Ablation of retinal ciliopathy protein RPGR results in altered photoreceptor ciliary composition

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Rao, Kollu N ^a   Li, Linjing ^a   Anand, Manisha ^a   Khanna, Hemant ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; EYE PROTEIN; RPGR PROTEIN, MOUSE;

ANIMAL; EUKARYOTIC FLAGELLUM; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; MUTATION; PATHOLOGY; PHOTORECEPTOR CELL; RETINA DISEASE;

ANIMALS; CARRIER PROTEINS; CILIA; EYE PROTEINS; MICE; MICE, KNOCKOUT; MUTATION; PHOTORECEPTOR CELLS, VERTEBRATE; RETINAL DISEASES;

EID: 84931275470     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11137     Document Type: Article

References (70)

1. Oh, E. C., Vasanth, S. , Katsanis, N. Metabolic Regulation and Energy Homeostasis through the Primary Cilium. Cell metabolism, doi:10.1016/j.cmet.2014.11.019 (2014).
2. Singla, V. , Reiter, J. F. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313, 629-633 (2006).
3. Czarnecki, P. G. , Shah, J. V. The ciliary transition zone: from morphology and molecules to medicine. Trends Cell Biol 22, 201-210, doi:10.1016/j.tcb.2012.02.001 (2012).
4. Kozminski, K. G., Johnson, K. A., Forscher, P. , Rosenbaum, J. L. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci USA 90, 5519-5523 (1993).
5. Rosenbaum, J. L. , Witman, G. B. Intraflagellar transport. Nat Rev Mol Cell Biol 3, 813-825 (2002).
6. Badano, J. L., Mitsuma, N., Beales, P. L. , Katsanis, N. The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 7, 125-148 (2006).
7. Hildebrandt, F., Benzing, T. , Katsanis, N. Ciliopathies. The New England journal of medicine 364, 1533-1543, doi:10.1056/NEJMra1010172 (2011).
8. Cheng, T. et al. The effect of peripherin/rds haploinsufficiency on rod and cone photoreceptors. JNeurosci 17, 8118-8128 (1997).
9. Insinna, C. , Besharse, J. C. Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Dev Dyn 237, 1982-1992 (2008).
10. Liu, Q. et al. The proteome of the mouse photoreceptor sensory cilium complex. Mol Cell Proteom 6, 1299-1317 (2007).
11. Anand, M. , Khanna, H. Ciliary transition zone (TZ) proteins RPGR and CEP290: role in photoreceptor cilia and degenerative diseases. Exp Opin Ther Tar 16, 541-551, doi:10.1517/14728222.2012.680956 (2012).
12. Heckenlively, J. R., Yoser, S. L., Friedman, L. H. , Oversier, J. J. Clinical findings and common symptoms in retinitis pigmentosa. Am J Ophthalmol 105, 504-511 (1988).
13. Fishman, G. A., Farber, M. D. , Derlacki, D. J. X-linked retinitis pigmentosa. Profile of clinical findings. Arch Ophthalmol 106, 369-375 (1988).
14. Meindl, A. et al. A gene (RPGR) with homology to the RCC1 guanine nucleotide exchange factor is mutated in X-linked retinitis pigmentosa (RP3). Nat Genet 13, 35-42 (1996).
15. Roepman, R. et al. Positional cloning of the gene for X-linked retinitis pigmentosa 3: homology with the guanine-nucleotideexchange factor RCC1. Hum Mol Gen 5, 1035-1041 (1996).
16. Breuer, D. K. et al. A comprehensive mutation analysis of RP2 and RPGR in a North American cohort of families with X-linked retinitis pigmentosa. Am J Hum Genet 70, 1545-1554 (2002).
17. Sharon, D. et al. X-linked retinitis pigmentosa: mutation spectrum of the RPGR and RP2 genes and correlation with visual function. Invest Ophthalmol Vis Sci 41, 2712-2721 (2000).
18. Shu, X. et al. RPGR mutation analysis and disease: an update. Hum Mutat 28, 322-328 (2007).
19. Sullivan, L. S. et al. Prevalence of mutations in eyeGENE probands with a diagnosis of autosomal dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci 54, 6255-6261, doi:10.1167/iovs.13-12605 (2013).
20. Sullivan, L. S. , Daiger, S. P. Inherited retinal degeneration: exceptional genetic and clinical heterogeneity. Mol Med Today 2, 380-386 (1996).
21. Iannaccone, A. et al. Clinical and immunohistochemical evidence for an X linked retinitis pigmentosa syndrome with recurrent infections and hearing loss in association with an RPGR mutation. J Med Genet 40, e118 (2003).
22. Koenekoop, R. K. et al. Novel RPGR mutations with distinct retinitis pigmentosa phenotypes in French-Canadian families. Am J Ophthalmol 136, 678-687 (2003).
23. Moore, A. et al. RPGR is mutated in patients with a complex X linked phenotype combining primary ciliary dyskinesia and retinitis pigmentosa. J Med Genet 43, 326-333 (2006).
24. Ayyagari, R. et al. X-linked recessive atrophic macular degeneration from RPGR mutation. Genomics 80, 166-171 (2002).
25. Hong, D. H. et al. RPGR isoforms in photoreceptor connecting cilia and the transitional zone of motile cilia. Invest Ophthalmol Vis Sci 44, 2413-2421 (2003).
26. Khanna, H. et al. RPGR-ORF15, which is mutated in retinitis pigmentosa, associates with SMC1, SMC3, and microtubule transport proteins. J Biol Chem 280, 33580-33587 (2005).
27. Murga-Zamalloa, C., Swaroop, A. , Khanna, H. Multiprotein Complexes of Retinitis Pigmentosa GTPase Regulator (RPGR), a Ciliary Protein Mutated in X-Linked Retinitis Pigmentosa (XLRP). Adv Exp Med Biol 664, 105-114, doi:10.1007/978-1-4419-1399-9-13 (2010).
28. Murga-Zamalloa, C. A., Atkins, S. J., Peranen, J., Swaroop, A. , Khanna, H. Interaction of retinitis pigmentosa GTPase regulator (RPGR) with RAB8A GTPase: implications for cilia dysfunction and photoreceptor degeneration. Hum Mol Genet 19, 3591-3598, DOI:10.1093/hmg/ddq275 (2010).
29. Roepman, R. et al. The retinitis pigmentosa GTPase regulator (RPGR) interacts with novel transport-like proteins in the outer segments of rod photoreceptors. Hum Mol Genet 9, 2095-2105 (2000).
30. Shu, X. et al. RPGR ORF15 isoform co-localizes with RPGRIP1 at centrioles and basal bodies and interacts with nucleophosmin. Hum Mol Genet 14, 1183-1197 (2005).
31. Zhao, Y. et al. The retinitis pigmentosa GTPase regulator (RPGR)-interacting protein: subserving RPGR function and participating in disk morphogenesis. Proc Natl Acad Sci USA 100, 3965-3970 (2003).
32. Hong, D. H. et al. A retinitis pigmentosa GTPase regulator (RPGR)-deficient mouse model for X-linked retinitis pigmentosa (RP3). Proc Natl Acad Sci USA 97, 3649-3654 (2000).
33. Mitton, K. P. et al. The leucine zipper of NRL interacts with the CRX homeodomain. A possible mechanism of transcriptional synergy in rhodopsin regulation. J Biol Chem 275, 29794-29799 (2000).
34. Zhang, Q. et al. Different RPGR exon ORF15 mutations in Canids provide insights into photoreceptor cell degeneration. Hum Mol Genet 11, 993-1003 (2002).
35. Thompson, D. A. et al. Rd9 is a naturally occurring mouse model of a common form of retinitis pigmentosa caused by mutations in RPGR-ORF15. PloS one 7, e35865, doi:10.1371/journal.pone.0035865 (2012).
36. Awata, J. et al. NPHP4 controls ciliary trafficking of membrane proteins and large soluble proteins at the transition zone. J Cell Sci 127, 4714-4727, doi:10.1242/jcs.155275 (2014).
37. Craige, B. et al. CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 190, 927-940, DOI: 10.1083/jcb.201006105 (2010).
38. Nachury, M. V., Seeley, E. S. , Jin, H. Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu Rev Cell Dev Biol 26, 59-87, doi:10.1146/annurev.cellbio.042308.113337 (2010).
39. Liu, Y. P. et al. Ciliopathy proteins regulate paracrine signaling by modulating proteasomal degradation of mediators. J Clin Invest, doi:10.1172/JCI71898 (2014).
40. White, C. D., Erdemir, H. H. , Sacks, D. B. IQGAP1 and its binding proteins control diverse biological functions. Cell Signal 24, 826-834, doi:10.1016/j.cellsig.2011.12.005 (2012).
41. Deretic, D. et al. rab8 in retinal photoreceptors may participate in rhodopsin transport and in rod outer segment disk morphogenesis. J Cell Sci 108 (Pt 1), 215-224 (1995).
42. Jin, H. et al. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141, 1208-1219, DOI: 10.1016/j.cell.2010.05.015 (2010).
43. Swaroop, A. What's in a name? RPGR mutations redefine the genetic and phenotypic landscape in retinal degenerative diseases. Invest Ophthalmol Vis Sci 54, 1417, doi:10.1167/iovs.13-11750 (2013).
44. Besharse, J. C., Hollyfield, J. G. , Rayborn, M. E. Turnover of rod photoreceptor outer segments. II. Membrane addition and loss in relationship to light. J Cell Biol 75, 507-527 (1977).
45. LaVail, M. M. Kinetics of rod outer segment renewal in the developing mouse retina. J Cell Biol 58, 650-661 (1973).
46. Wang, J. , Deretic, D. Molecular complexes that direct rhodopsin transport to primary cilia. Prog Ret Eye Res 38, 1-19, doi:10.1016/j.preteyeres.2013.08.004 (2014).
47. Young, R. W. Passage of newly formed protein through the connecting cilium of retina rods in the frog. J Ultrastruct Res 23, 462-473 (1968).
48. Hollingsworth, T. J. , Gross, A. K. Defective trafficking of rhodopsin and its role in retinal degenerations. Int Rev Cell Molecular Biol 293, 1-44, doi:10.1016/B978-0-12-394304-0.00006-3 (2012).
49. Calvert, P. D., Schiesser, W. E. , Pugh, E. N. Jr. Diffusion of a soluble protein, photoactivatable GFP, through a sensory cilium. J Gen Physiol 135, 173-196, DOI: 10.1085/jgp.200910322 (2010).
50. Calvert, P. D., Strissel, K. J., Schiesser, W. E., Pugh, E. N. Jr. , Arshavsky, V. Y. Light-driven translocation of signaling proteins in vertebrate photoreceptors. Trends Cell Biol 16, 560-568, doi:10.1016/j.tcb.2006.09.001 (2006).
51. Nair, K. S. et al. Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by protein-protein interactions. Neuron 46, 555-567 (2005).
52. Slepak, V. Z. , Hurley, J. B. Mechanism of light-induced translocation of arrestin and transducin in photoreceptors: interactionrestricted diffusion. IUBMB life 60, 2-9, doi:10.1002/iub.7 (2008).
53. Hurd, T. W., Fan, S. , Margolis, B. L. Localization of retinitis pigmentosa 2 to cilia is regulated by Importin beta2. J Cell Sci 124, 718-726, doi:10.1242/jcs.070839 (2011).
54. Dishinger, J. F. et al. Ciliary entry of the kinesin-2 motor KIF17 is regulated by importin-beta2 and RanGTP. Nat Cell Biol 12, 703-710, doi:10.1038/ncb2073 (2010).
55. Li, S. et al. Rescue of enzymatic function for disease-associated RPE65 proteins containing various missense mutations in nonactive sites. J Biol Chem 289, 18943-18956, doi:10.1074/jbc.M114.552117 (2014).
56. Lobanova, E. S., Finkelstein, S., Skiba, N. P. , Arshavsky, V. Y. Proteasome overload is a common stress factor in multiple forms of inherited retinal degeneration. Proc Natl Acad Sci USA 110, 9986-9991, doi:10.1073/pnas.1305521110 (2013).
57. Rome, S., Meugnier, E. , Vidal, H. The ubiquitin-proteasome pathway is a new partner for the control of insulin signaling. Curr Opin Clin Nut Metab Care 7, 249-254 (2004).
58. Bennett, R. G., Fawcett, J., Kruer, M. C., Duckworth, W. C. , Hamel, F. G. Insulin inhibition of the proteasome is dependent on degradation of insulin by insulin-degrading enzyme. J Endocrinol 177, 399-405 (2003).
59. Zheng, J. S. et al. Genetic variants at PSMD3 interact with dietary fat and carbohydrate to modulate insulin resistance. J Nut 143, 354-361, doi:10.3945/jn.112.168401 (2013).
60. Agbaga, M. P., Mandal, M. N. , Anderson, R. E. Retinal very long-chain PUFAs: new insights from studies on ELOVL4 protein. J Lipid Res 51, 1624-1642, doi:10.1194/jlr.R005025 (2010).
61. Aveldano, M. I. , Bazan, N. G. Molecular species of phosphatidylcholine,-ethanolamine,-serine, and-inositol in microsomal and photoreceptor membranes of bovine retina. J Lipid Res 24, 620-627 (1983).
62. Mazelova, J., Ransom, N., Astuto-Gribble, L., Wilson, M. C. , Deretic, D. Syntaxin 3 and SNAP-25 pairing, regulated by omega-3 docosahexaenoic acid, controls the delivery of rhodopsin for the biogenesis of cilia-derived sensory organelles, the rod outer segments. J Cell Sci 122, 2003-2013, DOI:10.1242/jcs.039982 (2009).
63. Webb, T. R. et al. Deep intronic mutation in OFD1, identified by targeted genomic next-generation sequencing, causes a severe form of X-linked retinitis pigmentosa (RP23). Hum Mol Genet 21, 3647-3654, doi:10.1093/hmg/dds194 (2012).
64. Maeda, A. et al. Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J Biol Chem 280, 18822-18832, doi:10.1074/jbc.M501757200 (2005).
65. Li, L. et al. Ablation of the X-linked retinitis pigmentosa 2 (Rp2) gene in mice results in opsin mislocalization and photoreceptor degeneration. Invest Ophthalmol Vis Sci 54, 4503-4511, doi:10.1167/iovs.13-12140 (2013).
66. Subramanian, B. A.M, Khan, N. W. , Khanna, H. Loss of Raf-1 kinase inhibitory protein delays early-onset severe retinal ciliopathy in Cep290rd16 mouse. Invest Ophthalmol Vis Sci. 14, 5788-5794, doi:10.1167/iovs.14-14954 (2014).
67. Keller, A., Nesvizhskii, A. I., Kolker, E. , Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74, 5383-5392 (2002).
68. Nesvizhskii, A. I., Keller, A., Kolker, E. , Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75, 4646-4658 (2003).
69. Ishihama, Y. et al. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics : MCP 4, 1265-1272, doi:10.1074/mcp. M500061-MCP200 (2005).
70. Smialowski, P. et al. Protein solubility: sequence based prediction and experimental verification. Bioinformatics 23, 2536-2542, doi:10.1093/bioinformatics/btl623 (2007).