Hox genes and regional patterning of the vertebrate body plan

Developmental Biology

Volumn 344, Issue 1, 2010, Pages 7-15

  Mallo, Moises ^a,b   Wellik, Deneen M ^c,d   Deschamps, Jacqueline ^e  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Function of Hox genes in vertebrates; Hox function in axial extension; Hox paralogous groups; Molecular genetics of axial patterning by Hox genes; Regional patterning of anatomical regions

Indexed keywords

HOX PROTEIN; HOXPG10 PROTEIN; HOXPG11 PROTEIN; HOXPG13 PROTEIN; HOXPG5 9 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CDX; UNCLASSIFIED DRUG;

ANTERIOR POSTERIOR AXIS; BODY HEIGHT; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE MUTATION; LUMBAR VERTEBRA; MOLECULAR GENETICS; MOLECULAR INTERACTION; MORPHOGENESIS; MUTATIONAL ANALYSIS; NECK; NONHUMAN; PARALOGY; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; REVIEW; RIB; SACRUM; THORAX; VERTEBRATE;

DROSOPHILA MELANOGASTER; VERTEBRATA;

EID: 77955053847     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.04.024     Document Type: Review

References (102)

1. Aoyama H., Mizutani-koseki S., Koseki H. Three developmental compartments involved in rib formation. Int. J. Dev. Biol. 2005, 49:325-333.
2. Bajard L., Relaix F., Lagha M., Rocancourt D., Daubas P., Buckingham M.E. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 2006, 20:2450-2464.
3. Bolognesi R., Farzana L., Fischer T.D., Brown S.J. Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr. Biol. 2008, 18:1624-1629.
4. Braun T., Arnold H.H. Inactivation of Myf-6 and Myf-5 genes in mice leads to alterations in skeletal muscle development. EMBO J. 1995, 14:1176-1186.
5. Braun T., Rudnicki M.A., Arnold H.H., Jaenisch R. Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 1992, 71:369-382.
6. Brent A.E., Tabin C.J. Developmental regulation of somite derivatives: muscle, cartilage and tendon. Curr. Opin. Genet. Dev. 2002, 12:548-557.
7. Buchberger A., Freitag D., Arnold H.H. A homeo-paired domain-binding motif directs Myf5 expression in progenitor cells of limb muscle. Development 2007, 134:1171-1180.
8. Burke A.C. Hox genes and the global patterning of the somitic mesoderm. Curr. Top. Dev. Biol. 2000, 47:155-181.
9. Burke A.C., Nowicki J.L. A new view of patterning domains in the vertebrate mesoderm. Dev. Cell 2003, 4:159-165.
10. Burke A.C., Nelson C.E., Morgan B.A., Tabin C. Hox genes and the evolution of vertebrate axial morphology. Development 1995, 121:333-346.
11. Cambray N., Wilson V. Axial progenitors with extensive potency are localised to the mouse chordoneural hinge. Development 2002, 129:4855-4866.
12. Cambray N., Wilson V. Two distinct sources for a population of maturing axial progenitors. Development 2007, 134:2829-2840.
13. Carapuco M., Novoa A., Bobola N., Mallo M. Hox genes specify vertebral types in the presomitic mesoderm. Genes Dev. 2005, 19:2116-2121.
14. Charite J., de Graaff W., Consten D., Reijnen M.J., Korving J., Deschamps J. Transducing positional information to the Hox genes: critical interaction of cdx gene products with position-sensitive regulatory elements. Development 1998, 125:4349-4358.
15. Chawengsaksophak K., James R., Hammond V.E., Kontgen F., Beck F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 1997, 386:84-87.
16. Chawengsaksophak K., de Graaff W., Rossant J., Deschamps J., Beck F. Cdx2 is essential for axial elongation in mouse development. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7641-7645.
17. Christ B., Huang R., Scaal M. Amniote somite derivatives. Dev. Dyn. 2007, 236:2382-2396.
18. Condie B.G., Capecchi M.R. Mice with targeted disruptions in the paralogous genes hoxa-3 and hoxd-3 reveal synergistic interactions. Nature 1994, 370:304-307.
19. Copf T., Schroder R., Averof M. Ancestral role of caudal genes in axis elongation and segmentation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:17711-17715.
20. Deschamps J., van Nes J. Developmental regulation of the Hox genes during axial morphogenesis in the mouse. Development 2005, 132:2931-2942.
21. Di-Poi N., Montoya-Burgos J.I., Miller H., Pourquie O., Milinkovitch M.C., Duboule D. Changes in Hox genes' structure and function during the evolution of the squamate body plan. Nature 2010, 464:99-103.
22. Dressler G.R., Gruss P. Anterior boundaries of Hox gene expression in mesoderm-derived structures correlate with the linear gene order along the chromosome. Differentiation 1989, 41:193-201.
23. Duboule D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev. Suppl. 1994, 135-142.
24. Duboule D. The rise and fall of Hox gene clusters. Development 2007, 134:2549-2560.
25. Duboule D., Dolle P. The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J. 1989, 8:1497-1505.
26. Duboule D., Morata G. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 1994, 10:358-364.
27. Dubrulle J., Pourquie O. fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 2004, 427:419-422.
28. Economides K.D., Zeltser L., Capecchi M.R. Hoxb13 mutations cause overgrowth of caudal spinal cord and tail vertebrae. Dev. Biol. 2003, 256:317-330.
29. Evans D.J. Contribution of somitic cells to the avian ribs. Dev. Biol. 2003, 256:114-126.
30. Faas L., Isaacs H.V. Overlapping functions of Cdx1, Cdx2, and Cdx4 in the development of the amphibian Xenopus tropicalis. Dev. Dyn. 2009, 238:835-852.
31. Forlani S., Lawson K.A., Deschamps J. Acquisition of Hox codes during gastrulation and axial elongation in the mouse embryo. Development 2003, 130:3807-3819.
32. Garcia-Fernandez J. Hox, ParaHox, ProtoHox: facts and guesses. Heredity 2005, 94:145-152.
33. Gaunt S.J. Expression patterns of mouse Hox genes: clues to an understanding of developmental and evolutionary strategies. Bioessays 1991, 13:505-513.
34. Gaunt S.J. Conservation in the Hox code during morphological evolution. Int. J. Dev. Biol. 1994, 38:549-552.
35. Gaunt S.J., Strachan L. Temporal colinearity in expression of anterior Hox genes in developing chick embryos. Dev. Dyn. 1996, 207:270-280.
36. Gaunt S.J., Krumlauf R., Duboule D. Mouse homeo-genes within a subfamily, Hox-1.4, -2.6 and -5.1, display similar anteroposterior domains of expression in the embryo, but show stage- and tissue-dependent differences in their regulation. Development 1989, 107:131-141.
37. Giordani J., Bajard L., Demignon J., Daubas P., Buckingham M., Maire P. Six proteins regulate the activation of Myf5 expression in embryonic mouse limbs. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11310-11315.
38. Gomez C., Ozbudak E.M., Wunderlich J., Baumann D., Lewis J., Pourquie O. Control of segment number in vertebrate embryos. Nature 2008, 454:335-339.
39. Gong K.Q., Yallowitz A.R., Sun H., Dressler G.R., Wellik D.M. A Hox-Eya-Pax complex regulates early kidney developmental gene expression. Mol. Cell. Biol. 2007, 21:7661-7668.
40. Graham A., Papalopulu N., Krumlauf R. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 1989, 57:367-378.
41. Grass S., Arnold H.H., Braun T. Alterations in somite patterning of Myf-5-deficient mice: a possible role for FGF-4 and FGF-6. Development 1996, 122:141-150.
42. Grifone R., Demignon J., Houbron C., Souil E., Niro C., Seller M.J., Hamard G., Maire P. Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 2005, 132:2235-2249.
43. Gruss P., Kessel M. Axial specification in higher vertebrates. Curr. Opin. Genet. Dev. 1991, 1:204-210.
44. Henderson D.J., Conway S.J., Copp A.J. Rib truncations and fusions in the Sp2H mouse reveal a role for Pax3 in specification of the ventro-lateral and posterior parts of the somite. Dev. Biol. 1999, 209:143-158.
45. Hirsinger E., Jouve C., Dubrulle J., Pourquie O. Somite formation and patterning. Int. Rev. Cytol. 2000, 198:1-65.
46. Horan G.S., Ramirez-Solis R., Featherstone M.S., Wolgemuth D.J., Bradley A., Behringer R.R. 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. 1995, 9:1667-1677.
47. Huang R., Zhi Q., Brand-Saberi B., Christ B. New experimental evidence for somite resegmentation. Anat. Embryol. (Berl). 2000, 202:195-200.
48. Huang R., Stolte D., Kurz H., Ehehalt F., Cann G.M., Stockdale F.E., Patel K., Christ B. Ventral axial organs regulate expression of myotomal Fgf-8 that influences rib development. Dev. Biol. 2003, 255:30-47.
49. Iimura T., Pourquie O. Collinear activation of Hoxb genes during gastrulation is linked to mesoderm cell ingression. Nature 2006, 442:568-571.
50. Iimura T., Denans N., Pourquie O. Establishment of Hox vertebral identities in the embryonic spine precursors. Curr. Top. Dev. Biol. 2009, 88:201-234.
51. Isaacs H.V., Pownall M.E., Slack J.M. Regulation of Hox gene expression and posterior development by the Xenopus caudal homologue Xcad3. EMBO J. 1998, 17:3413-3427.
52. Izpisua-Belmonte J.C., Falkenstein H., Dolle P., Renucci A., Duboule D. Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 1991, 10:2279-2289.
53. Kassar-Duchossoy L., Gayraud-Morel B., Gomes D., Rocancourt D., Buckingham M., Shinin V., Tajbakhsh S. Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 2004, 431:466-471.
54. Kessel M., Gruss P. Murine developmental control genes. Science 1990, 249:374-379.
55. Krumlauf R. Mouse Hox genetic functions. Curr. Opin. Genet. Dev. 1993, 3:621-625.
56. Lawson K.A., Meneses J.J., Pedersen R.A. Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 1991, 113:891-911.
57. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570.
58. Mallo M., Vinagre T., Carapuco M. The road to the vertebral formula. Int. J. Dev. Biol. 2009, 53:1469-1481.
59. Manley N.R., Capecchi M.R. Hox group 3 paralogs regulate the development and migration of the thymus, thyroid, and parathyroid glands. Dev. Biol. 1998, 195:1-15.
60. Martin B.L., Kimelman D. Regulation of canonical Wnt signaling by Brachyury is essential for posterior mesoderm formation. Dev. Cell 2008, 15:121-133.
61. Martin B.L., Kimelman D. Wnt signaling and the evolution of embryonic posterior development. Curr. Biol. 2009, 19:R215-R219.
62. Mathis L., Nicolas J.F. Clonal organization in the postnatal mouse central nervous system is prefigured in the embryonic neuroepithelium. Dev. Dyn. 2000, 219:277-281.
63. Mathis L., Nicolas J.F. Different clonal dispersion in the rostral and caudal mouse central nervous system. Development 2000, 127:1277-1290.
64. Mathis L., Nicolas J.F. Progressive restriction of cell fates in relation to neuroepithelial cell mingling in the mouse cerebellum. Dev. Biol. 2003, 258:20-31.
65. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell 1992, 68:283-302.
66. McGregor A.P., Pechmann M., Schwager E.E., Feitosa N.M., Kruck S., Aranda M., Damen W.G. Wnt8 is required for growth-zone establishment and development of opisthosomal segments in a spider. Curr. Biol. 2008, 18:1619-1623.
67. McIntyre D.C., Rakshit S., Yallowitz A.R., Loken L., Jeannotte L., Capecchi M.R., Wellik D.M. Hox patterning of the vertebrate rib cage. Development 2007, 134:2981-2989.
68. Nagashima H., Sugahara F., Takechi M., Ericsson R., Kawashima-Ohya Y., Narita Y., Kuratani S. Evolution of the turtle body plan by the folding and creation of new muscle connections. Science 2009, 325:193-196.
69. Ohya Y.K., Usuda R., Kuraku S., Nagashima H., Kuratani S. Unique features of Myf-5 in turtles: nucleotide deletion, alternative splicing, and unusual expression pattern. Evol. Dev. 2006, 8:415-423.
70. Patapoutian A., Yoon J.K., Miner J.H., Wang S., Stark K., Wold B. Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome. Development 1995, 121:3347-3358.
71. Pownall M.E., Gustafsson M.K., Emerson C.P. Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 2002, 18:747-783.
72. Savory J.G., Pilon N., Grainger S., Sylvestre J.R., Beland M., Houle M., Oh K., Lohnes D. Cdx1 and Cdx2 are functionally equivalent in vertebral patterning. Dev. Biol. 2009, 330:114-122.
73. Schultz A.H., Straus W.L. The numbers of vertebrae in primates. Proc. Am. Philos. Soc. 1945, 89:601-626.
74. Selleck M.A., Stern C.D. Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development 1991, 112:615-626.
75. Shimizu T., Bae Y.K., Muraoka O., Hibi M. Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Dev. Biol. 2005, 279:125-141.
76. Shinmyo Y., Mito T., Matsushita T., Sarashina I., Miyawaki K., Ohuchi H., Noji S. caudal is required for gnathal and thoracic patterning and for posterior elongation in the intermediate-germband cricket Gryllus bimaculatus. Mech. Dev. 2005, 122:231-239.
77. Soriano P. The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 1997, 124:2691-2700.
78. Stern C.D., Hatada Y., Selleck M.A., Storey K.G. Relationships between mesoderm induction and the embryonic axes in chick and frog embryos. Dev. Suppl. 1992, 151-156.
79. Subramanian V., Meyer B.I., Gruss P. Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell 1995, 83:641-653.
80. Sudo H., Takahashi Y., Tonegawa A., Arase Y., Aoyama H., Mizutani-Koseki Y., Moriya H., Wilting J., Christ B., Koseki H. Inductive signals from the somatopleure mediated by bone morphogenetic proteins are essential for the formation of the sternal component of avian ribs. Dev. Biol. 2001, 232:284-300.
81. Tabaries S., Lapointe J., Besch T., Carter M., Woollard J., Tuggle C.K., Jeannotte L. Cdx protein interaction with Hoxa5 regulatory sequences contributes to Hoxa5 regional expression along the axial skeleton. Mol. Cell. Biol. 2005, 25:1389-1401.
82. Tajbakhsh S., Rocancourt D., Buckingham M. Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature 1996, 384:266-270.
83. Tallquist M.D., Weismann K.E., Hellstrom M., Soriano P. Early myotome specification regulates PDGFA expression and axial skeleton development. Development 2000, 127:5059-5070.
84. Trainor P.A., Krumlauf R. Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nat. Rev. Neurosci. 2000, 1:116-124.
85. Tzouanacou E., Wegener A., Wymeersch F.J., Wilson V., Nicolas J.F. Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev. Cell. 2009, 17:365-376.
86. van den Akker E., Forlani S., Chawengsaksophak K., de Graaff W., Beck F., Meyer B.I., Deschamps J. Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 2002, 129:2181-2193.
87. van Nes J., de Graaff W., Lebrin F., Gerhard M., Beck F., Deschamps J. The Cdx4 mutation affects axial development and reveals an essential role of Cdx genes in the ontogenesis of the placental labyrinth in mice. Development 2006, 133:419-428.
88. Vinagre T., Moncaut N., Carapuco M., Novoa A., Bom J., Mallo M. Evidence for a myotomal Hox/Myf cascade governing nonautonomous control of rib specification within global vertebral domains. Dev. Cell 2010, 18:655-661.
89. Wellik D.M. Hox patterning of the vertebrate axial skeleton. Dev. Dyn. 2007, 236:2454-2463.
90. Wellik D.M. Hox genes and vertebrate axial pattern. Curr. Top. Dev. Biol. 2009, 88:257-278.
91. Wellik D.M., Capecchi M.R. Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 2003, 301:363-367.
92. Wellik D.M., Hawkes P.J., Capecchi M.R. Hox11 paralogous genes are essential for metanephric kidney induction. Genes Dev. 2002, 16:1423-1432.
93. Wilkinson D.G., Bhatt S., Herrmann B.G. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 1990, 343:657-659.
94. Wilson V., Beddington R. Expression of T protein in the primitive streak is necessary and sufficient for posterior mesoderm movement and somite differentiation. Dev. Biol. 1997, 192:45-58.
95. Wilson V., Olivera-Martinez I., Storey K.G. Stem cells, signals and vertebrate body axis extension. Development 2009, 136:1591-1604.
96. Woltering J.M., Durston A.J. The zebrafish hoxDb cluster has been reduced to a single microRNA. Nat. Genet. 2006, 38:601-602.
97. Woltering J.M., Vonk F.J., Muller H., Bardine N., Tuduce I.L., de Bakker M.A., Knochel W., Sirbu I.O., Durston A.J., Richardson M.K. Axial patterning in snakes and caecilians: evidence for an alternative interpretation of the Hox code. Dev. Biol. 2009, 332:82-89.
98. Yallowitz A.R., Gong K.Q., Swinehart I.T., Nelson L.T., Wellik D.M. Non-homeodomain regions of Hox proteins mediate activation versus repression of Six2 via a single enhancer site in vivo. Dev. Biol. 2009, 335:156-165.
99. Yoon J.K., Olson E.N., Arnold H.H., Wold B.J. Different MRF4 knockout alleles differentially disrupt Myf-5 expression: cis-regulatory interactions at the MRF4/Myf-5 locus. Dev. Biol. 1997, 188:349-362.
100. Young T., Deschamps J. Hox, Cdx, and anteroposterior patterning in the mouse embryo. Curr. Top. Dev. Biol. 2009, 88:235-255.
101. Young T., Rowland J.E., van de Ven C., Bialecka M., Novoa A., Carapuco M., van Nes J., de Graaff W., Duluc I., Freund J.N., Beck F., Mallo M., Deschamps J. Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Dev. Cell. 2009, 17:516-526.
102. Zhang W., Behringer R.R., Olson E.N. Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies. Genes Dev. 1995, 9:1388-1399.