Advertisement

Caged Compounds: Applications in Cardiac Muscle Research

  • Ernst Niggli
  • Natalia Shirokova
Chapter

Abstract

Photolysis of “caged compounds” is a powerful biophysical technique with the capability to very rapidly convert inert chemicals into their biologically active form with a flash of light. The resulting concentration jumps allow to probe biological functions with exceptional temporal resolution, and in conjunction with imaging techniques, with excellent spatial precision. This chapter presents an overview of various applications for photolysis of caged compounds in the exploration of cardiac muscle function. After a synopsis of general features of caged compounds, studies focusing on several areas of cardiac muscle research are briefly described together with examples of caged compounds used in that particular field of research. Finally, more general information is presented regarding the methods and instrumentation available to apply these techniques, but also with reference to possible problems and pitfalls that need to be considered. Finally, an outlook into future developments of this and related technologies is outlined.

Notes

Acknowledgements

This work was supported by the Swiss National Science Foundation (31-132689 and 31-156375 to E.N.), by the National Institutes of Health (NIH; R01AR053933 and R01HL093342 to N.S), by the Swiss Foundation for Research on Muscle diseases and by the Microscopy Imaging Center (MIC) of the University of Bern (to E.N. and N.S.).

References

  1. 1.
    Severs NJ. The cardiac muscle cell. Bioessays. 2000;22:188–99. https://doi.org/10.1002/(SICI)1521-1878(200002)22:2<188::AID-BIES10>3.0.CO;2-T.CrossRefPubMedGoogle Scholar
  2. 2.
    Ellis-Davies GCR. Caged compounds: photorelease technology for control of cellular chemistry and physiology. Nat Methods. 2007;4:619–28.  https://doi.org/10.1038/nmeth1072.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    McCray JA, Trentham DR. Properties and uses of photoreactive caged compounds. Annu Rev Biophys Biophys Chem. 1989;18:239–70.  https://doi.org/10.1146/annurev.bb.18.060189.001323.CrossRefPubMedGoogle Scholar
  4. 4.
    Escobar AL, Velez P, Kim AM, et al. Kinetic properties of DM-nitrophen and calcium indicators: rapid transient response to flash photolysis. Pflugers Arch. 1997;434:615–31.  https://doi.org/10.1007/s004240050444.CrossRefPubMedGoogle Scholar
  5. 5.
    Zucker RS. Effects of photolabile calcium chelators on fluorescent calcium indicators. Cell Calcium. 1992;13:29–40.CrossRefPubMedGoogle Scholar
  6. 6.
    Brieke C, Rohrbach F, Gottschalk A, et al. Light-controlled tools. Angew Chem Int Ed Engl. 2012;51:8446–76.  https://doi.org/10.1002/anie.201202134.CrossRefPubMedGoogle Scholar
  7. 7.
    Kaplan JH, Ellis-Davies GCR. Photolabile chelators for the rapid photorelease of divalent cations. Proc Natl Acad Sci U S A. 1988;85:6571–5.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Ellis-Davies GCR, Kaplan JH. Nitrophenyl-EGTA, a photolabile chelator that selectively binds Ca2+ with high affinity and releases it rapidly upon photolysis. Proc Natl Acad Sci U S A. 1994;91:187–91.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Adams SR, Kao JPY, Grynkiewicz G, et al. Biologically useful chelators that release Ca2+ upon illumination. J Am Chem Soc. 1988;110:3212–20.  https://doi.org/10.1021/ja00218a034.CrossRefGoogle Scholar
  10. 10.
    Adams SR, Kao JPY, Tsien RY. Biologically useful chelators that take up Ca2+ upon illumination. J Am Chem Soc. 1989;111:7957–68.  https://doi.org/10.1021/ja00202a042.CrossRefGoogle Scholar
  11. 11.
    Lipp P, Lüscher C, Niggli E. Photolysis of caged compounds characterized by ratiometric confocal microscopy: a new approach to homogeneously control and measure the calcium concentration in cardiac myocytes. Cell Calcium. 1996;19:255–66.CrossRefPubMedGoogle Scholar
  12. 12.
    Fabiato A. Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985;85:247–89.CrossRefPubMedGoogle Scholar
  13. 13.
    Peterson BZ, DeMaria CD, Adelman JP, Yue DT. Calmodulin is the Ca2+ sensor for Ca2+ -dependent inactivation of L-type calcium channels. Neuron. 1999;22:549–58.CrossRefGoogle Scholar
  14. 14.
    Zühlke RD, Pitt GS, Deisseroth K, et al. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature. 1999;399:159–62.  https://doi.org/10.1038/20200.CrossRefPubMedGoogle Scholar
  15. 15.
    Gurney AM, Charnet P, Pye JM, Nargeot J. Augmentation of cardiac calcium current by flash photolysis of intracellular caged-Ca2+ molecules. Nature. 1989;341:65–8.  https://doi.org/10.1038/341065a0.CrossRefPubMedGoogle Scholar
  16. 16.
    Bates SE, Gurney AM. Ca2+-dependent block and potentiation of L-type calcium current in guinea-pig ventricular myocytes. J Physiol. 1993;466:345–65.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Hadley RW, Lederer WJ. Ca2+ and voltage inactivate Ca2+ channels in guinea-pig ventricular myocytes through independent mechanisms. J Physiol. 1991;444:257–68.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Niggli E, Lederer WJ. Activation of Na-Ca exchange current by photolysis of caged calcium. Biophys J. 1993;65:882–91.  https://doi.org/10.1016/S0006-3495(93)81105-6.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    DelPrincipe F, Egger M, Niggli E. Calcium signalling in cardiac muscle: refractoriness revealed by coherent activation. Nat Cell Biol. 1999;1:323–9.  https://doi.org/10.1038/14013.CrossRefPubMedGoogle Scholar
  20. 20.
    Szentesi P, Pignier C, Egger M, et al. Sarcoplasmic reticulum Ca2+ refilling controls recovery from Ca2+-induced Ca2+ release refractoriness in heart muscle. Circ Res. 2004;95:807–13.  https://doi.org/10.1161/01.RES.0000146029.80463.7d.CrossRefPubMedGoogle Scholar
  21. 21.
    Kappl M, Nagel G, Hartung K. Voltage and Ca2+ dependence of pre-steady-state currents of the Na-Ca exchanger generated by Ca2+ concentration jumps. Biophys J. 2001;81:2628–38.  https://doi.org/10.1016/S0006-3495(01)75906-1.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Niggli E, Lederer WJ. Molecular operations of the sodium-calcium exchanger revealed by conformation currents. Nature. 1991a;349:621–4.  https://doi.org/10.1038/349621a0.CrossRefPubMedGoogle Scholar
  23. 23.
    Kentish JC, Barsotti RJ, Lea TJ, et al. Calcium release from cardiac sarcoplasmic reticulum induced by photorelease of calcium or Ins(1,4,5)P3. Am J Physiol. 1990;258:H610–5.CrossRefPubMedGoogle Scholar
  24. 24.
    Näbauer M, Morad M. Ca2+-induced Ca2+ release as examined by photolysis of caged Ca2+ in single ventricular myocytes. Am J Physiol. 1990;258:C189–93.CrossRefPubMedGoogle Scholar
  25. 25.
    Niggli E, Lederer WJ. Voltage-independent calcium release in heart muscle. Science. 1990;250:565–8.CrossRefPubMedGoogle Scholar
  26. 26.
    Valdeolmillos M, O’Neill SC, Smith GL, Eisner DA. Calcium-induced calcium release activates contraction in intact cardiac cells. Pflugers Arch. 1989;413:676–8.CrossRefPubMedGoogle Scholar
  27. 27.
    Shirokova N, Rios E. Small event Ca2+ release: a probable precursor of Ca2+ sparks in frog skeletal muscle. J Physiol. 1997;502:3–11.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Cannell MB, Berlin JR, Lederer WJ. Effect of membrane potential changes on the calcium transient in single rat cardiac muscle cells. Science. 1987;238:1419–23.CrossRefPubMedGoogle Scholar
  29. 29.
    Hobai IA, Howarth FC, Pabbathi VK, et al. “Voltage-activated Ca release” in rabbit, rat and guinea-pig cardiac myocytes, and modulation by internal cAMP. Pflugers Arch. 1997;435:164–73.CrossRefPubMedGoogle Scholar
  30. 30.
    Cheng H, Lederer WJ, Cannell MB. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science. 1993;262:740–4.CrossRefPubMedGoogle Scholar
  31. 31.
    Klein MG, Cheng H, Santana LF, et al. Two mechanisms of quantized calcium release in skeletal muscle. Nature. 1996;379:455–8.  https://doi.org/10.1038/379455a0.CrossRefPubMedGoogle Scholar
  32. 32.
    Shirokova N, García J, Rios E. Local calcium release in mammalian skeletal muscle. J Physiol (Lond). 1998;512:377–84.CrossRefGoogle Scholar
  33. 33.
    Niggli E, Shirokova N. A guide to sparkology: the taxonomy of elementary cellular Ca2+ signaling events. Cell Calcium. 2007;42:379–87.  https://doi.org/10.1016/j.ceca.2007.02.010.CrossRefPubMedGoogle Scholar
  34. 34.
    Lipp P, Niggli E. Submicroscopic calcium signals as fundamental events of excitation--contraction coupling in guinea-pig cardiac myocytes. J Physiol (Lond). 1996;492:31–8.CrossRefGoogle Scholar
  35. 35.
    Shirokova N, Niggli E. Studies of RyR function in situ. Methods. 2008;46:183–93.  https://doi.org/10.1016/j.ymeth.2008.09.017.CrossRefPubMedGoogle Scholar
  36. 36.
    Lipp P, Niggli E. Fundamental calcium release events revealed by two-photon excitation photolysis of caged calcium in Guinea-pig cardiac myocytes. J Physiol (Lond). 1998;508:801–9.CrossRefGoogle Scholar
  37. 37.
    Brochet DXP, Xie W, Yang D, et al. Quarky calcium release in the heart. Circ Res. 2011;108:210–8.  https://doi.org/10.1161/CIRCRESAHA.110.231258.CrossRefPubMedGoogle Scholar
  38. 38.
    Stern MD. Theory of excitation-contraction coupling in cardiac muscle. Biophys J. 1992;63:497–517.  https://doi.org/10.1016/S0006-3495(92)81615-6.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Terentyev D, Viatchenko-Karpinski S, Valdivia HH, et al. Luminal Ca2+ controls termination and refractory behavior of Ca2+-induced Ca2+ release in cardiac myocytes. Circ Res. 2002;91:414–20.CrossRefPubMedGoogle Scholar
  40. 40.
    Gillespie D, Fill M. Pernicious attrition and inter-RyR2 CICR current control in cardiac muscle. J Mol Cell Cardiol. 2013;58:53–8.  https://doi.org/10.1016/j.yjmcc.2013.01.011.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Laver DR, Kong CHT, Imtiaz MS, Cannell MB. Termination of calcium-induced calcium release by induction decay: an emergent property of stochastic channel gating and molecular scale architecture. J Mol Cell Cardiol. 2013;54:98–100.  https://doi.org/10.1016/j.yjmcc.2012.10.009.CrossRefPubMedGoogle Scholar
  42. 42.
    Györke S, Fill M. Ryanodine receptor adaptation: control mechanism of Ca2+-induced Ca2+ release in heart. Science. 1993;260:807–9.CrossRefPubMedGoogle Scholar
  43. 43.
    Valdivia HH, Kaplan JH, Ellis-Davies GCR, Lederer WJ. Rapid adaptation of cardiac ryanodine receptors: modulation by Mg2+ and phosphorylation. Science. 1995;267:1997–2000.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Lindegger N, Niggli E. Paradoxical SR Ca2+ release in guinea-pig cardiac myocytes after beta-adrenergic stimulation revealed by two-photon photolysis of caged Ca2+. J Physiol (Lond). 2005;565:801–13.  https://doi.org/10.1113/jphysiol.2005.084376.CrossRefGoogle Scholar
  45. 45.
    Ogrodnik J, Niggli E. Increased Ca2+ leak and spatiotemporal coherence of Ca2+ release in cardiomyocytes during beta-adrenergic stimulation. J Physiol (Lond). 2010;588:225–42.  https://doi.org/10.1113/jphysiol.2009.181800.CrossRefGoogle Scholar
  46. 46.
    Gutierrez DA, Fernandez-Tenorio M, Ogrodnik J, Niggli E. NO-dependent CaMKII activation during β-adrenergic stimulation of cardiac muscle. Cardiovasc Res. 2013;100:392–401.  https://doi.org/10.1093/cvr/cvt201.CrossRefPubMedGoogle Scholar
  47. 47.
    Barsotti RJ, Ferenczi MA. Kinetics of ATP hydrolysis and tension production in skinned cardiac muscle of the guinea pig. J Biol Chem. 1988;263:16750–6.PubMedGoogle Scholar
  48. 48.
    Martin H, Barsotti RJ. Relaxation from rigor of skinned trabeculae of the guinea pig induced by laser photolysis of caged ATP. Biophys J. 1994;66:1115–28.  https://doi.org/10.1016/S0006-3495(94)80892-6.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Iribe G, Ward CW, Camelliti P, et al. Axial stretch of rat single ventricular cardiomyocytes causes an acute and transient increase in Ca2+ spark rate. Circ Res. 2009;104:787–95.  https://doi.org/10.1161/CIRCRESAHA.108.193334.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Niggli E, Lederer WJ. Restoring forces in cardiac myocytes. Insight from relaxations induced by photolysis of caged ATP. Biophys J. 1991b;59:1123–35.  https://doi.org/10.1016/S0006-3495(91)82327-X.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Il’ichev YV, Schwörer MA, Wirz J. Photochemical reaction mechanisms of 2-nitrobenzyl compounds: methyl ethers and caged ATP. J Am Chem Soc. 2004;126:4581–95.  https://doi.org/10.1021/ja039071z.CrossRefPubMedGoogle Scholar
  52. 52.
    Frace AM, Méry PF, Fischmeister R, Hartzell HC. Rate-limiting steps in the beta-adrenergic stimulation of cardiac calcium current. J Gen Physiol. 1993;101:337–53.CrossRefPubMedGoogle Scholar
  53. 53.
    Nakashima Y, Ono K. Rate-limiting steps in activation of cardiac Cl current revealed by photolytic application of cAMP. Am J Physiol. 1994;267:H1514–22.PubMedGoogle Scholar
  54. 54.
    Fischmeister R, Castro LRV, Abi-Gerges A, et al. Compartmentation of cyclic nucleotide signaling in the heart: the role of cyclic nucleotide phosphodiesterases. Circ Res. 2006;99:816–28.  https://doi.org/10.1161/01.RES.0000246118.98832.04.CrossRefPubMedGoogle Scholar
  55. 55.
    Saucerman JJ, Zhang J, Martin JC, et al. Systems analysis of PKA-mediated phosphorylation gradients in live cardiac myocytes. Proc Natl Acad Sci U S A. 2006;103:12923–8.  https://doi.org/10.1073/pnas.0600137103.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Nakayama H, Bodi I, Maillet M, et al. The IP3 receptor regulates cardiac hypertrophy in response to select stimuli. Circ Res. 2010;107:659–66.  https://doi.org/10.1161/CIRCRESAHA.110.220038.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Yamada J, Ohkusa T, Nao T, et al. Up-regulation of inositol 1,4,5 trisphosphate receptor expression in atrial tissue in patients with chronic atrial fibrillation. J Am Coll Cardiol. 2001;37:1111–9.  https://doi.org/10.1016/S0735-1097(01)01144-5.CrossRefGoogle Scholar
  58. 58.
    Wu X, Zhang T, Bossuyt J, et al. Local InsP3-dependent perinuclear Ca2+ signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest. 2006;116:675–82.  https://doi.org/10.1172/JCI27374.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Jaconi M, Bony C, Richards SM, et al. Inositol 1,4,5-trisphosphate directs Ca2+ flow between mitochondria and the endoplasmic/sarcoplasmic reticulum: a role in regulating cardiac autonomic Ca2+ spiking. Mol Biol Cell. 2000;11:1845–58.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Horn T, Ullrich ND, Egger M. “Eventless” InsP3-dependent SR-Ca2+ release affecting atrial Ca2+ sparks. J Physiol (Lond). 2013;591:2103–11.  https://doi.org/10.1113/jphysiol.2012.247288.CrossRefGoogle Scholar
  61. 61.
    Hohendanner F, Walther S, Maxwell JT, et al. Inositol-1,4,5-trisphosphate induced Ca2+ release and excitation-contraction coupling in atrial myocytes from normal and failing hearts. J Physiol (Lond). 2015;593:1459–77.  https://doi.org/10.1113/jphysiol.2014.283226.CrossRefGoogle Scholar
  62. 62.
    Keller M, Kao JPY, Egger M, Niggli E. Calcium waves driven by “sensitization” wave-fronts. Cardiovasc Res. 2007;74:39–45.  https://doi.org/10.1016/j.cardiores.2007.02.006.CrossRefPubMedGoogle Scholar
  63. 63.
    Ni J, Auston DA, Freilich DA, et al. Photochemical gating of intracellular Ca2+ release channels. J Am Chem Soc. 2007;129:5316–7.  https://doi.org/10.1021/ja069361q.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Avlonitis N, Chalmers S, McDougall C, et al. Caged AG10: new tools for spatially predefined mitochondrial uncoupling. Mol Biosyst. 2009;5:450–7.  https://doi.org/10.1039/b820415m.CrossRefPubMedGoogle Scholar
  65. 65.
    Guo X, Laflamme MA, Becker PL. Cyclic ADP-ribose does not regulate sarcoplasmic reticulum Ca2+ release in intact cardiac myocytes. Circ Res. 1996;79:147–51.CrossRefPubMedGoogle Scholar
  66. 66.
    Rapp G, Güth K. A low cost high intensity flash device for photolysis experiments. Pflugers Arch. 1988;411:200–3.CrossRefPubMedGoogle Scholar
  67. 67.
    Walker JW, Somlyo AV, Goldman YE, et al. Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate. Nature. 1987;327:249–52.  https://doi.org/10.1038/327249a0.CrossRefPubMedGoogle Scholar
  68. 68.
    Engert F, Paulus GG, Bonhoeffer T. A low-cost UV laser for flash photolysis of caged compounds. J Neurosci Methods. 1996;66:47–54.  https://doi.org/10.1016/0165-0270(95)00157-3.CrossRefPubMedGoogle Scholar
  69. 69.
    Trigo FF, Corrie JET, Ogden D. Laser photolysis of caged compounds at 405 nm: photochemical advantages, localisation, phototoxicity and methods for calibration. J Neurosci Methods. 2009;180:9–21.  https://doi.org/10.1016/j.jneumeth.2009.01.032.CrossRefPubMedGoogle Scholar
  70. 70.
    Bernardinelli Y, Haeberli C, Chatton J-Y. Flash photolysis using a light emitting diode: an efficient, compact, and affordable solution. Cell Calcium. 2005;37:565–72.  https://doi.org/10.1016/j.ceca.2005.03.001.CrossRefPubMedGoogle Scholar
  71. 71.
    Sobie EA, Kao JPY, Lederer WJ. Novel approach to real-time flash photolysis and confocal [Ca2+] imaging. Pflugers Arch. 2007;454:663–73.  https://doi.org/10.1007/s00424-007-0229-z.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Wang SS, Augustine GJ. Confocal imaging and local photolysis of caged compounds: dual probes of synaptic function. Neuron. 1995;15:755–60.CrossRefPubMedGoogle Scholar
  73. 73.
    Shkryl VM, Maxwell JT, Blatter LA. A novel method for spatially complex diffraction-limited photoactivation and photobleaching in living cells. J Physiol. 2012;590:1093–100.  https://doi.org/10.1113/jphysiol.2011.223446.CrossRefPubMedGoogle Scholar
  74. 74.
    Ellis-Davies GCR. DM-nitrophen AM is caged magnesium. Cell Calcium. 2006;39:471–3.  https://doi.org/10.1016/j.ceca.2006.02.002.CrossRefPubMedGoogle Scholar
  75. 75.
    Pelliccioli AP, Wirz J. Photoremovable protecting groups: reaction mechanisms and applications. Photochem Photobiol Sci. 2002;1:441–58.  https://doi.org/10.1039/b200777k.CrossRefPubMedGoogle Scholar
  76. 76.
    Kaplan JH, Forbush B, Hoffman JF. Rapid photolytic release of adenosine 5′-triphosphate from a protected analogue: utilization by the Na:K pump of human red blood cell ghosts. Biochemistry. 1978;17:1929–35.CrossRefPubMedGoogle Scholar
  77. 77.
    Goldman YE, Hibberd MG, Trentham DR. Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5′-triphosphate. J Physiol (Lond). 1984;354:577–604.CrossRefGoogle Scholar
  78. 78.
    Nichols CG, Niggli E, Lederer WJ. Modulation of ATP-sensitive potassium channel activity by flash-photolysis of “caged-ATP” in rat heart cells. Pflugers Arch. 1990;415:510–2.CrossRefPubMedGoogle Scholar
  79. 79.
    Hadley RW, Kirby MS, Lederer WJ, Kao JPY. Does the use of DM-nitrophen, nitr-5, or diazo-2 interfere with the measurement of indo-1 fluorescence? Biophys J. 1993;65:2537–46.  https://doi.org/10.1016/S0006-3495(93)81328-6.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Hagen V, Bendig J, Frings S, Eckardt T. Highly efficient and ultrafast phototriggers for cAMP and cGMP by using long‐wavelength UV/VIS‐activation. Angew Chem Int Ed Engl. 2001;40(6):1045. https://doi.org/10.1002/1521-3773(20010316)40:6<1045::AID-ANIE10450>3.0.CO;2-F.CrossRefPubMedGoogle Scholar
  81. 81.
    Momotake A, Lindegger N, Niggli E, et al. The nitrodibenzofuran chromophore: a new caging group for ultra-efficient photolysis in living cells. Nat Methods. 2006;3:35–40.  https://doi.org/10.1038/nmeth821.CrossRefPubMedGoogle Scholar
  82. 82.
    Kantevari S, Hoang CJ, Ogrodnik J, et al. Synthesis and two-photon photolysis of 6-(ortho-nitroveratryl)-caged IP3 in living cells. ChemBioChem. 2006;7:174–80.  https://doi.org/10.1002/cbic.200500345.CrossRefPubMedGoogle Scholar
  83. 83.
    Russell AG, Ragoussi M-E, Ramalho R, et al. Alpha-carboxy-6-nitroveratryl: a photolabile protecting group for carboxylic acids. J Org Chem. 2010;75:4648–51.  https://doi.org/10.1021/jo100783v.CrossRefPubMedGoogle Scholar
  84. 84.
    Agarwal HK, Janíček R, Chi S-H, et al. Calcium uncaging with visible light. J Am Chem Soc. 2016;138:3687–93.  https://doi.org/10.1021/jacs.5b11606.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Brown EB, Shear JB, Adams SR, et al. Photolysis of caged calcium in femtoliter volumes using two-photon excitation. Biophys J. 1999;76:489–99.  https://doi.org/10.1016/S0006-3495(99)77217-6.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Kantevari S, Matsuzaki M, Kanemoto Y, et al. Two-color, two-photon uncaging of glutamate and GABA. Nat Methods. 2010;7:123–5.  https://doi.org/10.1038/nmeth.1413.CrossRefPubMedGoogle Scholar
  87. 87.
    Olson JP, Banghart MR, Sabatini BL, Ellis-Davies GCR. Spectral evolution of a photochemical protecting group for orthogonal two-color uncaging with visible light. J Am Chem Soc. 2013;135:15948–54.  https://doi.org/10.1021/ja408225k.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Entcheva E. Cardiac optogenetics. Am J Physiol Heart Circ Physiol. 2013;304:H1179–91.  https://doi.org/10.1152/ajpheart.00432.2012.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of PhysiologyUniversity of BernBernSwitzerland
  2. 2.Department of Pharmacology, Physiology and NeuroscienceRutgers, The State University of New JerseyNewarkUSA

Personalised recommendations