Skip to main content

Interactions of mast cells with the nervous system —Recent advances

Neurochemical Research volume 17, pages 939–951 (1992)Cite this article

Abstract

This article reviews recent advances in the understanding of mast cell-nervous system interactions. It is drawn largely from work published within the last ten years, and discusses the anatomical and biochemical evidence of a functional connection between mast cells and the nervous system, and the implications that such a relationship may have for normal and abnormal physiological functioning. Mast cells are found at varying levels of association with the nervous system; in CNS parenchyma (mainly thalamus), in connective tissue coverings (e.g. meninges, endonerium), and in close apposition to peripheral nerve endings in a variety of tissues. There is, as yet, no clearly defined role for mast cells in nervous system function, or vice-versa, and it seems most likely that their interactions fulfil mutually modulatory roles. By extension, pathological situations where one of the partners in this relationship is overly stimulated may lead to a dysregulation of the other, and contribute to disease symptomatology.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Abbreviations

ACh:

acetylcholine

BMMC:

bone marrow-derived mast cells

CGRP:

calcitonin gene-related peptide

EAE:

experimental allergic encephalomyelitis

EAN:

experimental allergic neuritis

5-HT:

serotonin

IgE:

immunoglobulin E

IL-3:

interleukin-3

MS:

multiple sclerosis

NA:

noradrenaline

NF:

neurofibromatosis

NGF:

nerve growth factor

VIP:

Vasoactive intestinal polypeptide

References

  1. Neuman, J. 1890. Ueber das Vorkommen der sogenannten “Mastzellen” bei pathologischen Veraenderungen des Gehirns. Arch. Pathol. Anat. Physiol. Virchows 122:378.

    Google Scholar 

  2. Olsson, Y. 1968. Mast cells in the nervous system. Int. Rev. Cytol. 24:27–70.

    Google Scholar 

  3. Ibrahim, M. Z. M. 1974. The mast cells of the mammalian central nervous system. Part I. Morphology, distribution and histochemistry. J. Neurol. Sci. 21:431–478.

    Google Scholar 

  4. Dropp, J. J. 1976. Mast cells in mammalian brain. Acta Anat. 94:1–21.

    Google Scholar 

  5. Stevens, R. L., and Austen, K. F. 1989. Recent advances in the cellular and molecular biology of mast cells. Immunol. Today 10:381–386.

    Google Scholar 

  6. Gordon, J. R., Burd, P. R., and Galli, S. J. 1990. Mast cells as a source of multifunctional cytokines. Immunol. Today 11:458–464.

    Google Scholar 

  7. Bernstein, J. A., and Lawrence, I. D. 1990. The mast cell: a comprehensive updated review. Allergy Proc. 11:209–223.

    Google Scholar 

  8. Befus, A. D., Bienenstock, J., and Denburg, J. A. 1986 (eds.) Mast cell differentiation and heterogeneity. Raven Press, New York.

    Google Scholar 

  9. Galli, S. J. 1990. New insights into “the riddle of the mast cells”: microenvironmental regulation of mast cell development and phenotypic heterogeneity. Lab. Invest. 62:5–33.

    Google Scholar 

  10. Goldschmidt, R. C., Hough, L. B., Glick, S. D., and Padawer, J. 1984. Mast cells in rat thalamus: nuclear localization, sex difference and left-right asymmetry. Brain Res. 323:209–217.

    Google Scholar 

  11. Dimitriadou, V., Lambracht-Hall, M., Reichler, J., and Theoharides, T. C. 1990. Histochemical and ultrastructural characteristics of rat brain perivascular mast cells stimulated with compound 48/80 and carbachol. Neuroscience 39:209–224.

    Google Scholar 

  12. Orr, E. L. 1988. Presence and distribution of nervous system-associated mast cells that may modulate experimental allergic encephalomyelitis. Ann. NY Acad. Sci. 723–726.

  13. Dimlich, R. W. W., Keller, J. T., Strauss, T. A., and Fritts, M. J. 1991. Linear arrays of homogeneous mast cells in the dura mater of rat. J. Neurocytol. 20:485–503.

    Google Scholar 

  14. Dimitriadou, V., Aubineau, P., Taxi, J., and Seylaz, J. 1987. Ultrastructural evidence for a functional unit between nerve fibers and type 2 cerebral mast cells in the cerebral vascular wall. Neuroscience 22:621–630.

    Google Scholar 

  15. Ferrante, F., Ricci, A., Felici, L., Cavallotti, C., and Amenta, F. 1990. Suggestive evidence for a functional association between mast cells and sympathetic nerves in meningeal membranes. Acta Histochem. Cytochem. 23:637–646.

    Google Scholar 

  16. Brosnan, C. F., Lyman, W. D., Tansey, F. A., and Carter, T. H. 1985. Quantitation of mast cells in experimental allergic neuritis. J. Neuropathol. Exp. Neurol. 44:196–203.

    Google Scholar 

  17. Johnson, D., Yasui, D. H., and Seeldrayers, P. A. 1991. An analysis of mast cell frequency in the rodent nervous system: Numbers vary between different strains and can be reconstituted in mast cell-deficient mice. J. Neuropath. Exp. Neurol. 50:227–234.

    Google Scholar 

  18. Kimura, M., Tohya, K., and Toda, S. 1988. An electron microscopical observation of endoneurial mast cells of the laboratory musk shrew: suncus murinus. Anat. Anz. 165:143–150.

    Google Scholar 

  19. Heine, H., and Forster, F. J. 1975. Relationship between mast cells and terminal nerve fibers. Z. Mikrosk. Anat. Forsch. 89:934–937.

    Google Scholar 

  20. Heine, H., and Forster, F. J. 1975. Histophysiology of mast cells in skin and other organs. Arch. Dermatol. Res. 253:225–228.

    Google Scholar 

  21. Stach, W., Weiss, R., and Radke, R. 1975. Licht-und Elektronenmikroskopische Untersuchungen ueber die Nervengeflechte der Magenschleimhaut und deren Beziehungen zu Belug- und Mastzellen. Dtsch. Z. Verdau. Stoffwechselkrankheiten 35:205–218.

    Google Scholar 

  22. Williams, J. M., and Felten, D. L. 1981. Sympathetic innervation of murine thymus and spleen: a comparative histofluorescence study. Anat. Rec. 199:531–542.

    Google Scholar 

  23. Newson, B., Dahlstrom, A., Enerback, L., and Ahlman, H. 1983. Suggestive evidence for a direct innervation of mucosal mast cells. Neuroscience 10:565–570.

    Google Scholar 

  24. Skofitsch, G., Savitt, J. M., and Jacobowitz, D. M. 1985. Suggestive evidence for a functional unit between mast cells and substance P fibers in the rat diaphragm and mesentery. Histochemistry 82:5–8.

    Google Scholar 

  25. Stead, R. H., Tomioka, M., Quinonez, G., Simon, G. T., Felten, S. Y., and Bienenstock, J. 1987. Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves. Proc. Natl Acad. Sci. 84:2975–2979.

    Google Scholar 

  26. Bienenstock, J., Perdue, M., Blennerhassett, M., Stead, R., Kakuta, N., Sestini, P., Vancheri, C., and Marshall, J. 1988. Inflammatory cells and the epithelium. Mast cell/nerve interactions in the lung in vitro and in vivo. Am. Rev. Respir. Dis. 1988 138:S31-S34.

    Google Scholar 

  27. Stead, R. H., Dixon, M. F., Bramwell, M. H., Riddell, R. H., and Bienenstock, J. 1989. Mast cells are closely apposed to nerves in the human gastrointestinal mucosa. Gastroenterology 97:575–585.

    Google Scholar 

  28. Weihe, E., Mueller, S., Fink, T., and Zontel, H. J. 1989. Tachykinins, calcitonin gene-related peptide and neuropeptide Y in nerves of the mammalian thymus: interactions with mast cells in autonomic and sensory neuroimmunomodulation? Neurosci. Lett. 100:77–82.

    Google Scholar 

  29. Alving, K., Sundstrom, C., Matran, R., Panula, P., Hokfelt, T., and Lundberg, J. M. 1991. Association between histamine-containing mast cells and sensory nerves in the skin and airways of controls and capsaicin-treated pigs. Cell Tissue Res. 264:529–538.

    Google Scholar 

  30. Muller, S., and Weihe, E. 1991. Interrelation of peptidergic innervation with mast cells and ED1-positive cells in rat thymus. Brain Behav. Immun. 5:55–72.

    Google Scholar 

  31. Wiesner-Menzel, L., Schulz, B., Vaküzadeh, F., and Czarnetzki, B. M. 1981. Electron microscopical evidence for a direct contact between nerve fibres and mast cells. Acta Derm. Venereol. 61:465–469.

    Google Scholar 

  32. Janiszewski, J., Bienenstock, J., and Blennerhassett, M. G. 1990. Activation of rat peritoneal mast cells in coculture with sympathetic neurons alters neuronal physiology. Brain Behav. Immun. 4:139–150.

    Google Scholar 

  33. Blennerhassett, M. G., Tomioka, M., and Bienenstock, J. 1991. Formation of contacts between mast cells and sympathetic neurons in vitro. Cell Tissue Res. 265:121–128.

    Google Scholar 

  34. Arizono, N., Matsuda, S., Hattori, T., Kojima, Y., Maeda, T., and Galli, S. J. 1990. Anatomical variation in mast cell-nerve associations in the rat small intestine, heart, lung, and skin. Lab. Invest. 62:626–634.

    Google Scholar 

  35. Persinger, M. A. 1981. Developmental alterations in mast cell numbers and distributions within the thalamus of the albino rat. Dev. Neurosci. 4:220–224.

    Google Scholar 

  36. Ibrahim, M. Z. M. 1985. The mast cells of the mammalian central nervous system. IX. Development of the mast cells in the brain of the young rat. Acta Anat. 124:149–158.

    Google Scholar 

  37. Lambracht-Hall, M., Dimitriadou, V., and Theoharides, T. C. 1990. Migration of mast cells in developing rat brain. Dev. Brain Res. 56:151–159.

    Google Scholar 

  38. Sabria, J., Ferrer, I., Toledo, A., Sentis, M., and Blanco, I. 1987. Effects of altered thyroid function on histamine levels and mast cell number in neonatal rat brain. J. Pharm. Exp. Ther. 240:612–615.

    Google Scholar 

  39. Padawer, J. 1974. Mast cells: extended lifespan and lack of granule turnover under normal in vivo conditions. Exp. Mol. Pathol. 20:269–280.

    Google Scholar 

  40. Persinger, M. A. 1980. Handling factors not body marking influence thalamic mast cell numbers in the preweaned albino rat. Behav. Neural Biol. 30:448–459.

    Google Scholar 

  41. Karedina, V. S., and Dovbysch, T. V. 1981. Circadian rhythm of mast cell function in the rat dura. Biull. Eksper. Biol. I Medit. 90:1286–1288.

    Google Scholar 

  42. Mochizuki, M., Kuwabara, T., Chan, C. C., Nussenblatt, R. B., Metcalfe, D. D., and Gery, I. 1984. An association between susceptibility to experimental autoimmune uveitis and choroidal mast cell numbers. J. Immunol. 133:1699–1702.

    Google Scholar 

  43. Orr, E. L. 1984. Dural mast cells: source of contaminating histamine in analyses of mouse brain histamine levels. J. Neurochem. 43:1497–1499.

    Google Scholar 

  44. Markowitz, S., Saito, K., Buzzi, M. G., and Moskowitz, M. A. 1989. The development of neurogenic plasma extravasation in the rat dura mater does not depend upon the degranulation of mast cells. Brain Res. 477:157–165.

    Google Scholar 

  45. Levi-Schaffer, F., Austen, K. F., Caulfield, J., Hein, A., Bloes, W., and Stevens, R. 1985. Fibroblasts maintain the phenotype and the viability of the rat heparin-containing mast cell in vitro. J. Immunol. 135:3454–3462.

    Google Scholar 

  46. Seeldrayers, P. A., Levin, L., and Johnson, D. Astrocytes support mast cell viability in vitro. J. Neuroimmunol. 36:239–243.

  47. Ryan, J. J., and Huff, T. F. 1990. Schwann cell-conditioned medium supports development of mast cell-committed progenitors. FASEB J.:A1006.

  48. Ibrahim, M. Z. M., Al-Wirr, M. E., and Bahuth, N. 1979. The mast cells of the nervous system. III. Ultrastructural characteristics in the adult rat brain. Acta Anatomica 104:134–154.

    Google Scholar 

  49. Sturrock, R. R. 1980. A morphological lifespan study of neurolipomastocytes in various regions of mouse forebrain. Neuropathol. Exp. Neurobio. 6:211–219.

    Google Scholar 

  50. Dimlich, R. V. W. 1990. “Neurolipomastocyte” of the rat brain: a misnomer. Soc. Neuroscience Abstracts 16:246.

    Google Scholar 

  51. Mannaioni, P. F., Moroni, F., Fantozzi, R., and Masini, E. 1975. Studies on the14C-histamine release induced by noradrenaline in mouse neoplastic mast cells. Agents and Actions 5:417–423.

    Google Scholar 

  52. Alm, P. E., and Bloom, G. D. 1981. What-if any-is the role of adrenergic mechanisms in histamine release from mast cells? Agents and Actions 11:60–66.

    Google Scholar 

  53. Botana, L. M., Espinosa, J., and Eleno, N. 1987. Adrenergic activity on rat pleural and peritoneal mast cells. Loss of beta-receptors during the purification procedure. Gen Pharmacol. 18:141–148.

    Google Scholar 

  54. Fantozzi, R., Moroni, F., Blandina, P., Mannaioni, P. F., and Bani-Sacchi, T. 1978. Release of histamine from rat mast cells by acetylcholine. Nature 273:473–474.

    Google Scholar 

  55. Motavkin, P. A., Chertok, V. M., and Shulga, S. D. 1979. Effect of acetylcholine on the mast cells of the dura mater. Biull. Eksp. Biol. Med. 87:489–491.

    Google Scholar 

  56. Kazimierczak, W., Adamas, B., and Malinski, C. Z. 1980. Failure of acetycholine to release histamine from rat mast cells. Agents and Actions 10:1–3.

    Google Scholar 

  57. Masini, E., Fantozzi, R., Conti, A., Blandina, P., Brunelleschi, S., and Mannaioni, P. F. 1985. Mast cell heterogeneity in response to cholinergic stimulation. Int. Arch. Allergy Appl. Immunol. 77:184–185.

    Google Scholar 

  58. West, G. B. 1985. Thoughts on mast cells, histamine release and immunoglobulin E. Int. Arch. Allergy Appl. Immunol. 78:221–223.

    Google Scholar 

  59. Theoharides, T. C., and Douglas, W. W. 1978. Somatostatin induces histamine secretion from rat peritoneal mast cells. Endocrinology 102:1143–1145.

    Google Scholar 

  60. Erjavec, F., Lembeck, F., Florjanc-Irman, T., Skofitsch, G., Donnerer, J., Saria, A., and Holzer, P. 1981. Release of histamine by substance P. Naunyn Schmiedebergs Arch. Pharmacol. 317:67–70.

    Google Scholar 

  61. Fewtrell, C. M., Foreman, J. C., Jordan, C. C., Oehme, P., Renner, H., and Stewart, J. M. 1982. The effects of substance P on histamine and 5-hydroxytryptamine in the rat. J. Physiol. 330:393–411.

    Google Scholar 

  62. Yawasaki, Y., Shimamura, O., Kizu, A., Nakagawa, M., and Ijichi, H. 1982. IgE-mediated14C-serotonin release from rat mast cells modulated by morphine and endorphins. Life Sci. 31:471–478.

    Google Scholar 

  63. Sydbom, A. 1982. Histamine release from isolated rat mast cells by neurotensin and other peptides. Agents and Actions 12:91–93.

    Google Scholar 

  64. Casale, T. B., Bowman, S., and Kaliner, M. 1984. Induction of human cutaneous mast cell degranulation by opiates and endogenous opioid peptides: evidence for opiate and nonopiate receptor participation. J. Allergy Clin. Immunol. 73:775–781.

    Google Scholar 

  65. Foreman, J. C. 1984. Peptides and histamine release. J. Allergy Clin. Immunol. 74:127–131.

    Google Scholar 

  66. Shanahan, F., Lee, T. D., Bienenstock, J., and Befus, A. D. 1984. The influence of endorphins on peritoneal and mucosal mast cell secretion. J. Allergy Clin. Immunol. 74:499–504.

    Google Scholar 

  67. Piotrowski, W., and Foreman, J. C. 1985. On the actions of substance P, somatostatin, and vasoactive intestinal polypeptide on rat peritoneal mast cells and in human skin. Naunyn Schmiedebergs Arch. Pharmacol. 331:364–368.

    Google Scholar 

  68. Shibata, H., Mio, M., and Tasaka, K. 1985. Analysis of the mechanism of histamine-release induced by substance P. Biochem. Biophys. Acta 846:1–7.

    Google Scholar 

  69. Ebertz, J. M., Hirshman, C. A., Kettlekamp, M. S., Uno, H., and Hanifin, J. M. 1987. Substance P-induced histamine release in human cutaneous mast cells. J. Invest. Dermatol. 88:682–685.

    Google Scholar 

  70. Foreman, J. C. 1987. Substance P and calcitonin gene-related peptide: effects on mast cells and human skin. Int. Arch. Allergy Appl. Immunol. 82:366–371.

    Google Scholar 

  71. Wallengren, J., and Hakanson, R. 1987. Effects of substance P, neurokinin A and calcitonin gene-related peptide in human skin and their involvement in sensory nerve-mediated responses. Eur. J. Pharmacol. 143:267–273.

    Google Scholar 

  72. Sydbom, A. 1988. Effects of beta-endorphin on rat mast cells. Agents and Actions 23:204–206.

    Google Scholar 

  73. Arock, M., Devillier, P., Luffau, G., Guillosson, J. J., and Renoux, M. 1989. Histamine-releasing activity of endogeneous peptides on mast cells derived from different sites and species. Int. Arch. Allergy Appl. Immunol. 89:229–235.

    Google Scholar 

  74. Levi-Schaffer, F., and Shalit, M. 1989. Differential release of histamine and prostaglandin D2 in rat peritoneal mast cells activated with peptides. Int. Arch. Allergy Appl. Immunol. 90:352–357.

    Google Scholar 

  75. Arzubiaga, C., Morrow, J., Roberts, L. J., and Biaggioni, I. 1991. Neuropeptide Y, a putative cotransmitter in noradrenergic neurons, induces mast cell degranulation but not prostaglandin D2 release. J. Allergy Clin. Immunol. 87:88–93.

    Google Scholar 

  76. Lazarus, L. H., Perrin, M. H., and Brown, M. R. 1977. Mast cell binding of neurotensin. Iodination of neurotensin and characterization of the interaction of neurotensin with mast cell receptor sites. J. Biol. Chem. 252:7174–7179.

    Google Scholar 

  77. Donlon, W., Hunt, W. A., Catravas, G. N., and Kahner, M. 1982. A characterization of beta-adrenergic receptors on cellular and perigranular membranes of rat peritoneal mast cells. Life Sci. 31:411–416.

    Google Scholar 

  78. Marquardt, D. L., and Wasserman, S. I. 1982. Characterization of the rat mast cell beta-adrenergic receptor in resting and stimulated cells by radioligand binding. J. Immunol. 129:2122–2127.

    Google Scholar 

  79. Masini, E., Fantozzi, R., Blandina, P., Brunelleschi, S., and Mannaioni, P. F. 1983. Muscarinic cholinergic receptor binding in rat mast cells. Agents and Actions 13:327–332.

    Google Scholar 

  80. Renold, F. K., Dazin, P., Goetzl, E. J., and Payan, D. G. 1987. Interleukin-3 modulation of mouse bone marrow derived mast cell receptors for somatostatin. J. Neurosci. Res. 18:195–202.

    Google Scholar 

  81. Arbabian, M., Graziano, F. M., Jicinsky, J., Hadcock, J., Malbon, C., and Ruoho, A. E. 1989. Photoaffinity labeling of the guinea pig pulmonary mast cell beta-adrenergic receptor. Am. J. Respir. Cell Mol. Biol. 1:351–359.

    Google Scholar 

  82. Lowman, M. A., Benyon, R. C., and Church, M. K. 1988. Characteization of neuropeptide-induced histamine release from human dispersed skin mast cells. Br. J. Pharmacol. 95:121–130.

    Google Scholar 

  83. Bienenstock, J., Ernst, P. B., and Underdown, B. J. 1987. The gastrointestinal tract as a immunologic organ-state of the art. Ann. Allergy 59:17–20.

    Google Scholar 

  84. Bienenstock, J., Tomioka, M., Matsuda, H., Stead, R. H., Quinonez, G., Simon, G. T., Coughlin, M. D., and Denburg, J. A. 1987. The role of mast cells in inflammatory processes: evidence for nerve/mast cell interactions. Int. Arch. Allergy Appl. Immunol. 82:238–243.

    Google Scholar 

  85. Stanisz, A., Scicchitano, R., Stead, R., Matsuda, H., Tomioka, M., Denburg, J., and Bienenstock, J. 1987. Neuropeptides and immunity. Am. Rev. Respir. Dis. 136:48–51.

    Google Scholar 

  86. Church, M. K., Benyon, R. C., Lowman, M. A., Hutson, P. A., and Holgate, S. T. 1989. Allergy or inflammation: From neuropeptide stimulation of human skin mast cells to studies on the mechanism of the late asthmatic response. Agents and Actions 26:22–30.

    Google Scholar 

  87. Goetzl, E. J., Cheng, P. P., Hassner, A., Adelman, D. C., Frick, O. L., and Sreedharan, S. P. 1990. Neuropeptides, mast cells and allergy: novel mechanisms and therapeutic possibilities. Clin. Exp. Allergy 20 Suppl. 4:5–7.

    Google Scholar 

  88. Marshall, J. S., and Bienenstock, J. 1990. Mast cells. Springer Semin. Immunopathol. 12:191–202.

    Google Scholar 

  89. Stead, R. H., Perdue, M. H., Blennerhassett, M. G., Kakuta, Y., Sestini, P., and Bienenstock, J. 1990. The innervation of mast cells,in Freir, S. (ed.), The Neuroendocrine-Immune Network, CRC Press.

  90. Bienenstock, J., MacQueen, G., Sestini, P., Marshall, J. S., Stead, R. H., and Perdue, M. H. 1991. Mast cell/nerve interactions in vitro and in vivo. Am. Rev. Respir. Dis. 143:55–58.

    Google Scholar 

  91. Marshall, J. S., Bienenstock, J., Perdue, M. H., Stanisz, A. M., Stead, R. H., and Ernst, P. B. 1989. Novel cellular interactions and networks involving the intestinal immune system and its microenvironment. APMIS 97:383–394.

    Google Scholar 

  92. Bani-Sacchi, T., Barattini, M., Bianchi, S., Blandina, P., Brunelleschi, S., Fantozzi, R., Mannaioni, P. F., and Masini, E. 1986. The release of histamine by parasympathetic stimulation in guinea pig auricle and rat ileum. J. Physiol. 371:29–43.

    Google Scholar 

  93. Leff, A. R., Stimler, N. P., Munoz, M. N., Shioya, T., Tallet, J., and Dame, C. 1986. Augmentation of respiratory mast cell secretion of histamine caused by vagus nerve stimulation during antigen chanllenge. J. Immunol. 136:1066–1073.

    Google Scholar 

  94. Rucci, L., Masini, E., Cirri Borghi, M. B., Giannella, E., and Mannaioni, P. F. 1988. Histamine release from nasal mucosal mast cells in patients with chronic hypertrophic non-allergic rhinitis, after parasympathetic nerve stimulation. Agents and Actions 25:314–320.

    Google Scholar 

  95. Kiernan, J. A. 1990. Degranulation of mast cells in the trachea and bronchi of the rat following stimulation of the vagus nerve. Int. Arch. Allergy Appl. Immunol. 91:398–402.

    Google Scholar 

  96. Garrity, E. R., Stimler, N. P., Munoz, N. M., Tallet, J., David, A. C., and Leff, A. R. 1985. Sympathetic modulation of biochemical and physiological response to immune degranulation in canine bronchial airways in vivo. J Clin. Invest. 75:2038–2046.

    Google Scholar 

  97. Lembeck, F., and Holzer, P. 1979. Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn Schmiedeberg's Arch. Pharmacol. 310:175.

    Google Scholar 

  98. Coutts, A. A., Jorizzo, J. L., Creaves, M. W., and Burnstock, G. 1981. Mechanisms of vasodilation due to substance P in humans. Br. J. Dermatol. 105:354–355.

    Google Scholar 

  99. Payan, D. G., and Goetzl, E. J. 1988. Neuropeptide regulation of immediate and delayed hypersensitivity. Int. J. Neurosci. 38:211–221.

    Google Scholar 

  100. Girolomoni, G., and Tigelaar, R. E. 1990. Capsaicin-sensitive primary sensory neurons are potent modulators of murine delayed-type hypersensitivity reaction. J. Immunol. 145:1105–1112.

    Google Scholar 

  101. Levine, J. D., Coderre, T. J., Covinsky, K., and Basbaum, A. I. 1990. Neural influences on synovial mast cell density in rat. J. Neurosci. Res. 26:301–307.

    Google Scholar 

  102. Aloe, L. 1977. Mast cells increase in tissues of neonatal rats injected with nerve growth factor. Brain Res. 133:358–366.

    Google Scholar 

  103. Aloe, L. 1988. The effect of nerve growth factor and its antibody on mast cells in vivo. J. Neuroimmunol. 18:1–12.

    Google Scholar 

  104. Aloe, L., and DeSimone, R. 1989. NGF primed spleen cells injected in brain of developing rats differentiate into mast cells. Int. J. Dev. Neuroscience 7:565–573.

    Google Scholar 

  105. Houlgatte, R., Mallat, M., Brachet, P., and Prochiantz, A. 1989. Secretion of nerve growth factor in cultures of glial cells and neurons derived from different regions of the mouse brain. J. Neurosci. Res. 24:143–152.

    Google Scholar 

  106. Lindholm, D., Heumann, R., Meyer, M., and Thoenen, H. 1987. Interleukin-1 regulates synthesis of nerve growth factor in non-neural cells of rat sciatic nerve. Nature 330:658–659.

    Google Scholar 

  107. Steinbusch, H. W. M., and Mulder, A. H. 1984. Immunohistochemical localization of histamine in neurons and mast cells in the rat brain. Pages 126–140,in Bjoerklund, A., Hoekfelt, T., and Kuhar, M. J. (eds.), Handbook of Chemical Neuroanatomy, vol. 3.

  108. Wada, H., Inagaki, N., Yamatodani, A., and Watanabe, T. 1991. Is the histaminergic neuron system a regulatory center for whole brain activity? TINS 14:415–418.

    Google Scholar 

  109. Goldschmidt, R. C., Hough, L. B., and Glick, S. D. 1985. Rat brain mast cells: contribution to brain histamine levels. J. Neurochem. 44:1943–1947.

    Google Scholar 

  110. Donoso, A. O. 1986. The possible role of brain histamine in neuroendocrine and cardiovascular regulation. Med. Res. Rev. 6:365–368.

    Google Scholar 

  111. Prell, D. P., and Green, J. P. 1986. Histamine as a neuroregulator. Ann. Rev. Neurosci. 9:209–254.

    Google Scholar 

  112. Christian, E. P., Undem, B. J., and Weinreich, D. 1989. Endogenous histamine excites neurons in the guinea pig superior cervical ganglion in vitro. J. Physiol. 409:297–312.

    Google Scholar 

  113. Villena, F., Montoya, G. A., Roa, J., Jofre, A., and Goset, C. 1986. Mast cells and synaptic transmission in sympathetic ganglia. Cell Mol. Biol. 32:253–256.

    Google Scholar 

  114. Weinreich, D., and Undem, B. J. 1987. Immunological regulation of synaptic transmission in isolated guinea pig autonomic ganglia. J. Clin. Invest. 79:1529–1532.

    Google Scholar 

  115. Green, R., Fowler, J., MacGlashan, D., and Weinreich, D. 1988. IgE-challenged human lung mast cells excite vagal sensory neurons in vitro. J. Appl. Physiol. 64:2249–2253.

    Google Scholar 

  116. Casale, T. B. 1983. The role of the autonomic nervous system in allergic disease. Ann. Allergy 51:423–429.

    Google Scholar 

  117. Inoue, F., Hasegawa, H., Nishimura, M., Yanagisawa, M., and Ichiyama, A. 1985. Distribution of 5-hydroxytryptamine (5HT) in tissue of a mutant mouse deficient in mast cell (W/Wv). Demonstration of the contribution of mast cells to the 5HT content in various organs. Agents and Actions 16:295–301.

    Google Scholar 

  118. Lambracht-Hall, M., Konstantinidou, A. D., and Theoharides, T. C. 1990. Serotonin release from brain mast cells in vitro. Neuroscience 39:199–207.

    Google Scholar 

  119. Kai Kai, M. A., and Keen, P. 1985 Localization of 5-hydroxytryptamine to neurons and endoneurial mast cells in rat sensory ganglia. J. Neurocytol. 14:63–78.

    Google Scholar 

  120. Bueno, L., Fargeas, M. J., Theodorou, V., and Fioramonti, J. 1991. Involvement of 5-hydroxytryptamine in the intestinal motor disturbances by mast cell degranulation in rats. Eur. J. Pharmacol. 192:263–269.

    Google Scholar 

  121. Cutz, E., Chan, W., and Track, N. S. 1978. Release of vasoactive intestinal peptide in mast cells by histamine liberators. Nature 275:661–662.

    Google Scholar 

  122. Goetzl, E. J., Chernov-Rogan, T., Cooke, M. P., Renold, F., and Payan, D. G. 1985. Endogenous somatostatin-like peptides of rat basophilic leukemia cells. J. Immunol. 135:2707–2711.

    Google Scholar 

  123. Rosenblum, W. I. 1973. A possible role for mast cells in controlling the diameter of arterioles on the surface of the brain. Brain Res. 42:75–82.

    Google Scholar 

  124. Mokhtarian, F., and Griffin, D. E. 1984. The role of mast cells in virus-induced inflammation in the murine central nervous system. Cell. Immunol. 86:491–500.

    Google Scholar 

  125. Griffin, D. E., and Mendoza, Q. P. 1986. Identification of the inflammatory cells present in the central nervous system of normal and mast cell-deficient mice during Sinbis virus encephalitis. Cell. Immunol. 97:454–459.

    Google Scholar 

  126. Olsson, Y. 1975. Mast cells in plaques of multiple sclerosis. Acta Neurol. Scand. 50:611–621.

    Google Scholar 

  127. Kruger, P. G., Bo, L., Myhr, K-M., Karlsen, A. E., Taule, A., Nyland, H. I., and Mork, S. 1990. Mast cells and multiple sclerosis: a light and electron microscopic study of mast cells in multiple sclerosis, emphasizing staining procedures. Acta Neurol. Scand. 81:31–36.

    Google Scholar 

  128. Toms, R., Weiner, H. L., and Johnson, D. 1990. Identification of IgE-positive cells and mast cells in frozen sections of multiple sclerosis brain. J. Neuroimmunol. 30:169–177.

    Google Scholar 

  129. Prineas, J. W., and Wright, R. G. 1978. Macrophages, lymphocytes, and plasma cells in the perivascular compartment in chronic multiple sclerosis. Lab. Invest. 38:409–421.

    Google Scholar 

  130. Johnson, D., Seeldrayers, P. A., and Weiner, H. L. 1988. The role of mast cells in demyelination. 1: Myelin proteins are degraded by mast cell proteases and myelin basic protein and P2 can stimulate mast cell degranulation. Brain Research 44:195–198.

    Google Scholar 

  131. Dietsch, G. N., and Hinrichs, D. J. 1991. Mast cell proteases liberate stable encephalitogenic fragments from intact myelin. Cell. Immunol. 135:541–548.

    Google Scholar 

  132. Powell, H. C., Braheny, S. L., Myers, R. R., Rodriguez, M., and Lampert, P. W. 1983. Early changes in experimental allergic neuritis. Lab. Invest. 48:332–338.

    Google Scholar 

  133. Izumo, S., Linington, C., Wekerle, H., and Meyermann, R. 1985. Morphologic study on experimental allergic neuritis mediated by T cell line specific for bovine P2 protein in Lewis rats. Lab. Invest. 53:209–218.

    Google Scholar 

  134. Seeldrayers, P. A., Yasui, D., Weiner, H. L., and Johnson, D. 1989. Treatment of experimental allergic neuritis with nedocromil sodium, an anti-inflammatory drug with mast cell stabilizing properties. J. Neuroimmunol. 25:221–226.

    Google Scholar 

  135. Bo, L., Olsson, T., Nyland, H., Kruger, P. G., Taule, A., and Mork, S. 1991. Mast cells in brains during experimental allergic encephalomyelitis in Lewis rats. J. Neurol. Sci. 105:135–142.

    Google Scholar 

  136. Levi-Schaffer, F., Riesel, N., Soffer, D., Abramsky, O., and Brenner, T. Mast cell activity in experimental allergic encephalomyelitis. Mol. Chem. Neuropathol. (in press).

  137. Krenger, W., Yasui, D. H., Al-Sabbagh, A., Sriram, S., and Johnson, D. 1991. Mast cell activation in murine EAE. J. Neuroimmunol. (Suppl 1):45.

    Google Scholar 

  138. Matsuura, N., and Zetter, B. R. 1989. Stimulation of mast cell chemotaxis by interleukin 3. J. Exp. Med. 170:1421–1426.

    Google Scholar 

  139. Linthicum, D. S., and Frelinger, J. 1982. Acute autoimmune encephalomyelitis in mice. II. Susceptibility is controlled by the combination of H-2 and histamine response genes. J. Exp. Med. 155:31–42.

    Google Scholar 

  140. Orr, E. L., and Stanley, N. C. 1989. Brain and spinal cord levels of histamine in Lewis rats with acute experimental allergic encephalomyelitis. J. Neurochem. 53:111–118.

    Google Scholar 

  141. Brosnan, C. F., and Tansey, F. A. 1984. Delayed onset of experimental allergic neuritis in rats treated with reserpine. J. Neuropath. Exp. Neurol. 43:84–93.

    Google Scholar 

  142. Dietsch, G. N., and Hinrichs, D. J. 1989. The role of mast cells in the elicitation of experimental allergic encephalomyelitis. J. Immunol. 142:1476–1481.

    Google Scholar 

  143. Mekori, Y. A., Weitzmann, G. L., and Galli, S. J. 1985. Reevaluation of reserpine-induced suppression of contact sensitivity. Evidence that reserpine interferes with T lymphocyte function independently of an effect on mast cells. J. Exp. Med. 162:1935–53.

    Google Scholar 

  144. Rogers, M. P., Bloomingdalo, K., Murawski, B. J., Soter, N. A., Reich, P., and Austen, K. F. 1986. Mixed organic brain syndrome as a manifestation of systemic mastocytosis. Psychosomatic Med. 48:437–447.

    Google Scholar 

  145. Iriarte, L. M., Mateu, J., Cruz, G., and Escudero, J. 1988. Chorea: a new manifestation of mastocytosis. J. Neurol. Neurosurg. Psych. 51:1457–1463.

    Google Scholar 

  146. Lal, S. M., Brooks, C. S., Luger, A. M., Davenport, J. G., Weber, R. D., Loy, T. S., and Haibach, H. H. 1988. Systemic mastocytosis associated with membranous nephropathy, and peripheral neuropathy. Am. J. Kidney Disease. 12:538–543.

    Google Scholar 

  147. Riccardi, V. M., and Eichner, J. E. 1986. Neurofibromatosis: Phenotype, Natural History, and Pathogenesis. Johns Hopkins Press, Baltimore.

    Google Scholar 

  148. Isaacson, P. 1976. Mast cells in benign sheath tumours. J. Pathol. 119:193–196.

    Google Scholar 

  149. Johnson, M. D., Kamso-Pratt, J., Federspiel, C. F., and Whetsell, W. O., Jr. 1989. Mast cells and lymphoreticular infiltrates in neurofibromas. Comparison with nerve sheath tumors. Arch. Pathol. Lab. Med. 113:1263–1270.

    Google Scholar 

  150. Claman, H. N. 1987. New hope for Neurofibromatosis? The mast cell connection. J. A. M. A. 258:823.

    Google Scholar 

  151. Riccardi, V. M. 1987. Mast cell stabilisation to decrease neurofibroma growth. Arch. Dermatol. 123:1011–1016.

    Google Scholar 

  152. Riccardi, V. M. 1989. Genetic alterations and growth factors in the pathogenesis of von Recklinghausen's neurofibromatosis. Neurofibromatosis. 2:292–298.

    Google Scholar 

  153. Barnes, P. J., Belvisi, M. G., and Rogers, D. F. 1990. Modulation of neurogenic inflammation: novel approaches to inflammatory disease. Trends in Pharmacol. Sci. 11:185–189.

    Google Scholar 

  154. Kiernan, J. A. 1990. Interactions between mast cells and nerves. Neurogenic inflammation. Trends in Pharmacol. Sci. 11:316.

    Google Scholar 

  155. Kowalski, M. L., and Kaliner, M. 1988. Neurogenic inflammation, vascular permeability and mast cells. J. Immunol. 140:3905–3911.

    Google Scholar 

  156. Kowalski, M. L., Sliwinska-Kowalska, M., and Kaliner, M. A. 1990. Neurogenic inflammation, vascular permeability, and mast cells. II. Additional evidence indicating that mast cells are not involved in neurogenic inflammation. J. Immunol. 145:1214–1221.

    Google Scholar 

  157. Liberski, P. P., and Prusinski, A. 1982. Further observations on the mast cells over the painful region in cluster headache patients. Headache 22:115–117.

    Google Scholar 

  158. Moskowitz, M. A. 1984. The neurobiology of vascular head pain. Ann. Nuerol 16:157–168.

    Google Scholar 

  159. Theoharides, T. C. 1983. Mast cells and migraines, brief proposal. Perspect. Biol. Med. 26:672–675.

    Google Scholar 

  160. Markowitz, S., Saito, K., Buzzi, M. G., and Moskowitz, M. A. 1989. The development of neurogenic plasma extravasation in the rat dura mater does not depend upon the degranulation. Brain Res. 477:157–165.

    Google Scholar 

  161. Appenzeller, O., Becker, W. J., and Ragaz, A. 1981. Cluster headache. Ultrastructural aspects and pathogenetic mechanisms. Arch. Neurol. 38:302–306.

    Google Scholar 

  162. Dimitriadou, V., Henry, P., Brochet, B., Mathiau, P., and Aubineau, P. 1990. Cluster headache: ultrastructural evidence for mast cell degranulation and interaction with nerve fibres in the human temporal artery. Cephalalgia 10:221–228.

    Google Scholar 

  163. Alving, K., Sundstrom, C., Matran, R., Panula, P., Hokfelt, T., and Lundberg, J. M. 1991. Association between histamine-containing mast cells and sensory nerves in the skin and airways of control and capsaicin-treated pigs. Cell Tissue Res. 264:529–538.

    Google Scholar 

  164. Alving, K. 1991. Airways vasodilation in the immediate allergic reaction. Involvement of inflammatory mediators and sensory nerves. Acta Physiol. Scand. 597:1–64.

    Google Scholar 

  165. Holgate, S. T., Djukanovic, R., Wilson, J., Roche, W., and Howarth, P. H. 1991. Inflammatory processes and bronchial hyperresponsiveness. Clin. Exp. Allergy. 21:30–36.

    Google Scholar 

  166. Christian, E. P., Undem, B. J., and Weinreich, D. 1989. Endogenous histamine excites neurones in the guinea pig superior cervical ganglion in vitro. J. Physiol (Lond) 409:297–312.

    Google Scholar 

Download references

Author information

Affiliations

  1. Center for Neurologic Diseases, Divison of Neurology, Department of Medicine LMRC 118, Brigham and Women's Hospital, 75 Francis Street, 02115, Boston, MA

    David Johnson PhD & Werner Krenger

Authors
  1. David Johnson PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Werner Krenger
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Special issue dedicated to Dr. Alan N. Davison.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Johnson, D., Krenger, W. Interactions of mast cells with the nervous system —Recent advances. Neurochem Res 17, 939–951 (1992). https://doi.org/10.1007/BF00993271

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00993271

Key Words

  • Mast cells
  • nervous system
  • neuropeptides
  • neurotransmitters
  • demyelination
  • review