Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-84b7d79bbc-rnpqb Total loading time: 0 Render date: 2024-07-26T12:27:53.889Z Has data issue: false hasContentIssue false

10 - Photoactivatable Nucleotide Cyclases for Synthetic Photobiology Applications

from Part II - Opsin Biology, Tools, and Technology Platform

Published online by Cambridge University Press:  28 April 2017

By
Marc Folcher
Edited by
Krishnarao Appasani
Krishnarao Appasani
Affiliation:
GeneExpression Systems, Inc., Massachusetts
Get access
Type
Chapter
Information
Optogenetics
From Neuronal Function to Mapping and Disease Biology
 , pp. 132 - 150
Publisher: Cambridge University Press
Print publication year: 2017

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdul-Sater, A.A., Grajkowski, A., Erdjument-Bromage, H., Plumlee, C., Levi, A., Schreiber, M.T., Lee, C., Shuman, H., Beaucage, S.L., and Schindler, C. (2012). The overlapping host responses to bacterial cyclic dinucleotides. Microbes Infect, 14, 188–97.CrossRefGoogle ScholarPubMed
Airan, R.D., Thompson, K.R., Fenno, L.E., Bernstein, H., and Deisseroth, K. (2009). Temporally precise in vivo control of intracellular signalling. Nature, 458, 1025–9.CrossRefGoogle ScholarPubMed
Arrenberg, A.B., Stainier, D.Y., Baier, H., and Huisken, J. (2010). Optogenetic control of cardiac function. Science, 330, 971–4.CrossRefGoogle ScholarPubMed
Auslander, S., Wieland, M., and Fussenegger, M. (2012). Smart medication through combination of synthetic biology and cell microencapsulation. Metab Eng, 14, 252–60.CrossRefGoogle ScholarPubMed
Bagheri, A., Gabran, S.R., Salam, M.T., Perez Velazquez, J.L., Mansour, R.R., Salama, M.M., and Genov, R. (2013). Massively-parallel neuromonitoring and neurostimulation rodent headset with nanotextured flexible microelectrodes. IEEE Trans Biomed Circuits Syst, 7, 601–9.CrossRefGoogle ScholarPubMed
Bailes, H.J., Zhuang, L.Y., and Lucas, R.J. (2012). Reproducible and sustained regulation of Galphas signalling using a metazoan opsin as an optogenetic tool. PLoS One, 7, e30774.CrossRefGoogle Scholar
Basar, M.R., Ahmad, M.Y., Cho, J., and Ibrahim, F. (2014). Application of wireless power transmission systems in wireless capsule endoscopy: an overview. Sensors (Basel), 14, 10929–51.CrossRefGoogle Scholar
Baumann, P., Spulber, M., Dinu, I.A., and Palivan, C.G. (2014). Cellular Trojan horse based polymer nanoreactors with light-sensitive activity. J. Phys. Chem. B, 118, 9361–70.CrossRefGoogle ScholarPubMed
Bellmann, D., Richardt, A., Freyberger, R., Nuwal, N., Schwarzel, M., Fiala, A., and Stortkuhl, K.F. (2010). Optogenetically induced olfactory stimulation in Drosophila larvae reveals the neuronal basis of odor-aversion behavior. Front. Behav. Neurosci., 4, 27.CrossRefGoogle ScholarPubMed
Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G., and Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci., 8, 1263–8.CrossRefGoogle ScholarPubMed
Bruegmann, T., Malan, D., Hesse, M., Beiert, T., Fuegemann, C.J., Fleischmann, B.K., and Sasse, P. (2010). Optogenetic control of heart muscle in vitro and in vivo. Nat Methods, 7, 897–900.CrossRefGoogle Scholar
Bucher, D. and Buchner, E. (2009). Stimulating PACalpha increases miniature excitatory junction potential frequency at the Drosophila neuromuscular junction. J. Neurogenet., 23, 220–4.CrossRefGoogle ScholarPubMed
Bugaj, L.J., Choksi, A.T., Mesuda, C.K., Kane, R.S., and Schaffer, D.V. (2013). Optogenetic protein clustering and signaling activation in mammalian cells. Nat Methods, 10, 249–52.CrossRefGoogle ScholarPubMed
Cao, Z., Livoti, E., Losi, A., and Gartner, W. (2010). A blue light-inducible phosphodiesterase activity in the cyanobacterium Synechococcus elongatus. Photochem. Photobiol., 86, 606–11.CrossRefGoogle ScholarPubMed
Chen, Z.H., Raffelberg, S., Losi, A., Schaap, P., and Gartner, W. (2014). A cyanobacterial light activated adenylyl cyclase partially restores development of a Dictyostelium discoideum, adenylyl cyclase a null mutant. J. Biotechnol., 191, 246–9.CrossRefGoogle Scholar
Christen, M., Kulasekara, H.D., Christen, B., Kulasekara, B.R., Hoffman, L.R., and Miller, S.I. (2010). Asymmetrical distribution of the second messenger c-di-GMP upon bacterial cell division. Science, 328, 1295–7.CrossRefGoogle ScholarPubMed
Clement, R.G., Bugler, K.E., and Oliver, C.W. (2011). Bionic prosthetic hands: a review of present technology and future aspirations. Surgeon, 9, 336–40.CrossRefGoogle Scholar
Daly, J.J. and Wolpaw, J.R. (2008). Brain–computer interfaces in neurological rehabilitation. Lancet Neurol, 7, 1032–43.CrossRefGoogle ScholarPubMed
Diring, S., Wang, D.O., Kim, C., Kondo, M., Chen, Y., Kitagawa, S., Kamei, K., and Furukawa, S. (2013). Localized cell stimulation by nitric oxide using a photoactive porous coordination polymer platform. Nat Commun, 4, 2684.CrossRefGoogle ScholarPubMed
Efetova, M., Petereit, L., Rosiewicz, K., Overend, G., Haussig, F., Hovemann, B.T., Cabrero, P., Dow, J.A., and Schwarzel, M. (2013). Separate roles of PKA and EPAC in renal function unraveled by the optogenetic control of cAMP levels in vivo. J. Cell Sci., 126, 778–88.Google ScholarPubMed
Enomoto, G., Ni-Ni-Win, R. Narikawa, and Ikeuchi, M. (2015). Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation. Proc. Natl. Acad. Sci. U. S. A., 112, 8082–7.CrossRefGoogle Scholar
Escalante, C.R., Nistal-Villan, E., Shen, L., Garcia-Sastre, A., and Aggarwal, A.K. (2007). Structure of IRF-3 bound to the PRDIII-I regulatory element of the human interferon-beta enhancer. Mol Cell, 26, 703–16.CrossRefGoogle Scholar
Folcher, M., Oesterle, S., Zwicky, K., Thekkottil, T., Heymoz, J., Hohmann, M., Christen, M., Daoud El-Baba, M., Buchmann, P., and Fussenegger, M. (2014). Mind-controlled transgene expression by a wireless-powered optogenetic designer cell implant. Nat Commun, 5, 5392.CrossRefGoogle ScholarPubMed
Galan, F., Nuttin, M., Lew, E., Ferrez, P.W., Vanacker, G., Philips, J., and Millan Jdel, R. (2008). A brain-actuated wheelchair: asynchronous and non-invasive brain–computer interfaces for continuous control of robots. Clin Neurophysiol, 119, 2159–69.CrossRefGoogle ScholarPubMed
Gasser, C., Taiber, S., Yeh, C.M., Wittig, C.H., Hegemann, P., Ryu, S., Wunder, F., and Moglich, A. (2014). Engineering of a red-light-activated human cAMP/cGMP-specific phosphodiesterase. Proc. Natl. Acad. Sci. U. S. A., 111, 8803–8.CrossRefGoogle ScholarPubMed
Gomelsky, M. (2011). cAMP, c-di-GMP, c-di-AMP and now cGMP: bacteria use them all! Mol. Microbiol., 79, 562–5.CrossRefGoogle Scholar
Gomelsky, M. and Klug, G. (2002). BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem. Sci., 27, 497–500.CrossRefGoogle ScholarPubMed
Guenther, T., Lovell, N.H., and Suaning, G.J. (2012). Bionic vision: system architectures: a review. Expert Rev. Med. Devices, 9, 33–48.CrossRefGoogle Scholar
Gutierrez-Triana, J.A., Herget, U., Castillo-Ramirez, L.A., Lutz, M., Yeh, C.M., De Marco, R.J., and Ryu, S. (2015). Manipulation of interrenal cell function in developing zebrafish using genetically targeted ablation and an optogenetic tool. Endocrinology, 156, 3394–401.CrossRefGoogle Scholar
Hartmann, A., Arroyo-Olarte, R.D., Imkeller, K., Hegemann, P., Lucius, R., and Gupta, N. (2013). Optogenetic modulation of an adenylate cyclase in Toxoplasma gondii demonstrates a requirement of the parasite cAMP for host-cell invasion and stage differentiation. J. Biol. Chem., 288, 13705–17.CrossRefGoogle ScholarPubMed
He, J., Zhang, P., Babu, T., Liu, Y., Gong, J., and Nie, Z. (2013). Near-infrared light-responsive vesicles of Au nanoflowers. Chem. Commun. (Camb.), 49, 576–8.Google ScholarPubMed
Herrou, J. and Crosson, S. (2011). Function, structure and mechanism of bacterial photosensory LOV proteins. Nat. Rev. Microbiol., 9, 713–23.CrossRefGoogle ScholarPubMed
Ieda, N., Hotta, Y., Miyata, N., Kimura, K., and Nakagawa, H. (2014). Photomanipulation of vasodilation with a blue-light-controllable nitric oxide releaser. J. Am. Chem. Soc., 136, 7085–91.CrossRefGoogle ScholarPubMed
Jansen, V., Alvarez, L., Balbach, M., Strunker, T., Hegemann, P., Kaupp, U.B., and Wachten, D. (2015). Controlling fertilization and cAMP signaling in sperm by optogenetics. Elife, 4, e05161.CrossRefGoogle ScholarPubMed
Jenal, U. and Malone, J. (2006). Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet., 40, 385–407.CrossRefGoogle Scholar
Jordheim, L.P., Durantel, D., Zoulim, F., and Dumontet, C. (2013). Advances in the development of nucleoside and nucleotide analogues for cancer and viral diseases. Nat. Rev. Drug Discov., 12, 447–64.CrossRefGoogle ScholarPubMed
Joung, Y.H. (2013). Development of implantable medical devices: from an engineering perspective. Int. Neurourol. J., 17, 98–106.CrossRefGoogle ScholarPubMed
Kale, R.P., Kouzani, A.Z., Walder, K., Berk, M., and Tye, S.J. (2015). Evolution of optogenetic microdevices. Neurophotonics, 2, 031206.CrossRefGoogle ScholarPubMed
Karami, A., Eyjolfsdottir, H., Vijayaraghavan, S., Lind, G., Almqvist, P., Kadir, A., Linderoth, B., Andreasen, N., Blennow, K., Wall, A., Westman, E., Ferreira, D., Wiberg, M. Kristoffersen, Wahlund, L.O., Seiger, A., Nordberg, A., Wahlberg, L., Darreh-Shori, T., and Eriksdotter, M. (2015). Changes in CSF cholinergic biomarkers in response to cell therapy with NGF in patients with Alzheimer’s disease. Alzheimers Dement.CrossRefGoogle Scholar
Kasahara, M., Unno, T., Yashiro, K., and Ohmori, M. (2001). CyaG, a novel cyanobacterial adenylyl cyclase and a possible ancestor of mammalian guanylyl cyclases. J. Biol. Chem., 276, 10564–9.CrossRefGoogle Scholar
Kim, J.M., Hwa, J., Garriga, P., Reeves, P.J., RajBhandary, U.L., and Khorana, H.G. (2005). Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops. Biochemistry, 44, 2284–92.CrossRefGoogle ScholarPubMed
Kim, T., Folcher, M., Charpin-El Hamri, G., and Fussenegger, M. (2015a). A synthetic cGMP-sensitive gene switch providing Viagra®-controlled gene expression in mammalian cells and mice. Metab. Eng, 29, 169–79.CrossRefGoogle ScholarPubMed
Kim, T., Folcher, M., Doaud-El Baba, M., and Fussenegger, M. (2015b). A synthetic erectile optogenetic stimulator enabling blue-light-inducible penile erection. Angew. Chem. Int. Ed. Engl., 54, 5933–8.CrossRefGoogle ScholarPubMed
Kim, T.I., McCall, J.G., Jung, Y.H., Huang, X., Siuda, E.R., Li, Y., Song, J., Song, Y.M., Pao, H.A., Kim, R.H., Lu, C., Lee, S.D., Song, I.S., Shin, G., Al-Hasani, R., Kim, S., Tan, M.P., Huang, Y., Omenetto, F.G., Rogers, J.A., and Bruchas, M.R. (2013). Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science, 340, 211–6.CrossRefGoogle ScholarPubMed
Leung, D.W., Otomo, C., Chory, J., and Rosen, M.K. (2008). Genetically encoded photoswitching of actin assembly through the Cdc42–WASP–Arp2/3 complex pathway. Proc. Natl. Acad. Sci. U. S. A., 105, 12797–802.CrossRefGoogle Scholar
Looser, J., Schroder-Lang, S., Hegemann, P., and Nagel, G. (2009). Mechanistic insights in light-induced cAMP production by photoactivated adenylyl cyclase alpha (PACalpha). Biol. Chem., 390, 1105–11.CrossRefGoogle ScholarPubMed
Losi, A. and Gartner, W. (2008). Bacterial bilin- and flavin-binding photoreceptors. Photochem. Photobiol. Sci., 7, 1168–78.CrossRefGoogle Scholar
Mandalari, C., Losi, A., and Gartner, W. (2013). Distance-tree analysis, distribution and co-presence of bilin- and flavin-binding prokaryotic photoreceptors for visible light. Photochem Photobiol Sci, 12, 1144–57.CrossRefGoogle Scholar
Marden, J.N., Dong, Q., Roychowdhury, S., Berleman, J.E., and Bauer, C.E. (2011). Cyclic GMP controls Rhodospirillum centenum cyst development. Mol. Microbiol., 79, 600–15.CrossRefGoogle ScholarPubMed
Moglich, A. and Moffat, K. (2010). Engineered photoreceptors as novel optogenetic tools. Photochem. Photobiol. Sci., 9, 1286–300.CrossRefGoogle ScholarPubMed
Montgomery, K.L., Yeh, A.J., Ho, J.S., Tsao, V., Mohan Iyer, S., Grosenick, L., Ferenczi, E.A., Tanabe, Y., Deisseroth, K., Delp, S.L., and Poon, A.S. (2015). Wirelessly powered, fully internal optogenetics for brain, spinal and peripheral circuits in mice. Nat Methods, 12, 969–74.CrossRefGoogle ScholarPubMed
Motta-Mena, L.B., Reade, A., Mallory, M.J., Glantz, S., Weiner, O.D., Lynch, K.W., and Gardner, K.H. (2014). An optogenetic gene expression system with rapid activation and deactivation kinetics. Nat. Chem. Biol., 10, 196–202.CrossRefGoogle ScholarPubMed
Myakishev-Rempel, M., Stadler, I., Brondon, P., Axe, D.R., Friedman, M., Nardia, F.B., and Lanzafame, R. (2012). A preliminary study of the safety of red light phototherapy of tissues harboring cancer. Photomed. Laser Surg., 30, 551–8.CrossRefGoogle Scholar
Nagahama, T., Suzuki, T., Yoshikawa, S., and Iseki, M. (2007). Functional transplant of photoactivated adenylyl cyclase (PAC) into Aplysia sensory neurons. Neurosci. Res., 59, 81–8.CrossRefGoogle ScholarPubMed
Oplander, C., Deck, A., Volkmar, C.M., Kirsch, M., Liebmann, J., Born, M., van Abeelen, F., van Faassen, E.E., Kroncke, K.D., Windolf, J., and Suschek, C.V. (2013). Mechanism and biological relevance of blue-light (420–453 nm)-induced nonenzymatic nitric oxide generation from photolabile nitric oxide derivates in human skin in vitro and in vivo. Free Radic. Biol. Med., 65, 1363–77.CrossRefGoogle Scholar
Piatkevich, K.D., Subach, F.V., and Verkhusha, V.V. (2013). Far-red light photoactivatable near-infrared fluorescent proteins engineered from a bacterial phytochrome. Nat Commun, 4, 2153.CrossRefGoogle ScholarPubMed
Roembke, B.T., Zhou, J., Zheng, Y., Sayre, D., Lizardo, A., Bernard, L., and Sintim, H.O. (2014). A cyclic dinucleotide containing 2-aminopurine is a general fluorescent sensor for c-di-GMP and 3′,3′-cGAMP. Mol. Biosyst., 10, 1568–75.CrossRefGoogle Scholar
Ryu, M.H., Kang, I.H., Nelson, M.D., Jensen, T.M., Lyuksyutova, A.I., Siltberg-Liberles, J., Raizen, D.M., and Gomelsky, M. (2014). Engineering adenylate cyclases regulated by near-infrared window light. Proc Natl Acad Sci U S A, 111, 10167–72.CrossRefGoogle Scholar
Ryu, M.H., Moskvin, O.V., Siltberg-Liberles, J., and Gomelsky, M. (2010). Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J. Biol. Chem., 285, 41501–8.CrossRefGoogle ScholarPubMed
Ryu, M.H., Youn, H., Kang, I.H., and Gomelsky, M. (2015). Identification of bacterial guanylate cyclases. Proteins, 83, 799–804.CrossRefGoogle ScholarPubMed
Samanta, A., Thunemann, M., Feil, R., and Stafforst, T. (2014). Upon the photostability of 8-nitro-cGMP and its caging as a 7-dimethylaminocoumarinyl ester. Chem. Commun. (Camb.), 50, 7120–3.CrossRefGoogle ScholarPubMed
Scheib, U., Stehfest, K., Gee, C.E., Korschen, H.G., Fudim, R., Oertner, T.G., and Hegemann, P. (2015). The rhodopsin-guanylyl cyclase of the aquatic fungus Blastocladiella emersonii enables fast optical control of cGMP signaling. Sci Signal, 8, rs8.CrossRefGoogle ScholarPubMed
Schroder-Lang, S., Schwarzel, M., Seifert, R., Strunker, T., Kateriya, S., Looser, J., Watanabe, M., Kaupp, U.B., Hegemann, P., and Nagel, G. (2007). Fast manipulation of cellular cAMP level by light in vivo. Nat Methods, 4, 39–42.CrossRefGoogle ScholarPubMed
Sikka, G., Hussmann, G.P., Pandey, D., Cao, S., Hori, D., Park, J.T., Steppan, J., Kim, J.H., Barodka, V., Myers, A.C., Santhanam, L., Nyhan, D., Halushka, M.K., Koehler, R.C., Snyder, S.H., Shimoda, L.A., and Berkowitz, D.E. (2014). Melanopsin mediates light-dependent relaxation in blood vessels. Proc. Natl. Acad. Sci. U. S. A., 111, 17977–82.CrossRefGoogle ScholarPubMed
Sinha, S.C. and Sprang, S.R. (2006). Structures, mechanism, regulation and evolution of class III nucleotidyl cyclases. Rev. Physiol. Biochem. Pharmacol., 157, 105–40.CrossRefGoogle ScholarPubMed
Stierl, M., Penzkofer, A., Kennis, J.T., Hegemann, P., and Mathes, T. (2014). Key residues for the light regulation of the blue light-activated adenylyl cyclase from Beggiatoa sp. Biochemistry, 53, 5121–30.CrossRefGoogle Scholar
Stortkuhl, K.F. and Fiala, A. (2011). The smell of blue light: a new approach toward understanding an olfactory neuronal network. Front. Neurosci., 5, 72.CrossRefGoogle Scholar
Sun, L., Wu, J., Du, F., Chen, X., and Chen, Z.J. (2013). Cyclic GMP–AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science, 339, 786–91.CrossRefGoogle ScholarPubMed
Takala, H., Bjorling, A., Berntsson, O., Lehtivuori, H., Niebling, S., Hoernke, M., Kosheleva, I., Henning, R., Menzel, A., Ihalainen, J.A., and Westenhoff, S. (2014). Signal amplification and transduction in phytochrome photosensors. Nature, 509, 245–8.CrossRefGoogle ScholarPubMed
Tang, X., Zhang, J., Sun, J., Wang, Y., Wu, J., and Zhang, L. (2013). Caged nucleotides/nucleosides and their photochemical biology. Org. Biomol. Chem., 11, 7814–24.CrossRefGoogle ScholarPubMed
Weissenberger, S., Schultheis, C., Liewald, J.F., Erbguth, K., Nagel, G., and Gottschalk, A. (2011). PACalpha – an optogenetic tool for in vivo manipulation of cellular cAMP levels, neurotransmitter release, and behavior in Caenorhabditis elegans. J. Neurochem., 116, 616–25.CrossRefGoogle ScholarPubMed
Werner, G.S., Schaefer, C., Dirks, R., Figulla, H.R., and Kreuzer, H. (1993). Doppler echocardiographic assessment of left ventricular filling in idiopathic dilated cardiomyopathy during a one-year follow-up: relation to the clinical course of disease. Am. Heart J., 126, 1408–16.CrossRefGoogle Scholar
Wu, Y., Li, S.S., Jin, X., Cui, N., Zhang, S., and Jiang, C. (2015). Optogenetic approach for functional assays of the cardiovascular system by light activation of the vascular smooth muscle. Vascul. Pharmacol., 71, 192–200.CrossRefGoogle ScholarPubMed
Yasukawa, H., Sato, A., Kita, A., Kodaira, K., Iseki, M., Takahashi, T., Shibusawa, M., Watanabe, M., and Yagita, K. (2013). Identification of photoactivated adenylyl cyclases in Naegleria australiensis and BLUF-containing protein in Naegleria fowleri. J. Gen. Appl. Microbiol., 59, 361–9.CrossRefGoogle ScholarPubMed
Ye, H., Baba, M. Daoud-El, Peng, R.W., and Fussenegger, M. (2011). A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science, 332, 1565–8.CrossRefGoogle Scholar
Yizhar, O., Fenno, L.E., Davidson, T.J., Mogri, M., and Deisseroth, K. (2011). Optogenetics in neural systems. Neuron, 71, 9–34.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×