Vertebrate cone opsins enable sustained and highly sensitive rapid control of gi/o signaling in anxiety circuitry

Neuron

Volumn 81, Issue 6, 2014, Pages 1263-1273

  Masseck, Olivia A ^a   Spoida, Katharina ^a   Dalkara, Deniz ^b   Maejima, Takashi ^a   Rubelowski, Johanna M ^a   Wallhorn, Lutz ^a   Deneris, Evan S ^c   Herlitze, Stefan ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b INSERM   (France)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONE OPSIN; SEROTONIN 1A RECEPTOR; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; LONG-WAVELENGTH OPSIN; SCOTOPSIN;

ANIMAL BEHAVIOR; ANXIETY; ARTICLE; BRAIN REGION; BRAIN SLICE; DORSAL RAPHE NUCLEUS; HYPERPOLARIZATION; IN VITRO STUDY; IN VIVO STUDY; NEUROMODULATION; PRIORITY JOURNAL; PROTEIN DOMAIN; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; ANIMAL; HUMAN; LIGHT; METABOLISM; MOUSE; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA CONE;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CONE OPSINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HUMANS; LIGHT; MICE; NEURONS; RECEPTOR, SEROTONIN, 5-HT1A; RETINAL CONE PHOTORECEPTOR CELLS; ROD OPSINS; SIGNAL TRANSDUCTION;

EID: 84896311257     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.01.041     Document Type: Article

References (41)

1. Armbruster B.N., Li X., Pausch M.H., Herlitze S., Roth B.L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA 2007, 104:5163-5168.
2. Atwood B.K., Lopez J., Wager-Miller J., Mackie K., Straiker A. Expression of G protein-coupled receptors and related proteins in HEK293, AtT20, BV2, and N18 cell lines as revealed by microarray analysis. BMC Genomics 2011, 12:14.
3. Aurnhammer C., Haase M., Muether N., Hausl M., Rauschhuber C., Huber I., Nitschko H., Busch U., Sing A., Ehrhardt A., Baiker A. Universal real-time PCR for the detection and quantification of adeno-associated virus serotype 2-derived inverted terminal repeat sequences. Hum. Gene. Ther. Methods 2012, 23:18-28.
4. Beck S.G., Pan Y.Z., Akanwa A.C., Kirby L.G. Median and dorsal raphe neurons are not electrophysiologically identical. J.Neurophysiol. 2004, 91:994-1005.
5. Brueggemann L.I., Sullivan J.M. HEK293S cells have functional retinoid processing machinery. J.Gen. Physiol. 2002, 119:593-612.
6. Chen M.H., Kuemmel C., Birge R.R., Knox B.E. Rapid release of retinal from a cone visual pigment following photoactivation. Biochemistry 2012, 51:4117-4125.
7. Choi V.W., Asokan A., Haberman R.A., Samulski R.J. Production of recombinant adeno-associated viral vectors for invitro and invivo use. Curr. Protoc. Mol. Biol. 2007, Chapter 16. Unit 16.25.
8. Ebrey T., Koutalos Y. Vertebrate photoreceptors. Prog. Retin. Eye Res. 2001, 20:49-94.
9. Gocho Y., Sakai A., Yanagawa Y., Suzuki H., Saitow F. Electrophysiological and pharmacological properties of GABAergic cells in the dorsal raphe nucleus. J.Physiol. Sci. 2013, 63:147-154.
10. Gradinaru V., Zhang F., Ramakrishnan C., Mattis J., Prakash R., Diester I., Goshen I., Thompson K.R., Deisseroth K. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 2010, 141:154-165.
11. Graeff F.G., Netto C.F., Zangrossi H. The elevated T-maze as an experimental model of anxiety. Neurosci. Biobehav. Rev. 1998, 23:237-246.
12. Gross C., Santarelli L., Brunner D., Zhuang X., Hen R. Altered fear circuits in 5-HT(1A) receptor KO mice. Biol. Psychiatry 2000, 48:1157-1163.
13. Gutierrez D.V., Mark M.D., Masseck O., Maejima T., Kuckelsberg D., Hyde R.A., Krause M., Kruse W., Herlitze S. Optogenetic control of motor coordination by Gi/o protein-coupled vertebrate rhodopsin in cerebellar Purkinje cells. J.Biol. Chem. 2011, 286:25848-25858.
14. Heisler L.K., Chu H.M., Brennan T.J., Danao J.A., Bajwa P., Parsons L.H., Tecott L.H. Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc. Natl. Acad. Sci. USA 1998, 95:15049-15054.
15. Herlitze S., Landmesser L.T. New optical tools for controlling neuronal activity. Curr. Opin. Neurobiol. 2007, 17:87-94.
16. Higgins G.A., Bradbury A.J., Jones B.J., Oakley N.R. Behavioural and biochemical consequences following activation of 5HT1-like and GABA receptors in the dorsal raphé nucleus of the rat. Neuropharmacology 1988, 27:993-1001.
17. Higgins G.A., Jones B.J., Oakley N.R. Effect of 5-HT1A receptoragonists in two models of anxiety after dorsal raphe injection. Psychopharmacology (Berl.) 1992, 106:261-267.
18. Hille B. Modulation of ion-channel function by G-protein-coupled receptors. Trends Neurosci. 1994, 17:531-536.
19. Hogg S., Andrews N., File S.E. Contrasting behavioural effects of8-OH DPAT in the dorsal raphé nucleus and ventral hippocampus. Neuropharmacology 1994, 33:343-348.
20. Karunarathne W.K., Giri L., Kalyanaraman V., Gautam N. Optically triggering spatiotemporally confined GPCR activity in a cell and programming neurite initiation and extension. Proc. Natl. Acad. Sci. USA 2013, 110:E1565-E1574.
21. Kawamura S., Tachibanaki S. Rod and cone photoreceptors: molecular basis of the difference in their physiology. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2008, 150:369-377.
22. Kirby L.G., Pernar L., Valentino R.J., Beck S.G. Distinguishing characteristics of serotonin and non-serotonin-containing cells in the dorsal raphe nucleus: electrophysiological and immunohistochemical studies. Neuroscience 2003, 116:669-683.
23. 2+-permeable channelrhodopsin CatCh. Nat. Neurosci. 2011, 14:513-518.
24. Levitz J., Pantoja C., Gaub B., Janovjak H., Reiner A., Hoagland A., Schoppik D., Kane B., Stawski P., Schier A.F., et al. Optical control of metabotropic glutamate receptors. Nat. Neurosci. 2013, 16:507-516.
25. Li X., Gutierrez D.V., Hanson M.G., Han J., Mark M.D., Chiel H., Hegemann P., Landmesser L.T., Herlitze S. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc. Natl. Acad. Sci. USA 2005, 102:17816-17821.
26. Maejima T., Masseck O.A., Mark M.D., Herlitze S. Modulation of firing and synaptic transmission of serotonergic neurons by intrinsic G protein-coupled receptors and ion channels. Front Integr. Neurosci. 2013, 7:40.
27. Mark M.D., Herlitze S. G-protein mediated gating of inward-rectifier K+ channels. Eur. J. Biochem. 2000, 267:5830-5836.
28. Masseck O.A., Rubelowski J.M., Spoida K., Herlitze S. Light- and drug-activated G-protein-coupled receptors to control intracellular signalling. Exp. Physiol. 2011, 96:51-56.
29. McDevitt R.A., Neumaier J.F. Regulation of dorsal raphe nucleus function by serotonin autoreceptors: a behavioral perspective. J.Chem. Neuroanat. 2011, 41:234-246.
30. Nikonov S.S., Kholodenko R., Lem J., Pugh E.N. Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. J.Gen. Physiol. 2006, 127:359-374.
31. Oh E., Maejima T., Liu C., Deneris E., Herlitze S. Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor. J.Biol. Chem. 2010, 285:30825-30836.
32. Parks C.L., Robinson P.S., Sibille E., Shenk T., Toth M. Increased anxiety of mice lacking the serotonin1A receptor. Proc. Natl. Acad. Sci. USA 1998, 95:10734-10739.
33. Ramboz S., Oosting R., Amara D.A., Kung H.F., Blier P., Mendelsohn M., Mann J.J., Brunner D., Hen R. Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc. Natl. Acad. Sci. USA 1998, 95:14476-14481.
34. Remy S.M., Schreiber R., Dalmus M., De Vry J. Somatodendritic 5-HT1A receptors are critically involved in the anxiolytic effects of 8-OH-DPAT. Psychopharmacology (Berl.) 1996, 125:89-91.
35. Richardson-Jones J.W., Craige C.P., Guiard B.P., Stephen A., Metzger K.L., Kung H.F., Gardier A.M., Dranovsky A., David D.J., Beck S.G., et al. 5-HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron 2010, 65:40-52.
36. Richardson-Jones J.W., Craige C.P., Nguyen T.H., Kung H.F., Gardier A.M., Dranovsky A., David D.J., Guiard B.P., Beck S.G., Hen R., Leonardo E.D. Serotonin-1A autoreceptors are necessary and sufficient for the normal formation of circuits underlying innate anxiety. J.Neurosci. 2011, 31:6008-6018.
37. Romaniuk A., Koprowska M., Krotewicz M., Strzelczuk M., Wieczorek M. Effects of 8-OHDPAT administration into the dorsal raphe nucleus and dorsal hippocampus on fear behavior and regional brain monoamines distribution in rats. Behav. Brain Res. 2001, 120:47-57.
38. Sharp T., Boothman L., Raley J., Quérée P. Important messages in the 'post': recent discoveries in 5-HT neurone feedback control. Trends Pharmacol. Sci. 2007, 28:629-636.
39. Sommer M.E., Hofmann K.P., Heck M. Distinct loops in arrestindifferentially regulate ligand binding within the GPCR opsin. Nat. Commun. 2012, 3:995.
40. Wittemann S., Mark M.D., Rettig J., Herlitze S. Synaptic localization and presynaptic function of calcium channel beta 4-subunits in cultured hippocampal neurons. J.Biol. Chem. 2000, 275:37807-37814.
41. Wylie C.J., Hendricks T.J., Zhang B., Wang L., Lu P., Leahy P., Fox S., Maeno H., Deneris E.S. Distinct transcriptomes define rostral and caudal serotonin neurons. J.Neurosci. 2010, 30:670-684.