Disruption of intraflagellar protein transport in photoreceptor cilia causes Leber congenital amaurosis in humans and mice

Journal of Clinical Investigation

Volumn 121, Issue 6, 2011, Pages 2169-2180

  Boldt, Karsten ^a,b   Mans, Dorus A ^c,d   Won, Jungyeon ^e   Van Reeuwijk, Jeroen ^c,d   Vogt, Andreas ^a,b   Kinkl, Norbert ^a,b   Letteboer, Stef J F ^c,d   Hicks, Wanda L ^e   Hurd, Ron E ^e   Naggert, Jürgen K ^e   Texier, Yves ^a,b   Den Hollander, Anneke I ^c,d,f   Koenekoop, Robert K ^g   Bennett, Jean ^h,i   Cremers, Frans P M ^c,d   Gloeckner, Christian J ^a,b   Nishina, Patsy M ^e   Roepman, Ronald ^c,d,f   Ueffing, Marius ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e JACKSON LABORATORY   (United States)

^f RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^g MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^h UNIVERSITY OF PENNSYLVANIA   (United States)

ⁱ CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEBERCILIN; OPSIN; RETINA S ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; EUKARYOTIC FLAGELLUM; GENE MUTATION; HUMAN; HUMAN CELL; LEBER CONGENITAL AMAUROSIS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

ANIMALS; ARRESTINS; CELL LINE; DISEASE MODELS, ANIMAL; EYE PROTEINS; HUMANS; LEBER CONGENITAL AMAUROSIS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MULTIPROTEIN COMPLEXES; OPSINS; PHOTORECEPTOR CONNECTING CILIUM; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; ROD CELL OUTER SEGMENT; VISION, OCULAR;

EID: 79957915102     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45627     Document Type: Article

References (52)

1. den Hollander AI, Black A, Bennett J, Cremers FP. Lighting a candle in the dark: advances in genetics and gene therapy of recessive retinal dystrophies. J Clin Invest. 2010;120(9):3042-3053.
2. Estrada-Cuzcano A, et al. IQCB1 mutations in patients with Leber congenital amaurosis. Invest Ophthalmol Vis Sci. 2011;52(2):834-839.
3. den Hollander AI, Roepman R, Koenekoop RK, Cremers FP. Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog Retin Eye Res. 2008;27(4):391-419.
4. den Hollander AI, et al. Mutations in LCA5, encoding the ciliary protein lebercilin, cause Leber congenital amaurosis. Nat Genet. 2007;39(7):889-895.
5. Blacque OE, Cevik S, Kaplan OI. Intraflagellar transport: from molecular characterisation to mechanism. Front Biosci. 2008;13:2633-2652. (Pubitemid 351599709)
6. Qin H, Diener DR, Geimer S, Cole DG, Rosenbaum JL. Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J Cell Biol. 2004;164(2):255-266. (Pubitemid 38133945)
7. Rosenbaum JL, Witman GB. Intraflagellar transport. Nat Rev Mol Cell Biol. 2002;3(11):813-825. (Pubitemid 35285272)
8. Scholey JM. Intraflagellar transport. Annu Rev Cell Dev Biol. 2003;19:423-443. (Pubitemid 37487355)
9. Piperno G, Siuda E, Henderson S, Segil M, Vaananen H, Sassaroli M. Distinct mutants of retrograde intraflagellar transport (IFT) share similar morphological and molecular defects. J Cell Biol. 1998;143(6):1591-1601. (Pubitemid 29006505)
10. Piperno G, Mead K. Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagella. Proc Natl Acad Sci U S A. 1997;94(9):4457-4462. (Pubitemid 27194263)
11. Young RW. The renewal of photoreceptor cell outer segments. J Cell Biol. 1967;33(1):61-72.
12. Won J, et al. RPGRIP1 is essential for normal rod photoreceptor outer segment elaboration and morphogenesis. Hum Mol Genet. 2009;18(22):4329-4339.
13. Chang B, et al. In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet. 2006;15(11):1847-1857. (Pubitemid 43821775)
14. Gloeckner CJ, Boldt K, Schumacher A, Roepman R, Ueffing M. A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics. 2007;7(23):4228-4234. (Pubitemid 350250468)
15. Ong SE, et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics. 2002;1(5):376-386.
16. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26(12):1367-1372.
17. Cole DG, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol. 1998;141(4):993-1008. (Pubitemid 28243966)
18. Adhiambo C, Blisnick T, Toutirais G, Delannoy E, Bastin P. A novel function for the atypical small G protein Rab-like 5 in the assembly of the trypanosome flagellum. J Cell Sci. 2009;122(pt 6):834-841.
19. Blacque OE, et al. Functional genomics of the cilium, a sensory organelle. Curr Biol. 2005;15(10):935-941. (Pubitemid 40772063)
20. Li C, et al. An essential role for DYF-11/MIP-T3 in assembling functional intraflagellar transport complexes. PLoS Genet. 2008;4(3):e1000044.
21. Ou G, Blacque OE, Snow JJ, Leroux MR, Scholey JM. Functional coordination of intraflagellar transport motors. Nature. 2005;436(7050):583-587. (Pubitemid 41112934)
22. Schafer JC, Winkelbauer ME, Williams CL, Haycraft CJ, Desmond RA, Yoder BK. IFTA-2 is a conserved cilia protein involved in pathways regulating longevity and dauer formation in Caenorhabditis elegans. J Cell Sci. 2006;119(pt 19):4088-4100. (Pubitemid 44650881)
23. 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(3):677-687. (Pubitemid 40247710)
24. Omori Y, et al. Elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8. Nat Cell Biol. 2008;10(4):437-444.
25. Wang Z, Fan ZC, Williamson SM, Qin H. Intraflagellar transport (IFT) protein IFT25 is a phosphoprotein component of IFT complex B and physically interacts with IFT27 in Chlamydomonas. PLoS One. 2009;4(5):e5384.
26. Follit JA, Xu F, Keady BT, Pazour GJ. Characterization of mouse IFT complex B. Cell Motil Cytoskeleton. 2009;66(8):457-468.
27. Behm-Ansmant I, Izaurralde E. Quality control of gene expression: a stepwise assembly pathway for the surveillance complex that triggers nonsense-mediated mRNA decay. Genes Dev. 2006;20(4):391-398. (Pubitemid 43244392)
28. Kunitomo H, Iino Y. Caenorhabditis elegans DYF-11, an orthologue of mammalian Traf3ip1/MIP-T3, is required for sensory cilia formation. Genes Cells. 2008;13(1):13-25.
29. Insinna C, Besharse JC. Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Dev Dyn. 2008;237(8):1982-1992.
30. Pasadhika S, et al. Differential macular morphology in patients with RPE65-, CEP290-, GUCY2D-, and AIPL1-related Leber congenital amaurosis. Invest Ophthalmol Vis Sci. 2010;51(5):2608-2614.
31. Cideciyan AV, et al. Centrosomal-ciliary gene CEP290/NPHP6 mutations result in blindness with unexpected sparing of photoreceptors and visual brain: implications for therapy of Leber congenital amaurosis. Hum Mutat. 2007;28(11):1074-1083. (Pubitemid 350036911)
32. Jacobson SG, et al. Leber congenital amaurosis caused by Lebercilin (LCA5) mutation: retained photoreceptors adjacent to retinal disorganization. Mol Vis. 2009;15:1098-1106.
33. Jacobson SG, et al. Leber congenital amaurosis caused by an RPGRIP1 mutation shows treatment potential. Ophthalmology. 2007;114(5):895-898. (Pubitemid 46656404)
34. Liu Q, et al. The proteome of the mouse photoreceptor sensory cilium complex. Mol Cell Proteomics. 2007;6(8):1299-1317. (Pubitemid 47365430)
35. Coene KL, et al. OFD1 is mutated in X-linked Joubert syndrome and interacts with LCA5-encoded lebercilin. Am J Hum Genet. 2009;85(4):465-481.
36. Li Y, et al. Resequencing of 200 human exomes identifies an excess of low-frequency non-synonymous coding variants. Nat Genet. 2010;42(11):969-972.
37. Pazour GJ, et al. The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J Cell Biol. 2002;157(1):103-113. (Pubitemid 34847833)
38. Marszalek JR, et al. Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell. 2000;102(2):175-187.
39. Krock BL, Perkins BD. The intraflagellar transport protein IFT57 is required for cilia maintenance and regulates IFT-particle-kinesin-II dissociation in vertebrate photoreceptors. J Cell Sci. 2008;121(pt 11):1907-1915. (Pubitemid 351943384)
40. Lechtreck KF, et al. The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J Cell Biol. 2009;187(7):1117-1132.
41. Beales PL, et al. IFT80, which encodes a conserved intraflagellar transport protein, is mutated in Jeune asphyxiating thoracic dystrophy. Nat Genet. 2007;39(6):727-729. (Pubitemid 46848589)
42. Khanna H, et al. RPGR-ORF15, which is mutated in retinitis pigmentosa, associates with SMC1, SMC3, and microtubule transport proteins. J Biol Chem. 2005;280(39):33580-33587. (Pubitemid 41397159)
43. Gilissen C, et al. Exome sequencing identifies WDR35 variants involved in Sensenbrenner syndrome. Am J Hum Genet. 2010;87(3):418-423.
44. Walczak-Sztulpa J, et al. Cranioectodermal Dysplasia, Sensenbrenner syndrome, is a ciliopathy caused by mutations in the IFT122 gene. Am J Hum Genet. 2010;86(6):949-956.
45. Collin GB, et al. Alms1-disrupted mice recapitulate human Alstrom syndrome. Hum Mol Genet. 2005;14(16):2323-2333. (Pubitemid 41417995)
46. Wall FE, Henkel RD, Stern MP, Jenson HB, Moyer MP. An efficient method for routine Epstein-Barr virus immortalization of human B lymphocytes. In Vitro Cell Dev Biol Anim. 1995;31(2):156-159.
47. Gloeckner CJ, Boldt K, Ueffing M. Strep/FLAG tandem affinity purification (SF-TAP) to study protein interactions. Curr Protoc Protein Sci. 2009; Chapter 19:Unit19.20.
48. Bendall SC, Hughes C, Stewart MH, Doble B, Bhatia M, Lajoie GA. Prevention of amino acid conversion in SILAC experiments with embryonic stem cells. Mol Cell Proteomics. 2008;7(9):1587-1597.
49. van Wijk E, et al. Usher syndrome and Leber congenital amaurosis are molecularly linked via a novel isoform of the centrosomal ninein-like protein. Hum Mol Genet. 2009;18(1):51-64.
50. Olsen JV, et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics. 2005;4(12):2010-2021. (Pubitemid 41830195)
51. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365-386.
52. Arts HH, et al. Mutations in the gene encoding the basal body protein RPGRIP1L, a nephrocystin-4 interactor, cause Joubert syndrome. Nat Genet. 2007;39(7):882-888. (Pubitemid 47014499)