Skip to main content
SpringerLink
Log in

The Cellular Basis for Opioid-Induced Immunosuppression

  • Chapter
The Brain Immune Axis and Substance Abuse

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 373))

Abstract

Endogenous and exogenous opioid compounds have been shown to alter cellular and humoral immune responses. Opioid administration has been reported to alter both humoral immune responses (5–7, 14, 23, 25, 39) and cell-mediated immune responses (4, 27, 29). It is likely that the mechanism of immunomodulation is complex since studies have suggested that macrophage (1, 10, 16, 17, 33, 38, 44, 45), T cell (2, 32, 46, 47), and B cell functions are specifically altered following administration of opioid compounds.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Apte, R.N., Durum, S.K., & Oppenheim, J.J. (1990). Opioids modulate interleukin-1 production and secretion by bone-marrow macrophages. Immunol. Lett. 24, 141–148.

    Article  PubMed  CAS  Google Scholar 

  2. Hessler, H., Sztein, M.B., & Serrate, S.A. (1990). β-Endorphin modulation of IL-1-induced IL-2 production. Immunopharmacol. 19, 5–14.

    Article  Google Scholar 

  3. Bidlack, J.M., Saripalli, L.D., & Lawrence, D.M.P. (1992). κ-opioid binding sites on a nurine lymphoma cell line. Eur J. Pharmacol. Mol. Pharmacol. Sect. 227, 257–265.

    Article  CAS  Google Scholar 

  4. Bryant, H.U., & Roudebush, R.E. (1990). Suppressive effects of morphine pellet implants on in vivo parameters of immune function. J. Pharmacol. Exp. Thee. 255, 410–414.

    CAS  Google Scholar 

  5. Bussiere, J.L., Adler, M.W., Rogers, T.J., & Eisenstein, T.K. (1992). Differential effects of morphine and naltrexone on the antibody response in various mouse strains. Immunopharmacol. Immunotoxicol. 14, 657–693.

    Article  PubMed  CAS  Google Scholar 

  6. Bussiere, J.L., Adler, M.W., Rogers, T.J., & Eisenstein, T.K. (1992). Effects of in vivo morphine treatment on antibody responses in C57B1/6 bgj/bgj (beige) mice. Life Sciences 52, 43–48.

    Google Scholar 

  7. Bussiere, J.L., Adler, M.W., Rogers, T.J., & Eisenstein, T.K. (1993). Cytokine reversal of morphine-induced suppression of the antibody response. J. Pharmacol. Exp. Ther. 264, 591–597.

    PubMed  CAS  Google Scholar 

  8. Carr, D.J.J., DeCosta, B.A., Kim, C.-H., Jacobson, A.E., Guarcello, V., Rice, K.C., & Blalock, J.E. (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 

  9. Carr, D.J.J., Kim, C.-H., DeCosta, B.R., Jacobson, A.E., Rice, K.C., & Blalock, J.E. (1988). Evidence for a κ-class opioid receptor on cells of the immune system. Cell. Immunol. 116, 44–51.

    Article  PubMed  CAS  Google Scholar 

  10. Cassellas, A.M., Guardioloa, H., & Renaud, F.I. (1991). Inhibition by opioids of phagocytosis in peritoneal macrophages. Neuropeptides 18, 35–40.

    Article  Google Scholar 

  11. Cunningham, A.J., & Szenberg, A. (1968). Other improvements in the plaque technique fordetecting single antibody-forming cells. Immunol. 14, 599–604.

    CAS  Google Scholar 

  12. Donahoe, R.M., Bueso-Ramos, C., Donahoe, F., Madden, J.J., & Falek, A. (1987). Mechanistic implications of the findings that opiates and other drugs of abuse moderate T-cell-surface receptors and antigenic markers. Ann. N.Y. Acad. Sci. 496, 711–717.

    Article  PubMed  CAS  Google Scholar 

  13. Donahoe, R.M., Bueso-Ramos, C., Falek, A., McClure, H., & Nicholson, J.K.A. (1988). Comparative effects of morphine on leukocytic antigenic markers of monkeys and humans. J. Neurosci. Res. 19, 157–165.

    Article  PubMed  CAS  Google Scholar 

  14. Eisenstein, T.K., Meissler, J.J., Jr., Geller, E.B., & Adler, M.W. (1990). Immunosuppression to tetanus toxoid induced by implanted morphine pellets. N.Y. Acad. Sci. 594, 377–379.

    Article  Google Scholar 

  15. Fischer, E.G. (1988). Opioid peptides modulate immune function. A review. Immunopharmacol. Immunotoxicol. 10, 265–326.

    Article  PubMed  CAS  Google Scholar 

  16. Foris, G., Medgyesi, G.A., Gyimesi, E., & Hauck, M. (1984). Met-enkephalin induced alterations of macrophage functions. Mol. Immunol. 21, 747–750.

    Article  PubMed  CAS  Google Scholar 

  17. Foris, G., Medgyesi, G.A., & Hauck, J. (1986). Bidirectional effect of met-enkephalin on macrophage effector functions. Mol. Cell. Biochem. 76, 127–137.

    Google Scholar 

  18. Foster, J.S., & Moore, R.N. (1987). Dynorphin and related opioid peptides enhance tumoricidal activity mediated by murine peritoneal macrophages. J. Leukocyte Biol. 42, 171–174.

    PubMed  CAS  Google Scholar 

  19. Fraser, J. D. (1989). High-affinity binding of staphylococcal enterotoxins A and B to HLA-DR. Nature 339, 221–225.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  22. Heagy, W., Shipp, M.A., & Finberg, R.W. (1992). Opioid receptor agonists and Ca2+ modulation in human B cell lines. J. Immunol. 149, 4074–4081.

    PubMed  CAS  Google Scholar 

  23. Heijnen, C.J., Bevers, C., Kavelaars, A., & Ballieux, R.E. (1986). Effect of a-endorphin on the antigen-induced primary antibody response of human blood B cells in vitro. J. Immunol. 136, 213–216.

    PubMed  CAS  Google Scholar 

  24. Holly, M., Lin, Y.-S., & Rogers, T.J. (1988). Induction of suppressor cells by staphylococcal enterotoxin B: identification of a suppressor cell circuit in the generation of suppressor-effector cells. Immunol. 64, 643–649.

    CAS  Google Scholar 

  25. Johnson, H.M., Smith, E.M., Tones, B.A., & Blalock, J.E. (1982). Regulation of the in vitro antibody response by neuroendocrine hormones. Proc. Natl. Acad. Sci. U.S.A. 79, 4171–4174.

    Article  PubMed  CAS  Google Scholar 

  26. Kappler, J.W. (1974). A micro-technique for hemolytic plaque assays. J Immunol. 112,127–135.

    Google Scholar 

  27. Molitor, T.W., Morilla, A., Risdahl, J.M., Murtaugh, M.P., Chao, C.C., & Peterson, P.K. (1992). Chronic morphine administration impairs cell-mediated immune responses in swine. J. Pharmacol. Exp. Ther 260, 581–586.

    PubMed  CAS  Google Scholar 

  28. Mollick, J.A., Cook, R.G., & Rich, R.R.. (1989). Class II molecules are specific receptors for staphylococcus enterotoxin A. Science 244, 817–820.

    Article  PubMed  CAS  Google Scholar 

  29. Pellis, N.R., Harper, C., & Dafny, N. (1986). Suppression of the induction of Delayed-Type Hypersensitivity in rats by repetitive morphine treatments. Exp. Neurol. 93, 92–97.

    Article  PubMed  CAS  Google Scholar 

  30. Perez-Castrillon, J.-L., Perez-Arellanos, J.-L., Carcia-Palomo, J.-D., Jimeniz-Lopez, A., & De Castro, S. (1992). Opioids depress in vitro human monocyte chemotaxis. Immunopharmacology 23, 57–61.

    Article  PubMed  CAS  Google Scholar 

  31. Peterson, P.K., Sharp, B., Gekker, G., Brummitt, C., & Keane, W.F. (1987). Opioid-mediated suppression of cultured peripheral blood mononnuclear cell respiratory activity. J. Immunol. 138, 3907–3912.

    PubMed  CAS  Google Scholar 

  32. Peterson, P.K., Sharp, B., Gekker, G., Brummitt, C., & Keane, W.F. (1987). Opioid-mediated suppression of interferon-y production by cultured peripheral blood mononuclear cells. J. Clin. Invest. 80, 824–831.

    Article  PubMed  CAS  Google Scholar 

  33. Rojavin, M., Szabo, I., Bussiere, J.L., Rogers, T.J., Adler, M.W., & Eisenstein, T.K. (1993). Morphine treatment in vitro or in vivo decreases phagocytic functions of murine macrophages. Life Sci. 53, 997–1006.

    Article  PubMed  CAS  Google Scholar 

  34. Ruff, M.R., Wahl, S.M., Mergenhagen, S., & Pert, C.B. (1985). Opiate receptor-mediated chemotaxis of human monocytes. Neuropeptides 5, 363–369.

    Article  PubMed  CAS  Google Scholar 

  35. Salamon, F.T., Fayen, J.D., Leonard, M.L., Finegan, C.K., & Rich, E.A. (1992). Accessory function of human mononuclear phagocytes for lymphocyte responses to the superantigen staphylococcal enterotoxin B. Cell Immunol. 141, 466–484.

    Article  PubMed  CAS  Google Scholar 

  36. See, R.H., & Chow, A.W. (1992). Role of adhesion molecule lymphocyte function associated antigen 1 in toxic shock syndrome toxin 1-induced tumor necrosis factor alpha and interleukin 1 secretion by human monocytes. Infect Immun. 60, 4957–4960.

    PubMed  CAS  Google Scholar 

  37. Sharp, B.M., Keane, W.F., Suh, J.J., Gekker, G., Tsukayama, D., & Peterson, P.K. (1985). Opioid peptides rapidly stimulate superoxide production by human polymorphonuclear leukocytes and macrophages. Endocrinology 117, 793–795.

    Article  PubMed  CAS  Google Scholar 

  38. Szabo, I., Rojavin, M., Bussiere, J.L., Eisenstein, T.K., Adler, M.W., & Rogers, T.J. (1993). Suppression of peritoneal macrophage phagocytosis of Candida albicans by opioids. J. Pharmacol. Exp. Ther. 267, 703–706.

    PubMed  CAS  Google Scholar 

  39. Taub, D.D., Eisenstein, T.K., Geller, E.B., Adler, M.W., & Rogers, T.J. (1991). Immunomodulatory activity of u-and x-selective opioid agonists. Proc. Natl. Acad. Sci. U.S.A. 88, 360–364.

    Article  PubMed  CAS  Google Scholar 

  40. Taub, D.D., Lin, Y.-S., & Rogers, T.J. (1990). Characterization and genetic restriction of suppressor-effector cells induced by staphylococcal enterotoxin B. J. Immunol. 144, 456–462.

    PubMed  CAS  Google Scholar 

  41. Taub, D.D., & Rogers, T.J. (1992). Direct activation of murine T cells by staphylococcal enterotoxins. Cell. Immunol. 140, 267–281.

    Article  PubMed  CAS  Google Scholar 

  42. Tittle, T.V., & Rittenberg, M.A. (1978). Expression of IgG memory response in vitro to thymus-dependent and thymus-independent antigens. Cell. Immunol. 35,180–185.

    Article  PubMed  CAS  Google Scholar 

  43. Tosk, J.M., Grim, J.R., Kinback, K.M., Sale, E.J., Bozzetti, L.P., & Will, A.D. (1993). Modulation of chemiluminescence in a murine macrophage cell line by neuroendocrine hormones. Int. J. Immunopharmacol. 15, 615–620.

    Article  PubMed  CAS  Google Scholar 

  44. Tubaro, E., Borelli, G., Croce, C., Cavallo, G., & Santiangeli, C. (1983). Effect of morphine on resistance to infection. J. Infect. Dis. 448, 656–666.

    Article  Google Scholar 

  45. 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, 79–88.

    Article  PubMed  CAS  Google Scholar 

  46. van den Bergh, P., Rozing, J., & Nagelkerken, L. (1993). β-Endorphin stimulates Ia expression on mouse B cells by inducing interleukin-4 secretion by CD4+ T cells. Cell. Immunol. 149, 180–192.

    Article  PubMed  Google Scholar 

  47. van den Bergh, P., Dobber, R., Ramlal, S., Rozing, J., & Nagelkerken, L. (1994). Role of opioid peptides in the regulation of cytokine production by murine CD4+ T cells. Cell. Immunol. 154, 109–122.

    Article  PubMed  Google Scholar 

  48. Wybran, J., Appelboom, T., Famaey, J.-P., & Govaerts, A. (1979). Suggestive evidence for receptors for morphine and methionine-enkephalin on normal human blood T lymphocytes. J. Immunol. 123, 1068–1070.

    PubMed  CAS  Google Scholar 

  49. Wysocki, L.J., & Sato, V.L. (1978). Panning for lymphocytes. A method for cell selection. Proc. Natl. Acad. Sci. U.S.A. 75, 2844–2848.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology and Immunology, USA

    Liming Guan, Robert Townsend, Toby K. Eisenstein & Thomas J. Rogers

  2. Department of Pharmacology, USA

    Martin W. Adler

  3. Fels Institute for Cancer Research and Molecular Biology Temple, University School of Medicine, Philadelphia, Pennsylvania, 19140, USA

    Thomas J. Rogers

Authors
  1. Liming Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert Townsend
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Toby K. Eisenstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martin W. Adler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thomas J. Rogers
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Hennepin County Medical Center and University of Minnesota, Minneapolis, Minnesota, USA

    Burt M. Sharp

  2. Temple University School of Medicine, Philadelphia, Pennsylvania, USA

    Toby K. Eisenstein

  3. Emory University School of Medicine, Atlanta, Georgia, USA

    John J. Madden

  4. University of South Florida College of Medicine, Tampa, Florida, USA

    Herman Friedman

Rights and permissions

Reprints and permissions

Copyright information

© 1995 Springer Science+Business Media New York

About this chapter

Cite this chapter

Guan, L., Townsend, R., Eisenstein, T.K., Adler, M.W., Rogers, T.J. (1995). The Cellular Basis for Opioid-Induced Immunosuppression. In: Sharp, B.M., Eisenstein, T.K., Madden, J.J., Friedman, H. (eds) The Brain Immune Axis and Substance Abuse. Advances in Experimental Medicine and Biology, vol 373. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1951-5_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-1951-5_9

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5801-5

  • Online ISBN: 978-1-4615-1951-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation