Direct interaction of the Usher syndrome 1G protein SANS and myomegalin in the retina

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 10, 2011, Pages 1883-1892

  Overlack, Nora ^a   Kilic, Dilek ^a,e   Bauß, Katharina ^a   Märker, Tina ^a,f   Kremer, Hannie ^b,c,d   van Wijk, Erwin ^b,c,d   Wolfrum, Uwe ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d RADBOUD UNIVERSITY   (Netherlands)

^e SABANCI UNIVERSITY   (Turkey)

^f LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

Author keywords

Intracellular transport; Microtubule based transport; Phosphodiesterase 4D interacting protein (PDE4DIP); Photoreceptor cell function; Sensorineuronal degeneration

Indexed keywords

COMPLEMENTARY DNA; MYOMEGALIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; USHER SYNDROME 1G PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; ELECTRON MICROSCOPY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MACACA; MICROTUBULE; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RETINA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CATTLE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; MACACA MULATTA; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MUSCLE PROTEINS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PHOTORECEPTOR CELLS, VERTEBRATE; PROTEIN BINDING; RETINA; YEASTS;

MAMMALIA;

EID: 81155161016     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.05.015     Document Type: Article

References (37)

1. Reiners J., Nagel-Wolfrum K., Jürgens K., Märker 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.
2. Ebermann I., Wilke R., Lauhoff T., Lubben D., Zrenner E., Bolz H.J. Two truncating USH3A mutations, including one novel, in a German family with Usher syndrome. Mol. Vis. 2007, 13:1539-1547.
3. Davenport S.L.H., Omenn G.S. The Heterogeneity of Usher Syndrome 1977.
4. Petit C. Usher syndrome: from genetics to pathogenesis. Annu. Rev. Genomics Hum. Genet. 2001, 2:271-297.
5. Ahmed Z.M., Morell R.J., Riazuddin S., Gropman A., Shaukat S., Ahmad M.M., Mohiddin S.A., Fananapazir L., Caruso R.C., Husnain T., Khan S.N., Riazuddin S., Griffith A.J., Friedman T.B., Wilcox E.R. Mutations of MYO6 are associated with recessive deafness, DFNB37. Am. J. Hum. Genet. 2003, 72:1315-1322.
6. Kremer H., van W.E., Marker T., Wolfrum U., Roepman R. Usher syndrome: molecular links of pathogenesis, proteins and pathways. Hum. Mol. Genet. 2006, 15(Spec No 2):R262-R270.
7. Wolfrum U. Protein networks related to the Usher syndrome gain insights in the molecular basis of the disease. Usher Syndrome: Pathogenesis, Diagnosis and Therapy 2011, 1-23. Nova Science Publishers. A. Satpal (Ed.).
8. Weil D., El Amraoui A., Masmoudi S., Mustapha M., Kikkawa Y., Laine S., Delmaghani S., Adato A., Nadifi S., Zina Z.B., 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, 12:463-471.
9. 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, 118:4593-4603.
10. Muller U. Cadherins and mechanotransduction by hair cells. Curr. Opin. Cell Biol. 2008, 20:557-566.
11. 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., Muller U. Harmonin mutations cause mechanotransduction defects in cochlear hair cells. Neuron 2009, 62:375-387.
12. Schwander M., Kachar B., Muller U. Review series: the cell biology of hearing. J. Cell Biol. 2010, 190:9-20.
13. Maerker T., van Wijk E., Overlack N., Kersten F.F., McGee J., Goldmann T., Sehn E., Roepman R., Walsh E.J., 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.
14. Overlack N., Maerker T., Latz M., Nagel-Wolfrum K., Wolfrum U. SANS (USH1G) expression in developing and mature mammalian retina. Vision Res. 2008, 48:400-412.
15. van Wijk E., Kersten F.F., Kartono A., Mans D.A., Brandwijk K., Letteboer S.J., Peters T.A., Marker T., Yan X., Cremers C.W., Cremers F.P., Wolfrum U., Roepman R., Kremer H. Usher syndrome and Leber congenital amaurosis are molecularly linked via a novel isoform of the centrosomal ninein-like protein. Hum. Mol. Genet. 2009, 18:51-64.
16. Yang J., Liu X., Zhao Y., Adamian M., Pawlyk B., Sun X., McMillan D.R., Liberman M.C., Li T. Ablation of whirlin long isoform disrupts the USH2 protein complex and causes vision and hearing loss. PLoS. Genet. 2010, 6:e1000955.
17. Zou J., Luo L., Shen Z., Chiodo V.A., Ambati B.K., Hauswirth W.W., Yang J. Whirlin replacement restores the formation of the USH2 protein complex in whirlin knockout photoreceptors. Invest Ophthalmol. Vis. Sci. 2011, 52:2343-2351.
18. Roepman R., Wolfrum U. Protein networks and complexes in photoreceptor cilia. Subcell. Biochem. 2007, 43:209-235.
19. Adato A., Lefevre G., Delprat B., Michel V., Michalski N., Chardenoux S., Weil D., El Amraoui A., Petit C. 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. 2005, 14:3921-3932.
20. Caberlotto E., Michel V., Foucher I., Bahloul A., Goodyear R.J., Pepermans E., Michalski N., Perfettini I., Alegria-Prevot O., Chardenoux S., Do C.M., Hardelin J.P., Richardson G.P., Avan P., Weil D., Petit C. Usher type 1G protein sans is a critical component of the tip-link complex, a structure controlling actin polymerization in stereocilia. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5825-5830.
21. Zallocchi M., Sisson J.H., Cosgrove D. Biochemical characterization of native Usher protein complexes from a vesicular subfraction of tracheal epithelial cells. Biochemistry 2010, 49:1236-1247.
22. Yan J., Pan L., Chen X., Wu L., Zhang M. The structure of the harmonin/sans complex reveals an unexpected interaction mode of the two Usher syndrome proteins. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4040-4045.
23. Wu L., Pan L., Wei Z., Zhang M. Structure of MyTH4-FERM domains in myosin VIIa tail bound to cargo. Science 2011, 331:757-760.
24. Verde I., Pahlke G., Salanova M., Zhang G., Wang S., Coletti D., Onuffer J., Jin S.L., Conti M. Myomegalin is a novel protein of the golgi/centrosome that interacts with a cyclic nucleotide phosphodiesterase. J. Biol. Chem. 2001, 276:11189-11198.
25. Gießl A., Trojan P., Pulvermüller A., Wolfrum U. Centrins, potential regulators of transducin translocation in photoreceptor cells. Cell Bilogy and Related Disease of the Outer Retina 2004, 195-222. World Scientific Publishing Company Pte Ltd, Singapore. D.S. Williams (Ed.).
26. Trojan P., Rausch S., Giessl A., Klemm C., Krause E., Pulvermuller A., Wolfrum U. Light-dependent CK2-mediated phosphorylation of centrins regulates complex formation with visual G-protein. Biochim. Biophys. Acta 2008, 1783:1248-1260.
27. Wolfrum U. Centrin- and α-actinin-like immunoreactivity in the ciliary rootlets of insect sensilla. Cell Tissue Res. 1991, 266:231-238.
28. Sedmak T., Sehn E., Wolfrum U. Immunoelectron microscopy of vesicle transport to the primary cilium of photoreceptor cells. Methods Cell Biol. 2009, 94:259-272.
29. Hatzfeld M. The armadillo family of structural proteins. Int. Rev. Cytol. 1999, 186:179-224.
30. Burkhard P., Stetefeld J., Strelkov S.V. Coiled coils: a highly versatile protein folding motif. Trends Cell Biol. 2001, 11:82-88.
31. Mason J.M., Arndt K.M. Coiled coil domains: stability, specificity, and biological implications. ChemBioChem 2004, 5:170-176.
32. Faul C., Dhume A., Schecter A.D., Mundel P. Protein kinase A, Ca2+/calmodulin-dependent kinase II, and calcineurin regulate the intracellular trafficking of myopodin between the Z-disc and the nucleus of cardiac myocytes. Mol. Cell. Biol. 2007, 27:8215-8227.
33. Conti M., Richter W., Mehats C., Livera G., Park J.Y., Jin C. Cyclic AMP-specific PDE4 phosphodiesterases as critical components of cyclic AMP signaling. J. Biol. Chem. 2003, 278:5493-5496.
34. Tasken K.A., Collas P., Kemmner W.A., Witczak O., Conti M., Tasken K. Phosphodiesterase 4D and protein kinase a type II constitute a signaling unit in the centrosomal area. J. Biol. Chem. 2001, 276:21999-22002.
35. Rivero S., Cardenas J., Bornens M., Rios R.M. Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J. 2009, 28:1016-1028.
36. Tai A.W., Chuang J.Z., Bode C., Wolfrum U., Sung C.H. Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1. Cell 1999, 97:877-887.
37. Papermaster D.S. The birth and death of photoreceptors: the Friedenwald Lecture. Invest. Ophthalmol. Vis. Sci. 2002, 43:1300-1309.