Journal of Neuroimmunology
Volume 178, Issue 1 , Pages 62-75 , September 2006

Amphetamine triggers an increase in met-enkephalin simultaneously in brain areas and immune cells

  • María A. Assis

      Affiliations

    • Departamento de Farmacología, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Ciudad Universitaria, X5000HUA, Córdoba, Argentina
    • Fellowship from CONICET.
    • ,
  • César Collino

      Affiliations

    • Departamento de Bioquímica Clínica, CIBIC-CONICET, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Ciudad Universitaria, X5000HUA, Córdoba, Argentina
    • Centro de Química Aplicada, CEQUIMAP, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Ciudad Universitaria, X5000HUA, Córdoba, Argentina
    • ,
  • María de L. Figuerola

      Affiliations

    • Centro de Investigaciones Endocrinólogicas (CEDIE), CONICET, Hospital de Niños Ricardo Gutiérrez, Gallo 1360, 1425, Buenos Aires, Argentina
    • ,
  • Claudia Sotomayor

      Affiliations

    • Departamento de Bioquímica Clínica, CIBIC-CONICET, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Ciudad Universitaria, X5000HUA, Córdoba, Argentina
    • ,
  • Liliana M. Cancela

      Affiliations

    • Departamento de Farmacología, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Ciudad Universitaria, X5000HUA, Córdoba, Argentina
    • Corresponding Author InformationCorresponding author. Tel.: +54 351 4344974x161; fax: +54 351 4334420.

Received 21 October 2005 ,Revised 16 May 2006 ,Accepted 17 May 2006.

References 

  1. Abarca C, Albrecht U, Spanagel R. Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc. Natl. Acad. Sci. U. S. A. 2002;99(13):9026–9030
  2. Álvarez Fischer D, Schafer MK, Ferger B, Gross S, Westermann R, Weihe E, et al. Sensitization to the behavioural effects of cocaine: alterations in tyrosine hydroxylase or endogenous opioid mRNAs are not necessarily involved. Naunyn-Schmiedeberg's Arch. Pharmacol. 2001;363(3):288–294
  3. Amenta F, Bronzetti E, Cantalamessa F, El-Assouad D, Felici L, Ricci A, et al. Identification of dopamine plasma membrane and vesicular transporters in human peripheral blood lymphocytes. J. Neuroimmunol. 2001;177:133–142
  4. Antelman SM, Eichler AJ, Black CA, Kocan D. Interchangeability of stress and amphetamine in sensitization. Science. 1980;207:329–331
  5. Baldwing GC, Roth MD, Tashkin DP. Acute and chronic effects of cocaine on the immune system and the possible link to AIDS. J. Neuroimmunol. 1998;83:133–138
  6. Basso AM, Gioino G, Molina VA, Cancela LM. Chronic amphetamine facilitates immunosuppression in response to a novel aversive stimulus: Reversal by Haloperidol pretreatment. Pharmacol. Biochem. Behav. 1999;62:307–314
  7. Basu S, Dasgupta S. Dopamine, a neurotransmitter, influences the immune system. J. Neuroimmunol. 2000;102:113–124
  8. Behar OZ, Ovadia H, Polakiewicz RD, Abramsky O, Rosen H. Regulation of proenkephalin A messenger ribonucleic acid levels in normal B lymphocytes: specific inhibition by glucocorticoid hormones and superinduction by cycloheximide. Endocrinology. 1991;129:649–655
  9. Bencsics A, Sershen H, Baranyi M, Hashim A, Lajtha A, Vizi ES. Dopamine, as well as norepinephrine, is a link between noradrenergic nerve terminals and splenocytes. Brain Res. 1997;761:236–343
  10. Bergquist J, Tarkowski A, Ekman R, Ewing A. Discovery of endogenous catecholamines in lymphocytes and evidence for catecholamine regulation of lymphocyte function via an autocrine loop. Proc. Natl. Acad. Sci. U. S. A. 1994;91:12912–12916
  11. Borsook D, Konradi C, Falkowski O, Comb M, Hyman SE. Molecular mechanisms of stress-induced proenkephalin gene regulation: CREB interacts with the proenkephalin gene in the mouse hypothalamus and is phosphorylated in response to hyperosmolar stress. Mol. Endocrinol. 1994;8:240–248
  12. Brar BK, Lowry PJ. The differential processing of proenkephalin A in mouse and human breast tumour cell lines. J. Endocrinol. 1999;161:475–484
  13. Cador M, Bjijou Y, Cailhol S, Stinus L. d-Amphetamine-induced behavioral sensitization: implication of a glutamatergic medial prefrontal cortex–ventral tegmental area innervation. Neuroscience. 1999;94:705–721
  14. Chen J, Kelz MB, Hope BT, Nakabeppu Y, Nestler EJ. Chronic Fos-related antigens: stable variants of ΔFosB induced in brain by chronic treatments. J. Neurosci. 1997;17:4933–4941
  15. Cosentino M, Zaffaroni M, Marino F, Bombelli R, Ferrari M, Rasini E, et al. Catecholamine production and tyrosine hydroxylase expression in peripheral blood mononuclear cells from multiple sclerosis patients: effects of cell stimulation and possible relevance for activation-induced apoptosis. J. Neuroimmunol. 2002;133(1–2):233–240
  16. Cosentino M, Marino F, Bombelli R, Ferrari M, Lecchini S, Frigo G. Unravelling dopamine (and catecholamine) physiopharmacology in lymphocytes: open questions. Trends Immunol. 2003;24(11):581–582
  17. Daunais JB, McGinty JF. Acute and chronic cocaine administration differentially alters striatal opioid and nuclear transcription factor mRNAs. Synapse. 1994;18(1):35–45
  18. Diaz-Otañez CS, Capriles N, Cancela LM. D1 and D2 dopamine receptors are involved in the restraint stress induced sensitization to the psychostimulant effects of amphetamine. Pharmacol. Biochem. Behav. 1997;58(1):9–14
  19. Ehrlich ME, Sommer J, Canas E, Unterwald EM. Periadolescent mice show enhanced ΔFosB upregulation in response to cocaine and amphetamine. J. Neurosci. 2002;22(21):9155–9159
  20. Freire-Garabal M, Balboa JL, Núñez MJ, Castaño MT, Llovo JB, Fernández-Rial JC, et al. Effects of amphetamine on T-cell immune response in mice. Life Sci. 1991;49(16):PL107–PL112
  21. Friedman H, Eisenstein TK. Neurological basis of drug dependence and its effects on the immune system. J. Neuroimmunol. 2004;147(1–2):106–108
  22. Fulford AJ, Harbuz MS, Jessop DS. Antisense inhibition of pro-opiomelanocortin and proenkephalin A messenger RNA translation alters rat immune cell function in vitro. J. Neuroimmunol. 2000;106(1–2):6–13
  23. Galinowski A, Levy-Soussan P, Loo H. Schizophrenia and immunity. Ann. Med. Psychol. 1992;150:138–142
  24. Gordon J, Barnes NM. Lymphocytes transport serotonin and dopamine: agony or ecstasy?. Trends Immunol. 2003;24(8):438–443
  25. Haus E, Smolensky MH. Biologic rhythms in the immune system. Chronobiol. Int. 1999;16(5):581–622
  26. Jankovic BD, Radulovic J. Enkephalins, brain and immunity: modulation of immune responses by methionine-enkephalin injected into the cerebral cavity. Int. J. Neurosci. 1992;67(1–4):241–270
  27. Kalivas PW, Stewart J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res. Rev. 1991;16:223–244
  28. Knych ET, Eisenberg RM. Effect of amphetamine on plasma corticosterone in the conscious rat. Neuroendocrinology. 1979;29:110–118
  29. Konradi C, Cole RL, Heckers S, Hyman SE. Amphetamine regulates gene expression in rat striatum via transcription factor CREB. J. Neurosci. 1994;14(9):5623–5634
  30. Kubera M, Filip M, Basta-Kaim A, Nowak E, Budziszewska B, Tetich M, et al. The effect of amphetamine sensitization on mouse immunoreactivity. J. Physiol. Pharmacol. 2002;53(2):233–252
  31. Kuis W, Villiger PM, Leser HG, Lotz M. Eifferential processing of proenkephalin-A by human peripheral blood monocytes and T lymphocytes. J. Clin. Invest. 1991;88(3):817–824
  32. Lightman SL, Young WS. Changes in hypothalamic preproenkephalin A mRNA following stress and opiate withdrawal. Nature. 1987;328:643–645
  33. Lindberg I, Shaw E. Posttranslational processing of proenkephalin in SK-N-MC cells: evidence for phosphorylation. J. Neurochem. 1992;58:448–453
  34. Linner KM, Beyer HS, Sharp BM. Induction of the messenger ribonucleic acid for proenkephalin A in cultured murine CD4-positive thymocytes. Endocrinology. 1991;128(2):717–724
  35. Linner KM, Quist HE, Sharp BM. Met-enkephalin-containing peptides encoded by proenkephalin A mRNA expressed in activated murine thymocytes inhibit thymocyte proliferation. J. Immunol. 1995;154(10):5049–5060
  36. Malaplate-Armand C, Becuwe P, Ferrari L, Masson C, Dauca M, Visvikis S, et al. Effect of acute and chronic psychostimulant drugs on redox status, AP-1 activation and pro-enkephalin mRNA in the human astrocyte-like U373 MG cells. Neuropharmacology. 2005;48(5):673–684
  37. Mao L, Wang JQ. Contribution of ionotropic glutamate receptors to acute amphetamine-stimulated preproenkephalin mRNA expression in the rat striatum in vivo. Neurosci. Lett. 2003;31; 346(1–2):17–20
  38. Mathis JP, Lindberg I. Posttranslational processing of proenkephalin in AtT-20 cells: evidence for cleavage at a Lys-Lys site. Endocrinology. 1992;131(5):2287–2296
  39. McClung CA, Ulery PG, Perrotti LI, Zachariou V, Berton O, Nestler EJ. ΔFosB: a molecular switch for long-term adaptation in the brain. Brain Res. Mol. Brain Res. 2004;20; 132(2):146–154
  40. McKenna F, McLaughlin PJ, Lewis BJ, Sibbring GC, Cummerson JA, Bowen-Jones D, et al. Dopamine receptor expression on human T- and B-lymphocytes, monocytes, neutrophils, eosinophils and NK cells: a flow cytometric study. J. Neuroimmunol. 2002;132:34–40
  41. Monnier D, Loeffler JP. Pituitary adenylate cyclase-activating polypeptide stimulates proenkephalin gene transcription through AP1- and CREB-dependent mechanisms. DNA Cell Biol. 1998;17(2):151–159
  42. Nestler EJ. Molecular neurobiology of addiction. Am. J. Addict. 2001;10(3):201–217
  43. Pacchioni AM, Gioino G, Assis MA, Cancela LM. A single exposure to restraint stress induces behavioral and neurochemical sensitization to stimulating effects of amphetamine: involvement of NMDA receptors. Ann. N. Y. Acad. Sci. 2002;965:233–246
  44. Pacchioni, A.M., Cador, M., Bregonzio, C., Cancela, L.M., in press. A glutamate–dopamine interaction in the persistent enhanced response to amphetamine in nucleus accumbens core but not shell following a single restraint stress. Neuropsychopharmacology (Advanced online publication 19 April 2006).
  45. Padgett DA, Glaser R. How stress influences the immune response. Trends Immunol. 2003;24(8):444–448
  46. Padrós MR, Vindrola O, Zunszain P, Fainboin L, Finkielman S, Nahmod VE. Mitogenic activation of human lymphocytes induce the release of proENK derived peptides. Life Sci. 1989;242:229-223
  47. Padrós MR, Saravia F, Vindrola O. Antibodies against the amino-terminal portion of pro-enkephalin inhibit DNA synthesis in human peripheral mononuclear cells. J. Neuroimmunol. 1995;61(1):79–83
  48. Pellegrino T, Bayer BM. Modulation of immune cell function following fluoxetine administration in rats. Pharmacol. Biochem. Behav. 1998;59(1):151–157
  49. Pellegrino T, Bayer BM. In vivo effects of cocaine on immune cell function. J. Neuroimmunol. 1998;83:139–147
  50. Pellegrino TC, Bayer BM. Specific serotonin reuptake inhibitor-induced decrease in lymphocyte activity requires endogenous serotonin release. Neuroimmunomodulation. 2000;8:179–187
  51. Pierce RC, Kalivas PW. A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res. Rev. 1997;25:192–216
  52. Pierce RC, Kalivas PW. A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res. Rev. 1997;25:192–216
  53. Pruett SB. Quantitative aspects of stress-induced immunomodulation. Int. Immunopharmacol. 2001;1:507–520
  54. Rajadhyaksha A, Barczak A, Macias W, Leveque JC, Lewis SE, Konradi C. l-Type Ca(2+) channels are essential for glutamate-mediated CREB phosphorylation and c-fos gene expression in striatal neurons. J. Neurosci. 1999;1; 19(15):6348–6359
  55. Rittner HL, Brack A, Machelska HS, Mousa A, Bauer M, Schäfer M, et al. Opioid peptide-expressing leukocytes: identification, recruitment, and simultaneously increasing inhibition of inflammatory pain. Anesthesiology. 2001;95(2):500–508
  56. Robinson TE, Berridge KC. The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction. 2000;95(Supplement 2):S91–S117
  57. Roda LG, Bongiorno L, Trani E, Urbani A, Marini M. Positive and negative immunomodulation by opioid peptides. Int. J. Immunopharmacol. 1996;18:1–16
  58. Roth KA, Lorenz RG, Unanue RA, Weaver CT. Non-opiate active proenkephalin-derived peptides are secreted by T helper cells. FASEB J. 1989;3(12):2401–2407
  59. Roy S, Loh HH. Effects of opioids on the immune system. Neurochem. Res. 1996;21:1375–1386
  60. Saal D, Dong Y, Bonci A, Malenka RC. Drugs of abuse and stress trigger a common report synaptic adaptation in dopamine neurons. Neuron. 2003;37:1–20
  61. Saravia FA, Ase A, Aloyz R, Kleid MC, Ines M, Vida R, et al. Differential post-translational processing of proENK in rat bone marrow and spleen mononuclear cells: evidence for synenkephalin cleavage. Endocrinolgy. 1993;132:1431–1437
  62. Saravia F, Padros MR, Ase A, Aloyz R, Duran S, Vindrola O. Differential response to a stress stimulus of proENK peptide content in immune cells of naive and chronically stressed rats. Neuropeptides. 1998;32(4):351–359
  63. Tjon GH, Voorn P, Vanderschuren LJ, de Vries TJ, Michiels NH, Jonker AJ, et al. Delayed occurrence of enhanced striatal preprodynorphin gene expression in behaviorally sensitized rats: differential long-term effects of intermittent and chronic morphine administration. Neuroscience. 1997;76(1):167–176
  64. Turchan J, Maj M, Przewlocka B, Przewlocki R. Effect of cocaine and amphetamine on biosynthesis of proenkephalin and prodynorphin in some regions of the rat limbic system. Pol. J. Pharmacol. 2002;54(4):367–372
  65. Vanderschuren LJMJ, Kalivas PW. Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology (Berl). 2000;151(2–3):99–120
  66. Vanderschuren LJMJ, Schoffelmeer ANM, Mulder AH, De Vries TJ. Dopaminergic mechanisms mediating the long-term expression of locomotor sensitization following pre-exposure to morphine or amphetamine. Psychopharmacology. 1999;143:244–253
  67. Vanderschuren LJMJ, Schmidt ED, De Vries TJ, Van Moorsel CA, Tilders FJ, Schoffelmeer AN. A single exposure to amphetamine is sufficient to induce long-term behavioral, neuroendocrine, and neurochemical sensitization in rats. J. Neurosci. 1999;19(21):9579–9586
  68. Vezina P, Lorrain DS, Arnold GM, Austin D, Suto N. Sensitization of midbrain dopamine neuron reactivity promotes the pursuit of amphetamine. J. Neurosci. 2002;22(11):4654–4662
  69. Vindrola O, Lindberg I. Biosynthesis of the prohormone convertase mPC1 in AtT-20 cells. Mol. Endocrinol. 1992;6(7):1088–1094
  70. Vindrola O, Padrós MR, Sterin-Prync A, Ase A, Finkielman S, Nahmod VE. Proenkephalin system in human polymorphonuclear cells. J. Clin. Invest. 1990;86:531–537
  71. Vindrola O, Mayer AM, Citera G, Spitzer JA, Espinoza LR. Prohormone convertases PC2 and PC3 in rat neutrophils and macrophages. Neuropeptides. 1994;27:235–244
  72. Vindrola O, Chervin A, Vitale M, Mella AN, Aloyz R, Basso A. Elevated proenkephalin-derived peptide levels in ACTH-producing adenomas: nucleus and cytoplasm localization. Endocrine. 1998;8(3):231–240
  73. Wang JQ, McGinty JF. Alterations in striatal zif/268, preprodynorphin and preproenkephalin mRNA expression induced by repeated amphetamine administration in rats. Brain Res. 1995;6; 673(2):262–274
  74. Wang JQ, McGinty JF. D1 and D2 receptor regulation of preproenkephalin and preprodynorphin mRNA in rat striatum following acute injection of amphetamine or methamphetamine. Synapse. 1996;22(2):114–122
  75. Weisinger G. The transcriptional regulation of the preproenkephalin gene. Biochem. J. 1995;307:617–629
  76. Woiciechowsky C, Schöning B, Lanksch WR, Volk HD, Döcke WD. Mechanisms of brain-mediated systemic anti-inflammatory syndrome causing immunodepression. J. Mol. Med. 1999;77:769–780
  77. Wolf ME. The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog. Neurobiol. 1998;54:679–720

PII: S0165-5728(06)00195-0

doi: 10.1016/j.jneuroim.2006.05.009

Journal of Neuroimmunology
Volume 178, Issue 1 , Pages 62-75 , September 2006

Article Tools

* Image Usage & Resolution