Comparison of tolerance to morphine-induced respiratory and analgesic effects in mice

Toxicology Letters

Volumn 217, Issue 3, 2013, Pages 251-259

  Mohammed, Wasseem ^a,b,c   Alhaddad, Hisham ^a,b,c   Marie, Nicolas ^a,b,c   Tardy, Floriane ^a,b,c   Lamballais, Florence ^a,b,c   Risède, Patricia ^a,b,c   Noble, Florence ^a,b,c   Baud, Frédéric J ^a,b,c,d   Mégarbane, Bruno ^a,b,c,d  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b INSERM   (France)

^c CNRS   (France)

^d HÔPITAL LARIBOISIÈRE   (France)

Author keywords

Analgesia; Morphine; Mu opioid receptor; Respiratory effects; Tolerance

Indexed keywords

ADENYLATE CYCLASE; MORPHINE; MU OPIATE RECEPTOR;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN STEM; CONTROLLED STUDY; DOSE RESPONSE; DRUG BINDING; DRUG TOLERANCE; ENZYME ACTIVITY; LATENT PERIOD; MALE; MOUSE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PLETHYSMOGRAPHY; PRIORITY JOURNAL; RESPIRATION DEPRESSION;

ADENYLATE CYCLASE; ANALGESICS, OPIOID; ANIMALS; BRAIN; DRUG TOLERANCE; MALE; MICE; MORPHINE; PAIN MEASUREMENT; PLETHYSMOGRAPHY, WHOLE BODY; RANDOM ALLOCATION; RECEPTORS, OPIOID, MU; RESPIRATION;

EID: 84874013688     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.12.021     Document Type: Article

References (65)

1. Alhaddad H., Cisternino S., Declèves X., Tournier N., Schlatter J., Chiadmi F., et al. Respiratory toxicity of buprenorphine results from the blockage of P-glycoprotein-mediated efflux of norbuprenorphine at the blood-brain barrier in mice. Critical Care Medicine 2012, 40:3215-3223.
2. Al-Hasani R., Bruchas M.R. Molecular mechanisms of opioid receptor-dependent signaling and behavior. Anesthesiology 2011, 115:1363-1381.
3. Athanasos P., Smith C.S., White J.M., Somogyi A.A., Bochner F., Ling W. Methadone maintenance patients are cross-tolerant to the antinociceptive effects of very high plasma morphine concentrations. Pain 2006, 120:267-275.
4. Avidor-Reiss T., Bayewitch M., Levy R., Matus-Leibovitch N., Nevo I., Vogel Z. Adenylylcyclase supersensitization in mu-opioid receptor-transfected Chinese hamster ovary cells following chronic opioid treatment. Journal of Biological Chemistry 1995, 270:29732-29738.
5. Bailey C.P., Oldfield S., Llorente J., Caunt C.J., Teschemacher A.G., Roberts L., McArdle C.A., Smith F.L., Dewey W.L., Kelly E., Henderson G. Involvement of PKC alpha and G-protein-coupled receptor kinase 2 in agonist-selective desensitization of mu-opioid receptors in mature brain neurons. British Journal of Pharmacology 2009, 158:157-164.
6. Bailey C.P., Connor M. Opioids: cellular mechanisms of tolerance and physical dependence. Current Opinion in Pharmacology 2005, 5:60-68.
7. Bartlett D.J.R., Tenney S.M. Control of breathing in experimental anemia. Respiration Physiology 1970, 10:384-395.
8. Bernstein M.A., Welch S.P. Mu-opioid receptor down-regulation and cAMP-dependent protein kinase phosphorylation in a mouse model of chronic morphine tolerance. Brain Research. Molecular Brain Research 1998, 55:237-242.
9. Bhargava H.N., Gulati A. Down-regulation of brain and spinal cord mu-opiate receptors in morphine tolerant-dependent rats. European Journal of Pharmacology 1990, 190:305-311.
10. Bilkei-Gorzo A., Berner J., Zimmermann J., Wickström R., Racz I., Zimmer A. Increased morphine analgesia and reduced side effects in mice lacking the tac1 gene. British Journal of Pharmacology 2010, 160:1443-1452.
11. Bohn L.M., Lefkowitz R.J., Gainetdinov R.R., Peppel K., Caron M.G., Lin F.T. Enhanced morphine analgesia in mice lacking beta-arrestin 2. Science 1999, 286:2495-2498.
12. Bohn L.M., Gainetdinov R.R., Lin F.T., Lefkowitz R.J., Caron M.G. Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature 2000, 408:720-723.
13. Bohn L.M., Lefkowitz R.J., Caron M.G. Differential mechanisms of morphine antinociceptive tolerance revealed in (beta)arrestin-2 knock-out mice. Journal of Neuroscience 2002, 22:10494-10500.
14. Bohnert A.S., Valenstein M., Bair M.J., Ganoczy D., McCarthy J.F., Ilgen M.A., Blow F.C. Association between opioid prescribing patterns and opioid overdose-related deaths. Journal of the American Medical Association 2011, 305:1315-1321.
15. -/-. Pediatric Research 2004, 55:738-746.
16. Bronstein A.C., Spyker D.A., Cantilena L.R., Green J.L., Rumack B.H., Dart R.C. Annual report of the American Association of Poison Control Centers' National Poison Data System (NPDS): 28th annual report. Clinical Toxicology (Philadelphia, PA) 2011, 49:910-941.
17. Brown B.L., Albano J.D., Ekins R.P., Sgherzi A.M. A simple and sensitive saturation assay method for the measurement of adenosine 3':5'-cyclic monophosphate. Biochemical Journal 1971, 121:561-562.
18. Cao J.L., Vialou V.F., Lobo M.K., Robison A.J., Neve R.L., Cooper D.C., Nestler E.J., Han M.H. Essential role of the cAMP-cAMP response-element binding protein pathway in opiate-induced homeostatic adaptations of locus coeruleus neurons. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:17011-17016.
19. Chakrabarti S., Gintzler A.R. Phosphorylation of Gbeta is augmented by chronic morphine and enhances Gbetagamma stimulation of adenylyl cyclase activity. Brain Research. Molecular Brain Research 2003, 119:144-151.
20. Chevillard L., Mégarbane B., Risède P., Baud F.J. Characteristics and comparative severity of respiratory response to toxic doses of fentanyl, methadone, morphine, and buprenorphine in rats. Toxicology Letters 2009, 191:327-340.
21. Christie M.J. Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addiction. British Journal of Pharmacology 2008, 154:384-396.
22. Dumas E.O., Pollack G.M. Opioid tolerance development: a pharmacokinetic/pharmacodynamic perspective. AAPS Journal 2008, 10:537-551.
23. Eddy N.B., Leimbach D. Synthetic analgesics. II. Dithienylbutenyl- and dithienylbutylamines. Journal of Pharmacology and Experimental Therapeutics 1953, 107:385-393.
24. Fabian G., Bozo B., Szikszay M., Horvath G., Coscia C.J., Szucs M. Chronic morphine-induced changes in mu-opioid receptors and G proteins of different subcellular loci in rat brain. Journal of Pharmacology and Experimental Therapeutics 2002, 302:774-780.
25. Gabra B.H., Bailey C.P., Kelly E., Smith F.L., Henderson G., Dewey W.L. Pre-treatment with a PKC or PKA inhibitor prevents the development of morphine tolerance but not physical dependence in mice. Brain Research 2008, 1217:70-77.
26. Garzón J., Rodríguez-Muñoz M., Sánchez-Blázquez P. Direct association of mu-opioid and NMDA glutamate receptors supports their cross-regulation: molecular implications for opioid tolerance. Current Drug Abuse Reviews 2012, 5:199-226.
27. Goineau S., Rompion S., Guillaume P., Picard S. Ventilatory function assessment in safety pharmacology: optimization of rodent studies using normocapnic or hypercapnic conditions. Toxicology and Applied Pharmacology 2010, 247:191-197.
28. Gomes T., Mamdani M.M., Dhalla I.A., Paterson J.M., Juurlink D.N. Opioid dose and drug-related mortality in patients with nonmalignant pain. Archives of Internal Medicine 2011, 171:686-691.
29. Greer J.J., Carter J.E. Effects of cyanide on the neural mechanisms controlling breathing in the neonatal rat in vitro. Neurotoxicology 1995, 16:211-215.
30. Hayashida M., Fukunaga A., Hanaoka K. Detection of acute tolerance to the analgesic and nonanalgesic effects of remifentanil infusion in a rabbit model. Anesthesia and Analgesia 2003, 97:1347-1352.
31. Janczewski W.A., Feldman J.L. Distinct rhythm generators for inspiration and expiration in the juvenile rat. Journal of Physiology 2006, 570:407-420.
32. Kamei J., Ohsawa M., Hayashi S.S., Nakanishi Y. Effect of chronic pain on morphine-induced respiratory depression in mice. Neuroscience 2011, 174:224-233.
33. Ladd L.A., Kam P.C., Williams D.B., Wright A.W., Smith M.T., Mather L.E. Ventilatory responses of healthy subjects to intravenous combinations of morphine and oxycodone under imposed hypercapnic and hypoxaemic conditions. British Journal of Clinical Pharmacology 2005, 59:524-535.
34. Law P.Y., Wong Y.H., Loh H.H. Molecular mechanisms and regulation of opioid receptor signaling. Annual Review of Pharmacology and Toxicology 2000, 40:389-430.
35. Lembke A. Why doctors prescribe opioids to known opioid abusers. New England Journal of Medicine 2012, 367:1580-1581.
36. Lin H.Y., Law P.Y., Loh H.H. Activation of PKCα or PKC{epsilon} as an approach to increase morphine tolerance in respiratory depression and lethal overdose. Journal of Pharmacology and Experimental Therapeutics 2012, 341:115-125.
37. Ling G.S., Paul D., Simantov R., Pasternak G.W. Differential development of acute tolerance to analgesia, respiratory depression, gastrointestinal transit and hormone release in a morphine infusion model. Life Sciences 1989, 45:1627-1636.
38. Macintyre P.E. Safety and efficacy of patient-controlled analgesia. British Journal of Anaesthesia 2001, 87:36-46.
39. McGilliard K.L., Takemori A.E. Alterations in the antagonism by naloxone of morphine-induced respiratory depression and analgesia after morphine pretreatment. Journal of Pharmacology and Experimental Therapeutics 1978, 207:884-891.
40. Mercadante S., Bruera E. Opioid switching: a systematic and critical review. Cancer Treatment Reviews 2006, 32:304-315.
41. Millan M.J. Descending control of pain. Progress in Neurobiology 2002, 66:355-474.
42. Noble F., Cox B.M. Differential desensitization of mu- and delta-opioid receptors in selected neural pathways following chronic morphine treatment. British Journal of Pharmacology 1996, 117:161-169.
43. Noble F., Cox B.M. Differential regulation of D1 dopamine receptor- and of A2a adenosine receptor-stimulated adenylyl cyclase by mu-, delta 1-, and delta 2-opioid agonists in rat caudate putamen. Journal of Neurochemistry 1995, 65:125-133.
44. Okie S. A flood of opioids, a rising tide of deaths. New England Journal of Medicine 2010, 363:1981-1985.
45. Paronis C.A., Woods J.H. Ventilation in morphine-maintained rhesus monkeys. II: Tolerance to the antinociceptive but not the ventilatory effects of morphine. Journal of Pharmacology and Experimental Therapeutics 1997, 282:355-362.
46. Paulozzi L.J., Budnitz D.S., Xi Y. Increasing deaths from opioid analgesics in the United States. Pharmacoepidemiology and Drug Safety 2006, 15:618-627.
47. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Elsevier Academic Press, San Diego. 6th ed.
48. Raehal K.M., Walker J.K., Bohn L.M. Morphine side effects in beta-arrestin 2 knockout mice. Journal of Pharmacology and Experimental Therapeutics 2005, 314:1195-1201.
49. Romberg R., Sarton E., Teppema L., Matthes H.W., Kieffer B.L., Dahan A. Comparison of morphine-6-glucuronide and morphine on respiratory depressant and antinociceptive responses in wild type and mu-opioid receptor deficient mice. British Journal of Anaesthesia 2003, 91:862-870.
50. Shimoyama M., Kuwaki T., Nakamura A., Fukuda Y., Shimoyama N., Schiller P.W., Szeto H.H. Differential respiratory effects of [Dmt1]DALDA and morphine in mice. European Journal of Pharmacology 2005, 511:199-206.
51. Shook J.E., Watkins W.D., Camporesi E.M. Differential roles of opioid receptors in respiration, respiratory disease, and opiate-induced respiratory depression. American Review of Respiratory Disease 1990, 142:895-909.
52. Smith F.L., Javed R.R., Smith P.A., Dewey W.L., Gabra B.H. PKC and PKA inhibitors reinstate morphine-induced behaviors in morphine tolerant mice. Pharmacological Research 2006, 54:474-480.
53. Stafford K., Gomes A.B., Shen J., Yoburn B.C. Mu-opioid receptor downregulation contributes to opioid tolerance in vivo. Pharmacology Biochemistry and Behavior 2001, 69:233-237.
54. Stoermer R., Drewe J., Dursteler-Mac Farland K.M., Hock C., Mueller-Spahn F., Ladewig D., Stohler R., Mager R. Safety of injectable opioid maintenance treatment for heroin dependence. Biological Psychiatry 2003, 54:854-861.
55. Takeda S., Eriksson L.I., Yamamoto Y., Joensen H., Onimaru H., Lindahl S.G. Opioid action on respiratory neuron activity of the isolated respiratory network in newborn rats. Anesthesiology 2001, 95:740-749.
56. Tallarida R., Murray R.B. Area under a curve: Simpson's rule and trapezoidal rule. Manual of Pharmacologic Calculations with Computer Programs 1981, 47-49. Springer-Verlag, New York. R. Tallarida, R.B. Murray (Eds.).
57. Teichtahl H., Wang D., Cunnington D., Quinnell T., Tran H., Kronborg I., Drummer O.H. Ventilatory responses to hypoxia and hypercapnia in stable methadone maintenance treatment patients. Chest 2005, 128:1339-1347.
58. van Bockstaele E.J., Commons K.G. Internalization of mu-opioid receptors produced by etorphine in the rat locus coeruleus. Neuroscience 2001, 108:467-477.
59. van den Hoogen R.H., Colpaert F.C. Respiratory effects of morphine in awake unrestrained rats. Journal of Pharmacology and Experimental Therapeutics 1986, 237:252-259.
60. Wang D., Teichtahl H. Opioids, sleep architecture and sleep-disordered breathing. Sleep Medicine Reviews 2007, 11:35-46.
61. Watts V.J., Neve K.A. Sensitization of adenylate cyclase by Galpha i/o-coupled receptors. Pharmacology & Therapeutics 2005, 106:405-421.
62. Webster L.R., Choi Y., Desai H., Webster L., Grant B.J. Sleep-disordered breathing and chronic opioid therapy. Pain Medicine 2008, 9:425-432.
63. White J.M., Irvine R.J. Mechanisms of fatal opioid overdose. Addiction 1999, 94:961-972.
64. Yoburn B.C., Purohit V., Patel K., Zhang Q. Opioid agonist and antagonist treatment differentially regulates immunoreactive mu-opioid receptors and dynamin-2 in vivo. European Journal of Pharmacology 2004, 498:87-96.
65. Zuo Z. The role of opioid receptor internalization and β-arrestins in the development of opioid tolerance. Anesthesia and Analgesia 2005, 101:728-734.