Distinct steps of neural induction revealed by Asterix, Obelix and TrKC, genes induced by different signals from the organizer

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Pinho, Sonia ^a,c   Simonsson, Pamela R ^a   Trevers, Katherine E ^a   Stower, Matthew J ^a   Sherlock, William T ^a   Khan, Mohsin ^a   Streit, Andrea ^b   Sheng, Guojun ^a,d   Stern, Claudio D ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF PORTO   (Portugal)

^d RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASTERIX PROTEIN; BONE MORPHOGENETIC PROTEIN; CERBERUS PROTEIN; CHORDIN; COMPLEMENTARY DNA; DICKKOPF 1 PROTEIN; FIBROBLAST GROWTH FACTOR; NEUROTROPHIN 3 RECEPTOR; NOGGIN; OBELIX PROTEIN; RETINOIC ACID; RNA BINDING PROTEIN; SCATTER FACTOR; SOMATOSTATIN; TRANSCRIPTION FACTOR SOX3; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CHICK; CONTROLLED STUDY; EMBRYO; EMBRYO INDUCTION; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; GENE CONTROL; GENE EXPRESSION; NERVOUS SYSTEM DEVELOPMENT; NEUROECTODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CHICK EMBRYO; GENE EXPRESSION REGULATION; GENE LIBRARY; METABOLISM; NERVOUS SYSTEM; PHYLOGENY; PRENATAL DEVELOPMENT; TIME;

ANIMALS; CHICK EMBRYO; EMBRYONIC INDUCTION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; MODELS, BIOLOGICAL; NERVOUS SYSTEM; NEURAL PLATE; ORGANIZERS, EMBRYONIC; PHYLOGENY; RECEPTOR, TRKC; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 79955740061     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019157     Document Type: Article

References (84)

1. Spemann H, Mangold H, (1924) Über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Roux' Arch EntwMech Org 100: 599-638.
2. Gurdon JB, (1987) Embryonic induction- molecular prospects. Development 99: 285-306.
3. Waddington CH, (1930) Developmental mechanics of chick and duck embryos. Nature 125: 924-925.
4. Waddington CH, (1932) Experiments on the development of chick and duck embryos cultivated in vitro. Philos Trans R Soc Lond B Biol Sci 221: 179-230.
5. Waddington CH, (1933) Induction by the primitive streak and its derivatives in the chick. J Exp Biol 10: 38-48.
6. Waddington CH, (1934) Experiments on embryonic induction. J exp Biol 11: 211-227.
7. Waddington CH, (1937) Experiments on determination in the rabbit embryo. Arch Biol 48: 273-290.
8. Waddington CH, Schmidt CA, (1933) Induction by heteroplastic grafts of the primitive streak in birds. Roux' Arch EntwMech Org 128: 522-563.
9. Oppenheimer JM, (1936) Structures developed in amphibians by implantation of living fish organizer. Proc Soc Exp Biol Med 34: 461-463.
10. Oppenheimer JM, (1936) Transplantation experiments on developing teleosts (Fundulus and Perca). J Exp Zool 72: 409-437.
11. Luther WH, (1935) Entwicklungsphysiologische Untersuchungen am Forellenkeim: die Rolle des Organisationszentrums bei der Entstehung der Embryonalanlage. Biol Zentralbl 55: 114-137.
12. Dale L, Slack JMW, (1987) Regional specification within the mesoderm of early embryos of Xenopus laevis. Development 100: 279-295.
13. Smith JC, Slack JM, (1983) Dorsalization and neural induction: properties of the organizer in Xenopus laevis. J Embryol Exp Morphol 78: 299-317.
14. Smith JC, Cooke J, Green JB, Howes G, Symes K, (1989) Inducing factors and the control of mesodermal pattern in Xenopus laevis. Development 107: 149-159.
15. Streit A, Stern CD, (1999) Mesoderm patterning and somite formation during node regression: differential effects of chordin and noggin. Mech Dev 85: 85-96.
16. Tonegawa A, Funayama N, Ueno N, Takahashi Y, (1997) Mesodermal subdivision along the mediolateral axis in chicken controlled by different concentrations of BMP-4. Development 124: 1975-1984.
17. Harland R, Gerhart J, (1997) Formation and function of Spemann's organizer. Annu Rev Cell Dev Biol 13: 611-667.
18. Stern CD, (2005) Neural induction: old problem, new findings, yet more questions. Development 132: 2007-2021.
19. Dale L, Howes G, Price BM, Smith JC, (1992) Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development. Development 115: 573-585.
20. Dale L, Wardle FC, (1999) A gradient of BMP activity specifies dorsal-ventral fates in early Xenopus embryos. Semin Cell Dev Biol 10: 319-326.
21. Smith WC, Harland RM, (1992) Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70: 829-840.
22. Smith WC, Knecht AK, Wu M, Harland RM, (1993) Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature 361: 547-549.
23. Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, et al. (1994) Xenopus chordin: A novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79: 779-790.
24. Hemmati-Brivanlou A, Melton D, (1997) Vertebrate embryonic cells will become nerve cells unless told otherwise. Cell 88: 13-17.
25. Wilson PA, Hemmati-Brivanlou A, (1995) Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376: 331-333.
26. Linker C, Stern CD, (2004) Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists. Development 131: 5671-5681.
27. Linker C, De Almeida I, Papanayotou C, Stower M, Sabado V, et al. (2009) Cell communication with the neural plate is required for induction of neural markers by BMP inhibition: evidence for homeogenetic induction and implications for Xenopus animal cap and chick explant assays. Dev Biol 327: 478-486.
28. Streit A, Lee KJ, Woo I, Roberts C, Jessell TM, et al. (1998) Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development 125: 507-519.
29. Streit A, Stern CD, (1999) Establishment and maintenance of the border of the neural plate in the chick: involvement of FGF and BMP activity. Mech Dev 82: 51-66.
30. Delaune E, Lemaire P, Kodjabachian L, (2005) Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. Development 132: 299-310.
31. Sasai Y, Lu B, Piccolo S, De Robertis EM, (1996) Endoderm induction by the organizer-secreted factors chordin and noggin in Xenopus animal caps. Embo J 15: 4547-4555.
32. Launay C, Fromentoux V, Shi DL, Boucaut JC, (1996) A truncated FGF receptor blocks neural induction by endogenous Xenopus inducers. Development 122: 869-880.
33. Storey KG, Crossley JM, De Robertis EM, Norris WE, Stern CD, (1992) Neural induction and regionalisation in the chick embryo. Development 114: 729-741.
34. Gallera J, Ivanov I, (1964) La compétence neurogène du feuillet externe du blastoderme de poulet en fonction du facteur 'temps'. J Embryol Exp Morphol 12: 693.
35. Streit A, Berliner AJ, Papanayotou C, Sirulnik A, Stern CD, (2000) Initiation of neural induction by FGF signalling before gastrulation. Nature 406: 74-78.
36. Sheng G, dos Reis M, Stern CD, (2003) Churchill, a zinc finger transcriptional activator, regulates the transition between gastrulation and neurulation. Cell 115: 603-613.
37. Gibson A, Robinson N, Streit A, Sheng G, Stern CD, (2010) Regulation of programmed cell death during neural induction in the chick embryo. submitted.
38. Bernd P, Li R, (1999) Differential expression of trkC mRNA in the chicken embryo from gastrulation to development of secondary brain vesicles. Brain Res Dev Brain Res 116: 205-209.
39. Papanayotou C, Mey A, Birot AM, Saka Y, Boast S, et al. (2008) A mechanism regulating the onset of Sox2 expression in the embryonic neural plate. PLoS Biol 6: e2.
40. Battiste JL, Pestova TV, Hellen CU, Wagner G, (2000) The eIF1A solution structure reveals a large RNA-binding surface important for scanning function. Mol Cell 5: 109-119.
41. Gouy M, Guindon S, Gascuel O, (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular biology and evolution 27: 221-224.
42. Eyal-Giladi H, Kochav S, (1976) From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick. I. General morphology. Dev Biol 49: 321-337.
43. Yao L, Zhang D, Bernd P, (1994) The onset of neurotrophin and trk mRNA expression in early embryonic tissues of the quail. Dev Biol 165: 727-730.
44. Zhang D, Yao L, Bernd P, (1994) Expression of trk and neurotrophin mRNA in dorsal root and sympathetic ganglia of the quail during development. J Neurobiol 25: 1517-1532.
45. Zhang D, Yao L, Bernd P, (1996) Expression of neurotrophin trk and p75 receptors in quail embryos undergoing gastrulation and neurulation. Dev Dyn 205: 150-161.
46. Mohammadi M, McMahon G, Sun L, Tang C, Hirth P, et al. (1997) Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276: 955-960.
47. Benne R, Brown-Luedi ML, Hershey JW, (1978) Purification and characterization of protein synthesis initiation factors eIF-1, eIF-4C, eIF-4D, and eIF-5 from rabbit reticulocytes. J Biol Chem 253: 3070-3077.
48. Dever TE, Wei CL, Benkowski LA, Browning K, Merrick WC, et al. (1994) Determination of the amino acid sequence of rabbit, human, and wheat germ protein synthesis factor eIF-4C by cloning and chemical sequencing. J Biol Chem 269: 3212-3218.
49. Keeling PJ, Doolittle WF, (1995) An archaebacterial elF-1A: new grist for the mill. Mol Microbiol 17: 399-400.
50. Kyrpides NC, Woese CR, (1998) Universally conserved translation initiation factors. Proc Natl Acad Sci U S A 95: 224-228.
51. Sorensen HP, Hedegaard J, Sperling-Petersen HU, Mortensen KK, (2001) Remarkable conservation of translation initiation factors: IF1/eIF1A and IF2/eIF5B are universally distributed phylogenetic markers. IUBMB Life 51: 321-327.
52. Sette M, van Tilborg P, Spurio R, Kaptein R, Paci M, et al. (1997) The structure of the translational initiation factor IF1 from E.coli contains an oligomer-binding motif. Embo J 16: 1436-1443.
53. Murzin AG, (1993) OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. Embo J 12: 861-867.
54. Zhang C, Kim SH, (2000) A comprehensive analysis of the Greek key motifs in protein beta-barrels and beta-sandwiches. Proteins 40: 409-419.
55. Baig MA, Khan MA, (1996) The induction of neurotrophin and TRK receptor mRNA expression during early avian embryogenesis. Int J Dev Neurosci 14: 55-60.
56. Rex M, Orme A, Uwanogho D, Tointon K, Wigmore PM, et al. (1997) Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev Dyn 209: 323-332.
57. Uwanogho D, Rex M, Cartwright EJ, Pearl G, Healy C, et al. (1995) Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development. Mech Dev 49: 23-36.
58. Foley AC, Skromne I, Stern CD, (2000) Reconciling different models of forebrain induction and patterning: a dual role for the hypoblast. Development 127: 3839-3854.
59. Albazerchi A, Cinquin O, Stern CD, (2007) A new method to transfect the hypoblast of the chick embryo reveals conservation of the regulation of an Otx2 enhancer between mouse and chick extraembryonic endoderm. BMC Dev Biol 7: 25.
60. Albazerchi A, Stern CD, (2007) A role for the hypoblast (AVE) in the initiation of neural induction, independent of its ability to position the primitive streak. Dev Biol 301: 489-503.
61. Dias MS, Schoenwolf GC, (1990) Formation of ectopic neurepithelium in chick blastoderms: age-related capacities for induction and self-differentiation following transplantation of quail Hensen's nodes. Anat Rec 228: 437-448.
62. Gallera J, Nicolet G, (1969) Le pouvoir inducteur de l'endoblaste presomptif contenu dans la ligne primitive jeune de l'embryon de poulet. J Embryol Exp Morphol 21: 105-118.
63. Gallera J, (1971) Différence de la reactivité à l'inducteur neurogène entre l'ectoblaste de l'aire opaque et celui de l'aire pellucide chez le poulet. Experientia 26: 1953-1954.
64. Chen Y, Solursh M, (1992) Comparison of Hensen's node and retinoic acid in secondary axis induction in the early chick embryo. Dev Dyn 195: 142-151.
65. Chen Y, Huang L, Russo AF, Solursh M, (1992) Retinoic acid is enriched in Hensen's node and is developmentally regulated in the early chicken embryo. Proc Natl Acad Sci U S A 89: 10056-10059.
66. Marchal L, Luxardi G, Thome V, Kodjabachian L, (2009) BMP inhibition initiates neural induction via FGF signaling and Zic genes. Proc Natl Acad Sci U S A 106: 17437-17442.
67. Wilson SI, Graziano E, Harland R, Jessell TM, Edlund T, (2000) An early requirement for FGF signalling in the acquisition of neural cell fate in the chick embryo. Curr Biol 10: 421-429.
68. Wilson SI, Rydstrom A, Trimborn T, Willert K, Nusse R, et al. (2001) The status of Wnt signalling regulates neural and epidermal fates in the chick embryo. Nature 411: 325-330.
69. Streit A, Stern CD, Thery C, Ireland GW, Aparicio S, et al. (1995) A role for HGF/SF in neural induction and its expression in Hensen's node during gastrulation. Development 121: 813-824.
70. Streit A, Sockanathan S, Perez L, Rex M, Scotting PJ, et al. (1997) Preventing the loss of competence for neural induction: HGF/SF, L5 and Sox-2. Development 124: 1191-1202.
71. Piccolo S, Agius E, Leyns L, Bhattacharyya S, Grunz H, et al. (1999) The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397: 707-710.
72. Bertocchini F, Stern CD, (2002) The hypoblast of the chick embryo positions the primitive streak by antagonizing nodal signaling. Dev Cell 3: 735-744.
73. Zhu L, Marvin MJ, Gardiner A, Lassar AB, Mercola M, et al. (1999) Cerberus regulates left-right asymmetry of the embryonic head and heart. Current Biology 9: 931-938.
74. de Almeida I, Rolo A, Batut J, Hill C, Stern CD, et al. (2008) Unexpected activities of Smad7 in Xenopus mesodermal and neural induction. Mech Dev 125: 421-431.
75. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular cloning: a laboratory manual. New York Cold Spring Harbor Press.
76. Hamburger V, Hamilton HL, (1951) A series of normal stages in the development of the chick embryo. J Morphol 88: 49-92.
77. New DAT, (1955) A new technique for the cultivation of the chick embryo in vitro. J Embryol exp Morph 3: 326-331.
78. Stern CD, Ireland GW, (1981) An integrated experimental study of endoderm formation in avian embryos. Anat Embryol 163: 245-263.
79. Stern CD, (2008) Grafting Hensen's node. Methods Mol Biol 461: 265-276.
80. Streit A, Stern CD, (2008) Operations on primitive streak stage avian embryos. Methods Cell Biol 87: 3-17.
81. Lamb TM, Knecht AK, Smith WC, Stachel SE, Economides AN, et al. (1993) Neural induction by the secreted polypeptide noggin. Science 262: 713-718.
82. Skromne I, Stern CD, (2001) Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo. Development 128: 2915-2927.
83. Stern CD, (1998) Detection of multiple gene products simultaneously by in situ hybridization and immunohistochemistry in whole mounts of avian embryos. Curr Top Dev Biol 36: 223-243.
84. Streit A, Stern CD, (2001) Combined whole-mount in situ hybridization and immunohistochemistry in avian embryos. Methods 23: 339-344.