Patterns of expression of Bardet-Biedl syndrome proteins in the mammalian cochlea suggest noncentrosomal functions

Journal of Comparative Neurology

Volumn 514, Issue 2, 2009, Pages 174-188

  May Simera, Helen L ^a   Ross, Alison ^a   Rix, Suzanne ^a   Forge, Andrew ^b   Beales, Philip L ^a   Jagger, Daniel J ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Basal body; Cilium; Cochlea; Deafness; Hair cells; Stereocilia

Indexed keywords

BARDET BIEDL SYNDROME 4 PROTEIN; BARDET BIEDL SYNDROME 6 PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PCM 1 PROTEIN; UNCLASSIFIED DRUG; BBS4 PROTEIN, MOUSE; CELL CYCLE PROTEIN; CHAPERONE; KIF1A PROTEIN, MOUSE; KINESIN; MKKS PROTEIN, MOUSE; PCM1 PROTEIN, MOUSE; TUBULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BARDET BIEDL SYNDROME; CELLULAR DISTRIBUTION; CENTROSOME; COCHLEA; CONTROLLED STUDY; CYTOPLASM; DEPOLYMERIZATION; DEVELOPMENT; HAIR CELL; HEARING IMPAIRMENT; MICROTUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; STEREOCILIUM; ANIMAL; CELL CULTURE; CERCOPITHECUS; ELECTRON MICROSCOPE TOMOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; HUMAN; IMMUNOPRECIPITATION; IN VITRO STUDY; MAMMAL; METABOLISM; METHODOLOGY; MOUSE MUTANT; RAT; SENSORY NERVE CELL; TWO HYBRID SYSTEM; ULTRASTRUCTURE;

ANIMALS; CELL CYCLE PROTEINS; CELLS, CULTURED; CENTROSOME; CERCOPITHECUS AETHIOPS; COCHLEA; ELECTRON MICROSCOPE TOMOGRAPHY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOPRECIPITATION; KINESIN; MAMMALS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR CHAPERONES; NEURONS, AFFERENT; RATS; TUBULIN; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 67649238467     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22001     Document Type: Article

References (48)

1. Ansley SJ, Badano JL, Blacque OE, Hill J, Hoskins BE, Leitch CC, Kim JC, Ross AJ, Eichers ER, Teslovich TM, Mah AK, Johnsen RC, Cavender JC, Lewis RA, Leroux MR, Beales PL, Katsanis N. 2003. Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425:628-633.
2. Badano JL, Ansley SJ, Leitch CC, Lewis RA, Lupski JR, Katsanis N. 2003a. Identification of a novel Bardet-Biedl syndrome protein, BBS7, that shares structural features with BBS1 and BBS2. Am J Hum Genet 72:650-658.
3. Badano JL, Kim JC, Hoskins BE, Lewis RA, Ansley SJ, Cutler DJ, Castellan C, Beales PL, Leroux MR, Katsanis N. 2003b. Heterozygous mutations in BBS1, BBS2 and BBS6 have a potential epistatic effect on Bardet-Biedl patients with two mutations at a second BBS locus. Hum Mol Genet 12:1651-1659.
4. Bane BC, MacRae TH, Xiang H, Bateman J, Slepecky NB. 2002. Microtubule cold stability in supporting cells of the gerbil auditory sensory epithelium: correlation with tubulin post-translational modifications. Cell Tissue Res 307:57- 67.
5. Blacque OE, Leroux MR. 2006. Bardet-Biedl syndrome: an emerging pathomechanism of intracellular transport. Cell Mol Life Sci 63:2145- 2161.
6. Blacque OE, Reardon MJ, Li C, McCarthy J, Mahjoub MR, Ansley SJ, Badano JL, Mah AK, Beales PL, Davidson WS, Johnsen RC, Audeh M, Plasterk RH, Baillie DL, Katsanis N, Quarmby LM, Wicks SR, Leroux MR. 2004. Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev 18:1630-1642.
7. Dammermann A, Merdes A. 2002. Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J Cell Biol 159:255-266.
8. Deacon SW, Serpinskaya AS, Vaughan PS, Lopez Fanarraga M, Vernos I, Vaughan KT, Gelfand VI. 2003. Dynactin is required for bidirectional organelle transport. J Cell Biol 160:297-301.
9. Denman-Johnson K, Forge A. 1999. Establishment of hair bundle polarity and orientation in the deveoping vestibular system of the mouse. J Neurocytol 28:821- 835.
10. Fath MA, Mullins RF, Searby C, Nishimura DY, Wei J, Rahmouni K, Davis RE, Tayeh MK, Andrews M, Yang B, Sigmund CD, Stone EM, Sheffield VC. 2005. Mkks-null mice have a phenotype resembling Bardet-Biedl syndrome. Hum Mol Genet 14:1109-1118.
11. Frolenkov GI, Belyantseva IA, Friedman TB, Griffith AJ. 2004. Genetic insights into the morphogenesis of inner ear hair cells. Nat Rev Genet 5:489-498.
12. Gerdes JM, Liu Y, Zaghloul NA, Leitch CC, Lawson SS, Kato M, Beachy PA, Beales PL, Demartino GN, Fisher S, Badano JL, Katsanis N. 2007. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat Genet 39:1350-1360.
13. Henderson CG, Tucker JB, Mogensen MM, Mackie JB, Chaplin MA, Slepecky NB, Leckie LM. 1995. Three microtubule-organizing centres collaborate in a mouse cochlear epithelial cell during supracellularly coordinated control of microtubule positioning. J Cell Sci 108:37-50.
14. Ikegami K, Heier RL, Taruishi M, Takagi H, Mukai M, Shimma S, Taira S, Hatanaka K, Morone N, Yao I, Campbell PK, Yuasa S, Janke C, Macgregor GR, Setou M. 2007. Loss of alpha-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function. Proc Natl Acad Sci U S A 104:3213- 3218.
15. Jagger DJ, Forge A. 2006. Compartmentalized and signal-selective gap junctional coupling in the hearing cochlea. J Neurosci 26:1260-1268.
16. Katsanis N. 2004. The oligogenic properties of Bardet-Biedl syndrome. Hum Mol Genet 13:R65-R71.
17. Katsanis N, Ansley SJ, Badano JL, Eichers ER, Lewis RA, Hoskins BE, Scambler PJ, Davidson WS, Beales PL, Lupski JR. 2001. Triallelic inheritance in Bardet-Biedl syndrome, a Mendelian recessive disorder. Science 293:2256-2259.
18. Kim JC, Badano JL, Sibold S, Esmail MA, Hill J, Hoskins BE, Leitch CC, Venner K, Ansley SJ, Ross AJ, Leroux MR, Katsanis N, Beales PL. 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.
19. Kim JC, Ou YY, Badano JL, Esmail MA, Leitch CC, Fiedrich E, Beales P, Archibald JM, Katsanis N, Rattner JB, Leroux MR. 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.
20. Kulaga HM, Leitch CC, Eichers ER, Badano JL, Lesemann A, Hoskins BE, Lupski JR, Beales PL, Reed RR, Katsanis N. 2004. Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat Genet 36:994-998.
21. Lagziel A, Ahmed ZM, Schultz JM, Morell RJ, Belyantseva IA, Friedman TB. 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.
22. Leibovici M, Verpy E, Goodyear RJ, Zwaenepoel I, Blanchard S, Laine S, Richardson GP, Petit C. 2005. Initial characterization of kinocilin, a protein of the hair cell kinocilium. Hear Res 203:144-153.
23. Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, May-Simera H, Li H, Blacque OE, Li L, Leitch CC, Lewis RA, Green JS, Parfrey PS, Leroux MR, Davidson WS, Beales PL, Guay-Woodford LM, Yoder BK, Stormo GD, Katsanis N, Dutcher SK. 2004. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117:541-552.
24. Lin C-M, Chen H-J, Leung CL, Parry D, Liem R. 2005. Microtubule actin crosslinking factor 1b: a novel plakin that localizes to the Golgi complex. J Cell Sci 118:3727-3738.
25. Mogensen MM, Mackie JB, Doxsey SJ, Stearns T, Tucker JB. 1997. Centrosomal deployment of gamma-tubulin and pericentrin: evidence for a microtubule-nucleating domain and a minus-end docking domain in certain mouse epithelial cells. Cell Motil Cytoskeleton 36:276-290.
26. Mogensen MM, Henderson CG, Mackie JB, Lane EB, Garrod DR, Tucker JB. 1998. Keratin filament deployment and cytoskeletal networking in a sensory epithelium that vibrates during hearing. Cell Motil Cytoskeleton 41:138-153.
27. Mogensen MM, Malik A, Piel M, Bouckson-Castaing V, Bornens M. 2000. Microtubule minus-end anchorage at centrosomal and noncentrosomal sites: the role of ninein. J Cell Sci 113:3013-3023.
28. Mogensen MM, Tucker JB, Mackie JB, Prescott AR, Nathke IS. 2002. The adenomatous polyposis coli protein unambiguously localizes to microtubule plus ends and is involved in establishing parallel arrays of microtubule bundles in highly polarized epithelial cells. J Cell Biol 157:1041-1048.
29. Moss DK, Bellett G, Carter JM, Liovic M, Keynton J, Prescott AR, Lane EB, Mogensen MM. 2007. Ninein is released from the centrosome and moves bi-directionally along microtubules. J Cell Sci 120:3064-3074.
30. Mykytyn K, Braun T, Carmi R, Haider NB, Searby CC, Shastri M, Beck G, Wright AF, Iannaccone A, Elbedour K, Riise R, Baldi A, Raas-Rothschild A, Gorman SW, Duhl DM, Jacobson SG, Casavant T, Stone EM, Sheffield VC. 2001. Identification of the gene that, when mutated, causes the human obesity syndrome BBS4. Nat Genet 28:188-191.
31. Mykytyn K, Nishimura DY, Searby CC, Shastri M, Yen HJ, Beck JS, Braun T, Streb LM, Cornier AS, Cox GF, Fulton AB, Carmi R, Luleci G, Chandrasekharappa SC, Collins FS, Jacobson SG, Heckenlively JR, Weleber RG, Stone EM, Sheffield VC. 2002. Identification of the gene (BBS1) most commonly involved in Bardet-Biedl syndrome, a complex human obesity syndrome. Nat Genet 15:15.
32. Mykytyn K, Mullins RF, Andrews M, Chiang AP, Swiderski RE, Yang B, Braun T, Casavant T, Stone EM, Sheffield VC. 2004. Bardet-Biedl syndrome type 4 (BBS4)-null mice implicate Bbs4 in flagella formation but not global cilia assembly. Proc Natl Acad Sci U S A 101:8664-8669.
33. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peranen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK. 2007. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129:1201-1213.
34. Nishimura DY, Fath M, Mullins RF, Searby C, Andrews M, Davis R, Andorf JL, Mykytyn K, Swiderski RE, Yang B, Carmi R, Stone EM, Sheffield VC. 2004. Bbs2-null mice have neurosensory deficits, a defect in social dominance, and retinopathy associated with mislocalization of rhodopsin. Proc Natl Acad Sci U S A 101:16588-16593.
35. Oeffner F, Moch C, Neundorf A, Hofmann J, Koch M, Grzeschik KH. 2008. Novel interaction partners of Bardet-Biedl syndrome proteins. Cell Motil Cytoskeleton 65:143-155.
36. Okada Y, Yamazaki H, Sekine-Aizawa Y, Hirokawa N. 1995. The neuronspecific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81:769-780.
37. Ou G, Blacque OE, Snow JJ, Leroux MR, Scholey JM. 2005. Functional coordination of intraflagellar transport motors. Nature 436:583-587.
38. Ross AJ, May-Simera H, Eichers ER, Kai M, Hill J, Jagger DJ, Leitch CC, Chapple JP, Munro PM, Fisher S, Tan PL, Phillips HM, Leroux MR, Henderson DJ, Murdoch JN, Copp AJ, Eliot MM, Lupski JR, Kemp DT, Dollfus H, Tada M, Katsanis N, Forge A, Beales PL. 2005. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat Genet 37:1135-1140.
39. Slepecky NB, Henderson CG, Saha S. 1995. Post-translational modifications of tubulin suggest that dynamic microtubules are present in sensory cells and stable microtubules are present in supporting cells of the mammalian cochlea. Hear Res 91:136-147.
40. Stoetzel C, Laurier V, Davis EE, Muller J, Rix S, Badano JL, Leitch CC, Salem N, Chouery E, Corbani S, Jalk N, Vicaire S, Sarda P, Hamel C, Lacombe D, Holder M, Odent S, Holder S, Brooks AS, Elcioglu NH, Silva ED, Rossillion B, Sigaudy S, de Ravel TJ, Lewis RA, Leheup B, Verloes A, Amati-Bonneau P, Megarbane A, Poch O, Bonneau D, Beales PL, Mandel JL, Katsanis N, Dollfus H. 2006. BBS10 encodes a vertebrate-specific chaperonin-like protein and is a major BBS locus. Nat Genet 38:521-524.
41. Stoetzel C, Muller J, Laurier V, Davis EE, Zaghloul NA, Vicaire S, Jacquelin C, Plewniak F, Leitch CC, Sarda P, Hamel C, de Ravel TJ, Lewis RA, Friederich E, Thibault C, Danse JM, Verloes A, Bonneau D, Katsanis N, Poch O, Mandel JL, Dollfus H. 2007. Identification of a novel BBS gene (BBS12) highlights the major role of a vertebrate-specific branch of chaperonin-related proteins in Bardet-Biedl syndrome. Am J Hum Genet 80:1-11.
42. Tobin JL, Beales PL. 2007. Bardet-Biedl syndrome: beyond the cilium. Pediatr Nephrol 22:926-936.
43. Tucker JB, Paton CC, Richardson GP, Mogensen MM, Russell IJ. 1992. A cell surface-associated centrosomal layer of microtubule-organizing material in the inner pillar cell of the mouse cochlea. J Cell Sci 102: 215-226.
44. Tucker JB, Paton CC, Henderson CG, Mogensen MM. 1993. Microtubule rearrangement and bending during assembly of large curved microtubule bundles in mouse cochlear epithelial cells. Cell Motil Cytoskeleton 25:49-58.
45. Tucker JB, Mogensen MM, Paton CC, Mackie JB, Henderson CG, Leckie LM. 1995. Formation of two microtubule-nucleating sites which perform differently during centrosomal reorganization in a mouse cochlear epithelial cell. J Cell Sci 108:1333-1345.
46. Valpuesta JM, Martin-Benito J, Gomez-Puertas P, Carrascosa JL, Willison KR. 2002. Structure and function of a protein folding machine: the eukaryotic cytosolic chaperonin CCT. FEBS Lett 529:11-16.
47. Yen HJ, Tayeh MK, Mullins RF, Stone EM, Sheffield VC, Slusarski DC. 2006. Bardet-Biedl syndrome genes are important in retrograde intracellular trafficking and Kupffer's vesicle cilia function. Hum Mol Genet 15:667- 677.
48. Yonekawa Y, Harada A, Okada Y, Funakoshi T, Kanai Y, Takei Y, Terada S, Noda T, Hirokawa N. 1998. Defect in synaptic vesicle precursor transport and neuronal cell death in KIF1A motor protein-deficient mice. J Cell Biol 141:431-441.