Phospholipid scrambling by rhodopsin

Photochemical and Photobiological Sciences

Volumn 14, Issue 11, 2015, Pages 1922-1931

  Ernst, Oliver P ^a   Menon, Anant K ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOLIPID; RHODOPSIN;

ANIMAL; HUMAN; METABOLISM;

ANIMALS; HUMANS; PHOSPHOLIPIDS; RHODOPSIN;

EID: 84946599896     PISSN: 1474905X     EISSN: 14749092     Source Type: Journal    
DOI: 10.1039/c5pp00195a     Document Type: Article

References (82)

1. F. Quazi S. Lenevich R. S. Molday ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer Nat. Commun. 2012 3 925
2. J. A. Coleman M. C. Kwok R. S. Molday Localization, purification, and functional reconstitution of the P4-ATPase Atp8a2, a phosphatidylserine flippase in photoreceptor disc membranes J. Biol. Chem. 2009 284 32670 32679
3. G. Wu W. L. Hubbell Phospholipid asymmetry and transmembrane diffusion in photoreceptor disc membranes Biochemistry 1993 32 879 888
4. E. Hessel A. Herrmann P. Muller P. P. Schnetkamp K. P. Hofmann The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium evidence for rapid flip and flop movement Eur. J. Biochem. 2000 267 1473 1483
5. E. Hessel P. Muller A. Herrmann K. P. Hofmann Light-induced reorganization of phospholipids in rod disc membranes J. Biol. Chem. 2001 276 2538 2543
6. I. Menon T. Huber S. Sanyal S. Banerjee P. Barre S. Canis J. D. Warren J. Hwa T. P. Sakmar A. K. Menon Opsin is a phospholipid flippase Curr. Biol. 2011 21 149 153
7. M. A. Goren T. Morizumi I. Menon J. S. Joseph J. S. Dittman V. Cherezov R. C. Stevens O. P. Ernst A. K. Menon Constitutive phospholipid scramblase activity of a G protein-coupled receptor Nat. Commun. 2014 5 5115
8. O. P. Ernst D. T. Lodowski M. Elstner P. Hegemann L. S. Brown H. Kandori Microbial and animal rhodopsins: structures, functions, and molecular mechanisms Chem. Rev. 2014 114 126 163
9. S. Sanyal A. K. Menon Flipping lipids: why an' what's the reason for? ACS Chem. Biol. 2009 4 895 909
10. E. M. Bevers P. L. Williamson Phospholipid scramblase: an update FEBS Lett. 2010 584 2724 2730
11. P. A. Leventis S. Grinstein The distribution and function of phosphatidylserine in cellular membranes Annu. Rev. Biophys. 2010 39 407 427
12. T. Mohammadi V. van Dam R. Sijbrandi T. Vernet A. Zapun A. Bouhss M. Diepeveen-de Bruin M. Nguyen-Disteche B. de Kruijff E. Breukink Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane EMBO J. 2011 30 1425 1432
13. J. Helenius D. T. Ng C. L. Marolda P. Walter M. A. Valvano M. Aebi Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein Nature 2002 415 447 450
14. P. D. Rick K. Barr K. Sankaran J. Kajimura J. S. Rush C. J. Waechter Evidence that the wzxE gene of Escherichia coli K-12 encodes a protein involved in the transbilayer movement of a trisaccharide-lipid intermediate in the assembly of enterobacterial common antigen J. Biol. Chem. 2003 278 16534 16542
15. F. Basse J. G. Stout P. J. Sims T. Wiedmer Isolation of an erythrocyte membrane protein that mediates Ca2+-dependent transbilayer movement of phospholipid J. Biol. Chem. 1996 271 17205 17210
16. C. M. Ernst A. Peschel Broad-spectrum antimicrobial peptide resistance by MprF-mediated aminoacylation and flipping of phospholipids Mol. Microbiol. 2011 80 290 299
17. L. T. Sham E. K. Butler M. D. Lebar D. Kahne T. G. Bernhardt N. Ruiz Bacterial cell wall. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis Science 2014 345 220 222
18. J. Suzuki M. Umeda P. J. Sims S. Nagata Calcium-dependent phospholipid scrambling by TMEM16F Nature 2010 468 834 838
19. A. Picollo M. Malvezzi A. Accardi TMEM16 proteins: unknown structure and confusing functions J. Mol. Biol. 2015 427 94 105
20. M. Malvezzi M. Chalat R. Janjusevic A. Picollo H. Terashima A. K. Menon A. Accardi Ca2+-dependent phospholipid scrambling by a reconstituted TMEM16 ion channel Nat. Commun. 2013 4 2367
21. J. D. Brunner N. K. Lim S. Schenck A. Duerst R. Dutzler X-ray structure of a calcium-activated TMEM16 lipid scramblase Nature 2014 516 207 212
22. R. D. Kornberg H. M. McConnell Inside-outside transitions of phospholipids in vesicle membranes Biochemistry 1971 10 1111 1120
23. M. Nakano M. Fukuda T. Kudo H. Endo T. Handa Determination of interbilayer and transbilayer lipid transfers by time-resolved small-angle neutron scattering Phys. Rev. Lett. 2007 98 238101
24. M. Chalat I. Menon Z. Turan A. K. Menon Reconstitution of glucosylceramide flip-flop across endoplasmic reticulum: implications for mechanism of glycosphingolipid biosynthesis J. Biol. Chem. 2012 287 15523 15532
25. W. L. Hubbell Transbilayer coupling mechanism for the formation of lipid asymmetry in biological membranes. Application to the photoreceptor disc membrane Biophys. J. 1990 57 99 108
26. X. Zhou T. T. Sebastian T. R. Graham Auto-inhibition of Drs2p, a yeast phospholipid flippase, by its carboxyl-terminal tail J. Biol. Chem. 2013 288 31807 31815
27. F. M. Roelants A. G. Baltz A. E. Trott S. Fereres J. Thorner A protein kinase network regulates the function of aminophospholipid flippases Proc. Natl. Acad. Sci. U. S. A. 2010 107 34 39
28. S. Lee Y. Uchida J. Wang T. Matsudaira T. Nakagawa T. Kishimoto K. Mukai T. Inaba T. Kobayashi R. S. Molday T. Taguchi H. Arai Transport through recycling endosomes requires EHD1 recruitment by a phosphatidylserine translocase EMBO J. 2015 34 669 688
29. J. A. Coleman X. Zhu H. R. Djajadi L. L. Molday R. S. Smith R. T. Libby S. W. John R. S. Molday Phospholipid flippase ATP8A2 is required for normal visual and auditory function and photoreceptor and spiral ganglion cell survival J. Cell Sci. 2014 127 1138 1149
30. Q. L. Chang S. N. Gummadi A. K. Menon Chemical modification identifies two populations of glycerophospholipid flippase in rat liver ER Biochemistry 2004 43 10710 10718
31. R. A. Vishwakarma S. Vehring A. Mehta A. Sinha T. Pomorski A. Herrmann A. K. Menon New fluorescent probes reveal that flippase-mediated flip-flop of phosphatidylinositol across the endoplasmic reticulum membrane does not depend on the stereochemistry of the lipid Org. Biomol. Chem. 2005 3 1275 1283
32. S. Y. Lee J. A. Letts R. MacKinnon Functional reconstitution of purified human Hv1 H+ channels J. Mol. Biol. 2009 387 1055 1060
33. G. D. Eytan Use of liposomes for reconstitution of biological functions Biochim. Biophys. Acta 1982 694 185 202
34. A. F. Goldberg C. Miller Solubilization and functional reconstitution of a chloride channel from Torpedo californica electroplax J. Membr. Biol. 1991 124 199 206
35. L. Heginbotham L. Kolmakova-Partensky C. Miller Functional reconstitution of a prokaryotic K+ channel J. Gen. Physiol. 1998 111 741 749
36. F. J. Sharom Flipping and flopping-lipids on the move IUBMB Life 2011 63 736 746
37. S. Shukla V. Rai P. Saini D. Banerjee A. K. Menon R. Prasad Candida drug resistance protein 1, a major multidrug ATP binding cassette transporter of Candida albicans, translocates fluorescent phospholipids in a reconstituted system Biochemistry 2007 46 12081 12090
38. F. Quazi R. S. Molday Differential phospholipid substrates and directional transport by ATP-binding cassette proteins ABCA1, ABCA7, and ABCA4 and disease-causing mutants J. Biol. Chem. 2013 288 34414 34426
39. S. Sanyal A. K. Menon Specific transbilayer translocation of dolichol-linked oligosaccharides by an endoplasmic reticulum flippase Proc. Natl. Acad. Sci. U. S. A. 2009 106 767 772
40. S. Sanyal A. K. Menon Stereoselective transbilayer translocation of mannosyl phosphoryl dolichol by an endoplasmic reticulum flippase Proc. Natl. Acad. Sci. U. S. A. 2010 107 11289 11294
41. K. Henzler-Wildman D. Kern Dynamic personalities of proteins Nature 2007 450 964 972
42. J. Lubelski W. N. Konings A. J. Driessen Distribution and physiology of ABC-type transporters contributing to multidrug resistance in bacteria Microbiol. Mol. Biol. Rev. 2007 71 463 476
43. A. J. Venkatakrishnan X. Deupi G. Lebon C. G. Tate G. F. Schertler M. M. Babu Molecular signatures of G-protein-coupled receptors Nature 2013 494 185 194
44. M. A. Kol A. N. van Laak D. T. Rijkers J. A. Killian A. I. de Kroon B. de Kruijff Phospholipid flop induced by transmembrane peptides in model membranes is modulated by lipid composition Biochemistry 2003 42 231 237
45. M. A. Kol A. I. de Kroon J. A. Killian B. de Kruijff Transbilayer movement of phospholipids in biogenic membranes Biochemistry 2004 43 2673 2681
46. M. Langer R. Sah A. Veser M. Gutlich D. Langosch Structural properties of model phosphatidylcholine flippases Chem. Biol. 2013 20 63 72
47. D. Fotiadis Y. Liang S. Filipek D. A. Saperstein A. Engel K. Palczewski The G protein-coupled receptor rhodopsin in the native membrane FEBS Lett. 2004 564 281 288
48. M. Gunkel J. Schoneberg W. Alkhaldi S. Irsen F. Noe U. B. Kaupp A. Al-Amoudi Higher-order architecture of rhodopsin in intact photoreceptors and its implication for phototransduction kinetics Structure 2015 23 628 638
49. G. F. Schertler Rhodopsin on tracks: new ways to go in signaling Structure 2015 23 606 608
50. D. Dell'Orco A physiological role for the supramolecular organization of rhodopsin and transducin in rod photoreceptors FEBS Lett. 2013 587 2060 2066
51. L. Ruggiero M. P. Connor J. Chen R. Langen S. C. Finnemann Diurnal, localized exposure of phosphatidylserine by rod outer segment tips in wild-type but not Itgb5-/- or Mfge8-/- mouse retina Proc. Natl. Acad. Sci. U. S. A. 2012 109 8145 8148
52. J. C. Holthuis A. K. Menon Lipid landscapes and pipelines in membrane homeostasis Nature 2014 510 48 57
53. A. Grossfield S. E. Feller M. C. Pitman A role for direct interactions in the modulation of rhodopsin by omega-3 polyunsaturated lipids Proc. Natl. Acad. Sci. U. S. A. 2006 103 4888 4893
54. K. Boesze-Battaglia A. D. Albert Cholesterol modulation of photoreceptor function in bovine retinal rod outer segments J. Biol. Chem. 1990 265 20727 20730
55. D. C. Mitchell S. L. Niu B. J. Litman Enhancement of G protein-coupled signaling by DHA phospholipids Lipids 2003 38 437 443
56. S. L. Niu D. C. Mitchell B. J. Litman Manipulation of cholesterol levels in rod disk membranes by methyl-beta-cyclodextrin: effects on receptor activation J. Biol. Chem. 2002 277 20139 20145
57. A. D. Albert K. Boesze-Battaglia The role of cholesterol in rod outer segment membranes Prog. Lipid Res. 2005 44 99 124
58. K. Boesze-Battaglia S. J. Fliesler A. D. Albert Relationship of cholesterol content to spatial distribution and age of disc membranes in retinal rod outer segments J. Biol. Chem. 1990 265 18867 18870
59. B. Jastrzebska A. Debinski S. Filipek K. Palczewski Role of membrane integrity on G protein-coupled receptors: Rhodopsin stability and function Prog. Lipid Res. 2011 50 267 277
60. K. Arikawa L. L. Molday R. S. Molday D. S. Williams Localization of peripherin/rds in the disk membranes of cone and rod photoreceptors: relationship to disk membrane morphogenesis and retinal degeneration J. Cell Biol. 1992 116 659 667
61. A. D. Albert J. E. Young Z. Paw Phospholipid fatty acyl spatial distribution in bovine rod outer segment disk membranes Biochim. Biophys. Acta 1998 1368 52 60
62. S. E. Feller K. Gawrisch Properties of docosahexaenoic-acid-containing lipids and their influence on the function of rhodopsin Curr. Opin. Struct. Biol. 2005 15 416 422
63. V. T. Armstrong M. R. Brzustowicz S. R. Wassall L. J. Jenski W. Stillwell Rapid flip-flop in polyunsaturated (docosahexaenoate) phospholipid membranes Arch. Biochem. Biophys. 2003 414 74 82
64. O. Soubias W. E. Teague K. Gawrisch Evidence for specificity in lipid-rhodopsin interactions J. Biol. Chem. 2006 281 33233 33241
65. N. Pedemonte L. J. Galietta Structure and function of TMEM16 proteins (anoctamins) Physiol. Rev. 2014 94 419 459
66. S. Resnikoff D. Pascolini D. Etya'ale I. Kocur R. Pararajasegaram G. P. Pokharel S. P. Mariotti Global data on visual impairment in the year 2002 Bull. World Health Organ. 2004 82 844 851
67. D. S. Friedman B. J. O'Colmain B. Munoz S. C. Tomany C. McCarty P. T. de Jong B. Nemesure P. Mitchell J. Kempen The Eye Diseases Prevalence Research Group, Prevalence of age-related macular degeneration in the United States Arch. Ophthalmol. 2004 122 564 572
68. P. T. de Jong Age-related macular degeneration N. Engl. J. Med. 2006 355 1474 1485
69. K. Palczewski Chemistry and biology of vision J. Biol. Chem. 2012 287 1612 1619
70. J. R. Sparrow N. Fishkin J. Zhou B. Cai Y. P. Jang S. Krane Y. Itagaki K. Nakanishi A2E, a byproduct of the visual cycle Vision Res. 2003 43 2983 2990
71. P. D. Kiser M. Golczak K. Palczewski Chemistry of the retinoid (visual) cycle Chem. Rev. 2014 114 194 232
72. C. A. Parish M. Hashimoto K. Nakanishi J. Dillon J. Sparrow Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium Proc. Natl. Acad. Sci. U. S. A. 1998 95 14609 14613
73. N. L. Mata J. Weng G. H. Travis Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular degeneration Proc. Natl. Acad. Sci. U. S. A. 2000 97 7154 7159
74. J. R. Sparrow Y. Wu C. Y. Kim J. Zhou Phospholipid meets all-trans-retinal: the making of RPE bisretinoids J. Lipid Res. 2010 51 247 261
75. N. P. Boyer D. Higbee M. B. Currin L. R. Blakeley C. Chen Z. Ablonczy R. K. Crouch Y. Koutalos Lipofuscin and N-retinylidene-N-retinylethanolamine (A2E) accumulate in retinal pigment epithelium in absence of light exposure: their origin is 11-cis-retinal J. Biol. Chem. 2012 287 22276 22286
76. F. Quazi R. S. Molday ATP-binding cassette transporter ABCA4 and chemical isomerization protect photoreceptor cells from the toxic accumulation of excess 11-cis-retinal Proc. Natl. Acad. Sci. U. S. A. 2014 111 5024 5029
77. M. P. Sheetz S. J. Singer Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions Proc. Natl. Acad. Sci. U. S. A. 1974 71 4457 4461
78. J. C. Saari Vitamin A metabolism in rod and cone visual cycles Annu. Rev. Nutr. 2012 32 125 145
79. H. Sun Membrane receptors and transporters involved in the function and transport of vitamin A and its derivatives Biochim. Biophys. Acta 2012 1821 99 112
80. A. K. Menon W. E. 3rd Watkins S. Hrafnsdottir Specific proteins are required to translocate phosphatidylcholine bidirectionally across the endoplasmic reticulum Curr. Biol. 2000 10 241 252
81. T. Mohammadi R. Sijbrandi M. Lutters J. Verheul N. I. Martin T. den Blaauwen B. de Kruijff E. Breukink Specificity of the transport of lipid II by FtsW in Escherichia coli J. Biol. Chem. 2014 289 14707 14718
82. T. Pomorski A. K. Menon Lipid flippases and their biological functions Cell. Mol. Life Sci. 2006 63 2908 2921