Convergent evolutionary counterion displacement of bilaterian opsins in ciliary cells.
Ciliary photoreceptor cell
Counterion
Molecular evolution
Opsin
Rhodopsin
Xenopsin
Journal
Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402
Informations de publication
Date de publication:
24 Aug 2022
24 Aug 2022
Historique:
received:
11
04
2022
accepted:
10
08
2022
revised:
10
08
2022
entrez:
24
8
2022
pubmed:
25
8
2022
medline:
27
8
2022
Statut:
epublish
Résumé
Opsins are universal photoreceptive proteins in animals. Vertebrate rhodopsin in ciliary photoreceptor cells photo-converts to a metastable active state to regulate cyclic nucleotide signaling. This active state cannot photo-convert back to the dark state, and thus vertebrate rhodopsin is categorized as a mono-stable opsin. By contrast, mollusk and arthropod rhodopsins in rhabdomeric photoreceptor cells photo-convert to a stable active state to stimulate IP
Identifiants
pubmed: 36001156
doi: 10.1007/s00018-022-04525-6
pii: 10.1007/s00018-022-04525-6
doi:
Substances chimiques
Nucleotides, Cyclic
0
Opsins
0
Rhodopsin
9009-81-8
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
493Subventions
Organisme : Core Research for Evolutional Science and Technology
ID : JPMJCR1753
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Arendt D (2003) Evolution of eyes and photoreceptor cell types. Int J Dev Biol 47:563–571
pubmed: 14756332
Shichida Y, Matsuyama T (2009) Evolution of opsins and phototransduction. Philos Trans R Soc Lond B Biol Sci 364:2881–2895
doi: 10.1098/rstb.2009.0051
Yau KW, Hardie RC (2009) Phototransduction motifs and variations. Cell 139:246–264
doi: 10.1016/j.cell.2009.09.029
Fain GL, Hardie R, Laughlin SB (2010) Phototransduction and the evolution of photoreceptors. Curr Biol 20:R114-124
doi: 10.1016/j.cub.2009.12.006
Eakin RM (1979) Evolutionary significance of photoreceptors—retrospect. Am Zool 19:647–653
doi: 10.1093/icb/19.2.647
Lamb TD, Collin SP, Pugh EN Jr (2007) Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci 8:960–976
doi: 10.1038/nrn2283
Koyanagi M, Terakita A (2014) Diversity of animal opsin-based pigments and their optogenetic potential. Biochim Biophys Acta 1837:710–716
doi: 10.1016/j.bbabio.2013.09.003
Sakmar TP, Franke RR, Khorana HG (1989) Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc Natl Acad Sci USA 86:8309–8313
doi: 10.1073/pnas.86.21.8309
Zhukovsky EA, Oprian DD (1989) Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science 246:928–930
doi: 10.1126/science.2573154
Nathans J (1990) Determinants of visual pigment absorbance: identification of the retinylidene Schiff’s base counterion in bovine rhodopsin. Biochemistry 29:9746–9752
doi: 10.1021/bi00493a034
Terakita A, Koyanagi M, Tsukamoto H, Yamashita T, Miyata T, Shichida Y (2004) Counterion displacement in the molecular evolution of the rhodopsin family. Nat Struct Mol Biol 11:284–289
doi: 10.1038/nsmb731
Murakami M, Kouyama T (2008) Crystal structure of squid rhodopsin. Nature 453:363–367
doi: 10.1038/nature06925
Varma N, Mutt E, Muhle J, Panneels V, Terakita A, Deupi X, Nogly P, Schertler GFX, Lesca E (2019) Crystal structure of jumping spider rhodopsin-1 as a light sensitive GPCR. Proc Natl Acad Sci USA 116:14547–14556
doi: 10.1073/pnas.1902192116
Ramirez MD, Pairett AN, Pankey MS, Serb JM, Speiser DI, Swafford AJ, Oakley TH (2016) The last common ancestor of most bilaterian animals possessed at least nine opsins. Genome Biol Evol 8:3640–3652
doi: 10.1093/gbe/evw135
Kojima K, Yamashita T, Imamoto Y, Kusakabe TG, Tsuda M, Shichida Y (2017) Evolutionary steps involving counterion displacement in a tunicate opsin. Proc Natl Acad Sci USA 114:6028–6033
doi: 10.1073/pnas.1701088114
Lamb TD (2009) Evolution of vertebrate retinal photoreception. Philos Trans R Soc Lond B Biol Sci 364:2911–2924
doi: 10.1098/rstb.2009.0102
Tsukamoto H, Farrens DL, Koyanagi M, Terakita A (2009) The magnitude of the light-induced conformational change in different rhodopsins correlates with their ability to activate G proteins. J Biol Chem 284:20676–20683
doi: 10.1074/jbc.M109.016212
Sato K, Yamashita T, Ohuchi H, Shichida Y (2011) Vertebrate ancient-long opsin has molecular properties intermediate between those of vertebrate and invertebrate visual pigments. Biochemistry 50:10484–10490
doi: 10.1021/bi201212z
Baldwin MW, Ko MC (2020) Functional evolution of vertebrate sensory receptors. Horm Behav 124:104771
doi: 10.1016/j.yhbeh.2020.104771
Passamaneck YJ, Furchheim N, Hejnol A, Martindale MQ, Luter C (2011) Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo 2:6
doi: 10.1186/2041-9139-2-6
Vocking O, Kourtesis I, Tumu SC, Hausen H (2017) Co-expression of xenopsin and rhabdomeric opsin in photoreceptors bearing microvilli and cilia. Elife 6:e23435. https://doi.org/10.7554/eLife.23435
doi: 10.7554/eLife.23435
pubmed: 28876222
pmcid: 5648526
Rawlinson KA, Lapraz F, Ballister ER, Terasaki M, Rodgers J, McDowell RJ, Girstmair J, Criswell KE, Boldogkoi M, Simpson F, Goulding D, Cormie C, Hall B, Lucas RJ, Telford MJ (2019) Extraocular, rod-like photoreceptors in a flatworm express xenopsin photopigment. Elife 8:e45465. https://doi.org/10.7554/eLife.45465
doi: 10.7554/eLife.45465
pubmed: 31635694
pmcid: 6805122
Doring CC, Kumar S, Tumu SC, Kourtesis I, Hausen H (2020) The visual pigment xenopsin is widespread in protostome eyes and impacts the view on eye evolution. Elife 9:e55193. https://doi.org/10.7554/eLife.55193
doi: 10.7554/eLife.55193
pubmed: 32880369
pmcid: 7529461
Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193–199
doi: 10.1016/0378-1119(91)90434-D
Motohashi K (2017) Seamless ligation cloning extract (SLiCE) method using cell lysates from laboratory Escherichia coli strains and its application to SLiP site-directed mutagenesis. Methods Mol Biol 1498:349–357
doi: 10.1007/978-1-4939-6472-7_23
Lamb TD (1995) Photoreceptor spectral sensitivities: common shape in the long-wavelength region. Vision Res 35:3083–3091
doi: 10.1016/0042-6989(95)00114-F
Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528
doi: 10.1017/S0952523800174036
Tsutsui K, Imai H, Shichida Y (2007) Photoisomerization efficiency in UV-absorbing visual pigments: protein-directed isomerization of an unprotonated retinal Schiff base. Biochemistry 46:6437–6445
doi: 10.1021/bi7003763
Bailes HJ, Lucas RJ (2013) Human melanopsin forms a pigment maximally sensitive to blue light (lambdamax approximately 479 nm) supporting activation of G(q/11) and G(i/o) signalling cascades. Proc Biol Sci 280:20122987
pubmed: 23554393
pmcid: 3619500
Yamashita T, Terakita A, Shichida Y (2000) Distinct roles of the second and third cytoplasmic loops of bovine rhodopsin in G protein activation. J Biol Chem 275:34272–34279
doi: 10.1074/jbc.M002954200
Yamashita T, Ohuchi H, Tomonari S, Ikeda K, Sakai K, Shichida Y (2010) Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. Proc Natl Acad Sci USA 107:22084–22089
doi: 10.1073/pnas.1012498107
Lee E, Linder ME, Gilman AG (1994) Expression of G-protein alpha subunits in Escherichia coli. Methods Enzymol 237:146–164
doi: 10.1016/S0076-6879(94)37059-1
Tachibanaki S, Imai H, Mizukami T, Okada T, Imamoto Y, Matsuda T, Fukada Y, Terakita A, Shichida Y (1997) Presence of two rhodopsin intermediates responsible for transducin activation. Biochemistry 36:14173–14180
doi: 10.1021/bi970932o
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
doi: 10.1016/j.jmb.2004.07.044
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 USA 100:9262–9267
doi: 10.1073/pnas.1531970100
Ludeke S, Beck M, Yan EC, Sakmar TP, Siebert F, Vogel R (2005) The role of Glu181 in the photoactivation of rhodopsin. J Mol Biol 353:345–356
doi: 10.1016/j.jmb.2005.08.039
Tsutsui K, Shichida Y (2010) Multiple functions of Schiff base counterion in rhodopsins. Photochem Photobiol Sci 9:1426–1434
doi: 10.1039/c0pp00134a
Terakita A, Yamashita T, Nimbari N, Kojima D, Shichida Y (2002) Functional interaction between bovine rhodopsin and G protein transducin. J Biol Chem 277:40–46
doi: 10.1074/jbc.M104960200
Matsuo R, Koyanagi M, Nagata A, Matsuo Y (2019) Co-expression of opsins in the eye photoreceptor cells of the terrestrial slug Limax valentianus. J Comp Neurol 527:3073–3086
doi: 10.1002/cne.24732
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
doi: 10.1038/nature09789