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. 1993 Apr 1;90(7):2729–2733. doi: 10.1073/pnas.90.7.2729

Homeobox genes are expressed in the retina and brain of adult goldfish.

E M Levine 1, N Schechter 1
PMCID: PMC46169  PMID: 8096640

Abstract

The goldfish (Carassius auratus) visual pathway displays continuous growth and plasticity throughout life. Since homeobox genes are important transcriptional regulators in development, we searched for homeobox genes in the adult goldfish retina and brain. Using the PCR, we discovered a repertoire of homeobox sequences expressed in these tissues. In addition to isolating homeodomain sequences found in the vertebrate Hox gene clusters, a sequence identical to the chicken CHox7 homeodomain was characterized. Furthermore, a sequence with significant homologies to the Xenopus XIHbox8 and leech Htr-A2 homeodomains was identified, and these sequences may define an additional class of homeodomain. Finally, a sequence belonging to the paired class (prd) of homeodomains is reported. Homeobox gene expression in the adult goldfish retina and brain may be associated with the persistent developmental features of these tissues.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Acampora D., D'Esposito M., Faiella A., Pannese M., Migliaccio E., Morelli F., Stornaiuolo A., Nigro V., Simeone A., Boncinelli E. The human HOX gene family. Nucleic Acids Res. 1989 Dec 25;17(24):10385–10402. doi: 10.1093/nar/17.24.10385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baron A., Featherstone M. S., Hill R. E., Hall A., Galliot B., Duboule D. Hox-1.6: a mouse homeo-box-containing gene member of the Hox-1 complex. EMBO J. 1987 Oct;6(10):2977–2986. doi: 10.1002/j.1460-2075.1987.tb02603.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boncinelli E., Acampora D., Pannese M., D'Esposito M., Somma R., Gaudino G., Stornaiuolo A., Cafiero M., Faiella A., Simeone A. Organization of human class I homeobox genes. Genome. 1989;31(2):745–756. doi: 10.1139/g89-133. [DOI] [PubMed] [Google Scholar]
  4. Bopp D., Burri M., Baumgartner S., Frigerio G., Noll M. Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila. Cell. 1986 Dec 26;47(6):1033–1040. doi: 10.1016/0092-8674(86)90818-4. [DOI] [PubMed] [Google Scholar]
  5. Brown R., Brockes J. P. Identification and expression of a regeneration-specific homeobox gene in the newt limb blastema. Development. 1991 Feb;111(2):489–496. doi: 10.1242/dev.111.2.489. [DOI] [PubMed] [Google Scholar]
  6. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Easter S. S., Jr, Stuermer C. A. An evaluation of the hypothesis of shifting terminals in goldfish optic tectum. J Neurosci. 1984 Apr;4(4):1052–1063. doi: 10.1523/JNEUROSCI.04-04-01052.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fainsod A., Greunbaum Y. A chicken homeo box gene with developmentally regulated expression. FEBS Lett. 1989 Jul 3;250(2):381–385. doi: 10.1016/0014-5793(89)80760-4. [DOI] [PubMed] [Google Scholar]
  9. Frohman M. A., Boyle M., 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. 1990 Oct;110(2):589–607. doi: 10.1242/dev.110.2.589. [DOI] [PubMed] [Google Scholar]
  10. Giordano S., Glasgow E., Tesser P., Schechter N. A type II keratin is expressed in glial cells of the goldfish visual pathway. Neuron. 1989 May;2(5):1507–1516. doi: 10.1016/0896-6273(89)90197-9. [DOI] [PubMed] [Google Scholar]
  11. Glasgow E., Druger R. K., Levine E. M., Fuchs C., Schechter N. Plasticin, a novel type III neurofilament protein from goldfish retina: increased expression during optic nerve regeneration. Neuron. 1992 Aug;9(2):373–381. doi: 10.1016/0896-6273(92)90175-d. [DOI] [PubMed] [Google Scholar]
  12. Gruss P., Walther C. Pax in development. Cell. 1992 May 29;69(5):719–722. doi: 10.1016/0092-8674(92)90281-g. [DOI] [PubMed] [Google Scholar]
  13. Harvey R. P., Tabin C. J., Melton D. A. Embryonic expression and nuclear localization of Xenopus homeobox (Xhox) gene products. EMBO J. 1986 Jun;5(6):1237–1244. doi: 10.1002/j.1460-2075.1986.tb04352.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hawkins N. C., McGhee J. D. Homeobox containing genes in the nematode Caenorhabditis elegans. Nucleic Acids Res. 1990 Oct 25;18(20):6101–6106. doi: 10.1093/nar/18.20.6101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Heacock A. M., Agranoff B. W. Enhanced labeling of a retinal protein during regeneration of optic nerve in goldfish. Proc Natl Acad Sci U S A. 1976 Mar;73(3):828–832. doi: 10.1073/pnas.73.3.828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hill R. E., Jones P. F., Rees A. R., Sime C. M., Justice M. J., Copeland N. G., Jenkins N. A., Graham E., Davidson D. R. A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1. Genes Dev. 1989 Jan;3(1):26–37. doi: 10.1101/gad.3.1.26. [DOI] [PubMed] [Google Scholar]
  17. Hitchcock P. F., Lindsey Myhr K. J., Easter S. S., Jr, Mangione-Smith R., Jones D. D. Local regeneration in the retina of the goldfish. J Neurobiol. 1992 Mar;23(2):187–203. doi: 10.1002/neu.480230209. [DOI] [PubMed] [Google Scholar]
  18. Holland P. W. Cloning and evolutionary analysis of msh-like homeobox genes from mouse, zebrafish and ascidian. Gene. 1991 Feb 15;98(2):253–257. doi: 10.1016/0378-1119(91)90182-b. [DOI] [PubMed] [Google Scholar]
  19. James R., Kazenwadel J. Homeobox gene expression in the intestinal epithelium of adult mice. J Biol Chem. 1991 Feb 15;266(5):3246–3251. [PubMed] [Google Scholar]
  20. Johns P. R., Easter S. S., Jr Growth of the adult goldfish eye. II. Increase in retinal cell number. J Comp Neurol. 1977 Dec 1;176(3):331–341. doi: 10.1002/cne.901760303. [DOI] [PubMed] [Google Scholar]
  21. Johns P. R., Fernald R. D. Genesis of rods in teleost fish retina. Nature. 1981 Sep 10;293(5828):141–142. doi: 10.1038/293141a0. [DOI] [PubMed] [Google Scholar]
  22. Kessel M., Gruss P. Murine developmental control genes. Science. 1990 Jul 27;249(4967):374–379. doi: 10.1126/science.1974085. [DOI] [PubMed] [Google Scholar]
  23. Kongsuwan K., Webb E., Housiaux P., Adams J. M. Expression of multiple homeobox genes within diverse mammalian haemopoietic lineages. EMBO J. 1988 Jul;7(7):2131–2138. doi: 10.1002/j.1460-2075.1988.tb03052.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Krauss S., Johansen T., Korzh V., Fjose A. Expression pattern of zebrafish pax genes suggests a role in early brain regionalization. Nature. 1991 Sep 19;353(6341):267–270. doi: 10.1038/353267a0. [DOI] [PubMed] [Google Scholar]
  25. Krauss S., Johansen T., Korzh V., Moens U., Ericson J. U., Fjose A. Zebrafish pax[zf-a]: a paired box-containing gene expressed in the neural tube. EMBO J. 1991 Dec;10(12):3609–3619. doi: 10.1002/j.1460-2075.1991.tb04927.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Laughon A. DNA binding specificity of homeodomains. Biochemistry. 1991 Dec 3;30(48):11357–11367. doi: 10.1021/bi00112a001. [DOI] [PubMed] [Google Scholar]
  27. McGinnis W., Garber R. L., Wirz J., Kuroiwa A., Gehring W. J. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell. 1984 Jun;37(2):403–408. doi: 10.1016/0092-8674(84)90370-2. [DOI] [PubMed] [Google Scholar]
  28. Meyer R. L. Evidence from thymidine labeling for continuing growth of retina and tectum in juvenile goldfish. Exp Neurol. 1978 Mar;59(1):99–111. doi: 10.1016/0014-4886(78)90204-2. [DOI] [PubMed] [Google Scholar]
  29. Monaghan A. P., Davidson D. R., Sime C., Graham E., Baldock R., Bhattacharya S. S., Hill R. E. The Msh-like homeobox genes define domains in the developing vertebrate eye. Development. 1991 Aug;112(4):1053–1061. doi: 10.1242/dev.112.4.1053. [DOI] [PubMed] [Google Scholar]
  30. Murtha M. T., Leckman J. F., Ruddle F. H. Detection of homeobox genes in development and evolution. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10711–10715. doi: 10.1073/pnas.88.23.10711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Njølstad P. R., Molven A., Hordvik I., Apold J., Fjose A. Primary structure, developmentally regulated expression and potential duplication of the zebrafish homeobox gene ZF-21. Nucleic Acids Res. 1988 Oct 11;16(19):9097–9111. doi: 10.1093/nar/16.19.9097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Perry G. W., Burmeister D. W., Grafstein B. Fast axonally transported proteins in regenerating goldfish optic axons. J Neurosci. 1987 Mar;7(3):792–806. doi: 10.1523/JNEUROSCI.07-03-00792.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Püschel A. W., Gruss P., Westerfield M. Sequence and expression pattern of pax-6 are highly conserved between zebrafish and mice. Development. 1992 Mar;114(3):643–651. doi: 10.1242/dev.114.3.643. [DOI] [PubMed] [Google Scholar]
  34. Raymond P. A., Reifler M. J., Rivlin P. K. Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. J Neurobiol. 1988 Jul;19(5):431–463. doi: 10.1002/neu.480190504. [DOI] [PubMed] [Google Scholar]
  35. Raymond P. A., Rivlin P. K. Germinal cells in the goldfish retina that produce rod photoreceptors. Dev Biol. 1987 Jul;122(1):120–138. doi: 10.1016/0012-1606(87)90338-1. [DOI] [PubMed] [Google Scholar]
  36. Robert B., Sassoon D., Jacq B., Gehring W., Buckingham M. Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. EMBO J. 1989 Jan;8(1):91–100. doi: 10.1002/j.1460-2075.1989.tb03352.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. SPERRY R. W. CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS. Proc Natl Acad Sci U S A. 1963 Oct;50:703–710. doi: 10.1073/pnas.50.4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Savard P., Gates P. B., Brockes J. P. Position dependent expression of a homeobox gene transcript in relation to amphibian limb regeneration. EMBO J. 1988 Dec 20;7(13):4275–4282. doi: 10.1002/j.1460-2075.1988.tb03325.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Scott M. P., Tamkun J. W., Hartzell G. W., 3rd The structure and function of the homeodomain. Biochim Biophys Acta. 1989 Jul 28;989(1):25–48. doi: 10.1016/0304-419x(89)90033-4. [DOI] [PubMed] [Google Scholar]
  40. Scott M. P., Weiner A. J. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4115–4119. doi: 10.1073/pnas.81.13.4115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Shen W. F., Detmer K., Mathews C. H., Hack F. M., Morgan D. A., Largman C., Lawrence H. J. Modulation of homeobox gene expression alters the phenotype of human hematopoietic cell lines. EMBO J. 1992 Mar;11(3):983–989. doi: 10.1002/j.1460-2075.1992.tb05137.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stornaiuolo A., Acampora D., Pannese M., D'Esposito M., Morelli F., Migliaccio E., Rambaldi M., Faiella A., Nigro V., Simeone A. Human HOX genes are differentially activated by retinoic acid in embryonal carcinoma cells according to their position within the four loci. Cell Differ Dev. 1990 Aug;31(2):119–127. doi: 10.1016/0922-3371(90)90015-o. [DOI] [PubMed] [Google Scholar]
  43. Thor S., Ericson J., Brännström T., Edlund T. The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron. 1991 Dec;7(6):881–889. doi: 10.1016/0896-6273(91)90334-v. [DOI] [PubMed] [Google Scholar]
  44. Walther C., Gruss P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development. 1991 Dec;113(4):1435–1449. doi: 10.1242/dev.113.4.1435. [DOI] [PubMed] [Google Scholar]
  45. Wedden S. E., Pang K., Eichele G. Expression pattern of homeobox-containing genes during chick embryogenesis. Development. 1989 Mar;105(3):639–650. doi: 10.1242/dev.105.3.639. [DOI] [PubMed] [Google Scholar]
  46. Wedeen C. J., Kostriken R. G., Matsumura I., Weisblat D. A. Evidence for a new family of evolutionarily conserved homeobox genes. Nucleic Acids Res. 1990 Apr 11;18(7):1908–1908. doi: 10.1093/nar/18.7.1908. [DOI] [PMC free article] [PubMed] [Google Scholar]

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