The role of interstitial collagens in cleft formation of mouse embryonic submandibular gland during initial branching.

An interstitial collagenase was purified from the explant medium of bovine dental pulp and was shown to degrade collagens I and III but not IV and V. The enzyme halted cleft initiation in the epithelium of 12-day mouse embryonic submandibular glands in vitro, indicating the active involvement of interstitial collagens in the branching morphogenesis. Transmission electron microscopic observation of the intact 12-day gland without any clefts showed the scattered localization of a few collagen fibrils at the epithelial-mesenchymal interface of the bulb and also revealed the presence of numerous microfibrils around the stalk. Collagen bundles were regularly seen close to the wavy basal lamina at the bottom of clefts of the intact 13-day gland and 12-day gland cultured for 17 h under normal conditions. Mesenchymal cells were found in the clefts together with the frequent localization of peripheral nerve fibres and capillary endothelial cells. The collagen bundles were more often observed in the 12-day gland cultured in the presence of bovine dental pulp collagenase inhibitor, which had been shown to enhance cleft formation. In contrast, collagen fibrils were rarely found at the epithelial-mesenchymal interface of the 12-day gland cultured in the presence of Clostridial or bovine dental pulp collagenase. The findings indicated that the formation of interstitial collagen bundles is essential to form clefts in the epithelium both in vivo and in vitro.

[1]  J. Kishi,et al.  Scanning electron microscopic observation of mouse embryonic submandibular glands during initial branching: preferential localization of fibrillar structures at the mesenchymal ridges participating in cleft formation. , 1986, Journal of embryology and experimental morphology.

[2]  J. Kishi,et al.  Local effects of implanted Elvax chips containing collagenase inhibitor and bacterial collagenase on branching morphogenesis of mouse embryonic submandibular glands in vitro , 1986 .

[3]  E Bell,et al.  Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Kishi,et al.  Purification and characterization of bovine dental pulp collagenase inhibitor. , 1984, Journal of biochemistry.

[5]  N. K. Wessells,et al.  Intra- and extracellular control of epithelial morphogenesis. , 1970, The ... Symposium. Society for Developmental Biology. Symposium.

[6]  R. Jaenisch,et al.  Normal epithelial branching morphogenesis in the absence of collagen I. , 1986, Developmental biology.

[7]  J. Woessner.  Mammalian collagenases. , 1973, Clinical orthopaedics and related research.

[8]  Y. Nakanishi,et al.  Mechanical aspects of the mesenchymal influence on epithelial branching morphogenesis of mouse salivary gland , 1987 .

[9]  G. Vaes,et al.  Purification of procollagenase and collagenase by affinity chromatography on sepharose—collagen , 1977, FEBS letters.

[10]  B. Spooner,et al.  Collagen involvement in branching morphogenesis of embryonic lung and salivary gland. , 1980, Developmental biology.

[11]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[12]  K. Lawson.  Mesenchyme specificity in rodent salivary gland development: the response of salivary epithelium to lung mesenchyme in vitro. , 1974, Journal of embryology and experimental morphology.

[13]  C. Grobstein,et al.  Collagenase: effect on the morphogenesis of embryonic salivary epithelium in vitro. , 1965, Science.

[14]  J. Kishi,et al.  Collagenase inhibitor stimulates cleft formation during early morphogenesis of mouse salivary gland. , 1986, Developmental biology.

[15]  H. Nogawa.  Determination of the curvature of epithelial cell mass by mesenchyme in branching morphogenesis of mouse salivary gland. , 1983, Journal of embryology and experimental morphology.

[16]  M. Coughlin,et al.  Early development of parasympathetic nerves in the mouse submandibular gland. , 1975, Developmental biology.

[17]  B. Steinberg,et al.  Establishment and transformation diminish the ability of fibroblasts to contract a native collagen gel , 1980, The Journal of cell biology.

[18]  S. Katsuda,et al.  An improved electron stain for elastic fibers using tannic acid. , 1975, Journal of electron microscopy.

[19]  N. K. Wessells,et al.  Effects of collagenase on developing epithelia in vitro: lung, ureteric bud, and pancreas. , 1968, Developmental biology.

[20]  D. Woolley,et al.  Small molecular weight β1 serum protein which specifically inhibits human collagenases , 1976, Nature.

[21]  K. Tryggvason,et al.  Biosynthesis of type IV procollagens. , 1980, Biochemistry.

[22]  Y Nakanishi,et al.  Cell proliferation is not required for the initiation of early cleft formation in mouse embryonic submandibular epithelium in vitro. , 1987, Development.

[23]  J. Kishi,et al.  Dental pulp collagenase: initial demonstration and characterization. , 1979, Biochemical and biophysical research communications.

[24]  H. Ehrlich,et al.  Studies on vascular smooth muscle cells and dermal fibroblasts in collagen matrices. Effects of heparin. , 1986, Experimental cell research.

[25]  A K Harris,et al.  Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations. , 1982, Developmental biology.

[26]  C. Little,et al.  Cellular events associated with lung branching morphogenesis including the deposition of collagen type IV. , 1987, Developmental biology.

[27]  Y. Nagai,et al.  A rapid assay method of collagenase activity using 14C-labeled soluble collagen as substrate. , 1976, Biochimica et biophysica acta.

[28]  N. K. Wessells.  Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. , 1970, The Journal of experimental zoology.

[29]  L. Liotta,et al.  Partial purification and characterization of a neutral protease which cleaves type IV collagen. , 1981, Biochemistry.

[30]  G. Murphy,et al.  [52] Mammalian collagenases , 1981 .

[31]  J. Bard.  The Role of Extracellular Matrix in Development , 1990 .