Transient protonation changes in channelrhodopsin-2 and their relevance to channel gating

Lorenz-Fonfria VA, Resler T, Krause N, Nack M, Gossing M, Fischer von Mollard G, Bamann C, Bamberg E, Schlesinger R, Heberle J (2013)
Proceedings Of The National Academy Of Sciences 110(14): E1273-E1281.

Download
No fulltext has been uploaded. References only!
Journal Article | Original Article | Published | English

No fulltext has been uploaded

Author
; ; ; ; ; ; ; ; ;
Abstract
The discovery of the light-gated ion channel channelrhodopsin (ChR) set the stage for the novel field of optogenetics, where cellular processes are controlled by light. However, the underlying molecular mechanism of light-induced cation permeation in ChR2 remains unknown. Here, we have traced the structural changes of ChR2 by time-resolved FTIR spectroscopy, complemented by functional electrophysiological measurements. We have resolved the vibrational changes associated with the open states of the channel (P-2(390) and P-3(520)) and characterized several proton transfer events. Analysis of the amide I vibrations suggests a transient increase in hydration of transmembrane a-helices with a t(1/2) = 60 mu s, which tallies with the onset of cation permeation. Aspartate 253 accepts the proton released by the Schiff base (t(1/2) = 10 mu s), with the latter being reprotonated by aspartic acid 156 (t(1/2) = 2 ms). The internal proton acceptor and donor groups, corresponding to D212 and D115 in bacteriorhodopsin, are clearly different from other microbial rhodopsins, indicating that their spatial position in the protein was relocated during evolution. Previous conclusions on the involvement of glutamic acid 90 in channel opening are ruled out by demonstrating that E90 deprotonates exclusively in the nonconductive P-4(480) state. Our results merge into a mechanistic proposal that relates the observed proton transfer reactions and the protein conformational changes to the gating of the cation channel.
Publishing Year
ISSN
eISSN
PUB-ID

Cite this

Lorenz-Fonfria VA, Resler T, Krause N, et al. Transient protonation changes in channelrhodopsin-2 and their relevance to channel gating. Proceedings Of The National Academy Of Sciences. 2013;110(14):E1273-E1281.
Lorenz-Fonfria, V. A., Resler, T., Krause, N., Nack, M., Gossing, M., Fischer von Mollard, G., Bamann, C., et al. (2013). Transient protonation changes in channelrhodopsin-2 and their relevance to channel gating. Proceedings Of The National Academy Of Sciences, 110(14), E1273-E1281. doi:10.1073/pnas.1219502110
Lorenz-Fonfria, V. A., Resler, T., Krause, N., Nack, M., Gossing, M., Fischer von Mollard, G., Bamann, C., Bamberg, E., Schlesinger, R., and Heberle, J. (2013). Transient protonation changes in channelrhodopsin-2 and their relevance to channel gating. Proceedings Of The National Academy Of Sciences 110, E1273-E1281.
Lorenz-Fonfria, V.A., et al., 2013. Transient protonation changes in channelrhodopsin-2 and their relevance to channel gating. Proceedings Of The National Academy Of Sciences, 110(14), p E1273-E1281.
V.A. Lorenz-Fonfria, et al., “Transient protonation changes in channelrhodopsin-2 and their relevance to channel gating”, Proceedings Of The National Academy Of Sciences, vol. 110, 2013, pp. E1273-E1281.
Lorenz-Fonfria, V.A., Resler, T., Krause, N., Nack, M., Gossing, M., Fischer von Mollard, G., Bamann, C., Bamberg, E., Schlesinger, R., Heberle, J.: Transient protonation changes in channelrhodopsin-2 and their relevance to channel gating. Proceedings Of The National Academy Of Sciences. 110, E1273-E1281 (2013).
Lorenz-Fonfria, Victor A., Resler, Tom, Krause, Nils, Nack, Melanie, Gossing, Michael, Fischer von Mollard, Gabriele, Bamann, Christian, Bamberg, Ernst, Schlesinger, Ramona, and Heberle, Joachim. “Transient protonation changes in channelrhodopsin-2 and their relevance to channel gating”. Proceedings Of The National Academy Of Sciences 110.14 (2013): E1273-E1281.
This data publication is cited in the following publications:
This publication cites the following data publications:

48 Citations in Europe PMC

Data provided by Europe PubMed Central.

Light-induced helix movements in channelrhodopsin-2.
Müller M, Bamann C, Bamberg E, Kühlbrandt W., J Mol Biol 427(2), 2015
PMID: 25451024
Comparison of the structural changes occurring during the primary phototransition of two different channelrhodopsins from Chlamydomonas algae.
Ogren JI, Yi A, Mamaev S, Li H, Lugtenburg J, DeGrip WJ, Spudich JL, Rothschild KJ., Biochemistry 54(2), 2015
PMID: 25469620
Considering optogenetic stimulation for cochlear implants.
Jeschke M, Moser T., Hear Res 322(), 2015
PMID: 25601298
Kinetic evaluation of photosensitivity in bi-stable variants of chimeric channelrhodopsins.
Hososhima S, Sakai S, Ishizuka T, Yawo H., PLoS One 10(3), 2015
PMID: 25789474
Chimeras of channelrhodopsin-1 and -2 from Chlamydomonas reinhardtii exhibit distinctive light-induced structural changes from channelrhodopsin-2.
Inaguma A, Tsukamoto H, Kato HE, Kimura T, Ishizuka T, Oishi S, Yawo H, Nureki O, Furutani Y., J Biol Chem 290(18), 2015
PMID: 25796616
Platymonas subcordiformis Channelrhodopsin-2 Function: I. THE PHOTOCHEMICAL REACTION CYCLE.
Szundi I, Li H, Chen E, Bogomolni R, Spudich JL, Kliger DS., J Biol Chem 290(27), 2015
PMID: 25971972
Mechanism divergence in microbial rhodopsins.
Spudich JL, Sineshchekov OA, Govorunova EG., Biochim Biophys Acta 1837(5), 2014
PMID: 23831552
Of ion pumps, sensors and channels - perspectives on microbial rhodopsins between science and history.
Grote M, Engelhard M, Hegemann P., Biochim Biophys Acta 1837(5), 2014
PMID: 23994288
The role of protein-bound water molecules in microbial rhodopsins.
Gerwert K, Freier E, Wolf S., Biochim Biophys Acta 1837(5), 2014
PMID: 24055285
Proteorhodopsin.
Bamann C, Bamberg E, Wachtveitl J, Glaubitz C., Biochim Biophys Acta 1837(5), 2014
PMID: 24060527
Channelrhodopsin unchained: structure and mechanism of a light-gated cation channel.
Lórenz-Fonfría VA, Heberle J., Biochim Biophys Acta 1837(5), 2014
PMID: 24212055
Channelrhodopsins: a bioinformatics perspective.
Del Val C, Royuela-Flor J, Milenkovic S, Bondar AN., Biochim Biophys Acta 1837(5), 2014
PMID: 24252597
Philosophy of voltage-gated proton channels.
DeCoursey TE, Hosler J., J R Soc Interface 11(92), 2014
PMID: 24352668
Microbial and animal rhodopsins: structures, functions, and molecular mechanisms.
Ernst OP, Lodowski DT, Elstner M, Hegemann P, Brown LS, Kandori H., Chem Rev 114(1), 2014
PMID: 24364740
Conversion of channelrhodopsin into a light-gated chloride channel.
Wietek J, Wiegert JS, Adeishvili N, Schneider F, Watanabe H, Tsunoda SP, Vogt A, Elstner M, Oertner TG, Hegemann P., Science 344(6182), 2014
PMID: 24674867
Role of a helix B lysine residue in the photoactive site in channelrhodopsins.
Li H, Govorunova EG, Sineshchekov OA, Spudich JL., Biophys J 106(8), 2014
PMID: 24739160
Resonance Raman and FTIR spectroscopic characterization of the closed and open states of channelrhodopsin-1.
Muders V, Kerruth S, Lórenz-Fonfría VA, Bamann C, Heberle J, Schlesinger R., FEBS Lett 588(14), 2014
PMID: 24859039
Retinal chromophore structure and Schiff base interactions in red-shifted channelrhodopsin-1 from Chlamydomonas augustae.
Ogren JI, Mamaev S, Russano D, Li H, Spudich JL, Rothschild KJ., Biochemistry 53(24), 2014
PMID: 24869998
Mycobacterium tuberculosis alters the metalloprotease activity of the COP9 signalosome.
Danelishvili L, Babrak L, Rose SJ, Everman J, Bermudez LE., MBio 5(4), 2014
PMID: 25139900
Light-induced movement of the transmembrane helix B in channelrhodopsin-2.
Sattig T, Rickert C, Bamberg E, Steinhoff HJ, Bamann C., Angew Chem Int Ed Engl 52(37), 2013
PMID: 23893661
Structural differences between the closed and open states of channelrhodopsin-2 as observed by EPR spectroscopy.
Krause N, Engelhard C, Heberle J, Schlesinger R, Bittl R., FEBS Lett 587(20), 2013
PMID: 24036447

Export

0 Marked Publications

Open Data PUB

Web of Science

View record in Web of Science®

Sources

PMID: 23509282
PubMed | Europe PMC

Search this title in

Google Scholar