Conversion of Microbial Rhodopsins: Insights into Functionally Essential Elements and Rational Protein Engineering

Overview

Journal Biophys Rev

Publisher Springer

Specialty Biophysics

Date 2017 Nov 28

PMID 29178082

Citations 8

Authors

Akimasa Kaneko

Keiichi Inoue

Keiichi Kojima

Hideki Kandori

Yuki Sudo

Affiliations

Soon will be listed here.

Abstract

Technological progress has enabled the successful application of functional conversion to a variety of biological molecules, such as nucleotides and proteins. Such studies have revealed the functionally essential elements of these engineered molecules, which are difficult to characterize at the level of an individual molecule. The functional conversion of biological molecules has also provided a strategy for their rational and atomistic design. The engineered molecules can be used in studies to improve our understanding of their biological functions and to develop protein-based tools. In this review, we introduce the functional conversion of membrane-embedded photoreceptive retinylidene proteins (also called rhodopsins) and discuss these proteins mainly on the basis of results obtained from our own studies. This information provides insights into the molecular mechanism of light-induced protein functions and their use in optogenetics, a technology which involves the use of light to control biological activities.

Citing Articles

Solid-state NMR for the characterization of retinal chromophore and Schiff base in TAT rhodopsin embedded in membranes under weakly acidic conditions.

Arikawa S, Sugimoto T, Okitsu T, Wada A, Katayama K, Kandori H Biophys Physicobiol. 2024; 20(Supplemental):e201017.

PMID: 38362323 PMC: 10865839. DOI: 10.2142/biophysico.bppb-v20.s017.

Recent advances in signaling and activation mechanism in microbial rhodopsins: Report for the session 6 at the 19 International Conference on Retinal Proteins.

Shimono K, Dencher N Biophys Physicobiol. 2024; 20(Supplemental):e201009.

PMID: 38362314 PMC: 10865883. DOI: 10.2142/biophysico.bppb-v20.s009.

Microbial Rhodopsins.

Gordeliy V, Kovalev K, Bamberg E, Rodriguez-Valera F, Zinovev E, Zabelskii D Methods Mol Biol. 2022; 2501:1-52.

PMID: 35857221 DOI: 10.1007/978-1-0716-2329-9_1.

Rhodopsins: An Excitingly Versatile Protein Species for Research, Development and Creative Engineering.

de Grip W, Ganapathy S Front Chem. 2022; 10:879609.

PMID: 35815212 PMC: 9257189. DOI: 10.3389/fchem.2022.879609.

Exploring the Retinal Binding Cavity of Archaerhodopsin-3 by Replacing the Retinal Chromophore With a Dimethyl Phenylated Derivative.

Tsuneishi T, Takahashi M, Tsujimura M, Kojima K, Ishikita H, Takeuchi Y Front Mol Biosci. 2022; 8:794948.

PMID: 34988122 PMC: 8721008. DOI: 10.3389/fmolb.2021.794948.

References

Inoue K, Nomura Y, Kandori H . Asymmetric Functional Conversion of Eubacterial Light-driven Ion Pumps. J Biol Chem. 2016; 291(19):9883-93. PMC: 4858992. DOI: 10.1074/jbc.M116.716498. View

Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P . Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A. 2003; 100(24):13940-5. PMC: 283525. DOI: 10.1073/pnas.1936192100. View

Hoff W, Jung K, Spudich J . Molecular mechanism of photosignaling by archaeal sensory rhodopsins. Annu Rev Biophys Biomol Struct. 1997; 26:223-58. DOI: 10.1146/annurev.biophys.26.1.223. View

Sudo Y, Spudich J . Three strategically placed hydrogen-bonding residues convert a proton pump into a sensory receptor. Proc Natl Acad Sci U S A. 2006; 103(44):16129-34. PMC: 1637548. DOI: 10.1073/pnas.0607467103. View

Mogi T, Stern L, Marti T, Chao B, Khorana H . Aspartic acid substitutions affect proton translocation by bacteriorhodopsin. Proc Natl Acad Sci U S A. 1988; 85(12):4148-52. PMC: 280383. DOI: 10.1073/pnas.85.12.4148. View

Ito S, Kato H, Taniguchi R, Iwata T, Nureki O, Kandori H . Water-containing hydrogen-bonding network in the active center of channelrhodopsin. J Am Chem Soc. 2014; 136(9):3475-82. DOI: 10.1021/ja410836g. View

Takahashi T, Mochizuki Y, Kamo N, Kobatake Y . Evidence that the long-lifetime photointermediate of s-rhodopsin is a receptor for negative phototaxis in Halobacterium halobium. Biochem Biophys Res Commun. 1985; 127(1):99-105. DOI: 10.1016/s0006-291x(85)80131-5. View

Ogren J, Mamaev S, Russano D, Li H, Spudich J, Rothschild K . Retinal chromophore structure and Schiff base interactions in red-shifted channelrhodopsin-1 from Chlamydomonas augustae. Biochemistry. 2014; 53(24):3961-70. PMC: 4072394. DOI: 10.1021/bi500445c. View

Inoue K, Kato Y, Kandori H . Light-driven ion-translocating rhodopsins in marine bacteria. Trends Microbiol. 2014; 23(2):91-8. DOI: 10.1016/j.tim.2014.10.009. View

10.

Koyanagi M, Terakita A . Gq-coupled rhodopsin subfamily composed of invertebrate visual pigment and melanopsin. Photochem Photobiol. 2008; 84(4):1024-30. DOI: 10.1111/j.1751-1097.2008.00369.x. View

11.

Kato H, Kamiya M, Sugo S, Ito J, Taniguchi R, Orito A . Atomistic design of microbial opsin-based blue-shifted optogenetics tools. Nat Commun. 2015; 6:7177. PMC: 4479019. DOI: 10.1038/ncomms8177. View

12.

Sudo Y, Ihara K, Kobayashi S, Suzuki D, Irieda H, Kikukawa T . A microbial rhodopsin with a unique retinal composition shows both sensory rhodopsin II and bacteriorhodopsin-like properties. J Biol Chem. 2010; 286(8):5967-76. PMC: 3057805. DOI: 10.1074/jbc.M110.190058. View

13.

Muders V, Kerruth S, Lorenz-Fonfria V, Bamann C, Heberle J, Schlesinger R . Resonance Raman and FTIR spectroscopic characterization of the closed and open states of channelrhodopsin-1. FEBS Lett. 2014; 588(14):2301-6. DOI: 10.1016/j.febslet.2014.05.019. View

14.

Shibata M, Yamashita H, Uchihashi T, Kandori H, Ando T . High-speed atomic force microscopy shows dynamic molecular processes in photoactivated bacteriorhodopsin. Nat Nanotechnol. 2010; 5(3):208-12. DOI: 10.1038/nnano.2010.7. View

15.

Suzuki D, Furutani Y, Inoue K, Kikukawa T, Sakai M, Fujii M . Effects of chloride ion binding on the photochemical properties of salinibacter sensory rhodopsin I. J Mol Biol. 2009; 392(1):48-62. DOI: 10.1016/j.jmb.2009.06.050. View

16.

Lin J, Knutsen P, Muller A, Kleinfeld D, Tsien R . ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat Neurosci. 2013; 16(10):1499-508. PMC: 3793847. DOI: 10.1038/nn.3502. View

17.

Varo G, Brown L, Sasaki J, Kandori H, Maeda A, Needleman R . Light-driven chloride ion transport by halorhodopsin from Natronobacterium pharaonis. 1. The photochemical cycle. Biochemistry. 1995; 34(44):14490-9. DOI: 10.1021/bi00044a027. View

18.

Schobert B, Lanyi J . Halorhodopsin is a light-driven chloride pump. J Biol Chem. 1982; 257(17):10306-13. View

19.

Hou S, Govorunova E, Ntefidou M, Lane C, Spudich E, Sineshchekov O . Diversity of Chlamydomonas channelrhodopsins. Photochem Photobiol. 2011; 88(1):119-28. PMC: 3253254. DOI: 10.1111/j.1751-1097.2011.01027.x. View

20.

Sasaki J, Brown L, Chon Y, Kandori H, Maeda A, Needleman R . Conversion of bacteriorhodopsin into a chloride ion pump. Science. 1995; 269(5220):73-5. DOI: 10.1126/science.7604281. View