XIRP2, an actin-binding protein essential for inner ear hair-cell stereocilia

Cell Reports

Volumn 10, Issue 11, 2015, Pages 1811-1818

  Scheffer, Déborah I ^a,b   Zhang, Duan Sun ^a   Shen, Jun ^a,c   Indzhykulian, Artur ^a   Karavitaki, K Domenica ^a   Xu, Yichao Joy ^a   Wang, Qinchuan ^d   Lin, Jim Jung Ching ^d   Chen, Zheng Yi ^b   Corey, David P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; UNCLASSIFIED DRUG; XIRP2 PROTEIN; DNA BINDING PROTEIN; ISOPROTEIN; LIM PROTEIN; NUCLEAR PROTEIN; XIRP2 PROTEIN, MOUSE;

ACTIN FILAMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DEGENERATION; GENE; GENE EXPRESSION; HAIR CELL; INNER EAR; MECHANOTRANSDUCTION; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEREOCILIUM; ULTRASTRUCTURE; UTRICLE; XIRP2 GENE; ANIMAL; COCHLEAR HAIR CELL; GENETICS; METABOLISM; PROTEIN TRANSPORT;

MUS;

ACTIN CYTOSKELETON; ANIMALS; DNA-BINDING PROTEINS; HAIR CELLS, AUDITORY; LIM DOMAIN PROTEINS; MICE; NUCLEAR PROTEINS; PROTEIN ISOFORMS; PROTEIN TRANSPORT; STEREOCILIA;

EID: 84925674615     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.02.042     Document Type: Article

References (34)

1. Avenarius M.R., Saylor K.W., Lundeberg M.R., Wilmarth P.A., Shin J.B., Spinelli K.J., Pagana J.M., Andrade L., Kachar B., Choi D., et al. Correlation of actin crosslinker and capper expression levels with stereocilia growth phases. Mol. Cell. Proteomics 2014, 13:606-620.
2. Belyantseva I.A., Perrin B.J., Sonnemann K.J., Zhu M., Stepanyan R., McGee J., Frolenkov G.I., Walsh E.J., Friderici K.H., Friedman T.B., Ervasti J.M. Gamma-actin is required for cytoskeletal maintenance but not development. Proc. Natl. Acad. Sci. USA 2009, 106:9703-9708.
3. Cherepanova O., Orlova A., Galkin V.E., van der Ven P.F., Fürst D.O., Jin J.P., Egelman E.H. Xin-repeats and nebulin-like repeats bind to F-actin in a similar manner. J.Mol. Biol. 2006, 356:714-723.
4. Choi S., Gustafson-Wagner E.A., Wang Q., Harlan S.M., Sinn H.W., Lin J.L., Lin J.J. The intercalated disk protein, mXinalpha, is capable of interacting with beta-catenin and bundling actin filaments [corrected]. J.Biol. Chem. 2007, 282:36024-36036.
5. Drenckhahn D., Engel K., Höfer D., Merte C., Tilney L., Tilney M. Three different actin filament assemblies occur in every hair cell: each contains a specific actin crosslinking protein. J.Cell Biol. 1991, 112:641-651.
6. Duka A., Schwartz F., Duka I., Johns C., Melista E., Gavras I., Gavras H. A novel gene (Cmya3) induced in the heart by angiotensin II-dependent but not salt-dependent hypertension in mice. Am. J. Hypertens. 2006, 19:275-281.
7. Fasquelle L., Scott H.S., Lenoir M., Wang J., Rebillard G., Gaboyard S., Venteo S., François F., Mausset-Bonnefont A.L., Antonarakis S.E., et al. Tmprss3, a transmembrane serine protease deficient in human DFNB8/10 deafness, is critical for cochlear hair cell survival at the onset of hearing. J.Biol. Chem. 2011, 286:17383-17397.
8. Flock A., Bretscher A., Weber K. Immunohistochemical localization of several cytoskeletal proteins in inner ear sensory and supporting cells. Hear. Res. 1982, 7:75-89.
9. Fukushima K., Kasai N., Ueki Y., Nishizaki K., Sugata K., Hirakawa S., Masuda A., Gunduz M., Ninomiya Y., Masuda Y., et al. A gene for fluctuating, progressive autosomal dominant nonsyndromic hearing loss, DFNA16, maps to chromosome 2q23-24.3. Am. J. Hum. Genet. 1999, 65:141-150.
10. Gale J.E., Marcotti W., Kennedy H.J., Kros C.J., Richardson G.P. FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J.Neurosci. 2001, 21:7013-7025.
11. Gillespie P.G., Hudspeth A.J. High-purity isolation of bullfrog hair bundles and subcellular and topological localization of constituent proteins. J.Cell Biol. 1991, 112:625-640.
12. Hoffmann C., Moreau F., Moes M., Luthold C., Dieterle M., Goretti E., Neumann K., Steinmetz A., Thomas C. Human muscle LIM protein dimerizes along the actin cytoskeleton and cross-links actin filaments. Mol. Cell. Biol. 2014, 34:3053-3065.
13. Huang H.T., Brand O.M., Mathew M., Ignatiou C., Ewen E.P., McCalmon S.A., Naya F.J. Myomaxin is a novel transcriptional target of MEF2A that encodes a Xin-related alpha-actinin-interacting protein. J.Biol. Chem. 2006, 281:39370-39379.
14. Indzhykulian A.A., Stepanyan R., Nelina A., Spinelli K.J., Ahmed Z.M., Belyantseva I.A., Friedman T.B., Barr-Gillespie P.G., Frolenkov G.I. Molecular remodeling of tip links underlies mechanosensory regeneration in auditory hair cells. PLoS Biol. 2013, 11:e1001583.
15. Jagger D.J., Nickel R., Forge A. Gap junctional coupling is essential for epithelial repair in the avian cochlea. J.Neurosci. 2014, 34:15851-15860.
16. Jung-Ching Lin J., Gustafson-Wagner E.A., Sinn H.W., Choi S., Jaacks S.M., Wang D.Z., Evans S., Li-Chun Lin J. Structure, expression, and function of a novel intercalated disc protein, Xin. J.Med. Sci. 2005, 25:215-222.
17. Karavitaki K.D., Corey D.P. Sliding adhesion confers coherent motion to hair cell stereocilia and parallel gating to transduction channels. J.Neurosci. 2010, 30:9051-9063.
18. Kasai N., Fukushima K., Ueki Y., Prasad S., Nosakowski J., Sugata K., Sugata A., Nishizaki K., Meyer N.C., Smith R.J. Genomic structures of SCN2A and SCN3A-candidate genes for deafness at the DFNA16 locus. Gene 2001, 264:113-122.
19. Loomis P.A., Zheng L., Sekerková G., Changyaleket B., Mugnaini E., Bartles J.R. Espin cross-links cause the elongation of microvillus-type parallel actin bundles invivo. J.Cell Biol. 2003, 163:1045-1055.
20. Meyers J.R., MacDonald R.B., Duggan A., Lenzi D., Standaert D.G., Corwin J.T., Corey D.P. Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J.Neurosci. 2003, 23:4054-4065.
21. Okazaki Y., Furuno M., Kasukawa T., Adachi J., Bono H., Kondo S., Nikaido I., Osato N., Saito R., Suzuki H., et al. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 2002, 420:563-573. FANTOM Consortium, RIKEN Genome Exploration Research Group Phase I & II TeamRIKEN Genome Exploration Research Group Phase I & II Team.
22. Pacholsky D., Vakeel P., Himmel M., Löwe T., Stradal T., Rottner K., Fürst D.O., van der Ven P.F. Xin repeats define a novel actin-binding motif. J.Cell Sci. 2004, 117:5257-5268.
23. Pan P.W., Li K., Tuggle C.K., Yu M., Liu B., Zhao S.H. Sequencing, tissue distribution and physical mapping of the porcine homologue of cardiomyopathy associated 3 (CMYA3). Anim. Genet. 2003, 34:473-474.
24. Pulleyn L.J., Jackson A.P., Roberts E., Carridice A., Muxworthy C., Houseman M., Al-Gazali L.I., Lench N.J., Markham A.F., Mueller R.F. A new locus for autosomal recessive non-syndromal sensorineural hearing impairment (DFNB27) on chromosome 2q23-q31. Eur. J. Hum. Genet. 2000, 8:991-993.
25. Shepherd G.M., Barres B.A., Corey D.P. "Bundle blot" purification and initial protein characterization of hair cell stereocilia. Proc. Natl. Acad. Sci. USA 1989, 86:4973-4977.
26. Shin J.B., Longo-Guess C.M., Gagnon L.H., Saylor K.W., Dumont R.A., Spinelli K.J., Pagana J.M., Wilmarth P.A., David L.L., Gillespie P.G., Johnson K.R. The R109H variant of fascin-2, a developmentally regulated actin crosslinker in hair-cell stereocilia, underlies early-onset hearing loss of DBA/2J mice. J.Neurosci. 2010, 30:9683-9694.
27. Shin J.B., Krey J.F., Hassan A., Metlagel Z., Tauscher A.N., Pagana J.M., Sherman N.E., Jeffery E.D., Spinelli K.J., Zhao H., et al. Molecular architecture of the chick vestibular hair bundle. Nat. Neurosci. 2013, 16:365-374.
28. Tilney L.G., DeRosier D.J. Actin filaments, stereocilia, and hair cells of the bird cochlea. IV. How the actin filaments become organized in developing stereocilia and in the cuticular plate. Dev. Biol. 1986, 116:119-129.
29. Tilney L.G., Derosier D.J., Mulroy M.J. The organization of actin filaments in the stereocilia of cochlear hair cells. J.Cell Biol. 1980, 86:244-259.
30. Tilney M.S., Tilney L.G., Stephens R.E., Merte C., Drenckhahn D., Cotanche D.A., Bretscher A. Preliminary biochemical characterization of the stereocilia and cuticular plate of hair cells of the chick cochlea. J.Cell Biol. 1989, 109:1711-1723.
31. Wang D.Z., Hu X., Lin J.L., Kitten G.T., Solursh M., Lin J.J. Differential displaying of mRNAs from the atrioventricular region of developing chicken hearts at stages 15 and 21. Front. Biosci. 1996, 1:a1-a15.
32. Wang D.Z., Reiter R.S., Lin J.L., Wang Q., Williams H.S., Krob S.L., Schultheiss T.M., Evans S., Lin J.J. Requirement of a novel gene, Xin, in cardiac morphogenesis. Development 1999, 126:1281-1294.
33. Wang Q., Lin J.L., Reinking B.E., Feng H.Z., Chan F.C., Lin C.I., Jin J.P., Gustafson-Wagner E.A., Scholz T.D., Yang B., Lin J.J. Essential roles of an intercalated disc protein, mXinbeta, in postnatal heart growth and survival. Circ. Res. 2010, 106:1468-1478.
34. Zhang D.S., Piazza V., Perrin B.J., Rzadzinska A.K., Poczatek J.C., Wang M., Prosser H.M., Ervasti J.M., Corey D.P., Lechene C.P. Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature 2012, 481:520-524.