Harmonin in the murine retina and the retinal phenotypes of Ushlc-mutant mice and human USH1C

Investigative Ophthalmology and Visual Science

Volumn 50, Issue 8, 2009, Pages 3881-3889

  Williams, David S ^a,b,c   Aleman, Tomas S ^d   Lillo, Conceptión ^b,e   Lopes, Vanda S ^a,b   Hughes, Louise C ^a,b   Stone, Edwin M ^f   Jacobson, Samuel G ^d  

^a JULES STEIN EYE INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF SALAMANCA   (Spain)

^f UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HARMONIN PROTEIN; ISOPROTEIN; PDZ PROTEIN; PROTEIN USH1C; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; USH1C PROTEIN, HUMAN; USH1C PROTEIN, MOUSE;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL ULTRASTRUCTURE; CHILD; CLINICAL ARTICLE; CYTOARCHITECTURE; ELECTRORETINOGRAPHY; HOMOZYGOSITY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; MOUSE; MOUSE MUTANT; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; PERIMETRY; PHENOTYPE; PHOTORECEPTOR; PHOTOSENSITIVITY; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RETINA CONE; RETINA DEGENERATION; RETINA ROD; SIBLING; USHER SYNDROME; VISUAL FIELD; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CONFOCAL MICROSCOPY; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MIDDLE AGED; PHOTORECEPTOR CELL; PRESCHOOL CHILD; RETINA; ULTRASTRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADOLESCENT; ADULT; ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CHILD; CHILD, PRESCHOOL; ELECTRORETINOGRAPHY; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; MIDDLE AGED; PHENOTYPE; PHOTORECEPTOR CELLS, VERTEBRATE; PROTEIN ISOFORMS; RETINA; RETINAL DEGENERATION; SIBLINGS; TOMOGRAPHY, OPTICAL COHERENCE; USHER SYNDROMES;

EID: 68349104989     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-3358     Document Type: Article

References (42)

1. Verpy E, Leibovici M, Zwaenepoel I, et al. A defect in harmonin, a PDZ domain-containing protein expressed in the inner ear sensory hair cells, underlies Usher syndrome type 1C. Nat Genet. 2000;26: 51-55.
2. Scanlan MJ, Chen YT, Williamson B, et al. Characterization of human colon cancer antigens recognized by autologous antibodies. Int J Cancer. 1998;76:652-658.
3. Scanlan MJ, Williamson B, Jungbluth A, et al. Isoforms of the human PDZ-73 protein exhibit differential tissue expression. Bio-chim BiophysActa. 1999;1445:39-52.
4. Boeda B, El-Amraoui A, Bahloul A, et al. Myosin Vila, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle. EMBO J. 2002;21:6689-6699.
5. Siemens J, Kazmierczak P, Reynolds A, Sticker M, Littlewood-Evans A, Muller U. The Usher syndrome proteins cadherin 23 and har-monin form a complex by means of PDZ-domain interactions. Proc Natl Acad SciUSA. 2002;99:14946-14951.
6. Adato A, Michel V, Kikkawa Y, et al. Interactions in the network of Usher syndrome type 1 proteins. Hum Mol Genet. 2005;14:347-356.
7. Reiners J, van Wijk E, Marker T, et al. Scaffold protein harmonin (USH1C) provides molecular links between Usher syndrome type 1 and type 2. Hum Mol Genet. 2005;14:3933-3943.
8. Kremer H, van Wijk E, Marker T, Wolfrum U, Roepman R. Usher syndrome: molecular links of pathogenesis, proteins and pathways. Hum Mol Genet. 2006;15:R262-R270.
9. Reiners J, Nagel-Wolfrum K, Jurgens K, Marker T, Wolfrum U. Molecular basis of human Usher syndrome: deciphering the meshes of the Usher protein network provides insights into the pathomechanisms of the Usher disease. Exp Eye Res. 2006;83:97-119.
10. van Wijk E, van der Zwaag B, Peters T, et al. The DFNB31 gene product whirlin connects to the Usher protein network in the cochlea and retina by direct association with USH2A and VLGR1. Hum Mol Genet. 2006;15:751-765.
11. Johnson KR, Gagnon LH, Webb LS, et al. Mouse models of USH1C and DFNB18: phenotypic and molecular analyses of two new spontaneous mutations of the Ush1c gene. Hum Mol Genet. 2003; 12:3075-3086.
12. Liu X, Vansant G, Udovichenko IP, Wolfrum U, Williams DS. Myosin VIIa, the product of the Usher 1B syndrome gene, is concentrated in the connecting cilia of photoreceptor cells. Cell Motil Cytoskel. 1997;37:240-252.
13. Buckley K, Kelly RB. Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol. 1985;100:1284-1294.
14. Johnson BA, Ikeda S, Pinto LH, Ikeda A. Reduced synaptic vesicle density and aberrant synaptic localization caused by a splice site mutation in the Rs1h gene. Vis Neurosci. 2006;23: 887-898.
15. Roman AJ, Boye SL, Aleman TS, et al. Electroretinographic analyses of Rpe65-mutant rd12 mice: developing an in vivo bioassay for human gene therapy trials of Leber congenital amaurosis. Mol Vis. 2007;13:1701-1710.
16. Jacobson SG, Yagasaki K, Feuer WJ, Roman AJ. Interocular asymmetry of visual function in heterozygotes of X-linked retinitis pigmentosa. Exp Eye Res. 1989;48:679-691.
17. Aleman TS, Cideciyan AV, Volpe NJ, Stevanin G, Brice A, Jacobson SG. Spinocerebellar ataxia type 7 (SCA7) shows a cone-rod dystrophy phenotype. Exp Eye Res. 2002;74:737-745.
18. Jacobson SG, Voigt WJ, Parel JM, et al. Automated light- and dark-adapted perimetry for evaluating retinitis pigmentosa. Ophthalmology. 1986;93:1604-1611.
19. Schwartz SB, Aleman TS, Cideciyan AV, et al. Disease expression in Usher syndrome caused by VLGR1 gene mutation (USH2C) and comparison with USH2A phenotype. Invest Ophthalmol Vis Sci. 2005;46:734-743.
20. Huang Y, Cideciyan AV, Papastergiou GI, et al. Relation of optical coherence tomography to microanatomy in normal and rd chickens. Invest Ophthalmol Vis Sci. 1998;39:2405-2416.
21. Jacobson SG, Aleman TS, Cideciyan AV, et al. Identifying photore-ceptors in blind eyes caused by RPE65 mutations: prerequisite for human gene therapy success. Proc Natl Acad Sci USA. 2005;102: 6177-6182.
22. Jacobson SG, Aleman TS, Sumaroka A, et al. Disease boundaries in the retina of patients with Usher syndrome caused by MYO7A gene mutations. Invest Ophthalmol Vis Sci. 2009;50(4):1886-1894.
23. Sale WS, Besharse JC, Piperno G. Distribution of acetylated alpha-tubulin in retina and in vitro-assembled microtubules. Cell Motil Cytoskeleton. 1988;9:243-253.
24. Goodyear R, Richardson G. The ankle-link antigen: an epitope sensitive to calcium chelation associated with the hair-cell surface and the calycal processes of photoreceptors. J Neurosci. 1999;19: 3761-3772.
25. Liu X, Bulgakov OV, Darrow KN, et al. Usherin is required for maintenance of retinal photoreceptors and normal development of cochlear hair cells. Proc Natl Acad SciUSA.2007;104:4413-4418.
26. Maerker T, van Wijk E, Overlack N, et al. A novel Usher protein network at the periciliary reloading point between molecular transport machineries in vertebrate photoreceptor cells. Hum Mol Genet. 2008;17:71-86.
27. Aleman TS, LaVail MM, Montemayor R, et al. Augmented rod bipolar cell function in partial receptor loss: an ERG study in P23H rhodopsin transgenic and aging normal rats. Vision Res. 2001;41: 2779-2797.
28. Bitner-Glindzicz M, Lindley KJ, Rutland P, et al. A recessive contiguous gene deletion causing infantile hyperinsulinism, enterop-athy and deafness identifies the Usher type 1C gene. Nat Genet. 2000;26:56-60.
29. Zwaenepoel I, Verpy E, Blanchard S, et al. Identification of three novel mutations in the USH1C gene and detection of thirty-one polymorphisms used for haplotype analysis. Hum Mutat. 2001;17: 34-41.
30. Ahmed ZM, Smith TN, Riazuddin S, et al. Nonsyndromic recessive deafness DFNB18 and Usher syndrome type IC are allelic mutations of USHIC. Hum Genet. 2002;110:527-531.
31. Blaydon DC, Mueller RF, Hutchin TP, et al. The contribution of USH1C mutations to syndromic and non-syndromic deafness in the UK. Clin Genet. 2003;63:303-307.
32. Azari AA, Aleman TS, Cideciyan AV, et al. Retinal disease expression in Bardet-Biedl syndrome-1 (BBS1) is a spectrum from macu-lopathy to retina-wide degeneration. Invest Ophthalmol Vis Sci. 2006;47:5004-5010.
33. Reiners J, Reidel B, El-Amraoui A, et al. Differential distribution of harmonin isoforms and their possible role in Usher-1 protein complexes in mammalian photoreceptor cells. Invest Ophthalmol Vis Sci. 2003;44:5006-5015.
34. Weil D, El-Amraoui A, Masmoudi S, et al. Usher syndrome type I G (USH1G) is caused by mutations in the gene encoding SANS, a protein that associates with the USH1C protein, harmonin. Hum Mol Genet. 2003;12:463-471.
35. Senften M, Schwander M, Kazmierczak P, et al. Physical and functional interaction between protocadherin 15 and myosin VIIa in mechanosensory hair cells. J Neurosci. 2006;26:2060-2071.
36. Reiners J, Marker T, Jurgens K, Reidel B, Wolfrum U. Photorecep-tor expression of the Usher syndrome type 1 protein protocad-herin 15 (USH1F) and its interaction with the scaffold protein harmonin (USH1C). Mol Vis. 2005;11:347-355.
37. Reiners J, Wolfrum U. Molecular analysis of the supramolecular usher protein complex in the retina: harmonin as the key protein of the Usher syndrome. Adv Exp Med Biol. 2006;572:349-353.
38. Williams DS. Usher syndrome: animal models, retinal function of Usher proteins, and prospects for gene therapy. Vision Res. 2008; 48:433-441.
39. Hasson T, Heintzelman MB, Santos-Sacchi J, Corey DP, Mooseker MS. Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type 1B. Proc Natl Acad Sci USA. 1995;92:9815-9819.
40. Gibbs D, Azarian SM, Lillo C, et al. Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes. J Cell Sci. 2004;117:6473-6483.
41. Hashimoto T, Gibbs D, Lillo C, et al. Lentiviral gene replacement therapy of retinas in a mouse model for Usher syndrome type 1B. Gene Ther. 2007;14:584-594.
42. Ouyang XM, Xia XJ, Verpy E, et al. Mutations in the alternatively spliced exons of USH1C cause non-syndromic recessive deafness. Hum Genet. 2002;111:26-30.