An intramembrane glutamic acid governs peripherin/rds function for photoreceptor disk morphogenesis

Investigative Ophthalmology and Visual Science

Volumn 48, Issue 7, 2007, Pages 2975-2986

  Goldberg, Andrew F X ^a   Ritter, Linda M ^a   Khattree, Nidhi ^a   Peachey, Neal S ^b,c   Fariss, Robert N ^d   Dang, Loan ^a   Yu, Minzhong ^b   Bottrell, Alyssa R ^a  

^a OAKLAND UNIVERSITY   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^d NATIONAL EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; GLUTAMINE; PERIPHERIN; TETRASPANIN; INTERMEDIATE FILAMENT PROTEIN; MEMBRANE PROTEIN; NERVE PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAPHY; IMMUNOPRECIPITATION; MICROSCOPY; MORPHOGENESIS; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RETINA DEGENERATION; SEDIMENTATION; TRANSGENIC MOUSE; WESTERN BLOTTING; WILD TYPE; ANIMAL; C57BL MOUSE; CELL STRAIN COS1; CERCOPITHECUS; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; IMMUNOELECTRON MICROSCOPY; METABOLISM; PATHOLOGY; PHYSIOLOGY; RETINA; SITE DIRECTED MUTAGENESIS; TRANSGENE; ULTRASTRUCTURE;

AMINO ACID SUBSTITUTION; ANIMALS; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; COS CELLS; ELECTRORETINOGRAPHY; GENE EXPRESSION REGULATION; GENOTYPE; GLUTAMIC ACID; IMMUNOPRECIPITATION; INTERMEDIATE FILAMENT PROTEINS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, IMMUNOELECTRON; MORPHOGENESIS; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; PHOTORECEPTORS, VERTEBRATE; RETINA; RETINAL DEGENERATION; TRANSGENES;

EID: 34548076673     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.07-0049     Document Type: Article

References (60)

1. Young RW. Visual cells and the concept of renewal. Invest Ophthalmol Vis Sci. 1976;15:700-725.
2. van Soest S, Westerveld A, de Jong PT, Bleeker-Wagemakers EM, Bergen AA. Retinitis pigmentosa: defined from a molecular point of view. Surv Ophthalmol. 1999;43:321-334.
3. Goldberg AFX. Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations. Int Rev Cytol. 2006;253:131-175.
4. Hawkins RK, Jansen HG, Sanyal S. Development and degeneration of retina in rds mutant mice: photoreceptor abnormalities in the heterozygotes. Exp Eye Res. 1985;41:701-720.
5. Sanyal S, Jansen HG. Absence of receptor outer segments in the retina of rds mutant mice. Neurosci Lett. 1981;21:23-26.
6. Bascom RA, Manara S, Collins L, Molday RS, Kalnins VI, McInnes RR. Cloning of the cDNA for a novel photoreceptor membrane protein (rom-1) identifies a disk rim protein family implicated in human retinopathies. Neuron. 1992;8:1171-1184.
7. Clarke G, Goldberg AF, Vidgen D, et al. Rom-1 is required for rod photoreceptor viability and the regulation of disk morphogenesis. Nat Genet. 2000;25:67-73.
8. Moritz OL, Molday RS. Molecular cloning, membrane topology, and localization of bovine rom-1 in rod and cone photoreceptor cells. Invest Ophthalmol Vis Sci. 1996;37:352-362.
9. Goldberg AF, Moritz OL, Molday RS. Heterologous expression of photoreceptor peripherin/rds and Rom-1 in COS-1 cells: assembly, interactions, and localization of multisubunit complexes. Biochemistry. 1995;34:14213-14219.
10. Kedzierski W, Weng J, Travis GH. Analysis of the rds/peripherin-.rom1 complex in transgenic photoreceptors that express a chimeric protein. J Biol Chem. 1999;274:29181-29187.
11. Goldberg AF, Molday RS. Defective subunit assembly underlies a digenic form of retinitis pigmentosa linked to mutations in peripherin/rds and rom-1. Proc Natl Acad Sci U S A. 1996;93:13726-13730.
12. Goldberg AF, Loewen CJ, Molday RS. Cysteine residues of photoreceptor peripherin/rds: role in subunit assembly and autosomal dominant retinitis pigmentosa. Biochemistry. 1998;37:680-685.
13. Loewen CJ, Molday RS. Disulfide-mediated oligomerization of peripherin/rds and Rom-1 in photoreceptor disk membranes: implications for photoreceptor outer segment morphogenesis and degeneration. J Biol Chem. 2000;275:5370-5378.
14. Travis GH, Brennan MB, Danielson PE, Kozak CA, Sutcliffe JG. Identification of a photoreceptor-specific mRNA encoded by the gene responsible for retinal degeneration slow (rds). Nature. 1989;338:70-73.
15. Dryja TP, Hahn LB, Kajiwara K, Berson EL. Dominant and digenic mutations in the peripherin/RDS and ROM1 genes in retinitis pigmentosa. Invest Ophthalmol Vis Sci. 1997;38:1972-1982.
16. Kajiwara K, Berson EL, Dryja TP. Digenic retinitis pigmentosa due to mutations at the unlinked peripherin/RDS and ROM1 loci. Science. 1994;264:1604-1608.
17. Goldberg AF, Fales LM, Hurley JB, Khattree N. Folding and subunit assembly of photoreceptor peripherin/rds is mediated by determinants within the extracellular/intradiskal EC2 domain: implications for heterogeneous molecular pathologies. J Biol Chem. 2001;276:42700-42706.
18. Tam BM, Moritz OL, Papermaster DS. The C terminus of peripherin/rds participates in rod outer segment targeting and alignment of disk incisures. Mol Biol Cell. 2004;15:2027-2037.
19. Boesze-Battaglia K, Lamba OP, Napoli AA Jr, Sinha S, Guo Y. Fusion between retinal rod outer segment membranes and model membranes: a role for photoreceptor peripherin/rds. Biochemistry. 1998;37:9477-9487.
20. Wright MD, Tomlinson MG. The ins and outs of the transmembrane 4 superfamily. Immunol Today. 1994;15:588-594.
21. Maecker HT, Todd SC, Levy S. The tetraspanin superfamily: molecular facilitators. FASEB J. 1997;11:428-442.
22. Kovalenko OV, Metcalf DG, DeGrado WF, Hemler ME. Structural organization and interactions of transmembrane domains in tetraspanin proteins. BMC Struct Biol. 2005;5:11.
23. Hemler ME. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol. 2003;19:397-422.
24. Goldberg AF, Molday RS. Expression and characterization of peripherin/rds-rom-1 complexes and mutants implicated in retinal degenerative diseases. Methods Enzymol. 2000;316:671-687.
25. Woodford BJ, Chen J, Simon MI. Expression of rhodopsin promoter transgene product in both rods and cones. Exp Eye Res. 1994;58:631-635.
26. 2+ and causes photoreceptor degeneration in transgenic mice. J Neurosci. 2004;24:6078-6085.
27. Raport CJ, Lem J, Makino C, et al. Downregulation of cGMP phosphodiesterase induced by expression of GTPase-deficient cone transducin in mouse rod photoreceptors. Invest Ophthalmol Vis Sci. 1994;35:2932-2947.
28. Connell GJ, Molday RS. Molecular cloning, primary structure, and orientation of the vertebrate photoreceptor cell protein peripherin in the rod outer segment disk membrane. Biochemistry. 1990;29:4691-4698.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-408.
30. Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods. 2001;25:386-401.
31. Ding XQ, Nour M, Ritter LM, Goldberg AF, Fliesler SJ, Naash MI. The R172W mutation in peripherin/rds causes a cone-rod dystrophy in transgenic mice. Hum Mol Genet. 2004;13:2075-2087.
32. Ritter LM, Boesze-Battaglia K, Tam BM, et al. Uncoupling of photoreceptor peripherin/rds fusogenic activity from biosynthesis, subunit assembly, and targeting: a potential mechanism for pathogenic effects. J Biol Chem. 2004;279:39958-39967.
33. Lee Y, Kameya S, Cox GA, et al. Ocular abnormalities in Large-(myd) and Large(vls) mice, spontaneous models for muscle, eye, and brain diseases. Mol Cell Neurosci. 2005;30:160-172.
34. Goto Y, Peachey NS, Ziroli NE, et al. Rod phototransduction in transgenic mice expressing a mutant opsin gene. J Opt Soc Am A Opt Image Sci Vis. 1996;13:577-585.
35. Hale IL, Matsumoto B. Resolution of subcellular detail in thick tissue sections: immunohistochemical preparation and fluorescence confocal microscopy. Methods Cell Biol. 1993;38:289-324.
36. Barthel LK, Raymond PA. Improved method for obtaining 3-microns cryosections for immunocytochemistry. J Histochem Cytochem. 1990;38:1383-1388.
37. Molday RS, Hicks D, Molday L. Peripherin: a rim-specific membrane protein of rod outer segment discs. Invest Ophthalmol Vis Sci. 1987;28:50-61.
38. Stricker HM, Ding XQ, Quiambao A, Fliesler SJ, Naash MI. The Cys(214)->Ser mutation in peripherin/rds causes a loss-of-function phenotype in transgenic mice. Biochem J. 2005:388:605-613.
39. Van Nie R, Ivanyi D, Demant P. A new H-2-linked mutation, rds, causing retinal degeneration in the mouse. Tissue Antigens. 1978;12:106-108.
40. Ma J, Norton JC, Allen AC, et al. Retinal degeneration slow (rds) in mouse results from simple insertion of a t haplotype-specific element into protein-coding exon II. Genomics. 1995;28:212-219.
41. Connell G, Bascom R, Molday L, Reid D, McInnes RR, Molday RS. Photoreceptor peripherin is the normal product of the gene responsible for retinal degeneration in the rds mouse. Proc Natl Acad Sci USA. 1991;88:723-726.
42. Weng J, Belecky-Adams T, Adler R, Travis GH. Identification of two rds/peripherin homologs in the chick retina. Invest Ophthalmol Vis Sci. 1998;39:440-443.
43. Kedzierski W, Moghrabi WN, Allen AC, et al. Three homologs of rds/peripherin in Xenopus laevis photoreceptors that exhibit covalent and non-covalent interactions. J Cell Sci. 1996;109(pt 10):2551-2560.
44. Travis GH, Groshan KR, Lloyd M, Bok D. Complete rescue of photoreceptor dysplasia and degeneration in transgenic retinal degeneration slow (rds) mice. Neuron. 1992;9:113-119.
45. Nour M, Ding XQ, Stricker H, Fliesler SJ, Naash MI. Modulating expression of peripherin/rds in transgenic mice: critical levels and the effect of overexpression. Invest Ophthalmol Vis Sci. 2004;45:2514-2521.
46. Jansen HG, Sanyal S. Development and degeneration of retina in rds mutant mice: electron microscopy. J Comp Neurol. 1984;224:71-84.
47. Michon JJ, Li ZL, Shioura N, Anderson RJ, Tso MO. A comparative study of methods of photoreceptor morphometry. Invest Ophthalmol Vis Sci. 1991;32:280-284.
48. Kedzierski W, Lloyd M, Birch DG, Bok D, Travis GH. Generation and analysis of transgenic mice expressing P216L-substituted rds/peripherin in rod photoreceptors. Invest Ophthalmol Vis Sci. 1997;38:498-509.
49. Robson JG, Saszik SM, Ahmed J, Frishman LJ. Rod and cone contributions to the a-wave of the electroretinogram of the macaque. J Physiol. 2003;547:509-530.
50. Robson JG, Frishman LJ. Photoreceptor and bipolar cell contributions to the cat electroretinogram: a kinetic model for the early part of the flash response. J Opt Soc Am A Opt Image Sci Vis. 1996;13:613-622.
51. Sharma S, Ball SL, Peachey NS. Pharmacological studies of the mouse cone electroretinogram. Vis Neurosci. 2005;22:631-636.
52. Chen J, Makino CL, Peachey NS, Baylor DA, Simon MI. Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science. 1995,267:374-377.
53. Goldberg AF, Molday RS. Subunit composition of the peripherin/rds-rom-1 disk rim complex from rod photoreceptors: hydrodynamic evidence for a tetrameric quaternary structure. Biochemistry. 1996;35:6144-6149.
54. Kedzierski W, Nusinowitz S, Birch D, et al. Deficiency of rds/peripherin causes photoreceptor death in mouse models of digenic and dominant retinitis pigmentosa. Proc Natl Acad Sci USA. 2001;98:7718-7723.
55. Boesze-Battaglia K, Stefano FP, Fitzgerald C, Muller-Weeks S. ROM1 potentiates photoreceptor specific membrane fusion processes. Exp Eye Res. 2007;84:22-31.
56. Charrin S, Manie S, Billard M, et al. Multiple levels of interactions within the tetraspanin web. Biochem Biophys Res Commun. 2003;304:107-112.
57. Seigneuret M, Delaguillaumie A, Lagaudriere-Gesbert C, Conjeaud H. Structure of the tetraspanin main extracellular domain: a partially conserved fold with a structurally variable domain insertion. J Biol Chem. 2001;276:40055-40064.
58. Seigneuret M. Complete predicted three-dimensional structure of the facilitator transmembrane protein and hepatitis C virus receptor CD81: conserved and variable structural domains in the tetraspanin superfamily. Biophys J. 2006;90:212-227.
59. Min G, Wang H, Sun TT, Kong XP. Structural basis for tetraspanin functions as revealed by the cryo-EM structure of uroplakin complexes at 6-A resolution. J Cell Biol. 2006;173:975-983.
60. Chen C, Jiang Y, Koutalos Y. Dynamic behavior of rod photoreceptor disks. Biophys J. 2002;83:1403-1412.