Hox gene expression patterns in Lethenteron japonicum embryos-Insights into the evolution of the vertebrate Hox code

Developmental Biology

Volumn 308, Issue 2, 2007, Pages 606-620

  Takio, Yoko ^a   Kuraku, Shigehiro ^a   Murakami, Yasunori ^b   Pasqualetti, Massimo ^c   Rijli, Filippo M ^d   Narita, Yuichi ^a   Kuratani, Shigeru ^a   Kusakabe, Rie ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b EHIME UNIVERSITY   (Japan)

^c UNIVERSITY OF PISA   (Italy)

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

Author keywords

Evolution; Hindbrain; Hox; Lamprey; Neural crest; Pharyngeal arches; Rhombomere; Tail bud

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; HOX GENE; LAMPREY; LETHENTERON JAPONICUM; MALE; MOLECULAR EVOLUTION; NONHUMAN; PHARYNX; PRIORITY JOURNAL; RHOMBENCEPHALON;

GNATHOSTOMATA (VERTEBRATE); LETHENTERON JAPONICUM; PETROMYZONTIDAE; VERTEBRATA;

EID: 34547746941     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.05.009     Document Type: Article

References (101)

1. Amores A., Force A., Yan Y.-L., Amemiya C., Fritz A., Ho R.K., Joly L., Langeland J., Prince V., Wang Y.-L., et al. Genome duplications in vertebrate evolution: evidence from zebrafish Hox clusters. Science 282 (1998) 1711-1714
2. Araki I., and Nakamura H. Engrailed defines the position of dorsal di-mesencephalic boundary by repressing diencephalic fate. Development 126 (1999) 5127-5135
3. Baltzinger M., Ori M., Pasqualetti M., Nardi I., and Rijli F.M. Hoxa2 knockdown in Xenopus results in hyoid to mandibular homeosis. Dev. Dyn. 234 (2005) 858-867
4. Barrow J.R., and Capecchi M.R. Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development 122 (1996) 3817-3828
5. Briscoe J., and Wilkinson D.G. Establishing neuronal circuitry: Hox genes make the connection. Genes Dev. 18 (2004) 1643-1648
6. Bruce A.E., Oates A.C., Prince V.E., and Ho R.K. Additional hox clusters in the zebrafish: divergent expression patterns belie equivalent activities of duplicate hoxB5 genes. Evol. Dev. 3 (2001) 127-144
7. Bulfone A., Puelles L., Porteus M.H., Frohman M.A., Martin G.R., and Rubenstein J.L. Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J. Neurosci. 13 (1993) 3155-3172
8. Burke A.C., Nelson C.E., Morgan B.A., and Tabin C. Hox genes and the evolution of vertebrate axial morphology. Development 121 (1995) 333-346
9. Carr J.L., Shashikant C.S., Bailey W.J., and Ruddle F.H. Molecular evolution of Hox gene regulation: cloning and transgenic analysis of the lamprey HoxQ8 gene. J. Exp. Zool. 280 (1998) 73-85
10. Carroll S.B., Grenier J.K., and Scott D.W. Building animals. In: Carrol S.B., et al. (Ed). From DNA to Diversity. Second edition (2005), Blackwell Publishing, Ltd., Massachusetts 51-102
11. Chisaka O., Musci T.S., and Capecchi M.R. Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature 355 (1992) 516-520
12. Cohn M.J. Lamprey Hox genes and the origin of jaws. Nature 416 (2002) 386-387
13. Condie B.G., and Capecci M.R. Mice homozygous for a targeted disruption of Hoxd-3 (Hox-4.1) exhibit anterior transformations of the first and second cervical vertebrae, the atlas and the axis. Development 119 (1993) 579-595
14. Couly G., Grapin-Botton A., Coltey P., Ruhin B., and Le Douarin N.M. Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 125 (1998) 3445-3459
15. Damas H. Recherches sur le development de Lampetra fluviatilis L.-contribution a l'étude de la céphalogenèse des vertébrés. Arch. Biol. Paris 55 (1944) 1-289
16. Dasen J.S., Tice B.C., Brenner-Morton S., and Jessell T.M. A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123 (2005) 477-491
17. Dehal P., and Boore J.L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3 (2005) e314
18. Dekker E.-J., Pannese M., Houtzager E., Boncinelli E., and Durston A. Colinearity in the Xenopus laevis Hox-2 complex. Mech. Dev. 40 (1993) 3-12
19. Dollé P., and Duboule D. Two gene members of the murine HOX-5 complex show regional and cell-type specific expression in developing limbs and gonads. EMBO J. 8 (1989) 1507-1515
20. Duboule D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development (1994) 135-142
21. Duboule D., and Morata G. Colinearity and functional hierarchy among genes of he nomeotic complexes. Trends Genet. 10 (1994) 358-364
22. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.L., and Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 (1999) 1531-1545
23. Force A., Amores A., and Postlethwait J.H. Hox cluster organization in the jawless vertebrate Petromyzon marinus. J. Exp. Zool. Part B 294 (2002) 30-46
24. Freitas R., Zhang G.-J., and Cohn M.J. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442 (2006) 1033-1037
25. Fried C., Prohaska S.J., and Stadler P.F. Independent Hox-cluster duplications in lampreys. J. Exp. Zool. Part B (Mol. Dev. Evol.) 299 (2003) 18-25
26. Fritzsch B., and Northcutt R.G. Cranial and spinal nerve organization in amphioxus and lampreys: evidence for an ancestral craniate pattern. Acta Anat. (Basel) 148 (1993) 96-109
27. Frohman M.A., Dush M.K., and Martin G.R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 8998-9002
28. Frohman M.A., Boyle M., and Martin G.R. Isolation of the mouse Hox-2.9 gene; analysis of embryonic expression suggests that positional information along the anterior-posterior axis is specified by mesoderm. Development 110 (1990) 589-607
29. Galliot B. Relaxed constraints on Hox gene clustering during evolution. Heredity 94 (2005) 277
30. Garcia-Fernàndez J., and Holland P.W.H. Archetypal organization of the amphioxus Hox gene cluster. Nature 379 (1994) 563-566
31. Gendron-Maguire M., Mallo M., Zhang M., and Gridley T. Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 75 (1993) 1317-1331
32. Gilland E., and Baker R. Evolutionary patterns of cranial nerve efferent nuclei in vertebrates. Brain Behav. Evol. 66 (2005) 234-254
33. Graham A., Papalopulu N., and Krumlauf R. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 57 (1989) 367-378
34. Grammatopoulos G.A., Bell E., Toole L., Lumsden A., and Tucker A.S. Homeotic transformation of branchial arch identity after Hoxa2 overexpression. Development 127 (2000) 5355-5365
35. Guthrie S., Muchamore I., Kuroiwa A., Marshall H., Krumlauf R., and Lumsden A. Neuroectodermal autonomy of Hox-2.9 expression revealed by rhombomere transpositions. Nature 356 (1992) 157-159
36. Hogan B.L.M., Thaller C., and Eichele G. Evidence that Hensen's node is a site of retinoic acid synthesis. Nature 359 (1992) 237-241
37. Horigome N., Myojin M., Hirano S., Ueki T., Aizawa S., and Kuratani S. Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev. Biol. 207 (1999) 287-308
38. Hunt P., Gulisano M., Cook M., Sham M.H., Faiella A., Wilkinson D., Boncinelli E., and Krumlauf R. A distinct Hox code for the branchial region of the vertebrate head. Nature 353 (1991) 861-864
39. Hunter M.P., and Prince V.E. Zebrafish hox paralogue group 2 genes function redundantly as selector genes to pattern the second pharyngeal arch. Dev. Biol. 247 (2002) 367-389
40. Ikuta T., and Saiga H. Organization of Hox genes in ascidians: present, past, and future. Dev. Dyn. 233 (2005) 382-389
41. Ikuta T., Yoshida N., Satoh N., and Saiga H. Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 15118-15123
42. Irvine S.Q., Carr J.L., Bailey W.J., Kawasaki K., Shimizu N., Amemiya C.T., and Ruddle F.H. Genomic analysis of Hox clusters in the sea lamprey Petromyzon marinus. J. Exp. Zool. Part B 294 (2002) 47-62
43. Izpisúa-Belmonte J.-C., Falkenstein H., Dollé P., Renucci A., and Duboule D. Murine genes related to the Drosophila AbdB homeotic gene are sequentially expressed during development of the posterior part of the body. EMBO J. 10 (1991) 2279-2289
44. Johnels A.G. On the development and morphology of the skeleton of the head of Petromyozon. Acta Zool. 29 (1948) 139-279
45. Jollie M.T. On the origin of the chordates. Acta Zool. (Stockh.) 54 (1973) 81-100
46. Katsuyama Y., Wada S., Yasugi S., and Saiga H. Expression of the labial group Hox gene HrHox-1 and its lateration induced by retinoic acid in development of the ascidian Halocynthia roretzi. Development 121 (1995) 3197-3205
47. Kaufman T.C., Seeger M.A., and Olsen G. Molecular and genetic organization of the Antennapedia gene complex of Drosophila melanogaster. Adv. Genet. 27 (1990) 309-362
48. Kessel M. Respecification of vertebral identities by retinoic acid. Development 115 (1992) 487-501
49. Kessel M., Balling R., and Gruss P. Variations of cervical vertebrate after expression of a Hox-1.1 transgene in mice. Cell 61 (1990) 301-308
50. Keys D.N., Lee B., Di Gregorio A., Harafuji N., Detter J.C., Wang M., Kahsai O., Ahn S., Zhang C., Doyle S.A., et al. A saturation screen for cis-acting regulatory DNA in the Hox genes of Ciona intestinalis. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 679-683
51. Kimmel C.B., Miller C.T., and Keynes R.J. Neural crest patterning and the evolution of the jaw. J. Anat. 199 (2001) 105-120
52. Kmita M., and Duboule D. Organizing axes in time and space; 25 years of collinear tinkering. Science 301 (2003) 331-333
53. Koltzoff N.K. Entwicklungsgeschichte des Kopfes von Petromyozon planeri. Bull. Soc. Nat. Moscou 15 (1901) 259-289
54. Krumlauf R. Hox genes in vertebrate development. Cell 78 (1994) 191-201
55. Kuraku S., and Kuratani S. Timescale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zool. Sci. 23 (2006) 1053-1064
56. Kuratani S. Cephalic neural crest cells and the evolution of craniofacial structures in vertebrates: morphological and embryological significance of the premandibular-mandibular boundary. Zoology 108 (2005) 13-25
57. Kuratani S., Ueki T., Aizawa S., and Hirano S. Peripheral development of the cranial nerves in a cyclostome, Lampetra japonica: morphological distribution of nerve branches and the vertebrate body plan. J. Comp. Neurol. 384 (1997) 483-500
58. Kuratani S., Horigome N., Ueki T., Aizawa S., and Hirano S. Stereotyped axonal bundle formation and neuromeric patterns in embryos of a cyclostome, Lampetra japonica. J. Comp. Neurol. 391 (1998) 99-114
59. Kuratani S., Nobusada Y., Horigome N., and Shigetani Y. Embryology of the lamprey and evolution of the vertebrate jaw: insights from molecular and developmental perspectives. Philos. Trans. R. Soc. Lond., B Biol. Sci. 356 (2001) 1615-1632
60. Lance-Jones C., Omelchenko N., Bailis A., Lynch S., and Sharma K. Hoxd10 induction and regionalization in the developing lumbosacral spinal cord. Development 128 (2001) 2255-2268
61. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 276 (1978) 565-570
62. Lumsden A., and Krumlauf R. Patterning the vertebrate neuraxis. Science 274 (1996) 1109-1115
63. Matsuo I., Kuratani S., Kimura C., Takeda N., and Aizawa S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9 (1995) 2558-2646
64. McCauley D.W., and Bronner-Fraser M. Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441 (2006) 750-752
65. McGinnis W., and Krumlauf R. Homeobox genes and axial paterning. Cell 68 (1992) 283-302
66. McLysaght A., Hokamp K., and Wolfe K.H. Extensive genomic duplication during early chordate evolution. Nat. Genet. 31 (2002) 200-204
67. Minguillón C., Gardenyes J., Serra E., Catro L.F.C., Hill-Force A., Holland P.W.H., Amemiya C.T., and Garcia-Fernàndez J. No more than 14: the end of the amphioxus Hox cluster. Int. J. Biol. Sci. 1 (2005) 19-23
68. Morgan B.A., Izpisua-Belmonte J.C., Duboule D., and Tabin C.J. Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358 (1992) 236-239
69. Murakami Y., Ogasawara M., Sugahara F., Hirano S., Satoh N., and Kuratani S. Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates. Development 128 (2001) 3521-3531
70. Murakami Y., Pasqualetti M., Takio Y., Hirano S., Rijli F.M., and Kuratani S. Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain. Development 131 (2004) 983-995
71. Murakami Y., Uchida K., Rijli F.M., and Kuratani S. Evolution of the brain developmental plan: insights from agnathans. Dev. Biol. 280 (2005) 249-259
72. Murphy P., and Hill R.E. Expression of the mouse labial-like homeobox-containing genes, Hox2.9 and Hox1.6, during segmentation of the hindbrain. Development 111 (1991) 71-74
73. Nakao T., and Ishizawa A. Light- and electron-microscopic observations of the tail bud of the larval lamprey (Lampetra japonica), with special reference to neural tube formation. Am. J. Anat. 170 (1984) 55-71
74. Nieto M.A., Bradley L.C., Hunt P., Das Gupta R., Krumlauf R., and Wilkinson D.G. Molecular mechanisms of pattern formation in the vertebrate hindbrain. Ciba Found. Symp. 165 (1992) 92-102
75. Omelchenko N., and Lance-Jones C. Programming neural Hoxd10: in vivo evidence that early node-associated signals predominate over paraxial mesoderm signals at posterior spinal levels. Dev. Biol. 261 (2003) 99-115
76. Pasqualetti M., Ori M., Nardi I., and Rijli F.M. Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus. Development 127 (2000) 5367-5378
77. Pearson J.C., Lemons D., and McGinnis W. Modulating Hox gene functions during animal body patterning. Nat. Rev., Genet. 6 (2005) 893-904
78. Rhinn M., Lun K., Amores A., Yan Y.L., Postlethwait J.H., and Brand M. Cloning, expression and relationship of zebrafish gbx1 and gbx2 genes to Fgf signaling. Mech. Dev. 120 (2003) 919-936
79. Rhinn M., Lun K., Werner M., Simeone A., and Brand M. Isolation and expression of the homeobox gene Gbx1 during mouse development. Dev. Dyn. 229 (2004) 334-339
80. Rijli F.M., Mark M., Lakkaraju S., Dierich A., Dolle P., and Chambon P. 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 (1993) 1333-1349
81. Rijli F.M., Matyas R., Pellegrini M., Dierich A., Gruss P., Dolle P., and Chambon P. Cryptorchidism and homeotic transformations of spinal nerves and vertebrae in Hoxa-10 mutant mice. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 8185-8189
82. Santagati F., Minoux M., Ren S.-Y., and Rijli F.M. Temporal requirement of Hoxa2 in cranial neural crest skeletal morphogenesis. Development 132 (2005) 4927-4936
83. Schubert M., Holland N.D., Laudet V., and Holland L.Z. A retinoic acid-Hox hierarchy controls both anterior/posterior patterning and neuronal specification in the developing central nervous system of the cephalochordate amphioxus. Dev. Biol. 296 (2006) 190-202
84. Seo H.-C., Edvardsen R.B., Maeland A.D., Bjordal M., Jensen M.F., Hansen A., Flaat M., Weissenbach J., Lehrach H., Wincker P., Reinhardt R., and Chourrout D. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431 (2004) 67-71
85. Shamim H., and Mason I. Expression of Gbx-2 during early development of the chick embryo. Mech. Dev. 76 (1998) 157-159
86. Shigetani Y., Sugahara F., and Kuratani S. A new evolutionary scenario for the vertebrate jaw. BioEssays 27 (2005) 331-338
87. Slack J.M., Holland P.W., and Graham C.F. The zootype and the phylotypic stage. Nature 361 (1993) 490-492
88. Stadler P.F., Fried C., Prohaska S.J., Bailey W.J., Misof B.Y., Ruddle F.H., and Wagner G.P. Evidence for independent Hox gene duplications in the hagfish lineage: a PCR-based gene inventory of Eptatretus stoutii. Mol. Phylogenet. Evol. 32 (2004) 686-694
89. Steinberg M. A nonnutrient culture medium for amphibian embryonic tissues. Carnegie Inst. Washington Year Book 56 (1957) 347-348
90. Stern C.D., and Foley A.C. Molecular dissection of Hox gene induction and maintenance in the hindbrain. Cell 94 (1998) 143-145
91. Su Y., and Meng A. The expression of gbx-2 during zebrafish embryogenesis. Mech. Dev. 113 (2002) 107-110
92. Sundin O.H., and Eichele G. A homeo domain protein reveals the metameric nature of the developing chick hindbrain. Genes Dev. 4 (1990) 1267-1276
93. Tahara Y. Normal stages of development in the lamprey, Lampetra reissneri (Dybowski). Zool. Sci. 5 (1988) 109-118
94. Takahashi T., and Holland P.W.H. Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development. Development 131 (2004) 3285-3294
95. Takio, Y., Pasqualetti, M., Kuraku, S., Hirano, M. Rijli, F., Kuratani, S., 2004. Lamprey Hox genes and the evolution of jaws. Nature OnLine 429, 1 p following 262. http://www.nature.com/cgi-taf/DynaPage.taf?file=/nature/journal/v429/n69 89/full/nature02616_fs.html.
96. Tiret L., Le Mouellic H., Maury M., and Brulet P. Increased apoptosis of motorneurons and altered somatotopic maps in the brachial spinal cord of Hoxc-8-deficient mice. Development 125 (1998) 279-291
97. Trainor P.A., and Krumlauf R. Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nat. Rev., Neurosci. 1 (2000) 116-124
98. van der Hoeven F., Sordino P., Fraudeau N., Izpisúa-Belmonte J.-C., and Duboule D. Teleost HoxD and HoxA genes: comparison with tetrapods and functional evolution of the HOXD complex. Mech. Dev. 54 (1996) 9-21
99. von Kupffer C. Studien zur vergleichenden Entwickelungsgeschichte des Kopfes der Kranioten (1900), Verlag von J.F. Lehmann, München and Leipzig
100. Wada H., Saiga H., Satoh N., and Holland P.W.H. Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax-2/5/8, Hox and Otx genes. Development 125 (1998) 1113-1122
101. Wada H., Garcia-Fernandez J., and Holland P.W. Colinear and segmental expression of amphioxus Hox genes. Dev. Biol. 213 (1999) 131-141