Molecular Properties and Optogenetic Applications of Enzymerhodopsins.
Cyclic nucleotide
Guanylate cyclase
Microbial rhodopsin
Phosphodiesterase
Signal transduction
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2021
2021
Historique:
entrez:
5
1
2021
pubmed:
6
1
2021
medline:
7
2
2021
Statut:
ppublish
Résumé
The cyclic nucleotides cAMP and cGMP are ubiquitous secondary messengers that regulate multiple biological functions including gene expression, differentiation, proliferation, and cell survival. In sensory neurons, cyclic nucleotides are responsible for signal modulation, amplification, and encoding. For spatial and temporal manipulation of cyclic nucleotide dynamics, optogenetics have a great advantage over pharmacological approaches. Enzymerhodopsins are a unique family of microbial rhodopsins. These molecules are made up of a membrane-embedded rhodopsin domain, which binds an all trans-retinal to form a chromophore, and a cytoplasmic water-soluble catalytic domain. To date, three kinds of molecules have been identified from lower eukaryotes such as fungi, algae, and flagellates. Among these, histidine kinase rhodopsin (HKR) is a light-inhibited guanylyl cyclase. Rhodopsin GC (Rh-GC) functions as a light-activated guanylyl cyclase, while rhodopsin PDE (Rh-PDE) functions as a light-activated phosphodiesterase that degrades cAMP and cGMP. These enzymerhodopsins have great potential in optogenetic applications for manipulating the intracellular cyclic nucleotide dynamics of living cells. Here we introduce the molecular function and applicability of these molecules.
Identifiants
pubmed: 33398812
doi: 10.1007/978-981-15-8763-4_9
doi:
Substances chimiques
Rhodopsins, Microbial
0
Cyclic AMP
E0399OZS9N
Phosphoric Diester Hydrolases
EC 3.1.4.-
Guanylate Cyclase
EC 4.6.1.2
Cyclic GMP
H2D2X058MU
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
153-165Références
Avelar GM, Schumacher RI, Zaini PA et al (2014) A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr Biol 24:1234–1240. https://doi.org/10.1016/j.cub.2014.04.009
doi: 10.1016/j.cub.2014.04.009
pubmed: 24835457
pmcid: 4046227
Bender AT, Beavo JA (2006) Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58:488–520. https://doi.org/10.1124/pr.58.3.5
doi: 10.1124/pr.58.3.5
pubmed: 16968949
Boyden ES, Zhang F, Bamberg E et al (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268. https://doi.org/10.1038/nn1525
doi: 10.1038/nn1525
pubmed: 16116447
Brunet T, Larson BT, Linden TA et al (2019) Light-regulated collective contractility in a multicellular choanoflagellate. Science 366:326–334. https://doi.org/10.1126/science.aay2346
doi: 10.1126/science.aay2346
pubmed: 31624206
Butryn A, Raza H, Rada H et al (2019) Molecular basis for GTP recognition by light-activated guanylate cyclase RhGC. FEBS J 287:2797. https://doi.org/10.1111/febs.15167
doi: 10.1111/febs.15167
pubmed: 31808997
pmcid: 7384201
Cai X (2012) Evolutionary genomics reveals the premetazoan origin of opposite gating polarity in animal-type voltage-gated ion channels. Genomics 99:241–245. https://doi.org/10.1016/j.ygeno.2012.01.007
doi: 10.1016/j.ygeno.2012.01.007
pubmed: 22326743
Deisseroth K, Hegemann P (2017) The form and function of channelrhodopsin. Science 357(6356):eaan5544. https://doi.org/10.1126/science.aan5544
Ernst OP, Sánchez Murcia PA, Daldrop P et al (2008) Photoactivation of channelrhodopsin. J Biol Chem 283:1637–1643. https://doi.org/10.1074/jbc.M708039200
doi: 10.1074/jbc.M708039200
pubmed: 17993465
Ernst OP, Lodowski DT, Elstner M et al (2014) Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem Rev 114:126–163. https://doi.org/10.1021/cr4003769
doi: 10.1021/cr4003769
pubmed: 24364740
Gao S, Nagpal J, Schneider MW et al (2015) Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp. Nat Commun 6:8046. https://doi.org/10.1038/ncomms9046
doi: 10.1038/ncomms9046
pubmed: 26345128
pmcid: 4569695
Gasser C, Taiber S, Yeh C-M et al (2014) Engineering of a red-light-activated human cAMP/cGMP-specific phosphodiesterase. Proc Natl Acad Sci U S A 111:8803–8808. https://doi.org/10.1073/pnas.1321600111
doi: 10.1073/pnas.1321600111
pubmed: 24889611
pmcid: 4066486
Govorunova EG, Sineshchekov OA, Li H, Spudich JL (2017) Microbial rhodopsins: diversity, mechanisms, and optogenetic applications. Annu Rev Biochem 86:845–872. https://doi.org/10.1146/annurev-biochem-101910-144233
doi: 10.1146/annurev-biochem-101910-144233
pubmed: 28301742
pmcid: 5747503
Gradinaru V, Zhang F, Ramakrishnan C et al (2010) Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141:154–165. https://doi.org/10.1016/j.cell.2010.02.037
doi: 10.1016/j.cell.2010.02.037
pubmed: 20303157
pmcid: 4160532
Hara KY, Wada T, Kino K et al (2013) Construction of photoenergetic mitochondria in cultured mammalian cells. Sci Rep 3:1–4. https://doi.org/10.1038/srep01635
doi: 10.1038/srep01635
Hegemann P (2008) Algal sensory photoreceptors. Annu Rev Plant Biol 59:167. https://doi.org/10.1146/annurev.arplant.59.032607.092847
doi: 10.1146/annurev.arplant.59.032607.092847
pubmed: 18444900
Inoue K, Ito S, Kato Y et al (2016) A natural light-driven inward proton pump. Nat Commun 7:13415. https://doi.org/10.1038/ncomms13415
doi: 10.1038/ncomms13415
pubmed: 27853152
pmcid: 5118547
Iseki M, Matsunaga S, Murakami A et al (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis. Nature 415:1047–1051. https://doi.org/10.1038/4151047a
doi: 10.1038/4151047a
pubmed: 11875575
Jansen V, Alvarez L, Balbach M et al (2015) Controlling fertilization and cAMP signaling in sperm by optogenetics. Elife 4:e05161. https://doi.org/10.7554/eLife.05161
doi: 10.7554/eLife.05161
pmcid: 4298566
Kateriya S, Nagel G, Bamberg E, Hegemann P (2004) “Vision” in single-celled algae. News Physiol Sci 19:133–137
pubmed: 15143209
Kato HE, Zhang F, Yizhar O et al (2012) Crystal structure of the channelrhodopsin light-gated cation channel. Nature 482:369–374. https://doi.org/10.1038/nature10870
doi: 10.1038/nature10870
pubmed: 22266941
pmcid: 4160518
Kawanabe A, Furutani Y, Jung KH, Kandori H (2007) Photochromism of Anabaena sensory rhodopsin. J Am Chem Soc 129:8644. https://doi.org/10.1021/ja072085a
doi: 10.1021/ja072085a
pubmed: 17569538
Kianianmomeni A, Hallmann A (2014) Transcriptional analysis of Volvox photoreceptors suggests the existence of different cell-type specific light-signaling pathways. Curr Genet 61:3. https://doi.org/10.1007/s00294-014-0440-3
doi: 10.1007/s00294-014-0440-3
pubmed: 25117716
Kumar RP, Morehouse BR, Fofana J et al (2017) Structure and monomer/dimer equilibrium for the guanylyl cyclase domain of the optogenetics protein RhoGC. J Biol Chem 292:21578–21589. https://doi.org/10.1074/jbc.M117.812685
doi: 10.1074/jbc.M117.812685
pubmed: 29118188
pmcid: 5766957
Lamarche LB, Kumar RP, Trieu MM et al (2017) Purification and characterization of RhoPDE, a retinylidene/phosphodiesterase fusion protein and potential optogenetic tool from the Choanoflagellate Salpingoeca rosetta. Biochemistry 56:5812–5822. https://doi.org/10.1021/acs.biochem.7b00519
doi: 10.1021/acs.biochem.7b00519
pubmed: 28976747
pmcid: 5685503
Linder JU (2006) Class III adenylyl cyclases: molecular mechanisms of catalysis and regulation. Cell Mol Life Sci 63:1736
doi: 10.1007/s00018-006-6072-0
Lindner R, Hartmann E, Tarnawski M et al (2017) Photoactivation mechanism of a bacterial light-regulated adenylyl cyclase. J Mol Biol 429:1336. https://doi.org/10.1016/j.jmb.2017.03.020
doi: 10.1016/j.jmb.2017.03.020
pubmed: 28336405
Luck M, Mathes T, Bruun S et al (2012) A photochromic histidine kinase rhodopsin (HKR1) that is bimodally switched by ultraviolet and blue light. J Biol Chem 287:40083–40090. https://doi.org/10.1074/jbc.M112.401604
doi: 10.1074/jbc.M112.401604
pubmed: 23027869
pmcid: 3501036
Mattis J, Tye KM, Ferenczi EA et al (2012) Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat Methods 9:159–172. https://doi.org/10.1038/nmeth.1808
doi: 10.1038/nmeth.1808
Ohki M, Sugiyama K, Kawai F et al (2016) Structural insight into photoactivation of an adenylate cyclase from a photosynthetic cyanobacterium. Proc Natl Acad Sci U S A 113:6659–6664. https://doi.org/10.1073/pnas.1517520113
doi: 10.1073/pnas.1517520113
pubmed: 27247413
pmcid: 4914150
Pandit J, Forman MD, Fennell KF et al (2009) Mechanism for the allosteric regulation of phosphodiesterase 2A deduced from the X-ray structure of a near full-length construct. Proc Natl Acad Sci U S A 106:18225–18230. https://doi.org/10.1073/pnas.0907635106
doi: 10.1073/pnas.0907635106
pubmed: 19828435
pmcid: 2775329
Penzkofer A, Luck M, Mathes T, Hegemann P (2014) Bistable retinal Schiff base photodynamics of histidine kinase rhodopsin HKR1 from chlamydomonas reinhardtii. Photochem Photobiol 90:773–785. https://doi.org/10.1111/php.12246
doi: 10.1111/php.12246
pubmed: 24460585
Pfeuty B, Thommen Q, Corellou F et al (2012) Circadian clocks in changing weather and seasons: lessons from the picoalga ostreococcus tauri. BioEssays 34:781
doi: 10.1002/bies.201200012
Prakash R, Yizhar O, Grewe B et al (2012) Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nat Methods 9:1171. https://doi.org/10.1038/nmeth.2215
doi: 10.1038/nmeth.2215
pubmed: 23169303
pmcid: 5734860
Raffelberg S, Wang L, Gao S et al (2013) A LOV-domain-mediated blue-light-activated adenylate (adenylyl) cyclase from the cyanobacterium Microcoleus chthonoplastes PCC 7420. Biochem J 455:359. https://doi.org/10.1042/BJ20130637
doi: 10.1042/BJ20130637
pubmed: 24112109
Ryu MH, Moskvin OV, Siltberg-Liberles J, Gomelsky M (2010) Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J Biol Chem 285:41501–41508. https://doi.org/10.1074/jbc.M110.177600
doi: 10.1074/jbc.M110.177600
pubmed: 21030591
pmcid: 3009876
Scheib U, Stehfest K, Gee CE et al (2015) The rhodopsin – guanylyl cyclase of the aquatic fungus Blastocladiella emersonii enables fast optical control of cGMP signaling. Sci Signal 8:1–9
doi: 10.1126/scisignal.aab0611
Scheib U, Broser M, Constantin OM, et al (2018) Rhodopsin-cyclases for photocontrol of cGMP/cAMP and 2.3 Å structure of the adenylyl cyclase domain. Nat Commun 9. https://doi.org/10.1038/s41467-018-04428-w
Schneider F, Grimm C, Hegemann P (2015) Biophysics of Channelrhodopsin. Annu Rev Biophys 44:167–186. https://doi.org/10.1146/annurev-biophys-060414-034014
doi: 10.1146/annurev-biophys-060414-034014
pubmed: 26098512
Steegborn C (2014) Structure, mechanism, and regulation of soluble adenylyl cyclases—similarities and differences to transmembrane adenylyl cyclases. Biochim Biophys Acta Mol Basis Dis 1842:2535
doi: 10.1016/j.bbadis.2014.08.012
Steuer Costa W, S chieh Y, Liewald JF, Gottschalk A (2017) Fast cAMP modulation of neurotransmission via neuropeptide signals and vesicle loading. Curr Biol 27:495. https://doi.org/10.1016/j.cub.2016.12.055
doi: 10.1016/j.cub.2016.12.055
pubmed: 28162892
Stierl M, Stumpf P, Udwari D et al (2011) Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa. J Biol Chem 286:1181–1188. https://doi.org/10.1074/jbc.M110.185496
doi: 10.1074/jbc.M110.185496
pubmed: 21030594
Sugiura M, Tsunoda SP, Hibi M, Kandori H (2020) Molecular properties of new enzyme rhodopsins with phosphodiesterase activity. https://doi.org/10.1021/acsomega.0c01113
Sunahara RK, Beuve A, Tesmer JJG et al (1998) Exchange of substrate and inhibitor specificities between adenylyl and guanylyl cyclases. J Biol Chem 273:16332. https://doi.org/10.1074/jbc.273.26.16332
doi: 10.1074/jbc.273.26.16332
pubmed: 9632695
Tian Y, Gao S, Heyde EL et al (2018a) Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases. BMC Biol 16:1–18. https://doi.org/10.1186/s12915-018-0613-5
doi: 10.1186/s12915-018-0613-5
Tian Y, Gao S, Yang S, Nagel G (2018b) A novel rhodopsin phosphodiesterase from Salpingoeca rosetta shows light-enhanced substrate affinity. Biochem J 475:1121. https://doi.org/10.1042/BCJ20180010
doi: 10.1042/BCJ20180010
pubmed: 29483295
Trieu MM, Devine EL, Lamarche LB et al (2017) Expression, purification, and spectral tuning of RhoGC, a retinylidene/guanylyl cyclase fusion protein and optogenetics tool from the aquatic fungus Blastocladiella emersonii. J Biol Chem 292:10379–10389. https://doi.org/10.1074/jbc.M117.789636
doi: 10.1074/jbc.M117.789636
pubmed: 28473465
pmcid: 5481551
Tucker CL, Hurley JH, Miller TR, Hurley JB (1998) Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase. Proc Natl Acad Sci U S A 95:5993–5997. https://doi.org/10.1073/pnas.95.11.5993
doi: 10.1073/pnas.95.11.5993
pubmed: 9600905
pmcid: 27573
Volkov O, Kovalev K, Polovinkin V et al (2017) Structural insights into ion conduction by channelrhodopsin 2. Science (80-) 358:eaan8862. https://doi.org/10.1126/science.aan8862
doi: 10.1126/science.aan8862
Wang H, Liu Y, Hou J et al (2007) Structural insight into substrate specificity of phosphodiesterase 10. Proc Natl Acad Sci U S A 104:5782–5787. https://doi.org/10.1073/pnas.0700279104
doi: 10.1073/pnas.0700279104
pubmed: 17389385
pmcid: 1851569
Watari M, Ikuta T, Yamada D et al (2019) Spectroscopic study of the transmembrane domain of a rhodopsin–phosphodiesterase fusion protein from a unicellular eukaryote. J Biol Chem 294:3432. https://doi.org/10.1074/jbc.RA118.006277
doi: 10.1074/jbc.RA118.006277
pubmed: 30622140
pmcid: 6416415
Yoshida K, Tsunoda SP, Brown LS, Kandori H (2017) A unique choanoflagellate enzyme rhodopsin exhibits lightdependent cyclic nucleotide phosphodiesterase activity. J Biol Chem 292:7531–7541. https://doi.org/10.1074/jbc.M117.775569
doi: 10.1074/jbc.M117.775569
pubmed: 28302718
pmcid: 5418051
Zhang F, Vierock J, Yizhar O et al (2011) The microbial opsin family of optogenetic tools. Cell 147:1446–1457. https://doi.org/10.1016/j.cell.2011.12.004
doi: 10.1016/j.cell.2011.12.004
pubmed: 22196724
pmcid: 4166436
Zhou Z, Tanaka KF, Matsunaga S et al (2016) Photoactivated adenylyl cyclase (PAC) reveals novel mechanisms underlying cAMP-dependent axonal morphogenesis. Sci Rep 5:19679. https://doi.org/10.1038/srep19679
doi: 10.1038/srep19679
pubmed: 26795422
pmcid: 4726437
Ziegler M, Bassler J, Beltz S et al (2017) Characterization of a novel signal transducer element intrinsic to class IIIa/b adenylate cyclases and guanylate cyclases. FEBS J 284:1204. https://doi.org/10.1111/febs.14047
doi: 10.1111/febs.14047
pubmed: 28222489