Molecular mechanisms in the control of limb regeneration: The role of homeobox genes

International Journal of Developmental Biology

Volumn 40, Issue 4, 1996, Pages 797-805

  Gardiner, David M ^a   Bryant, Susan V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Homeobox; Limbs; Pattern formation; Regeneration; Retinoic acid

Indexed keywords

RETINOIC ACID;

AMBYSTOMA; BLASTEMA; GENE EXPRESSION; HOMEOBOX; LIMB DEVELOPMENT; LIMB REGENERATION; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

AMBYSTOMA; ANIMALS; BODY PATTERNING; EXTREMITIES; GENES, HOMEOBOX; MODELS, BIOLOGICAL; REGENERATION;

EID: 0029792120     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (75)

1. BEAUCHEMIN, M. and SAVARD, P (1992). Two Distal-less related homeobox-containing genes expressed in regenerating blastemas of the newt. Dev Biol 154: 55-56
2. BEAUCHEMIN, M. and SAVARD, P (1993). Expression of five homeobox genes in the adult newt appendages and regeneration blastemas. In Limb Development and Regeneration (Eds. J.F. Fallon, P F. Goetinck, R O Kelley and D.L Stocum). Wiley-Liss, New York, pp. 41-50.
3. BOILLY, B., CAVANAUGH, K.P., THOMAS, D , HONDERMARCK, H , BRYANT, S.V and BRADSHAW, R A (1991). Acidic fibroblast growth factor is present in regenerating limb blastemas of axolotls and binds specifically to blastema tissues Dev. Biol 145: 302-310
4. BORGENS, R B (1982). Mice regrow the tips of their foretoes. Science 217. 747-750.
5. BROWN, R and BROCKES, J P. (1991). Identification and expression of a regeneration-specific homeobox gene in the newt limb blastema. Development 111: 489-496.
6. BRYANT, S.V and GARDINER, D M. (1992) Retinoic acid, local cell-cell interactions, and pattern formation in vertebrate limbs Dev. Biol 152: 1-25.
7. BRYANT, S.V , FRENCH, V. and BRYANT, P.J. (1981). Distal regeneration and symmetry. Science 212: 993-1002.
8. CARRASCO, A.E., MCGINNIS, W., GEHRING, W J. and DE ROBERTIS, E.M. (1984). Cloning of an X. laevis gene expressed during early embryogenesis coding for a peptide region homologous to Drosophila homeotic genes. Cell 37: 409-414.
9. CHARITÉ, J., DE GRAAFF, W., SHEN, S. and DESCHAMPS, J. (1994). Ectopic expression of Hoxb-8 causes duplication of the ZPA in the forelimb and homeotic transformation of axial structures. Cell 78: 589-601.
10. CONDIE, B.G. and CAPECCHI, M.R (1994). Mice with targeted disruptions in the paralogous genes hoxa-3 and hoxd-3 reveal synergistic interactions. Nature 370: 304-307.
11. CREWS, L., GATES, P.B., BROWN, R., JOLIOT, A , FOLEY, C , BROCKES, J.P and GANN, A.A. (1995). Expression and activity of the newt Msx-1 gene in relation to limb regeneration Proc R. Soc Lond. B Biol Sci. 259. 161-171.
12. DAVIS, A P. and CAPECCHI, M.R. (1994). Axial homeosis and appendicular skeleton defects in mice with a targeted disruption of hoxd-11. Development 120: 2187-2198.
13. DENT, J.N. (1962). Limb regeneration in larvae and metamorphosing individuals of the South African clawed toad. J. Morphol. 110. 61-77.
14. DOLLÉ, P., DIERICH, A., LEMEUR, M., SCHIMMANG, T., SCHUHBAUR, B., CHAMBON, P. and DUBOULE, D (1993). Disruption of Hoxd-13 gene induces localized heterochrony leading to mice with neotenic limbs Cell 75:431 -441.
15. DOLLÉ, P , IZPISUA-BELMONTE, J-C , FALKENSTEIN, H., RENUCCI, A. and DUBOULE, D. (1989). Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern formation. Nature 342: 767-772.
16. DOLLÉ, P., PRICE, M. and DUBOULE, D. (1992). Expression of the murine Dlx-1 homeobox gene during facial, ocular and limb development. Differentiation 49: 93-99.
17. DUBOULE, D. (1994a). Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development (Suppl.). 135-142.
18. DUBOULE, D (1994b). Guidebook to the Homeobox Genes. Oxford University Press, Oxford
19. DUBOULE, D. and MORATA, G. (1994). Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet 10. 358-364.
20. 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
21. FRENCH, V., BRYANT, P.J and BRYANT, S V. (1976) Pattern regulation in epimorphic fields Science 193: 969-981.
22. GARDINER, D.M and BRYANT, S.V. (1989) Organization of positional information in the axolotl limb. J. Exp. Zool. 251. 47-55.
23. GARDINER, D.M , BLUMBERG, B., KOMINE, Y. and BRYANT, S.V. (1995). Regulation of HoxA expression in developing and regenerating axolotl limbs. Development 121. 1731-1741.
24. GARDINER, D M., MUNEOKA, K and BRYANT, S.V (1986). The migration of dermal cells during blastema formation in axolotls. Dev Biol. 118: 488-493
25. GRAHAM, A. (1994). Developmental patterning-The Hox code out on a limb. Curr. Biol 4: 1135-1137.
26. HAACK, H. and GRUSS, P. (1993). The establishment of murine Hox-1 expression domains during patterning of the limb. Dev. Biol 157: 410-422.
27. HAYAMIZU, T F and BRYANT, S V (1994) Reciprocal changes in Hox D13 and RAR-ß2 expression in response to retinoic acid in chick limb buds. Dev. Biol. 166. 123-132.
28. HAYAMIZU, T.F , WANEK, N., TAYLOR, G , TREVINO, C , SHI, C., ANDERSON, R., GARDINER, D M., MUNEOKA, K and BRYANT, S V. (1994). Regeneration of HoxD expression domains during pattern regulation in chick wing buds. Dev Biol. 161: 504-512.
29. IZPISUA-BELMONTE, J-C. and DUBOULE, D. (1992). Homeobox genes and pattern formation in the vertebrate limb. Dev. Biol. 152: 26-36.
30. IZPISUA-BELMONTE, J-C., TICKLE, C , DOLLE, P , WOLPERT, L. and DUBOULE, D. (1991). Expression of the homeobox Hox-4 genes and the specification of position in chick wing development. Nature 350 585-589
31. JOHNSON, R.L., RIDDLE, R.D. and TABIN, C.J. (1994) Mechanisms of limb patterning. Curr Opin. Genet Dev. 4: 535-542.
32. KAPPEN, C., SCHUGHART, K. and RUDDLE, F H (1993). Early evolutionary origin of major homeodomain sequence classes. Genomics 18: 54-70.
33. KESSEL, M. and GRUSS, P. (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67 89-104.
34. KRUMLAUF, R. (1994) Hox genes in vertebrate development. Cell 78: 191-201
35. MADEN, M. (1982) Vitamin A and pattern formation in the regenerating limb. Nature 295: 672-675.
36. MCGINNIS, N., KUZIORA, M.A and MCGINNIS, W. (1990). Human Hox-4.2 and Drosophila deformed encode similar regulatory specificities in Drosophila embryos and larvae. Cell 63: 969-976.
37. MCGINNIS, W., GARBER, R.L , WIRZ, J., KUROIWA, A and GEHRING, W.J. (1984). A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 37: 403-408
38. MENDELSOHN, C , LOHNES, D , DÉCIMO, D., LUFKIN, T., LEMEUR, M., CHAMBON, P. and MARK, M. (1994). Function of the retinoic acid receptors (RARs) during development. (II) Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120: 2749-2771.
39. MENDELSOHN, C., RUBERTE, E., LEMEUR, M., MORRISS-KAY, G. and CHAMBON, P. (1991). Developmental analysis of the retinoic acid-inducible RAR-B2 promoter in transgenic animals. Development 113. 723-734.
40. MESCHER, A.L. and LOH, J.J. (1981). Newt forelimb regeneration blastemas in vitro: cellular response to explanation and effects of various growth-promoting substances. J. Exp. Zool. 216. 235-45.
41. MORGAN, B.A., IZPISUA-BELMONTE, J-C., DUBOULE, D. and TABIN, C.J (1992). Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358: 236-239.
42. MUNEOKA, K. and SASSOON, D. (1992). Limb development and regeneration. Dev. Biol. 152: 37-49.
43. 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
44. 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.
45. NOHNO, T., NOJI, S., KOYAMA, E., OHYAMA, K., MYOKAI, F., KUROIWA, A., SAITO, T. and TANIGUCHI, S. (1991). Involvement of the Chox-4 chicken homeobox genes in determination of anteroposterior axial polarity during limb development. Cell 64: 1197-1205.
46. NOJI, S., NOHNO, T., KOYAMA, E , MUTO, K., OHYAMA, K., AOKI, Y., TAMURA, K., OHSUGi, K , IDE, H , TANIGUCHI, S. and SAITO, T. (1991) Retinoic acid induces polarizing activity but is unlikely to be a morphogen in the chick limb bud. Nature 350. 83-86
47. OLIVER, G., WRIGHT, C.V., HARDWICKE, J. and DE ROBERTIS, E M (1988). A gradient of homeodomain protein in developing forelimbs of Xenopus and mouse embryos. Cell 55 1017-1024.
48. POULIN, M.L., PATRIE, K.M., BOTELHO, M.J., TASSAVA, R A. and CHIU, I M. (1993) Heterogeneity in the expression of fibroblast growth factor receptors during limb regeneration in newts (Notophthalmus viridescens). Development 119: 353-361.
49. ROS, M A., LYONS, G., A., K.R., UPHOLT, W.B., COEHLO, C.N.D. and FALLON, J.F. (1992) Apical ridge dependent and independent domains of GHox-7 and GHox-8 expression in chick limb buds. Development 116. 811-818.
50. ROSSANT, J., ZIRNGIBL, R., CADO, D , SHAGO, M. and GIGUERE, V. (1991). Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis Genes Dev. 5: 1333-1344
51. RUBIN, L. and SAUNDERS, J.W Jr. (1972) Ectodermal-mesodermal interactions in the growth of limb buds in the chick embryo constancy and temporal limits of the ectodermal induction. Dev. Biol. 28: 94-112.
52. SAUNDERS, J.W. Jr. (1948) The proximo-distal sequence of origin of the parts of the chick wing and the role of ectoderm. J. Exp. Zool. 108: 363-403.
53. SAVARD, P., GATES, P.B. and BROCKES, J P. (1988) Position dependent expression of a homeobox gene transcript in relation to amphibian limb regeneration. EMBO J. 7: 4275-4282.
54. SCOTT, M.P. and WEINER, A.J. (1984). Structural relationships among genes that control development, sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc. Natl Acad. Sci. USA 81: 4115-9.
55. SESSIONS, S.K. and BRYANT, S.V. (1988). Evidence that regenerative ability is an intrinsic property of limb cells in Xenopus J. Exp Zool. 247. 39-44.
56. SIMEONE, A., ACAMPORA, D., NIGRO, V., FAIELLA, A., D'ESPOSITO, M., STORNAIUOLO, A., MAVILIO, F. and BONCINELLI, E. (1991). Differential regulation by retinoic acid of the homeobox genes of the four HOX loci in human embryonal carcinoma cells. Mech. Dev 33: 215-228.
57. SIMON, H-G. and TABIN, C.J. (1993). Analysis of Hox-4.5 and Hox-3 6 expression during newt limb regeneration: differential regulation of paralogous Hox genes suggest different roles for members of different Hox clusters. Development 117: 1397-1407.
58. SIMON, H-G., NELSON, C., GOFF, D., LAUFER, E., MORGAN, B.A and TABIN, C. (1995). Differential expression of myogenic regulatory genes and Msx-1 during dedifferentiation and redifferentiation of regenerating amphibian limbs. Dev. Dynamics 202: 1-12.
59. SINGER, M. (1978). On the nature of the neurotrophic phenomenon in urodele limb regeneration. Am. Zool. 18: 829-841.
60. SLACK, J M.W. (1980). A serial threshold theory of regeneration. J. Theor. Biol. 82: 105-140.
61. SMALL, K.M. and POTTER, S S. (1993). Homeotic transformations and limb defects in Hox A11 mutant mice. Genes Dev. 7: 2318-2328.
62. SONG, K., WANG, Y. and SASSOON, D. (1992). Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation. Nature 360: 477-481.
63. STOCUM, D.L (1991). Limb regeneration. a call to arms (and legs). Cell 67: 5-8.
64. STOCUM, D.L. and DEARLOVE, G.E. (1972). Epidermal-mesodermal interaction during morphogenesis of the limb regeneration blastemal in larval salamanders. J. Exp Zool 181: 49-62
65. SUMMERBELL, D., LEWIS, J H and WOLPERT, L. (1973). Positional information in chick limb morphogenesis. Nature 244. 492-496.
66. TABIN, C. and LAUFER, E. (1993) Hox genes and serial homology Nature 361: 692-693
67. TABIN, C J. (1989). Isolation of potential vertebrate limb-identity genes. Development 105: 813-820
68. TASSAVA, R.A. (1992). Retinoic acid enhances monoclonal antibody WE3 reactivity in the regenerate epithelium of the adult newt. J Morphol 213: 159-169.
69. TAYLOR, G.P., ANDERSON, R , REGINELLI, A.D. and MUNEOKA, K. (1994). FGF-2 induces regeneration of the chick limb bud Dev. Biol. 163: 282-284.
70. TICKLE, C , SUMMERBELL, D. and WOLPERT, L (1975). Positional signaling and specification of digits in chick limb morphogenesis Nature 254: 199-202.
71. TSCHUMI, P A. (1957) The growth of the hind limb bud of Xenopus laevis and its dependence upon the epidermis. J Anat. 91: 149-173.
72. WALLACE, H. (1981) Vertebrate Limb Regeneration John Wiley and Sons, Chichester
73. WANEK, N , MUNEOKA, K and BRYANT, S.V (1989). Evidence for regulation following amputation and tissue grafting in the developing mouse limb. J. Exp. Zool. 249. 55-61
74. YANG, E.V and BRYANT, S V. (1994). Developmental regulation of a matrix metalloproteinase during regeneration of axolotl appendages. Dev. Biol. 166: 696-703
75. YOKOUCHI, Y., SASAKI, H. and KUROIWA, A. (1991). Homeobox gene expression correlated with the bifurcation process of limb cartilage development Nature 353: 443-445.