Engrailed-1 misexpression in chick embryos prevents apical ridge formation but preserves segregation of dorsal and ventral ectodermal compartments

Developmental Biology

Volumn 222, Issue 2, 2000, Pages 307-316

  Altabef, Muriel ^a,b   Logan, Cairine ^a   Tickle, Cheryll ^b   Lumsden, Andrew ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Compartment; En 1; Limb development; Rhodamine dextran; Selector gene

Indexed keywords

RHODAMINE;

ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CELL COMPARTMENTALIZATION; CELL LINEAGE; CHICK EMBRYO; CONTROLLED STUDY; ECTODERM; EMBRYO; GENE DISRUPTION; GENE EXPRESSION; GENE FUNCTION; LIMB DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA; VERTEBRATA;

EID: 0034660129     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2000.9659     Document Type: Article

References (48)

1. Altabef M., Clarke J. D., Tickle C. Dorso-ventral ectodermal compartments and origin of apical ectodermal ridge in developing chick limb. Development. 124:1997;4547-4556.
2. Blair S. S. Compartments and appendage development in Drosophila. Bioessays. 17:1995;299-309.
3. Blair S. S., Ralston A. Smoothened-mediated Hedgehog signalling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila. Development. 124:1997;4053-4063.
4. Chen H., Lun Y., Ovchinnikov D., Kokubo H., Oberg K. C., Pepicelli C. V., Gan L., Lee B., Johnson R. L. Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nature Genet. 19:1998;51-55.
5. Cohn M. J., Izpisua B. J., Abud H., Heath J. K., Tickle C. Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell. 80:1995;739-746.
6. Cygan J. A., Johnson R. L., McMahon A. P. Novel regulatory interactions revealed by studies of murine limb pattern in Wnt-7a and En-1 mutants. Development. 124:1997;5021-5032.
7. Davis C. A., Holmyard D. P., Millen K. J., Joyner A. L. Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum. Development. 111:1991;287-298.
8. Dealy C. N., Roth A., Ferrari D., Brown A. M., Kosher R. A. Wnt-5a and Wnt-7a are expressed in the developing chick limb bud in a manner suggesting roles in pattern formation along the proximodistal and dorsoventral axes. Mech. Dev. 43:1993;175-186.
9. Diaz-Benjumea F. J., Cohen S. M. Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell. 75:1993;741-752.
10. Fekete D. M., Cepko C. L. Replication-competent retroviral vectors encoding alkaline phosphatase reveal spatial restriction of viral gene expression/transduction in the chick embryo. Mol. Cell. Biol. 13:1993;2604-2613.
11. Figdor M. C., Stern C. D. Segmental organization of embryonic diencephalon. Nature. 363:1993;630-634.
12. Fraser S., Keynes R., Lumsden A. Segmentation in the chick embryo hindbrain is defined by cell lineage restriction. Nature. 344:1990;431-435.
13. Garcia-Bellido A., Ripoll P., Morata G. Developmental compartmentalisation of the wing disk of Drosophila. Nature New Biol. 245:1973;251-253.
14. Garcia-Bellido A. Genetic control of wing disc development in Drosophila. Ciba Found. Symp. 29:1975;161-182.
15. Gardner C. A., Barald K. F. Expression patterns of engrailed-like proteins in the chick embryo. Dev. Dynam. 193:1992;370-388.
16. Grieshammer U., Minowada G., Pisenti J. M., Abbott U. K., Martin G. R. The chick limbless mutation causes abnormalities in limb bud dorsal-ventral patterning: implications for the mechanism of apical ridge formation. Development. 122:1996;3851-3861.
17. Guillen I., Mullor J. L., Capdevila J., Sanchez-Herrero E., Morata G., Guerrero I. The function of engrailed and the specification of Drosophila wing pattern. Development. 121:1995;3447-3456.
18. Hamburger V., Hamilton H. L. A series of normal stages in the development of the chick embryo. J. Exp. Morphol. 88:1951;49-92.
19. Hanks M. C., Loomis C. A., Harris E., Tong C. X., Anson-Cartwright L., Auerbach A., Joyner A. Drosophila engrailed can substitute for mouse Engrailed1 function in mid-hindbrain, but not limb development. Development. 125:1998;4521-4530.
20. Hidalgo A. Three distinct roles for the engrailed gene in Drosophila wing development. Curr. Biol. 4:1994;1087-1098.
21. Hidalgo A. The roles of engrailed. Trends Genet. 12:1996;1-4.
22. Johnson R. L., Tabin C. J. Molecular models for vertebrate limb development. Cell. 90:1997;979-990.
23. Kengaku M., Capdevila J., Rodriguez-Esteban C., De La Pena J., Johnson R. L., Belmonte J. C. I., Tabin C. J. Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science. 280:1998;1274-1277.
24. Laufer E., Dahn R., Orozco O. E., Yeo C.-Y., Pisenti J., Henrique D., Ursula K. A., Fallon J. F., Tabin C. Expression of Radical Fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature. 386:1997;366-373.
25. Lawrence P. A., Morata G. Compartments in the wing of Drosophila: A study of the engrailed gene. Dev. Biol. 50:1976;321-337.
26. Lawrence P. A., Struhl G. Morphogens, compartments, and pattern: Lessons from Drosophila? Cell. 85:1996;951-961.
27. Logan C., Wizenmann A., Drescher U., Monschau B., Bonhoeffer F., Lumsden A. Rostral optic tectum acquires caudal characteristics following ectopic engrailed expression. Curr. Biol. 6:1996;1006-1014.
28. Logan C. C., Hornbruch A., Campbell I., Lumsden A. The role of Engrailed in establishing the dorso-ventral axis in chick limb. Development. 124:1997;2317-2324.
29. Loomis C. A., Harris E., Michaud J., Wurst W., Hanks M., Joyner A. L. The mouse Engrailed-1 gene and ventral limb patterning. Nature. 382:1996;360-363.
30. Loomis C. A., Kimmel R. A., Tong C. X., Michaud J., 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.
31. Meinhardt H. A boundary model for pattern formation in vertebrate limbs. J. Embryol. Exp. Morphol. 76:1983;115-137.
32. Morata G., Lawrence P. A. Control of compartment development by the engrailed gene in Drosophila. Nature. 255:1975;614-617.
33. Nittenberg R., Patel K., Joshi Y., Krumlauf R., Wilkinson D. G., Brickell P. M., Tickle C., Clarke J. D. W. Cell movements, neuronal organisation and gene expression in hindbrains lacking morphological boundaries. Development. 124:1997;2297-2306.
34. Noramly S., Pisenti J., Abbott U., Morgan B. Gene expression in the limbless mutant: Polarized gene expression in the absence of Shh and an AER. Dev. Biol. 179:1996;339-346.
35. Parr B. A., 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.
36. Riddle R. D., Ensini M., Nelson C., Tsuchida T., Jessell T. M., Tabin C. Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell. 83:1995;631-640.
37. Rodriguez-Esteban C., Schwabe J. W. R., De La Peña J., Foys B., Eshelman B., Izpisùa Belmonte J. C. Radical Fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature. 386:1997;360-366.
38. Rodriguez-Esteban C., Schwabe J. W., Pena J. D., Rincon-Limas D. E., Magallon J., Botas J., Belmonte J. C. Lhx2, a vertebrate homologue of apterous, regulates vertebrate limb outgrowth [in process citation]. Development. 125:1998;3925-3934.
39. Ros M. A., Lopez M. A., Simandl B. K., Rodriguez C., Izpisua B. J., Dahn R., Fallon J. F. The limb field mesoderm determines initial limb bud anteroposterior asymmetry and budding independent of sonic hedgehog or apical ectodermal gene expressions. Development. 122:1996;2319-2330.
40. Schwabe J. W., Rodriguez-Esteban C., Izpisua Belmonte J. C. Limbs are moving: Where are they going? Trends Genet. 14:1998;229-235.
41. Simmonds A. J., Brook W. J., Cohen S. M., Bell J. B. Distinguishable functions for engrailed and invected in anterior-posterior patterning in the Drosophila wing. Nature. 376:1995;424-427.
42. Tabata T., Schwartz C., Gustavson E., Ali Z., Kornberg T. B. Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development. 121:1995;3359-3369.
43. Takada S., Stark K. L., Shea M. J., Vassileva G., McMahon J. A., McMahon A. P. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8:1994;174-189.
44. Vogel A., Rodriguez C., Warnken W., Izpisua Belmonte J. C. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature. 378:1995;716-720.
45. Wilkinson D. G. Whole-Mount in Situ Hybridisation of Vertebrate Embryos. 1992;IRL Press, Oxford.
46. Wizenmann A., Lumsden A. Segregation of rhombomeres by differential chemoaffinity. Mol. Cell. Neurosci. 9:1997;448-459.
47. Wurst W., Auerbach A. B., Joyner A. L. Multiple developmental defects in Engrailed-1 mutant mice: An early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development. 120:1994;2065-2075.
48. Zecca M., Basler K., Struhl G. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development. 121:1995;2265-2278.