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Volume 43 Issue 3
Mar.  2016
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Article Navigation >  Journal of Genetics and Genomics  > 2016  >  43(3): 107-120

Zebrafish as a Model for Human Ciliopathies

doi: 10.1016/j.jgg.2016.02.001
  • a 

    Institute of Evolution & Marine Biodiversity, College of Marine Life Science, Ocean University of China, Qingdao 266003, China

  • b 

    Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266003, China

  • c 

    Department of Orthodontics, Division of Craniofacial and Molecular Genetics, Tufts University, Boston, MA 02111, USA

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  • Corresponding author: E-mail address: chengtian_zhao@ouc.edu.cn (Chengtian Zhao)
  • Received Date: 2016-01-29
  • Accepted Date: 2016-02-05
  • Rev Recd Date: 2016-02-04
    • Available Online: 2016-02-12
  • Publish Date: 2016-03-20
    Abstract
  • Cilia, microtubule-based structures found on the surface of almost all vertebrate cells, play an array of diverse biological functions. Abnormal ciliary axonemal structure and function can result in a class of genetic disorders that are collectively termed ciliopathies. Model organisms, including Chlamydomonas reinhardtii and Caenorhabditis elegans have been widely used to study the complex genetic basis of ciliopathies. Here, we review the advantages of the zebrafish as a vertebrate model for human ciliopathies. We summarize the features of zebrafish cilia, and the major findings and contributions of the zebrafish model in recent studies of human ciliopathies. We also discuss the new genome editing approaches being efficiently used in zebrafish, and the exciting prospects of these approaches in modeling human ciliopathies.
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  • [1]
    Aldahmesh, M.A., Li, Y., Alhashem, A. et al. Hum. Mol. Genet., 23 (2014),pp. 3307-3315
    [2]
    Auer, T.O., Del Bene, F. CRISPR/Cas9 and TALEN-mediated knock-in approaches in zebrafish Methods, 69 (2014),pp. 142-150
    [3]
    Austin-Tse, C., Halbritter, J., Zariwala, M.A. et al. Am. J. Hum. Genet., 93 (2013),pp. 672-686
    [4]
    Bachmann-Gagescu, R., Phelps, I.G., Dempsey, J.C. et al. Hum. Mutat., 36 (2015),pp. 831-835
    [5]
    Bachmann-Gagescu, R., Phelps, I.G., Stearns, G. et al. Hum. Mol. Genet., 20 (2011),pp. 4041-4055
    [6]
    Baker, K., Beales, P.L. Making sense of cilia in disease: the human ciliopathies Am. J. Med. Genet. C Semin. Med. Genet., 151C (2009),pp. 281-295
    [7]
    Basten, S.G., Davis, E.E., Gillis, A.J. et al. PLoS Genet., 9 (2013)
    [8]
    Baye, L.M., Patrinostro, X., Swaminathan, S. et al. The N-terminal region of centrosomal protein 290 (CEP290) restores vision in a zebrafish model of human blindness Hum. Mol. Genet., 20 (2011),pp. 1467-1477
    [9]
    Beales, P.L., Bland, E., Tobin, J.L. et al. Nat. Genet., 39 (2007),pp. 727-729
    [10]
    Becker-Heck, A., Zohn, I.E., Okabe, N. et al. The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation Nat. Genet., 43 (2011),pp. 79-84
    [11]
    Bedell, V.M., Wang, Y., Campbell, J.M. et al. Nature, 491 (2012),pp. 114-118
    [12]
    Ben, J., Elworthy, S., Ng, A.S. et al. Development, 138 (2011),pp. 4969-4978
    [13]
    Bisgrove, B.W., Snarr, B.S., Emrazian, A. et al. Polaris and Polycystin-2 in dorsal forerunner cells and Kupffer's vesicle are required for specification of the zebrafish left-right axis Dev. Biol., 287 (2005),pp. 274-288
    [14]
    Bizet, A.A., Becker-Heck, A., Ryan, R. et al. Nat. Commun., 6 (2015),p. 8666
    [15]
    Borovina, A., Superina, S., Voskas, D. et al. Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia Nat. Cell Biol., 12 (2010),pp. 407-412
    [16]
    Burckle, C., Gaude, H.M., Vesque, C. et al. Control of the Wnt pathways by nephrocystin-4 is required for morphogenesis of the zebrafish pronephros Hum. Mol. Genet., 20 (2011),pp. 2611-2627
    [17]
    Cantagrel, V., Silhavy, J.L., Bielas, S.L. et al. Am. J. Hum. Genet., 83 (2008),pp. 170-179
    [18]
    Cao, Y., Semanchik, N., Lee, S.H. et al. Chemical modifier screen identifies HDAC inhibitors as suppressors of PKD models Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 21819-21824
    [19]
    Caspary, T., Larkins, C.E., Anderson, K.V. The graded response to Sonic Hedgehog depends on cilia architecture Dev. Cell, 12 (2007),pp. 767-778
    [20]
    Castleman, V.H., Romio, L., Chodhari, R. et al. Am. J. Hum. Genet., 84 (2009),pp. 197-209
    [21]
    Chamling, X., Seo, S., Bugge, K. et al. PLoS One, 8 (2013),p. e59101
    [22]
    Chang, N., Sun, C., Gao, L. et al. Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos Cell Res., 23 (2013),pp. 465-472
    [23]
    Chen, J., Knowles, H.J., Hebert, J.L. et al. Mutation of the mouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry J. Clin. Invest., 102 (1998),pp. 1077-1082
    [24]
    Chiang, A.P., Beck, J.S., Yen, H.J. et al. Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 6287-6292
    [25]
    Choksi, S.P., Babu, D., Lau, D. et al. Systematic discovery of novel ciliary genes through functional genomics in the zebrafish Development, 141 (2014),pp. 3410-3419
    [26]
    Colantonio, J.R., Vermot, J., Wu, D. et al. The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear Nature, 457 (2009),pp. 205-209
    [27]
    Cole, D.G., Snell, W.J. SnapShot: intraflagellar transport Cell, 137 (2009)
    [28]
    Coppieters, F., Lefever, S., Leroy, B.P. et al. Hum. Mutat., 31 (2010),pp. 1097-1108
    [29]
    Cortellino, S., Wang, C., Wang, B. et al. Dev. Biol., 325 (2009),pp. 225-237
    [30]
    Coxam, B., Sabine, A., Bower, N.I. et al. Pkd1 regulates lymphatic vascular morphogenesis during development Cell Rep., 7 (2014),pp. 623-633
    [31]
    Craft, J.M., Harris, J.A., Hyman, S. et al. Tubulin transport by IFT is upregulated during ciliary growth by a cilium-autonomous mechanism J. Cell Biol., 208 (2015),pp. 223-237
    [32]
    Davis, E.E., Zhang, Q., Liu, Q. et al. Nat. Genet., 43 (2011),pp. 189-196
    [33]
    Delling, M., DeCaen, P.G., Doerner, J.F. et al. Primary cilia are specialized calcium signalling organelles Nature, 504 (2013),pp. 311-314
    [34]
    Duldulao, N.A., Lee, S., Sun, Z. Development, 136 (2009),pp. 4033-4042
    [35]
    Endoh-Yamagami, S., Evangelista, M., Wilson, D. et al. The mammalian Cos2 homolog Kif7 plays an essential role in modulating Hh signal transduction during development Curr. Biol., 19 (2009),pp. 1320-1326
    [36]
    Ferrante, M.I., Romio, L., Castro, S. et al. Hum. Mol. Genet., 18 (2009),pp. 289-303
    [37]
    Fogelgren, B., Lin, S.Y., Zuo, X. et al. The exocyst protein Sec10 interacts with Polycystin-2 and knockdown causes PKD-phenotypes PLoS Genet., 7 (2011),p. e1001361
    [38]
    Fowkes, M.E., Mitchell, D.R. The role of preassembled cytoplasmic complexes in assembly of flagellar dynein subunits Mol. Biol. Cell, 9 (1998),pp. 2337-2347
    [39]
    Francescatto, L., Rothschild, S.C., Myers, A.L. et al. The activation of membrane targeted CaMK-II in the zebrafish Kupffer's vesicle is required for left-right asymmetry Development, 137 (2010),pp. 2753-2762
    [40]
    Garcia-Gonzalo, F.R., Corbit, K.C., Sirerol-Piquer, M.S. et al. A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition Nat. Genet., 43 (2011),pp. 776-784
    [41]
    Gerdes, J.M., Liu, Y., Zaghloul, N.A. et al. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response Nat. Genet., 39 (2007),pp. 1350-1360
    [42]
    Gorden, N.T., Arts, H.H., Parisi, M.A. et al. Am. J. Hum. Genet., 83 (2008),pp. 559-571
    [43]
    Haddon, C., Lewis, J. J. Comp. Neurol., 365 (1996),pp. 113-128
    [44]
    Halbritter, J., Bizet, A.A., Schmidts, M. et al. Defects in the IFT-B component IFT172 cause Jeune and Mainzer-Saldino syndromes in humans Am. J. Hum. Genet., 93 (2013),pp. 915-925
    [45]
    Hao, L., Thein, M., Brust-Mascher, I. et al. Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments Nat. Cell Biol., 13 (2011),pp. 790-798
    [46]
    Harris, P.C., Torres, V.E. Polycystic kidney disease Annu. Rev. Med., 60 (2009),pp. 321-337
    [47]
    Hildebrandt, F., Attanasio, M., Otto, E. Nephronophthisis: disease mechanisms of a ciliopathy J. Am. Soc. Nephrol., 20 (2009),pp. 23-35
    [48]
    Hildebrandt, F., Benzing, T., Katsanis, N. Ciliopathies N. Engl. J. Med., 364 (2011),pp. 1533-1543
    [49]
    Hjeij, R., Onoufriadis, A., Watson, C.M. et al. Am. J. Hum. Genet., 95 (2014),pp. 257-274
    [50]
    Howe, K., Clark, M.D., Torroja, C.F. et al. The zebrafish reference genome sequence and its relationship to the human genome Nature, 496 (2013),pp. 498-503
    [51]
    Huangfu, D., Anderson, K.V. Cilia and Hedgehog responsiveness in the mouse Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 11325-11330
    [52]
    Hudak, L.M., Lunt, S., Chang, C.H. et al. The intraflagellar transport protein Ift80 is essential for photoreceptor survival in a zebrafish model of jeune asphyxiating thoracic dystrophy Invest. Ophthalmol. Vis. Sci., 51 (2010),pp. 3792-3799
    [53]
    Huet, D., Blisnick, T., Perrot, S. et al. The GTPase IFT27 is involved in both anterograde and retrograde intraflagellar transport eLife, 3 (2014),p. e02419
    [54]
    Hurd, T., Zhou, W., Jenkins, P. et al. The retinitis pigmentosa protein RP2 interacts with polycystin 2 and regulates cilia-mediated vertebrate development Hum. Mol. Genet., 19 (2010),pp. 4330-4344
    [55]
    Ishikawa, H., Marshall, W.F. Ciliogenesis: building the cell's antenna Nat. Rev. Mol. Cell Biol., 12 (2011),pp. 222-234
    [56]
    Jeanson, L., Copin, B., Papon, J.F. et al. Am. J. Hum. Genet., 97 (2015),pp. 153-162
    [57]
    Jin, H., White, S.R., Shida, T. et al. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia Cell, 141 (2010),pp. 1208-1219
    [58]
    Kardon, J.R., Vale, R.D. Regulators of the cytoplasmic dynein motor Nat. Rev. Mol. Cell Biol., 10 (2009),pp. 854-865
    [59]
    Kettleborough, R.N., Busch-Nentwich, E.M., Harvey, S.A. et al. A systematic genome-wide analysis of zebrafish protein-coding gene function Nature, 496 (2013),pp. 494-497
    [60]
    Khanna, H., Davis, E.E., Murga-Zamalloa, C.A. et al. Nat. Genet., 41 (2009),pp. 739-745
    [61]
    Kishimoto, N., Cao, Y., Park, A. et al. Dev. Cell, 14 (2008),pp. 954-961
    [62]
    Knowles, M.R., Ostrowski, L.E., Loges, N.T. et al. Am. J. Hum. Genet., 93 (2013),pp. 711-720
    [63]
    Kok, F.O., Shin, M., Ni, C.W. et al. Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish Dev. Cell, 32 (2015),pp. 97-108
    [64]
    Kramer-Zucker, A.G., Olale, F., Haycraft, C.J. et al. Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis Development, 132 (2005),pp. 1907-1921
    [65]
    Kurkowiak, M., Zietkiewicz, E., Witt, M. Recent advances in primary ciliary dyskinesia genetics J. Med. Genet., 52 (2015),pp. 1-9
    [66]
    Le Corre, S., Eyre, D., Drummond, I.A. Modulation of the secretory pathway rescues zebrafish polycystic kidney disease pathology J. Am. Soc. Nephrol., 25 (2014),pp. 1749-1759
    [67]
    Lechtreck, K.F., Witman, G.B. J. Cell Biol., 176 (2007),pp. 473-482
    [68]
    , He, M., Ocbina, P.J., Anderson, K.V. Mouse Kif7/Costal2 is a cilia-associated protein that regulates Sonic hedgehog signaling Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 13377-13382
    [69]
    Lindstrand, A., Davis, E.E., Carvalho, C.M. et al. Am. J. Hum. Genet., 94 (2014),pp. 745-754
    [70]
    Liu, A., Wang, B., Niswander, L.A. Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors Development, 132 (2005),pp. 3103-3111
    [71]
    Liu, D., Wang, Z., Xiao, A. et al. J. Genet. Genomics, 41 (2014),pp. 43-46
    [72]
    Liu, Y., Pathak, N., Kramer-Zucker, A. et al. Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros Development, 134 (2007),pp. 1111-1122
    [73]
    Lopez-Schier, H., Hudspeth, A.J. A two-step mechanism underlies the planar polarization of regenerating sensory hair cells Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 18615-18620
    [74]
    Lu, H., Toh, M.T., Narasimhan, V. et al. A function for the Joubert syndrome protein Arl13b in ciliary membrane extension and ciliary length regulation Dev. Biol., 397 (2015),pp. 225-236
    [75]
    Malicki, J., Avanesov, A., Li, J. et al. Analysis of cilia structure and function in zebrafish Methods Cell Biol., 101 (2011),pp. 39-74
    [76]
    Mangos, S., Lam, P.Y., Zhao, A. et al. Dis. Model. Mech., 3 (2010),pp. 354-365
    [77]
    Maurya, A.K., Ben, J., Zhao, Z. et al. Positive and negative regulation of Gli activity by Kif7 in the zebrafish embryo PLoS Genet., 9 (2013),p. e1003955
    [78]
    May, S.R., Ashique, A.M., Karlen, M. et al. Loss of the retrograde motor for IFT disrupts localization of Smo to cilia and prevents the expression of both activator and repressor functions of Gli Dev. Biol., 287 (2005),pp. 378-389
    [79]
    Merrick, D., Chapin, H., Baggs, J.E. et al. The gamma-secretase cleavage product of polycystin-1 regulates TCF and CHOP-mediated transcriptional activation through a p300-dependent mechanism Dev. Cell, 22 (2012),pp. 197-210
    [80]
    Mitchison, H.M., Schmidts, M., Loges, N.T. et al. Nat. Genet., 44 (2012),pp. 381-389
    [81]
    Mockel, A., Perdomo, Y., Stutzmann, F. et al. Retinal dystrophy in Bardet-Biedl syndrome and related syndromic ciliopathies Prog. Retin. Eye Res., 30 (2011),pp. 258-274
    [82]
    Mukhopadhyay, S., Wen, X., Chih, B. et al. TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia Genes Dev., 24 (2010),pp. 2180-2193
    [83]
    Nachury, M.V., Loktev, A.V., Zhang, Q. et al. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis Cell, 129 (2007),pp. 1201-1213
    [84]
    Narasimhan, V., Hjeij, R., Vij, S. et al. Hum. Mutat., 36 (2015),pp. 307-318
    [85]
    Nauli, S.M., Alenghat, F.J., Luo, Y. et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells Nat. Genet., 33 (2003),pp. 129-137
    [86]
    Ni, T.T., Lu, J., Zhu, M. et al. Conditional control of gene function by an invertible gene trap in zebrafish Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 15389-15394
    [87]
    Noone, P.G., Leigh, M.W., Sannuti, A. et al. Primary ciliary dyskinesia: diagnostic and phenotypic features Am. J. Respir. Crit. Care Med., 169 (2004),pp. 459-467
    [88]
    Olbrich, H., Schmidts, M., Werner, C. et al. Am. J. Hum. Genet., 91 (2012),pp. 672-684
    [89]
    Omori, Y., Zhao, C., Saras, A. et al. Nat. Cell Biol., 10 (2008),pp. 437-444
    [90]
    Paavola, J., Schliffke, S., Rossetti, S. et al. Polycystin-2 mutations lead to impaired calcium cycling in the heart and predispose to dilated cardiomyopathy J. Mol. Cell Cardiol., 58 (2013),pp. 199-208
    [91]
    Panizzi, J.R., Becker-Heck, A., Castleman, V.H. et al. Nat. Genet., 44 (2012),pp. 714-719
    [92]
    Parisi, M.A., Doherty, D., Chance, P.F. et al. Joubert syndrome (and related disorders) (OMIM 213300) Eur. J. Hum. Genet., 15 (2007),pp. 511-521
    [93]
    Pazour, G.J. Comparative genomics: prediction of the ciliary and basal body proteome Curr. Biol., 14 (2004),pp. R575-R577
    [94]
    Roosing, S., Hofree, M., Kim, S. et al. eLife, 4 (2015),p. e06602
    [95]
    Ross, A.J., May-Simera, H., Eichers, E.R. et al. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates Nat. Genet., 37 (2005),pp. 1135-1140
    [96]
    Rossi, A., Kontarakis, Z., Gerri, C. et al. Genetic compensation induced by deleterious mutations but not gene knockdowns Nature, 524 (2015),pp. 230-233
    [97]
    Ryan, S., Willer, J., Marjoram, L. et al. Rapid identification of kidney cyst mutations by whole exome sequencing in zebrafish Development, 140 (2013),pp. 4445-4451
    [98]
    Salonen, R., Paavola, P. Meckel syndrome J. Med. Genet., 35 (1998),pp. 497-501
    [99]
    Sang, L., Miller, J.J., Corbit, K.C. et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways Cell, 145 (2011),pp. 513-528
    [100]
    Sarmah, B., Winfrey, V.P., Olson, G.E. et al. A role for the inositol kinase Ipk1 in ciliary beating and length maintenance Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 19843-19848
    [101]
    Satir, P., Christensen, S.T. Overview of structure and function of mammalian cilia Annu. Rev. Physiol., 69 (2007),pp. 377-400
    [102]
    Sayer, J.A., Otto, E.A., O'Toole, J.F. et al. The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4 Nat. Genet., 38 (2006),pp. 674-681
    [103]
    Schaefer, E., Stoetzel, C., Scheidecker, S. et al. Identification of a novel mutation confirms the implication of IFT172 (BBS20) in Bardet-Biedl syndrome J. Hum. Genet. (2016)
    [104]
    Schmidts, M. Clinical genetics and pathobiology of ciliary chondrodysplasias J. Pediatr. Genet., 3 (2014),pp. 46-94
    [105]
    Scholey, J.M. Intraflagellar transport motors in cilia: moving along the cell's antenna J. Cell Biol., 180 (2008),pp. 23-29
    [106]
    Schottenfeld, J., Sullivan-Brown, J., Burdine, R.D. Zebrafish curly up encodes a Pkd2 ortholog that restricts left-side-specific expression of southpaw Development, 134 (2007),pp. 1605-1615
    [107]
    Serluca, F.C., Xu, B., Okabe, N. et al. Mutations in zebrafish leucine-rich repeat-containing six-like affect cilia motility and result in pronephric cysts, but have variable effects on left-right patterning Development, 136 (2009),pp. 1621-1631
    [108]
    Slanchev, K., Putz, M., Schmitt, A. et al. Nephrocystin-4 is required for pronephric duct-dependent cloaca formation in zebrafish Hum. Mol. Genet., 20 (2011),pp. 3119-3128
    [109]
    Snow, J.J., Ou, G., Gunnarson, A.L. et al. Nat. Cell Biol., 6 (2004),pp. 1109-1113
    [110]
    Stephen, L.A., Tawamie, H., Davis, G.M. et al. eLife, 4 (2015)
    [111]
    Stoetzel, C., Laurier, V., Davis, E.E. et al. Nat. Genet., 38 (2006),pp. 521-524
    [112]
    Stoetzel, C., Muller, J., Laurier, V. et al. Am. J. Hum. Genet., 80 (2007),pp. 1-11
    [113]
    Stooke-Vaughan, G.A., Huang, P., Hammond, K.L. et al. The role of hair cells, cilia and ciliary motility in otolith formation in the zebrafish otic vesicle Development, 139 (2012),pp. 1777-1787
    [114]
    Stubbs, J.L., Oishi, I., Izpisua Belmonte, J.C. et al. Nat. Genet., 40 (2008),pp. 1454-1460
    [115]
    Sukumaran, S., Perkins, B.D. Vision Res., 49 (2009),pp. 479-489
    [116]
    Sullivan-Brown, J., Schottenfeld, J., Okabe, N. et al. Dev. Biol., 314 (2008),pp. 261-275
    [117]
    Sun, Z., Amsterdam, A., Pazour, G.J. et al. A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney Development, 131 (2004),pp. 4085-4093
    [118]
    Takakura, A., Contrino, L., Beck, A.W. et al. J. Am. Soc. Nephrol., 19 (2008),pp. 2351-2363
    [119]
    Tarkar, A., Loges, N.T., Slagle, C.E. et al. DYX1C1 is required for axonemal dynein assembly and ciliary motility Nat. Genet., 45 (2013),pp. 995-1003
    [120]
    Taschner, M., Bhogaraju, S., Lorentzen, E. Architecture and function of IFT complex proteins in ciliogenesis Differentiation, 83 (2012),pp. S12-S22
    [121]
    Tayeh, M.K., Yen, H.J., Beck, J.S. et al. Genetic interaction between Bardet-Biedl syndrome genes and implications for limb patterning Hum. Mol. Genet., 17 (2008),pp. 1956-1967
    [122]
    Tran, P.V., Haycraft, C.J., Besschetnova, T.Y. et al. THM1 negatively modulates mouse sonic hedgehog signal transduction and affects retrograde intraflagellar transport in cilia Nat. Genet., 40 (2008),pp. 403-410
    [123]
    van Rooijen, E., Giles, R.H., Voest, E.E. et al. LRRC50, a conserved ciliary protein implicated in polycystic kidney disease J. Am. Soc. Nephrol., 19 (2008),pp. 1128-1138
    [124]
    Walczak-Sztulpa, J., Eggenschwiler, J., Osborn, D. et al. Am. J. Hum. Genet., 86 (2010),pp. 949-956
    [125]
    Wallingford, J.B. Planar cell polarity signaling, cilia and polarized ciliary beating Curr. Opin. Cell Biol., 22 (2010),pp. 597-604
    [126]
    Waters, A.M., Beales, P.L. Ciliopathies: an expanding disease spectrum Pediatr. Nephrol., 26 (2011),pp. 1039-1056
    [127]
    Yen, H.J., Tayeh, M.K., Mullins, R.F. et al. Bardet-Biedl syndrome genes are important in retrograde intracellular trafficking and Kupffer's vesicle cilia function Hum. Mol. Genet., 15 (2006),pp. 667-677
    [128]
    Yin, X., Takei, Y., Kido, M.A. et al. Neuron, 70 (2011),pp. 310-325
    [129]
    Young, I.D. Cranioectodermal dysplasia (Sensenbrenner's syndrome) J. Med. Genet., 26 (1989),pp. 393-396
    [130]
    Yu, X., Lau, D., Ng, C.P. et al. Cilia-driven fluid flow as an epigenetic cue for otolith biomineralization on sensory hair cells of the inner ear Development, 138 (2011),pp. 487-494
    [131]
    Yu, X., Ng, C.P., Habacher, H. et al. Foxj1 transcription factors are master regulators of the motile ciliogenic program Nat. Genet., 40 (2008),pp. 1445-1453
    [132]
    Yuan, S., Zhao, L., Brueckner, M. et al. Intraciliary calcium oscillations initiate vertebrate left-right asymmetry Curr. Biol., 25 (2015),pp. 556-567
    [133]
    Zariwala, M.A., Knowles, M.R., Omran, H. Genetic defects in ciliary structure and function Annu. Rev. Physiol., 69 (2007),pp. 423-450
    [134]
    Zhao, C., Malicki, J. Genetic defects of pronephric cilia in zebrafish Mech. Dev., 124 (2007),pp. 605-616
    [135]
    Zhao, C., Malicki, J. Nephrocystins and MKS proteins interact with IFT particle and facilitate transport of selected ciliary cargos EMBO J., 30 (2011),pp. 2532-2544
    [136]
    Zhao, C., Omori, Y., Brodowska, K. et al. Kinesin-2 family in vertebrate ciliogenesis Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 2388-2393
    [137]
    Zu, Y., Tong, X., Wang, Z. et al. TALEN-mediated precise genome modification by homologous recombination in zebrafish Nat. Methods, 10 (2013),pp. 329-331
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