The zebrafish galectin drgal1-L2 is expressed by proliferating müller glia and photoreceptor progenitors and regulates the regeneration of rod photoreceptors

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 6, 2010, Pages 3244-3252

  Craig, Sonya E L ^a   Thummel, Ryan ^b   Ahmed, Hafiz ^c   Vasta, Gerardo R ^c   Hyde, David R ^d   Hitchcock, Peter F ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDE; BETA GALACTOSIDE BINDING PROTEIN GALECTIN 1 LIKE 2; GALECTIN 1; MESSENGER RNA; UNCLASSIFIED DRUG; GAL1 L2 PROTEIN, ZEBRAFISH; GAL1-L2 PROTEIN, ZEBRAFISH; GALECTIN; MORPHOLINE DERIVATIVE; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CELL REGENERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GLIA; GLIA CELL; IMMUNOCYTOCHEMISTRY; MICROGLIA; MUELLER CELL; MUELLERIAN DUCT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RETINA CONE; RETINA ROD; ZEBRA FISH; ANIMAL; CELL COUNT; CELL DEATH; ELECTROPORATION; GENETICS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; LIGHT; METABOLISM; PATHOLOGY; PHOTORECEPTOR CELL; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION INJURY; REGENERATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

ANIMALS; CELL COUNT; CELL DEATH; CELL PROLIFERATION; ELECTROPORATION; GALECTINS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; LIGHT; MICROGLIA; MORPHOLINES; PHOTORECEPTOR CELLS, VERTEBRATE; RADIATION INJURIES, EXPERIMENTAL; REGENERATION; RETINAL ROD PHOTORECEPTOR CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77953282863     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4879     Document Type: Article

References (44)

1. Hitchcock PF, Lindsey Myhr KJ, Easter SS, Mangione-Smith R, Jones DD. Local regeneration in the retina of the goldfish. J Neu-robiol. 1992;23:187-203.
2. Raymond PA, Reifler MJ, Rivlin PK. Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. J Neurobiol. 1988;19:431-463.
3. Vihtelic TS, Hyde DR. Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J Neurobiol. 2000;44:289-307.
4. 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;42:2115-2124.
5. Fausett BV, Goldman D. A role for alpha1 tubulin-expressing Mul-ler glia in regeneration of the injured zebrafish retina. J Neurosci 2006;26:6303-6313
6. Bernardos RL, Barthel LK, Meyers JR, Raymond PA. Late-stage neuronal progenitors in the retina are radial Muller glia that function as retinal stem cells. JNeurosci. 2007;27:7028-7040.
7. Thummel R, Kassen SC, Montgomery JE, Enright JM, Hyde DR. Inhibition of Muller glial cell division blocks regeneration of the light-damaged zebrafish retina. Dev Neurobiol. 2008;68:392-408.
8. Hitchcock PF. Tracer coupling among regenerated amacrine cells in the retina of the goldfish. Vis Neurosci. 1997;14:463-472.
9. Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ. Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev Biol. 2006;6:36.
10. Kassen SC, Ramanan V, Montgomery JE, et al. Time course analysis of gene expression during light-induced photoreceptor cell death and regeneration in albino zebrafish. Dev Neurobiol. 2007;67: 1009-1031.
11. Fausett BV, Gumerson JD, Goldman D. The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. J Neurosci. 2008;28:1109-1117.
12. Qin Z, Barthel LK, Raymond PA. Genetic evidence for shared mechanisms of epimorphic regeneration in zebrafish. Proc Natl Acad Sci USA. 2009;106:9310-9315
13. Kassen SC, Thummel R, Campochiaro LA, Harding MJ, Bennett NA, Hyde DR. CNTF induces photoreceptor neuroprotection and Muller glial cell proliferation through two different signaling pathways in the adult zebrafish retina. Exp Eye Res. 2009;88:1051-1064.
14. Calinescu AA, Vihtelic TS, Hyde DR, Hitchcock PF. Cellular expression of midkine-a and midkine-b during retinal development and photoreceptor regeneration in zebrafish. J Comp Neurol. 2009;514:1-10.
15. Rattner A, Nathans J. The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia. JNeurosci. 2005;25:4540-4549.
16. Craig SEL, Calinescu A-A, Hitchcock PF. Identification of the molecular signatures integral to regenerating photoreceptors in the retina of the zebrafish. J Ocul Biol Dis Informatics. 2008;1:73-83.
17. Moiseeva EP, Javed Q, Spring EL, de Bono DP. Galectin 1 is involved in vascular smooth muscle cell proliferation. Cardiovasc Res. 2000;45:493-502.
18. Moiseeva EP, Williams B, Samani NJ. Galectin 1 inhibits incorporation of vitronectin and chondroitin sulfate B into the extracellular matrix of human vascular smooth muscle cells. Biochim Bio-phys Acta. 2003;1619:125-132.
19. Moiseeva EP, Williams B, Goodall AH, Samani NJ. Galectin-1 interacts with /3-1 subunit of integrin. Biochem Biophys Res Commun. 2003;310:1010-1016.
20. Camby I, le Mercier M, Lefranc F, Kiss R. Galectin-1: a small protein with major functions. Glycobiology. 2006;16:137R-157R
21. Rabinovich GA, Toscano MA, Jackson SS, Vasta GR. Functions of cell surface galectin-glycoprotein lattices. Curr Opin Struct Biol. 2007;17:513-520.
22. Sakaguchi M, Shingo T, Shimazaki T, et al. A carbohydrate-binding protein, Galectin-1, promotes proliferation of adult neural stem cells. Proc Natl Acad Sci USA. 2006;103:7112-7117.
23. Horie H, Kadoya T. Galectin-1 plays essential roles in adult mammalian nervous tissues: roles of oxidized galectin-1. Glycoconj J. 2004;19:479-89.
24. Plachta N, Annaheim C, Bissiere S, et al. Identification of a lectin causing the degeneration of neuronal processes using engineered embryonic stem cells. Nat Neurosci. 2007;10:712-719
25. Akama K, Tatsuno R, Otsu M, et al. Proteomic identification of differentially expressed genes in mouse neural stem cells and neurons differentiated from embryonic stem cells in vitro. Biochim Biophys Acta. 2008;1784:773-782.
26. Ishibashi S, Kuroiwa T, Sakaguchi M, et al. Galectin-1 regulates neurogenesis in the subventricular zone and promotes functional recovery after stroke. Exp Neurol. 2007;207:302-313
27. Ahmed H, Du SJ, O'Leary N, Vasta GR. Biochemical and molecular characterization of galectins from zebrafish (Danio rerio): noto-chord-specific expression of a prototype galectin during early embryogenesis. Glycobiology. 2004;14:219-232.
28. Vasta GR, Ahmed H, Du S, Henrikson D. Galectins in teleost fish: zebrafish (Danio rerio) as a model species to address their biological roles in development and innate immunity. Glycoconj J. 2004; 21:503-521.
29. Ahmed H, Du SJ, Vasta GR. Knockdown of a galectin-1-like protein in zebrafish (Danio rerio) causes defects in skeletal muscle development. Glycoconj J. 2009;26:277-283.
30. Bernardos RL, Raymond PA. GFAP transgenic zebrafish. Gene Expr Patterns. 2006;6:1007-1013
31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-AAC(T)) method. Methods. 2001;25:402-408.
32. 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;477:108-117.
33. Elola MT, Wolfenstein-Todel C, Vasta GR, Rabinovich GA. Galectins: matricellular glycan-binding proteins linking cell adhesion, migration, and survival. Cell Mol Life Sci. 2007;64:1679-1700.
34. Fischer AJ, Reh TA. Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci. 2001; 4:247-252.
35. Ooto S, Akagi T, Kageyama R, et al. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci USA. 2004;101:13654-13659
36. 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;27:4210-4219.
37. Morris AC, Scholz TL, Brockerhoff SE, Fadool JM. Genetic dissection reveals two separate pathways for rod and cone regeneration in the teleost retina. Dev Neurobiol. 2008;68:605-619
38. Hitchcock PF, Raymond PA. The zebrafish retina as a model for developmental and regeneration biology. Zebrafish. 2004;1:257-271.
39. Puche AC, Poirier F, Hair M, Bartlett PF, Key B. Role of galectin-1 in the developing mouse olfactory system. Dev Biol. 1996;179: 274-287.
40. Fischer C, Sanchez-Ruderisch H, Welzel M, et al. Galectin-1 interacts with the α5βfibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J Biol Chem. 2005;280: 37266-37277.
41. Dyer MA, Cepko CL. p27Kip1 and p57Kip2 regulate proliferation in distinct retinal progenitor cell populations. J Neurosci. 2001; 21:4259-4271.
42. Belvindrah R, Graus-Porta D, Goebbels S, Nave KA, Muller U. Beta1 integrins in radial glia but not in migrating neurons are essential for the formation of cell layers in the cerebral cortex. J Neurosci. 2007;27:13854-13865.
43. Biehlmaier O, Makhankov Y, Neuhauss SC. Impaired retinal differentiation and maintenance in zebrafish laminin mutants. Invest Ophthalmol Vis Sci. 2007;48:2887-2894.
44. Doetsch F. A niche for adult neural stem cells. Curr Opin Genet Dev. 2003;13:543-550.