Developmental functions of mammalian Hox genes

Molecular Human Reproduction

Volumn 3, Issue 2, 1997, Pages 115-131

  Favier, Bertrand ^a,b   Dollé, Pascal ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSTITUT ALBERT BONNIOT   (France)

Author keywords

Gene targeting; Homeobox; Hox genes; Mouse development; Pattern formation

Indexed keywords

ANIMAL; BONE; BRANCHIAL ARCH; COMPARATIVE STUDY; DROSOPHILA; EVOLUTION; FEMALE; GENE; GENE EXPRESSION REGULATION; GENETICS; GENITAL SYSTEM; HOMEOBOX; LIMB; MALE; MAMMAL; MOUSE; MOUSE MUTANT; PHYLOGENY; PRENATAL DEVELOPMENT; REVIEW; RHOMBENCEPHALON; TRANSGENIC MOUSE;

ANIMALS; BONE AND BONES; BRANCHIAL REGION; DROSOPHILA; EVOLUTION; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; GENES, INSECT; GENITALIA; MALE; MAMMALS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PHYLOGENY; RHOMBENCEPHALON;

EID: 0031062972     PISSN: 13609947     EISSN: None     Source Type: Journal    
DOI: 10.1093/molehr/3.2.115     Document Type: Article

References (129)

1. Bateson, W. (1894) Materials for the Study of Variation Treated with Special Regards to Discontinuity in the Origin of Species Macmillan Press, London.
2. Beeman, R.W. (1987) A homeotic cluster in the red flour beetle. Nature, 327, 247-249.
3. Benson, G.V., Lim, H., Paria, B.C. et al. (1996) Mechanism of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development, 122, 2687-2696
4. Blatt, C., Aberdam, D., Schwarz, R. et al. (1988) DNA rearrangement of a homeobox gene in myeloid leukemia cells. EMBO J., 7, 4283-4290.
5. Boncinelli, E., Simeone, A., Acampora, D. et al. (1991) Hox gene activation by retinoic acid Trends Genet., 7, 329-334.
6. Bürglin, T.R., Ruvkun, G., Coulson, A. et al. (1991) Nematode homeobox cluster. Nature, 351, 703.
7. Burke, A.C., Nelson, C.E., Morgan, B.A. et al. (1995) Hox genes and the evolution of vertebrate axial morphology. Development, 121, 333-346.
8. Carpenter, E.M., Goddard, J.M., Chisaka, O. et al. (1993) Loss of Hoxa-1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development, 118, 1063-1075.
9. Carrasco, A.E., McGinnis, W., Gehring, W.J. et al. (1984) Cloning of a X. laevis gene expressed during early embryogenesis coding for a peptide region homologous to Drosophila homeotic genes. Cell. 37, 409-414
10. Celniker, S.E., Sharma, S., Keelan, D J. et al (1990) The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J., 9, 4277-4286.
11. Charité, J., De Graaf, W. and Deschamps, J. (1995) Specification of multiple vertebral identities by ectopically expressed Hoxb-8. Dev. Dynamics, 204, 13-21.
12. Chuaka, O., and Capecchi, M.R. (1991) Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene Hox-1.5. Nature, 350, 473-479.
13. Coates, M.I (1995). Fish fins or tetrapod limbs: a simple twist of fate? Curr. Biol., 8, 844-848.
14. Condie, B.C. and Capecchi, M. (1993) Mice homozygous for a targeted disruption of Hoxd-3 (Hox4-1) exhibit anterior transformations of the first and second cervical vertebrae, the atlas and the axis. Development, 119, 579-595.
15. Condie, B.G. and Capecchi, M. (1994) Mice with targeted disruption in the paralogous genes Hoxa-3 and Hoxd-3 reveal synergistic interactions Nature, 370, 304-306.
16. Davidson, E.H., Peterson, K.J. and Cameron, R.A. (1995) Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science, 270, 1319-1325.
17. 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.
18. Davis, A.P. and Capecchi, M.R. (1996) A mutational analysis of the 5′ HoxD genes: dissection of genetic interactions during limb development in the mouse. Development, 122, 1175-1185.
19. Davis, A.P., Witte, D.P., Hsieh-Li, H.M. et al. (1995) Absence of radius and ulna in mice lacking Hoxa-11 and Hoxd-11. Nature, 375, 791-795.
20. de Beer G. (1985) The Development of the Vertebrate Skull. The University of Chicago Press, Chicago.
21. Deschamps, J. and Wijgerde, M. (1993) Two phases in the establishment of Hox expression domains. Dev. Biol., 156, 473-480.
22. Dollé, P. and Duboule, D. (1993) Structural and functional aspects of mammalian Hox genes. Adv. Dev. Biochem., 2, 55-106.
23. Dollé, P., Izpisúa-Belmonte, J.-C., Falkenstein, H. et al. (1989) Coordinate expression of the murine Hox-5 complex homeobox-containing genes during limb pattern formation. Nature, 342, 767-772.
24. Dollé, P., Izpisúa-Belmonte, J.-C., Brown, J. et al. (1991a) Hox-4 genes and the morphogenesis of mammalian genitalia. Genes Dev., 5, 1767-1776.
25. Dollé, P., Izpisua-Belmonte, J., Boncinelli, E. et al. (1991b) The Hox-4.8 gene is localized at the 5′ extremity of the Hox-4 complex and is expressed in the posterior end of the body during development. Mech. Dev., 36, 3-14.
26. Dollé, P., Lufkin, T., Krumlauf, R. et al. (1993a) Local alterations of Krox- 20 and Hox gene expression in the hindbrain suggest lack of rhombomeres 4 and 5 in homozygote null Hoxa-1 (Hox 1-6) mutant embryos. Proc. Natl. Acad. Sci. USA, 90, 7666-7670
27. Dollé, P., Dierich, A., LeMeur, M. et al. (1993b) Disruption of the Hoxd-13 gene induces localized heterochrony leading to mice with neotenic limbs. Cell, 75, 431-441.
28. Duboule, D. (1991) Patterning in the vertebrate limb. Curr. Opin. Genet. Dev., 1, 211-216.
29. Duboule, D. (ed) (1994) Guidebook to the Homeobox Genes Oxford University Press, Oxford.
30. Duboule, D (1995) Vertebrate Hox genes and proliferation: an alternative pathway to homeosis? Curr. Opin. Genet. Dev., 5, 525-528.
31. Duboule, D. and Dollé, P. (1989) The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J., 8, 1497-1505.
32. Duboule, D. and Morata, M. (1994) Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet., 10, 358-364.
33. Duboule, D., Galliot, B., Baron, A. et al. (1989) Murine homeogenes: some aspects of their organisation and structure. In Cell to Cell Signals in Mammalian Development. NATO ASI series. Springer Verlag, Berlin p. 97-108.
34. Favier, B., Lemeur, M., Chambon, P. et al. (1995) Axial skeleton homeosis and forelimb malformations in Hoxd-11 mutant mice. Proc. Natl. Acad. Sci. USA. 92, 310-314.
35. Favier, B., Rijli P.M., Fromental-Ramain C. et al (1996) Functional cooperation between the non-paralogous genes Hoxa-10 and Hoxd-11 in the developing forelimb and axial skeleton. Development, 122, 449-460.
36. Fraser, S.E., Keynes, R.J. and Lumsden, A. (1990) Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature, 344, 431-435.
37. Fromental-Ramain, C., Warot, X., Lakkaraju, S. et al. (1996) Specific and redundant functions of the paralogous Hoxa-9 and Hoxd-9 genes in forelimb and axial skeleton patterning. Development, 122, 461-472.
38. Gaunt, S.J. (1987) Homeo-box gene Hox-1.5 expression in mouse embryos: earliest detection by in situ hybridization is during gastrulation. Development, 101, 51-60.
39. Gaunt, S.J. (1994) Conservation in the Hox code during morphological evolution. Int. J. Dev. Biol., 38, 549-552.
40. Gaunt, S.J. and Sirachan, L. (1994) Forward spreading in the establishment of a vertebrate Hox expression boundary: the expression domain separates into anterior and posterior zones, and the spread occurs across implanted glass barriers. Dev. Dynamics, 199, 229-240.
41. Gehring, W.J. (1987) Homeoboxes in the study of development. Science, 236, 1245-1252.
42. Gehring, W.J., Müller, M., Affolter, M. et al. (1990) The structure of the homeodomain and its functional implications. Trends Genet.. 6, 323-329.
43. Gehring, W.J., Qian, Y. Q., Billeter et al. (1994) Homeodomam-DNA recognition. Cell, 78, 211-223.
44. Gendron-Maguire, M., Mallo, M., Zhang, M. et al (1993) Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell, 75, 1317-1331.
45. Goomer, R.S., Holst, B D., Wood, I.C. et al. (1994) Regulation in vitro of an L-CAM enhancer by homeobox genes HoxD9 and HNF-1. Proc. Natl. Acad. Sci. USA, 91, 7985-7989.
46. Gould, A.P, Brookman, J.J., Strutt, D.I. et al. (1990) Targets of homeotic gene control in Drosophila. Nature, 348, 308-312. (Published erratum appears in Nature, 348, 560.)
47. Graham, A., Papalopulu, N. and Krumlauf, R. (1989) The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell, 57, 367-378.
48. Grapin-Botton, A., Bonnin, M.A., McNaughton, L.A. et al. (1995) Plasticity of transposed rhombomeres. Hox gene induction is correlated with phenotypic modifications. Development. 121, 2707-2721.
49. Guthrie, S., Muchamore, I., Kuroiwa, A. et al. (1992) Neuroectodermal autonomy of Hox-2.9 expression revealed by rhombomere transpositions. Nature, 356, 157-159.
50. Haack, H. and Gruss, P. (1993) The establishment of murine Hox-1 expression domains during patterning of the limb. Dev. Biol. 157, 410-422.
51. Holland, P.W.H. and Garcia-Fernandez, J. (1996) Hox genes and chordatc evolution. Dev. Biol., 173, 382-395.
52. Horan, G.S.B., Ramirez-Sollis, R., Featherstone, M.S. et al. (1995) Compound mutants for the paralogous Hoxa-4, Hoxb-4, and Hoxd-4 genes show more complete homeotic transformations and a dose-dependent increase in the number of vertebrae transformed. Genes Dev., 9, 1667-1677.
53. Hsieh-Li, H.M., Wine, D.P., Weinstein, M. et al. (1995) Hoxa-11 structure, extensive antisense transcription, and function in male and female fertility. Development, 121, 1373-1385.
54. Hunt, P., Gulisano, M., Cook, M. et al. (1991) A distinct Hox code for the branchial region of the vertebrate head. Nature, 353, 861-864.
55. Hunt, P., Ferretti, P., Krumlauf, R. et al. (1995) Restoration of normal Hox code and branchial arch morphogenesis after extensive deletion of hindbrain neural crest. Dev. Biol., 168, 584-597.
56. Itasaki, N, Sharpe, J., Morrison, A et al. (1996) Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition. Neuron, 16, 487-500.
57. Izpisúa-Belmonte, J.-C., Tickle, C., Dollé, P. et al (1991a) Expression of the homeobox Hox-4 genes and the specification of position in chick wing development. Nature, 350, 585-589.
58. Izpisúa-Belmonte, J.-C., Falkenstein, H., Dollé, P. et al. (1991b) Murine genes related to the Drosophila Abd B homeotic gene are sequentially expressed during development of the posterior part of the body. EMBO J., 10, 2279-2289.
59. Jeannotte, L., Lemieux, M., Charon, J. et al. (1993) Specification of axial identity in the mouse: role of the Hoxa-5 (Hoxl-3) gene. Genes Dev., 7, 2085-2096.
60. Jegalian, E.G. and DeRobertis, E.M. (1992) Homeotic transformations in the mouse induced overexpression of a human Hox3.3 transgene. Cell, 71, 901-910
61. Jones, F.S . Prediger, E.A., Bittner, D.A. et al. (1992) Cell adhesion molecules as targets for Hox. genes: neural cell adhesion molecule promoter activity is modulated by cotransfection with Hox-2.5 and Hox-2.4. Proc. Natl. Acad. Sci. USA, 89, 2086-2990.
62. Kanzler, B., Viallet, J.P., Le Mouellic, H. et al. (1994) Differential expression of two different homeobox gene families during mouse tegument morphogenesis. Int. J. Dev. Biol., 38, 633-640.
63. Kastner, P., Mark, M., and Chambon, P. (1995) Non-steroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell, 83, 859-869.
64. Kessel, M. (1992) Respecification of vertebral identity by retinoic acid. Development, 115, 487-501
65. 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.
66. Kessel, M., Balling, R., and Gruss, P. (1990) Variations of cervical vertebrae after expression of a Hox-1.1 transgene in mice. Cell, 61, 301-308.
67. Kondo, T., Dollé, P., Zàkàny, J. et al. (1996) Function of posterior HoxD genes in the morphogenesis of the anal sphincter. Development, 122, 2651-2659.
68. Kuratani, S.C. and Eichele, G. (1993) Rhombomere transplantation repatterns the segmental organization of cranial nerves and reveals cell-autonomous expression of a homeodomain protein. Development, 117, 105-117.
69. Labosky, P.A., Weir, M. and Grabel, L.B. (1993) Homeobox-containing gene in teratocarcinoma embryoid bodies: a possible role for Hoxd-12 (Hox4- 7) in establishing the extraembryonic endoderm lineage in the mouse. Dev. Biol., 159, 232-244.
70. Lawrence, P.A. (1992) The Making of a Fly The Genetics of Animal Design. Blackwell Scientific Publications, Oxford.
71. LeMouellic, H., Lallemand, Y. and Brûlet. P. (1992) Homeosis in the mouse induced by a null mutation in the Hox3.1 gene. Cell, 69, 251-264.
72. Lewis, E.B. (1978) A gene complex controlling segmentation in Drosophila. Nature, 276, 565-570.
73. Lewis, E.B. (1994) Homeosis: the first 100 years. Trends Genet., 10, 341-343
74. Lufkin, T., Dierich, A., LeMeur, M. et al. (1991) Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Cell. 66, 1105-1119.
75. Lufkin, T., Mark, M., Hart, C. P. et al. (1992) Homeotic transformation of the occipital bones of the skull by ectopic expression of a homeobox gene. Nature, 359, 835-841
76. Mangelsdorf, D.J., Umesono, K. and Evans, R. (1994) The retinoid receptors. In Sporn, M.B., Roberts, A.B. and Goodman, D.S. (eds), The Retinoids. Biology, Chemistry and Medicine. Raven Press Ltd, New York, pp. 319-350.
77. Manley, N R. and Capecchi, M.R. (1995) The role of Hoxa-3 in mouse thymus and thyroid development. Development, 121, 1989-2003.
78. Mark, M., Rijli, F.M. and Chambon, P. (1995) Alteration of Hox gene expression in the branchial region of the head causes homeotic transformations, hindbrain segmentation defects and atavistic changes. Seminars Dev. Biol., 6, 275-284.
79. Mark, M., Lufkin, T., Vonesch, J.L. et al. (1993) Two rhombomeres are altered in Hoxa-1 mutant mice. Development, 119, 319-338.
80. Maulbecker, C.C. and Gruss, P. (1993) The oncogenic potential of deregulated homeobox genes. Cell Growth Diff., 4, 431-441.
81. McGinnis, W. and Krurnlauf, R. (1992). Homeobox genes and axial patterning. Cell, 68, 283-302.
82. McGinnis, W., Hart, C.P., Gehring, W. J. et al. (1984) Molecular cloning and chromosome mapping of a mouse DNA sequence homologous to homeotic genes of Drosophila. Cell, 38, 675-680.
83. Morgan, B. A., Izpisúa-Belmonte, J.-C., Duboule, D. et al. (1992) Targeted expression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature, 358, 236-239.
84. Muragaki, Y., Mundlos, S., Upton, J. et al. (1996) Altered growth and branching patterns in synpolydactyly caused by mutations in HOXD13. Science, 272, 448-151.
85. Nelson, C.E., Morgan, B.A. Burke, A.C. et al. (1996) Analysis of Hox gene expression in the chick limb bud. Development, 122, 1449-1466.
86. Noden, D. (1988) Interactions and fates of avian craniofacial mesenchyme. Development, 103 (Suppl.), 121-140.
87. Nohno, T., Noji, S., Koyama, E. et al (1991) Involvement of the Chox-4 chicken homeobox genes in determination of anteroposterior axial polarity during limb development. Cell, 64, 1197-1205.
88. Oliver, G., De Robertis, E. M., Wolpert, L. et al (1990) Expression of a homeobox gene in the chick wing bud following application of retinoic acid and grafts of polarizing region tissue. EMBO J., 9, 3093-3099.
89. Oudejans, C.B. Pannese, M., Simeone, A. et al. (1990) The three most downstream genes of the Hox-3 cluster are expressed in human extraembryonic tissues including trophoblast of androgenetic origin. Development, 108, 471-477.
90. Peterson, R.L., Papenbrock, T., Davda, M.M. et al. (1994) The murine HOXC cluster contains five neighboring AbdB-related Hox genes that show unique spatially coordinated expression in posterior embryonic subregions. Mech. Dev., 47, 253-260.
91. Pollock, A. R., Sreenath, T., Ngo, L. et al. (1995) Gain of function mutations for paralogous Hox genes: implications for the evolution of Hox gene function. Proc. Natl. Acad. Sci. USA, 92, 4492-4496
92. Pöpperl, H and Featherstone, M.S. (1992) An autoregulatory element of the murine Hox-4.2 gene. EMBO J., 11, 3673-3680.
93. Popperl, H., Brenz, M., Studer, M. et al. (1995) Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell, 81, 1031-1042.
94. Ramirez-Solis, R., Zheng, H., Whiting, J. et al (1993) Hoxb-4 (Hox2-6) mutant mice show homeotic transformation of a cervical vertebra and defects in the closure of the sternal rudiments. Cell, 73, 279-294.
95. Rancourt, D.E., Tsusuki, T. and Capecchi, M.R. (1995) Genetic interaction between Hoxb-5 and Hoxb-6 is revealed by nonallelic noncomplementation. Genes Dev., 9, 108-122.
96. Redline, R.W., Williams, A.J., Patterson, P. et al. (1992). Human HOX4E: a gene strongly expressed in the adult male and female urogenital tracts. Genomics, 13, 425-130.
97. Riddle, R.D., Johnson, R.L., Laufer, E. et al. (1993) Sonic hedgehog mediates the polarizing activity of the ZPA Cell. 75, 1401-1416
98. Rijli, M. R., Mark, M., Lakkaraju, S. et al. (1993) A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell, 75, 1333-1349
99. Rijli, F., Matyas, R., Pellegrini, M. et al. (1995) Cryptorchidism and homeotic transformations of spinal nerves and vertebrae in Hoxa-10 mutant mice. Proc. Natl. Acad. Sci. USA, 92, 8185-8189.
100. Roberts, D.J., Johnson, R.L., Burke, A.C. et al (1995) Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick bindgut. Development 121, 3163-3174.
101. Satokata, I., Benson, G. and Maas, R. (1995). Sexually dimorphic sterility phenotypes in Hoxa 10-deficient mice. Nature, 374, 460-463.
102. Sauvageau, G., Thorsteindottir, U., Eaves, C. J. et al (1995) Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev., 9, 1753-1765.
103. Schneider-Maunoury, S., Topilko, P., Seitanidou, T. et al. (1993) Disruption of Krox20 results in elimination of rhombomeres 3 and 5 in the developing hindbrain. Cell, 75, 1199-1214.
104. Scott, M. (1992) Vertebrate homeobox gene nomenclature. Cell, 71, 551-553.
105. Shen, W.-F., Detmer, K., Mathews, C.H.E. et al (1993) Modulation of homeobox gene expression alters the phenotype of human hematopoietic cell lines. EMBO J., 11, 983-989.
106. Shubin, N.H. and Alberch, P. (1986) A morphogenetic approach to the origin and basic organisation of the tetrapod limb. Evol. Biol., 20, 319-387.
107. Slack, I.M.W., Holland, P.W.H. and Graham, C.F. (1993) The zootype and the phylotypic stage. Nature. 361, 490-492.
108. Small, K.M. and Potter, S.S. (1993) Homeotic transformations and limb defects in Hoxa-11 mutant mice. Genes Dev., 7, 2318-2328.
109. Sordino, P. and Duboule, D. (1996) A molecular approach to the evolution of vertebrate paired appendages. TRRE, 11, 114-119.
110. Sordino, P., Van der Hoeven, R. and Duboule D. (1995) Hox gene expression in teleost fins and the origin of vertebrate digits. Nature, 375, 678-681.
111. Sundin, O. and Eichele, G. (1992) An early marker of axial pattern in the chick embryo and its respecification by retinoic acid. Development, 114, 841-852.
112. Swiatek, P.J. and Gridley, T. (1993) Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev., 7, 2071-2084.
113. Tabin, C.J. (1992) Why we have (only) five fingers per hand: Hox genes and the evolution of paired limbs. Development, 116, 289-296.
114. Tickle, C. and Eichele, G. (1994) Vertebrate limb development. Ann. Rev. Cell Biol. 10, 121-152.
115. Tickle, C., Alberts, B., Wolpert, L. et al. (1982) Local application of retinoic acid to the limb bud mimics the action of the polarizing region. Nature, 296, 564-566.
116. Tiret, L., Le Mouellic, H., Lallemand, Y. et al. (1993) Altering the spatial determinations in the mouse embryos by manipulating the Hox genes. C.R. Acad. Sci. Paris, (Life Sci.), 316, 1017-1024.
117. van der Hoeven, F., Sordino, P., Fraudeau, N. et al. (1996) Teleost HoxD and HoxA genes: comparison with tetrapods and functional evolution of the HOXD complex. Mech. Dev., 54, 9-21.
118. Verlinsky, Y., Morozov, G., Gindlis, V. et al. (1995) Homeobox gene expression in human oocytes and preembryos. Mol. Reprod. Dev., 41, 127-132.
119. Vieille-Grosjean, I., Roullot, V. and Courtois, G. (1992) Lineage specific expression of HOX-1 genes in the human hematopoietic system. Biochem Biophys. Res. Comm., 183, 1124-1130.
120. Vogels, R., De Graaf, W. and Deschamps, J. (1990) Expression of the murine homeobox-containing gene Hox-2.3 suggests multiple time-dependent and tissue-specific roles during development. Development. 110, 1159-1168.
121. Wang, B.B., Müller-Immerglück, M.M., Austin, J. et al. (1993) A homeotic gene cluster patterns the anteroposterior axis of C.elegans. Cell, 74, 29-42.
122. Wilkinson, D.G., Bhatt, S., Cook, M. et al. (1989) Segmental expression of Hox 2 homeobox genes in the developing hindbrain Nature, 341, 405-409.
123. Yokouchi, Y., Sasaki, H., and Kuroiwa, A. (1991) Homeobox gene expression correlated with the bifurcation process of limb cartilage development. Nature, 353, 443-445.
124. Yokouchi, Y., Nakazato, S., Yamamoto, M. et al. (1995a) Misexpression of Hoxa-13 induces cartilage homeotic transformation and changes cell adhesiveness in chick limb buds. Genes Dev.. 9, 2509-2522.
125. Yokouchi, Y., Satayama, J. and Kuroiwa, A (1995b) Coordinated expression of Abd-B subfamily genes of the HoxA cluster in the developing digestive tract of chick embryo. Dev. Biol., 169, 76-89.
126. Zappavigna, V., Renucci, A., Izpisua-Belmonte, J.-C. et al. (1991) Hox-4 genes encode transcription factors with potential auto- and cross-regulatory capacities. EMBO J., 10, 4177-4187.
127. Zàkàny, J., Gérard, M., Favier, B. et al. (1996) Functional equivalence and rescue among group 11 Hox gene products in vertebral patterning. Dev. Biol., 176, 325-328.
128. Zeltser, L., Desplan, C and Heintz, N. (1996) Hoxb-13: a new Hox gene in a distant region of the HOXB cluster maintains colinearity. Development, 122, 2475-2484.
129. Zhang M., Kim H. J., Marshall H. et al. (1994) Ectopic Hoxa-1 induces rhombomere transformation in mouse hindbrain. Development, 120, 2431-2442.