Ventralization of an indirect developing hemichordate by NiCl2 suggests a conserved mechanism of dorso-ventral (D/V) patterning in Ambulacraria (hemichordates and echinoderms)

Developmental Biology

Volumn 354, Issue 1, 2011, Pages 173-190

  Rottinger E ^a   Martindale, M Q ^a  

^a UNIVERSITY OF HAWAII   (United States)

Author keywords

Dorso ventral patterning; Enteropneust; Hemichordate; Indirect development; Nickel chloride (NiCl2)

Indexed keywords

NICKEL CHLORIDE;

AMBULACRARIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DORSO VENTRAL PATTERNING; ECHINODERM; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GASTRULATION; GERM LAYER; HEMICHORDATA; LARVA; MOUTH; NONHUMAN; PRIORITY JOURNAL; SACCOGLOSSUS KOWALEVSKII;

CHORDATA; DEUTEROSTOMIA; ECHINODERMATA; ECHINOIDA; ECHINOIDEA; HEMICHORDATA; PTYCHODERA FLAVA; SACCOGLOSSUS KOWALEVSKII;

EID: 79955501273     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.03.030     Document Type: Article

References (144)

1. Agca C., Klein W.H., Venuti J.M. Respecification of ectoderm and altered Nodal expression in sea urchin embryos after cobalt and nickel treatment. Mech. Dev. 2009, 126:430-442.
2. Angerer L.M., Angerer R.C. Animal-vegetal axis patterning mechanisms in the early sea urchin embryo. Dev. Biol. 2000, 218:1-12.
3. Angerer L.M., Oleksyn D.W., Logan C.Y., McClay D.R., Dale L., Angerer R.C. A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. Development 2000, 127:1105-1114.
4. Arendt D., Nubler-Jung K. Inversion of dorsoventral axis?. Nature 1994, 371:26.
5. Bateson W. The early stages in the development of Balanoglossus. Q. J. Microsc. Sci. 1884, 24:208-236.
6. Bateson W. Continued account of the later stages in the development of Balanoglossus kowalevskii and of the morphology of the enteropneusta. Q. J. Microsc. Sci. 1886, 26:511-534.
7. Bateson W. The ancestry of the chordata. Q. J. Microsc. Sci. 1886, 26:535-571.
8. Benito-Gutierrez E., Arendt D. CNS evolution: new insight from the mud. Curr. Biol. 2009, 19:R640-R642.
9. Bertrand S., Somorjai I., Garcia-Fernandez J., Lamonerie T., Escriva H. FGFRL1 is a neglected putative actor of the FGF signalling pathway present in all major metazoan phyla. BMC Evol. Biol. 2009, 9:226.
10. Bourlat S.J., Nielsen C., Lockyer A.E., Littlewood D.T., Telford M.J. Xenoturbella is a deuterostome that eats molluscs. Nature 2003, 424:925-928.
11. Bourlat S.J., Juliusdottir T., Lowe C.J., Freeman R., Aronowicz J., Kirschner M., Lander E.S., Thorndyke M., Nakano H., Kohn A.B., Heyland A., Moroz L.L., Copley R.R., Telford M.J. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 2006, 444:85-88.
12. Bradham C.A., Oikonomou C., Kuhn A., Core A.B., Modell J.W., McClay D.R., Poustka A.J. Chordin is required for neural but not axial development in sea urchin embryos. Dev. Biol. 2009, 328:221-233.
13. Bradley L., Wainstock D., Sive H. Positive and negative signals modulate formation of the Xenopus cement gland. Development 1996, 122:2739-2750.
14. Calabrese A., MacInnes J.R., Nelson D.A., Miller J.E. Survival and growth of bivalve larvae under heavy-metal stress. Mar. Biol. 1977, 41:179-184.
15. Cameron R.A., Hough-Evans B.R., Britten R.J., Davidson E.H. Lineage and fate of each blastomere of the eight-cell sea urchin embryo. Genes Dev. 1987, 1:75-85.
16. Cameron C.B., Garey J.R., Swalla B.J. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4469-4474.
17. Cannon J.T., Rychel A.L., Eccleston H., Halanych K.M., Swalla B.J. Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts. Mol. Phylogenet. Evol. 2009, 52:17-24.
18. Cebria F., Kobayashi C., Umesono Y., Nakazawa M., Mineta K., Ikeo K., Gojobori T., Itoh M., Taira M., Sanchez Alvarado A., Agata K. FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 2002, 419:620-624.
19. Child C.M. Formation and reduction of indophenol blue in development of an echinoderm. Proc. Natl. Acad. Sci. U. S. A. 1941, 27:523-528.
20. Clary J.J. Nickel chloride induced metabolic changes in the rat and guinea pig. Toxicol. Appl. Pharmacol. 1975, 31:55-56.
21. Coffman J.A., Davidson E.H. Oral-aboral axis specification in the sea urchin embryo. I. Axis entrainment by respiratory asymmetry. Dev. Biol. 2001, 230:18-28.
22. Coffman J.A., Denegre J.M. Mitochondria, redox signaling and axis specification in metazoan embryos. Dev. Biol. 2007, 308:266-280.
23. Coffman J.A., Coluccio A., Planchart A., Robertson A.J. Oral-aboral axis specification in the sea urchin embryo III. Role of mitochondrial redox signaling via H2O2. Dev. Biol. 2009, 330:123-130.
24. Colwin A.C.A. The normal embryology of Saccoglossus kowalevskii (Enteropneusta). J. Morphol. 1953, 92:401-453.
25. Croce J., Lhomond G., Gache C. Expression pattern of Brachyury in the embryo of the sea urchin Paracentrotus lividus. Dev. Genes Evol. 2001, 211:617-619.
26. Croce J., Duloquin L., Lhomond G., McClay D.R., Gache C. Frizzled5/8 is required in secondary mesenchyme cells to initiate archenteron invagination during sea urchin development. Development 2006, 133:547-557.
27. Czihak G., Meyer G.F. Differentiation of the oral field of the sea urchin embryo. Nature 1964, 201:315.
28. Davidson E.H., Rast J.P., Oliveri P., Ransick A., Calestani C., Yuh C.H., Minokawa T., Amore G., Hinman V., Arenas-Mena C., Otim O., Brown C.T., Livi C.B., Lee P.Y., Revilla R., Rust A.G., Pan Z., Schilstra M.J., Clarke P.J., Arnone M.I., Rowen L., Cameron R.A., McClay D.R., Hood L., Bolouri H. A genomic regulatory network for development. Science 2002, 295:1669-1678.
29. Davidson E.H., Rast J.P., Oliveri P., Ransick A., Calestani C., Yuh C.H., Minokawa T., Amore G., Hinman V., Arenas-Mena C., Otim O., Brown C.T., Livi C.B., Lee P.Y., Revilla R., Schilstra M.J., Clarke P.J., Rust A.G., Pan Z., Arnone M.I., Rowen L., Cameron R.A., McClay D.R., Hood L., Bolouri H. A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Dev. Biol. 2002, 246:162-190.
30. De Robertis E.M., Sasai Y. A common plan for dorsoventral patterning in Bilateria. Nature 1996, 380:37-40.
31. Di Bernardo M., Castagnetti S., Bellomonte D., Oliveri P., Melfi R., Palla F., Spinelli G. Spatially restricted expression of PlOtp, a Paracentrotus lividus orthopedia-related homeobox gene, is correlated with oral ectodermal patterning and skeletal morphogenesis in late-cleavage sea urchin embryos. Development 1999, 126:2171-2179.
32. Doll R. Cancer of the lung and nose in nickel workers. Br. J. Ind. Med. 1958, 15:217-223.
33. Doll R., Morgan L.G., Speizer F.E. Cancers of the lung and nasal sinuses in nickel workers. Br. J. Cancer 1970, 24:623-632.
34. 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.
35. Duboc V., Rottinger E., Lapraz F., Besnardeau L., Lepage T. Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev. Cell 2005, 9:147-158.
36. Dunn C.W., Hejnol A., Matus D.Q., Pang K., Browne W.E., Smith S.A., Seaver E., Rouse G.W., Obst M., Edgecombe G.D., Sorensen M.V., Haddock S.H., Schmidt-Rhaesa A., Okusu A., Kristensen R.M., Wheeler W.C., Martindale M.Q., Giribet G. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749.
37. Emlet R.B. Larval spicules, cilia, and symmetry as remnants of indirect development in the direct developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 1995, 167:405-415.
38. Ettensohn C.A., Sweet H.C. Patterning the early sea urchin embryo. Curr. Top. Dev. Biol. 2000, 50:1-44.
39. Finnerty J.R., Pang K., Burton P., Paulson D., Martindale M.Q. Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 2004, 304:1335-1337.
40. Flowers V.L., Courteau G.R., Poustka A.J., Weng W., Venuti J.M. Nodal/activin signaling establishes oral-aboral polarity in the early sea urchin embryo. Dev. Dyn. 2004, 231:727-740.
41. Freeman R.M., Wu M., Cordonnier-Pratt M.M., Pratt L.H., Gruber C.E., Smith M., Lander E.S., Stange-Thomann N., Lowe C.J., Gerhart J., Kirschner M. cDNA sequences for transcription factors and signaling proteins of the hemichordate Saccoglossus kowalevskii: efficacy of the expressed sequence tag (EST) approach for evolutionary and developmental studies of a new organism. Biol. Bull. 2008, 214:284-302.
42. Gerhart J. Inversion of the chordate body axis: are there alternatives?. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4445-4448.
43. Gross J.M., McClay D.R. The role of Brachyury (T) during gastrulation movements in the sea urchin Lytechinus variegatus. Dev. Biol. 2001, 239:132-147.
44. Hadfield M. Reproduction of Marine Invertebrates 1975, Academic Press, New York.
45. Hamada H., Meno C., Watanabe D., Saijoh Y. Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 2002, 3:103-113.
46. Harada Y., Yasuo H., Satoh N. A sea urchin homologue of the chordate Brachyury (T) gene is expressed in the secondary mesenchyme founder cells. Development 1995, 121:2747-2754.
47. Harada Y., Akasaka K., Shimada H., Peterson K.J., Davidson E.H., Satoh N. Spatial expression of a forkhead homologue in the sea urchin embryo. Mech. Dev. 1996, 60:163-173.
48. Harada Y., Okai N., Taguchi S., Tagawa K., Humphreys T., Satoh N. Developmental expression of the hemichordate otx ortholog. Mech. Dev. 2000, 91:337-339.
49. Harada Y., Okai N., Taguchi S., Shoguchi E., Tagawa K., Humphreys T., Satoh N. Embryonic expression of a hemichordate distal-less gene. Zoolog. Sci. 2001, 18:57-61.
50. Harada Y., Shoguchi E., Taguchi S., Okai N., Humphreys T., Tagawa K., Satoh N. Conserved expression pattern of BMP-2/4 in hemichordate acorn worm and echinoderm sea cucumber embryos. Zoolog. Sci. 2002, 19:1113-1121.
51. Hardin J., Coffman J.A., Black S.D., McClay D.R. Commitment along the dorsoventral axis of the sea urchin embryo is altered in response to NiCl2. Development 1992, 116:671-685.
52. Hartwig A. Zinc finger proteins as potential targets for toxic metal ions: differential effects on structure and function. Antioxid. Redox Signal. 2001, 3:625-634.
53. Hejnol A., Obst M., Stamatakis A., Ott M., Rouse G.W., Edgecombe G.D., Martinez P., Baguna J., Bailly X., Jondelius U., Wiens M., Muller W.E., Seaver E., Wheeler W.C., Martindale M.Q., Giribet G., Dunn C.W. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. Biol. Sci. 2009, 276:4261-4270.
54. Henry J.Q., Tagawa K., Martindale M.Q. Deuterostome evolution: early development in the enteropneust hemichordate, Ptychodera flava. Evol. Dev. 2001, 3:375-390.
55. Howard-Ashby M., Materna S.C., Brown C.T., Chen L., Cameron R.A., Davidson E.H. Identification and characterization of homeobox transcription factor genes in Strongylocentrotus purpuratus, and their expression in embryonic development. Dev. Biol. 2006, 300:74-89.
56. Huang Y., Ding X.Y. Ni2+ treatment causes cement gland formation in ectoderm explants of Xenopus laevis embryo. Cell Res. 1999, 9:71-76.
57. Huang H.C., Klein P.S. The Frizzled family: receptors for multiple signal transduction pathways. Genome Biol. 2004, 5:234.
58. Hunter J.G., Vergnano O. Trace element toxicities in oat plants. Ann. Appl. Biol. 1953, 40:761-777.
59. Jaffe L.F. Organization of early development by calcium patterns. Bioessays 1999, 21:657-667.
60. Kostich M., English J., Madison V., Gheyas F., Wang L., Qiu P., Greene J., Laz T.M. Human members of the eukaryotic protein kinase family. Genome Biol. 2002, 3. RESEARCH0043.
61. Kuhl M., Sheldahl L.C., Malbon C.C., Moon R.T. Ca(2+)/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 2000, 275:12701-12711.
62. Kumano G., Smith W.C. Revisions to the Xenopus gastrula fate map: implications for mesoderm induction and patterning. Dev. Dyn. 2002, 225:409-421.
63. Kume S., Inoue T., Mikoshiba K. Galphas family G proteins activate IP(3)-Ca(2+) signaling via gbetagamma and transduce ventralizing signals in Xenopus. Dev. Biol. 2000, 226:88-103.
64. Lacalli T.C. Dorsoventral axis inversion. Nature 1995, 373:110-111.
65. Lallier R. Research on embryonal determination in echinoderms; effect of oxidizing agents and p-chloromercuribenzoic acid on development of the egg of the sea urchin Paracentrotus lividus. Arch. Biol. (Liege) 1956, 67:181-209.
66. Lapraz F., Rottinger E., Duboc V., Range R., Duloquin L., Walton K., Wu S.Y., Bradham C., Loza M.A., Hibino T., Wilson K., Poustka A., McClay D., Angerer L., Gache C., Lepage T. RTK and TGF-beta signaling pathways genes in the sea urchin genome. Dev. Biol. 2006, 300:132-152.
67. 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.
68. Lee H.H., Frasch M. Survey of forkhead domain encoding genes in the Drosophila genome: classification and embryonic expression patterns. Dev. Dyn. 2004, 229:357-366.
69. Letunic I., Copley R.R., Pils B., Pinkert S., Schultz J., Bork P. SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 2006, 34:D257-D260.
70. Lieber M.J., Luckhart S. Transforming growth factor-betas and related gene products in mosquito vectors of human malaria parasites: signaling architecture for immunological crosstalk. Mol. Immunol. 2004, 41:965-977.
71. Logan C.Y., McClay D.R. The allocation of early blastomeres to the ectoderm and endoderm is variable in the sea urchin embryo. Development 1997, 124:2213-2223.
72. Lowe C.J., Wu M., Salic A., Evans L., Lander E., Stange-Thomann N., Gruber C.E., Gerhart J., Kirschner M. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 2003, 113:853-865.
73. Lowe C.J., Terasaki M., Wu M., Freeman R.M., Runft L., Kwan K., Haigo S., Aronowicz J., Lander E., Gruber C., Smith M., Kirschner M., Gerhart J. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol. 2006, 4:e291.
74. Lu C.C., Matsumoto N., Iijima S. Teratogenic effects of nickel chloride on embryonic mice and its transfer to embryonic mice. Teratology 1979, 19:137-142.
75. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
76. Matus D.Q., Thomsen G.H., Martindale M.Q. Dorso/ventral genes are asymmetrically expressed and involved in germ-layer demarcation during cnidarian gastrulation. Curr. Biol. 2006, 16:499-505.
77. McClay D.R. Specification of endoderm and mesoderm in the sea urchin. Zygote 2000, 8(Suppl 1):S41.
78. Minsuk S.B., Raff R.A. Co-option of an oral-aboral patterning mechanism to control left-right differentiation: the direct-developing sea urchin Heliocidaris erythrogramma is sinistralized, not ventralized, by NiCl2. Evol. Dev. 2005, 7:289-300.
79. Mlinar B., Enyeart J.J. Block of current through T-type calcium channels by trivalent metal cations and nickel in neural rat and human cells. J. Physiol. 1993, 469:639-652.
80. Momose T., Houliston E. Two oppositely localised frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol. 2007, 5:e70.
81. Morgan T.H. The growth and metamorphosis of Tornaria. J. Morphol. 1891, 5:407-458.
82. Morgan T.H. The development of Balanoglossus. J. Morphol. 1894, 9:1-86.
83. Morokuma J., Ueno M., Kawanishi H., Saiga H., Nishida H. HrNodal, the ascidian nodal-related gene, is expressed in the left side of the epidermis, and lies upstream of HrPitx. Dev. Genes Evol. 2002, 212:439-446.
84. Nagaoka M., Kuwahara J., Sugiura Y. Alteration of DNA binding specificity by nickel (II) substitution in three zinc (II) fingers of transcription factor Sp1. Biochem. Biophys. Res. Commun. 1993, 194:1515-1520.
85. Nam J., Su Y.H., Lee P.Y., Robertson A.J., Coffman J.A., Davidson E.H. Cis-regulatory control of the nodal gene, initiator of the sea urchin oral ectoderm gene network. Dev. Biol. 2007, 306:860-869.
86. Nielsen C., Hay-Schmidt A. Development of the enteropneust Ptychodera flava: ciliary bands and nervous system. J. Morphol. 2007, 268:551-570.
87. Nomaksteinsky M., Rottinger E., Dufour H.D., Chettouh Z., Lowe C.J., Martindale M.Q., Brunet J.F. Centralization of the deuterostome nervous system predates chordates. Curr. Biol. 2009, 19:1264-1269.
88. Okai N., Tagawa K., Humphreys T., Satoh N., Ogasawara M. Characterization of gill-specific genes of the acorn worm Ptychodera flava. Dev. Dyn. 2000, 217:309-319.
89. Oliveri P., Walton K.D., Davidson E.H., McClay D.R. Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 2006, 133:4173-4181.
90. Palma V., Kukuljan M., Mayor R. Calcium mediates dorsoventral patterning of mesoderm in Xenopus. Curr. Biol. 2001, 11:1606-1610.
91. Pang K., Martindale M.Q. Developmental expression of homeobox genes in the ctenophore Mnemiopsis leidyi. Dev. Genes Evol. 2008, 218:307-319.
92. Pease D.C. Echinoderm bilateral determination in chemical concentration gradients: I. J. Exp. Zool. 1941, 86:381-404.
93. Pease D.C. Echinoderm bilateral determination in chemical concentration gradients: II. J. Exp. Zool. 1942, 89:329-345.
94. Perseke M., Hankeln T., Weich B., Fritzsch G., Stadler P.F., Israelsson O., Bernhard D., Schlegel M. The mitochondrial DNA of Xenoturbella bocki: genomic architecture and phylogenetic analysis. Theory Biosci. 2007, 126:35-42.
95. Peterson K.J., Cameron R.A., Tagawa K., Satoh N., Davidson E.H. A comparative molecular approach to mesodermal patterning in basal deuterostomes: the expression pattern of Brachyury in the enteropneust hemichordate Ptychodera flava. Development 1999, 126:85-95.
96. Peterson K.J., Harada Y., Cameron R.A., Davidson E.H. Expression pattern of Brachyury and Not in the sea urchin: comparative implications for the origins of mesoderm in the basal deuterostomes. Dev. Biol. 1999, 207:419-431.
97. Philippe H., Brinkmann H., Martinez P., Riutort M., Baguna J. Acoel flatworms are not platyhelminthes: evidence from phylogenomics. PLoS One 2007, 2:e717.
98. Poustka A.J., Kuhn A., Radosavljevic V., Wellenreuther R., Lehrach H., Panopoulou G. On the origin of the chordate central nervous system: expression of onecut in the sea urchin embryo. Evol. Dev. 2004, 6:227-236.
99. Prodon F., Pruliere G., Chenevert J., Sardet C. Establishment and expression of embryonic axes: comparisons between different model organisms. Med. Sci. (Paris) 2004, 20:526-538.
100. Range R., Lapraz F., Quirin M., Marro S., Besnardeau L., Lepage T. Cis-regulatory analysis of nodal and maternal control of dorsal-ventral axis formation by Univin, a TGF-beta related to Vg1. Development 2007, 134:3649-3664.
101. Rast J.P., Cameron R.A., Poustka A.J., Davidson E.H. Brachyury target genes in the early sea urchin embryo isolated by differential macroarray screening. Dev. Biol. 2002, 246:191-208.
102. Rizzo F., Fernandez-Serra M., Squarzoni P., Archimandritis A., Arnone M.I. Identification and developmental expression of the ets gene family in the sea urchin (Strongylocentrotus purpuratus). Dev. Biol. 2006, 300:35-48.
103. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
104. 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.
105. Rulon O. The modification of developmental patterns in the sand dollar with nickelous chloride. Anat. Rec. 1953, 117:615.
106. Rychel A.L., Smith S.E., Shimamoto H.T., Swalla B.J. Evolution and development of the chordates: collagen and pharyngeal cartilage. Mol. Biol. Evol. 2006, 23:541-549.
107. Salnikow K., Costa M. Epigenetic mechanisms of nickel carcinogenesis. J. Environ. Pathol. Toxicol. Oncol. 2000, 19:307-318.
108. Salnikow K., Zhitkovich A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic, and chromium. Chem. Res. Toxicol. 2008, 21:28-44.
109. Salnikow K., Blagosklonny M.V., Ryan H., Johnson R., Costa M. Carcinogenic nickel induces genes involved with hypoxic stress. Cancer Res. 2000, 60:38-41.
110. Salnikow K., Su W., Blagosklonny M.V., Costa M. Carcinogenic metals induce hypoxia-inducible factor-stimulated transcription by reactive oxygen species-independent mechanism. Cancer Res. 2000, 60:3375-3378.
111. Salnikow K., Davidson T., Kluz T., Chen H., Zhou D., Costa M. GeneChip analysis of signaling pathways effected by nickel. J. Environ. Monit. 2003, 5:206-209.
112. Salnikow K., Davidson T., Zhang Q., Chen L.C., Su W., Costa M. The involvement of hypoxia-inducible transcription factor-1-dependent pathway in nickel carcinogenesis. Cancer Res. 2003, 63:3524-3530.
113. Satoh H. Role of T-type Ca2+ channel inhibitors in the pacemaker depolarization in rabbit sino-atrial nodal cells. Gen. Pharmacol. 1995, 26:581-587.
114. Saudemont A., Haillot E., Mekpoh F., Bessodes N., Quirin M., Lapraz F., Duboc V., Rottinger E., Range R., Oisel A., Besnardeau L., Wincker P., Lepage T. Ancestral regulatory circuits governing ectoderm patterning downstream of Nodal and BMP2/4 revealed by gene regulatory network analysis in an echinoderm. PLoS Genet. 2010, 6:e1001259.
115. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:5857-5864.
116. Sherwood D.R., McClay D.R. Identification and localization of a sea urchin Notch homologue: insights into vegetal plate regionalization and Notch receptor regulation. Development 1997, 124:3363-3374.
117. Shoguchi E., Satoh N., Maruyama Y.K. Pattern of Brachyury gene expression in starfish embryos resembles that of hemichordate embryos but not of sea urchin embryos. Mech. Dev. 1999, 82:185-189.
118. Smith J., Davidson E.H. 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.
119. Smith M.S., Turner F.R., Raff R.A. Nodal expression and heterochrony in the evolution of dorsal-ventral and left-right axes formation in the direct-developing sea urchin Heliocidaris erythrogramma. J. Exp. Zool. B Mol. Dev. Evol. 2008, 310:609-622.
120. Sodergren E., Weinstock G.M., Davidson E.H., Cameron R.A., Gibbs R.A., Angerer R.C., Angerer L.M., Arnone M.I., Burgess D.R., Burke R.D., Coffman J.A., Dean M., Elphick M.R., Ettensohn C.A., Foltz K.R., Hamdoun A., Hynes R.O., Klein W.H., Marzluff W., McClay D.R., Morris R.L., Mushegian A., Rast J.P., Smith L.C., Thorndyke M.C., Vacquier V.D., Wessel G.M., Wray G., Zhang L., Elsik C.G., Ermolaeva O., Hlavina W., Hofmann G., Kitts P., Landrum M.J., Mackey A.J., Maglott D., Panopoulou G., Poustka A.J., Pruitt K., Sapojnikov V., Song X., Souvorov A., Solovyev V., Wei Z., Whittaker C.A., Worley K., Durbin K.J., Shen Y., Fedrigo O., Garfield D., Haygood R., Primus A., Satija R., Severson T., Gonzalez-Garay M.L., Jackson A.R., Milosavljevic A., Tong M., Killian C.E., Livingston B.T., Wilt F.H., Adams N., Belle R., Carbonneau S., Cheung R., Cormier P., Cosson B., Croce J., Fernandez-Guerra A., Geneviere A.M., Goel M., Kelkar H., Morales J., Mulner-Lorillon O., Robertson A.J., Goldstone J.V., Cole B., Epel D., Gold B., Hahn M.E., Howard-Ashby M., Scally M., Stegeman J.J., Allgood E.L., Cool J., Judkins K.M., McCafferty S.S., Musante A.M., Obar R.A., Rawson A.P., Rossetti B.J., Gibbons I.R., Hoffman M.P., Leone A., Istrail S., Materna S.C., Samanta M.P., Stolc V., Tongprasit W., Tu Q., Bergeron K.F., Brandhorst B.P., Whittle J., Berney K., Bottjer D.J., Calestani C., Peterson K., Chow E., Yuan Q.A., Elhaik E., Graur D., Reese J.T., Bosdet I., Heesun S., Marra M.A., Schein J., Anderson M.K., Brockton V., Buckley K.M., Cohen A.H., Fugmann S.D., Hibino T., Loza-Coll M., Majeske A.J., Messier C., Nair S.V., Pancer Z., Terwilliger D.P., Agca C., Arboleda E., Chen N., Churcher A.M., Hallbook F., Humphrey G.W., Idris M.M., Kiyama T., Liang S., Mellott D., Mu X., Murray G., Olinski R.P., Raible F., Rowe M., Taylor J.S., Tessmar-Raible K., Wang D., Wilson K.H., Yaguchi S., Gaasterland T., Galindo B.E., Gunaratne H.J., Juliano C., Kinukawa M., Moy G.W., Neill A.T., Nomura M., Raisch M., Reade A., Roux M.M., Song J.L., Su Y.H., Townley I.K., Voronina E., Wong J.L., Amore G., Branno M., Brown E.R., Cavalieri V., Duboc V., Duloquin L., Flytzanis C., Gache C., Lapraz F., Lepage T., Locascio A., Martinez P., Matassi G., Matranga V., Range R., Rizzo F., Rottinger E., Beane W., Bradham C., Byrum C., Glenn T., Hussain S., Manning G., Miranda E., Thomason R., Walton K., Wikramanayke A., Wu S.Y., Xu R., Brown C.T., Chen L., Gray R.F., Lee P.Y., Nam J., Oliveri P., Smith J., Muzny D., Bell S., Chacko J., Cree A., Curry S., Davis C., Dinh H., Dugan-Rocha S., Fowler J., Gill R., Hamilton C., Hernandez J., Hines S., Hume J., Jackson L., Jolivet A., Kovar C., Lee S., Lewis L., Miner G., Morgan M., Nazareth L.V., Okwuonu G., Parker D., Pu L.L., Thorn R., Wright R. The genome of the sea urchin Strongylocentrotus purpuratus. Science 2006, 314:941-952.
121. Stainier D.Y. A glimpse into the molecular entrails of endoderm formation. Genes Dev. 2002, 16:893-907.
122. Steinberg F., Zhuang L., Beyeler M., Kalin R.E., Mullis P.E., Brandli A.W., Trueb B. The FGFRL1 receptor is shed from cell membranes, binds fibroblast growth factors (FGFs), and antagonizes FGF signaling in Xenopus embryos. J. Biol. Chem. 2009, 285:2193-2202.
123. Storeng R., Jonsen J. Effect of nickel chloride and cadmium acetate on the development of preimplantation mouse embryos in vitro. Toxicology 1980, 17:183-187.
124. Sun Y., Oberley L.W. Redox regulation of transcriptional activators. Free Radic. Biol. Med. 1996, 21:335-348.
125. Sunderman F.W. A review of the metabolism and toxicology of nickel. Ann. Clin. Lab. Sci. 1977, 7:377-398.
126. Swalla B.J. Building divergent body plans with similar genetic pathways. Heredity 2006, 97:235-243.
127. Swalla B.J., Smith A.B. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:1557-1568.
128. Tagawa K., Humphreys T., Satoh N. Novel pattern of Brachyury gene expression in hemichordate embryos. Mech. Dev. 1998, 75:139-143.
129. Tagawa K., Nishino A., Humphreys T., Satoh N. The spawning and early development of the Hawaiian acorn worm (Hemichordate), Ptychodera flava. Zoolog. Sci. 1998, 15:85-91.
130. Taguchi S., Tagawa K., Humphreys T., Nishino A., Satoh N., Harada Y. Characterization of a hemichordate fork head/HNF-3 gene expression. Dev. Genes Evol. 2000, 210:11-17.
131. Taguchi S., Tagawa K., Humphreys T., Satoh N. Group B sox genes that contribute to specification of the vertebrate brain are expressed in the apical organ and ciliary bands of hemichordate larvae. Zoolog. Sci. 2002, 19:57-66.
132. Takumi S., Kimura H., Matsusaki H., Kawazoe S., Tominaga N., Arizono K. DNA microarray analysis of genomic responses of yeast Saccharomyces cerevisiae to nickel chloride. J. Toxicol. Sci. 2010, 35:125-129.
133. Timourian H., Watchmaker G. Nickel uptake by sea urchin embryos and their subsequent development. J. Exp. Zool. 1972, 182:379-387.
134. Tu Q., Brown C.T., Davidson E.H., Oliveri P. Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev. Biol. 2006, 300:49-62.
135. Umbhauer M., Djiane A., Goisset C., Penzo-Mendez A., Riou J.F., Boucaut J.C., Shi D.L. The C-terminal cytoplasmic Lys-thr-X-X-X-Trp motif in frizzled receptors mediates Wnt/beta-catenin signalling. EMBO J. 2000, 19:4944-4954.
136. Webb S.E., Miller A.L. Ca2+ signaling during vertebrate somitogenesis. Acta Pharmacol. Sin. 2006, 27:781-790.
137. Whitman M. Nodal signaling in early vertebrate embryos: themes and variations. Dev. Cell 2001, 1:605-617.
138. Whitman M., Mercola M. TGF-beta superfamily signaling and left-right asymmetry. Sci. STKE 2001, 2001:re1.
139. Wiedemann M., Trueb B. Characterization of a novel protein (FGFRL1) from human cartilage related to FGF receptors. Genomics 2000, 69:275-279.
140. Wilson K.A., Andrews M.E., Rudolf Turner F., Raff R.A. Major regulatory factors in the evolution of development: the roles of goosecoid and Msx in the evolution of the direct-developing sea urchin Heliocidaris erythrogramma. Evol. Dev. 2005, 7:416-428.
141. Yaguchi S., Yaguchi J., Angerer R.C., Angerer L.M. A Wnt-FoxQ2-nodal pathway links primary and secondary axis specification in sea urchin embryos. Dev. Cell 2008, 14:97-107.
142. Yu J.K., Holland L.Z., Holland N.D. An amphioxus nodal gene (AmphiNodal) with early symmetrical expression in the organizer and mesoderm and later asymmetrical expression associated with left-right axis formation. Evol. Dev. 2002, 4:418-425.
143. Zamponi G.W., Bourinet E., Snutch T.P. Nickel block of a family of neuronal calcium channels: subtype- and subunit-dependent action at multiple sites. J. Membr. Biol. 1996, 151:77-90.
144. Zhuang L., Karotki A.V., Bruecker P., Trueb B. Comparison of the receptor FGFRL1 from sea urchins and humans illustrates evolution of a zinc binding motif in the intracellular domain. BMC Biochem. 2009, 10:33.