Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Oct 25;91(22):10440–10444. doi: 10.1073/pnas.91.22.10440

Emotional stress induced by parachute jumping enhances blood nerve growth factor levels and the distribution of nerve growth factor receptors in lymphocytes.

L Aloe 1, L Bracci-Laudiero 1, E Alleva 1, A Lambiase 1, A Micera 1, P Tirassa 1
PMCID: PMC45036  PMID: 7937971

Abstract

We examined the plasma nerve growth factor (NGF) level and the distribution of NGF receptors in peripheral lymphocytes of young soldiers (mean age, 20-24 yr) experiencing the thrill of a novice about to make their first parachute jumps. Blood was collected from soldiers who knew they were selected to jump (n = 26), as well as from soldiers who knew they were not selected (n = 17, controls). The former group was sampled the evening before the jump and 20 min after landing. Compared with controls, NGF levels increased 84% in prejump and 107% in postjump sampling. Our studies also showed that the increase of NGF levels preceded the increase of plasma cortisol and adrenocorticotropic hormone. No changes in the baseline levels of circulating interleukin 1 beta or tumor necrosis factor were found, suggesting that the increased levels of NGF were not correlated with change in these cytokines. Moreover, immunofluorescence analysis demonstrated that parachuting stress enhances the distribution of low-affinity p75LNGFR and high-affinity p140trkA NGF receptors in circulating peripheral blood mononuclear cells. These observations suggest that the release of NGF might be involved in the activation of cells of the immune system and is most probably associated with homeostatic adaptive mechanisms, as previously shown for stressed rodents.

Full text

PDF
10440

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aloe L., Alleva E., Böhm A., Levi-Montalcini R. Aggressive behavior induces release of nerve growth factor from mouse salivary gland into the bloodstream. Proc Natl Acad Sci U S A. 1986 Aug;83(16):6184–6187. doi: 10.1073/pnas.83.16.6184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baldwin H. A., Rassnick S., Rivier J., Koob G. F., Britton K. T. CRF antagonist reverses the "anxiogenic" response to ethanol withdrawal in the rat. Psychopharmacology (Berl) 1991;103(2):227–232. doi: 10.1007/BF02244208. [DOI] [PubMed] [Google Scholar]
  3. Barde Y. A., Edgar D., Thoenen H. Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1982;1(5):549–553. doi: 10.1002/j.1460-2075.1982.tb01207.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bigi S., Maestripieri D., Aloe L., Alleva E. NGF decreases isolation-induced aggressive behavior, while increasing adrenal volume, in adult male mice. Physiol Behav. 1992 Feb;51(2):337–343. doi: 10.1016/0031-9384(92)90150-z. [DOI] [PubMed] [Google Scholar]
  5. Bing O., Möller C., Engel J. A., Söderpalm B., Heilig M. Anxiolytic-like action of centrally administered galanin. Neurosci Lett. 1993 Dec 24;164(1-2):17–20. doi: 10.1016/0304-3940(93)90846-d. [DOI] [PubMed] [Google Scholar]
  6. Bischoff S. C., Dahinden C. A. Effect of nerve growth factor on the release of inflammatory mediators by mature human basophils. Blood. 1992 May 15;79(10):2662–2669. [PubMed] [Google Scholar]
  7. Brodie C., Gelfand E. W. Functional nerve growth factor receptors on human B lymphocytes. Interaction with IL-2. J Immunol. 1992 Jun 1;148(11):3492–3497. [PubMed] [Google Scholar]
  8. De Simone R., Alleva E., Tirassa P., Aloe L. Nerve growth factor released into the bloodstream following intraspecific fighting induces mast cell degranulation in adult male mice. Brain Behav Immun. 1990 Mar;4(1):74–81. doi: 10.1016/0889-1591(90)90008-e. [DOI] [PubMed] [Google Scholar]
  9. Dugué B., Leppänen E. A., Teppo A. M., Fyhrquist F., Gräsbeck R. Effects of psychological stress on plasma interleukins-1 beta and 6, C-reactive protein, tumour necrosis factor alpha, anti-diuretic hormone and serum cortisol. Scand J Clin Lab Invest. 1993 Oct;53(6):555–561. [PubMed] [Google Scholar]
  10. Dunn A. J., File S. E. Corticotropin-releasing factor has an anxiogenic action in the social interaction test. Horm Behav. 1987 Jun;21(2):193–202. doi: 10.1016/0018-506x(87)90044-4. [DOI] [PubMed] [Google Scholar]
  11. Ernfors P., Ibáez C. F., Ebendal T., Olson L., Persson H. Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: developmental and topographical expression in the brain. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5454–5458. doi: 10.1073/pnas.87.14.5454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Esterling B., Rabin B. S. Stress-induced alteration of T-lymphocyte subsets and humoral immunity in mice. Behav Neurosci. 1987 Feb;101(1):115–119. doi: 10.1037//0735-7044.101.1.115. [DOI] [PubMed] [Google Scholar]
  13. Hattori A., Tanaka E., Murase K., Ishida N., Chatani Y., Tsujimoto M., Hayashi K., Kohno M. Tumor necrosis factor stimulates the synthesis and secretion of biologically active nerve growth factor in non-neuronal cells. J Biol Chem. 1993 Feb 5;268(4):2577–2582. [PubMed] [Google Scholar]
  14. Heilig M., McLeod S., Brot M., Heinrichs S. C., Menzaghi F., Koob G. F., Britton K. T. Anxiolytic-like action of neuropeptide Y: mediation by Y1 receptors in amygdala, and dissociation from food intake effects. Neuropsychopharmacology. 1993 Jun;8(4):357–363. doi: 10.1038/npp.1993.35. [DOI] [PubMed] [Google Scholar]
  15. Heinrichs S. C., Pich E. M., Miczek K. A., Britton K. T., Koob G. F. Corticotropin-releasing factor antagonist reduces emotionality in socially defeated rats via direct neurotropic action. Brain Res. 1992 May 29;581(2):190–197. doi: 10.1016/0006-8993(92)90708-h. [DOI] [PubMed] [Google Scholar]
  16. Herberman R. B., Ortaldo J. R. Natural killer cells: their roles in defenses against disease. Science. 1981 Oct 2;214(4516):24–30. doi: 10.1126/science.7025208. [DOI] [PubMed] [Google Scholar]
  17. Heumann R., Lindholm D., Bandtlow C., Meyer M., Radeke M. J., Misko T. P., Shooter E., Thoenen H. Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8735–8739. doi: 10.1073/pnas.84.23.8735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Horigome K., Bullock E. D., Johnson E. M., Jr Effects of nerve growth factor on rat peritoneal mast cells. Survival promotion and immediate-early gene induction. J Biol Chem. 1994 Jan 28;269(4):2695–2702. [PubMed] [Google Scholar]
  19. Jessop J. J., Gale K., Bayer B. M. Enhancement of rat lymphocyte proliferation after prolonged exposure to stress. J Neuroimmunol. 1987 Oct;16(2):261–271. doi: 10.1016/0165-5728(87)90080-4. [DOI] [PubMed] [Google Scholar]
  20. Larsson P. T., Olsson G., Hjemdahl P., Nilsson J. Mental stress and adrenaline increase plasma growth factor activity in humans. Acta Physiol Scand. 1989 Dec;137(4):565–566. doi: 10.1111/j.1748-1716.1989.tb08803.x. [DOI] [PubMed] [Google Scholar]
  21. Leon A., Buriani A., Dal Toso R., Fabris M., Romanello S., Aloe L., Levi-Montalcini R. Mast cells synthesize, store, and release nerve growth factor. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3739–3743. doi: 10.1073/pnas.91.9.3739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Levi-Montalcini R. The nerve growth factor 35 years later. Science. 1987 Sep 4;237(4819):1154–1162. doi: 10.1126/science.3306916. [DOI] [PubMed] [Google Scholar]
  23. Luppi P., Levi-Montalcini R., Bracci-Laudiero L., Bertolini A., Arletti R., Tavernari D., Vigneti E., Aloe L. NGF is released into plasma during human pregnancy: an oxytocin-mediated response? Neuroreport. 1993 Aug;4(8):1063–1065. doi: 10.1097/00001756-199308000-00018. [DOI] [PubMed] [Google Scholar]
  24. Maestripieri D., De Simone R., Aloe L., Alleva E. Social status and nerve growth factor serum levels after agonistic encounters in mice. Physiol Behav. 1990 Jan;47(1):161–164. doi: 10.1016/0031-9384(90)90056-a. [DOI] [PubMed] [Google Scholar]
  25. Matsuda H., Coughlin M. D., Bienenstock J., Denburg J. A. Nerve growth factor promotes human hemopoietic colony growth and differentiation. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6508–6512. doi: 10.1073/pnas.85.17.6508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mohammed A. H., Henriksson B. G., Söderström S., Ebendal T., Olsson T., Seckl J. R. Environmental influences on the central nervous system and their implications for the aging rat. Behav Brain Res. 1993 Nov 30;57(2):183–191. doi: 10.1016/0166-4328(93)90134-c. [DOI] [PubMed] [Google Scholar]
  27. Nisipeanu P., Korczyn A. D. Psychological stress as risk factor for exacerbations in multiple sclerosis. Neurology. 1993 Jul;43(7):1311–1312. doi: 10.1212/wnl.43.7.1311. [DOI] [PubMed] [Google Scholar]
  28. Otten U., Ehrhard P., Peck R. Nerve growth factor induces growth and differentiation of human B lymphocytes. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10059–10063. doi: 10.1073/pnas.86.24.10059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Patterson P. H., Nawa H. Neuronal differentiation factors/cytokines and synaptic plasticity. Cell. 1993 Jan;72 (Suppl):123–137. doi: 10.1016/s0092-8674(05)80032-7. [DOI] [PubMed] [Google Scholar]
  30. Rende M., Provenzano C., Tonali P. Modulation of low-affinity nerve growth factor receptor in injured adult rat spinal cord motoneurons. J Comp Neurol. 1993 Dec 22;338(4):560–574. doi: 10.1002/cne.903380406. [DOI] [PubMed] [Google Scholar]
  31. Ritz J., Campen T. J., Schmidt R. E., Royer H. D., Hercend T., Hussey R. E., Reinherz E. L. Analysis of T-cell receptor gene rearrangement and expression in human natural killer clones. Science. 1985 Jun 28;228(4707):1540–1543. doi: 10.1126/science.2409597. [DOI] [PubMed] [Google Scholar]
  32. Ross A. H., Grob P., Bothwell M., Elder D. E., Ernst C. S., Marano N., Ghrist B. F., Slemp C. C., Herlyn M., Atkinson B. Characterization of nerve growth factor receptor in neural crest tumors using monoclonal antibodies. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6681–6685. doi: 10.1073/pnas.81.21.6681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schedlowski M., Jacobs R., Stratmann G., Richter S., Hädicke A., Tewes U., Wagner T. O., Schmidt R. E. Changes of natural killer cells during acute psychological stress. J Clin Immunol. 1993 Mar;13(2):119–126. doi: 10.1007/BF00919268. [DOI] [PubMed] [Google Scholar]
  34. Schwartz J. T., Brotman A. W. A clinical guide to antipsychotic drugs. Drugs. 1992 Dec;44(6):981–992. doi: 10.2165/00003495-199244060-00007. [DOI] [PubMed] [Google Scholar]
  35. Solomon G. F. Psychoneuroimmunology: interactions between central nervous system and immune system. J Neurosci Res. 1987;18(1):1–9. doi: 10.1002/jnr.490180103. [DOI] [PubMed] [Google Scholar]
  36. Spillantini M. G., Aloe L., Alleva E., De Simone R., Goedert M., Levi-Montalcini R. Nerve growth factor mRNA and protein increase in hypothalamus in a mouse model of aggression. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8555–8559. doi: 10.1073/pnas.86.21.8555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Taniuchi M., Clark H. B., Schweitzer J. B., Johnson E. M., Jr Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties. J Neurosci. 1988 Feb;8(2):664–681. doi: 10.1523/JNEUROSCI.08-02-00664.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Taniuchi M., Schweitzer J. B., Johnson E. M., Jr Nerve growth factor receptor molecules in rat brain. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1950–1954. doi: 10.1073/pnas.83.6.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Thorpe L. W., Werrbach-Perez K., Perez-Polo J. R. Effects of nerve growth factor on the expression of interleukin-2 receptors on cultured human lymphocytes. Ann N Y Acad Sci. 1987;496:310–311. doi: 10.1111/j.1749-6632.1987.tb35781.x. [DOI] [PubMed] [Google Scholar]
  40. Thorpe L. W., Werrbach-Perez K., Perez-Polo J. R. Effects of nerve growth factor on the expression of interleukin-2 receptors on cultured human lymphocytes. Ann N Y Acad Sci. 1987;496:310–311. doi: 10.1111/j.1749-6632.1987.tb35781.x. [DOI] [PubMed] [Google Scholar]
  41. Weskamp G., Otten U. An enzyme-linked immunoassay for nerve growth factor (NGF): a tool for studying regulatory mechanisms involved in NGF production in brain and in peripheral tissues. J Neurochem. 1987 Jun;48(6):1779–1786. doi: 10.1111/j.1471-4159.1987.tb05736.x. [DOI] [PubMed] [Google Scholar]
  42. Wood S. J., Pritchard J., Sofroniew M. V. Re-expression of Nerve Growth Factor Receptor after Axonal Injury Recapitulates a Developmental Event in Motor Neurons: Differential Regulation when Regeneration is Allowed or Prevented. Eur J Neurosci. 1990;2(7):650–657. doi: 10.1111/j.1460-9568.1990.tb00454.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES