Antisense inhibition of pro-opiomelanocortin and proenkephalin A messenger RNA translation alters rat immune cell function in vitro

Journal of Neuroimmunology

Volumn 106, Issue 1-2, 2000, Pages 6-13

  Fulford, Allison J ^a   Harbuz, Michael S ^a   Jessop, David S ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Endorphin; ACTH; Antisense; Immune system; POMC; Proenkephalin; Rat; Spleen

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; BETA ENDORPHIN; CONCANAVALIN A; CORTICOTROPIN; ENKEPHALIN[2 DEXTRO ALANINE 5 DEXTRO LEUCINE]; MESSENGER RNA; METENKEPHALIN; OPIATE PEPTIDE; PROENKEPHALIN; PROOPIOMELANOCORTIN;

ADOLESCENT; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RNA TRANSLATION; SPLEEN CELL;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; BETA-ENDORPHIN; CELLS, CULTURED; ENKEPHALINS; IMMUNE SYSTEM; MALE; OLIGONUCLEOTIDES, ANTISENSE; PRO-OPIOMELANOCORTIN; PROTEIN BIOSYNTHESIS; PROTEIN PRECURSORS; RATS; RATS, WISTAR; RNA, MESSENGER; SPLEEN;

EID: 0034237426     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-5728(00)00215-0     Document Type: Article

References (47)

1. Blalock J.E. The syntax of immune-neuroendocrine communication. Immunol. Today. 15:1994;504-511.
2. Buzzetti R., McLoughlin L., Lavender P., Clark A., Rees L.H. Expression of proopiomelanocortin gene and quantification of adrenocorticotropic hormone-like immunoreactivity in human normal peripheral mononuclear cells and lymphoid and myeloid malignancies. J. Clin. Invest. 83:1989;733-737.
3. Cabot P.J., Carter L., Gaiddon C., Zhang Q., Schafer M., Loeffler J.P., Stein C. Immune-cell derived β-endorphin: production, release and control of inflammatory pain in rats. J. Clin. Invest. 100:1997;142-148.
4. Carr D.J.J., Rogers T.J., Weber R.J. The relevance of opioid receptors on immunocompetence and immune homeostasis. Proc. Soc. Exp. Biol. Med. 213:1996;248-257.
5. Casellas A.M., Guardiola H., Renaud F.L. Inhibition by opioids of phagocytosis in peritoneal macrophages. Neuropeptides. 18:1991;35-40.
6. Chuang L.F., Chuang T.K., Killam K.F., Chuang A.J., Kung H.F., Lu L., Chuang R.Y. Delta opioid gene expression in lymphocytes. Biochem. Biophys. Res. Commun. 202:1994;1291-1299.
7. Clarke B.L., Bost K.L. Differential expression of functional adrenocorticotropic hormone receptors by subpopulations of lymphocytes. J. Immunol. 143:1989;464-469.
8. Gaillard R.C. Neuroendocrine-immune system interactions: the immune-hypothalamo-pituitary-adrenal axis. Trends Endocrinol. Metab. 5:1994;303-309.
9. Geenen V., Legros J.J., Franchimont P., Defresne M.P., Boniver J., Ivell R., Richter D. The thymus as a neuroendocrine organ. Synthesis of vasopressin and oxytocin in human thymic epithelium. Ann. New York Acad. Sci. 496:1987;56-66.
10. Getting S.J., Gibbs L., Clark A.J., Flower R.J., Perretti M. POMC gene-derived peptides activate melanocortin type 3 receptor on murine macrophages, suppress cytokine release, and inhibit neutrophil migration in acute experimental inflammation. J. Immunol. 162:1999;7446-7453.
11. Gilman S.J., Schwartz J.M., Miner R.J., Bloom F.E., Feldman J.D. β-Endorphin enhances lymphocyte proliferative responses. Proc. Natl. Acad. Sci. USA. 79:1982;4226-4230.
12. Hassan A.H.S., Przewlocki R., Herz A., Stein C. Dynorphin, a preferential ligand for k-opioid receptors, is present in nerve fibres and immune cells within inflamed tissue of the rat. Neurosci. Lett. 140:1992;85-88.
13. Jessop D.S. Neuropeptides: modulators of the immune system. Curr. Opin. Endocrinol. Diabetes. 5:1998;52-58.
14. Jessop D.S., Eckland D.J., Todd K., Lightman S.L. Osmotic regulation of hypothalamo-neurointermediate lobe corticotrophin-releasing factor-41 in the rat. J. Endocrinol. 120:1989;119-124.
15. Jessop D.S., Lightman S.L., Chowdrey H.S. Effects of a chronic inflammatory stress on levels of pro-opiomelanocortin-derived peptides in the rat spleen and thymus. J. Neuroimmunol. 49:1994;197-203.
16. Jessop D.S., Renshaw D., Lightman S.L., Harbuz M.S. Changes in ACTH and β-endorphin immunoreactivity in immune tissues during a chronic inflammatory stress are not correlated with changes in corticotropin-releasing hormone and arginine vasopressin. J. Neuroimmunol. 60:1995;29-35.
17. Jessop D.S., Harbuz M.S., Snelson C.L., Dayan C.M., Lightman S.L. An antisense oligodeoxynucleotide complementary to corticotropin-releasing hormone mRNA inhibits rat splenocyte proliferation in vitro. J. Neuroimmunol. 75:1997;135-140.
18. Kern D.E., Lachman L.B., Greenberg P.D. Lyt-2+ cells: requirements for concanavalin A-induced proliferation and interleukin 2 production. J. Immunol. 139:1987;2880-2887.
19. Linner K.M., Beyer H.S., Sharp B.M. Induction of the messenger ribonucleic acid for proenkephalin A in cultured murine CD4-positive thymocytes. Endocrinology. 128:1991;717-724.
20. Linner K.M., Nicol S.E., Sharp B.M. Il-1b modulates the concanavalin A-induced expression of proenkephalin A mRNA in murine thymocytes. J. Pharmacol. Exp. Ther. 267:1993;1566-1572.
21. 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.
22. Lolait S., Clements J.A., Markwick A., Cheng C., McNulty M., Smith A.I., Funder J.W. Pro-opiomelanocortin messenger ribonucleic acid and posttranslational processing of beta-endorphin in spleen macrophages. J. Clin. Invest. 77:1986;1776-1779.
23. Lyons P.D., Blalock J.E. The kinetics of ACTH expression in rat leukocyte subpopulations. J. Neuroimmunol. 63:1995;103-112.
24. Lyons P.D., Blalock J.E. Pro-opiomelanocortin gene expression and protein processing in rat mononuclear leukocytes. J. Neuroimmunol. 78:1997;47-56.
25. Madden J.J., Whaley W.L., Ketelson D. Opiate binding sites in the cellular immune system: expression and regulation. J. Neuroimmunol. 83:1998;57-62.
26. Martin J., Prystowsky M.B., Angeletti R.H. Preproenkephalin mRNA in T cells, macrophages and mast cells. J. Neurosci. Res. 18:1987;82-87.
27. McCain H.W., Lamster I.B., Bozzone J.M., Grbic J.T. β-Endorphin modulates human immune activity via non-opiate receptor mechanisms. Life Sci. 31:1982;1619-1624.
28. Owen D.L., Morley J.S., Ensor D.M., Miles J.B. The C-terminal tetrapeptide of β-endorphin (MPF) enhances lymphocyte proliferative responses. Neuropeptides. 32:1998;131-139.
29. Panerai A.E., Sacerdote P. b-Endorphin in the immune system: a role at last? Immunol. Today. 18:1997;317-319.
30. Przewlocki R., Hassan A.H.S., Lason W., Epplen C., Herz A., Stein C. Gene expression and localisation of opioid peptides in immune cells of inflamed tissue. Functional role in antinociception. Neuroscience. 48:1992;491-500.
31. Rosen H., Behar O., Abramsky O., Ovadia H. Regulated expression of proenkephalin A in normal lymphocytes. J. Immunol. 143:1989;3703-3707.
32. Roy S., Chapin R., Cain K., Charboneau R., Ramakrishnan S., Barke R.A. Morphine inhibits transcriptional regulation of Il-2 synthesis in thymocytes. Cell. Immunol. 179:1997;1-9.
33. Roy S., Cain K., Chapin R., Charboneau R., Barke R.A. Morphine modulates NFkB activation in macrophages. Biochem. Biophys. Res. Commun. 245:1998;392-396.
34. Shahabi N.A., Burtness M.Z., Sharp B.M. N-Acetyl-β-endorphin 1-31 antagonises the suppressive effect of β-endorphin 1-31 on murine splenocyte proliferation via a naloxone-resistant receptor. Biochem. Biophys. Res. Commun. 175:1991;936-942.
35. Sharp B.M., Roy S., Bidlack J.M. Evidence for opioid receptors on cells involved in host response and the immune system. J. Neuroimmunol. 83:1998;45-56.
36. Sibinga N.E.S., Goldstein A. Opioid peptides and opioid receptors in cells of the immune system. Annu. Rev. Immunol. 6:1988;219-249.
37. Spruce B.A., Jackson S., Lowry P.J., Lane D.P., Glover D.M. Monoclonal antibodies to a proenkephalin A fusion peptide synthesised in Escherichia coli recognise novel proenkephalin A precursor forms. J. Biol. Chem. 263:1988;19788-19799.
38. Stein C., Hassan A.H.S., Przewlocki R., Gramsch C., Herz A. Opioids from immunocytes interact with sensory nerves to inhibit nociception in inflammatory cells. Proc. Natl. Acad. Sci. USA. 87:1990;5935-5939.
39. Stein C., Hassan A.H.S., Lehrberger K., Giefing J., Yassourdis A. Local analgesic effects of endogenous opioid peptides. Lancet. 342:1993;321-324.
40. Stephanou A., Jessop D.S., Knight R.A., Lightman S.L. Corticotrophin-releasing factor-like immunoreactivity and mRNA in human leukocytes. Brain Behav. Immun. 4:1990;67-73.
41. Stephanou A., Fitzharris P., Knight R.A., Lightman S.L. Characteristics and kinetics of proopiomelanocortin mRNA expression by human leucocytes. Brain Behav. Immun. 5:1991;319-327.
42. Weigent D., Blalock J. Interactions between the neuroendocrine and immune systems: common hormones and receptors. Immunol. Rev. 100:1987;79-108.
43. Williams M., Carter D., Lightman S.L. Sexual dimorphism in the posterior pituitary response to stress in the rat. Endocrinology. 116:1985;738-740.
44. Williamson S.A., Knight R.A., Lightman S.L., Hobbs J.R. Differential effects of β-endorphin fragments on human natural killing. Brain Behav. Immun. 1:1987;329-335.
45. Williamson S.A., Knight R.A., Lightman S.L., Hobbs J.R. Effects of β-endorphin on specific immune responses in man. Immunology. 65:1988;47-51.
46. Yin D., Mufson A., Wang R., Shi Y. Fas-mediated cell death promoted by opioids. Nature. 297:1999;218.
47. Zurawski P., Benedik G.M., Kamb B.J., Abrams J.S., Zurawski S.M., Lee F.D. Activation of mouse T-helper cells induces abundant preproenkephalin mRNA synthesis. Science. 232:1986;772.