Nanodomain organization of rhodopsin in native human and murine rod outer segment disc membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn , Issue Part A, 2015, Pages 26-34

  Whited, Allison M ^a   Park, Paul S H ^a  

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

Author keywords

Atomic force microscopy; G protein coupled receptor; Lipid raft; Membrane structure; Photoreceptor; Phototransduction

Indexed keywords

RHODOPSIN; NANOMATERIAL;

ANIMAL EXPERIMENT; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; MALE; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PARTICLE SIZE; PHOTOTRANSDUCTION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUALITATIVE ANALYSIS; RETINA ROD OUTER SEGMENT; STRUCTURE ANALYSIS; ANIMAL; C57BL MOUSE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN TERTIARY STRUCTURE; RETINAL ROD OUTER SEGMENT;

ANIMALS; CELL MEMBRANE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; HUMANS; MALE; MEMBRANE MICRODOMAINS; MICE, INBRED C57BL; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NANOSTRUCTURES; PROTEIN STRUCTURE, TERTIARY; RHODOPSIN; ROD CELL OUTER SEGMENT;

EID: 84908181391     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.10.007     Document Type: Article

References (89)

1. S. Nickell, P.S. Park, W. Baumeister, and K. Palczewski Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography J. Cell Biol. 177 2007 917 925
2. J.C. Gilliam, J.T. Chang, I.M. Sandoval, Y. Zhang, T. Li, S.J. Pittler, W. Chiu, and T.G. Wensel Three-dimensional architecture of the rod sensory cilium and its disruption in retinal neurodegeneration Cell 151 2012 1029 1041
3. F.J. Daemen Vertebrate rod outer segment membranes Biochim. Biophys. Acta 300 1973 255 288
4. P.A. Liebman, K.R. Parker, and E.A. Dratz The molecular mechanism of visual excitation and its relation to the structure and composition of the rod outer segment Annu. Rev. Physiol. 49 1987 765 791
5. D.S. Papermaster, and W.J. Dreyer Rhodopsin content in the outer segment membranes of bovine and frog retinal rods Biochemistry 13 1974 2438 2444
6. H.E. Hamm, and M.D. Bownds Protein complement of rod outer segments of frog retina Biochemistry 25 1986 4512 4523
7. W. Godchaux III, and W.F. Zimmerman Soluble proteins of intact bovine rod cell outer segments Exp. Eye Res. 28 1979 483 500
8. H. Heitzmann Rhodopsin is the predominant protein of rod outer segment membranes Nat. New Biol. 235 1972 114
9. N.W. Downer, and S.W. Englander Hydrogen exchange study of membrane-bound rhodopsin. I. Protein structure J. Biol. Chem. 252 1977 8092 8100
10. D.A. Baylor, T.D. Lamb, and K.W. Yau Responses of retinal rods to single photons J. Physiol. 288 1979 613 634
11. S. Hecht, S. Shlaer, and M.H. Pirenne Energy, quanta, and vision J. Gen. Physiol. 25 1942 819 840
12. H.J. Dartnall The photosensitivities of visual pigments in the presence of hydroxylamine Vision Res. 8 1968 339 358
13. L. Cangiano, and D. Dell'Orco Detecting single photons: a supramolecular matter? FEBS Lett. 587 2013 1 4
14. S.J. Singer, and G.L. Nicolson The fluid mosaic model of the structure of cell membranes Science 175 1972 720 731
15. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
16. K. Jacobson, O.G. Mouritsen, and R.G. Anderson Lipid rafts: at a crossroad between cell biology and physics Nat. Cell Biol. 9 2007 7 14
17. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
18. M. Edidin The state of lipid rafts: from model membranes to cells Annu. Rev. Biophys. Biomol. Struct. 32 2003 257 283
19. A. Mugler, F. Tostevin, and P.R. ten Wolde Spatial partitioning improves the reliability of biochemical signaling Proc. Natl. Acad. Sci. U. S. A. 110 2013 5927 5932
20. I. Bethani, S.S. Skanland, I. Dikic, and A. Acker-Palmer Spatial organization of transmembrane receptor signalling EMBO J. 29 2010 2677 2688
21. K. Radhakrishnan, A. Halasz, M.M. McCabe, J.S. Edwards, and B.S. Wilson Mathematical simulation of membrane protein clustering for efficient signal transduction Ann. Biomed. Eng. 40 2012 2307 2318
22. L.J. Pike Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function J. Lipid Res. 47 2006 1597 1598
23. A.M. Whited, and P.S. Park Atomic force microscopy: a multifaceted tool to study membrane proteins and their interactions with ligands Biochim. Biophys. Acta 1838 2014 56 68
24. A. Engel, and H.E. Gaub Structure and mechanics of membrane proteins Annu. Rev. Biochem. 77 2008 127 148
25. D.J. Muller AFM: a nanotool in membrane biology Biochemistry 47 2008 7986 7998
26. I. Casuso, F. Rico, and S. Scheuring Biological AFM: where we come from-where we are-where we may go J. Mol. Recognit. 24 2011 406 413
27. D. Fotiadis Atomic force microscopy for the study of membrane proteins Curr. Opin. Biotechnol. 23 2012 510 515
28. 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
29. D. Fotiadis, Y. Liang, S. Filipek, D.A. Saperstein, A. Engel, and K. Palczewski Atomic-force microscopy: rhodopsin dimers in native disc membranes Nature 421 2003 127 128
30. D. Fotiadis, Y. Liang, S. Filipek, D.A. Saperstein, A. Engel, and K. Palczewski The G protein-coupled receptor rhodopsin in the native membrane FEBS Lett. 564 2004 281 288
31. Y. Liang, D. Fotiadis, T. Maeda, A. Maeda, A. Modzelewska, S. Filipek, D.A. Saperstein, A. Engel, and K. Palczewski Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice J. Biol. Chem. 279 2004 48189 48196
32. N. Buzhynskyy, C. Salesse, and S. Scheuring Rhodopsin is spatially heterogeneously distributed in rod outer segment disk membranes J. Mol. Recognit. 24 2011 483 489
33. G. Milligan, and M. Bouvier Methods to monitor the quaternary structure of G protein-coupled receptors FEBS J. 272 2005 2914 2925
34. S. Ferre, V. Casado, L.A. Devi, M. Filizola, R. Jockers, M.J. Lohse, G. Milligan, J.P. Pin, and X. Guitart G protein-coupled receptor oligomerization revisited: functional and pharmacological perspectives Pharmacol. Rev. 66 2014 413 434
35. P.S.-H. Park, S. Filipek, J.W. Wells, and K. Palczewski Oligomerization of G protein-coupled receptors: past, present, and future Biochemistry 43 2004 15643 15656
36. S. Filipek, K.A. Krzysko, D. Fotiadis, Y. Liang, D.A. Saperstein, A. Engel, and K. Palczewski A concept for G protein activation by G protein-coupled receptor dimers: the transducin/rhodopsin interface Photochem. Photobiol. Sci. 3 2004 628 638
37. B. Jastrzebska, P. Ringler, K. Palczewski, and A. Engel The rhodopsin-transducin complex houses two distinct rhodopsin molecules J. Struct. Biol. 182 2013 164 172
38. M.E. Sommer, K.P. Hofmann, and M. Heck Arrestin-rhodopsin binding stoichiometry in isolated rod outer segment membranes depends on the percentage of activated receptors J. Biol. Chem. 286 2011 7359 7369
39. M.E. Sommer, K.P. Hofmann, and M. Heck Distinct loops in arrestin differentially regulate ligand binding within the GPCR opsin Nat. Commun. 3 2012 995
40. B. Jastrzebska, T. Orban, M. Golczak, A. Engel, and K. Palczewski Asymmetry of the rhodopsin dimer in complex with transducin FASEB J. 27 2013 1572 1584
41. 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
42. 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
43. P.S. Park, K.T. Sapra, B. Jastrzebska, T. Maeda, A. Maeda, W. Pulawski, M. Kono, J. Lem, R.K. Crouch, S. Filipek, D.J. Muller, and K. Palczewski Modulation of molecular interactions and function by rhodopsin palmitylation Biochemistry 48 2009 4294 4304
44. P.L. Frederix, P.D. Bosshart, and A. Engel Atomic force microscopy of biological membranes Biophys. J. 96 2009 329 338
45. H.G. Hansma, and J.H. Hoh Biomolecular imaging with the atomic force microscope Annu. Rev. Biophys. Biomol. Struct. 23 1994 115 139
46. M.J. Allen, N.V. Hud, M. Balooch, R.J. Tench, W.J. Siekhaus, and R. Balhorn Tip-radius-induced artifacts in AFM images of protamine-complexed DNA fibers Ultramicroscopy 42-44 1992 1095 1100
47. S.W. Chen, M. Odorico, M. Meillan, L. Vellutini, J.M. Teulon, P. Parot, B. Bennetau, and J.L. Pellequer Nanoscale structural features determined by AFM for single virus particles Nanoscale 5 2013 10877 10886
48. K.T. Sapra, P.S. Park, S. Filipek, A. Engel, D.J. Muller, and K. Palczewski Detecting molecular interactions that stabilize native bovine rhodopsin J. Mol. Biol. 358 2006 255 269
49. D.C. Teller, T. Okada, C.A. Behnke, K. Palczewski, and R.E. Stenkamp 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
50. R.S. Molday, D. Hicks, and L. Molday Peripherin. A rim-specific membrane protein of rod outer segment discs Invest. Ophthalmol. Vis. Sci. 28 1987 50 61
51. C.L. Makino, X.H. Wen, N.A. Michaud, H.I. Covington, E. DiBenedetto, H.E. Hamm, J. Lem, and G. Caruso Rhodopsin expression level affects rod outer segment morphology and photoresponse kinetics PLoS One 7 2012 e37832
52. X.H. Wen, L. Shen, R.S. Brush, N. Michaud, M.R. Al-Ubaidi, V.V. Gurevich, H.E. Hamm, J. Lem, E. Dibenedetto, R.E. Anderson, and C.L. Makino Overexpression of rhodopsin alters the structure and photoresponse of rod photoreceptors Biophys. J. 96 2009 939 950
53. M. Haeri, P.D. Calvert, E. Solessio, E.N. Pugh Jr., and B.E. Knox Regulation of rhodopsin-eGFP distribution in transgenic xenopus rod outer segments by light PLoS One 8 2013 e80059
54. J.G. Hollyfield, M.E. Rayborn, G.E. Verner, M.B. Maude, and R.E. Anderson Membrane addition to rod photoreceptor outer segments: light stimulates membrane assembly in the absence of increased membrane biosynthesis Invest. Ophthalmol. Vis. Sci. 22 1982 417 427
55. M.J. Saxton, and J.C. Owicki Concentration effects on reactions in membranes: rhodopsin and transducin Biochim. Biophys. Acta 979 1989 27 34
56. S. Mondal, J.M. Johnston, H. Wang, G. Khelashvili, M. Filizola, and H. Weinstein Membrane driven spatial organization of GPCRs Sci. Rep. 3 2013 2909
57. X. Periole, T. Huber, S.J. Marrink, and T.P. Sakmar G protein-coupled receptors self-assemble in dynamics simulations of model bilayers J. Am. Chem. Soc. 129 2007 10126 10132
58. O. Soubias, S.L. Niu, D.C. Mitchell, and K. Gawrisch Lipid-rhodopsin hydrophobic mismatch alters rhodopsin helical content J. Am. Chem. Soc. 130 2008 12465 12471
59. O. Soubias, W.E. Teague, and K. Gawrisch Evidence for specificity in lipid-rhodopsin interactions J. Biol. Chem. 281 2006 33233 33241
60. S.L. Niu, D.C. Mitchell, and B.J. Litman Manipulation of cholesterol levels in rod disk membranes by methyl-beta-cyclodextrin: effects on receptor activation J. Biol. Chem. 277 2002 20139 20145
61. S.L. Niu, D.C. Mitchell, S.Y. Lim, Z.M. Wen, H.Y. Kim, N. Salem Jr., and B.J. Litman Reduced G protein-coupled signaling efficiency in retinal rod outer segments in response to n- 3 fatty acid deficiency J. Biol. Chem. 279 2004 31098 31104
62. A.V. Botelho, T. Huber, T.P. Sakmar, and M.F. Brown Curvature and hydrophobic forces drive oligomerization and modulate activity of rhodopsin in membranes Biophys. J. 91 2006 4464 4477
63. Y. Wang, A.V. Botelho, G.V. Martinez, and M.F. Brown Electrostatic properties of membrane lipids coupled to metarhodopsin II formation in visual transduction J. Am. Chem. Soc. 124 2002 7690 7701
64. A.D. Albert, J.E. Young, and Z. Paw Phospholipid fatty acyl spatial distribution in bovine rod outer segment disk membranes Biochim. Biophys. Acta 1368 1998 52 60
65. K. Boesze-Battaglia, S.J. Fliesler, and A.D. Albert Relationship of cholesterol content to spatial distribution and age of disc membranes in retinal rod outer segments J. Biol. Chem. 265 1990 18867 18870
66. R.B. Caldwell, and B.J. McLaughlin Freeze-fracture study of filipin binding in photoreceptor outer segments and pigment epithelium of dystrophic and normal retinas J. Comp. Neurol. 236 1985 523 537
67. L.D. Andrews, and A.I. Cohen Freeze-fracture evidence for the presence of cholesterol in particle-free patches of basal disks and the plasma membrane of retinal rod outer segments of mice and frogs J. Cell Biol. 81 1979 215 228
68. P.A. Liebman, and G. Entine Lateral diffusion of visual pigment in photoreceptor disk membranes Science 185 1974 457 459
69. R.A. Cone Rotational diffusion of rhodopsin in the visual receptor membrane Nat. New Biol. 236 1972 39 43
70. M. Poo, and R.A. Cone Lateral diffusion of rhodopsin in the photoreceptor membrane Nature 247 1974 438 441
71. M.M. Poo, and R.A. Cone Lateral diffusion of phodopsin in Necturus rods Exp. Eye Res. 17 1973 503 510
72. M. Chabre, R. Cone, and H. Saibil Biophysics: is rhodopsin dimeric in native retinal rods? Nature 426 2003 30 31
73. P.G. Saffman, and M. Delbruck Brownian motion in biological membranes Proc. Natl. Acad. Sci. U. S. A. 72 1975 3111 3113
74. C.L. Wey, R.A. Cone, and M.A. Edidin Lateral diffusion of rhodopsin in photoreceptor cells measured by fluorescence photobleaching and recovery Biophys. J. 33 1981 225 232
75. Q. Wang, X. Zhang, L. Zhang, F. He, G. Zhang, M. Jamrich, and T.G. Wensel Activation-dependent hindrance of photoreceptor G protein diffusion by lipid microdomains J. Biol. Chem. 283 2008 30015 30024
76. B.D. Gupta, and T.P. Williams Lateral diffusion of visual pigments in toad (Bufo marinus) rods and in catfish (Ictalurus punctatus) cones J. Physiol. 430 1990 483 496
77. R.E. Drzymala, H.L. Weiner, C.A. Dearry, and P.A. Liebman A barrier to lateral diffusion of porphyropsin in Necturus rod outer segment disks Biophys. J. 45 1984 683 692
78. V.I. Govardovskii, D.A. Korenyak, S.A. Shukolyukov, and L.V. Zueva Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal Mol. Vis. 15 2009 1717 1729
79. M. Najafi, M. Haeri, B.E. Knox, W.E. Schiesser, and P.D. Calvert Impact of signaling microcompartment geometry on GPCR dynamics in live retinal photoreceptors J. Gen. Physiol. 140 2012 249 266
80. M.H. Elliott, Z.A. Nash, N. Takemori, S.J. Fliesler, M.E. McClellan, and M.I. Naash Differential distribution of proteins and lipids in detergent-resistant and detergent-soluble domains in rod outer segment plasma membranes and disks J. Neurochem. 104 2008 336 352
81. P. Cicuta, S.L. Keller, and S.L. Veatch Diffusion of liquid domains in lipid bilayer membranes J. Phys. Chem. B 111 2007 3328 3331
82. D. Dell'Orco A physiological role for the supramolecular organization of rhodopsin and transducin in rod photoreceptors FEBS Lett. 587 2013 2060 2066
83. E.N. Pugh Jr., and T.D. Lamb Amplification and kinetics of the activation steps in phototransduction Biochim. Biophys. Acta 1141 1993 111 149
84. D. Dell'Orco, and H. Schmidt Mesoscopic Monte Carlo simulations of stochastic encounters between photoactivated rhodopsin and transducin in disc membranes J. Phys. Chem. B 112 2008 4419 4426
85. J. Schoneberg, M. Heck, K.P. Hofmann, and F. Noe Explicit spatiotemporal simulation of receptor-G protein coupling in rod cell disk membranes Biophys. J. 107 2014 1042 1053
86. D. Dell'Orco, and K.W. Koch A dynamic scaffolding mechanism for rhodopsin and transducin interaction in vertebrate vision Biochem. J. 440 2011 263 271
87. M. Haeri, and B.E. Knox Rhodopsin mutant P23H destabilizes rod photoreceptor disk membranes PLoS One 7 2012 e30101
88. N. Zhang, A.V. Kolesnikov, B. Jastrzebska, D. Mustafi, O. Sawada, T. Maeda, C. Genoud, A. Engel, V.J. Kefalov, and K. Palczewski Autosomal recessive retinitis pigmentosa E150K opsin mice exhibit photoreceptor disorganization J. Clin. Invest. 123 2013 121 137
89. A. Ianoul, D.D. Grant, Y. Rouleau, M. Bani-Yaghoub, L.J. Johnston, and J.P. Pezacki Imaging nanometer domains of beta-adrenergic receptor complexes on the surface of cardiac myocytes Nat. Chem. Biol. 1 2005 196 202