Biochemical characterization of native usher protein complexes from a vesicular subfraction of tracheal epithelial cells

Biochemistry

Volumn 49, Issue 6, 2010, Pages 1236-1247

  Zallocchi, Marisa ^a   Sisson, Joseph H ^b   Cosgrove, Dominic ^a  

^a BOYS TOWN NATIONAL RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ANALYSIS; BIOCHEMICAL CHARACTERIZATION; EPITHELIAL CELLS; HAIR CELLS; IMMUNO-ISOLATION; IN-VIVO; ISOFORMS; PROTEIN COMPLEXES; SEDIMENTATION COEFFICIENTS; SUCROSE GRADIENTS; TEM ANALYSIS; USHER SYNDROMES;

ASSOCIATION REACTIONS; CELLS; COMPLEXATION; GENE EXPRESSION; SUGAR (SUCROSE);

PROTEINS;

ANTIBODY; ARYLBUTYRIC ACID DERIVATIVE; BIOLOGICAL MARKER; CADHERIN; CADHERIN 23; CELL ADHESION MOLECULE; CLARIN 1; G PROTEIN COUPLED RECEPTOR; HARMONIN A; HARMONIN B; HARMONIN C; MEMBRANE PROTEIN; MYOSIN VIIA; PROTEIN S6; PROTOCADHERIN 15; RAB PROTEIN; SCAFFOLD PROTEIN; SUCROSE; UNCLASSIFIED DRUG; USHERIN B; VERY LARGE G PROTEIN COUPLED RECEPTOR 1; WHIRLIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COW; ELECTRON MICROSCOPY; EPITHELIUM CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SMALL RIBOSOMAL SUBUNIT; SUCROSE GRADIENT; TRACHEA MUCOSA; TRANSPORT VESICLE; USHER SYNDROME; WESTERN BLOTTING;

ANIMALS; CADHERINS; CARRIER PROTEINS; CATTLE; CELL FRACTIONATION; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MEMBRANE PROTEINS; MICE; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; PROTEIN ISOFORMS; PROTEIN PRECURSORS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; RECOMBINANT PROTEINS; RESPIRATORY MUCOSA; TRACHEA; TRANSPORT VESICLES;

BOVINAE;

EID: 76749156791     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi9020617     Document Type: Article

References (61)

1. Hallgren, B. (1959) Retinitis pigmentosa combined with congenital deafness; with vestibulo-cerebellar ataxia and neural abnormality in a proportion of cases. Acta Psychiatr. Scand., Suppl. 138, 1-100.
2. Nuutila, A. (1970) Dystrophia retinae pigmentosa-dysacusis syndrome (DRD): a study of the Usher or Hallgren syndrome. J. Genet. Hum. 18 (1), 57-88.
3. Boughman, J. A., Vernon, M., and Shaver, K. A. (1993) Usher syndrome: definition and estimate of prevalence from two high risk populations. J. Chron. Dis. 36, 595-603.
4. Ahmed, Z. M., Riazuddin, S., Riazuddin, S., and Wilcox, E. R. (2003) Themolecular genetics of Usher syndrome. Clin.Genet. 63 (6), 431-444.
5. Reiners, J.,Nagel-Wolfrum,K., Jürgens, K.,Märker, T., andWolfrum, U. (2006) 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. 83 (1), 97-119.
6. Weil, D., Blanchard, S., Kaplan, J., Guilford, P., Gibson, F., Walsh, J., Mburu, P., Varela, A., Levilliers, J., and Weston, M. D. (1995) Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 374 (6517), 60-61.
7. Ahmed, Z. M., Riazuddin, S., Bernstein, S. L., Ahmed, Z., Khan, S., Griffith, A. J., Morell, R. J., Friedman, T. B., Riazuddin, S., and Wilcox, E. R. (2001) Mutations of the protocadherin gene PCDH15 cause Usher syndrome type 1F. Am. J. Hum. Genet. 69 (1), 25-34.
8. Alagramam, K. N., Yuan, H., Kuehn, M. H., Murcia, C. L., Wayne, S., Srisailpathy, C. R., Lowry,R. B., Knaus, R., Van Laer, L., Bernier, F. P., Schwartz, S., Lee, C., Morton, C. C., Mullins, R. F., Ramesh, A., Van Camp, G., Hageman, G. S., Woychik, R. P., and Smith, R. J. (2001) Mutations in the novel protocadherin PCDH15 cause Usher syndrome type 1F. Hum. Mol. Genet. 10 (16), 1709-1718.
9. Bitner-Glindzicz, M., Lindley, K. J., Rutland, P., Blaydon, D., Smith, V. V., Milla, P. J., Hussain, K., Furth-Lavi, J., Cosgrove, K. E., Shepherd, R. M., Barnes, P. D., O'Brien, R. E., Farndon, P. A., Sowden, J., Liu, X. Z., Scanlan, M. J., Malcolm, S., Dunne, M. J., Aynsley-Green, A., and Glaser, B. (2000) A recessive contiguous gene deletion causing infantile hyperinsulinism, enteropathy and deafness identifies the Usher type 1C gene. Nat. Genet. 26 (1), 6-7.
10. Verpy, E., Leibovici, M., Zwaenepoel, I., Liu, X. Z., Gal, A., Salem, N., Mansour, A., Blanchard, S., Kobayashi, I., Keats, B. J., Slim, R., and Petit, C. (2000) A defect in harmonin, a PDZ domain-containing protein expressed in the inner ear sensory hair cells, underlies Usher syndrome type 1C. Nat. Genet. 26 (1), 51-55.
11. Weil, D., El-Amraoui, A., Masmoudi, S., Mustapha, M., Kikkawa, Y., Lainé, S., Delmaghani, S., Adato, A., Nadifi, S., Zina, Z. B., Hamel, C., Gal, A., Ayadi, H., Yonekawa, H., and Petit, C. (2003) Usher syndrome type IG(USH1G) is caused by mutations in the gene encoding SANS, a protein that associates with the USH1C protein, harmonin. Hum. Mol. Genet. 12 (5), 463-471.
12. Bork, J. M., Peters, L. M., Riazuddin, S., Bernstein, S. L., Ahmed, Z. M., Ness, S. L., Polomeno, R., Ramesh, A., Schloss, M., Srisailpathy, C. R., Wayne, S., Bellman, S., Desmukh, D., Ahmed, Z., Khan, S. N., Kaloustian,V.M.,Li,X.C.,Lalwani,A.,Riazuddin, S.,Bitner-Glindzicz, M., Nance, W. E., Liu, X. Z.,Wistow, G., Smith, R. J., Griffith, A. J., Wilcox, E. R., Friedman, T. B., andMorell, R. J. (2001) Usher syndrome 1D and nonsyndromic autosomal recessive deafness DFNB12 are caused by allelic mutations of the novel cadherin-like gene CDH23. Am. J. Hum. Genet. 68 (1), 26-37.
13. Bolz, H., von Brederlow, B., Ramírez, A., Bryda, E. C., Kutsche, K., Nothwang, H. G., Seeliger, M., del C-Salcedó Cabrera, M., Vila, M. C., Molina, O. P., Gal, A., and Kubisch, C. (2001) Mutation of CDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat. Genet. 27 (1), 108-112.
14. Sankila, E. M., Pakarinen, L., Kääriäinen, H., Aittomäki, K., Karjalainen, S., Sistonen, P., and de la Chapelle, A. (1995) Assignment of an Usher syndrome type III (USH3) gene to chromosome 3q. Hum. Mol. Genet. 4 (1), 93-98.
15. Ebermann, I., Scholl, H. P., Charbel Issa, P., Becirovic, E., Lamprecht, J., Jurklies, B., Millán, J. M., Aller, E., Mitter, D., and Bolz, H. (2007) 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. 121 (2), 203-211.
16. Eudy, J. D., Weston, M. D., Yao, S., Hoover, D. M., Rehm, H. L., Ma-Edmonds, M., Yan, D., Ahmad, I., Cheng, J. J., Ayuso, C., Cremers, C., Davenport, S., Moller, C., Talmadge, C. B., Beisel, K. W., Tamayo, M., Morton, C. C., Swaroop, A., Kimberling, W. J., and Sumegi, J. (1998) Mutation of a gene encoding a protein with extracellular matrix motifs in Usher syndrome type IIa. Science 280 (5370), 1753-1757.
17. van Wijk, E., Pennings, R. J., te Brinke, H., Claassen, A., Yntema, H. G., Hoefsloot, L. H., Cremers, F. P., Cremers, C. W., and Kremer, H. (2004) 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. 74 (4), 738-744.
18. Petit, C. (2001) Usher syndrome: from genetics to pathogenesis. Annu. Rev. Genomics Hum. Genet. 2, 271-297.
19. Kremer, H., van Wijk, E., Märker, T., Wolfrum, U., and Roepman, R. (2006) Usher syndrome: molecular links of pathogenesis, proteins and pathways. Hum. Mol. Genet. 15 (2), R262-R270.
20. Hasson, T. (1997) Unconventional myosins, the basis for deafness in mouse and man. Am. J. Hum. Genet. 61 (4), 801-805.
21. Reiners, J., van Wijk, E.,Märker, T., Zimmermann, U., Jürgens, K., te Brinke, H., Overlack, N., Roepman, R., Knipper, M., Kremer, H., and Wolfrum, U. (2005) Scaffold protein harmonin (USH1C) provides molecular links between Usher syndrome type 1 and type 2. Hum. Mol. Genet. 14 (24), 3933-3943.
22. Kalay, E., de Brouwer,A. P., Caylan, R., Nabuurs, S. B., Wollnik, B., Karaguzel, A., Heister, J. G., Erdol, H., Cremers, F. P., Cremers, C. W., Brunner, H. G., and Kremer, H. (2005) A novel D458V mutation in the SANS PDZ binding motif causes atypical Usher syndrome. J. Mol. Med. 83 (12), 1025-1032.
23. Delprat, B., Michel, V., Goodyear, R., Yamasaki, Y., Michalski, N., El-Amraoui, A., Perfettini, I., Legrain, P., Richardson, G., Hardelin, J. P., and Petit, C. (2005) Myosin XVa and whirlin, two deafness gene products required for hair bundle growth, are located at the stereocilia tips and interact directly. Hum. Mol. Genet. 14 (3), 401-410.
24. Reiners, J., and Wolfrum, U. (2006) Molecular analysis of the supramolecular Usher protein complex in the retina. Harmonin as the key protein of the Usher syndrome. Adv. Exp. Med. Biol. 572, 349-353.
25. van Wijk,E., van derZwaag, B., Peters, T.,Zimmermann, U.,TeBrinke, H., Kersten, F. F., Märker, T., Aller, E., Hoefsloot, L. H., Cremers, C. W., Cremers, F. P., Wolfrum, U., Knipper, M., Roepman, R., and Kremer, H. (2006) 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. 15 (5), 751-765.
26. Overlack, N., Maerker, T., Latz, M., Nagel-Wolfrum, K., and Wolfrum, U. (2008) SANS (USH1G) expression in developing and mature mammalian retina. Vision Res. 48 (3), 400-412.
27. Siemens, J., Kazmierczak, P., Reynolds, A., Sticker, M., Littlewood-Evans, A., and Müller, U. (2002) The Usher syndrome proteins cadherin 23 and harmonin form a complex by means of PDZ-domain interactions. Proc. Natl. Acad. Sci. U.S.A. 99 (23), 14946-14951.
28. Müller, U. (2008) Cadherins and mechanotransduction by hair cells. Curr. Opin. Cell. Biol. 20 (5), 557-566.
29. Maerker, T., van Wijk, E., Overlack, N., Kersten, F. F., McGee, J., Goldmann, T., Sehn, E., Roepman, R., Walsh, E. J., Kremer, H., and Wolfrum, U. (2008) A novel Usher protein network at the periciliary reloading point between molecular transport machineries in vertebrate photoreceptor cells. Hum. Mol. Genet. 17 (1), 71-86.
30. Ahmed, Z.M.,Riazuddin, S., Aye, S.,Ali,R. A.,Venselaar, H.,Anwar, S., Belyantseva, P. P., Qasim, M., Riazuddin, S., and Friedman, T. B. (2008) Gene structure and mutant alleles of PCDH15: nonsyndromic deafness DFNB23 and type 1 Usher syndrome. Hum. Genet. 124 (3), 215-223.
31. Pearsall, N., Bhattacharya, G., Wisecarver, J., Adams, J., Cosgrove, D., and Kimberling, W. (2002) Usherin expression is highly conserved in mouse and human tissues. Hear. Res. 174 (1-2), 55-63.
32. Bhattacharya, G., Miller, C., Kimberling, W. J., Jablonski, M. M., and Cosgrove, D. (2002) Localization and expression of usherin: a novel basement membrane protein defective in people with Usher's syndrome type IIa. Hear. Res. 163 (1-2), 1-11.
33. Bhattacharya, G., Kalluri, R., Orten, D. J., Kimberling, W. J., and Cosgrove,D. (2004)A domain-specific usherin/collagen IV interaction may be required for stable integration into the basement membrane superstructure. J. Cell. Sci. 117 (Part 2), 233-242.
34. Bhattacharya, G., and Cosgrove, D. (2005) Evidence for functional importance of usherin/fibronectin interactions in retinal basement membranes. Biochemistry 44 (34), 11518-11524.
35. McMillan, D. R., Kayes-Wandover, K. M., Richardson, J. A., and White, P. C. (2002) Very large G protein-coupled receptor-1, the largest known cell surface protein, is highly expressed in the developing central nervous system. J. Biol. Chem. 277 (1), 785-792.
36. Adato, A., Vreugde, S., Joensuu, T., Avidan, N., Hamalainen, R., Belenkiy, O., Olender, T., Bonne-Tamir, B., Ben-Asher, E., Espinos, C., Millán, J. M., Lehesjoki, A. E., Flannery, J. G., Avraham, K. B., Pietrokovski, S., Sankila, E. M., Beckmann, J. S., and Lancet, D. (2002) USH3A transcripts encode clarin-1, a four-transmembrane-domain protein with a possible role in sensory synapses. Eur. J. Hum. Genet. 10 (6), 339-350.
37. Zallocchi, M., Meehan, D. T., Delimont, D., Askew, C., Garige, S., Gratton, M. A., Rothermund-Franklin, C. A., and Cosgrove, D. (2009) Localization and expression of clarin-1, the Clrn1 gene product, in auditory hair cells and photoreceptors, Hear. Res. (Epub ahead of print).
38. Johnson, K. R., Gagnon, L. H., Webb, L. S., Peters, L. L., Hawes, N. L., Chang, B., and Zheng, Q. Y. (2003) Mouse models of USH1C and DFNB18: phenotypic and molecular analyses of two new spontaneous mutations of the Ush1c gene. Hum. Mol. Genet. 12 (23), 3075-3086.
39. Siemens, J., Lillo, C., Dumont, R. A., Reynolds, A., Williams, D. S., Gillespie, P. G., and Müller, U. (2004) Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428 (6986), 950-955.
40. Boëda, B., El-Amraoui, A., Bahloul, A., Goodyear, R., Daviet, L., Blanchard, S., Perfettini, I., Fath, K. R., Shorte, S., Reiners, J., Houdusse, A., Legrain, P., Wolfrum, U., Richardson, G., and Petit, C. (2002) Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle. EMBO J. 21 (24), 6689-6699.
41. Reiners, J., Reidel, B., El-Amraoui, A., Boëda, B., Huber, I., Petit, C., and Wolfrum, U. (2003) Differential distribution of harmonin isoforms and their possible role in Usher-1 protein complexes in mammalian photoreceptor cells. Invest. Ophthalmol. Visual Sci. 44 (11), 5006-5015.
42. Reiners, J., Märker, T., Jürgens, K., Reidel, B., and Wolfrum, U. (2005) Photoreceptor expression of the Usher syndrome type 1 protein protocadherin 15 (USH1F) and its interaction with the scaffold protein harmonin (USH1C). Mol. Vision 11, 347-355.
43. Lillo, C., Kitamoto, J., and Williams, D. S. (2006) Roles and interactions of Usher 1 proteins in the outer retina. Adv. Exp. Med. Biol. 572, 341-348.
44. Adato, A., Lefèvre, G., Delprat, B., Michel, V., Michalski, N., Chardenoux, S., Weil, D., El-Amraoui, A., and Petit, C. (2005) Usherin, the defective protein in Usher syndrome type IIA, is likely to be a component of interstereocilia ankle links in the inner ear sensory cells. Hum. Mol. Genet. 14 (24), 3921-3932.
45. Adato, A., Michel, V., Kikkawa, Y., Reiners, J., Alagramam, K. N., Weil, D., Yonekawa, H., Wolfrum, U., El-Amraoui, A., and Petit, C. (2005) Interactions in the network of Usher syndrome type 1 proteins. Hum. Mol. Genet. 14 (3), 347-356.
46. El-Amraoui, A., and Petit, C. (2005) Usher I syndrome: unraveling the mechanisms that underlie the cohesion of the growing hair bundle in inner ear sensory cells. J. Cell Sci. 118 (Part 20), 4593-4603.
47. Senften, M., Schwander, M., Kazmierczak, P., Lillo, C., Shin, J. B., Hasson, T., Géléoc, G. S., Gillespie, P. G., Williams, D., Holt, J. R., and Müller, U. (2006) Physical and functional interaction between protocadherin 15 and myosin VIIa in mechanosensory hair cells. J. Neurosci. 26 (7), 2060-2071.
48. Kazmierczak, P., Sakaguchi, H., Tokita, J., Wilson-Kubalek, E. M., Milligan, R. A., Müller, U., and Kachar, B. (2007) Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 449 (7158), 87-91.
49. Wolfrum, U., Liu, X., Schmitt, A., Udovichenko, I. P., and Williams, D. S. (1998) Myosin VIIa as a common component of cilia and microvilli. Cell. Motil. Cytoskeleton 40 (3), 261-271.
50. Soni, L. E., Warren, C. M., Bucci, C., Orten, D. J., and Hasson, T. (2005) The unconventional myosin-VIIa associates with lysosomes. Cell. Motil. Cytoskeleton 62 (1), 13-26.
51. McGee, J., Goodyear, R. J., McMillan, D. R., Stauffer, E. A., Holt, J. R., Locke, K. G., Birch, D. G., Legan, P. K., White, P. C., Walsh, E. J., and Richardson, G. P. (2006) The very large G-protein-coupled receptor VLGR1: a component of the ankle link complex required for the normal development of auditory hair bundles. J. Neurosci. 26 (24), 6543-6553.
52. Deretic, D., and Papermaster, D. S. (1991) Polarized sorting of rhodopsin on post-Golgi membranes in frog retinal photoreceptor cells. J. Cell. Biol. 113 (6), 1281-1293.
53. Papermaster, D. S., and Dreyer, W. J. (1974) Rhodopsin content in the outer segment membranes of bovine and frog retinal rods. Biochemistry 13 (11), 2438-2444.
54. Napoli, I., Mercaldo, V., Boyl, P. P., Eleuteri, B., Zalfa, F., De Rubeis, S., Di Marino, D., Mohr, E., Massimi, M., Falconi, M., Witke, W., Costa-Mattioli, M., Sonenberg, N., Achsel, T., and Bagni, C. (2008) The fragileXsyndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 134 (6), 1042-1054.
55. Lagziel, A., Ahmed, Z. M., Schultz, J. M., Morell, R. J., Belyantseva, I. A., and Friedman, T. B. (2005) Spatiotemporal pattern and isoforms of cadherin 23 in wild type and waltzer mice during inner ear hair cell development. Dev. Biol. 280 (2), 295-306.
56. Tsarouhas, V., Senti, K., Jayaram, S., Tiklova, K., Hemphala, J., Adler, J., and Samakovlis, C. (2007) Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila. Dev. Cell 13, 214-225.
57. Inden, M., Kitamura, Y., Takeuchi, H., Yanagida, T., Takata, K., Kobayashi, Y., Taniguchi, T., Yoshimoto, K., Kaneko, M., Okuma, Y., Taira, T., Ariga, H., and Shimohama, S. (2007) Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. J. Neurochem. 101 (6), 1491-1504.
58. Li, J., Wang, J. J., Yu, Q., Wang, M., and Zhang, S. X. (2009) Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy. FEBS Lett. 583 (9), 1521-1527.
59. Grillet, N., Xiong, W., Reynolds, A., Kazmierczak, P., Sato, T., Lillo, C., Dumont, R. A., Hintermann, E., Sczaniecka, A., Schwander, M., Williams, D., Kachar, B., Gillespie, P. G., and Müller, U. (2009) Harmonin mutations cause mechanotransduction defects in cochlear hair cells. Neuron 62 (3), 375-387.
60. Nieuwenhuysen, P., and Clauwaert, J. (1981) Physicochemical characterization of ribosomal particles from the eukaryote Artemia. J. Biol. Chem. 256 (18), 9626-9632.
61. Marriq, C., Rolland, M., and Lissitzky, S. (1977) Polypeptide chains of 19-S thyroglobulin from several mammalian species and of porcine 27-S iodoprotein. Eur. J. Biochem. 79 (1), 143-149.