIS; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GASTRULATION; GENE; GENE EXPRESSION; GENE FUNCTION; IMMUNOHISTOCHEMISTRY; LYTECHINUS VARIEGATUS; MESENCHYME CELL; MESODERM; NEURAL CREST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SEA URCHIN; SEQUENCE HOMOLOGY; SNAIL GENE; VERTEBRATE;

ANIMALS; CELL DIFFERENTIATION; DOWN-REGULATION; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; GASTRULA; LYTECHINUS; MESODERM; SEA URCHINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

CHORDATA; DEUTEROSTOMIA; ECHINODERMATA; ECHINOIDEA; GASTROPODA; LYTECHINUS VARIEGATUS; PLUTEUS; VERTEBRATA;

EID: 33751004136     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20941     Document Type: Article

References (76)

1. Alberga A, Boulay JL, Kempe E, Dennefeld C, Haenlin M. 1991. The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers. Development 111:983-992.
2. Armstrong N, Hardin J, McClay DR. 1993. Cell-cell interactions regulate skeleton formation in the sea urchin embryo. Development 119:833-840.
3. Battle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A. 2000. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2:84-89.
4. Beach RL, Seo P, Venuti JM. 1999. Expression of the sea urchin MyoD homologue. SUM1, is not restricted to the myogenic lineage during embryogeriesis. Mech Dev 86:209-212.
5. Boulay JC, Dennefield C, Alberga A. 1987. The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 330:395-398.
6. Butler E, Hardin J, Benson S. 1987. The role of lysyl oxidase and collagen crosslinking during sea urchin development. Exp Cell Res 173:174-182.
7. Calestani C, Rast JP, Davidson EH. 2003. Isolation of pigment cell specific genes in the sea urchin embryo by differential macroarray screening. Development 130: 4587-4596.
8. Cano A, Perez-Moreno MA, Rodrigo I, Loeascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. 2000. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2: 76-83.
9. Carver EA, Jiang R, Lan Y, Oram KF, Gridley T. 2001. The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 21:8184-8188.
10. Coffman JA, McClay DR. 1990. A hyaline layer protein that becomes localized to the oral ectoderm and foregut of sea urchin embryos. Dev Biol 140:93-104.
11. Corbo JC, Erives A, Di Gregorio A, Chang A, Levine M. 1997. Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate. Development 124:2335-2344.
12. Croce J, Duloquin L, Lhomond G, McClay DR, Cache C. 2006. Frizzled5/8 is required in secondary mesenchyme cells to initiate archenteron invagination during sea urchin development. Development 133:547-557.
13. Davidson EH, Erwin DH. 2006. Gene regulatory networks and the evolution of animal body plans. Science 311:796-800.
14. Davidson EH, Rast JP, Oliven P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Schilstra MJ, Clarke PJ, Rust AG, Pan Z, Armine MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H. 2002. A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Dev Biol 246: 162-190.
15. Duboc V, Rottinger E, Besnardeau L, Lepage T. 2004. Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev Cell 6:397-410.
16. Duboc V, Rottinger E, Lapraz F, Besnardeau L, Lepage T. 2005. Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev Cell 9:147-158.
17. Ettensohn CA, Malinda KM. 1993. Size regulation and morphogenesis: a cellular analysis of skeletogenesis in the sea urchin embryo. Development 119:155-167.
18. Ettensohn CA, McClay DR. 1986. The regulation of primary mesenchyme cell migration in the sea urchin embryo: transplantations of cells and latex beads. Dev Biol 117:380-391.
19. Ettensohn CA, Ruffins SW. 1993. Mesodermal cell interactions in the sea urchin embryo: properties of skeletogenic secondary mesenchyme cells. Development 117:1275-1285.
20. Ettensohn CA, Wessel GM, Wray GA. 2004. The invertebrate deuterostomes: an introduction to their phylogeny, reproduction, development, and genomics. Methods Cell Biol 74:1-13.
21. Flowers VL, Courteau GR, Poustka AJ, Weng W, Venuti JM. 2004. Nodal/activin signaling establishes oral-aboral polarity in the early sea urchin embryo. Dev Dyn 231:727-740.
22. Fujiwara S, Corbo JC, Levine M. 1998. The snail repressor establishes a muscle/notochord boundary in the Ciona embryo. Development 125:2511-2520.
23. Gibson AW, Burke RD. 1985. The origin of pigment cells in embryos of the sea urchin Strongylocentrotus purpuratus. Dev Biol 107:414-419.
24. Gong ZY, Cserjesi P, Wessel GM, Brandhorst BP. 1991. Structure and expression of the polyubiquitin gene in sea urchin embryos. Mol Reprod Dev 28:111-118.
25. Hammerschmidt M, Nusslein-Volhard C. 1993. The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation. Development 119:1107-1118.
26. Hardin J. 1996. The cellular basis of sea urchin gastrulation. Curr Top Dev Biol 33:159-262.
27. Hardin JD, Cheng LY. 1986. The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation. Dev Biol 115:490-501.
28. 2. J Cell Biol 111:237a.
29. Harkey MA, Whiteley HR, Whiteley AH. 1992. Differential expression of the msp130 gene among skeletal lineage cells in the sea urchin embryo: a three dimensional in situ hybridization analysis. Mech Dev 37:173-184.
30. Harlow E, Lane D. 1988. Antibodies: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Press.
31. Ip YT, Park RE, Kosman D, Yazdanbakhsh K, Levine M. 1992. dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev 6:1518-1530.
32. Isaac A, Sargent MG, Cooke J. 1997. Control of vertebrate left-right asymmetry by a snail-related zinc finger gene. Science 275:1301-1304.
33. Ishimoda-Takagi T, Chino I, Sato H. 1984. Evidence for the involvement of muscle tropomyosin in the contractile elements of the coelom-esophagus complex in sea urchin embryos. Dev Biol 105:365-376.
34. Kanoh K, Aizu G, Katow H. 2001. Disappearance of an epithelial cell surface-specific glycoprotein (Epith-1) associated with epithelial-mesenchymal conversion in sea urchin embryogenesis. Dev Growth Differ 43:83-95.
35. Katow H, Yaguchi S, Kiyomoto M, Washio M. 2004. The 5-HT receptor cell is a new member of secondary mesenchyme cell descendants and forms a major blastocoelar network in sea urchin larvae. Mech Dev 121:325-337.
36. Langeland JA, Tomsa JM, Jackman WR Jr, Kimmel CB. 1998. An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo. Dev Genes Evol 208:569-577.
37. Leptin M. 1991. twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev 5:1568-1576.
38. Mann RS, Carroll SB. 2002. Molecular mechanisms of selector gene function and evolution. Curr Opin Genet Dev 12: 592-600.
39. Manzanares M, Locascio A, Nieto MA. 2001. The increasing complexity of the Snail gene superfamily in metazoan evolution. Trends Genet 17:178-181.
40. Mayor R, Morgan R, Sargent MG. 1995. Induction of the prospective neural crest of Xenopus. Development 121:767-777.
41. McClay DR, Peterson RE, Range RC, Winter-Vann AM, Ferkowicz MJ. 2000. A micromere induction signal is activated by beta-catenin and acts through notch to initiate specification of secondary mesenchyme cells in the sea urchin embryo. Development 127:5113-5122.
42. Miller JR, McClay DR. 1997. Characterization of the role of cadherin in regulating cell adhesion during sea urchin development. Dev Biol 192:323-339.
43. Morales AV, Nieto MA. 2004. The Snail gene family during gastrulation. In: Stern CD, editor. Gastrulation: from cells to embryos. New York: Cold Spring Harbor Laboratory Press, p 631-641.
44. Nemer M. 1986. An altered series of ectodermal gene expressions accompanying the reversible suspension of differentiation in the zinc-animalized sea urchin embryo. Dev Biol 114:214-224.
45. Nieto MA. 2002. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3:155-166.
46. Nieto MA, Bennett MF, Sargent MG, Wilkinson DG. 1992. Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene. Development 116:227-237.
47. Nieto AM, Sargent MG, Wilkinson DG, Cooke J. 1994. Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264:835-839.
48. Nocente-McGrath C, McIsaac R, Ernst SG. 1991. Altered cell fate in LiCl-treated sea urchin embryos. Dev Biol 147:445-450.
49. Oda H, Tsukita S, Takeichi M. 1998. Dynamic behavior of the cadherin-based cell-cell adhesion system during Drosophila gastrulation. Dev Biol 203:435-450.
50. Oram KF, Gridley T. 2005. Mutations in snail family genes enhance craniosynostosis of Twist1 haplo-insufficient mice: implications for Saethre-Chotzen Syndrome. Genetics 170:971-974.
51. Pearson JC, Lemons D, McGinnis W. 2005. Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6:893-904.
52. Peterson RE, McClay DR. 2005. A Fringe-modified Notch signal affects specification of mesoderm and endoderm in the sea urchin embryo. Dev Biol 282:126-137.
53. Ransick A, Ernst S, Britten RJ, Davidson EH. 1993. Whole mount in situ hybridization shows Endo 16 to be a marker for the vegetal plate territory in sea urchin embryos. Mech Dev 42:117-124.
54. Ruffins SW, Ettensohn CA. 1993. A clonal analysis of secondary mesenchyme cell fates in the sea urchin embryo. Dev Biol 160:285-288.
55. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning. A laboratory manual. Cold Spring Harbor: Cold Spring Harbor Press.
56. Sanger F, Nicklen S, Coulson AR. 1977. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74: 5463-5467.
57. Sargent MG, Bennett MF. 1990. Identification in Xenopus of a structural homologue of the Drosophila gene snail. Development 109:967-973.
58. Sefton M, Sanchez S, Nieto MA. 1998. Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 125:3111-3121.
59. Sherwood DR, McClay DR. 1999. LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development 126:1703-1713.
60. Smith DE, Franco del Amo F, Gridley T. 1992. Isolation of Sna, a mouse gene homologous to the Drosophila genes snail and escargot: its expression pattern suggests multiple roles during postimplantation development [published erratum appears in Development 1993 Mar; 117(3):preceding table of contents]. Development 116:1033-1039.
61. Sommer RJ, Retzlaff M, Goerlich K, Sander K, Tautz D. 1992. Evolutionary conservation pattern of zinc-finger domains of Drosophila segmentation genes. Proc Natl Acad Sci U S A 89:10782-10786.
62. Sommer RJ, Tautz D. 1994. Expression patterns of twist and snail in Tribolium (Coleoptera) suggest a homologous formation of mesoderm in long and short germ band insects. Dev Gen 15:32-37.
63. Sweet HC, Hodor PG, Ettensohn CA. 1999. The role of micromere signaling in Notch activation and mesoderm specification during sea urchin embryogenesis. Development 126:5255-5265.
64. Sweet HC, Gehring M, Ettensohn CA. 2002. LvDelta is a mesoderm-inducing signal in the sea urchin embryo and can endow blastomeres with organizer-like properties. Development 129:1945-1955.
65. Takata H, Kominami T. 2004. Pigment cells trigger the onset of gastrulation in tropical sea urchin Echinometra mathaei. Dev Growth Differ 46:23-35.
66. Tamboline CR, Burke RD. 1992. Secondary mesenchyme cells of the sea urchin embryo: ontogeny of blastocoelar cells. J Exp Zool 262:51-60.
67. Thisse C, Thisse B, Schilling TF, Postlethwait JH. 1993. Structure of the zebrafish snaill gene and its expression in wildtype, spadetail and no tail mutant embryos. Development 119:1203-1215.
68. Thisse C, Thisse B, Postlethwait JH. 1995. Expression of snail2, a second member of the zebrafish snail family, in cephalic mesendoderm and presumptive neural crest of wild-type and spadetail mutant embryos. Dev Biol 172:86-99.
69. Venuti JM, Gan L, Kozlowski MT, Klein WH. 1993. Developmental potential of muscle cell progenitors and the myogenic factor SUM-1 in the sea urchin embryo. Mech Dev 41:3-14.
70. Wada S, Saiga H. 1999. Cloning and embryonic expression of Hrsna, a snail family gene of the ascidian Halocynthia roretzi: implication in the origins of mechanisms for mesoderm specification and body axis formation in chordates. Dev Growth Differ 41:9-18.
71. Wessel GM, MeClay DR. 1987. Gastrulation in the sea urchin embryo requires the deposition of crosslinked collagen within the extracellular matrix. Dev Biol 121:149-165.
72. Wessel GM, Zhang W, Klein WH. 1990. Myosin heavy chain accumulates in dissimilar cell types of the macromere lineage in the sea urchin embryo. Dev Biol 140:447-454.
73. Whiteley M, Noguchi PD, Sensabaugh SM, Odenwald WF, Kassis JA. 1992. The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes. Mech Dev 36:117-127.
74. Wolpert L, Gustafson T. 1961. Studies on the cellular basis of morphogenesis in the sea urchin embryo. Gastrulation in vegetalized larvae. Exp Cell Res 22:437-449.
75. Wray GA, Lowe CJ. 2000. Developmental regulatory genes and echinoderm evolution. Syst Biol 49:28-51.
76. Wray GA, Levinton JS, Shapiro LH. 1996. Molecular evidence for deep precambrian divergences among metazoan phyla. Science 274:568-573.