Methyl Substituents at the 11 or 12 Position of Retinal Profoundly and Differentially Affect Photochemistry and Signalling Activity of Rhodopsin

Journal of Molecular Biology

Volumn 363, Issue 1, 2006, Pages 98-113

  Verhoeven, Michiel A ^c   Bovee Geurts, Petra H M ^b   de Groot, Huub J M ^a   Lugtenburg, Johan ^a   DeGrip, Willem J ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c NONE

Author keywords

Fourier transform infrared spectroscopy; photoactivation; quantum yield; retinal synthesis; rhodopsin analog pigment

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; METHYL GROUP; RHODOPSIN;

ARTICLE; BINDING SITE; CHROMATOPHORE; INFRARED SPECTROSCOPY; ISOMER; ISOMERIZATION; PHOTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; ULTRAVIOLET SPECTROSCOPY;

EID: 33748787144     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.07.039     Document Type: Article

References (85)

1. Wald G. The molecular basis of visual excitation. Nature 219 (1968) 800-807
2. Hofmann K.P. Late photoproducts and signaling states of bovine rhodopsin. In: Stavenga D.G., DeGrip W.J., and Pugh Jr. E.N. (Eds). Molecular Mechanisms in Visual Transduction (2000), Elsevier Science Publisher, Amsterdam 91-142
3. 13C MAS NMR spectroscopy. J. Am. Chem. Soc. 119 (1997) 169-174
4. 13C-labeling and 1-D rotational resonance MAS NMR. Biochemistry-USA 38 (1999) 11316-11324
5. 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
6. Bifone A., DeGroot H.J.M., and Buda F. Ab initio molecular dynamics of rhodopsin. Pure Appl. Chem. 69 (1997) 2105-2110
7. Cembran A., Bernardi F., Olivucci M., and Garavelli M. The retinal chromophore/chloride ion pair: structure of the photo-isomerization path and interplay of charge transfer and covalent states. Proc. Natl Acad. Sci. USA 102 (2005) 6255-6260
8. Mathies R.A., and Lugtenburg J. The primary photoreaction of rhodopsin. In: Stavenga D.G., DeGrip W.J., and Pugh Jr. E.N. (Eds). Molecular Mechanisms in Visual Transduction (2000), Elsevier Science Publisher, Amsterdam 55-90
9. Yan E.C.Y., Ganim Z., Kazmi M.A., Chang B.S.W., Sakmar T.P., and Mathies R.A. Resonance Raman analysis of the mechanism of energy storage and chromophore distortion in the primary visual photoproduct. Biochemistry-USA 43 (2004) 10867-10876
10. Kukura P., McCamant D.W., Yoon S., Wandschneider D.B., and Mathies R.A. Structural observation of the primary isomerization in vision with femtosecond-stimulated Raman. Science 310 (2005) 1006-1009
11. Nakamichi H., and Okada T. Crystallographic analysis of primary visual photochemistry. Angew. Chem. Int. Ed. 45 (2006) 4270-4273
12. Kliger D.S., and Lewis J.W. Spectral and kinetic characterization of visual pigment photointermediates. Isr. J. Chem. 35 (1995) 309-323
13. Kochendoerfer G.G., Verdegem P.J.E., VanDerHoef I., Lugtenburg J., and Mathies R.A. Retinal analog study of the role of steric interactions in the excited state isomerization dynamics of rhodopsin. Biochemistry-USA 35 (1996) 16230-16240
14. Ganter U.M., Gärtner W., and Siebert F. The influence of the 13-methyl group of the retinal on the photoreaction of rhodopsin revealed by FTIR difference spectroscopy. Eur. Biophys. J. 18 (1990) 295-299
15. Ganter U.M., Schmid E.D., Perez-Sala D., Rando R.R., and Siebert F. Removal of the 9-methyl group of retinal inhibits signal transduction in the visual process. A Fourier-transform infrared and biochemical investigation. Biochemistry-USA 28 (1989) 5954-5962
16. Meyer C.K., Böhme M., Ockenfels A., Gärtner W., Hofmann K.P., and Ernst O.P. Signaling states of rhodopsin - Retinal provides a scaffold for activating proton transfer switches. J. Biol. Chem. 275 (2000) 19713-19718
17. Kropf A., Whittenberger B.P., Goff S.P., and Waggoner A.S. The spectral properties of some visual pigment analogs. Expt. Eye Res. 17 (1973) 591-606
18. Vogel R., Fan G.-B., Sheves M., and Siebert F. The molecular origin of the inhibition of transducin activation in rhodopsin lacking the 9-methyl group of the retinal chromophore: a UV-Vis and FTIR spectroscopic study. Biochemistry-USA 39 (2000) 8895-8908
19. Ebrey T.G., Tsuda M., Sassenrath G., West J.L., and Waddell W.H. Light activation of bovine rod phosphodiesterase by non-physiological visual pigments. FEBS Letters 116 (1980) 217-219
20. Corson D.W., Kefalov V.J., Cornwall M.C., and Crouch R.K. Effect of 11-cis 13-demethylretinal on phototransduction in bleach-adapted rod and cone photoreceptors. J. Gen. Physiol. 116 (2000) 283-297
21. Corson D.W., Cornwall M.C., MacNichol Jr. E.F., Tsang S.H., Derguini F., Crouch R.K., and Nakanishi K. Relief of opsin desensitization and prolonged excitation of rod photoreceptors by 9-desmethylretinal. Proc. Natl Acad. Sci. USA 91 (1994) 6958-6962
22. Vogel R., Lüdeke S., Siebert F., Sakmar T.P., Hirshfeld A., and Sheves M. Agonists and partial agonists of rhodopsin: Retinal polyene methylation affects receptor activation. Biochemistry-USA 45 (2006) 1640-1652
23. DeLange F., Bovee-Geurts P.H.M., VanOostrum J., Portier M.D., Verdegem P.J.E., Lugtenburg J., and DeGrip W.J. An additional methyl group at the 10-position of retinal dramatically slows down the kinetics of the rhodopsin photocascade. Biochemistry-USA 37 (1998) 1411-1420
24. Einterz C.M., Hug S.J., Lewis J.W., and Kliger D.S. Early photolysis intermediates of the artificial visual pigment 13-demethylrhodopsin. Biochemistry-USA 29 (1990) 1485-1491
25. Liu R.S.H., Crescitelli F., Denny M., Matsumoto H., and Asato A.E. Photosensitivity of 10-substituted visual pigment analogues: Detection of a specific secondary opsin-retinal interaction. Biochemistry-USA 25 (1986) 7026-7030
26. Liu R.S.H., Asato A.E., Denny M., and Mead D.A. The nature of restrictions in the binding site of rhodopsin. A model study. J. Amer. Chem. Soc. 106 (1984) 8298-8300
27. Liu R.S.H., and Asato A.E. The binding site of opsin based on analog studies with isomeric, fluorinated, alkylated, and other modified retinals. In: Dawson M.I., and Okamura W.H. (Eds). Chemistry and Biology of Synthetic Retinoids (1990), CRC Press, Boca Raton, FL 52-75
28. Bifone A., DeGroot H.J.M., and Buda F. Energy storage in the primary photoproduct of vision. J. Phys. Chem. B 101 (1997) 2954-2958
29. Buda F., DeGroot H.J.M., and Bifone A. Charge localization and dynamics in rhodopsin. Phys. Rev. Letters 77 (1996) 4474-4477
30. DeGrip W.J., and Rothschild K.J. Structure and mechanism of vertebrate visual pigments. In: Stavenga D.G., DeGrip W.J., and Pugh Jr. E.N. (Eds). Molecular Mechanisms in Visual Transduction (2000), Elsevier Science Publisher, Amsterdam 1-54
31. Kim J.E., Pan D.H., and Mathies R.A. Picosecond dynamics of G-protein coupled receptor activation in rhodopsin from time-resolved UV resonance Raman spectroscopy. Biochemistry-USA 42 (2003) 5169-5175
32. Pan D.H., Ganim Z., Kim J.E., Verhoeven M.A., Lugtenburg J., and Mathies R.A. Time-resolved resonance Raman analysis of chromophore structural changes in the formation and decay of rhodopsin's BSI intermediate. J. Am. Chem. Soc. 124 (2002) 4857-4864
33. Pan D.H., and Mathies R.A. Chromophore structure in lumirhodopsin and metarhodopsin I by time-resolved resonance Raman microchip spectroscopy. Biochemistry-USA 40 (2001) 7929-7936
34. Cooper A. Rhodopsin photoenergetics-lumirhodopsin and the complete energy profile. FEBS Letters 123 (1981) 324-326
35. Cooper A. Energy uptake in the first step of visual excitation. Nature 282 (1979) 531-533
36. DeGrip W.J., Gray D., Gillespie J., Bovee-Geurts P.H.M., VanDenBerg E.M.M., Lugtenburg J., and Rothschild K.J. Photoexcitation of rhodopsin: conformation changes in the chromophore, protein and associated lipid, as determined by FTIR difference spectroscopy. Photochem. Photobiol. 48 (1988) 497-504
37. Rothschild K.J., Cantore W.A., and Marrero H. Fourier transform infrared difference spectra of intermediates in rhodopsin bleaching. Science 219 (1983) 1333-1335
38. Han M., Groesbeek M., Smith S.O., and Sakmar T.P. Role of the C9 methyl group in rhodopsin activation: characterization of mutant opsins with the artificial chromophore 11-cis-9-demethylretinal. Biochemistry-USA 37 (1998) 538-545
39. Rodieck R.W. The Vertebrate Retina - Principles of Structure and Function (1973), W.H. Freeman and Company, San Francisco, CA
40. Sperling W., and Rafferty C.N. Relationship between absorption spectrum and molecular conformations of 11-cis-retinal. Nature 224 (1969) 590-594
41. Tsujimoto K., Shirasaka Y., Mizukami T., and Ohashi M. Unusual conformation and photoisomerization of retinochrome analogues with 11-methylretinals. Chem. Letters (1997) 813-814
42. Wang Y.-J., Bovee-Geurts P.H.M., Lugtenburg J., and DeGrip W.J. Constraints of the 9-methyl group binding pocket of the rhodopsin chromophore probed by 9-halogeno substitution. Biochemistry-USA 43 (2004) 14802-14810
43. Palczewski K., Kumasaka T., Hori T., Behnke C.A., Motoshima H., Fox B.A., et al. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289 (2000) 739-745
44. Sheves M., Albeck A., Ottolenghi M., Bovee-Geurts P.H.M., DeGrip W.J., Einterz C.M., et al. An artifical visual pigment with restricted C9-C11 motion forms normal photolysis intermediates. J. Am. Chem. Soc. 108 (1986) 6440-6441
45. Asato A.E., Denny M., and Liu R.S.H. Bioorganic studies of visual pigment analogs. 5. Retinal and rhodopsin analogs directed toward a better understanding of the H.T.-n model of the primary process of vision. J. Am. Chem. Soc. 108 (1986) 5032-5033
46. Eyring G., Curry B., Broek A., Lugtenburg J., and Mathies R.A. Assignment and interpretation of hydrogen out-of-plane vibrations in the resonance Raman spectra of rhodopsin and bathorhodopsin. Biochemistry-USA 21 (1982) 384-393
47. Mathies R.A., Smith S.O., and Palings I. Determination of retinal chromophore structure in rhodopsins. In: Spiro T.G. (Ed). Resonance Raman Spectra of Polyenes and Aromatics (1987), John Wiley and Sons, New York, NY 59-108
48. Touw S.I.E., DeGroot H.J.M., and Buda F. Ab initio modeling of the spatial, electronic, and vibrational structure of Schiff base models for visual photoreceptors. J. Phys. Chem. B 108 (2004) 13560-13572
49. Palings I., Pardoen J.A., VanDenBerg E.M.M., Winkel C., Lugtenburg J., and Mathies R.A. Assignment of fingerprint vibrations in the resonance Raman spectra of rhodopsin, isorhodopsin, and bathorhodopsin: implications for chromophore structure and environment. Biochemistry-USA 26 (1987) 2544-2556
50. Palings I., VanDenBerg E.M.M., Lugtenburg J., and Mathies R.A. Complete assignment of the hydrogen out-of-plane wagging vibrations of bathorhodopsin: Chromophore structure and energy storage in the primary photoproduct of vision. Biochemistry-USA 28 (1989) 1498-1507
51. Wang Q., Kochendoerfer G.G., Schoenlein R.W., Verdegem P.J.E., Lugtenburg J., Mathies R.A., and Shank C.V. Femtosecond spectroscopy of a 13-demethylrhodopsin visual pigment analogue: The role of non-bonded interactions in the isomerization process. J. Phys. Chem. B 100 (1996) 17388-17394
52. Parkes J.H., and Liebman P.A. Temperature and pH dependence of the Metarhodopsin I-Metarhodopsin II kinetics and equilibria in bovine rod disk membrane suspensions. Biochemistry-USA 23 (1984) 5054-5061
53. Matthews R.G., Hubbard R., Brown P.K., and Wald G. Tautomeric forms of metarhodopsin. J. Gen. Physiol. 47 (1963) 215-240
54. Kolesnikov A.V., Golobokova E.Y., and Govardovskii V.I. The identity of metarhodopsin III. Visual Neurosci. 20 (2003) 249-265
55. Kusnetzow A.K., Altenbach C., and Hubbell W.L. Conformational states and dynamics of rhodopsin in micelles and bilayers. Biochemistry-USA 45 (2006) 5538-5550
56. Vogel R., Siebert F., Zhang X.Y., Fan G.-B., and Sheves M. Formation of meta III during the decay of activated rhodopsin proceeds via meta I and not via meta. Biochemistry-USA 43 (2004) 9457-9466
57. Vogel R., Siebert F., Lüdeke S., Hirshfeld A., and Sheves M. Agonists and partial agonists of rhodopsin: Retinals with ring modifications. Biochemistry-USA 44 (2005) 11684-11699
58. Bartl F.J., Fritze O., Ritter E., Herrmann R., Kuksa V., Palczewski K., et al. Partial agonism in a G protein-coupled receptor - role of the retinal ring structure in rhodopsin activation. J. Biol. Chem. 280 (2005) 34259-34267
59. DeLange F., Bovee-Geurts P.H.M., Pistorius A.M.A., Rothschild K.J., and DeGrip W.J. Probing intramolecular orientations in rhodopsin and metarhodopsin II by polarized infrared difference spectroscopy. Biochemistry-USA 38 (1999) 13200-13209
60. Spooner P.J.R., Sharples J.M., Goodall S.C., Bovee-Geurts P.H.M., Verhoeven M.A., Lugtenburg J., et al. The ring of the rhodopsin chromophore in a hydrophobic activation switch within the binding pocket. J. Mol. Biol. 343 (2004) 719-730
61. Patel A.B., Crocker E., Eilers M., Hirshfeld A., Sheves M., and Smith S.O. Coupling of retinal isomerization to the activation of rhodopsin. Proc. Natl Acad. Sci. USA 101 (2004) 10048-10053
62. Verhoeven, M. A. (2005). Electronic and spatial characteristics of the retinylidene chromophore of rhodopsin. PhD Thesis, Leiden University, The Netherlands.
63. Liu R.S.H., and Colmenares L.U. The molecular basis for the high photosensitivity of rhodopsin. Proc. Natl Acad. Sci. USA 100 (2003) 14639-14644
64. Birge R.R., and Vought B.W. Energetics of rhodopsin photobleaching: photocalorimetric studies of energy storage in early and later intermediates. Methods Enzymol. 315 (2000) 143-163
65. 5 route - exploring the possibility of preparing any retinoid rationally chemically modified at any position in the conjugated tail. Eur. J. Org. Chem. (2004) 5100-5110
66. Schick G.A., Cooper T.M., Holloway R.A., Murray L.P., and Birge R.R. Energy-storage in the primary photochemical events of rhodopsin and isorhodopsin. Biochemistry-USA 26 (1987) 2556-2562
67. Kim J.E., Tauber M.J., and Mathies R.A. Wavelength dependent cis-trans isomerization in vision. Biochemistry-USA 40 (2001) 13774-13778
68. 13C-labeled retinal via a modular total organic synthetic strategy. Emerging central contribution of organic synthesis toward the structure and function study with atomic resolution in protein research. J. Am. Chem. Soc. 124 (2002) 6324-6334
69. 13C-labeled retinals. Pure Appl. Chem. 57 (1985) 753-762
70. 13C-labeled conjugated systems. Rec. Trav. Chim. J. Roy. Neth. Chem. 111 (1992) 149-154
71. Olivè J.-L., Mousseron-Canet M., and Dornand J. Acetylenic intermediates in synthesis of vitamin A and its isomers. Bull. Soc. Chim. Fr. (1969) 3247-3252
72. 2)astaxanthin. Rec. Trav. Chim. J. Roy. Neth. Chem. 113 (1994) 552-562
73. Sato K., Mizuno S., and Hirayama M. A total synthesis of phytol. J. Org. Chem. 32 (1967) 177-180
74. Friese A., Hell-Momeni K., Zundorf I., Winckler T., Dingermann T., and Dannhardt G. Synthesis and biological evaluation of cycloalkylidene carboxylic acids as novel effectors of Ras/Raf interaction. J. Med. Chem. 45 (2002) 1535-1542
75. Cooke M.P. Acylation of organolithium reagents by esters in the presence of chlorotrimethylsilane. J. Org. Chem. 51 (1986) 951-953
76. Hubbard R., Brown P.K., and Bownds M.D. Methodology of vitamin A and visual pigments. Methods Enzymol. 18 (1971) 615-653
77. DeGrip W.J., VanOostrum J., Bovee-Geurts P.H.M., VanDerSteen R., VanAmsterdam L.J.P., Groesbeek M., and Lugtenburg J. 10,20-Methanorhodopsins: (7E,9E,13E)-10,20-methanorhodopsin and (7E,9Z,13Z)-10,20-methanorhodopsin - 11-cis-locked rhodopsin analog pigments with unusual thermal and photo-stability. Eur. J. Biochem. 191 (1990) 211-220
78. DeGrip W.J., VanOostrum J., and Bovee-Geurts P.H.M. Selective detergent-extraction from mixed detergent/lipid/protein micelles, using cyclodextrin inclusion compounds: a novel generic approach for the preparation of proteoliposomes. Biochem. J. 330 (1998) 667-674
79. Dartnall H.J.A. Photosensitivity. In: Dartnall H.J.A. (Ed). Photochemistry of Vision (1972), Springer-Verlag, Berlin 122-145
80. Hubbard R., and Wald G. Cis-trans isomers of vitamin A and retinene in the rhodopsin system. J. Gen. Physiol. 36 (1952) 269-315
81. Clark N.A., Rothschild K.J., Simon B.A., and Luippold D.A. Surface induced orientation of multilayer membrane arrays: Theoretical analysis and a new method with application to purple membrane fragments. Biophys. J. 31 (1980) 65-96
82. DeLange F., Merkx M., Bovee-Geurts P.H.M., Pistorius A.M.A., and DeGrip W.J. Modulation of the metarhodopsin I/metarhodopsin II equilibrium of bovine rhodopsin by ionic strength - evidence for a surface charge effect. Eur. J. Biochem. 243 (1997) 174-180
83. Phillips W.J., and Cerione R.A. The intrinsic fluorescence of the a subunit of transducin - Measurement of receptor-dependent guanine nucleotide exchange. J. Biol. Chem. 263 (1988) 15498-15505
84. Fahmy K., and Sakmar T.P. Regulation of the rhodopsin-transducin interaction by a highly conserved carboxylic acid group. Biochemistry-USA 32 (1993) 7229-7236
85. Kühn H. Interactions between photoexcited rhodopsin and light-activated enzymes in rods. Prog. Retin. Res. 3 (1984) 123-156