Misfolded opsin mutants display elevated β-sheet structure

FEBS Letters

Volumn 589, Issue 20, 2015, Pages 3119-3125

  Miller, Lisa M ^a   Gragg, Megan ^b   Kim, Tae Gyun ^b   Park, Paul S H ^b  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

G protein coupled receptor; Membrane protein; Protein aggregation; Protein misfolding; Retinal degeneration; Secondary structure

Indexed keywords

OPSIN; RHODOPSIN; PHOTOPROTEIN;

ALPHA HELIX; ARTICLE; BETA SHEET STRUCTURE; CHROMATOPHORE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FLUORESCENCE RESONANCE ENERGY TRANSFER; INFRARED SPECTROSCOPY; ISOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN MISFOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; ANIMAL; CHEMISTRY; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; MUTATION; RETINITIS PIGMENTOSA; SPECTROPHOTOMETRY;

ANIMALS; ENDOPLASMIC RETICULUM; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HUMANS; LUMINESCENT PROTEINS; MICE; MICROSCOPY, CONFOCAL; MUTATION; OPSINS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RETINITIS PIGMENTOSA; RHODOPSIN; SPECTROPHOTOMETRY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84943198794     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.08.042     Document Type: Article

References (45)

1. D.T. Hartong, E.L. Berson, and T.P. Dryja Retinitis pigmentosa Lancet 368 2006 1795 1809
2. S.P. Daiger, L.S. Sullivan, and S.J. Bowne Genes and mutations causing retinitis pigmentosa Clin. Genet. 84 2013 132 141
3. H.F. Mendes, J. van der Spuy, J.P. Chapple, and M.E. Cheetham Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy Trends Mol. Med. 11 2005 177 185
4. C.H. Sung, C.M. Davenport, and 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
5. M.P. Krebs, D.C. Holden, P. Joshi, C.L. Clark 3rd, A.H. Lee, and S. Kaushal Molecular mechanisms of rhodopsin retinitis pigmentosa and the efficacy of pharmacological rescue J. Mol. Biol. 395 2010 1063 1078
6. M.E. Illing, R.S. Rajan, N.F. Bence, and R.R. Kopito A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system J. Biol. Chem. 277 2002 34150 34160
7. R.S. Saliba, P.M. Munro, P.J. Luthert, and M.E. Cheetham The cellular fate of mutant rhodopsin: quality control, degradation and aggresome formation J. Cell Sci. 115 2002 2907 2918
8. A. Surguchev, and A. Surguchov Conformational diseases: looking into the eyes Brain Res. Bull. 81 2010 12 24
9. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366
10. T.P. Knowles, M. Vendruscolo, and C.M. Dobson The amyloid state and its association with protein misfolding diseases Nat. Rev. Mol. Cell Biol. 15 2014 384 396
11. N.F. Bence, R.M. Sampat, and R.R. Kopito Impairment of the ubiquitin-proteasome system by protein aggregation Science 292 2001 1552 1555
12. X. Liu, P. Garriga, and H.G. Khorana Structure and function in rhodopsin: correct folding and misfolding in two point mutants in the intradiscal domain of rhodopsin identified in retinitis pigmentosa Proc. Natl. Acad. Sci. U.S.A. 93 1996 4554 4559
13. L.M. Miller, M.W. Bourassa, and R.J. Smith FTIR spectroscopic imaging of protein aggregation in living cells Biochim. Biophys. Acta 1828 2013 2339 2346
14. S.C. Hovan, S. Howell, and P.S. Park Forster resonance energy transfer as a tool to study photoreceptor biology J. Biomed. Opt. 15 2010 067001
15. J. Goedhart, L. van Weeren, M.A. Hink, N.O. Vischer, K. Jalink, and T.W. Gadella Jr. Bright cyan fluorescent protein variants identified by fluorescence lifetime screening Nat. Methods 7 2010 137 139
16. R.S. Molday, and D. MacKenzie Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes Biochemistry 22 1983 653 660
17. N. Zerangue, M.J. Malan, S.R. Fried, P.F. Dazin, Y.N. Jan, L.Y. Jan, and B. Schwappach Analysis of endoplasmic reticulum trafficking signals by combinatorial screening in mammalian cells Proc. Natl. Acad. Sci. U.S.A. 98 2001 2431 2436
18. S. Kawamura, A.T. Colozo, D.J. Muller, and P.S. Park Conservation of molecular interactions stabilizing bovine and mouse rhodopsin Biochemistry 49 2010 10412 10420
19. D.L. Farrens, and H.G. Khorana Structure and function in rhodopsin. Measurement of the rate of metarhodopsin II decay by fluorescence spectroscopy J. Biol. Chem. 270 1995 5073 5076
20. T.P. Dryja, T.L. McGee, E. Reichel, L.B. Hahn, G.S. Cowley, D.W. Yandell, M.A. Sandberg, and E.L. Berson A point mutation of the rhodopsin gene in one form of retinitis pigmentosa Nature 343 1990 364 366
21. T.P. Dryja, L.B. Hahn, G.S. Cowley, T.L. McGee, and E.L. Berson Mutation spectrum of the rhodopsin gene among patients with autosomal dominant retinitis pigmentosa Proc. Natl. Acad. Sci. U.S.A. 88 1991 9370 9374
22. A. Iannaccone, D. Man, N. Waseem, B.J. Jennings, M. Ganapathiraju, K. Gallaher, E. Reese, S.S. Bhattacharya, and J. Klein-Seetharaman Retinitis pigmentosa associated with rhodopsin mutations: correlation between phenotypic variability and molecular effects Vision. Res. 46 2006 4556 4567
23. R. McKeone, M. Wikstrom, C. Kiel, and P.E. Rakoczy Assessing the correlation between mutant rhodopsin stability and the severity of retinitis pigmentosa Mol. Vis. 20 2014 183 199
24. G.J. Kremers, J. Goedhart, E.B. van Munster, and T.W. Gadella Jr. Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Forster radius Biochemistry 45 2006 6570 6580
25. R. Hubbard, and G. Wald Cis-trans isomers of vitamin A and retinene in the rhodopsin system J. Gen. Physiol. 36 1952 269 315
26. P.S. Park Constitutively active rhodopsin and retinal disease Adv. Pharmacol. 70 2014 1 36
27. S. Jin, T.D. McKee, and D.D. Oprian An improved rhodopsin/EGFP fusion protein for use in the generation of transgenic Xenopus laevis FEBS Lett. 542 2003 142 146
28. B.A. Price, I.M. Sandoval, F. Chan, D.L. Simons, S.M. Wu, T.G. Wensel, and J.H. Wilson Mislocalization and degradation of human P23H-rhodopsin-GFP in a knockin mouse model of retinitis pigmentosa Invest. Ophthalmol. Vis. Sci. 52 2011 9728 9736
29. B.M. Tam, and O.L. Moritz Characterization of rhodopsin P23H-induced retinal degeneration in a Xenopus laevis model of retinitis pigmentosa Invest. Ophthalmol. Vis. Sci. 47 2006 3234 3241
30. J.M. Frederick, N.V. Krasnoperova, K. Hoffmann, J. Church-Kopish, K. Ruther, K. Howes, J. Lem, and W. Baehr Mutant rhodopsin transgene expression on a null background Invest. Ophthalmol. Vis. Sci. 42 2001 826 833
31. S. Sakami, T. Maeda, G. Bereta, K. Okano, M. Golczak, A. Sumaroka, A.J. Roman, A.V. Cideciyan, S.G. Jacobson, and K. Palczewski Probing mechanisms of photoreceptor degeneration in a new mouse model of the common form of autosomal dominant retinitis pigmentosa due to P23H opsin mutations J. Biol. Chem. 286 2011 10551 10567
32. Y. Liang, D. Fotiadis, S. Filipek, D.A. Saperstein, K. Palczewski, and A. Engel Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes J. Biol. Chem. 278 2003 21655 21662
33. B. Jastrzebska, T. Maeda, L. Zhu, D. Fotiadis, S. Filipek, A. Engel, R.E. Stenkamp, and K. Palczewski Functional characterization of rhodopsin monomers and dimers in detergents J. Biol. Chem. 279 2004 54663 54675
34. A.M. Whited, and P.S. Park Nanodomain organization of rhodopsin in native human and murine rod outer segment disc membranes Biochim. Biophys. Acta 1848 2015 26 34
35. T. Rakshit, and P.S. Park Impact of reduced rhodopsin expression on the structure of rod outer segment disc membranes Biochemistry 54 2015 2885 2894
36. S.E. Mansoor, K. Palczewski, and D.L. Farrens Rhodopsin self-associates in asolectin liposomes Proc. Natl. Acad. Sci. U.S.A. 103 2006 3060 3065
37. P. Kota, P.J. Reeves, U.L. Rajbhandary, and H.G. Khorana Opsin is present as dimers in COS1 cells: identification of amino acids at the dimeric interface Proc. Natl. Acad. Sci. U.S.A. 2006
38. O.P. Ernst, V. Gramse, M. Kolbe, K.P. Hofmann, and M. Heck Monomeric G protein-coupled receptor rhodopsin in solution activates its G protein transducin at the diffusion limit Proc. Natl. Acad. Sci. U.S.A. 104 2007 10859 10864
39. A. Barth, and C. Zscherp What vibrations tell us about proteins Q. Rev. Biophys. 35 2002 369 430
40. H. Lavoie, B. Desbat, D. Vaknin, and C. Salesse Structure of rhodopsin in monolayers at the air-water interface: a PM-IRRAS and X-ray reflectivity study Biochemistry 41 2002 13424 13434
41. R.S. Rajan, M.E. Illing, N.F. Bence, and R.R. Kopito Specificity in intracellular protein aggregation and inclusion body formation Proc. Natl. Acad. Sci. U.S.A. 98 2001 13060 13065
42. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and C.G. Glabe Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489
43. H. LeVine 3rd Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: detection of amyloid aggregation in solution Protein Sci. 2 1993 404 410
44. H. Naiki, K. Higuchi, M. Hosokawa, and T. Takeda Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1 Anal. Biochem. 177 1989 244 249
45. Y.X. Tao, and P.M. Conn Chaperoning G protein-coupled receptors: from cell biology to therapeutics Endocr. Rev. 35 2014 602 647