Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp

Nature Communications

Volumn 6, Issue , 2015, Pages

  Gao, Shiqiang ^a   Nagpal, Jatin ^b   Schneider, Martin W ^b   Kozjak Pavlovic, Vera ^a   Nagel, Georg ^a   Gottschalk, Alexander ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; GUANYLATE CYCLASE; OPSIN; CAENORHABDITIS ELEGANS PROTEIN; CARBON DIOXIDE; CYCLIC NUCLEOTIDE GATED CHANNEL; ION CHANNEL; OXYGEN; RHODOPSIN; TAX-2 PROTEIN, C ELEGANS; TAX-4 PROTEIN, C ELEGANS;

CARBON DIOXIDE; CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; NEMATODE; NEUROLOGY; SENSORY SYSTEM;

ARTICLE; BEHAVIOR; BLASTOCLADIELLA; BLASTOCLADIELLA EMERSONII; CAENORHABDITIS ELEGANS; CONDUCTANCE; CONTROLLED STUDY; DEPOLARIZATION; HETEROLOGOUS EXPRESSION; LIGHT; LIGHT INTENSITY; NONHUMAN; OOCYTE; OPTOGENETICS; PHOTOACTIVATION; SENSORY NERVE CELL; XENOPUS; ANIMAL; CHEMORECEPTOR CELL; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; HEK293 CELL LINE; HUMAN; METABOLISM; PATCH CLAMP TECHNIQUE; PROCEDURES;

ANIMALIA; BLASTOCLADIELLA EMERSONII; CAENORHABDITIS ELEGANS;

ANIMALS; BLASTOCLADIELLA; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARBON DIOXIDE; CHEMORECEPTOR CELLS; CYCLIC GMP; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; GUANYLATE CYCLASE; HEK293 CELLS; HUMANS; ION CHANNELS; LIGHT; MICROSCOPY, FLUORESCENCE; OOCYTES; OPSINS; OPTICAL IMAGING; OPTOGENETICS; OXYGEN; PATCH-CLAMP TECHNIQUES; RHODOPSIN; XENOPUS;

EID: 84941070059     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9046     Document Type: Article

References (56)

1. Fenno, L., Yizhar, O. & Deisseroth, K. The development and application of optogenetics. Annu. Rev. Neurosci. 34, 389-412 (2011).
2. Kramer, R. H., Mourot, A. & Adesnik, H. Optogenetic pharmacology for control of native neuronal signaling proteins. Nat. Neurosci. 16, 816-823 (2013).
3. Dugue, G. P., Akemann, W. & Knopfel, T. A comprehensive concept of optogenetics. Prog. Brain. Res. 196, 1-28 (2012).
4. Knopfel, T. et al. Toward the second generation of optogenetic tools. J. Neurosci. 30, 14998-15004 (2010).
5. Mei, Y. & Zhang, F. Molecular tools and approaches for optogenetics. Biol. Psychiatry 71, 1033-1038 (2012).
6. Bamann, C., Nagel, G. & Bamberg, E. Microbial rhodopsins in the spotlight. Curr. Opin. Neurobiol. 20, 610-616 (2010).
7. Zhang, F. et al. The microbial opsin family of optogenetic tools. Cell 147, 1446-1457 (2011).
8. Filipek, S., Stenkamp, R. E., Teller, D. C. & Palczewski, K. G protein-coupled receptor rhodopsin: a prospectus. Annu. Rev. Physiol. 65, 851-879 (2003).
9. Wensel, T. G. Signal transducing membrane complexes of photoreceptor outer segments. Vision. Res. 48, 2052-2061 (2008).
10. Shichida, Y. & Matsuyama, T. Evolution of opsins and phototransduction. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364, 2881-2895 (2009).
11. Hardie, R. C. & Franze, K. Photomechanical responses in Drosophila photoreceptors. Science 338, 260-263 (2012).
12. Oesterhelt, D. & Stoeckenius, W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nat. New. Biol. 233, 149-152 (1971).
13. Schobert, B. & Lanyi, J. K. Halorhodopsin is a light-driven chloride pump. J. Biol. Chem. 257, 10306-10313 (1982).
14. Spudich, E. N., Takahashi, T. & Spudich, J. L. Sensory rhodopsins I and II modulate a methylation/demethylation system in Halobacterium halobium phototaxis. Proc. Natl Acad. Sci. USA 86, 7746-7750 (1989).
15. Nagel, G. et al. Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296, 2395-2398 (2002).
16. Nagel, G. et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl Acad. Sci. USA 100, 13940-13945 (2003).
17. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268 (2005).
18. Nagel, G. et al. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15, 2279-2284 (2005).
19. Zhang, F. et al. Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639 (2007).
20. Kateriya, S., Nagel, G., Bamberg, E. & Hegemann, P. 'Vision' in single-celled algae. News. Physiol. Sci. 19, 133-137 (2004).
21. Schroder-Lang, S. et al. Fast manipulation of cellular cAMP level by light in vivo. Nat. Methods. 4, 39-42 (2007).
22. Stierl, M. et al. Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa. J. Biol. Chem. 286, 1181-1188 (2011).
23. Ryu, M. H., Moskvin, O. V., Siltberg-Liberles, J. & Gomelsky, M. Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J. Biol. Chem. 285, 41501-41508 (2010).
24. Weissenberger, S. et al. PACalpha - an optogenetic tool for in vivo manipulation of cellular cAMP levels, neurotransmitter release, and behavior in Caenorhabditis elegans. J. Neurochem. 116, 616-625 (2011).
25. Kim, T., Folcher, M., Baba, M. D. & Fussenegger, M. A synthetic erectile optogenetic stimulator enabling blue-light-inducible penile erection. Angew. Chem. Int. Ed. Engl. 54, 5933-5938 (2015).
26. Avelar, G. M. et al. A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr. Biol. 24, 1234-1240 (2014).
27. Coburn, C. M. & Bargmann, C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17, 695-706 (1996).
28. Komatsu, H., Mori, I., Rhee, J. S., Akaike, N. & Ohshima, Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17, 707-718 (1996).
29. Ullrich, S., Gueta, R. & Nagel, G. Degradation of channelopsin-2 in the absence of retinal and degradation resistance in certain mutants. Biol. Chem. 394, 271-280 (2013).
30. Linder, J. U. Class III adenylyl cyclases: molecular mechanisms of catalysis and regulation. Cell. Mol. Life. Sci. 63, 1736-1751 (2006).
31. Linder, J. U. & Schultz, J. E. The class III adenylyl cyclases: multi-purpose signalling modules. Cell. Signal. 15, 1081-1089 (2003).
32. Raffelberg, S. et al. A LOV-domain-mediated blue-light-activated adenylate (adenylyl) cyclase from the cyanobacterium Microcoleus chthonoplastes PCC 7420. Biochem. J. 455, 359-365 (2013).
33. Hu, C. D., Chinenov, Y. & Kerppola, T. K. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell. 9, 789-798 (2002).
34. Altenhofen, W. et al. Control of ligand specificity in cyclic nucleotide-gated channels from rod photoreceptors and olfactory epithelium. Proc. Natl Acad. Sci. USA 88, 9868-9872 (1991).
35. Komatsu, H. et al. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain. Res. 821, 160-168 (1999).
36. Ramot, D., MacInnis, B. L. & Goodman, M. B. Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat. Neurosci. 11, 908-915 (2008).
37. Liewald, J. F. et al. Optogenetic analysis of synaptic function. Nat. Methods. 5, 895-902 (2008).
38. AzimiHashemi, N. et al. Synthetic retinal analogues modify the spectral and kinetic characteristics of microbial rhodopsin optogenetic tools. Nat. Commun. 5, 5810 (2014).
39. Edwards, S. L. et al. A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol. 6, 0060198 (2008).
40. Bretscher, A. J., Busch, K. E. & de Bono, M. A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 105, 8044-8049 (2008).
41. Bretscher, A. J. et al. Temperature, oxygen, and salt-sensing neurons in C. elegans are carbon dioxide sensors that control avoidance behavior. Neuron 69, 1099-1113 (2011).
42. Zimmer, M. et al. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases. Neuron 61, 865-879 (2009).
43. Hallem, E. A. & Sternberg, P. W. Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 105, 8038-8043 (2008).
44. Swierczek, N. A., Giles, A. C., Rankin, C. H. & Kerr, R. A. High-throughput behavioral analysis in C. elegans. Nat. Methods. 8, 592-598 (2011).
45. Gasser, C. et al. Engineering of a red-light-activated human cAMP/cGMP-specific phosphodiesterase. Proc. Natl Acad. Sci. USA 111, 8803-8808 (2014).
46. Liu, S., Schulze, E. & Baumeister, R. Temperature- and touch-sensitive neurons couple CNG and TRPV channel activities to control heat avoidance in Caenorhabditis elegans. PLoS One 7, e32360 (2012).
47. Redemann, S. et al. Codon adaptation-based control of protein expression in C. elegans. Nat. Methods. 8, 250-252 (2011).
48. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
49. Fire, A. Integrative transformation of Caenorhabditis elegans. EMBO J. 5, 2673-2680 (1986).
50. Stirman, J. N., Crane, M. M., Husson, S. J., Gottschalk, A. & Lu, H. A multispectral optical illumination system with precise spatiotemporal control for the manipulation of optogenetic reagents. Nat. Protoc. 7, 207-220 (2012).
51. Stirman, J. N. et al. Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat. Methods. 8, 153-158 (2011).
52. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics. 23, 2947-2948 (2007).
53. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190 (2004).
54. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580 (2001).
55. Omasits, U., Ahrens, C. H., Muller, S. & Wollscheid, B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics. 30, 884-886 (2014).
56. Kall, L., Krogh, A. & Sonnhammer, E. L. A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 338, 1027-1036 (2004).