Morphogenesis in sea urchin embryos: Linking cellular events to gene regulatory network states

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 1, Issue 2, 2012, Pages 231-252

  Lyons, Deirdre C ^a   Kaltenbach, Stacy L ^a   Mcclay, David R ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CADHERIN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; GOOSECOID PROTEIN; LAMININ; LYMPHOID ENHANCER FACTOR 1; MSP130 PROTEIN; NOTCH RECEPTOR; PEPTIDES AND PROTEINS; PROTEIN NODAL; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR DRI; TRANSCRIPTION FACTOR ERG; TRANSCRIPTION FACTOR ETV6; TRANSCRIPTION FACTOR FOXB; TRANSCRIPTION FACTOR FOXN2; TRANSCRIPTION FACTOR FOXN3; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR HESC; TRANSCRIPTION FACTOR HEX; TRANSCRIPTION FACTOR PMAR1; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TGIF; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN RECEPTOR; WNT PROTEIN;

ARTICLE; BONE DEVELOPMENT; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; ECTODERM; EMBRYO PATTERN FORMATION; ENDOCYTOSIS; ENDODERM; EXTRACELLULAR MATRIX; FILOPODIUM; GASTRULATION; GENE REGULATORY NETWORK; GENOTYPE; MESENCHYME CELL; MORPHOGENESIS; NONHUMAN; PROTEIN EXPRESSION; SEA URCHIN; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINEAGE; GENE REGULATORY NETWORKS; OSTEOGENESIS; SEA URCHINS; STEM CELLS;

EID: 84868116085     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.18     Document Type: Article

References (101)

1. Ettensohn C, Wessel G, Wray GA. Development of Sea Urchins, Ascidians, and Other Invertebrate Deuterostomes: Experimental Approaches, vol 74. San Diego, CA: Elsevier, Academic Press; 2004.
2. Driesch H. Entwicklungsmechanische Studien. I. Der Werth der beiden ersten Furchungszellen in der Echinodermenentwickelung. Zeitschr Wiss Zool 1891, 53:160-182.
3. Boveri T. Uber mehrpolige mitosen als mittel zur analyse des zellkerns. Verh d phys-med Ges Wursburg N F 1902, 35:67-90.
4. Boveri T. Zwei Fehlerquellen bei Merogoniegversuchen und die Entwicklungsfähigkeit merogonischer partiellmerogonischer Seeigelbastarde. Arch Entwicklungsmech Org 1918, 44:417-471.
5. Horstadius S. The mechanics of sea urchin development as studied by operative methods. Biol Rev 1939, 14:132-179.
6. Rapaport R. Experiments concerning the cleavage stimulus in sand dollar eggs. J Exp Zool 1961, 148:81-89.
7. Davidson E. The Regulatory Genome. Gene Regulatory Networks in Development and Evolution. San Diego: Academic Press; 2006.
8. Oliveri P, Tu Q, Davidson EH. Global regulatory logic for specification of an embryonic cell lineage. Proc Natl Acad Sci U S A 2008, 105:5955-5962.
9. Peter IS, Davidson EH. The endoderm gene regulatory network in sea urchin embryos up to mid-blastula stage. Dev Biol 2010, 340:188-199.
10. Davidson EH. Emerging properties of animal gene regulatory networks. Nature 2010, 468:911-920.
11. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T, et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 2008, 26:317-325.
12. Materna SC, Nam J, Davidson EH. High accuracy, high-resolution prevalence measurement for the majority of locally expressed regulatory genes in early sea urchin development. Gene Expr Patterns 2010, 10:177-184.
13. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, et al. A genomic regulatory network for development. Science 2002, 295:1669-1678.
14. Nam J, Dong P, Tarpine R, Istrail S, Davidson EH. Functional cis-regulatory genomics for systems biology. Proc Natl Acad Sci U S A 2010, 107:3930-3935.
15. Davidson EH. Network design principles from the sea urchin embryo. Curr Opin Genet Dev 2009, 19:535-540.
16. Ettensohn CA. Lessons from a gene regulatory network: echinoderm skeletogenesis provides insights into evolution, plasticity and morphogenesis. Development 2009, 136:11-21.
17. Gao F, Davidson EH. Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution. Proc Natl Acad Sci U S A 2008, 105:6091-6096.
18. Hinman VF, Yankura KA, McCauley BS. Evolution of gene regulatory network architectures: examples of subcircuit conservation and plasticity between classes of echinoderms. Biochim Biophys Acta 2009, 1789:326-332.
19. Angerer LM, Angerer RC. Patterning the sea urchin embryo: gene regulatory networks, signaling pathways, and cellular interactions. Curr Top Dev Biol 2003, 53:159-198.
20. Hörstadius S. Experimental Embryology of Echinoderms. Oxford: Clarendon Press; 1973.
21. Logan CY, McClay DR. The allocation of early blastomeres to the ectoderm and endoderm is variable in the sea urchin embryo. Development 1997, 124:2213-2223.
22. Yajima M, Wessel GM. Small micromeres contribute to the germline in the sea urchin. Development 2011, 138:237-243.
23. Duboc V, Lepage T. A conserved role for the nodal signaling pathway in the establishment of dorso-ventral and left-right axes in deuterostomes. J Exp Zool B Mol Dev Evol 2008, 310:41-53.
24. Lapraz F, Besnardeau L, Lepage T. Patterning of the dorsal-ventral axis in echinoderms: insights into the evolution of the BMP-chordin signaling network. PLoS Biol 2009, 7:e1000248.
25. Yamashita M. Embryonic development of the brittle-star Amphipholis kochii in laboratory culture. Biol Bull 1985, 169:131-142.
26. Yajima M. A switch in the cellular basis of skeletogenesis in late-stage sea urchin larvae. Dev Biol 2007, 307:272-281.
27. Logan CY, Miller JR, Ferkowicz MJ, McClay DR. Nuclear β-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development 1999, 126:345-357.
28. Wikramanayake AH, Huang L, Klein WH. β-Catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo. Proc Natl Acad Sci U S A 1998, 95:9343-9348.
29. Okazaki K. Spicule formation by isolated micromeres of the sea urchin embryo. Amer Zool 1975, 15:567-581.
30. Revilla-i-Domingo R, Oliveri P, Davidson EH. A missing link in the sea urchin embryo gene regulatory network: hesC and the double-negative specification of micromeres. Proc Natl Acad Sci U S A 2007, 104:12383-12388.
31. Sharma T, Ettensohn CA. Activation of the skeletogenic gene regulatory network in the early sea urchin embryo. Development 2010, 137:1149-1157.
32. Ransick A, Davidson EH. Micromeres are required for normal vegetal plate specification in sea urchin embryos. Development 1995, 121:3215-3222.
33. Sethi AJ, Angerer RC, Angerer LM. Gene regulatory network interactions in sea urchin endomesoderm induction. PLoS Biol 2009, 7:248-264.
34. Smith J, Davidson EH. Gene regulatory network subcircuit controlling a dynamic spatial pattern of signaling in the sea urchin embryo. Proc Natl Acad Sci U S A 2008, 105:20089-20094.
35. Wikramanayake AH, Peterson R, Chen J, Huang L, Bince JM, McClay DR, Klein WH. Nuclear β-catenin-dependent Wnt8 signaling in vegetal cells of the early sea urchin embryo regulates gastrulation and differentiation of endoderm and mesodermal cell lineages. Genesis 2004, 39:194-205.
36. Sherwood DR, McClay DR. Identification and localization of a sea urchin Notch homologue: insights into vegetal plate regionalization and Notch receptor regulation. Development 1997, 124:3363-3374.
37. Sherwood DR, McClay DR. LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development 1999, 126:1703-1713.
38. Sweet HC, Gehring M, Ettensohn CA. LvDelta is a mesoderm-inducing signal in the sea urchin embryo and can endow blastomeres with organizer-like properties. Development 2002, 129:1945-1955.
39. Magie CR, Martindale MQ. Cell-cell adhesion in the cnidaria: insights into the evolution of tissue morphogenesis. Biol Bull 2008, 214:218-232.
40. Micalizzi D, Farabaugh S, Ford H. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Neoplasia 2010, 15:117-134.
41. Schock F, Perrimon N. Molecular mechanisms of epithelial morphogenesis. Annu Rev Cell Dev Biol 2002, 18:463-493.
42. Oliveri P, Davidson EH, McClay DR. Activation of pmar1 controls specification of micromeres in the sea urchin embryo. Dev Biol 2003, 258:32-43.
43. Oliveri P, Carrick DM, Davidson EH. A regulatory gene network that directs micromere specification in the sea urchin embryo. Dev Biol 2002, 246:209-228.
44. Wu SY, Yang YP, McClay DR. Twist is an essential regulator of the skeletogenic gene regulatory network in the sea urchin embryo. Dev Biol 2008, 319:406-415.
45. Wu SY, McClay DR. The Snail repressor is required for PMC ingression in the sea urchin embryo. Development 2007, 134:1061-1070.
46. Rho HK, McClay DR. The control of foxN2/3 expression in sea urchin embryos and its function in the skeletogenic gene regulatory network. Development 2011, 138:937-945.
47. Davidson EH, Levine MS. Properties of developmental gene regulatory networks. Proc Natl Acad Sci U S A 2008, 105:20063-20066.
48. Smith J, Davidson EH. Regulative recovery in the sea urchin embryo and the stabilizing role of fail-safe gene network wiring. Proc Natl Acad Sci U S A 2009, 106:18291-18296.
49. Katow H, Solursh M. Ultrastructural and time-lapse studies of primary mesenchyme cell behavior in normal and sulfate-deprived sea urchin embryos. Exp Cell Res 1981, 136:233-245.
50. Miller JR, McClay DR. Characterization of the role of cadherin in regulating cell adhesion during sea urchin development. Dev Biol 1997, 192:323-339.
51. Peterson RE, McClay DR. Primary mesenchyme cell patterning during the early stages following ingression. Dev Biol 2003, 254:68-78.
52. Fink RD, McClay DR. Three cell recognition changes accompany the ingression of sea urchin primary mesenchyme cells. Dev Biol 1985, 107:66-74.
53. Hertzler PL, McClay DR. αSU2, an epithelial integrin that binds laminin in the sea urchin embryo. Dev Biol 1999, 207:1-13.
54. Miller JR, McClay DR. Changes in the pattern of adherens junction-associated β-catenin accompany morphogenesis in the sea urchin embryo. Dev Biol 1997, 192:310-322.
55. Leaf DS, Anstrom JA, Chin JE, Harkey MA, Raff RA. A sea urchin primary mesenchyme cell surface protein, msp130, defined by cDNA probes and antibody to fusion protein. Dev Biol 1987, 121:29-40.
56. Duloquin L, Lhomond G, Gache C. Localized VEGF signaling from ectoderm to mesenchyme cells controls morphogenesis of the sea urchin embryo skeleton. Development 2007, 134:2293-2302.
57. Anstrom JA. Microfilaments, cell shape changes, and the formation of primary mesenchyme in sea urchin embryos. J Exp Zool 1992, 264:312-322.
58. Anstrom JA. Sea urchin primary mesenchyme cells: ingression occurs independent of microtubules. Dev Biol 1989, 131:269-275.
59. Quigley JP, Braithwaite RS, Armstrong PB. Matrix metalloproteases of the developing sea urchin embryo. Differentiation 1993, 54:19-23.
60. Rise M, Burke RD. SpADAM, a sea urchin ADAM, has conserved structure and expression. Mech Dev 2002, 117:275-281.
61. Miller J, Fraser SE, McClay D. Dynamics of thin filopodia during sea urchin gastrulation. Development 1995, 121:2501-2511.
62. Malinda KM, Fisher GW, Ettensohn CA. Four-dimensional microscopic analysis of the filopodial behavior of primary mesenchyme cells during gastrulation in the sea urchin embryo. Dev Biol 1995, 172:552-566.
63. Malinda KM, Ettensohn CA. Primary mesenchyme cell migration in the sea urchin embryo: distribution of directional cues. Dev Biol 1994, 164:562-578.
64. McClay DR. The role of thin filopodia in motility and morphogenesis. Exp Cell Res 1999, 253:296-301.
65. Hodor PG, Ettensohn CA. The dynamics and regulation of mesenchymal cell fusion in the sea urchin embryo. Dev Biol 1998, 199:111-124.
66. Wilt FH. Biomineralization of the spicules of sea urchin embryos. Zoolog Sci 2002, 19:253-261.
67. Hardin J, Coffman JA, Black SD, McClay DR. Commitment along the dorsoventral axis of the sea urchin embryo is altered in response to NiCl2. Development 1992, 116:671-685.
68. Armstrong N, McClay DR. Skeletal pattern is specified autonomously by the primary mesenchyme cells in sea urchin embryos. Dev Biol 1994, 162:329-338.
69. Duboc V, Rottinger E, Besnardeau L, Lepage T. Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev Cell 2004, 6:397-410.
70. Armstrong N, Hardin J, McClay DR. Cell-cell interactions regulate skeleton formation in the sea urchin embryo. Development 1993, 119:833-840.
71. McClay DR, Armstrong NA, Hardin J. Pattern formation during gastrulation in the sea urchin embryo. Dev Suppl 1992, 33-41.
72. Wilt FH, Killian CE, Hamilton P, Croker L. The dynamics of secretion during sea urchin embryonic skeleton formation. Exp Cell Res 2008, 314:1744-1752.
73. Wilt FH. Developmental biology meets materials science: morphogenesis of biomineralized structures. Dev Biol 2005, 280:15-25.
74. Killian CE, Wilt FH. Molecular aspects of biomineralization of the echinoderm endoskeleton. Chem Rev 2008, 108:4463-4474.
75. Anstrom JA, Chin JE, Leaf DS, Parks AL, Raff RA. Localization and expression of msp130, a primary mesenchyme lineage-specific cell surface protein in the sea urchin embryo. Development 1987, 101:255-265.
76. Wessel GM, McClay DR. Sequential expression of germ-layer specific molecules in the sea urchin embryo. Dev Biol 1985, 111:451-463.
77. Benson S, Sucov H, Stephens L, Davidson E, Wilt F. A lineage-specific gene encoding a major matrix protein of the sea urchin embryo spicule. I. Authentication of the cloned gene and its developmental expression. Dev Biol 1987, 120:499-506.
78. Rottinger E, Saudemont A, Duboc V, Besnardeau L, McClay D, Lepage T. FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis [corrected] and regulate gastrulation during sea urchin development. Development 2008, 135:353-365.
79. Livingston BT, Killian CE, Wilt F, Cameron A, Landrum MJ, Ermolaeva O, Sapojnikov V, Maglott DR, Buchanan AM, Ettensohn CA. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Dev Biol 2006, 300:335-348.
80. Illies MR, Peeler MT, Dechtiaruk AM, Ettensohn CA. Identification and developmental expression of new biomineralization proteins in the sea urchin Strongylocentrotus purpuratus. Dev Genes Evol 2002, 212:419-431.
81. Kominami T, Takata H. Gastrulation in the sea urchin embryo: a model system for analyzing the morphogenesis of a monolayered epithelium. Dev Growth Differ 2004, 46:309-326.
82. Cole AG, Rizzo F, Martinez P, Fernandez-Serra M, Arnone MI. Two ParaHox genes, SpLox and SpCdx, interact to partition the posterior endoderm in the formation of a functional gut. Development 2009, 136:541-549.
83. Ettensohn CA. Mechanisms of epithelial invagination. Quart Rev Biol 1984, 60:289-307.
84. Kimberly EL, Hardin J. Bottle cells are required for the initiation of primary invagination in the sea urchin embryo. Dev Biol 1998, 204:235-250.
85. Nakajima Y, Burke RD. The initial phase of gastrulation in sea urchins is accompanied by the formation of bottle cells. Dev Biol 1996, 179:436-446.
86. Sawyer JM, Harrell JR, Shemer G, Sullivan-Brown J, Roh-Johnson M, Goldstein B. Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 2010, 341:5-19.
87. Lane MC, Koehl MA, Wilt F, Keller R. A role for regulated secretion of apical extracellular matrix during epithelial invagination in the sea urchin. Development 1993, 117:1049-1060.
88. Davidson LA, Koehl MA, Keller R, Oster GF. How do sea urchins invaginate? Using biomechanics to distinguish between mechanisms of primary invagination. Development 1995, 121:2005-2018.
89. Davidson LA, Oster GF, Keller RE, Koehl MA. Measurements of mechanical properties of the blastula wall reveal which hypothesized mechanisms of primary invagination are physically plausible in the sea urchin Strongylocentrotus purpuratus. Dev Biol 1999, 209:221-238.
90. Takata H, Kominami T. Pigment cells trigger the onset of gastrulation in tropical sea urchin Echinometra mathaei. Dev Growth Differ 2004, 46:23-35.
91. Croce J, Duloquin L, Lhomond G, McClay DR, Gache C. Frizzled5/8 is required in secondary mesenchyme cells to initiate archenteron invagination during sea urchin development. Development 2006, 133:547-557.
92. Beane WS, Gross JM, McClay DR. RhoA regulates initiation of invagination, but not convergent extension, during sea urchin gastrulation. Dev Biol 2006, 292:213-225.
93. Ettensohn CA. Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells. Dev Biol 1985, 112:383-390.
94. Hardin J. Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation. Dev Biol 1989, 136:430-445.
95. Hardin JD, Cheng LY. The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation. Dev Biol 1986, 115:490-501.
96. Hardin J, McClay DR. Target recognition by the archenteron during sea urchin gastrulation. Dev Biol 1990, 142:86-102.
97. Hardin J, Morrill J, McClay D. Mechanisms of filopodial guidance during sea urchin gastrulation. J. Cell Biol 1988, 107:814a.
98. Martins GG, Summers RG, Morrill JB. Cells are added to the archenteron during and following secondary invagination in the sea urchin Lytechinus variegatus. Dev Biol 1998, 198:330-342.
99. Piston DW, Summers RG, Knobel SM, Morrill JB. Characterization of involution during sea urchin gastrulation using two-photon excited photorelease and confocal microscopy. Microsc Microanal 1998, 4:404-414.
100. Su YH, Li E, Geiss GK, Longabaugh WJ, Kramer A, Davidson EH. A perturbation model of the gene regulatory network for oral and aboral ectoderm specification in the sea urchin embryo. Dev Biol 2009, 329:410-421.
101. Duboc V, Lapraz F, Saudemont A, Bessodes N, Mekpoh F, Haillot E, Quirin M, Lepage T. Nodal and BMP2/4 pattern the mesoderm and endoderm during development of the sea urchin embryo. Development 2010, 137:223-235.