DOI: 10.1073/pnas.96.1.162. Placental failure in mice lacking the homeobox gene <i>Dlx</i> <i>3</i>

Placental failure in mice lacking the homeobox gene Dlx 3

10.1073/pnas.96.1.162

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

Dlx3 is a homeodomain transcription factor and a member of the vertebrate Distal-less family. Targeted deletion of the mouse Dlx3 gene results in embryonic death between day 9.5 and day 10 because of placental defects that alter the development of the labyrinthine layer. In situ hybridization reveals that the Dlx3 gene is initially expressed in ectoplacental cone cells and chorionic plate, and later in the labyrinthine trophoblast of the chorioallantoic placenta, where major defects are observed in the Dlx3 −/− embryos. The expression of structural genes, such as 4311 and PL-1 , which were used as markers to follow the fate of different derivatives of the placenta, was not affected in the Dlx3 -null embryos. However, by day 10.5 of development, expression of the paired-like homeodomain gene Esx1 was strongly down-regulated in affected placenta tissue, suggesting that Dlx3 is required for the maintenance of Esx1 expression, normal placental morphogenesis, and embryonic survival.

Bibliography

Morasso, M. I., Grinberg, A., Robinson, G., Sargent, T. D., & Mahon, K. A. (1999). Placental failure in mice lacking the homeobox gene Dlx 3. Proceedings of the National Academy of Sciences, 96(1), 162â167.

Authors 5

Maria I. Morasso (first)
Alexander Grinberg (additional)
Gertraud Robinson (additional)
Thomas D. Sargent (additional)
Kathleen A. Mahon (additional)

References 35 Referenced 229

M H Kaufman Biology of Trophoblast, eds Y W Loke, A White (Elsevier, Amsterdam), pp. 23–68 (1983). / Biology of Trophoblast by Kaufman M H (1983)
10.1126/science.7985020
10.1210/mend-2-6-579
10.1101/gad.2.12a.1639
10.1242/dev.113.3.815
10.1242/dev.120.11.3257
10.1038/371333a0
10.1242/dev.121.8.2513
10.1101/gad.12.9.1315
10.1016/0012-1606(90)90400-D
T P Lin, I Chen, C MacLeod Dev Biol 170, 756 (1995). / Dev Biol by Lin T P (1995)
10.1016/S0378-1119(96)00706-8
10.1016/S0143-4004(98)90103-5
10.1071/R97025
10.1006/dbio.1997.8640
10.1038/338432a0
G W Robinson, S Wray, K A Mahon New Biol 3, 1183–1194 (1991). / New Biol by Robinson G W (1991)
10.1073/pnas.91.6.2250
10.1006/geno.1996.0634
10.1007/s003359900427
10.1016/0925-4773(94)90060-4
10.1083/jcb.135.6.1879
10.1093/hmg/7.3.563
10.1016/0092-8674(91)90011-M
10.1073/pnas.89.20.9929
10.1016/0092-8674(92)90471-N
10.1016/0092-8674(92)90611-F
10.1016/0012-1606(86)90399-4
10.1073/pnas.81.7.1991
10.1159/000111238
10.1242/dev.112.3.791
10.1038/42022
10.1006/dbio.1997.8556
10.1016/S0896-6273(00)80345-1
J E Long, M Depew, J K Liu, J J Meneses, R A Pedersen, J L R Rubenstein Dev Biol 198, 195 (1998). / Dev Biol by Long J E (1998)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 10:32 a.m.)
Deposited	3 years, 4 months ago (April 13, 2022, 3:41 p.m.)
Indexed	3 weeks, 5 days ago (Aug. 2, 2025, 12:58 a.m.)
Issued	26 years, 7 months ago (Jan. 5, 1999)
Published	26 years, 7 months ago (Jan. 5, 1999)
Published Online	26 years, 7 months ago (Jan. 5, 1999)
Published Print	26 years, 7 months ago (Jan. 5, 1999)

Funders 0

None

BibTeX

@article{Morasso_1999, title={Placental failure in mice lacking the homeobox gene Dlx 3}, volume={96}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.96.1.162}, DOI={10.1073/pnas.96.1.162}, number={1}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Morasso, Maria I. and Grinberg, Alexander and Robinson, Gertraud and Sargent, Thomas D. and Mahon, Kathleen A.}, year={1999}, month=jan, pages={162–167} }

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