Aberrant FGF signaling, independent of ectopic hedgehog signaling, initiates preaxial polydactyly in Dorking chickens

Developmental Biology

Volumn 334, Issue 1, 2009, Pages 133-141

  Bouldin, Cortney M ^a   Harfe, Brian D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Cell death; Fgf; Preaxial polydactyly; Shh

Indexed keywords

FIBROBLAST GROWTH FACTOR 4; SONIC HEDGEHOG PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CHICKEN; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; HINDLIMB; LIMB DEVELOPMENT; MUTANT; NONHUMAN; PATHOGENESIS; POLYDACTYLY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ERINACEIDAE; GALLUS GALLUS;

EID: 69949153826     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.07.009     Document Type: Article

References (62)

1. Ahn S., and Joyner A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118 (2004) 505-516
2. Bell S.M., Schreiner C.M., Waclaw R.R., Campbell K., Potter S.S., and Scott W.J. Sp8 is crucial for limb outgrowth and neuropore closure. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 12195-12200
3. Biesecker L.G. Polydactyly: how many disorders and how many genes?. Am. J. Med. Genet. 112 (2002) 279-283
4. 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
5. Chan D.C., Laufer E., Tabin C., and Leder P. Polydactylous limbs in Strong's Luxoid mice result from ectopic polarizing activity. Development 121 (1995) 1971-1978
6. Chen J.K., Taipale J., Cooper M.K., and Beachy P.A. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16 (2002) 2743-2748
7. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., and Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383 (1996) 407-413
8. Chiang C., Litingtung Y., Harris M.P., Simandl B.K., Li Y., Beachy P.A., and Fallon J.F. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol. 236 (2001) 421-435
9. Columella L. On Agriculture, with a recension of the text and an English translation (1941), Harvard University Press, Cambridge, Massachusetts
10. Crossley P.H., Minowada G., MacArthur C.A., and Martin G.R. Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell 84 (1996) 127-136
11. Darwin C. The Variation of Animals and Plants under Domestication (1890), D. Appleton and Company, New York.
12. Dvorak L., and Fallon J.F. Talpid2 mutant chick limb has anteroposterior polarity and altered patterns of programmed cell death. Anat. Rec. 231 (1991) 251-260
13. Fallon J.F., Lopez A., Ros M.A., Savage M.P., Olwin B.B., and Simandl B.K. FGF-2: apical ectodermal ridge growth signal for chick limb development. Science 264 (1994) 104-107
14. Fernandez-Teran M.A., Hinchliffe J.R., and Ros M.A. Birth and death of cells in limb development: a mapping study. Dev. Dyn. 235 (2006) 2521-2537
15. Fraidenraich D., Lang R., and Basilico C. Distinct regulatory elements govern Fgf4 gene expression in the mouse blastocyst, myotomes, and developing limb. Dev. Biol. 204 (1998) 197-209
16. Francis P.H., Richardson M.K., Brickell P.M., and Tickle C. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 120 (1994) 209-218
17. Grotewold L., and Ruther U. The Wnt antagonist Dickkopf-1 is regulated by Bmp signaling and c-Jun and modulates programmed cell death. EMBO J. 21 (2002) 966-975
18. Hamburger V., and Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morphol. 88 (1951) 49-92
19. 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
20. Hinchliffe J.R., and Ede D.A. Cell death and the development of limb form and skeletal pattern in normal and wingless (ws) chick embryos. J. Embryol. Exp. Morphol. 30 (1973) 753-772
21. Incardona J.P., Gaffield W., Kapur R.P., and Roelink H. The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development 125 (1998) 3553-3562
22. Izpisua-Belmonte J.C., Tickle C., Dolle P., Wolpert L., and Duboule D. Expression of the homeobox Hox-4 genes and the specification of position in chick wing development. Nature 350 (1991) 585-589
23. Kawakami Y., Esteban C.R., Matsui T., Rodriguez-Leon J., Kato S., and Belmonte J.C. Sp8 and Sp9, two closely related buttonhead-like transcription factors, regulate Fgf8 expression and limb outgrowth in vertebrate embryos. Development 131 (2004) 4763-4774
24. Laufer E., Nelson C.E., Johnson R.L., Morgan B.A., and Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79 (1994) 993-1003
25. Lettice L.A., Horikoshi T., Heaney S.J., van Baren M.J., van der Linde H.C., Breedveld G.J., Joosse M., Akarsu N., Oostra B.A., Endo N., et al. Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 7548-7553
26. Lettice L.A., Heaney S.J., Purdie L.A., Li L., de Beer P., Oostra B.A., Goode D., Elgar G., Hill R.E., and de Graaff E. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 12 (2003) 1725-1735
27. Li S., and Muneoka K. Cell migration and chick limb development: chemotactic action of FGF-4 and the AER. Dev. Biol. 211 (1999) 335-347
28. Lu P., Minowada G., and Martin G.R. Increasing Fgf4 expression in the mouse limb bud causes polysyndactyly and rescues the skeletal defects that result from loss of Fgf8 function. Development 133 (2006) 33-42
29. Mariani F.V., Ahn C.P., and Martin G.R. Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature 30 (2008) 30
30. Marigo V., Johnson R.L., Vortkamp A., and Tabin C.J. Sonic hedgehog differentially regulates expression of GLI and GLI3 during limb development. Dev. Biol. 180 (1996) 273-283
31. Marigo V., Scott M.P., Johnson R.L., Goodrich L.V., and Tabin C.J. Conservation in hedgehog signaling: induction of a chicken patched homolog by Sonic hedgehog in the developing limb. Development 122 (1996) 1225-1233
32. Martin G.R. The roles of FGFs in the early development of vertebrate limbs. Genes Dev. 12 (1998) 1571-1586
33. Masuya H., Sagai T., Wakana S., Moriwaki K., and Shiroishi T. A duplicated zone of polarizing activity in polydactylous mouse mutants. Genes Dev. 9 (1995) 1645-1653
34. Masuya H., Sagai T., Moriwaki K., and Shiroishi T. Multigenic control of the localization of the zone of polarizing activity in limb morphogenesis in the mouse. Dev. Biol. 182 (1997) 42-51
35. Mohammadi M., McMahon G., Sun L., Tang C., Hirth P., Yeh B.K., Hubbard S.R., and Schlessinger J. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276 (1997) 955-960
36. Montero J.A., Ganan Y., Macias D., Rodriguez-Leon J., Sanz-Ezquerro J.J., Merino R., Chimal-Monroy J., Nieto M.A., and Hurle J.M. Role of FGFs in the control of programmed cell death during limb development. Development 128 (2001) 2075-2084
37. Niswander L. Interplay between the molecular signals that control vertebrate limb development. Int. J. Dev. Biol. 46 (2002) 877-881
38. Niswander L., Tickle C., Vogel A., Booth I., and Martin G.R. FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75 (1993) 579-587
39. Niswander L., Jeffrey S., Martin G.R., and Tickle C. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371 (1994) 609-612
40. Punnett R.C., and Pease M.S. Genetic studies in poultry VII Notes in polydactyly. J. Genet. 21 (1929) 341-366
41. 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
42. Riley B.B., Savage M.P., Simandl B.K., Olwin B.B., and Fallon J.F. Retroviral expression of FGF-2 (bFGF) affects patterning in chick limb bud. Development 118 (1993) 95-104
43. Roelink H., Augsburger A., Heemskerk J., Korzh V., Norlin S., Ruiz i Altaba A., Tanabe Y., Placzek M., Edlund T., Jessell T.M., et al. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76 (1994) 761-775
44. Ros M.A., Dahn R.D., Fernandez-Teran M., Rashka K., Caruccio N.C., Hasso S.M., Bitgood J.J., Lancman J.J., and Fallon J.F. The chick oligozeugodactyly (ozd) mutant lacks sonic hedgehog function in the limb. Development 130 (2003) 527-537
45. Sanz-Ezquerro J.J., and Tickle C. Autoregulation of Shh expression and Shh induction of cell death suggest a mechanism for modulating polarising activity during chick limb development. Development 127 (2000) 4811-4823
46. Sato K., Koizumi Y., Takahashi M., Kuroiwa A., and Tamura K. Specification of cell fate along the proximal-distal axis in the developing chick limb bud. Development 134 (2007) 1397-1406
47. Saunders J.W. The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108 (1948) 363-403
48. Saunders J.W., and Gasseling M.T. Ectodermal-mesenchymal interactions in the origin of limb symmetry. In: Fleischmajer R., and Billingham R.E. (Eds). Epithelial-Mesenchymal Interactions; 18th Hahnemann Symposium (1968), Williams and Wilkins, Baltimore 78-97
49. 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
50. Sesgin M.Z., and Stark R.B. The incidence of congenital defects. Plast. Reconstr. Surg. Transplant. Bull. 27 (1961) 261-267
51. Sharpe J., Lettice L., Hecksher-Sorensen J., Fox M., Hill R., and Krumlauf R. Identification of sonic hedgehog as a candidate gene responsible for the polydactylous mouse mutant Sasquatch. Curr. Biol. 9 (1999) 97-100
52. 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
53. 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
54. Tanaka M., Cohn M.J., Ashby P., Davey M., Martin P., and Tickle C. Distribution of polarizing activity and potential for limb formation in mouse and chick embryos and possible relationships to polydactyly. Development 127 (2000) 4011-4021
55. Vargesson N., Clarke J.D., Vincent K., Coles C., Wolpert L., and Tickle C. Cell fate in the chick limb bud and relationship to gene expression. Development 124 (1997) 1909-1918
56. Verheyden J.M., and Sun X. An Fgf/Gremlin inhibitory feedback loop triggers termination of limb bud outgrowth. Nature 25 (2008) 25
57. Verheyden J.M., Lewandoski M., Deng C., Harfe B.D., and Sun X. Conditional inactivation of Fgfr1 in mouse defines its role in limb bud establishment, outgrowth and digit patterning. Development 132 (2005) 4235-4245
58. Wilkinson D.G. In situ hybridization: a practical approach (1992), IRL Press, Oxford
59. Yada Y., Makino S., Chigusa-Ishiwa S., and Shiroishi T. The mouse polydactylous mutation, luxate (lx), causes anterior shift of the anteroposterior border in the developing hindlimb bud. Int. J. Dev. Biol. 46 (2002) 975-982
60. Yang Y., Drossopoulou G., Chuang P.T., Duprez D., Marti E., Bumcrot D., Vargesson N., Clarke J., Niswander L., McMahon A., et al. Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development 124 (1997) 4393-4404
61. Zguricas J., Heus H., Morales-Peralta E., Breedveld G., Kuyt B., Mumcu E.F., Bakker W., Akarsu N., Kay S.P., Hovius S.E., et al. Clinical and genetic studies on 12 preaxial polydactyly families and refinement of the localisation of the gene responsible to a 1.9 cM region on chromosome 7q36. J. Med. Genet. 36 (1999) 32-40
62. Zucker R.M., Hunter III E.S., and Rogers J.M. Apoptosis and morphology in mouse embryos by confocal laser scanning microscopy. Methods 18 (1999) 473-480