Skip to main content

Advertisement

Log in

Geschlechtsunterschiede Bei Der Neuromodulation von Mukosamastzellen im Rattenjejunum

Different response of mucosal mast cells in rat jejunum to electrical stimulation of the cervical vagal nerves depending on sex

  • Originalarbeit
  • Published:
Langenbecks Archiv für Chirurgie Aims and scope Submit manuscript

Abstract

The effect of electrical stimulation of both cervical vagal nerves on mucosal mast cells in the jejunum was investigated in an in vivo animal model with rats of both sexes. Males showed a significant increase of mast cell densities after electrical stimulation (1.0 mA, 5 Hz, 5 ms, 12 min) in the lamina propria. Simultaneously, we observed a significant increase of tissue histamine levels (ANOVA:P<0.05), whereas serum levels remained unchanged. However, even though females had significantly higher levels throughout compared to males (ANOVA;P<0.05), they did not show any significant reaction to electrical stimulation. These in vivo data support morphological and in vitro data from other investigators, who hypothesized a functional interaction between mucosal mast cells and nerves. However, degranulation seems to be a poor in situ indicator for mast-cell stimulation, as mastcell densities increased in males, while the percentage of degranulated cells remained the same in all groups (about 40%). Instead, electrical stimulation of the vagal nerve seems to trigger histamine synthesis, or simply stabilization of mast cells. Interestingly, this phenomenon seems to be sex-dependent, suggesting a regulatory role for sex hormones in this scenario.

Zusammenfassung

Im Rahmen einer tierexperimentellen Studie an der Ratte wurde der Effekt einer elektrischen In-vivo-Stimulation des zervikalen N. vagus auf die Mukosamastzellen im Jejunum untersucht. Dabei zeigten männliche Tiere nach Stimulation mit 1,0 mA (5 Hz, 5 ms, 12 min) eine deutliche Zunahme der Mastzelldichte in der Lamina propria; gleichzeitig kam es zu einem signifikanten Anstieg des Gewebehistaminspiegels (ANOVA:p<0,05), während die Serumspiegel nicht signifikant anstiegen. Anders sah dies bei den weiblichen Tieren aus, die zwar im Vergleich zu den Männchen durchweg höhere Ausganswerte boten (p<0,05), bei denen jedoch die elektrische Stimulation keine signifikanten Veränderungen bewirkte. Diese Studie bestätigt in vivo die Bedeutung morphologischer und funktioneller In-vitro Daten, die eine funktionelle Interaktion zwischen Mukosamastzellen und Nerven nahelegen. Im Gegensatz zu den klassischen allergischen Reaktionen löst die elektrische Stimulation jedoch offensichtlich keine Degranulation der Mastzelle aus (ca. 40% degranulierte Mastzellen in allen Gruppen), sondern eher eine Stabilisierung oder verstärkte Histaminsynthese der Mastzellen. Zusätzlich scheinen die Phänomene der Neuroimmunmodulation teilweise von Sexualhormonen beeinflußt zu werden, wie die Geschlechtsunterschiede nahelegen.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Literatur

  1. Ader R (1992) On the clinical relevance of psychoneuroimmunology. Clin Immunol Immunopathol 64:6–9

    Article  PubMed  CAS  Google Scholar 

  2. Aldenborg F, Enerbäck L (1985) Histamine content and mast cell numbers in tissues of normal and athymic rats. Agents Actions 17:454–459

    Article  CAS  Google Scholar 

  3. Arizono N, Matsuda S, Hattori T, Kojima Y, Maeda T, Galli SJ (1990) Anatomical variation in mast cell nerve associations in the rat small intestine, heart, lung, and skin: Similarities between neural processes and mast cells, eosinophils, or plasma cells in the jejunal lamina proprial. Lab Invest 62:626–634

    PubMed  CAS  Google Scholar 

  4. Bäck N, Ahonen M, Häppölä O, Kivilaakso E, Kiviluoto T (1994) Effet of vagotomy on expression of neuropeptides and histamine in rat oxyntic mucosa. Dig Dis Sci 2:353–361

    Article  Google Scholar 

  5. Berthoud HR, Carlson NR, Powley TL (1991) Topography of efferent vagal innervation of the rat gastrointestinal tract. Am J Physiol 260:R200-R207

    PubMed  CAS  Google Scholar 

  6. Betancur C, Neveu PJ, Vitiello S, Le Moal M (1991) Natural killer cell activity is associated with brain asymmetry in male mice. Brain Behav Immun 5:162–169

    Article  PubMed  CAS  Google Scholar 

  7. Cooke H (1986) Neurobiology of the intestinal mucosa. Gastroenterology 40:1057

    Google Scholar 

  8. Dimitriadou V, Buzzi MG, Moskowitz MA, Theoharides TC (1991) Trigeminal sensory fiber stimulation induces morphological changes reflecting secretion in rat dura mater. Neuroscience 44:97–107

    Article  PubMed  CAS  Google Scholar 

  9. Enerbäck L (1966) Mast cells in rat gastrointestinal mucosa. 2. Dye binding and metachromatic properties. Acta Pathol Microbiol Scand 66:303–313

    PubMed  Google Scholar 

  10. Fewtrell CM, Foreman JC, Jordan CC, Oehme P, Renner H, Stewart JM (1982) The effects of substance P on histamine and 5-hydroxy-tryptamine release in the rat. J Physiol 330:393–411

    PubMed  CAS  Google Scholar 

  11. Galli SJ (1993) New concepts about the mast cell. N Engl J Med 328:257–265

    Article  PubMed  CAS  Google Scholar 

  12. Gaytan F, Bellido C, Carrera G, Aguilar E (1990) Differentiation of mast cells during postnatal development of neonatally estrogen-treated rats. Cell Tissue Res 259:25–31

    Article  PubMed  CAS  Google Scholar 

  13. Gordon JR, Burd PR, Galli SJ (1990) Mast cells as a source of multifunctional cytokines. Immunol Today 11:458–464

    Article  PubMed  CAS  Google Scholar 

  14. Gottwald TP, Hewlett BR, Lhoták Ŝ, Stead RH (1995) Electrical stimulation of the vagus nerve modulates histamine content and mast cells in the rat jejunal mucosa. Neuroreport 7:313–317

    PubMed  CAS  Google Scholar 

  15. Grossman JC, Roselle GA, Medenhall CL (1991) Sex steroid regulation of autoimmunity. J Steroid Biochem Mol Biol 40:649–659

    Article  PubMed  CAS  Google Scholar 

  16. Hirschowitz BI, Groarke J (1993) Vagal effects on acid and pepsin secretion and serum gastrin in duodenal ulcer and controls. Dig Dis Sci 38:1874–1884.

    Article  PubMed  CAS  Google Scholar 

  17. Jankoric BD (1989) Neuroimmunomodulation. Facts and dilemmas. Immunol Lett 21:101–118

    Article  Google Scholar 

  18. Kiernan JA (1990) Degranulation of mast cells in the trachea and bronchi of the rat following stimulation of the vagus nerve. Int Arch Allergy Immunol 91:398–406

    Article  CAS  Google Scholar 

  19. MacQueen G, Marshall J, Perdue M, Siegel S, Bienenstock J (1989) Pavlovian conditioning of rat mucosal mast cell protease II. Science 243:83–85

    Article  PubMed  CAS  Google Scholar 

  20. Marchetti B, Gallo F, Farinella Z, Romeo C, Morale MC (1996) LHRH receptors in the neuroendocrine-immune network. Biochemical bases and implications for reproductive physiopathology. Ann N Y Acad Sci 784:209–236

    PubMed  CAS  Google Scholar 

  21. McDermott MR, Clark DA, Bienenstock J (1980) Evidence for a common mucosal immune system. N. Influence of estrus cycle on B immonoblast migration into genital and intestinal tissue. J Immunol 124:2436–2439

    Google Scholar 

  22. Mirski S, Befus AD, Bienenstock J (1983) Effects of sex differences and gonadal hormone alterations on the accumulation of mesenteric lymphoblasts in small intestine. Ann N Y Acad Sci 409:845–847

    Google Scholar 

  23. Ottway C.A. (1991) Neuroimmunomodulation in the intestinal mucosa. Gastroenterol Clin North Am 20:511–529

    Google Scholar 

  24. Shaff RE, Beaven MA (1979) Increased sensitivity of the enzymatic isotopic assay of histamine in plasma and serum Anal Biochem 94:425–430

    Article  PubMed  CAS  Google Scholar 

  25. Shanahan F, Anton P (1988) Neuroendocirne modulation of the immune system. Dig Dis Sci 33:41S-49S

    Article  PubMed  CAS  Google Scholar 

  26. Skofitsch G, Savitt JM, Jacobowitz DM (1985) Suggestive evidence for a functional unit between mast cells and substance P fibers in the rat diaphragm and mesentery. Histochemistry 81:5–8

    Article  Google Scholar 

  27. Stach W (1973) Über die Nervengeflechte der Duodenalzotten: licht- und elektronenmikroskopische Untersuchungen. Acta Anat 85:216–231

    Article  PubMed  CAS  Google Scholar 

  28. Stanisz AM, Kataeva G, Bienenstock J (1994) Hormones and local immunity. Int Arch Allergy Immunol 103:217–222

    PubMed  CAS  Google Scholar 

  29. Stead RH, Dixon MF, Bramwell NH, Riddell RH, Bienenstock J (1989) Mast cells are closely apposed to nerves in the human gastrointestinal mucosa. Gastroenterology 97:575–585

    PubMed  CAS  Google Scholar 

  30. Stead RH, Tamioka M, Riddell RH, Bienenstock J (1988) Substance P and/or calcitonin gene-related peptide are present in subepithelial enteric nerves apposed to intestinal and mucosal mast cells. In: McDermott RP (ed) Inflammatory bowel disease. Current status and future approach. Elsvier, Amsterdam New York

    Google Scholar 

  31. Williams RM, Bienenstock J, Stead RH (1995) Mast cells: the neuroimmune connection. Chem Immunol 61:208–235

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gottwald, T., Becker, H.D., Stead, R.H. et al. Geschlechtsunterschiede Bei Der Neuromodulation von Mukosamastzellen im Rattenjejunum. Langenbecks Arch Chiv 382, 157–163 (1997). https://doi.org/10.1007/BF02498669

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02498669

Key words

Schlüsselwörter

Navigation