In the limb AER Bmp2 and Bmp4 are required for dorsal-ventral patterning and interdigital cell death but not limb outgrowth

Developmental Biology

Volumn 327, Issue 2, 2009, Pages 516-523

  Maatouk, Danielle M ^a   Choi, Kyung Suk ^a   Bouldin, Cortney M ^a   Harfe, Brian D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

AER; Bmp; Conditional inactivation; En1; Limb development; Patterning

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR; OSTEOGENIC PROTEIN 1;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENOTYPE; LIMB DEVELOPMENT; MESODERM; MOUSE; NONHUMAN; POLYDACTYLY; PRIORITY JOURNAL; SYNDACTYLY;

MUS; VERTEBRATA;

EID: 60549103019     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.01.004     Document Type: Article

References (40)

1. Ahn K., Mishina Y., Hanks M.C., Behringer R.R., and Crenshaw III E.B. BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development 128 (2001) 4449-4461
2. Bandyopadhyay A., Tsuji K., Cox K., Harfe B.D., Rosen V., and Tabin C.J. Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet. 2 (2006) e216
3. Boulet A.M., Moon A.M., Arenkiel B.R., and Capecchi M.R. The roles of Fgf4 and Fgf8 in limb bud initiation and outgrowth. Dev. Biol. 273 (2004) 361-372
4. Chang W., Lin Z., Kulessa H., Hebert J., Hogan B.L., and Wu D.K. Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements. PLoS Genet. 4 (2008) e1000050
5. Chi C.L., Martinez S., Wurst W., and Martin G.R. The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130 (2003) 2633-2644
6. Harfe B.D., Scherz P.J., Nissim S., Tian H., McMahon A.P., and Tabin C.J. Evidence for an expansion-based temporal shh gradient in specifying vertebrate digit identities. Cell 118 (2004) 517-528
7. Joyner A.L., and Martin G.R. En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene: expression during embryogenesis. Genes Dev. 1 (1987) 29-38
8. Karp S.J., Schipani E., St-Jacques B., Hunzelman J., Kronenberg H., and McMahon A.P. Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development 127 (2000) 543-548
9. Kulessa H., and Hogan B.L. Generation of a loxP flanked bmp4loxP-lacZ allele marked by conditional lacZ expression. Genesis 32 (2002) 66-68
10. Lewandoski M., Sun X., and Martin G.R. Fgf8 signalling from the AER is essential for normal limb development. Nat. Genet. 26 (2000) 460-463
11. Loomis C.A., Harris E., Michaud J., Wurst W., Hanks M., and Joyner A.L. The mouse Engrailed-1 gene and ventral limb patterning. Nature 382 (1996) 360-363
12. Loomis C.A., Kimmel R.A., Tong C.X., Michaud J., and Joyner A.L. Analysis of the genetic pathway leading to formation of ectopic apical ectodermal ridges in mouse Engrailed-1 mutant limbs. Development 125 (1998) 1137-1148
13. Marazzi G., Wang Y., and Sassoon D. Msx2 is a transcriptional regulator in the BMP4-mediated programmed cell death pathway. Dev. Biol. 186 (1997) 127-138
14. Mariani F.V., Ahn C.P., and Martin G.R. Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature 453 (2008) 401-405
15. Murtaugh L.C., Chyung J.H., and Lassar A.B. Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev. 13 (1999) 225-237
16. Ovchinnikov D.A., Selever J., Wang Y., Chen Y.T., Mishina Y., Martin J.F., and Behringer R.R. BMP receptor type IA in limb bud mesenchyme regulates distal outgrowth and patterning. Dev. Biol. 295 (2006) 103-115
17. Pajni-Underwood S., Wilson C.P., Elder C., Mishina Y., and Lewandoski M. BMP signals control limb bud interdigital programmed cell death by regulating FGF signaling. Development 134 (2007) 2359-2368
18. Panman L., Galli A., Lagarde N., Michos O., Soete G., Zuniga A., and Zeller R. Differential regulation of gene expression in the digit forming area of the mouse limb bud by SHH and gremlin 1/FGF-mediated epithelial-mesenchymal signalling. Development 133 (2006) 3419-3428
19. Panman L., and Zeller R. Patterning the limb before and after SHH signalling. J. Anat. 202 (2003) 3-12
20. Parr B.A., and McMahon A.P. Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374 (1995) 350-353
21. Pizette S., Abate-Shen C., and Niswander L. BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb. Development 128 (2001) 4463-4474
22. Plikus M., Wang W.P., Liu J., Wang X., Jiang T.X., and Chuong C.M. Morpho-regulation of ectodermal organs: integument pathology and phenotypic variations in K14-Noggin engineered mice through modulation of bone morphogenic protein pathway. Am. J. Pathol. 164 (2004) 1099-1114
23. Riddle R.D., Ensini M., Nelson C., Tsuchida T., Jessell T.M., and Tabin C. Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 83 (1995) 631-640
24. Riddle R.D., Johnson R.L., Laufer E., and Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75 (1993) 1401-1416
25. Robert B. Bone morphogenetic protein signaling in limb outgrowth and patterning. Dev. Growth Differ. 49 (2007) 455-468
26. Sanz-Ezquerro J.J., and Tickle C. Fgf signaling controls the number of phalanges and tip formation in developing digits. Curr. Biol. 13 (2003) 1830-1836
27. Satokata I., Ma L., Ohshima H., Bei M., Woo I., Nishizawa K., Maeda T., Takano Y., Uchiyama M., Heaney S., Peters H., Tang Z., Maxson R., and Maas R. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat. Genet. 24 (2000) 391-395
28. Saunders, J.W., Gasseling, M.T., 1968. Ectodermal-Mesodermal Interactions in the Origin of Limb Symmetry. Baltimore: Willilams & Wilkins, pp. 78-97.
29. Scherz P.J., Harfe B.D., McMahon A.P., and Tabin C.J. The limb bud Shh-Fgf feedback loop is terminated by expansion of former ZPA cells. Science 305 (2004) 396-399
30. Selever J., Liu W., Lu M.F., Behringer R.R., and Martin J.F. Bmp4 in limb bud mesoderm regulates digit pattern by controlling AER development. Dev. Biol. 276 (2004) 268-279
31. Shore E.M., Xu M., Shah P.B., Janoff H.B., Hahn G.V., Deardorff M.A., Sovinsky L., Spinner N.B., Zasloff M.A., Wozney J.M., and Kaplan F.S. The human bone morphogenetic protein 4 (BMP-4) gene: molecular structure and transcriptional regulation. Calcif. Tissue Int. 63 (1998) 221-229
32. Sun X., Lewandoski M., Meyers E.N., Liu Y.H., Maxson Jr. R.E., and Martin G.R. Conditional inactivation of Fgf4 reveals complexity of signalling during limb bud development. Nat. Genet. 25 (2000) 83-86
33. Sun X., Mariani F.V., and Martin G.R. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418 (2002) 501-508
34. Tickle C. Patterning systems-from one end of the limb to the other. Dev. Cell 4 (2003) 449-458
35. Tsuji K., Bandyopadhyay A., Harfe B.D., Cox K., Kakar S., Gerstenfeld L., Einhorn T., Tabin C.J., and Rosen V. BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat. Genet. 38 (2006) 1424-1429
36. Verheyden J.M., and Sun X. An Fgf/Gremlin inhibitory feedback loop triggers termination of the limb bud outgrowth. Nature (2008) 1-4 on line
37. Wang C.K., Omi M., Ferrari D., Cheng H.C., Lizarraga G., Chin H.J., Upholt W.B., Dealy C.N., and Kosher R.A. Function of BMPs in the apical ectoderm of the developing mouse limb. Dev. Biol. 269 (2004) 109-122
38. Wilkinson D.G. Whole mount in situ hybridization to vertebrate embryos. In: Wilkinson D.G. (Ed). In Situ Hybridization: a Practical Approach (1992), IRL Press, Oxford 75-83
39. Yang Y., Drossopoulou G., Chuang P.T., Duprez D., Marti E., Bumcrot D., Vargesson N., Clarke J., Niswander L., McMahon A., and Tickle C. Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development 124 (1997) 4393-4404
40. Zou H., and Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 272 (1996) 738-741