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Stress
The International Journal on the Biology of Stress
Volume 6, 2003 - Issue 4
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Original Article

Stress Applied During Primary Immunization Affects the Secondary Humoral Immune Response in the Rat: Involvement of Opioid Peptides

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Pages 247-258 | Received 04 Mar 2003, Accepted 27 May 2003, Published online: 03 Aug 2009

References

  • Abbas, A.K., Lichtman, A.H. and Pober, J.S. (2000) Effector mechanisms of humoral immunity, In: Abbas, A.K., Lichtman, A.H. and Pober, J.S., eds, Cellular and Molecular Immunology, 4th Ed. (W.B. Saunders Company, Philadelphia/London/New York/St. Louis/ Sydney/Toronto), pp 309–334.
  • Altier, N. and Stewart, J. (1996) Opioid receptors in ventral tegmental area contribute to stress-induced analgesia in the formalin test for tonic pain, Brain Res. 718, 203–206.
  • Basu, S. and Dasgupta, P.S. (2000) Dopamine, a neurotransmitter, influences the immune system, J. Neuroimmunol. 102, 113–124.
  • Brenner, G.J., Cohen, N., Ader, R. and Moynihan, J.A. (1990) Increased pulmonary metastases in mice following handling, Life Sci. 47, 1813–1819.
  • Bukilica, M., Andrejevic', S., Dimitrijevic', M., Laban, O., Stanojevic', S., Vasiljevic', T., Kovac?evic'-Jovanovic', V., Vujic', V. and Radulovic', J. (1996) Strain differences in the effect of stress on experimental allergic encephalomyelitis in the rats, Iugosl. Physiol. Pharmacol. Acta 32, 99–108.
  • Cabot, P.J., Carter, L., Scha¨fer, M. and Stein, C. (2001) Methionineenkephalin and Dynorphine-A release from immune cells and control of inflammatory pain, Pain 93, 207–212.
  • Chrousos, G.O. and Gold, P.W. (1992) The concept of stress and stress system disorders: overview of behavioral and physical homeostasis, J. Am. Med. Assoc. 267, 1244–1252.
  • Cocke, R., Moynihan, J.A., Cohen, N., Grota, L.J. and Ader, N. (1993) Exposure to conspecific alarm chemosignals alters immune responses in BALB/c mice, Brain Behav. Immun. 7, 36–46.
  • Croiset, G., Heijnen, C.J., Veldhuis, H.D., deWied, D. and Ballieux, R.E. (1987) Modulation of the immune response by emotional stress, Life Sci. 40, 775–782.
  • Dhabhar, F.S. and McEwen, B.S. (1996) Stress-induced enhancement of antigen-specific cell-mediated immunity, J. Immunol. 156, 2608–2615.
  • Dhabhar, F.S., Miller, A.H., McEwen, B.S. and Spencer, R.L. (1995) Differential activation of adrenal steroid receptors in neural and immune tissues of Sprague Dawley, Fischer 344, and Lewis rats, J. Neuroimmunol. 56, 77–90.
  • Dimitrijevic', M., Stanojevic', S., Kovac?evic'-Jovanovic', V., Miletic', T., Vujic'-Redz?ic', V. and Radulovic', J. (2000) Modulation of humoral immune responses in the rat by centrally applied Met-Enk and opioid receptor antagonists: functional interactions of brain OP1, OP2 and OP3 receptors, Immunopharmacology 49, 255–262.
  • Dom, L.D. and Chrousos, G.P. (1993) The endocrinology of stress and stress system disorders in adolescence, Endocrinol. Metab. Clin. N. Am. 22, 685–700.
  • Drugan, R.C. and Maier, S.F. (1982) The nature of the activity deficit produced by inescapable shock, Anim. Learn. Behav. 10, 401–406.
  • Dziedzicka-Wasylewska, M., Dlaboga, D., Pierzchala-Koziec, K. and Rogoz, Z. (2002) Effect of tianeptine and fluoxetine on the levels of Met-Enkephalin and mRNA encoding proenkephalin in the rat, J. Physiol. Pharmacol. 53, 117–126.
  • Fanselow, M.S. (1985) Odors released by stressed rats produce opioid analgesia in unstressed rats, Behav. Neurosci. 99, 589–592.
  • Fanselow, M.S. and Sigmundi, R.A. (1986) Species-specific danger signals, endogenous opioid analgesia and defensive behavior, J. Exp. Psychol. Anim. Behav. Proc. 12, 301–309.
  • Feng, N., Pagniano, R., Tovar, C.A., Bonneau, R.H., Glaser, R. and Sheridan, J.F. (1991) The effect of restraint stress on the kinetics, magnitude, and isotype of the humoral immune response to influenza virus infection, Brain Behav. Immun. 5, 370–382.
  • Fleshner, M., Watkins, L.R., Lockwood, L.L., Bellgrau, D., Laudenslager, M.L. and Maier, S.F. (1992) Specific changes in lymphocyte subpopulations: a potential mechanism for stressinduced immunomodulation, J. Neuroimmunol. 41, 131–142.
  • Fleshner, M., Bellgrau, D., Watkins, L.R., Laudenslager, M.L. and Maier, S.F. (1995) Stress-induced reduction in the rat mixed lymphocyte reaction is due to macrophages and not to changes in T cell phenotypes, J. Neuroimmunol. 56, 45–52.
  • Fleshner, M., Brennan, F.X., Nguyen, K.T., Watkins, L.R. and Maier, S.F. (1996) RU-486 blocks differentially suppressive effect of stress on in vivo anti-KLH immunoglobulin response, Am. J. Physiol. 271, R1344–R1352.
  • Fleshner, M., Nguyen, K.T., Cotter, C.S., Watkins, L.R. and Maier, S.F. (1998) Acute stress exposure both suppresses acquired immunity and potentiates innate immunity, Am. J. Physiol. 275, R870–R878.
  • Gabrilovac, J. and Marotti, T. (2000) Gender-related differences in murine T- and B-lymphocyte proliferative ability in response to in vivo [Met5]enkephalin administration, Eur. J. Pharmacol. 392, 101–108.
  • Gave'riaux, C., Peluso, J., Simonin, F., Laforet, J. and Kieffer, B. (1995) Identification of k and d-opioid receptors transcripts in immune cells, FASEB Lett. 369, 272–276.
  • Goldstein, D.S. and McEwen, B. (2002) Allostasis, homeostasis and the nature of the stress, Stress 5, 55–58.
  • Hambrook, J.M., Morgan, B.A., Rance, M.J. and Smith, C.F.C. (1976) Mode of the deactivation of the enkephalins by rat and human plasma and rat brain homogenates, Nature 262, 782–783.
  • Hermann, G., Tovar, C.A., Beck, F.M. and Sheridan, J.F. (1994) Kinetics of glucocorticoid response to restraint stress and/or experimental influenza viral infection in two inbred strains of mice, J. Neuroimmunol. 9, 25–33.
  • Ignatowski, T.A. and Bidlack, J.M. (1999) Differential kappa-opioid receptor expression on mouse lymphocytes at varying stages of maturation and on mouse macrophages after selective elicitation, J. Pharmacol. Exp. Ther. 290, 2863–2870.
  • Irwin, M.R., Vale, W. and Rivier, C. (1990) Central corticotropinreleasing factor mediate the suppressive effect of stress on natural killer cytotoxicity, Endocrinology 126, 2837–2844.
  • Ishihara, S., Tsuchiya, S., Horie, S., Murayama, T. and Watanabe, K. (2001) Gastric acid secretion by central injection of dynorphin A-(1–17), an endogenous ligand of kappa-opioid receptor, in urethane-anesthetized rats, Jpn J. Pharmacol. 87, 14–20.
  • Jackson, R.L., Alexander, J.H. and Maier, S.F. (1980) Learned helplessness, inactivity and associative deficits: effects of inescapable shock on response choice escape learning, J. Exp. Psychol. Anim. Behav. Proc. 6, 1–20.
  • Jain, R., Zwickler, D., Hollander, C.S., Brand, H., Saperstein, A., Hutchinson, B., Brown, C. and Audhya, T. (1991) Corticotropinreleasing factor modulates the immune response to stress in the rat, Endocrinology 128, 1329–1336.
  • Janak, P.H., Schulteis, G. and Martinez, Jr., J.L. (1992) Uptake and metabolism of [3H]-Leu-enkephalin following either its intraperitoneal or subcutaneous administration to mice, Peptides 13, 551–555.
  • Jankovic', B.D. and Maric', D. (1987a) Enkephalins and anaphylactic shock: modulation and prevention of shock in the rat, Immunol. Lett. 15, 153–160.
  • Jankovic', B.D. and Maric', D. (1987b) Enkephalins and autoimmunity: differential effect of methionine-enkephalin on experimental allergic encephalomyelitis in Wistar and Lewis rats, J. Neurosci. Res. 18, 88–94.
  • Jankovic', B.D. and Maric', D. (1987c) Enkephalins and immunity. I. In vivo suppression and potentiation of humoral immune response, Ann. NY Acad. <i>Sci. 496, 115–125.
  • Jankovic', B.D. and Maric', D. (1991) Enkephalin-induced stimulation of humoral and cellular immune reactions in aged rats, Ann. NY Acad. Sci. 621, 135–147.
  • Jankovic', B.D. and Radulovic', J. (1992) Enkephalins, brain and immunity: modulation of immune responses by methionineenkephalin injected into the cerebral cavity, Int. J. Neurosci. 67, 241–270.
  • Kirst, A., Wack, C., Lutz, W.K., Eggert, A., Kampgen, E. and Fischer, W.H. (2002) Expression of functional kappa-opioid receptors on murine dendritic cells, Immunol. Lett. 84, 41–48.
  • Knutson, B., Burgdof, J. and Panksepp, J. (2002) Ultrasonic vocalizations as indices of affective states in rats, Psychol. Bull. 128, 961–977.
  • Kusnecov, A.W. and Rabin, B.S. (1993) Inescapable footshock exposure differentially alters antigen- and mitogen-stimulated spleen cell proliferation in rats, J. Neuroimmunol. 44, 33–42.
  • Larsen, P.J. and Mau, A.S.E. (1994) Effect of acute stress on expression of hypothalamic messenger ribonucleic acid encoding the endogenous opioid precursors preproenkephalin A and proopiomelanocortin, Peptides 15, 783–790.
  • Laudenslager, M.L., Fleshner, M., Hofstadter, P., Held, P.E., Simons, L. and Maier, S.F. (1988) Suppression of specific antibody production by inescapable shock: stability under varying conditions, Brain Behav. Immun. 2, 92–101.
  • Lee, R.K.K. and Maier, S.F. (1988) Inescapable shock and attention to internal versus external cues in a water maze discrimination task, J. Exp. Psychol. Anim. Behav. Proc. 14, 302–310.
  • Lewis, J.W., Shavit, Y., Terman, G.W., Nelson, L.R., Martin, F.C., Gale, R.P. and Liebskind, J.C. (1985) Involvement of opioid peptides in the analgesic, immunosuppressive and tumor-enhancing effects of stress, Psychopharmacol. Bull. 21, 479–484.
  • Lysle, D.T., Cunnick, J.E. and Rabin, B.S. (1990) Stressor-induced alteration of lymphocyte proliferation in mice: evidence for enhancement of mitogenic responsiveness, Brain Behav. Immun. 4, 269–277.
  • Maier, S.F., Sherman, J.E., Lewis, J.W., Terman, G.W. and Liebskind, J.C. (1983) The opioid/nonopioid nature of stress-induced analgesia and learned helplessness, J. Exp. Psychol. Anim. Behav. Proc. 9, 80–90.
  • Mansour, A., Khachaturian, H., Lewis, M.E., Akil, H. and Watson, S.J. (1988) Anatomy of CNS opioid receptors, Trends Neurosci. 11, 308–314.
  • Meerlo, P., Overkamp, G.J.F., Daan, S., van den Hoofdakker, R.H. and Koolhaas, J.M. (1996) Changes in behaviour and body weight following a single or double social defeat in rats, Stress 1, 21–32.
  • Mormede, P., Dantzer, R., Michaud, B., Kelley, K.W. and Le Moal, M. (1988) Influence of stressor predictability and behavioral control on lymphocyte reactivity, antibody responses and neuroendocrine activation in rats, Physiol. Behav. 43, 577–583.
  • Moynihan, J.A., Ader, R., Grota, L.J., Schachtman, T.R. and Cohen, N. (1990) The effects of stress on the development of immunological memory following low-dose antigen priming in mice, Brain Behav. Immun. 4, 1–12.
  • Moynihan, J.A., Karp, J.D., Cohen, N. and Cocke, R. (1994) Alterations in interleukin-4 and antibody production following pheromone exposure: role of glucocorticoids, J. Neuroimmunol. 54, 51–58.
  • Moynihan, J.A., Karp, J.D., Cohen, N. and Ader, R. (2000) Immune deviation following stress odor exposure: role of endogenous opioids, J. Immunol. 102, 145–153.
  • Nock, B., Giordano, A.L., Moore, B.W. and Cicero, T.J. (1993) Properties of the putative epsilon receptor-identification in rat, guinea-pig, cow, pig and chicken brain, J. Pharmacol. Exp. Ther. 264, 349–359.
  • Odio, M., Goliszek, A., Brodish, A. and Ricardo, Jr., M.J. (1986) Impairment of immune function after cessation of long-term chronic stress, Immunol. Lett. 13, 25–31.
  • Ottenweller, J.E., Natelson, B.H., Pitman, D.L. and Drastal, S.D. (1989) Adrenocortical and behavioral responses to repeated stressors: toward an animal model of chronic stress and stress-related mental illness, Biol. Psychiatr. 26, 829–841.
  • Ovadia, H., Magenheim, Y., Behar, O. and Rosen, H. (1996) Molecular characterization of immune derived proenkephalin mRNA and the involvement of the adrenergic system in its expression in rat lymphoid cells, J. Neuroimmunol. 68, 77–83.
  • Pan, Y.Z., Li, D.P., Chen, S.R. and Pan, H.L. (2002) Activation of deltaopioid receptors excites spinally projecting locus coeruleus neurons through inhibition of GABAergic inputs, J. Neurophysiol. 88, 2675–2683.
  • Parsons, C.G., Czlonkowski, A., Stein, C. and Herz, A. (1990) Peripheral opioid receptors mediating antinociception in inflammation: activation by endogenous opioids and role of the pituitary-adrenal axis, Pain 41, 81–93.
  • Pierzchala, K. and Van Loon, G.R. (1990) Plasma native and peptidasederivable Met-enkephalin responses to restraint stress in rats. Adaptation to repeated restraint, J. Clin. Investig. 85, 861–873.
  • Radulovic', J. and Jankovic', B.D. (1994) Opposing activities of brain opioid receptors in the regulation of humoral and cell-mediated immune response in the rat, Brain Res. 661, 189–195.
  • Radulovic', J., Dimitrijevic', M., Laban, O., Stanojevic', S., Vasiljevic', T., Kovac?evic'-Jovanovic', V. and Markovic', B.M.M. (1995) Effect of Met-enkephalin and opioid antagonists on rat macrophages, Peptides 16, 1209–1213.
  • Rinner, I., Schauenstein, K., Mangge, H., Porta, S. and Kvetnansky, R. (1992) Opposite effects of mild and severe stress on in vitro activation of rat peripheral blood lymphocytes, Brain Behav. Immun. 6, 130–140.
  • Sacerdote, P., Manfredi, B., Bianchi, M. and Panerai, A.E. (1994) Intermittent but not continuous inescapable footshock stress affects immune responses and immunocyte beta-endorphin concentrations in the rat, Brain Behav. Immun. 8, 251–260.
  • Scha¨fer, M., Carter, L. and Stein, C. (1994) Interleukin-1 beta and corticotropin-releasing factor inhibit pain by releasing opioids from immune cells in inflamed tissue, Proc. Natl Acad. Sci. 91, 4219–4223.
  • Sedqui, M., Roy, S., Ramakrishnan, S. and Loh, H.H. (1996) Expression cloning of a full-length cDNA coding delta opioid receptor from mouse thymocytes, J. Neuroimmunol. 65, 167–170.
  • Shavit, Y., Lewis, J.W., Terman, G.W., Gale, R.P. and Liebskind, J.C. (1984) Opioid peptides mediate the suppressive effect of stress on natural killer cell cytotoxicity, Science 223, 188–190.
  • Shurin, M.R., Kusnecov, A.W., Riechman, S.E. and Rabin, B.S. (1995) Effect of a conditioned aversive stimulus on the immune response in three strains of rats, Psychoneuroendocrinology 20, 837–849.
  • Simon, E.J. (1986) Recent studies on opioid receptors: heterogeneity and purification, Ann. NY Acad. Sci. 463, 31–45.
  • Solbrig, M.V., Koob, G.F. and Lipkin, W.I. (2002) Key role for enkephalinergic tone in cortico-striatal thalamic function, Eur. J. Neurosci. 16, 1819–1822.
  • Sonnenfeld, G., Cunnick, J.E., Armfield, A.V., Wood, P.G. and Rabin, B.S. (1992) Stress-induced alterations in interferon production and class II histocompatibility antigen expression, Brain Behav. Immun. 6, 170–178.
  • Stefano, G.B., Scharrer, B., Smith, E.M., Hughes, T.K. Jr., Magazine, H.I., Bilfinger, T.V., Hartman, A.R., Fricchione, G.L., Liu, Y. and Makman, M.H. (1996) Opioid and opiate immunoregulatory processes, Crit. Rev. Immunol. 16, 109–144.
  • Stein, C., Hassan, A.H.S., Przewlocki, R., Gramsch, C., Peter, K. and Herz, A. (1990) Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation, Proc. Natl Acad. Sci. 87, 5935–5939.
  • Stanojevic', S., Vujic', V., Kovac?evic'-Jovanovic', V. and Dimitrijevic', M. (2002) Strain-specific effects of corticosterone (CORT) and Neuropeptide Y (NPY) on H2O2 production in macrophages from stressed rats, Stress 5, 82.
  • Sutton, L.C., Fleshner, M., Mazzeo, R., Maier, S.F. and Watkins, L.R. (1994) A permissive role of corticosterone in an opioid form of stressinduced analgesia: blockade of opiate analgesia is not due to stressinduced hormone release, Brain Res. 663, 19–29.
  • Suzuki, S., Chuang, T.K., Chuang, L.F., Doi, R.H. and Chuang, R.Y. (2001) Morphine upregulates kappa-opioid receptors of human lymphocytes, Adv. Exp. Med. Biol. 493, 81–87.
  • Tarcic, N., Levitan, G., Ben-Yosef, D., Prous, D., Ovadia, H. and Weiss, D.W. (1995) Restraint stress-induced changes in lymphocyte subsets and the expression of adhesion molecules, Neuroimmunomodulation 2, 249–257.
  • Tseng, L. (2001) Evidence for epsilon-opioid receptor-mediated beta-endorphin-induced analgesia, Trends Pharmacol. Sci. 22, 623–630.
  • Vujic'-Redz?ic', V., Dimitrijevic', M., Stanojevic', S., Kovac?evic'-Jovanovic', V., Miletic', T. and Radulovic', J. (2000) Peripheral effect of methionine-enkephalin on inflammatory reaction and behavior in the rat, Neuroimmunomodulation 8, 70–77.
  • Wiedenmayer, C.P., Noailles, P.A., Angulo, J.A. and Barr, G.A. (2002) Stress-induced preproenkephalin mRNA expression in the amygdala changes during early ontogeny in the rat, Neuroscience 114, 7–11.
  • Wood, P.G., Karol, M.H., Kusnecov, A.W. and Rabin, B.S. (1993) Enhancement of antigen-specific humoral and cell-mediated immunity by electric footshock stress in rats, Brain Behav. Immun. 7, 121–134.
  • Zalaquett, C. and Thiessen, D. (1991) The effects of odor from stressed mice on conspecific behavior, Physiol. Behav. 50, 221–227.
  • Zalcman, S. and Anisman, H. (1993) Acute and chronic stressor effects on the antibody response to sheep red blood cells, Pharmacol. Biochem. Behav. 46, 445–452.
  • Zalcman, S., Minkiewicz-Janda, A., Richter, M. and Anisman, H. (1988) Critical periods associated with stressor effects on antibody titers and on the plaque-forming cell response to sheep red blood cells, Brain Behav. Immun. 2, 254–266.
  • Zhang, D., Kishihara, K., Wang, B., Mizobe, K., Kubo, C. and Nomoto, K. (1998) Restraint stress induced immunosuppression by inhibiting leukocyte migration and Th1 cytokine expression during the intraperitoneal infection of Listeria monocytogenes, J. Neuroimmunol. 91, 139–151.
  • Zwilling, B.S., Brown, D., Christner, R., Faris, M., Hilburger, M., Mc Peek, M., Van Epps, C. and Hartlaub, B.A. (1990) Differential effect of restraint stress on MHC II expression by murine peritoneal macrophages, Brain Behav. Immun. 4, 330–338.

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