Genesis of rods in the zebrafish retina occurs in a microenvironment provided by polysialic acid-expressing Müller glia

Journal of Comparative Neurology

Volumn 518, Issue 5, 2010, Pages 636-646

  Kustermann, Stefan ^a   Hildebrandt, Herbert ^b   Bolz, Sylvia ^a   Dengler, Katja ^a   Kohler, Konrad ^a,c  

^a Centre for Ophthalmology   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c Center for Regenerative Biology and Medicine   (Germany)

Author keywords

Development; Photoreceptors; Rod precursors; Stem cells

Indexed keywords

ANTIBODY; BROXURIDINE; ENHANCED GREEN FLUORESCENT PROTEIN; POLYSIALIC ACID; RETINOID BINDING PROTEIN; RHODOPSIN; 11 CIS RETINAL BINDING PROTEIN; 11-CIS-RETINAL-BINDING PROTEIN; CARRIER PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NCAM1 PROTEIN, ZEBRAFISH; NERVE CELL ADHESION MOLECULE; SIALIC ACID DERIVATIVE; ZEBRAFISH PROTEIN;

ADULT ANIMAL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FERTILIZATION; FLUORESCENCE MICROSCOPY; GLIA; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LARVA; MUELLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA DEVELOPMENT; RETINA ROD; ZEBRA FISH; ANIMAL; CELL PROLIFERATION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE FIBER; PRENATAL DEVELOPMENT; RETINA; STEM CELL; TRANSGENIC ANIMAL; ULTRASTRUCTURE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; BROMODEOXYURIDINE; CARRIER PROTEINS; CELL PROLIFERATION; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; NEURAL CELL ADHESION MOLECULES; NEUROGLIA; RECOMBINANT FUSION PROTEINS; RETINA; RETINAL ROD PHOTORECEPTOR CELLS; RHODOPSIN; SIALIC ACIDS; STEM CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77649262073     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22232     Document Type: Article

References (51)

1. Alvarez-Buylla A, Lim DA. 2004. For the long run: maintaining germinal niches in the adult brain. Neuron 41:683-686.
2. Amoureux MC, Cunningham BA, Edelman GM, Crossin KL. 2000. N-CAM binding inhibits the proliferation of hippocampal progenitor cells and promotes their differentiation to a neuronal phenotype. J Neurosci 20:3631-3640.
3. Angata K, Huckaby V, Ranscht B, Terskikh A, Marth JD, Fukuda M. 2007. Polysialic acid-directed migration and differentiation of neural precursors are essential for mouse brain development. Mol Cell Biol 27:6659-6668.
4. Bartsch U, Kirchhoff F, Schachner M. 1990. Highly sialylated N-CAM is expressed in adult mouse optic nerve and retina. J Neurocytol 19:550-565.
5. Becker T, Becker CG, Niemann U, Naujoks-Manteuffel C, Gerardy-Schahn R, Roth G. 1993. Amphibian-specific regulation of polysialic acid and the neural cell adhesion molecule in development and regeneration of the retinotectal system of the salamander Pleurodeles waltl. J Comp Neurol 336:532-544.
6. Bernardos RL, Barthel LK, Meyers JR, Raymond PA. 2007. Latestage neuronal progenitors in the retina are radial Muller glia that function as retinal stem cells. J Neurosci 27:7028-7040.
7. Bilotta J, Saszik S. 2001. The zebrafish as a model visual system. Int J Dev Neurosci 19:621-629.
8. Bonfanti L. 2006. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 80:129-164.
9. Bonfanti L, Theodosis DT. 2009. Polysialic acid and activity-dependent synapse remodeling. Cell Adh Migr 3(1).
10. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A. 2006. Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25:397-424.
11. Bunt-Milam AH, Saari JC. 1983. Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina. J Cell Biol 97:703-712.
12. Burgess A, Wainwright SR, Shihabuddin LS, Rutishauser U, Seki T, Aubert I. 2008. Polysialic acid regulates the clustering, migration, and neuronal differentiation of progenitor cells in the adult hippocampus. Dev Neurobiol 68:1580-1590.
13. Canger AK, Rutishauser U. 2004. Alteration of neural tissue structure by expression of polysialic acid induced by viral delivery of PST polysialyltransferase. Glycobiology 14:83-93.
14. Cid E, Velasco A, Ciudad J, Orfao A, Aijon J, Lara JM. 2002. Quantitative evaluation of the distribution of proliferating cells in the adult retina in three cyprinid species. Cell Tissue Res 308:47-59.
15. Collery R, McLoughlin S, Vendrell V, Finnegan J, Crabb JW, Saari JC, Kennedy BN. 2008. Duplication and divergence of zebrafish CRALBP genes uncovers novel role for RPE-and Muller-CRALBP in cone vision. Invest Ophthalmol Vis Sci 49:3812-3820.
16. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS. 2007. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243-1249.
17. Durbec P, Cremer H. 2001. Revisiting the function of PSA-NCAM in the nervous system. Mol Neurobiol 24:53-64.
18. Fadool JM. 2003. Rod genesis in the teleost retina as a model of neural stem cells. Exp Neurol 184:14-19.
19. Fleisch VC, Schonthaler HB, von Lintig J, Neuhauss SC. 2008. Subfunctionalization of a retinoid-binding protein provides evidence for two parallel visual cycles in the cone-dominant zebrafish retina. J Neurosci 28:8208-8216.
20. Frosch M, Gorgen I, Boulnois GJ, Timmis KN, Bitter-Suermann D. 1985. NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc Natl Acad Sci U S A 82:1194-1198.
21. Gascon E, Vutskits L, Kiss JZ. 2008. The role of PSA-NCAM in adult neurogenesis. Neurochem Res [Epub ahead of print].
22. Gerardy-Schahn R, Bethe A, Brennecke T, Muhlenhoff M, Eckhardt M, Ziesing S, Lottspeich F, Frosch M. 1995. Molecular cloning and functional expression of bacteriophage PK1E-encoded endoneuraminidase Endo NE. Mol Microbiol 16:441-450.
23. Hekmat A, Bitter-Suermann D, Schachner M. 1990. Immunocytological localization of the highly polysialylated form of the neural cell adhesion molecule during development of the murine cerebellar cortex. J Comp Neurol 291:457-467.
24. Herman JP, Victor JC, Sanes JR. 1993. Developmentally regulated and spatially restricted antigens of radial glial cells. Dev Dyn 197:307-318.
25. Hildebrandt H, Muhlenhoff M, Weinhold B, Gerardy-Schahn R. 2007. Dissecting polysialic acid and NCAM functions in brain development. J Neurochem 103(Suppl 1):56-64.
26. Hitchcock P, Ochocinska M, Sieh A, Otteson D. 2004. Persistent and injury-induced neurogenesis in the vertebrate retina. Prog Retin Eye Res 23:183-194.
27. Johns PR. 1982. Formation of photoreceptors in larval and adult goldfish. J Neurosci 2:178 -198.
28. Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, Reh TA. 2008. Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci U S A 105:19508-19513.
29. Kempermann G, Jessberger S, Steiner B, Kronenberg G. 2004. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
30. Kleene R, Schachner M. 2004. Glycans and neural cell interactions. Nat Rev Neurosci 5:195-208.
31. Lee E, Chang BS, Mun GH, Chung YH, Kim J, Shin DH. 2005. An ultramicroscopic study on the distribution of Muller cell processes in the outer retinal layers of the zebrafish. Ann Anat 187:43-50.
32. Marx M, Rutishauser U, Bastmeyer M. 2001. Dual function of polysialic acid during zebrafish central nervous system development. Development 128:4949-4958.
33. Monlezun S, Ouali S, Poulain DA, Theodosis DT. 2005. Polysialic acid is required for active phases of morphological plasticity of neurosecretory axons and their glia. Mol Cell Neurosci 29:516-524.
34. Otteson DC, Hitchcock PF. 2003. Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res 43:927-936.
35. Otteson DC, D'Costa AR, Hitchcock PF. 2001. Putative stem cells and the lineage of rod photoreceptors in the mature retina of the goldfish. Dev Biol 232:62-76.
36. Peterson RE, Fadool JM, McClintock J, Linser PJ. 2001. Muller cell differentiation in the zebrafish neural retina: evidence of distinct early and late stages in cell maturation. J Comp Neurol 429:530-540.
37. Petridis AK, El Maarouf A, Rutishauser U. 2004. Polysialic acid regulates cell contact-dependent neuronal differentiation of progenitor cells from the subventricular zone. Dev Dyn 230: 675-684.
38. Pinto L, Götz M. 2007. Radial glial cell heterogeneity - the source of diverse progeny in the CNS. Prog Neurobiol 83:2-23.
39. Rieger S, Volkmann K, Köster RW. 2008. Polysialyltransferase expression is linked to neuronal migration in the developing and adult zebrafish. Dev Dyn 237:276-285.
40. Röckle I, Seidenfaden R, Weinhold B, Muhlenhoff M, Gerardy-Schahn R, Hildebrandt H. 2008. Polysialic acid controls NCAM-induced differentiation of neuronal precursors into calretinin-positive olfactory bulb interneurons. Dev Neurobiol 68:1170-1184.
41. Rutishauser U. 2008. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 9:26 -35.
42. Sawaguchi A, Idate Y, Ide S, Kawano J, Nagaike R, Oinuma T, Suganuma T. 1999. Multistratified expression of polysialic acid and its relationship to VAChT-containing neurons in the inner plexiform layer of adult rat retina. J Histochem Cytochem 47:919-928.
43. Schlosshauer B, Schwarz U, Rutishauser U. 1984. Topological distribution of different forms of neural cell adhesion molecule in the developing chick visual system. Nature 310:141-143.
44. Schmitt EA, Dowling JE. 1999. Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J Comp Neurol 404:515-536.
45. Seidenfaden R, Krauter A, Schertzinger F, Gerardy-Schahn R, Hildebrandt H. 2003. Polysialic acid directs tumor cell growth by controlling heterophilic neural cell adhesion molecule interactions. Mol Cell Biol 23:5908-5918.
46. Seki T. 2002. Hippocampal adult neurogenesis occurs in a microenvironment provided by PSA-NCAM-expressing immature neurons. J Neurosci Res 69:772-783.
47. Seki T, Namba T, Mochizuki H, Onodera M. 2007. Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 502:275-290.
48. Stummeyer K, Dickmanns A, Muhlenhoff M, Gerardy-Schahn R, Ficner R. 2005. Crystal structure of the polysialic aciddegrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 12:90 -96.
49. Thummel R, Kassen SC, Montgomery JE, Enright JM, Hyde DR. 2008. Inhibition of Muller glial cell division blocks regeneration of the light-damaged zebrafish retina. Dev Neurobiol 68:392-408.
50. Weinhold B, Seidenfaden R, Rockle I, Muhlenhoff M, Schertzinger F, Conzelmann S, Marth JD, Gerardy-Schahn R, Hildebrandt H. 2005. Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem 280:42971-42977.
51. Yazulla S, Studholme KM. 2001. Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry. J Neurocytol 30:551-592.