Endothelin-B receptor activation triggers an endogenous analgesic cascade at sites of peripheral injury

Nature Medicine

Volumn 9, Issue 8, 2003, Pages 1055-1061

  Khodorova, Alla ^a   Navarro, Betsy ^b   Jouaville, Laurence Sophie ^a   Murphy, Jo Ellen ^a   Rice, Frank L ^c   Mazurkiewicz, Joseph E ^c   Long Woodward, Denise ^a   Stoffel, Markus ^d   Strichartz, Gary R ^a   Yukhananov, Rus ^a   Davar, Gudarz ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c ALBANY MEDICAL COLLEGE   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ENDORPHIN; DELTA OPIATE RECEPTOR; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLORNITHYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; ENDOTHELIN 1; ENDOTHELIN B RECEPTOR; G PROTEIN COUPLED RECEPTOR; INWARDLY RECTIFYING POTASSIUM CHANNEL; KAPPA OPIATE RECEPTOR; MU OPIATE RECEPTOR; NALOXONE; NALTRINDOLE; OPIATE RECEPTOR; SUCCINYLENDOTHELIN 1 [8-21][9 GLUTAMIC ACID 11,15 ALANINE];

ANALGESIA; ANALGESIC ACTIVITY; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PAIN; CONTROLLED STUDY; DISEASE CONTROL; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; KERATINOCYTE; MEDIATOR RELEASE; NONHUMAN; PAIN; PAIN RECEPTOR; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION; SKIN INJURY;

ANALGESIA; ANIMALS; BETA-ENDORPHIN; CELLS, CULTURED; ENDOTHELIN-1; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; HUMANS; KERATINOCYTES; MALE; PAIN; PAIN MEASUREMENT; POTASSIUM CHANNELS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ENDOTHELIN B; RECEPTORS, ENDOTHELIN; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, KAPPA; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION; SKIN;

ANIMALIA;

EID: 0041888477     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm885     Document Type: Article

References (49)

1. McQuay, H. & Moore, A. Introduction. in An Evidence-Based Resource For Pain Relief. (eds. McQuay, H & Moore, A.) 23 (Oxford University Press, Oxford, 1998).
2. Scholz, J. & Woolf, C.J. Can we conquer pain? Nat. Neurosci. 5 (suppl. 1), 1062-1067 (2002).
3. Julius, D. & Basbaum, A.I. Molecular mechanisms of nociception. Nature 413, 203-210 (2001).
4. Hickey, K.A., Rubanyi, G.M., Paul, R.J. & Highsmith, R.F. Characterization of a coronary vasoconstrictor produced by cultured endothelial cells. Am. J. Physiol. 248, C550-C556 (1985).
5. Yanagisawa, M. et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332, 411-415 (1988).
6. Rubanyi, G.M. & Polokoff, A. Endothelins: molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol. Rev. 48, 325-415 (1994).
7. Ahn, G.Y. et al. The expression of endothelin-1 and its binding sites in mouse skin increased after ultraviolet B irradiation of local injection of tumor necrosis factor alpha. J. Dermatol. 25, 78-44 (1998).
8. Luscher, T.F. & Barton, M. Endothelins and endothelin receptor antagonists: therapeutic considerations for a novel class of cardiovascular drugs. Circulation 102, 2434-2440 (2000).
9. Nelson, J. et al. Identification of endothelin-1 in the pathophysiology of metastatic adenocarcinoma of the prostate. Nat. Med. 1, 944-949 (1995).
10. Ferreira, S.H., Romitelli, M. & de Nucci, G. Endothelin-1 participation in overt and inflammatory pain. J. Cardiovasc. Pharmacol. 13 (suppl, 5), S220-S222 (1989).
11. Davar, G., Hans, G., Fareed, M.U., Sinnott, C. & Strichartz, G. Behavioral signs of acute pain produced by application of endothelin-1 to rat sciatic nerve. NeuroReport 9, 2279-2283 (1998).
12. Piovezan, A.P., D'Orleans-Juste, P., Souza, G.E. & Rae, G.A. Endothelin-1-induced ET(A) receptor-mediated nociception, hyperalgesia and oedema in the mouse hind-paw: modulation by simultaneous ET(B) receptor activation. Br. J. Pharmacol. 129, 961-968 (2000).
13. Jarvis, M. F. et al. ABT-627, an endothelin ET(A) receptor-selective antagonist, attenuates tactile allodynia in a diabetic rat model of neuropathic pain. Eur. J. Pharmacol. 388, 29-35 (2000).
14. Fareed, M.U., Hans, G., Atanda, A., Strichartz, G. & Davar, G, Pharmacological characterization of acute pain behavior produced by application of endothelin-1 to rat sciatic nerve. J. Pain 1, 46-53 (2000).
15. Gokin, A.P. et al. Local injection of endothelin-1 produces pain-like behavior and excitation of nociceptors in rats. J. Neurosci. 21, 5358-5366 (2001).
16. Pomonis, J.D., Rogers, S.D., Peters, C.M., Ghilardi, J.R. & Mantyh, P.W. Expression and localization of endothelin receptors: implications for the involvement of peripheral glia in nociception. J. Neurosci. 21, 999-1006 (2001).
17. De-Melo, J.D., Tonussi, C.R., D'Orleans-Juste, P. & Rae, G.A, Articular nociception induced by endothelin-1, carrageenan and LPS in naive and previously inflamed knee-joints in the rat: inhibition by endothelin receptor antagonists. Pain 77, 261-269 (1998).
18. Wacnik, P.W. et al. Functional interactions between tumor and peripheral nerve: morphology, algogen identification, and behavioral characterization of a new murine model of cancer pain. J. Neurosci. 21, 9355-9366 (2001).
19. Carducci, M.A. et al. Atrasentan, an endothelin-receptor antagonist for refractory adenocarcinomas: safety and pharmacokinetics. J. Clin. Oncol. 8, 2171-2180 (2002).
20. Khodorova, A., Fareed, M.U., Gokin, A., Strichartz, G.R. & Davar, G. Local injection of a selective endothelin-b receptor agonist inhibits endothelin-1 induced pain-like behavior and excitation of nociceptors in a naloxone-sensitive manner. J. Neurosci. 22, 7788-7796 (2002).
21. Fields, H.L., Emson, P.C., Leigh, B.K., Gilbert, R.F. & Iversen, L.L. Multiple opiate receptor sites on primary afferent fibers. Nature 284, 351-353 (1980).
22. Stein, C. Peripheral mechanisms of opioid analgesia. Anesth. Analg. 76, 182-191 (1993).
23. Machelska, H. Cabot, P.J., Mousa, S.A., Zhang, Q. & Stein C. Pain control in inflammation governed by selectins. Nat. Med. 4, 1425-1428 (1998).
24. Akil, H., Mayer, D.J. & Liebeskind, J.C. Comparison in the rat between analgesia induced by stimulation of periacqueducal gray matter and morphine analgesia. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D274, 3603-3605 (1972).
25. Hughes, J. et al. Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature 258, 577-580 (1975).
26. Akil, H. Mayer, D.J. & Liebeskind, J.C. Antagonism of stimulation-produced analgesia by naloxone, a narcotic antagonist. Science 191, 961-962 (1976).
27. Fields, H.L., Heinricher, M.M. & Mason, P. Neurotransmitters in nociceptive modulatory circuits. Ann. Rev. Neurosci. 14, 219-245 (1991).
28. Harris, J.A. Descending artirociceptive mechanisms in the brainstem: their role in the animal's defensive system. J. Physiol. (Paris) 90, 15-25 (1996).
29. Gutstein, H.B., Mansour, A., Watson, S.J., Akil, H. & Fields, H.L. Mu and κ-opioid receptors in periaqueductal gray and rostral ventromedial medulla. NeuroReport 9, 1777-1781 (1998).
30. Stein C. The control of pain in peripheral tissue by opioids. N. Engl. J. Med. 332, 168-590 (1995).
31. Calignano, A., La Rana, G., Giuffrida, A. & Piomelli, D. Control of pain initiation by endogenous cannabinoids. Nature 394, 277-281 (1998).
32. Wettstein, G. & Grouhel, A. Opioid antagonist profile of SC nor-binaltorphimine in the formalin paw assay. Pharmacol. Biochem. Behav. 53, 411-416 (1996).
33. Wintzen, M., Yaar, M., Burbach, J.P. & Gilchrest, B.A. Proopiomelanocortin gene product regulation in keratinocytes. J. Invest. Dermatol. 106, 673-678 (1996).
34. Zanello, S.B. Jackson, D.M. & Holick, M.F. An immunocytochemical approach to the study of beta-endorphin production in human keratinocytes using confocal microscopy. Ann. NY Acad. Sci. 885, 85-99 (1999).
35. Hargreaves, K.M., Flores, C.M., Dionne, R.A. & Mueller, G.P. The role of pituitary beta-endorphin in mediating corticotropin-releasing factor-induced antinociception. Am. J. Physiol. 258, E235-E242 (1990).
36. + channels. Eur. J. Biochem. 267, 5830-5836 (2000).
37. Rogalski, S.L., Cyr, C. & Chavkin, C. Activation of the endothelin receptor inhibits the G protein-coupled inwardly rectifying potassium channel by a phospholipase A2-mediated mechanism. J. Neurochem. 72, 1409-1416 (1999).
38. Ikeda, K., Kobayashi, T., Kumanishi, T., Niki, H. & Yano, R. Involvement of G-protein-activated inwardly rectifying K (GIRK) channels in opioid-induced analgesia. Neurosci. Res. 38, 113-116 (2000).
39. Blanchet, C. & Luscher, C. Desensitization of mu-opioid receptor-evoked potassium currents: initiation at the receptor, expression at the effector. Proc. Natl. Acad. Sci. USA 99, 4674-4679 (2002).
40. Torrecilla, M. et al. G-protein-gated potassium channels containing Kir3.2 and Kir3.3 subunits mediate the acute inhibitory effects of opioids on locus ceruleus neurons. J. Neurosci. 22, 432-834 (2002).
41. Mitrovic, I., et al. Contribution of GIRK2-mediated postsynaptic signaling to opiate and alpha 2-adrenergic analgesia and analgesic sex differences. Proc. Natl. Acad. Sci. USA 100, 271-276 (2003).
42. Blednov, Y.A., Stoffel, M., Alva, H. & Harris, R.A. A pervasive mechanism for analgesia: Activation of GIRK2 channels. Proc. Natl. Acad. Sci. USA 100, 77-82 (2003).
43. Zhou, Q.L., Strichartz, G. & Davar, G. Endothelin-1 activates ET(A) receptors to increase irtracellular calcium in model sensory neurons. NeuroReport 12, 3853-3857 (2001).
44. Zhou, Z., Davar, G. & Strichartz, G. Endothelin-A receptor dependent enhanced activation gating of tetrodotoxin-resistant sodium currents in rat sensory neurons: a possible mechanism of ET-1 induced pain. J. Neurosci. 22, 6325-6330 (2002).
45. Slominski, A., Wortsman, J., Luger, T., Paus, R. & Solomon, S. Corticotropin releasing hormone and proopiomelanocortin involvement in the cutaneous response to stress. Physiol. Rev. 80, 979-1020 (2000).
46. Peier, A.M. et al. A heat-sensitive TRP channel expressed in keratinocytes. Science 296, 2046-2049 (2002).
47. Zimmermann, M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16, 109-110 (1983).
48. + channel GIRK2. Proc. Natl. Acad. Sci. USA 94, 923-927 (1997).
49. Broadbear, J.H. et al. Methocinnamox is a potent, long-lasting, and selective antagonist of morphine-mediated antinociception in the mouse: comparison with clocinnamox, β-funaltrexamine, and β-chlomaltrexamine. J. Pharmacol. Exp. Ther. 294, 933-940 (2000).