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Sex-Specific Mediation of Opioid-Induced Hyperalgesia by the Melanocortin-1 Receptor

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Sex-Specific Mediation of Opioid-Induced Hyperalgesia by the Melanocortin-1 Receptor PAIN MEDICINE Anesthesiology 2010; 112:181–8 Copyright © 2009, the American Society of Anesthesiologists, Inc. Lippincott Williams & Wilkins Sex-specific Mediation of Opioid-induced Hyperalgesia by the Melanocortin-1 Receptor Aaron Juni, Ph.D.,* Minying Cai, Ph.D.,† Magda Stankova, Ph.D.,‡ Amanda R. Waxman, M.A.,§ Caroline Arout, M.A.,§ Gad Klein, Ph.D.,* Albert Dahan, M.D., Ph.D.,ʈ Victor J. Hruby, Ph.D.,† Jeffrey S. Mogil, Ph.D.# Benjamin Kest, Ph.D.** Downloaded from http://pubs.asahq.org/anesthesiology/article-pdf/112/1/181/248994/0000542-201001000-00031.pdf by guest on 23 September 2021 ABSTRACT only, increasing latencies by 72%, MSG606 increased latencies by Background: N-Methyl-D-aspartate receptor antagonists reverse approximately 60% exclusively in females. A lower morphine infusion Ϫ Ϫ hyperalgesia during morphine infusion in male mice only. Because dose (1.6 mg ⅐ kg 1 ⅐ 24 h 1) reduced baseline withdrawal latencies the melanocortin-1 receptor can act as a female-specific counter- by 45–52% in B6 and e/e mice of both sexes, which was reversed by part to N-methyl-D-aspartate receptors in ␬-opioid analgesic mech- MK-801, but not MSG606, in both male and female B6 mice. anisms, the authors assessed the contribution of melanocortin-1 Conclusions: The data indicate the sex-specific mediation of high- receptors to the sex-specific mechanisms underlying morphine hy- dose morphine-induced hyperalgesia by N-methyl-D-aspartate and peralgesia. melanocortin-1 receptors in male and female mice, respectively, Methods: The tail-withdrawal test was used to compare the noci- suggesting a broader relevance of this known sexual dimorphism. ceptive responses of male and female C57BL/6J (B6) mice with The data further indicate that the neural substrates contributing to those of C57BL/6J-Mc1re/e (e/e) mice, spontaneous mutants of the hyperalgesia are morphine dose-dependent. B6 background lacking functional melanocortin-1 receptors, during continuous morphine infusion (1.6 and 40.0 mgkgϪ1 ⅐ 24 hϪ1). Sep- What We Already Know about This Topic arate groups of hyperalgesic B6 and outbred CD-1 mice were in- jected with MK-801 or MSG606, selective N-methyl-D-aspartate and ❖ Continued opioid exposure leads to hyperalgesia, an effect melanocortin-1 receptor antagonists, respectively. which is blocked only in male rodents by N-methyl-D-aspar- Results: Morphine infusion (40.0 mg ⅐ kgϪ1 ⅐ 24 hϪ1) reduced base- tate (NMDA) receptor antagonists line withdrawal latencies by 45–55% in B6 mice of both sexes, indi- cating hyperalgesia; this increased nociception was manifest in male What This Article Tells Us That Is New e/e mice only. Although MK-801 reversed hyperalgesia in male mice ❖ High dose opioid exposure induced hyperalgesia was blocked only in male mice by NMDA receptor antagonists, and only in female mice by melanocortin-1 receptor * Research Associate, Neuropsychology Doctoral Program, antagonists Queens College, City University of New York, Flushing, New York. ❖ Hyperalgesia from low doses was blocked in both sexes by † Professor, ‡ Research Associate, Department of Chemistry and NMDA receptor antagonists Biochemistry, University of Arizona, Tucson, Arizona. § Ph.D. Stu- dent, Neuropsychology Doctoral Program, Queens College, City University of New York. ʈ Professor, Department of Anesthesiology, Leiden University Medical Center, Leiden, The Netherlands. # Pro- USTAINED morphine delivery can paradoxically en- fessor, Department of Psychology and Alan Edwards Centre for Shance pain sensitivity in humans1,2 and nociceptive be- Research on Pain, McGill University, Montreal, Quebec, Canada. ** havior in rodents.3,4 This opioid-induced hyperalgesia is ob- Professor, Neuropsychology Doctoral Program, Queens College, City University of New York, and Department of Psychology and viously a major challenge to the clinical treatment of pain, for Center for Developmental Neuroscience, The College of Staten which ␮-opioid agonists such as morphine are a mainstay. Island, City University of New York. Interestingly, morphine enhances nociception in mice even Received from Department of Psychology and Center for Devel- when opioid receptors are effectively blocked by concurrent opmental Neuroscience, The College of Staten Island, City Univer- sity of New York, Staten Island, New York. Submitted for publica- treatment with high doses of the broad-spectrum opioid re- tion April 20, 2009. Accepted for publication September 23, 2009. ceptor antagonist, naltrexone,5,6 or absent entirely in mice Supported by Professional Staff Congress/City University of New lacking all three opioid receptor genes,7 indicating that mor- York (New York, New York; to B.K.); National Institute for Neuro- logical Diseases and Stroke R01 NS41670 (Bethesda, Maryland; to phine hyperalgesia is independent of previous or concurrent J.S.M.); National Institute for Digestive and Kidney Diseases 17240 opioid receptor activation. (Bethesda, Maryland; to V.J.H.); and National Institute on Drug We have recently reported a qualitative sex difference in Abuse 06248 and 348900 (Bethesda, Maryland; to V.J.H.). morphine hyperalgesia.6 Specifically, male and female mice Address correspondence to Dr Kest: Department of Psychology, manifest hyperalgesia of equal magnitude and duration dur- 2800 Victory Boulevard, Staten Island, New York 10314. Ϫ Ϫ [email protected]. Information on purchasing reprints may be ing 12 days of continuous morphine (40.0 mg ⅐ kg 1 ⅐ 24 h 1) found at www.anesthesiology.org or on the masthead page at the infusion, but blockade of N-methyl-D-aspartate (NMDA) beginning of this issue. ANESTHESIOLOGY’s articles are made freely accessible to all readers, for personal use only, 6 months from the receptors with LY235959 or MK-801 markedly reversed hy- cover date of the issue. peralgesia in male mice only. This sex-specific response does Anesthesiology, V 112 • No 1 181 January 2010 182 Sex-specific Mediation of Morphine Hyperalgesia not seem to be related to any putative sex-dependent poten- 47.3° Ϯ 0.2°C using an immersion circulator pump (Iso- tiation of morphine analgesia by NMDA receptor antago- temp Model 71; Fisher, Pittsburgh, PA). In previous studies nists8,9 because mice were concurrently treated with naltrex- with females and males,5,6 this temperature consistently one during morphine infusion. This sex difference was not yielded premorphine baseline latencies of 8–10 s, thereby attributable to antagonist dosing as well because MK-801 did minimizing possible floor effects during the hyperalgesia reverse hyperalgesia in males and ovariectomized females but phase of morphine infusion. Latency to respond with a vig- not in ovariectomized females treated with estrogen. These orous flexion of the tail was recorded twice at 30-s intervals data collectively indicate that female mice possess functional and averaged. A cutoff latency of 18 s (i.e., roughly twice the male-typical NMDA receptor-mediated hyperalgesic mech- baseline) for analgesic responses was used throughout. Noci- anisms, but they are diverted from their use by ovarian sex ception was always tested near mid-photophase to reduce 10 steroids. But what neurochemical system mediates morphine possible circadian effects on nociception. Downloaded from http://pubs.asahq.org/anesthesiology/article-pdf/112/1/181/248994/0000542-201001000-00031.pdf by guest on 23 September 2021 hyperalgesia in intact female mice? There are previous reports that NMDA receptor antago- Drug Doses and Delivery nists effectively reduce ␬-opioid analgesia10,11 and nonopi- Osmotic pumps (Alzet Model 2001; Alza, Mountain View, oid swim stress-induced analgesia12 in male but not in female CA) containing morphine or saline vehicle were implanted mice. In the latter study, MK-801 was an effective antagonist subcutaneously via a small dorsal midline incision made dur- in ovariectomized females but not in ovariectomized females ing anesthesia. Osmotic pumps provide continuous infusion treated with estrogen, which parallels exactly our findings for 7 days, thereby preventing hyperalgesia associated with with morphine hyperalgesia. By using genetic and pharma- withdrawal in morphine-dependent subjects that can poten- cological tools, Mogil et al.11 subsequently demonstrated the tially confound experiments in which chronic morphine critical contribution of melanocortin-1 receptors to the sex- treatment is accomplished via repeated acute injections.17 specific mediation of ␬-opioid analgesic mechanisms in in- When testing exceeded 7 days, pumps were replaced on Day tact female mice. Accordingly, we assessed the contribution 6 as in previous studies.5,6 Pellets containing 30 mg of the of this receptor to sex differences in morphine hyperalgesia general opioid receptor antagonist, naltrexone, or a placebo using MSG606, a selective melanocortin-1 receptor antago- formulation were wrapped in nylon mesh and implanted nist, and by assaying nociception during morphine infusion subcutaneously in the nape of the neck. Pellets were im- in melanocortin-1 receptor-deficient C57BL/6J-Mc1re/e (e/e) planted 24 h before the start of morphine infusion. In rats, mice. The sensitivity of these mutants was compared with identical naltrexone pellets substantially increase naltrexone that of their genetic background, C57BL/6J (B6) mice. plasma levels 1 h after implant and sustain pharmacologically active levels of naltrexone such that there is a greater than Materials and Methods 50-fold rightward shift in the morphine analgesia dose– response curve 8 days later.18 In
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