Skip to main content
Top
Published in: Journal of Ocular Biology, Diseases, and Informatics 2-4/2008

Open Access 01-12-2008

Identification of the molecular signatures integral to regenerating photoreceptors in the retina of the zebra fish

Authors: Sonya E. L. Craig, Anda-Alexandra Calinescu, Peter F. Hitchcock

Published in: Journal of Ocular Biology, Diseases, and Informatics | Issue 2-4/2008

Login to get access

Abstract

Investigating neuronal and photoreceptor regeneration in the retina of zebra fish has begun to yield insights into both the cellular and molecular means by which this lower vertebrate is able to repair its central nervous system. However, knowledge about the signaling molecules in the local microenvironment of a retinal injury and the transcriptional events they activate during neuronal death and regeneration is still lacking. To identify genes involved in photoreceptor regeneration, we combined light-induced photoreceptor lesions, laser-capture microdissection of the outer nuclear layer (ONL) and analysis of gene expression to characterize transcriptional changes for cells in the ONL as photoreceptors die and are regenerated. Using this approach, we were able to characterize aspects of the molecular signature of injured and dying photoreceptors, cone photoreceptor progenitors, and microglia within the ONL. We validated changes in gene expression and characterized the cellular expression for three novel, extracellular signaling molecules that we hypothesize are involved in regulating regenerative events in the retina.
Appendix
Available only for authorised users
Literature
2.
3.
go back to reference Bernardos RL, Barthel LK, Meyers JR, Raymond PA. Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci 2007;27:7028–40.PubMedCrossRef Bernardos RL, Barthel LK, Meyers JR, Raymond PA. Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci 2007;27:7028–40.PubMedCrossRef
4.
go back to reference Cadieux B, Chitramuthu BP, Baranowski D, Bennett HP. The zebra fish progranulin gene family and antisense transcripts. BMC Genomics 2005;6:156.PubMedCrossRef Cadieux B, Chitramuthu BP, Baranowski D, Bennett HP. The zebra fish progranulin gene family and antisense transcripts. BMC Genomics 2005;6:156.PubMedCrossRef
5.
go back to reference Camby I, Le Mercier M, Lefranc F, Kiss R. Galectin-1: a small protein with major functions. Glycobiology 2006;16:137R–157R.PubMedCrossRef Camby I, Le Mercier M, Lefranc F, Kiss R. Galectin-1: a small protein with major functions. Glycobiology 2006;16:137R–157R.PubMedCrossRef
6.
go back to reference Cameron DA, Gentile KL, Middleton FA, Yurco P. Gene expression profiles of intact and regenerating zebra fish retina. Mol Vis 2005;11:775–91.PubMed Cameron DA, Gentile KL, Middleton FA, Yurco P. Gene expression profiles of intact and regenerating zebra fish retina. Mol Vis 2005;11:775–91.PubMed
7.
go back to reference Chen L, Wu W, Dentchev T, Zeng Y, Wang J, Tsui I, Tobias JW, Bennett J, Baldwin D, Dunaief JL. Light damage induced changes in mouse retinal gene expression. Exp Eye Res 2004;79:239–47.PubMedCrossRef Chen L, Wu W, Dentchev T, Zeng Y, Wang J, Tsui I, Tobias JW, Bennett J, Baldwin D, Dunaief JL. Light damage induced changes in mouse retinal gene expression. Exp Eye Res 2004;79:239–47.PubMedCrossRef
8.
go back to reference Eustace BK, Sakurai T, Stewart JK, Yimlamai D, Unger C, Zehetmeier C, Lain B, Torella C, Henning SW, Beste G, Scroggins BT, Neckers L, Ilag LL, Jay DG. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat Cell Biol 2004;6:507–14.PubMedCrossRef Eustace BK, Sakurai T, Stewart JK, Yimlamai D, Unger C, Zehetmeier C, Lain B, Torella C, Henning SW, Beste G, Scroggins BT, Neckers L, Ilag LL, Jay DG. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat Cell Biol 2004;6:507–14.PubMedCrossRef
9.
go back to reference Fausett BV, Goldman D. A role for alpha1 tubulin-expressing Müller glia in regeneration of the injured zebra fish retina. J Neurosci 2006;26:6303–13.PubMedCrossRef Fausett BV, Goldman D. A role for alpha1 tubulin-expressing Müller glia in regeneration of the injured zebra fish retina. J Neurosci 2006;26:6303–13.PubMedCrossRef
10.
go back to reference Fausett BV, Gumerson JD, Goldman D. The proneural basic helix–loop–helix gene ascl1a is required for retina regeneration. J Neurosci 2008;28:1109–17.PubMedCrossRef Fausett BV, Gumerson JD, Goldman D. The proneural basic helix–loop–helix gene ascl1a is required for retina regeneration. J Neurosci 2008;28:1109–17.PubMedCrossRef
11.
go back to reference Fimbel SM, Montgomery JE, Burket CT, Hyde DR. Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebra fish. J Neurosci 2007;27:1712–24.PubMedCrossRef Fimbel SM, Montgomery JE, Burket CT, Hyde DR. Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebra fish. J Neurosci 2007;27:1712–24.PubMedCrossRef
12.
go back to reference Fischer AJ, Reh TA. Müller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci 2001;4:247–52.PubMedCrossRef Fischer AJ, Reh TA. Müller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci 2001;4:247–52.PubMedCrossRef
13.
go back to reference Green CB, Besharse JC. Retinal circadian clocks and control of retinal physiology. J Biol Rhythms 2004;19:91–102.PubMedCrossRef Green CB, Besharse JC. Retinal circadian clocks and control of retinal physiology. J Biol Rhythms 2004;19:91–102.PubMedCrossRef
14.
go back to reference Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007;10:1387–94.PubMedCrossRef Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007;10:1387–94.PubMedCrossRef
15.
go back to reference He Z, Ong CH, Halper J, Bateman A. Progranulin is a mediator of the wound response. Nat. Med. 2003;9:225–9.PubMedCrossRef He Z, Ong CH, Halper J, Bateman A. Progranulin is a mediator of the wound response. Nat. Med. 2003;9:225–9.PubMedCrossRef
16.
go back to reference Herbomel P, Thisse B, Thisse C. Zebra fish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev Biol 2001;238:274–88.PubMedCrossRef Herbomel P, Thisse B, Thisse C. Zebra fish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev Biol 2001;238:274–88.PubMedCrossRef
17.
go back to reference Hero AO, Fleury G, Mears AJ, Swaroop A. Multicriteria gene screening for analysis of differential expression with DNA microarrays. EURASIP JASP 2004;2004:43–52. Hero AO, Fleury G, Mears AJ, Swaroop A. Multicriteria gene screening for analysis of differential expression with DNA microarrays. EURASIP JASP 2004;2004:43–52.
18.
go back to reference Hitchcock PF. Tracer coupling among regenerated amacrine cells in the retina of the goldfish. Vis Neurosci 1997;14:463–72.PubMedCrossRef Hitchcock PF. Tracer coupling among regenerated amacrine cells in the retina of the goldfish. Vis Neurosci 1997;14:463–72.PubMedCrossRef
19.
go back to reference Hitchcock P, Kakuk-Atkins L. The basic helix-loop-helix transcription factor neuroD is expressed in the rod lineage of the teleost retina. J Comp Neurol 2004;477:108–17.PubMedCrossRef Hitchcock P, Kakuk-Atkins L. The basic helix-loop-helix transcription factor neuroD is expressed in the rod lineage of the teleost retina. J Comp Neurol 2004;477:108–17.PubMedCrossRef
20.
go back to reference Hitchcock PF, Lindsey Myhr KJ, Easter SS Jr, Mangione-Smith R, Jones DD. Local regeneration in the retina of the goldfish. J Neurobiol 1992;23:187–203.PubMedCrossRef Hitchcock PF, Lindsey Myhr KJ, Easter SS Jr, Mangione-Smith R, Jones DD. Local regeneration in the retina of the goldfish. J Neurobiol 1992;23:187–203.PubMedCrossRef
21.
go back to reference Kassen SC, Ramanan V, Montgomery JE, Burket CT, Liu CG, Vihtelic TS, Hyde DR. Time course analysis of gene expression during light-induced photoreceptor cell death and regeneration in albino zebra fish. Dev Neurobiol 2007;67:1009–31.PubMedCrossRef Kassen SC, Ramanan V, Montgomery JE, Burket CT, Liu CG, Vihtelic TS, Hyde DR. Time course analysis of gene expression during light-induced photoreceptor cell death and regeneration in albino zebra fish. Dev Neurobiol 2007;67:1009–31.PubMedCrossRef
22.
go back to reference Lien CL, Schebesta M, Makino S, Weber GJ, Keating MT. Gene expression analysis of zebra fish heart regeneration. PLoS Biol 2006;4:e260.PubMedCrossRef Lien CL, Schebesta M, Makino S, Weber GJ, Keating MT. Gene expression analysis of zebra fish heart regeneration. PLoS Biol 2006;4:e260.PubMedCrossRef
23.
go back to reference Mader MM, Cameron DA. Photoreceptor differentiation during retinal development, growth, and regeneration in a metamorphic vertebrate. J Neurosci 2004;24:11463–72.PubMedCrossRef Mader MM, Cameron DA. Photoreceptor differentiation during retinal development, growth, and regeneration in a metamorphic vertebrate. J Neurosci 2004;24:11463–72.PubMedCrossRef
24.
go back to reference Mallat M, Marín-Teva JL, Chéret C. Phagocytosis in the developing CNS: more than clearing the corpses. Curr Opin Neurobiol 2005;15:101–7.PubMedCrossRef Mallat M, Marín-Teva JL, Chéret C. Phagocytosis in the developing CNS: more than clearing the corpses. Curr Opin Neurobiol 2005;15:101–7.PubMedCrossRef
25.
go back to reference Ooto S, Akagi T, Kageyama R, Akita J, Mandai M, Honda Y, Takahashi M. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci U S A 2004;101:13654–9.PubMedCrossRef Ooto S, Akagi T, Kageyama R, Akita J, Mandai M, Honda Y, Takahashi M. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci U S A 2004;101:13654–9.PubMedCrossRef
26.
go back to reference Osakada F, Ooto S, Akagi T, Mandai M, Akaike A, Takahashi M. Wnt signaling promotes regeneration in the retina of adult mammals. J Neurosci 2007;27:4210–9.PubMedCrossRef Osakada F, Ooto S, Akagi T, Mandai M, Akaike A, Takahashi M. Wnt signaling promotes regeneration in the retina of adult mammals. J Neurosci 2007;27:4210–9.PubMedCrossRef
27.
go back to reference Rabinovich GA, Toscano MA, Jackson SS, Vasta GR. Functions of cell surface galectin–glycoprotein lattices. Curr. Opin. Struct. Biol 2007;17:513–20.PubMedCrossRef Rabinovich GA, Toscano MA, Jackson SS, Vasta GR. Functions of cell surface galectin–glycoprotein lattices. Curr. Opin. Struct. Biol 2007;17:513–20.PubMedCrossRef
28.
go back to reference Rattner A, Nathans J. The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia. J Neurosci 2005;25:4540–9.PubMedCrossRef Rattner A, Nathans J. The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia. J Neurosci 2005;25:4540–9.PubMedCrossRef
29.
go back to reference Raymond PA. Retinal regeneration in teleost fish. Ciba Found Symp 1991;160:171–86.PubMed Raymond PA. Retinal regeneration in teleost fish. Ciba Found Symp 1991;160:171–86.PubMed
30.
go back to reference Raymond PA, Reifler MJ, Rivlin PK. Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. J Neurobiol 1988;19:431–63.PubMedCrossRef Raymond PA, Reifler MJ, Rivlin PK. Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. J Neurobiol 1988;19:431–63.PubMedCrossRef
31.
go back to reference Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ. Molecular characterization of retinal stem cells and their niches in adult zebra fish. BMC Dev Biol 2006;6:36.PubMedCrossRef Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ. Molecular characterization of retinal stem cells and their niches in adult zebra fish. BMC Dev Biol 2006;6:36.PubMedCrossRef
32.
go back to reference Schebesta M, Lien CL, Engel FB, Keating MT. Transcriptional profiling of caudal fin regeneration in zebra fish. Scientific World Journal 2006;6(Suppl 1):38–54.PubMed Schebesta M, Lien CL, Engel FB, Keating MT. Transcriptional profiling of caudal fin regeneration in zebra fish. Scientific World Journal 2006;6(Suppl 1):38–54.PubMed
33.
go back to reference Thummel R, Kassen SC, Montgomery JE, Enright JM, Hyde DR. Inhibition of Müller glial cell division blocks regeneration of the light-damaged zebra fish retina. Dev Neurobiol 2008;68:392–408.PubMedCrossRef Thummel R, Kassen SC, Montgomery JE, Enright JM, Hyde DR. Inhibition of Müller glial cell division blocks regeneration of the light-damaged zebra fish retina. Dev Neurobiol 2008;68:392–408.PubMedCrossRef
34.
go back to reference Veldman MB, Bemben MA, Thompson RC, Goldman D. Gene expression analysis of zebra fish retinal ganglion cells during optic nerve regeneration identifies KLF6a and KLF7a as important regulators of axon regeneration. Dev Biol 2007;312:596–612.PubMedCrossRef Veldman MB, Bemben MA, Thompson RC, Goldman D. Gene expression analysis of zebra fish retinal ganglion cells during optic nerve regeneration identifies KLF6a and KLF7a as important regulators of axon regeneration. Dev Biol 2007;312:596–612.PubMedCrossRef
35.
go back to reference Vihtelic TS, Hyde DR. Light-induced rod and cone cell death and regeneration in the adult albino zebra fish (Danio rerio) retina. J Neurobiol 2000;44:289–307.PubMedCrossRef Vihtelic TS, Hyde DR. Light-induced rod and cone cell death and regeneration in the adult albino zebra fish (Danio rerio) retina. J Neurobiol 2000;44:289–307.PubMedCrossRef
36.
go back to reference Vihtelic TS, Soverly JE, Kassen SC, Hyde DR. Retinal regional differences in photoreceptor cell death and regeneration in light-lesioned albino zebra fish. Exp Eye Res 2006;82:558–75.PubMedCrossRef Vihtelic TS, Soverly JE, Kassen SC, Hyde DR. Retinal regional differences in photoreceptor cell death and regeneration in light-lesioned albino zebra fish. Exp Eye Res 2006;82:558–75.PubMedCrossRef
37.
go back to reference Wagner EC, Raymond PA. Müller glial cells of the goldfish retina are phagocytic in vitro but not in vivo. Exp Eye Res 1991;53:583–9.PubMedCrossRef Wagner EC, Raymond PA. Müller glial cells of the goldfish retina are phagocytic in vitro but not in vivo. Exp Eye Res 1991;53:583–9.PubMedCrossRef
38.
go back to reference Wu DM, Schneiderman T, Burgett J, Gokhale P, Barthel L, Raymond PA. Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Invest Ophthalmol Vis Sci 2001;42:2115–24.PubMed Wu DM, Schneiderman T, Burgett J, Gokhale P, Barthel L, Raymond PA. Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Invest Ophthalmol Vis Sci 2001;42:2115–24.PubMed
Metadata
Title
Identification of the molecular signatures integral to regenerating photoreceptors in the retina of the zebra fish
Authors
Sonya E. L. Craig
Anda-Alexandra Calinescu
Peter F. Hitchcock
Publication date
01-12-2008
Publisher
Humana Press Inc
DOI
https://doi.org/10.1007/s12177-008-9011-5

Other articles of this Issue 2-4/2008

Journal of Ocular Biology, Diseases, and Informatics 2-4/2008 Go to the issue