Analysis of disease-linked rhodopsin mutations based on structure, function, and protein stability calculations

Journal of Molecular Biology

Volumn 405, Issue 2, 2011, Pages 584-606

  Rakoczy, Elizabeth P ^a   Kiel, Christina ^b   McKeone, Richard ^c   Stricher, François ^b   Serrano, Luis ^b,d  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c LIONS EYE INSTITUTE   (Australia)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

energy calculation; FoldX; protein stability; retinitis pigmentosa; rhodopsin

Indexed keywords

MUTANT PROTEIN; RETINA S ANTIGEN; RHODOPSIN; TRANSDUCIN;

ARTICLE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; RETINA;

EID: 78650855405     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.11.003     Document Type: Article

References (69)

1. Ranganathan R. A matter of life or death Science 299 2003 1677 1679
2. Massof R.W., and Finkelstein D. Two forms of autosomal dominant primary retinitis pigmentosa Doc. Ophthalmol. 51 1981 289 346
3. Chen P., Hao W., Rife L., Wang X.P., Shen D., and Chen J. A photic visual cycle of rhodopsin regeneration is dependent on Rgr Nat. Genet. 28 2001 256 260
4. Bok D. Processing and transport of retinoids by the retinal pigment epithelium Eye (Lond.) 4 1990 326 332 (Pubitemid 20307089)
5. Palczewski K., Kumasaka T., Hori T., Behnke C.A., Motoshima H., and Fox B.A. Crystal structure of rhodopsin: a G protein-coupled receptor Science 289 2000 739 745
6. Morris M.B., Dastmalchi S., and Church W.B. Rhodopsin: structure, signal transduction and oligomerisation Int. J. Biochem. Cell Biol. 41 2009 721 724
7. Okada T., Sugihara M., Bondar A.N., Elstner M., Entel P., and Buss V. The retinal conformation and its environment in rhodopsin in light of a new 2.2 Å crystal structure J. Mol. Biol. 342 2004 571 583
8. Li J, Edwards P.C., Burghammer M., Villa C., and Schertler G.F. Structure of bovine rhodopsin in a trigonal crystal form J. Mol. Biol. 343 2004 1409 1438
9. Teller D.C, Okada T., Behnke C.A., Palczewski K., and Stenkamp R.E. 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
10. Stenkamp R.E. Alternative models for two crystal structures of bovine rhodopsin Acta Crystallogr., Sect. D: Biol. Crystallogr. 64 2008 902 904
11. Nakamichi H., and Okada T. Local peptide movement in the photoreaction intermediate of rhodopsin Proc. Natl Acad. Sci. USA 103 2006 12729 12734
12. Salom D., Lodowski D.T., Stenkamp R.E., Le Trong I., Golczak M., and Jastrzebska B. Crystal structure of a photoactivated deprotonated intermediate of rhodopsin Proc. Natl Acad. Sci. USA 103 2006 16123 16128
13. Park J.H., Scheerer P., Hofmann K.P., Choe H.W., and Ernst O.P. Crystal structure of the ligand-free G-protein-coupled receptor opsin Nature 454 2008 183 187
14. Mendes H.F., van der Spuy J., Chapple J.P., and Cheetham M.E. Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy Trends Mol. Med. 11 2005 177 185
15. Gal A., Apfelstedt-Sylla E., Janecke A.R., and Zrenner E. Rhodopsin mutations in inherited retinal dystrophies and dysfunctions Prog. Retinal Eye Res. 16 1997 5179
16. Sohocki M.M., Daiger S.P., Bowne S.J., Rodriquez J.A., Northrup H., and Heckenlively J.R. Prevalence of mutations causing retinitis pigmentosa and other inherited retinopathies Hum. Mutat. 17 2001 42 51
17. Sullivan L.S., Bowne S.J., Birch D.G., Hughbanks-Wheaton D., Heckenlively J.R., and Lewis R.A. Prevalence of disease-causing mutations in families with autosomal dominant retinitis pigmentosa: a screen of known genes in 200 families Invest. Ophthalmol. Visual Sci. 47 2006 3052 3064
18. Guerois R., Nielsen J.E., and Serrano L. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations J. Mol. Biol. 320 2002 369 387
19. Schymkowitz J., Borg J., Stricher F., Nys R., Rousseau F., and Serrano L. The FoldX web server: an online force field Nucleic Acids Res. 33 2005 W382 388
20. Kaushal S., and Khorana H.G. Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa Biochemistry 33 1994 6121 6128
21. Angel T.E., Chance M.R., and Palczewski K. Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors Proc. Natl Acad. Sci. USA 106 2009 8555 8560
22. Lodowski D.T., Angel T.E., and Palczewski K. Comparative analysis of GPCR crystal structures Photochem. Photobiol. 85 2009 425 430
23. Worth C.L., Kleinau G., and Krause G. Comparative sequence and structural analyses of G-protein-coupled receptor crystal structures and implications for molecular models PLoS ONE 4 2009 e7011
24. Fotiadis D., Liang Y., Filipek S., Saperstein D.A., Engel A., and Palczewski K. Atomic-force microscopy: rhodopsin dimers in native disc membranes Nature 421 2003 127 128
25. Webel R., Menon I., O'Tousa J.E., and Colley N.J. Role of asparagine-linked oligosaccharides in rhodopsin maturation and association with its molecular chaperone, NinaA J. Biol. Chem. 275 2000 24752 24759
26. Kaushal S., Ridge K.D., and Khorana H.G. Structure and function in rhodopsin: the role of asparagine-linked glycosylation Proc. Natl Acad. Sci. USA 91 1994 4024 4028
27. Xue L., Gollapalli D.R., Maiti P., Jahng W.J., and Rando R.R. A palmitoylation switch mechanism in the regulation of the visual cycle Cell 117 2004 761 771
28. Park P.S., Sapra K.T., Jastrzebska B., Maeda T., Maeda A., and Pulawski W. Modulation of molecular interactions and function by rhodopsin palmitylation Biochemistry 48 2009 4294 4304
29. Wang Z., Wen X.H., Ablonczy Z., Crouch R.K., Makino C.L., and Lem J. Enhanced shutoff of phototransduction in transgenic mice expressing palmitoylation-deficient rhodopsin J. Biol. Chem. 280 2005 24293 24300
30. Zhang L., Sports C.D., Osawa S., and Weiss E.R. Rhodopsin phosphorylation sites and their role in arrestin binding J. Biol. Chem. 272 1997 14762 14768
31. Sommer M.E., Farrens D.L., McDowell J.H., Weber L.A., and Smith W.C. Dynamics of arrestin-rhodopsin interactions: loop movement is involved in arrestin activation and receptor binding J. Biol. Chem. 282 2007 25560 25568
32. Arshavsky V.Y. Rhodopsin phosphorylation: from terminating single photon responses to photoreceptor dark adaptation Trends Neurosci. 25 2002 124 126
33. Schädel S.A., Heck M., Maretzki D., Filipek S., Teller D.C., Palczewski K., and Hofmann K.P. Ligand channeling within a G-protein-coupled receptor. The entry and exit of retinals in native opsin J. Biol. Chem. 278 2003 24896 24903
34. Mazelova J., Astuto-Gribble L., Inoue H., Tam B.M., Schonteich E., and Prekeris R. Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4 EMBO J. 28 2009 183 192
35. Kuemin M., Schweizer S., Ochsenfeld C., and Wennemers H. Effects of terminal functional groups on the stability of the polyproline II structure: a combined experimental and theoretical study J. Am. Chem. Soc. 131 2009 15474 15482
36. Fanelli F., and De Benedetti P.G. Computational modeling approaches to structure-function analysis of G protein-coupled receptors Chem. Rev. 105 2005 3297 3351
37. Scheerer P., Park J.H., Hildebrand P.W., Kim Y.J., Krauss N., and Choe H.W. Crystal structure of opsin in its G-protein-interacting conformation Nature 455 2008 497 502
38. Murakami M., and Kouyama T. Crystal structure of squid rhodopsin Nature 453 2008 363 367
39. Okada T., Fujiyoshi Y., Silow M., Navarro J., Landau E.M., and Shichida Y. Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography Proc. Natl Acad. Sci. USA 99 2002 5982 5987
40. Standfuss J., Xie G., Edwards P.C., Burghammer M., Oprian D.D., and Schertler G.F. Crystal structure of a thermally stable rhodopsin mutant J. Mol. Biol. 372 2007 1179 1188
41. Dowhan W., and Bogdanov M. Lipid-dependent membrane protein topogenesis Annu. Rev. Biochem. 78 2009 515 540
42. Hessa T., Kim H., Lundin C., Boekel J., Andersson H., and Nilsson I. Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 433 2005 377 381
43. Hessa T., Meindl-Beinker N., Bernsel A., Kim J., Sato Y., and Lerch M. Molecular code for transmembrane-helix recognition by the Sec61 translocon Nature 450 2007 1026 1030
44. Macke J.P., Davenport C.M., Jacobson S.G., Hennessey J.C., Gonzalez-Fernandez F., and Conway B.P. Identification of novel rhodopsin mutations responsible for retinitis pigmentosa: implications for the structure and function of rhodopsin Am. J. Hum. Genet. 53 1993 80 89
45. Palczewski K. G protein-coupled receptor rhodopsin Annu. Rev. Biochem. 75 2006 743 767
46. Medina R., Perdomo D., and Bubis J. The hydrodynamic properties of dark- and light-activated states of n-dodecyl beta-d-maltoside-solubilized bovine rhodopsin support the dimeric structure of both conformations J. Biol. Chem. 279 2004 39565 39573
47. Ruprecht J.J., Mielke T., Vogel R., Villa C., and Schertler G.F. Electron crystallography reveals the structure of metarhodopsin I EMBO J. 23 2004 3609 3620
48. Briscoe A.D., Gaur C., and Kumar S. The spectrum of human rhodopsin disease mutations through the lens of interspecific variation Gene 332 2004 107 118
49. Ng P.C., and Henikoff S. Predicting deleterious amino acid substitutions Genome Res. 11 2001 863 874
50. Ng P.C., and Henikoff S. Accounting for human polymorphisms predicted to affect protein function Genome Res. 12 2002 436 446
51. Ng P.C., and Henikoff S. SIFT: predicting amino acid changes that affect protein function Nucleic Acids Res. 31 2003 3812 3814
52. Kumar P., Henikoff S., and Ng P.C. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm Nat. Protoc. 4 2009 1073 1081
53. Sung C.H., Davenport C.M., and Nathans J. Rhodopsin mutations responsible for autosomal dominant retinitis pigmentosa. Clustering of functional classes along the polypeptide chain J. Biol. Chem. 268 1993 26645 26649
54. Tam B.M., Moritz O.L., Hurd L.B., and Papermaster D.S. Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis J. Cell Biol. 151 2000 1369 1380
55. Sung C.H., Makino C., Baylor D., and Nathans J. A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment J. Neurosci. 14 1994 5818 5833
56. Frederick J.M., Krasnoperova N.V., Hoffmann K., Church-Kopish J., Rüther K., and Howes K. Mutant rhodopsin transgene expression on a null background Invest. Ophthalmol. Visual Sci. 42 2001 826 833
57. Mustafi D., and Palczewski K. Topology of class A G protein-coupled receptors: insights gained from crystal structures of rhodopsins, adrenergic and adenosine receptors Mol. Pharmacol. 75 2009 1 12
58. Reumers J., Schymkowitz J., Ferkinghoff-Borg J., Stricher F., Serrano L., and Rousseau F. SNPeffect: a database mapping molecular phenotypic effects of human non-synonymous coding SNPs Nucleic Acids Res. 33 2005 D527 532
59. Pey A.L., Stricher F., Serrano L., and Martinez A. Predicted effects of missense mutations on native-state stability account for phenotypic outcome in phenylketonuria, a paradigm of misfolding diseases Am. J. Hum. Genet. 81 2007 1006 1024
60. Reumers J., Schymkowitz J., and Rousseau F. Using structural bioinformatics to investigate the impact of non synonymous SNPs and disease mutations: scope and limitations BMC Bioinformatics 10 2009 S9
61. Berson E.L., Rosner B., Sandberg M.A., and Dryja T.P. Ocular findings in patients with autosomal dominant retinitis pigmentosa and a rhodopsin gene defect (Pro-23-His) Arch. Ophthalmol. 109 1991 92 101
62. Kemp C.M., Jacobson S.G., Roman A.J., Sung C.H., and Nathans J. Abnormal rod dark adaptation in autosomal dominant retinitis pigmentosa with proline-23-histidine rhodopsin mutation Am. J. Ophthalmol. 113 1992 165 174
63. Rosas D.J., Roman A.J., Weissbrod P., Macke J.P., and Nathans J. Autosomal dominant retinitis pigmentosa in a large family: a clinical and molecular genetic study Invest. Ophthalmol. Visual Sci. 35 1994 3134 3144
64. Kelly J.W., and Balch W.E. The integration of cell and chemical biology in protein folding Nat. Chem. Biol. 2 2006 224 227
65. Connelly S., Choi S., Johnson S.M., Kelly J.W., and Wilson I.A. Structure-based design of kinetic stabilizers that ameliorate the transthyretin amyloidoses Curr. Opin. Struct. Biol. 20 2010 54 62
66. Stone E.M., Kimura A.E., Nichols B.E., Khadivi P., Fishman G.A., and Sheffield V.C. Regional distribution of retinal degeneration in patients with the proline to histidine mutation in codon 23 of the rhodopsin gene Ophthalmology 98 1991 1806 1813
67. Berson E.L., Sandberg M.A., and Dryja T.P. Search for correlations between severity of retinitis pigmentosa and primary mutations Digit. J. Ophthalmol. 4 1998
68. UniProt Consortium The Universal Protein Resource (UniProt) in 2010 Nucleic Acids Res. 38 2010 D142 D148
69. Pearson W.R., and Lipman D.J. Improved tools for biology sequence comparison Proc. Natl Acad. Sci. USA 85 1988 2444 2448