Ciliary proteins bbs8 and ift20 promote planar cell polarity in the cochlea

Development (Cambridge)

Volumn 142, Issue 3, 2015, Pages 555-566

  May Simera, Helen L ^a   Petralia, Ronald S ^a   Montcouquiol, Mireille ^b   Wang, Ya Xian ^a   Szarama, Katherine B ^a,c   Liu, Yun ^d   Lin, Weichun ^d   Deans, Michael R ^e   Pazour, Gregory J ^f   Kelley, Matthew W ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^b INSERM   (France)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Actin; Cilia; Cochlea; Microtubules; Mouse; Polarity

Indexed keywords

ACTIN; MEMBRANE PROTEIN; PROTEIN BBS8; PROTEIN IFT20; UNCLASSIFIED DRUG; CARRIER PROTEIN; IFT20 PROTEIN, MOUSE; LTAP PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; TTC8 PROTEIN, MOUSE;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL POLARITY; COCHLEA; CYTOSKELETON; EUKARYOTIC FLAGELLUM; IMMUNOGOLD LABELING; IMMUNOHISTOCHEMISTRY; MICROTUBULE; MICROTUBULE ORGANIZING CENTER; MOUSE; MUTANT; NONHUMAN; PHENOTYPE; PLANAR CELL POLARITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SCANNING ELECTRON MICROSCOPY; TEMPORAL BONE; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; COCHLEAR HAIR CELL; EMBRYOLOGY; GENETICS; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

MUS;

ANIMALS; CARRIER PROTEINS; CELL POLARITY; CILIA; COCHLEA; HAIR CELLS, AUDITORY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS;

EID: 84921446597     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.113696     Document Type: Article

References (62)

1. 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.
2. Aw, S. and Levin, M. (2009). Is left-right asymmetry a form of planar cell polarity? Development 136, 355-366.
3. Blacque, O. E., Reardon, M. J., Li, C., McCarthy, J., Mahjoub, M. R., Ansley, S. J., Badano, J. L., Mah, A. K., Beales, P. L., Davidson, W. S. et al. (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.
4. Borovina, A. and Ciruna, B. (2013). IFT88 plays a cilia- and PCP-independent role in controlling oriented cell divisions during vertebrate embryonic development. Cell Rep. 5, 37-43.
5. Carreira-Barbosa, F., Kajita, M., Morel, V., Wada, H., Okamoto, H., Martinez Arias, A., Fujita, Y., Wilson, S. W. and Tada, M. (2009). Flamingo regulate sepiboly and convergence/extension movements through cell cohesive and signalling functions during zebrafish gastrulation. Development 136, 383-392.
6. Copley, C. O., Duncan, J. S., Liu, C., Cheng, H. and Deans, M. R. (2013). Postnatal refinement of auditory hair cell planar polarity deficits occurs in the absence of Vangl2. J. Neurosci. 33, 14001-14016.
7. Cotanche, D. A. and Corwin, J. T. (1991). Stereociliary bundles reorient during hair cell development and regeneration in the chick cochlea. Hear. Res. 52, 379-402.
8. Cui, C., Chatterjee, B., Lozito, T. P., Zhang, Z., Francis, R. J., Yagi, H., Swanhart, L. M., Sanker, S., Francis, D., Yu, Q. et al. (2013). Wdpcp, a PCP protein required for ciliogenesis, regulates directional cell migration and cell polarity by direct modulation of the actin cytoskeleton. PLoS Biol. 11, e1001720.
9. Delaval, B., Bright, A., Lawson, N. D. and Doxsey, S. (2011). The cilia protein IFT88 is required for spindle orientation in mitosis. Nat. Cell Biol. 13, 461-468.
10. 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.
11. Dickinson, M. E. and McMahon, A. P. (1992). The role of Wnt genes in vertebrate development. Curr. Opin. Genet. Dev. 2, 562-566.
12. Eguether, T., San Agustin, J. T., Keady, B.T., Jonassen, J.A., Liang, Y., Francis, R., Tobita, K., Johnson, C. A., Abdelhamed, Z. A., Lo, C. W. and Pazour, G. J. (2014). IFT27 links the BBSome to IFT for maintenance of the ciliary signaling compartment. Dev. Cell 31, 279-290.
13. Ezan, J. and Montcouquiol, M. (2013). Revisiting planar cell polarity in the inner ear. Semin. Cell Dev. Biol. 24, 499-506.
14. Ezan, J., Lasvaux, L., Gezer, A., Novakovic, A., May-Simera, H., Belotti, E., Lhoumeau, A.-C., Birnbaumer, L., Beer-Hammer, S., Borg, J.-P. et al. (2013). Primary cilium migration depends on G-protein signalling control of subapical cytoskeleton. Nat. Cell Biol. 15, 1107-1115.
15. Finetti, F., Paccani, S. R., Riparbelli, M. G., Giacomello, E., Perinetti, G., Pazour, G. J., Rosenbaum, J. L. and Baldari, C. T. (2009). Intraflagellar transport is required for polarized recycling of the TCR/CD3 complex to the immune synapse. Nat. Cell Biol. 11, 1332-1339.
16. Fisch, C. and Dupuis-Williams, P. (2011). Ultrastructure of cilia and flagella – back to the future! Biol. Cell 103, 249-270.
17. Follit, J. A., Tuft, R. A., Fogarty, K. E. and Pazour, G. J. (2006). The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol. Biol. Cell 17, 3781-3792.
18. Follit, J. A., San Agustin, J.T., Xu, F., Jonassen, J. A., Samtani, R., Lo, C.W. and Pazour, G. J. (2008). The Golgin GMAP210/TRIP11 anchors IFT20 to the Golgi complex. PLoS Genet. 4, e1000315.
19. Follit, J. A., Xu, F., Keady, B. T. and Pazour, G. J. (2009). Characterization of mouse IFT complex B. Cell Motil. Cytoskeleton 66, 457-468.
20. Forsythe, E. and Beales, P. L. (2013). Bardet-Biedl syndrome. Eur. J. Hum. Genet. 21, 8-13.
21. Hebert, J. M. and McConnell, S. K. (2000). Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev. Biol. 222, 296-306.
22. Hernandez-Hernandez, V., Pravincumar, P., Diaz-Font, A., May-Simera, H., Jenkins, D., Knight, M. and Beales, P. L. (2013). Bardet-Biedl syndrome proteins control the cilia length through regulation of actin polymerization. Hum. Mol. Genet. 22, 3858-3868.
23. Huang, P. and Schier, A.F. (2009).DampenedHedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development 136, 3089-3098.
24. Jagger, D., Collin, G., Kelly, J., Towers, E., Nevill, G., Longo-Guess, C., Benson, J., Halsey, K., Dolan, D., Marshall, J. et al. (2011). Alstrom Syndrome protein ALMS1 localizes to basal bodies of cochlear hair cells and regulates cilium-dependent planar cell polarity. Hum. Mol. Genet. 20, 466-481.
25. Jonassen, J. A., San Agustin, J., Follit, J. A. and Pazour, G. J. (2008). Deletion of IFT20 in the mouse kidney causes misorientation of the mitotic spindle and cystic kidney disease. J. Cell Biol. 183, 377-384.
26. 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.
27. Keady, B.T., Samtani, R., Tobita, K., Tsuchya, M., San Agustin, J.T., Follit, J.A., Jonassen, J. A., Subramanian, R., Lo, C. W. and Pazour, G. J. (2012). IFT25 links the signal-dependent movement of Hedgehog components to intraflagellar transport. Dev. Cell 22, 940-951.
28. Kim, S. and Tsiokas, L. (2011). Cilia and cell cycle re-entry: more than a coincidence. Cell Cycle 10, 2683-2690.
29. Kobayashi, T. and Dynlacht, B. D. (2011). Regulating the transition from centriole to basal body. J. Cell Biol. 193, 435-444.
30. Lee, J.E. and Gleeson, J. G. (2011). Asystems-biology approach to understanding the ciliopathy disorders. Genome Med. 3, 59.
31. Lienkamp, S., Ganner, A. and Walz, G. (2012). Inversin, Wnt signaling and primary cilia. Differentiation 83, S49-S55.
32. Lucker, B. F., Behal, R. H., Qin, H., Siron, L.C., Taggart, W.D., Rosenbaum, J.L. and Cole, D. G. (2005). Characterization of the intraflagellar transport complex B core: direct interaction of the IFT81 and IFT74/72 subunits. J. Biol. Chem. 280, 27688-27696.
33. May-Simera, H. and Kelley, M. W. (2012a). Examining planar cell polarity in the Mammalian cochlea. Methods Mol. Biol. 839, 157-171.
34. May-Simera, H. L. and Kelley, M. W. (2012b). Cilia, Wnt signaling, and the cytoskeleton. Cilia 1, 7.
35. 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.
36. May-Simera, H. L., Kai, M., Hernandez, V., Osborn, D.P. S., Tada, M. and Beales, P. L. (2010). Bbs8, together with the planar cell polarity protein Vangl2, is required to establish left-right asymmetry in zebrafish. Dev. Biol. 345, 215-225.
37. Montcouquiol, M., Rachel, R. A., Lanford, P. J., Copeland, N. G., Jenkins, N. A. and Kelley, M. W. (2003). Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173-177.
38. Morsli, H., Choo, D., Ryan, A., Johnson, R. and Wu, D. K. (1998). Development of the mouse inner ear and origin of its sensory organs. J. Neurosci. 18, 3327-3335.
39. Moser, J. J., Fritzler, M. J., Ou, Y. and Rattner, J. B. (2010). The PCM-basal body/primary cilium coalition. Semin. Cell Dev. Biol. 21, 148-155.
40. 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.
41. Narimatsu, M., Bose, R., Pye, M., Zhang, L., Miller, B., Ching, P., Sakuma, R., Luga, V., Roncari, L., Attisano, L. et al. (2009). Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 137, 295-307.
42. Ocbina, P. J. R., Tuson, M. and Anderson, K. V. (2009). Primary cilia are not required for normal canonical Wnt signaling in the mouse embryo. PLoS ONE 4, e6839.
43. Pedersen, L. B., Veland, I. R., Schrøder, J. M. and Christensen, S. T. (2008). Assembly of primary cilia. Dev. Dyn. 237, 1993-2006.
44. Petralia, R. S. and Wenthold, R. J. (1999). Immunocytochemistry of NMDA receptors. Methods Mol. Biol. 128, 73-92.
45. Petralia, R. S., Wang, Y. X., Hua, F., Yi, Z., Zhou, A., Ge, L., Stephenson, F.A. and Wenthold, R. J. (2010). Organization of NMDA receptors at extrasynaptic locations. Neuroscience 167, 68-87.
46. Robert, A., Margall-Ducos, G., Guidotti, J.-E., Bregerie, O., Celati, C., Brechot, C. and Desdouets, C. (2007). The intraflagellar transport component IFT88/polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells. J. Cell Sci. 120, 628-637.
47. 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.
48. Saburi, S. and McNeill, H. (2005). Organising cells into tissues: new roles for cell adhesion molecules in planar cell polarity. Curr. Opin. Cell Biol. 17, 482-488.
49. Sedmak, T. and Wolfrum, U. (2010). Intraflagellar transport molecules in ciliary and nonciliary cells of the retina. J. Cell Biol. 189, 171-186.
50. Simons, M. and Mlodzik, M. (2008). Planar cell polarity signaling: from fly development to human disease. Annu. Rev. Genet. 42, 517-540.
51. Simons, M., Gloy, J., Ganner, A., Bullerkotte, A., Bashkurov, M., Kronig, C., Schermer, B., Benzing, T., Cabello, O. A., Jenny, A. et al. (2005). Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 37, 537-543.
52. Sipe, C. W. and Lu, X. (2011). Kif3a regulates planar polarization of auditory hair cells through both ciliary and non-ciliary mechanisms. Development 138, 3441-3449.
53. Tadenev, A. L. D., Kulaga, H. M., May-Simera, H. L., Kelley, M. W., Katsanis, N. and Reed, R. R.(2011). Loss of Bardet-Biedl syndrome protein-8 (BBS8) perturbs olfactory function, protein localization, and axon targeting. Proc. Natl. Acad. Sci. USA 108, 10320-10325.
54. Tissir, F., Qu, Y., Montcouquiol, M., Zhou, L., Komatsu, K., Shi, D., Fujimori, T., Labeau, J., Tyteca, D., Courtoy, P. et al. (2010). Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat. Neurosci. 13, 700-707.
55. Tobin, J. L., Di Franco, M., Eichers, E., May-Simera, H., Garcia, M., Yan, J., Quinlan, R., Justice, M. J., Hennekam, R. C., Briscoe, J. et al. (2008). Inhibition of neural crest migration underlies craniofacial dysmorphology and Hirschsprung’s disease in Bardet-Biedl syndrome. Proc. Natl. Acad. Sci. USA 105, 6714-6719.
56. van Dam, T. J. P., Wheway, G., Slaats, G., Huynen, M. A. and Giles, R. H., SYSCILIA Study Group, (2013). The SYSCILIA gold standard (SCGSv1) of known ciliary components and its applications within a systems biology consortium. Cilia 2, 7.
57. Veland, I. R., Montjean, R., Eley, L., Pedersen, L. B., Schwab, A., Goodship, J., Kristiansen, K., Pedersen, S. F., Saunier, S. and Christensen, S. T. (2013). Inversin/Nephrocystin-2 is required for fibroblast polarity and directional cell migration. PLoS ONE 8, e60193.
58. Vladar, E. K., Antic, D. and Axelrod, J. D. (2009). Planar cell polarity signaling: the developing cell’s compass. Cold Spring Harb. Perspect. Biol. 1, a002964.
59. Wallingford, J. B. and Mitchell, B. (2011). Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. Genes Dev. 25, 201-213.
60. Wang, Y., Guo, N. and Nathans, J. (2006). The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J. Neurosci. 26, 2147-2156.
61. Waters, A. M. and Beales, P. L. (2011). Ciliopathies: an expanding disease spectrum. Pediatr. Nephrol. 26, 1039-1056.
62. Yuan, S. and Sun, Z. (2013). Expanding horizons: ciliary proteins reach beyond cilia. Annu. Rev. Genet. 47, 353-376.