Opiate antagonist prevents μ- and δ-opiate receptor dimerization to facilitate ability of agonist to control ethanol-altered natural killer cell functions and mammary tumor growth

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16734-16747

  Sarkar, Dipak K ^a   Sengupta, Amitabha ^a   Zhang, Changqing ^a   Boyadjieva, Nadka ^a   Murugan, Sengottuvelan ^a  

^a The State University of New Jersey   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FUNCTIONS; CELLULAR LEVELS; CHRONIC TREATMENT; COMBINED TREATMENT; CYTOTOXIC; ETHANOL TREATMENT; FEEDBACK INTERACTION; HETERODIMERIZATION; HETERODIMERS; HOMODIMERIZATION; HOMODIMERS; IMMUNE CELLS; IN-VIVO; LIGAND BINDING; MAMMARY TUMORS; NATURAL KILLER CELLS; NK CELLS; OPIATE RECEPTORS; OPIOID RECEPTORS; PROTEIN LEVEL; RECEPTOR ANTAGONISTS; RECEPTOR BINDING; RECEPTOR GENES;

CELL CULTURE; DIMERIZATION; DIMERS; DISEASE CONTROL; DISEASES; ETHANOL; GENES; MONOMERS; TUMORS;

CELLS;

ALCOHOL; CYTOTOXIC FACTOR; DELTA OPIATE RECEPTOR; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; HOMODIMER; LIGAND; MONOMER; MU OPIATE RECEPTOR; NALTREXONE; NALTRINDOLE; OPIATE ANTAGONIST; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ARTICLE; BREAST TUMOR; CELL FUNCTION; CONTROLLED STUDY; DIMERIZATION; IMMUNOCOMPETENT CELL; IMMUNOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; MALE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; RECEPTOR GENE; TUMOR GROWTH;

ANIMALS; CELL LINE, TUMOR; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; FEMALE; KILLER CELLS, NATURAL; LIGANDS; MALE; MAMMARY NEOPLASMS, ANIMAL; PROTEIN MULTIMERIZATION; RATS; RATS, INBRED F344; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, MU;

RATTUS;

EID: 84860843928     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.347583     Document Type: Article

References (39)

1. Mandler, R. N., Biddison, W. E., Mandler R., and Serrate, S. A. (1986) β-Endorphin augments the cytolytic activity and interferon production of natural killer cells. J. Immunol. 136, 934-939 (Pubitemid 16146379)
2. Pruett, S. B., Han, Y. C., and Wu, W. J. (1994) A brief review of immunomodulation caused by acute administration of ethanol. Involvement of neuroendocrine pathways. Alcohol Alcohol. Suppl. 2, 431-437
3. Boyadjieva, N., Dokur, M., Advis, J. P., Meadows, G. G., and Sarkar, D. K. (2001) Chronic ethanol inhibits NK cell cytolytic activity. Role of opioid peptide β-endorphin. J. Immunol. 167, 5645-5652 (Pubitemid 33062754)
4. Boyadjieva, N., Advis, J. P., and Sarkar, D. K. (2006) Role of β-endorphin, corticotropin-releasing hormone, and autonomic nervous system in mediation of the effect of chronic ethanol on natural killer cell cytolytic activity. Alcohol Clin. Exp. Res. 30, 1761-1767 (Pubitemid 44465615)
5. Dokur, M., Chen, C. P., Advis, J. P., and Sarkar, D. K. (2005) β-Endorphin modulation of interferon-γ, perforin, and granzyme B levels in splenic NK cells. Effects of ethanol. J. Neuroimmunol. 166, 29-38 (Pubitemid 41074654)
6. Dokur, M., Boyadjieva, N. I., Advis, J. P., and Sarkar, D. K. (2004) Modulation of hypothalamic β-endorphin-regulated expression of natural killer cell cytolytic activity regulatory factors by ethanol in male Fischer-344 rats. Alcohol Clin. Exp. Res. 28, 1180-1186 (Pubitemid 39108615)
7. Brownstein, M. J. (1993) A brief history of opiates, opioid peptides, and opioid receptors. Proc. Natl. Acad. Sci. U.S.A. 90, 5391-5393
8. Shahabi, N. A., McAllen, K., Matta, S. G., and Sharp, B. M. (2000) Expression of δ-opioid receptors by splenocytes from SEB-treated mice and effects on phosphorylation of MAP kinase. Cell. Immunol. 205, 84-93 (Pubitemid 32005724)
9. Boyadjieva, N. I., Chaturvedi, K., Poplawski, M. M., and Sarkar, D. K. (2004) Opioid antagonist naltrexone disrupts feedback interaction between μ- and δ-opioid receptors in splenocytes to prevent alcohol inhibition of NK cell function. J. Immunol. 173, 42-49 (Pubitemid 38797324)
10. 3H]DAMGO binding in discrete regions of the rat brain. Neuropeptides 44, 9-16
11. Sarkar, D. K., Kuhn, P., Marano, J., Chen, C., and Boyadjieva, N. (2007) Alcohol exposure during the developmental period induces β-endorphin neuronal death and causes alteration in the opioid control of stress axis function. Endocrinology 148, 2828-2834 (Pubitemid 46984784)
12. Rasmussen, D. D., Boldt, B. M., Wilkinson, C. W., and Mitton, D. R. (2002) Chronic daily ethanol and withdrawal. 3. Forebrain pro-opiomelanocortin gene expression and implications for dependence, relapse, and deprivation effect. Alcohol Clin. Exp. Res. 26, 535-546 (Pubitemid 34408720)
13. Saland, L. C., Chavez, J. B., Lee, D. C., Garcia, R. R., and Caldwell, K. K. (2008) Chronic ethanol exposure increases the association of hippocampal μ-opioid receptors with G-protein receptor kinase 2. Alcohol 42, 493-497
14. Law, P. Y., Wong, Y. H., and Loh, H. H. (2000) Molecular mechanisms and regulation of opioid receptor signaling. Annu. Rev. Pharmacol. Toxicol. 40, 389-430 (Pubitemid 30340688)
15. Merkouris, M., Mullaney, I., Georgoussi, Z., and Milligan, G. (1997) Regulation of spontaneous activity of the δ-opioid receptor. Studies of inverse agonism in intact cells. J. Neurochem. 69, 2115-2122 (Pubitemid 27452759)
16. Burford, N. T., Wang, D., and Sadée, W. (2000) G-protein coupling of μ-opioid receptors (OP3). Elevated basal signaling activity. Biochem. J. 348, 531-537 (Pubitemid 30410241)
17. George, S. R., Fan, T., Xie, Z., Tse, R., Tam, V., Varghese, G., and O'Dowd, B. F. (2000) Oligomerization of μ- and δ-opioid receptors. Generation of novel functional properties. J. Biol. Chem. 275, 26128-26135
18. Gomes, I., Filipovska, J., Jordan, B. A., and Devi, L. A. (2002) Oligomerization of opioid receptors. Methods 27, 358-365
19. Bidlack, J. M., Khimich, M., Parkhill, A. L., Sumagin, S., Sun, B., and Tipton C. M. (2006) Opioid receptors and signaling on cells from the immune system. J. Neuroimmune. Pharmacol. 1, 260-269 (Pubitemid 44244131)
20. De, A., Boyadjieva, N., Oomizu, S., Sarkar, D. K. (2002) Ethanol induces hyperprolactinemia by increasing prolactin release and lactotrope growth in female rats. Alcohol. Clin. Exp. Res. 26, 1420-1429
21. Sharp, B. M. (2006) Multiple opioid receptors on immune cells modulate intracellular signaling. Brain Behav. Immun. 20, 9-14
22. Brogden, K. A., Guthmiller, J. M., Salzet, M., and Zasloff, M. (2005) The nervous system and innate immunity. The neuropeptide connection. Nat. Immunol. 6, 558-564 (Pubitemid 41710725)
23. Sharp, B. M. (2003) Opioid receptor expression and intracellular signaling by cells involved in host defense and immunity. Adv. Exp. Med. Biol. 521, 98-105
24. Ueda, H., and Ueda, M. (2009) Mechanisms underlying morphine analgesic tolerance and dependence. Front. Biosci. 14, 5260-52672
25. Prather, P. L., Tsai, A. W., and Law, P. Y. (1994) μ- and δ-opioid receptor desensitization in undifferentiated human neuroblastoma SHSY5Y cells. J. Pharmacol. Exp. Ther. 270, 177-184
26. Christie, M. J. (2008) Cellular neuroadaptations to chronic opioids. Tolerance, withdrawal, and addiction. Br. J. Pharmacol. 154, 384-396
27. Kovoor, A., Nappey, V., Kieffer, B. L., and Chavkin, C. (1997) μ- and δ-opioid receptors are differentially desensitized by the coexpression of β-adrenergic receptor kinase 2 and β-arrestin 2 in Xenopus oocytes. J. Biol. Chem. 272, 27605-27611
28. Chakrabarti, S., Yang, W., Law, P. Y., and Loh, H. H. (1997) The μ-opioid receptor down-regulates differently from the δ-opioid receptor. Requirement of a high affinity receptor/G protein complex formation. Mol. Pharmacol. 52, 105-113 (Pubitemid 27318625)
29. Keith, D. E., Murray, S. R., Zaki, P. A., Chu, P. C., Lissin, D. V., Kang, L., Evans, C. J., and von Zastrow, M. (1996) Morphine activates opioid receptors without causing their rapid internalization. J. Biol. Chem. 271, 19021-19024 (Pubitemid 26271556)
30. Wang, Z. J., and Wang, L. X. (2006) Phosphorylation: a molecular switch in opioid tolerance. Life Sci. 79, 1681-1691 (Pubitemid 44374547)
31. Sharma, S. K., Klee, W. A., and Nirenberg, M. (1975) Dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance. Proc. Natl. Acad. Sci. U.S.A. 72, 3092-3096
32. Liu, J. G., and Prather, P. L. (2002) Chronic agonist treatment converts antagonists into inverse agonists at δ-opioid receptors. J. Pharmacol. Exp. Ther. 302, 1070-1079
33. Law, P. Y., Erickson-Herbrandson, L. J., Zha, Q. Q., Solberg, J., Chu, J., Sarre, A., and Loh, H. H. (2005) Heterodimerization of μ- and δ-opioid receptors occurs at the cell surface only and requires receptor-G protein interactions. J. Biol. Chem. 280, 11152-11164 (Pubitemid 40418422)
34. Balenga, N. A., Henstridge, C. M., Kargl, J., and Waldhoer, M. (2011) Pharmacology, signaling, and physiological relevance of the G protein-coupled receptor 55. Adv. Pharmacol. 62, 251-277
35. van Rijn, R. M., Whistler, J. L., and Waldhoer, M. (2010) Opioid-receptor-heteromer-specific trafficking and pharmacology. Curr. Opin. Pharmacol. 10, 73-79
36. Rozenfeld, R., Abul-Husn, N. S., Gomez, I., and Devi, L. A. (2007) An emerging role for the δ-opioid receptor in the regulation of μ-opioid receptor function. Scientific World J. 7, 64-73 (Pubitemid 350292609)
37. Wang, D., Sun, X., Bohn, L. M., and Sadée, W. (2005) Opioid receptor homo- and heterodimerization in living cells by quantitative bioluminescence resonance energy transfer. Mol. Pharmacol. 67, 2173-2184 (Pubitemid 41007796)
38. 35S]guanosine-5′-O-(3-thio) triphosphate in the fawn-hooded rat brain. A quantitative autoradiography study. J. Pharmacol. Exp. Ther. 293, 159-165
39. Stefano, G. B., Kream, R. M., and Esch, T. (2009) Revisiting tolerance from the endogenous morphine perspective. Med. Sci. Monit. 15, RA189-RA198