Subcellular concentration of β-dystroglycan in photoreceptors and glial cells of the chick retina

Journal of Comparative Neurology

Volumn 389, Issue 4, 1997, Pages 668-678

  Blank, Martina ^a   Koulen, Peter ^a   Kröger, Stephan ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

Agrin; Calcium channel; Dystrophin glycoprotein complex; Inner limiting membrane; Muller glial cells; Outer plexiform layer

Indexed keywords

CALCIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHICKEN; GLIA CELL; MUELLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; RETINA CELL;

AGRIN; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; CHICK EMBRYO; CHICKENS; CYTOSKELETAL PROTEINS; DYSTROGLYCANS; DYSTROPHIN; IMMUNOHISTOCHEMISTRY; MEMBRANE GLYCOPROTEINS; MICROSCOPY, IMMUNOELECTRON; NEUROGLIA; NEUROMUSCULAR JUNCTION; PHOTORECEPTORS; RATS; RETINA; SPECIES SPECIFICITY; VITREOUS BODY;

EID: 0031590677     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19971229)389:4<668::AID-CNE9>3.0.CO;2-Z     Document Type: Article

References (82)

1. Apel, E.D., S.L. Roberds, K.P. Campbell, and J.P. Merlie (1995) Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex. Neuron 15:115-126.
2. Bewick, G.S., L.V.B. Nicholson, C. Young, E. O'Donnell, and C.R. Slater (1992) Different distributions of dystrophin and related proteins at nerve-muscle junctions. Neuroreport 3:857-860.
3. Bewick, G.S., L.V.B. Nicholson, C. Young, and C.R. Slater (1993) Relationship of a dystrophin-associated glycoprotein to junctional acetylcholine receptor clusters in rat skeletal muscle. Neuromusci. Disord. 3:503-506.
4. Bewick, G.S., C. Young, and C.R. Slater (1996) Spatial relationship of utrophin, dystrophin, β-dystroglycan and β-spectrin to acetylcholine receptor clusters during postnatal maturation of the rat neuromuscular junction. J. Neurocytol. 25:367-379.
5. Blake, D.J., J.M. Tinsley, and K.E. Davies (1996) Utrophin: A structural and functional comparison to dystrophin. Brain Pathol. 6:37-47.
6. Bowe, M.A., K.A. Deyst, J.D. Leszyk, and J.R. Fallen (1994) Identification and purification of an agrin receptor from Torpedo postsynaptic membranes: A heteromeric complex related to the dystroglycans. Neuron 12:1173-1180.
7. Brandstätter, J.H., P. Koulen, R. Kuhn, H. van der Putten, and H. Wässle (1996) Compartmental localization of a metabotrophic glutamate receptor (mGluR7): Two different active sites at a retinal synapse. J. Neurosci. 16:4749-4756.
8. Brew, H., P.T. Gray, P. Mobbs, and D. Attwell (1986) End-feet of retinal glial cells have higher densities of ion channels that mediate K+ buffering. Nature 324:466-468.
9. Brew, H., and D. Attwell (1987) Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327:707-709.
10. Brown, R.H.J. (1996) Dystrophin-associated proteins and the muscular dystrophies: A glossary. Brain Pathol. 6:19-24.
11. Campanelli, J.T., S.L. Roberds, K.P. Campbell, and R.H. Scheller (1994) A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell 77:663-674.
12. Campbell, K.P. (1995) Three muscular dystrophies: Loss of cytoskeleton-extracellular matrix linkage. Cell 80:675-679.
13. Campbell, K.P., and S.D. Kahl (1989) Association of dystrophin and an integral membrane glycoprotein. Nature 338:259-262.
14. Cibis, G.W., K.M. Fitzgerald, D.J. Harris, P.G. Rothberg, and M. Rupani (1993) The effects of dystrophin gene mutations on the ERG in mice and humans. Invest. Ophthalmol. Vis. Sci. 34:3646-3652.
15. Cullen, M.J., J. Walsh, and L.V.B. Nicholson (1994) Immunogold localization of the 43-kDa dystroglycan at the plasma membrane in control and dystrophic human muscle. Acta Neuropathol. 87:349-354.
16. D'Souza, V.N., T.M. Nguyen, G.E. Morris, W. Karges, D.M. Pillers, and P.N. Ray (1995) A novel dystrophin isoform is required for normal retinal electrophysiology. Hum. Mol. Genet. 4:837-842.
17. Denzer, A. J., M. Gesemann, and M.A. Ruegg (1996) Diverse functions of the extracellular-matrix molecule agrin. Semin. Neurosci. 8:357-366.
18. Drenckhahn, D., M. Holbach, W. Ness, F. Schmitz, and L.V.B. Anderson (1996) Dystrophin and the dystrophin-associated glycoprotein, β-dystroglycan, co-localize in photoreceptor synaptic complexes of the human retina. Neuroscience 73:605-612.
19. Eldred, W.D., C. Zucker, H.J. Karten, and S. Yazulla (1983) Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. J. Histochem. Cytochem. 31:285-292.
20. Ervasti, J.M., K. Ohlendieck, S.D. Kahl, M.G. Gaver, and K.P. Campbell (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345:315-319.
21. Ervasti, J.M., and K.P. Campbell (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell 66:1121-1131.
22. Fitzgerald, K.M., G.W. Cibis, S.A. Giambrone, and D.J. Harris (1994) Retinal signal transmission in Duchenne muscular dystrophy: Evidence for dysfunction in the photoreceptor/depolarizing bipolar cell pathway. J. Clin. Invest. 93:2425-2430.
23. Fong, P.Y., P.R. Turner, W.F. Denetclaw, and H.A. Steinhardt (1990) Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250:673-676.
24. Franco, A., Jr., and J.B. Lansman (1990) Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature 344:670-673.
25. Gee, S.H., F. Montanaro, M.H. Lindenbaum, and S. Carbonetto (1994) Dystroglycan-α, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77:675-686.
26. Gesemann, M., V. Cavalli, A.J. Denzer, A. Brancaccio, B. Schumacher, and M.A. Ruegg (1996) Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron 16:755-767.
27. Gorecki, D.C., J.M. Derry, and E.A. Barnard (1994) Dystroglycan: Brain localisation and chromosome mapping in the mouse. Hum. Mol. Genet. 3:1589-1597.
28. Halfter, W., W. Reckhaus, and S. Kroger (1987) Nondirected axonal growth on basal lamina from avian embryonic neural retina. J. Neurosci. 7:3712-3722.
29. Hall, Z.W., and J.R. Sanes (1993) Synaptic structure and development: The neuromuscular junction. Cell/Neuron 72(Suppl. 10):99-121.
30. Haws, C.M., and J.B. Lansman (1991) Calcium-permeable ion channels in cerebellar neurons from mdx mice. Proc. R. Soc. Lond. Biol. 244:185-189.
31. Henry, M.D., and K.P. Campbell (1996) Dystroglycan: An extracellular matrix receptor linked to the cytoskeleton. Curr. Opin. Cell Biol. 8:625-631.
32. Hoffman, E.P., R.H.J. Brown, and L.M. Kunkel (1987) Dystrophin: The protein product of the Duchenne muscular dystrophy locus. Cell 51:919-928.
33. Hopf, C., and W. Hoch (1996) Agrin binding to α-dystroglycan: Domains of agrin necessary to induce acetylcholine-receptor clustering are overlapping but not identical to the α-dystroglycan-binding region. J. Biol. Chem. 271:5231-5236.
34. Hopf, F.W., and R.A. Steinhardt (1992) Regulation of intracellular free calcium in normal and dystrophic mouse cerebellar neurons. Brain Res. 578:49-54.
35. Hyser, C.L., and J.R. Mendell (1988) Recent advances in Duchenne and Becker muscular dystrophy. Neurol. Clin. 6:429-453.
36. Ibraghimov-Beskrovnaya, O., J.M. Ervasti, C.J. Leveille, C.A. Slaughter, S.W. Sernett, and K.P. Campbell (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696-702.
37. Ibraghimov-Beskrovnaya, O., A. Milatovich, T. Ozcelik, B. Yang, K. Koepnick, U. Francke, and K.P. Campbell (1993) Human dystroglycan: Skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum. Mol. Genet. 2:1651-1657.
38. Jung, D., B. Yang, J. Meyer, J.S. Chamberlain, and K.P. Campbell (1995) Identification and characterization of the dystrophin anchoring site on β-dystroglycan. J. Biol. Chem. 270:27305-27310.
39. Jung, D., F. Leturcq, Y. Sunada, F. Duclos, F.M. Tomé, C.R. Moomaw, L. Merlini, K. Azibi, M. Chaouch, C. Slaughter, M. Fardeau, J.C. Kaplan, and K.P. Campbell (1996) Absence of γ-sarcoglycan (35 DAG) in autosomal recessive muscular dystrophy linked to chromosome 13q12. FEBS Lett. 381:15-20.
40. Kirsch, J., and S. Kröger (1996) Postsynaptic anchoring of receptors: A cellular approach to neuronal and muscular sensitivity. The Neuroscientist 2:100-108.
41. Kröger, S., S.E. Horton, and L.S. Honig (1996) The developing avian retina expresses agrin isoforms during synaptogenesis. J. Neurobiol. 29:165-182.
42. Kröger S., and S. Mann (1996) Biochemical and functional characterization of basal lamina-bound agrin in the chick central nervous system. Eur. J. Neurosci. 8:500-509.
43. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
44. Lasansky, A. (1969) Basal junctions at synaptic endings of turtle visual cells. J. Cell Biol. 40:577-581.
45. Lidov, H.G.W. (1996) Dystrophin in the nervous system. Brain Pathol. 6:63-77.
46. Love, D.R., D.F. Hill, G. Dickson, N.K. Spurr, B.C. Byth, R.F. Marsden, F.S. Walsh, Y.H. Edwards, and K.E. Davies (1989) An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 339:55-58.
47. Mann, S., and S. Kroger (1996) Agrin is synthesized by retinal cells and colocalizes with gephyrin. Mol. Cell. Neurosci. 8:1-13.
48. Masu, M., H. Iwakabe, Y. Tagawa, T. Miyoshi, M. Yamashita, Y. Fukuda, H. Sasaki, K. Hiroi, Y. Nakamura, R. Shigemoto, M. Takada, K. Nakamura, K. Nakao, M. Katsuki, and S. Nakanishi (1995) Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80:757-765.
49. Matsumura, K., J.M. Ervasti, K. Ohlendieck, S.D. Kahl, and K.P. Campbell (1992) Association of dystrophin-related protein with dystrophm-associated proteins in mdx mouse muscle. Nature 360:588-591.
50. McMahan, U.J. (1990) The agrin hypothesis. Cold Spring Harb. Symp. Quant. Biol. 55:407-418.
51. McMahan, U.J., S.E. Horton, M.J. Werle, L.S. Honig, S. Kröger, M.A. Ruegg and G. Escher (1992) Agrin isoforms and their role in synaptogenesis. Curr. Opin. Cell Biol. 4:869-874.
52. Mehler, M.F., K.Z. Haas, J.A. Kessler, and P.K. Stanton (1992) Enhanced sensitivity of hippocampal pyramidal neurons from mdx mice to hypoxia-induced loss of synaptic transmission. Proc. Natl. Acad. Sci. USA 89:2461-2465.
53. Montanaro F., S. Carbonetto, K.P. Campbell, and M. Lindenbaum (1995) Dystroglycan expression in the wild type and mdx mouse neural retina: Synaptic colocalization with dystrophin, dystrophin-related protein but not laminin. J. Neurosci. Res. 42:528-538.
54. Muntoni, F., A. Mateddu, and G. Serra (1991) Passive avoidance behaviour deficit in the mdx mouse. Neuromuscl. Disord. 1:121-123.
55. Newman, E.A. (1984) Regional specialization of retinal glial cell membrane. Nature 309:155-157.
56. Newman, E.A. (1991) Sodium-bicarbonate cotransport in retinal Müller (glial) cells of the salamander. J. Neurosci. 11:3972-3983.
57. Nomura, A., R. Shigemoto, Y. Nakamura, N. Okamoto, N. Mizuno, and S. Nakanishi (1994) Developmental regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77:361-369.
58. Pillers, D.M., D.E. Bulman, R.G. Weleber, D.A. Sigesmund, M.A. Musaralla, B.R. Powell, W.H. Murphey, C. Westall, C. Panton, L.E. Becker, R.G. Worton, and P.N. Ray (1993) Dystrophin expression in the human retina is required for normal function as defined by electroretinography. Nat. Genet. 4:82-86.
59. Cv3 mouse is a model for electroretinography of Duchenne/Becker muscular dystrophy. Invest. Ophthalmol. Vis. Sci. 36:462-466.
60. Rafael, J.A., G.A. Cox, K. Corrado, D. Jung, K.P. Campbell, and J.S. Chamberlain (1996) Forced expression of dystrophin deletion constructs reveals structure-function correlations. J. Cell Biol. 134:93-102.
61. +-ATPase activity of isolated Müller (glial) cells from the rabbit retina. Neurosci. Lett. 55:29-34.
62. 1 subunit of the glycine receptor. J. Neurosci. 14:5131-5146.
63. Schmitz, F., M. Holbach, and D. Drenckhahn (1993) Colocalization of retinal dystrophin and actin in postsynaptic dendrites of rod and cone photoreceptor synapses. Histochemistry 100:473-479.
64. Sigesmund, D.A., R.G. Weleber, D.M. Pillers, C.A. Westall, C.M. Panton, B.R. Powell, E. Heon, W.H. Murphey, M.A. Musarella, and P.N. Ray (1994) Characterization of the ocular phenotype of Duchenne and Becker muscular dystrophy. Ophthalmology 101:856-865.
65. Stockton, R.A., and M.M. Slaughter (1989) B-wave of the electroretinogram: A reflection of ON bipolar cell activity. J. Gen. Physiol. 93:101-122.
66. Sugiyama, J., D.C. Bowen, and Z.W. Hall (1994) Dystroglycan binds nerve and muscle agrin. Neuron 13:103-115.
67. Suzuki, A., M. Yoshida, H. Yamamoto, and E. Ozawa (1992) Glycoprotein-binding site of dystrophin is confined to the cysteine-rich domain and the first half of the carboxy-terminal domain. FEBS Lett. 308:154-160.
68. Suzuki, A., M. Yoshida, K. Hayashi, Y. Mizuno, Y. Hagiwara, and E. Ozawa (1994) Molecular organization at the glycoprotein complex-binding site of dystrophin. Eur. J. Biochem. 220:283-292.
69. Tian, M., C. Jacobson, S.H. Gee, K.P. Campbell, S. Carbonetto, and M. Jucker (1997) Dystroglycan in the cerebellum is a laminin α2-chain binding protein at the glial-vascular interface and is expressed in Purkinje cells. Eur. J. Neurosci. 8:2739-2747.
70. Tinsley, J.M., D.J. Blake, A. Roche, U. Fairbrother, J. Riss, B.C. Byth, A.E. Knight, J. Kendrick-Jones, G.K. Suthers, D.R. Love, Y.H. Edwards, and K.E. Davies (1992) Primary structure of dystrophin-related protein. Nature 360:591-593.
71. Towbin, H., T. Staehlin, and J. Gordon (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedures and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
72. Tsen, G., W. Halfter, S. Kröger, and G.J. Cole (1995) Agrin is a heparan sulfate proteoglycan. J. Biol. Chem. 270:3392-3399.
73. Ueda, H., T. Kobayashi, K. Mitsui, K. Tsurugi, S. Tsukahara, and S. Ohno (1995) Dystrophin localization at presynapse in rat retina revealed by immunoelectron microscopy. Invest. Ophthalmol. Vis. Sci. 36:2318-2322.
74. Vaillend, C., A. Rendon, R. Misslin, and A. Ungerer (1995) Influence of dystrophin-gene mutation on mdx mouse behavior: I. Retention deficits at long delays in spontaneous alternation and bar-pressing tasks. Behav. Genet. 25:569-579.
75. 1 subunit. Neuron 9:1099-1115.
76. 1A subunits of brain calcium channels. J. Neurosci. 15:6403-6418.
77. Wolburg, H. (1995) Orthogonal arrays of intramembranous particles: A review with special reference to astrocytes. J. Brain Res. 36:239-258.
78. Yamada, H., A.J. Denzer, H. Hori, T. Tanaka, L.V.B. Anderson, S. Fujita, H. Fukutaohi, T. Shimizu, M.A. Ruegg, and K. Matsumura (1996) Dystroglycan is a dual receptor for agrin and laminin-2 in Schwann cell membrane. J. Biol. Chem. 271:23418-23423.
79. Yang, B., D. Jung, D. Motto, J. Meyer, G. Koretzky, and K.P. Campbell (1995) SH3 domain-mediated interaction of dystroglycan and Grb2. J. Biol. Chem. 270:11711-11714.
80. Yoshida, M., Y. Mizuno, I. Nonaka, and E. Ozawa (1993) A dystrophin-associated glycoprotein, A3a (one of 43DAG doublets), is retained in Duchenne muscular dystrophy muscle. J. Biochem. 114:634-639.
81. Yoshida, M., A. Suzuki, H. Yammamoto, S. Noguchi, Y. Mizuno, and E. Ozawa (1994) Dissociation of the complex of dystrophin and its associated proteins into several unique groups by n-octyl β?D-glucoside. Eur. J. Biochem. 222:1055-1061.
82. Yoshida, M., and E. Ozawa (1990) Glycoprotein complex anchoring dystrophin to sarcolemma. J. Biochem. 108:748-752.