Generation of pattern and form in the developing limb

International Journal of Developmental Biology

Volumn 53, Issue 5-6, 2009, Pages 805-812

  Towers, Matthew ^a   Tickle, Cheryll ^a  

^a University of Bath   (United Kingdom)

Author keywords

Growth; Limb; Patterning

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; CELL ADHESION; CELL LINEAGE; CELL MOTION; CELL PROLIFERATION; CHICK EMBRYO; DEVELOPMENTAL BIOLOGY; GENE EXPRESSION REGULATION; GENOMICS; HUMAN; LIMB; METHODOLOGY; MORPHOGENESIS; MOUSE; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; CELL ADHESION; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; CHICK EMBRYO; DEVELOPMENTAL BIOLOGY; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMICS; HUMANS; MICE; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 69449096274     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.072499mt     Document Type: Review

References (81)

1. ALLEN, F., TICKLE, C. and WARNER, A. (1990). The role of gap junctions in patterning of the chick limb bud. Development 108: 623-634.
2. ALTABEF, M., CLARKE, J.D. and TICKLE, C. (1997). Dorso-ventral ectodermal compartments and origin of apical ectodermal ridge in developing chick limb. Development 124: 4547-4556.
3. AMPRINO, R. (1977). Morphogenetic interrelationships between ectoderm and mesoderm in chick embryo limb development. In Vertebrate Limb and Somite Morphogenesis. (Ed. Ede, D.A., Hinchliffe, R. and Balls, M.J. ) Cambridge University Press, Cambridge.
4. ARAUJO, M., PIEDRA, M.E., HERRERA, M.T., ROS, M.A. and NIETO, M.A. (1998). The expression and regulation of chick EphA7 suggests roles in limb patterning and innervation. Development 125: 4195-4204.
5. ARQUES, C.G., DOOHAN, R., SHARPE, J. and TORRES, M. (2007). Cell tracing reveals a dorsoventral lineage restriction plane in the mouse limb bud mesenchyme. Development 134: 3713-3722.
6. BARNA, M. and NISWANDER, L. (2007). Visualization of cartilage formation: insight into cellular properties of skeletal progenitors and chondrodysplasia syndromes. Dev Cell 12: 931-941.
7. BASTIDA, M.F., ROS, M.A. (2008). How do we get a perfect complement of digits? Curr Opin Genet Dev 18: 374-380.
8. BLASCHKE, R.J. and RAPPOLD, G. (2006). The pseudoautosomal regions, SHOX and disease. Curr Opin Genet Dev 16: 233-239.
9. BOWEN, J., HINCHLIFFE, J.R., HORDER, T.J. and REEVE, A.M. (1989). The fate map of the chick forelimb-bud and its bearing on hypothesized developmental control mechanisms. Anat Embryol (Berl) 179: 269-283.
10. BROCKES, J.P. (1992). Introduction of a retinoid reporter gene into the urodele limb blastema. Proc Natl Acad Sci U S A 89: 11386-11390.
11. CAMERON, J.A. and FALLON, J.F. (1977). The absence of cell death during development of free digits in amphibians. Dev Biol 55: 331-338.
12. CHIANG, C., LITINGTUNG, Y., LEE, E., YOUNG, K.E., CORDEN, J.L., WESTPHAL, H. and BEACHY, P.A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
13. CLARKE, J.D. and TICKLE, C. (1999). Fate maps old and new. Nat Cell Biol 1: E103-E109.
14. COOKE, J. and SUMMERBELL, D. (1980). Cell cycle and experimental pattern duplication in the chick wing during embryonic development. Nature 287: 697-701.
15. DAHN, R.D. and FALLON, J.F. (2000). Interdigital regulation of digit identity and homeotic transformation by modulated BMP signaling. Science 289: 438-441.
16. DAWD, D.S. and HINCHLIFFE, J.R. (1971). Cell death in the «opaque patch» in the central mesenchyme of the developing chick limb: a cytological, cytochemical and electron microscopic analysis. J Embryol Exp Morphol 26: 401-424.
17. DUDLEY, A.T., ROS, M.A. and TABIN, C.J. (2002). A re-examination of proximodistal patterning during vertebrate limb development. Nature 418: 539-544.
18. DVORAK, L. and FALLON, J.F. (1991). Talpid2 mutant chick limb has anteroposterior polarity and altered patterns of programmed cell death. Anat Rec 231: 251-260.
19. ECHEVERRI, K. and TANAKA, E.M. (2005). Proximodistal patterning during limb regeneration. Dev Biol 279: 391-401.
20. EDE, D.A. (1977). The development of pre-cartilage condensations in limb bud mesencyme in vivo and in vivo. In Vertebrate Limb and Somite Morphogenesis (Ed. Ede, D.A., Hinchliffe, R. and Balls, M.J.). Cambridge University Press, Cambridge, pp. 161-180.
21. EDE, D.A. and KELLY, W.A. (1964). Developmental Abnormalities in the Trunk and Limbs of the Talpid3 Mutant of the Fowl. J Embryol Exp Morphol 12: 339-356.
22. ERRICK, J.E. and SAUNDERS, J.W., JR. (1976). Limb outgrowth in the chick embryo induced by dissociated and reaggregated cells of the apical ectodermal ridge. Dev Biol 50: 26-34.
23. FALLON, J.F., LOPEZ, A., ROS, M.A., SAVAGE, M.P., OLWIN, B.B. and SIMANDL, B.K. (1994). FGF-2: apical ectodermal ridge growth signal for chick limb development. Science 264: 104-107.
24. FERNANDEZ-TERAN, M.A., HINCHLIFFE, J.R. and ROS, M.A. (2006). Birth and death of cells in limb development: a mapping study. Dev Dyn 235: 2521-2537.
25. FERNANDEZ-TERAN, M.A. and ROS, M.A. (2008). The Apical Ectodermal Ridge: morphological aspects and signaling pathways. Int. J. Dev. Biol. 52: 857-871.
26. FRANCIS-WEST, P and HILL, R. (2008). Uncoupling the role of sonic hedgehog in limb development: growth and specification. Sci Signal. 26: 34.
27. GREEN, C.R., BOWLES, L., CRAWLEY, A. and TICKLE, C. (1994). Expression of the connexin43 gap junctional protein in tissues at the tip of the chick limb bud is related to the epithelial-mesenchymal interactions that mediate morphogenesis. Dev Biol 161: 12-21.
28. GUMPEL-PINOT, M., EDE, D.A. and FLINT, O.P. (1984). Myogenic cell movement in the developing avian limb bud in presence and absence of the apical ectodermal ridge (AER). J Embryol Exp Morphol 80: 105-125.
29. HARDY, A., RICHARDSON, M.K., FRANCIS-WEST, P.H., RODRIGUEZ, C., IZPISUA-BELMONTE, J.C., DUPREZ, D. and WOLPERT, L. (1995). Gene expression, polarising activity and skeletal patterning in reaggregated hind limb mesenchyme. Development 121: 4329-4337.
30. HARFE, B.D., SCHERZ, P.J., NISSIM, S., TIAN, H., MCMAHON, A.P. and TABIN, C.J. (2004). Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118: 517-528.
31. KIENY, M. (1977). Proximo-distal pattern formation in vertebrate limb development. In Vertebrate Limb and Somite Morphogenesis (Ed. Ede, D.A., Hinchliffe, R. and Balls, M.J.) . Cambridge UniversityPress, Cambridge.
32. KIMMEL, R.A., TURNBULL, D.H., BLANQUET, V., WURST, W., LOOMIS, C.A. and JOYNER, A.L. (2000). Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev 14: 1377-1389.
33. KOSTAKOPOULOU, K., VARGESSON, N., CLARKE, J.D., BRICKELL, P.M. and TICKLE, C. (1997). Local origin of cells in FGF-4 - induced outgrowth of amputated chick wing bud stumps. Int J Dev Biol 41: 747-750.
34. LI, S. and MUNEOKA, K. (1999). Cell migration and chick limb development: chemotactic action of FGF-4 and the AER. Dev Biol 211: 335-347.
35. LI, X., LIU, J, DAVEY, M, DUCE, S, JABERI, N, LIU, G, DAVIDSON, G, TENENT, S, MAHOOD, R, BROWN, P, CUNNINGHAM, C, BAIN, A, BEATTIE, K, MCDONALD, L, SCHMIDT, K, TOWERS, M, TICKLE, C AND CHUDEK, S. (2007). Micro-magnetic resonance imaging of avian embryos. J. Anatomy 211: 798-809.
36. LOGAN, M., MARTIN, J.F., NAGY, A., LOBE, C., OLSON, E.N. and TABIN, C.J. (2002). Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33: 77-80.
37. MADEN, M. (1982). Vitamin A and pattern formation in the regenerating limb. Nature 295: 672-675.
38. MAKARENKOVA, H., BECKER, D.L., TICKLE, C. and WARNER, A.E. (1997). Fibroblast growth factor 4 directs gap junction expression in the mesenchyme of the vertebrate limb Bud. J Cell Biol 138: 1125-1137.
39. MARIANI, F.V., AHN, C.P., MARTIN, G.R. (2008). Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature 453: 401-5.
40. MERCADER, N., LEONARDO, E., PIEDRA, M.E., MARTINEZ, A.C., ROS, M.A. and TORRES, M. (2000). Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 127: 3961-3970.
41. MEYER, R.A., COHEN, M.F., RECALDE, S., ZAKANY, J., BELL, S.M., SCOTT, W.J., JR. and LO, C.W. (1997). Developmental regulation and asymmetric expression of the gene encoding Cx43 gap junctions in the mouse limb bud. Dev Genet 21: 290-300.
42. NARDI, J.B. and STOCUM, D. L. (1984). Surface properties of regenerating limb cells: Evidence for gradation along the proximodistal axis. Differentiation 25: 27-31.
43. NISSIM, S., ALLARD, P., BANDYOPADHYAY, A., HARFE, B.D. and TABIN, C.J. (2007). Characterization of a novel ectodermal signaling center regulating Tbx2 and Shh in the vertebrate limb. Dev Biol 304: 9-21.
44. NISWANDER, L. (2003). Pattern formation: old models out on a limb. Nat Rev Genet 4: 133-143.
45. NISWANDER, L., JEFFREY, S., MARTIN, G.R. and TICKLE, C. (1994). A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371: 609-612.
46. NISWANDER, L., TICKLE, C., VOGEL, A., BOOTH, I. and MARTIN, G.R. (1993). FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75: 579-587.
47. PEARSE, R.V., 2ND, SCHERZ, P.J., CAMPBELL, J.K. and TABIN, C.J. (2007). A cellular lineage analysis of the chick limb bud. Dev Biol 310: 388-400.
48. PIZARD, A., BURGON, P.G., PAUL, D.L., BRUNEAU, B.G., SEIDMAN, C.E. and SEIDMAN, J.G. (2005). Connexin 40, a target of transcription factor Tbx5, patterns wrist, digits, and sternum. Mol Cell Biol 25: 5073-5083.
49. 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. (2003). The chick oligozeugodactyly (ozd) mutant lacks sonic hedgehog function in the limb. Development 130: 527-537.
50. ROS, M.A., LYONS, G.E., MACKEM, S. and FALLON, J.F. (1994). Recombinant limbs as a model to study homeobox gene regulation during limb development. Dev Biol 166: 59-72.
51. SALSI, V. and ZAPPAVIGNA, V. (2006). Hoxd13 and Hoxa13 directly control the expression of the EphA7 Ephrin tyrosine kinase receptor in developing limbs. J Biol Chem 281: 1992-1999.
52. SATO, K., KOIZUMI, Y., TAKAHASHI, M., KUROIWA, A. and TAMURA, K. (2007). Specification of cell fate along the proximal-distal axis in the developing chick limb bud. Development 134: 1397-1406.
53. SAUNDERS, J.W. and GASSELING, M.T. (1968). Ectodermal-mesenchymal interactions in the origin of limb symmetry. In mesenchymal-epithelial interactions (ed. R. Fleichmeyer and R. E. Billingham), illiams and Wilkins , Baltimore, pp. 78-97.
54. SAUNDERS, J.W., JR. (1948). The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm.. J Exp Zool 282: 628-668.
55. SAUNDERS, J.W., JR. and GASSELING, M.T. (1962). Cellular death in morphogenesis of the avian wing. Dev Biol 5: 147-178.
56. SHARPE, J., AHLGREN, U., PERRY, P., HILL, B., ROSS, A., HECKSHERSORENSEN, J., BALDOCK, R. and DAVIDSON, D. (2002). Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296: 541-545.
57. SMITH, J.C. (1979). Evidence for a positional memory in the development of the chick wing bud. J Embryol Exp Morphol 52: 105-113.
58. SMITH, J.C. and WOLPERT, L. (1981). Pattern formation along the anteroposterior axis of the chick wing: the increase in width following a polarizing region graft and the effect of X-irradiation. J Embryol Exp Morphol 63: 127-144.
59. SUMMERBELL, D., LEWIS, J.H. and WOLPERT, L. (1973). Positional information in chick limb morphogenesis. Nature 244: 492-496.
60. SUMMERBELL, D. and WOLPERT, L. (1972). Cell density and cell division in the early morphogenesis of the chick wing. Nat New Biol 239: 24-26.
61. TABIN, C. and WOLPERT, L. (2007). Rethinking the proximodistal axis of the vertebrate limb in the molecular era. Genes Dev 21: 1433-1442.
62. TABIN, C.J, MCMAHON, A.P. (2008). Developmental biology. Grasping limb patterning. Science 321: 350-352.
63. TAMURA, K., YOKOUCHI, Y., KUROIWA, A. and IDE, H. (1997). Retinoic acid changes the proximodistal developmental competence and affinity of distal cells in the developing chick limb bud. Dev Biol 188: 224-234.
64. TICKLE, C. (2006). Making digit patterns in the vertebrate limb. Nature Reviews Molecular Biology 7: 45-53.
65. TICKLE, C., ALBERTS, B., WOLPERT, L. and LEE, J. (1982). Local application of retinoic acid to the limb bond mimics the action of the polarizing region. Nature 296: 564-566.
66. TICKLE, C., GOODMAN, M. and WOLPERT, L. (1978). Cell contacts and sorting out in vivo: the behaviour of some embryonic tissues implanted into the developing chick wing. J Embryol Exp Morphol 48: 225-237.
67. TODT, W.L. and FALLON, J.F. (1986). Development of the apical ectodermal ridge in the chick leg bud and a comparison with the wing bud. Anat Rec 215: 288-304.
68. TOOLE, B.P., MUNAIM, S.I., WELLES, S. and KNUDSON, C.B. (1989). Hyaluronate-cell interactions and growth factor regulation of hyaluronate synthesis during limb development. Ciba Found Symp 143: 138-45.
69. TOWERS, M., MAHOOD, R., YIN, Y., TICKLE C. (2008). Integration of growth and specification in chick wing digit-patterning. Nature 452: 882-6.
70. TOWERS, M and TICKLE, C. (2009). Growing models of vertebrate limb development. Development 136: 179-190.
71. TRELSTAD, R.L. (1977). Mesenchymal cell polarity and morphogenesis of chick cartilage. Dev Biol 59: 153-163.
72. VARGESSON, N., CLARKE, J.D., VINCENT, K., COLES, C., WOLPERT, L. and TICKLE, C. (1997). Cell fate in the chick limb bud and relationship to gene expression. Development 124: 1909-1918.
73. VARGESSON, N., PATEL, K., LEWIS, J. and TICKLE, C. (1998). Expression patterns of Notch1, Serrate1, Serrate2 and Delta1 in tissues of the developing chick limb. Mech Dev 77: 197-199.
74. WADA, N. and IDE, H. (1994). Sorting out of limb bud cells in monolayer culture. Int J Dev Biol 38: 351-356.
75. YALLUP, B.L., AND J.R. HINCHLIFFE. (1983). Regulation along the anteroposterior axis of the chick wing bud. In Limb Development and Regeneration, Part A. (Ed. J.F. Fallon and A.I. Caplan), Alan R. Liss, Inc., New York, pp. 131-140.
76. YANG, X., DORMANN, D., MUNSTERBERG, A.E. and WEIJER, C.J. (2002). Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev Cell 3: 425-437.
77. ZHU, J., NAKAMURA, E., NGUYEN, M.T., BAO, X., AKIYAMA, H. and MACKEM. S. (2008). Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev Cell. 14: 624-632.
78. ZUNIGA, A., HARAMIS, A.P., MCMAHON, A.P. and ZELLER, R. (1999). Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature 401: 598-602.
79. ZUZARTE-LUIS, V. and HURLE, J.M. (2002). Programmed cell death in the developing limb. Int J Dev Biol 46: 871-876.
80. ZWILLING, E. (1964). Development of Fragmented and of Dissociated Limb Bud Mesoderm. Dev Biol 89: 20-37.
81. ZWILLING, E. and HANSBOROUGH, L. (1956). Interactions between limb bud ectoderm and mesoderm in the chick embryo. III. Experiments with polydactylous limbs. J Exp Zoo 132: 219-239.