Limited proteolysis differentially modulates the stability and subcellular localization of domains of RPGRIP1 that are distinctly affected by mutations in Leber's congenital amaurosis

Human Molecular Genetics

Volumn 14, Issue 10, 2005, Pages 1327-1340

  Lu, Xinrong ^a   Guruju, Mallikarjuna ^a   Oswald, John ^a   Ferreira, Paulo A ^a,b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; REGULATOR PROTEIN; RETINITIS PIGMENTOSA GTPASE REGULATOR INTERACTING PROTEIN 1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; GENE MUTATION; HEAT SHOCK; HOMOZYGOSITY; HUMAN; IN VIVO STUDY; LEBER CONGENITAL AMAUROSIS; NONHUMAN; OSMOSIS; PATHOGENESIS; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

ANIMALS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; OPTIC ATROPHY, HEREDITARY, LEBER; PROTEIN ISOFORMS; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEINS; TRANSFECTION;

EID: 19744371800     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddi143     Document Type: Article

References (45)

1. Breuer, D.K., Yashar, B.M., Filippova, E., Hiriyanna, S., Lyons, R.H., Mears, A.J., Asaye, B., Acar, C., Vervoort, R., Wright, A.F. et al. (2002) 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.
2. Yang, Z., Peachey, N.S., Moshfeghi, D.M., Thirumalaichary, S., Chorich, L., Shugart, Y.Y., Fan, K. and Zhang, K. (2002) Mutations in the RPGR gene cause X-linked cone dystrophy. Hum. Mol. Genet., 11, 605-611.
3. Demirci, F.Y., Rigatti, B.W., Wen, G., Radak, A.L., Mah, T.S., Baic, C.L., Traboulsi, E.I., Alitalo, T., Ramser, J. and Gorin, M.B. (2002) X-linked cone-rod dystrophy (locus COD1): identification of mutations in RPGR exon ORF15. Am. J. Hum. Genet., 70, 1049-1053.
4. Ayyagari, R., Demirci, F.Y., Liu, J., Bingham, E.L., Stringham, H., Kakuk, L.E., Boehnke, M., Gorin, M.B., Richards, J.E. and Sieving, P.A. (2002) X-linked recessive atrophic macular degeneration from RPGR mutation. Genomics, 80, 166-171.
5. Iannaccone, A., Breuer, D.K., Wang, X.F., Kuo, S.F., Normando, E.M., Filippova, E., Baldi, A., Hiriyanna, S., MacDonald, C.B., Baldi, F. et al. (2003) 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.
6. Koenekoop, R.K., Loyer, M., Hand, C.K., Al Mahdi, H., Dembinska, O., Beneish, R., Racine, J. and Rouleau, G.A. (2003) Novel RPGR mutations with distinct retinitis pigmemosa phenotypes in French-Canadian families. Am. J. Ophthalmol., 136, 678-687.
7. Zito, I., Downes, S.M., Patel, R.J., Cheetham, M.E., Ebenezer, N.D., Jenkins, S.A., Bhattacharya, S.S., Webster, A.R., Holder, G.E., Bird, A.C. et al. (2003) RPGR mutation associated with retinitis pigmentosa, impaired hearing, and sinorespiratory infections. J. Med. Genet., 40, 609-615.
8. Meindl, A., Dry, K., Herrmann, K., Manson, F., Ciccodicola, A., Edgar, A., Carvalho, M.R., Achatz, H., Hellebrand, H., Lennon, A. et al. (1996) 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.
9. Roepman, R., van Duijnhoven, G., Rosenberg, T., Pinckers, A.J., Bleeker-Wagemakers, L.M., Bergen, A.A., Post, J., Beck, A., Reinhardt, R., Ropers, H.H. et al. (1996) Positional cloning of the gene for X-linked retinitis pigmentosa 3: homology with the guanine-nucleotide-exchange factor RCC1. Hum. Mol. Genet., 5, 1035-1041.
10. Vervoort, R., Lennon, A., Bird, A.C., Tulloch, B., Axton, R., Miano, M.G., Meindl, A., Meitinger, T., Ciccodicola, A. and Wright, A.F. (2000) Mutational hot spot within a new RPGR exon in X-linked retinitis pigmentosa. Nat. Genet., 25, 462-466.
11. Bischoff, F.R. and Ponstingl, H. (1991) Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature, 354, 80-82.
12. Yan, D., Swain, P.K., Breuer, D., Tucker, R.M., Wu, W., Fujita, R., Rehemtulla, A., Burke, D. and Swaroop, A. (1998) Biochemical characterization and subcellular localization of the mouse retinitis pigmentosa GTPase regulator (mRpgr). J. Biol. Chem., 273, 19656-19663.
13. Roepman, R., Bernoud-Hubac, N., Schick, D.E., Maugeri, A., Berger, W., Ropers, H.H., Cremers, F.P. and Ferreira, P.A. (2000) 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.
14. Roepman, R., Schick, D. and Ferreira, P.A. (2000) Isolation of retinal proteins that interact with retinitis pigmentosa GTPase regulator by interaction trap screen in yeast. Methods Enzymol., 316, 688-704.
15. Boylan, J.P. and Wright, A.F. (2000) Identification of a novel protein interacting with RPGR. Hum. Mol. Genet., 9, 2085-2093.
16. Hong, D.H., Yue, G., Adamian, M. and Li, T. (2001) Retinitis pigmentosa GTPase regulator (RPGRr)-interacting protein is stably associated with the photoreceptor ciliary axoneme and anchors RPGR to the connecting cilium. J. Biol. Chem., 276, 12091-12099.
17. Mavlyutov, T.A., Zhao, H. and Ferreira, P.A. (2002) Species-specific subcellular localization of RPGR and RPGRIP isoforms: implications for the phenotypic variability of congenital retinopathies among species. Hum. Mol. Genet., 11, 1899-1907.
18. Lu, X. and Ferreira, P.A. (2005) Identification of novel murine- and human-specific RPGRIP1 splice-variants with distinct expression profiles and subcellular localization. Invest. Ophthalmol. Vis. Sci., in press.
19. Castagnet, P., Mavlyutov, T., Cai, Y., Zhong, F. and Ferreira, P. (2003) RPGRIP1s with distinct neuronal localization and biochemical properties associate selectively with RanBP2 in amacrine neurons. Hum. Mol. Genet., 12, 1847-1863.
20. Dryja, T.P., Adams, S.M., Grimsby, J.L., McGee, T.L., Hong, D.H., Li, T., Andreasson, S. and Berson, E.L. (2001) Null RPGRIP1 alleles in patients with Leber congenital amaurosis. Am. J. Hum. Genet., 68, 1295-1298.
21. Gerber, S., Perrault, I., Hanein, S., Barbet, F., Ducroq, D., Ghazi, I., Martin-Coignard, D., Leowski, C., Homfray, T., Dufier, J.L. et al. (2001) Complete exon-intron structure of the RPGR-interacting protein (RPGRIP1) gene allows the identification of mutations underlying Leber congenital amaurosis. Eur. J. Hum. Genet., 9, 561-571.
22. Hanein, S., Perrault, I., Gerber, S., Tanguy, G., Barbet, F., Ducroq, D., Calvas, P., Dollfus, H., Hamel, C., Lopponen, T. et al. (2004) Leber congenital amaurosis: comprehensive survey of the genetic heterogeneity, refinement of the clinical definition, and genotype-phenotype correlations as a strategy for molecular diagnosis. Hum. Mutat., 23, 306-317.
23. Koenekoop, R.K. (2004) An overview of Leber congenital amaurosis: a model to understand human retinal development. Surv. Ophthalmol., 49, 379-398.
24. Hampsey, M. (1997) A review of phenotypes in Saccharomyces cerevisiae. Yeast, 13, 1099-1133.
25. Stockwell, B.R. (2000) Chemical genetics: ligand-based discovery of gene function. Nat. Rev. Genet., 1, 116-125.
26. Jakobi, R., McCarthy, C.C. and Koeppel, M.A. (2002) Mammalian expression vectors for epitope tag fusion proteins that are toxic in E. coli. Biotechniques, 33, 1218-1220.
27. Sharon, D., Sandberg, M.A., Rabe, V.W., Stillberger, M., Dryja, T.P. and Berson, E.L. (2003) RP2 and RPGR mutations and clinical correlations in patients with X-linked retinitis pigmentosa. Am. J. Hum. Genet., 73, 1131-1146.
28. Kaplan, J., Bonneau, D., Frezal, J., Munnich, A. and Dufier, J.L. (1990) Clinical and genetic heterogeneity in retinitis pigmentosa. Hum. Genet., 85, 635-642.
29. Dryja, T.P. and Berson, E.L. (1995) Retinitis pigmentosa and allied diseases. Implications of genetic heterogeneity. Invest. Ophthalmol. Vis. Sci., 36, 1197-200.
30. Dryja, T.P. and Li, T. (1995) Molecular genetics of retinitis pigmentosa. Hum. Mol. Genet., 4, 1739-1743.
31. Cremers, F.P., Van Den Hurk, J.A. and Den Hollander, A.I. (2002) Molecular genetics of Leber congenital amaurosis. Hum. Mol. Genet., 11, 1169-1176.
32. Dryja, T.P., Hahn, L.B., Kajiwara, K. and Berson, E.L. (1997) Dominant and digenic mutations in the peripherin/RDS and ROM1 genes in retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci., 38, 1972-1982.
33. Silva, E., Yang, J.M., Li, Y., Dharmaraj, S., Sundin, O.H. and Maumenee, I.H. (2000) A CRX null mutation is associated with both Leber congenital amaurosis and a normal ocular phenotype. Invest. Ophthalmol. Vis. Sci., 41, 2076-2079.
34. Stockwell, B.R. (2000) Frontiers in chemical genetics. Trends Biotechnol., 18, 449-455.
35. Ferreira, P.A., Yunfei, C., Schick, D. and Roepman, R. (1998) The cyclophilin-like domain mediates the association of Ran-binding protein 2 with subunits of the 19 S regulatory complex of the proteasome. J. Biol. Chem., 273, 24676-24682.
36. Hodel, M.R., Corbett, A.H. and Hodel, A.E. (2001) Dissection of a nuclear localization signal. J. Biol. Chem., 276, 1317-1325.
37. Chen, C.H., von Kessler, D.P., Park, W., Wang, B., Ma, Y. and Beachy, P.A. (1999) Nuclear trafficking of Cubitus interruptus in the transcriptional regulation of Hedgehog target gene expression. Cell, 98, 305-316.
38. Chauvet, V., Tian, X., Husson, H., Grimm, D.H., Wang, T., Hieseberger, T., Igarashi, P., Bennett, A.M., Ibraghimov-Beskrovnaya, O., Somlo, S. et al. (2004) Mechanical stimuli induce cleavage and nuclear translocation of the polycystin-1 C terminus. J. Clin. Invest., 114, 1433-1443.
39. Guay-Woodford, L.M. (2004) RIP-ed and ready to dance: new mechanisms for polycystin-1 signaling. J. Clin. Invest., 114, 1404-1406.
40. Davies, S.W., Turmaine, M., Cozens, B.A., DiFiglia, M., Sharp, A.H., Ross, C.A., Scherzinger, E., Wanker, E.E., Mangiarini, L. and Bates, G.P. (1997) Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell, 90, 537-548.
41. Bates, G. and Eberwine, J. (2000) Hunting in the calm before the storm. Nat. Genet., 25, 365-366.
42. Bates, G.P. (2001) Huntington's disease. Exploiting expression. Nature, 413, 691-694.
43. Hsieh, J.J., Ernst, P., Erdjument-Bromage, H., Tempst, P. and Korsmeyer, S.J. (2003) Proteolytic cleavage of MLL generates a complex of N- and C-terminal fragments that confers protein stability and subnuclear localization. Mol. Cell. Biol., 23, 186-194.
44. Miller, M.J., Rauer, H., Tomita, H., Gargus, J.J., Gutman, G.A., Cahalan, M.D. and Chandy, K.G. (2001) Nuclear localization and dominant-negative suppression by a mutant SKCa3 N-terminal channel fragment identified in a patient with schizophrenia. J. Biol. Chem., 276, 27753-27756.
45. Ferreira, P.A. (2000) Characterization of RanBP2-associated molecular components in neuroretina. Methods Enzymol., 315, 455-468.