Alström Syndrome protein ALMS1 localizes to basal bodies of cochlear hair cells and regulates cilium-dependent planar cell polarity

Human Molecular Genetics

Volumn 20, Issue 3, 2011, Pages 466-481

  Jagger, Daniel ^a   Collin, Gayle ^b   Kelly, John ^a   Towers, Emily ^a   Nevill, Graham ^a   Longo Guess, Chantal ^b   Benson, Jennifer ^c   Halsey, Karin ^c   Dolan, David ^c   Marshall, Jan ^b   Naggert, Jürgen ^b   Forge, Andrew ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b JACKSON LABORATORY   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALSTROM SYNDROME PROTEIN 1; PROTEIN; UNCLASSIFIED DRUG;

ALSTROM SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL POLARITY; COCHLEA; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; HAIR CELL; HISTOPATHOLOGY; MATURITY; MOUSE; NONHUMAN; PERCEPTION DEAFNESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REGULATORY MECHANISM; STEREOCILIUM;

ALSTROM SYNDROME; ANIMALS; CELL DIFFERENTIATION; CELL POLARITY; CENTRIOLES; CILIA; COCHLEA; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HAIR CELLS, AUDITORY; HEARING LOSS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; ORGAN OF CORTI; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STRIA VASCULARIS;

MUS; RATTUS;

EID: 78651094693     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq493     Document Type: Article

References (49)

1. Collin, G.B., Marshall, J.D., Ikeda, A., So, W.V., Russell-Eggitt, I., Maffei, P., Beck, S., Boerkoel, C.F., Sicolo, N., Martin, M. et al. (2002) Mutations in ALMS1 cause obesity, type 2 diabetes and neurosensory degeneration in Alstrom syndrome. Nat. Genet., 31, 74-78.
2. Hearn, T., Renforth, G.L., Spalluto, C., Hanley, N.A., Piper, K., Brickwood, S., White, C., Connolly, V., Taylor, J.F., Russell-Eggitt, I. et al. (2002) Mutation of ALMS1, a large gene with a tandem repeat encoding 47 amino acids, causes Alstrom syndrome. Nat. Genet., 31, 79-83.
3. Alström, C.H., Hallgren, B., Nilsson, L.B. and Asander, H. (1959) Retinal degeneration combined with obesity, diabetes mellitus and neurogenous deafness: a specific syndrome (not hitherto described) distinct from the Laurence-Moon-Bardet-Biedl syndrome: a clinical, endocrinological and genetic examination based on a large pedigree. Acta Psychiatr. Neurol. Scand. Suppl., 129, 1-35.
4. Marshall, J.D., Bronson, R.T., Collin, G.B., Nordstrom, A.D., Maffei, P., Paisey, R.B., Carey, C., Macdermott, S., Russell-Eggitt, I., Shea, S.E. et al. (2005) New Alstrom syndrome phenotypes based on the evaluation of 182 cases. Arch. Intern. Med., 165, 675-683.
5. Marshall, J.D., Beck, S., Maffei, P. and Naggert, J.K. (2007) Alstrom syndrome. Eur. J. Hum. Genet., 15, 1193-1202.
6. Marshall, J.D., Hinman, E.G., Collin, G.B., Beck, S., Cerqueira, R., Maffei, P., Milan, G., Zhang, W., Wilson, D.I., Hearn, T. et al. (2007) Spectrum of ALMS1 variants and evaluation of genotype-phenotype correlations in Alstrom syndrome. Hum. Mutat., 28, 1114-1123.
7. Welsh, L.W. (2007) Alstrom syndrome: progressive deafness and blindness. Ann. Otol. Rhinol. Laryngol., 116, 281-285.
8. Loudon, M.A., Bellenger, N.G., Carey, C.M. and Paisey, R.B. (2009) Cardiac magnetic resonance imaging in Alstrom syndrome. Orphanet. J. Rare Dis., 4, 14.
9. Hearn, T., Spalluto, C., Phillips, V.J., Renforth, G.L., Copin, N., Hanley, N.A. and Wilson, D.I. (2005) Subcellular localization of ALMS1 supports involvement of centrosome and basal body dysfunction in the pathogenesis of obesity, insulin resistance, and type 2 diabetes. Diabetes, 54, 1581-1587.
10. Li, G., Vega, R., Nelms, K., Gekakis, N., Goodnow, C., McNamara, P., Wu, H., Hong, N.A. and Glynne, R. (2007) A role for Alstrom syndrome protein, alms1, in kidney ciliogenesis and cellular quiescence. PLoS Genet., 3, e8.
11. Knorz, V.J., Spalluto, C., Lessard, M., Purvis, T.L., Adigun, F.F., Collin, G.B., Hanley, N.A., Wilson, D.I. and Hearn, T. (2010) Centriolar association of ALMS1 and likely centrosomal functions of the ALMS motif-containing proteins C10orf90 and KIAA1731. Mol. Biol. Cell., 21, 3617-3629.
12. Nachury, M.V., Loktev, A.V., Zhang, Q., Westlake, C.J., Peranen, J., Merdes, A., Slusarski, D.C., Scheller, R.H., Bazan, J.F., Sheffield, V.C. et al. (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell, 129, 1201-1213.
13. May-Simera, H.L., Ross, A., Rix, S., Forge, A., Beales, P.L. and Jagger, D.J. (2009) Patterns of expression of Bardet-Biedl syndrome proteins in the mammalian cochlea suggest noncentrosomal functions. J. Comp. Neurol., 514, 174-188.
14. Ansley, S.J., Badano, J.L., Blacque, O.E., Hill, J., Hoskins, B.E., Leitch, C.C., Kim, J.C., Ross, A.J., Eichers, E.R., Teslovich, T.M. et al. (2003) Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature, 425, 628-633.
15. Kim, J.C., Ou, Y.Y., Badano, J.L., Esmail, M.A., Leitch, C.C., Fiedrich, E., Beales, P.L., Archibald, J.M., Katsanis, N., Rattner, J.B. et al. (2005) MKKS/BBS6, a divergent chaperonin-like protein linked to the obesity disorder Bardet-Biedl syndrome, is a novel centrosomal component required for cytokinesis. J. Cell Sci., 118, 1007-1020.
16. Kim, J.C., Badano, J.L., Sibold, S., Esmail, M.A., Hill, J., Hoskins, B.E., Leitch, C.C., Venner, K., Ansley, S.J., Ross, A.J. et al. (2004) The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat. Genet., 36, 462-470.
17. Yen, H.J., Tayeh, M.K., Mullins, R.F., Stone, E.M., Sheffield, V.C. and Slusarski, D.C. (2006) Bardet-Biedl syndrome genes are important in retrograde intracellular trafficking and Kupffer's vesicle cilia function. Hum. Mol. Genet., 15, 667-677.
18. Kim, S.K., Shindo, A., Park, T.J., Oh, E.C., Ghosh, S., Gray, R.S., Lewis, R.A., Johnson, C.A., Attie-Bittach, T., Katsanis, N. et al. (2010) Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science, 329, 1337-1440.
19. Wiens, C.J., Tong, Y., Esmail, M.A., Oh, E., Gerdes, J.M., Wang, J., Tempel, W., Rattner, J.B., Katsanis, N., Park, H.W. et al. (2010) Bardet-Biedl syndrome-associated small GTPase ARL6 (BBS3) functions at or near the ciliary gate and modulates Wnt signaling. J. Biol. Chem., 285, 16218-16230.
20. Badano, J.L., Mitsuma, N., Beales, P.L. and Katsanis, N. (2006) The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet., 7, 125-148.
21. Fliegauf, M., Benzing, T. and Omran, H. (2007) When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol., 8, 880-893.
22. Adams, M., Smith, U.M., Logan, C.V. and Johnson, C.A. (2008) Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. J. Med. Genet., 45, 257-267.
23. Ross, A.J., May-Simera, H., Eichers, E.R., Kai, M., Hill, J., Jagger, D.J., Leitch, C.C., Chapple, J.P., Munro, P.M., Fisher, S. et al. (2005) Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet., 37, 1135-1140.
24. Dabdoub, A. and Kelley, M.W. (2005) Planar cell polarity and a potential role for a Wnt morphogen gradient in stereociliary bundle orientation in the mammalian inner ear. J. Neurobiol., 64, 446-457.
25. Jones, C., Roper, V.C., Foucher, I., Qian, D., Banizs, B., Petit, C., Yoder, B.K. and Chen, P. (2008) Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat. Genet., 40, 69-77.
26. Jones, C. and Chen, P. (2008) Primary cilia in planar cell polarity regulation of the inner ear. Curr. Top. Dev. Biol., 85, 197-224.
27. Denman-Johnson, K. and Forge, A. (1999) Establishment of hair bundle polarity and orientation in the developing vestibular system of the mouse. J. Neurocytol., 28, 821-835.
28. 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, 295-306.
29. Brown, S.D., Hardisty-Hughes, R.E. and Mburu, P. (2008) Quiet as a mouse: dissecting the molecular and genetic basis of hearing. Nat. Rev. Genet., 9, 277-290.
30. Collin, G.B., Cyr, E., Bronson, R., Marshall, J.D., Gifford, E.J., Hicks, W., Murray, S.A., Zheng, Q.Y., Smith, R.S., Nishina, P.M. et al. (2005) Alms1-disrupted mice recapitulate human Alstrom syndrome. Hum. Mol. Genet., 14, 2323-2333.
31. Trowe, M.O., Maier, H., Schweizer, M. and Kispert, A. (2008) Deafness in mice lacking the T-box transcription factor Tbx18 in otic fibrocytes. Development, 135, 1725-1734.
32. Wangemann, P. (2002) K+ cycling and the endocochlear potential. Hear. Res., 165, 1-9.
33. Leibovici, M., Verpy, E., Goodyear, R.J., Zwaenepoel, I., Blanchard, S., Laine, S., Richardson, G.P. and Petit, C. (2005) Initial characterization of kinocilin, a protein of the hair cell kinocilium. Hear. Res., 203, 144-153.
34. Nakazawa, K., Spicer, S.S., Gratton, M.A. and Schulte, B.A. (1996) Localization of actin in basal cells of stria vascularis. Hear. Res., 96, 13-19.
35. Karolyi, I.J., Dootz, G.A., Halsey, K., Beyer, L., Probst, F.J., Johnson, K.R., Parlow, A.F., Raphael, Y., Dolan, D.F. and Camper, S.A. (2007) Dietary thyroid hormone replacement ameliorates hearing deficits in hypothyroid mice. Mamm. Genome, 18, 596-608.
36. Noben-Trauth, K. and Johnson, K.R. (2009) Inheritance patterns of progressive hearing loss in laboratory strains of mice. Brain Res., 1277, 42-51.
37. Taylor, R.R., Nevill, G. and Forge, A. (2008) Rapid hair cell loss: a mouse model for cochlear lesions. J. Assoc. Res. Otolaryngol., 9, 44-64.
38. Ando, M. and Takeuchi, S. (1999) Immunological identification of an inward rectifier K+ channel (Kir4.1) in the intermediate cell (melanocyte) of the cochlear stria vascularis of gerbils and rats. Cell Tissue Res., 298, 179-183.
39. Jagger, D.J. and Forge, A. (2006) Compartmentalized and signal-selective gap junctional coupling in the hearing cochlea. J. Neurosci., 26, 1260-1268.
40. Demeester, K., van Wieringen, A., Hendrickx, J.J., Topsakal, V., Fransen, E., van Laer, L., Van Camp, G. and Van de Heyning, P. (2009) Audiometric shape and presbycusis. Int. J. Audiol., 48, 222-232.
41. Schmiedt, R.A., Lang, H., Okamura, H.O. and Schulte, B.A. (2002) Effects of furosemide applied chronically to the round window: a model of metabolic presbyacusis. J. Neurosci., 22, 9643-9650.
42. Schuknecht, H.F. and Gacek, M.R. (1993) Cochlear pathology in presbycusis. Ann. Otol. Rhinol. Laryngol., 102, 1-16.
43. Schulte, B.A. and Schmiedt, R.A. (1992) Lateral wall Na, K-ATPase and endocochlear potentials decline with age in quiet-reared gerbils. Hear. Res., 61, 35-46.
44. Wangemann, P., Itza, E.M., Albrecht, B., Wu, T., Jabba, S.V., Maganti, R.J., Lee, J.H., Everett, L.A., Wall, S.M., Royaux, I.E. et al. (2004) Loss of KCNJ10 protein expression abolishes endocochlear potential and causes deafness in Pendred syndrome mouse model. BMC Med., 2, 30.
45. Mustapha, M., Fang, Q., Gong, T.W., Dolan, D.F., Raphael, Y., Camper, S.A. and Duncan, R.K. (2009) Deafness and permanently reduced potassium channel gene expression and function in hypothyroid Pit1dw mutants. J. Neurosci., 29, 1212-1223.
46. Hirose, K. and Liberman, M.C. (2003) Lateral wall histopathology and endocochlear potential in the noise-damaged mouse cochlea. J. Assoc. Res. Otolaryngol., 4, 339-352.
47. Gale, J.E. and Jagger, D.J. (2010) Cochlear supporting cells. In Fuchs, P.A. (ed.), The Oxford Handbook of Auditory Science: The Ear. Oxford University Press, Oxford, UK, pp. 307-327.
48. Hildebrandt, F. and Zhou, W. (2007) Nephronophthisis-associated ciliopathies. J. Am. Soc. Nephrol., 18, 1855-1871.
49. Davies, S. and Forge, A. (1987) Preparation of the mammalian organ of Corti for scanning electron microscopy. J. Microsc., 147, 89-101.