DOI: 10.1523/jneurosci.20-01-00401.2000. Mast Cells Migrate from Blood to Brain

10.1523/jneurosci.20-01-00401.2000

Crossref journal-article

Society for Neuroscience

The Journal of Neuroscience (393)

Abstract

It is well established that mast cells (MCs) occur within the CNS of many species. Furthermore, their numbers can increase rapidly in adults in response to altered physiological conditions. In this study we found that early postpartum rats had significantly more mast cells in the thalamus than virgin controls. Evidence from semithin sections from these females suggested that mast cells were transiting across the medium-sized blood vessels. We hypothesized that the increases in mast cell number were caused by their migration into the neural parenchyma. To this end, we purified rat peritoneal mast cells, labeled them with the vital dyes PKH26 or CellTracker Green, and injected them into host animals. One hour after injection, dye-filled cells, containing either histamine or serotonin (mediators stored in mast cells), were located close to thalamic blood vessels. Injected cells represented ∼2–20% of the total mast cell population in this brain region. Scanning confocal microscopy confirmed that the biogenic amine and the vital dye occurred in the same cell. To determine whether the donor mast cells were within the blood–brain barrier, we studied the localization of dye-marked donor cells and either Factor VIII, a component of endothelial basal laminae, or glial fibrillary acidic protein, the intermediate filament found in astrocytes. Serial section reconstructions of confocal images demonstrated that the mast cells were deep to the basal lamina, in nests of glial processes. This is the first demonstration that mast cells can rapidly penetrate brain blood vessels, and this may account for the rapid increases in mast cell populations after physiological manipulations.

Bibliography

Silverman, A.-J., Sutherland, A. K., Wilhelm, M., & Silver, R. (2000). Mast Cells Migrate from Blood to Brain. The Journal of Neuroscience, 20(1), 401â408.

Authors 4

Ann-Judith Silverman (first)
Anne K. Sutherland (additional)
Marta Wilhelm (additional)
Rae Silver (additional)

References 85 Referenced 185

10.1002/ar.1090940210
10.1146/annurev.pa.30.040190.003021
10.1002/cne.902730204
Bacallao R Kiai K Jesaitis L (1995) Guiding principles in specimen preservation for confocal microscopy. in Handbook of biological confocal microscopy, ed Pawley JB (Plenum, New York), pp 311–326. (10.1007/978-1-4757-5348-6_18)
10.1007/BF00269011
10.1161/01.CIR.91.2.275
10.4049/jimmunol.149.11.3665 / J Immunol / IL-3-dependent mast cells attach to plate-bound vitronectin. Demonstration of augmented proliferation in response to signals transduced via cell surface vitronectin receptors. by Bianchine (1992)
10.1002/aja.1001670209
10.1002/ana.410270719 / Ann Neurol / Mechanisms of autoimmune neuropathies. by Brosnan (1990)
10.1016/0306-4522(86)90051-5
10.1097/00001756-199902250-00024
10.1002/cne.903690102
10.1038/275661a0
10.1016/0165-5728(92)90047-O
10.1016/0306-4522(90)90234-U
{'key': '2023041302435191000_20.1.401.16', 'first-page': '5', 'article-title': 'Learned sensitivity.', 'volume': '71', 'author': 'Djuric', 'year': '1993', 'journal-title': 'Ann Allergy'} / Ann Allergy / Learned sensitivity. by Djuric (1993)
10.1002/ar.1091740207
10.1159/000144540
Enerback L Miller HRP Mayrhofer G (1986) Methods for the identification and characterization of mast cells by light microscopy. in Mast cell differentiation and heterogeneity, eds Befus AD Bienenstock J Denburg JA (Raven, New York), pp 405–417.
10.1182/blood.V73.1.137.137 / Blood / In situ hybridization histochemistry localization of interleukin-3 mRNA in mouse brain. by Farrar (1989)
10.4049/jimmunol.135.6.4044 / J Immunol / Astrocytes of the brain synthesize interleukin-3 like factors. by Frei (1985)
10.1159/000143462 / Acta Anat / Fine structure of mast cells in the central nervous system of the hedgehog. by Flood (1970)
Galli SJ Wershil BK Gordon JR Tsai M Hammel I (1993) Insight into mast cell development and function derived from analyses of mice carrying mutations at beige, W/c-kit, or SI/SCF (c-kit ligand) loci. in The mast cell in health and disease, eds Marcel M Kaliner A Metcalfe DD (Marcel Dekker, New York), pp 109–128.
10.1016/S0165-3806(98)00121-7
10.1111/j.1471-4159.1985.tb07191.x
Goldstein SM Wintroub BU (1993) Mast cell proteases. in The mast cell in health and disease, eds Kaliner MA Metcalfe DD (Marcel Dekker, New York), pp 343–380.
Gruber BL Kaplan AP (1993) Mast cells and rheumatic disease, Ed 12 (McCarty DJ, Koopman WJ, eds), pp 5860–5867. (Lea and Febiger, Philadelphia).
10.4049/jimmunol.152.12.5860 / J Immunol / Transforming growth factor-β1 mediates mast cell chemotaxis. by Gruber (1994)
10.1182/blood.V86.7.2488.2488 / Blood / Angiogenic factors stimulate mast cell migration. by Gruber (1995)
10.1016/S0092-8674(00)81594-9
10.4049/jimmunol.149.6.1964 / J Immunol / Expression of murine β7, α4 and β1 integrin genes by rodent mast cells. by Gurish (1992)
10.1016/S0733-8635(18)30221-3 / Dermatol Clin / Mast cell and myofibroblast in wound healing. by Hebda (1993)
10.1002/jnr.490280213
10.1016/0022-510X(74)90043-4
10.1159/000145062 / Acta Anat / The mast cells of the mammalian central nervous system. III. Ultrastructural characteristics in the adult rat brain. by Ibrahim (1979)
10.1016/0006-8993(88)90929-8
10.1128/cdli.2.3.297-301.1995 / Clin Diagn Lab Immunol / Connective tissue mast cells exhibit time-dependent degranulation heterogeneity. by Kaminer (1995)
10.1182/blood.V82.8.2353.2353 / Blood / Stage specific expression of c-kit protein by murine hematopoietic progenitors. by Katayama (1993)
10.1016/S0021-9258(18)68793-9 / J Biol Chem / Synthesis, processing and secretion of recombinant human factor VIII expressed in mammalian cells. by Kaufman (1988)
10.1097/00000441-199309000-00011
{'key': '2023041302435191000_20.1.401.41', 'first-page': '191', 'article-title': 'Proteoglycans in haematoapoietic cells.', 'volume': '1032', 'author': 'Kolset', 'year': '1990', 'journal-title': 'Biochim Biophys Acta'} / Biochim Biophys Acta / Proteoglycans in haematoapoietic cells. by Kolset (1990)
10.1016/0165-3806(90)90077-C
10.1073/pnas.91.9.3739
10.1159/000235052 / Int Arch Allergy Appl Immunol / Differential release of histamine and prostaglandin D2 in rat peritoneal mast cells activated with peptides. by Levi-Schaffer (1989)
10.1002/j.1460-2075.1985.tb03963.x / EMBO J / Laminin-immunoreactive glia distinguish regenerative adult CNS systems from non-regenerative ones. by Liesi (1985)
10.1126/science.2911721
10.1016/0306-4522(94)90016-7
10.4049/jimmunol.156.5.1942 / J Immunol / The phosphatidylinositol 3-kinase inhibitor wortmannin blocks mast cell exocytosis but not IL-6 production. by Marquardt (1996)
10.1002/eji.1830230911 / Eur J Immunol / Leukemia inhibitory factor production by rat mast cells. by Marshall (1993)
10.1159/000236931
10.1002/(SICI)1096-9861(19960226)366:1<44::AID-CNE4>3.0.CO;2-K
10.1007/BF00150617
10.1007/BF00489511
10.1007/BF01884453 / Virchows Arch Pathol Anat / Über das Vorkommen der sogenannten “Mastzellen” bei pathologischen Veranderungen des Gehirns. by Neumann (1890)
10.1038/359241a0
{'key': '2023041302435191000_20.1.401.56', 'first-page': '93', 'article-title': 'Histamine content and mast cells distribution in mouse uterus: the effect of sexual hormones, gestation and labor.', 'volume': '36', 'author': 'Padilla', 'year': '1990', 'journal-title': 'Cell Mol Biol'} / Cell Mol Biol / Histamine content and mast cells distribution in mouse uterus: the effect of sexual hormones, gestation and labor. by Padilla (1990)
10.1016/S0163-1047(83)90995-0
{'key': '2023041302435191000_20.1.401.58', 'first-page': '332', 'article-title': 'Early changes in experimental allergic neuritis.', 'volume': '48', 'author': 'Powell', 'year': '1983', 'journal-title': 'Lab Invest'} / Lab Invest / Early changes in experimental allergic neuritis. by Powell (1983)
10.1159/000235059 / Int Arch Allergy Appl Immunol / Contribution of post-secretory mechanisms to the observed pattern of histamine and 5HT secretion from peritoneal mast cells in response to compound 48/80. by Purcell (1989)
10.1126/science.271.5250.818
10.1016/0006-291X(90)90372-T / Biophys Biochem Res Commun / Synthesis of a nitric oxide-like factor from l-arginine by rat serosal mast cells. by Salvemini (1990)
10.1016/0165-5728(89)90140-9
10.1111/j.1365-2826.1992.tb00160.x / J Neuroendocrinol / Sexual behavior triggers the appearance of non-neuronal cells containing gonadotropin-releasing hormone-like immunoreactivity. by Silver (1992)
10.1016/0166-2236(96)81863-7
10.1073/pnas.91.9.3695
{'key': '2023041302435191000_20.1.401.66', 'first-page': '634', 'article-title': 'Mouse bone marrow-derived mast cells roll on P-selectin under conditions of flow in vivo.', 'volume': '74', 'author': 'Sriramarao', 'year': '1996', 'journal-title': 'Lab Invest'} / Lab Invest / Mouse bone marrow-derived mast cells roll on P-selectin under conditions of flow in vivo. by Sriramarao (1996)
10.1016/0149-7634(82)90003-3
10.1016/0024-3205(90)90129-F
{'key': '2023041302435191000_20.1.401.69', 'first-page': '137', 'article-title': 'Activated rat peritoneal mast cells can cause syngeneic brain demyelination in vitro.', 'volume': '4', 'author': 'Theoharides', 'year': '1991', 'journal-title': 'Int J Immunopathol Pharmacol'} / Int J Immunopathol Pharmacol / Activated rat peritoneal mast cells can cause syngeneic brain demyelination in vitro. by Theoharides (1991)
10.1210/en.136.12.5745
Thompson HL Metcalfe DD (1993) Adhesion receptors and their relevance to the biology of mast cells and basophils. in The mast cell in health and disease, eds Kaliner MA Metcalfe DD (Marcel Dekker, New York), pp 763–799.
10.4049/jimmunol.145.10.3425 / J Immunol / Regulation of adhesion of mouse bone marrow-derived mast cells to laminin. by Thompson (1990)
{'key': '2023041302435191000_20.1.401.73', 'first-page': '144', 'article-title': 'Identification of an amino acid sequence in the laminin A chain mediating mast cell attachment and spreading.', 'volume': '72', 'author': 'Thompson', 'year': '1991', 'journal-title': 'Immunology'} / Immunology / Identification of an amino acid sequence in the laminin A chain mediating mast cell attachment and spreading. by Thompson (1991)
10.1111/j.1365-2222.1993.tb00321.x
10.1084/jem.174.1.125
10.1159/000236976
10.1016/S0021-9258(19)40239-1 / J Biol Chem / Mast cells contain spleen-type prostaglandin D synthetase. by Urade (1990)
10.1523/JNEUROSCI.17-20-07683.1997
10.1002/ar.1092310411
{'key': '2023041302435191000_20.1.401.80', 'first-page': '221', 'article-title': 'Traffic of hematogenous cells through the central nervous system.', 'volume': '202', 'author': 'Williams', 'year': '1995', 'journal-title': 'Curr Top Microbiol Immunol'} / Curr Top Microbiol Immunol / Traffic of hematogenous cells through the central nervous system. by Williams (1995)
Woodbury RG Le Trong H Cole K Neurath H Miller HRP (1989) Rat mast cell proteases. in Mast cells and basophil differentiation and function in health and disease, eds Galli SJ Austen KF (Raven, New York), pp 71–79.
10.1172/JCI114295
10.1006/hbeh.1993.1021
10.1002/(SICI)1097-4695(199612)31:4<393::AID-NEU1>3.0.CO;2-4
10.1002/(SICI)1096-9861(19990614)408:4<477::AID-CNE3>3.0.CO;2-O

Dates

Type	When
Created	7 years, 5 months ago (April 4, 2018, 4:40 p.m.)
Deposited	2 years, 4 months ago (April 13, 2023, 9:06 a.m.)
Indexed	1 week ago (Aug. 30, 2025, 12:48 p.m.)
Issued	25 years, 8 months ago (Jan. 1, 2000)
Published	25 years, 8 months ago (Jan. 1, 2000)
Published Online	25 years, 8 months ago (Jan. 1, 2000)
Published Print	25 years, 8 months ago (Jan. 1, 2000)

Funders 0

None

BibTeX

@article{Silverman_2000, title={Mast Cells Migrate from Blood to Brain}, volume={20}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.20-01-00401.2000}, DOI={10.1523/jneurosci.20-01-00401.2000}, number={1}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Silverman, Ann-Judith and Sutherland, Anne K. and Wilhelm, Marta and Silver, Rae}, year={2000}, month=jan, pages={401–408} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        30
      ]
    ],
    "date-time": "2025-08-30T16:48:43Z",
    "timestamp": 1756572523055
  },
  "reference-count": 85,
  "publisher": "Society for Neuroscience",
  "issue": "1",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2000,
            7,
            1
          ]
        ],
        "date-time": "2000-07-01T00:00:00Z",
        "timestamp": 962409600000
      },
      "content-version": "vor",
      "delay-in-days": 182,
      "URL": "https://creativecommons.org/licenses/by-nc-sa/4.0/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        1,
        1
      ]
    ]
  },
  "abstract": "<jats:p>It is well established that mast cells (MCs) occur within the CNS of many species. Furthermore, their numbers can increase rapidly in adults in response to altered physiological conditions. In this study we found that early postpartum rats had significantly more mast cells in the thalamus than virgin controls. Evidence from semithin sections from these females suggested that mast cells were transiting across the medium-sized blood vessels. We hypothesized that the increases in mast cell number were caused by their migration into the neural parenchyma. To this end, we purified rat peritoneal mast cells, labeled them with the vital dyes PKH26 or CellTracker Green, and injected them into host animals. One hour after injection, dye-filled cells, containing either histamine or serotonin (mediators stored in mast cells), were located close to thalamic blood vessels. Injected cells represented \u223c2\u201320% of the total mast cell population in this brain region. Scanning confocal microscopy confirmed that the biogenic amine and the vital dye occurred in the same cell. To determine whether the donor mast cells were within the blood\u2013brain barrier, we studied the localization of dye-marked donor cells and either Factor VIII, a component of endothelial basal laminae, or glial fibrillary acidic protein, the intermediate filament found in astrocytes. Serial section reconstructions of confocal images demonstrated that the mast cells were deep to the basal lamina, in nests of glial processes. This is the first demonstration that mast cells can rapidly penetrate brain blood vessels, and this may account for the rapid increases in mast cell populations after physiological manipulations.</jats:p>",
  "DOI": "10.1523/jneurosci.20-01-00401.2000",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2018,
        4,
        4
      ]
    ],
    "date-time": "2018-04-04T20:40:32Z",
    "timestamp": 1522874432000
  },
  "page": "401-408",
  "source": "Crossref",
  "is-referenced-by-count": 185,
  "title": "Mast Cells Migrate from Blood to Brain",
  "prefix": "10.1523",
  "volume": "20",
  "author": [
    {
      "given": "Ann-Judith",
      "family": "Silverman",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Anne K.",
      "family": "Sutherland",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Marta",
      "family": "Wilhelm",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Rae",
      "family": "Silver",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "393",
  "published-online": {
    "date-parts": [
      [
        2000,
        1,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2023041302435191000_20.1.401.1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1090940210"
    },
    {
      "key": "2023041302435191000_20.1.401.2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.pa.30.040190.003021"
    },
    {
      "key": "2023041302435191000_20.1.401.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.902730204"
    },
    {
      "key": "2023041302435191000_20.1.401.4",
      "doi-asserted-by": "crossref",
      "unstructured": "Bacallao R Kiai K Jesaitis L (1995) Guiding principles in specimen preservation for confocal microscopy. in Handbook of biological confocal microscopy, ed Pawley JB (Plenum, New York), pp 311\u2013326.",
      "DOI": "10.1007/978-1-4757-5348-6_18"
    },
    {
      "key": "2023041302435191000_20.1.401.5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00269011"
    },
    {
      "key": "2023041302435191000_20.1.401.6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1161/01.CIR.91.2.275"
    },
    {
      "key": "2023041302435191000_20.1.401.7",
      "doi-asserted-by": "crossref",
      "first-page": "3665",
      "DOI": "10.4049/jimmunol.149.11.3665",
      "article-title": "IL-3-dependent mast cells attach to plate-bound vitronectin. Demonstration of augmented proliferation in response to signals transduced via cell surface vitronectin receptors.",
      "volume": "149",
      "author": "Bianchine",
      "year": "1992",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/aja.1001670209"
    },
    {
      "key": "2023041302435191000_20.1.401.9",
      "doi-asserted-by": "crossref",
      "first-page": "S75",
      "DOI": "10.1002/ana.410270719",
      "article-title": "Mechanisms of autoimmune neuropathies.",
      "volume": "27",
      "author": "Brosnan",
      "year": "1990",
      "journal-title": "Ann Neurol"
    },
    {
      "key": "2023041302435191000_20.1.401.10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(86)90051-5"
    },
    {
      "key": "2023041302435191000_20.1.401.11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00001756-199902250-00024"
    },
    {
      "key": "2023041302435191000_20.1.401.12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.903690102"
    },
    {
      "key": "2023041302435191000_20.1.401.13",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/275661a0"
    },
    {
      "key": "2023041302435191000_20.1.401.14",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0165-5728(92)90047-O"
    },
    {
      "key": "2023041302435191000_20.1.401.15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(90)90234-U"
    },
    {
      "key": "2023041302435191000_20.1.401.16",
      "first-page": "5",
      "article-title": "Learned sensitivity.",
      "volume": "71",
      "author": "Djuric",
      "year": "1993",
      "journal-title": "Ann Allergy"
    },
    {
      "key": "2023041302435191000_20.1.401.17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1091740207"
    },
    {
      "key": "2023041302435191000_20.1.401.18",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000144540"
    },
    {
      "key": "2023041302435191000_20.1.401.19",
      "unstructured": "Enerback L Miller HRP Mayrhofer G (1986) Methods for the identification and characterization of mast cells by light microscopy. in Mast cell differentiation and heterogeneity, eds Befus AD Bienenstock J Denburg JA (Raven, New York), pp 405\u2013417."
    },
    {
      "key": "2023041302435191000_20.1.401.20",
      "doi-asserted-by": "crossref",
      "first-page": "137",
      "DOI": "10.1182/blood.V73.1.137.137",
      "article-title": "In situ hybridization histochemistry localization of interleukin-3 mRNA in mouse brain.",
      "volume": "73",
      "author": "Farrar",
      "year": "1989",
      "journal-title": "Blood"
    },
    {
      "key": "2023041302435191000_20.1.401.21",
      "doi-asserted-by": "crossref",
      "first-page": "4044",
      "DOI": "10.4049/jimmunol.135.6.4044",
      "article-title": "Astrocytes of the brain synthesize interleukin-3 like factors.",
      "volume": "135",
      "author": "Frei",
      "year": "1985",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.22",
      "doi-asserted-by": "crossref",
      "first-page": "443",
      "DOI": "10.1159/000143462",
      "article-title": "Fine structure of mast cells in the central nervous system of the hedgehog.",
      "volume": "75",
      "author": "Flood",
      "year": "1970",
      "journal-title": "Acta Anat"
    },
    {
      "key": "2023041302435191000_20.1.401.23",
      "unstructured": "Galli SJ Wershil BK Gordon JR Tsai M Hammel I (1993) Insight into mast cell development and function derived from analyses of mice carrying mutations at beige, W/c-kit, or SI/SCF (c-kit ligand) loci. in The mast cell in health and disease, eds Marcel M Kaliner A Metcalfe DD (Marcel Dekker, New York), pp 109\u2013128."
    },
    {
      "key": "2023041302435191000_20.1.401.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0165-3806(98)00121-7"
    },
    {
      "key": "2023041302435191000_20.1.401.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1985.tb07191.x"
    },
    {
      "key": "2023041302435191000_20.1.401.26",
      "unstructured": "Goldstein SM Wintroub BU (1993) Mast cell proteases. in The mast cell in health and disease, eds Kaliner MA Metcalfe DD (Marcel Dekker, New York), pp 343\u2013380."
    },
    {
      "key": "2023041302435191000_20.1.401.27",
      "unstructured": "Gruber BL Kaplan AP (1993) Mast cells and rheumatic disease, Ed 12 (McCarty DJ, Koopman WJ, eds), pp 5860\u20135867. (Lea and Febiger, Philadelphia)."
    },
    {
      "key": "2023041302435191000_20.1.401.28",
      "doi-asserted-by": "crossref",
      "first-page": "5860",
      "DOI": "10.4049/jimmunol.152.12.5860",
      "article-title": "Transforming growth factor-\u03b21 mediates mast cell chemotaxis.",
      "volume": "152",
      "author": "Gruber",
      "year": "1994",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.29",
      "doi-asserted-by": "crossref",
      "first-page": "2488",
      "DOI": "10.1182/blood.V86.7.2488.2488",
      "article-title": "Angiogenic factors stimulate mast cell migration.",
      "volume": "86",
      "author": "Gruber",
      "year": "1995",
      "journal-title": "Blood"
    },
    {
      "key": "2023041302435191000_20.1.401.30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81594-9"
    },
    {
      "key": "2023041302435191000_20.1.401.31",
      "doi-asserted-by": "crossref",
      "first-page": "1964",
      "DOI": "10.4049/jimmunol.149.6.1964",
      "article-title": "Expression of murine \u03b27, \u03b14 and \u03b21 integrin genes by rodent mast cells.",
      "volume": "149",
      "author": "Gurish",
      "year": "1992",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.32",
      "doi-asserted-by": "crossref",
      "first-page": "685",
      "DOI": "10.1016/S0733-8635(18)30221-3",
      "article-title": "Mast cell and myofibroblast in wound healing.",
      "volume": "11",
      "author": "Hebda",
      "year": "1993",
      "journal-title": "Dermatol Clin"
    },
    {
      "key": "2023041302435191000_20.1.401.33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jnr.490280213"
    },
    {
      "key": "2023041302435191000_20.1.401.34",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-510X(74)90043-4"
    },
    {
      "key": "2023041302435191000_20.1.401.35",
      "doi-asserted-by": "crossref",
      "first-page": "134",
      "DOI": "10.1159/000145062",
      "article-title": "The mast cells of the mammalian central nervous system. III. Ultrastructural characteristics in the adult rat brain.",
      "volume": "104",
      "author": "Ibrahim",
      "year": "1979",
      "journal-title": "Acta Anat"
    },
    {
      "key": "2023041302435191000_20.1.401.36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(88)90929-8"
    },
    {
      "key": "2023041302435191000_20.1.401.37",
      "doi-asserted-by": "crossref",
      "first-page": "297",
      "DOI": "10.1128/cdli.2.3.297-301.1995",
      "article-title": "Connective tissue mast cells exhibit time-dependent degranulation heterogeneity.",
      "volume": "2",
      "author": "Kaminer",
      "year": "1995",
      "journal-title": "Clin Diagn Lab Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.38",
      "doi-asserted-by": "crossref",
      "first-page": "2353",
      "DOI": "10.1182/blood.V82.8.2353.2353",
      "article-title": "Stage specific expression of c-kit protein by murine hematopoietic progenitors.",
      "volume": "82",
      "author": "Katayama",
      "year": "1993",
      "journal-title": "Blood"
    },
    {
      "key": "2023041302435191000_20.1.401.39",
      "doi-asserted-by": "crossref",
      "first-page": "6352",
      "DOI": "10.1016/S0021-9258(18)68793-9",
      "article-title": "Synthesis, processing and secretion of recombinant human factor VIII expressed in mammalian cells.",
      "volume": "263",
      "author": "Kaufman",
      "year": "1988",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023041302435191000_20.1.401.40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00000441-199309000-00011"
    },
    {
      "key": "2023041302435191000_20.1.401.41",
      "first-page": "191",
      "article-title": "Proteoglycans in haematoapoietic cells.",
      "volume": "1032",
      "author": "Kolset",
      "year": "1990",
      "journal-title": "Biochim Biophys Acta"
    },
    {
      "key": "2023041302435191000_20.1.401.42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0165-3806(90)90077-C"
    },
    {
      "key": "2023041302435191000_20.1.401.43",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.91.9.3739"
    },
    {
      "key": "2023041302435191000_20.1.401.44",
      "doi-asserted-by": "crossref",
      "first-page": "352",
      "DOI": "10.1159/000235052",
      "article-title": "Differential release of histamine and prostaglandin D2 in rat peritoneal mast cells activated with peptides.",
      "volume": "90",
      "author": "Levi-Schaffer",
      "year": "1989",
      "journal-title": "Int Arch Allergy Appl Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.45",
      "doi-asserted-by": "crossref",
      "first-page": "2505",
      "DOI": "10.1002/j.1460-2075.1985.tb03963.x",
      "article-title": "Laminin-immunoreactive glia distinguish regenerative adult CNS systems from non-regenerative ones.",
      "volume": "4",
      "author": "Liesi",
      "year": "1985",
      "journal-title": "EMBO J"
    },
    {
      "key": "2023041302435191000_20.1.401.46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2911721"
    },
    {
      "key": "2023041302435191000_20.1.401.47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(94)90016-7"
    },
    {
      "key": "2023041302435191000_20.1.401.48",
      "doi-asserted-by": "crossref",
      "first-page": "1942",
      "DOI": "10.4049/jimmunol.156.5.1942",
      "article-title": "The phosphatidylinositol 3-kinase inhibitor wortmannin blocks mast cell exocytosis but not IL-6 production.",
      "volume": "156",
      "author": "Marquardt",
      "year": "1996",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.49",
      "doi-asserted-by": "crossref",
      "first-page": "2116",
      "DOI": "10.1002/eji.1830230911",
      "article-title": "Leukemia inhibitory factor production by rat mast cells.",
      "volume": "23",
      "author": "Marshall",
      "year": "1993",
      "journal-title": "Eur J Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000236931"
    },
    {
      "key": "2023041302435191000_20.1.401.51",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1096-9861(19960226)366:1<44::AID-CNE4>3.0.CO;2-K"
    },
    {
      "key": "2023041302435191000_20.1.401.52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00150617"
    },
    {
      "key": "2023041302435191000_20.1.401.53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00489511"
    },
    {
      "key": "2023041302435191000_20.1.401.54",
      "doi-asserted-by": "crossref",
      "first-page": "378",
      "DOI": "10.1007/BF01884453",
      "article-title": "\u00dcber das Vorkommen der sogenannten \u201cMastzellen\u201d bei pathologischen Veranderungen des Gehirns.",
      "volume": "122",
      "author": "Neumann",
      "year": "1890",
      "journal-title": "Virchows Arch Pathol Anat"
    },
    {
      "key": "2023041302435191000_20.1.401.55",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/359241a0"
    },
    {
      "key": "2023041302435191000_20.1.401.56",
      "first-page": "93",
      "article-title": "Histamine content and mast cells distribution in mouse uterus: the effect of sexual hormones, gestation and labor.",
      "volume": "36",
      "author": "Padilla",
      "year": "1990",
      "journal-title": "Cell Mol Biol"
    },
    {
      "key": "2023041302435191000_20.1.401.57",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0163-1047(83)90995-0"
    },
    {
      "key": "2023041302435191000_20.1.401.58",
      "first-page": "332",
      "article-title": "Early changes in experimental allergic neuritis.",
      "volume": "48",
      "author": "Powell",
      "year": "1983",
      "journal-title": "Lab Invest"
    },
    {
      "key": "2023041302435191000_20.1.401.59",
      "doi-asserted-by": "crossref",
      "first-page": "387",
      "DOI": "10.1159/000235059",
      "article-title": "Contribution of post-secretory mechanisms to the observed pattern of histamine and 5HT secretion from peritoneal mast cells in response to compound 48/80.",
      "volume": "90",
      "author": "Purcell",
      "year": "1989",
      "journal-title": "Int Arch Allergy Appl Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.60",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.271.5250.818"
    },
    {
      "key": "2023041302435191000_20.1.401.61",
      "doi-asserted-by": "crossref",
      "first-page": "596",
      "DOI": "10.1016/0006-291X(90)90372-T",
      "article-title": "Synthesis of a nitric oxide-like factor from l-arginine by rat serosal mast cells.",
      "volume": "169",
      "author": "Salvemini",
      "year": "1990",
      "journal-title": "Biophys Biochem Res Commun"
    },
    {
      "key": "2023041302435191000_20.1.401.62",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0165-5728(89)90140-9"
    },
    {
      "key": "2023041302435191000_20.1.401.63",
      "doi-asserted-by": "crossref",
      "first-page": "207",
      "DOI": "10.1111/j.1365-2826.1992.tb00160.x",
      "article-title": "Sexual behavior triggers the appearance of non-neuronal cells containing gonadotropin-releasing hormone-like immunoreactivity.",
      "volume": "4",
      "author": "Silver",
      "year": "1992",
      "journal-title": "J Neuroendocrinol"
    },
    {
      "key": "2023041302435191000_20.1.401.64",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0166-2236(96)81863-7"
    },
    {
      "key": "2023041302435191000_20.1.401.65",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.91.9.3695"
    },
    {
      "key": "2023041302435191000_20.1.401.66",
      "first-page": "634",
      "article-title": "Mouse bone marrow-derived mast cells roll on P-selectin under conditions of flow in vivo.",
      "volume": "74",
      "author": "Sriramarao",
      "year": "1996",
      "journal-title": "Lab Invest"
    },
    {
      "key": "2023041302435191000_20.1.401.67",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0149-7634(82)90003-3"
    },
    {
      "key": "2023041302435191000_20.1.401.68",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0024-3205(90)90129-F"
    },
    {
      "key": "2023041302435191000_20.1.401.69",
      "first-page": "137",
      "article-title": "Activated rat peritoneal mast cells can cause syngeneic brain demyelination in vitro.",
      "volume": "4",
      "author": "Theoharides",
      "year": "1991",
      "journal-title": "Int J Immunopathol Pharmacol"
    },
    {
      "key": "2023041302435191000_20.1.401.70",
      "doi-asserted-by": "publisher",
      "DOI": "10.1210/en.136.12.5745"
    },
    {
      "key": "2023041302435191000_20.1.401.71",
      "unstructured": "Thompson HL Metcalfe DD (1993) Adhesion receptors and their relevance to the biology of mast cells and basophils. in The mast cell in health and disease, eds Kaliner MA Metcalfe DD (Marcel Dekker, New York), pp 763\u2013799."
    },
    {
      "key": "2023041302435191000_20.1.401.72",
      "doi-asserted-by": "crossref",
      "first-page": "3425",
      "DOI": "10.4049/jimmunol.145.10.3425",
      "article-title": "Regulation of adhesion of mouse bone marrow-derived mast cells to laminin.",
      "volume": "145",
      "author": "Thompson",
      "year": "1990",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.73",
      "first-page": "144",
      "article-title": "Identification of an amino acid sequence in the laminin A chain mediating mast cell attachment and spreading.",
      "volume": "72",
      "author": "Thompson",
      "year": "1991",
      "journal-title": "Immunology"
    },
    {
      "key": "2023041302435191000_20.1.401.74",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2222.1993.tb00321.x"
    },
    {
      "key": "2023041302435191000_20.1.401.75",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.174.1.125"
    },
    {
      "key": "2023041302435191000_20.1.401.76",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000236976"
    },
    {
      "key": "2023041302435191000_20.1.401.77",
      "doi-asserted-by": "crossref",
      "first-page": "371",
      "DOI": "10.1016/S0021-9258(19)40239-1",
      "article-title": "Mast cells contain spleen-type prostaglandin D synthetase.",
      "volume": "265",
      "author": "Urade",
      "year": "1990",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023041302435191000_20.1.401.78",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.17-20-07683.1997"
    },
    {
      "key": "2023041302435191000_20.1.401.79",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1092310411"
    },
    {
      "key": "2023041302435191000_20.1.401.80",
      "first-page": "221",
      "article-title": "Traffic of hematogenous cells through the central nervous system.",
      "volume": "202",
      "author": "Williams",
      "year": "1995",
      "journal-title": "Curr Top Microbiol Immunol"
    },
    {
      "key": "2023041302435191000_20.1.401.81",
      "unstructured": "Woodbury RG Le Trong H Cole K Neurath H Miller HRP (1989) Rat mast cell proteases. in Mast cells and basophil differentiation and function in health and disease, eds Galli SJ Austen KF (Raven, New York), pp 71\u201379."
    },
    {
      "key": "2023041302435191000_20.1.401.82",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI114295"
    },
    {
      "key": "2023041302435191000_20.1.401.83",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/hbeh.1993.1021"
    },
    {
      "key": "2023041302435191000_20.1.401.84",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-4695(199612)31:4<393::AID-NEU1>3.0.CO;2-4"
    },
    {
      "key": "2023041302435191000_20.1.401.85",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1096-9861(19990614)408:4<477::AID-CNE3>3.0.CO;2-O"
    }
  ],
  "container-title": "The Journal of Neuroscience",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1523/JNEUROSCI.20-01-00401.2000",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        4,
        13
      ]
    ],
    "date-time": "2023-04-13T13:06:18Z",
    "timestamp": 1681391178000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.jneurosci.org/lookup/doi/10.1523/JNEUROSCI.20-01-00401.2000"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        1,
        1
      ]
    ]
  },
  "references-count": 85,
  "journal-issue": {
    "issue": "1",
    "published-online": {
      "date-parts": [
        [
          2000,
          1,
          1
        ]
      ]
    },
    "published-print": {
      "date-parts": [
        [
          2000,
          1,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1523/JNEUROSCI.20-01-00401.2000"
  ],
  "URL": "http://dx.doi.org/10.1523/JNEUROSCI.20-01-00401.2000",
  "relation": {},
  "ISSN": [
    "0270-6474",
    "1529-2401"
  ],
  "subject": [],
  "container-title-short": "J. Neurosci.",
  "published": {
    "date-parts": [
      [
        2000,
        1,
        1
      ]
    ]
  }
}