Retinitis pigmentosa-associated rhodopsin mutations in three membrane-located cysteine residues present three different biochemical phenotypes

Biochemical and Biophysical Research Communications

Volumn 297, Issue 4, 2002, Pages 847-853

  Breikers, Githa ^a   Portier VandeLuytgaarden, Margriet J M ^a   Bovee Geurts, Petra H M ^a   DeGrip, Willem J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Baculovirus; Functional expression; Protein folding; Retinitis pigmentosa; Rhodopsin; Targeting

Indexed keywords

11 CIS RETINAL; CYSTEINE; MEMBRANE PROTEIN; MUTANT PROTEIN; RHODOPSIN;

ANIMAL CELL; ARTICLE; BACULOVIRUS; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE MUTATION; INSECT CELL; MEMBRANE TRANSPORT; MOLECULAR GENETICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RETINITIS PIGMENTOSA; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CLONING, MOLECULAR; CYSTEINE; DARKNESS; GENE EXPRESSION; HUMANS; LIGHT; MOLECULAR SEQUENCE DATA; PHENOTYPE; PROTEIN CONFORMATION; PROTEIN FOLDING; RECOMBINANT PROTEINS; RETINITIS PIGMENTOSA; RHODOPSIN; SPECTROPHOTOMETRY; SPODOPTERA; TRANSFECTION;

UNIDENTIFIED BACULOVIRUS;

EID: 0036033426     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-291X(02)02308-2     Document Type: Article

References (41)

1. T. Okada, O.P. Ernst, K. Palczewski, K.P. Hofmann, Activation of rhodopsin: new insights from structural and biochemical studies, Trends Biochem.Sci. 26 (2001) 318-324.
2. J. Lem, N.V. Krasnoperova, P.D. Calvert, B. Kosaras, D.A. Cameron, M. Nicolò, C.L. Makino, R.L. Sidman, Morphological, physiological, and biochemical changes in rhodopsin knockout mice, Proc. Natl. Acad. Sci. USA 96 (1999) 736-741.
3. J.R. Heckenlively, Retinitis Pigmentosa, Lippencott, Philadelphia, 1988.
4. S. VanSoest, A. Westerveld, P.T. DeJong, E.M. Bleeker-Wagemakers, A.A.B. Bergen, Retinitis pigmentosa: defined from a molecular point of view, Surv. Ophthalmol. 43 (1999) 321-334.
5. M. Al-Maghtheh, C.Y. Gregory, C.F. Inglehearn, A.J. Hardcastle, S.S. Bhattacharya, Rhodopsin mutations in autosomal dominant retinitis pigmentosa, Hum. Mutat. 2 (1993) 249-255.
6. A. Gal, E. Apfelstedt-Sylla, A.R. Janecke, E. Zrenner, Rhodopsin mutations in inherited retinal dystrophies and dysfunctions, Prog. Retin. Eye Res. 16 (1997) 51-79.
7. S.P. Daiger, L.S. Sullivan, J.A. Rodriguez, Correlation of phenotype with genotype in inherited retinal degeneration, Behav. Brain Sci. 18 (1995) 452-467.
8. S. Bunge, H. Wedemann, D. David, D.J. Terwilliger, L.I. VanDen-Born, C. Aulehla-Scholz, C. Samanns, M. Horn, J. Ott, E. Schwinger, A. Schinzel, M.J. Denton, A. Gal, Molecular analysis and genetic mapping of the rhodopsin gene in families with autosomal dominant retinitis pigmentosa, Genomics 17 (1993) 230-233.
9. C.F. Inglehearn, D.H. Lester, R. Bashir, U. Atif, T.J. Keen, A. Sertedaki, J. Lindsey, M.R. Jay, A.C. Bird, G.J. Farrar, P. Humphries, S.S. Bhattacharya, Recombination between rhodopsin and locus D3S47 (C17) in rhodopsin retinitis pigmentosa families, Am. J. Hum. Gen. 50 (1992) 590-597.
10. T.P. Drya, L.B. Hahn, G.S. Cowley, T.L. McGee, E.L. Berson, Mutation spectrum of the rhodopsin gene among patients with autosomal dominant retinitis pigmentosa, Proc. Natl. Acad. Sci. USA 88 (1991) 9370-9374.
11. C.H. Sung, B.G. Schneider, N. Agarwal, D.S. Papermaster, J. Nathans, Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis-pigmentosa, Proc. Natl. Acad. Sci. USA 88 (1991) 8840-8844.
12. J.P. Macke, C.M. Davenport, S.G. Jacobson, J.C. Hennessey, F. Gonzalez-Fernandez, B.P. Conway, J.R. Heckenliveley, R.M.J. Palmer, I.H. Maumenee, P.A. Sieving, P. Gouras, W. Good, J. Nathans, Identification of novel rhodopsin mutations responsible for retinitis pigmentosa: implications for the structure and function of rhodopsin, Am. J. Hum. Gen. 53 (1993) 80-89.
13. R. Vaithinathan, E.L. Berson, T.P. Drya, Further screening of the rhodopsin gene in patients with autosomal dominant retinitis pigmentosa, Genomics 21 (1994) 461-463.
14. C.H. Sung, C.M. Davenport, J. Nathans, Rhodopsin mutations responsible for autosomal dominant retinitis pigmentosa - clustering of functional classes along the polypeptide chain, J. Biol. Chem. 268 (1993) 26645-26649.
15. S. Kaushal, H.G. Khorana, Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa, Biochemistry 33 (1994) 6121-6128.
16. T.A. Kunkel, Rapid and eScient site-specific mutagenesis without phenotypic selection, Proc. Natl. Acad. Sci. USA 82 (1985) 488-492.
17. M.D. Summers, G.E. Smith, A manual of methods for baculovirus vectors and insect culture procedures, Texas, Exp. Station Bulletin No. 1555, 1987.
18. G.L.J. DeCaluwé, J. VanOosttrum, J.J.M. Janssen, W.J. DeGrip, In vitro synthesis of bovine rhodopsin using recombinant baculovirus, Methods Neurol. 15 (1993) 307-321.
19. C.H.W. Klaassen, P.H.M. Bovee-Geurts, G.L.J. DeCaluwé, W.J. DeGrip, Large-scale production and purification of functional recombinant bovine rhodopsin using the baculovirus expression system, Biochem. J. 342 (1999) 293-300.
20. C.H.W. Klaassen, W.J. DeGrip, Baculovirus expression system for expression and characterization of functional recombinant visual pigments, Methods Enzymol. 315 (2000) 12-29.
21. J.W.H. Janssen, P.H.M. Bovee-Geurts, A.P.A. Peeters, J.K. Bowmaker, H.M. Cooper, Z.K. David-Gray, E. Nevo, W.J. DeGrip, A fully functional rod visual pigment in a blind mammal - a case for adaptive functional reorganization? J. Biol. Chem. 275 (2000) 38674-38679.
22. P.M.A.M. Vissers, W.J. DeGrip, Functional expression of human cone pigments using recombinant baculovirus: compatibility with histidine tagging and evidence for N-glycosylation, FEBS Lett. 396 (1996) 26-30.
23. W.J. DeGrip, Immunochemistry of rhodopsin, Prog. Retin. Eye Res. 4 (1985) 137-180.
24. G. Adamus, Z.S. Zam, A. Arendt, K. Palczewski, J.H. McDowell, P.A. Hargrave, Anti-rhodopsin monoclonal antibodies of defined specificity: characterization and application, Vis. Res. 31 (1991) 17-31.
25. G. Adamus, A. Arendt, Z.S. Zam, J.H. McDowell, P.A. Hargrave, Use of peptides to select for anti-rhodopsin antibodies with desired amino acid sequence specificities, Pept. Res 1 (1988) 42-47.
26. E.A. Pierce, Pathways to photoreceptor cell death in inherited retinal degenerations, Bioessays 23 (2001) 605-618.
27. P. Rath, P.H.M. Bovee-Geurts, W.J. DeGrip, K.J. Rothschild, Photo activation of rhodopsin involves alterations in cysteine side chains: detection of an S-H band in the meta I → meta II FTIR difference spectrum, Biophys. J. 66 (1994) 2085-2091.
28. G. Breikers, P.H.M. Bovee-Geurts, G.L.J. DeCaluwe, W.J. DeGrip, A structural role for Asp83 in the photoactivation of rhodopsin, Biol. Chem. 382 (2001) 1263-1270.
29. J.J.M. Janssen, W.J.M. VanDeVen, W.A.H.M. VanGroningen-Luyben, J. Roosien, J.M. Vlak, W.J. DeGrip, Synthesis of functional bovine opsin in insect cells under control of the baculovirus polyhedrin promoter, Mol. Biol. Rep. 13 (1988) 65-71.
30. S.S. Karnik, T.P. Sakmar, H.B. Chen, H.G. Khorana, Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin, Proc. Natl. Acad. Sci. USA 85 (1988) 8459-8463.
31. J.J.M. Janssen, W.R. Mulder, G.L.J. DeCaluwé, J.M. Vlak, W.J. DeGrip, In vitro expression of bovine opsin using recombinant baculovirus: the role of glutamic acid (134) in opsin biosynthesis and glycosylation, Biochim. Biophys. Acta 1089 (1991) 68-76.
32. D.C. Teller, T. Okada, C.A. Behnke, K. Palczewski, R.E. Stehnkamp, Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G-protein-coupled receptors (GPCRs), Biochemistry 40 (2001) 7761-7772.
33. D.C. Deretic, S. Schmerl, P.A. Hargrave, A. Arendt, J.H. McDowell, Regulation of sorting and post-Golgi traScking of rhodopsin by its C-terminal sequence QVS(A)PA, Proc. Natl. Acad. Sci. USA 95 (1998) 10620-10625.
34. 135 sequence in rhodopsin, J. Biol. Chem 271 (1996) 25405-25411.
35. F. Simonelli, M. Rinaldi, A. Nesti, F. Testa, E. Rinaldi, A. Ciccodicola, L. Flagiello, M.G. Miano, V. Ventruto, M. D'Urso, Ocular signs associated with a rhodopsin mutation (Cys-167 → Arg) in a family with autosomal dominant retinitis pigmentosa, Br. J. Ophthalmol. 82 (1998) 709.
36. Z. Kawar, D.L. Jarvis, Biosynthesis and subcellular localization of a lepidopteran insect α1, 2-mannosidase, Insect Biochem. Mol. Biol. 31 (2001) 289-297.
37. Y.A. Ovchinnikov, Probing the folding of membrane proteins, Trends Biochem Sci. 12 (1987) 434-438.
38. M. Ibba, D. Soll, Quality control mechanisms during translation, Science 286 (1999) 1893-1897.
39. F.W. Fitzke, S. Owens, A.T. Moore, M. Jay, C.F. Inglehearn, S. Bhattacharya, A.C. Bird, Comparison of functional characteristics of autosomal dominant retinitis pigmentosa with different amino acid changes in the rhodopsin molecule, Invest. Ophthalmol Vis. Sci. Suppl. 32 (1991) 1200.
40. P.A. Hargrave, J.H. McDowell, Rhodopsin and phototransduction - A model system for G-protein-linked receptors, FASEB J. 6 (1992) 2323-2331.
41. K. Palczewski, T. Kumasaka, T. Hori, C.A. Behnke, H. Motoshims, B.A. Fox, R.E. Stenkamp, M. Yamamoto, M. Miyano, Crystal structure of rhodopsin: a G protein-coupled receptor, Science 289 (2000) 739-745.