Summary
The distribution of various extracellular matrix components was studied in frozen sections of embryonic (14–18 days) and early postnatal (birth and 4 days post parturn) dorsal mouse skin using monospecific antibodies and indirect immunofluorescence. Basement membrane zone components — type IV collagen, laminin and heparan sulphate proteoglycan — were found to be uniformly and unchangingly distributed along the dermal-epidermal junction. In contrast, the distribution of interstitial matrix components — types I and III collagen, and fibronectin — was heterogeneous and varied with the stages of hair development. Collagens became sparse and were eventually completely removed from the prospective dermal papilla and from a one-cell-thick sheath of dermal cells around hair buds. They remained absent from the dermal papilla throughout hair organogenesis. Fibronectin was always present around dermal papilla cells and was particularly abundant along the dermal-epidermal junction of hair rudiments, as well as underneath hair buds. In contrast, in interfollicular skin, collagens accumulated in increasing density, while fibronectin became progressively sparser. It thus appears that interstitial collagens and fibronectin are distributed in a manner which is related to hair morphogenesis. In morphogenetically active regions, collagen density is low, while that of fibronectin is high. Conversely, in histologically stabilized zones, collagen is abundant and fibronectin is sparse. This microheterogeneous distribution of interstitial collagens and of fibronectin might thus constitute part of the morphogenetic message that the dermis is known to transmit to the epidermis during the development of skin and of cutaneous appendages.
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References
Armstrong PB (1985) Cell recognition, the extracellular matrix, and heart morphogenesis. In: Haemmerli G, Sträuli P (eds) Motility of vertebrate cells in culture and in the organism. Molecular mechanisms and morphological manifestations. Karger, Basel, pp 222–230
Bard S, Micouin C, Thivolet J, Sengel P (1981) Heterogeneous distribution of bullous pemphigoid antigen during hair development in the mouse. Arch Anat Microsc Morphol Exp 70:141–148
Bernfield MR (1981) Organization and remodeling of the extracellular matrix in morphogenesis. In: Connelly TG, Brinkley LL, Carlson BM (eds) Morphogenesis and pattern formation. Raven Press, New York, pp 139–162
Bernfield MR, Wessells NK (1970) Intra- and extra-cellular control of epithelial morphogenesis. Dev Biol [Suppl] 4:195–249
Boucaut JC, Darribère T, Boulekbache H, Thiéry JP (1984) Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. Nature 307:364–367
Clark RAF, Lanigan JM, Dellapelle P, Manseau E, Dvorak HF, Colvin RB (1982) Fibronectin and fibrin provide a provisional matrix for epidermal cell migration during wound healing. J Invest Dermatol 70:264–269
Cohen J (1969) Dermis, epidermis and dermal papillae interacting. In: Montagna W, Dobson RL (eds) Advances in Biology of skin, vol XI, Hair growth. Pergamon Press, Oxford and NewYork, pp 1–18
Corthier G, Boschetti E, Charley-Poulain J (1984) Improved method for IgG purification from various animal species by ion exchange chromatography. J Immunol Meth 66:75–79
Couchman JR, Blencowe S (1985) Adhesion and cell surface relationships during fibroblast and epithelial migration in vitro. In: Haemmerli G, Sträuli P (eds) Motility of vertebrate cells in culture and in the organism. Molecular mechanisms and morphological manifestations. S. Karger, Basel, pp 22–38
Critchley DR, England MA, Wakely J, Hynes RO (1979) Distribution of fibronectin in the ectoderm of gastrulating chick embryos. Nature 280:498–500
David G, Bernfield MR (1979) Collagen reduces glycosaminoglycan degradation by cultured mammary epithelial cells: Possible mechanism for basal lamina formation. Proc Natl Acad Sci USA 76:786–790
Davis EM, Trinkaus JP (1981) Significance of cell-to-cell contacts for the directional movement of neural crest cells within a hydrated collagen lattice. J Embryol Exp Morphol 63:29–51
Donaldson DJ, Mahan JT (1983) Fibrinogen and fibronectin as substrates for epidermal cell migration during wound closure. J Cell Sci 62:117–127
Engvall E, Ruoslahti E (1977) Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int J Cancer 20:1–5
Foidart JM, Reddi AH (1980) Immunofluorescent localization of type IV collagen and laminin during endochondral bone differentiation and regulation by pituitary growth hormone. Dev Biol 75:130–136
Foidart JM, Berman JJ, Paglia L, Rennard S, Abe S, Perantoni A, Martin GR (1980) Synthesis of fibronectin, laminin, and several collagens by a liver-derived epithelial line. Lab Invest 42:525–532
Foidart JB, Foidart JM, Hassell J, Mahieu P (1983) Localization by immunofluorescent microscopy of several collagen types and of a basement membrane proteoglycan in rat glomerular epithelial and mesangial cell cultures. Renal Physiol 6:163–170
Gibson WT, Couchman JR, Weaver AC (1983) Fibronectin distribution during the development of fetal rat skin. J Invest Dermatol 81:480–485
Grobstein C (1967) Mechanisms of organogenetic tissue interactions. Natl Cancer Inst Monogr 26:279–299
Grobstein C, Cohen J (1965) Collagenase: effect on the morphogenesis of embryonic salivary epithelium in vitro. Science 150:626–628
Hardy MH (1969) The differentiation of hair follicles and hairs in organ culture. In: Montagna W, Dobson RL (eds) Advances in biology of skin, vol IX. Pergamon Press, Oxford, New York, pp 35–60
Hardy MH, Van Exan RJ, Sonstegard KS, Sweeny PR (1983) Basal lamina changes during tissue interactions in hair follicles — An in vitro study of normal dermal papillae and vitamin A-induced glandular morphogenesis. J Invest Dermatol 80:27–34
Hassell JR, Robey PG, Barrach HJ, Wilczek J, Rennard SI, Martin GR (1980) Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci USA 77:4494–4498
Kratochwil K, Dziadek M, Löhler J, Harbers K, Jaenisch R (1986) Normal epithelial branching morphogenesis in the absence of collagen I. Dev Biol 117:596–606
Leung Tack J, Thivolet J, Beyvin AJ, Schmitt D (1971) Corrélations immunologiques et ultrastructurales au cours de l'ontogenèse de la membrane basale dermo-épidermique chez la souris. Ann Dermatol Syphiligr 98:525–528
Linask KK, Lash JW (1986) Precardiac cell migration: fibronectin localization at mesoderm-endoderm interface during directional movement. Dev Biol 114:87–101
Mauger A, Démarchez M, Herbage D, Grimaud JA, Druguet M, Hartmann D, Sengel P (1982) Immunofluorescent localization of collagen types I and III, and of fibronectin during feather morphogenesis in the chick embryo. Dev Biol 94:93–105
Mauger A, Démarchez M, Herbage D, Grimaud JA, Druguet M, Hartmann DJ, Foidart JM, Sengel P (1983) Immunofluorescent localization of collagen types I, III, IV, fibronectin and laminin during the morphogenesis of scales and scaleless skin in the chick embryo. Wilhelm Roux's Arch 192:205–215
Mayer BW, Hay ED, Hynes RO (1981) Immunocytochemical localization of fibronectin in embryonic trunk and area vasculosa. Dev Biol 82:267–286
Miller EJ, Rhodes RK (1982) Preparation and characterization of the different types of collagen. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 82. Academic Press, New York, pp 33–64
Newgreen DF (1985) Control of the timing of commencement of migration of embryonic neural crest cells. In: Haemmerli G, Sträuli P (eds) Motility of vertebrate cells in culture and in the organism. Molecular mechanisms and morphological manifestations. Karger, Basel, pp 209–221
Newgreen D, Thiéry JP (1980) Fibronectin in early avian embryos: synthesis and distribution along migration pathways of neural crest cells. Cell Tissue Res 221:269–291
Nishida T, Nakagawa S, Awata T, Ohashi Y, Watanabe K, Manabe R (1983) Fibronectin promotes epithelial migration of cultured rabbit cornea in situ. J Cell Biol 97:1653–1657
O'Keefe EJ, Rayne RE, Russell N, Woodley DT (1985) Spreading and enhanced motility of human keratinocytes on fibronectin. J Invest Dermatol 85:125–130
Rovasio RA, Delouvée A, Yamada KM, Timpl R, Thiéry JP (1983) Neural crest cell migration: requirement for exogenous fibronectin and high cell density. J Cell Biol 96:462–473
Sengel P (1976) Morphogenesis of skin. In: Abercrombie M, Newth DR, Torrey JG (eds) Developmental and cell biology series. Cambridge University Press, Cambridge, London, New York, Melbourne, pp 1–277
Sengel P, Kieny M (1984) Influence of collagen and fibronectin substrates on the behaviour of cultured embryonic dermal cells. Br J Dermatol [Suppl 111] 27:88–97
Sengel P, Dhouailly D, Mauger A (1980) Region-specific determination of epidermal differentiation in amniotes. In: Spearman RIC, Riley PA (eds) Skin of vertebrates. Linnean Society Symposium Series Number 9. Academic Press, London, pp 185–200
Sengel P, Mauger A, Robert J, Kieny M (1985) Extracellular matrix in skin morphogenesis. In: Edelman GM (ed) Molecular determinants of animal form. AR Liss, New York, p 319–347
Slavkin HC, Greulich RC (1975) Extracellular matrix influences on gene expression. Academic Press, New York
Spooner BS, Faubion JM (1980) Collagen involvement in branching morphogenesis of embryonic lung and salivary gland. Dev Biol 77:84–102
Takashima A, Grinnell F (1985) Fibronectin-mediated keratinocyte migration and initiation of fibronectin receptor function in vitro. J Invest Dermatol 85:304–308
Thiéry JP (1984) Mechanisms of cell migration in the vertebrate embryo. Cell Differ 15:1–15
Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM, Martin OR (1979a) Laminin — a glycoprotein from basement membranes. J Biol Chem 254:9933–9937
Timpl R, Glanville RW, Wick G, Martin GR (1979b) Immunochemical study on basement membrane (type IV) collagens. Immunology 38:109–116
Timpl R, Martin GR, Bruckner P, Wick G, Weidemann H (1978) Nature of the collagenous protein in a tumor basement membrane. Eur J Biochem 84:43–52
Trelstad RL (1982) Methods of collagen fractionation. In: Furthmayr H (ed) Immunochemistry of the extracellular matrix. CRC Press Inc, Boca Raton, pp 31–41
Turner DC, Lawton J, Dollenmeier P, Ehrismann R, Chiquet M (1983) Guidance of myogenic cell migration by oriented deposits of fibronectin. Dev Biol 95:497–504
Wessells NK (1970) Mammalian lung development and interactions in formation and morphogenesis of tracheal buds. J Exp Zool 175:455–466
Westgate GE, Shaw DA, Harrap GJ, Couchman JR (1984) Immunohistochemical localization of basement membrane components during hair follicle morphogenesis. J Invest Dermatol 82:259–264
Yaoita H, Foidart JM, Katz SI (1978) Localization of the collagenous component in skin basement membrane. J Invest Dermatol 70:191–193
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Mauger, A., Emonard, H., Hartmann, D.J. et al. Immunofluorescent localization of collagen types I, III and IV, fibronectin, laminin, and basement membrane proteoglycan in developing mouse skin. Roux's Arch Dev Biol 196, 295–302 (1987). https://doi.org/10.1007/BF00395953
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DOI: https://doi.org/10.1007/BF00395953