Caged vanilloid ligands for activation of TRPV1 receptors by 1- and 2-photon excitation

Biochemistry

Volumn 45, Issue 15, 2006, Pages 4915-4926

  Zhao, Jun ^a   Gover, Tony D ^b   Muralidharan, Sukumaran ^a   Auston, Darryl A ^a,c   Weinreich, Daniel ^b,c   Kao, Joseph P Y ^a,b,c  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MATERIALS; PHOTONS; POSITIVE IONS; QUANTUM EFFICIENCY; SENSORS; ULTRAVIOLET RADIATION;

CAGED VANILLOID LIGANDS; INTRACELLULAR STORES; PHOTON EXCITATION;

NEUROLOGY;

CALCIUM; CAPSAICIN; CAPSAZEPINE; CATION CHANNEL; FLUO 3; VANILLOID RECEPTOR 1;

ANIMAL CELL; ARTICLE; CHEMICAL STRUCTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DECARBOXYLATION; FLUORESCENCE MICROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIGHT ABSORPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PHOTOLYSIS; PHOTON; PRIORITY JOURNAL; QUANTUM YIELD; RAT; RECEPTOR UPREGULATION; SENSORY NERVE CELL; SPINAL GANGLION; VOLTAGE CLAMP;

ANIMALS; LIGANDS; MALE; MICROSCOPY, CONFOCAL; NEURONS; PHOTOLYSIS; PHOTONS; RATS; RATS, SPRAGUE-DAWLEY; TRPV CATION CHANNELS; VANILLIC ACID;

ANIMALIA; CAPSICUM FRUTESCENS;

EID: 33645947960     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052082f     Document Type: Article

References (47)

1. Perl, E. R. (1996) Pain and the Discovery of Nociceptors, in Neurobiology of Nociceptors (Belmonte, C., and Cervero, F., Eds.) pp 5-36, Oxford University Press, New York.
2. Wood, J. N., Winter, J., James, I. F., Rang, H. P., Yeats, J., and Bevan, S. (1988) Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture, J. Neurosci. 8, 3208-3220.
3. Bevan, S. J., and Docherty, R. J. (1993) Cellular Mechanisms of the Action of Capsaicin, in Capsaicin in the Study of Pain (Wood, J. N., Ed.) pp 2-44, Academic Press, London.
4. Walpole, C. S. J., and Wrigglesworth, R. (1993) Structural Requirements for Capsaicin Agonists and Antagonists, in Capsaicin in the Study of Pain (Wood, J. N., Ed.) pp 63-81, Academic Press, London.
5. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., and Julius, D. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway, Nature 389, 816-824.
6. Kaplan, J. H., Forbush, B., III, and Hoffman, J. F. (1978) 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.
7. Adams, S. R., and Tsien, R. Y. (1993) Controlling cell chemistry with caged compounds, Annu. Rev. Physiol. 55, 755-784.
8. Kao, J. P. Y., and Adams, S. R. (1993) Photosensitive caged compounds. Design, properties, and biological applications, in Optical Microscopy: Emerging Methods and Applications (Herman, B., and Lemasters, J. J., Eds.) pp 27-85, Academic Press, San Diego.
9. Nerbonne, J. M. (1996) Caged compounds: tools for illuminating neuronal responses and connections, Curr. Opin. Neurobiol. 6, 379-386.
10. Marriott, G., and Walker, J. W. (1999) Caged peptides and proteins: new probes to study polypeptide function in complex biological systems, Trends Plant Sci. 4, 330-334.
11. Shigeri, Y., Tatsu, Y., and Yumoto, N. (2001) Synthesis and application of caged peptides and proteins, Pharmacol. Ther. 91, 85-92.
12. Lawrence, D. S. (2005) The preparation and in vivo applications of caged peptides and proteins, Curr. Opin. Chem. Biol. 9, 570-575.
13. de Mayo, P., and Shizuka, H. (1976) Measurements of Reaction Quantum Yields, in Creation and Detection of Excited States (Ware, W. R., Ed.) Vol. 4, pp 139-215, Marcel Dekker, Inc., New York.
14. Hatchard, C. G., and Parker, C. A. (1956) A new sensitive chemical actinometer. II. Potassium ferrioxalate as a standard chemical actinometer, Proc. R. Soc. London, Ser. A 235, 518-536.
15. - conductances in vagal afferent neurones of the guinea pig, J. Physiol. 558, 513-526.
16. Walpole, C. S. J., Wrigglesworth, R., Bevan, S., Campbell, E. A., Dray, A., James, I. F., Masdin, K. J., Perkins, M. N., and Winter, J. (1993) Analogues of capsaicin with agonist activity as novel analgesic agents; structure-activity studies. 3. The hydrophobic side-chain "C-region", J. Med. Chem. 36, 2381-2389.
17. Walpole, C. S. J., Wrigglesworth, R., Bevan, S., Campbell, E. A., Dray, A., James, I. F., Masdin, K. J., Perkins, M. N., and Winter, J. (1993) Analogues of capsaicin with agonist activity as novel analgesic agents; structure-activity studes. 2. The amide bond "B-region", J. Med. Chem. 36, 2373-2380.
18. Lang, W., Qin, C., Lin, S., Khanolkar, A. D., Goutopoulos, A., Fan, P., Abouzid, K., Meng, Z., Biegel, D., Makriyannis, A. (1999) Substrate specificity and stereoselectivity of rat brain microsomal anandamide amidohydrolase, J. Med. Chem. 42, 896-902.
19. Katritzky, A. R., Xu, Y.-J., Vakulenko, A. V., Wilcox, A. L., and Bley, K. R. (2003) Model compounds of caged capsaicin: Design, synthesis, and photoreactivity, J. Org. Chem. 68, 9100-9104.
20. Zemelman, B. V., Nesnas, N., Lee, G. A., and Miesenböck, G. (2003) Photochemical gating of heterologous ion channels: Remote control over genetically designated populations of neurons, Proc. Natl. Acad. Sci. U.S.A. 100, 1352-1357.
21. Muralidharan S., and Nerbonne, J. M. (1995) Photolabile "caged" adrenergic receptor agonists and related model compounds, J. Photochem. Photobiol. B 27, 123-137.
22. 2+ ATPase activity with light flashes, J. Biol. Chem. 272, 3266-3271.
23. Rossi, F. M., Margulis, M., Tang, C.-M., and Kao, J. P. Y. (1997) N-Nmoc-glutamate: A new caged glutamate with high chemical stability and low pre-photolysis activity, J. Biol. Chem. 272, 32933-32939.
24. Yip, R. D., Sharma, D. K., Giasson, R., and Gravel, D. (1985) Photochemistry of the o-nitrobenzyl system in solution: evidence for singlet-state intramolecular hydrogen abstraction, J. Phys. Chem. 89, 5328-5330.
25. Schupp, H., Wong, W. K., and Schnabel, W. (1987) Mechanistic studies of the photorearrangement of o-nitrobenzyl esters, J. Photochem. 36, 85-97.
26. Zhu, Q. Q., Schnabel, W., and Schupp, H. (1987) Formation and decay of nitronic acid in the photorearrangement of o-nitrobenzyl esters, J. Photochem. 39, 317-332.
27. Yip, R. W., Wen, Y. X., Gravel, D., Giasson, R., and Sharma, D. K. (1991) Photochemistry of the o-nitrobenzyl system in solution: identification of the biradical intermediate in the intramolecular rearrangement, J. Phys. Chem. 95, 6078-6081.
28. Walker, J. W., Reid, G. P., McCray, J. A., and Trentham, D. R. (1988) Photolabile 1-(2-nitrophenyl)ethyl phosphate esters of adenine nucleotide analogs. Synthesis and mechanism of photolysis, J. Am. Chem. Soc. 110, 7170-7177.
29. McCray, J. A., and Trentham, D. R. (1989) Properties and uses of photoreactive caged compounds, Annu. Rev. Biophys. Biophys. Chem. 18, 239-270.
30. Sauers, C. K., Jencks, W. P., and Groh, S. (1975) The alcohol-bicarbonate-water system. Structure-reactivity studies on the equilibria for formation of alkyl monocarbonates and on the rates of their decomposition in aqueous alkali, J. Am. Chem. Soc. 97, 5546-5553.
31. Biggs, A. I., and Robinson, R. A. (1961) The ionisation constants of some substituted anilines and phenols: a test of the Hammett relation, J. Chem. Soc. 388-393.
32. a Prediction for Organic Acids and Bases, Chapman and Hall, London.
33. Winter J. (1987) Characterization of capsaicin-sensitive neurones in adult rat dorsal root ganglion cultures, Neurosci. Lett. 80, 134-140.
34. Cardenas, C. G., Del Mar, L. P., and Scrogg, R. S. (1995) Variation in serotonergic inhibition of calcium channel currents in four types of rat sensory neurons differentiated by membrane properties, J. Neurophysiol. 74, 1870-1879.
35. Bevan, S., Hothi, S., Hughes, G., James, I. F., Rang, H. P., Shah, K., Walpole, C. J. S., and Yeats, J. C. (1992) Capsazepine: a competitive antagonist of the sensory neurone excitant capsaicin, Br. J. Pharmacol. 107, 544-552.
36. Marsh, S. J., Stansfeld, C. E., Brown, D. A., Davey, R., and McCarthy, D. (1987) The mechanism of action of capsaicin on sensory C-type neurons and their axons in vitro, Neuroscience 23, 275-289.
37. Boyd, R. W. (2003) Nonlinear Optics, 2nd ed., pp 515-532, Academic Press, San Diego.
38. 2+ stores in the dorsal root ganglion cells of adult rats, Biochem. Biophys. Res. Commun. 285, 1114-1120.
39. 2+ by vanilloid receptor I in rat dorsal root ganglion neurons, J. Biol. Chem. 278, 5462-5472.
40. Koplas, P. A., Rosenberg, R. L., and Oxford, G. S. (1997) The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons, J. Neurosci. 17, 3525-3537.
41. Gunthorpe, M. J., Harries, M. H., Prinjha, R. K., Davis, J. B., Randall, A. (2000) Voltage- and time-dependent properties of the recombinant rat vanilloid receptor (rVR1), J. Physiol. 525, 747-759.
42. Jung, J., Hwang, S. W., Kwak, J., Lee, S. Y., Kang, C. J., Kim, W. B., Kim, D., and Oh, U. (1999) Capsaicin binds to the intracellular domain of the capsaicin-activated ion channel, J. Neurosci. 19, 529-538.
43. Furuta, T., Wang, S. S., Dantzker, J. L., Dore, T. M., Bybee, W. J., Callaway, E. M., Denk, W., and Tsien, R. Y. (1999) Brominated 7-hydroxycoumarin-4-ylmethyls: photolabile protecting groups with biologically useful cross-sections for two photon photolysis, Proc. Natl. Acad. Sci. U.S.A., 96, 1193-1200.
44. Tominaga, M., Caterina, M. J., Malmberg, A. B., Rosen, T. A., Gilbert, H., Skinner, K., Raumann, B. E., Basbaum, A. I., Julius, D. (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli, Neuron 21, 531-543.
45. Williams, R. M., Piston, D. W., Webb, W. W. (1994) Two-photon molecular excitation provides intrinsic 3-dimensional resolution for laser-based microscopy and microphotochemistry, FASEB J. 8, 804-813.
46. Zander, E., Weddell, G. (1951) Observations on the innervation of the cornea, J. Anat. 85, 68-69.
47. MacIver, M. B., Tanelian, D. L. (1993) Structural and functional specialization of Aδ and C fiber free nerve endings innervating rabbit corneal epithelium, J. Neurosci. 13, 4511-4524.