Disease-causing mutations in the CLRN1 gene alter normal CLRN1 protein trafficking to the plasma membrane

Molecular Vision

Volumn 15, Issue , 2009, Pages 1806-1818

  Isosomppi, Juha ^a,b   Västinsalo, Hanna ^a,b   Geller, Scott F ^c   Heon, Elise ^d   Flannery, John G ^c   Sankila, Eeva Marja ^a,e  

^a FOLKHÄLSAN INSTITUTE OF GENETICS   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

^e HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; CLARIN 1; CYCLOHEXIMIDE; GLYCOPEPTIDASE; GLYCOPROTEIN; HEMAGGLUTININ; HYBRID PROTEIN; LEUCINE; MUTANT PROTEIN; SUGAR; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CANADA; CELL MEMBRANE; CELL STRAIN; CELL STRAIN BHK 21; CELLULAR DISTRIBUTION; COHORT ANALYSIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA SEQUENCE; ENDOPLASMIC RETICULUM; FINLAND; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENETIC SCREENING; GENETIC TRANSFECTION; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; IN VITRO STUDY; MAJOR CLINICAL STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN STABILITY; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; USHER SYNDROME; USHER SYNDROME TYPE 3; WESTERN BLOTTING; WILD TYPE;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CELL MEMBRANE; CONSERVED SEQUENCE; DNA MUTATIONAL ANALYSIS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; PEPTIDES; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; TOMOGRAPHY, OPTICAL COHERENCE; TRANSFECTION; USHER SYNDROMES;

EID: 70149120714     PISSN: None     EISSN: 10900535     Source Type: Journal    
DOI: None     Document Type: Article

References (42)

1. Petit C. Usher syndrome: from genetics to pathogenesis. Annu Rev Genomics Hum Genet 2001; 2:271-97.
2. Ahmed ZM, Riazuddin S, Wilcox ER. The molecular genetics of Usher syndrome. Clin Genet 2003; 63:431-44.
3. 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.
4. Kremer H, van Wijk E, Märker T, Wolfrum U, Roepman R. Usher syndrome: molecular links of pathogenesis, proteins and pathways. Hum Mol Genet 2006; 15:R262-70.
5. Spandau UH, Rohrschneider K. Prevalence and geographical distribution of Usher syndrome in Germany. Graefes Arch Clin Exp Ophthalmol 2002; 240:495-8.
6. Cohen M, Bitner-Glindzicz M, Luxon L. The changing face of Usher syndrome: clinical implications. Int J Audiol 2007; 46:82-93.
7. Plantinga RF, Kleemola L, Huygen PL, Joensuu T, Sankila EM, Pennings RJ, Cremers CW. Serial audiometry and speech recognition findings in Finnish Usher syndrome type III patients. Audiol Neurootol 2005; 10:79-89.
8. Sadeghi M, Cohn ES, Kimberling WJ, Tranebjaerg L, Moller C. Audiological and vestibular features in affected subjects with USH3: a genotype/ phenotype correlation. Int J Audiol 2005; 44:307-16.
9. Pakarinen L, Tuppurainen K, Laippala P, Mantyjarvi M, Puhakka H. The ophthalmological course of Usher syndrome type III. Int Ophthalmol 1995; 19:307-11.
10. Plantinga RF, Pennings RJ, Huygen PL, Sankila EM, Tuppurainen K, Kleemola L, Cremers CW, Deutman AF. Visual impairment in Finnish Usher syndrome type III. Acta Ophthalmol Scand 2006; 84:36-41.
11. Herrera W, Aleman TS, Cideciyan AV, Roman AJ, Banin E, Ben-Yosef T, Gardner LM, Sumaroka A, Windsor EA, Schwartz SB, Stone EM, Liu XZ, Kimberling WJ, Jacobson SG. Retinal disease in Usher syndrome III caused by mutations in the clarin-1 gene. Invest Ophthalmol Vis Sci 2008; 49:2651-60.
12. Weil D, Blanchard S, Kaplan J, Guilford P, Gibson F, Walsh J, Mburu P, Varela A, Levilliers J, Weston MD, Kelley PM, Kimberling WJ, Levi-Acobas MWF, Larget-Piet D, Munnich A, Steel KP, Brown SDM, Petit C. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 1995; 374:60-1.
13. Bolz H, von Brederlow B, Ramírez A, Bryda EC, Kutsche K, Nothwang HG, Seeliger M. del C-Salcedó Cabrera M, Vila MC, Molina OP, Gal A, Kubisch C. Mutation of CDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat Genet 2001; 27:108-12.
14. Ahmed ZM, Riazuddin S, Bernstein SL, Ahmed Z, Khan S, Griffith AJ, Morell RJ, Friedman TB, Riazuddin S, Wilcox ER. Mutations of the protocadherin gene PCDH15 cause Usher syndrome type 1F. Am J Hum Genet 2001; 69:25-34.
15. Alagramam KN, Yuan H, Kuehn MH, Murcia CL, Wayne S, Srisailpathy CR, Lowry RB, Knaus R, Van Laer L, Bernier FP, Schwartz S, Lee C, Morton CC, Mullins RF, Ramesh A, Van Camp G, Hageman GS, Woychik RP, Smith RJ. Mutations in the novel protocadherin PCDH15 cause Usher syndrome type 1F. Hum Mol Genet 2001; 10:1709-18.
16. Verpy E, Leibovici M, Zwaenepoel I, Liu XZ, Gal A, Salem N, Mansour A, Blanchard S, Kobayashi I, Keats BJ, Slim R, Petit C. 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; 26:51-5.
17. Weil D, El-Amraoui A, Masmoudi S, Mustapha M, Kikkawa Y, Lainé S, Delmaghani S, Adato A, Nadifi S, Zina ZB, Hamel C, Gal A, Ayadi H, Yonekawa H, Petit C. 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; 12:463-71.
18. Ebermann I, Scholl HP, Charbel Issa P, Becirovic E, Lamprecht J, Jurklies B, Millán JM, Aller E, Mitter D, Bolz H. A novel gene for Usher syndrome type 2: mutations in the long isoform of whirlin are associated with retinitis pigmentosa and sensorineural hearing loss. Hum Genet 2007; 121:203-11.
19. Weston MD, Luijendijk MW, Humphrey KD, Moller C, Kimberling WJ. Mutations in the VLGR1 gene implicate G-protein signaling in the pathogenesis of Usher syndrome type II. Am J Hum Genet 2004; 74:357-66.
20. Eudy JD, Yao S, Weston MD, Ma-Edmonds M, Talmadge CB, Cheng JJ, Kimberling WJ, Sumegi J. Isolation of a gene encoding a novel member of the nuclear receptor superfamily from the critical region of Usher syndrome type IIa at 1q41. Genomics 1998; 50:382-4.
21. van Wijk E, Pennings RJ, te Brinke H, Claassen A, Yntema HG, Hoefsloot LH, Cremers FP, Cremers CW, Kremer H. Identification of 51 novel exons of the Usher syndrome type 2A (USH2A) gene that encode multiple conserved functional domains and that are mutated in patients with Usher syndrome type II. Am J Hum Genet 2004; 74:738-44.
22. Joensuu T, Hämäläinen R, Yuan B, Johnson C, Tegelberg S, Gasparini P, Zelante L, Pirvola U, Pakarinen L, Lehesjoki AE, de la Chapelle A, Sankila EM. Mutations in a novel gene with transmembrane domains underlie Usher syndrome type 3. Am J Hum Genet 2001; 69:673-84.
23. Adato A, Vreugde S, Joensuu T, Avidan N, Hamalainen R, Belenkiy O, Olender T, Bonne-Tamir B, Ben-Asher E, Espinos C, Millán JM, Lehesjoki AE, Flannery JG, Avraham KB, Pietrokovski S, Sankila EM, Beckmann JS, Lancet D. USH3A transcripts encode clarin-1, a four-transmembrane-domain protein with a possible role in sensory synapses. Eur J Hum Genet 2002; 10:339-50.
24. El-Amraoui A, Petit C. Usher I syndrome: unravelling the mechanisms that underlie the cohesion of the growing hair bundle in inner ear sensory cells. J Cell Sci 2005; 118:4593-603.
25. Reiners J, van Wijk E, Märker T, Zimmermann U, Jürgens K, te Brinke H, Overlack N, Roepman R, Knipper M, Kremer H, Wolfrum U. Scaffold protein harmonin (USH1C) provides molecular links between Usher syndrome type 1 and type 2. Hum Mol Genet 2005; 14:3933-43.
26. Adato A, Michel V, Kikkawa Y, Reiners J, Alagramam KN, Weil D, Yonekawa H, Wolfrum U, El-Amraoui A, Petit C. Interactions in the network of Usher syndrome type 1 proteins. Hum Mol Genet 2005; 14:347-56.
27. Maerker T, van Wijk E, Overlack N, Kersten FF, McGee J, Goldmann T, Sehn E, Roepman R, Walsh EJ, Kremer H, Wolfrum U. 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.
28. Tian G, Zhou Y, Hajkova D, Miyagi M, Dinculescu A, Hauswirth WW, Palczewski K, Geng R, Alagramam KN, Isosomppi J, Sankila EM, Flannery JG, Imanishi Y. Clarin-1, encoded by the Usher syndrome III causative gene, forms a membranous microdomain: possible role of clarin-1 in organizing the actin cytoskeleton. J Biol Chem 2009; 284:18980-93.
29. Fields RR, Zhou G, Huang D, Davis JR, Möller C, Jacobson SG, Kimberling WJ, Sumegi J. Usher syndrome type III: revised genomic structure of the USH3 gene and identification of novel mutations. Am J Hum Genet 2002; 71:607-17.
30. Geng R, Geller SF, Hayashi T, Ray CA, Reh TA, Bermingham-McDonogh O, Jones SM, Wright CG, Melki S, Imanishi Y, Palczewski K, Alagramam KN, Flannery JG. Usher syndrome IIIA gene clarin-1 is essential for hair cell function and associated neural activation. Hum Mol Genet 2009; 18:2748-60.
31. Zallocchi M, Meehan DT, Delimont D, Askew C, Garige S, Gratton MA, Rothermund-Franklin CA, Cosgrove D. Localization and expression of clarin-1, the Clrn1 gene product, in auditory hair cells and photoreceptors. Hear Res 2009; 255:109-20.
32. Ness SL, Ben-Yosef T, Bar-Lev A, Madeo AC, Brewer CC, Avraham KB, Kornreich R, Desnick RJ, Willner JP, Friedman TB, Griffith AJ. Genetic homogeneity and phenotypic variability among Ashkenazi Jews with Usher syndrome type III. J Med Genet 2003; 40:767-72.
33. Aller E, Jaijo T, Oltra S, Alió J, Galán F, Nájera C, Beneyto M, Millán JM. Mutation screening of USH3 gene (clarin-1) in Spanish patients with Usher syndrome: low prevalence and phenotypic variability. Clin Genet 2004; 66:525-9.
34. Ebermann I, Lopez I, Bitner-Glindzicz M, Brown C, Koenekoop RK, Bolz HJ. Deafblindness in French Canadians from Quebec: a predominant founder mutation in the USH1C gene provides the first genetic link with the Acadian population. Genome Biol 2007; 8:R47.
35. Stothard P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 2000; 28:1102.
36. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305:567-80.
37. Khajavi M, Inoue K, Lupski JR. Nonsense-mediated mRNA decay modulates clinical outcome of genetic disease. Eur J Hum Genet 2006; 14:1074-81.
38. Lee ES, Flannery JG. Transport of truncated rhodopsin and its effects on rod function and degeneration. Invest Ophthalmol Vis Sci 2007; 48:2868-76.
39. Green ES, Menz MD, LaVail MM, Flannery JG. Characterization of rhodopsin mis-sorting and constitutive activation in a transgenic rat model of retinitis pigmentosa. Invest Ophthalmol Vis Sci 2000; 41:1546-53.
40. Lin JH, Walter P, Yen TS. Endoplasmic reticulum stress in disease pathogenesis. Annu Rev Pathol 2008; 3:399-425.
41. Sanders CR, Myers JK. Disease-related misassembly of membrane proteins. Annu Rev Biophys Biomol Struct 2004; 33:25-51.
42. Aarnisalo AA, Pietola L, Joensuu J, Isosomppi J, Aarnisalo P, Dinculescu A, Lewin AS, Flannery J, Hauswirth WW, Sankila EM, Jero J. Anti-clarin-1 AAV-delivered ribozyme induced apoptosis in the mouse cochlea. Hear Res 2007; 230:9-16.