Clinically employed opioid analgesics produce antinociception via μ-δ Opioid receptor heteromers in rhesus monkeys

ACS Chemical Neuroscience

Volumn 3, Issue 9, 2012, Pages 720-727

  Yekkirala, Ajay S ^a,d   Banks, Matthew L ^b   Lunzer, Mary M ^d   Negus, Stevens S ^b   Rice, Kenner C ^c   Portoghese, Philip S ^a,d  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Allosterism; Analgesics; GPCR heteromers; opioid antagonism; primates

Indexed keywords

DELTA OPIATE RECEPTOR; FENTANYL; METHADONE; MORPHINE; MU OPIATE RECEPTOR;

ALLOSTERISM; ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG RECEPTOR BINDING; FEMALE; HUMAN; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY;

ANALGESICS; ANALGESICS, OPIOID; ANIMALS; CALCIUM SIGNALING; DATA INTERPRETATION, STATISTICAL; FEMALE; FENTANYL; HEK293 CELLS; HUMANS; INJECTIONS, SPINAL; MACACA MULATTA; MALE; METHADONE; MICE; NALTREXONE; NARCOTIC ANTAGONISTS; PAIN MEASUREMENT; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, MU;

MACACA MULATTA; MUS; PRIMATES; RODENTIA;

EID: 84866405449     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn300049m     Document Type: Article

References (41)

1. Dubois, M. Y., Gallagher, R. M., and Lippe, P. M. (2009) Pain medicine position paper Pain Med. 10 (6) 972-1000
2. Gutstein, H. B. and Akil, H. (2006) Opioid analgesics, in Goodman & Gilman's The Pharmacological Basis of Therapeutics (Brunton, L. L., Lazo, J. S., and Parker, K. L., Eds.) 11 th ed., pp 547-90, McGraw Hill, New York.
3. Bowen, C. A., Fischer, B. D., Mello, N. K., and Negus, S. S. (2002) Antagonism of the antinociceptive and discriminative stimulus effects of heroin and morphine by 3-methoxynaltrexone and naltrexone in rhesus monkeys J. Pharmacol. Exp. Ther. 302 (1) 264-73 (Pubitemid 34680447)
4. Emmerson, P. J., Liu, M. R., Woods, J. H., and Medzihradsky, F. (1994) Binding affinity and selectivity of opioids at mu, delta and kappa receptors in monkey brain membranes J. Pharmacol. Exp. Ther. 271 (3) 1630-7 (Pubitemid 24382680)
5. Emmerson, P. J., Clark, M. J., Mansour, A., Akil, H., Woods, J. H., and Medzihradsky, F. (1996) Characterization of opioid agonist efficacy in a C6 glioma cell line expressing the mu opioid receptor J. Pharmacol. Exp. Ther. 278 (3) 1121-7 (Pubitemid 27166961)
6. Negus, S. S., Burke, T. F., Medzihradsky, F., and Woods, J. H. (1993) Effects of opioid agonists selective for mu, kappa and delta opioid receptors on schedule-controlled responding in rhesus monkeys: antagonism by quadazocine J. Pharmacol. Exp. Ther. 267 (2) 896-903 (Pubitemid 23352553)
7. Matthes, H. W., Maldonado, R., Simonin, F., Valverde, O., Slowe, S., Kitchen, I., Befort, K., Dierich, A., Le Meur, M., Dolle, P., Tzavara, E., Hanoune, J., Roques, B. P., and Kieffer, B. L. (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene Nature 383 (6603) 819-23
8. Evans, C. J., Keith, D. E., Jr., Morrison, H., Magendzo, K., and Edwards, R. H. (1992) Cloning of a delta opioid receptor by functional expression Science (New York, N.Y.) 258 (5090) 1952-5
9. Kieffer, B. L., Befort, K., Gaveriaux-Ruff, C., and Hirth, C. G. (1992) The delta-opioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization Proc. Natl. Acad. Sci. U.S.A. 89 (24) 12048-52 (Pubitemid 23004782)
10. Meng, F., Xie, G. X., Thompson, R. C., Mansour, A., Goldstein, A., Watson, S. J., and Akil, H. (1993) Cloning and pharmacological characterization of a rat kappa opioid receptor Proc. Natl. Acad. Sci. U.S.A. 90 (21) 9954-8 (Pubitemid 23328229)
11. Thompson, R. C., Mansour, A., Akil, H., and Watson, S. J. (1993) Cloning and pharmacological characterization of a rat mu opioid receptor Neuron 11 (5) 903-13 (Pubitemid 23347475)
12. Stevenson, G. W., Folk, J. E., Linsenmayer, D. C., Rice, K. C., and Negus, S. S. (2003) Opioid interactions in rhesus monkeys: effects of delta + mu and delta + kappa agonists on schedule-controlled responding and thermal nociception J. Pharmacol. Exp. Ther. 307 (3) 1054-64 (Pubitemid 37494225)
13. Kieffer, B. L. (1995) Recent advances in molecular recognition and signal transduction of active peptides: receptors for opioid peptides Cell Mol. Neurobiol. 15 (6) 615-35 (Pubitemid 26019815)
14. Mansour, A., Fox, C. A., Akil, H., and Watson, S. J. (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications Trends Neurosci. 18 (1) 22-9
15. Jordan, B. A., Cvejic, S., and Devi, L. A. (2000) Opioids and their complicated receptor complexes Neuropsychopharmacology 23 (4) S5-S18
16. Wang, D., Sun, X., Bohn, L. M., and Sadee, W. (2005) Opioid receptor homo- and heterodimerization in living cells by quantitative bioluminescence resonance energy transfer Mol. Pharmacol. 67 (6) 2173-84 (Pubitemid 41007796)
17. Jordan, B. A. and Devi, L. A. (1999) G-protein-coupled receptor heterodimerization modulates receptor function Nature 399 (6737) 697-700 (Pubitemid 29289066)
18. George, S. R., Fan, T., Xie, Z., Tse, R., Tam, V., Varghese, G., and ODowd, B. F. (2000) Oligomerization of mu- and delta-opioid receptors. Generation of novel functional properties J. Biol. Chem. 275 (34) 26128-35
19. Sanchez-Blazquez, P., Garcia-Espana, A., and Garzon, J. (1997) Antisense oligodeoxynucleotides to opioid mu and delta receptors reduced morphine dependence in mice: role of delta-2 opioid receptors J. Pharmacol. Exp. Ther. 280 (3) 1423-31 (Pubitemid 27166741)
20. Nitsche, J. F., Schuller, A. G., King, M. A., Zengh, M., Pasternak, G. W., and Pintar, J. E. (2002) Genetic dissociation of opiate tolerance and physical dependence in delta-opioid receptor-1 and preproenkephalin knock-out mice J. Neurosci. 22 (24) 10906-13 (Pubitemid 36005166)
21. Abdelhamid, E. E., Sultana, M., Portoghese, P. S., and Takemori, A. E. (1991) Selective blockage of delta opioid receptors prevents the development of morphine tolerance and dependence in mice J. Pharmacol. Exp. Ther. 258 (1) 299-303
22. Daniels, D. J., Lenard, N. R., Etienne, C. L., Law, P. Y., Roerig, S. C., and Portoghese, P. S. (2005) Opioid-induced tolerance and dependence in mice is modulated by the distance between pharmacophores in a bivalent ligand series Proc. Natl. Acad. Sci. U.S.A. 102 (52) 19208-13 (Pubitemid 43049591)
23. Lenard, N. R., Daniels, D. J., Portoghese, P. S., and Roerig, S. C. (2007) Absence of conditioned place preference or reinstatement with bivalent ligands containing mu-opioid receptor agonist and delta-opioid receptor antagonist pharmacophores Eur. J. Pharmacol. 566 (1-3) 75-82 (Pubitemid 46782790)
24. Scherrer, G., Imamachi, N., Cao, Y. Q., Contet, C., Mennicken, F., ODonnell, D., Kieffer, B. L., and Basbaum, A. I. (2009) Dissociation of the opioid receptor mechanisms that control mechanical and heat pain Cell 137 (6) 1148-59
25. Wang, H. B., Zhao, B., Zhong, Y. Q., Li, K. C., Li, Z. Y., Wang, Q., Lu, Y. J., Zhang, Z. N., He, S. Q., Zheng, H. C., Wu, S. X., Hokfelt, T. G., Bao, L., and Zhang, X. (2010) Coexpression of delta- and mu-opioid receptors in nociceptive sensory neurons Proc. Natl. Acad. Sci. U.S.A. 107 (29) 13117-22
26. Gupta, A., Mulder, J., Gomes, I., Rozenfeld, R., Bushlin, I., Ong, E., Lim, M., Maillet, E., Junek, M., Cahill, C. M., Harkany, T., and Devi, L. A. (2010) Increased abundance of opioid receptor heteromers after chronic morphine administration Sci. Signaling 3 (131) ra54
27. Hasbi, A., Nguyen, T., Fan, T., Cheng, R., Rashid, A., Alijaniaram, M., Rasenick, M. M., ODowd, B. F., and George, S. R. (2007) Trafficking of preassembled opioid mu-delta heterooligomer-Gz signaling complexes to the plasma membrane: coregulation by agonists Biochemistry 46 (45) 12997-3009 (Pubitemid 350086219)
28. Yekkirala, A. S., Kalyuzhny, A. E., and Portoghese, P. S. (2010) Standard opioid agonists activate heteromeric opioid receptors: evidence for morphine and [D-Ala2-MePhe4-Glyol5]enkephalin as selective μ-Δ agonists ACS Chem. Neurosci. 1 (1) 146-54
29. Portoghese, P. S., Sultana, M., and Takemori, A. E. (1988) Naltrindole, a highly selective and potent non-peptide delta opioid receptor antagonist Eur. J. Pharmacol. 146 (1) 185-6 (Pubitemid 18030440)
30. Yekkirala, A. S., Lunzer, M. M., McCurdy, C. R., Powers, M. D., Kalyuzhny, A. E., Roerig, S. C., and Portoghese, P. S. (2011) N-naphthoyl-beta-naltrexamine (NNTA), a highly selective and potent activator of mu/kappa-opioid heteromers Proc. Natl. Acad. Sci. U.S.A. 108 (12) 5098-103
31. Waldhoer, M., Fong, J., Jones, R. M., Lunzer, M. M., Sharma, S. K., Kostenis, E., Portoghese, P. S., and Whistler, J. L. (2005) A heterodimer-selective agonist shows in vivo relevance of G protein-coupled receptor dimers Proc. Natl. Acad. Sci. U.S.A. 102 (25) 9050-5 (Pubitemid 40881076)
32. van Rijn, R. M. and Whistler, J. L. (2009) The δ1 Opioid Receptor Is a Heterodimer That Opposes the Actions of the δ2 Receptor on Alcohol Intake Biol. Psychiatry 66 (8) 777-84
33. Negus, S. S., Butelman, E. R., Chang, K. J., DeCosta, B., Winger, G., and Woods, J. H. (1994) Behavioral effects of the systemically active delta opioid agonist BW373U86 in rhesus monkeys J. Pharmacol. Exp. Ther. 270 (3) 1025-34 (Pubitemid 24315216)
34. Negus, S. S., Gatch, M. B., Mello, N. K., Zhang, X., and Rice, K. (1998) Behavioral effects of the delta-selective opioid agonist SNC80 and related compounds in rhesus monkeys J. Pharmacol. Exp. Ther. 286 (1) 362-75 (Pubitemid 28318012)
35. Brandt, M. R., Negus, S. S., Mello, N. K., Furness, M. S., Zhang, X., and Rice, K. C. (1999) Discriminative stimulus effects of the nonpeptidic delta-opioid agonist SNC80 in rhesus monkeys J. Pharmacol. Exp. Ther. 290 (3) 1157-64 (Pubitemid 29400256)
36. Brandt, M. R., Furness, M. S., Mello, N. K., Rice, K. C., and Negus, S. S. (2001) Antinociceptive effects of delta-opioid agonists in Rhesus monkeys: effects on chemically induced thermal hypersensitivity J. Pharmacol. Exp. Ther. 296 (3) 939-46 (Pubitemid 32187368)
37. Dewey, W. L., Harris, L. S., Howes, J. F., and Nuite, J. A. (1970) The effect of various neurohumoral modulators on the activity of morphine and the narcotic antagonists in the tail-flick and phenylquinone tests J. Pharmacol. Exp. Ther. 175 (2) 435-42
38. Hylden, J. L. and Wilcox, G. L. (1981) Intrathecal substance P elicits a caudally-directed biting and scratching behavior in mice Brain Res. 217 (1) 212-5 (Pubitemid 11072722)
39. Haley, T. J. and McCormick, W. G. (1957) Pharmacological effects produced by intracerebral injection of drugs in the conscious mouse Br. J. Pharmacol. Chemother. 12 (1) 12-5
40. Harris, L. S. and Pierson, A. K. (1964) Some Narcotic Antagonists in the Benzomorphan Series J. Pharmacol. Exp. Ther. 143, 141-8
41. Kostenis, E. (2001) Is Galpha16 the optimal tool for fishing ligands of orphan G-protein-coupled receptors? Trends Pharmacol. Sci. 22 (11) 560-564 (Pubitemid 33042645)