Use of Optogenetic Approaches to Control Intracellular Signaling of G Protein-Coupled Receptors

  • Olivia A. Masseck
  • Melanie D. Mark
  • Stefan Herlitze
Protocol
First Online:
Part of the Methods in Pharmacology and Toxicology book series (MIPT)

Abstract

The tractability of light-activated receptors makes them attractive tools by which to study the brain. They allow for the noninvasive and specific control of neuronal signaling and could allow for the study of receptor pathways that occur faster than the rate of diffusion. Furthermore, with the aid of implantable light devices, light-activated receptors have the potential for use in live animals and later in humans to control and cure G protein-coupled receptor (GPCR) pathways involved in diseases. We will summarize here the latest developments for controlling intracellular signaling pathways by light-activated GPCRs and enzymes.

Keywords

Rhodopsin GPCR G protein Gαq/11 Gαi/o Gαs Adenylyl cyclase Optogenetics OptoXR 
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Notes

Acknowledgments

This work was supported by grants of the Deutsche Forschungsgemeinschaft to OAM (MA 4692/3-1), MDM (MA5806/1-1), and SH (He2471/8-1). Additional support was from NIH (MH081127) to SH.

References

  1. 1.
    Herlitze S, Landmesser LT (2007) New optical tools for controlling neuronal activity. Curr Opin Neurobiol 17:87–94PubMedCrossRefGoogle Scholar
  2. 2.
    Li X, Gutierrez DV, Hanson MG et al (2005) Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc Natl Acad Sci U S A 102:17816–17821PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Boyden ES, Zhang F, Bamberg E et al (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268PubMedCrossRefGoogle Scholar
  4. 4.
    Nagel G, Brauner M, Liewald JF et al (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15:2279–2284PubMedCrossRefGoogle Scholar
  5. 5.
    Knox BE, Khorana HG, Nasi E (1993) Light-induced currents in Xenopus oocytes expressing bovine rhodopsin. J Physiol 466:157–172PubMedGoogle Scholar
  6. 6.
    Khorana HG, Knox BE, Nasi E et al (1988) Expression of a bovine rhodopsin gene in Xenopus oocytes: demonstration of light-dependent ionic currents. Proc Natl Acad Sci U S A 85:7917–7921PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Gonzalez-Fernandez F (2002) Evolution of the visual cycle: the role of retinoid-binding proteins. J Endocrinol 175:75–88PubMedCrossRefGoogle Scholar
  8. 8.
    Brueggemann LI, Sullivan JM (2002) HEK293S cells have functional retinoid processing machinery. J Gen Physiol 119:593–612PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Zemelman BV, Lee GA, Ng M et al (2002) Selective photostimulation of genetically chARGed neurons. Neuron 33:15–22PubMedCrossRefGoogle Scholar
  10. 10.
    Nakagawa M, Iwasa T, Kikkawa S et al (1999) How vertebrate and invertebrate visual pigments differ in their mechanism of photoactivation. Proc Natl Acad Sci U S A 96:6189–6192PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Hille B (1994) Modulation of ion-channel function by G-protein-coupled receptors. Trends Neurosci 17:531–536PubMedCrossRefGoogle Scholar
  12. 12.
    Gutierrez DV, Mark MD, Masseck O et al (2011) Optogenetic control of motor coordination by Gi/o protein-coupled vertebrate rhodopsin in cerebellar Purkinje cells. J Biol Chem 286:25848–25858PubMedCrossRefGoogle Scholar
  13. 13.
    Oh E, Maejima T, Liu C et al (2010) Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor. J Biol Chem 285:30825–30836PubMedCrossRefGoogle Scholar
  14. 14.
    Kim JM, Hwa J, Garriga P et al (2005) Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops. Biochemistry 44:2284–2292PubMedCrossRefGoogle Scholar
  15. 15.
    Airan RD, Thompson KR, Fenno LE et al (2009) Temporally precise in vivo control of intracellular signalling. Nature 458:1025–1029PubMedCrossRefGoogle Scholar
  16. 16.
    Wess J (1997) G-protein-coupled receptors: molecular mechanisms involved in receptor activation and selectivity of G-protein recognition. FASEB J 11:346–354PubMedGoogle Scholar
  17. 17.
    Bockaert J, Claeysen S, Compan V et al (2004) 5-HT4 receptors. Curr Drug Targets CNS Neurol Disord 3:39–51PubMedCrossRefGoogle Scholar
  18. 18.
    Jolimay N, Franck L, Langlois X et al (2000) Dominant role of the cytosolic C-terminal domain of the rat 5-HT1B receptor in axonal-apical targeting. J Neurosci 20:9111–9118PubMedGoogle Scholar
  19. 19.
    Darmon M, Langlois X, Suffisseau L et al (1998) Differential membrane targeting and pharmacological characterization of chimeras of rat serotonin 5-HT1A and 5-HT1B receptors expressed in epithelial LLC-PK1 cells. J Neurochem 71:2294–2303PubMedCrossRefGoogle Scholar
  20. 20.
    Carrel D, Masson J, Al Awabdh S et al (2008) Targeting of the 5-HT1A serotonin receptor to neuronal dendrites is mediated by Yif1B. J Neurosci 28:8063–8073PubMedCrossRefGoogle Scholar
  21. 21.
    Renner U, Glebov K, Lang T et al (2007) Localization of the mouse 5-hydroxytryptamine(1A) receptor in lipid microdomains depends on its palmitoylation and is involved in receptor-mediated signaling. Mol Pharmacol 72:502–513PubMedCrossRefGoogle Scholar
  22. 22.
    Mure LS, Cornut PL, Rieux C et al (2009) Melanopsin bistability: a fly’s eye technology in the human retina. PLoS One 4:e5991PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Peirson S, Foster RG (2006) Melanopsin: another way of signaling light. Neuron 49:331–339PubMedCrossRefGoogle Scholar
  24. 24.
    Hankins MW, Peirson SN, Foster RG (2008) Melanopsin: an exciting photopigment. Trends Neurosci 31:27–36PubMedCrossRefGoogle Scholar
  25. 25.
    Melyan Z, Tarttelin EE, Bellingham J et al (2005) Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433:741–745PubMedCrossRefGoogle Scholar
  26. 26.
    Panda S, Nayak SK, Campo B et al (2005) Illumination of the melanopsin signaling pathway. Science 307:600–604PubMedCrossRefGoogle Scholar
  27. 27.
    Qiu X, Kumbalasiri T, Carlson SM et al (2005) Induction of photosensitivity by heterologous expression of melanopsin. Nature 433:745–749PubMedCrossRefGoogle Scholar
  28. 28.
    Lin B, Koizumi A, Tanaka N et al (2008) Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc Natl Acad Sci U S A 105:16009–16014PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Ye H, Daoud-El Baba M, Peng RW et al (2011) A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science 332:1565–1568PubMedCrossRefGoogle Scholar
  30. 30.
    Hartwick AT, Bramley JR, Yu J et al (2007) Light-evoked calcium responses of isolated melanopsin-expressing retinal ganglion cells. J Neurosci 27:13468–13480PubMedCrossRefGoogle Scholar
  31. 31.
    Crabtree GR, Schreiber SL (2009) SnapShot: Ca2+−calcineurin-NFAT signaling. Cell 138:210, 210 e211PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Auslander D, Fussenegger M (2012) Optogenetic therapeutic cell implants. Gastroenterology 143:301–306PubMedCrossRefGoogle Scholar
  33. 33.
    Koizumi A, Tanaka KF, Yamanaka A (2012) The manipulation of neural and cellular activities by ectopic expression of melanopsin. Neurosci Res 75:3–5PubMedCrossRefGoogle Scholar
  34. 34.
    Tsunematsu T, Tanaka KF, Yamanaka A et al (2012) Ectopic expression of melanopsin in orexin/hypocretin neurons enables control of wakefulness of mice in vivo by blue light. Neurosci Res 75:23–28PubMedCrossRefGoogle Scholar
  35. 35.
    Cao P, Sun W, Kramp K et al (2012) Light-sensitive coupling of rhodopsin and melanopsin to G(i/o) and G(q) signal transduction in Caenorhabditis elegans. FASEB J 26:480–491PubMedCrossRefGoogle Scholar
  36. 36.
    Yau KW, Hardie RC (2009) Phototransduction motifs and variations. Cell 139:246–264PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Koyanagi M, Takano K, Tsukamoto H et al (2008) Jellyfish vision starts with cAMP signaling mediated by opsin-G(s) cascade. Proc Natl Acad Sci U S A 105:15576–15580PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Bailes HJ, Zhuang LY, Lucas RJ (2012) Reproducible and sustained regulation of Galphas signalling using a metazoan opsin as an optogenetic tool. PLoS One 7:e30774PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Ryu MH, Moskvin OV, Siltberg-Liberles J et al (2010) Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J Biol Chem 285:41501–41508PubMedCrossRefGoogle Scholar
  40. 40.
    Stierl M, Stumpf P, Udwari D et al (2011) Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa. J Biol Chem 286:1181–1188PubMedCrossRefGoogle Scholar
  41. 41.
    Schroder-Lang S, Schwarzel M, Seifert R et al (2007) Fast manipulation of cellular cAMP level by light in vivo. Nat Methods 4:39–42PubMedCrossRefGoogle Scholar
  42. 42.
    Nagahama T, Suzuki T, Yoshikawa S et al (2007) Functional transplant of photoactivated adenylyl cyclase (PAC) into Aplysia sensory neurons. Neurosci Res 59:81–88PubMedCrossRefGoogle Scholar
  43. 43.
    Wu YI, Frey D, Lungu OI et al (2009) A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461:104–108PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Levskaya A, Weiner OD, Lim WA et al (2009) Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461:997–1001PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Dietz DM, Sun H, Lobo MK et al (2012) Rac1 is essential in cocaine-induced structural plasticity of nucleus accumbens neurons. Nat Neurosci 15:891–896PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Welch CM, Elliott H, Danuser G et al (2011) Imaging the coordination of multiple signalling activities in living cells. Nat Rev Mol Cell Biol 12:749–756PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Olivia A. Masseck
    • 1
  • Melanie D. Mark
    • 1
  • Stefan Herlitze
    • 1
  1. 1.Department of Zoology and NeurobiologyRuhr-University BochumBochumGermany

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