Evidence for opioid receptors on cells involved in host defense and the immune system

Journal of Neuroimmunology

Volumn 83, Issue 1-2, 1998, Pages 45-56

  Sharp, Burt M ^a,b   Roy, Sabita ^b   Bidlack, Jean M ^c  

^a MINNEAPOLIS MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c Minneapolis Vet Admin Univ M ^*

Author keywords

Delta; Kappa; Mu

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; BETA ENDORPHIN; BREMAZOCINE; CYTOKINE; DELTA OPIATE RECEPTOR; DELTORPHIN; ENKEPHALIN DERIVATIVE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; ENKEPHALIN[2 DEXTRO ALANINE 5 DEXTRO LEUCINE]; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; KAPPA OPIATE RECEPTOR; MESSENGER RNA; METENKEPHALINAMIDE[2 DEXTRO ALANINE]; MU OPIATE RECEPTOR; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE; NALOXONE; NALTRINDOLE; OPIATE; OPIATE AGONIST; OPIATE RECEPTOR; PROENKEPHALIN;

ANIMAL CELL; ARTICLE; BINDING SITE; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; LIGAND BINDING; LYMPHOCYTE; LYMPHOMA CELL LINE; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

HUMANS; IMMUNE SYSTEM; LEUKOCYTES, MONONUCLEAR; NEUROIMMUNOMODULATION; RECEPTORS, OPIOID;

EID: 0032520701     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-5728(97)00220-8     Document Type: Article

References (104)

1. Apte R.N., Durum S.K., Oppenheim J.J. Opioids modulate interleukin-1 production and secretion by bone-marrow macrophages. Immunol. Lett. 24:1990;141-148.
2. Arora P.K., Fride E., Petitto J., Waggie K., Skolnick P. Morphine-induced immune alterations in vivo. Cell. Immunol. 126:1990;343-353.
3. Bayer B.M., Daussin S., Hernandez M., Irvin L. Morphine inhibition of lymphocyte activity is mediated by an opioid dependent mechanism. Neuropharmacology. 29:1990;369-374.
4. Bayer B.M., Gastonguay M.R., Hernandez M.C. Distinction between the in vitro and in vivo inhibitory effects of morphine on lymphocyte proliferation based on agonist sensitivity and naltrexone reversibility. Immunopharmacology. 23:1992;117-124.
5. Belkowski S.M., Alicea C., Eisenstein T.K., Adler M.W., Rogers T.J. Inhibition of interleukin-1 and tumor necrosis factor-a synthesis following treatment of macrophages with the kappa opioid agonist U50,488H. J. Pharmacol. Exp. Ther. 273:1995;1491-1496.
6. Belkowski S.M., Zhu J., Liu-Chen L.-Y., Eisenstein T.K., Adler M.W., Rogers T.J. Detection of kappa-opioid receptor mRNA in immature T-cells. Adv. Exp. Med. Biol. 373:1995;11-16.
7. Belkowski S.M., Zhu J., Liu-Chen L.-Y., Eisenstein T.K., Adler M.W., Rogers T.J. Sequence of κ-opioid receptor cDNA in the R1.1 thymoma cell line. J. Neuroimmunol. 62:1995;113-117.
8. Bidlack J.M., Saripalli L.D., Lawrence D.M.P. κ-Opioid binding sites on a murine lymphoma cell line. Eur. J. Pharmacol. 227:1992;257-265.
9. Bidlack, J.M., Lawrence, D.M.P., Ignatowski, T.A., in press. Kappa opioid receptors on immune cells as studied by fluorescent ligands. In: Friedman, H., Eisenstein, T., Madden, J., Sharp, B. (Eds.), AIDS, Drugs of Abuse, and the Neuroimmune Axis. Plenum, New York.
10. Bryant H.U., Bernton E.W., Holaday J.W. Immunosuppressive effects of chronic morphine treatment in mice. Life Sci. 41:1987;1731-1738.
11. Bryant H.U., Yoburn B.C., Inturrisi C.E., Bernton E.W., Holaday J.W. Morphine-induced immunomodulation is not related to serum morphine concentrations. Eur. J. Pharmacol. 149:1988;165-169.
12. Bryant H.U., Bernton E.W., Kenner J.R., Holaday J.W. Role of adrenal cortical activation in the immunosuppressive effects of chronic morphine treatment. Endocrinology. 128:1991;3253-3258.
13. Bussiere J.L., Adler M.W., Rogers R.J., Eisenstein T.K. Cytokine reversal of morphine-induced suppression of the antibody response. J. Pharmacol. Exp. Ther. 264:1993;591-597.
14. Caroleo M.C., Arbitrio M., Melchiorri D., Nistico G. A reappraisal of the role of the various opioid receptor subtypes in cell-mediated immunity. Neuroimmunomodulation. 1:1994;141-147.
15. Carr D.J., Kim C.H., DeCosta B., Jacobson A.E., Rice K.C., Blalock J.E. Evidence for delta-class opioid receptor on cells of the immune system. Cell Immnol. 116(1):1988;44-51.
16. Carr D.J.J., DeCosta B.R., Kim C.-H., Jacobson A.E., Guarcello V., Rice K.C., Blalock J.E. Opioid receptors on cells of the immune system: evidence for δ- and κ-classes. J. Endocrinol. 122:1989;161-168.
17. Chao C.C., Sharp B.M., Pomeroy C., Filice G.A., Peterson P.K. Lethality of morphine in mice infected with Toxoplasma gondii. J. Pharmacol. Exp. Ther. 252:1990;605-609.
18. Chao C.C., Gekker G., Hu S., Sheng W.S., Portoghese P.S., Peterson P.K. Upregulation of HIV-1 expression in co-cultures of chronically infected promonocytes and human brain cells by dynorphin. Biochem. Pharmacol. 50:1995;715-722.
19. Chao C.C., Gekker G., Hu S., Sheng W.S., Shark K.B., Bu D.-F., Archer S., Bidlack J.M., Peterson P.K. Kappa opioid receptors in human microglia downregulate human immunodeficiency virus-1 expression. Proc. Natl. Acad. Sci. USA. 93:1996;8051-8056.
20. Chuang L.F., Chuang T.K., Killam K.F., Chuang A.J., Kung H.F., Yu L., Chuang R.Y. Delta opioid receptor gene expression in lymphocytes. Biochem. Biophys. Res. Commun. 202:1994;1291-1299.
21. Chuang L.F., Chuang T.K., Killam K.F. Jr., Qiu Q., Wang X.R., Lin J.-J., Kung H.-F., Sheng W., Chao C., Yu L., Chuang R.Y. Expression of kappa opioid receptors in human and monkey lymphocytes. Biochem. Biophys. Res. Commun. 209:1995;1003-1010.
22. Chuang T.K., Killam K.F., Chuang L.F., Kung H.F., Sheng W.S., Chao C.C., Yu L., Chuang R.Y. Mu opioid receptor gene expression in immune cells. Biochem. Biophys. Res. Commun. 216:1995;922-930.
23. Clark J.A., Liu L., Price M., Hersh B., Edelson M., Pasternak G.W. Kappa opioid receptor multiplicity: evidence for two U50,488-sensitive kappa 1 subtypes and a novel kappa 3 subtype. J. Pharmacol. Exp. Ther. 251:1989;461-468.
24. Cooper D.M.F., Londos C., Gill D.L., Rodbell M. Opiate receptor-mediated inhibition of adenylate cyclase in rat striatal plasma membranes. J. Neurochem. 38:1982;1164-1167.
25. Evans C.J., Keith D.E. Jr., Morrison H., Magendzo K., Edwards R.H. Cloning of a delta opioid receptor by functional expression. Science. 258:1992;1952-1955.
26. Fecho K., Dykstra L.A., Lysle D.T. Evidence for β-adrenergic receptor involvement in the immunomodulatory effects of morphine. J. Pharmacol. Exp. Ther. 265:1993;1079-1087.
27. Fiorica E., Spector S. Opioid binding site in EL-4 thymoma cell line. Life Sci. 42:1988;199-206.
28. Foris G., Medgyesi G.A., Hauck M. Bidirectional effect of met-enkephalin on macrophage effector functions. Mol. Cell. Biochem. 69:1986;127-137.
29. Foris G., Medgyesi G.A., Nagy J.T., Varga Z. Concentration-dependent effect of met-enkephalin on human polymorphonuclear leukocytes. Ann. NY Acad. Sci. 496:1987;151-157.
30. Foster J.S., Moore R.N. Dynorphin and related opioid peptides enhance tumoricidal activity mediated by murine peritoneal macrophages. J. Leukoc. Biol. 42:1987;171-174.
31. Fowler C.J., Fraser G.L. μ-, δ-, κ-opioid receptors and their subtypes. A critical review with emphasis on radioligand binding experiments. Neurochem. Int. 24:1994;401-426.
32. Fuchs B.A., Pruett S.B. Morphine induces apoptosis in murine thymocytes in vivo but not in vitro: involvement of both opiate and glucocorticoid receptors. J. Pharm. Exp. Ther. 266:1993;417-423.
33. Gaveriaux C., Peluso J., Simonin F., Laforet J., Kieffer B. Identification of kappa- and delta-opioid receptor transcripts in immune cells. FEBS Lett. 369:1995;272-276.
34. George R., Way E.L. Studies on the mechanism of pituitary-adrenal activation by morphine. Br. J. Pharmacol. 10:1955;260-264.
35. Guan L., Townsend R., Eisenstien T.K., Adler M.W., Rogers T.J. Both T-cells and macrophages are targets of κ-opioid-induced immunosuppression. Brain Behav. Immun. 8:1994;229-240.
36. Gungor M., Genc E., Sogduyu H., Eroglu L., Koyuncuoglu H. Effect of chronic administration of morphine on primary immune response in mice. Experientia. 36:1980;1309-1310.
37. Hagi K., Uno K., Inaba K., Muramatsu S. Augmenting effect of opioid peptides on murine macrophage activation. J. Neuroimmunol. 50:1994;71-76.
38. Heagy W., Laurance M., Cohen E., Finberg R. Neurohormones regulate T-cell function. J. Exp. Med. 171:1990;1625-1633.
39. Heagy W., Shipp M.A., Finberg R.W. Opioid receptor agonists and Ca2+ modulation in human B-cell lines. J. Immunol. 149:1992;4074-4081.
40. Ignatowski, T.A., Bidlack, J.M., 1996. Fluorescent labeling of the kappa opioid receptor on cells of the immune system. Abstr. from the 4th Ann. Symp. on AIDS, Drugs of Abuse and the Neuroimmune Axis. Symposium conducted in San Juan, Puerto Rico.
41. Jankovic B.D., Radulovic J. Quaternary naltrexone: its immunomodulatory activity and interaction with brain delta and kappa opioid receptors. Immunopharmacology. 28:1994;105-112.
42. Joseph D.B., Bidlack J.M. The kappa opioid receptor expressed on the mouse R1.1 thymoma cell line down-regulates without desensitizing during chronic opioid exposure. J. Pharmacol. Exp. Ther. 272:1995;970-976.
43. Katada T., Ui M. ADP Ribosylation of the specific membrane protein of C6 cells by islet-activating protein associated with modification of adenylate cyclase activity. J. Biol. Chem. 257:1982;7210-7216.
44. Konkoy C.S., Childers S.R. Dynorphin-selective inhibition of adenylyl cyclase in guinea pig cerebellum membranes. Mol. Pharmacol. 36:1989;627-633.
45. Konkoy C.S., Childers S.R. Relationship between kappa 1 opioid receptor binding and inhibition of adenylyl cyclase in guinea pig brain membranes. Biochem. Pharmacol. 45:1993;207-216.
46. Laugwitz K.L., Offermans S., Spicher K., Schultz G. Mu and delta opioid receptors differentially couple to G protein subtypes in membranes of human neuroblastoma SH-SY5Y cells. Neuron. 10:1993;233-242.
47. Law P.-Y., Wu J., Koehler J.E., Loh H.H. Demonstration and characterization of opiate inhibition of the striatal adenylate cyclase. J. Neurochem. 36:1981;1834-1846.
48. Law P.-Y., Louie A.K., Loh H.H. Effect of pertussis toxin treatment on the down-regulation of opiate receptors in neuroblastoma×glioma NG108-15 hybrid cells. J. Biol. Chem. 260:1985;14818-14823.
49. Lawrence D.M.P., Bidlack J.M. Kappa opioid binding sites on the R1.1 murine lymphoma cell line: sensitivity to cations and guanine nucleotides. J. Neuroimmunol. 41:1992;223-230.
50. Lawrence D.M.P., Bidlack J.M. 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. 266:1993;1678-1683.
51. Lawrence D.M.P., El-Hamouly W., Archer S., Leary J.F., Bidlack J.M. Identification of κ opioid receptors in the immune system by indirect immunofluorescence. Proc. Natl. Acad. Sci. USA. 92:1995;1062-1066.
52. Lawrence D.M.P., Joseph D.B., Bidlack J.M. Kappa opioid receptors expressed on three related thymoma cell lines. Difference in receptor-effector coupling. Biochem. Pharmacol. 49:1995;81-89.
53. Lefkowiz S.S., Chiang C.Y. Effects of certain abused drugs on hemolysin forming cells. Life Sci. 17:1975;1763-1768.
54. Li S., Zhu J., Chen C., Chen Y.-W., DeRiel J.K., Ashby B., Liu-Chen L.-Y. Molecular cloning and expression of a rat kappa opioid receptor. Biochem. J. 295:1993;629-633.
55. 4-positive thymocytes. Endocrinology. 128:1991;717-724.
56. Linner K.M., Nicol S.E., Sharp B.M. IL-1β modulates the concanavalin-A-induced expression of proenkephalin A nRNA in murine thymocytes. J. Pharmacol. Exp. Ther. 267:1993;1566-1572.
57. Linner K.M., Quist H.E., Sharp B.M. Met-enkephalin-containing peptides encoded by proenkephalin A mRNA expressed in activated murine thymocytes inhibit thymocyte proliferation. J. Immunol. 154:1995;5049-5060.
58. Linner K.M., Quist H.E., Sharp B.M. Expression and function of proenkephalin A messenger ribonucleic acid in murine fetal thymocytes. Endocrinology. 137:1996;857-863.
59. Lolait S.J., Clements J.A., Markwick A.J., Cheng C., McNally M., Smith A.I., Funder J.W. Pro-opiomelanocortin messenger ribonucleic acid and post-translational processing of beta endorphin in spleen macrophages. J. Clin. Invest. 77:1986;1776-1779.
60. Mack K.J., Lee M.F., Weyhenmeyer J.A. Effects of guanyl nucleotides and ions on kappa opioid binding. Brain Res. Bull. 14:1985;301-306.
61. Madden, J.J., Donahue, R.M., 1990. Opiate binding to cells of the immune system. In: Watson, R.R. (Ed.), Drugs of Abuse and the Immune Function. CRC Press, Boca Raton, FL, pp. 213-228.
62. 3-opiate receptors. Eur. J. Pharmacol. 273:1995;5-6.
63. Martin-Kleiner I., Osmak M., Gabrilovac J. Regulation of NK cell activity and the level of the intracellular cAMP in human peripheral blood lymphocytes by met-enkephalin. Exp. Med. (Berl.). 192(2):1991;145-150.
64. Mehrishi J.N., Mills I.H. Opiate receptors on lymphocytes and platelets in man. Clin. Immunol. Immunopathol. 27:1983;240-249.
65. Mendelsohn L.G., Kerchner G.A., Culwell M., Ades E.W. Immunoregulation by opiate peptides: I. Absence of classical opioid receptor on human mononuclear cells. J. Clin. Lab. Immunol. 16:1985;125-129.
66. North R.A., Williams J.T. Opiate activation of potassium conductance inhibits calcium action potentials in rat locus coeruleus neurones. Br. J. Pharmacol. 80:1983;225-228.
67. North R.A., Williams J.T., Surprenant A., Christie M.J. Mu and delta receptors belong to a family of receptors that are coupled to potassium channels. Proc. Natl. Acad. Sci. USA. 84:1987;5487-5491.
68. Osugi T., Taniura H., Ikemoto M., Miki N. Effects of chronic exposure of NG108-15 cells to morphine or ethanol on binding of nuclear factors to cAMP-response element. Biochem. Biophys. Res. Commun. 174:1991;25-31.
69. Pacifici R., Patrini G., Venier I., Parolaro D., Zuccarro P., Gori E. Effect of morphine and methadone acute treatment on immunological activity in mice: pharmacokinetic and pharmacodynamic correlates. J. Pharmacol. Exp. Ther. 269:1994;1112-1116.
70. Pardros M.R., Vindrola O., Zunszain P., Fainboin L., Finkielman S., Nahmod V.E. Mitogenic activation of the human lymphocytes induce the release of proenkephalin derived peptides. Life Sci. 45:1989;1805-1811.
71. Paterson S.J., Robson L.E., Kosterlitz H.W. Control by cations of opioid binding in guinea pig brain membranes. Proc. Natl. Acad. Sci. USA. 83:1986;6216-6220.
72. Peterson P.K., Sharp B., Gekker G., Brummit C., Keane W.F. Opioid mediated suppression of interferon g production by cultured peripheral blood mononuclear cells. J. Clin. Invest. 80:1987;824-831.
73. Peterson P.K., Molitor T.W., Chao C.C. Mechanisms of morphine induced immunomodulation. Biochem. Pharmacol. 46:1993;343-348.
74. Petrov R.V., Mikhailova A.A., Zakharova L.A., Vasilenko A.M., Katlinsky A.V. Myelopeptides-bone marrow mediators with immunostimulating and endorphin like activity. Scand. J. Immunol. 24:1986;237-243.
75. Portoghese P.S., Sultana M., Takemori A.E. Naltrindole, a highly selective and potent non-peptide delta opioid receptor antagonist. Eur. J. Pharmacol. 146:1988;185-186.
76. Radulovic J., Miljevic C., Djergovic D., Vujic V., Antic J., Von Hšrsten S., Jankovic B.D. Opioid receptor-mediated suppression of humoral immune response in vivo and in vitro: involvement of κ opioid receptors. J. Neuroimmunol. 57:1995;55-62.
77. Raynor K., Kong H., Hines J., Kong G., Benovic J., Yasuda K., Bell G.I., Reisine T. Molecular mechanisms of agonist-induced desensitization of the cloned mouse kappa receptor. J. Pharmacol. Exp. Ther. 270:1994;1381-1386.
78. Rosen H., Behar O., Abramsky O., Ovadia H. Regulated expression of proenkephalin A in normal lymphocytes. J. Immunol. 143:1989;3703-3707.
79. Roy S., Ramakrishnan S., Loh H.H., Lee N.M. Chronic morphine treatment selectively suppresses macrophage colony formation in bone marrow. Eur. J. Pharmacol. 195:1991;359-363.
80. 3H]-morphine binding to thymocytes is enhanced by IL-1 stimulation. FEBS Lett. 287:1991;93-96.
81. Roy S., Loh H.H., Barke R.A. Morphine induced suppression of thymocyte proliferation is mediated by inhibition of IL-2 synthesis. Adv. Exp. Med. Biol. 373:1995;41-48.
82. Roy S., Sedqi M., Ramakrishnan S., Barke R.A., Loh H.H. Differential effects of opioids on the proliferation of a macrophage cell line. Cell. Immunol. 169(2):1996;271-277.
83. Saravia F., Ase A., Aloyz R., Kleid M.C., Ines M., Rodriguez V., Nahmod V.E., Vindrola O. Differential post-translational processing of proenkephalin in rat bone marrow and spleen mononuclear cells: evidence for synenkephalin cleavage. Endocrinology. 132:1993;1431-1437.
84. Sedqi M., Roy S., Ramakrishnan S., Elde R., Loh H.H. Complementary DNA cloning of a μ-opioid receptor from rat peritoneal macrophages. Biochem. Biophys. Res. Commun. 209:1995;563-574.
85. Sei Y., Yoshimoto K., McIntyre T., Skolnick P., Arora P.K. Morphine induced thymic hypoplasia is glucocorticoid dependent. J. Immunol. 146:1991;194-198.
86. + murine T-cells. J. Pharmacol. Exp. Ther. 273:1995;1105-1113.
87. Shahabi N.A., Heagy W., Sharp B.M. β-Endorphin enhances concanavalin A-stimulated calcium mobilization by murine splenic T-cells. Endocrinology. 137:1996;3386-3393.
88. Sharp B.M., Keane W.F., Suh J.J., Gekker G., Tsukayama D., Peterson P.K. Opioid peptides rapidly stimulate superoxide production by human polymorphonuclear leukocytes and macrophages. Endocrinology. 117:1985;793-795.
89. Sharp B.M., Shahabi N.A., Heagy W., McAllen K., Bell M., Huntoon C., McKeane D.J. Dual signal transduction through delta opioid receptors in a transfected human T-cell line. Proc. Natl. Acad. Sci. USA. 93:1996;8294-8299.
90. Sharp B.M., Shahabi N., McKean D., Li M.D., McAllen K. Detection of basal levels and induction of delta opioid receptor mRNA in murine splenocytes. J. Neuroimmunol. 78:1997;198-202.
91. Shavit Y., Martin F.C., Angarita L.H., Gale R.P., Liebeskind J.C. Morphine-induced suppression of natural killer cell activity is mediated by the adrenal gland. Soc. Neurosci. Abstr. 12:1986;339.
92. Sibinga N.E.S., Goldstein A. Opioid peptides and opioid receptors in cells of the immune system. Ann. Rev. Immunol. 6:1988;219-249.
93. Stefano G.B., Cadet P., Scharrer B. Stimulatory effects of opioid neuropeptides on locomotory activity and conformational changes in invertebrate and human immunocytes: evidence for a subtype of delta receptor. Proc. Natl. Acad. Sci. USA. 86:1989;6307-6311.
94. Stefano G.B., Melchiorri P., Negri L., Hughes T.K. Jr., Scharrer B. [D-Ala2] deltorphin I binding and pharmacological evidence for a special subtype of delta opioid receptor on human and invertebrate immune cells. Proc. Natl. Acad. Sci. USA. 89:1992;9316-9320.
95. Szabo I., Rojavin M., Bussiere J.L., Eisenstein T.K., Adler M.W., Rogers T.J. Suppression of peritoneal macrophage phagocytosis of Candida albicans by opioids. J. Pharmacol. Exp. Ther. 267:1993;703-706.
96. Taub D.D., Eisenstein T.K., Geller E.B., Adler M.W., Rogers T.J. Immunomodulatory activity of μ- and κ-selective opioid agonists. Proc. Natl. Acad. Sci. USA. 88:1991;360-364.
97. Tosk J.M., Grim J.R., Kinback K.M., Sale E.J., Bozzetti L.P., Will A.D. Modulation of chemiluminescence in a murine macrophage cell line by neuroendocrine hormones. Int. J. Immunopharmacol. 15:1993;615-620.
98. Tubaro E., Avico U., Santiangeli C., Zuccaro P., Cavallo G., Pacifici R., Croce C., Borelli G. Morphine and methadone impact of human phagocytic physiology. Int. J. Immunopharmacol. 7:1985;865-874.
99. VanEpps D.E., Saland L. β-endorphin and met-enkephalin stimulate human peripheral blood mononuclear cell chemotaxis. J. Immunol. 132:1984;3046.
100. Weber R.J., Pert A. The periaqueductal gray matter mediates opiate-induced immunosuppression. Science. 245:1989;188-190.
101. Wick M.J., Minnerath S.R., Roy S., Ramakrishnan S., Loh H.H. Differential expression of opioid receptor genes in human lymphoid cell lines and peripheral blood lymphocytes. J. Neuroimmunol. 64(1):1996;29-36.
102. Yasuda K., Raynor K., Kong H., Breder C.D., Takeda J., Reisine T., Bell G.I. Cloning and functional comparison of κ and δ opioid receptors form mouse brain. Proc. Natl. Acad. Sci. USA. 90:1993;6736-6740.
103. Zhu J., Chen C., Xue J.C., Kunapuli S., DeRiel J.K., Liu-Chen L.Y. Cloning of a human kappa opioid receptor from the brain. Life Sci. 56:1995;201-207.
104. Zurawski G., Benedik M., Kamb B.J., Abrams J.S., Zurawski S.M., Lee F.D. Activation of mouse T-helper cells induces abundant pre-proenkephalin mRNA synthesis. Science. 232:1986;772-775.