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Published online
doi:10.1083/jcb.200808044
The Journal of Cell Biology, Vol. 184, No. 2, 323-334
The Rockefeller University Press, 0021-9525 $30.00
© Yamamoto et al.
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Article

Antagonism between Smad1 and Smad2 signaling determines the site of distal visceral endoderm formation in the mouse embryo



Masamichi Yamamoto1,2, Hideyuki Beppu3, Katsuyoshi Takaoka1,2, Chikara Meno1, En Li4, Kohei Miyazono5, and Hiroshi Hamada1,2

1 Developmental Genetics Group, Graduate School of Frontier Biosciences, Osaka University, and 2 Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Suita, Osaka 565-0871, Japan
3 Cardiovascular Research Center, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129
4 Epigenetics Program, Novartis Institutes for Biomedical Research, Cambridge, MA 02139
5 Department of Molecular Pathology, Graduate School of Medicine, University of Tokyo, Hongo, Tokyo 113-0033, Japan

Correspondence to Masamichi Yamamoto: myamamoto{at}fbs.osaka-u.ac.jp; or Hiroshi Hamada: hamada{at}fbs.osaka-u.ac.jp

The anterior–posterior axis of the mouse embryo is established by formation of distal visceral endoderm (DVE) and its subsequent migration. The precise mechanism of DVE formation has remained unknown, however. Here we show that bone morphogenetic protein (BMP) signaling plays dual roles in DVE formation. BMP signaling is required at an early stage for differentiation of the primitive endoderm into the embryonic visceral endoderm (VE), whereas it inhibits DVE formation, restricting it to the distal region, at a later stage. A Smad2-activating factor such as Activin also contributes to DVE formation by generating a region of VE positive for the Smad2 signal and negative for Smad1 signal. DVE is thus formed at the distal end of the embryo, the only region of VE negative for the Smad1 signal and positive for Smad2 signal. An inverse relation between the level of phosphorylated Smad1 and that of phosphorylated Smad2 in VE suggests an involvement of antagonism between Smad1- and Smad2-mediated signaling.

C. Meno's present address is Dept. of Developmental Biology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan.

Abbreviations used in this paper: A-P, anterior–posterior; AVE, anterior visceral endoderm; BMP, bone morphogenetic protein; DVE, distal visceral endoderm; E, embryonic day; ES, embryonic stem; ExE, extraembryonic ectoderm; p-Smad, phosphorylated Smad; VE, visceral endoderm.

© 2009 Yamamoto et al.
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