Skip to main content
NCBI home page
Journal of Anatomy logoLink to Journal of Anatomy
. 1999 Nov;195(Pt 4):577–586. doi: 10.1046/j.1469-7580.1999.19540577.x

Mast cells in the sheep, hedgehog and rat forebrain

HELEN C MICHALOUDI 1,✉, GEORGIOS C PAPADOPOULOS 1
PMCID: PMC1468028  PMID: 10634696

Abstract

The study was designed to reveal the distribution of various mast cell types in the forebrain of the adult sheep, hedgehog and rat. Based on their histochemical and immunocytochemical characteristics, mast cells were categorised as (1) connective tissue-type mast cells, staining metachromatically purple with the toluidine blue method, or pale red with the Alcian blue/safranin method, (2) mucosal-type or immature mast cells staining blue with the Alcian blue/safranin method and (3) serotonin immunopositive mast cells. All 3 types of brain mast cells in all species studied were located in both white and grey matter, often associated with intraparenchymal blood vessels. Their distribution pattern exhibited interspecies differences, while their number varied considerably not only between species but also between individuals of each species. A distributional left-right asymmetry, with more cells present on the left side, was observed in all species studied but it was most prominent in the sheep brain. In the sheep, mast cells were abundantly distributed in forebrain areas, while in the hedgehog and the rat forebrain, mast cells were less widely distributed and were relatively or substantially fewer in number respectively. A limited number of brain mast cells, in all 3 species, but primarily in the rat, were found to react both immunocytochemically to 5-HT antibody and histochemically with Alcian blue/safranin staining.

Keywords: Neuroendocrine interaction, immunocytes, brain

Full Text

The Full Text of this article is available as a PDF (332.1 KB).

Selected References

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

  1. Appenzeller O., Becker W. J., Ragaz A. Cluster headache. Ultrastructural aspects and pathogenetic mechanisms. Arch Neurol. 1981 May;38(5):302–306. doi: 10.1001/archneur.1981.00510050068012. [DOI] [PubMed] [Google Scholar]
  2. Askenase P. W., Rosenstein R. W., Ptak W. T cells produce an antigen-binding factor with in vivo activity analogous to IgE antibody. J Exp Med. 1983 Mar 1;157(3):862–873. doi: 10.1084/jem.157.3.862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aubineau P., Dimitriadou V., Bouchaud C., Seylaz J. Direct innervation of neurolipomastocytes in the rabbit and rat cerebral artery wall. Acta Physiol Scand Suppl. 1986;552:21–24. [PubMed] [Google Scholar]
  4. Auvinen S., Panula P. Development of histamine-immunoreactive neurons in the rat brain. J Comp Neurol. 1988 Oct 8;276(2):289–303. doi: 10.1002/cne.902760211. [DOI] [PubMed] [Google Scholar]
  5. Bebo B. F., Jr, Yong T., Orr E. L., Linthicum D. S. Hypothesis: a possible role for mast cells and their inflammatory mediators in the pathogenesis of autoimmune encephalomyelitis. J Neurosci Res. 1996 Aug 15;45(4):340–348. doi: 10.1002/(SICI)1097-4547(19960815)45:4<340::AID-JNR3>3.0.CO;2-9. [DOI] [PubMed] [Google Scholar]
  6. Bergendorff A., Uvnäs B. Storage of 5-hydroxytryptamine in rat mast cells. Evidence for an ionic binding to carboxyl groups in a granule heparin-protein complex. Acta Physiol Scand. 1972 Mar;84(3):320–331. doi: 10.1111/j.1748-1716.1972.tb05183.x. [DOI] [PubMed] [Google Scholar]
  7. Bienenstock J., Tomioka M., Matsuda H., Stead R. H., Quinonez G., Simon G. T., Coughlin M. D., Denburg J. A. The role of mast cells in inflammatory processes: evidence for nerve/mast cell interactions. Int Arch Allergy Appl Immunol. 1987;82(3-4):238–243. doi: 10.1159/000234197. [DOI] [PubMed] [Google Scholar]
  8. Bugajski A. J., Chłap Z., Gadek-Michalska, Bugajski J. Effect of isolation stress on brain mast cells and brain histamine levels in rats. Agents Actions. 1994 Jun;41(Spec No):C75–C76. doi: 10.1007/BF02007774. [DOI] [PubMed] [Google Scholar]
  9. Campbell D. J., Kernan J. A. Mast cells in the central nervous system. Nature. 1966 May 14;210(5037):756–757. doi: 10.1038/210756b0. [DOI] [PubMed] [Google Scholar]
  10. Cuypers J., Westphal K., Bunge S. Mast cells in cluster headache. Acta Neurol Scand. 1980 May;61(5):327–329. doi: 10.1111/j.1600-0404.1980.tb01500.x. [DOI] [PubMed] [Google Scholar]
  11. Dayton E. T., Pharr P., Ogawa M., Serafin W. E., Austen K. F., Levi-Schaffer F., Stevens R. L. 3T3 fibroblasts induce cloned interleukin 3-dependent mouse mast cells to resemble connective tissue mast cells in granular constituency. Proc Natl Acad Sci U S A. 1988 Jan;85(2):569–572. doi: 10.1073/pnas.85.2.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dimitriadou V., Aubineau P., Taxi J., Seylaz J. Ultrastructural evidence for a functional unit between nerve fibers and type II cerebral mast cells in the cerebral vascular wall. Neuroscience. 1987 Aug;22(2):621–630. doi: 10.1016/0306-4522(87)90358-7. [DOI] [PubMed] [Google Scholar]
  13. Dimitriadou V., Buzzi M. G., Moskowitz M. A., Theoharides T. C. Trigeminal sensory fiber stimulation induces morphological changes reflecting secretion in rat dura mater mast cells. Neuroscience. 1991;44(1):97–112. doi: 10.1016/0306-4522(91)90253-k. [DOI] [PubMed] [Google Scholar]
  14. Dimitriadou V., Lambracht-Hall M., Reichler J., Theoharides T. C. Histochemical and ultrastructural characteristics of rat brain perivascular mast cells stimulated with compound 48/80 and carbachol. Neuroscience. 1990;39(1):209–224. doi: 10.1016/0306-4522(90)90234-u. [DOI] [PubMed] [Google Scholar]
  15. Dimitriadou V., Rouleau A., Tuong M. D., Ligneau X., Newlands G. F., Miller H. R., Schwartz J. C., Garbarg M. Rat cerebral mast cells undergo phenotypic changes during development. Brain Res Dev Brain Res. 1996 Nov 22;97(1):29–41. doi: 10.1016/s0165-3806(96)00127-7. [DOI] [PubMed] [Google Scholar]
  16. Dropp J. J. Mast cells in mammalian brain. Acta Anat (Basel) 1976;94(1):1–21. doi: 10.1159/000144540. [DOI] [PubMed] [Google Scholar]
  17. Dropp J. J. Mast cells in the central nervous system of several rodents. Anat Rec. 1972 Oct;174(2):227–237. doi: 10.1002/ar.1091740207. [DOI] [PubMed] [Google Scholar]
  18. Edvinsson L., Cervós-Navarro J., Larsson L. I., Owman C., Rönnberg A. L. Regional distribution of mast cells containing histamine, dopamine, or 5-hydroxytryptamine in the mammalian brain. Neurology. 1977 Sep;27(9):878–883. doi: 10.1212/wnl.27.9.878. [DOI] [PubMed] [Google Scholar]
  19. Eng L. F., Ghirnikar R. S., Lee Y. L. Inflammation in EAE: role of chemokine/cytokine expression by resident and infiltrating cells. Neurochem Res. 1996 Apr;21(4):511–525. doi: 10.1007/BF02527717. [DOI] [PubMed] [Google Scholar]
  20. Flood P. R., Krüger P. G. Fine structure of mast cells in the central nervous system of the hedgehog. Acta Anat (Basel) 1970;75(3):443–452. doi: 10.1159/000143462. [DOI] [PubMed] [Google Scholar]
  21. Fritz F. J., Pabst R. Numbers and heterogeneity of mast cells in the male genital tract of the rat. Int Arch Allergy Appl Immunol. 1989;88(3):360–362. doi: 10.1159/000234826. [DOI] [PubMed] [Google Scholar]
  22. Galli S. J. New approaches for the analysis of mast cell maturation, heterogeneity, and function. Fed Proc. 1987 Apr;46(5):1906–1914. [PubMed] [Google Scholar]
  23. Galli S. J. New insights into "the riddle of the mast cells": microenvironmental regulation of mast cell development and phenotypic heterogeneity. Lab Invest. 1990 Jan;62(1):5–33. [PubMed] [Google Scholar]
  24. Geffard M., Dulluc J., Rock A. M. Antisera against the indolealkylamines: tryptophan, 5-hydroxytryptophan, 5-hydroxytryptamine, 5-methoxytryptophan, and 5-methoxytryptamine tested by an enzyme-linked immunosorbent assay method. J Neurochem. 1985 Apr;44(4):1221–1228. doi: 10.1111/j.1471-4159.1985.tb08747.x. [DOI] [PubMed] [Google Scholar]
  25. Goldschmidt R. C., Hough L. B., Glick S. D., Padawer J. Mast cells in rat thalamus: nuclear localization, sex difference and left-right asymmetry. Brain Res. 1984 Dec 10;323(2):209–217. doi: 10.1016/0006-8993(84)90291-9. [DOI] [PubMed] [Google Scholar]
  26. Goldschmidt R. C., Hough L. B., Glick S. D. Rat brain mast cells: contribution to brain histamine levels. J Neurochem. 1985 Jun;44(6):1943–1947. doi: 10.1111/j.1471-4159.1985.tb07191.x. [DOI] [PubMed] [Google Scholar]
  27. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
  28. Ibrahim M. Z., Reder A. T., Lawand R., Takash W., Sallouh-Khatib S. The mast cells of the multiple sclerosis brain. J Neuroimmunol. 1996 Nov;70(2):131–138. doi: 10.1016/s0165-5728(96)00102-6. [DOI] [PubMed] [Google Scholar]
  29. Ibrahim M. Z. The mast cells of the mammalian central nervous system. IX. Development of the mast cells in the brain of the young rat. Acta Anat (Basel) 1985;124(3-4):149–158. doi: 10.1159/000146111. [DOI] [PubMed] [Google Scholar]
  30. Johnson D., Krenger W. Interactions of mast cells with the nervous system--recent advances. Neurochem Res. 1992 Sep;17(9):939–951. doi: 10.1007/BF00993271. [DOI] [PubMed] [Google Scholar]
  31. KELSALL M. A., LEWIS P. MAST CELLS IN THE BRAIN. Fed Proc. 1964 Sep-Oct;23:1107–1108. [PubMed] [Google Scholar]
  32. Kanakura Y., Thompson H., Nakano T., Yamamura T., Asai H., Kitamura Y., Metcalfe D. D., Galli S. J. Multiple bidirectional alterations of phenotype and changes in proliferative potential during the in vitro and in vivo passage of clonal mast cell populations derived from mouse peritoneal mast cells. Blood. 1988 Sep;72(3):877–885. [PubMed] [Google Scholar]
  33. Karagogeos D., Papadopoulos G. C. Localization of molluscan R15 alpha 2 peptide immunoreactivity in the mammalian brain. Brain Res. 1994 Jul 11;650(2):275–282. doi: 10.1016/0006-8993(94)91792-2. [DOI] [PubMed] [Google Scholar]
  34. Kelsall M. A. Aging on mast cells and plasmacytes in the brain of hamsters. Anat Rec. 1966 Apr;154(4):727–739. doi: 10.1002/ar.1091540404. [DOI] [PubMed] [Google Scholar]
  35. Kermode A. G., Thompson A. J., Tofts P., MacManus D. G., Kendall B. E., Kingsley D. P., Moseley I. F., Rudge P., McDonald W. I. Breakdown of the blood-brain barrier precedes symptoms and other MRI signs of new lesions in multiple sclerosis. Pathogenetic and clinical implications. Brain. 1990 Oct;113(Pt 5):1477–1489. doi: 10.1093/brain/113.5.1477. [DOI] [PubMed] [Google Scholar]
  36. Krüger P. G., Bø L., Myhr K. M., Karlsen A. E., Taule A., Nyland H. I., Mørk S. Mast cells and multiple sclerosis: a light and electron microscopic study of mast cells in multiple sclerosis emphasizing staining procedures. Acta Neurol Scand. 1990 Jan;81(1):31–36. doi: 10.1111/j.1600-0404.1990.tb00927.x. [DOI] [PubMed] [Google Scholar]
  37. Krüger P. G. Demonstration of mast cells in the albino rat brain. Experientia. 1974 Jul 15;30(7):810–811. doi: 10.1007/BF01924200. [DOI] [PubMed] [Google Scholar]
  38. Lambracht-Hall M., Dimitriadou V., Theoharides T. C. Migration of mast cells in the developing rat brain. Brain Res Dev Brain Res. 1990 Nov 1;56(2):151–159. doi: 10.1016/0165-3806(90)90077-c. [DOI] [PubMed] [Google Scholar]
  39. Lambracht-Hall M., Konstantinidou A. D., Theoharides T. C. Serotonin release from rat brain mast cells in vitro. Neuroscience. 1990;39(1):199–207. doi: 10.1016/0306-4522(90)90233-t. [DOI] [PubMed] [Google Scholar]
  40. Levi-Schaffer F., Austen K. F., Gravallese P. M., Stevens R. L. Coculture of interleukin 3-dependent mouse mast cells with fibroblasts results in a phenotypic change of the mast cells. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6485–6488. doi: 10.1073/pnas.83.17.6485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mares V., Brückner G., Narovec T., Biesold D. The effect of different light regimes on DNA synthesis and cell division in the rat visual centres. Life Sci. 1977 Sep 1;21(5):727–732. doi: 10.1016/0024-3205(77)90082-0. [DOI] [PubMed] [Google Scholar]
  42. Markey A. C., Churchill L. J., MacDonald D. M. Human cutaneous mast cells--a study of fixative and staining reactions in normal skin. Br J Dermatol. 1989 May;120(5):625–631. doi: 10.1111/j.1365-2133.1989.tb01347.x. [DOI] [PubMed] [Google Scholar]
  43. Michaloudi E. C., Papadopoulos G. C. Atlas of the serotonin-containing cell bodies and fibers in the central nervous system of the hedgehog. J Hirnforsch. 1995;36(1):77–100. [PubMed] [Google Scholar]
  44. Miller H. R., Huntley J. F., Newlands G. F., Irvine J. Granule chymases and the characterization of mast cell phenotype and function in rat and mouse. Monogr Allergy. 1990;27:1–30. [PubMed] [Google Scholar]
  45. Nakano T., Sonoda T., Hayashi C., Yamatodani A., Kanayama Y., Yamamura T., Asai H., Yonezawa T., Kitamura Y., Galli S. J. Fate of bone marrow-derived cultured mast cells after intracutaneous, intraperitoneal, and intravenous transfer into genetically mast cell-deficient W/Wv mice. Evidence that cultured mast cells can give rise to both connective tissue type and mucosal mast cells. J Exp Med. 1985 Sep 1;162(3):1025–1043. doi: 10.1084/jem.162.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Newlands G. F., Huntley J. F., Miller H. R. Concomitant detection of mucosal mast cells and eosinophils in the intestines of normal and Nippostrongylus-immune rats. A re-evaluation of histochemical and immunocytochemical techniques. Histochemistry. 1984;81(6):585–589. doi: 10.1007/BF00489539. [DOI] [PubMed] [Google Scholar]
  47. Newson B., Dahlström A., Enerbäck L., Ahlman H. Suggestive evidence for a direct innervation of mucosal mast cells. Neuroscience. 1983 Oct;10(2):565–570. doi: 10.1016/0306-4522(83)90153-7. [DOI] [PubMed] [Google Scholar]
  48. Olesen S. P. Leakiness of rat brain microvessels to fluorescent probes following craniotomy. Acta Physiol Scand. 1987 May;130(1):63–68. doi: 10.1111/j.1748-1716.1987.tb08112.x. [DOI] [PubMed] [Google Scholar]
  49. Olsson Y. Mast cells in plaques of multiple sclerosis. Acta Neurol Scand. 1974;50(5):611–618. doi: 10.1111/j.1600-0404.1974.tb02806.x. [DOI] [PubMed] [Google Scholar]
  50. Olsson Y. Mast cells in the nervous system. Int Rev Cytol. 1968;24:27–70. doi: 10.1016/s0074-7696(08)61396-0. [DOI] [PubMed] [Google Scholar]
  51. Orr E. L., Pace K. R. The significance of mast cells as a source of histamine in the mouse brain. J Neurochem. 1984 Mar;42(3):727–732. doi: 10.1111/j.1471-4159.1984.tb02743.x. [DOI] [PubMed] [Google Scholar]
  52. Otsu K., Nakano T., Kanakura Y., Asai H., Katz H. R., Austen K. F., Stevens R. L., Galli S. J., Kitamura Y. Phenotypic changes of bone marrow-derived mast cells after intraperitoneal transfer into W/Wv mice that are genetically deficient in mast cells. J Exp Med. 1987 Mar 1;165(3):615–627. doi: 10.1084/jem.165.3.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pang X., Letourneau R., Rozniecki J. J., Wang L., Theoharides T. C. Definitive characterization of rat hypothalamic mast cells. Neuroscience. 1996 Aug;73(3):889–902. doi: 10.1016/0306-4522(95)00606-0. [DOI] [PubMed] [Google Scholar]
  54. Papadopoulos G. C., Parnavelas J. G., Buijs R. M. Light and electron microscopic immunocytochemical analysis of the serotonin innervation of the rat visual cortex. J Neurocytol. 1987 Dec;16(6):883–892. doi: 10.1007/BF01611992. [DOI] [PubMed] [Google Scholar]
  55. Pitton C., Michel L., Salem P., Benhamou M., Mencia-Huerta J. M., Maclouf J., Prost C., Burtin C., Dubertret L., Benveniste J. Biochemical and morphological modifications in dexamethasone-treated mouse bone marrow-derived mast cells. J Immunol. 1988 Oct 1;141(7):2437–2444. [PubMed] [Google Scholar]
  56. Razin E., Stevens R. L., Akiyama F., Schmid K., Austen K. F. Culture from mouse bone marrow of a subclass of mast cells possessing a distinct chondroitin sulfate proteoglycan with glycosaminoglycans rich in N-acetylgalactosamine-4,6-disulfate. J Biol Chem. 1982 Jun 25;257(12):7229–7236. [PubMed] [Google Scholar]
  57. Reynolds D. S., Serafin W. E., Faller D. V., Wall D. A., Abbas A. K., Dvorak A. M., Austen K. F., Stevens R. L. Immortalization of murine connective tissue-type mast cells at multiple stages of their differentiation by coculture of splenocytes with fibroblasts that produce Kirsten sarcoma virus. J Biol Chem. 1988 Sep 5;263(25):12783–12791. [PubMed] [Google Scholar]
  58. Reynolds D. S., Stevens R. L., Lane W. S., Carr M. H., Austen K. F., Serafin W. E. Different mouse mast cell populations express various combinations of at least six distinct mast cell serine proteases. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3230–3234. doi: 10.1073/pnas.87.8.3230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Ribatti D., Bertossi M., Nico B., Roncali L. Mast cells in the chick embryo choroid plexuses. J Submicrosc Cytol. 1987 Apr;19(2):371–373. [PubMed] [Google Scholar]
  60. Rosenblum W. I. A possible role for mast cells in controlling the diameter of arterioles on the surface of the brain. Brain Res. 1973 Jan 15;49(1):75–82. doi: 10.1016/0006-8993(73)90402-2. [DOI] [PubMed] [Google Scholar]
  61. Rozniecki J. J., Hauser S. L., Stein M., Lincoln R., Theoharides T. C. Elevated mast cell tryptase in cerebrospinal fluid of multiple sclerosis patients. Ann Neurol. 1995 Jan;37(1):63–66. doi: 10.1002/ana.410370112. [DOI] [PubMed] [Google Scholar]
  62. SICUTERI F. MAST CELLS AND THEIR ACTIVE SUBSTANCES: THEIR ROLE IN THE PATHOGENESIS OF MIGRAINE. Headache. 1963 Oct;3:86–92. doi: 10.1111/j.1526-4610.1963.hed0303086.x. [DOI] [PubMed] [Google Scholar]
  63. Schrader J. W., Lewis S. J., Clark-Lewis I., Culvenor J. G. The persisting (P) cell: histamine content, regulation by a T cell-derived factor, origin from a bone marrow precursor, and relationship to mast cells. Proc Natl Acad Sci U S A. 1981 Jan;78(1):323–327. doi: 10.1073/pnas.78.1.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Seldin D. C., Adelman S., Austen K. F., Stevens R. L., Hein A., Caulfield J. P., Woodbury R. G. Homology of the rat basophilic leukemia cell and the rat mucosal mast cell. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3871–3875. doi: 10.1073/pnas.82.11.3871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Serafin W. E., Reynolds D. S., Rogelj S., Lane W. S., Conder G. A., Johnson S. S., Austen K. F., Stevens R. L. Identification and molecular cloning of a novel mouse mucosal mast cell serine protease. J Biol Chem. 1990 Jan 5;265(1):423–429. [PubMed] [Google Scholar]
  66. Silver R., Silverman A. J., Vitković L., Lederhendler I. I. Mast cells in the brain: evidence and functional significance. Trends Neurosci. 1996 Jan;19(1):25–31. doi: 10.1016/0166-2236(96)81863-7. [DOI] [PubMed] [Google Scholar]
  67. Silverman A. J., Millar R. P., King J. A., Zhuang X., Silver R. Mast cells with gonadotropin-releasing hormone-like immunoreactivity in the brain of doves. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3695–3699. doi: 10.1073/pnas.91.9.3695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Sugimoto K., Maeyama K., Alam K., Sakurai E., Onoue H., Kasugai T., Kitamura Y., Watanabe T. Brain histaminergic system in mast cell-deficient (Ws/Ws) rats: histamine content, histidine decarboxylase activity, and effects of (S) alpha-fluoromethylhistidine. J Neurochem. 1995 Aug;65(2):791–797. doi: 10.1046/j.1471-4159.1995.65020791.x. [DOI] [PubMed] [Google Scholar]
  69. Theoharides T. C., Dimitriadou V., Letourneau R., Rozniecki J. J., Vliagoftis H., Boucher W. Synergistic action of estradiol and myelin basic protein on mast cell secretion and brain myelin changes resembling early stages of demyelination. Neuroscience. 1993 Dec;57(3):861–871. doi: 10.1016/0306-4522(93)90030-j. [DOI] [PubMed] [Google Scholar]
  70. Theoharides T. C. Mast cells and migraines. Perspect Biol Med. 1983 Summer;26(4):672–675. doi: 10.1353/pbm.1983.0028. [DOI] [PubMed] [Google Scholar]
  71. Theoharides T. C. Mast cells: the immune gate to the brain. Life Sci. 1990;46(9):607–617. doi: 10.1016/0024-3205(90)90129-f. [DOI] [PubMed] [Google Scholar]
  72. Theoharides T. C. The mast cell: a neuroimmunoendocrine master player. Int J Tissue React. 1996;18(1):1–21. [PubMed] [Google Scholar]
  73. Toda N., Okamura T. Neurogenic nitric oxide (NO) in the regulation of cerebroarterial tone. J Chem Neuroanat. 1996 Jun;10(3-4):259–265. doi: 10.1016/0891-0618(96)00135-4. [DOI] [PubMed] [Google Scholar]
  74. Toms R., Weiner H. L., Johnson D. Identification of IgE-positive cells and mast cells in frozen sections of multiple sclerosis brains. J Neuroimmunol. 1990 Dec;30(2-3):169–177. doi: 10.1016/0165-5728(90)90101-r. [DOI] [PubMed] [Google Scholar]
  75. Welle M. Development, significance, and heterogeneity of mast cells with particular regard to the mast cell-specific proteases chymase and tryptase. J Leukoc Biol. 1997 Mar;61(3):233–245. doi: 10.1002/jlb.61.3.233. [DOI] [PubMed] [Google Scholar]
  76. Zhuang X., Silverman A. J., Silver R. Reproductive behavior, endocrine state, and the distribution of GnRH-like immunoreactive mast cells in dove brain. Horm Behav. 1993 Sep;27(3):283–295. doi: 10.1006/hbeh.1993.1021. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES