Rhodopsin forms nanodomains in rod outer segment disc membranes of the cold-blooded Xenopus laevis

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Rakshit, Tatini ^a   Senapati, Subhadip ^a   Sinha, Satyabrata ^a   Whited, A M ^a   Park, Paul S H ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; RHODOPSIN; NANOMATERIAL;

ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; MOUSE; NONHUMAN; PHASE SEPARATION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PURIFICATION; RETINA ROD OUTER SEGMENT; XENOPUS LAEVIS; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CELL MEMBRANE; CHEMISTRY; COLD; COMPARATIVE STUDY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; RETINAL ROD OUTER SEGMENT;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; COLD TEMPERATURE; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NANOSTRUCTURES; RHODOPSIN; ROD CELL OUTER SEGMENT; XENOPUS LAEVIS;

EID: 84950108669     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141114     Document Type: Article

References (41)

1. Baylor DA, Lamb TD, Yau KW. Responses of retinal rods to single photons. J Physiol. 1979; 288:613-34. PMID: 112243.
2. Kirchhoff H. Diffusion of molecules and macromolecules in thylakoid membranes. Biochim Biophys Acta. 2014; 1837(4):495-502. doi: 10.1016/j.bbabio.2013.11.003 PMID: 24246635.
3. Dell'Orco D. A physiological role for the supramolecular organization of rhodopsin and transducin in rod photoreceptors. FEBS Lett. 2013; 587(13):2060-6. doi: 10.1016/j.febslet.2013.05.017 PMID: 23684654.
4. Gunkel M, Schoneberg J, Alkhaldi W, Irsen S, Noe F, Kaupp UB, et al. Higher-order architecture of rhodopsin in intact photoreceptors and its implication for phototransduction kinetics. Structure. 2015; 23 (4):628-38. doi: 10.1016/j.str.2015.01.015 PMID: 25728926.
5. Whited AM, Park PS. Atomic force microscopy: a multifaceted tool to study membrane proteins and their interactions with ligands. Biochim Biophys Acta. 2014; 1838(1 Pt A):56-68. Epub 2013/04/23. doi: S0005-2736(13)00123-5 [pii] doi: 10.1016/j.bbamem.2013.04.011 PMID: 23603221; PubMed Central PMCID: PMC3779510.
6. Muller DJ. AFM: a nanotool in membrane biology. Biochemistry. 2008; 47(31):7986-98. Epub 2008/07/12. doi: 10.1021/bi800753x PMID: 18616288.
7. Engel A, Gaub HE. Structure and mechanics of membrane proteins. Annu Rev Biochem. 2008; 77:127-48. Epub 2008/06/04. doi: 10.1146/annurev.biochem.77.062706.154450 PMID: 18518819.
8. Liang Y, Fotiadis D, Filipek S, Saperstein DA, Palczewski K, Engel A. Organization of the G proteincoupled receptors rhodopsin and opsin in native membranes. J Biol Chem. 2003; 278(24):21655-62. PMID: 12663652
9. Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A, Palczewski K. Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature. 2003; 421(6919):127-8. PMID: 12520290.
10. Sapra KT, Park PS, Filipek S, Engel A, Muller DJ, Palczewski K. Detecting molecular interactions that stabilize native bovine rhodopsin. J Mol Biol. 2006; 358(1):255-69. PMID: 16519899.
11. Buzhynskyy N, Salesse C, Scheuring S. Rhodopsin is spatially heterogeneously distributed in rod outer segment disk membranes. J Mol Recognit. 2011; 24(3):483-9. Epub 2011/04/20. doi: 10.1002/jmr.1086 PMID: 21504027.
12. Chabre M, Cone R, Saibil H. Biophysics: is rhodopsin dimeric in native retinal rods? Nature. 2003; 426 (6962):30-1. PMID: 14603306.
13. Heck M, Hofmann KP. Maximal rate and nucleotide dependence of rhodopsin-catalyzed transducin activation: initial rate analysis based on a double displacement mechanism. J Biol Chem. 2001; 276 (13):10000-9. doi: 10.1074/jbc.M009475200 PMID: 11116153.
14. Fung BK-K, Stryer L. Photolyzed rhodopsin catalyzes the exchange of GTP for bound GDP in retinal rod outer segments. ProcNatlAcadSciUSA. 1980; 77(5):2500-4.
15. Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A, Palczewski K. The G protein-coupled receptor rhodopsin in the native membrane. FEBS Lett. 2004; 564(3):281-8. PMID: 15111110.
16. Liang Y, Fotiadis D, Maeda T, Maeda A, Modzelewska A, Filipek S, et al. Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice. J Biol Chem. 2004; 279(46):48189-96. PMID: 15337746.
17. Molday RS, Hicks D, Molday L. Peripherin. A rim-specific membrane protein of rod outer segment discs. Invest Ophthalmol Vis Sci. 1987; 28(1):50-61. PMID: 2433249.
18. Whited AM, Park PS. Nanodomain organization of rhodopsin in native human and murine rod outer segment disc membranes. Biochim Biophys Acta. 2015; 1848(1PA):26-34. doi: 10.1016/j.bbamem.2014.10.007 PMID: 25305340.
19. Rakshit T, Park PS. Impact of reduced rhodopsin expression on the structure of rod outer segment disc membranes. Biochemistry. 2015; 54(18):2885-94. doi: 10.1021/acs.biochem.5b00003 PMID: 25881629; PubMed Central PMCID: PMC4430375.
20. Chabre M. X-ray diffraction studies of retinal rods. I. Structure of the disc membrane, effect of illumination. BiochimBiophysActa. 1975; 382(3):322-35. PMID: 1079141.
21. Tam BM, Moritz OL, Hurd LB, Papermaster DS. Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis. J Cell Biol. 2000; 151(7):1369-80. Epub 2001/01/03. PMID: 11134067; PubMed Central PMCID: PMC2150681.
22. Tam BM, Moritz OL. Characterization of rhodopsin P23H-induced retinal degeneration in a Xenopus laevis model of retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2006; 47(8):3234-41. doi: 10.1167/ iovs.06-0213 PMID: 16877386.
23. Jin S, Cornwall MC, Oprian DD. Opsin activation as a cause of congenital night blindness. Nat Neurosci. 2003; 6(7):731-5. Epub 2003/06/05. doi: 10.1038/nn1070 nn1070 [pii]. PMID: 12778053.
24. Mazelova J, Astuto-Gribble L, Inoue H, Tam BM, Schonteich E, Prekeris R, et al. Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J. 2009; 28(3):183-92. Epub 2009/ 01/21. doi: emboj2008267 [pii] doi: 10.1038/emboj.2008.267 PMID: 19153612; PubMed Central PMCID: PMC2637330.
25. Najafi M, Haeri M, Knox BE, Schiesser WE, Calvert PD. Impact of signaling microcompartment geometry on GPCR dynamics in live retinal photoreceptors. J Gen Physiol. 2012; 140(3):249-66. doi: 10.1085/jgp.201210818 PMID: 22891277; PubMed Central PMCID: PMC3434098.
26. Haeri M, Knox BE. Rhodopsin mutant P23H destabilizes rod photoreceptor disk membranes. PLoS One. 2012; 7(1):e30101. doi: 10.1371/journal.pone.0030101 PMID: 22276148; PubMed Central PMCID: PMC3261860.
27. Lodowski KH, Lee R, Ropelewski P, Nemet I, Tian G, Imanishi Y. Signals governing the trafficking and mistrafficking of a ciliary GPCR, rhodopsin. J Neurosci. 2013; 33(34):13621-38. doi: 10.1523/ JNEUROSCI.1520-13.2013 PMID: 23966685; PubMed Central PMCID: PMC3755712.
28. Park PS, Muller DJ. Dynamic single-molecule force spectroscopy of rhodopsin in native membranes. Methods Mol Biol. 2015; 1271:173-85. doi: 10.1007/978-1-4939-2330-4-12 PMID: 25697524.
29. Bownds D, Brodie AE. Light-sensitive swelling of isolated frog rod outer segments as an in vitro assay for visual transduction and dark adaptation. J Gen Physiol. 1975; 66(4):407-25. PMID: 52687; PubMed Central PMCID: PMC2226212.
30. Rosenkranz J. New aspects of the ultrastructure of frog rod outer segments. Int Rev Cytol. 1977; 50:25-158. PMID: 332656.
31. Korenbrot JI, Cone RA. Dark ionic flux and the effects of light in isolated rod outer segments. J Gen Physiol. 1972; 60(1):20-45. PMID: 4537779; PubMed Central PMCID: PMC2226056.
32. Nilsson SE. The Ultrastructure of the Receptor Outer Segments in the Retina of the Leopard Frog (Rana Pipiens). J Ultrastruct Res. 1965; 12:207-31. PMID: 14289429.
33. Liebman PA, Entine G. Visual pigments of frog and tadpole (Rana pipiens). Vision Res. 1968; 8 (7):761-75. PMID: 5664012.
34. Papermaster DS, Dreyer WJ. Rhodopsin content in the outer segment membranes of bovine and frog retinal rods. Biochemistry. 1974; 13(11):2438-44. Epub 1974/05/21. PMID: 4545509.
35. Hamm HE, Bownds MD. Protein complement of rod outer segments of frog retina. Biochemistry. 1986; 25(16):4512-23. PMID: 3021191
36. Tsukamoto Y. The number, depth and elongation of disc incisures in the retinal rod of Rana catesbeiana. Exp Eye Res. 1987; 45(1):105-16. PMID: 3498638.
37. Papermaster DS, Schneider BG, Zorn MA, Kraehenbuhl JP. Immunocytochemical localization of a large intrinsic membrane protein to the incisures and margins of frog rod outer segment disks. J Cell Biol. 1978; 78(2):415-25. Epub 1978/08/01. PMID: 690173; PubMed Central PMCID: PMC2110123.
38. Teller DC, Okada T, Behnke CA, Palczewski K, Stenkamp RE. Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G-protein-coupled receptors (GPCRs). Biochemistry. 2001; 40(26):7761-72. PMID: 11425302.
39. Kawamura S, Colozo AT, Muller DJ, Park PS. Conservation of molecular interactions stabilizing bovine and mouse rhodopsin. Biochemistry. 2010; 49(49):10412-20. Epub 2010/11/03. doi: 10.1021/ bi101345x PMID: 21038881; PubMed Central PMCID: PMC2999666.
40. Lamba OP, Borchman D, O'Brien PJ. Fourier transform infrared study of the rod outer segment disk and plasma membranes of vertebrate retina. Biochemistry. 1994; 33(7):1704-12. PMID: 8110772.
41. Nickell S, Park PS, Baumeister W, Palczewski K. Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography. J Cell Biol. 2007; 177(5):917-25. PMID: 17535966.