Nodal Signaling in Early Vertebrate Embryos: Themes and Variations

Developmental Cell

Volumn 1, Issue 5, 2001, Pages 605-617

  Whitman, Malcolm ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANURA; VERTEBRATA;

DNA BINDING PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXH1 PROTEIN, MOUSE; PROTEIN NODAL; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL; FEEDBACK SYSTEM; GENETICS; METABOLISM; MORPHOGENESIS; MOUSE; PRENATAL DEVELOPMENT; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE; XENOPUS LAEVIS; ZEBRA FISH;

ANIMALS; BODY PATTERNING; DNA-BINDING PROTEINS; FEEDBACK, BIOCHEMICAL; FORKHEAD TRANSCRIPTION FACTORS; MICE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; VERTEBRATES; XENOPUS LAEVIS; ZEBRAFISH;

EID: 0035512155     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(01)00076-4     Document Type: Review

References (101)

1. Agius E., Oelgeschlager M., Wessely O., Kemp C., De Robertis E.M. Endodermal Nodal-related signals and mesoderm induction in Xenopus. Development. 127:2000;1173-1183.
2. Baker J.C., Harland R.M. A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Dev. 10:1996;1880-1889.
3. Beddington R.S. Induction of a second neural axis by the mouse node. Development. 120:1994;613-620.
4. Beddington R., Robertson E. Axis development and early asymmetry in mammals. Cell. 96:1999;195-210.
5. Bouwmeester T., Kim S., Sasai Y., Lu B., De Robertis E.M. Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature. 382:1996;595-601.
6. Brennan J., Lu C.C., Norris D.P., Rodriguez T.A., Beddington R.S., Robertson E.J. Nodal signalling in the epiblast patterns the early mouse embryo. Nature. 411:2001;965-969.
7. Chen S., Kimelman D. The role of the yolk syncytial layer in germ layer patterning in zebrafish. Development. 127:2000;4681-4689.
8. Chen Y., Schier A.F. The zebrafish Nodal signal Squint functions as a morphogen. Nature. 411:2001;607-610.
9. Chen X., Rubock M.J., Whitman M. A transcriptional partner for Mad proteins in TGF-β signalling. Nature. 383:1996;691-696.
10. Cheng A.M., Thisse B., Thisse C., Wright C.V. The lefty-related factor Xatv acts as a feedback inhibitor of nodal signaling in mesoderm induction and L-R axis development in xenopus. Development. 127:2000;1049-1061.
11. Conlon F., Lyons K., Takaesu N., Barth K., Kispert A., Hermann B., Robertson E. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development. 129:1994;1919-1928.
12. Datto M.B., Frederick J.P., Pan L., Borton A.J., Zhuang Y., Wang X.F. Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol. Cell. Biol. 19:1999;2495-2504.
13. Davidson E. Genomic Regulatory Systems. 2001;Academic Press, San Diego, CA.
14. De Robertis E.M., Larrain J., Oelgeschlager M., Wessely O. The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat. Rev. Genet. 1:2000;171-181.
15. Derynck R., Zhang Y., Feng X.H. Smads. transcriptional activators of TGF-β responses Cell. 95:1998;737-740.
16. Ding J., Yang L., Yan Y.T., Chen A., Desai N., Wynshaw-Boris A., Shen M.M. Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature. 395:1998;702-707.
17. Episkopou V., Arkell R., Timmons P.M., Walsh J.J., Andrew R.L., Swan D. Induction of the mammalian node requires Arkadia function in the extraembryonic lineages. Nature. 410:2001;825-830.
18. Erter C.E., Solnica-Krezel L., Wright C.V.E. Zebrafish nodal related-2 encodes an early mesendodermal inducer signaling from the extraembryonic yolk syncytial layer. Dev. Biol. 204:1998;361-372.
19. Faure S., Lee M.A., Keller T., ten Dijke P., Whitman M. Endogenous patterns of TGFβ superfamily signaling during early Xenopus development. Development. 127:2000;2917-2931.
20. Feldman B., Gates M.A., Egan E.S., Dougan S.T., Rennebeck G., Sirotkin H.I., Schier A.F., Talbot W.S. Zebrafish organizer development and germ-layer formation require nodal-related signals. Nature. 395:1998;181-185.
21. Germain S., Howell M., Esslemont G.M., Hill C.S. Homeodomain and winged-helix transcription factors recruit activated Smads to distinct promoter elements via a common Smad interaction motif. Genes Dev. 14:2000;435-451.
22. Graff J.M., Bansal A., Melton D.A. Xenopus Mad proteins transduce distinct subsets of signals for the TGFβ superfamily. Cell. 85:1996;479-487.
23. Green J.B.A., Smith J.C. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature. 347:1990;391-394.
24. Gritsman K., Zhang J., Cheng S., Heckscher E., Talbot W.S., Schier A.F. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell. 97:1999;121-132.
25. Gritsman K., Talbot W.S., Schier A.F. Nodal signaling patterns the organizer. Development. 127:2000;921-932.
26. Gu Z.Y., Nomura M., Simpson B.B., Lei H., Feijen A., van den Rijnden-van Raaij J., Donahoe P.K., Li E. The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes Dev. 12:1998;844-857.
27. Hansen C.S., Marion C.D., Steele K., George S., Smith W.C. Direct neural induction and selective inhibition of mesoderm and epidermis inducers by Xnr3. Development. 124:1997;483-492.
28. Harland R., Gerhart J. Formation and function of Spemann's Organizer. Annu. Rev. Cell Dev. Biol. 13:1997;611-667.
29. Henry G.L., Melton D.A. Mixer, a homeobox gene required for endoderm development. Science. 281:1998;91-96.
30. Hill C. TGFβ signaling pathways in early Xenopus development. Curr. Opin. Genet. Dev. 11:2001;. in press.
31. Hoodless P.A., Pye M., Chazaud C., Labbe E., Attisano L., Rossant J., Wrana J.L. FoxH1 (Fast) functions to specify the anterior primitive streak in the mouse. Genes Dev. 15:2001;1257-1271.
32. Huang H.C., Murtaugh L.C., Vize P.D., Whitman M. Identification of a potential regulator of early transcriptional responses to mesoderm inducers In the frog embryo. EMBO J. 14:1995;5965-5973.
33. Hyde C.E., Old R.W. Regulation of the early expression of the Xenopus nodal-related 1 gene, Xnr1. Development. 127:2000;1221-1229.
34. Joubin K., Stern C.D. Formation and maintenance of the organizer among the vertebrates. Int. J. Dev. Biol. 45:2001;165-175.
35. Kikuchi Y., Trinh L.A., Reiter J.F., Alexander J., Yelon D., Stainier D.Y. The zebrafish bonnie and clyde gene encodes a Mix family homeodomain protein that regulates the generation of endodermal precursors. Genes Dev. 14:2000;1279-1289.
36. Kimelman D., Griffin K.J. Mesoderm induction. a postmodern view Cell. 94:1998;419-421.
37. Kinoshita N., Minshull J., Kirschner M.W. The identification of two novel ligands of the FGF receptor by a yeast screening method and their activity in Xenopus development. Cell. 83:1995;621-630.
38. Kofron M., Demel T., Xanthos J., Lohr J., Sun B., Sive H., Osada S., Wright C., Wylie C., Heasman J. Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFβ growth factors. Development. 126:1999;5759-5770.
39. Kumar A., Novoselov V., Celeste A.J., Wolfman N.M., ten Dijke P., Kuehn M.R. Nodal signaling uses Activin and Transforming Growth Factor-β receptor-regulated Smads. J. Biol. Chem. 276:2001;656-661.
40. Labbé E., Silvestri C., Hoodless P.A., Wrana J.L., Attisano L. Smad2 and Smad3 positively and negatively regulate TGF beta-dependent transcription through the forkhead DNA-binding protein FAST2. Mol. Cell. 2:1998;109-120.
41. Lee M.A., Heasman J., Whitman M. Timing of endogenous activin-like signals and regional specification of the Xenopus embryo. Development. 128:2001;2939-2952.
42. Liang J.O., Etheridge A., Hantsoo L., Rubinstein A.L., Nowak S.J., Izpisua Belmonte J.C., Halpern M.E. Asymmetric nodal signaling in the zebrafish diencephalon positions the pineal organ. Development. 127:2000;5101-5112.
43. Lowe L.A., Yamada S., Kuehn M.R. Genetic dissection of nodal function in patterning the mouse embryo. Development. 128:2001;1831-1843.
44. Lu C.C., Brennan J., Robertson E.J. From fertilization to gastrulation. axis formation in the mouse embryo Curr. Opin. Genet. Dev. 11:2001;384-392.
45. Massagué J. TGF-β Signal Transduction. Annu. Rev. Biochem. 67:1998;753-791.
46. Massagué J., Wotton D. Transcriptional control by the TGF-β/Smad signaling system. EMBO J. 19:2000;1745-1754.
47. McDowell N., Gurdon J.B. Activin as a morphogen in Xenopus mesoderm induction. Semin Cell Dev. Biol. 10:1999;311-317.
48. McKendry R., Harland R.M., Stachel S.E. Activin-induced factors maintain goosecoid transcription through a paired homeodomain binding site. Dev. Biol. 204:1998;172-186.
49. Meno C., Gritsman K., Ohishi S., Ohfuji Y., Heckscher E., Mochida K., Shimono A., Kondoh H., Talbot W.S., Robertson E.J.et al. Mouse Lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation. Mol. Cell. 4:1999;287-298.
50. Meno C., Takeuchi J., Sakuma R., Koshiba-Takeuchi K., Ohishi S., Saijoh Y., Miyazaki J., ten Dijke P., Ogura T., Hamada H. Diffusion of nodal signaling activity in the absence of the feedback inhibitor Lefty2. Dev. Cell. 1:2001;127-138.
51. Moon R.T., Kimelman D. From cortical rotation to organizer gene expression. toward a molecular explanation of axis specification in Xenopus Bioessays. 20:1998;536-545.
52. Niederlander C., Walsh J.J., Episkopou V., Jones C.M. Arkadia enhances nodal-related signalling to induce mesendoderm. Nature. 410:2001;830-834.
53. Nomura M., Li E. Roles for Smad2 in mesoderm formation, left right patterning, and craniofacial development in mice. Nature. 393:1998;786-789.
54. Norris D.P., Robertson E.J. Asymmetric and node-specific nodal expression patterns are controlled by two distinct cis-acting regulatory elements. Genes Dev. 13:1999;1575-1588.
55. Oh S.P., Li E. The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes Dev. 11:1997;1812-1826.
56. Osada S.I., Wright C.V. Xenopus nodal-related signaling is essential for mesendodermal patterning during early embryogenesis. Development. 126:1999;3229-3240.
57. Osada S.-I., Saijoh Y., Frisch A., Yeo C.-Y., Adachi H., Watanabe M., Whitman M., Hamada H., Wright C.V.E. Activin/Nodal responsiveness and asymmetric expression of a Xenopus nodal-related gene converge on a FAST-regulated module in intron 1. Development. 127:2000;2503-2514.
58. Piccolo S., Agius E., Leyns L., Bhattacharyya S., Grunz H., Bouwmeester T., De Robertis E.M. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature. 397:1999;707-710.
59. Pogoda H.-M., Solnica-Krezel L., Driever W., Meyer D. The zebrafish forkhead transcription factor FoxH1/Fast1 is a modulator of Nodal signaling required for organizer formation. Curr. Biol. 10:2000;1041-1049.
60. Rebagliati M.R., Toyama R., Fricke C., Haffter P., Dawid I.B. Zebrafish nodal-related genes are implicated in axial patterning and establishing left-right asymmetry. Dev. Biol. 199:1998;261-272. a.
61. Rebagliati M.R., Toyama R., Haffter P., Dawid I.B. cyclops encodes a nodal-related factor involved in midline signaling. Proc. Natl. Acad. Sci. USA. 95:1998;9932-9937. b.
62. Rebbert M., Dawid I. Transcriptional regulation of the Xlim-1 gene by activin is mediated by an element in intron I. Proc. Natl. Acad. Sci. USA. 94:1997;9717-9722.
63. Reissmann E., Jornvall H., Blokzijl A., Andersson O., Chang C., Minchiotti G., Persico M.G., Ibanez C.F., Brivanlou A.H. The orphan receptor ALK7 and the Activin receptor ALK4 mediate signaling by Nodal proteins during vertebrate development. Genes Dev. 15:2001;2010-2022.
64. Renucci A., Lemarchandel V., Rosa F. An activated form of type I serine/threonine kinase receptor TARAM-A reveals a specific signalling pathway involved in fish head organiser formation. Development. 122:1996;3735-3743.
65. Ruvinsky I., Silver L.M., Ho R.K. Characterization of the zebrafish tbx16 gene and evolution of the vertebrate T-box family. Dev. Genes Evol. 208:1998;94-99.
66. Ryan K., Garrett N., Bourillot P., Stennard F., Gurdon J.B. The Xenopus eomesodermin promoter and its concentration-dependent response to activin. Mech. Dev. 94:2000;133-146.
67. Saijoh Y., Adachi H., Sakuma R., Yeo C.-Y., Yashiro K., Watanabe M., Hashiguchi H., Mochida K., Ohishi S., Kawabata M.et al. Left-right asymmetric expression of lefty2 and nodal is induced by a signaling pathway that includes the transcription factor FAST2. Mol. Cell. 5:2000;35-47.
68. Sampath K., Rubinstein A.L., Cheng A.M., Liang J.O., Fekany K., Solnica-Krezel L., Korzh V., Halpern M.E., Wright C.V. Induction of the zebrafish ventral brain and floorplate requires cyclops/nodal signalling. Nature. 395:1998;185-189.
69. Schier A.F. Axis formation and patterning in zebrafish. Curr. Opin. Genet. Dev. 11:2001;393-404.
70. Schier A.F., Shen M.M. Nodal signalling in vertebrate development. Nature. 403:2000;385-389.
71. Schier A.F., Talbot W.S. Nodal signaling and the zebrafish organizer. Int. J. Dev. Biol. 45:2001;289-297.
72. Schiffer S.G., Foley S., Kaffashan A., Hronowski X., Zichittella A., Yeo C.Y., Miatkowski K., Adkins H.B., Damon B., Whitman M.et al. Fucosylation of Cripto is required for its ability to facilitate Nodal signaling. J. Biol. Chem. 10:2001;10.
73. Schneider S., Steinbeisser H., Warga R.M., Hausen P. Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech. Dev. 57:1996;191-198.
74. Shen M.M., Schier A.F. The EGF-CFC gene family in vertebrate development. Trends Genet. 16:2000;303-309.
75. Shiratori H., Sakuma R., Watanabe M., Hashiguchi H., Mochida K., Sakai Y., Nishino J., Saijoh Y., Whitman M., Hamada H. Two-step regulation of left-right asymmetric expression of Pitx2. initiation by Nodal signaling and maintenance by Nkx2 Mol. Cell. 7:2001;137-149.
76. Sirard C., de la Pompa J.L., Elia A., Itie A., Mirtsos C., Cheung A., Hahn S., Wakeham A., Schwartz L., Kern S.et al. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 12:1998;107-119.
77. Sirotkin H.I., Gates M.A., Kelly P.D., Schier A.F., Talbot W.S. fast1 is required for the development of dorsal axial structures in zebrafish. Curr. Biol. 10:2000;1051-1054.
78. Smith J.C. Mesoderm-inducing factors and mesodermal patterning. Curr. Opin. Cell Biol. 7:1995;856-861.
79. Song J., Oh S.P., Schrewe H., Nomura M., Lei H., Okano M., Gridley T., Li E. The type II activin receptors are essential for egg cylinder growth, gastrulation, and rostral head development in mice. Dev. Biol. 213:1999;157-169.
80. Spemann H., Mangold H. Uber Induktion von Embryonanlagen durch Implantation artfremder Organisatoren. Arch mikr Anat EntwMech. 100:1924;599-638.
81. Takahashi S., Yokota C., Takano K., Tanegashima K., Onuma Y., Goto J.I., Asashima M. Two novel nodal-related genes initiate early inductive events in Xenopus Nieuwkoop center. Development. 127:2000;5319-5329.
82. Tanegashima K., Yokota C., Takahashi S., Asashima M. Expression cloning of Xantivin, a Xenopus lefty/antivin-related gene, involved in the regulation of activin signaling during mesoderm induction. Mech. Dev. 99:2000;3-14.
83. Thisse B., Wright C.V., Thisse C. Activin- and Nodal-related factors control antero-posterior patterning of the zebrafish embryo. Nature. 403:2000;425-428.
84. Thomas P., Beddington R.S.P. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6:1996;1487-1496.
85. Turing A.M. The chemical basis of morphogenesis. 1953. Bull. Math. Biol. 52:1990;153-197.
86. Varlet I., Collignon J., Robertson E. nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development. 124:1997;1033-1044.
87. Vogel A.M., Gerster T. Promoter activity of the zebrafish bhikhari retroelement requires an intact activin signaling pathway. Mech. Dev. 85:1999;133-146.
88. Waldrip W., Bikoff E., Hoodless P., Wrana J., Robertson E. Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell. 92:1998;797-808.
89. Watanabe M., Whitman M. FAST-1 is a key maternal effector of mesoderm inducers in the early Xenopus embryo. Development. 126:1999;5621-5634.
90. Weinstein M., Yang X., Li C., Xu X., Gotay J., Deng C.X. Failure of egg cylinder elongation and mesoderm induction in mouse embryos lacking the tumor suppressor smad2. Proc. Natl. Acad. Sci. USA. 95:1998;9378-9383.
91. Weisberg E., Winnier G.E., Chen X., Farnsworth C., Hogan B.L.M., Whitman M. A mouse homologue of FAST-1 transduces TGFβ superfamily signals and is expressed during early embryogenesis. Mech. Dev. 79:1998;17-27.
92. Whitman M. Smads and early developmental signaling by the TGFβ superfamily. Genes Dev. 12:1998;2443-2453.
93. Wright C. Mechanisms of left-right asymmetry. what's right and what's left? Dev.Cell. 1:2001;179-186.
94. Xanthos J.B., Kofron M., Wylie C., Heasman J. Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development. 128:2001;167-180.
95. Yamamoto M., Meno C., Sakai Y., Shiratori H., Mochida K., Ikawa Y., Saijoh Y., Hamada H. The transcription factor FoxH1 (FAST) mediates Nodal signaling during anterior-posterior patterning and node formation in the mouse. Genes Dev. 15:2001;1242-1256.
96. Yeo C., Whitman M. Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol. Cell. 7:2001;949-957.
97. Yeo C.-Y., Chen X., Whitman M. The role of FAST-1 and Smads in transcriptional regulation of by activin during early Xenopus embryogenesis. J. Biol. Chem. 274:1999;26584-26590.
98. Zhang J., King M.L. Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning. Development. 124:1996;4119-4129.
99. Zhou X., Sasaki H., Lowe L., Hogan B.L., Kuehn M.R. Nodal is a novel TGF-β-like gene expressed in the mouse node during gastrulation. Nature. 361:1993;543-547.
100. Zhou S., Zawel L., Lengauer C., Kinzler K.W., Vogelstein B. Characterization of human FAST-1, a TGF beta and activin signal transducer. Mol. Cell. 2:1998;121-127.
101. Zhu Y., Richardson J., Parada L., Graff J. Smad3 mutant mice develop metastatic colorectal cancer. Cell. 94:1998;703-714.