Pain and U-shaped dose responses: Occurrence, mechanisms, and clinical implications

Critical Reviews in Toxicology

Volumn 38, Issue 7, 2008, Pages 579-590

  Calabrese, Edward J ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Analgesia; Anandamide; Anti nociception; Biphasic; Calcitonin; Dopamine; Histogranin; Hormesis; L DOPA; Nausea; Nociception; Nocistatin; Opioids; Pain; Prostaglandin; U shaped; Yohimbine

Indexed keywords

11 DEOXY 16 PHENOXY 17,18,19,20 TETRANORPROSTAGLANDIN E1; 2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 7 CHLOROKYNURENIC ACID; ANANDAMIDE; APOMORPHINE; BUPRENORPHINE; BUTAPROST; CALCITONIN; CLONIDINE; CYCLAZOCINE; DIZOCILPINE; DOPAMINE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; KETAMINE; LEVODOPA; MIRTAZAPINE; MORPHINE; NALOXONE; NALTREXONE; NOCISTATIN; OPIATE; ORIPAVINE; PENTAZOCINE; PROMETHAZINE; PROSTAGLANDIN; PROSTAGLANDIN E2; SULPIRIDE; TROPISETRON; UNINDEXED DRUG; YOHIMBINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTHRITIS; BIOLOGICAL MODEL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG MEGADOSE; HORMESIS; HYPERALGESIA; LOW DRUG DOSE; NAUSEA; NOCICEPTION; NONHUMAN; PAIN; RAT; RECEPTOR UPREGULATION; REVIEW; VOMITING;

ADAPTATION, PHYSIOLOGICAL; ANALGESICS; ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MICE; NEUROPHARMACOLOGY; PAIN; PAIN MEASUREMENT; RATS;

EID: 49749149547     PISSN: 10408444     EISSN: 15476898     Source Type: Journal    
DOI: 10.1080/10408440802026281     Document Type: Review

References (73)

1. Angst, M.S., Koppert, W., Pahl, I., Clark, D.J., and Schmelz, M. (2003). Short-term infusion of the mu-opioid agonist remifentanil in humans causes hyperalgesia during withdrawal. Pain 10:49-57.
2. Blane, G.F., and Dugdall, D. (1968). Interaction of narcotic antagonists and analgesics. J. Pharmacol. Pharm. 20:547-552.
3. Calabrese, E.J. (2001). Dopamine: Biphasic dose responses. Crit. Rev. Toxicol. 31:563-584.
4. Calabrese, E.J. (2008). Converging concepts: Adaptive response, preconditioning, and the Yerkes-Dodson Law are manifestations of hormesis. Ageing Res. Rev. 7:8-20.
5. Calabrese, E.J., Bachmann, K.A., Bailer, A.J., Bolger, P.M., Borak, J., Cai, L., Cedergreen, N., Cherian, M.G., Chiueh, C.C., Clarkson, T.W., et al. (2007). Biological stress terminology: Integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework. Tox. Appl. Pharmacol 222:122-128.
6. Calabrese, E.J., and Baldwin, L.A. (2001). The frequency of U-shaped dose-responses in the toxicological literature. Tox. Sci. 62:330-338.
7. Calabrese, E.J., and Baldwin, L.A. (2003). The hermetic dose response model is more common than the threshold model in toxicology. Tax. Sci. 71:246-250.
8. Calabrese, E.J., and Blain, R. (2005). The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: An overview. Toxicol. Appl. Pharmacol. 202:289-301.
9. Calabrese, E.J., Staudenmayer, J.W., Stanek, EJ., and Hoffmann, G.R. (2006). Hormesis outperforms threshold model in NCI anti-tumor drug screening data. Tox. Sci. 94:368-378.
10. Celerier, E., Laulin, J., Larcher, A., Le Moal, M., and Simonnet, G. (1999). Evidence for opiate-activated NMDA processes masking opiate analgesia in rats. Brain Res. 847:18-25.
11. Celerier, E., Rivat, C., Jun, Y., Laulin, J.P., Larcher, A., Reynier, P., and Simonnet, G. (2000). Long-lasting hyperalgesia induced by fentanyl in rats: Preventive effect of ketamine. Anesthesiology 92:465-472.
12. Celerier, E., Laulin, J.P., Corcuff, J.B., Le Moal, M., and Simonnet, G. (2001). Progressive enhancement of delayed hyperalgesia induced by repeated heroin administration: A sensitization process. J. Neurosci. 21:4074-4080.
13. Compton, P., Athanasos, P., and Elashoff, D. (2003). Withdrawal hyperalgesia after acute opioid physical dependence in nonaddicted humans: A preliminary study. J. Pain 4:511-519.
14. Conceicao, I.M., Maiolini, M., Jr., Mattia, N., Vital, M.A., Santos, B.R., Smaili, S., and Frussa-Filho, R. (1992). Anxiety-induced antinociception in the mouse. Braz. J. Med. Biol. Res. 25:831-834.
15. Cowan, A. (2003). Buprenorphine: New pharmacological aspects. Int. J. Clin. Proctol. 133(Suppl.):3-8.
16. Cowan, A., Lewis, J.W., and MacFarlane, I.R. (1977). Agonist and antagonist properties of buprenonphine, a newantinociceptive agent. Br. J. Pharmacol. 60:537-545.
17. Dennis, S.G., Melzack, R., Gutman, S., and Boucher, F. (1980). Pain modulation by adrenergic agents and morphine as measured by three pain tests. Life Sci. 26:1247-1259.
18. Dewey, W.L. (1986). Cannabinoid pharmacology. Pharmacol. Rev. 38:151-178.
19. Dickenson, A.H., and Sullivan, A.F. (1986). Electrophysiological studies on the effects of intrathecal morphine on nociceptive neurons in the rat dorsal horn. Pain 24:211-222.
20. Dum, J.E., and Herz, A. (1981). In vivo receptor binding of the opiate partial agonist, buprenorphine, correlated with its agonistic and antagonistic actions. Br. J. Pharmacol. 74:627-633.
21. 3 receptor network after 20 years of research - Evolving concepts in management of pain and inflammation. Eur. J. Pharmacol. 560:1-8.
22. Farber, L., Stratz, T., Bruckle, W., Spath, M., Pongratz, D., Lautenschlager, J., Kotter, I., Zoller, B., Peter, H.-H., Neeck, G., Alten, R., and Muller, W. (2000). Efficacy and tolerability of tropisetron in primary fibromyalgia - A highly selective and competitive 5-HT3 receptor antagonist. Scand. J. Rheumatol. 29(Suppl.):49-54.
23. Fielding, S., Wilker, J., Hynes, M., Szewczak, M., Novick Jr., W.J., and Lal, H. (1978). A comparison of clonidine with morphine for antinociceptive and antiwithdrawal actions. J. Pharmacol. Exp. Ther. 207:899-905.
24. Galeotti, N., Stefano, G.B., Guarna, M., Bianchi, E., and Ghelardini, C. (2006). Signaling pathway of morphine induced acute thermal hyperalgesia in mice. Pain 123:294-305.
25. Guignard, B., Bossard, A.E., Coste, C., Sessler, D.I., Lebrault, C., Alfonsi, P., et al. (2000). Acute opioid tolerance: intraoperative remifentanil increases postoperative pain and morphine requirement. Anesthesiology 93:409-417.
26. Guimaraes, F.S., Chiaretti, T.M., Graeff, F.G., and Zuardi, A.W. (1990). Antianxiety effect of cannabidiol in the elevated plus-maze. Psychopharmacology 100:558-559.
27. Hollt, V. (1978). The in vivo occupation of opiate receptors. In: Factors Affecting the Action of Narcotics (M.L. Adler, L. Manara, and R. Samanin, Eds.). Raven Press, New York, pp. 207-220.
28. Hosoi, M., Oka, T., and Hori, T. (1997). Prostaglandin E receptor EP3 subtype is involved in thermal hyperalgesia through its actions in the preoptic hypothalamus and the diagonal band of Broca in rats. Pain 71:303-311.
29. Inoue, M., Matsunaga, S., Rashid, M.H., Yoshida, A., Mizuno, K., Sakurada, T., Takeshima, H., and Ueda, H. (2001). Pronociceptive effects of nociceptin/orphanin FQ (13-17) at peripheral and spinal level in mice. J. Pharmacol. Exp. Ther. 299:213-219.
30. Inoue, M., Shimohira, I., Yoshida, A., Zimmer, A., Takeshima, H., Sakurada, T., and Ueda, H. (1999). Dose-related opposite modulation by nociceptin/orphanin FQ of substance P nociception in the nociceptors and spinal cord. J. Pharmacol. Exp. Ther. 291:308-313.
31. Kayser, V., and Guilbaud, G. (1981). Dose-dependent analgesic and hyperalgesic effects of systemic naloxone in arthritic rats. Brain Res. 226:344-348.
32. Kayser, V., and Guilbaud, G. (1983). The analgesic effects of morphine, but not those of the enkephalinase inhibitor thiorphan, are enhanced in arthritic rats. Brain Res. 267:131-138.
33. Kayser, V., and Guilbaud, G. (1987). Cross-tolerance between analgesic low doses of morphine and naloxone in arthritic rats. Brain Res. 405:123-129.
34. Kayser, V., Besson, J.M., and Guilbaud, G. (1986). Analgesia produced by low doses of the opiate antagonist naloxone in arthritic rats is reduced in morphine-tolerant animals. Brain Res. 371:37-41.
35. Kayser, V., Besson, J.M., and Guilbaud, G. (1987). Paradoxical hyperalgesic effect of exceedingly low doses of systemic morphine in an animal model of persistent pain (Freund's adjuvant-induced arthritic rats). Brain Res. 414:155-157.
36. Kwiatkowska, M., Parker, L.A., Buton, P., and Mechoulam, R. (2004). A comparative analysis of the potential of cannabinoids and ondansetron to suppress cisplatin-induced emesis in the Suncus murinus (house musk shrew). Psychopharmacology 174:254-259.
37. Laulin, J.P., Larcher, A., Celerier, E., Le Moal, M., and Simonnet, G. (1998). Long-lasting increased pain sensitivity in rat following exposure to heroin for the first time. Eur. J. Neurosci. 10:782-785.
38. Laulin, J.P., Maurette, P., Corcuff, J.B., Rivat, C., Chauvin, M., and Simonnet, G. (2002). The role of ketamine in preventing fentanyl-induced hyperalgesia and subsequent acute morphine tolerance. Anesth. Analg. 94:1263-1269.
39. Lee, C., and Rodgers, R.J. (1990). Antinociceptive effects of elevated plus-maze exposure: Influence of opiate receptor manipulations. Psychopharmacology 102:507-513.
40. Lewis, J.W. (1974). Ring C-bridged derivatives of thebaine and oripavine. Adv. Biochem. Psychopharm. 8:123-135.
41. Maeda, Y., Yamada, K., Hasegawa, T., Kawamata, Y., Uchida, K., Iyo, M., Fukui, S., and Nabeshima, T. (1994). Relationship between anti-aversive effects of salmon calcitonin and plasma levels of ACTH, beta-endorphin and prostaglandin E2 in mice. Res. Comm. Chem. Pathol. Pharmacol. 83:15-24.
42. Malfait, A.M., Gallily, R., Sumariwalla, P.F., Malik, A.S., Andreakos, E., Mechoulam, R., and Feldman, M. (2000). The non-psychoactive cannabis-constituent cannabidiol is an oral anti-arthritic therapeutic in murine collagen-induced arthritis. Proc. Natl. Acad. Sci. USA 97:9561-9566.
43. Martin, W.R. (1967). Opioid antagonists. Pharmacol. Rev. 19:463-521.
44. Nakano, H., Minami, T., Abe, K., Arai, T., Tokumura, M., Ibii, N., Okuda-Ashitaka, E., Mori, H., and Ito, S. (2000). Effect of intrathecal nocistatin on the formalin-induced pain in mice versus that of nociceptin/orphanin FQ1. J. Pharmacol. Exp. Ther. 292:331-336.
45. 2-induced hyperalgesia in conscious mice. Brain Res. 677:138-144.
46. Nunes-de-Souza, R.L., Canto-de-Souza, A., Da-Costa, M., Fornari, R.V., Graeff, F.G., and Pela, I.R. (2000). Anxiety-induced antinociception in mice: Effects of systemic and intra-amygdala administration of 8-OH-DPAT and midazolam. Psychopharmacology 150:300-310.
47. Paalzow, G.H.M. (1992). L-Dopa induces opposing effects on pain in intact rats: (-)-Sulpiride, SCH 23390 or α-methyl-DL-p-tyrosine methylester hydrochloride reveals profound hyperalgesia in large antinociceptive doses. J. Pharmacol. Exp. Ther. 263:470-479.
48. Paalzow, L. (1974). Analgesia produced by clonidine in mice and rats. J. Pharm. Pharmacol. 26:361-363.
49. Paalzow, L.K., and Paalzow, G.H.M. (1986). Concentration-response relations for apomorphine effects on heart rate in conscious rats. Eur. J. Pharmacol. 88:28-34.
50. Paalzow, G.H.M., and Paalzow, L.K. (1985). Promethazine both facilitates and inhibits nociception in rats: effect of the testing procedure. Psychopharmacology 85:31-36.
51. Paalzow, G.H.M., and Paalzow, L.K. (1983a). Opposing effects of apomorphine on pain in rats. Evaluation of the dose-response curve. Eur. J. Pharmacol. 88:27-35.
52. Paalzow, G.H.M., and Paalzow, L.K. (1983b). Yohimbine both increases and decreases nociceptive thresholds in rats: Evaluation of the dose-response relationship. Naunyn-Schmied. Arch. Pharmacol. 322:193-197.
53. Paalzow, G., and Paalzow, L. (1982). Separate noradrenergic receptors could mediate clonidine induced antinociception. J. Pharmacol. Exp. Ther. 223:795-800.
54. Parker, L.A., Kwiatkowska, M., Burton, P., and Mechoulam, R. (2004). Effect of cannabinoids on lithium-induced vomiting in the Suncus murinus (house musk shrew). Psychopharmacology 171:156-161.
55. Paton, W.D.M., and Pertwee, R.G. (1973). The pharmacology of cannabis in man. In: Marijana: Chemistry, Pharmacology, Metabolism and Clinical Effects. Academic Press, New York, pp. 287-333.
56. 2 receptor antagonists. Eur. J. Pharmacol. 546:40-47.
57. Protais, P., Dubuc, I., and Costentin, J. (1983). Pharmacological characteristics of dopamine receptors involved in the dual effect of dopamine agonists on yawning behaviour in rats. Eur. J. Pharmacol. 94:271-280.
58. Rance, M.J. (1979). Animal and molecular pharmacology of mixed agonist-antagonist analgesic drugs. Br. J. Clin. Pharmacol. 7:281S-286S.
59. Rance, M.J., Lord, J.A.H., and Robinson, T. (1980). Biphasic dose response curve to buprenorphine in the rat tail flick assay: effect of naloxone pretreatment. In: Endogenous and Exogenous Opiate Agonists and Antagonists (E.L. Way, Editor). Pergamon Press, New York, pp. 387-390.
60. Reddy, S.V.R., Maderdrut, J.L., and Yaksh, T.L. (1980). Spinal cord pharmacology of adrenergic agonist-mediated antinociception. J. Pharmacol. Exp. Ther. 213:525-533.
61. 2+ pathway. Brain Res. Mol. Brain Res. 110:261-266.
62. Sadee, W., Rosenbaum, J.S., and Herz, A. (1982). Buprenorphine: Differential interaction with opiate receptor subtypes in vivo. J. Pharmacol. Exp. Ther. 223:157-162.
63. Schreiber, S., Rigai, T., Katz, Y., and Pick, C.G. (2002). The antinociceptive effect of mirtazapine in mice is mediated through serotonergic, noradrenergic and opioid mechanisms. Brain Res. Bull. 58:601-605.
64. Schmitt, H., LeDouarec, L.-D., and Petillot, N. (1974). Antinociceptive effects of some α-sympathomimetic agents. Neuropharmacology 13:289-293.
65. Siegan, J.B., and Sagen, J. (1997). A natural peptide with NMDA inhibitory activity reduces tonic pain in the formalin model. NeuroReport 8:1379-1381.
66. Stromberg, U. (1970). Dopa effects on motility in mice - Potentiation by MK-485 and dexchlorpheniramine. Psychopharmacologia, 18:58-67.
67. Strombom, U. (1976). Catecholamine receptor agonists: Effect of motor activity and rate of tyrosine hydroxylation in mouse brain. Naunyn- Schmiedeberg Arch. Pharmacol. 292:167-176.
68. Suen, P.C., Wu, K., Xu, J.L., Lin, S.Y., Levine, E.S., and Black, I.B. (1998). NMDA receptor subunits in the postsynaptic density of rat brain: Expression and phosphorylation by endogenous protein kinases. Brain Res. Mol. Brain Res. 59:215-228.
69. Sulcova, E., Mechoulam, R., and Fride, E. (1998). Biphasic effects of anandamide. Pharmacol. Biochem. Behav. 59:347-352.
70. Taukulis, H.K., and Goggin, C.E. (1990). Diazepam-stress interactions in the rat: Effects on autoanalgesia and a plus-maze model of anxiety. Behav. Neural. Biol. 53:205-216.
71. Van Elstraete, A.C., Sitbon, P., Trabold, F., Mazoit, J.X., and Benhamou, D. (2005). A single dose of intrathecal morphine in rats induces long-lasting hyperalgesia: The protective effect of prior administration of ketamine. Anesth. Analg. 101:1750-1756.
72. Villiger, J.W., and Taylor, K.M. (1981). Buprenorphine: Characteristics of binding sites in the rat central nervous system. Life Sci. 29:2699-2709.
73. Zhou, Y., Sun, Y.-H., Zhang, Z.-W., and Han, J.-S. (1993). Increased release of immunoreactive cholecystokinin octapeptide by morphine and potentiation of μ-opioid analgesia by CCKB receptor antagonist L-365,260 in rat spinal cord. Eur. J. Pharmacol. 234:147-154.