Role of the mu-opioid receptor in opioid modulation of immune function

Amino Acids

Volumn 45, Issue 1, 2013, Pages 9-24

  Ninković, Jana ^a   Roy, Sabita ^b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Immunosuppression; Morphine; Opioid; Opioid receptors

Indexed keywords

BETA ENDORPHIN; BUPRENORPHINE; DEXTROPROPOXYPHENE; ENDORPHIN; ENKEPHALIN; FENTANYL; GAMMA INTERFERON; HYDROMORPHONE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 8; METHADONE; MORPHINE; MORPHINE 3 GLUCURONIDE; MU OPIATE RECEPTOR; NALOXONE; NALTREXONE; OPIATE; OPIATE RECEPTOR; PETHIDINE; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ADDICTION; ANALGESIC ACTIVITY; ANTIBODY RESPONSE; ANTIMICROBIAL ACTIVITY; APOPTOSIS; B LYMPHOCYTE; BACTERIAL LOAD; BINDING AFFINITY; BINDING SITE; CANCER PAIN; CANDIDA ALBICANS; CELL FUNCTION; CELL PROLIFERATION; CELL VIABILITY; CHEMOTAXIS; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG ABUSE; DRUG MECHANISM; HEROIN DEPENDENCE; HIGH RISK BEHAVIOR; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFECTION SENSITIVITY; INNATE IMMUNITY; LIGAND BINDING; LYMPHOCYTE PROLIFERATION; MACROPHAGE; NEUROTRANSMISSION; NONHUMAN; PAIN; PHAGOCYTOSIS; POSTOPERATIVE PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; STREPTOCOCCUS PNEUMONIA; T LYMPHOCYTE;

ANALGESICS, OPIOID; ANIMALS; BINDING SITES; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; IMMUNOMODULATION; LEUKOCYTES, MONONUCLEAR; MORPHINE; OPIOID PEPTIDES; PAIN; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION;

EID: 84879238439     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-011-1163-0     Document Type: Review

References (141)

1. Aherne GW, Piall EM, Twycross RG (1979) Serum morphine concentration after oral administration of diamorphine hydrochloride and morphine sulphate. Br J Clin Pharmacol 8:577-580
2. Akil H, Watson SJ, Young E, Lewis ME, Khachaturian H, Walker JM (1984) Endogenous opioids: biology and function. Annu Rev Neurosci 7:223-255
3. Andersen YS, Gillin FD, Eckmann L (2006) Adaptive immunity-dependent intestinal hypermotility contributes to host defense against Giardia spp. Infect Immun 74:2473-2476
4. Antonijevic I, Mousa SA, Schafer M, Stein C (1995) Perineurial defect and peripheral opioid analgesia in inflammation. J Neurosci 15:165-172
5. Asakura H, Kawamoto K, Igimi S, Yamamoto S, Makino S (2006) Enhancement of mice susceptibility to infection with Listeria monocytogenes by the treatment of morphine. Microbiol Immunol 50:543-547
6. Bhargava HN, Thomas PT, Thorat S, House RV (1994) Effects of morphine tolerance and abstinence on cellular immune function. Brain Res 642:1-10
7. Bhaskaran M, Kapasi AA, Reddy K, Singhal PC (2007) Morphine priming rescues high-dose morphine-induced biological perturbations. J Infect Dis 195:1860-1869
8. Bhaskaran M, Reddy K, Sharma S, Singh J, Radhakrishnan N, Kapasi A, Singhal PC (2001) Morphine-induced degradation of the host defense barrier: role of macrophage injury. J Infect Dis 184:1524-1531
9. Bidlack JM, Khimich M, Parkhill AL, Sumagin S, Sun B, Tipton CM (2006) Opioid receptors and signaling on cells from the immune system. J Neuroimmune Pharmacol 1:260-269
10. Bloch B, Bugnon C, Fellman D, Lenys D (1978) Immunocytochemical evidence that the same neurons in the human infundibular nucleus are stained with anti-endorphins and antisera of other related peptides. Neurosci Lett 10:147-152
11. Bloom F, Battenberg E, Rossier J, Ling N, Leppaluoto J, Vargo TM, Guillemin R (1977) Endorphins are located in the intermediate and anterior lobes of the pituitary gland, not in the neurohypophysis. Life Sci 20:43-47
12. Borner C, Kraus J, Bedini A, Schraven B, Hollt V (2008) T-cell receptor/CD28-mediated activation of human T lymphocytes induces expression of functional mu-opioid receptors. Mol Pharmacol 74:496-504
13. Brack A, Rittner HL, Stein C (2011) Immunosuppressive effects of opioids-clinical relevance. J Neuroimmune Pharmacol 6:490-502
14. Bryant HU, Bernton EW, Holaday JW (1988a) Morphine pellet-induced immunomodulation in mice: temporal relationships. J Pharmacol Exp Ther 245:913-920
15. Bryant HU, Yoburn BC, Inturrisi CE, Bernton EW, Holaday JW (1988b) Morphine-induced immunomodulation is not related to serum morphine concentrations. Eur J Pharmacol 149:165-169
16. 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
17. Bunzow JR, Saez C, Mortrud M, Bouvier C, Williams JT, Low M, Grandy DK (1994) Molecular cloning and tissue distribution of a putative member of the rat opioid receptor gene family that is not a mu, delta or kappa opioid receptor type. FEBS Lett 347:284-288
18. Bussiere JL, Adler MW, Rogers TJ, Eisenstein TK (1993) Cytokine reversal of morphine-induced suppression of the antibody response. J Pharmacol Exp Ther 264:591-597
19. Bussiere JL, Adler MW, Rogers TJ, Eisenstein TK (1992) Differential effects of morphine and naltrexone on the antibody response in various mouse strains. Immunopharmacol Immunotoxicol 14:657-673
20. Cabot PJ, Carter L, Gaiddon C, Zhang Q, Schafer M, Loeffler JP, Stein C (1997) Immune cell-derived beta-endorphin. Production, release, and control of inflammatory pain in rats. J Clin Invest 100:142-148
21. Cabral GA (2006) Drugs of abuse, immune modulation, and AIDS. J Neuroimmune Pharmacol 1:280-295
22. Carr DJJ, DeCosta BR, Jacobson AE, Rice KC, Edwin Blalock J (1991) Enantioselective kappa opioid binding sites on the macrophage cell line, P388d1. Life Sci 49:45-51
23. Casellas AM, Guardiola H, Renaud FL (1991) Inhibition by opioids of phagocytosis in peritoneal macrophages. Neuropeptides 18:35-40
24. Chao CC, Gekker G, Hu S, Sheng WS, Shark KB, Bu DF, 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
25. Choi HS, Kim CS, Hwang CK, Song KY, Wang W, Qiu Y, Law PY, Wei LN, Loh HH (2006) The opioid ligand binding of human mu-opioid receptor is modulated by novel splice variants of the receptor. Biochem Biophys Res Commun 343:1132-1140
26. Chuang TK, Killam KF, Chuang LF, Kung HF, Sheng WS, Chao CC, Yu L, Chuang RY (1995) Mu Opioid Receptor Gene Expression in Immune Cells. Biochem Biophys Res Commun 216:922-930
27. Compton WM, Volkow ND (2006) Abuse of prescription drugs and the risk of addiction. Drug Alcohol Depend 83(Suppl 1):S4-S7
28. Dahan A, van Dorp E, Smith T, Yassen A (2008) Morphine-6-glucuronide (M6G) for postoperative pain relief. Eur J Pain 12:403-411
29. Eisenstein TK, Hilburger ME (1998) Opioid modulation of immune responses: effects on phagocyte and lymphoid cell populations. J Neuroimmunol 83:36-44
30. Elde R, Hokfelt T, Johansson O, Terenius L (1976) Immunohistochemical studies using antibodies to leucine-enkephalin: initial observations on the nervous system of the rat. Neuroscience 1:349-351
31. Evans CJ (2004) Secrets of the opium poppy revealed. Neuropharmacology 47(Suppl 1):293-299
32. Falke NE, Fischer EG, Martin R (1985) Stereospecific opiate binding in living human polymorphonuclear leucocytes. Cell Biol Int Rep 9:1041-1047
33. Gaveriaux 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
34. Gaveriaux-Ruff C, Matthes HW, Peluso J, Kieffer BL (1998) Abolition of morphine-immunosuppression in mice lacking the mu-opioid receptor gene. Proc Natl Acad Sci USA 95:6326-6330
35. Glaum SR, Miller RJ, Hammond DL (1994) Inhibitory actions of delta 1-, delta 2-, and mu-opioid receptor agonists on excitatory transmission in lamina II neurons of adult rat spinal cord. J Neurosci 14:4965-4971
36. Goodsell DS (2005) The molecular perspective: morphine. Stem Cells 23:144-145
37. Grimm MC, Ben-Baruch A, Taub DD, Howard OM, Resau JH, Wang JM, Ali H, Richardson R, Snyderman R, Oppenheim JJ (1998a) Opiates transdeactivate chemokine receptors: delta and mu opiate receptor-mediated heterologous desensitization. J Exp Med 188:317-325
38. Grimm MC, Ben-Baruch A, Taub DD, Howard OM, Wang JM, Oppenheim JJ (1998b) Opiate inhibition of chemokine-induced chemotaxis. Ann N Y Acad Sci 840:9-20
39. Gylbert L (1973). The crystal and molecular structure of morphine hydrochloride trihydrate. Acta Crystallographica Section B 29(8):1630-1635
40. Hanner M, Moebius FF, Flandorfer A, Knaus HG, Striessnig J, Kempner E, Glossmann H (1996) Purification, molecular cloning, and expression of the mammalian sigma1-binding site. Proc Natl Acad Sci USA 93:8072-8077
41. Haverkos HW, Lange WR (1990) From the alcohol, drug abuse, and mental health administration. Serious infections other than human immunodeficiency virus among intravenous drug abusers. J Infect Dis 161:894-902
42. Hilburger ME, Adler MW, Truant AL, Meissler JJ Jr, Satishchandran V, Rogers TJ, Eisenstein TK (1997) Morphine induces sepsis in mice. J Infect Dis 176:183-188
43. Hokfelt T, Elde R, Johansson O, Terenius L, Stein L (1977) The distribution of enkephalin-immunoreactive cell bodies in the rat central nervous system. Neurosci Lett 5:25-31
44. Horsburgh CR Jr, Anderson JR, Boyko EJ (1989) Increased incidence of infections in intravenous drug users. Infect Control Hosp Epidemiol 10:211-215
45. HUSSEY HH, KATZ S (1950) Infections resulting from narcotic addiction; report of 102 cases. Am J Med 9:186-193
46. 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
47. Inturrisi CE (2002) Clinical pharmacology of opioids for pain. Clin J Pain 18:S3-S13
48. Jacobowitz DM, O'Donohue TL (1978) alpha-Melanocyte stimulating hormone: immunohistochemical identification and mapping in neurons of rat brain. Proc Natl Acad Sci USA 75:6300-6304
49. Ji RR, Zhang Q, Law PY, Low HH, Elde R, Hokfelt T (1995) Expression of mu-, delta-, and kappa-opioid receptor-like immunoreactivities in rat dorsal root ganglia after carrageenan-induced inflammation. J Neurosci 15:8156-8166
50. Joe GW, Knezek L, Watson D, Simpson DD (1991) Depression and decision-making among intravenous drug users. Psychol Rep 68:339-347
51. Khachaturian H, Lewis ME, Watson SJ (1982a) Immunocytochemical studies with antisera against leu-enkephalin and an enkephalin-precursor fragment (BAM-22P) in the rat brain. Life Sci 31:1879-1882
52. Khachaturian H, Watson SJ, Lewis ME, Coy D, Goldstein A, Akil H (1982b) Dynorphin immunocytochemistry in the rat central nervous system. Peptides 3:941-954
53. Kirst A, Wack C, Lutz WK, Eggert A, Kämpgen E, Fischer WH (2002) Expression of functional κ-opioid receptors on murine dendritic cells. Immunol Lett 84:41-48
54. Kohno T, Kumamoto E, Higashi H, Shimoji K, Yoshimura M (1999) Actions of opioids on excitatory and inhibitory transmission in substantia gelatinosa of adult rat spinal cord. J Physiol 518(Pt 3):803-813
55. Krieger DT, Liotta A, Brownstein MJ (1977) Presence of corticotropin in limbic system of normal and hypophysectomized rats. Brain Res 128:575-579
56. Kulkarni-Narla A, Walcheck B, Brown DR (2001) Opioid receptors on bone marrow neutrophils modulate chemotaxis and CD11b/CD18 expression. Eur J Pharmacol 414:289-294
57. Lefkowitz DL, Stuart R, Gnade BT, Roberts E, Lefkowitz SS (2000) Effects of a glyconutrient on macrophage functions. Int J Immunopharmacol 22:299-308
58. Liu H, Li H, Guo L, Li M, Li C, Wang S, Jiang W, Liu X, McNutt MA, Li G (2010) Mechanisms involved in phosphatidylinositol 3-kinase pathway mediated up-regulation of the mu opioid receptor in lymphocytes. Biochem Pharmacol 79:516-523
59. Lopker A, Abood LG, Hoss W, Lionetti FJ (1980) Stereoselective muscarinic acetylcholine and opiate receptors in human phagocytic leukocytes. Biochem Pharmacol 29:1361-1365
60. Lord JA, Waterfield AA, Hughes J, Kosterlitz HW (1977) Endogenous opioid peptides: multiple agonists and receptors. Nature 267:495-499
61. Louria DB, Hensle T, Rose J (1967) The major medical complications of heroin addiction. Ann Intern Med 67:1-22
62. Lugo-Chinchilla AM, Baez D, Velez M, Ildefonso C, Renaud FL (2006) Altered subcellular signaling in murine peritoneal macrophages upon chronic morphine exposure. J Neuroimmunol 176:86-94
63. Lustman F, Walters EG, Shroff NE, Akbar FA (1987) Diphenoxylate hydrochloride (Lomotil) in the treatment of acute diarrhoea. Br J Clin Pract 41:648-651
64. Machelska H, Cabot PJ, Mousa SA, Zhang Q, Stein C (1998) Pain control in inflammation governed by selectins. Nat Med 4:1425-1428
65. Machelska H, Mousa SA, Brack A, Schopohl JK, Rittner HL, Schafer M, Stein C (2002) Opioid control of inflammatory pain regulated by intercellular adhesion molecule-1. J Neurosci 22:5588-5596
66. Machelska H (2007) Targeting of opioid-producing leukocytes for pain control. Neuropeptides 41:355-363
67. Makarenkova VP, Esche C, Kost NV, Shurin GV, Rabin BS, Zozulya AA, Shurin MR (2001) Identification of delta- and mu-type opioid receptors on human and murine dendritic cells. J Neuroimmunol 117:68-77
68. Martin JL, Koodie L, Krishnan AG, Charboneau R, Barke RA, Roy S (2010) Chronic morphine administration delays wound healing by inhibiting immune cell recruitment to the wound site. Am J Pathol 176:786-799
69. Martin WR, Eades CG, Thompson JA, Huppler RE, Gilbert PE (1976) The effects of morphine- and nalorphine- like drugs in the nondependent and morphine-dependent chronic spinal dog. J Pharmacol Exp Ther 197:517-532
70. McCoy CB, Metsch LR, Collado-Mesa F, Arheart KL, Messiah SE, Katz D, Shapshak P (2004) The prevalence of human immunodeficiency virus type 1 and hepatitis C virus among injection drug users who use high risk inner-city locales in Miami, Florida. Mem Inst Oswaldo Cruz 99:789-793
71. Menzebach A, Hirsch J, Nost R, Mogk M, Hempelmann G, Welters ID (2004) Morphine inhibits complement receptor expression, phagocytosis and oxidative burst by a nitric oxide dependent mechanism. Anasthesiol Intensivmed Notfallmed Schmerzther 39:204-211
72. Meunier JC, Mollereau C, Toll L, Suaudeau C, Moisand C, Alvinerie P, Butour JL, Guillemot JC, Ferrara P, Monsarrat B (1995) Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 377:532-535
73. Mizoguchi H, Watanabe C, Higashiya T, Takeda S, Moriyama K, Yonezawa A, Sato T, Komatsu T, Sakurada T, Sakurada S (2011) Involvement of mouse mu-opioid receptor splice variants in the spinal antinociception induced by the dermorphin tetrapeptide analog amidino-TAPA. Eur J Pharmacol 651:66-72
74. Mollereau C, Parmentier M, Mailleux P, Butour JL, Moisand C, Chalon P, Caput D, Vassart G, Meunier JC (1994) ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett 341:33-38
75. Monassier L, Bousquet P (2002) Sigma receptors: from discovery to highlights of their implications in the cardiovascular system. Fundam Clin Pharmacol 16:1-8
76. Moon HD, Li CH, Jennings BM (1973) Immunohistochemical and histochemical studies of pituitary beta-lipotrophs. Anat Rec 175:529-537
77. Mousa SA, Shakibaei M, Sitte N, Schafer M, Stein C (2004) Subcellular pathways of beta-endorphin synthesis, processing, and release from immunocytes in inflammatory pain. Endocrinology 145:1331-1341
78. Mousa SA, Zhang Q, Sitte N, Ji R, Stein C (2001) β-Endorphin- containing memory-cells and μ-opioid receptors undergo transport to peripheral inflamed tissue. J Neuroimmunol 115:71-78
79. Nemoto T, Brown LS Jr, Foster K, Chu A (1990) Behavioral risk factors of human immunodeficiency virus infection among intravenous drug users and implications for preventive interventions. AIDS Educ Prev 2:116-126
80. Nestler EJ (2001) Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2:119-128
81. Pacifici R, di Carlo S, Bacosi A, Pichini S, Zuccaro P (2000) Pharmacokinetics and cytokine production in heroin and morphine-treated mice. Int J Immunopharmacol 22:603-614
82. Pan L, Xu J, Yu R, Xu MM, Pan YX, Pasternak GW (2005) Identification and characterization of six new alternatively spliced variants of the human mu opioid receptor gene. Oprm. Neuroscience 133:209-220
83. Pan YX (2005) Diversity and complexity of the mu opioid receptor gene: alternative pre-mRNA splicing and promoters. DNA Cell Biol 24:736-750
84. Pelletier G (1980) Ultrastructural localization of a fragment (16 K) of the common precursor for adrenocorticotropin (ACTH) and beta-lipotropin (beta-LPH) in the rat hypothalamus. Neurosci Lett 16:85-90
85. Pelletier G, Leclerc R, Labrie F, Cote J, Chretien M, Lis M (1977) Immunohistochemical localization of beta-lipotropic hormone in the pituitary gland. Endocrinology 100:770-776
86. Perez-Castrillon JL, Perez-Arellano JL, Garcia-Palomo JD, Jimenez-Lopez A, De Castro S (1992) Opioids depress in vitro human monocyte chemotaxis. Immunopharmacology 23:57-61
87. Peterson PK, Gekker G, Brummitt C, Pentel P, Bullock M, Simpson M, Hitt J, Sharp B (1989) Suppression of human peripheral blood mononuclear cell function by methadone and morphine. J Infect Dis 159:480-487
88. Peterson PK, Molitor TW, Chao CC (1993) Mechanisms of morphine-induced immunomodulation. Biochem Pharmacol 46:343-348
89. Peterson PK, Sharp B, Gekker G, Brummitt C, Keane WF (1987) Opioid-mediated suppression of cultured peripheral blood mononuclear cell respiratory burst activity. J Immunol 138:3907-3912
90. Przewlocki R, Hassan AH, Lason W, Epplen C, Herz A, Stein C (1992) Gene expression and localization of opioid peptides in immune cells of inflamed tissue: functional role in antinociception. Neuroscience 48:491-500
91. Reichman LB, Felton CP, Edsall JR (1979) Drug dependence, a possible new risk factor for tuberculosis disease. Arch Intern Med 139:337-339
92. Rittner HL, Brack A, Machelska H, Mousa SA, Bauer M, Schafer M, Stein C (2001) Opioid peptide-expressing leukocytes: identification, recruitment, and simultaneously increasing inhibition of inflammatory pain. Anesthesiology 95:500-508
93. Rittner HL, Machelska H, Stein C (2005) Leukocytes in the regulation of pain and analgesia. J Leukoc Biol 78:1215-1222
94. Rittner HL, Roewer N, Brack A (2010) The clinical (ir)relevance of opioid-induced immune suppression. Curr Opin Anaesthesiol 23:588-592
95. Rojavin M, Szabo I, Bussiere JL, Rogers TJ, Adler MW, Eisenstein TK (1993) Morphine treatment in vitro or in vivo decreases phagocytic functions of murine macrophages. Life Sci 53:997-1006
96. Roy S, Balasubramanian S, Sumandeep S, Charboneau R, Wang J, Melnyk D, Beilman GJ, Vatassery R, Barke RA (2001) Morphine directs T cells toward T(H2) differentiation. Surgery 130:304-309
97. Roy S, Barke RA, Loh HH (1998a) MU-opioid receptor-knockout mice: role of mu-opioid receptor in morphine mediated immune functions. Brain Res Mol Brain Res 61:190-194
98. Roy S, Cain KJ, Charboneau RG, Barke RA (1998b) Morphine accelerates the progression of sepsis in an experimental sepsis model. Adv Exp Med Biol 437:21-31
99. Roy S, Chapin RB, Cain KJ, Charboneau RG, Ramakrishnan S, Barke RA (1997) Morphine inhibits transcriptional activation of IL-2 in mouse thymocytes. Cell Immunol 179:1-9
100. Roy S, Wang J, Kelschenbach J, Koodie L, Martin J (2006) Modulation of Immune Function by Morphine: Implications for Susceptibility to Infection. JNIP 1:77-89
101. Schafer M, Mousa SA, Zhang Q, Carter L, Stein C (1996) Expression of corticotropin-releasing factor in inflamed tissue is required for intrinsic peripheral opioid analgesia. Proc Natl Acad Sci USA 93:6096-6100
102. Schmitt TK, Mousa SA, Brack A, Schmidt DK, Rittner HL, Welte M, Schafer M, Stein C (2003) Modulation of peripheral endogenous opioid analgesia by central afferent blockade. Anesthesiology 98:195-202
103. Sedqi M, Roy S, Ramakrishnan S, Elde R, Loh HH (1995) Complementary DNA cloning of a mu-opioid receptor from rat peritoneal macrophages. Biochem Biophys Res Commun 209:563-574
104. Sedqi M, Roy S, Ramakrishnan S, Loh HH (1996) Expression cloning of a full-length cDNA encoding delta opioid receptor from mouse thymocytes. J Neuroimmunol 65:167-170
105. 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
106. 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
107. Simpkins CO, Alailima ST, Tate EA, Johnson M (1986) The effect of enkephalins and prostaglandins on O-2 release by neutrophils. J Surg Res 41:645-652
108. Simpkins CO, Dickey CA, Fink MP (1984) Human neutrophil migration is enhanced by beta-endorphin. Life Sci 34:2251-2255
109. Singh PP, Singal P (2007) Morphine-induced neuroimmunomodulation in murine visceral leishmaniasis: the role(s) of cytokines and nitric oxide. J Neuroimmune Pharmacol 2:338-351
110. Spittal PM, Bruneau J, Craib KJ, Miller C, Lamothe F, Weber AE, Li K, Tyndall MW, O'Shaughnessy MV, Schechter MT (2003) Surviving the sex trade: a comparison of HIV risk behaviours among street-involved women in two Canadian cities who inject drugs. AIDS Care 15:187-195
111. Stefano GB, Digenis A, Spector S, Leung MK, Bilfinger TV, Makman MH, Scharrer B, Abumrad NN (1993) Opiate-like substances in an invertebrate, an opiate receptor on invertebrate and human immunocytes, and a role in immunosuppression. Proc Natl Acad Sci USA 90:11099-11103
112. Stein C (1995) The control of pain in peripheral tissue by opioids. N Engl J Med 332:1685-1690
113. Stiene-Martin A, Knapp PE, Martin K, Gurwell JA, Ryan S, Thornton SR, Smith FL, Hauser KF (2001) Opioid system diversity in developing neurons, astroglia, and oligodendroglia in the subventricular zone and striatum: impact on gliogenesis in vivo. Glia 36:78-88
114. Suzuki S, Chuang LF, Yau P, Doi RH, Chuang RY (2002) Interactions of opioid and chemokine receptors: oligomerization of mu, kappa, and delta with CCR5 on immune cells. Exp Cell Res 280:192-200
115. Suzuki S, Chuang LF, Doi RH, Bidlack JM, Chuang RY (2001) Kappa-opioid receptors on lymphocytes of a human lymphocytic cell line: morphine-induced up-regulation as evidenced by competitive RT-PCR and indirect immunofluorescence. Int Immunopharmacol 1:1733-1742
116. Szabo I, Rojavin M, Bussiere JL, Eisenstein TK, Adler MW, Rogers TJ (1993) Suppression of peritoneal macrophage phagocytosis of Candida albicans by opioids. J Pharmacol Exp Ther 267:703-706
117. Tomassini N, Renaud F, Roy S, Loh HH (2004) Morphine inhibits Fc-mediated phagocytosis through mu and delta opioid receptors. J Neuroimmunol 147:131-133
118. Tomei EZ, Renaud FL (1997) Effect of morphine on Fc-mediated phagocytosis by murine macrophages in vitro. J Neuroimmunol 74:111-116
119. Tubaro E, Borelli G, Croce C, Cavallo G, Santiangeli C (1983) Effect of morphine on resistance to infection. J Infect Dis 148:656-666
120. Uhl GR, Kuhar MJ, Synder SH (1978) Enkephalin-containing pathway: amygdaloid efferents in the stria terminalis. Brain Res 149:223-228
121. Vallejo R, de Leon-Casasola O, Benyamin R (2004) Opioid therapy and immunosuppression: a review. Am J Ther 11:354-365
122. van Rijn RM, Whistler JL, Waldhoer M (2010) Opioid-receptor-heteromer- specific trafficking and pharmacology. Curr Opin Pharmacol 10:73-79
123. Waldhoer M, Bartlett SE, Whistler JL (2004) Opioid receptors. Annu Rev Biochem 73:953-990
124. Wang J, Barke RA, Charboneau R, Loh HH, Roy S (2003) Morphine negatively regulates interferon-gamma promoter activity in activated murine T cells through two distinct cyclic AMP-dependent pathways. J Biol Chem 278:37622-37631
125. Wang J, Barke RA, Charboneau R, Roy S (2005) Morphine impairs host innate immune response and increases susceptibility to Streptococcus pneumoniae lung infection. J Immunol 174:426-434
126. Wang J, Barke RA, Ma J, Charboneau R, Roy S (2008) Opiate abuse, innate immunity, and bacterial infectious diseases. Arch Immunol Ther Exp (Warsz) 56:299-309
127. Wang J, Charboneau R, Balasubramanian S, Barke RA, Loh HH, Roy S (2001) Morphine modulates lymph node-derived T lymphocyte function: role of caspase-3, -8, and nitric oxide. J Leukoc Biol 70:527-536
128. Watson SJ, Akil H, Ghazarossian VE, Goldstein A (1981) Dynorphin immunocytochemical localization in brain and peripheral nervous system: preliminary studies. Proc Natl Acad Sci USA 78:1260-1263
129. Weber E, Roth KA, Barchas JD (1982) Immunohistochemical distribution of alpha-neo-endorphin/dynorphin neuronal systems in rat brain: evidence for colocalization. Proc Natl Acad Sci USA 79:3062-3066
130. Weber E, Evans CJ, Barchas JD (1983) Multiple endogenous ligands for opioid receptors. Trends Neurosci 6:333-336
131. Weber RJ, Ikejiri B, Rice KC, Pert A, Hagan AA (1987) Opiate receptor mediated regulation of the immune response in vivo. NIDA Res Monogr 76:341-348
132. Wee, B.; Browning, J.; Adams, A.; Benson, D.; Howard, P.; Klepping, G.; Molassiotis, A.; Taylor, D.; 2011. Management of chronic cough in patients receiving palliative care: review of evidence and recommendations by a task group of the Association for Palliative Medicine of Great Britain and Ireland. Palliat Med 1-8
133. Welters ID, Menzebach A, Goumon Y, Langefeld TW, Teschemacher H, Hempelmann G, Stefano GB (2000) Morphine suppresses complement receptor expression, phagocytosis, and respiratory burst in neutrophils by a nitric oxide and mu(3) opiate receptor-dependent mechanism. J Neuroimmunol 111:139-145
134. Wick MJ, Minnerath SR, Roy S, Ramakrishnan S, Loh HH (1996) Differential expression of opioid receptor genes in human lymphoid cell lines and peripheral blood lymphocytes. J Neuroimmunol 64:29-36
135. Woolf CJ, Salter MW (2000) Neuronal plasticity: increasing the gain in pain. Science 288:1765-1769
136. Woolf CJ, Ma Q (2007) Nociceptors - Noxious Stimulus Detectors. Neuron 55:353-364
137. Wuster M, Schulz R, Herz A (1979) Specificity of opioids towards the mu-, delta- and epsilon-opiate receptors. Neurosci Lett 15:193-198
138. Xu J, Xu M, Rossi GC, Pasternak GW, Pan YX (2011) Identification and characterization of seven new exon 11-associated splice variants of the rat mu opioid receptor gene, OPRM1. Mol Pain 7:9
139. Yoshimura M, North RA (1983) Substantia gelatinosa neurones hyperpolarized in vitro by enkephalin. Nature 305:529-530
140. Zagon IS, Gibo DM, McLaughlin PJ (1991) Zeta (zeta), a growth-related opioid receptor in developing rat cerebellum: identification and characterization. Brain Res 551:28-35
141. Zagon IS, Verderame MF, Allen SS, McLaughlin PJ (2000) Cloning, sequencing, chromosomal location, and function of cDNAs encoding an opioid growth factor receptor (OGFr) in humans. Brain Res 856:75-83