The central versus peripheral antinociceptive effects of μ-opioid receptor agonists in the new model of rat visceral pain

Brain Research Bulletin

Volumn 87, Issue 2-3, 2012, Pages 238-243

  Al Khrasani, Mahmoud ^a   Lackó, Erzsébet ^a   Riba, Pál ^a   Király, Kornél ^a   Sobor, Melinda ^a,c   Timár, Júlia ^a   Mousa, Shaaban ^b   Schäfer, Michael ^b   Fürst, Susanna ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c National Inst for Quality and Organizational Development of Healthcare and Medicine   (Hungary)

Author keywords

Antinociception; DAMGO; Morphine; Peripheral MOR; Rat acetic acid induced late permanent visceral pain

Indexed keywords

17 METHYLNALOXONE; ACETIC ACID; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MORPHINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENCY; LATENT PERIOD; MALE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; VISCERAL PAIN;

ACETIC ACID; ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; DRUG INTERACTIONS; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; MORPHINE; NALOXONE; NARCOTIC ANTAGONISTS; QUATERNARY AMMONIUM COMPOUNDS; RATS; VISCERAL PAIN;

EID: 84856606059     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2011.10.018     Document Type: Article

References (56)

1. Al-Khrasani M., Spetea M., Friedmann T., Riba P., Kiraly K., Schmidhammer H., Furst S. DAMGO and 6beta-glycine substituted 14-O-methyloxymorphone but not morphine show peripheral, preemptive antinociception after systemic administration in a mouse visceral pain model and high intrinsic efficacy in the isolated rat vas deferens. Brain Research Bulletin 2007, 74:369-375.
2. Bagnol D., Mansour A., Akil H., Watson S.J. Cellular localization and distribution of the cloned mu and kappa opioid receptors in rat gastrointestinal tract. Neuroscience 1997, 81:579-591.
3. Bedini A., Baiula M., Gentilucci L., Tolomelli A., De Marco R., Spampinato S. Peripheral antinociceptive effects of the cyclic endomorphin-1 analog c[YpwFG] in a mouse visceral pain model. Peptides 2010, 31:2135-2140.
4. Bentley G.A., Newton S.H., Starr J. Evidence for an action of morphine and the enkephalins on sensory nerve endings in the mouse peritoneum. British Journal of Pharmacology 1981, 73:325-332.
5. Berg K.A., Patwardhan A.M., Sanchez T.A., Silva Y.M., Hargreaves K.M., Clarke W.P. Rapid modulation of micro-opioid receptor signaling in primary sensory neurons. The Journal of Pharmacology and Experimental Therapeutics 2007, 321:839-847.
6. Bianchi G., Fiocchi R., Tavani A., Manara L. Quaternary narcotic antagonists' relative ability to prevent antinociception and gastrointestinal transit inhibition in morphine-treated rats as an index of peripheral selectivity. Life Sciences 1982, 30:1875-1883.
7. Coggeshall R.E., Zhou S., Carlton S.M. Opioid receptors on peripheral sensory axons. Brain Research 1997, 764:126-132.
8. de Oliveira M.S., da Silva Fernandes M.J., Scorza F.A., Persike D.S., Scorza C.A., da Ponte J.B., de Albuquerque M., Cavalheiro E.A., Arida R.M. Acute and chronic exercise modulates the expression of MOR opioid receptors in the hippocampal formation of rats. Brain Research Bulletin 2010, 83:278-283.
9. Fickel J., Bagnol D., Watson S.J., Akil H. Opioid receptor expression in the rat gastrointestinal tract: a quantitative study with comparison to the brain. Brain Research. Molecular Brain Research 1997, 46:1-8.
10. Fields H.L. Understanding how opioids contribute to reward and analgesia. Regional Anesthesia and Pain Medicine 2007, 32:242-246.
11. Furst S. Transmitters involved in antinociception in the spinal cord. Brain Research Bulletin 1999, 48:129-141.
12. Furst S., Riba P., Friedmann T., Timar J., Al-Khrasani M., Obara I., Makuch W., Spetea M., Schutz J., Przewlocki R., Przewlocka B., Schmidhammer H. Peripheral versus central antinociceptive actions of 6-amino acid-substituted derivatives of 14-O-methyloxymorphone in acute and inflammatory pain in the rat. The Journal of Pharmacology and Experimental Therapeutics 2005, 312:609-618.
13. Giron R., Abalo R., Goicoechea C., Martin M.I., Callado L.F., Cano C., Goya P., Jagerovic N. Synthesis and opioid activity of new fentanyl analogs. Life Sciences 2002, 71:1023-1034.
14. Goicoechea C., Sanchez E., Cano C., Jagerovic N., Martin M.I. Analgesic activity and pharmacological characterization of N-[1-phenylpyrazol-3-yl]-N-[1-(2-phenethyl)-4-piperidyl] propenamide, a new opioid agonist acting peripherally. European Journal of Pharmacology 2008, 595:22-29.
15. Handa B.K., Land A.C., Lord J.A., Morgan B.A., Rance M.J., Smith C.F. Analogues of beta-LPH61-64 possessing selective agonist activity at mu-opiate receptors. European Journal of Pharmacology 1981, 70:531-540.
16. Harada H., Hosonuma K., Fujii T., Kawashima K. Enhancement of cerebral cortical acetylcholine release by intraperitoneal acetic acid and its suppression by analgesics in freely moving rats. Neuroscience Letters 2000, 284:163-166.
17. Hasegawa Y., Kishimoto S., Shibatani N., Nomura H., Ishii Y., Onishi M., Inotsume N., Takeuchi Y., Fukushima S. The pharmacokinetics of morphine and its glucuronide conjugate in a rat model of streptozotocin-induced diabetes and the expression of MRP2, MRP3 and UGT2B1 in the liver. The Journal of Pharmacy and Pharmacology 2010, 62:310-314.
18. Hassan A.H., Ableitner A., Stein C., Herz A. Inflammation of the rat paw enhances axonal transport of opioid receptors in the sciatic nerve and increases their density in the inflamed tissue. Neuroscience 1993, 55:185-195.
19. Hayashida K., Takeuchi T., Shimizu H., Ando K., Harada E. Novel function of bovine milk-derived lactoferrin on antinociception mediated by mu-opioid receptor in the rat spinal cord. Brain Research 2003, 965:239-245.
20. He L., Kim J., Ou C., McFadden W., van Rijn R.M., Whistler J.L. Methadone antinociception is dependent on peripheral opioid receptors. The Journal of Pain 2009, 10:369-379.
21. He L., Lee N.M. DynorphinA-(2-17) restores spinal/supraspinal morphine synergy in morphine-tolerant mice. The Journal of Pharmacology and Experimental Therapeutics 1997, 280:1210-1214.
22. Herz A., Teschemaker H.J. Activities and sites of antinocicpetive action of morphine-like analgesics and kinetics of distribution following intravenous, intracerebral and intraventricular application. Advances in Drug Research 1971, 79-119. Academic Press Limited, London. N. Harper, A.B. Simmonds (Eds.).
23. Ji Y., Murphy A.Z., Traub R.J. Sex differences in morphine-induced analgesia of visceral pain are supraspinally and peripherally mediated. American Journal of Physiology 2006, 291:R307-R314.
24. Kharkevich D.A., Churukanov V.V. Pharmacological regulation of descending cortical control of the nociceptive processing. European Journal of Pharmacology 1999, 375:121-131.
25. Labuz D., Mousa S.A., Schafer M., Stein C., Machelska H. Relative contribution of peripheral versus central opioid receptors to antinociception. Brain Research 2007, 1160:30-38.
26. Lewanowitsch T., Irvine R.J. Naloxone methiodide reverses opioid-induced respiratory depression and analgesia without withdrawal. European Journal of Pharmacology 2002, 445:61-67.
27. List T., Tegelberg A., Haraldson T., Isacsson G. Intra-articular morphine as analgesic in temporomandibular joint arthralgia/osteoarthritis. Pain 2001, 94:275-282.
28. Litchfield J.T., Wilcoxon F. A simplified method of evaluating dose-effect experiments. The Journal of Pharmacology and Experimental Therapeutics 1949, 96:99-113.
29. Mansour A., Fox C.A., Akil H., Watson S.J. Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends in Neurosciences 1995, 18:22-29.
30. Miller L., Shaw J.S., Whiting E.M. The contribution of intrinsic activity to the action of opioids in vitro. British Journal of Pharmacology 1986, 87:595-601.
31. Mousa S.A., Shaqura M., Brendl U., Al-Khrasani M., Furst S., Schafer M. Involvement of the peripheral sensory and sympathetic nervous system in the vascular endothelial expression of ICAM-1 and the recruitment of opioid-containing immune cells to inhibit inflammatory pain. Brain, Behavior, and Immunity 2010, 24:1310-1323.
32. Mousa S.A., Zhang Q., Sitte N., Ji R., Stein C. Beta-endorphin-containing memory-cells and mu-opioid receptors undergo transport to peripheral inflamed tissue. Journal of Neuroimmunology 2001, 115:71-78.
33. Mu X., Wu A., Wu J., Liu Y., Zhang Y., Yue Y., Fang L., Wang Y. Effects of anesthetic propofol on release of amino acids from the spinal cord during visceral pain. Neuroscience Letters 2010, 484:206-209.
34. Narayana Raju K.V., Ashok Kumar D., Arutselvan N., Thejomoorthy P., Puvanakrishnan R. Antinociceptive and antipyretic effects of a derivatized tetrapeptide from lactoferrin in rats. Peptides 2005, 26:615-619.
35. Negri L., Improta G. Distribution and metabolism of dermorphin in rats. Pharmacological Research Communications 1984, 16:1183-1191.
36. Negri L., Lattanzi R., Tabacco F., Scolaro B., Rocchi R. Glycodermorphins: opioid peptides with potent and prolonged analgesic activity and enhanced blood-brain barrier penetration. British Journal of Pharmacology 1998, 124:1516-1522.
37. Nozaki-Taguchi N., Yaksh T.L. Characterization of the antihyperalgesic action of a novel peripheral mu-opioid receptor agonist-loperamide. Anesthesiology 1999, 90:225-234.
38. Ossipov M.H., Lai J., King T., Vanderah T.W., Malan T.P., Hruby V.J., Porreca F. Antinociceptive and nociceptive actions of opioids. Journal of Neurobiology 2004, 61:126-148.
39. Patwardhan A.M., Diogenes A., Berg K.A., Fehrenbacher J.C., Clarke W.P., Akopian A.N., Hargreaves K.M. PAR-2 agonists activate trigeminal nociceptors and induce functional competence in the delta opioid receptor. Pain 2006, 125:114-124.
40. Pol O., Alameda F., Puig M.M. Inflammation enhances mu-opioid receptor transcription and expression in mice intestine. Molecular Pharmacology 2001, 60:894-899.
41. Porreca F., Mosberg H.I., Omnaas J.R., Burks T.F., Cowan A. Supraspinal and spinal potency of selective opioid agonists in the mouse writhing test. The Journal of Pharmacology and Experimental Therapeutics 1987, 240:890-894.
42. Riba P., Ben Y., Smith A.P., Furst S., Lee N.M. Morphine tolerance in spinal cord is due to interaction between mu- and delta-receptors. The Journal of Pharmacology and Experimental Therapeutics 2002, 300:265-272.
43. Rowan M.P., Ruparel N.B., Patwardhan A.M., Berg K.A., Clarke W.P., Hargreaves K.M. Peripheral delta opioid receptors require priming for functional competence in vivo. European Journal of Pharmacology 2009, 602:283-287.
44. Schafer M., Imai Y., Uhl G.R., Stein C. Inflammation enhances peripheral mu-opioid receptor-mediated analgesia, but not mu-opioid receptor transcription in dorsal root ganglia. European Journal of Pharmacology 1995, 279:165-169.
45. Schiller P.W., Nguyen T.M., Chung N.N., Dionne G., Martel R. Peripheral antinociceptive effect of an extremely mu-selective polar dermorphin analog (DALDA). Progress in Clinical and Biological Research 1990, 328:53-56.
46. Schiller P.W., Nguyen T.M., Chung N.N., Lemieux C. Dermorphin analogues carrying an increased positive net charge in their " message" domain display extremely high mu opioid receptor selectivity. Journal of Medicinal Chemistry 1989, 32:698-703.
47. Spampinato S., Qasem A.R., Calienni M., Murari G., Gentilucci L., Tolomelli A., Cardillo G. Antinociception by a peripherally administered novel endomorphin-1 analogue containing beta-proline. European Journal of Pharmacology 2003, 469:89-95.
48. Stein C., Clark J.D., Oh U., Vasko M.R., Wilcox G.L., Overland A.C., Vanderah T.W., Spencer R.H. Peripheral mechanisms of pain and analgesia. Brain Research Reviews 2009, 60:90-113.
49. Stein C., Hassan A.H., Przewlocki R., Gramsch C., Peter K., Herz A. Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation. Proceedings of the National Academy of Sciences of the United States of America 1990, 87:5935-5939.
50. Stein C., Pfluger M., Yassouridis A., Hoelzl J., Lehrberger K., Welte C., Hassan A.H. No tolerance to peripheral morphine analgesia in presence of opioid expression in inflamed synovia. The Journal of Clinical Investigation 1996, 98:793-799.
51. Stein C., Schafer M., Hassan A.H. Peripheral opioid receptors. Annals of Medicine 1995, 27:219-221.
52. Stein C., Schafer M., Machelska H. Attacking pain at its source: new perspectives on opioids. Nature Medicine 2003, 9:1003-1008.
53. Szeto H.H., Lovelace J.L., Fridland G., Soong Y., Fasolo J., Wu D., Desiderio D.M., Schiller P.W. In vivo pharmacokinetics of selective mu-opioid peptide agonists. The Journal of Pharmacology and Experimental Therapeutics 2001, 298:57-61.
54. Takasuna M., Negus S.S., DeCosta B.R., Woods J.H. Opioid pharmacology of the antinociceptive effects of loperamide in mice. Behavioural Pharmacology 1994, 5:189-195.
55. Tian Y.L., Guo Y., Cao D.Y., Zhang Q., Wang H.S., Zhao Y. Local application of morphine suppresses glutamate-evoked activities of C and adelta afferent fibers in rat hairy skin. Brain Research 2005, 1059:28-34.
56. Tsang B.K., He Z., Wongchanapai W., Ho I.K., Eichhorn J.H. Visceral analgesic tolerance to intrathecal butorphanol in rats. Canadian Journal of Anaesthesia=Journal Canadien D'anesthesie 1998, 45:1019-1023.