Patterning the ascidian nervous system: Structure, expression and transgenic analysis of the CiHox3 gene

Development

Volumn 126, Issue 21, 1999, Pages 4737-4748

  Locascio, Annamaria ^a   Aniello, Francesco ^a   Amoroso, Alessandro ^a   Manzanares, Miguel ^b   Krumlauf, Robb ^b   Branno, Margherita ^a  

^a STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

CiHox3; Hox genes; Nervous system; Transcriptional regulation; Urochordate

Indexed keywords

MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASCIDIACEA; AUTONOMIC GANGLION; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO PATTERN FORMATION; GENE EXPRESSION; GENE STRUCTURE; HOMEOBOX; MOLECULAR CLONING; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; TISSUE SPECIFICITY; TRANSGENIC ANIMAL;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BETA-GALACTOSIDASE; BODY PATTERNING; CENTRAL NERVOUS SYSTEM; CIONA INTESTINALIS; CONSERVED SEQUENCE; ELECTROPORATION; EMBRYO, NONMAMMALIAN; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NERVOUS SYSTEM PHYSIOLOGY; PROMOTER REGIONS (GENETICS); SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; ASCIDIA; ASCIDIACEA; CHORDATA; CIONA; CIONA INTESTINALIS; EUKARYOTA; INVERTEBRATA; VERTEBRATA;

EID: 0032727636     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Amores, A., Force, A., Yan, Y. L., Joly, L., Amemiya, C., Fritz, A., Ho, R., Langeland, J., Prince, V., Wang, Y. L., Westerfield, M., Ekker, M. and Postlehwait, J. (1998). Zebrafish box cluster and vertebrate genome evolution. Science 282, 1711-1714.
2. Aparicio, S., Hawker, K., Cottage, A., Mikawam Y., Zuo, L., Chen, E., Krumlauf, R. and Brenner, S. (1997). Organization of the Fugu rubripes Hox clusters, evidence for continuing evolution of vertebrate Hox complexes. Nature Genetics 16, 79-84.
3. Barnes, S. N. (1971). Fine structure of the photoreceptor and cerebral ganglion of the tadpole larva of Amaroucium constellation (Verrill) (Subphylum: Urochordata; Class: Ascidiacea). Z. Zellforsch 117, 1-16.
4. Beachy, P. A., Helfand, S. L. and Hogness, D. S. (1985). Segmental distribution of bithorax complex proteins during Drosophila development. Nature 313, 545-551.
5. Boncinelli, E., Somma, R., Acampora, D., Pannese, M., D'Esposito, M., Faiella, A. and Simeone, A. (1988). Organization of human homeobox genes. Human Reprod. 3, 880-886.
6. Burglin, T. R. and Ruvkun, G. (1993). The Caenorhabditis elegans homeobox gene cluster. Curr. Opinion Genes Dev. 3, 615-620.
7. Burgtorf, C., Welzel, K., Hasenbank, R., Zehetner, G., Weis, S. and Lehrach, H. (1998). Gridded genomic libraries of different chordate species: a reference library system for basic and comparative genetic studies of chordate genomes. Genomics 52, 230-232.
8. Caracciolo, A., Gesualdo, I., Branno, M., Aniello, F., Di Lauro, R. and Palumbo, A. (1997). Specific cellular localization of tyrosinase mRNA during dona intestinalis larval development. Dev. Growth Differ. 39, 437-444.
9. Carpenter, E. M., Goddard, J. M., Chisaka, O., Manley, N. R. and Capecchi, M. R. (1993). Loss of Hoxa-1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 118, 1063-1075.
10. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
11. Corbo, J. C., Erives, A., Di Gregorio, A., Chang, A. and Levine, M. (1997a). Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate. Development 124, 2335-2344.
12. Corbo, J. C., Levine, M. and Zeller, R. W. (1997b). Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. Development 124, 589-602.
13. Di Gregorio, A. and Levine, M. (1998). Ascidian embryogenesis and the origin of the chordate body plan. Curr. Opin. Genes Dev. 8, 457-463.
14. Di Gregorio, A., Spagnuolo, A., Ristoratore, F., Pischetola, M., Aniello, F., Branno, M., Cariello, L. and Di Lauro, R. (1995). Cloning of ascidian homeobox genes provides evidence for a primordial chordate cluster. Gene 156, 253-257.
15. Di Gregorio, A., Villani, M. G., Locascio, A., Ristoratore, F., Aniello, F. and Branno, M. (1998). Developmental regulation and tissue-specific localization of calmodulin mRNA in the protochordate Ciona intestinalis. Dev. Growth Diff. 40, 387-394.
16. Duboule, D. (1993). The function of Hox genes in the morphogenesis of the vertebrate limb. Ann. Genet. 36, 24-9.
17. Duboule, D. (1994). Guidebook of Homeobox Genes. Oxford: IRL Press.
18. Duboule, D. and Dollè, P. (1989). The structural and functional organization of the murine Hox gene family resembles that of Drosophila homeotic genes. EMBO J. 8, 1497-1505.
19. Field, K. G., Olsen, G. J., Lane, D. J., Giovannoni, S. J., Ghiselin, M. T., Raff, E. C., Pace, N. R. and Raff, R. A. (1988). Molecular phylogeny of the animal kingdom. Science 239, 748-753.
20. Gellon, G. and McGinnis, W. (1998). Shaping animal body plans in development and evolution by modulation of Hox expression patterns. BioEssays 20, 116-125.
21. Gionti, M., Ristoratore, F., Di Gregorio, A., Aniello, F., Branno, M. and Di Lauro, R. (1998). Cihox5, a new Ciona intestinalis Hox-related gene, is involved in regionalization of the spinal cord. Dev. Genes Evol. 207, 515-523.
22. Glardon, S., Callaerts, P., Halder, G. and Gehring, W. J. (1997). Conservation of Pax-6 in a lower chordate, the ascidian Phallusia mammillata. Development 124, 817-825.
23. Gould, A., Morrison, A., Sproat, G., White, R. and Krumlauf, R. (1997). Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 11, 900-913.
24. Graham, A., Papalopulu, N. and Krumlauf, R. (1989). The murine and Drosophila homeobox clusters have common features of organisation and expression. Cell 57, 367-378.
25. Holland, P. W. H. (1992). Homeobox genes in vertebrate evolution. BioEssays 14, 267-273.
26. Holland, P. W. H., Garcia-Fernandez, J., Williams, N. A. and Sidow, A. (1994). Gene duplications and the origins of vertebrate development. Development 1994 Supplement, 125-133.
27. Holland, P. W. H., Holland, L. Z., Williams, N. A. and Holland, N. D. (1992). An amphioxus homeobox gene: sequence conservation, spatial expression during development and insights into vertebrate evolution. Development 116, 653-661.
28. Hunt, P., Gulisano, M., Cook, M., Sham, M., Faiella, A., Wilkinson, D., Boncinelli, E. and Krumlauf, R. (1991). A distinct Hox code for the branchial region of the head. Nature 353, 861-864.
29. Kappen, C., Schugart, K. and Ruddle, F. (1989). Two steps in the evolution of Antennapedia-class vertebrate homeobox genes. Proc. Natl. Acad. Sci. USA 86, 5459-5463.
30. Katsuyama, Y., Wada, S., Yasugi, S. and Saiga, H. (1995). Expression of the labial group Hox gene HrHox-1 and its alteration induced by retinoic acid in development of the ascidian Halocynthia roretzi. Development 121, 3197-3205.
31. Keynes, R., and Krumlauf, R. (1994). Hox genes and regionalization of the nervous system. Ann. Rev. Neurosci. 17, 109-132.
32. Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78, 191-201.
33. Lewis, E. B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565-570.
34. Lufkin, T. (1996). Transcriptional control of Hox genes in the vertebrate nervous system. Curr. Opin. Gen. Dev. 6, 575-580.
35. Lumsden, A. (1990). The cellular basis of segmentation in the developing hindbrain. Trends Neurosci. 13, 329-335.
36. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
37. Maconochie, M. K., Nonchev, S., Morrison, A. and Krumlauf, R. (1996). Paralogous Hox Genes: Function and Regulation. Annu. Rev. Genet. 30, 529-556.
38. Manzanares, M., Cordes, S., Ariza-McNaughton, L., Sadl, V., Maruthainer, K., Barsh, G. and Krumlauf, R. (1999). Conserved and divergent roles of kreisler in regulation of the paralogous Hoxa3 and Hoxb3 genes. Development 126, 759-769.
39. Manzanares, M., Cordes, S., Kwan, C.-T., Sham, M. H., Barsh, G. S. and Krumlauf, R. (1997). Segmental regulation of Hoxb-3 by kreisler. Nature 387, 191-195.
40. Mark, M., Lufkin, T., Vonesch, J.-L., Ruberte, E., Olivo, J.-C., Dollé, P., Gorry, P., Lumsden, A. and Chambon, P. (1993). Two rhombomeres are altered in Hoxa-1 mutant mice. Development 119, 319-338.
41. Marshall, H., Nonchev, S., Sham, M. H., Muchamore, I., Lumsden, A. and Krumlauf, R. (1992). Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360, 737-741.
42. McGinnis, W. and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell 68, 283-302.
43. Nicol, D. and Meinertzhagen, I. A. (1991). Cell counts and maps in the larval central nervous system of the ascidian Ciona intestinalis (L). J. Comp. Neurol. 309, 415-429.
44. Popperl, H., Bienz, M., Studer, M., Chan, S.-K., Aparicio, S., Brenner, S., Mann, R. S. and Krumlauf, R. (1995). Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81, 1031-1042.
45. Rubenstein, J. L. and Puelles, L. (1994). Homeobox gene expression during development of the vertebrate brain. Curr. Top. Dev. Biol. 29, 1-63.
46. nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
47. Schugart, K., Kappen, C. and Ruddle, F. H. (1988). Mammalian homeobox-containing genes: genome organization, structure, expression and evolution. Br. J. Cancer 58, Suppl. IX, 9-13.
48. Sham, M. H., Hunt, P., Nonchev, S., Papalopulu, N., Graham, A., Boncinelli, E. and Krumlauf, R. (1992). Analysis of the murine Hox 2.7 gene: conserved alternative transcripts with differential distribution in the nervous system and the potential for shared regulatory regions. EMBO J. 11, 1825-1836.
49. Studer, M., Gavalas, A., Marshall, H., Ariza-McNaughton, L., Rijli, F., Chambon, P. and Krumlauf, R. (1998). Genetic interaction between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125, 1025-1036.
50. Studer, M., Lumsden, A., Ariza-McNaughton, L., Bradley, A. and Krumlauf, R. (1996). Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630-635.
51. Tiret, L., Le Mouelic, H., Maury, M. and Brulet, P. (1998). Increased apoptosis of motoneurons and altered somatotopic maps in the branchial spinal cord of Hoxc8-deficient mice. Development 125, 279-291.
52. Tomlinson, C. R., Kozlowski, M. T. and Krein, W. H. (1990). Ectoderm nuclei from sea urchin embryos contain a spec-DNA binding protein similar to the vertebrate transcription factor USF. Development 110, 259-272.
53. Wada, H., Holland, P. W. H., Sato, S., Yamamoto, H. and Satoh, N. (1997). Neural tube is partially dorsalized by overexpression of HrPax-37: the ascidian homologue of Pax-3 and Pax-7. Dev. Biol. 187, 240-252.
54. Wada, H., Saiga, H., Satoh, N. and Holland, P. W. H. (1998). 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, 1113-1122.
55. Whiting, J., Marshall, H., Cook, M., Krumlauf, R., Rigby, P. W. J., Stott, D. and Allemann, R. K. (1991). Multiple spatially specific enhancers are required to reconstruct the pattern of Hox-2.6 gene expression. Genes Dev. 5, 2048-2059.
56. Yee, S.-P. and Rigby, P. W. J. (1993). The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 7, 1277-1289.
57. Yuh, C-H., Ransick, A., Martinez, P., Britten, R. J. and Davidson, E. H. (1994). Complexity and organization of DNA-protein interactions in the 5′-regulatory region of an endoderm-specific marker gene in the sea urchin embryo. Mech. Dev. 47, 165-186.