The μ‐opioid receptor agonist morphine, but not agonists at δ‐ or κ‐opioid receptors, induces peripheral antinociception mediated by cannabinoid receptors

Da Fonseca Pacheco, D; Klein, A; De Castro Perez, A; Da Fonseca Pacheco, C M; De Francischi, J N; Duarte, I D G

doi:10.1038/bjp.2008.175

Cited by 81Cannabis and Cannabinoid ResearchPain Mechanisms and TreatmentsNeuropeptides and Animal Physiology

The μ‐opioid receptor agonist morphine, but not agonists at δ‐ or κ‐opioid receptors, induces peripheral antinociception mediated by cannabinoid receptors

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Da Fonseca Pacheco, D, Klein, A, De Castro Perez, A, Da Fonseca Pacheco, C M, De Francischi, J N, Duarte, I D G·2008·British Journal of Pharmacology

DOI 10.1038/bjp.2008.175PMC PMC2465574

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Abstract

Background and purpose: Although participation of opioids in antinociception induced by cannabinoids has been documented, there is little information regarding the participation of cannabinoids in the antinociceptive mechanisms of opioids. The aim of the present study was to determine whether endocannabinoids could be involved in peripheral antinociception induced by activation of μ‐, δ‐ and κ‐opioid receptors. Experimental approach: Nociceptive thresholds to mechanical stimulation of rat paws treated with intraplantar prostaglandin E 2 (PGE 2 , 2 μg) to induce hyperalgesia were measured 3 h after injection using an algesimetric apparatus. Opioid agonists morphine (200 μg), (+)‐4‐[(alphaR)‐alpha‐((2S,5R)‐4‐Allyl‐2,5‐dimethyl‐1‐piperazinyl)‐3‐ methoxybenzyl]‐ N , N ‐diethylbenzamide (SNC80) (80 μg), bremazocine (50 μg); cannabinoid receptor antagonists N ‐(piperidin‐1‐yl)‐5‐(4‐ iodophenyl)‐1‐(2,4‐dichlorophenyl)‐4‐methyl‐1 H ‐pyrazole‐3‐carboxamide (AM251) (20–80 μg), 6‐iodo‐2‐methyl‐1‐[2‐(4‐morpholinyl) ethyl]‐1 H ‐indol‐3‐yl(4‐methoxyphenyl) methanone (AM630) (12.5–100 μg); and an inhibitor of methyl arachidonyl fluorophosphonate (MAFP) (1–4 μg) were also injected in the paw. Key results: The CB 1 ‐selective cannabinoid receptor antagonist AM251 completely reversed the peripheral antinociception induced by morphine in a dose‐dependent manner. In contrast, the CB 2 ‐selective cannabinoid receptor antagonist AM630 elicited partial antagonism of this effect. In addition, the administration of the fatty acid amide hydrolase inhibitor, MAFP, enhanced the antinociception induced by morphine. The cannabinoid receptor antagonists AM251 and AM630 did not modify the antinociceptive effect of SNC80 or bremazocine. The antagonists alone did not cause any hyperalgesic or antinociceptive effect. Conclusions and implications: Our results provide evidence for the involvement of endocannabinoids, in the peripheral antinociception induced by the μ‐opioid receptor agonist morphine. The release of cannabinoids appears not to be involved in the peripheral antinociceptive effect induced by κ‐ and δ‐opioid receptor agonists. British Journal of Pharmacology (2008) 154 , 1143–1149; doi: 10.1038/bjp.2008.175 ; published online 12 May 2008

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CB1 receptors and MORs are also co-expressed within the dorsal horn of the spinal cord.
“CB 1 receptors and MORs are also co-expressed within the dorsal horn of the spinal cord (Desroches et al, 2014a;da Fonseca Pacheco et al, 2008).”
From The endogenous cannabinoid system: a budding source of targets for treating inflammatory and neuropathic pain (2018) · cites this paper as da Fonseca Pacheco et al, 2008

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“…including peripheral nociceptors (Desroches et al., 2008), dorsal root ganglia (Khasabova et al., 2004), dorsal horn of the spinal cord (da Fonseca Pacheco et al., 2008; Desroches et al., 2008), the periaqueductal gray and other brain regions (Paldy et al., 2008; Wilson-Poe et al., 2013).”
Cannabinoid CB2receptor attenuates morphine‐induced inflammatory responses in activated microglial cells
Merighi, S., Gessi, S., Varani, K., Fazzi, D., Mirandola, P., & Borea, P. A. (2012) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2012.01948.x · Cited by 79 · see citing works
“In contrast, the release of endocannabinoids appears not to be involved in the peripheral antinociceptive effect induced by k- and d-opioid receptor agonists (da Fonseca Pacheco et al., 2008).”
Background
Involvement of the opioid and cannabinoid systems in pain control: New insights from knockout studies
Nadal, X., La Porta, C., Andreea Bura, S., & Maldonado, R. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.01.077 · Cited by 76 · see citing works
Cannabinoids: Current and Future Options to Treat Chronic and Chemotherapy-Induced Neuropathic Pain
Blanton, H. L., Brelsfoard, J., Deturk, N., Pruitt, K., Narasimhan, M., Morgan, D. J., & Guindon, J. (2019) · Drugs · doi:10.1007/s40265-019-01132-x · Cited by 70 · see citing works
Central antinociception induced by µ‐opioid receptor agonist morphine, but not δ‐ or κ‐, is mediated by cannabinoid CB1receptor
Pacheco, D. D. F., Klein, A., Perez, A. C., Pacheco, C. M. D. F., Francischi, J. N., Reis, G. M. L., & Duarte, I. D. G. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00310.x · Cited by 68 · see citing works
Self-citation
The Selective Monoacylglycerol Lipase Inhibitor MJN110 Produces Opioid-Sparing Effects in a Mouse Neuropathic Pain Model
Wilkerson, J. L., Niphakis, M. J., Grim, T. W., Mustafa, M. A., Abdullah, R. A., Poklis, J. L., Dewey, W. L., Akbarali, H. I., Banks, M. L., Wise, L. E., et al. (2016) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.115.229971 · Cited by 67 · see citing works
“Given that m-opioid and cannabinoid receptors are widely expressed in both the CNS and periphery, it is important to note that the observed behavioral effects may be due to receptor function at the peripheral nociceptors (Desroches et al., 2014), dorsal root ganglia (Khasabova et al., 2004), dorsal horn of the spinal…”
Background
Cannabinoid receptor-mediated antinociception with acetaminophen drug combinations in rats with neuropathic spinal cord injury pain
Hama, A. T., & Sagen, J. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.12.010 · Cited by 61 · see citing works
“AM630 administered peripherally but not centrally attenuated the antinociceptive effect of morphine (da Fonseca Pacheco et al., 2008; Pacheco Dda et al., 2009).”
Focus on current and future management possibilities in inflammatory bowel disease-related chronic pain
Zielińska, A., Sałaga, M., Włodarczyk, M., & Fichna, J. (2018) · International Journal of Colorectal Disease · doi:10.1007/s00384-018-3218-0 · Cited by 56 · see citing works
Spider venom peptides as potential drug candidates due to their anticancer and antinociceptive activities
Wu, T., Wang, M., Wu, W., Luo, Q., Jiang, L., Tao, H., & Deng, M. (2019) · The Journal of venomous animals and toxins including tropical diseases · doi:10.1590/1678-9199-jvatitd-14-63-18 · Cited by 52 · see citing works
Role of cannabinoid receptors in hepatic fibrosis and apoptosis associated with bile duct ligation in rats
Mahmoud, M. F., El-Swefy, S. E., Hasan, R. A., & Ibrahim, A. A. E.-M. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.08.021 · Cited by 50 · see citing works
Involvement of cannabinoid receptors in peripheral and spinal morphine analgesia
Desroches, J., Bouchard, J., Gendron, L., & Beaulieu, P. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.030 · Cited by 49 · see citing works
Practical Strategies Using Medical Cannabis to Reduce Harms Associated With Long Term Opioid Use in Chronic Pain
MacCallum, C. A., Eadie, L., Barr, A. M., Boivin, M. R., & Lu, S. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.633168 · Cited by 47 · see citing works
Effects of Alterations in Cannabinoid Signaling, Alone and in Combination with Morphine, on Pain-Elicited and Pain-Suppressed Behavior in Mice
Miller, L. L., Picker, M. J., Umberger, M. D., Schmidt, K. T., & Dykstra, L. A. (2012) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.191478 · Cited by 44 · see citing works
Peripheral interactions between cannabinoid and opioid systems contribute to the antinociceptive effect of crotalphine
Machado, F. C., Zambelli, V. O., Fernandes, A. C., Heimann, A. S., Cury, Y., & Picolo, G. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12488 · Cited by 42 · see citing works
“In fact, the endogenous opioid system could be involved in cannabinoid antinociception, and the endogenous cannabinoid system could play a role in opioid antinociception (Smith et al., 1994; Pugh et al., 1996; Ibrahim et al., 2005; da Fonseca Pacheco et al., 2008; Welch, 2009; Desroches and Beaulieu, 2010).”
Background
Endogenous opiates and behavior: 2008
Bodnar, R. J. (2009) · Peptides · doi:10.1016/j.peptides.2009.09.027 · Cited by 39 · see citing works
Exploring the first Rimonabant analog-opioid peptide hybrid compound, as bivalent ligand for CB1 and opioid receptors
Mollica, A., Pelliccia, S., Famiglini, V., Stefanucci, A., Macedonio, G., Chiavaroli, A., Orlando, G., Brunetti, L., Ferrante, C., Pieretti, S., et al. (2017) · Journal of Enzyme Inhibition and Medicinal Chemistry · doi:10.1080/14756366.2016.1260565 · Cited by 39 · see citing works
CB2 cannabinoid receptor antagonist SR144528 decreases mu-opioid receptor expression and activation in mouse brainstem: Role of CB2 receptor in pain
Páldy, E., Bereczki, E., Sántha, M., Wenger, T., Borsodi, A. D., Zimmer, A., & Benyhe, S. (2008) · Neurochemistry International · doi:10.1016/j.neuint.2008.08.005 · Cited by 40 · see citing works
“There is evidence about the involvement of endocannabinoids in the peripheral antinociception induced by activation of mu-opioid receptors (da Fonseca et al., 2008) and it has been shown that the peripheral endocannabinoid system is an important component of endogenous pain control mechanisms…”
Background
Novel orally available salvinorin A analog PR-38 protects against experimental colitis and reduces abdominal pain in mice by interaction with opioid and cannabinoid receptors
Sałaga, M., Polepally, P. R., Zakrzewski, P. K., Cygankiewicz, A. I., Sobczak, M., Kordek, R., Zjawiony, J. K., Krajewska, W. M., & Fichna, J. (2014) · Biochemical Pharmacology · doi:10.1016/j.bcp.2014.09.018 · Cited by 37 · see citing works
“A crosstalk between MOP and CB1 receptors has already been reported in the in vivo studies on peripheral analgesia [18,26,27].”
Background
Involvement of opioid system in antidepressant‐like effect of the cannabinoid CB 1 receptor inverse agonist AM ‐251 after physical stress in mice
Ostadhadi, S., Haj‐Mirzaian, A., Nikoui, V., Kordjazy, N., & Dehpour, A. R. (2015) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12518 · Cited by 36 · see citing works
“On the other hand, AM-251, a selective CB1 receptor inverse agonist, antagonizes morphine-induced peripheral analgesia.(48) Furthermore, CB1 agonists were reported to strengthen morphine analgesia.”
Background
Effects of morphine on pain-elicited and pain-suppressed behavior in CB1 knockout and wildtype mice
Miller, L. L., Picker, M. J., Schmidt, K. T., & Dykstra, L. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2232-5 · Cited by 35 · see citing works
“The CB1 antagonist AM251 blocks morphine-induced antinociception as measured by an inflammatory pain model (Pacheco et al. 2008) and the tail-flick test in mice (Pacheco et al. 2009).”
Influential
Are Opioids Effective in Relieving Neuropathic Pain?
Schembri, E. (2018) · SN Comprehensive Clinical Medicine · doi:10.1007/s42399-018-0009-4 · Cited by 32 · see citing works
“Despite such negative reviews on cannabinoids, endocannabinoid activity may be critical for morphine’s action [225].”
Background
Opioid-sparing effects of cannabinoids: Myth or reality?
Foll, B. L. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110065 · Cited by 32 · see citing works
Receptome: Interactions between three pain-related receptors or the “Triumvirate” of cannabinoid, opioid and TRPV1 receptors
Zádor, F., & Wollemann, M. (2015) · Pharmacological Research · doi:10.1016/j.phrs.2015.10.015 · Cited by 30 · see citing works
Effects of neuropeptide FF system on CB1 and CB2 receptors mediated antinociception in mice
Fang, Q., Han, Z., Li, N., Wang, Z., He, N., & Wang, R. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.09.013 · Cited by 30 · see citing works
Morphine modulation of pain processing in medial and lateral pain pathways
Wang, J.-Y., Huang, J., Chang, J.-Y., Woodward, D. J., & Luo, F. (2009) · Molecular Pain · doi:10.1186/1744-8069-5-60 · Cited by 29 · see citing works
The Involvement of the Endocannabinoid System in the Peripheral Antinociceptive Action of Ketamine
Ferreira, R. C. M., Castor, M. G. M. E., Piscitelli, F., Marzo, V. D., Duarte, I. D. G., & Romero, T. R. L. (2017) · Journal of Pain · doi:10.1016/j.jpain.2017.12.002 · Cited by 26 · see citing works
Self-citation
PnPP‐19, a spider toxin peptide, induces peripheral antinociception through opioid and cannabinoid receptors and inhibition of neutral endopeptidase
Freitas, A. C. N., Pacheco, D. F., Machado, M. F. M., Carmona, A. K., Duarte, I. D. G., & de Lima, M. E. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13448 · Cited by 26 · see citing works
“In addition, our group has demonstrated that the opioidergic and endocannabinoidergic systems are strongly linked and the 1492 British Journal of Pharmacology (2016) 173 1491–1501 activation of one pathway is mediated by the other (Pacheco et al., 2008; Pacheco et al., 2009; Reis et al., 2009).”
BackgroundMethodResultInfluentialSelf-citation
The Endocannabinoid System Contributes to Electroacupuncture Analgesia
MacDonald, I. J., & Chen, Y. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.594219 · Cited by 24 · see citing works
A spider derived peptide, PnPP-19, induces central antinociception mediated by opioid and cannabinoid systems
Pacheco, D. D. F., Freitas, A. C. N., Pimenta, A. M. C., Duarte, I. D. G., & de Lima, M. E. (2016) · The Journal of venomous animals and toxins including tropical diseases · doi:10.1186/s40409-016-0091-6 · Cited by 21 · see citing works
“opioids and cannabinoids in the antinociceptive action of several substances [9, 10].”
BackgroundSelf-citation
The association between endogenous opioid function and morphine responsiveness: a moderating role for endocannabinoids
Bruehl, S. P., Burns, J. W., Morgan, A., Koltyn, K. F., Gupta, R. K., Buvanendran, A., Edwards, D. A., Chont, M., Kingsley, P. J., Marnett, L. J., et al. (2018) · Pain · doi:10.1097/j.pain.0000000000001447 · Cited by 20 · see citing works
“It has been suggested that endocannabinoid and EO systems may interact,(44,45) with a number of animal studies suggesting that endocannabinoids can influence responses to exogenous opioid analgesics.(2,3,28,34,35,46,53) However, human studies evaluating Sponsorships or competing interests that may be relevant to conte…”
Role of sex hormones in modulating breast and ovarian cancer associated pain
McHann, M. C., Blanton, H. L., & Guindon, J. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111320 · Cited by 17 · see citing works
Investigation of the Involvement of the Endocannabinoid System in TENS-Induced Antinociception
de Oliveira, H. U., dos Santos, R. S., Malta, I., Pinho, J. P., Almeida, A. F. S., Sorgi, C. A., Peti, A. P. F., Xavier, G. S., dos Reis, L. M., Faccioli, L. H., et al. (2019) · Journal of Pain · doi:10.1016/j.jpain.2019.11.009 · Cited by 16 · see citing works
Peripheral interactions between cannabinoid and opioid receptor agonists in a model of inflammatory mechanical hyperalgesia
Auh, Q.-S., Chun, Y. H., Melemedjian, O. K., Zhang, Y., & Ro, J. Y. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.07.009 · Cited by 14 · see citing works
Peripheral Antinociception Induced by Aripiprazole Is Mediated by the Opioid System
Ferreira, R. C. M., Almeida-Santos, A. F., Duarte, I. D. G., de Aguiar, D. C., Moreira, F. A., & Romero, T. R. L. (2017) · BioMed Research International · doi:10.1155/2017/8109205 · Cited by 14 · see citing works
Self-citation
CB1 Cannabinoid Agonist (WIN55,212-2) Within the Basolateral Amygdala Induced Sensitization to Morphine and Increased the Level of μ-Opioid Receptor and c-fos in the Nucleus Accumbens
Molaei, M., Fatahi, Z., Zaringhalam, J., & Haghparast, A. (2016) · Journal of Molecular Neuroscience · doi:10.1007/s12031-016-0716-9 · Cited by 14 · see citing works
Hemorphins Act as Homeostatic Agents in Response to Endotoxin-Induced Stress
Barkhudaryan, N., Zakaryan, H., Sarukhanyan, F. P., Gabrielyan, A., Dosch, D., Kellermann, J., & Lottspeich, F. (2009) · Neurochemical Research · doi:10.1007/s11064-009-0097-3 · Cited by 14 · see citing works
Peltatoside Isolated from Annona crassiflora Induces Peripheral Antinociception by Activation of the Cannabinoid System
de Oliveira, C. M., Veloso, C. C., Ferreira, R. C. M., Lage, G. A., Pimenta, L. P. S., Duarte, I. D. G., Romero, T. R. L., & Perez, A. C. (2016) · Planta Medica · doi:10.1055/s-0042-113386 · Cited by 14 · see citing works
Self-citation
Curcumin induces peripheral antinociception by opioidergic and cannabinoidergic mechanism: Pharmacological evidence
Aguiar, D. D., Gonzaga, A. C. R., Teófilo, A. L. H., Miranda, F. A., Perez, A. C., Duarte, I. D. G., & Romero, T. R. L. (2022) · Life Sciences · doi:10.1016/j.lfs.2021.120279 · Cited by 13 · see citing works
Self-citation
Tingenone, a pentacyclic triterpene, induces peripheral antinociception due to cannabinoid receptors activation in mice
Veloso, C. C., Ferreira, R. C. M., Rodrigues, V. G., Duarte, L. P., Klein, A., Duarte, I. D. G., Romero, T. R. L., & Perez, A. C. (2017) · Inflammopharmacology · doi:10.1007/s10787-017-0391-7 · Cited by 13 · see citing works
“Pacheco et al. (2008) demonstrated that antinociception induced by activation of l-opioid receptors was antagonized by CB1 receptor antagonist and partially by CB2 cannabinoid receptor antagonist.”
BackgroundSelf-citation
Evidence for the involvement of opioid and cannabinoid systems in the peripheral antinociception mediated by resveratrol
Oliveira, C. D. C., Castor, M. G. M. E., Castor, C. G. M. E., Costa, Á. D. F., Ferreira, R. C. M., da Silva, J. F., Pelaez, J. M. N., Capettini, L. D. S. A., Lemos, V. S., Duarte, I. D. G., et al. (2019) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2019.02.004 · Cited by 13 · see citing works
Self-citation
Practical Considerations for the Use of Cannabis in Cancer Pain Management—What a Medical Oncologist Should Know
Gorzo, A., Havasi, A. D., Spînu, Ș., Oprea, A. L., Burz, C. C., & Sur, D. G. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11175036 · Cited by 13 · see citing works
Cannabidiol induces systemic analgesia through activation of the PI3Kγ/nNOS/NO/KATP signaling pathway in neuropathic mice. A KATP channel S-nitrosylation-dependent mechanism
de Almeida, D. L., Ferreira, R. C. M., Fonseca, F. C. D. S., Machado, D. P. D., Aguiar, D. D., Guimarães, F. S., Duarte, I. D. G., & Romero, T. R. L. (2024) · Nitric Oxide · doi:10.1016/j.niox.2024.02.005 · Cited by 12 · see citing works
Self-citation
Fatty Acid Amide Hydrolase–morphine Interaction Influences Ventilatory Response to Hypercapnia and Postoperative Opioid Outcomes in Children
Chidambaran, V., Pilipenko, V. V., Spruance, K., Venkatasubramanian, R., Niu, J., Fukuda, T., Mizuno, T., Zhang, K., Kaufman, K. M., Vinks, A. A. T. M. M., et al. (2016) · Pharmacogenomics · doi:10.2217/pgs-2016-0147 · Cited by 11 · see citing works
The effect of chronic opioid vs. cannabinoid exposure on the expression of tolerance to morphine- or WIN-55,212-2-induced analgesia and hypothermia in the guinea pig
Maguma, H. T., & TAYLOR, D. A. H. B. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.04.010 · Cited by 11 · see citing works
Role of Endocannabinoid System in the Peripheral Antinociceptive Action of Aripiprazole
Ferreira, R. C. M., Almeida-Santos, A. F., Duarte, I. D. G., de Aguiar, D. C., Moreira, F. A., & Romero, T. R. L. (2018) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000003723 · Cited by 10 · see citing works
Self-citation
Endocannabinoid mechanism for orofacial antinociception induced by electroacupuncture in acupoint St36 in rats
Almeida, R. T., Romero, T. R. L., Castor, M. G. M. E., Galdino, G. S., Perez, A. C., & Duarte, I. D. G. (2016) · Pharmacological Reports · doi:10.1016/j.pharep.2016.07.004 · Cited by 10 · see citing works
Self-citation
PnAn13, an antinociceptive synthetic peptide inspired in the Phoneutria nigriventer toxin PnTx4(6–1) (δ-Ctenitoxin-Pn1a)
Emerich, B. L., Ferreira, R. C. M., Machado‐de‐Ávila, R. A., Resende, J. M., Duarte, I. D. G., & de Lima, M. E. (2020) · Toxicon X · doi:10.1016/j.toxcx.2020.100045 · Cited by 9 · see citing works
Self-citation
Probable involvement of Ca2+-activated Cl− channels (CaCCs) in the activation of CB1 cannabinoid receptors
Romero, T. R. L., Pacheco, D. D. F., & Duarte, I. D. G. (2012) · Life Sciences · doi:10.1016/j.lfs.2012.10.006 · Cited by 8 · see citing works
Self-citation
Nitric oxide and potassium channels but not opioid and cannabinoid receptors mediate tramadol-induced peripheral antinociception in rat model of paw pressure withdrawal
Santos, R. R. S., Machado, D. P., Romero, T. R. L., & Duarte, I. D. G. (2023) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2023-0314 · Cited by 7 · see citing works
Self-citation
Physiologic Advantages of Peripheral Nerve Blockade Translate to Decreased Length of Stay and Improved Patient Satisfaction
Kerfeld, M. J., Hambsch, Z. J., McEntire, D., Kirkpatrick, D. R., Cai, J., Youngblood, C. F., Agrawal, D. K., & Reisbig, M. D. (2016) · Research and Practice in Anesthesiology – Open Journal · doi:10.17140/aoj-1-103 · Cited by 7 · see citing works
Microinjection of WIN55,212-2 as A Cannabinoid Agonist into The Basolateral Amygdala Induces Sensitization to Morphine in Rats.
Molaei, M., Sanati, M. H., Zaringhalam, J., & Haghparast, A. (2014) · PubMed Central · Cited by 6 · see citing works
Cannabinoid CB1 receptor and mu-opioid receptor interaction: new insights from conditional knockout mice
Alton, H., Linz, E., Bi, G., Soler‐Cedeño, O., Maras, M., & Xi, Z. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02245-6 · Cited by 5 · see citing works
Kahweol, a natural diterpene from coffee, induces peripheral antinociception by endocannabinoid system activation
Guzzo, L. S., Oliveira, C. C., Ferreira, R. C. M., Machado, D., Castor, M. G. M. E., Perez, A. C., Piscitelli, F., Marzo, V. D., Romero, T. R. L., & Duarte, I. D. G. (2021) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x2021e11071 · Cited by 5 · see citing works
“The antinociceptive effect of a m-opioid receptor agonist, but not d and k agonists, was blocked by the administration of a CB1 cannabinoid receptor antagonist peripherally and centrally, suggesting that the central and peripheral antinociceptive effect of morphine may be mediated by the endocannabinoid system (12,13).”
BackgroundMethodInfluentialSelf-citation
Synergistic action between a synthetic cannabinoid compound and tramadol in neuropathic pain rats
Quiñonez‐Bastidas, G. N., Osuna‐Martínez, U., Reda-Licea, A. L., López‐Ortíz, M., Regla, I., & Navarrete, A. (2022) · Acta Pharmaceutica · doi:10.2478/acph-2022-0037 · Cited by 5 · see citing works
α2-Adrenoceptor agonist induces peripheral antinociception via the endocannabinoid system
Romero, T. R. L., Castor, M. G. M. E., Parrella, C., Piscitelli, F., Marzo, V. D., & Duarte, I. D. G. (2020) · Pharmacological Reports · doi:10.1007/s43440-019-00053-6 · Cited by 5 · see citing works
Self-citation
Electroacupuncture alleviates morphine‑induced hyperalgesia by regulating spinal CB1�receptors and ERK1/2 activity
Zheng, Y., Yu, Y., Xie, K., Yuan, Y., Chen, Y., Wang, C., Wang, G., & Yu, Y. (2019) · Molecular Medicine Reports · doi:10.3892/mmr.2019.10329 · Cited by 5 · see citing works
Class A GPCRs: Cannabinoid and Opioid Receptor Heteromers
Sierra, S., Gomes, I., & Devi, L. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-60174-8_7 · Cited by 3 · see citing works
Bradykinin induces peripheral antinociception in PGE2-induced hyperalgesia in mice
Ferreira, R. C. M., Fonseca, F. C. D. S., de Almeida, D. L., Freitas, A. C. N., Peigneur, S., Romero, T. R. L., Amaral, F. A., & Duarte, I. D. G. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.114965 · Cited by 2 · see citing works
Self-citation
Opioid-induced respiratory depression: the role of genetics
Chidambaran, V., & McAuliffe, J. J. (2017) · Expert Review of Precision Medicine and Drug Development · doi:10.1080/23808993.2017.1331704 · Cited by 2 · see citing works
“Some of the effects of cannabinoids involve activation of the opioid system [96] and vice versa [97].”
Background
Premedication and general anesthetic agents decrease plasma concentration of the endocannabinoid anandamide in dogs
Chua, A., McMichael, M., Jukier, T., Arnold, R. D., Hung, W., Harris, S., Zhang, C., & Bustamante, H. (2025) · American Journal of Veterinary Research · doi:10.2460/ajvr.24.11.0366 · Cited by 1 · see citing works
Mechanismen der endogenen Schmerzhemmung
Laube, W. (2022) · Springer eBooks · doi:10.1007/978-3-662-63846-0_6 · Cited by 1 · see citing works
Contribuição do sistema canabinóide e sua interação com o sistema opióide na antinocicepção induzida pela crotalfina, um analgésico tipo opióide.
Machado, F. C. (2013) · doi:10.11606/d.42.2013.tde-15032014-092511
Differential Effects of Repeated Low-Dose Ketamine on Cross-Frequency Interactions in Naïve and Preclinical Models of Movement Disorders
Ye, T. (2018) · UA Campus Repository (The University of Arizona)
Cannabinoids as a Substitute for Opioids: Basic Science and Clinical Evidence
MacCallum, C. A., de Freitas, L., Eadie, L., & Narouze, S. (2021) · Springer eBooks · doi:10.1007/978-3-030-69186-8_27
Bradykinin Induces Peripheral Antinociception in PGE 2-Induced Hyperalgesia in MicePreprint
Ferreira, R. C. M., Fonseca, F. C. D. S., de Almeida, D. L., Freitas, A. C. N., Peigneur, S., Romero, T. R. L., Amaral, F. A., & Duarte, I. D. G. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3982056
Self-citation
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Antinociceptive Effect of Dillenia indica (Linn.) Mediated by Opioid and Cannabinoid Systems: Pharmacological and Chemical Studies
de Souza, A. A., Viegas, F. P. D., Gontijo, V. S., Vieira, J. S., Giusti‐Paiva, A., Vilela, F. C., da Silva, G. A., Amaral, J. G., Lopes, N. P., & Viegas, C. (2023) · Chemistry & Biodiversity · doi:10.1002/cbdv.202301508
Antinociceptive synergy in a peripheral hyperalgesia model: interplay of cannabinoidergic, adrenergic, and opioidergic systems and their antagonismPreprint
Lopes, C. F. B., Santos‐Silva, T., Fonseca, F. C. D. S., de Queiroz, B. F. G., Duarte, I. D. G., & Romero, T. R. L. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.30.596637
“The dose of each drug used in this study was previously determined by other works published by our research group (Da Fonseca Pacheco et al., 2008; Romero et al., 2013, 2012; Romero and Duarte, 2009).”
MethodSelf-citation
The synthetic peptide, PnPP-15, derived from the PnTx2-6 toxin of the spider Phoneutria nigriventer, induces peripheral antinociception involving neprilysin, opioid, and cannabinoid systems
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Relative contribution of peripheral versus central opioid receptors to antinociception
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Authors: Da Fonseca Pacheco, D., Klein, A., De Castro Perez, A., Da Fonseca Pacheco, C. M., De Francischi, J. N., & Duarte, I. D. G.
Affiliations: Universidade Federal de Minas Gerais (BR)
Corresponding author: Duarte, I D G
ORCID: Klein, A
Duarte, I D G
Venue: British Journal of Pharmacology
Publisher: Wiley
Published: 2008-07
Volume: 154
Issue: 5
Pages: 1143-1149
ISSN: 0007-1188 (ISSN-L)
1476-5381
DOI: 10.1038/bjp.2008.175
PMC: PMC2465574
OpenAlex: W2029908981
Cited by: 81
References: 59
Citations by year: 2025: 3 · 2024: 3 · 2023: 2 · 2022: 5 · 2021: 7 · 2020: 3 · 2019: 6 · 2018: 6 · 2017: 9 · 2016: 10 · 2015: 2 · 2014: 4 · 2013: 4 · 2012: 5
FWCI: 2.80
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 212 d)
Locations: British Journal of Pharmacology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Topics: Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: morphine, mu-opioid receptor, delta opioid receptor, kappa opioid receptor, cannabinoid receptors, peripheral antinociception, endocannabinoids, CB1 receptor, CB2 receptor, AM251, AM630, fatty acid amide hydrolase, opioid-cannabinoid interaction
MeSH terms: Fatty Acid Amide Hydrolases, Amidohydrolases, Analgesics, Opioid, Animals, Arachidonic Acids, Benzamides, Benzomorphans, Disease Models, Animal, Dose-Response Relationship, Drug, Enzyme Inhibitors, Hyperalgesia, Indoles, Male, Morphine, Pain, Pain Measurement, Piperazines, Piperidines, Pyrazoles, Dinoprostone, Rats, Wistar, Receptors, Opioid, mu, Receptors, Opioid, delta, Receptors, Opioid, kappa, Receptor, Cannabinoid, CB1, Receptor, Cannabinoid, CB2, Rats, Organophosphonates, Cannabinoid Receptor Modulators

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The μ‐opioid receptor agonist morphine, but not agonists at δ‐ or κ‐opioid receptors, induces peripheral antinociception mediated by cannabinoid receptors

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