Caged compounds: Photorelease technology for control of cellular chemistry and physiology

Nature Methods

Volumn 4, Issue 8, 2007, Pages 619-628

  Ellis Davies, Graham C R ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; COFILIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DNA FRAGMENT; EDETIC ACID; EGTAZIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; G ACTIN; GLUTAMIC ACID; MESSENGER RNA;

CELL FUNCTION; CHEMICAL STRUCTURE; CYTOCHEMISTRY; ENCAPSULATION; FLUORESCENCE MICROSCOPY; HUMAN; IRRADIATION; MACROMOLECULE; NERVE CELL; NONHUMAN; PATCH CLAMP; PHOTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION;

CYTOLOGY; MICROSCOPY, FLUORESCENCE; MOLECULAR PROBES; PHOTOCHEMISTRY;

EID: 34547638628     PISSN: 15487091     EISSN: 15491676     Source Type: Journal    
DOI: 10.1038/nmeth1072     Document Type: Review

References (99)

1. Mayer, G. & Heckel, A. Biologically active molecules with a "light switch". Angew. Chem. Int. Ed. 45, 4900-4921 (2006).
2. Berridge, M.J., Bootman, M.D. & Lipp, P. Calcium-life and death signal. Nature 395, 645-649 (1998).
3. 2+ upon illumination. J. Am. Chem. Soc. 110, 3212-3220 (1988).
4. Ellis-Davies, G.C.R. & Kaplan, J.H. A new class of photolabile chelators for the rapid release of divalent cations: Generation of caged Ca and caged Mg. J. Org. Chem. 53, 1966-1969 (1988).
5. 2+ with high affinity and releases it rapidly upon photolysis. Proc. Natl. Acad. Sci. USA 91, 187-191 (1994).
6. Ellis-Davies, G.C.R. Synthesis of photolabile EGTA derivatives. Tetrahedr. Lett. 39, 953-957 (1998).
7. Walker, J.W., McCray, J.A. & Hess, G.P. Photolabile protecting groups for an acetylcholine receptor ligand. Synthesis and photochemistry of a new class of o-nitrobenzyl derivatives and their effects on receptor function. Biochemistry 25, 1799-1805 (1986).
8. Milburn, T. et al. Synthesis, photochemistry and biological activity of a caged photolabile acetylcholine receptor ligand. Biochemistry 28, 49-55 (1989).
9. Wieboldt, R. et al. Photolabile precursors of gtutamate: Synthesis, photochemical properties, activation of glutamate receptors in the microsecond time scale. Proc. Natl. Acad. Sci. USA 91 8752-8756 (1994).
10. Matsuzaki, M. et al. Dendritic spine morphology is critical for AMPA receptor expression in hippocampat CA1 pyramidal neurons. Nat. Neurosci. 4, 1086-1092 (2001).
11. Walker, J.W. et al. Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate. Nature 327, 249-252 (1987).
12. Walker, J.W., Feeney, J. & Trentham, D.R. Photolabite precursors of inositot phosphates. Preparation and properties of 1-(2-nitrophenyl)ethyl esters of myo-inositol 1,4,5-trisphosphate. Biochemistry 28, 3272-3280 (1989).
13. Kaplan, J.H., Forbush, B. & Hoffman, J.F. Rapid photolytic release of adenosine 5′-triphosphate from a protected analogue: Utilization by the Na:K pump of human red blood cell ghosts. Biochemistry 17 1929-1935 (1979).
14. Walker, J.H., Reid, G.P., McCray, J.A. & Trentham, D.R. Phototabile 1-(2-nitrophenyl)ethyl phosphate esters of adenine nucleotide analogues. Synthesis and mechanism of photolysis. J. Am. Chem. Soc. 110 7170-7177 (1988).
15. Walker, J.W. et al. Signaling pathways underlying eosinophil cell motility revealed by using caged peptides. Proc. Natl. Acad. Sci. USA 95, 1568-1573 (1998).
16. Rothman, D.M. et al. Caged phosphoprateins. J. Am. Chem. Soc. 127, 846-847 (2005).
17. Marriott, G. Caged protein conjugates and light-directed generation of protein activity: Preparation, photoactivation, and spectroscopic characterization of caged G-actin conjugates. Biochemistry 33 9092-9097 (1994).
18. Mendel, D., Elman, J.A. & Schultz, P.G. Construction of light-activated protein-protein interactions. J. Am. Chem. Soc. 113, 2758-2760 (1991).
19. Ghosh, M. et al. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304, 743-746 (2004).
20. Ando, H., Furuta, T., Tsien, R.Y. & Okamoto, H. Photo-mediated gene activation using caged RNA/DNA in zebrafish embryos. Nat. Genet. 28, 317-325 (2001).
21. Monroe W.T., McQuain, M.M., Chang, M.S., Alexander, J.S. & Haselton, F.R. Targeting expression with light using caged DNA. J. Biol. Chem. 274, 20895-20900 (1999).
22. Kasai, H. Comparative biology of Ca-dependent exocytosis: Implications of Kinetic diversity for societory function. Trends Neurosi. 22 88-93 (1999).
23. Judkewitz, B., Roth, A. & Hausser, M. Dendritic enlightenment: Using patterned two-photon uncaging to reveal the secrets of the brain's smallest dendrites. Neuro 50, 180-183 (2006).
24. Pellicioli, A.P. & Wirz, J. Photoremovable protecting grouping: Reaction mechanisms and applications. Photochem. Photobiol. Sci. 1, 441-458 (2002).
25. McGall, G.H. et al. The efficiency of light-directed synthesis of DNA arrays on glass substrates. J. Am. Chem. Soc. 119, 5081-5090 (1997).
26. McGall, G.H. & Christians, F.C. High-density genechip oligonucleotide probe arrays. Adv. Biochem. Eng. Biotechnol. 77, 22-42 (2002).
27. Ellis-Davies, G.C.R. Caged Glutamate For Use in the CNS. New Encyclopedia of Neuroscience. (eds., Squire, L., Albright, T., Bloom, F., Gage, F. & Spritzer N.) (Elsevier, Oxford, in the press).
28. Gee, K.R., Wieboldt, R. & Hess, G.P. Synthesis and photochemistry of a new photolabile derivative of GABA. J. Am. Chem. Soc. 116, 8366-8367 (1994).
29. Molnar, P. & Nadler, J.V. γ-Aminobutyrate, a-carboxy-2-nitrobenzyl ester selectively blocks inhibitory synaptic transmission in rat dentate gyrus. Eur. J. Pharm. 391, 255-262 (2000).
30. Engels, J. & Schlaeger, E-J. Synthesis, structure and reactivity of adenosine cyclic 3′,5′-phosphate benzyl triesters. J. Med. Chem. 20, 907-911 (1977).
31. Dantzig, J.A., Higuchi, H. & Goldman, Y.E. Studies of molecular motors using caged compounds. Methods Enzymol. 291, 307-348 (1998).
32. 3 in cerebellar Purkinje neurones. Acta Physiol. Scan. 157, 381-394 (1996).
33. +-ATPase probed by presteady state and relaxation studies. J. Bionerg. Biomembr. 33, 401-405 (2001).
34. Wang, L., Corrie, J.L & Wootton, J.F. Photolabile precursors of cyclic nucleotides with high aqueous solubility and stability. J. Org. Chem. 67, 3474-3478 (2002).
35. Thirlwell, H. et al. Kinetics of relaxation from rigor of permeabilized fast-twitch skeletal fibers from the rabbit using a novel caged ATP and apyrase. Biophys. J. 67, 2436-2447 (1994).
36. +-ATPase. Biophys. J. 79, 1346-1357 (2000).
37. 3. ChemBioChem 7, 174-180 (2006).
38. Hagen, V. et al. Highly efficient and ultrafast phototriggers for cAMP and cGMP by using long-wavelength UV/vis-activation. Angew. Chem. Int. Ed. 40, 1045-1048 (2001).
39. Furuta, T. et al. Bhc-cNMPs as either water-soluble or membrane-permeant photoreleasable cyclic nucleotides for both one- and two-photon excitation. ChemBioChem 5, 1119-1128 (2004).
40. 2+ spike frequency can optimize gene expression. Nature 392, 936-941 (1998).
41. Ellis-Davies, G.C.R. Development and application of calcium cages. Meth Enzymol. 3160A, 226-238 (2003).
42. 2+, azid-1, is far more photosensitive than nitrobenzyl-based chelators. Chem. Biol. 4, 867-878 (1997).
43. Momotake, A., Lindegger, N., Niggli, N., Barsotti, R.J. & Ellis-Davies, G.C.R. The nitrodibenzofuran chromophore-a new caging group for ultra efficient photolysis in living cells. Nat. Methods 3, 35-40 (2006).
44. 2+ microdomains: New tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399 (1998).
45. 2+-triggered exocytosis. Science 298, 781-785 (2002).
46. Marriott, G., Roy, P. & Jakobson, K. Preparation and light-directed activation of caged proteins. Methods Enzymol. 360, 274-289 (2003).
47. Chang, C., Fernandez, T., Panchal, R. & Bayley, H. Caged catalytic subunit of cAMP-dependent protein Idnase. J. Am. Chem. Soc. 120 7661-7662 (1998).
48. Curley, K. & Lawrence D.S. Photoactivation of a signal transduction pathway in living cells. J. Am. Chem. Soc. 120, 8573-8574 (1998).
49. Petersson, E.J., Brandt, G.S., Zacharias, N.M., Dougherty, D.A. & Lester, H.A. Caging proteins through unnatural amino acid mutagenesis. Methods Enzymol. 360, 258-273 (2003).
50. Muralidharan, V. & Muir, T.W. Protein ligation: An enabling technology for the biophysical analysis of proteins. Nat. Methods 3, 429-438 (2006).
51. Hahn, M.E. & Muir, T.W. Photocontrol of Smad2, a multiphosphorylated cell-signaling protein, through caging of activating phosphoserines. Angew. Chem. Int. Ed. 43, 5800-5803 (2004).
52. Vazquez, M.E., Nitz, M., Stehn, J., Yaffe, M.B. & Imperiali, B. Fluorescent caged phosphoserine peptides as probes to investigate phosphorylation-dependent protein associations. J. Am. Chem. Soc. 125, 10150-10151 (2003).
53. Nguyen, A., Rothman, D.M., Stehn, J., Imperiali, B. & Yaffe, M.B. Caged phosphopeptides reveal a temporal role for 14-3-3 in G1 arrest and S-phase checkpoint function. Nat. Biotechnol. 22, 993-1000 (2004).
54. Wood, J.S., Koszelak, M., Liu, J. & Lawrence, D.S. A caged protein kinase inhibitor. J. Am. Chem. Soc. 120, 7145-7146 (1998).
55. Basques, U. & Imperiali, B. Photolytic control of peptide self-assembly. J. Am. Chem. Soc. 125, 7530-7531 (2003).
56. Ottl, J., Gariel, D. & Marriott, G. Preparation and photoactivation of caged fluorophores and caged proteins using a new class of heterobifunctional, photocleavable cross-linking reagents. Bioconjug. Chem. 9, 143-151 (1998).
57. Ando, H. & Okamoto, H. Practical procedures for ectopic induction of gene expression in zebrafish embryos using Bhc-diazo-caged mRNA. Methods Cell Sci. 25, 25-31 (2003).
58. Okamoto, H., Hirate, Y. & Ando, H. Systematic identification of factors in zebrafish regulating the early midbrain and cerebellar development by ordered differential display and caged mRNA technology. Front. Biosci. 9, 93-99 (2004).
59. Ando, H. et al. Lhx2 mediates the activity of Six3 in zebrafish fbrebrain growth. Dev. Biol. 287, 456-468 (2005).
60. Khan, S. et al. Excitatory signaling in bacterial probed by caged a chemoeffectors. Biophys. J. 65, 2368-2382 (1993).
61. Namiki, S., Arai, T. & Fujimori, K. High-performance caged nitric oxide: a new molecular design, synthesis and photochemical reaction. J. Am. Chem. Soc. 119, 2840-3841 (1997).
62. Goeldner, M. & Givens, R., eds. Dynamic Studies in Biology. (Wiley-VCH, Weinheim, Germany 2005)
63. Furuta, T. et al. Brominated 7-hydroxycoumarin-4-ylmethyls: photolabile protecting groups with biologically useful cross-sections for two-photon photolysis. Proc. Natl. Acad. Sci. USA 96, 1193-1200 (1999).
64. Papageorglou, G., Ogden, D.C., Barth, A. & Corrie, J.T. Photorelease of carboxylic acids from 1-acyl-7-nitroindolines in aqueous solution: Rapid and efficient photorelease of L-glutamate. J. AM. Chem. Soc. 121, 6503-6504 (1999).
65. Wettermark, G. Photochromism of o-nitrotoluenes. Nature 194, 677 (1962).
66. Gaplovsky, M. et al. Photochemical reaction mechanisms of 2-nitrobenzyl compounds: 2-nitrobenzyl alcohols form 2-nitroso hydrates by dual proton transfer. Photochem. Photobiol. Sci. 4, 33-42 (2005).
67. Hirayama, Y., Iwamura, M. & Furuta, T. Design, synthesis and photochemical properties of caged bile acids. Bioorg. Med. Chem. Lett. 13, 905-908 (2003).
68. Havinga, E., De Jongh, R.O. & Dorst, W. Photochemical acceleration of the hydrolysis of nitrophenyl phosphates and nitrophenyt sulfates. Recl. Thav. Chim. Pays-gas. 75, 378-383 (1956).
69. Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513-515 (1994).
70. Gillis, K.D., Mossner, R. & Neher, E. Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretary granules. Neuron 16, 1209-1220 (1996).
71. Xu, T., Naraghi, M., Kang, H. & Neher, E. Kinetic studies of Ca binding and Ca clearance in the cytosol of adrenal chromaffin cells. Biophys. J. 73, 532-545 (1997).
72. Beutner, D., Voets, T., Neher, E. & Moser, T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29, 681-690 (2001).
73. 2+ permeation in cyclic nucleotide-gated channels. EMBO J. 18, 131-144 (1999).
74. Rapp, G. et al. Lasers and flashlamps in research on the mechanism of muscle contraction. Ber. Bunsenges. Phys. Chem 93, 410-415 (1989).
75. Gomez, T.M., Robles, E., Poo, M. & Spitzer, N.C. Filopodial calcium transients promote substrate-dependent growth cone turning. Science 291, 1983-1988 (2001).
76. Fellin, T. et al. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43, 729-743 (2005).
77. Zimmermann, B., Ellis-Davies, G.C.R., Kaplan, J.H., Somlyo, A.V. & Somlyo, A.P. Kinetics of contractions initiated by photolysis of caged calcium and caged ATP in smooth muscle. J. Biol. Chem. 270, 23966-23874 (1995).
78. Denk, W. Two-photon scanning photochemical microscopy: Mapping ligand-gated ion channel distributions. Proc Natl. Acad. Sci. USA 91, 6629-6633 (1994).
79. Neher, E. & Zucker, R.S. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10, 21-30 (1993).
80. Thomas, P., Wong, P.G., Lee, A. & Almers, W. W. A low affinity Ca receptor controls the final steps in peptide secretion from pituitary metanotrophs. Neuron 11, 93-104 (1993).
81. Kasai, H. et al. Two components of exocytosis and endocytosis in phaeochromocytoma cells studied using caged Ca compounds. J. Physiol. 494, 53-65 (1996).
82. Schneggenburger, R. & Neher, E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406 889-893 (2000).
83. Bollmann, J.H. Sakmann, B. & Borst, J.G.G. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289, 953-957 (2000).
84. Khodakhah, K. & Ogden, D. Functional heterogeneity of calcium release by inositol trisphosphate in single Purkinje neurones, cultured cerebellar astrocytes, and peripheral tissues. Proc. Natl. Acad. Sci. USA 90, 4976-4980 (1993).
85. Kaplan, J.H. & Ellis-Davies, G.C.R. Photolabile chelators for the rapid photorelease of divalent cations. Proc. Natl. Acad. Sci. USA 85 6571-6575 (1988).
86. Gomez, T.M. & Spitzer, N.C. In vivo regulation of axon and pathfinding by growth cone calcium transients. Nature 397, 350-355 (1999).
87. 3 in Purkinje cell dendrites. Nature 396, 753-756 (1998).
88. Smith, M.A., Ellis-Davies, G.C.R. & Magee, J.C. Synaptic mechanisms of the distance-dependent scaling of Schaffer collateral synapses in CA1 pyramidal neurons. J. Physiol. 548, 245-258 (2003).
89. Carter, A.G. & Sabatini, B.L. State-dependent calcium signaling in dendritic spines of striatal medium spiny neurons. Neuron 44 483-493 (2004).
90. 2+] signaling in individual hippocampal dendritic spines. J. Neurosci. 25, 6037-6046 (2005).
91. Béïque, J.C., Da-Ting Lin, D.T., Kang, M.G., Aizawa, H., Takamiya, K. & and Huganir, R.L. Synapse-specific regulation of AMPA receptor function by PSD-95. Proc. Natl. Acad. Sci. USA 103, 19535-19540 (2006).
92. Katz, B. & Miledi, R. The effect of calcium on acetylcholine release from motor nerve terminals. Proc. Roy. Soc. B. Biol. Sci. 161 496-503 (1965).
93. Ellis-Davies, G.C.R., Momotake, M., Paukert, M., Kasai, H. & Bergles, D.W. 4-carboxymethoxy-5,7-dinitroindolinyl-Glu: An improved caged glutamate for expeditious ultraviolet and 2-photan photolysis in brain slices. J. Neurosci. 27, 6601-6604 (2007).
94. Banghart, M., Borges, K., Isacoff, E., Trauner, D. & Kramer, R.H. Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7, 1381-1386 (2004).
95. Kumita, J.R., Smart, O.S. & Woolley, G.A. Photo-control of helix content in a short peptide. Proc. Natl. Acad. Sci. USA 97, 3803-3808 (2000).
96. Shingyoji, C., Higuchi, H., Yoshimura, M., Katayama, E. & Yanagida, T. Dynein arms are oscillating force generators. Nature 393, 711-714 (1998).
97. Denk, W., Stricker, J.H. & Webb, W.W. Two-photon laser scanning fluorescence microscopy. Science 248, 73-76 (1990).
98. Brown, E.B. et al. Photolysis of caged calcium in femtaliter volumes using two-photon excitation. Biophys. J. 76, 489-499 (1999).
99. Huang, Y.H., Sinha, S.R., Fedoryak, O.D., Ellis-Davies, G.C.R. & Bergles, D.E. Synthesis and characterization of MNI-D-aspartate, a caged compound for selective activation of glutamate transporters and NMDA receptors in brain tissue. Biochemistry 44, 3316-3326 (2005).