Reconstitution of the organizer is both sufficient and required to re-establish a fully patterned body plan in avian embryos

Development

Volumn 126, Issue 11, 1999, Pages 2461-2473

  Yuan, Shipeng ^a   Schoenwolf, Gary C ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac mesoderm; Chick embryos; Gastrulation; Gene expression; Heart; In situ hybridization; Neurulation; Nieuwkoop center; Regionalization

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTODERM; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; EMBRYO AXIS; EMBRYO PATTERN FORMATION; GASTRULA; HEART DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; TISSUE DIFFERENTIATION;

ANIMALS; BIOLOGICAL MARKERS; BLASTODERM; BODY PATTERNING; CHICK EMBRYO; EMBRYO, NONMAMMALIAN; FLUORESCENCE; GASTRULA; HEART; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION;

ANIMALIA; AVES; STAPHYLOCOCCUS PHAGE 3A; VERTEBRATA;

EID: 0032992758     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. Antin, P., Taylor, R. G. and Yatskievych, T. (1994). Precardiac mesoderm is specified during gastrulation in quail. Dev. Dynam. 200, 144-154.
2. Bally-Cuif, L. and Wassef, M. (1995). Determination events in the nervous system of the vertebrate embryo. Curr. Opin. Gene. Dev. 5, 450-458.
3. Beddington, R. S. P. (1994). Induction of a second neural axis by the mouse node. Development 120, 613-620.
4. Beddington, R. S. P. and Robertson, E. J. (1998). Anterior patterning in mouse. Trends Genetics 14, 277-284.
5. Beddington, R. S. P. and Robertson, E. J. (1999). Axis development and early asymmetry in mammals. Cell 96, 195-209.
6. Bernes, G. L., Alexander, P. G., Hsu, C. W., Mariani, B. D. and Tuan, R. S. (1997). Cloning and characterization of chicken Paraxis: A regulator of paraxial mesoderm development and somite formation. Dev. Biol. 189, 95-111.
7. Bortier, H. and Vakaet, L. (1992). Mesoblast anlage fields in the upper layer of the chicken blastoderm at stage 5V. In Formation and Differentiation of Early Embryonic Mesoderm (ed. Lash, J. W. and Bellairs, R.), New York: Plenum Publishing Co.
8. Bouwmeester, T. and Leyns, L. ( 1997). Vertebrate head induction by anterior primitive endoderm. BioEssays 19, 855-863.
9. Bovolenta, P., Mallamaci, A., Puelles, L. and Boncinelli, E. (1998). Expression pattern of cSix3, a member of the Six/sine oculis family of transcription factors. Mech. Dev. 70, 201-203.
10. Bronner-Fraser, M. (1986). Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev. Biol. 115, 44-55.
11. Butros, J. (1967). Limited axial structures in nodeless chick blastoderms. J. Embryol. exp. Morph. 17, 119-130.
12. Charlebois, T. S., Henty, J. H. and Grainger, R. M. (1990). Differential cytokeratin gene expression reveals early dorsal-ventral regionalization in chick mesoderm. Development 110, 417-425.
13. Crossley, P. H., Martinez, S. and Martin, G. R. (1996). Midbrain development induced by fgf8 in the chick embryo. Nature 380, 66-68.
14. Dale, L. and J. M. Slack. (1987). Regional specification within the mesoderm of early embryos of Xenopus laevis. Development 100, 279-295.
15. Darnell, D. K., Schoenwolf, G. C. and Ordahl, C. P. (1992). Changes in dorsoventral but not rostrocaudal regionalization of the chick neural tube in the absence of cranial notochord, as revealed by expression of Engrailed-2. Dev. Dynamics 193, 389-396.
16. Dias, M. S. and Schoenwolf, G. C. (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. 229, 437-448.
17. Ericson, J., Morton, S., Kawakami, A., Roelink, H. and Jessell, T. M. (1996). Two critical periods of Sonic hedgehog signaling required for the specification of motor neuron identity. Cell 87, 661-673.
18. Gallera, J. (1971). Primary induction in birds. Adv. Morphogenesis 9, 149-180.
19. Gallera, J. and Nicolet, G. (1974). Regulation in nodeless chick blastoderms. Experientia 30, 183-185.
20. Garcia-Martinez, V. and Schoenwolf, G. C. (1992). Positional control of mesoderm movement and fate during avian gastrulation and neurulation. Dev. Dynam. 193, 249-256.
21. Garcia-Martinez, V. and Schoenwolf, G. C. (1993). Primitive-streak origin of the cardiovascular system in avian embryos. Dev. Biol. 159, 706-719.
22. Garcia-Martinez, V., Alvarez, I. S. and Schoenwolf, G. C. (1993). Locations of the ectodermal and non-ectodermal subdivisions of the epiblast at stages 3 and 4 of avian gastrulation and neurulation. J. Exp. Zool. 267, 431-446.
23. Garcia-Martinez, V., Darnell, D. K., Lopez-Sanchez, C., Sosic, D., Olson, E. N. and Schoenwolf, G. C. (1997). State of commitment of prospective neural plate and prospective mesoderm in late gastrula/early neurula stages of avian embryos. Dev. Biol. 181, 102-115.
24. Gimlich, R. L. and Gerhart, J. C. (1984). Early cellular interactions promote embryonic axis formation in Xenopus laevis. Dev. Biol. 104, 117-30.
25. Giraldez, F. (1998). Regionalized organizing activity of the neural tube revealed by the regulation of lmx1 in the otic vesicle. Dev. Biol. 203, 189-200.
26. Grabowski, C. T. (1956). The effects of the excision of Hensen's node on the early development of the chick embryo. J Exp. Zool. 133, 301-344.
27. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morph. 88, 49-92.
28. Han, Y., Dennis, J. E., Cohen-Gould, L., Bader, D. M. and Fischman, D. A. (1992). Expression of sarcomeric myosin in the presumptive myocardium of chicken embryos occurs within six hours of myocyte commitment. Dev. Dynamics 193, 257-65.
29. Hatada, Y. and Stern, C. D. (1994). A fate map of the epiblast of the early chick embryo. Development 120, 2879-2889.
30. Hemmati-Brivanlou, A., Kelly, O. G. and Melton, D. A. (1994). Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 283-295.
31. Herbrand, H., Guthrie, S., Hadrys, T., Hoffmann, S., Arnold, H.-H., Rinkwitz-Brandt, S. and Bober, E. (1998). Two regulatory genes, cNkx5.1 and cPax2, show different responses to local signals during otic placode and vesicle formation in the chick embryo. Development 125, 645-654.
32. Ho, R. K. (1992). Axis formation in the embryo of the Zebrafish, Brachydanio rerio. Semin. Dev. Biol. 3, 53-64.
33. Inagaki, T., Garcia-Martinez, V. and Schoenwolf, G. C. (1993). Regulative ability of the prospective cardiogenic and vasculogenic areas of the primitive streak during avian gastrulation. Dev. Dynam. 197, 57-68.
34. Kessler, D. S. and Melton, D. A. (1994). Vertebrate embryonic induction: mesodermal and neural patterning. Science 262, 596-604.
35. Lamb, T. M., Knecht, A. K., Smith, W. C., Stachel, S. E., Economides, A. N., Stahl, N., Yancopolous, G. D. and Harland, R. M. (1993). Neural induction by the secreted polypeptide Noggin. Science 262, 713-718.
36. Lemaire, P. and Kodjabachian, L. (1996). The vertebrate organizer: Structure and molecules. Trends Genet. 12, 525-531.
37. Levin, M. and Mercola, M. (1998). Evolutionary conservation of mechanisms upstream of asymmetric Nodal expression: Reconciling chick and Xenopus. Dev. Genet. 23, 185-193.
38. Levin, M., Johnson, R. L., Stern, C. D., Kuehn, M. and Tabin, C, (1995). A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82, 803-814.
39. Levin, M., Pagan, S., Roberts, D. J., Cooke, J., Kuehn, M. R. and Tabin, C. J. (1997). Left-right patterning signals and the independent regulation of different aspects of situs in the chick embryo. Dev. Biol. 189, 57-67.
40. Logan, M., Pagán-Westphal, S. M., Smith, D. M., Paganessi, L. and Tabin, C. J. (1998). The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell 94, 307-317.
41. New, D. A. T. (1955). A new technique for the cultivation of the chick embryo in vitro. J. Embryol. exp. Morphol. 3, 326-331.
42. Nicolet, G. (1971). Avian gastrulation. Adv. Morphogenesis 9, 231-262.
43. Nieto, M. A., Patel, K. and Wilkinson, D. G. (1996). In situ hybridization analysis of chick embryos in whole mount and tissue sections. In Methods in Avian Embryology. Methods in Cell Biology, Vol. 51, (ed. M. Bronner-Fraser). New York: Academic Press, Inc.
44. Nieuwkoop, P. D, (1969). The formation of the mesoderm in urodelan amphibian. I. Induction by the endoderm. Wilhelm Roux's Arch. Entwicklungsmech. Org. 162, 341-373.
45. Nieuwkoop, P. D. (1973). The organization center of the amphibian embryo: Its origin, spatial organisation, and morphogenetic action. Adv. Morphogenesis 10, 1-39.
46. Oppenheimer, J. M. (1959). Extraembryonic transplantation of sections of the Fundulus embryonic shield. J. Exp. Zool. 140, 247-268.
47. Patel, N. H., Martin-Blanco, E., Coleman, K. G., Poole, S. J., Ellis, M. C., Kornberg, T. B. and Goodman, C. S. (1989). Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955-968.
48. Psychoyos, D. and Stern, C. D. (1996). Restoration of the organizer after radical ablation of Hensen's rode and the anterior end of the primitive streak in the chick embryo. Development 122, 3263-3273.
49. Rex, M., Orme, A., Uwanogho, D., Tointon, K., Wigmore, P. M., Sharpe, P. T. and Scotting, P. J. (1997). Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev. Dynamics 209, 323-332.
50. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
51. Roelink, H., Augsburger, A., Heemskerk, J., Korzh, V., Norlin, S., Ruiz i Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T. M. and Dodd, J. (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775.
52. Rosenquist, G. C. (1966). A radioautographic study of labeled grafts in the chick blastoderm. Development from primitive-streak stages to stage 12. Carnegie Contrib. Embryol. No. 262, 38, 31-110.
53. Sasai, Y., Lu, B., Steinbeisser, H. and Robertis, E. M. D. (1995). Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus. Nature 376, 333-336.
54. Schoenwolf, G. C. and Alvarez, I. S. (1991). Specification of neurepithelium and surface epithelium in avian transplantation chimeras. Development 112, 713-722.
55. Schoenwolf, G. C. and Yuan, S. (1995). Experimental analyses of the rearrangement of ectodermal cells during gastrulation and neurulation in avian embryos. Cell Tiss. Res. 280, 243-251.
56. Schoenwolf, G. C., Garcia-Martinez, V. and Dias, M. S. (1992). Mesoderm movement and fate during avian gastrulation and neurulation. Dev. Dynamics 193, 235-248.
57. Selleck, M. A. J. and Stern, C. D. (1992). Commitment of mesoderm cells in Hensen's node of the chick embryo to notochord and somite. Development 114, 403-415.
58. Shin, J. and Fraser, S. E. (1996). Characterizing the Zebrafish organizer: microsurgical analysis at the early-shield stage. Development 122, 1313-1322.
59. Sive, H. K. (1993). The frog princess: A molecular formula for dorsoventral patterning in Xenopus. Genes Dev. 7, 1-12.
60. Smith, W. C. and Harland, R. M. (1992). Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829-840.
61. Smith, J. L. and Schoenwolf, G. C. (1989). Notochordal induction of cell wedging in the chick neural plate and its role in neural tube formation. J. Exp. Zool. 250, 49-62.
62. Spemann, H. and Mangold, H. (1924). Über induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Wilhelm Roux's Arch. Entwicklungsmech. Org. 100, 599-638.
63. Storey, K. G., Crossley, J. M., DeRobertis, E. M., Norris, W. E. and Stern, C. D. (1992). Neural induction and regionalisation in the chick embryo. Development 114, 729-741.
64. Storey, K. G., Selleck, M. A. and Stern, C. D. (1995). Neural induction and regionalisation by different subpopulations of cells in Hensen's node. Development 121, 417-428.
65. Storey, K. G., Goriely, A., Sargent, C. M., Brown, J. M., Burns, H. M. and Heath, J. K. (1998). Early posterior neural tissue is induced by FGF in the chick embryo. Development 125, 473-484.
66. Sugi, Y. and Lough, J. (1994). Anterior endoderm is a specific effector of terminal cardiac myocyte differentiation of cells from the embryonic heart forming region. Dev. Dynamics 200, 155-162.
67. Tonegawa, A., Funayama, N., Ueno, N. and Takahashi, Y. (1997). Mesodermal subdivision along the mediolateral axis in chicken controlled by different concentrations of BMP-4. Development 124, 1975-1984.
68. Torres, M., Gomez-Pardo, E. and Gruss, P. (1995). Pax2 controls multiple steps of urogenital development. Development 121, 4057-4065.
69. Torres, M., Gomez-Pardo, E. and Gruss, P. (1996). Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122, 3381-3391.
70. Waddington, C. H. (1932). Experiments on the development of chick and duck embryos, cultivated in vitro. Phil. Trans. R. Soc. Lond. (Biol.) 221, 179-230.
71. Waterman, A. J. (1936). Experiments on young chick embryos cultured in vitro. Proc. Nat. Acad. Sci. USA 22, 1-3.
72. Wilkinson, D. G. (1989). Homeobox genes and development of the vertebrate CNS. BioEssay 10, 82-85.
73. Yamada, T., Placzek, M., Tanaka, H., Dodd, J. and Jessell, T. M. (1991). Control of cell pattern in the developing nervous system: Polarizing activity of the floor plate and notochord. Cell 64, 635-647.
74. Yamada, G., Mansouri, A., Torres, M., Stuart, E. T., Blum, M., Schultz, M., De Robertis, E. M. and Gruss, P. (1995). Targeted mutation of the murine goosecoid gene results in craniofacial defects and neonatal death. Development 121, 2917-2922.
75. Yuan, S., Darnell, D. K. and Schoenwolf, G. C. (1995a). Mesodermal patterning during avian gastrulation and neurulation: experimental induction of notochord from non-notochordal precursor cells. Dev. Genetics 17, 38-54.
76. Yuan, S., Darnell, D. K. and Schoenwolf, G. C. (1995b). Identification of inducing, responding, and suppressing regions in an experimental model of notochord formation in avian embryos. Dev. Biol. 172, 567-584.
77. Yuan, S. and Schoenwolf, G. C. (1998). De novo induction of the organizer and formation of the primitive streak in an experimental model of notochord reconstitution in avian embryos. Development 125, 201-213.
78. Yutzey, K. E., Rhee, J. T. and Bader, D. (1994). Expression of the atrial-specific myosin heavy chain AMHCI and the establishment of anteroposterior polarity in the developing chicken heart. Development 120, 871-883.