Mouse lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation

Molecular Cell

Volumn 4, Issue 3, 1999, Pages 287-298

  Meno, Chikara ^a   Gritsman, Kira ^d   Ohishi, Sachiko ^b   Ohfuji, Yasuhisa ^b   Heckscher, Elizabeth ^d   Mochida, Kyoko ^b   Shimono, Akihiko ^c,f   Kondoh, Hisato ^c   Talbot, William S ^d   Robertson, Elizabeth J ^e   Schier, Alexander F ^d   Hamada, Hiroshi ^a,b  

^a Division of Molecular Biology   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e HARVARD UNIVERSITY   (United States)

^f NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; EMBRYO; GASTRULATION; GENE EXPRESSION REGULATION; MESODERM; MOUSE; MOUSE MUTANT; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; PRIMITIVE STREAK; ZEBRA FISH;

CYCLOPS; DANIO RERIO; MAMMALIA; VERTEBRATA;

EID: 0033197552     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80331-7     Document Type: Article

References (46)

1. Adachi, H., Saijoh, Y., Mochida, K., Ohishi, S., Hashiguchi, H., Hirao, A., and Hamada, H. (1999). Determination of left-right asymmetric expression of nodal by a left side-specific enhancer with sequence similarity to a lefty2 enhancer. Genes Dev., 13, 1589-1600.
2. Ang, S.-L., Conlon, R.A., Jin, O., and Rossant, J. (1994). Positive and negative signals from mesoderm regulates the expression of mouse Otx2 in ectoderm explants. Development 120, 2979-2989.
3. Beddington, R., and Robertson, E.J. (1999). Axis development and early asymmetry in mammals. Cell 96, 195-209.
4. Candia, A.F., Hu, J., Crosby, J., Lalley, P.A., Noden, D., Nadeau, J.H., and Wright, C.V.E. (1992). Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. Development 116, 1123-1136.
5. Collignon, J., Varlet, I., and Robertson, E.J. (1996). Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature 381, 155-158.
6. Conlon, F.L., Lyons, K.M., Takaesu, N., Barth, K.S., Kispert, A.K., Herrmann, B., and Robertson, E.J. (1994). A primary requirement of nodal in the formation and maintenance of the primitive streak in mouse. Development 120, 1919-1928.
7. Crossley, P.H., and Martin, G.R. (1995). The mouse Fgf8 gene encodes a family of polypeptide and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439-451.
8. Dyson, S., and Gurdon, J.B. (1997). Activin signaling has a necessary function in Xenopus early development. Curr. Biol. 7, 81-84.
9. Feldman, B., Gates, M.A., Egan, E.S., Dougan, S.T., Renneback, G., Sirotkin, H.I., Schier, A.F., and Talbot, W.S. (1998). Zebrafish organizer development and germ-layer formation require nodal-related signals. Nature 395, 181-185.
10. Gritsman, K., Zhang, J., Cheng, S., Heckscher, E., Talbot, W.S., and Schier, A.F. (1999). The EGF-CFC protein one-eyed pinhead is essential for Nodal signaling. Cell 97, 121-132.
11. Gu, Z., Nomura, M., Simpson, B.B., Lei, H., Feijen, A., van den Eijnden-vanRaaij, J., Donahoe, P.K., and Li, E. (1998). The type I activin receptor ActRIB required for egg cylinder organization and gastrulation in the mouse. Genes Dev. 12, 844-857.
12. Harland, R., and Gerhart, J. (1997). Formation and function of Spemann's organizer. Annu. Rev. Cell. Dev. Biol. 13, 611-667.
13. Hatta, K., Kimmel, C.B., Ho, R.K., and Walker, C. (1991). The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system. Nature 350, 339-341.
14. Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., and Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Developmental Dynamics 203, 253-310.
15. Kispert, A., and Herrmann, B.G. (1994). Immunohistochemical analysis of the Brachyury protein in wild-type and mutant mouse embryos. Dev. Biol. 161, 179-193.
16. Logan, M., Pagan-Westphal, S.M., Smith, D.M., Paganessi, L., and Tabin, C. (1998). The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell 94, 307-318.
17. Lowe, L., Supp, D.M., Sampath, K., Yokoyama, T., Wright, C.V.E., Potter, S.S., Overbeek, P., and Kuehn, M.R. (1996). Conserved left-right asymmetry of nodal expression and alteration in murine situs inversus. Nature 381, 158-161.
18. Massague, J. (1998). TGF β signal transduction. Annu. Rev. Biochem. 67, 753-791.
19. Meno, C., Saijoh, Y., Fujii, H., Ikeda, M., Yokoyama, T., Yokoyama, M., Toyoda, Y., and Hamada, H. (1996). Left-right asymmetric expression of the TGF β-family member lefty in mouse embryos. Nature 381, 151-155.
20. Meno, C., Itoh, Y., Saijoh, Y., Matsuda, Y., Tashiro, K., Kuhara, S., and Hamada, H. (1997). Two closely-related left-right asymmetrically expressed genes, lefty1 and lefty2: Their distinct expression domains, chromosomal linkage and direct neuralizing activity in Xenopus embryos. Genes Cells 2, 513-524.
21. Meno, C., Shimono, A., Saijoh, Y., Yashiro, K., Ohishi, S., Mochida, K., Noji, S., Kondoh, H., and Hamada, H. (1998). Lefty1 is required for left-right determination as a regulator of lefty2 and nodal. Cell 94, 287-298.
22. Norris, D.P., and Robertson, E.J. (1999). Asymmetric and node-specific nodal expression patterns are controlled by two distinct cis-acting regulatory elements. Genes Dev. 13, 1575-1588.
23. Oh, S.P., and Li, E. (1997). The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes Dev. 11, 1812-1826.
24. Oulad-Abdelghani, M., Chazaud, C., Bouillet, P., Mattei, M.G., Dolle, P., and Chambon, P. (1998). Stra3/lefty, a retinoic acid-inducible novel member of the TGF β superfamily. Int. J. Dev. Biol. 42, 23-32.
25. Perrimon, N., and McMahon, A.P. (1999). Negative feedback mechanisms and their roles during pattern formation. Cell 97, 13-16.
26. Piccolo, S., Sasai, Y., Lu, B., and DeRobertis, E.M. (1996). Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589-598.
27. Piedra, M.E., Icardo, J.M., Albajar, M., Rodriguez-Rey, J.C., and Ros, M.A. (1998). Pitx2 participates in the late phase of the pathway controlling left-right asymmetry. Cell 94, 319-324.
28. Rebagliati, M.R., Toyama, R., Haffter, P., and Dawid, I.B. (1998a). Cyclops encodes a nodal-related factor involved in midline signaling. Proc. Natl. Acad. Sci. USA 95, 9932-9937.
29. Rebagliati, M.R., Toyama, R., Fricke, C., Haffter, P., and Dawid, I.B. (1998b). Zebrafish nodal-related genes are implicated in axial patterning and establishing left-right asymmetry. Dev. Biol. 199, 261-272.
30. Ryan, A.K., Blumberg, B., Rodriguez-Estaban, C., Yonei-Tamura, S., Tamura, K., Tsukui, T., de la Pena, J., Sabbagh, W., Greenwald, J., Choe, S., et al. (1998). Pitx2 determines left-right asymmetry of internal organs in vertebrates. Nature 394, 545-551.
31. Saijoh, Y., Adachi, H., Hirao, A., Mochida, K., Ohishi, S., and Hamada, H. (1999). Distinct transcriptional regulatory mechanisms underlie left-right asymmetric expression of lefty1 and lefty2. Genes Dev. 13, 259-269.
32. Sampath, K., Rubinstein, A.L., Cheng, A.M., Liang, J.O., Fekany, K., Solnica-Krezel, L., Korzh, V., Halpern, M.E., and Wright, C.V.E. (1998). Induction of the zebrafish ventral brain and floor plate requires cyclops/nodal signaling. Nature 395, 185-189.
33. Sasaki, H., and Hogan, B.L.M. (1993). Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118, 47-59.
34. Sawai, S., Shimono, A., Hanaoka, K., and Kondoh, H. (1991). Embryonic lethality resulting from disruption of both N-myc alleles in mouse zygotes. New Biologists 9, 861-869
35. Schweitzer, R., and Shilo, B.Z. (1997). A thousand and one roles for the Drosophila EGF receptor. Trends Genet. 13, 191-196.
36. Thisse, C., and Thisse, B. (1999). Antivin, a novel and divergent member of the TGF β superfamily, negatively regulates mesoderm induction. Development 126, 229-240.
37. Thomas, P., and Beddington, R. (1996). Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6, 1487-1496.
38. Toyama, R., O'Connell, M.L., Wright, C.V., Kuehn, M.R., and Dawid, I.B. (1995). Nodal induces ectopic goosecoid and lim1 expression and axis duplication in zebrafish. Development 121, 383-391.
39. Varlet, I., Collignon, J., and Robertson, E.J. (1997a). Nodal expression in the primitive eododerm is required for the specification of the anterior axis during mouse gastrulation. Development 124, 1033-1044.
40. Varlet, I., Collignon, J., Norris, D.P., and Robertson, E.J. (1997b). Nodal signaling and axis formation in the mouse. Cold Spring Harb. Symp. Quant. Biol. 62, 105-113.
41. Wolf, C., Thisse, C., Stoetzel, C., Thisse, B., Gerlinger, P., and Perrin-Schmitt, F. (1991). The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev. Biol. 143, 363-373.
42. Wilkinson, D.G. Whole mount in situ hybridization of vertebrate embryos. In In Situ Hybridization: A Practical Approach, D.G. Wilkinson, ed. (IRL Press, Oxford 1992), 75-84
43. Yoshioka, H., Meno, C., Koshiba, K., Sugihara, M., Itoh, H., Ishimaru, Y., Inoue, T., Ohuchi, H., Semina, E.V., Murray, J.C., et al. (1998). Pitx2, a bicoid type homeobox gene, is involved in a lefty-signaling pathway in determination of Left-right asymmetry. Cell 94, 299-305.
44. Zhang, J., Talbot, W.S., and Schier, A.F. (1998). Positional cloning identifies zebrafish one-eyed pinhead as a permissive EGF-related ligand required for gastrulation. Cell 92, 241-251.
45. Zimmerman, L.B., De Jesus-Escobar, J.M., and Harland, R.M. (1996). The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606.
46. Zhou, X., Sasaki, H., Lowe, L., Hogan, B.L., and Kuehn, M.R. (1993). Nodal is a novel TGF β-like gene expressed in the mouse node during gastrulation. Nature 361, 543-547.