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. 1984 Apr;51(4):643–651.

In vitro studies on mast cell proliferation in N. brasiliensis infection.

D M Haig, E E Jarrett, J Tas
PMCID: PMC1454536  PMID: 6608486

Abstract

We have previously shown that mast cells with the morphological and biochemical properties of mucosal mast cells (MMC) proliferate and mature in rat bone marrow cultures stimulated with factors from antigen or mitogen-activated T lymphocytes. Here we have used this system to explore the MMC hyperplasia which occurs in infections with gastrointestinal nematode parasites. Lymphocytes producing MMC-growth factor were present from day 10 onwards in N. brasiliensis-infected rats and mesenteric lymph nodes (MLN) were the major source of activated lymphocytes. When different tissues of normal rats were cultured in the presence of conditioned medium by far the greatest proliferation of MMC occurred in bone marrow, indicating an origin of MMC from haemopoietic precursors. Cultures of infected rat bone marrow yielded considerably greater numbers of MMC than cultures of normal rat bone marrow and experiments using semisolid culture media indicated that N. brasiliensis infection causes an increase in the frequency of MMC progenitors in the bone marrow. A scheme is put forward for the sequence of events occurring in vivo based on the results of these and other published experiments. The reasons for the restricted in vivo localization of MMC to the mucous membranes and associated lymph nodes is discussed. Finally we give the results of microspectrophotometric analysis which has shown that the cultured mast cell contain a non-heparin proteoglycan, thus adding a further feature to the list of MMC-like properties of these cells.

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Selected References

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

  1. Bradley T. R., Metcalf D. The growth of mouse bone marrow cells in vitro. Aust J Exp Biol Med Sci. 1966 Jun;44(3):287–299. doi: 10.1038/icb.1966.28. [DOI] [PubMed] [Google Scholar]
  2. Crapper R. M., Schrader J. W. Frequency of mast cell precursors in normal tissues determined by an in vitro assay: antigen induces parallel increases in the frequency of P cell precursors and mast cells. J Immunol. 1983 Aug;131(2):923–928. [PubMed] [Google Scholar]
  3. Denburg J. A., Befus A. D., Bienenstock J. Growth and differentiation in vitro of mast cells from mesenteric lymph nodes of Nippostrongylus brasiliensis-infected rats. Immunology. 1980 Sep;41(1):195–202. [PMC free article] [PubMed] [Google Scholar]
  4. Ellis W. M., Dobrostanski B., Paton C. M., Aitken W. A reliable technique for making permanent preparations of bone marrow cultures. Pathology. 1980 Oct;12(4):587–590. doi: 10.3109/00313028009086811. [DOI] [PubMed] [Google Scholar]
  5. GINSBURG H., SACHS L. FORMATION OF PURE SUSPENSIONS OF MAST CELLS IN TISSUE CULTURE BY DIFFERENTIATION OF LYMPHOID CELLS FROM THE MOUSE THYMUS. J Natl Cancer Inst. 1963 Jul;31:1–39. [PubMed] [Google Scholar]
  6. Galli S. J., Dvorak A. M., Marcum J. A., Ishizaka T., Nabel G., Der Simonian H., Pyne K., Goldin J. M., Rosenberg R. D., Cantor H. Mast cell clones: a model for the analysis of cellular maturation. J Cell Biol. 1982 Nov;95(2 Pt 1):435–444. doi: 10.1083/jcb.95.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ginsburg H., Ben-Shahar D., Ben-David E. Mast cell growth on fibroblast monolayers: two-cell entities. Immunology. 1982 Feb;45(2):371–380. [PMC free article] [PubMed] [Google Scholar]
  8. Haig D. M., McKee T. A., Jarrett E. E., Woodbury R., Miller H. R. Generation of mucosal mast cells is stimulated in vitro by factors derived from T cells of helminth-infected rats. Nature. 1982 Nov 11;300(5888):188–190. doi: 10.1038/300188a0. [DOI] [PubMed] [Google Scholar]
  9. Haig D. M., McMenamin C., Gunneberg C., Woodbury R., Jarrett E. E. Stimulation of mucosal mast cell growth in normal and nude rat bone marrow cultures. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4499–4503. doi: 10.1073/pnas.80.14.4499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ishizaka T., Okudaira H., Mauser L. E., Ishizaka K. Development of rat mast cells in vitro. I. Differentiation of mast cells from thymus cells. J Immunol. 1976 Mar;116(3):747–754. [PubMed] [Google Scholar]
  11. Jarrett E. E., Miller H. R. Production and activities of IgE in helminth infection. Prog Allergy. 1982;31:178–233. [PubMed] [Google Scholar]
  12. Kitamura Y., Shimada M., Hatanaka K., Miyano Y. Development of mast cells from grafted bone marrow cells in irradiated mice. Nature. 1977 Aug 4;268(5619):442–443. doi: 10.1038/268442a0. [DOI] [PubMed] [Google Scholar]
  13. Mayrhofer G., Bazin H. Nature of the thymus dependency of mucosal mast cells. III. Mucosal mast cells in nude mice and nude rats, in B rats and in a child with the Di George syndrome. Int Arch Allergy Appl Immunol. 1981;64(3):320–331. doi: 10.1159/000232710. [DOI] [PubMed] [Google Scholar]
  14. Mayrhofer G. The nature of the thymus dependency of mucosal mast cells. II. The effect of thymectomy and of depleting recirculating lymphocytes on the response to Nippostrongylus brasilliensis. Cell Immunol. 1979 Oct;47(2):312–322. doi: 10.1016/0008-8749(79)90341-1. [DOI] [PubMed] [Google Scholar]
  15. McCarthy J. H., Mandel T. E., Garson O. M., Metcalf D. The presence of mast cells in agar cultures. Exp Hematol. 1980 May;8(5):562–567. [PubMed] [Google Scholar]
  16. Nabel G., Galli S. J., Dvorak A. M., Dvorak H. F., Cantor H. Inducer T lymphocytes synthesize a factor that stimulates proliferation of cloned mast cells. Nature. 1981 May 28;291(5813):332–334. doi: 10.1038/291332a0. [DOI] [PubMed] [Google Scholar]
  17. Nagao K., Yokoro K., Aaronson S. A. Continuous lines of basophil/mast cells derived from normal mouse bone marrow. Science. 1981 Apr 17;212(4492):333–335. doi: 10.1126/science.7209531. [DOI] [PubMed] [Google Scholar]
  18. Nakahata T., Spicer S. S., Cantey J. R., Ogawa M. Clonal assay of mouse mast cell colonies in methylcellulose culture. Blood. 1982 Aug;60(2):352–361. [PubMed] [Google Scholar]
  19. Nawa Y., Miller H. R. Adoptive transfer of the intestinal mast cell response in rats infected with Nippostrongylus brasiliensis. Cell Immunol. 1979 Feb;42(2):225–239. doi: 10.1016/0008-8749(79)90188-6. [DOI] [PubMed] [Google Scholar]
  20. Ogilvie B. M., Hesketh P. M., Rose M. E. Nippostrongylus brasiliensis: peripheral blood leucocyte response of rats, with special reference to basophils. Exp Parasitol. 1978 Nov;46(1):20–30. doi: 10.1016/0014-4894(78)90153-4. [DOI] [PubMed] [Google Scholar]
  21. Parrott D. M., Wilkinson P. C. Lymphocyte locomotion and migration. Prog Allergy. 1981;28:193–284. [PubMed] [Google Scholar]
  22. Razin E., Cordon-Cardo C., Good R. A. Growth of a pure population of mouse mast cells in vitro with conditioned medium derived from concanavalin A-stimulated splenocytes. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2559–2561. doi: 10.1073/pnas.78.4.2559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. Sredni B., Friedman M. M., Bland C. E., Metcalfe D. D. Ultrastructural, biochemical, and functional characteristics of histamine-containing cells cloned from mouse bone marrow: tentative identification as mucosal mast cells. J Immunol. 1983 Aug;131(2):915–922. [PubMed] [Google Scholar]
  26. Tas J., Berndsen R. G. Does heparin occur in mucosal mast cells of the rat small intestine? J Histochem Cytochem. 1977 Sep;25(9):1058–1062. doi: 10.1177/25.9.71326. [DOI] [PubMed] [Google Scholar]
  27. Tas J., Geenen L. H. Microspectrophotometric detection of heparin in mast cells and basophilic granulocytes stained metachromatically with Toluidine Blue O. Histochem J. 1975 May;7(3):231–248. doi: 10.1007/BF01003592. [DOI] [PubMed] [Google Scholar]
  28. Tertian G., Yung Y. P., Guy-Grand D., Moore M. A. Long-term in vitro culture of murine mast cells. I. Description of a growth factor-dependent culture technique. J Immunol. 1981 Aug;127(2):788–794. [PubMed] [Google Scholar]
  29. Woodbury R. G., Everitt M., Sanada Y., Katunuma N., Lagunoff D., Neurath H. A major serine protease in rat skeletal muscle: evidence for its mast cell origin. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5311–5313. doi: 10.1073/pnas.75.11.5311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Woodbury R. G., Gruzenski G. M., Lagunoff D. Immunofluorescent localization of a serine protease in rat small intestine. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2785–2789. doi: 10.1073/pnas.75.6.2785. [DOI] [PMC free article] [PubMed] [Google Scholar]

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