Summary
Mast cell (MC) secretion induces local cell proliferation lasting 48–72 h in fibroblasts and mesothelial cells in the almost avascular true mesentery of the rat. We studied this membranous tissue by transmission electron microscopy with regard to cellular and extracellular features occurring during the first 72 h following MC secretion.
After MC secretion elicited by compound 48/80, apparently all individual tissuebound cells (i.e. fibroblasts, mesothelial cells, and macrophages) show signs of accelerated metabolic activity. In fibroblasts, conspicuous increases in the volume of Golgi apparatus and rough endoplasmic reticulum and in the amount of plasmalemmal indentations suggest an increased production and secretion of the extracellular matrix. Released MC granules lying close to projections of nearby phagocytosing cells cause areas free from electrondense material in the extracellular matrix. MC secretion therefore appears to produce a remodelling of extracellular matrix. Most of the activities initiated by MC secretion start to subside within (48-)72 h.
The findings indicate a close functional relationship between the tissue MC and all its neighbouring cells and the surrounding extracellular matrix. The striking chain of events that it induces emphasizes strongly that the secreting MC plays a prominent although as yet in many respects enigmatic role in normal tissue.
Similar content being viewed by others
Abbreviations
- CM :
-
cytoplasmic matrix
- GA :
-
Golgi apparatus
- MC :
-
mast cell
- PL :
-
primary lysosome
- RER :
-
rough endoplasmic reticulum
- TEM :
-
transmission electron microscopy
References
Andrews PM, Porter KR (1973) The ultrastructural morphology and possible functional significance of mesothelial microvilli. Anat Rec 177:409–426
Azizkhan RG, Azizkhan JC, Zetter BR, Folkman J (1980) Mast cell heparin stimulates migration of capillary endothelial cells in vitro. J Exp Med 152:931–944
Birkedal-Hansen H, Cobb CM, Taylor RE, Fullmer HM (1976) Activation of fibroblast procollagenase by mast cell proteases. Biochim Biophys Acta 438:273–286
Bivin WS, Crawford MP, Brewer NR (1979) Morphophysiology. In: Baker HJ, Lindsey JR, Weisbroth SD (eds) The laboratory rat, vol I. Biology and diseases. Academic Press, New York, p 83
Bloom GD, Haegermark Ö (1965) A study on morphological changes and histamine release induced by Compound 48/80 in rat peritoneal mast cells. Exp Cell Res 40:637–654
Boréus LO (1960) A comparison of mastcell reactions in the rat, hamster and guineapig. Acta Physiol Scand 49:251–260
Combs JW (1966) Maturation of rat mast cells. An electron microscope study. J Cell Biol 31:563–575
Combs JW (1971) An electron microscope study of mouse mast cells arising in vivo and in vitro. J Cell Biol 48:674–684
Douglas WW (1980) Histamine and 5-hydroxytryptamine and their antagonists. In: Gilman AG, Goodman LS, Gilman A (eds) The pharmacological basis of therapeutics. Macmillan, New York, pp 609–649
Enerbäck L, Lundin PM (1974) Ultrastructure of mucosal mast cells in normal and compound 48/80treated rats. Cell Tissue Res 150:95–105
Eneström S, Hamberger A (1968) Respiration and mitochondrial content in single neurons of the supraoptic nucleus. J Cell Biol 38:483–493
Falke D, Kahl GF (1971) The inhibitory effect of compound 48/80 on the formation of giant cells induced by Herpes virus Hominis. J Gen Virol 10:273–277
Franzén L (1980) Mast cell secretion and connective tissue cell proliferation. Linköping University Medical Dissertations No 97
Franzén L (1981) Further studies on the relationship between druginduced mastcell secretion and local cell proliferation. Acta Pathol Microbiol Scand [A] 89:57–62
Franzén L, Norrby K (1977) Different proliferative responsiveness of fibroblasts and mesothelial cells in the rat mesentery following administration of compound 48/80 at various hours of the day. Virchows Arch (Cell Pathol) 24:91–99
Franzén L, Norrby K (1980) Local mitogenic effect of tissue mast cell secretion. Cell Tissue Kinet 13:635–642
Franzén L, Norrby K (1982) Immunological challenge causes mitogenic stimulation in normal connective tissue cells. Acta Pathol Microbiol Scand [A] 90:385–389
Holgate ST, Church MK (1982) Control of mediator release from mast cells. Clin Allergy 12 (Suppl):5–13
Holm Nielsen E, Clausen J (1982) Electron microscopic study of the regeneration in vivo of rat peritoneal mast cells after histamine secretion. Cell Tissue Res 224:465–468
Horsfield GI (1965) The effect of compound 48/80 on the rat mast cell. J Pathol Bact 90:599–605
Keiser HD (1980) The effects of lysosomal enzymes on extracellular substances. In: Weissman G (ed) The cell biology of inflammation. Elsevier North Holland, Amsterdam, pp 431–467
Lagunoff D (1968) The properties of mast cell proteases. Biochem Pharmacol Suppl: 221–227
Lagunoff D, Chi EY (1980) Cell biology of mast cells and basophils. In: Weissman G (ed) The cell biology of inflammation. Elsevier/North Holland, Amsterdam, pp 217–265
Lewis RA, Soter NA, Diamond PT, Austen KF, Oates JA, Jackson Roberts III L (1982) Prostaglandin D2 generation after activation of rat and human mast cells with antiIgE. J Immunol 129:1616–1631
Madison LD, BergstromPorter B, Torres AR, Shelton E (1979) Regulation of surface topography of mouse peritoneal cells. Formation of microvilli and vesiculated pits on omental mesothelial cells by serum and other proteins J Cell Biol 82:783–797
Metcalfe DD, Kaliner M (1981) Mast cells and basophils. In: Oppenheim JJ, Rosenstreich DL, Potter M (eds) Cellular functions in immunity and inflammation. Edward Arnold, London, pp 301–322
Mota I, Vugman J (1956) Action of compound 48/80 on the mast cells and histamine content of guinea pig tissues. Br J Pharmacol 11:304–307
Norrby K (1980) Mast cell histamine, a local mitogen acting via H2receptors in nearby tissue cells. Virchows Arch [Cell Pathol] 34:13–20
Norrby K (1981) On the 48/80induced secretion of tissue mast cells and its mitogenic effect on nearby cells in the intact rat. Virchows Arch [Cell Pathol] 38:57–65
Norrby K (1983) Intradermal mastcell secretion causing cutaneous mitogenesis. Virchows Arch [Cell Pathol] 42:263–269
Norrby K, Franzén L (1980) A tissue model for the study of cell proliferation in vitro. In Vitro 16:31–37
Norrby K, Enerbäck L, Franzén L (1976) Mast cell activation and tissue cell proliferation. Cell Tissue Res 170:289–303
Norrby K, Bergström S, Druvefors P (1981) Agedependent mitogenesis in normal connective tissue cells. Virchows Arch [Cell Pathol] 36:27–43
Norrby K, Arnqvist HJ, Bergström S, Druvefors P (1982) Augmented mitogenesis in normal connective tissue cells following mastcell secretion in diabetic rats. Virchows Arch [Cell Pathol] 39:137–144
Norrby K, Bergström S, Druvefors P (1983a) Hyperplasia and growth of the true mesentery in diabetic rat. Acta Pathol Microbiol Scand [A] 91:195–202
Norrby K, Bergström S, Druvefors P (1983b) On disturbance of homeostasis in organcultured tissue. Submitted for publication Paton WDM (1957) Histamine release by compounds of simple chemical structure. Pharmacol Rev 9:269–327
Patt LM, Houck JC (1983) Inhibition of normal and leukemic lymphocyte proliferation by compound 48/80. Biochem Pharmacol 32:565–567
Rothschild AM (1970) Mechanisms of histamine release by compound 48/80. Br J Pharmacol 38:253–262
Sakamoto S, Sakamoto M (1981) Heparin and bone metabolism. In: Lundblad RL, Brown WV, Mann KG, Roberts HR (eds) Chemistry and biology of heparin. Elsevier/North Holland, New York, pp 133–142
Schwartz LB, Austen KF (1982) Mast cells and mediators. In: Lachmann PJ, Peters DK (eds) Clinical aspects of immunology, (4th edition) vol 1. Blackwell Scientific Publications, Oxford, pp 130–157
Singleton EM, Clark SL Jr (1965) The response of mast cells to compound 48/80 studied with the electron microscope. Lab Invest 14:1744–1763
Sträuli P, Haemmerli G, Tschenett C, Krstić RV (1981) Different modes of mesenteric infiltration displayed by two rat leukemias. Virchows Arch [Cell Pathol] 35:93–108
Tannenbaum S, Oertel H, Henderson W, Kaliner M (1980) The biologic activity of mast cell granules. I. Elicitation of inflammatory responses in rat skin. J Immunol 125:325–335
Trelstad RL, Hayashi K (1979) Tendon collagen fibrillogenesis: intracellular subassemblies and surface changes associated with fibril growth. Dev Biol 71:228–242
Welsh RA, Geer JC (1959) Phagocytosis of mast cell granules by the eosinophilic leucocyte in the rat. Am J Pathol 35:103–111
Author information
Authors and Affiliations
Additional information
Supported by grants from the Swedish Medical Research Council, Project 5942
Rights and permissions
About this article
Cite this article
Norrby, K., Eneström, S. Cellular and extracellular changes following mast-cell secretion in avascular rat mesentery. Cell Tissue Res. 235, 339–345 (1984). https://doi.org/10.1007/BF00217858
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00217858