Structural aspects of rod opsin and their implication in genetic diseases.
Conformational diseases
GPCRs
Molecular simulations
Protein structure networks
Rhodopsin
Journal
Pflugers Archiv : European journal of physiology
ISSN: 1432-2013
Titre abrégé: Pflugers Arch
Pays: Germany
ID NLM: 0154720
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
received:
03
01
2021
accepted:
22
02
2021
revised:
17
02
2021
pubmed:
18
3
2021
medline:
24
2
2022
entrez:
17
3
2021
Statut:
ppublish
Résumé
Vision in dim-light conditions is triggered by photoactivation of rhodopsin, the visual pigment of rod photoreceptor cells. Rhodopsin is made of a protein, the G protein coupled receptor (GPCR) opsin, and the chromophore 11-cis-retinal. Vertebrate rod opsin is the GPCR best characterized at the atomic level of detail. Since the release of the first crystal structure 20 years ago, a huge number of structures have been released that, in combination with valuable spectroscopic determinations, unveiled most aspects of the photobleaching process. A number of spontaneous mutations of rod opsin have been found linked to vision-impairing diseases like autosomal dominant or autosomal recessive retinitis pigmentosa (adRP or arRP, respectively) and autosomal congenital stationary night blindness (adCSNB). While adCSNB is mainly caused by constitutive activation of rod opsin, RP shows more variegate determinants affecting different aspects of rod opsin function. The vast majority of missense rod opsin mutations affects folding and trafficking and is linked to adRP, an incurable disease that awaits light on its molecular structure determinants. This review article summarizes all major structural information available on vertebrate rod opsin conformational states and the insights gained so far into the structural determinants of adCSNB and adRP linked to rod opsin mutations. Strategies to design small chaperones with therapeutic potential for selected adRP rod opsin mutants will be discussed as well.
Identifiants
pubmed: 33728518
doi: 10.1007/s00424-021-02546-x
pii: 10.1007/s00424-021-02546-x
doi:
Substances chimiques
Rhodopsin
9009-81-8
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1339-1359Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Aguila M, Bevilacqua D, McCulley C, Schwarz N, Athanasiou D, Kanuga N, Novoselov SS, Lange CA, Ali RR, Bainbridge JW, Gias C, Coffey PJ, Garriga P, Cheetham ME (2014) Hsp90 inhibition protects against inherited retinal degeneration. Hum Mol Genet 23:2164–2175. https://doi.org/10.1093/hmg/ddt613
doi: 10.1093/hmg/ddt613
pubmed: 24301679
pmcid: 24301679
Andres A, Garriga P, Manyosa J (2003) Altered functionality in rhodopsin point mutants associated with retinitis pigmentosa. Biochem Biophys Res Commun 303:294–301
pubmed: 12646201
doi: 10.1016/S0006-291X(03)00328-0
pmcid: 12646201
Arnis S, Hofmann KP (1993) Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling state. Proc Natl Acad Sci U S A 90:7849–7853
pubmed: 8356093
pmcid: 47240
doi: 10.1073/pnas.90.16.7849
Arvanitakis L, Geras-Raaka E, Gershengorn MC (1998) Constitutively signaling G-protein coupled receptor and human disease. Trends Endocrinol Metab 9:27–31
pubmed: 18406231
doi: 10.1016/S1043-2760(98)00007-1
pmcid: 18406231
Athanasiou D, Aguila M, Bellingham J, Li WW, McCulley C, Reeves PJ, Cheetham ME (2018) The molecular and cellular basis of rhodopsin retinitis pigmentosa reveals potential strategies for therapy. Prog Retin Eye Res 62:1–23. https://doi.org/10.1016/j.preteyeres.2017.10.002
doi: 10.1016/j.preteyeres.2017.10.002
pubmed: 29042326
pmcid: 29042326
Baldwin JM (1993) The probable arrangement of the helices in G protein-coupled receptors. EMBO J 12:1693–1703
pubmed: 8385611
pmcid: 413383
doi: 10.1002/j.1460-2075.1993.tb05814.x
Baldwin JM, Schertler GF, Unger VM (1997) An alpha-carbon template for the transmembrane helices in the rhodopsin family of G-protein-coupled receptors. J Mol Biol 272:144–164
pubmed: 9299344
doi: 10.1006/jmbi.1997.1240
pmcid: 9299344
Ballesteros JA, Weinstein H (1995) Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors. Methods Neurosci 25:366–428
doi: 10.1016/S1043-9471(05)80049-7
Bartl FJ, Ritter E, Hofmann KP (2001) Signaling states of rhodopsin: absorption of light in active metarhodopsin II generates an all-trans-retinal bound inactive state. J Biol Chem 276:30161–30166
pubmed: 11384968
doi: 10.1074/jbc.M101506200
pmcid: 11384968
Bayburt TH, Leitz AJ, Xie G, Oprian DD, Sligar SG (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J Biol Chem 282:14875–14881. https://doi.org/10.1074/jbc.M701433200
doi: 10.1074/jbc.M701433200
pubmed: 17395586
pmcid: 17395586
Baylor D (1996) How photons start vision. Proc Natl Acad Sci U S A 93:560–565
pubmed: 8570595
pmcid: 40091
doi: 10.1073/pnas.93.2.560
Behnen P, Felline A, Comitato A, Di Salvo MT, Raimondi F, Gulati S, Kahremany S, Palczewski K, Marigo V, Fanelli F (2018) A small chaperone improves folding and routing of rhodopsin mutants linked to inherited blindness. iScience 4:1–19
pubmed: 30240733
pmcid: 6147235
doi: 10.1016/j.isci.2018.05.001
Blankenship E, Vahedi-Faridi A, Lodowski DT (2015) The high-resolution structure of activated opsin reveals a conserved solvent network in the transmembrane region essential for activation. Structure 23:2358–2364. https://doi.org/10.1016/j.str.2015.09.015
doi: 10.1016/j.str.2015.09.015
pubmed: 26526852
pmcid: 4670590
Bockaert J, Pin JP (1999) Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J 18:1723–1729
pubmed: 10202136
pmcid: 1171258
doi: 10.1093/emboj/18.7.1723
Bouvier M (2001) Oligomerization of G-protein-coupled transmitter receptors. Nat Rev Neurosci 2:274–286
pubmed: 11283750
doi: 10.1038/35067575
pmcid: 11283750
Brady AE, Limbird LE (2002) G protein-coupled receptor interacting proteins: emerging roles in localization and signal transduction. Cell Signal 14:297–309
pubmed: 11858937
doi: 10.1016/S0898-6568(01)00239-X
pmcid: 11858937
Breikers G, Portier-VandeLuytgaarden MJ, Bovee-Geurts PH, DeGrip WJ (2002) Retinitis pigmentosa-associated rhodopsin mutations in three membrane-located cysteine residues present three different biochemical phenotypes. Biochem Biophys Res Commun 297:847–853
pubmed: 12359230
doi: 10.1016/S0006-291X(02)02308-2
pmcid: 12359230
Briscoe AD, Gaur C, Kumar S (2004) The spectrum of human rhodopsin disease mutations through the lens of interspecific variation. Gene 332:107–118. https://doi.org/10.1016/j.gene.2004.02.037
doi: 10.1016/j.gene.2004.02.037
pubmed: 15145060
pmcid: 15145060
Chabre M, Cone R, Saibil H (2003) Biophysics: is rhodopsin dimeric in native retinal rods? Nature 426:30–31 discussion 31
pubmed: 14603306
doi: 10.1038/426030b
Chabre M, Deterre P, Antonny B (2009) The apparent cooperativity of some GPCRs does not necessarily imply dimerization. Trends Pharmacol Sci 30:182–187. https://doi.org/10.1016/j.tips.2009.01.003
doi: 10.1016/j.tips.2009.01.003
pubmed: 19269046
Chabre M, le Maire M (2005) Monomeric G-protein-coupled receptor as a functional unit. Biochemistry 44:9395–9403
pubmed: 15996094
doi: 10.1021/bi050720o
Chen Y, Jastrzebska B, Cao P, Zhang J, Wang B, Sun W, Yuan Y, Feng Z, Palczewski K (2014) Inherent instability of the retinitis pigmentosa P23H mutant opsin. J Biol Chem 289:9288–9303. https://doi.org/10.1074/jbc.M114.551713
doi: 10.1074/jbc.M114.551713
pubmed: 24515108
pmcid: 3979360
Chen YY, Chen Y, Jastrzebska B, Golczak M, Gulati S, Tang H, Seibel W, Li XYY, Jin H, Han Y, Gao SQ, Zhang JY, Liu XJ, Heidari-Torkabadi H, Stewart PL, Harte WE, Tochtrop GP, Palczewski K (2018) A novel small molecule chaperone of rod opsin and its potential therapy for retinal degeneration. Nat Commun 9. 1976 https://doi.org/10.1038/S41467-018-04261-1
Choe HW, Kim YJ, Park JH, Morizumi T, Pai EF, Krauss N, Hofmann KP, Scheerer P, Ernst OP (2011) Crystal structure of metarhodopsin II. Nature 471:651–655. https://doi.org/10.1038/nature09789
doi: 10.1038/nature09789
pubmed: 21389988
Chuang JZ, Vega C, Jun W, Sung CH (2004) Structural and functional impairment of endocytic pathways by retinitis pigmentosa mutant rhodopsin-arrestin complexes. J Clin Invest 114:131–140
pubmed: 15232620
pmcid: 437971
doi: 10.1172/JCI200421136
Cohen GB, Yang T, Robinson PR, Oprian DD (1993) Constitutive activation of opsin: influence of charge at position 134 and size at position 296. Biochemistry 32:6111–6115
pubmed: 8099498
doi: 10.1021/bi00074a024
pmcid: 8099498
Conn PM, Ulloa-Aguirre A (2010) Trafficking of G-protein-coupled receptors to the plasma membrane: insights for pharmacoperone drugs. Trends Endocrinol Metab 21:190–197. https://doi.org/10.1016/j.tem.2009.11.003
doi: 10.1016/j.tem.2009.11.003
pubmed: 20005736
pmcid: 20005736
Costa T, Cotecchia S (2005) Historical review: negative efficacy and the constitutive activity of G-protein-coupled receptors. Trends Pharmacol Sci 26:618–624. https://doi.org/10.1016/j.tips.2005.10.009
doi: 10.1016/j.tips.2005.10.009
pubmed: 16260046
Dell'Orco D, Koch KW (2015) Transient complexes between dark rhodopsin and transducin: circumstantial evidence or physiological necessity? Biophys J 108:775–777. https://doi.org/10.1016/j.bpj.2014.12.031
doi: 10.1016/j.bpj.2014.12.031
pubmed: 25650944
pmcid: 4317538
Dell'Orco D, Schmidt H, Mariani S, Fanelli F (2009) Network-level analysis of light adaptation in rod cells under normal and altered conditions. Mol BioSyst 5:1232–1246. https://doi.org/10.1039/b908123b
doi: 10.1039/b908123b
pubmed: 19756313
Deupi X, Edwards P, Singhal A, Nickle B, Oprian D, Schertler G, Standfuss J (2012) Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II. Proc Natl Acad Sci U S A 109:119–124. https://doi.org/10.1073/pnas.1114089108
doi: 10.1073/pnas.1114089108
pubmed: 22198838
Dizhoor AM, Woodruff ML, Olshevskaya EV, Cilluffo MC, Cornwall MC, Sieving PA, Fain GL (2008) Night blindness and the mechanism of constitutive signaling of mutant G90D rhodopsin. J Neurosci 28:11662–11672. https://doi.org/10.1523/JNEUROSCI.4006-08.2008
doi: 10.1523/JNEUROSCI.4006-08.2008
pubmed: 18987202
pmcid: 2590870
Ernst OP, Gramse V, Kolbe M, Hofmann KP, Heck M (2007) Monomeric G protein-coupled receptor rhodopsin in solution activates its G protein transducin at the diffusion limit. Proc Natl Acad Sci U S A 104:10859–10864
pubmed: 17578920
pmcid: 1904172
doi: 10.1073/pnas.0701967104
Fahmy K, Sakmar TP, Siebert F (2000) Transducin-dependent protonation of glutamic acid 134 in rhodopsin. Biochemistry 39:10607–10612
pubmed: 10956053
doi: 10.1021/bi000912d
Fanelli F, De Benedetti PG (2011) Update 1 of: computational modeling approaches to structure-function analysis of G protein-coupled receptors. Chem Rev 111:PR438–PR535. https://doi.org/10.1021/cr100437t
doi: 10.1021/cr100437t
pubmed: 22165845
pmcid: 22165845
Fanelli F, Felline A, Raimondi F (2013) Network analysis to uncover the structural communication in GPCRs. Methods Cell Biol 117:43–61. https://doi.org/10.1016/B978-0-12-408143-7.00003-7
doi: 10.1016/B978-0-12-408143-7.00003-7
pubmed: 24143971
Fanelli F, Seeber M (2010) Structural insights into retinitis pigmentosa from unfolding simulations of rhodopsin mutants. FASEB J 24:3196–3209. https://doi.org/10.1096/fj.09-151084
doi: 10.1096/fj.09-151084
pubmed: 20395457
Farrens DL, Khorana HG (1995) Structure and function in rhodopsin. Measurement of the rate of metarhodopsin II decay by fluorescence spectroscopy. J Biol Chem 270:5073–5076
pubmed: 7890614
doi: 10.1074/jbc.270.10.5073
pmcid: 7890614
Felline A, Seeber M, Rao F, Fanelli F (2009) Computational screening of rhodopsin mutations associated with retinitis pigmentosa. J Chem Theory Comput 5:2472–2485. https://doi.org/10.1021/Ct900145u
doi: 10.1021/Ct900145u
pubmed: 26616627
pmcid: 26616627
Ferrari S, Di Iorio E, Barbaro V, Ponzin D, Sorrentino FS, Parmeggiani F (2011) Retinitis pigmentosa: genes and disease mechanisms. Curr Genom 12:238–249
doi: 10.2174/138920211795860107
Flock T, Ravarani CN, Sun D, Venkatakrishnan AJ, Kayikci M, Tate CG, Veprintsev DB, Babu MM (2015) Universal allosteric mechanism for Galpha activation by GPCRs. Nature 524:173–179. https://doi.org/10.1038/nature14663
doi: 10.1038/nature14663
pubmed: 26147082
pmcid: 4866443
Fotiadis D, Jastrzebska B, Philippsen A, Muller DJ, Palczewski K, Engel A (2006) Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr Opin Struct Biol 16:252–259
pubmed: 16567090
doi: 10.1016/j.sbi.2006.03.013
Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A, Palczewski K (2003) Atomic-force microscopy: rhodopsin dimers in native disc membranes. Nature 421:127–128
pubmed: 12520290
doi: 10.1038/421127a
Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A, Palczewski K (2004) The G protein-coupled receptor rhodopsin in the native membrane. FEBS Lett 564:281–288
pubmed: 15111110
pmcid: 1393389
doi: 10.1016/S0014-5793(04)00194-2
Frins S, Bonigk W, Muller F, Kellner R, Koch KW (1996) Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods. Cloning, heterologous expression, and localization. J Biol Chem 271:8022–8027
pubmed: 8626484
doi: 10.1074/jbc.271.14.8022
Gao Y, Hu H, Ramachandran S, Erickson JW, Cerione RA, Skiniotis G (2019) Structures of the rhodopsin-transducin complex: insights into G-protein activation. Mol Cell 75:781–790 e783. https://doi.org/10.1016/j.molcel.2019.06.007
doi: 10.1016/j.molcel.2019.06.007
pubmed: 31300275
pmcid: 6707884
Garriga P, Liu X, Khorana HG (1996) Structure and function in rhodopsin: correct folding and misfolding in point mutants at and in proximity to the site of the retinitis pigmentosa mutation Leu-125-->Arg in the transmembrane helix C. Proc Natl Acad Sci U S A 93:4560–4564. https://doi.org/10.1073/pnas.93.10.4560
doi: 10.1073/pnas.93.10.4560
pubmed: 8643443
pmcid: 39316
Gether U (2000) Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr Rev 21:90–113
pubmed: 10696571
doi: 10.1210/edrv.21.1.0390
Goricanec D, Stehle R, Egloff P, Grigoriu S, Pluckthun A, Wagner G, Hagn F (2016) Conformational dynamics of a G-protein alpha subunit is tightly regulated by nucleotide binding. Proc Natl Acad Sci U S A 113:E3629–E3638. https://doi.org/10.1073/pnas.1604125113
doi: 10.1073/pnas.1604125113
pubmed: 27298341
pmcid: 4932968
Gragg M, Kim TG, Howell S, Park PS (2016) Wild-type opsin does not aggregate with a misfolded opsin mutant. Biochim Biophys Acta 1858:1850–1859. https://doi.org/10.1016/j.bbamem.2016.04.013
doi: 10.1016/j.bbamem.2016.04.013
pubmed: 27117643
pmcid: 4900927
Gragg M, Park PS (2018) Misfolded rhodopsin mutants display variable aggregation properties. Biochim Biophys Acta Mol basis Dis 1864:2938–2948. https://doi.org/10.1016/j.bbadis.2018.06.004
doi: 10.1016/j.bbadis.2018.06.004
pubmed: 29890221
Gragg M, Park PS (2019) Detection of misfolded rhodopsin aggregates in cells by Forster resonance energy transfer. Methods Cell Biol 149:87–105. https://doi.org/10.1016/bs.mcb.2018.08.007
doi: 10.1016/bs.mcb.2018.08.007
pubmed: 30616829
Gulati S, Jastrzebska B, Banerjee S, Placeres AL, Miszta P, Gao SQ, Gunderson K, Tochtrop GP, Filipek S, Katayama K, Kiser PD, Mogi M, Stewart PL, Palczewski K (2017) Photocyclic behavior of rhodopsin induced by an atypical isomerization mechanism. Proc Natl Acad Sci U S A 114:E2608–E2615. https://doi.org/10.1073/pnas.1617446114
doi: 10.1073/pnas.1617446114
pubmed: 28289214
pmcid: 5380078
Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. Lancet 368:1795–1809. https://doi.org/10.1016/S0140-6736(06)69740-7
doi: 10.1016/S0140-6736(06)69740-7
pubmed: 17113430
Heck M, Schadel SA, Maretzki D, Bartl FJ, Ritter E, Palczewski K, Hofmann KP (2003) Signaling states of rhodopsin. Formation of the storage form, metarhodopsin III, from active metarhodopsin II. J Biol Chem 278:3162–3169
pubmed: 12427735
doi: 10.1074/jbc.M209675200
Heck M, Schadel SA, Maretzki D, Hofmann KP (2003) Secondary binding sites of retinoids in opsin: characterization and role in regeneration. Vis Res 43:3003–3010
pubmed: 14611936
doi: 10.1016/j.visres.2003.08.011
Hilger D, Masureel M, Kobilka BK (2018) Structure and dynamics of GPCR signaling complexes. Nat Struct Mol Biol 25:4–12. https://doi.org/10.1038/s41594-017-0011-7
doi: 10.1038/s41594-017-0011-7
pubmed: 29323277
pmcid: 6535338
Hirsch JA, Schubert C, Gurevich VV, Sigler PB (1999) The 2.8 A crystal structure of visual arrestin: a model for arrestin’s regulation. Cell 97:257–269. https://doi.org/10.1016/s0092-8674(00)80735-7
doi: 10.1016/s0092-8674(00)80735-7
pubmed: 10219246
Hofmann KP, Scheerer P, Hildebrand PW, Choe HW, Park JH, Heck M, Ernst OP (2009) A G protein-coupled receptor at work: the rhodopsin model. Trends Biochem Sci 34:540–552. https://doi.org/10.1016/j.tibs.2009.07.005
doi: 10.1016/j.tibs.2009.07.005
pubmed: 19836958
Hwa J, Garriga P, Liu X, Khorana HG (1997) Structure and function in rhodopsin: packing of the helices in the transmembrane domain and folding to a tertiary structure in the intradiscal domain are coupled. Proc Natl Acad Sci U S A 94:10571–10576
pubmed: 9380676
pmcid: 23405
doi: 10.1073/pnas.94.20.10571
Hwa J, Klein-Seetharaman J, Khorana HG (2001) Structure and function in rhodopsin: mass spectrometric identification of the abnormal intradiscal disulfide bond in misfolded retinitis pigmentosa mutants. Proc Natl Acad Sci U S A 98:4872–4876. https://doi.org/10.1073/pnas.061632798
doi: 10.1073/pnas.061632798
pubmed: 11320236
pmcid: 33130
Hwa J, Reeves PJ, Klein-Seetharaman J, Davidson F, Khorana HG (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
pubmed: 10051572
pmcid: 26714
doi: 10.1073/pnas.96.5.1932
Jaeger K, Bruenle S, Weinert T, Guba W, Muehle J, Miyazaki T, Weber M, Furrer A, Haenggi N, Tetaz T, Huang CY, Mattle D, Vonach JM, Gast A, Kuglstatter A, Rudolph MG, Nogly P, Benz J, Dawson RJP, Standfuss J (2019) Structural basis for allosteric ligand recognition in the human CC chemokine receptor 7. Cell 178:1222–1230 e1210. https://doi.org/10.1016/j.cell.2019.07.028
doi: 10.1016/j.cell.2019.07.028
pubmed: 31442409
pmcid: 6709783
Jastrzebska B, Fotiadis D, Jang GF, Stenkamp RE, Engel A, Palczewski K (2006) Functional and structural characterization of rhodopsin oligomers. J Biol Chem 281:11917–11922. https://doi.org/10.1074/jbc.M600422200
doi: 10.1074/jbc.M600422200
pubmed: 16495215
pmcid: 16495215
Jastrzebska B, Maeda T, Zhu L, Fotiadis D, Filipek S, Engel A, Stenkamp RE, Palczewski K (2004) Functional characterization of rhodopsin monomers and dimers in detergents. J Biol Chem 279:54663–54675
pubmed: 15489507
doi: 10.1074/jbc.M408691200
Jin S, Cornwall MC, Oprian DD (2003) Opsin activation as a cause of congenital night blindness. Nat Neurosci 6:731–735. https://doi.org/10.1038/nn1070
doi: 10.1038/nn1070
pubmed: 12778053
Kang Y, Zhou XE, Gao X, He Y, Liu W, Ishchenko A, Barty A, White TA, Yefanov O, Han GW, Xu Q, de Waal PW, Ke J, Tan MH, Zhang C, Moeller A, West GM, Pascal BD, Van Eps N, Caro LN, Vishnivetskiy SA, Lee RJ, Suino-Powell KM, Gu X, Pal K, Ma J, Zhi X, Boutet S, Williams GJ, Messerschmidt M, Gati C, Zatsepin NA, Wang D, James D, Basu S, Roy-Chowdhury S, Conrad CE, Coe J, Liu H, Lisova S, Kupitz C, Grotjohann I, Fromme R, Jiang Y, Tan M, Yang H, Li J, Wang M, Zheng Z, Li D, Howe N, Zhao Y, Standfuss J, Diederichs K, Dong Y, Potter CS, Carragher B, Caffrey M, Jiang H, Chapman HN, Spence JC, Fromme P, Weierstall U, Ernst OP, Katritch V, Gurevich VV, Griffin PR, Hubbell WL, Stevens RC, Cherezov V, Melcher K, Xu HE (2015) Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523:561–567. https://doi.org/10.1038/nature14656
doi: 10.1038/nature14656
pubmed: 26200343
pmcid: 4521999
Kang YY, Kuybeda O, de Waal PW, Mukherjee S, Van Eps N, Dutka P, Zhou XE, Bartesaghi A, Erramilli S, Morizumi T, Gu X, Yin YT, Liu P, Jiang Y, Meng X, Zhao GP, Melcher K, Ernst OP, Kossiakoff AA, Subramaniam S, Xu HE (2018) Cryo-EM structure of human rhodopsin bound to an inhibitory G protein. Nature 558:553. https://doi.org/10.1038/s41586-018-0215-y
doi: 10.1038/s41586-018-0215-y
pubmed: 29899450
pmcid: 8054211
Karnik SS, Sakmar TP, Chen HB, Khorana HG (1988) Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin. Proc Natl Acad Sci U S A 85:8459–8463
pubmed: 3186735
pmcid: 282477
doi: 10.1073/pnas.85.22.8459
Katritch V, Cherezov V, Stevens RC (2013) Structure-function of the G protein-coupled receptor superfamily. Annu Rev Pharmacol Toxicol 53:531–556. https://doi.org/10.1146/annurev-pharmtox-032112-135923
doi: 10.1146/annurev-pharmtox-032112-135923
pubmed: 23140243
pmcid: 23140243
Kaushal S, Khorana HG (1994) Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33:6121–6128
pubmed: 8193125
doi: 10.1021/bi00186a011
pmcid: 8193125
Kefalov VJ, Crouch RK, Cornwall MC (2001) Role of noncovalent binding of 11-cis-retinal to opsin in dark adaptation of rod and cone photoreceptors. Neuron 29:749–755. https://doi.org/10.1016/s0896-6273(01)00249-5
doi: 10.1016/s0896-6273(01)00249-5
pubmed: 11301033
pmcid: 11301033
Kennan A, Aherne A, Humphries P (2005) Light in retinitis pigmentosa. Trends Genet 21:103–110
pubmed: 15661356
doi: 10.1016/j.tig.2004.12.001
Kim TH, Chung KY, Manglik A, Hansen AL, Dror RO, Mildorf TJ, Shaw DE, Kobilka BK, Prosser RS (2013) The role of ligands on the equilibria between functional states of a G protein-coupled receptor. J Am Chem Soc 135:9465–9474. https://doi.org/10.1021/ja404305k
doi: 10.1021/ja404305k
pubmed: 23721409
pmcid: 3763947
Kim YJ, Hofmann KP, Ernst OP, Scheerer P, Choe HW, Sommer ME (2013) Crystal structure of pre-activated arrestin p44. Nature 497:142–146. https://doi.org/10.1038/nature12133
doi: 10.1038/nature12133
pubmed: 23604253
pmcid: 23604253
Kiser PD, Golczak M, Palczewski K (2014) Chemistry of the retinoid (visual) cycle. Chem Rev 114:194–232. https://doi.org/10.1021/cr400107q
doi: 10.1021/cr400107q
pubmed: 23905688
pmcid: 23905688
Kliger DS, Lewis JW (1995) Spectral and kinetic characterization of visual pigment photointermediates. Israel J Chem 35:289–307
doi: 10.1002/ijch.199500032
Knierim B, Hofmann KP, Ernst OP, Hubbell WL (2007) Sequence of late molecular events in the activation of rhodopsin. Proc Natl Acad Sci U S A 104:20290–20295. https://doi.org/10.1073/pnas.0710393104
doi: 10.1073/pnas.0710393104
pubmed: 18077356
pmcid: 2154424
Koch KW, Duda T, Sharma RK (2002) Photoreceptor specific guanylate cyclases in vertebrate phototransduction. Mol Cell Biochem 230:97–106
pubmed: 11952100
doi: 10.1023/A:1014209711793
Kono M, Goletz PW, Crouch RK (2008) 11-cis- and all-trans-retinols can activate rod opsin: rational design of the visual cycle. Biochemistry 47:7567–7571. https://doi.org/10.1021/bi800357b
doi: 10.1021/bi800357b
pubmed: 18563917
pmcid: 18563917
Kota P, Reeves PJ, Rajbhandary UL, Khorana HG (2006) Opsin is present as dimers in COS1 cells: identification of amino acids at the dimeric interface. Proc Natl Acad Sci U S A 103:3054–3059. https://doi.org/10.1073/pnas.0510982103
doi: 10.1073/pnas.0510982103
pubmed: 16492774
pmcid: 1413904
Krebs MP, Holden DC, Joshi P, Clark CL 3rd, Lee AH, Kaushal S (2010) Molecular mechanisms of rhodopsin retinitis pigmentosa and the efficacy of pharmacological rescue. J Mol Biol 395:1063–1078. https://doi.org/10.1016/j.jmb.2009.11.015
doi: 10.1016/j.jmb.2009.11.015
pubmed: 19913029
pmcid: 19913029
Kristiansen K (2004) Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacol Ther 103:21–80
pubmed: 15251227
doi: 10.1016/j.pharmthera.2004.05.002
pmcid: 15251227
Lamb TD (1996) Gain and kinetics of activation in the G-protein cascade of phototransduction. Proc Natl Acad Sci U S A 93:566–570
pubmed: 8570596
pmcid: 40092
doi: 10.1073/pnas.93.2.566
Lefkowitz RJ (2000) The superfamily of heptahelical receptors. Nat Cell Biol 2:E133–E136
pubmed: 10878827
doi: 10.1038/35017152
pmcid: 10878827
Lefkowitz RJ, Cotecchia S, Samama P, Costa T (1993) Constitutive activity of receptors coupled to guanine nucleotide regulatory proteins. Trends Pharmacol Sci 14:303–307
pubmed: 8249148
doi: 10.1016/0165-6147(93)90048-O
pmcid: 8249148
Li J, Edwards PC, Burghammer M, Villa C, Schertler GF (2004) Structure of bovine rhodopsin in a trigonal crystal form. J Mol Biol 343:1409–1438
pubmed: 15491621
doi: 10.1016/j.jmb.2004.08.090
pmcid: 15491621
Li T, Sandberg MA, Pawlyk BS, Rosner B, Hayes KC, Dryja TP, Berson EL (1998) Effect of vitamin A supplementation on rhodopsin mutants threonine-17 --> methionine and proline-347 --> serine in transgenic mice and in cell cultures. Proc Natl Acad Sci U S A 95:11933–11938
pubmed: 9751768
pmcid: 21743
doi: 10.1073/pnas.95.20.11933
Liang Y, Fotiadis D, Filipek S, Saperstein DA, Palczewski K, Engel A (2003) Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J Biol Chem 278:21655–21662
pubmed: 12663652
doi: 10.1074/jbc.M302536200
pmcid: 12663652
Lin JC, Liu HL (2006) Protein conformational diseases: from mechanisms to drug designs. Curr Drug Discov Technol 3:145–153
pubmed: 16925522
doi: 10.2174/157016306778108866
pmcid: 16925522
Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B, Shokat KM, Lavail MM, Walter P (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318:944–949. https://doi.org/10.1126/science.1146361
doi: 10.1126/science.1146361
pubmed: 17991856
pmcid: 3670588
Lodowski DT, Salom D, Le Trong I, Teller DC, Ballesteros JA, Palczewski K, Stenkamp RE (2007) Crystal packing analysis of Rhodopsin crystals. J Struct Biol 158:455–462. https://doi.org/10.1016/j.jsb.2007.01.017
doi: 10.1016/j.jsb.2007.01.017
pubmed: 17374491
pmcid: 1950280
Lohse MJ (2010) Dimerization in GPCR mobility and signaling. Curr Opin Pharmacol 10:53–58. https://doi.org/10.1016/j.coph.2009.10.007
doi: 10.1016/j.coph.2009.10.007
pubmed: 19910252
pmcid: 19910252
Makino CL, Riley CK, Looney J, Crouch RK, Okada T (2010) Binding of more than one retinoid to visual opsins. Biophys J 99:2366–2373. https://doi.org/10.1016/j.bpj.2010.08.003
doi: 10.1016/j.bpj.2010.08.003
pubmed: 20923672
pmcid: 3042582
Mattle D, Kuhn B, Aebi J, Bedoucha M, Kekilli D, Grozinger N, Alker A, Rudolph MG, Schmid G, Schertler GFX, Hennig M, Standfuss J, Dawson RJP (2018) Ligand channel in pharmacologically stabilized rhodopsin. Proc Natl Acad Sci U S A 115:3640–3645. https://doi.org/10.1073/pnas.1718084115
doi: 10.1073/pnas.1718084115
pubmed: 29555765
pmcid: 5889642
McAlear SD, Kraft TW, Gross AK (2010) 1 rhodopsin mutations in congenital night blindness. Adv Exp Med Biol 664:263–272. https://doi.org/10.1007/978-1-4419-1399-9_30
doi: 10.1007/978-1-4419-1399-9_30
pubmed: 20238025
pmcid: 20238025
McBee JK, Palczewski K, Baehr W, Pepperberg DR (2001) Confronting complexity: the interlink of phototransduction and retinoid metabolism in the vertebrate retina. Prog Retin Eye Res 20:469–529
pubmed: 11390257
doi: 10.1016/S1350-9462(01)00002-7
pmcid: 11390257
Melia TJ Jr, Cowan CW, Angleson JK, Wensel TG (1997) A comparison of the efficiency of G protein activation by ligand-free and light-activated forms of rhodopsin. Biophys J 73:3182–3191
pubmed: 9414230
pmcid: 1181221
doi: 10.1016/S0006-3495(97)78344-9
Mendes HF, Cheetham ME (2008) Pharmacological manipulation of gain-of-function and dominant-negative mechanisms in rhodopsin retinitis pigmentosa. Hum Mol Genet 17:3043–3054. https://doi.org/10.1093/hmg/ddn202
doi: 10.1093/hmg/ddn202
pubmed: 18635576
pmcid: 18635576
Mendes HF, van der Spuy J, Chapple JP, Cheetham ME (2005) Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy. Trends Mol Med 11:177–185
pubmed: 15823756
doi: 10.1016/j.molmed.2005.02.007
pmcid: 15823756
Milligan G (2010) The role of dimerisation in the cellular trafficking of G-protein-coupled receptors. Curr Opin Pharmacol 10:23–29. https://doi.org/10.1016/j.coph.2009.09.010
doi: 10.1016/j.coph.2009.09.010
pubmed: 19850521
pmcid: 19850521
Mirzadegan T, Benko G, Filipek S, Palczewski K (2003) Sequence analyses of G-protein-coupled receptors: similarities to rhodopsin. Biochemistry 42:2759–2767
pubmed: 12627940
doi: 10.1021/bi027224+
pmcid: 12627940
Mishra AK, Gragg M, Stoneman MR, Biener G, Oliver JA, Miszta P, Filipek S, Raicu V, Park PS (2016) Quaternary structures of opsin in live cells revealed by FRET spectrometry. Biochem J 473:3819–3836. https://doi.org/10.1042/BCJ20160422
doi: 10.1042/BCJ20160422
pubmed: 27623775
pmcid: 27623775
Nakamichi H, Buss V, Okada T (2007) Photoisomerization mechanism of rhodopsin and 9-cis-rhodopsin revealed by X-ray crystallography. Biophys J 92:L106–L108. https://doi.org/10.1529/biophysj.107.108225
doi: 10.1529/biophysj.107.108225
pubmed: 17449675
pmcid: 1877761
Nakamichi H, Okada T (2006) Crystallographic analysis of primary visual photochemistry. Angew Chem Int Ed Eng 45:4270–4273. https://doi.org/10.1002/anie.200600595
doi: 10.1002/anie.200600595
Nakamichi H, Okada T (2006) Local peptide movement in the photoreaction intermediate of rhodopsin. Proc Natl Acad Sci U S A 103:12729–12734. https://doi.org/10.1073/pnas.0601765103
doi: 10.1073/pnas.0601765103
pubmed: 16908857
pmcid: 1562544
Nakamichi H, Okada T (2007) X-ray crystallographic analysis of 9-cis-rhodopsin, a model analogue visual pigment. Photochem Photobiol 83:232–235. https://doi.org/10.1562/2006-13-Ra-920
doi: 10.1562/2006-13-Ra-920
pubmed: 17576343
pmcid: 17576343
Noel JP, Hamm HE, Sigler PB (1993) The 2.2 A crystal structure of transducin-alpha complexed with GTP gamma S. Nature 366:654–663. https://doi.org/10.1038/366654a0
doi: 10.1038/366654a0
pubmed: 8259210
pmcid: 8259210
Noorwez SM, Malhotra R, McDowell JH, Smith KA, Krebs MP, Kaushal S (2004) Retinoids assist the cellular folding of the autosomal dominant retinitis pigmentosa opsin mutant P23H. J Biol Chem 279:16278–16284. https://doi.org/10.1074/jbc.M312101200
doi: 10.1074/jbc.M312101200
pubmed: 14769795
pmcid: 14769795
Noorwez SM, Sama RR, Kaushal S (2009) Calnexin improves the folding efficiency of mutant rhodopsin in the presence of pharmacological chaperone 11-cis-retinal. J Biol Chem 284:33333–33342. https://doi.org/10.1074/jbc.M109.043364
doi: 10.1074/jbc.M109.043364
pubmed: 19801547
pmcid: 2785176
Okada T, Ernst OP, Palczewski K, Hofmann KP (2001) Activation of rhodopsin: new insights from structural and biochemical studies. Trends Biochem Sci 26:318–324
pubmed: 11343925
doi: 10.1016/S0968-0004(01)01799-6
pmcid: 11343925
Okada T, Fujiyoshi Y, Silow M, Navarro J, Landau EM, 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
pubmed: 11972040
pmcid: 122888
doi: 10.1073/pnas.082666399
Okada T, Sugihara M, Bondar AN, Elstner M, Entel P, Buss V (2004) The retinal conformation and its environment in rhodopsin in light of a new 2.2 A crystal structure. J Mol Biol 342:571–583
pubmed: 15327956
doi: 10.1016/j.jmb.2004.07.044
pmcid: 15327956
Palczewski K (1997) GTP-binding-protein-coupled receptor kinases--two mechanistic models. Eur J Biochem 248:261–269
pubmed: 9346277
doi: 10.1111/j.1432-1033.1997.00261.x
pmcid: 9346277
Palczewski K (2006) G protein-coupled receptor rhodopsin. Annu Rev Biochem 75:743–767. https://doi.org/10.1146/annurev.biochem.75.103004.142743
doi: 10.1146/annurev.biochem.75.103004.142743
pubmed: 1560097
pmcid: 1560097
Palczewski K (2010) Oligomeric forms of G protein-coupled receptors (GPCRs). Trends Biochem Sci 35:595–600. https://doi.org/10.1016/j.tibs.2010.05.002
doi: 10.1016/j.tibs.2010.05.002
pubmed: 20538466
pmcid: 2937196
Palczewski K (2010) Retinoids for treatment of retinal diseases. Trends Pharmacol Sci 31:284–295. https://doi.org/10.1016/j.tips.2010.03.001
doi: 10.1016/j.tips.2010.03.001
pubmed: 20435355
pmcid: 2882531
Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739–745
pubmed: 10926528
doi: 10.1126/science.289.5480.739
pmcid: 10926528
Park JH, Morizumi T, Li Y, Hong JE, Pai EF, Hofmann KP, Choe HW, Ernst OP (2013) Opsin, a structural model for olfactory receptors? Angew Chem Int Ed Eng 52:11021–11024. https://doi.org/10.1002/anie.201302374
doi: 10.1002/anie.201302374
Park JH, Scheerer P, Hofmann KP, Choe HW, Ernst OP (2008) Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454:183–187. https://doi.org/10.1038/nature07063
doi: 10.1038/nature07063
pubmed: 18563085
Park PS, Filipek S, Wells JW, Palczewski K (2004) Oligomerization of G protein-coupled receptors: past, present, and future. Biochemistry 43:15643–15656
pubmed: 15595821
doi: 10.1021/bi047907k
pmcid: 15595821
Pierce KL, Premont RT, Lefkowitz RJ (2002) Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3:639–650
pubmed: 12209124
pmcid: 12209124
doi: 10.1038/nrm908
Ploier B, Caro LN, Morizumi T, Pandey K, Pearring JN, Goren MA, Finnemann SC, Graumann J, Arshavsky VY, Dittman JS, Ernst OP, Menon AK (2016) Dimerization deficiency of enigmatic retinitis pigmentosa-linked rhodopsin mutants. Nat Commun 7:12832. https://doi.org/10.1038/ncomms12832
doi: 10.1038/ncomms12832
pubmed: 27694816
pmcid: 5059438
Pulvermuller A, Palczewski K, Hofmann KP (1993) Interaction between photoactivated rhodopsin and its kinase: stability and kinetics of complex formation. Biochemistry 32:14082–14088
pubmed: 8260489
doi: 10.1021/bi00214a002
pmcid: 8260489
Punzo C, Kornacker K, Cepko CL (2009) Stimulation of the insulin/mTOR pathway delays cone death in a mouse model of retinitis pigmentosa. Nat Neurosci 12:44–52. https://doi.org/10.1038/nn.2234
doi: 10.1038/nn.2234
pubmed: 19060896
Raimondi F, Seeber M, Benedetti PG, Fanelli F (2008) Mechanisms of inter- and intramolecular communication in GPCRs and G proteins. J Am Chem Soc 130:4310–4325. https://doi.org/10.1021/ja077268b
doi: 10.1021/ja077268b
pubmed: 18335928
pmcid: 18335928
Rakoczy EP, Kiel C, McKeone R, Stricher F, Serrano L (2010) Analysis of disease-linked rhodopsin mutations based on structure, function, and protein stability calculations. J Mol Biol 405:584–606. https://doi.org/10.1016/j.jmb.2010.11.003
doi: 10.1016/j.jmb.2010.11.003
pubmed: 21094163
pmcid: 21094163
Rao VR, Cohen GB, Oprian DD (1994) Rhodopsin mutation G90D and a molecular mechanism for congenital night blindness. Nature 367:639–642. https://doi.org/10.1038/367639a0
doi: 10.1038/367639a0
pubmed: 8107847
pmcid: 8107847
Rasmussen SG, Devree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, Mathiesen JM, Shah ST, Lyons JA, Caffrey M, Gellman SH, Steyaert J, Skiniotis G, Weis WI, Sunahara RK, Kobilka BK (2011) Crystal structure of the beta(2) adrenergic receptor-Gs protein complex. Nature 469:175–181. https://doi.org/10.1038/nature10361
doi: 10.1038/nature10361
pubmed: 21228869
pmcid: 3058308
Reeves PJ, Hwa J, Khorana HG (1999) Structure and function in rhodopsin: kinetic studies of retinal binding to purified opsin mutants in defined phospholipid-detergent mixtures serve as probes of the retinal binding pocket. Proc Natl Acad Sci U S A 96:1927–1931
pubmed: 10051571
pmcid: 26713
doi: 10.1073/pnas.96.5.1927
Richards JE, Scott KM, Sieving PA (1995) Disruption of conserved rhodopsin disulfide bond by Cys187Tyr mutation causes early and severe autosomal dominant retinitis pigmentosa. Ophthalmology 102:669–677
pubmed: 7724183
doi: 10.1016/S0161-6420(95)30972-4
Ritter E, Zimmermann K, Heck M, Hofmann KP, Bartl FJ (2004) Transition of rhodopsin into the active metarhodopsin II state opens a new light-induced pathway linked to Schiff base isomerization. J Biol Chem 279:48102–48111
pubmed: 15322129
doi: 10.1074/jbc.M406857200
Ruprecht JJ, Mielke T, Vogel R, Villa C, Schertler GF (2004) Electron crystallography reveals the structure of metarhodopsin I. EMBO J 23:3609–3620
pubmed: 15329674
pmcid: 517614
doi: 10.1038/sj.emboj.7600374
Sakami S, Maeda T, Bereta G, Okano K, Golczak M, Sumaroka A, Roman AJ, Cideciyan AV, Jacobson SG, Palczewski K (2011) Probing mechanisms of photoreceptor degeneration in a new mouse model of the common form of autosomal dominant retinitis pigmentosa due to P23H opsin mutations. J Biol Chem 286:10551–10567. https://doi.org/10.1074/jbc.M110.209759
doi: 10.1074/jbc.M110.209759
pubmed: 21224384
pmcid: 3060508
Salom D, Lodowski DT, Stenkamp RE, Le Trong I, Golczak M, Jastrzebska B, Harris T, Ballesteros JA, Palczewski K (2006) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc Natl Acad Sci U S A 103:16123–16128
pubmed: 17060607
pmcid: 1637547
doi: 10.1073/pnas.0608022103
Sandberg MN, Amora TL, Ramos LS, Chen MH, Knox BE, Birge RR (2011) Glutamic acid 181 is negatively charged in the bathorhodopsin photointermediate of visual rhodopsin. J Am Chem Soc 133:2808–2811. https://doi.org/10.1021/ja1094183
doi: 10.1021/ja1094183
pubmed: 21319741
pmcid: 3050519
Sanders CR, Myers JK (2004) Disease-related misassembly of membrane proteins. Annu Rev Biophys Biomol Struct 33:25–51. https://doi.org/10.1146/annurev.biophys.33.110502.140348
doi: 10.1146/annurev.biophys.33.110502.140348
pubmed: 15139803
Sato K, Morizumi T, Yamashita T, Shichida Y (2010) Direct observation of the pH-dependent equilibrium between metarhodopsins I and II and the pH-independent interaction of metarhodopsin II with transducin C-terminal peptide. Biochemistry 49:736–741. https://doi.org/10.1021/bi9018412
doi: 10.1021/bi9018412
pubmed: 20030396
Schadel SA, Heck M, Maretzki D, Filipek S, Teller DC, Palczewski K, Hofmann KP (2003) Ligand channeling within a G-protein-coupled receptor. The entry and exit of retinals in native opsin. J Biol Chem 278:24896–24903
pubmed: 12707280
doi: 10.1074/jbc.M302115200
Scheerer P, Heck M, Goede A, Park JH, Choe HW, Ernst OP, Hofmann KP, Hildebrand PW (2009) Structural and kinetic modeling of an activating helix switch in the rhodopsin-transducin interface. Proc Natl Acad Sci U S A 106:10660–10665. https://doi.org/10.1073/pnas.0900072106
doi: 10.1073/pnas.0900072106
pubmed: 19541654
pmcid: 2705592
Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauss N, Choe HW, Hofmann KP, Ernst OP (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455:497–502. https://doi.org/10.1038/nature07330
doi: 10.1038/nature07330
pubmed: 18818650
Scheerer P, Sommer ME (2017) Structural mechanism of arrestin activation. Curr Opin Struct Biol 45:160–169. https://doi.org/10.1016/j.sbi.2017.05.001
doi: 10.1016/j.sbi.2017.05.001
pubmed: 28600951
pmcid: 28600951
Shenker A (1995) G protein-coupled receptor structure and function: the impact of disease-causing mutations. Bailliere Clin Endocrinol Metab 9:427–451
doi: 10.1016/S0950-351X(95)80519-2
Sieving PA, Fowler ML, Bush RA, Machida S, Calvert PD, Green DG, Makino CL, McHenry CL (2001) Constitutive “light” adaptation in rods from G90D rhodopsin: a mechanism for human congenital nightblindness without rod cell loss. J Neurosci 21:5449–5460
pubmed: 11466416
pmcid: 6762654
doi: 10.1523/JNEUROSCI.21-15-05449.2001
Sieving PA, Richards JE, Naarendorp F, Bingham EL, Scott K, Alpern M (1995) Dark-light: model for nightblindness from the human rhodopsin Gly-90-->Asp mutation. Proc Natl Acad Sci U S A 92:880–884. https://doi.org/10.1073/pnas.92.3.880
doi: 10.1073/pnas.92.3.880
pubmed: 7846071
pmcid: 42724
Singhal A, Guo Y, Matkovic M, Schertler G, Deupi X, Yan EC, Standfuss J (2016) Structural role of the T94I rhodopsin mutation in congenital stationary night blindness. EMBO Rep 17:1431–1440. https://doi.org/10.15252/embr.201642671
doi: 10.15252/embr.201642671
pubmed: 27458239
pmcid: 5048376
Singhal A, Ostermaier MK, Vishnivetskiy SA, Panneels V, Homan KT, Tesmer JJ, Veprintsev D, Deupi X, Gurevich VV, Schertler GF, Standfuss J (2013) Insights into congenital stationary night blindness based on the structure of G90D rhodopsin. EMBO Rep. https://doi.org/10.1038/embor.2013.44
Standfuss J, Edwards PC, D'Antona A, Fransen M, Xie G, Oprian DD, Schertler GF (2011) The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471:656–660. https://doi.org/10.1038/nature09795
doi: 10.1038/nature09795
pubmed: 21389983
pmcid: 3715716
Standfuss J, Xie G, Edwards PC, Burghammer M, Oprian DD, Schertler GF (2007) Crystal structure of a thermally stable rhodopsin mutant. J Mol Biol 372:1179–1188. https://doi.org/10.1016/j.jmb.2007.03.007
doi: 10.1016/j.jmb.2007.03.007
pubmed: 17825322
pmcid: 2258155
Stenkamp RE (2008) Alternative models for two crystal structures of bovine rhodopsin. Acta Crystallogr D Biol Crystallogr D64:902–904. https://doi.org/10.1107/S0907444908017162
doi: 10.1107/S0907444908017162
pubmed: 18645239
Stojanovic A, Hwang I, Khorana HG, Hwa J (2003) Retinitis pigmentosa rhodopsin mutations L125R and A164V perturb critical interhelical interactions: new insights through compensatory mutations and crystal structure analysis. J Biol Chem 278:39020–39028. https://doi.org/10.1074/jbc.M303625200
doi: 10.1074/jbc.M303625200
pubmed: 12871954
Suda K, Filipek S, Palczewski K, Engel A, Fotiadis D (2004) The supramolecular structure of the GPCR rhodopsin in solution and native disc membranes. Mol Membr Biol 21:435–446
pubmed: 15764373
pmcid: 1351286
doi: 10.1080/09687860400020291
Sun D, Flock T, Deupi X, Maeda S, Matkovic M, Mendieta S, Mayer D, Dawson RJ, Schertler GF, Babu MM, Veprintsev DB (2015) Probing Galphai1 protein activation at single-amino acid resolution. Nat Struct Mol Biol 22:686–694. https://doi.org/10.1038/nsmb.3070
doi: 10.1038/nsmb.3070
pubmed: 26258638
pmcid: 4876908
Sung CH, Davenport CM, 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
pubmed: 8253795
doi: 10.1016/S0021-9258(19)74360-9
Sung CH, Schneider BG, Agarwal N, Papermaster DS, Nathans J (1991) Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci U S A 88:8840–8844
pubmed: 1924344
pmcid: 52606
doi: 10.1073/pnas.88.19.8840
Szczepek M, Beyriere F, Hofmann KP, Elgeti M, Kazmin R, Rose A, Bartl FJ, von Stetten D, Heck M, Sommer ME, Hildebrand PW, Scheerer P (2014) Crystal structure of a common GPCR-binding interface for G protein and arrestin. Nat Commun 5:4801. https://doi.org/10.1038/ncomms5801
doi: 10.1038/ncomms5801
pubmed: 25205354
Tam BM, Moritz OL (2009) The role of rhodopsin glycosylation in protein folding, trafficking, and light-sensitive retinal degeneration. J Neurosci 29:15145–15154. https://doi.org/10.1523/JNEUROSCI.4259-09.2009
doi: 10.1523/JNEUROSCI.4259-09.2009
pubmed: 19955366
pmcid: 6665958
Tao YX (2008) Constitutive activation of G protein-coupled receptors and diseases: insights into mechanisms of activation and therapeutics. Pharmacol Ther 120:129–148. https://doi.org/10.1016/j.pharmthera.2008.07.005
doi: 10.1016/j.pharmthera.2008.07.005
pubmed: 18768149
pmcid: 2668812
Teller DC, Okada T, Behnke CA, Palczewski K, Stenkamp RE (2001) Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G-protein-coupled receptors (GPCRs). Biochemistry 40:7761–7772
pubmed: 11425302
doi: 10.1021/bi0155091
Themmen AP, Martens JW, Brunner HG (1998) Activating and inactivating mutations in LH receptors. Mol Cell Endocrinol 145:137–142
pubmed: 9922110
doi: 10.1016/S0303-7207(98)00180-4
Tsai CJ, Marino J, Adaixo R, Pamula F, Muehle J, Maeda S, Flock T, Taylor NM, Mohammed I, Matile H, Dawson RJ, Deupi X, Stahlberg H, Schertler G (2019) Cryo-EM structure of the rhodopsin-Galphai-betagamma complex reveals binding of the rhodopsin C-terminal tail to the gbeta subunit. Elife 8. https://doi.org/10.7554/eLife.46041
Tsai CJ, Pamula F, Nehme R, Muhle J, Weinert T, Flock T, Nogly P, Edwards PC, Carpenter B, Gruhl T, Ma P, Deupi X, Standfuss J, Tate CG, Schertler GFX (2018) Crystal structure of rhodopsin in complex with a mini-Go sheds light on the principles of G protein selectivity. Sci Adv 4:eaat7052. https://doi.org/10.1126/sciadv.aat7052
doi: 10.1126/sciadv.aat7052
pubmed: 30255144
pmcid: 6154990
Van Eps N, Preininger AM, Alexander N, Kaya AI, Meier S, Meiler J, Hamm HE, Hubbell WL (2011) Interaction of a G protein with an activated receptor opens the interdomain interface in the alpha subunit. Proc Natl Acad Sci U S A 108:9420–9424. https://doi.org/10.1073/pnas.1105810108
doi: 10.1073/pnas.1105810108
pubmed: 21606326
pmcid: 3111277
Vishveshwara S, Ghosh A, Hansia P (2009) Intra and inter-molecular communications through protein structure network. Curr Protein Pept Sci 10:146–160
pubmed: 19355982
doi: 10.2174/138920309787847590
Wittinghofer A, Vetter IR (2011) Structure-function relationships of the G domain, a canonical switch motif. Annu Rev Biochem 80:943–971. https://doi.org/10.1146/annurev-biochem-062708-134043
doi: 10.1146/annurev-biochem-062708-134043
pubmed: 21675921
Yan EC, Kazmi MA, De S, Chang BS, Seibert C, Marin EP, Mathies RA, Sakmar TP (2002) Function of extracellular loop 2 in rhodopsin: glutamic acid 181 modulates stability and absorption wavelength of metarhodopsin II. Biochemistry 41:3620–3627
pubmed: 11888278
doi: 10.1021/bi0160011
Yan EC, Kazmi MA, Ganim Z, Hou JM, Pan D, Chang BS, Sakmar TP, Mathies RA (2003) Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc Natl Acad Sci U S A 100:9262–9267
pubmed: 12835420
pmcid: 170906
doi: 10.1073/pnas.1531970100
Zhang M, Wang W (2003) Organization of signaling complexes by PDZ-domain scaffold proteins. Acc Chem Res 36:530–538
pubmed: 12859214
doi: 10.1021/ar020210b
Zhao DY, Poge M, Morizumi T, Gulati S, Van Eps N, Zhang J, Miszta P, Filipek S, Mahamid J, Plitzko JM, Baumeister W, Ernst OP, Palczewski K (2019) Cryo-EM structure of the native rhodopsin dimer in nanodiscs. J Biol Chem 294:14215–14230. https://doi.org/10.1074/jbc.RA119.010089
doi: 10.1074/jbc.RA119.010089
pubmed: 31399513
pmcid: 6768649
Zhou XE, Gao X, Barty A, Kang YY, He YZ, Liu W, Ishchenko A, White TA, Yefanov O, Han GW, Xu QP, de Waal PW, Suino-Powell KM, Boutet S, Williams GJ, Wang MT, Li DF, Caffrey M, Chapman HN, Spence JCH, Fromme P, Weierstall U, Stevens RC, Cherezov V, Melcher K, Xu HE (2016) X-ray laser diffraction for structure determination of the rhodopsin-arrestin complex. Sci Data 3:160021. https://doi.org/10.1038/Sdata.2016.21
doi: 10.1038/Sdata.2016.21
pubmed: 27070998
pmcid: 4828943
Zhou XE, He YZ, de Waal PW, Gao X, Kang YY, Van Eps N, Yin YT, Pal K, Goswami D, White TA, Barty A, Latorraca NR, Chapman HN, Hubbell WL, Dror RO, Stevens RC, Cherezov V, Gurevich VV, Griffin PR, Ernst OP, Melcher K, Xu HE (2017) Identification of phosphorylation codes for arrestin recruitment by G protein-coupled receptors. Cell 170:457–469. https://doi.org/10.1016/j.cell.2017.07.002
doi: 10.1016/j.cell.2017.07.002
pubmed: 28753425
pmcid: 5567868