Spatiotemporal development of the embryonic nervous system of saccoglossus kowalevskii

Developmental Biology

Volumn 386, Issue 1, 2014, Pages 252-263

  Cunningham, Doreen ^a   Casey, Elena Silva ^a  

^a GEORGETOWN UNIVERSITY   (United States)

Author keywords

Deuterostome; Hemichordate; Neural induction; Neurogenesis; Saccoglossus

Indexed keywords

ANIMAL CELL; ARTICLE; BLASTULA; BRUA GENE; CONTROLLED STUDY; DCLK GENE; ELAV GENE; EMBRYO; EMBRYO DEVELOPMENT; GAD GENE; GASTRULA; GASTRULATION; GENE; GENE EXPRESSION; GENE IDENTIFICATION; HEMICHORDATA; MSI GENE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROX GENE; SACCOGLOSSUS KOWALEVSKII; SOXB1 GENE; STEM CELL; SYT1 GENE; TH GENE; TPH GENE; VMAT GENE; ADULT; ANIMAL TISSUE; BILATERIA; CELL MATURATION; CENTRAL NERVOUS SYSTEM; DEVELOPMENTAL STAGE; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; GENETIC ASSOCIATION; HATCHING; LARVA; LIFESTYLE MODIFICATION; METAMORPHOSIS; MORPHOGENESIS; ORTHOLOGY; SWIMMING;

BILATERIA; DEUTEROSTOMIA; HEMICHORDATA; INVERTEBRATA; SACCOGLOSSUS; SACCOGLOSSUS KOWALEVSKII;

CELL MARKER;

DEUTEROSTOME; HEMICHORDATE; NEURAL INDUCTION; NEUROGENESIS; SACCOGLOSSUS;

ANIMALS; BIOLOGICAL EVOLUTION; CHORDATA, NONVERTEBRATE; DNA, COMPLEMENTARY; GASTRULA; GASTRULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; GENETIC MARKERS; IN SITU HYBRIDIZATION; LARVA; NERVOUS SYSTEM; NEUROGENESIS; NEURONS; TIME FACTORS;

EID: 84892476708     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.12.001     Document Type: Article

References (62)

1. Abascal F., Zardoya R., Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
2. Angerer L.M., Angerer R.C. Patterning the sea urchin embryo: gene regulatory networks, signaling pathways, and cellular interactions. Curr. Top. Dev. Biol. 2003, 53:159-198.
3. Angerer L.M., Yaguchi S., Angerer R.C., Burke R.D. The evolution of nervous system patterning: insights from sea urchin development. Development 2011, 138:3613-3623.
4. Archer T.C., Jin J., Casey E.S. Interaction of Sox1, Sox2, Sox3 and Oct4 during primary neurogenesis. Dev. Biol. 2011, 350:429-440.
5. Bateson W. The early stages in the development of Balanoglossus (sp. incert.). Stud. Morphol. Lab. 1884, 24:208-236.
6. Bateson W. Continued account of the later stages in the development of Balanoglossus Kowalev- skii, and of the morphology of the Enterop. Q. J. Microsc. Sci. 1885, 1885:511-534.
7. Benito-Gutiérrez E., Illas M., Comella J.X., Garcia-Fernàndez J. Outlining the nascent nervous system of Branchiostoma floridae (amphioxus) by the pan-neural marker AmphiElav. Brain Res. Bull. 2005, 66:518-521.
8. Berger C., Renner S., Lüer K., Technau G.M. The commonly used marker ELAV is transiently expressed in neuroblasts and glial cells in the Drosophila embryonic CNS. Dev. Dyn. 2007, 236:3562-3568.
9. Bourlat S.J., Juliusdottir T., Lowe C.J., Freeman R.M., 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.
10. Brimacombe K.R., Ladd A.N. Cloning and embryonic expression patterns of the chicken CELF family. Dev. Dyn. 2007, 236:2216-2224.
11. Brown F.D., Prendergast A., Swalla B.J. Man is but a worm: chordate origins. Genesis 2008, 46:605-613.
12. Bullock T.H. The functional organization of the nervous system of Enteropneusta. Biol. Bull. 1940, 79:91.
13. Burgess H.A, Reiner O. Doublecortin-like kinase is associated with microtubules in neuronal growth cones. Mol. Cell. Neurosci. 2000, 16:529-541.
14. Bylund M., Andersson E., Novitch B.G., Muhr J. Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci. 2003, 6:1162-1168.
15. Choksi S.P., Southall T.D., Bossing T., Edoff K., de Wit E., Fischer B.E., van Steensel B., Micklem G., Brand A.H. Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev. Cell 2006, 11:775-789.
16. Colwin A.L., Colwin L.H. The normal embryology of Saccoglossus kowalevskii (enteropneusta). J. Morphol. 1953, 92:401-453.
17. Darras S., Gerhart J., Terasaki M., Kirschner M., Lowe C.J. β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii. Development 2011, 138:959-970.
18. Doe C.Q. Neural stem cells: balancing self-renewal with differentiation. Development 2008, 135:1575-1587.
19. Doe C.Q., Chu-LaGraff Q., Wright D.M., Scott M.P. The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 1991, 65:451-464.
20. Fei H., Grygoruk A., Brooks E.S., Chen A., Krantz D.E. Trafficking of Vesicular Neurotransmitter Transporters. Traffic 2010, 9:1425-1436.
21. 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.
22. Gillis J.A., Fritzenwanker J.H., Lowe C.J. A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network. Proc. Biol. Sci. 2012, 279:237-246.
23. Graham V., Khudyakov J., Ellis P., Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron 2003, 39:749-765.
24. Green S.A, Norris R.P., Terasaki M., Lowe C.J. FGF signaling induces mesoderm in the hemichordate Saccoglossus kowalevskii. Development 2013, 140(5):1024-1033. 10.1242/dev.083790.
25. Guindon S., Dufayard J.-F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
26. Hilgers V., Lemke S.B., Levine M. ELAV mediates 3' UTR extension in the Drosophila nervous system. Genes Dev. 2012, 2259-2264.
27. Huelsenbeck J.P., Ronquist F., Nielsen R., Bollback J.P. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 2001, 80(294):2310-2314.
28. Kamachi, Y., Uchikawa, M., Kondoh, H., Biology, C., 2000. Pairing SOX off 9525, 2-7.
29. Kaul S., Stach T. Ontogeny of the collar cord: neurulation in the hemichordate Saccoglossus kowalevskii. J. Morphol. 2010, 271:1240-1259.
30. Kawashima T., Murakami A.R., Ogasawara M., Tanaka K., Isoda R., Sasakura Y., Nishikata T., Okano H., Makabe K.W. Expression patterns of musashi homologs of the ascidians, Halocynthia roretzi and Ciona intestinalis. Dev. Genes Evol. 2000, 210:162-165.
31. Kenny A.P., Oleksyn D.W., Newman L.A., Angerer R.C., Angerer L.M. Tight regulation of SpSoxB factors is required for patterning and morphogenesis in sea urchin embryos. Dev. Biol. 2003, 261:412-425.
32. Kerner P., Simionato E., Le Gouar M., Vervoort M. Orthologs of key vertebrate neural genes are expressed during neurogenesis in the annelid Platynereis dumerilii. Evol. Dev. 2009, 11:513-524.
33. Kerner P., Degnan S.M., Marchand L., Degnan B.M., Vervoort M. Evolution of RNA-binding proteins in animals: insights from genome-wide analysis in the sponge Amphimedon queenslandica. Mol Biol Evol. 2011, 28:2289-2303.
34. Knecht A.K., Good P.J., Dawid I.B., Harland R.M. Dorsal-ventral patterning and differentiation of noggin-induced neural tissue in the absence of mesoderm. Development 1995, 121:1927-1935.
35. Knight-Jones E.W. On the nervous system of Saccoglossus cambrenis. Society 1951, 236:315-354.
36. Koizumi H., Tanaka T., Gleeson J.G. Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 2006, 49:55-66.
37. Larsen C.W., Zeltser L.M., Lumsden A. Boundary formation and compartition in the avian diencephalon. J. Neurosci. 2001, 21:4699-4711.
38. Lavado A., Lagutin O.V., Chow L.M.L., Baker S.J., Oliver G. Prox1 is required for granule cell maturation and intermediate progenitor maintenance during brain neurogenesis. PLoS Biol. 2010, 8:e1000460.
39. Lavado A., Oliver G. Prox1 expression patterns in the developing and adult murine brain. Dev. Dyn. 2007, 236:518-524.
40. Louvi A., Artavanis-Tsakonas S. Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 2006, 7:93-102.
41. Lowe C.J., Terasaki M., Wu M., Freeman R.M., Runft L., Kwan K., Haigo S., Aronowicz J., Lander E., Gruber C.E., Smith M., Kirschner M., Gerhart J. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol. 2006, 4:e291.
42. 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.
43. Misra K., Mishra K., Gui H., Matise M.P. Prox1 regulates a transitory state for interneuron neurogenesis in the spinal cord. Dev. Dyn. 2008, 237:393-402.
44. Niehrs C. On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 2010, 137:845-857.
45. Nomaksteinsky M., Röttinger 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.
46. Pani A.M., Mullarkey E.E., Aronowicz J., Assimacopoulos S., Grove E.A., Lowe C.J. Ancient deuterostome origins of vertebrate brain signalling centres. Nature 2012, 483:289-294.
47. Pascale A, Amadio M., Quattrone A. Defining a neuron: neuronal ELAV proteins. Cell. Mol. Life Sci. 2008, 65:128-140.
48. Perrone-Bizzozero N. Role of HuD and other RNA-binding proteins in neural development and plasticity. J. Neurosci. 2002, 126:121-126.
49. Poskanzer K.E., Marek K.W., Sweeney S.T., Davis G.W. Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 2003, 426:559-563.
50. Range R.C., Angerer R.C., Angerer L.M. Integration of canonical and noncanonical wnt signaling pathways patterns the neuroectoderm along the anterior-posterior axis of sea urchin embryos. PLoS Biol 2013, 11:e1001467.
51. Rasband, W., 2012. ImageJ. U. S. Natl. Institutes Heal. Bethesda, Maryland, USA //imagej.nih.gov/ij/.
52. Ratti A., Fallini C., Cova L., Fantozzi R., Calzarossa C., Zennaro E., Pascale A., Quattrone A., Silani V. A role for the ELAV RNA-binding proteins in neural stem cells: stabilization of Msi1 mRNA. J. Cell Sci. 2006, 119:1442-1452.
53. Richter K., Good P.J., Dawid I.B. A developmentally regulated, nervous system-specific gene in Xenopus encodes a putative RNA-binding protein. New Biol. 1990, 2:556-565.
54. Rogers C.D., Moody S.A., Casey E.S. Neural induction and factors that stabilize a neural fate. Birth Defects Res. C. Embryo Today 2009, 87:249-262.
55. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
56. Sakakibara S., Okano H. Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J. Neurosci. 1997, 17:8300-8312.
57. Sen A., Reddy G.V., Rodrigues V. Combinatorial expression of prospero, seven-up, and Elav identifies progenitor cell types during sense-organ differentiation in the Drosophila antenna. Dev. Biol. 2003, 254:79-92.
58. Sossey-Alaoui K., Srivastava A.K. DCAMKL1, a brain-specific transmembrane protein on 13q12.3 that is similar to doublecortin (DCX). Genomics 1999, 56:121-126.
59. Sprecher S. Drosophila Neural Development. eLS 2012, John, Wiley Sons Ltd., (Feb, ww.els.net). 10.1002/9780470015902.a0000791.pu.
60. Torii M.a, Matsuzaki F., Osumi N., Kaibuchi K., Nakamura S., Casarosa S., Guillemot F., Nakafuku M. Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development 1999, 126:443-456.
61. Wei Z., Yaguchi J., Yaguchi S., Angerer R.C., Angerer L.M. The sea urchin animal pole domain is a Six3-dependent neurogenic patterning center. Development 2009, 136:1179-1189.
62. Yaguchi S., Yaguchi J., Angerer R.C., Angerer L.M. Article a Wnt-FoxQ2-Nodal Pathway links primary and secondary axis specification in sea urchin embryos. Dev. Cell 2008, 14:97-107.