Thermal stability of rhodopsin and progression of retinitis pigmentosa: Comparison of S186W and D190N rhodopsin mutants

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17698-17712

  Liu, Monica Yun ^a   Liu, Jian ^a   Mehrotra, Devi ^a   Liu, Yuting ^a   Guo, Ying ^a   Baldera Aguayo, Pedro A ^a   Mooney, Victoria L ^a   Nour, Adel M ^a   Yan, Elsa C Y ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN BOND NETWORKS; MOLECULAR MECHANISM; ORDERS OF MAGNITUDE; PROTONATED SCHIFF BASE; RETINITIS PIGMENTOSA; THERMAL ISOMERIZATIONS; THERMAL REACTIONS; UV VISIBLE SPECTROSCOPY;

CHROMOPHORES; FUNCTIONAL GROUPS; HYDROGEN BONDS; HYDROLYSIS; ISOMERIZATION; ISOMERS; OPHTHALMOLOGY; ULTRAVIOLET VISIBLE SPECTROSCOPY;

THERMODYNAMIC STABILITY;

ASPARAGINE; ASPARTIC ACID; RHODOPSIN; SCHIFF BASE; SERINE; TRYPTOPHAN;

ARTICLE; CHEMICAL PARAMETERS; CONTROLLED STUDY; DISEASE COURSE; GENE; GENE MUTATION; HALF LIFE TIME; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; IMMUNOCYTOCHEMISTRY; ISOMERIZATION; MOLECULAR PATHOLOGY; MUTATIONAL ANALYSIS; NIGHT BLINDNESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; RATE CONSTANT; RETINITIS PIGMENTOSA; RHODOPSIN GENE; THERMAL ANALYSIS; THERMAL DECAY; THERMOSTABILITY;

7-HELIX RECEPTOR; DARK NOISE; G PROTEIN-COUPLED RECEPTORS; HYDROGEN BOND NETWORK; HYDROLYSIS; ISOMERIZATION; MEMBRANE PROTEINS; MUTANT; RHODOPSIN; THERMAL DECAY;

CATALYTIC DOMAIN; CELL MEMBRANE; HALF-LIFE; HEK293 CELLS; HUMANS; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; ISOMERISM; KINETICS; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN TRANSPORT; RETINITIS PIGMENTOSA; RHODOPSIN; SCHIFF BASES; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 84879056670     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.397257     Document Type: Article

References (74)

1. Shastry, B. S. (1994) Retinitis pigmentosa and related disorders: phenotypes of rhodopsin and peripherin/RDS mutations. Am. J. Med. Genet. 52, 467-474
2. Berson, E. L. (1996) Retinitis pigmentosa: unfolding its mystery. Proc. Natl. Acad. Sci. U.S.A. 93, 4526-4528
3. Kalloniatis, M., and Fletcher, E. L. (2004) Retinitis pigmentosa: understanding the clinical presentation, mechanisms, and treatment options. Clin. Exp. Optom. 87, 65-80
4. Kennan, A., Aherne, A., and Humphries, P. (2005) Light in retinitis pigmentosa. Trends Genet. 21, 103-110 (Pubitemid 40127354)
5. Hartong, D. T., Berson, E. L., and Dryja, T. P. (2006) Retinitis pigmentosa. Lancet 368, 1795-1809 (Pubitemid 44739028)
6. Shintani, K., Shechtman, D. L., and Gurwood, A. S. (2009) Review and update: current treatment trends for patients with retinitis pigmentosa. Optometry 80, 384-401
7. Rakoczy, E. P., Kiel, C., McKeone, R., Stricher, F., and Serrano, L. (2011) Analysis of disease-linked rhodopsin mutations based on structure, function, and protein stability calculations. J. Mol. Biol. 405, 584-606
8. Sung, C. H., Schneider, B. G., Agarwal, N., Papermaster, D. S., and Nathans, J. (1991) Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Proc. Natl. Acad. Sci. U.S.A. 88, 8840-8844 (Pubitemid 21915451)
9. Sung, C. H., Davenport, C. M., and Nathans, J. (1993) Rhodopsin mutations responsible for autosomal dominant retinitis pigmentosa. Clustering of functional classes along the polypeptide chain. J. Biol. Chem. 268, 26645-26649 (Pubitemid 23361747)
10. Mendes, H. F., van der Spuy, J., Chapple, J. P., and Cheetham, M. E. (2005) Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy. Trends Mol. Med. 11, 177-185
11. Ruther, K., vonBallestrem, C. L., Muller, A., Kremmer, S., Eckstein, A., ApfelstedtSylla, E., Gal, A., and Zrenner, E. (1995) in Clinical Features of Autosomal Dominant Retinitis Pigmentosa Associated with the SER 186TRP Mutation of Rhodopsin (Anderson, R. E., LaVail, M. M., and Hollyfield, J. G., eds) pp. 303-312, Plenum Publishing Corp., New York
12. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289, 739-745 (Pubitemid 30650186)
13. Menon, S. T., Han, M., and Sakmar, T. P. (2001) Rhodopsin: structural basis of molecular physiology. Physiol. Rev. 81, 1659-1688 (Pubitemid 32947780)
14. Okada, T., Ernst, O. P., Palczewski, K., and Hofmann, K. P. (2001) Activation of rhodopsin: new insights from structural and biochemical studies. Trends Biochem. Sci. 26, 318-324 (Pubitemid 32436382)
15. Filipek, S., Stenkamp, R. E., Teller, D. C., and Palczewski, K. (2003) G protein-coupled receptor rhodopsin: a prospectus. Annu. Rev. Physiol. 65, 851-879 (Pubitemid 38249179)
16. Li, J., Edwards, P. C., Burghammer, M., Villa, C., and Schertler, G. F. (2004) Structure of bovine rhodopsin in a trigonal crystal form. J. Mol. Biol. 343, 1409-1438 (Pubitemid 39387834)
17. Okada, T., Sugihara, M., Bondar, A. N., Elstner, M., Entel, P., and Buss, V. (2004) The retinal conformation and its environment in rhodopsin in light of a new 2.2 Å crystal structure. J. Mol. Biol. 342, 571-583 (Pubitemid 39149759)
18. Palczewski, K. (2006) G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 75, 743-767
19. Ridge, K. D., and Palczewski, K. (2007) Visual rhodopsin sees the light: structure and mechanism of G protein signaling. J. Biol. Chem. 282, 9297-9301 (Pubitemid 47104561)
20. Gleim, S., and Hwa, J. (2008) in Visual Transduction and Non-visual Light Perception (Tombran-Tink, J., and Barnstable, C. J., eds) pp. 171-196, Humana Press Inc., Totowa, NJ
21. Ahuja, S., Hornak, V., Yan, E. C., Syrett, N., Goncalves, J. A., Hirshfeld, A., Ziliox, M., Sakmar, T. P., Sheves, M., Reeves, P. J., Smith, S. O., and Eilers, M. (2009) Helix movement is coupled to displacement of the second extracellular loop in rhodopsin activation. Nat. Struct. Mol. Biol. 16, 168-175
22. Papermaster, D. S., and Dreyer, W. J. (1974) Rhodopsin content in the outer segment membranes of bovine and frog retinal rods. Biochemistry 13, 2438-2444
23. Hubbard, R., and Wald, G. (1951) The mechanism of rhodopsin synthesis. Proc. Natl. Acad. Sci. U.S.A. 37, 69-79
24. Hug, S. J., Lewis, J. W., Einterz, C. M., Thorgeirsson, T. E., and Kliger, D. S. (1990) Nanosecond photolysis of rhodopsin: evidence for a new, blue-shifted intermediate. Biochemistry 29, 1475-1485 (Pubitemid 20063378)
25. Randall, C. E., Lewis, J. W., Hug, S. J., Bjorling, S. C., Eisnershanas, I., Friedman, N., Ottolenghi, M., Sheves, M., and Kliger, D. S. (1991) J. Am. Chem. Soc. 113, 3473-3485
26. Schoenlein, R. W., Peteanu, L. A., Mathies, R. A., and Shank, C. V. (1991) The first step in vision: femtosecond isomerization of rhodopsin. Science 254, 412-415 (Pubitemid 21917354)
27. Pan, D., Ganim, Z., Kim, J. E., Verhoeven, M. A., Lugtenburg, J., and Mathies, R. A. (2002) Time-resolved resonance Raman analysis of chromophore structural changes in the formation and decay of rhodopsin's BSI intermediate. J. Am. Chem. Soc. 124, 4857-4864 (Pubitemid 34465025)
28. Lüdeke, S., Lórenz Fonfría, V. A., Siebert, F., and Vogel, R. (2006) Time-resolved rapid-scan Fourier transform infrared difference spectroscopy on a noncyclic photosystem: rhodopsin photointermediates from Lumi to Meta II. Biopolymers 83, 159-169 (Pubitemid 44454217)
29. Smith, S. O. (2010) Structure and activation of the visual pigment rhodopsin. Annu. Rev. Biophys. 39, 309-328
30. Fung, B. K., Hurley, J. B., and Stryer, L. (1981) Flow of information in the light-triggered cyclic nucleotide cascade of vision. Proc. Natl. Acad. Sci. U.S.A. 78, 152-156 (Pubitemid 11131256)
31. Burns, M. E., and Arshavsky, V. Y. (2005) Beyond counting photons: trials and trends in vertebrate visual transduction. Neuron 48, 387-401 (Pubitemid 41551946)
32. Bhatti, M. T. (2006) Retinitis pigmentosa, pigmentary retinopathies, and neurologic diseases. Curr. Neurol. Neurosci. Rep. 6, 403-413
33. Barlow, H. B. (1956) Retinal noise and absolute threshold. J. Opt. Soc. Am. 46, 634-639
34. Baylor, D. A., Lamb, T. D., and Yau, K. W. (1979) Responses of retinal rods to single photons. J. Physiol. 288, 613-634 (Pubitemid 9146907)
35. Ashmore, J. F., and Falk, G. (1977) Dark noise in retinal bipolar cells and stability of rhodopsin in rods. Nature 270, 69-71 (Pubitemid 8201716)
36. Baylor, D. A., Matthews, G., and Yau, K. W. (1980) Two components of electrical dark noise in toad retinal rod outer segments. J. Physiol. 309, 591-621 (Pubitemid 11199961)
37. Luo, D. G., Yue, W. W., Ala-Laurila, P., and Yau, K. W. (2011) Activation of visual pigments by light and heat. Science 332, 1307-1312
38. Robinson, P. R., Cohen, G. B., Zhukovsky, E. A., and Oprian, D. D. (1992) Constitutively active mutants of rhodopsin. Neuron 9, 719-725
39. Dryja, T. P., Berson, E. L., Rao, V. R., and Oprian, D. D. (1993) Heterozygous missense mutation in the rhodopsin gene as a cause of congenital stationary night blindness. Nat. Genet. 4, 280-283 (Pubitemid 23205177)
40. Rao, V. R., Cohen, G. B., and Oprian, D. D. (1994) Rhodopsin mutation G90D and a molecular mechanism for congenital night blindness. Nature 367, 639-642 (Pubitemid 24067704)
41. Cohen, G. B., Yang, T., Robinson, P. R., and Oprian, D. D. (1993) Constitutive activation of opsin: influence of charge at position 134 and size at position 296. Biochemistry 32, 6111-6115 (Pubitemid 23198773)
42. Liu, J., Liu, M. Y., Nguyen, J. B., Bhagat, A., Mooney, V., and Yan, E. C. (2009) Thermal decay of rhodopsin: role of hydrogen bonds in thermal isomerization of 11-cis-retinal in the binding site and hydrolysis of protonated Schiff base. J. Am. Chem. Soc. 131, 8750-8751
43. Liu, J., Liu, M. Y., Nguyen, J. B., Bhagat, A., Mooney, V., and Yan, E. C. (2011) Thermal properties of rhodopsin: insight into the molecular mechanism of dim-light vision. J. Biol. Chem. 286, 27622-27629
44. Liu, J., Liu, M. Y., Fu, L., Zhu, G. A., and Yan, E. C. (2011) Chemical kinetic analysis of thermal decay of rhodopsin reveals unusual energetics of thermal isomerization and hydrolysis of Schiff base. J. Biol. Chem. 286, 38408-38416
45. Okada, T., Fujiyoshi, Y., Silow, M., Navarro, J., Landau, E. M., and Shichida, Y. (2002) Functional role of internal water molecules in rhodopsin revealed by x-ray crystallography. Proc. Natl. Acad. Sci. U.S.A. 99, 5982-5987 (Pubitemid 34493251)
46. Janz, J. M., and Farrens, D. L. (2004) Role of the retinal hydrogen bond network in rhodopsin Schiff base stability and hydrolysis. J. Biol. Chem. 279, 55886-55894 (Pubitemid 40066596)
47. Yan, E. C., Kazmi, M. A., De, S., Chang, B. S., Seibert, C., Marin, E. P., Mathies, R. A., and Sakmar, T. P. (2002) Function of extracellular loop 2 in rhodopsin: glutamic acid 181 modulates stability and absorption wavelength of metarhodopsin II. Biochemistry 41, 3620-3627 (Pubitemid 34224674)
48. Yan, E. C., Kazmi, M. A., Ganim, Z., Hou, J. M., Pan, D., Chang, B. S., Sakmar, T. P., and Mathies, R. A. (2003) Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 100, 9262-9267 (Pubitemid 37033917)
49. Lüdeke, S., Beck, M., Yan, E. C., Sakmar, T. P., Siebert, F., and Vogel, R. (2005) The role of Glu-181 in the photoactivation of rhodopsin. J. Mol. Biol. 353, 345-356
50. Davidson, F. F., Loewen, P. C., and Khorana, H. G. (1994) Structure and function in rhodopsin: replacement by alanine of cysteine residues 110 and 187, components of a conserved disulfide bond in rhodopsin, affects the light-activated metarhodopsin II state. Proc. Natl. Acad. Sci. U.S.A. 91, 4029-4033 (Pubitemid 24139566)
51. Janz, J. M., and Farrens, D. L. (2003) Assessing structural elements that influence Schiff base stability: mutants E113Q and D190N destabilize rhodopsin through different mechanisms. Vision Res. 43, 2991-3002 (Pubitemid 37377611)
52. Janz, J. M., Fay, J. F., and Farrens, D. L. (2003) Stability of dark state rhodopsin is mediated by a conserved ion pair in intradiscal loop E-2. J. Biol. Chem. 278, 16982-16991 (Pubitemid 36799573)
53. Angel, T. E., Chance, M. R., and Palczewski, K. (2009) Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors. Proc. Natl. Acad. Sci. U.S.A. 106, 8555-8560
54. Yan, E. C., Epps, J., Lewis, J. W., Szundi, I., Bhagat, A., Sakmar, T. P., and Kliger, D. S. (2007) J. Phys. Chem. C 111, 8843-8848
55. Yan, E. C., Ganim, Z., Kazmi, M. A., Chang, B. S., Sakmar, T. P., and Mathies, R. A. (2004) Resonance Raman analysis of the mechanism of energy storage and chromophore distortion in the primary visual photoproduct. Biochemistry 43, 10867-10876 (Pubitemid 39433677)
56. Sandberg, M. N., Amora, T. L., Ramos, L. S., Chen, M. H., Knox, B. E., and Birge, R. R. (2011) Glutamic acid 181 is negatively charged in the bathorhodopsin photointermediate of visual rhodopsin. J. Am. Chem. Soc. 133, 2808-2811
57. Hwa, J., Reeves, P. J., Klein-Seetharaman, J., Davidson, F., and Khorana, H. G. (1999) Structure and function in rhodopsin: further elucidation of the role of the intradiscal cysteines, Cys-110, -185, and -187, in rhodopsin folding and function. Proc. Natl. Acad. Sci. U.S.A. 96, 1932-1935 (Pubitemid 29117845)
58. Krebs, M. P., Holden, D. C., Joshi, P., Clark, C. L., 3rd, Lee, A. H., and Kaushal, S. (2010) Molecular mechanisms of rhodopsin retinitis pigmentosa and the efficacy of pharmacological rescue. J. Mol. Biol. 395, 1063-1078
59. Matias-Florentino, M., Ayala-Ramirez, R., Graue-Wiechers, F., and Zenteno, J. C. (2009) Molecular screening of rhodopsin and peripherin/RDS genes in Mexican families with autosomal dominant retinitis pigmentosa. Curr. Eye Res. 34, 1050-1056
60. Tsui, I., Chou, C. L., Palmer, N., Lin, C. S., and Tsang, S. H. (2008) Phenotype-genotype correlations in autosomal dominant retinitis pigmentosa caused by RHO, D190N. Curr. Eye Res. 33, 1014-1022
61. Kaushal, S., and Khorana, H. G. (1994) Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33, 6121-6128 (Pubitemid 24190763)
62. Molday, R. S., and MacKenzie, D. (1983) Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry 22, 653-660
63. Ferretti, L., Karnik, S. S., Khorana, H. G., Nassal, M., and Oprian, D. D. (1986) Total synthesis of a gene for bovine rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 83, 599-603 (Pubitemid 16035522)
64. Reeves, P. J., Callewaert, N., Contreras, R., and Khorana, H. G. (2002) Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl. Acad. Sci. U.S.A. 99, 13419-13424 (Pubitemid 35215396)
65. Reeves, P. J., Kim, J. M., and Khorana, H. G. (2002) Structure and function in rhodopsin: a tetracycline-inducible system in stable mammalian cell lines for high-level expression of opsin mutants. Proc. Natl. Acad. Sci. U.S.A. 99, 13413-13418 (Pubitemid 35215395)
66. Oprian, D. D., Molday, R. S., Kaufman, R. J., and Khorana, H. G. (1987) Expression of a synthetic bovine rhodopsin gene in monkey kidney cells. Proc. Natl. Acad. Sci. U.S.A. 84, 8874-8878
67. Min, K. C., Zvyaga, T. A., Cypess, A. M., and Sakmar, T. P. (1993) Characterization of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Mutations on the cytoplasmic surface affect transducin activation. J. Biol. Chem. 268, 9400-9404 (Pubitemid 23145989)
68. Sakmar, T. P., Franke, R. R., and Khorana, H. G. (1989) Glutamic acid 113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 86, 8309-8313 (Pubitemid 19286049)
69. Wald, G., and Brown, P. K. (1953) The molar extinction of rhodopsin. J. Gen. Physiol. 37, 189-200
70. Kito, Y., Suzuki, T., Azuma, M., and Sekoguti, Y. (1968) Absorption spectrum of rhodopsin denatured with acid. Nature 218, 955-957
71. Ozaki, K., Terakita, A., Hara, R., and Hara, T. (1986) Rhodopsin and retinochrome in the retina of a marine gastropod, Conomulex luhuanus. Vision Res. 26, 691-705 (Pubitemid 16120961)
72. Sancho-Pelluz, J., Tosi, J., Hsu, C. W., Lee, F., Wolpert, K., Tabacaru, M. R., Greenberg, J. P., Tsang, S. H., and Lin, C. S. (2012) Mice with a D190N mutation in the gene encoding rhodopsin: a model for human autosomal-dominant retinitis pigmentosa. Mol. Med. 18, 549-555
73. Angel, T. E., Gupta, S., Jastrzebska, B., Palczewski, K., and Chance, M. R. (2009) Structural waters define a functional channel mediating activation of the GPCR, rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 106, 14367-14372
74. Fishman, G. A., Vandenburgh, K., Stone, E. M., Gilbert, L. D., Alexander, K. R., and Sheffield, V. C. (1992) Ocular findings associated with rhodopsin gene codon 267 and codon 190 mutations in dominant retinitis pigmentosa. Arch. Ophthalmol. 110, 1582-1588