Skip to main content
SpringerLink
Log in

Changes of natural killer cells during acute psychological stress

  • Original Articles
  • Published:
Journal of Clinical Immunology Aims and scope Submit manuscript

Abstract

Emotional stress is often followed by increased susceptibility to infections. One major role in the immediate immune response to infection is played by natural killer (NK) cells. This study was designed to establish whether acute psychological stress influences cellular immune functions and to elucidate the role of endocrine parameters as potent mediators of stress induced alterations of the immune system. Forty-five first-time tandem parachutists were examined continuously for their plasma concentrations of cortisol and catecholamines from 120 min before to 60 min after jumping. Lymphocyte subsets, NK activity, and ADCC were determined 2 hr before, immediately after, and 1 hr after jumping. There was a significant increase in sympathetic-adrenal hormones during (adrenaline, noradrenaline) and shortly after jumping (cortisol). Lymphocyte subsets and the functional capacity of NK cells revealed an increase immediately after jumping followed by a decrease significantly below starting values 1 hr later. These changes were significantly correlated to plasma concentrations of noradrenaline. Thus, quick mobilization of NK cells is suggested as one major mechanism for this effective adaptation of the immune system to stress situations.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Ader R, Felten DL, Cohen N: Psychoneuroimmunology. San Diego, Academic Press, 1991

    Google Scholar 

  2. Glaser R, Rice J, Speicher CE, Stout JC, Kiecolt-Glaser JK: Stress depresses interferon production by leucocytes concomitant with a decrease in natural killer cell activity. Behav Neurosci 100:675–678, 1986

    Google Scholar 

  3. Kiecolt-Glaser JK, Garner W, Speicher C, Penn GM, Holliday J, Glaser R: Psychological modifiers of immunocompetence in medical students. Psychosom Med 46:7–14, 1984

    Google Scholar 

  4. Irwin M, Daniels M, Smith TL, Bloom E, Weiner H: Impaired natural killer activity during bereavement. Brain Behav Immun 1:98–104, 1987

    Google Scholar 

  5. Cohen S, Tyrrell DAJ, Smith AP: Psychological stress and susceptibility to the common cold. N Engl J Med 325:606–612, 1991

    Google Scholar 

  6. Levy S, Herberman R, Lippman M, d'Angelo T: Correlation of stress factors with sustained depression of natural killer cell activity and predicted prognosis in patients with breast cancer. J Clin Oncol 5:348–353, 1987

    Google Scholar 

  7. Hercend T, Schmidt RE: Characteristics and uses of natural killer cells. Immunol Today 9:291–293, 1988

    Google Scholar 

  8. Schmidt RE, Michon J, MacMahon H, Woronicz J, Schlossman SF, Reinherz EL, Ritz J: Enhancement of natural killer (NK) function through activation of the T11/E rosette receptor. J Clin Invest 79:305–308, 1987

    Google Scholar 

  9. Trinchieri G: Biology of natural killer cells. Adv Immunol 47:187–376, 1989

    Google Scholar 

  10. Herberman R, Ortaldo J: Natural killer cells: Their role in defenses against disease. Science 214:24–30, 1981

    Google Scholar 

  11. Ritz J, Campen TJ, Schmidt RE, Royer HD, Hercend T, Hussey RE, Reinherz EL: Analysis of T cell receptor gene rearrangement and expression in human natural killer (NK) clones. Science 228:1540–1543, 1985

    Google Scholar 

  12. Lanier LL, Testi R, Bindl J, Phillips JH: Identity of Leu-19 (CD56) leukocyte differentiation antigen and neural cell adhesion molecule. J Exp Med 169:2233–2238, 1989

    Google Scholar 

  13. Hellstrand K, Hermodsson S, Strannegard Ö: Evidence for a β-adrenoceptor-mediated regulation of human natural killer cells. J Immunol 134:4095–4099, 1985

    Google Scholar 

  14. Tønnesen E, Christensen NJ, Brinkløv MM: Natural killer cell activity during cortisol and adrenaline infusion in healthy volunteers. Eur J Clin Invest 17:497–503, 1987

    Google Scholar 

  15. Kappel M, Tvede N, Galbo H, Haahr PM, Kjaer M, Linstow M, Klarlund K, Pedersen BK: Evidence that the effect of physical exercise on NK cell activity is mediated by epinephrine. J Appl Physiol 70:2530–2534, 1991

    Google Scholar 

  16. Brahmi Z, Thomas JE, Park M, Park M, Dowdeswell IRG: The effect of acute exercise on natural killer-cell activity of trained and sedentary subjects. J Clin Immunol 5:321–328, 1985

    Google Scholar 

  17. Pedersen BK, Tvede N, Hansen FR, Andersen V, Bendix T, Bendixen G, Bendtzen K, Galbo H, Haahr PM, Klarlund K, Sylvest J, Thomsen BS, Halkjaer-Kristensen J: Modulation of natural killer cell activity in peripheral blood by physical exercise. Scand J Immunol 27:673–678, 1988

    Google Scholar 

  18. Landmann RMA, Müller FB, Perini CH, Wesp M, Erne P, Bühler FR: Changes of immunoregulatory cells induced by psychological and physical stress: Relationship to plasma catecholamines. Clin Exp Immunol 58:127–135, 1984

    Google Scholar 

  19. Plaut M: Lymphocyte hormone receptors. Annu Rev Immunol 5:621–669, 1987

    Google Scholar 

  20. Ursin H, Baade E, Levine S: Psychobiology of Stress. A Study of Coping Men. New York, Academic Press, 1978

    Google Scholar 

  21. Schedlowski M, Wiechert D, Wagner TOF, Tewes U: Acute psychological stress increases plasma levels of cortisol, prolactin and TSH. Life Sci 50:1201–1205, 1992

    Google Scholar 

  22. Schedlowski M, Tewes U: Physiological arousal and perception of bodily state during parachute jumping. Psychophysiology 29:95–103, 1992

    Google Scholar 

  23. Laux L, Glanzmann P, Schaffner P, Spielberger CD: State-Trait-Angst Inventar (STAI). Weinheim, Beltz-Testgesell-schaft

  24. Kiparski Rv, Steffens HP: Possibilities of wireless recording of biosignals by means of digital memories. Biomed Tech 30:76–84, 1985

    Google Scholar 

  25. Knapp W, Dörken B, Gilks WR, Rieber EP, Schmidt RE, Stein H, Kr. von dem Borne AEG: Leukocyte Typing IV. Oxford, University Press, 1989

    Google Scholar 

  26. Schmidt RE, Bartley G, Levine H, Schlossmann SF, Ritz J: Functional characterization of LFA-1 antigens in the interaction of human NK clones and target cells. J Immunol 135:1020–1025, 1985

    Google Scholar 

  27. Schmidt RE, Mac Dermott RP, Bartley GT, Bertovich M, Amato DA, Austen KF, Schlossman SF, Stevens RL, Ritz J: Specific release of proteoglycans from human natural killer cells during target lysis. Nature 318:289–291, 1985

    Google Scholar 

  28. Pross HF, Baines MG, Rubin P, Shragge P, Patterson MS: Spontaneous human lymphocyte-mediated cytotoxicity against tumor target cells. IX. The quantitation of natural killer cell activity. J Clin Immunol 1:51–63, 1981

    Google Scholar 

  29. Vasey MW, Thayer JF: The continuing problem of false positives in repeated measures ANOVA in psychophysiology: A multivariate solution. Psychophysiology 24:479–486, 1987

    Google Scholar 

  30. Khansari DN, Murgo AJ, Faith RE: Effects of stress on the immune system. Immunol Today 11:170–175, 1990

    Google Scholar 

  31. Nieman DC, Nehlsen-Cannarella SL, Donohue KM, Chritton DBW, Haddock BL, Stout RW, Lee JW: The effect of acute moderate exercise on leukocyte and lymphocyte subpopulations. Med Sci Sport Exer 23:578–585, 1991

    Google Scholar 

  32. Jacobs R, Stoll M, Stratmann G, Leo R, Link H, Schmidt RE: CD16− CD56+ NK cells after bone marrow transplantation. Blood 79, 3239–3244, 1992

    Google Scholar 

  33. Witte T, Wordelmann K, Schmidt RE: Heterogeneity of human NK cells in the spleen. Immunology 69:166–170, 1989

    Google Scholar 

  34. Gatti G, Cavallo R, Sartori ML, Del Ponte D, Masera R, Salvadori A, Carignola R, Angeli A: Inhibition by cortisol of human natural killer (NK) cell activity. J Steroid Biochem 26:49–58, 1987

    Google Scholar 

  35. Crary B, Hauser SL, Borysenko M, Kutz I, Hoban C, Ault KA, Weiner HL, Benson H: Epinephrine-induced changes in the distribution of lymphocyte subsets in peripheral blood of humans. J Immunol 131:1178–1181, 1983

    Google Scholar 

  36. Khan MM, Sansoni P, Silverman ED, Engleman ED, Melmon KL: Beta-adrenergic receptors on human suppressor, helper, and cytolytic lymphocytes. Biochem Pharmacol 35:1137–1142, 1986

    Google Scholar 

  37. Van Tits LJH, Michel MC, Grosse-Wilde H, Happel M, Eigler FW, Soliman A, Brodde OE: Catecholamines increase lymphocyte β2-adrenergic receptors via a β2-adrenergic, spleen-dependent process. Am J Physiol 258:E191-E202, 1990

    Google Scholar 

  38. Maisel AS, Harris T, Rearden CA, Michel MC: β-adrenergic receptors in lymphocyte subsets after exercise. Circulation 82:2003–2010, 1990

    Google Scholar 

  39. Locke S, Kraus L, Kutz I, Edbril S, Phillips K, Benson H: Altered natural killer activity during norepinephrine infusion in humans.In Neuroimmunomodulation, NH Spector (ed). Proceedings of the First International Workshop on Neuroimmunomodulation, Bethesda, Maryland, 1984, p 297

  40. Felten DL, Felten SY, Bellinger DL, Carlson SL, Ackerman KD, Madden KS, Olschowki JA, Livnat S: Noradrenergic sympathetic neural interactions with the immune system: Structure and function. Immunol Rev 100:225–260, 1987

    Google Scholar 

  41. Williamson SA, Knight RA, Lightman SL, Hobbs JR: Differential effects of β-endorphin fragments on human natural killing. Brain Behav Immun 1:329–335, 1987

    Google Scholar 

  42. Heijnen CJ, Kavelaars A, Ballieux RE: β-endorphin: Cytokine and neuropeptide. Immunol Rev 119:41–63, 1991

    Google Scholar 

  43. Naliboff BD, Benton D, Solomon GF, Morley JE, Fahey JL, Bloom ET, Makinodan T, Gilmore SL: Immunological changes in young and old adults during brief laboratory stress. Psychosom Med 53:121–132, 1991

    Google Scholar 

  44. Fiatarone MA, Morley JE, Bloom ET, Benton D, Makinodan T, Solomon GF: Endogenous opioids and the exercise-induced augmentation of natural killer cell activity. J Lab Clin Med 112:544–552, 1988

    Google Scholar 

  45. Shimizu Y, Newman W, Tanaka Y, Shaw S: Lymphocyte interaction with endothelial cells. Immunol Today 13:106–112, 1992

    Google Scholar 

  46. Westermann J, Pabst R: Distribution of lymphocyte subsets and natural killer cells in the human body. Clin Invest 70:539–544, 1992

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Medical Psychology, Medizinische Hochschule Hannover, Postfach 61 01 80, 3000, Hannover 61, FRG

    Manfred Schedlowski & Uwe Tewes

  2. Division of Immunology, Medizinische Hochschule Hannover, Postfach 61 01 80, 3000, Hannover 61, FRG

    Roland Jacobs, Gertrud Stratmann & Reinhold E. Schmidt

  3. Division of Endocrinology, Medizinische Hochschule Hannover, Postfach 61 01 80, 3000, Hannover 61, FRG

    Stefan Richter, Andreas Hädicke & Thomas O. F. Wagner

Authors
  1. Manfred Schedlowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roland Jacobs
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gertrud Stratmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefan Richter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andreas Hädicke
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Uwe Tewes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Thomas O. F. Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Reinhold E. Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schedlowski, M., Jacobs, R., Stratmann, G. et al. Changes of natural killer cells during acute psychological stress. J Clin Immunol 13, 119–126 (1993). https://doi.org/10.1007/BF00919268

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00919268

Key words

Search

Navigation