Retinoschisin forms a multimolecular complex with extracellular matrix and cytoplasmic proteins: Interactions with β2 laminin and αB-crystallin

Molecular Vision

Volumn 12, Issue , 2006, Pages 892-901

  Steiner Champliaud, Marie France ^a   Sahel, José ^a   Hicks, David ^a,b  

^a HÔPITAL SAINT ANTOINE   (France)

^b Hopitaux Universitaires de Strasbourg   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; CYTOPLASM PROTEIN; EYE PROTEIN; LAMININ; LAMININ BETA2; MESSENGER RNA; PEANUT AGGLUTININ; RETINOSCHISIN; UNCLASSIFIED DRUG; BETA CRYSTALLIN; CARRIER PROTEIN; LAMININ S; RS1 PROTEIN, HUMAN; SCLEROPROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; COMPLEX FORMATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHOTORECEPTOR; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RETINA NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SWINE; WESTERN BLOTTING; ANIMAL; CYTOLOGY; CYTOPLASM; DRUG INTERACTION; METABOLISM; RETINA; TISSUE DISTRIBUTION;

ALPHA-CRYSTALLINS; ANIMALS; BETA-CRYSTALLINS; CARRIER PROTEINS; CELLS, CULTURED; CYTOPLASM; DRUG INTERACTIONS; EXTRACELLULAR MATRIX PROTEINS; EYE PROTEINS; LAMININ; PEANUT AGGLUTININ; PHOTORECEPTORS, VERTEBRATE; RETINA; SWINE; TISSUE DISTRIBUTION;

EID: 33748749534     PISSN: None     EISSN: 10900535     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Condon GP, Brownstein S, Wang NS, Kearns JA, Ewing CC. Congenital hereditary (juvenile X-linked) retinosehisis. Histopathologic and ultrastructural findings in three eyes. Arch Ophthalmol 1986; 104:576-83.
2. Kellner U, Brummer S, Foerster MH, Wessing A. X-linked congenital retinoschisis. Graefes Arch Clin Exp Ophthalmol 1990; 228:432-7.
3. George ND, Yates JR, Moore AT. Clinical features in affected males with X-linked retinoschisis. Arch Ophthalmol 1996; 114:274-80.
4. Tantri A, Vrabec TR, Cu-Unjieng A, Frost A, Annesley WH Jr, Donoso LA. X-linked refinoschisis: a clinical and molecular genetic review. Surv Ophthalmol 2004; 49:214-30.
5. Peachey NS, Fishman GA, Derlacki DJ, Brigell MG. Psychophysical and electroretinographic findings in X-linked juvenile retinoschisis. Arch Ophthalmol 1987; 105:513-6.
6. Sieving PA, Bingham EL, Kemp J, Richards J, Hiriyanna K. Juvenile X-linked retinoschisis from XLRS1 Arg213Trp mutation with preservation of the electroretinogram scotopic b-wave. Am J Ophthalmol 1999; 128:179-84.
7. Khan NW, Jamison JA, Kemp JA, Sieving PA. Analysis of photoreceptor function and inner retinal activity in juvenile X-linked retinoschisis. Vision Res 2001; 41:3931-42.
8. Sauer CG, Gehrig A, Warneke-Wittstock R, Marquardt A, Ewing CC, Gibson A, Lorenz B, Jurklies B, Weber BH. Positional cloning of the gene associated with X-linked juvenile retinoschisis. Nat Genet 1997; 17:164-70.
9. Springer WR, Cooper DN, Barondes SH. Discoidin I is implicated in cell-substratum attachment and ordered cell migration of Dictyostelium discoideum and resembles fibronectin. Cell 1984; 39:557-64.
10. Baumgartner S, Hofmann K, Chiquet-Ehrismann R, Bucher P. The discoidin domain family revisited: new members from prokaryotes and a homology-based fold prediction. Protein Sci 1998; 7:1626-31.
11. Vogel, W. Discoidin domain receptors: structural relations and functional implications. FASEB J 1999; 13:S77-82.
12. Wu WW, Wong JP, Kast J, Molday RS. RS1, a discoidin domain-containing retinal cell adhesion protein associated with X-linked retinoschisis, exists as a novel disulfide-linked octamer. J Biol Chem 2005; 280:10721-30.
13. Shastry BS, Hejtmancik FJ, Trese MT. Recurrent missense (R197C) and nonsense (Y89X) mutations in the XLRS1 gene in families with X-linked retinoschisis. Biochem Biophys Res Commun 1999; 256:317-9.
14. Inoue Y, Yamamoto S, Okada M, Tsujikawa M, Inoue T, Okada AA, Kusaka S, Saito Y, Wakabayashi K, Miyake Y, Fujikado T, Tano Y. X-linked retinoschisis with point mutations in the XLRS1 gene. Arch Ophthalmol 2000; 118:93-6.
15. Wang T, Waters CT, Rothman AM, Jakins TJ, Romisch K, Trump D. Intracellular retention of mutant retinoschisin is the pathological mechanism underlying X-linked retinoschisis. Hum Mol Genet 2002; 11:3097-105.
16. Wu WW, Molday RS. Defective discoidin domain structure, subunit assembly, and endoplasmic reticulum processing of retinoschisin are primary mechanisms responsible for X-linked retinoschisis. J Biol Chem 2003; 278:28139-46.
17. Wang T, Zhou A, Waters CT, O'Connor E, Read RJ, Trump D. Molecular pathology of X linked retinoschisis: mutations interfere with retinoschisin secretion and oligomerisation. Br J Ophthalmol 2006; 90:81-6.
18. Reid SN, Akhmedov NB, Piriev NI, Kozak CA, Danciger M, Farber DB. The mouse X-linked juvenile retinoschisis cDNA: expression in photoreceptors. Gene 1999; 227:257-66.
19. Grayson C, Reid SN, Ellis JA, Rutherford A, Sowden JC, Yates JR, Farber DB, Trump D. Retinoschisin, the X-linked retinoschisis protein, is a secreted photoreceptor protein, and is expressed and released by Weri-Rb1 cells. Hum Mol Genet 2000; 9:1873-9.
20. Reid SN, Yamashita C, Farber DB. Retinoschisin, a photoreceptor-secreted protein and its interaction with bipolar and muller cells. J Neurosci 2003; 23:6030-40.
21. Reid SN, Farber DB. Glial transcytosis of a photoreceptor-secreted signaling protein, retinoschisin. Glia 2005; 49:397-406.
22. Molday LL, Hicks D, Sauer CG, Weber BH, Molday RS. Expression of X-linked retinoschisis protein RS1 in photoreceptor and bipolar cells. Invest Ophthalmol Vis Sci 2001; 42:816-25.
23. Takada Y, Fariss RN, Tanikawa A, Zeng Y, Carper D, Bush R, Sieving PA. A retinal neuronal developmental wave of retinoschisin expression begins in ganglion cells during layer formation. Invest Ophthalmol Vis Sci 2004; 45:3302-12.
24. Weber BH, Schrewe H, Molday LL, Gehrig A, White KL, Seeliger MW, Jaissle GB, Friedlburg C, Tamm E, Molday RS. Inactivation of the murine X-linked juvenile retinoschisis gene, Rs1h, suggests a role of retinoschisin in retin cell layer organization and synaptic structure. Proc Natl Acad Sci U S A 2002; 99:6222-7.
25. Zeng Y, Takada Y, Kjellstrom S, Hiriyanna K, Tanikawa A, Wawrousek E, Smaoui N, Caruso R, Bush RA, Sieving PA. RS1 Gene Delivery to an Adult Rs1h Knockout Mouse Model Restores ERG b-Wave with Reversal of the Electronegative Wave-form of X-Linked Retinoschisis. Invest Ophthalmol Vis Sci 2004; 45:3279-85.
26. Min SH, Molday LL, Seeliger MW, Dinculescul, Timmers AM, Janssen A, Tonagel F, Tanimoto N, Weber BH, Molday RS, Hauswirth WW. Prolonged recovery of retinal structure/function after gene therapy in an Rs1h-deficient mouse model of x-linked juvenile retinoschisis. Mol Ther 2005; 12:644-51.
27. Libby RT, Hunter DD, Brunken WJ. Developmental expression of laminin beta 2 in rat retina. Further support for a role in rod morphogenesis. Invest Ophthalmol Vis Sci 1996; 37:1651-61.
28. Traverso V, Kinkl N, Grimm L, Sahel J, Hicks D. Basic fibroblast and epidermal growth factors stimulate survival in adult porcine photoreceptor cell cultures. Invest Ophthalmol Vis Sci 2003; 44:4550-8.
29. Cuatrecasas P. Protein purification by affinity chromatography. Derivatizations of agarose and polyacrylamide beads. J Biol Chem 1970; 245:3059-65.
30. Fontaine V, Kinkl N, Sahel J, Dreyfus H, Hicks D. Survival of purified rat photoreceptors in vitro is stimulated directly by fibroblast growth factor-2. J Neurosci 1998; 18:9662-72.
31. Nomura A, Shigemoto R, Nakamura Y, Okamoto N, Mizuno N, Nakanishi S. Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 1994; 77:361-9.
32. Stryer L. Cyclic GMP cascade of vision. Annu Rev Neurosci 1986; 9:87-119.
33. Aebersold RH, Leavitt J, Saavedra RA, Hood LE, Kent SB. Internal amino acid sequence analysis of proteins separated by one- or two-dimensional gel electrophoresis after in situ protease digestion on nitrocellulose. Proc Natl Acad Sci U S A 1987; 84:6970-4.
34. Chait BT, Kent SB. Weighing naked proteins: practical, high-accuracy mass measurement of peptides and proteins. Science 1992; 257:1885-94.
35. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-5.
36. Lunstrum GP, Sakai LY, Keene DR, Morris NP, Burgeson RE. Large complex globular domains of type VII procollagen contribute to the structure of anchoring fibrils. J Biol Chem 1986; 261:9042-8.
37. Mohand-Said S, Hicks D, Simonutti M, Tran-Minh D, Deudon-Combe A, Dreyfus H, Silverman MS, Ogilvie JM, Tenkova T, Sahel J. Photoreceptor transplants increase host cone survival in the retinal degeneration (rd) mouse. Ophthahnic Res 1997; 29:290-7.
38. Curat CA, Eck M, Dervillez X, Vogel W. Mapping of epitopes in discoidin domain receptor 1 critical for collagen binding. J Biol Chem 2001; 276:45952-8.
39. Cavaldesi M, Macchia G, Barca S, Defilippi P, Throne G, Petrucci TC. Association of the dystroglycan complex isolated from bovine brain synaptosomes with proteins involved in signal transduction. J Neurochem 1999; 72:1648-55.
40. Ervasti JM, Campbell KP. Membrane organization of the dystrophin-glycoprotein complex. Cell 1991; 66:1121-31.
41. Henry MD, Campbell KP. Dystroglycan: an extracellular matrix receptor linked to the cytoskeleton. Curr Opin Cell Biol 1996; 8:625-31.
42. Claudepierre T, Rodius F, Frasson M, Fontaine V, Picaud S, Dreyfus H, Mornet D, Rendon A. Differential distribution of dystrophins in rat retina. Invest Ophthalmol Vis Sci 1999; 40:1520-9.
43. Pillers DA, Bulman DE, Weleber RG, Sigesmund DA, Musarella MA, Powell BR, Murphey WH, Westall C, Panton C, Becker LE, Worton RG, Ray PN. Dystrophin expression in the human retina is required for normal function as defined by, electroretinography. Nat Genet 1993; 4:82-6.
44. Kameya S, Araki E, Katsuki M, Mizota A, Adachi E, Nakahara K, Nonaka I, Sakuragi S, Takeda S, Nabeshima Y. Dp260 disrupted mice revealed prolonged implicit time of the b-wave in ERG and loss of accumulation of beta-dystroglycan in the outer plexiform layer of the retina. Hum Mol Genet 1997; 6:2195-203.
45. Libby RT, Champliaud MF, Claudepierre T, Xu Y, Gibbons EP, Koch M, Burgeson RE, Hunter DD, Brunken WJ. Laminin expression in adult and developing retinae: evidepce of two novel CNS laminins. J Neurosci 2000; 20:6517-28.
46. Xi J, Farjo R, Yoshida S, Kern TS, Swaroop A, Andley UP. A comprehensive analysis of the expression of crystallins in mouse retina. Mol Vis 2003; 9:410-9.
47. Jones SE, Jomary C, Grist J, nomas MR, Neal MJ. Expression of alphaB-crystallin in a mouse model of inherited retinal degeneration. Neuroreport 1998; 9:4161-5.
48. Deretic D, Aebersold RH, Morrison HD, Papermaster DS. Alpha, A- and alpha B-crystallin in the retina. Association with the post-Golgi compartment of frog retinal photoreceptors. J Biol Chem 1994; 269:16853-61.
49. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc Nad Acad Sci U S A 1992; 89:10449-53.
50. Groenen PJ, Merck KB, de Jong WW, Bloemendal H. Structure and modifications of the junior chaperone alpha-crystallin. From lens transparency to molecular pathology. Eur J Biochem 1994; 225:1-19.
51. Mao YW, Liu JP, Xiang H, Li DW. Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ 2004; 11:512-26.
52. Sakaguchi H, Miyagi M, Darrow RM, Crabb JS, Hollyfield JG, Organisciak DT, Crabb JW. Intense light exposure changes the crystallin content in retina. Exp Eye Res 2003; 76:131-3. Erratum in: Exp Eye Res 2003; 77:121-2.
53. Cavusoglu N, Thierse D, Mohand-Said S, Chalmel F, Poch O, Van-Dorsselaer A, Sahel JA, Leveillard T. Differential proteomic analysis of the mouse retina: the induction of crystallin proteins by retinal degeneration in the rd1 mouse. Mol Cell Proteomics 2003; 2:494-505.:
54. Hageman GS, Johnson LV. Biochemical characterization of the major peanut-agglutinin-binding glycoproteins in vertebrate retinae. J Comp Neurol 1986; 249:499-510.
55. Durkin ME, Bartos BB, Liu SH, Phillips SL, Chung AE. Primary structure of the mouse laminin B2 chain and comparison with laminin B1. Biochemistry 1988; 27:5148-204.
56. Arumugham RG, Hsieh TC, Tanzer ML, Laine RA. Structures of the asparagine-linked sugar chains of laminin. Biochim Biophys Acta 1986; 883:112-26.
57. Uehara F, Yasumura D, LaVail MM. New isolation method of retina and interphotoreceptor matrix. Exp Eye Res 1989; 49:305-9.