The relevance of opioids and opioid receptors on immunocompetence and immune homeostasis

Proceedings of the Society for Experimental Biology and Medicine

Volumn 213, Issue 3, 1996, Pages 248-257

  Carr, Daniel J J ^a   Rogers, Thomas J ^b   Weber, Richard J ^c  

^a LOUISIANA STATE UNIV MEDICAL CENTER   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OPIATE DERIVATIVE; OPIATE RECEPTOR;

ADRENERGIC SYSTEM; AMINO ACID SEQUENCE; DNA SEQUENCE; HOMEOSTASIS; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOCOMPETENCE; LEUKOCYTE; NONHUMAN; REVIEW;

BACTERIA (MICROORGANISMS);

EID: 0030449599     PISSN: 00379727     EISSN: None     Source Type: Journal    
DOI: 10.3181/00379727-213-44056     Document Type: Review

References (97)

1. Wybran J, Appelboom T, Famaey J-P, Govaerts A. Suggestive evidence for receptors for morphine and methionine-enkephalin on normal human blood T lymphocytes. J Immunol 123:1068-1070, 1979.
2. Rojavin M, Szabo I, Bussiere JL, Rogers TJ, Adler MW, Eisenstein TK. Morphine treatment in vitro or in vivo decreases phagocytic functions of murine macrophages. Life Sci 53:997-1006, 1993.
3. Szabo I, Rojavin M, Bussiere JL, Eisenstein TK, Adler MW, Rogers TJ. Suppression of peritoneal macrophage phagocytosis of Candida albicans by opioids. J Pharmacol Exp Ther 267:703-706, 1900.
4. Liu Y, Blackbourn DJ, Chuang LF, Killam KF Jr., Chuang RY. Effects of in vivo and in vitro administration of morphine sulfate upon rhesus macaque polymorphonuclear cell phagocytosis and chemotaxis. J Pharmacol Exp Ther 263:533-539, 1992.
5. Makman MH, Bilfinger TV, Stefano GB. Human granulocytes contain an opiate alkaloid-selective receptor mediating inhibition of cytokine-induced activation and chemotaxis. J Immunol 154:1323-1330, 1995.
6. Hagi K, Uno K, Inaba K, Muramatsu S. Augmenting effect of opioid peptides on murine macrophage activation. J Neuroimmunol 50:71-76, 1994.
7. Taub DD, Eisenstein TK, Geller EB, Adler MW, Rogers TJ. Immunomodulatory activity of μ- and κ-selected opioid agonists. Proc Natl Acad Sci USA 88:360-364, 1991.
8. Guan L, Townsend R, Eisenstein TK, Adler MW, Rogers TJ. Both T cells and macrophages are targets of κ-opioid-induced immunosuppression. Brain Behav Immun 8:229-240, 1994.
9. Jankovic BD, Radulovic J. Quaternary naltrexone: Its immunomodulatory activity and interaction with brain delta and kappa opioid receptors. Immunopharmacology 28:105-112, 1994.
10. Radulovic J, Miljevic C, Djergovic D, Vujic V, Antic J, von Horsten S, Jankovic BD. Opioid receptor-mediated suppression of humoral immune response in vivo and in vitro: Involvement of κ opioid receptors. J Neuroimmunol 57:55-62, 1995.
11. Brown DR, Goldberg LI. The use of quaternary narcotic antagonists in opiate research. Neuropharmacology 24:181-191, 1985.
12. Chao CC, Hu S, Molitor TW, Zhou Y, Murtaugh MP, Tsang M, Peterson PK. Morphine potentiates transforming growth factor-β release from human peripheral blood mononuclear cell cultures. J Pharmacol Exp Ther 262:19-24, 1992.
13. Bussiere JL, Adler MW, Rogers TJ, Eisenstein TK. Cytokine reversal of morphine-induced suppression of the antibody response. J Pharmacol Exp Ther 264:591-597, 1993.
14. Chao CC, Molitor TW, Close K, Hu S, Peterson PK. Morphine inhibits the release of tumor necrosis factor in human peripheral blood mononuclear cell cultures. Int J Immunopharmacol 15:447-453, 1993.
15. Belkowski SM, Alicea C, Eisenstein TK, Adler MW, Rogers TJ. Inhibition of interleukin-1 and tumor necrosis factor-α synthesis following treatment of macrophages with the kappa opioid agonist U50,488H. J Pharmacol Exp Ther 273:1491-1496, 1995.
16. Weber RJ, Pert A, Rice KC, Hagan AA. Opioid receptor-mediated suppression of T-dependent antibody production in vivo. Brain Behav Immun (in press).
17. Dinari G, Ashkenazi S, Marcus H, Rosenbach Y, Zahaui I. The effect of opiates on the intestinal immune response to cholera toxin in mice. Digestion 44:14, 1989.
18. Jessop DS, Lightman SL, Chowdrey HS. Effects of a chronic inflammatory stress on levels of pro-opiomelanocortin-derived peptides in the rat spleen and thymus. J Neuroimmunol 49:197-203, 1994.
19. Jessop DS, Renshaw D, Lightman SL, Harbuz MS. Changes in ACTH and β-endorphin immunoreactivity in immune tissues during a chronic inflammatory stress are not correlated with changes in corticotropin-releasing hormone and arginine vasopressin. J Neuroimmunol 60:29-35, 1995.
20. Przewlocki R, Hassan HS, Lason W, Epplen C, Herz A, Stein C. Gene expression and localization of opioid peptides in immune cells of inflamed tissue: Functional role in antinociception. Neuroscience 48:491-500, 1992.
21. Cepeda MS, Lipkowski AW, Langlade A, Osgood PF, Ehrlich HP, Hargreaves K, Szyfelbein SK, Carr DB. Local increases of subcutaneous β-endorphin immunoreactivity at the site of thermal injury. Immunopharmacology 25:205-213, 1993.
22. Panerai AE, Radulovic J, Monastra G, Manfredi B, Locatelli L, Sacerdote P. β-endorphin concentrations in brain areas and peritoneal macrophages in rats susceptible and resistant to experimental allergic encephalomyelitis: A possible relationship between tumor necrosis factor α and opioids in the disease. J Neuroimmunol 51:169-176, 1994.
23. Walker JS, Howlett CR, Nayanar V. Anti-inflammatory effects of kappa-opioids in adjuvant arthritis. Life Sci 57:371-378, 1995.
24. Amoscato AA, Spiess RR, Sansoni SB, Herberman RB, Chambers CH. Degradation of enkephalins by rat lymphocyte and purified rat natural killer cell surface aminopeptidases. Brain Behav Immun 7:176-187, 1993.
25. + spleen T cells. Arch Biochem Biophys 311:174-179, 1994.
26. Miller BC, Ackroyd A, Hersh LB, Cottam GL. Methionine enkephalin metabolism by murine macrophage ectopeptidase. Regul Pep 50:87-98, 1994.
27. Pruett SB, Han Y-C, Fuchs BA. Morphine suppresses primary humoral immune responses by a predominantly indirect mechanism. J Pharmacol Exp Ther 262:923-928, 1992.
28. Levier DG, Brown RD, McCay JA, Fuchs BA, Harris LS, Munson AE. Hepatic and splenic phagocytosis in female B6C3F1 mice implanted with morphine sulfate pellets. J Pharmacol Exp Ther 267:357-363, 1993.
29. Sei Y, Yoshimoto K, McIntyre T, Skolnick P, Arora PK. Morphine-induced thymic hypoplasia is glucocorticoid-dependent. J Immunol 146:194-198, 1991.
30. Saini A, Sei Y. Morphine inhibits signal transduction subsequent to activation of protein kinase C in mouse splenocytes. Life Sci 52:1751-1758, 1993.
31. Freier DO, Fuchs BA. A mechanism of action for morphine-induced immunosuppression: Corticosterone mediates morphine-induced suppression of natural killer cell activity. J Pharmacol Exp Ther 270:1127-1133, 1994.
32. 2 opioid receptors are involved in morphine-induced suppression of splenocyte natural killer activity. J Pharmacol Exp Ther 264:1179-1186, 1993.
33. Carr DJJ, Mayo S, Gebhardt BM, Porter J. Central α-adrenergic involvement in morphine-mediated suppression of splenic NK activity. J Neuroimmunol 53:53-63, 1994.
34. Fecho K, Dykstra LA, Lysle DT. Evidence for beta adrenergic receptor involvement in the immunomodulatory effects of morphine. J Pharmacol Exp Ther 265:1079-1087, 1993.
35. Band LC, Pert A, Williams W, deCosta BR, Rice KC, Weber RJ. Central μ-opioid receptors mediate suppression of natural killer activity in vivo. Prog Neuroendocrinimmunol 5:95-101, 1992.
36. Hernandez MC, Flores LR, Bayer BM. Immunosuppression by morphine is mediated by central pathways. J Pharmacol Exp Ther 267:1336-1341, 1993.
37. Flores LR, Hernandez MC, Bayer BM. Acute immunosuppressive effects of morphine: Lack of involvement of pituitary and adrenal factors. J Pharmacol Exp Ther 268:1129-1134, 1995.
38. Fecho K, Maslonek KA, Dykstra LA, Lysle DT. Assessment of the involvement of central nervous system and peripheral opioid receptors in the immunomodulatory effects of acute morphine treatment in rats. J Pharmacol Exp Ther 276:626-636, 1996.
39. Carr DJJ. The role of endogenous opioids and their receptors in the immune system. Proc Soc Exp Biol Med 198:710-720, 1991.
40. Reisine T, Bell GI. Molecular biology of opioid receptors. Trends Neurosci 16:506-510, 1993.
41. Evans CJ, Keith D, Magendzo K, Morrison H, Edwards RH. Cloning of a delta opioid receptor by functional expression. Science 258:1952-1955, 1992.
42. Kieffer BL, Befort K, Gaveriaux-Ruff C, Hirth CG. The δ-opioid receptor: Isolation of a cDNA by expression cloning and pharmacological characterization. Proc Natl Acad Sci USA 89:12048-12052, 1992.
43. Yasuda K, Raynor K, Kong H, Breder CD, Takeda J, Reisine T, Bell GI. Cloning and functional comparison of κ and δ opioid receptors from mouse brain. Proc Natl Acad Sci USA 90:6736-6740, 1993.
44. Li S, Zhu J, Chen C, Chen Y-W, DeRiel JK, Ashby B, Liu-Chen L-Y. Molecular cloning and expression of a rat kappa opioid receptor. Biochem J 295:629-633, 1993.
45. Minami M, Toya T, Katao Y, Maekawa K, Nakamura S, Onogi T, Kaneko S, Satoh M. Cloning and expression of a cDNA for the rat kappa-opioid receptor. FEBS Lett 329:291-295, 1993.
46. Nishi M, Takeshima H, Fukuda K, Kato S, Mori K. cDNA cloning and pharmacological characterization of an opioid receptor with high affinities for kappa-subtype-selective ligands. FEBS Lett 330:77-80, 1993.
47. Zhu J, Chen C, Xue J-C, Kunapuli S, DeRiel JK, Liu-Chen L-Y. Cloning of a human opioid receptor from the brain. Life Sci 56:201-207, 1995.
48. Chen Y, Mestek A, Liu J, Yu L. Molecular cloning of a rat kappa opioid receptor reveals sequence similarities to the mu and delta opioid receptors. Biochem J 295:625-628, 1993.
49. Wang JB, Johnson PS, Wu JM, Wang WF, Uhl GR. Human κ opiate receptor second extracellular loop elevates dynorphin's affinity for human μ/κ chimeras. J Biol Chem 269:25966-25969, 1994.
50. Raynor K, Kong H, Mestek A, Bye LS, Tian M, Liu J, Yu L, Reisine T. Characterization of the cloned human mu opioid receptor. J Pharmacol Exp Ther 272:423-428, 1995.
51. Min BH, Augustin LB, Felsheim RF, Fuchs JA, Loh HH. Genomic structure analysis of promoter sequence of a mouse mu opioid receptor gene. Proc Natl Acad Sci USA 91:9081-9085, 1994.
52. Augustin LB, Felsheim RF, Min BH, Fuchs SM, Fuchs JA, Loh HH. Genomic structure of the mouse δ opioid receptor gene. Biochem Biophys Res Commun 207:111-119, 1995.
53. Nishi M, Takeshima H, Mori M, Nakagawara K-I, Takeuchi T. Structure and chromosomal mapping of genes for the mouse κ-opioid receptor and an opioid receptor homologue (MOR-C). Biochem Biophys Res Commun 205:1353-1357, 1994.
54. Yakovlev AG, Krueger KE, Faden AI. Structure and expression of a rat kappa opioid receptor gene. J Biol Chem 270:6421-6424, 1995.
55. Liu HC, Lu S, Augustin LB, Felsheim RF, Chen HC, Loh HH, Wei LN. Cloning and promoter mapping of mouse kappa opioid receptor gene. Biochem Biophys Res Commun 209:639-647, 1995.
56. Belkowski SM, Zhu J, Liu-Chen L-Y, Eisenstein TK, Adler MW, Rogers TJ. Sequence of κ-opioid receptor cDNA in the R1.1 thymoma cell line. J Neuroimmunol 62:113-117, 1995.
57. Fukuda K, Kato S, Mori K, Nishi M, Takeshima H, Iwabe N, Miyata T, Houtani T, Sugimoto T. cDNA cloning and regional distribution of a novel member of the opioid receptor family. FEBS Lett 343:42-46, 1994.
58. Mollereau C, Parmentier M, Mailleux P, Butour JL, Moisand C, Chalon P, Caput D, Vassart G, Meunier JC. ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett 341:33-38, 1994.
59. 1 receptor. Nature 377:532-535, 1995.
60. Reinscheid RK, Nothacker H-P, Bourson A, Ardati A, Henningsen RA, Bunzow JR, Grandy DK, Langen H, Monsma FJ Jr., Civelli O. Orphanin FQ: A neuropeptide that activates an opioidlike G protein-coupled receptor. Science 270:792-794, 1995.
61. Chuang LF, Chuang TK, Killam KFJr., Chuang AJ, Kung H-F, Yu L, Chuang RY. Delta opioid receptor gene expression in lymphocytes. Biochem Biophys Res Commun 202:1291-1299, 1994.
62. Sedqi M, Roy S, Ramakrishnan S, Elde R, Loh HH. Complementary DNA cloning of a μ-opioid receptor from rat peritoneal macrophages. Biochem Biophys Res Commun 209:563-574, 1995.
63. Chuang TK, Killam KF Jr., Chuang LF, Kung H-F, Sheng WS, Chao CC, Yu L, Chuang RY. Mu opioid receptor gene expression in immune cells. Biochem Biophys Res Commun 216:922-930, 1995.
64. Chuang LF, Chuang TK, Killam KF, Qiu Q, Wang XR, Lin J-J, Kung H-F, Sheng W, Chao C, Yu L, Chuang RY. Expression of kappa opioid receptors in human and monkey lymphocytes. Biochem Biophys Res Commun 209:1003-1010, 1995.
65. Bidlack JM, Saripalli LD, Lawrence DMP. κ-Opioid binding sites on a murine lymphoma cell line. Eur J Pharmacol 227:257-265, 1992.
66. Lawrence DMP, Bidlack JM. Kappa opioid binding sites on the R1.1 murine lymphoma cell line: Sensitivity to cations and guanine nucleotides. J Neuroimmunol 41:223-230, 1992.
67. Lawrence DMP, Bidlack JM. The kappa opioid receptor expressed on the mouse R1.1 thymoma cell line is coupled to adenylyl cyclase through a pertussis toxin-sensitive guanine nucleotide-binding regulatory protein. J Pharmacol Exp Ther 266:1678-1683, 1993.
68. Halford WP, Gebhardt BM, Carr DJJ. Functional role and sequence analysis of a lymphocyte orphan opioid receptor. J Neuroimmunol 59:91-101, 1995.
69. Most H. Falciporum malaria among drug addicts. Am J Pub Health 30:403-410, 1940.
70. Hussey HH, Katz S. Infections resulting from narcotic addiction: Report of 102 cases. Am J Med 9:186-193, 1950.
71. Briggs JH, McKerron CG, Souhami RL, Taylor DJE, Andrews H. Severe systemic infections complicating in "mainline" heroin addiction. Lancet ii:1227-1231, 1967.
72. Sapira J. The narcotic addict as a medical patient. Am J Med 45:555-588, 1968.
73. Brown SW, Stimmel B, Taub RN, Kouchwa S, Rosenfield RE. Immunological dysfunction in heroin addicts. Arch Intern Med 134:1001-1006, 1974.
74. Tubaro E, Borelli G, Croce C, Cavallo G, Santiangeli C. Effect of morphine on resistance to infection. J Infect Dis 148:656-666, 1983.
75. Pacifici R, Patrini G, Venier I, Parolaro D, Zuccaro P, Gori E. Effect of morphine and methadone acute treatment on immunological activity in mice: Pharmacokinetic and pharmacodynamic correlates. J Pharmacol Exp Ther 269:1112-1116, 1994.
76. Dismukes WE, Karchmer AW, Johnson RF, Dougherty WJ. Viral hepatitis associated with illicit parenteral use of drugs. JAMA 206:1048-1052, 1988.
77. Haverkos HW, Lange WR. Serious infections other than human immunodeficiency virus among intravenous drug abusers. J Infect Dis 161:894-901, 1990.
78. Lorenzo P, Portoles A Jr., Beneit JV, Ronda E, Portoles A. Physical dependence to morphine diminishes the interferon response in mice. Immunopharmacology 14:93-100, 1987.
79. Starec M, Rouveix B, Sinet M, Chau F, Desforges B, Pocidalo J-J, Lechat P. Immune status and survival of opiate- and cocaine-treated mice infected with Friend virus. J Pharmacol Exp Ther 259:745-750, 1991.
80. Veyries M-L, Sinet M, Desforges B, Rouveix B. Effects of morphine on the pathogenesis of murine Friend retrovirus infection. J Pharmacol Exp Ther 272:498-504, 1995.
81. Carpenter GW, Garza HH Jr., Gebhardt BM, Carr DJJ. Chronic morphine treatment suppresses CTL-mediated cytolysis, granulation, and cAMP responses to alloantigen. Brain Behav Immun 8:185-203, 1994.
82. Carpenter GW, Carr DJJ. Pretreatment with β-funaltrexamine blocks morphine-mediated suppression of CTL activity in alloimmunized mice. Immunopharmacol 29:129-140, 1995.
83. Carr DJJ, Carpenter GW. Morphine-induced suppression of cytotoxic T lymphocyte activity in alloimmunized mice is not mediated through a naltrindole-sensitive delta opioid receptor. Neuroimmunomodulation 2:44-53, 1995.
84. Molitor TW, Morilla A, Risdahl JM, Murtaugh MP, Chao CC, Peterson PK. Chronic morphine administration impairs cellmediated immune responses in swine. J Pharmacol Exp Ther 260:581-586, 1992.
85. Risdahl JM, Peterson PK, Chao CC, Pijoan C, Molitor TW. Effects of morphine dependence on the pathogenesis of swine herpesvirus infection. J Infect Dis 167:1281-1287, 1993.
86. Chuang LF, Killam KF, Chuang RY. Increased replication of simian immunodeficiency virus in CEM × 174 cells by morphine sulfate. Biochem Biophys Res Commun 195:1165-1173, 1993.
87. Nottet HSLM, Gendelman HE. Unraveling the neuroimmune mechanisms for the HIV-1-associated cognitive/motor complex. Immunol Today 16:441-448, 1995.
88. Peterson PK, Gekker G, Hu S, Anderson WR, Kravitz F, Portoghese PS, Balfour HH Jr., Chao CC. Morphine amplifies' HIV-1 expression in chronically infected promonocytes cocultured with human brain cells. J Neuroimmunol 50:167-175, 1994.
89. Peterson PK, Gekker G, Hu S, Schoolov Y, Balfour HH Jr., Chao CC. Microglial cell upregulation of HIV-1 expression in the chronically infected promonocytic cell line U1: The role of tumor necrosis factor-α. J Neuroimmunol 41:81-88, 1992.
90. Chao CC, Gekker G, Sheng WS, Hu S, Tsang M, Peterson PK. Priming effect of morphine on the production of tumor necrosis factor-α by microglia: Implications in respiratory burst activity and human immunodeficiency virus-1 expression. J Pharmacol Exp Ther 269:198-203, 1994.
91. Folks TM, Clouse KA, Justement J, Rabson A, Duh E, Kehrl JH, Fauci AS. Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T cell clone. Proc Natl Acad Sci USA 86:2365-2368, 1989.
92. Tadmori W, Mondal D, Tadmori I, Prakash O. Transactivation of human immunodeficiency virus type 1 long terminal repeats by cell surface tumor necrosis factor-α. J Virol 65:6425-6429, 1991.
93. Sundar KS, Kamaraju LS, Dingfelder J, McMahon J, Gollapudi S, Wilson WH, Kong L-Y, Hong JS, Weiss JM, Lee JE. Beta-endorphin enhances the replication of neurotropic human immunodeficiency virus in fetal perivascular microglia. J Neuroimmunol 61:97-104, 1995.
94. Lolait SJ, Clements JA, Markwick AJ, Cheng C, McNally M, Smith AI, Funder JW. Pro-opiomelanocortin messenger ribonucleic acid and posttranslational processing of beta-endorphin in spleen macrophages. J Clin Invest 77:1776-1779, 1986.
95. Chao CC, Sharp BM, Pomeroy C, Filice GA, Peterson PK. Lethality of morphine in mice infected with Toxoplasma gondii. J Pharmacol Exp Ther 252:605-609, 1990.
96. Singh PP, Singh S, Dutta GP, Srimal RC. Immunomodulation by morphine in Plasmodium berghei-infected mice. Life Sci 54:331-339, 1993.
97. Eisenstein TK. Opioids sensitize to endogenous and exogenous bacterial infection. 3rd Annual Symposium on AIDS, Drugs of Abuse and the Neuroimmune Axis, Abstract #17, November 9-11, San Diego, CA, 1995.