Modulation of immune function by morphine: Implications for susceptibility to infection

Journal of Neuroimmune Pharmacology

Volumn 1, Issue 1, 2006, Pages 77-89

  Roy, Sabita ^a   Wang, Jinghua ^a   Kelschenbach, Jennifer ^a   Koodie, Lisa ^a   Martin, Josephine ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MORPHINE; NARCOTIC AGENT;

ANIMAL; DISEASE PREDISPOSITION; DRUG EFFECT; HUMAN; IMMUNE SYSTEM; IMMUNOLOGY; INFECTION; REVIEW;

ANIMALS; DISEASE SUSCEPTIBILITY; HUMANS; IMMUNE SYSTEM; INFECTION; MORPHINE; NARCOTICS;

EID: 33747480225     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-005-9009-8     Document Type: Review

References (106)

1. Abbas A, Murphy KM, Sher A (1996) Functional diversity of helper T lymphocytes. Nature 383:787-793
2. Alicea C, Belkowski S, Eisenstein TK, Adler MW, Rogers TJ (1996) Inhibition of primary murine macrophage cytokine production in vitro following treatment with the k-opioid agonist U50,488H. J Neuroimmunol 64:83-90
3. Alonzo NC, Bayer BM (2002) Opioids, immunology, and host defenses of intravenous drug abusers. Infect Dis Clin North Am 16(3):553-569 (Sep. Review)
4. Avidor-Reiss T, Bayewitch M, Levy R, Matus-Leibovitch N, Nevo I, Vogel Z (1995) Adenylylcyclase super-sensitization in mu-opioid receptor-transfected Chinese hamster ovary cells following chronic opioid treatment. J Biol Chem 270(50):29732-29738
5. Avidor-Reiss T, Nevo I, Levy R, Pfeuffer T, Vogel Z (1996) Chronic opioid treatment induces adenylyl cyclase V super-activation: involvement of Gbg. J Biol Chem 271(35):21309-21315
6. 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
7. Beagles K, Wellstein A, Bayer B (2004) Systemic morphine administration suppresses genes involved in antigen presentation. Mol Pharmacol 65(2):437-442
8. Bhaskaran M, Reddy K, Sharma S, Singh J, Radhakrishnan N, Kapasi A, Singhal (2001) Morphine-induced degradation of the host defense barrier: role of macrophage injury. J Infect Dis 184(12):1524-1531
9. Bhat RS, Bhaskaran M, Mongia A, Hitosugi N, Singhal PC (2004) Morphine-induced macrophage apoptosis: oxidative stress and strategies for modulation. J Leukoc Biol 75(6):1131-1138
10. Bian TH, Wang XF, Li XY (1995) Effect of morphine on IL-1 and tumor necrosis factor alpha production from mouse peritoneal macrophages in vitro. Chung-Kuo Yao Li Hsueh Pao 16(5):449-451
11. Borner C, Kraus J, Schroder H, Ammer H, Hollt V (2004) Transcriptional regulation of the human mu-opioid receptor gene by interleukin-6. Mol Pharmacol 66(6):1719-1726
12. Bryant HU, Roudebush RE (1990) Suppressive effects of morphine pellet implants on in vivo parameters of immune function. J Pharmacol Exp Ther 255:410-414
13. Bryant HU, Yoburn BC, Intrissi CE, Bernton EW, Holaday JW (1988) Immunosuppressive effects of chronic morphine treatment. Eur J Pharm 149:165-169
14. 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
15. Bussiere JL, Adler MW, Rogers RJ, Eisenstein TK (1993) Cytokine reversal of morphine induced suppression of the Antibody response. J Pharmacol Exp Ther 264:591-597
16. Cantacuzene J (1898) Nouvelles recherches sur le monde de destruction des vibrions dans l'organisme. Ann Inst Pasteur 12:273-300
17. Carr DJ, France CP (1993) Immune alterations in chronic morphine treated rhesus monkeys. Adv Exp Med Biol 335:35-39
18. 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
19. Choi Y, Chuang LF, Lam KM, Kung H-F, Wang JM, Osburn BI, Chuang RY (1999) Inhibition of chemokine-induced chemotaxis of monkey leukocytes by mu-opioid receptor agonist. In Vivo 13:389-396
20. Chuang TK, Killam KF, Chuang LF, Kung H-F, Sheng WS, Chao CC, Yu L, Chuang RY (1995) Mu opioid receptor gene expression in immune cells. Biochem Biophys Res Commun 216:922-930
21. Dinda A, Gitman M, Singhal PC (2005) Immunomodulatory effect of morphine: therapeutic implications. Expert Opin Drug Saf 4(4):669-675
22. 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
23. Fecho K, Maslonek KA, Coussons-Read ME, Dykstra LA, Lysle DT (1994) Macrophage-derived nitric oxide is involved in the depressed con A-responsiveness of splenic lymphocytes from rats administered morphine in vivo. J Immunol 152:5845-5852
24. Fecho K, Maslonek KA, Dykstra LA, Lysle DT (1996) Evidence for sympathetic and adrenal involvement in the immunomodulatory effects of acute morphine treatment in rats. J Pharmacol Exp Ther 277(2):633-645
25. Felten LR, Felten SY, Carlson SL, Olschowka JA, Livnat S (1985) Noradrenergic and peptidergic innervation of lymphoid tissue. J Immunol 135:755-765
26. Flores LR, Hernandez MC, Bayer BM (1994) Acute immunosupressive effects of morphine: lack of involvement of pituitary and adrenal factors. J Pharmacol Exp Ther 268:1129-1134
27. Freier DO, Fuchs BA (1993) Morphine-induced alterations in thymocyte subpopulations of B6C3F1 mice. J Pharmacol Exp Ther 265:81-88
28. Friedman H, Eisenstein TK (2004) Neurological basis of drug dependence and its effects on the immune system. J Neuroimmunol 147(1-2):106-108
29. Georges H, Leroy O, Vandenbussche C, Guery B, Alfandari S, Tronchon L, Beaucaire G (1999) Epidemiological features and prognosis of severe community-acquired pneumococcal pneumonia. Intensive Care Med 25:198,
30. Greeneltch KM, Haudenschild CC, Keegan AD, Shi Y (2004) The opioid antagonist naltrexone blocks acute endotoxic shock by inhibiting tumor necrosis factor-alpha production. Brain Behav Immun 18(5):476-484
31. Grimm MC, Ben-Baruch A, Taub DD, Howard OM, Resau JH, Wang JM, Ali H, Richardson R, Snyderman R, Oppenheim JJ (1998) Opiates transdeactivate chemokine receptors: delta and mu opiate receptor-mediated heterologous desensitization. J Exp Med 188(2):(20)
32. Guo CJ, Li Y, Tian S, Wang X, Douglas SD, Ho WZ (2002) Morphine enhances HIV infection of human blood mononuclear phagocytes through modulation of beta-chemokines and CCR5 receptor. J Investig Med 50(6):435-442
33. Haverkos HW, Lange RW (1990) Serious infections other than human immunodeficiency virus among intravenous drug users. J Infect Dis 161:894-902
34. 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(1):183-188
35. House RV, Thomas PT, Bhargava HN (1995) In vitro evaluation of fentanyl and meperidine for immunomodulatory. Immunol Lett 46(1-2):117-124
36. Hussey HH, Katz S (1950) Infections resulting from narcotic addiction. Am J Med 9:186-193
37. Koff WC, Dunegon MA (1985) Modulation of macrophage-mediated tumoricidal activity by neuropeptides and neurohormones. J Immunol 135:350-354
38. Kowalski J (1998) Immunomodulatory action of class mu-, delta-and kappa-opioid receptor agonists in mice. Neuropeptides 32(4):301-306
39. Kraus J, Borner C, Giannini E, Hickfang K, Braun H, Mayer P, Hoehe MR, Ambrosch A, Konig W, Hollt V (2001) Regulation of μ-opioid receptor gene transcription by interleukin-4 and influence of an allelic variation within a STAT6 transcription factor binding site. J Biol Chem 276:43901-43908
40. Lanier LL (1995) Unusual lymphocytes T cells and NK cells. Immunologist 3:182-184
41. Law PY, Wong YH, Loh HH (2000) Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol 40(1):389,
42. Li Y, Wang X, Tian S, Guo CJ, Douglas SD, Ho WZ (2002) Methadone enhances human immunodeficiency virus infection of human immune cells. J Infect Dis 185(1):118-122
43. Louria DB, Hensle T, Rose J (1974) The major medical complications of heroin addiction. Ann Int Med 67:1-22
44. Lysle DT, Coussons ME, Watts VJ, Bennett EH, Dykstra LA (1993) Morphine-induced alterations of immune status: Dose dependency, compartment specificity and antagonism by naltrexone. J Pharmacol Exp Ther 265:1071-1078
45. Lysle DT, Hoffman KE, Dykstra LA (1996) Evidence for the involvement of the caudal region of the periaqueductal gray in a subset of morphine-induced alterations of immune status. J Pharmacol Exp Ther 277:1533-1540
46. Madden JJ, Donahue RM (1990) In: Watson RR (ed.) Opioid Binding to Cells of the Immune System in Drugs of Abuse and the Immune System. CRC Press, Boca Raton, FL, pp 212-224
47. Makman MH, Dvorkin B, Stefano GB (1995) Murine macrophage cell lines contain m3-opiate receptors. Eur J Pharm 273:5-6
48. McCarthy L, Szabo I, Nitsche JF, Pintar JE, Rogers TJ (2001) Expression of functional mu-opioid receptors during T cell development. J Neuroimmunol 114(1-2):(1)
49. Mehrishi JN, Mills IH (1983) Opiate receptors on lymphocytes and platelets in man. Clin Immunol Immunopathol 27:240-249
50. Mellon RD, Bayer BM (1998) Evidence for central opioid receptors in the immunomodulatory effects of morphine: review of potential mechanism(s) of action. J Neuroimmunol 83(1-2):19-28
51. Mendolsohn L, Kerchner GA, Culwell M, Ades EW (1985) Immunoregulation by opiate peptides. Clin Lab Immunol 16:125-129
52. Miyagi T, Chuang LF, Doi RH, Carlos MP, Torres JV, Chuang RY (2000a) Morphine induces gene expression of CCR5 in human CEM 174 lymphocytes. J Biol Chem 275:31305-31310
53. Miyagi T, Chuang LF, Lam KM, Kung H-F, Wang JM, Osburn BI, Chuang RY (2000b) Opioid suppress chemokine-mediated migration of monkey neutrophils and monocytes - an instant response. Immunopharmacology 47:53-62
54. Nair MP, Laing TJ, Schwartz S (1986) A decreased natural and antibody-dependent cellular cytotoxic activities in intravenous drug abusers. Clin Immunol Immunopathol 38:68-78
55. Nath A, Hauser KF, Wojna V, Booze RM, Maragos W, Prendergast M, Cass W, Turchan JT (2002) Molecular basis for interactions of HIV and drugs of abuse. J Acquir Immune Defic Syndr 31(Suppl 2):(Review)
56. Nestler EJ, Aghajanian GK (1997) Molecular and cellular basis of addiction. Science 278(5335):58,
57. Novick DM, Ochshorn M, Ghali V, Croxson TS, Mercer WD, Chiorazzi N, Kreek MJ (1989) Natural killer cell activity and lymphocyte subsets in parenteral heroin abusers and long-term methadone maintenance patients. J Pharmacol Exp Ther 250:606-610
58. Ocasio FM, Jiang Y, House SD, Chang SL (2004) Chronic morphine accelerates the progression of lipopolysaccharide-induced sepsis to septic shock. J Neuroimmunol 149(1-2):90-100
59. Pacifici R, Minetti M, Zuccaro P, Pietraforte D (1995) Morphine affects cytostatic activity of macrophages by the modulation of nitric oxide release. Int J Immunopharmacol 17(9):771-777
60. Patel K, Bhaskaran M, Dani D, Reddy K, Singhal PC (2002) Role of heme oxygenase-1 in morphine-modulated apoptosis and migration of macrophages. J Infect Dis 187(1):47-54
61. Peterson PK, Sharp B, Gekker G, Brummitt C, Keane WF (1987a) Opioid-mediated suppression of cultured peripheral blood mononuclear cell respiratory burst activity. J Immunol 138(11):3907-3912
62. Peterson PK, Sharp B, Gekker G, Brummitt C, Keane WF (1987b) Opioid-mediated suppression of interferon-gamma production by cultured peripheral blood mononuclear cells. J Clin Invest 80(3):824-831
63. 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(3):480-487
64. Quaglio G, Lugoboni F, Talamini G, Lechi A, Mezzelani P (2002) Prevalence of tuberculosis infection and comparison of multiple-puncture liquid tuberculin test and Mantoux test among drug users. Scand J Infect Dis 34(8):574-576
65. Reichman LB, Felton CP, Edsall JR (1979) Drug dependence, a possible new risk factor for tuberculosis disease. Arch Intern Med 139:337-339
66. Roy S, Loh HH (1996) Effects of opioids on the immune system. Neurochem Res 21(11):1375-1386
67. 3H]- Morphine binding to thymocytes is enhanced by IL-1 stimulation. FEBS Lett 287:93-96
68. Roy S, Ramakrishnan S, Loh HH, Lee NM (1991b) Chronic morphine treatment selectively suppresses macrophage colony formation in bone marrow. Eur J Pharmacol 195:359-363
69. Roy S, Ge BL, Loh LL, Lee NM (1992) Characterization of 3H-Morphine binding to interleukin-1 activated thymocytes. J Pharmacol Exp Ther 263:451-456
70. Roy S, Chapin R, Cain K, Charboneau R, Ramakrishnan S, Barke RA (1997) Morphine inhibits transcriptional regulation of IL-2 synthesis in thymocytes. Cell Immunol 179:1-9
71. Roy S, Barke RA, Loh HH (1998a) Mu-receptor knockout mice: the role of mu-opioid receptor in immune functions. Mol Brain Res 61(1-2):190-194
72. Roy S, Cain KJ, Chapin RB, Charboneau RG, Barke RA (1998b, Apr 17) Morphine modulates NF kappa B activation in macrophages. Biochem Biophys Res Commun 245(2):392-396
73. Roy S, Cain KJ, Charboneau RG, Barke RA (1998c) Morphine accelerates the progression of sepsis in an experimental sepsis model. Adv Exp Med Biol 437:21-31
74. Roy S, Balasubramanian S, Sumandeep S, Charboneau R, Wang J, Melnyk D, Beilman GJ, Vatassery R, Barke RA (2001a) Morphine directs T cells toward TH2 differentiation. Surgery 130(2):304-309
75. Roy S, Charboneau R, Barke RA, Loh HH (2001b) Role of muopioid receptor in immune function. Adv Exp Med Biol 493:117-126
76. Roy S, Wang JH, Balasubramanian S, Sumandeep , Charboneau R, Barke R, Loh HH (2001c) Role of hypothalamic-pituitary axis in morphine-induced alteration in thymic cell distribution using mu-opioid receptor knockout mice. J Neuroimmunol 116(2):147-155
77. Roy S, Wang JH, Sumandeep G, Charboneau RG, Loh HH, Barke RA (2004) Chronic morphine treatment differentiates T helper cells to Th2 effector cells by modulating transcription factors GATA 3 and T bet. J Neuroimmunol 147:78-81
78. Roy S, Wang JH, Charboneau RG, Loh HH, Barke RA (Nov. 15, 2005) Morphine induces CD4+ T cell IL-4 expression through an adenylyl cyclase mechanism independent of the protein kinase A pathway. J Immunol 175(10):6361-6367
79. Runkel NSF, Moody FG, Smith GS, Rodriguez LF, Chen Y, Larocco MT (1993) Alterations in rat intestinal transit by morphine promote bacterial translocation. Dig Dis Sci 38:1530-1536
80. Sacerdote P (2003) Effects of in vitro and in vivo opioids on the production of IL-12 and IL-10 by murine macrophages. Ann N Y Acad Sci 992:129-140
81. Saurer TB, Carrigan KA, Ijames SG, Lysle DT (2004) Morphine-induced alterations of immune status are blocked by the dopamine D2-like receptor agonist 7-OH-DPAT. J Neuroimmunol 148(1-2):54-62
82. Schulz S, Hollt V (1998) Opioid withdrawal activates MAP kinase in locus coeruleus neurons in morphine-dependent rats in vivo. Eur J Neurosci 10(3):1196-1201
83. Sedqui M, Roy S, Ramakrishnan S, Elde R, Loh HH (1995) Complementary cloning of a mu-opioid receptor from rat peritoneal macrophage. Biochem Biophys Res Commun 208:563-574
84. Sharma SK, Klee WA, Nirenberg M (1975) Dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance. Proc Natl Acad Sci USA 72:3092-3096
85. 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(2):793-795
86. 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
87. Shavit Y, Martin FC, Angarita LH, Gale RP, Liebeskind JC (1986) Morphine-induced suppression of natural killer cell activity is mediated by the adrenal gland. Soc Neurosci Abst 12:339
88. Singhal PC, Sharma P, Kapasi AA, Reddy K, Franki N, Gibbons N (1998) Morphine enhances macrophage apoptosis. J Immunol 160(4):1886-1893
89. Singhal PC, Kapasi AA, Franki N, Reddy K (2000) Morphine-induced macrophage apoptosis: the role of transforming growth factor-beta. Immunology 100(1):57-62
90. Singhal PC, Bhaskaran M, Patel J, Patel K, Kasinath BS, Duraisamy S, Franki N, Reddy K, Kapasi AA (2002) Role of p38 mitogen-activated protein kinase phosphorylation and Fas-Fas ligand interaction in morphine-induced macrophage apoptosis. J Immunol 168(8):4025-4033
91. Stefano GB, Cadet P, Fimiani C, Magazine HI (2001) Morphine stimulates iNOS expression via a rebound from inhibition in human macrophages: nitric oxide involvement. Int J Immunopathol Pharmacol 14(3):129-138
92. Szabo I, Rojavin M, Bussiere JL, Eisenstein TK, Adler MW, Rojers TJ (1993) Suppression of peritoneal macrophage phagocytosis of Candida albicans by opioids. J Pharmacol Exp Ther 267:703-706
93. Taub DD, Eisenstein TK, Geller EB, Adler MW, Rogers TJ (1991) Immunomodulatory activity of mu- and kappa-selective opioid agonists. Proc Natl Acad Sci USA 88:360-364
94. Thomas PT, Bhargava HN, House RV (1995) Immunomodulatory effects of in vitro exposure to morphine and its metabolites. Pharmacology 50(1):51-62
95. Tian M, Broxmeyer HE, Fan Y, Lai Z, Zhang S, Aronica S, Cooper S, Bigsby RM, Steinmetz R, Engle SJ, Mestek A, Pollock JD, Lehman MN, Jansen HT, Ying M, Stambrook PJ, Tischfield JA, Yu L (1997) Altered hematopoiesis, behavior, and sexual function in mu opioid receptor-deficient mice. J Exp Med 185(8):1517-1522
96. Tomassini N, Renaud F, Roy S, Loh HH (Feb. 2004) Morphine inhibits Fc-mediated phagocytosis through mu and delta opioid receptors. J Neuroimmunol 147(1-2):131-133 (No abstract available)
97. Tomei EZ, Renaud FL (1997) Effect of morphine on Fc-mediated phagocytosis by murine macrophages in vitro. J Neuroimmunol 74(1-2):111-116
98. Tsukayama D, Breitenbucher R, Steinberg S, Allen J, Nelson R, Gekker G, Keane W, Peterson P (1986) Polymorphonuclear leukocyte, T-lymphocyte, and natural killer cell activities in elderly nursing home residents. Eur J Clin Microbiol 5(4):468-471
99. Tubaro E, Borelli G, Croce C, Cavallo G, Santiangeli C (1983) Effect of morphine on resistance to infection. J Infect Dis 148:656-666
100. Tubaro E, Santiangeli C, Belogi L, Borelli G, Cavallo G, Croce C, Avico U (1987) Methadone vs morphine: comparison of their effect on phagocytic functions. Int J Immunopharmacol 9(1):79-88
101. Vallejo R, de Leon-Casasola O, Benyamin R (2004) Opioid therapy and immunosuppression: a review. Am J Ther 11(5):354-365
102. 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(4):527-536
103. Wang J, Charboneau R, Balasubramanian S, Barke RA, Loh HH, Roy S (2002) The immunosuppressive effects of chronic morphine treatment are partially dependent on corticosterone and mediated by the mu-opioid receptor. J Leukoc Biol 71(5):782-790
104. 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(1):426-434
105. Weber RJ, Pert A (1989) The periaqueductal grey matter mediates opiate-induced-immunosuppression. Science 245:188-190
106. Yukioka H, Rosen M, Evans KT, Leach KG, Hayward MWJ, Saggu GS (1987) Gastric emptying and small bowel transit times in volunteers after intravenous morphine and nalbuphine. Anaesthesia 42:704-710