Cluap1 is essential for ciliogenesis and photoreceptor maintenance in the vertebrate eye

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 7, 2014, Pages 4585-4592

  Lee, Chanjae ^a   Wallingford, John B ^a   Gross, Jeffrey M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Cilia; Cluap1; Photoreceptor degeneration; Zebrafish

Indexed keywords

CLUSTERIN; CLUSTERIN ASSOCIATED PROTEIN 1; MESSENGER RNA; MYOSIN LIGHT CHAIN 2; UNCLASSIFIED DRUG;

ACTIVE TRANSPORT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CILIOGENESIS; CLONING; CLUSTERIN ASSOCIATED PROTEIN 1 GENE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; EUKARYOTIC FLAGELLUM; GENE; GENE MUTATION; GENE SEQUENCE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTRAFLAGELLAR TRANSPORT; MUTANT; NONHUMAN; NONSENSE MUTATION; OPEN READING FRAME; PHOTORECEPTOR; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; XENOPUS LAEVIS; ZEBRA FISH;

CILIA; CLUAP1; PHOTORECEPTOR DEGENERATION; ZEBRAFISH;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CILIA; CODON, NONSENSE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENETIC VECTORS; IN SITU HYBRIDIZATION; MICROSCOPY, CONFOCAL; MORPHOGENESIS; PHOTORECEPTOR CELLS, VERTEBRATE; POLYMORPHISM, SINGLE NUCLEOTIDE; RETINAL DEGENERATION; RNA, MESSENGER; XENOPUS LAEVIS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84904795900     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-14888     Document Type: Article

References (53)

1. Wright AF, Chakarova CF, Abd El-Aziz MM, Bhattacharya SS. Photoreceptor degeneration: genetic and mechanistic dissection of a complex trait. Nat Rev Genet. 2010;11:273-284.
2. Estrada-Cuzcano A, Roepman R, Cremers FP, den Hollander AI, Mans DA. Non-syndromic retinal ciliopathies: translating gene discovery into therapy. Hum Mol Genet. 2012;21:R111-R124.
3. Wheway G, Parry DA, Johnson CA. The role of primary cilia in the development and disease of the retina. Organogenesis. 2014;10:69-85.
4. Ishikawa H, Marshall WF. Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol. 2011;12:222-234.
5. Sukumaran S, Perkins BD. Early defects in photoreceptor outer segment morphogenesis in zebrafish ift57, ift88 and ift172 intraflagellar transport mutants. Vision Res. 2009;49:479-489.
6. Tsujikawa M, Malicki J. Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron. 2004;42:703-716.
7. Pazour GJ, Baker SA, Deane JA, et al. The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J Cell Biol. 2002;157:103-113.
8. Hudak LM, Lunt S, Chang CH, 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. 2010;51:3792-3799.
9. Krock BL, Perkins BD. The intraflagellar transport protein IFT57 is required for cilia maintenance and regulates IFTparticle-kinesin-II dissociation in vertebrate photoreceptors.J Cell Sci. 2008;121:1907-1915.
10. Beales PL, Bland E, Tobin JL, et al. IFT80, which encodes a conserved intraflagellar transport protein, is mutated in Jeune asphyxiating thoracic dystrophy. Nat Genet. 2007;39:727-729.
11. Ishikura H, Ikeda H, Abe H, et al. Identification of CLUAP1 as a human osteosarcoma tumor-associated antigen recognized by the humoral immune system. Int J Oncol. 2007;30:461-467.
12. Takahashi M, Lin YM, Nakamura Y, Furukawa Y. Isolation and characterization of a novel gene CLUAP1 whose expression is frequently upregulated in colon cancer. Oncogene. 2004;23: 9289-9294.
13. Li J, Sun Z. Qilin is essential for cilia assembly and normal kidney development in zebrafish. PLoS One. 2011;6:e27365.
14. Sun Z, Amsterdam A, Pazour GJ, Cole DG, Miller MS, Hopkins N. A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development. 2004;131: 4085-4093.
15. Pasek RC, Berbari NF, Lewis WR, Kesterson RA, Yoder BK. Mammalian Clusterin associated protein 1 is an evolutionarily conserved protein required for ciliogenesis. Cilia. 2012;1:20.
16. Botilde Y, Yoshiba S, Shinohara K, et al. Cluap1 localizes preferentially to the base and tip of cilia and is required for ciliogenesis in the mouse embryo. Dev Biol. 2013;381:203-212.
17. Murayama T, Toh Y, Ohshima Y, Koga M. The dyf-3 gene encodes a novel protein required for sensory cilium formation in Caenorhabditis elegans. J Mol Biol. 2005;346:677-687.
18. Ou G, Qin H, Rosenbaum JL, Scholey JM. The PKD protein qilin undergoes intraflagellar transport. Curr Biol. 2005;15: R410-R411.
19. Boldt K, Mans DA, Won J, et al. Disruption of intraflagellar protein transport in photoreceptor cilia causes Leber congenital amaurosis in humans and mice. J Clin Invest. 2011;121: 2169-2180.
20. Westerfield M. TheZebrafishBook:AGuideforthe Laboratory use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press; 1995.
21. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203:253-310.
22. Sive HLG, Harland, RM. Early Development ofXenopus laevis: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2000.
23. Lee J, Cox BD, Daly CM, et al. An ENU mutagenesis screen in zebrafish for visual system mutants identifies a novel spliceacceptor site mutation in patched2 that results in Colobomas. Invest Ophthalmol Vis Sci. 2012;53:8214-8221.
24. Obholzer N, Swinburne IA, Schwab E, Nechiporuk AV, Nicolson T, Megason SG. Rapid positional cloning of zebrafish mutations by linkage and homozygosity mapping using wholegenome sequencing. Development. 2012;139:4280-4290.
25. Brooks ER, Wallingford JB. Control of vertebrate intraflagellar transport by the planar cell polarity effector Fuz. J Cell Biol. 2012;198:37-45.
26. Uribe RA, Gross JM. Immunohistochemistry on cryosections from embryonic and adult zebrafish eyes. CSH Protoc. 2007; 2007;pdb. prot4779.
27. Jowett T, Lettice L. Whole-mount in situ hybridizations on zebrafish embryos using a mixture of digoxigenin-and fluorescein-labelled probes. Trends Genet. 1994;10:73-74.
28. Yelon D, Horne SA, Stainier DY. Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev Biol. 1999;214:23-37.
29. Novarino G, Akizu N, Gleeson JG. Modeling human disease in humans: the ciliopathies. Cell. 2011;147:70-79.
30. Badano JL, Mitsuma N, Beales PL, Katsanis N. The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet. 2006;7:125-148.
31. Raymond PA, Barthel LK, Curran GA. Developmental patterning of rod and cone photoreceptors in embryonic zebrafish. J Comp Neurol. 1995;359:537-550.
32. Snow JJ, Ou G, Gunnarson AL, et al. Two anterograde intraflagellar transport motors cooperate to build sensory cilia onC. elegansneurons. Nat Cell Biol. 2004;6:1109-1113.
33. Pan X, Ou G, Civelekoglu-Scholey G, et al. Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors. J Cell Biol. 2006;174: 1035-1045.
34. Werner ME, Mitchell BJ. Understanding ciliated epithelia: the power ofXenopus. Genesis. 2012;50:176-185.
35. Chung MI, Kwon T, Tu F, et al. Coordinated genomic control of ciliogenesis and cell movement by RFX2. Elife. 2014;3:e01439.
36. Brooks ER, Wallingford JB. The small GTPase Rsg1 is important for the cytoplasmic localization and axonemal dynamics of intraflagellar transport proteins. Cilia. 2013;2:13.
37. Follit JA, Xu F, Keady BT, Pazour GJ. Characterization of mouse IFT complex B. Cell Motil Cytoskeleton. 2009;66:457-468.
38. Rachel RA, Li T, Swaroop A. Photoreceptor sensory cilia and ciliopathies: focus on CEP290, RPGR and their interacting proteins. Cilia. 2012;1:22.
39. Baker K, Beales PL. Making sense of cilia in disease: the human ciliopathies. Am J Med Genet C Semin Med Genet. 2009;151C: 281-295.
40. Duldulao NA, Lee S, Sun Z. Cilia localization is essential for in vivo functions of the Joubert syndrome protein Arl13b/ Scorpion. Development. 2009;136:4033-4042.
41. Pretorius PR, Aldahmesh MA, Alkuraya FS, Sheffield VC, Slusarski DC. Functional analysis of BBS3 A89V that results in non-syndromic retinal degeneration. Hum Mol Genet. 2011; 20:1625-1632.
42. Sayer JA, Otto EA, O'Toole JF, et al. The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat Genet. 2006;38:674-681.
43. Baye LM, 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. 2011; 20:1467-1477.
44. Miller KA, Ah-Cann CJ, Welfare MF, et al. Cauli: a mouse strain with an Ift140 mutation that results in a skeletal ciliopathy modelling Jeune syndrome. PLoS Genet. 2013;9:e1003746.
45. Lehman JM, Michaud EJ, Schoeb TR, Aydin-Son Y, Miller M, Yoder BK. The Oak Ridge Polycystic Kidney mouse: modeling ciliopathies of mice and men. Dev Dyn. 2008;237:1960-1971.
46. Ashe A, Butterfield NC, Town L, et al. Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies. Hum Mol Genet. 2012;21:1808-1823.
47. Chaya T, Omori Y, Kuwahara R, Furukawa T. ICK is essential for cell type-specific ciliogenesis and the regulation of ciliary transport. EMBO J. 2014;33:1227-1242.
48. Lahiry P, Wang J, Robinson JF, et al. A multiplex human syndrome implicates a key role for intestinal cell kinase in development of central nervous, skeletal, and endocrine systems. Am J Hum Genet. 2009;84:134-147.
49. Tran PV, Haycraft CJ, Besschetnova TY, et al. THM1 negatively modulates mouse sonic hedgehog signal transduction and affects retrograde intraflagellar transport in cilia. Nat Genet. 2008;40:403-410.
50. QinJ, LinY, NormanRX, KoHW, EggenschwilerJT. Intraflagellar transport protein 122 antagonizes Sonic Hedgehog signaling and controls ciliary localization of pathway components. Proc Natl Acad Sci U S A. 2011;108:1456-1461.
51. Huangfu D, Anderson KV. Cilia and Hedgehog responsiveness in the mouse. Proc Natl Acad Sci U S A. 2005;102:11325-11330.
52. Texier Y, Toedt G, Gorza M, et al. Elution profile analysis of SDS-induced subcomplexes by quantitative mass spectrometry. Mol Cell Proteomics. 2014;13:1382-1391.
53. Schou KB, Andersen JS, Pedersen LB. A divergent calponin homology (NN-CH) domain defines a novel family: implications for evolution of ciliary IFT complex B proteins. Bioinformatics. 2014;30:899-902.