Morphine-Induced Receptor Endocytosis in a Novel Knockin Mouse Reduces Tolerance and Dependence

Current Biology

Volumn 18, Issue 2, 2008, Pages 129-135

  Kim, Joseph A ^a   Bartlett, Selena ^a   He, Li ^a   Nielsen, Carsten K ^a   Chang, Amy M ^a   Kharazia, Viktor ^a   Waldhoer, Maria ^a   Ou, Chrissi J ^a   Taylor, Stacy ^a   Ferwerda, Madeline ^a   Cado, Dragana ^c   Whistler, Jennifer L ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

MOLNEURO

Indexed keywords

MORPHINE; MU OPIATE RECEPTOR;

ANIMAL; ARTICLE; DRUG EFFECT; DRUG TOLERANCE; ENDOCYTOSIS; METABOLISM; MORPHINE ADDICTION; MOUSE; TRANSGENIC MOUSE; WITHDRAWAL SYNDROME;

ANIMALS; DRUG TOLERANCE; ENDOCYTOSIS; MICE; MICE, TRANSGENIC; MORPHINE; MORPHINE DEPENDENCE; RECEPTORS, OPIOID, MU; SUBSTANCE WITHDRAWAL SYNDROME;

MUS;

EID: 38349074858     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2007.12.057     Document Type: Article

References (33)

1. Matthes H.W., Maldonado R., Simonin F., Valverde O., Slowe S., Kitchen I., Befort K., Dierich A., Le Meur M., Dolle P., et al. Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383 (1996) 819-823
2. Arden J.R., Segredo V., Wang Z., Lameh J., and Sadee W. Phosphorylation and agonist-specific intracellular trafficking of an epitope-tagged mu-opioid receptor expressed in HEK 293 cells. J. Neurochem. 65 (1995) 1636-1645
3. Keith D.E., Murray S.R., Zaki P.A., Chu P.C., Lissin D.V., Kang L., Evans C.J., and von Zastrow M. Morphine activates opioid receptors without causing their rapid internalization. J. Biol. Chem. 271 (1996) 19021-19024
4. Koch T., Schulz S., Pfeiffer M., Klutzny M., Schroder H., Kahl E., and Hollt V. C-terminal splice variants of the mouse mu-opioid receptor differ in morphine-induced internalization and receptor resensitization. J. Biol. Chem. 276 (2001) 31408-31414
5. Yu Y., Zhang L., Yin X., Sun H., Uhl G.R., and Wang J.B. Mu opioid receptor phosphorylation, desensitization, and ligand efficacy. J. Biol. Chem. 272 (1997) 28869-28874
6. Sternini C., Spann M., Anton B., Keith D.J., Bunnett N.W., von Zastrow M., Evans C., and Brecha N.C. Agonist-selective endocytosis of mu opioid receptor by neurons in vivo. Proc. Natl. Acad. Sci. USA 93 (1996) 9241-9246
7. Keith D.E., Anton B., Murray S.R., Zaki P.A., Chu P.C., Lissin D.V., Monteillet-Agius G., Stewart P.L., Evans C.J., and von Zastrow M. mu-Opioid receptor internalization: opiate drugs have differential effects on a conserved endocytic mechanism in vitro and in the mammalian brain. Mol. Pharmacol. 53 (1998) 377-384
8. Trafton J.A., Abbadie C., Marek K., and Basbaum A.I. Postsynaptic signaling via the [mu]-opioid receptor: responses of dorsal horn neurons to exogenous opioids and noxious stimulation. J. Neurosci. 20 (2000) 8578-8584
9. He L., Fong J., von Zastrow M., and Whistler J.L. Regulation of opioid receptor trafficking and morphine tolerance by receptor oligomerization. Cell 108 (2002) 271-282
10. He L., and Whistler J.L. An opiate cocktail that reduces morphine tolerance and dependence. Curr. Biol. 15 (2005) 1028-1033
11. Abbadie C., and Pasternak G.W. Differential in vivo internalization of MOR-1 and MOR-1C by morphine. Neuroreport 12 (2001) 3069-3072
12. Finn A.K., and Whistler J.L. Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32 (2001) 829-839
13. Fairbanks C.A., and Wilcox G.L. Spinal antinociceptive synergism between morphine and clonidine persists in mice made acutely or chronically tolerant to morphine. J. Pharmacol. Exp. Ther. 288 (1999) 1107-1116
14. Kest B., Palmese C.A., Hopkins E., Adler M., Juni A., and Mogil J.S. Naloxone-precipitated withdrawal jumping in 11 inbred mouse strains: evidence for common genetic mechanisms in acute and chronic morphine physical dependence. Neuroscience 115 (2002) 463-469
15. Alvarez V.A., Arttamangkul S., Dang V., Salem A., Whistler J.L., Von Zastrow M., Grandy D.K., and Williams J.T. mu-Opioid receptors: Ligand-dependent activation of potassium conductance, desensitization, and internalization. J. Neurosci. 22 (2002) 5769-5776
16. Blanchet C., Sollini M., and Luscher C. Two distinct forms of desensitization of G-protein coupled inwardly rectifying potassium currents evoked by alkaloid and peptide mu-opioid receptor agonists. Mol. Cell. Neurosci. 24 (2003) 517-523
17. Kovoor A., Celver J.P., Wu A., and Chavkin C. Agonist induced homologous desensitization of mu-opioid receptors mediated by G protein-coupled receptor kinases is dependent on agonist efficacy. Mol. Pharmacol. 54 (1998) 704-711
18. Connor M., Borgland S.L., and Christie M.J. Continued morphine modulation of calcium channel currents in acutely isolated locus coeruleus neurons from morphine-dependent rats. Br. J. Pharmacol. 128 (1999) 1561-1569
19. Ingram S.L., Vaughan C.W., Bagley E.E., Connor M., and Christie M.J. Enhanced opioid efficacy in opioid dependence is caused by an altered signal transduction pathway. J. Neurosci. 18 (1998) 10269-10276
20. Bagley E.E., Chieng B.C., Christie M.J., and Connor M. Opioid tolerance in periaqueductal gray neurons isolated from mice chronically treated with morphine. Br. J. Pharmacol. 146 (2005) 68-76
21. Bohn L.M., Lefkowitz R.J., Gainetdinov R.R., Peppel K., Caron M.G., and Lin F.T. Enhanced morphine analgesia in mice lacking beta-arrestin 2. Science 286 (1999) 2495-2498
22. Narita M., Mizoguchi H., Nagase H., Suzuki T., and Tseng L.F. Involvement of spinal protein kinase Cgamma in the attenuation of opioid mu-receptor-mediated G-protein activation after chronic intrathecal administration of [D-Ala2,N-MePhe4,Gly-Ol(5)]enkephalin. J. Neurosci. 21 (2001) 3715-3720
23. Bohn L.M., Lefkowitz R.J., and Caron M.G. Differential mechanisms of morphine antinociceptive tolerance revealed in (beta)arrestin-2 knock-out mice. J. Neurosci. 22 (2002) 10494-10500
24. Selley D.E., Nestler E.J., Breivogel C.S., and Childers S.R. Opioid receptor-coupled G-proteins in rat locus coeruleus membranes: decrease in activity after chronic morphine treatment. Brain Res. 746 (1997) 10-18
25. Bailey C.P., Kelly E., and Henderson G. Protein kinase C activation enhances morphine-induced rapid desensitization of mu-opioid receptors in mature rat locus ceruleus neurons. Mol. Pharmacol. 66 (2004) 1592-1598
26. Bushell T., Endoh T., Simen A.A., Ren D., Bindokas V.P., and Miller R.J. Molecular components of tolerance to opiates in single hippocampal neurons. Mol. Pharmacol. 61 (2002) 55-64
27. Borgland S.L., Connor M., Osborne P.B., Furness J.B., and Christie M.J. Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of mu-opioid receptors. J. Biol. Chem. 278 (2003) 18776-18784
28. Bohn L.M., Gainetdinov R.R., Lin F.T., Lefkowitz R.J., and Caron M.G. Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature 408 (2000) 720-723
29. Grecksch G., Bartzsch K., Widera A., Becker A., Hollt V., and Koch T. Development of tolerance and sensitization to different opioid agonists in rats. Psychopharmacology (Berl.) 186 (2006) 177-184
30. Duttaroy A., and Yoburn B.C. The effect of intrinsic efficacy on opioid tolerance. Anesthesiology 82 (1995) 1226-1236
31. Walker E.A., and Young A.M. Differential tolerance to antinociceptive effects of mu opioids during repeated treatment with etonitazene, morphine, or buprenorphine in rats. Psychopharmacology (Berl.) 154 (2001) 131-142
32. Patel M.B., Patel C.N., Rajashekara V., and Yoburn B.C. Opioid agonists differentially regulate mu-opioid receptors and trafficking proteins in vivo. Mol. Pharmacol. 62 (2002) 1464-1470
33. Narita M., Suzuki M., Niikura K., Nakamura A., Miyatake M., Yajima Y., and Suzuki T. mu-Opioid receptor internalization-dependent and -independent mechanisms of the development of tolerance to mu-opioid receptor agonists: Comparison between etorphine and morphine. Neuroscience 138 (2006) 609-619