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Opioid Receptors and Signaling on Cells from the Immune System

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Abstract

This review discusses the criteria for determining whether a binding site or functional response is directly mediated by either the mu, delta, or kappa opioid receptors. In 1988, Sibinga and Goldstein published the first review that addressed whether cells from the immune system express opioid receptors. The criteria that they used, namely, structure–activity relationships, stereoselectivity, dose- and concentration-dependence, and saturability are still relevant criteria today for determining if an immunological response is mediated by either the mu, delta or kappa opioid receptors. Radioligand receptor binding studies and functional studies that clearly show the presence of an opioid receptor on immunocytes are presented. Selective agonists and antagonists for the mu, delta, and kappa opioid receptors are discussed, and the need for their use in experiments is emphasized. Conditions used in functional assays are very important. Receptor desensitization and downregulation occur within minutes after the application of an agonist. However, many immunological assays are applying an agonist for days before measuring an immunological effect. The results obtained may reflect changes that are results of receptor desensitization and/or downregulation instead of changes that are observed with acute activation of the receptor. The future of receptor pharmacology lies in the crosstalk and dimerization of G protein-coupled receptors. In transfected systems, opioid receptors have been shown to dimerize with chemokine and cannabinoid receptors, resulting in crosstalk between different types of receptors.

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References

  • Alicea C, Belkowski SM, Sliker JK, Zhu J, Liu-Chen LY, Eisenstein TK, Adler MW, Rogers TJ (1998) Characterization of kappa-opioid receptor transcripts expressed by T cells and macrophages. J Neuroimmunol 91:55–62

    PubMed  CAS  Google Scholar 

  • Apte RN, Durum SK, Oppenheim JJ (1990) Opioids modulate interleukin-1 production and secretion by bone-marrow macrophages. Immunol Lett 24:141–148

    PubMed  CAS  Google Scholar 

  • Bayer BM, Daussin S, Hernandez M, Irvin L (1990) Morphine inhibition of lymphocyte activity is mediated by an opioid dependent mechanism. Neuropharmacology 29:369–374

    PubMed  CAS  Google Scholar 

  • Bayer BM, Gastonguay MR, Hernandez MC (1992) Distinction between the in vitro and in vivo inhibitory effects of morphine on lymphocyte proliferation based on agonist selectivity and naltrexone reversiblity. Immunopharmacology 23:117–124

    PubMed  CAS  Google Scholar 

  • Belkowski SM, Alicea C, Eisenstein TK, Adler MW, Rogers TJ (1995a) 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

    PubMed  CAS  Google Scholar 

  • Belkowski SM, Zhu JM, Liu-Chen L-Y, Eisenstein TK, Adler MW, Rogers TJ (1995b) Sequence of kappa-opioid receptor cDNA in the R1.1 thymoma cell line. J Neuroimmunol 62:113–117

    PubMed  CAS  Google Scholar 

  • Belkowski SM, Zhu J, Liu-Chen L-Y, Eisenstein TK, Adler MW, Rogers TJ (1995c) Detection of kappa-opioid receptor mRNA in immature T-cells. Adv Exp Med Biol 373:11–16

    PubMed  CAS  Google Scholar 

  • Bidlack JM (2000) Detection and function of opioid receptors on cells from the immune system. Clin Diagn Lab Immunol 7:719–723

    PubMed  CAS  Google Scholar 

  • Bidlack JM, Abraham MK (2001) Mitogen-induced activation of mouse T cells increases kappa opioid receptor expression. Adv Exp Med Biol 493:103–110

    PubMed  CAS  Google Scholar 

  • Bidlack JM, Saripalli LD, Lawrence DMP (1992) κ-Opioid binding sites on a murine lymphoma cell line. Eur J Pharmacol 227:257–265

    PubMed  CAS  Google Scholar 

  • Bilsky EJ, Calderon SN, Wang T, Bernstein RN, Davis P, Hruby VJ, McNutt RW, Rothman RB, Rice KC, Porreca F (1995) SNC 80, a selective, nonpeptidic and systemically active opioid delta agonist. J Pharmacol Exp Ther 273:359–366

    PubMed  CAS  Google Scholar 

  • Börner C, Höllt V, Kraus J (2006) Cannabinoid receptor type 2 agonists induce transcription of the mu-opioid receptor gene in Jurkat T cells. Mol Pharmacol 69:1486–1491

    PubMed  Google Scholar 

  • Boyadjieva NI, Chaturvedi K, Poplawski MM, Sarkar DK (2004) Opioid antagonist naltrexone disrupts feedback interaction between mu and delta opioid receptors in splenocytes to prevent alcohol inhibition of NK cell function. J Immunol 173:42–49

    PubMed  CAS  Google Scholar 

  • Bryant HU, Bernton EW, Holaday JW (1987) Immunosuppressive effects of chronic morphine treatment in mice. Life Sci 41:1731–1738

    PubMed  CAS  Google Scholar 

  • Bryant HU, Bernton EW, Kenner JR, Holaday JW (1991) Role of adrenal cortical activation in the immunosuppressive effects of chronic morphine treatment. Endocrinology 128:3253–3258

    PubMed  CAS  Google Scholar 

  • Calderon SN, Rothman RB, Porreca F, Flippen-Anderson JL, McNutt RW, Xu H, Smith, LE, Bilsky EJ, Davis P, Rice KC (1994) Probes for narcotic receptor mediated phenomena. 19. Synthesis of (+)-4-[(alpha R)-alpha-((2S,5R)-4-allyl-2,5-dimethyl-1-piperazinyl)-3-methoxybenzyl]-N,N-diethylbenzamide (SNC 80): a highly selective, nonpeptide delta opioid receptor agonist. J Med Chem 37:2125–2128

    PubMed  CAS  Google Scholar 

  • Caroleo MC, Arbitrio M, Melchiorri D, Nistico G (1994) A reappraisal of the role of the various opioid receptor subtypes in cell-mediated immunity. Neuroimmunomodulation 1:141–147

    PubMed  CAS  Google Scholar 

  • Carr DJJ, DeCosta BR, Kim C-H, Jacobson AE, Guarcello V, Rice KC, Blalock JE (1989) Opioid receptors on cells of the immune system: evidence for δ- and κ-classes. J Endocrinol 122:161–168

    Article  PubMed  CAS  Google Scholar 

  • Carrigan KA, Saurer TB, Ijames SG, Lysle DT (2004) Buprenorphine produces naltrexone reversible alterations of immune status. Int Immunopharmacol 4:419–428

    PubMed  CAS  Google Scholar 

  • Chang SL, Moldow RL, House SD, Zadina JE (1996) Morphine affects the brain-immune axis by modulating an interleukin-1 beta dependent pathway. Adv Exp Med Biol 402:35–42

    PubMed  CAS  Google Scholar 

  • Chao CC, Sharp BM, Pomeroy C, Filice GA, Peterson PK (1990) Lethality of morphine in mice infected with Toxoplasma gondii. J Pharmacol Exp Ther 252:605–609

    PubMed  CAS  Google Scholar 

  • Chao CC, Gekker G, Hu S, Sheng WS, Portoghese PS, Peterson PK (1995) Upregulation of HIV-1 expression in co-cultures of chronically infected promonocytes and human brain cells by dynorphin. Biochem Pharmacol 50:715–722

    PubMed  CAS  Google Scholar 

  • Chao CC, Gekker G, Hu S, Sheng WS, Bu D-F, Archer S, Bidlack JM, Peterson PK (1996) Kappa opioid receptors in human microglia downregulate human immunodeficiency virus-1 expression. Proc Natl Acad Sci USA 93:8051–8056

    PubMed  CAS  Google Scholar 

  • Chen Y, Mestek A, Liu J, Hurley JA, Yu L (1993) Molecular cloning and functional expression of a mu-opioid receptor from rat brain. Mol Pharmacol 44:8–12

    PubMed  CAS  Google Scholar 

  • Chen C, Li J, Bot G, Szabo I, Rogers TJ, Liu-Chen L-Y (2004) Heterodimerization and cross-desensitization between the mu-opioid receptor and the chemokine CCR5 receptor. Eur J Pharmacol 483:175–186

    PubMed  CAS  Google Scholar 

  • Chuang LF, Chuang TK, Killam KF Jr, Chuang AJ, Kung H, Yu L, Chuang RY (1994) Delta opioid receptor gene expression in lymphocytes. Biochem Biophys Res Commun 202:1291–1299

    PubMed  CAS  Google Scholar 

  • Chuang LF, Chuang TK, Killam KF Jr, Qui Q, Wang XR, Lin JJ, Kung HF, Sheng W, Chao C, Yu L, Chuang RY (1995a) Expression of kappa opioid receptors in human and monkey lymphocytes. Biochem Biophys Res Commun 209:1003–1010

    CAS  Google Scholar 

  • Chuang TK, Killam KF Jr, Chuang LF, Kung HF, Sheng WS, Chao CC, Yu L, Chuang RY (1995b) Mu opioid receptor gene expression in immune cells. Biochem Biophys Res Commun 216:922–930

    CAS  Google Scholar 

  • Eisenstein TK, Hilburger ME (1998) Opioid modulation of immune responses: effects on phagocyte and lymphoid cell populations. J Neuroimmumol 83:36–44

    CAS  Google Scholar 

  • Evans CJ, Keith DE Jr, Morrison H, Magendzo K, Edwards RH (1992) Cloning of a delta opioid receptor by functional expression. Science 258:1952–1955

    PubMed  CAS  Google Scholar 

  • Fecho K, Dykstra LA, Lysle DT (1993) Evidence for β-adrenergic receptor involvement in the immunomodulatory effects of morphine. J Pharmacol Exp Ther 265:1079–1087

    PubMed  CAS  Google Scholar 

  • Fiorica E, Spector S (1988) Opioid binding site in EL-4 thymoma cell line. Life Sci 42:199–206

    PubMed  CAS  Google Scholar 

  • Foris G, Medgyesi GA, Nagy JT, Varga Z (1987) Concentration-dependent effect of met-enkephalin on human polymorphonuclear leukocytes. Ann NY Acad Sci 496:51–157

    Google Scholar 

  • Foster JS, Moore RN (1987) Dynorphin and related opioid peptides enhance tumoricidal activity mediated by murine peritoneal macrophages. J Leuk Biol 42:171–174

    CAS  Google Scholar 

  • Gavériaux C, Peluso J, Simonin F, LaForet J, Kieffer B (1995) Identification of kappa- and delta-opioid receptor transcripts in immune cells. FEBS Lett 369:272–276

    PubMed  Google Scholar 

  • Gavériaux-Ruff C, Peluso J, Befort K, Simonin F, Zilliox C, Kieffer BL (1997) Detection of opioid receptor mRNA by RT-PCR reveals alternative splicing for the delta- and kappa-opioid receptors. Mol Brain Res 48:298–304

    PubMed  Google Scholar 

  • Gavériaux-Ruff C, Simonin, F, Filliol, D, Kieffer BL (2003) Enhanced humoral response in kappa-opioid receptor knockout mice. J Neuroimmunol 134:72–81

    PubMed  Google Scholar 

  • Guan L, Townsend R, Eisenstein TK, Adler MW, Rogers TK (1994) Both T-cells and macrophages are target of κ-opioid-induced immunosuppression. Brain Behav Immun 8:229–240

    PubMed  CAS  Google Scholar 

  • Guan L, Eisenstein TK, Adler MW, Rogers TJ (1997) Inhibition of T cell superantigen responses following treatment with the kappa-opioid agonist U50,488H. J Neuroimmunol 75:163–168

    PubMed  CAS  Google Scholar 

  • Gulya K, Liu GK, Pelton JT, Kazmierski W, Hruby VJ, Yamamura HI. (1986) H-d-Phe-Cys-Tyr-d-Trp-Orn-Thr-Pen-Thr-NH2: a potent and selective antagonist opioid receptors. NIDA Res Monogr 75:209–212

    PubMed  CAS  Google Scholar 

  • Gungor M, Genc E, Sogduyu H, Eroglu L, Koyuncuoglu H (1980) Effect of chronic administration of morphine on primary immune response in mice. Experientia 36:1309–1310

    PubMed  CAS  Google Scholar 

  • Gunji N, Nagashima M, Asano G, Yoshino S (2000) Expression of kappa-opioid receptor mRNA in human peripheral blood lymphocytes and the relationship between its expression and the inflammatory changes in rheumatoid arthritis. Rheumatol Int 19:95–100

    PubMed  CAS  Google Scholar 

  • Hagi K, Uno K, Inaba K, Muramatsu S (1994) Augmenting effect of opioid peptides on murine macrophage activation. J Neuroimmunol 50:71–76

    PubMed  CAS  Google Scholar 

  • Heagy W, Laurance M, Cohen E, Finberg R (1990) Neurohormones regulate T-cell function. J Exp Med 171:1625–1633

    PubMed  CAS  Google Scholar 

  • Ignatowski TA, Bidlack JM (1998) Detection of kappa opioid receptors on mouse thymocyte phenotypic subpopulations as assessed by flow cytometry. J Pharmacol Exp Ther 284:298–306

    PubMed  CAS  Google Scholar 

  • Ignatowski TA, Bidlack JM (1999) Differential κ-opioid receptor expression on mouse lymphocytes at varying stages of maturation and on mouse macrophages after selective elicitation. J Pharmacol Exp Ther 290:863–870

    PubMed  CAS  Google Scholar 

  • Khimich M, Bidlack JM (2005) Kappa-opioid induced IL-7 receptor mRNA expression in R1.1 thymoma cell line. Society on NeuroImmune Pharmacology Meeting, Clearwater Beach, Florida, April 6–9, 2005

  • Klein TW, Cabral GA (2006) Cannabinoid-induced immune suppression and modulation of antigen-presenting cells. J Neuroimmune Pharmacol 1:50–64

    PubMed  Google Scholar 

  • Lawrence DMP, Bidlack JM (1992) Kappa opioid binding sites on the R1.1 murine lymphoma cell line: sensitivity to cations and guanine nucleotides. J Neuroimmunol 41:223–230

    PubMed  CAS  Google Scholar 

  • Lawrence DMP, Bidlack JM (1993) 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 protein. J Pharmacol Exp Ther 266:1678–1683

    PubMed  CAS  Google Scholar 

  • Lawrence DMP, El-Hamouly W, Archer S, Leary JF, Bidlack JM (1995a) Identification of κ opioid receptors in the immune system by indirect immunofluorescence. Proc Natl Acad Sci USA 92:1062–1066

    PubMed  CAS  Google Scholar 

  • Lawrence DMP, Joseph DB, Bidlack JM (1995b) Kappa opioid receptors expressed on three related thymoma cell lines. Differences in receptor–effector coupling. Biochem Pharmacol 49:81–89

    PubMed  CAS  Google Scholar 

  • Lefkowiz SS, Chiang CY (1975) Effects of certain abused drugs on hemolysin forming cells. Life Sci 17:1763–1768

    Google Scholar 

  • Lewis JW (1995). Clinical pharmacology of buprenorphine in relation to its use as an analgesic. In: Cowan A, Lewis JW (eds) Buprenorphine: combating drug abuse with a unique opioid. Wiley-Liss, New York, pp 151–163

    Google Scholar 

  • Li S, Zhu J, Chen C, Chen Y-W, DeRiel JK, Ashby B, Liu-Chen L-Y (1993) Molecular cloning and expression of a rat kappa opioid receptor. Biochem J 295:629–633

    PubMed  CAS  Google Scholar 

  • Li MD, McAllen K, Sharp BM (1999) Regulation of delta opioid receptor expression by anti-CD3-ɛ, PMA, and ionomycin in murine splenocytes and T cells. J Leukoc Biol 65:707–714

    PubMed  CAS  Google Scholar 

  • Linner KM, Beyer HS, Sharp BM (1991) Induction of the messenger ribonucleic acid for proenkephalin A in cultured murine CD4-positive thymocytes. Endocrinology 128:717–724

    PubMed  CAS  Google Scholar 

  • Linner KM, Quist HE, Sharp BM (1995) Met-enkephalin-containing peptides encoded by proenkephalin A mRNA expressed in activated murine thymocytes inhibit thymocyte proliferation. J Immunol 154:5049–5060

    PubMed  CAS  Google Scholar 

  • Mack KJ, Lee MF, Weyhenmeyer JA (1985) Effects of guanyl nucleotides and ions on kappa opioid binding. Brain Res Bull 14:301–306

    PubMed  CAS  Google Scholar 

  • Madden JJ, Whaley WL, Ketelsen D (1998) Opiate binding sites in the cellular immune system: expression and regulation. J Neuroimmunol 83:57–62

    PubMed  CAS  Google Scholar 

  • Makman MH, Dvorkin B, Stefano GB (1995) Murine macrophage cell lines contain μ3-opiate receptors. Eur J Pharmacol 273:5–6

    Google Scholar 

  • McCarthy LE, Nitsche JF, Pintar JE, Rogers TJ (2004) The delta-opioid receptor participates in T-cell development by promoting negative selection. J Neuroimmunol 153:91–98

    PubMed  CAS  Google Scholar 

  • Mestas J, Hughes CCW (2004) Of mice and not men: differences between mouse and human immunology. J Immunol 172:2731–2738

    PubMed  CAS  Google Scholar 

  • Meunier JC, Mollereau C, Toll L, Suaudeau C, Moisand C, Alvinerie P, Butour JL, Guillemot JC, Ferrara P, Monsarrat B et al. (1995) Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 377:532–535

    PubMed  CAS  Google Scholar 

  • Miller B (1996) Delta opioid receptor expression is induced by concanavalin A in CD4+ T cells. J Immunol 157:5324–5328

    PubMed  CAS  Google Scholar 

  • Negus SS, Dykstra LA (1988) Kappa antagonist properties of buprenorphine in the shock titration procedure. Eur J Pharmacol 56:77–86

    Google Scholar 

  • Negus SS, Bidlack JM, Mello NK, Furness MK, Rice KC, Brandt MR (2002) Delta opioid antagonist effects of buprenorphine in rhesus monkeys. Behav Pharmacol 13:557–570

    PubMed  CAS  Google Scholar 

  • Parkhill AL, Bidlack JM (2002) Several δ-opioid receptor ligands display no subtype selectivity to human δ-opioid receptor. Eur J Pharmacol 451:257–264

    Google Scholar 

  • Parkhill AL, Bidlack JM (2006) Reduction of lipopolysaccharide-induced interleukin-6 production by the kappa opioid U50, 488 in a mouse monocyte-like cell line. Int Immunopharmacol 6:1013–1019

    PubMed  CAS  Google Scholar 

  • Paterson SJ, Robson LE, Kosterlitz HW (1986) Control by cations of opioid binding in guinea pig brain membranes. Proc Natl Acad Sci USA 83:6216–6220

    PubMed  CAS  Google Scholar 

  • Pello OM, Duthey B, Garcia-Bernal D, Rodriguez-Frade JM, Stein JV, Teixido J, Martinez AC, Mellado M (2006) Opioids trigger α5β1 integrin-mediated monocyte adhesion. J Immunol 176:1675–1685

    PubMed  CAS  Google Scholar 

  • Peluso J, Gaveriaux-Ruff C, Matthes HW, Filliol D, Kieffer BL (2001) Orphanin FQ/nociceptin binds to functionally coupled ORL1 receptors on human immune cell lines and alters peripheral blood mononuclear cell proliferation. Brain Res Bull 54:655–660

    PubMed  CAS  Google Scholar 

  • Peterson PK, Molitor TW, Chao CC (1998) The opioid–cytokine connection. J Neuroimmunol 83:63–69

    PubMed  CAS  Google Scholar 

  • Portoghese PS, Larson DL, Sayre LM, Fries DS, Takemori AE (1980) A novel opioid receptor site directed alkylating agent with irreversible narcotic antagonistic and reversible agonistic activities. J Med Chem 23:233–234

    PubMed  CAS  Google Scholar 

  • Portoghese PS, Lipkowski AW, Takemori AE (1987) Binaltorphimine and nor-binaltorphimine, potent and selective kappa-opioid receptor antagonists. Life Sci 40:1287–1292

    PubMed  CAS  Google Scholar 

  • Portoghese PS, Sultana M, Takemori AE (1988) Naltrindole, a highly selective and potent non-peptide delta opioid receptor antagonist. Eur J Pharmacol 146:185–186

    PubMed  CAS  Google Scholar 

  • Rios C, Gomes I, Devi LA (2006) Mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br J Pharmacol (in press)

  • Roy S, Ge BL, Ramakrishan S, Lee NM, Loh HH (1991) [3H]-Morphine binding to thymocytes is enhanced by IL-1 stimulation. FEBS Lett 287:93–96

    PubMed  CAS  Google Scholar 

  • Roy S, Sedqi M, Ramakrishnan S, Barke RA, Loh HH (1996) Differenctial effects of opioids on the proliferation of a macrophage cell line. Cell Immunol 169:271–277

    PubMed  CAS  Google Scholar 

  • Royal W, III, Leander MV, Bissonnett R (2005) Retinoid-induced mu opioid receptor expression by phytohemagglutinin-stimulated U937 cells. J Neurovirol 11:157–165

    PubMed  CAS  Google Scholar 

  • Sedqi M, Roy S, Ramakrishnan S, Elde R, Loh HH (1995) Complementary DNA cloning of a μ-opioid receptor from rat peritoneal macrophages. Biochem Biophys Res Commun 209:563–574

    PubMed  CAS  Google Scholar 

  • Shavit Y, Lewis JW, Terman GW, Gale RP, Liebeskind JC (1984) Opioid peptides mediate the suppressive effect of stress on natural killer cell cytotoxicity. Science 223:188–190

    Google Scholar 

  • Shahabi NA, Sharp BM (1995) Antiproliferative effects of delta opioids on highly purified CD4(+) and CD8(+) murine T cells. J Pharmacol Exp Ther 273:1105–1113

    PubMed  CAS  Google Scholar 

  • Shahabi NA, McAllen K, Sharp BM (2003) Phosphorylation of activating transcription factor in murine splenocytes through delta opioid receptors. Cell Immunol 221:122–127

    PubMed  CAS  Google Scholar 

  • Sharp BM (2003) In: Machelska H, Stein Ch (eds) Immune mechanisms of pain and analgesia. Plenum Publishers, New York

    Google Scholar 

  • Sharp BM (2006) Multiple opioid receptors on immune cells modulate intracellular signaling. Brain Behav Immun 20:9–14

    PubMed  CAS  Google Scholar 

  • Sharp BM, Keane WF, Suh HJ, Gekker G, Tsukayama D, Peterson PK (1985) Opioid peptides rapidly stimulate superoxide production by human polymorphonuclear leukocytes and macrophages. Endocrinology 117:793–795

    Article  PubMed  CAS  Google Scholar 

  • Sharp BM, Roy S, Bidlack JM (1998) Evidence for opioid receptors on cells involved in host defense and the immune system. J Neuroimmunol 83:45–56

    PubMed  CAS  Google Scholar 

  • Sharp BM, Shahabi N, McKean D, Li MD, McAllen K (1997) Detection of basal levels and induction of delta opioid receptor mRNA in murine splenocytes. J Neuroimmunol 78:198–202

    PubMed  CAS  Google Scholar 

  • Sibinga NES, Goldstein A (1988) Opioid peptides and opioid receptors in cells of the immune system. Annu Rev Immunol 6:219–249

    PubMed  CAS  Google Scholar 

  • Stefano GB, Cadet P, Scharrer B (1989) 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 86:6307–6311

    PubMed  CAS  Google Scholar 

  • Stefano GB, Melchiorri P, Negri L, Hughes TK Jr, Scharrer B (1992) [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 89:9316–9320

    PubMed  CAS  Google Scholar 

  • Sumagin S, Bidlack JM (2005) Delta opioid receptor mRNA expressed in BV-2, a mouse microglial cell line. Society on NeuroImmune Pharmacology Meeting, Clearwater Beach, Florida, April 6–9, 2005

  • Tosk JM, Grim JR, Kinback KM, Sale EJ, Bozetti LP, Will AD (1993) Modulation of chemiluminescence in a murine macrophage cell line by neuroendocrine hormones. Int J Immunopharmacol 15:615–620

    PubMed  CAS  Google Scholar 

  • Tubaro E, Borelli G, Croce C, Cavallo G, Santiangeli C (1983) Effect of morphine on resistance to infection. J Infect Dis 148:656–666

    PubMed  CAS  Google Scholar 

  • VanEpps DE, Saland L (1984) β-Endorphin and met-enkephalin stimulate human peripheral blood mononuclear cell chemotaxis. J Immunol 132:3046–3053

    CAS  Google Scholar 

  • Weber RJ, Pert A (1989) The periaqueductal gray matter mediates opiate-induced immunosuppression. Science 245:188–190

    PubMed  CAS  Google Scholar 

  • Wei E, Lei P, Liu X, Qian C, Li H, Xia W, Li G (2005) The potential promoter regions on the 5′ flank sequence of the mu opioid receptor gene in lymphocytes. J Cell Biochem 95:1204–1213

    PubMed  CAS  Google Scholar 

  • Wetzel MA, Steele AD, Eisenstein TK, Adler MW, Henderson EE, Rogers TJ (2000) Mu-opioid induction of monocyte chemoattractant protein-1, RANTES, and IFN-gamma-inducible protein-10 expression in human peripheral blood mononuclear cells. J Immunol 165:6519–6524

    PubMed  CAS  Google Scholar 

  • Wick MJ, Minnerath SR, Roy S, Ramakrishnan S, Loh HH (1995) Expression of alternate forms of brain opioid orphan receptor mRNA in activated human peripheral blood lymphocytes and lymphocytic cell lines. Mol Brain Res 32:342–347

    PubMed  CAS  Google Scholar 

  • Yasuda K, Raynor K, Kong H, Breder CD, Takeda J, Reisine T, Bell GI (1993) Cloning and functional comparison of κ and δ opioid receptors from mouse brain. Proc Natl Acad Sci USA 90:6736–6740

    PubMed  CAS  Google Scholar 

  • Zadina JE, Hackler L, Ge LJ, Kastin AJ (1997) A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386:499–502

    PubMed  CAS  Google Scholar 

  • Zhang L, Rogers TJ (2000) Kappa-opioid regulation of thymocyte IL-7 receptor and C–C chemokine receptor 2 expression. J Immunol 164:5088–5093

    PubMed  CAS  Google Scholar 

  • Zhang N, Oppenheim JJ (2005) Crosstalk between chemokines and neuronal receptors bridges immune and nervous systems. J Leukocyte Biol 78:1210–1214

    PubMed  CAS  Google Scholar 

  • Zhang N, Rogers TJ, Caterina M, Oppenheim JJ (2004) Proinflammatory chemokines, such as C–C chemokine ligand 3, desensitize mu-opioid receptors on dorsal root ganglia neurons. J Immunol 173:595–599

    Google Scholar 

  • Zhu J, Chen C, Xue JC, Kunapuli S, DeRiel JK, Liu-Chen L-Y (1995) Cloning of a human kappa opioid receptor from the brain. Life Sci 56:201–207

    Google Scholar 

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This work was supported by grants K05-DA00360 and DA04355.

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  1. Department of Pharmacology and Physiology, School of Medicine and Dentistry, University of Rochester, P.O. Box 711, 601 Elmwood Ave., Rochester, NY, 14642-8711, USA

    Jean M. Bidlack, Maxim Khimich, Amy L. Parkhill, Sarah Sumagin, Baoyong Sun & Christopher M. Tipton

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  1. Jean M. Bidlack
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Bidlack, J.M., Khimich, M., Parkhill, A.L. et al. Opioid Receptors and Signaling on Cells from the Immune System. Jrnl Neuroimmune Pharm 1, 260–269 (2006). https://doi.org/10.1007/s11481-006-9026-2

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