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4 - From Synapse to Behavior: Optogenetic Tools for the Investigation of the Caenorhabditis elegans Nervous System

from Part I - Optogenetics in Model Organisms

Published online by Cambridge University Press:  28 April 2017

By
Jatin Nagpal
Edited by
Krishnarao Appasani
Krishnarao Appasani
Affiliation:
GeneExpression Systems, Inc., Massachusetts
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Optogenetics
From Neuronal Function to Mapping and Disease Biology
 , pp. 55 - 65
Publisher: Cambridge University Press
Print publication year: 2017

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References

Akerboom, J, Carreras Calderón, N, Tian, L, Wabnig, S, Prigge, M, Tolö, J, Gordus, A, Orger, MB, Severi, KE, Macklin, JJ, Patel, R, Pulver, SR, Wardill, TJ, Fischer, E, Schüler, C, Chen, T-W, Sarkisyan, KS, Marvin, JS, Bargmann, CI, Kim, DS, Kügler, S, Lagnado, L, Hegemann, P, Gottschalk, A, Schreiter, ER, Looger, LL (2013) Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci, 6:2.CrossRefGoogle Scholar
Akerboom, J, Chen, T-W, Wardill, TJ, Tian, L, Marvin, JS, Mutlu, S, Calderón, NC, Esposti, F, Borghuis, BG, Sun, XR, Gordus, A, Orger, MB, Portugues, R, Engert, F, Macklin, JJ, Filosa, A, Aggarwal, A, Kerr, RA, Takagi, R, Kracun, S, Shigetomi, E, Khakh, BS, Baier, H, Lagnado, L, Wang, SS-H, Bargmann, CI, Kimmel, BE, Jayaraman, V, Svoboda, K, Kim, DS, Schreiter, ER, Looger, LL (2012) Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci, 32:13819–13840.CrossRefGoogle ScholarPubMed
Ardiel, EL, Rankin, CH (2010) An elegant mind: learning and memory in Caenorhabditis elegans. Learn Mem, 17:191–201.CrossRefGoogle ScholarPubMed
Avelar, GM, Schumacher, RI, Zaini, PA, Leonard, G, Richards, TA, Gomes, SL (2014) A Rhodopsin-Guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr Biol, 24:1234–1240.CrossRefGoogle Scholar
AzimiHashemi, N, Erbguth, K, Vogt, A, Riemensperger, T, Rauch, E, Woodmansee, D, Nagpal, J, Brauner, M, Sheves, M, Fiala, A, Kattner, L, Trauner, D, Hegemann, P, Gottschalk, A, Liewald, JF (2014) Synthetic retinal analogues modify the spectral and kinetic characteristics of microbial rhodopsin optogenetic tools. Nat Commun, 5:5810.CrossRefGoogle ScholarPubMed
Bamann, C, Kirsch, T, Nagel, G, Bamberg, E (2008) Spectral characteristics of the photocycle of channelrhodopsin-2 and its implication for channel function. J Mol Biol, 375:686–694.CrossRefGoogle ScholarPubMed
Banghart, M, Borges, K, Isacoff, E, Trauner, D, Kramer, RH (2004) Light-activated ion channels for remote control of neuronal firing. Nat Neurosci, 7:1381–1386.CrossRefGoogle Scholar
Beavo, JA, Brunton, LL (2002) Cyclic nucleotide research – still expanding after half a century. Nat Rev Mol Cell Biol, 3:710–718.CrossRefGoogle ScholarPubMed
Berndt, A, Lee, SY, Ramakrishnan, C, Deisseroth, K (2014) Structure-guided transformation of channelrhodopsin into a light-activated chloride channel. Science, 344:420–424.CrossRefGoogle ScholarPubMed
Berndt, A, Schoenenberger, P, Mattis, J, Tye, KM, Deisseroth, K, Hegemann, P, Oertner, TG (2011) High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels. Proc Natl Acad Sci U S A, 108:7595–7600.CrossRefGoogle Scholar
Berndt, A, Yizhar, O, Gunaydin, LA, Hegemann, P, Deisseroth, K (2009) Bi-stable neural state switches. Nat Neurosci, 12:229–234.CrossRefGoogle ScholarPubMed
Boyden, ES, Zhang, F, Bamberg, E, Nagel, G, Deisseroth, K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci, 8:1263–1268.CrossRefGoogle ScholarPubMed
Broussard, GJ, Liang, R, Tian, L (2014) Monitoring activity in neural circuits with genetically encoded indicators. Front Mol Neurosci, 7:97.CrossRefGoogle ScholarPubMed
Chen, T-W, Wardill, TJ, Sun, Y, Pulver, SR, Renninger, SL, Baohan, A, Schreiter, ER, Kerr, RA, Orger, MB, Jayaraman, V, Looger, LL, Svoboda, K, Kim, DS (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature, 499:295–300.CrossRefGoogle Scholar
Chow, BY, Han, X, Dobry, AS, Qian, X, Chuong, AS, Li, M, Henninger, M a, Belfort, GM, Lin, Y, Monahan, PE, Boyden, ES (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature, 463:98–102.CrossRefGoogle ScholarPubMed
Chung, SH, Sun, L, Gabel, CV (2013) In vivo neuronal calcium imaging in C. elegans. J Vis Exp, 74:50357.Google Scholar
Chuong, AS, Miri, ML, Busskamp, V, Matthews, GAC, Acker, LC, Sørensen, AT, Young, A, Klapoetke, NC, Henninger, MA, Kodandaramaiah, SB, Ogawa, M, Ramanlal, SB, Bandler, RC, Allen, BD, Forest, CR, Chow, BY, Han, X, Lin, Y, Tye, KM, Roska, B, Cardin, JA, Boyden, ES (2014) Noninvasive optical inhibition with a red-shifted microbial rhodopsin. Nat Neurosci, 17:1123–1129.CrossRefGoogle ScholarPubMed
de Bono, M, Maricq, AV (2005) Neuronal substrates of complex behaviors in C. elegans. Annu Rev Neurosci, 28:451–501.CrossRefGoogle ScholarPubMed
Dugué, GP, Akemann, W, Knöpfel, T (2012) A comprehensive concept of optogenetics. Prog Brain Res, 196:1–28.CrossRefGoogle ScholarPubMed
Erbguth, K, Prigge, M, Schneider, F, Hegemann, P, Gottschalk, A (2012) Bimodal activation of different neuron classes with the spectrally red-shifted channelrhodopsin chimera C1V1 in Caenorhabditis elegans. PLoS One, 7:e46827.CrossRefGoogle ScholarPubMed
Fang-Yen, C, Alkema, MJ, Samuel, ADT, Fang-yen, C (2015) Illuminating neural circuits and behaviour in Caenorhabditis elegans with optogenetics. Philos Trans R Soc Lond B Biol Sci, 370:20140212.CrossRefGoogle Scholar
Feldbauer, K, Zimmermann, D, Pintschovius, V, Spitz, J, Bamann, C, Bamberg, E (2009) Channelrhodopsin-2 is a leaky proton pump. Proc Natl Acad Sci U S A, 106:12317–12322.CrossRefGoogle ScholarPubMed
Fenno, L, Yizhar, O, Deisseroth, K (2011) The development and application of optogenetics. Annu Rev Neurosci, 34:389–412.CrossRefGoogle ScholarPubMed
Flavell, SW, Pokala, N, Macosko, EZ, Albrecht, DR, Larsch, J, Bargmann, CI (2013) Serotonin and the neuropeptide PDF initiate and extend opposing behavioral states in C. elegans. Cell, 154:1023–1035.CrossRefGoogle ScholarPubMed
Flytzanis, NC, Bedbrook, CN, Chiu, H, Engqvist, MKM, Xiao, C, Chan, KY, Sternberg, PW, Arnold, FH, Gradinaru, V (2014) Archaerhodopsin variants with enhanced voltage-sensitive fluorescence in mammalian and Caenorhabditis elegans neurons. Nat Commun, 5:4894.CrossRefGoogle ScholarPubMed
Gancedo, JM (2013) Biological roles of cAMP: variations on a theme in the different kingdoms of life. Biol Rev Camb Philos Soc, 88:645–68.CrossRefGoogle ScholarPubMed
Gao, S, Nagpal, J, Schneider, MW, Kozjak-pavlovic, V, Nagel, G, Gottschalk, A (2015) Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp. Nat Commun, 6:1–12.CrossRefGoogle Scholar
Gong, Y, Li, JZ, Schnitzer, MJ (2013) Enhanced archaerhodopsin fluorescent protein voltage indicators. PLoS One, 8:e66959.CrossRefGoogle Scholar
Govorunova, EG, Sineshchekov, OA, Janz, R, Liu, X, Spudich, JL (2015) Natural light-gated anion channels: a family of microbial rhodopsins for advanced optogenetics. Science, 349:647–650.CrossRefGoogle ScholarPubMed
Gradinaru, V, Thompson, KR, Deisseroth, K (2008) eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol, 36:129–139.CrossRefGoogle ScholarPubMed
Gunaydin, LA, Yizhar, O, Berndt, A, Sohal, VS, Deisseroth, K, Hegemann, P (2010) Ultrafast optogenetic control. Nat Neurosci, 13:387–392.CrossRefGoogle ScholarPubMed
Han, X, Chow, BY, Zhou, H, Klapoetke, NC, Chuong, A, Rajimehr, R, Yang, A, Baratta, MV, Winkle, J, Desimone, R, Boyden, ES (2011) A high-light sensitivity optical neural silencer: development and application to optogenetic control of non-human primate cortex. Front Syst Neurosci, 5:18.CrossRefGoogle ScholarPubMed
Hermann, A, Liewald, JF, Gottschalk, A (2015) A photosensitive degron enables acute light-induced protein degradation in the nervous system. Curr Biol, 25: R749–R750.CrossRefGoogle ScholarPubMed
Husson, SJ, Costa, WS, Wabnig, S, Stirman, JN, Watson, JD, Spencer, WC, Akerboom, J, Looger, LL, Treinin, M, Miller, DM, Lu, H, Gottschalk, A (2012a) Optogenetic analysis of a nociceptor neuron and network reveals ion channels acting downstream of primary sensors. Curr Biol, 22:743–752.CrossRefGoogle ScholarPubMed
Husson, SJ, Gottschalk, A, Leifer, AM (2013) Optogenetic manipulation of neural activity in C. elegans: from synapse to circuits and behaviour. Biol Cell, 105:235–250.CrossRefGoogle Scholar
Husson, SJ, Liewald, JF, Schultheis, C, Stirman, JN, Lu, H, Gottschalk, A (2012b) Microbial light-activatable proton pumps as neuronal inhibitors to functionally dissect neuronal networks in C. elegans. PLoS One, 7:e40937.CrossRefGoogle Scholar
Kerr, RA (2006) Imaging the activity of neurons and muscles. WormBook, 1–13.CrossRefGoogle Scholar
Klapoetke, NC, Murata, Y, Kim, SS, Pulver, SR, Birdsey-Benson, A, Cho, YK, Morimoto, TK, Chuong, AS, Carpenter, EJ, Tian, Z, Wang, J, Xie, Y, Yan, Z, Zhang, Y, Chow, BY, Surek, B, Melkonian, M, Jayaraman, V, Constantine-Paton, M, Wong, GK-S, Boyden, ES (2014) Independent optical excitation of distinct neural populations. Nat Methods, 11: 338–346.CrossRefGoogle ScholarPubMed
Kobayashi, J, Shidara, H, Morisawa, Y, Kawakami, M, Tanahashi, Y, Hotta, K, Oka, K (2013) A method for selective ablation of neurons in C. elegans using the phototoxic fluorescent protein, KillerRed. Neurosci Lett, 548:261–264.CrossRefGoogle Scholar
Kralj, JM, Douglass, AD, Hochbaum, DR, Maclaurin, D, Cohen, AE (2012) Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat Methods, 9:90–95.CrossRefGoogle Scholar
Lima, SQ, Miesenböck, G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell, 121:141–152.CrossRefGoogle Scholar
Lin, JY (2011) A user’s guide to channelrhodopsin variants: features, limitations and future developments. Exp Physiol, 96:19–25.CrossRefGoogle ScholarPubMed
Lin, JY, Lin, MZ, Steinbach, P, Tsien, RY (2009) Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys J, 96:1803–1814.CrossRefGoogle ScholarPubMed
Lin, JY, Sann, SB, Zhou, K, Nabavi, S, Proulx, CD, Malinow, R, Jin, Y, Tsien, RY (2013) Optogenetic inhibition of synaptic release with chromophore-assisted light inactivation (CALI). Neuron, 79:241–253.CrossRefGoogle Scholar
Lucas, KA, Pitari, GM, Kazerounian, S, Ruiz-Stewart, I, Park, J, Schulz, S, Chepenik, KP, Waldman, SA (2000) Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev, 52:375–414.Google ScholarPubMed
Maclaurin, D, Venkatachalam, V, Lee, H, Cohen, AE (2013) Mechanism of voltage-sensitive fluorescence in a microbial rhodopsin. Proc Natl Acad Sci U S A, 110:5939–5944.CrossRefGoogle Scholar
Mutoh, H, Akemann, W, Knöpfel, T (2012) Genetically engineered fluorescent voltage reporters. ACS Chem Neurosci, 3:585–592.CrossRefGoogle ScholarPubMed
Nagel, G, Brauner, M, Liewald, JF, Adeishvili, N, Bamberg, E, Gottschalk, A (2005) Light activation of channelrhodopsin-2 in excitable cells of caenorhabditis elegans triggers rapid behavioral responses. Curr Biol, 15:2279–2284.CrossRefGoogle ScholarPubMed
Nagel, G, Szellas, T, Huhn, W, Kateriya, S, Adeishvili, N, Berthold, P, Ollig, D, Hegemann, P, Bamberg, E (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A, 100:13940–13945.CrossRefGoogle ScholarPubMed
Okazaki, A, Takagi, S (2013) An optogenetic application of proton pump ArchT to C. elegans cells. Neurosci Res, 75:29–34.CrossRefGoogle ScholarPubMed
Prigge, M, Schneider, F, Tsunoda, SP, Shilyansky, C, Wietek, J, Deisseroth, K, Hegemann, P (2012) Color-tuned channelrhodopsins for multiwavelength optogenetics. J Biol Chem, 287:31804–31812.CrossRefGoogle Scholar
Qi, YB, Garren, EJ, Shu, X, Tsien, RY, Jin, Y (2012) Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singlet oxygen generating protein miniSOG. Proc Natl Acad Sci U S A, 109:7499–7504.CrossRefGoogle ScholarPubMed
Renicke, C, Schuster, D, Usherenko, S, Essen, L-O, Taxis, C (2013) A LOV2 domain-based optogenetic tool to control protein degradation and cellular function. Chem Biol, 20:619–626.CrossRefGoogle ScholarPubMed
Ryu, M-H, Moskvin, OV, Siltberg-Liberles, J, Gomelsky, M (2010) Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J Biol Chem, 285:41501–41508.CrossRefGoogle ScholarPubMed
Scheib, U, Stehfest, K, Gee, CE, Korschen, HG, Fudim, R, Oertner, TG, Hegemann, P (2015) The rhodopsin-guanylyl cyclase of the aquatic fungus Blastocladiella emersonii enables fast optical control of cGMP signaling. Sci Signal, 8:1–8.CrossRefGoogle ScholarPubMed
Schild, LC, Glauser, DA (2015) Dual color neural activation and behavior control with Chrimson and CoChR in C. elegans. Genetics, 200:1029–1034.CrossRefGoogle Scholar
Schröder-Lang, S, Schwärzel, M, Seifert, R, Strünker, T, Kateriya, S, Looser, J, Watanabe, M, Kaupp, UB, Hegemann, P, Nagel, G (2007) Fast manipulation of cellular cAMP level by light in vivo. Nat Methods, 4:39–42.CrossRefGoogle ScholarPubMed
Schultheis, C, Liewald, JF, Bamberg, E, Nagel, G, Gottschalk, A (2011) Optogenetic long-term manipulation of behavior and animal development. PLoS One, 6:e18766.CrossRefGoogle Scholar
Sengupta, P, Samuel, ADT (2009) Caenorhabditis elegans: a model system for systems neuroscience. Curr Opin Neurobiol, 19:637–643.CrossRefGoogle Scholar
Shipley, FB, Clark, CM, Alkema, MJ, Leifer, AM (2014) Simultaneous optogenetic manipulation and calcium imaging in freely moving C. elegans. Front Neural Circuits, 8:28.CrossRefGoogle ScholarPubMed
Stierl, M, Stumpf, P, Udwari, D, Gueta, R, Hagedorn, R, Losi, A, Gärtner, W, Petereit, L, Efetova, M, Schwarzel, M, Oertner, TG, Nagel, G, Hegemann, P (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.CrossRefGoogle ScholarPubMed
Tian, L, Hires, SA, Mao, T, Huber, D, Chiappe, ME, Chalasani, SH, Petreanu, L, Akerboom, J, McKinney, SA, Schreiter, ER, Bargmann, CI, Jayaraman, V, Svoboda, K, Looger, LL (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods, 6:875–881.CrossRefGoogle Scholar
Ullrich, S, Gueta, R, Nagel, G (2013) Degradation of channelopsin-2 in the absence of retinal and degradation resistance in certain mutants. Biol Chem, 394:271–280.CrossRefGoogle ScholarPubMed
Volgraf, M, Gorostiza, P, Numano, R, Kramer, RH, Isacoff, EY, Trauner, D (2006) Allosteric control of an ionotropic glutamate receptor with an optical switch. Nat Chem Biol, 2:47–52.CrossRefGoogle Scholar
Wabnig, S, Liewald, JF, Yu, S-C, Gottschalk, A (2015) High-throughput all-optical analysis of synaptic transmission and synaptic vesicle recycling in Caenorhabditis elegans. PLoS One, 10:e0135584.CrossRefGoogle ScholarPubMed
Watanabe, S, Liu, Q, Davis, MW, Hollopeter, G, Thomas, N, Jorgensen, NB, Jorgensen, EM (2013) Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. Elife, 2:e00723.CrossRefGoogle ScholarPubMed
Weissenberger, S, Schultheis, C, Liewald, JF, Erbguth, K, Nagel, G, Gottschalk, A (2011) PACα – an optogenetic tool for in vivo manipulation of cellular cAMP levels, neurotransmitter release, and behavior in Caenorhabditis elegans. J Neurochem, 116:616–625.CrossRefGoogle ScholarPubMed
White, JG, Southgate, E, Thomson, JN, Brenner, S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc B Biol Sci, 314:1–340.Google ScholarPubMed
Wietek, J, Wiegert, JS, Adeishvili, N, Schneider, F, Watanabe, H, Tsunoda, SP, Vogt, A, Elstner, M, Oertner, TG, Hegemann, P (2014) Conversion of channelrhodopsin into a light-gated chloride channel. Science, 344:409–412.CrossRefGoogle Scholar
Williams, DC, Bejjani, RE, Ramirez, PM, Coakley, S, Kim, SA, Lee, H, Wen, Q, Samuel, A, Lu, H, Hilliard, MA, Hammarlund, M (2013) Rapid and permanent neuronal inactivation in vivo via subcellular generation of reactive oxygen with the use of KillerRed. Cell Rep, 5:553–563.CrossRefGoogle ScholarPubMed
Xu, X, Kim, SK (2011) The early bird catches the worm: new technologies for the Caenorhabditis elegans toolkit. Nat Rev Genet, 12:793–801.CrossRefGoogle ScholarPubMed
Yemini, E, Jucikas, T, Grundy, LJ, Brown, AEX, Schafer, WR (2013) A database of Caenorhabditis elegans behavioral phenotypes. Nat Methods, 10:877–879.CrossRefGoogle ScholarPubMed
Yizhar, O, Fenno, LE, Prigge, M, Schneider, F, Davidson, TJ, O’Shea, DJ, Sohal, VS, Goshen, I, Finkelstein, J, Paz, JT, Stehfest, K, Fudim, R, Ramakrishnan, C, Huguenard, JR, Hegemann, P, Deisseroth, K (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature, 477:171–178.CrossRefGoogle ScholarPubMed
Zemelman, BV, Nesnas, N, Lee, GA, Miesenbock, G (2003) Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc Natl Acad Sci U S A, 100:1352–1357.CrossRefGoogle ScholarPubMed
Zemelman, BV, Lee, GA, Ng, M, Miesenböck, G (2002) Selective photostimulation of genetically chARGed neurons. Neuron, 33:15–22.CrossRefGoogle ScholarPubMed
Zhang, F, Prigge, M, Beyrière, F, Tsunoda, SP, Mattis, J, Yizhar, O, Hegemann, P, Deisseroth, K (2008) Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nat Neurosci, 11:631–633.CrossRefGoogle ScholarPubMed
Zhang, F, Wang, L-P, Brauner, M, Liewald, JF, Kay, K, Watzke, N, Wood, PG, Bamberg, E, Nagel, G, Gottschalk, A, Deisseroth, K (2007) Multimodal fast optical interrogation of neural circuitry. Nature, 446:633–639.CrossRefGoogle ScholarPubMed

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