Pathogenic NPHP5 mutations impair protein interaction with Cep290, a prerequisite for ciliogenesis

Human Molecular Genetics

Volumn 22, Issue 12, 2013, Pages 2482-2494

  Barbelanne, Marine ^a,b   Song, Jenny ^a   Ahmadzai, Mustafa ^a   Tsang, William Y ^a,b,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN CEP290; UNCLASSIFIED DRUG;

ARTICLE; CENTRIOLE; CENTROSOME; CILIOGENESIS; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; GENE; GENE MUTATION; HUMAN; HUMAN CELL; NPHP5 GENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INTERACTION;

ANTIGENS, NEOPLASM; CALMODULIN-BINDING PROTEINS; CELL LINE; CENTRIOLES; CILIA; HUMANS; KIDNEY DISEASES, CYSTIC; LEBER CONGENITAL AMAUROSIS; MUTATION; NEOPLASM PROTEINS; OPTIC ATROPHIES, HEREDITARY; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84878478625     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt100     Document Type: Article

References (37)

1. Brito, D.A., Gouveia, S.M. and Bettencourt-Dias, M. (2012) Deconstructing the centriole: structure and number control. Curr. Opin. Cell Biol., 24, 4-13.
2. Nigg, E.A. and Stearns, T. (2011) The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries. Nat. Cell Biol., 13, 1154-1160.
3. Ishikawa, H. and Marshall, W.F. (2011) Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol., 12, 222-234.
4. Avasthi, P. and Marshall, W.F. (2012) Stages of ciliogenesis and regulation of ciliary length. Differentiation, 83, S30-42.
5. Pedersen, L.B., Veland, I.R., Schroder, J.M. and Christensen, S.T. (2008) Assembly of primary cilia. Dev. Dyn., 237, 1993-2006.
6. Hildebrandt, F., Benzing, T. and Katsanis, N. (2011) Ciliopathies. N. Engl. J. Med., 364, 1533-1543.
7. Bettencourt-Dias, M., Hildebrandt, F., Pellman, D., Woods, G. and Godinho, S.A. (2011) Centrosomes and cilia in human disease. Trends Genet., 27, 307-315.
8. Sayer, J.A., Otto, E.A., O'Toole, J.F., Nurnberg, G., Kennedy, M.A., Becker, C., Hennies, H.C., Helou, J., Attanasio, M., Fausett, B.V. et al. (2006) The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat. Genet., 38, 674-681.
9. Coppieters, F., Lefever, S., Leroy, B.P. and De Baere, E. (2010) CEP290, a gene with many faces: mutation overview and presentation of CEP290base. Hum. Mutat., 31, 1097-1108.
10. Valente, E.M., Silhavy, J.L., Brancati, F., Barrano, G., Krishnaswami, S.R., Castori, M., Lancaster, M.A., Boltshauser, E., Boccone, L.,Al-Gazali, L. et al. (2006) Mutations in CEP290, which encodes a centrosomal protein, cause pleiotropic forms of Joubert syndrome. Nat. Genet., 38, 623-625.
11. Kim, J., Krishnaswami, S.R. and Gleeson, J.G. (2008) CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum. Mol. Genet., 17, 3796-3805.
12. Tsang, W.Y., Bossard, C., Khanna, H., Peranen, J., Swaroop, A., Malhotra, V. and Dynlacht, B.D. (2008) CP110 suppresses primary cilia formation through its interaction with CEP290, a protein deficient in human ciliary disease. Dev. Cell, 15, 187-197.
13. Graser, S., Stierhof, Y.D., Lavoie, S.B., Gassner, O.S., Lamla, S., Le Clech, M. and Nigg, E.A. (2007) Cep164, a novel centriole appendage protein required for primary cilium formation. J. Cell Biol., 179, 321-330.
14. Spektor, A., Tsang, W.Y., Khoo, D. and Dynlacht, B.D. (2007) Cep97 and CP110 suppress a cilia assembly program. Cell, 130, 678-690.
15. Otto, E.A., Loeys, B., Khanna, H., Hellemans, J., Sudbrak, R., Fan, S., Muerb, U., O'Toole, J.F., Helou, J., Attanasio, M. et al. (2005) Nephrocystin-5, a ciliary IQ domain protein, is mutated in Senior-Loken syndrome and interacts with RPGR and calmodulin. Nat. Genet., 37, 282-288.
16. Otto, E.A., Helou, J., Allen, S.J., O'Toole, J.F., Wise, E.L., Ashraf, S., Attanasio, M., Zhou, W., Wolf, M.T. and Hildebrandt, F. (2008) Mutation analysis in nephronophthisis using a combined approach of homozygosity mapping, CEL I endonuclease cleavage, and direct sequencing. Hum. Mutat., 29, 418-426.
17. Stone, E.M., Cideciyan, A.V., Aleman, T.S., Scheetz, T.E., Sumaroka, A., Ehlinger, M.A., Schwartz, S.B., Fishman, G.A., Traboulsi, E.I., Lam, B.L. et al. (2011) Variations in NPHP5 in patients with nonsyndromic leber congenital amaurosis and Senior-Loken syndrome. Arch. Ophthalmol., 129, 81-87.
18. Estrada-Cuzcano, A., Koenekoop, R.K., Coppieters, F., Kohl, S., Lopez, I., Collin, R.W., De Baere, E.B., Roeleveld, D., Marek, J., Bernd, A. et al. (2011) IQCB1 mutations in patients with leber congenital amaurosis. Invest. Ophthalmol. Vis. Sci., 52, 834-839.
19. Schafer, T., Putz, M., Lienkamp, S., Ganner, A., Bergbreiter, A., Ramachandran, H., Gieloff, V., Gerner, M., Mattonet, C., Czarnecki, P.G. et al. (2008) Genetic and physical interaction between the NPHP5 and NPHP6 gene products. Hum. Mol. Genet., 17, 3655-3662.
20. Chang, B., Khanna, H., Hawes, N., Jimeno, D., He, S., Lillo, C., Parapuram, S.K., Cheng, H., Scott, A., Hurd, R.E. et al. (2006) 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., 15, 1847-1857.
21. Sang, L., Miller, J.J., Corbit, K.C., Giles, R.H., Brauer, M.J., Otto, E.A., Baye, L.M., Wen, X., Scales, S.J., Kwong, M. et al. (2011) Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell, 145, 513-528.
22. Luo, X., He, Q., Huang, Y. and Sheikh, M.S. (2005) Cloning and characterization of a p53 and DNA damage down-regulated gene PIQ that codes for a novel calmodulin-binding IQ motif protein and is up-regulated in gastrointestinal cancers. Cancer Res., 65, 10725-10733.
23. Otto, E.A., Hurd, T.W., Airik, R., Chaki, M., Zhou, W., Stoetzel, C., Patil, S.B., Levy, S., Ghosh, A.K., Murga-Zamalloa, C.A. et al. (2010)Candidate exome capture identifies mutation of SDCCAG8 as the cause of a retinal-renal ciliopathy. Nat. Genet., 42, 840-850.
24. Kim, J., Lee, J.E., Heynen-Genel, S., Suyama, E., Ono, K., Lee, K., Ideker, T., Aza-Blanc, P. and Gleeson, J.G. (2010) Functional genomic screen for modulators of ciliogenesis and cilium length. Nature, 464, 1048-1051.
25. Dawe, H.R., Smith, U.M., Cullinane, A.R., Gerrelli, D., Cox, P., Badano, J.L., Blair-Reid, S., Sriram, N., Katsanis, N., Attie-Bitach, T. et al. (2007) The Meckel-Gruber Syndrome proteins MKS1 and meckelin interact and are required for primary cilium formation. Hum. Mol. Genet., 16, 173-186.
26. Chaki, M., Hoefele, J., Allen, S.J., Ramaswami, G., Janssen, S., Bergmann, C., Heckenlively, J.R., Otto, E.A. and Hildebrandt, F. (2011) Genotype-phenotype correlation in 440 patients with NPHP-related ciliopathies. Kidney Int., 80, 1239-1245.
27. Wang, X., Wang, H., Cao, M., Li, Z., Chen, X., Patenia, C., Gore, A., Abboud, E.B., Al-Rajhi, A.A., Lewis, R.A. et al. (2011) Whole-exome sequencing identifies ALMS1, IQCB1, CNGA3, and MYO7A mutations in patients with Leber congenital amaurosis. Hum. Mutat., 32, 1450-1459.
28. Otto, E.A., Ramaswami, G., Janssen, S., Chaki, M., Allen, S.J., Zhou, W., Airik, R., Hurd, T.W., Ghosh, A.K., Wolf, M.T. et al. (2011) Mutation analysis of 18 nephronophthisis associated ciliopathy disease genes using a DNA pooling and next generation sequencing strategy. J. Med. Genet., 48, 105-116.
29. Fahim, A.T., Bowne, S.J., Sullivan, L.S., Webb, K.D., Williams, J.T., Wheaton, D.K., Birch, D.G. and Daiger, S.P. (2011) Allelic heterogeneity and genetic modifier loci contribute to clinical variation in males with X-linked retinitis pigmentosa due to RPGR mutations. PLoS One, 6, e23021.
30. Kobayashi, T., Tsang, W.Y., Li, J., Lane, W. and Dynlacht, B.D. (2011) Centriolar kinesin Kif24 interacts with CP110 to remodel microtubules and regulate ciliogenesis. Cell, 145, 914-925.
31. Gakovic, M., Shu, X., Kasioulis, I., Carpanini, S., Moraga, I. and Wright, A.F. (2011) The role of RPGR in cilia formation and actin stability. Hum. Mol. Genet., 20, 4840-4850.
32. Stowe, T.R., Wilkinson, C.J., Iqbal, A. and Stearns, T. (2012) The centriolar satellite proteins Cep72 and Cep290 interact and are required for recruitment of BBS proteins to the cilium. Mol. Biol. Cell, 23, 3322-3335.
33. Lopes, C.A., Prosser, S.L., Romio, L., Hirst, R.A., O'Callaghan, C., Woolf, A.S. and Fry, A.M. (2011) Centriolar satellites are assembly points for proteins implicated in human ciliopathies, including oral-facial-digital syndrome 1. J. Cell Sci., 124, 600-612.
34. Singla, V., Romaguera-Ros, M., Garcia-Verdugo, J.M. and Reiter, J.F. (2010) Ofd1, a human disease gene, regulates the length and distal structure of centrioles. Dev. Cell, 18, 410-424.
35. Hard, T. and Lendel, C. (2012) Inhibition of amyloid formation. J. Mol. Biol., 421, 441-465.
36. Wakatsuki, T., Schwab, B., Thompson, N.C. and Elson, E.L. (2001) Effects of cytochalasin D and latrunculin B on mechanical properties of cells. J. Cell Sci., 114, 1025-1036.
37. Schultze, A. and Fiedler, W. (2010) Therapeutic potential and limitations of new FAK inhibitors in the treatment of cancer. Expert Opin. Investig. Drugs, 19, 777-788.