Investigating Neuronal Function with Optically Controllable Proteins

Overview

Journal Front Mol Neurosci

Specialty Molecular Biology

Date 2015 Aug 11

PMID 26257603

Citations 9

Authors

Xin X Zhou

Michael Pan

Michael Z Lin

Affiliations

Soon will be listed here.

Abstract

In the nervous system, protein activities are highly regulated in space and time. This regulation allows for fine modulation of neuronal structure and function during development and adaptive responses. For example, neurite extension and synaptogenesis both involve localized and transient activation of cytoskeletal and signaling proteins, allowing changes in microarchitecture to occur rapidly and in a localized manner. To investigate the role of specific protein regulation events in these processes, methods to optically control the activity of specific proteins have been developed. In this review, we focus on how photosensory domains enable optical control over protein activity and have been used in neuroscience applications. These tools have demonstrated versatility in controlling various proteins and thereby cellular functions, and possess enormous potential for future applications in nervous systems. Just as optogenetic control of neuronal firing using opsins has changed how we investigate the function of cellular circuits in vivo, optical control may yet yield another revolution in how we study the circuitry of intracellular signaling in the brain.

Citing Articles

Automating the High-Throughput Screening of Protein-Based Optical Indicators and Actuators.

Lee J, Campillo B, Hamidian S, Liu Z, Shorey M, St-Pierre F Biochemistry. 2022; 62(2):169-177.

PMID: 36315460 PMC: 9852035. DOI: 10.1021/acs.biochem.2c00357.

Optogenetics at the presynapse.

Rost B, Wietek J, Yizhar O, Schmitz D Nat Neurosci. 2022; 25(8):984-998.

PMID: 35835882 DOI: 10.1038/s41593-022-01113-6.

Optobiochemistry: Genetically Encoded Control of Protein Activity by Light.

Seong J, Lin M Annu Rev Biochem. 2021; 90:475-501.

PMID: 33781076 PMC: 11464261. DOI: 10.1146/annurev-biochem-072420-112431.

Near-Infrared Light-Controlled Gene Expression and Protein Targeting in Neurons and Non-neuronal Cells.

Redchuk T, Karasev M, Omelina E, Verkhusha V Chembiochem. 2018; 19(12):1334-1340.

PMID: 29465801 PMC: 6317872. DOI: 10.1002/cbic.201700642.

Locus Coeruleus and Dopamine-Dependent Memory Consolidation.

Yamasaki M, Takeuchi T Neural Plast. 2017; 2017:8602690.

PMID: 29123927 PMC: 5662828. DOI: 10.1155/2017/8602690.

References

Gasser C, Taiber S, Yeh C, Wittig C, Hegemann P, Ryu S . Engineering of a red-light-activated human cAMP/cGMP-specific phosphodiesterase. Proc Natl Acad Sci U S A. 2014; 111(24):8803-8. PMC: 4066486. DOI: 10.1073/pnas.1321600111. View

Nakamura M, Chen L, Howes S, Schindler T, Nogales E, Bryant Z . Remote control of myosin and kinesin motors using light-activated gearshifting. Nat Nanotechnol. 2014; 9(9):693-7. PMC: 4349207. DOI: 10.1038/nnano.2014.147. View

Polstein L, Gersbach C . Light-inducible spatiotemporal control of gene activation by customizable zinc finger transcription factors. J Am Chem Soc. 2012; 134(40):16480-3. PMC: 3468123. DOI: 10.1021/ja3065667. View

Zoltowski B, Schwerdtfeger C, Widom J, Loros J, Bilwes A, Dunlap J . Conformational switching in the fungal light sensor Vivid. Science. 2007; 316(5827):1054-7. PMC: 3682417. DOI: 10.1126/science.1137128. View

Duebel J, Marazova K, Sahel J . Optogenetics. Curr Opin Ophthalmol. 2015; 26(3):226-32. PMC: 5395664. DOI: 10.1097/ICU.0000000000000140. View

Renicke C, Schuster D, Usherenko S, Essen L, Taxis C . A LOV2 domain-based optogenetic tool to control protein degradation and cellular function. Chem Biol. 2013; 20(4):619-26. DOI: 10.1016/j.chembiol.2013.03.005. View

Barends T, Hartmann E, Griese J, Beitlich T, Kirienko N, Ryjenkov D . Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature. 2009; 459(7249):1015-8. DOI: 10.1038/nature07966. View

Muller K, Engesser R, Timmer J, Nagy F, Zurbriggen M, Weber W . Synthesis of phycocyanobilin in mammalian cells. Chem Commun (Camb). 2013; 49(79):8970-2. DOI: 10.1039/c3cc45065a. View

Crosson S, Moffat K . Structure of a flavin-binding plant photoreceptor domain: insights into light-mediated signal transduction. Proc Natl Acad Sci U S A. 2001; 98(6):2995-3000. PMC: 30595. DOI: 10.1073/pnas.051520298. View

10.

Maletic-Savatic M, Malinow R, Svoboda K . Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science. 1999; 283(5409):1923-7. DOI: 10.1126/science.283.5409.1923. View

11.

Bonger K, Rakhit R, Payumo A, Chen J, Wandless T . General method for regulating protein stability with light. ACS Chem Biol. 2013; 9(1):111-5. PMC: 3906921. DOI: 10.1021/cb400755b. View

12.

Lee J, Natarajan M, Nashine V, Socolich M, Vo T, Russ W . Surface sites for engineering allosteric control in proteins. Science. 2008; 322(5900):438-42. PMC: 3071530. DOI: 10.1126/science.1159052. View

13.

Harper S, Christie J, Gardner K . Disruption of the LOV-Jalpha helix interaction activates phototropin kinase activity. Biochemistry. 2004; 43(51):16184-92. DOI: 10.1021/bi048092i. View

14.

Li X, Gutierrez D, Gartz Hanson M, Han J, Mark M, Chiel H . Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc Natl Acad Sci U S A. 2005; 102(49):17816-21. PMC: 1292990. DOI: 10.1073/pnas.0509030102. View

15.

Losi A . Flavin-based Blue-Light photosensors: a photobiophysics update. Photochem Photobiol. 2007; 83(6):1283-300. DOI: 10.1111/j.1751-1097.2007.00196.x. View

16.

Harper S, Neil L, Gardner K . Structural basis of a phototropin light switch. Science. 2003; 301(5639):1541-4. DOI: 10.1126/science.1086810. View

17.

Heijde M, Ulm R . Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state. Proc Natl Acad Sci U S A. 2013; 110(3):1113-8. PMC: 3549095. DOI: 10.1073/pnas.1214237110. View

18.

Wu Y, Frey D, Lungu O, Jaehrig A, Schlichting I, Kuhlman B . A genetically encoded photoactivatable Rac controls the motility of living cells. Nature. 2009; 461(7260):104-8. PMC: 2766670. DOI: 10.1038/nature08241. View

19.

Masseck O, Spoida K, Dalkara D, Maejima T, Rubelowski J, Wallhorn L . Vertebrate cone opsins enable sustained and highly sensitive rapid control of Gi/o signaling in anxiety circuitry. Neuron. 2014; 81(6):1263-1273. DOI: 10.1016/j.neuron.2014.01.041. View

20.

Ramel D, Wang X, Laflamme C, Montell D, Emery G . Rab11 regulates cell-cell communication during collective cell movements. Nat Cell Biol. 2013; 15(3):317-24. PMC: 4006229. DOI: 10.1038/ncb2681. View