Epinephrine produces a β-adrenergic receptor-mediated mechanical hyperalgesia and in vitro sensitization of rat nociceptors

Journal of Neurophysiology

Volumn 81, Issue 3, 1999, Pages 1104-1112

  Khasar, Sachia G ^a   Mccarter, Gordon ^a   Levine, Jon D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; BISINDOLYLMALEIMIDE; CHELERYTHRINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; MU OPIATE RECEPTOR ANTAGONIST; PROPRANOLOL; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR;

ADRENALIN RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; DEPOLARIZATION; HYPERALGESIA; MALE; MUSCLE SPINDLE AFFERENT NERVE; NOCICEPTIVE RECEPTOR; NONHUMAN; PRIORITY JOURNAL; RAT; SECOND MESSENGER; SENSITIZATION; SODIUM CURRENT; SPIKE; SPINAL GANGLION;

EID: 0032977884     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.81.3.1104     Document Type: Article

References (55)

1. AHLQUIST, R. P. Present state of alpha-and beta-adrenergic drugs. I. The adrenergic receptor. Am. Heart J. 92: 661-664, 1976.
2. AKOPIAN, A. N., SIVILOTTI, L., AND WOOD, J. N. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379: 257-262, 1996.
3. ALEY, K. O. AND LEVINE, J. D. Different mechanisms mediate development and expression of tolerance and dependence for peripheral mu-opioid antinociception in rat. J. Neurosci. 17: 8018-8023, 1997.
4. BACCAGLINI, P. I. AND HOGAN, P. G. Some rat sensory neurons in culture express characteristics of differentiated pain sensory cells. Proc. Natl. Acad. Sci. USA 80: 594-598, 1983.
5. BARON, R., JÄNIG, W. AND KOLLMANN, W. Sympathetic and afferent somata projecting in hindlimb nerves and the anatomical organization of the lumbar sympathetic nervous system of the rat. J. Comp. Neurol. 275: 460-468, 1988.
6. CESARE, P. AND MCNAUGHTON, P. A novel heat-activated current in nociceptive neurons and its sensitization by bradykinin. Proc. Natl. Acad. Sci. USA 93: 15435-15439, 1996.
7. CODERRE, T. J., BASBAUM, A. I., DALLMAN, M. F., HELMS, C., AND LEVINE, J. D. Epinephrine exacerbates arthritis by an action at presynaptic β2-adrenoceptors. Neuroscience 34: 521-523, 1990.
8. CRYER, P. E. Physiology and pathophysiology of the human sympathoadrenal neuroendocrine system. N. Engl. J. Med. 303: 436-444, 1980.
9. DETURCK, K. H. AND VOGEL, W. H. Factors influencing plasma catecholamine levels in rats during immobilization. Pharmacol. Biochem. Behav. 13: 129-131, 1980.
10. DRAGLAND, M. C., ROTHERMEL, J. D., HOULIHAN, M. J., AND BOTELHO, L. H. Inhibition of cyclic AMP-dependent protein kinase-induced changes in the kinetic properties of hepatic pyruvate kinase by the specific cyclic AMP antagonist, the (Rp)-diastereomer of adenosine cyclic 3',5'-phosphorothioate. J. Cyclic Nucleotide Protein Phosphorylation Res. 10: 371-382, 1985.
11. ENGLAND, S., BEVAN, S., AND DOCHERTY, R. J. PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase A cascade. J. Physiol. (Lond.) 495: 429-440, 1996.
12. ERIKSSON, B., SVEDENHAG, J., MARTINSSON, A., AND SYLVEN, C. Effect of epinephrine infusion on chest pain in syndrome X in the absence of signs of myocardial ischemia. Am. J. Cardiol. 15: 241-245, 1995.
13. 2+, isoprenaline, and PGE2. Adv. Prostaglandin Thromboxane Res. 8: 1207-1215, 1980.
14. GLASS, D. B., LUNDQUIST, L. J., KATZ, B. M., AND WALSH, D. A. Protein kinase inhibitor-(6-22)-amide peptide analogs with standard and nonstandard amino acid substitutions for phenylalanine 10. Inhibition of cAMP-dependent protein kinase. J. Biol. Chem. 264: 14579-14584, 1989.
15. GOLD, M. S., DASTMALCHI, S., AND LEVINE, J. D. Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro. Neuroscience 71: 265-275, 1996a.
16. + current in rat sensory neurons in vitro. Neurosci. Lett. 212: 83-86, 1996.
17. + current in nociceptors. Proc. Natl. Acad. Sci. USA 93: 1108-1112, 1996b.
18. HARRIS, D. N., ASAAD, M. M., PHILLIPS, M. B., GOLDENBERG, H. J., AND ANTONACCIO, M. J. Inhibition of adenylate cyclase in human blood platelets by 9-substituted adenine derivatives. J. Cyclic Nucleotide Res. 5: 125-134, 1979.
19. HERBERT, J. M., AUGEREAU, J. M., GLEYE, J., AND MAFFRAND, J. P. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 172: 993-999, 1990.
20. JÄNIG, W., LEVINE, J. D., AND MICHAELIS, M. Interactions of sympathetic and primary afferent neurons following nerve injury and tissue trauma. Prog. Brain Res. 113: 161-184, 1996.
21. KAPLAN, R., ROBINSON, C. A., SCAVULLI, J. F., AND VAUGHAN, J. H. Propranolol and the treatment of rheumatoid arthritis. Arthritis Rheum. 23: 253-255, 1980.
22. KAWANISHI, C., FUKUDA, M., TAMURA, R., NISHIJO, H., AND ONO, T. Effects of repeated cold stress on feeding, avoidance behavior, and pain-related nerve fiber activity. Physiol. Behav. 62: 849-855, 1997.
23. KHASAR, S. G., HO, T., GREEN, P. G., AND LEVINE, J. D. Comparison of prostaglandin E1-and prostaglandin E2-induced hyperalgesia in the rat. Neuroscience 62: 345-350, 1994.
24. KHASAR, S. G., MIAO, F. J., JÄNIG, W., AND LEVINE, J. D. Vagotomy-induced enhancement of mechanical hyperalgesia in the rat is sympathoadrenal-mediated. J. Neurosci. 18: 3043-3049, 1998.
25. KHASAR, S. G., OUSEPH, A. K., CHOU, B., HO, T., GREEN, P. G., AND LEVINE J. D. Is there more than one prostaglandin E receptor subtype mediating hyperalgesia in the rat hindpaw? Neuroscience 64: 1161-1165, 1995a.
26. KHASAR, S. G., WANG, J. F., TAIWO, Y. O., HELLER, P. H., GREEN, P. G., AND LEVINE, J. D. Mu-opioid agonist enhancement of prostaglandin-induced hyperalgesia in the rat: a G-protein beta-gamma subunit-mediated effect? Neuroscience 67: 189-195, 1995b.
27. LEMBECK, F., POPPER, H., AND JUAN, H. Release of prostaglandins by bradykinin as an intrinsic mechanism of its algesic effect. Naunyn Schmiedebergs Arch. Pharmacol. 294: 69-73, 1976.
28. LENG, S., MEUMURA, K., KODA, H., AND KUMAZAWA, T. Excitation and sensitization of the heat response induced by a phorbol ester in canine visceral polymodal receptors studied in vitro. Neurosci. Lett. 206: 13-16, 1996.
29. LEVINE, J. D., CODERRE, T. J., HELMS, C., AND BASBAUM, A. I. Beta 2-adrenergic mechanisms in experimental arthritis. Proc. Natl. Acad. Sci. USA 85: 4553-4556, 1988.
30. LEVINE, J. D. AND TAIWO, Y. O. Involvement of the mu-opiate receptor in peripheral analgesia. Neuroscience 32: 571-575, 1989.
31. LEVINE, J. D., TAIWO, Y. O., COLLINS, S. D., AND TAM, J. K. Noradrenaline hyperalgesia is mediated through interaction with sympathetic postganglionic neurone terminals rather than activation of primary afferent nociceptors. Nature 323: 158-160, 1986.
32. MAZZEO, R. S., RAJKUMAR, C., JENNINGS, G., AND ESLER, M. Norepinephrine spillover at rest and during submaximal exercise in young and old subjects. J. Appl. Physiol. 82: 1869-1874, 1997.
33. MIAO, F. J., JÄNIO, W., GREEN, P. G., AND LEVINE, J. D. Inhibition of bradykinin-induced synovial plasma extravasation produced by intrathecal nicotine is mediated by the hypothalamopituitary adrenal axis. J. Neurophysiol. 76: 2813-2821, 1996.
34. MIAO, F.J.P., KINNMAN, E., JÄNIG, W., AND LEVINE, J. D. Variation in the anatomy of the lumbar sympathetic chain in the rat. J. Auton. Nerv Sys. 56: 115-118, 1995.
35. OKANO, K., UEDA, M., KURAISHI, Y., AND SATOH, M. Effect of repeated cold stress on capsaicin-evoked release of glutamate from rat spinal dorsal horn slices. Neurosci. Res. 29: 319-324, 1997.
36. OUSEPH, A. K., KHASAR, S. G., AND LEVINE, J. D. Multiple second messenger systems act sequentially to mediate rolipram-induced prolongation of prostaglandin E2-induced mechanical hyperalgesia in the rat. Neuroscience 64: 769-776, 1995.
37. PITCHFORD, S. AND LEVINE, J. D. Prostaglandins sensitize nociceptors in cell culture. Neurosci. Lett. 132: 105-108, 1991.
38. RAJA, S. N. Peripheral modulatory effects of catecholamines in inflammatory and neuropathic pain. Adv. Pharmacol. 42: 567-571, 1998.
39. SANGAMESWARAN, L., DELGADO, S. G., FISH, L. M., KOCH, B. D., JAKEMAN, L. B., STEWART, G. R., SZE, P., HUNTER, J. C., EGLEN, R. M., AND HERMAN, R. C. Structure and function of a novel voltage-gated, tetrodoxtoxin-resistant sodium channel specific to sensory neurons. J. Biol. Chem. 271: 5953-5956, 1996.
40. TAIWO, Y. O., CODERRE, T. J., AND LEVINE, J. D. The contribution of training to sensitivity in the nociceptive paw-withdrawal test. Brain Res. 487: 148-151, 1989.
41. TAIWO, Y. O., GOETZL, E. J., AND LEVINE, J. D. Hyperalgesia onset latency suggests a hierarchy of action. Brain Res. 423: 333-337, 1987.
42. TAIWO, Y. O., HELLER, P. H., AND LEVINE, J. D. Characterization of distinct phospholipases mediating bradykinin and noradrenaline hyperalgesia. Neuroscience 39: 523-531, 1990.
43. TAIWO, Y. O. AND LEVINE, J. D. Characterization of the arachidonic acid metabolites mediating bradykinin and noradrenaline hyperalgesia. Brain Res. 458: 402-406, 1988.
44. TAIWO, Y. O. AND LEVINE, J. D. Contribution of guanine nucleotide regulatory proteins to prostaglandin hyperalgesia in the rat. Brain Res. 492: 400-403, 1989a.
45. TAIWO, Y. O. AND LEVINE, J. D. Prostaglandin effects after elimination of indirect hyperalgesic mechanisms in the skin of the rat. Brain Res. 492: 397-399, 1989b.
46. TAIWO, Y. O. AND LEVINE, J. D. Direct cutaneous hyperalgesia induced by adenosine. Neuroscience 38: 757-762, 1990.
47. TAIWO, Y. O. AND LEVINE, J. D. Further confirmation of the role of adenyl cyclase and of cAMP-dependent protein kinase in primary afferent hyperalgesia. Neurosdence 44: 131-135, 1991.
48. TAIWO, Y. O. AND LEVINE, J. D. Serotonin is a directly-acting hyperalgesic agent in the rat. Neuroscience 48: 485-490, 1992.
49. TAYLOR, J., WEYERS, P., HARRIS, N., AND VOOEL, W. H. The plasma catecholamine stress response is characteristic for a given animal over a one-year period. Physiol. Behav. 46: 853-856, 1989.
50. TOULLEC, D., PIANETTI, P., COSTE, H., BELLEVERCUE, P., GRAND, P. T., AJAKANE, M., BAUDET, V., BOISSIN, P., BOURSIER, E., LORIOLLE, F., DUHAMEL, L., CHARON, D., AND KIRILOVSKY, J. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266: 15771-15781, 1991.
51. TSAPIS, A. AND KEPES, A. Transient breakdown of the permeability barrier of the membrane of Escherichia coli upon hypoosmotic shock. Biochim. Biophys. Acta 469: 1-12, 1977.
52. VIDAL, C. AND JACOB, J. Hyperalgesia induced by emotional stress in the rat: an experimental animal model of human anxiogenic hyperalgesia. Ann. NY Acad. Sci. 467: 73-81, 1986.
53. WEST, L. K. AND HUANG, L. Transient permeabilization induced osmotically in membrane vesicles from Torpedo electroplax: a mild procedure for trapping small molecules. Biochemistry 19: 4418-4423, 1980.
54. WIDDICOMBE, J. H., AZIZI, F., KANG, T., AND PITTET, J. F. Transient permeabilization of airway epithelium by mucosal water. J. Appl. Physiol. 81: 491-499, 1996.
55. WORTSMAN, J., FRANK, S., AND CRYER, P. E. Adrenomedullary response to maximal stress in humans. Am. J. Med. 77: 779-784, 1984.