Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T12:48:05.654Z Has data issue: false hasContentIssue false

Localization and expression of insulin-like growth factor in the teleost retina

Published online by Cambridge University Press:  02 June 2009

Andreas F. Mack
Affiliation:
Neuroscience Program, Jordan Hall, Stanford University, Stanford
Steven L. Balt
Affiliation:
Neuroscience Program, Jordan Hall, Stanford University, Stanford
Russell D. Fernald
Affiliation:
Neuroscience Program, Jordan Hall, Stanford University, Stanford

Abstract

Teleost fish retinas continue to add neurons throughout life, and evidence from in vitro experiments have implicated insulin-like growth factors (IGFs) in this process. To discover whether these factors are expressed in vivo, we have examined their expression in the cichlid fish, Haplochromis burtoni. Three lines of evidence show that IGFs are present in the fish retina. An IGF-I specific antibody, sm 1.2, binds preferentially to the retinal outer plexiform layer, in areas of cone photoreceptor synaptic endings. Northern blots of mRNA hybridized with riboprobes from trout IGF-I and IGF-II genes revealed transcripts of ~6.5 and 4.9 kb, respectively. The IGF-I probe detected an additional transcript of 1.2 kb in liver but not in retinal mRNA. In situ hybridization with digoxigenin-labeled riboprobes revealed that the IGF gene product is localized in the cone photoreceptors. These results show that cone photoreceptors are the source of IGFs in the fish retina, consistent with the hypothesis that IGFs play a role in regulating production of new neurons in the teleost retina.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bach, M.A., Shenorr, Z., Lowe, W.L., Roberts, C.T. & Leroith, D. (1991). Insulin-like growth factor-I messenger RNA levels are developmentally regulated in specific regions of the rat brain. Molecular Brain Research 10, 4348.CrossRefGoogle ScholarPubMed
Bartlett, W.P., Li, X.S., Williams, M. & Benkovic, S. (1991). Localization of insulin-like growth factor-I mRNA in murine central nervous system during postnatal development. Developmental Biology 147, 239250.CrossRefGoogle ScholarPubMed
Bichell, D.P., Kikuchi, K. & Rotwein, P. (1992). Growth hormone rapidly activates insulin-like growth factor-i gene transcription in vivo. Molecular Endocrinology 6, 18991908.Google ScholarPubMed
Bondy, C.A. (1991). Transient IGF-I gene expression during the maturation of functionally related central projection neurons. Journal of Neuroscience 11, 34423455.CrossRefGoogle ScholarPubMed
Bondy, C.A. & Lee, W.H. (1993). Patterns of insulin-like growth factor and IGF receptor gene expression in the brain-functional implications. In Role of Insulin-Like Growth Factors in the Nervous System, ed. Raizada, M.K. & Leroith, D., Annals of the New York Academy of Sciences 692, pp. 3343. New York: New York Academy of Sciences.Google Scholar
Cao, Q.P., DuGuay, S., Plisetskaya, E. & SteinerD.F., C.S.J. D.F., C.S.J. (1989). Nucleotide sequence and growth-hormone-regulated expression of salmon insulin-like growth factor-I mRNA. Molecular Endocrinology 3, 20052010.CrossRefGoogle ScholarPubMed
Chan, S.J., Cao, Q.P. & Steiner, D.F. (1990). Evolution of the insulin superfamily-cloning of a hybrid insulin insulin-like growth factor cDNA from Amphioxus. Proceedings of the National Academy of Sciences of the U.S.A. 87, 93199323.CrossRefGoogle ScholarPubMed
Cohick, W.S. & Clemmons, D.R. (1993). The insulin-like growth factors. Annual Review of Physiology 55, 131153.CrossRefGoogle ScholarPubMed
D'Ercole, A.J., Stiles, A.D. & Underwood, L.E. (1984). Tissue concentrations of somatomedin C: Further evidence for multiple sites of synthesis and paracrine or autocrine mechanisms. Proceedings of the National Academy of Sciences of the U.S.A. 81, 684691.CrossRefGoogle ScholarPubMed
DiCicco-Bloom, E. & Black, I.E. (1988). Insulin growth factors regulate the mitotic cycle in cultured rat sympathetic neuroblasts. Proceedings of the National Academy of Sciences of the U.S.A. 85, 40664070.CrossRefGoogle ScholarPubMed
Drakenberg, K., Sara, V.R., Linahl, K.I. & Kewish, B. (1989). The study of insulin-like growth factors in Tilapia, Oreochromis mossambicus. General and Comparative Endocrinology 4, 173180.CrossRefGoogle Scholar
Duguay, S.J., Swanson, P. & Dickhoff, W.W. (1994). Differential expression and hormonal regulation of alternatively spliced IGF-I mRNA transcripts in salmon. Journal of Molecular Endocrinology 12, 2537.CrossRefGoogle ScholarPubMed
Fernald, R. (1989). Retinal rod neurogenesis. In Development of the Vertebrate Retina, ed. Finlay, B.L. & Sengelaub, D.R., pp. 3142. New York, London: Plenum Press.CrossRefGoogle Scholar
Fernald, R.D. & Hirata, N.R. (1977). Field study of Haplochromis burtoni: Habitats and co-habitats. Environmental Biology of Fishes 2, 299308.CrossRefGoogle Scholar
Funkenstein, B., Silbergeld, A., Cavari, B. & Laron, Z. (1989). Growth hormone increases plasma levels of insulin-like growth factor (IGF-I) in a teleost, the gilthead seabream (Sparus aurata). Journal of Endocrinology 120, R19–R21.CrossRefGoogle Scholar
Furlanetto, R.W., Harwell, S.E. & Prick, K.K. (1994). Insulin-like growth factor-I induces cyclin-D1 expression in Mg63 human osteo-sarcoma cells in vitro. Molecular Endocrinology 8, 510517.Google Scholar
Henken, D.B. & Yoon, M.G. (1989). Optic nerve crush modulates proliferation of rod precursor cells in goldfish retina. Brain Research 501, 247259.CrossRefGoogle ScholarPubMed
Korenbrot, J.I. & Fernald, R.D. (1989). Orcadian rhythm and light regulate opsin mRNA in rod photoreceptors. Nature 337, 454457.CrossRefGoogle Scholar
Leroith, D. & Roberts, C.T. (1993). Insulin-like growth factors. In Role of Insulin-Like Growth Factors in the Nervous Systems, ed. Raizada, M. K. & Leroith, D., A nnals of the New York A cademy of Sciences 692, pp. 19. New York: New York Academy of Sciences.Google Scholar
Lillien, L. & Cepko, C. (1992). Control of proliferation in the retina: Temporal changes in responsiveness to FGF and TGFα. Development 115, 253266.CrossRefGoogle Scholar
Lindhal, K.I., Sara, V.R., Fridberg, G. & Nishimiya, T. (1985). The presence of somatomedin in the Baltic salmon, Salmo salar, with special reference to smoltification. Aquaculture 45, 177183.CrossRefGoogle Scholar
Lu, K.H. & Campisi, J. (1992). Ras proteins are essential and selective for the action of insulin-like growth factor-I late in the G1-phase of the cell cycle in balb/c murine fibroblasts. Proceedings of the National Academy of Sciences of the U.S.A. 89, 38893893.CrossRefGoogle ScholarPubMed
Lund, P.K., Moats-Staats, B.M., Hynes, M.A., Simmons, J.G., Jan-sen, M., D'Ercole, A.J. & Van Wyk, J.J. (1986). Somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II mRNAs in rat fetal and adult tissues. Journal of Biological Chemistry 261, 1453914545.CrossRefGoogle ScholarPubMed
Mack, A.F. (1992). Cell proliferation and differentiation in the retina of the African cichlid fish Haplochromis burtoni in slice culture and in vivo. Ph.D. Thesis, University of Oregon, Eugene, OR.Google Scholar
Mack, A.F. & Fernald, R.D. (1993). Regulation of cell division and rod differentiation in the teleost retina. Developmental Brain Research 16, 183187.CrossRefGoogle Scholar
Müller, H. (1952). Bau und Wachstum der Netzhaut des Guppy (Lebistes reticulatus). Zoologische Jahrbücher 63, 275324.Google Scholar
Negishi, K., Teranishi, T. & Kato, S. (1982). New dopaminergic and indoleamine-accumulating cells in the growth zone of goldfish retinas after neurotoxic destruction. Science 216, 747749.CrossRefGoogle ScholarPubMed
Ohno, S. (1970). Evolution by Gene Duplication, p. 130. New York: Springer Verlag.CrossRefGoogle Scholar
Pons, S., Rejas, M.T. & Torresaleman, I. (1991). Ontogeny of insulin-like growth factor-I, its receptor, and its binding proteins in the rat hypothalamus. Developmental Brain Research 62, 169175.CrossRefGoogle ScholarPubMed
Reh, T. & Kljavin, I.J. (1989). Age of differentiation determines rat retinal germinal cell phenotype: Induction of differentiation by dissociation. Journal of Neuroscience 9, 41794189.CrossRefGoogle ScholarPubMed
Reinecke, M., Betzler, D., Drakenberg, K., Falkmer, S. & Sara, V.R. (1993 a). Occurrence of members of the insulin superfamily in central nervous system and digestive tract of protochordates. Histochemistry 99, 277285.CrossRefGoogle ScholarPubMed
Reinecke, M., Maake, C., Falkmer, S. & Sara, V.R. (1993 b). The branching of insulin-like growth factor-I and insulin — an immunohistochemical analysis during phylogeny. Regulatory Peptides 48, 6576.CrossRefGoogle ScholarPubMed
Shamblott, M.J. & Chen, T.T. (1992). Identification of a 2nd insulin-like growth factor in a fish species. Proceedings of the National Academy of Sciences of the U.S.A. 89, 89138917.CrossRefGoogle Scholar
Turner, D., Snyder, E.Y. & Cepko, C.L. (1990). Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4, 833845.CrossRefGoogle ScholarPubMed
Waldbillig, R.J., Arnold, D.R., Fletcher, R.T. & Chader, G.J. (1991 b). Insulin and IGF-I binding in developing chick neural retina and pigment epithelium — a characterization of binding and structural differences. Experimental Eye Research 53, 1322.CrossRefGoogle ScholarPubMed
Waldbillig, R.J., Pfeffer, B.A., Schoen, T.J., Adler, A.A., Shenorr, Z., Scavo, L., Leroith, D. & Chader, G.J. (1991 b). Evidence for an insulin-like growth factor autocrine-paracrine system in the retinal photoreceptor-pigment epithelial cell complex. Journal of Neurochemistry 57, 15221533.CrossRefGoogle ScholarPubMed
Werner, H., Woloschek, M., Adamo, M., Shen-Orr, Z., Roberts, C.T. & Leroith, D. (1989). Developmental regulation of the rat IGF-I receptor gene. Proceedings of the National Academy of Sciences of the U.S.A. 86, 74517455.CrossRefGoogle Scholar