Summary
The expression and distribution of several major extracellular matrix macromolecules were investigated at the epithelial-mesenchymal interface of the human fetal small intestine from 8 to 20 weeks of gestation. Localization of heparan sulfate proteoglycan, type-IV collagen and laminin, three basement membrane components, as well as fibronectin and tenascin, were assessed by indirect immunofluorescence staining on cryostat sections, and correlated to morphogenesis and epithelial cell differentiation. Basement membrane components and fibronectin were all detected as early as 8 weeks (a time when the epithelium is still stratified and does not express sucrase-isomaltase). Tenascin appeared only after short villi had developed (around 10 weeks) and was restricted to the connective tissue at the tip of villus rudiments. At 18 weeks, well-formed villi and crypts were apparent. The antibody against heparan sulfate proteoglycan stained exclusively the epithelial basement membrane. Anti-type-IV collagen and anti-laminin anti-bodies stained the epithelial basement membrane and also cellular and fibrillar structures in the lamina propria. Fibronectin was found uniformly distributed over the lamina propria except in the upper third position of the villus core. On the contrary tenascin was mainly localized in the stroma at the tip of the villi. Staining for tenascin was also detected at the epithelial-mesenchymal interface of the villus and in the mesenchyme immediately surrounding budding crypts. These results provide basic data concerning the development of the human gut, and suggest that extracellular matrix components could be involved in the remodelling process of the intestinal mucosa.
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References
Abrahamson DR, Caulfield JP (1985) Distribution of laminin within rat and mouse renal, splenic, intestinal, and hepatic basement membranes identified after the intravenous injection of heterologous antilaminin IgG. Lab Invest 52:169–181
Arsenault P, Ménard D (1985) Influence of hydrocortisone on human fetal small intestine in organ culture. J Pediatr Gastroenterol Nutr 4:893–901
Aufderheide E, Ekblom P (1988) Tenascin during gut development: appearance in the mesenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions. J Cell Biol 107:2341–2349
Beaulieu J-F, Calvert R (1981) The effect of epidermal growth factor (EGF) on the differentiation of the rough endoplasmic reticulum in fetal mouse small intestine in organ culture. J Histochem Cytochem 29:765–770
Beaulieu J-F, Calvert R (1984) Effect of dexamethasone on the fetal mouse small intestine in organ culture. Anat Rec 210:61–71
Beaulieu J-F, Calvert R (1987) Hormonal regulation of epithelial cell proliferation in the fetal mouse duodenum in vitro. Anat Rec 217:250–255
Beaulieu J-F, Ménard D, Calvert R (1985) Influence of epidermal growth factor on the maturation of the fetal mouse duodenum in organ culture. J Pediatr Gastroenterol Nutr 4:476–481
Beaulieu J-F, Nichols B, Quaroni A (1989) Post-translational regulation of sucrase-isomaltase expression in intestinal crypt and villus cells. J Biol Chem 264:20000–20011
Beaulieu J-F, Weiser MM, Herrera L, Quaroni A (1990) Detection and characterization of sucrase-isomaltase in adult human colon and in colonie polyps. Gastroenterology 98:1467–1477
Bernfield M, Banerjee SD, Koda JE, Rapraeger A (1984) Remodeling of the basement membrane: morphogenesis and maturation. Ciba Found Symp 108:179–196
Bissell MJ, Barcellos-Hoff MH (1987) The influence of extracellular matrix on gene expression: is structure the message? J Cell Sci 58:327–343
Burtin P, Chavanel G, Foidart JM, Martin E (1982) Antigens of the basement membrane and the peritumoral stroma in human colonie adenocarcinoma: an immunofluorescence study. Int J Cancer 30:13–20
Bustamante S, Koldovsky O (1981) Synopsis of development of the main morphological structures of the human gastrointestinal tract. In: Lebenthal E (ed) Textbook of gastroenterology and nutrition in infancy. Raven Press, New York, pp 49–55
Chiquet-Ehrismann R, Macki EJ, Pearson CA, Sakakura T (1986) Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47:131–139
Chiquet-Ehrismann R, Kalla P, Pearson CA, Beck K, Chiquet M (1988) Tenascin interferes with fibronectin action. Cell 53:383–390
Colony PC (1983) Successive phases of human fetal intestinal development. In: Kretchmer N, Minkows A (eds) Nutritional adaptation of the gastrointestinal tract. Nestlé, Vevey/Raven Press, New York, pp 3–28
Daneker GW, Mercurio AM, Guerra L, Wolf B, Salem RP, Bagli DJ, Steele GD (1987) Laminin expression in colorectal carcinomas varying in degree of differentiation. Arch Surg 122:1470–1474
Engvall E, Davis GE, Dickerson K, Ruoslahti E, Varon S, Manthorpe M (1986) Mapping of domains in human laminin using monoclonal antibodies: localization of the neurite-promoting site. J Cell Biol 103:2457–2465
Gallagher JT, Lyon M, Steward WP (1986) Structure and function of heparan sulfate proteoglycans. Biochem J 236:313–325
Grand RJ, Watkins JB, Torti FM (1976) Development of the human gastrointestinal tract. Gastroenterology 70:790–810
Haffen K, Kedinger M, Simon-Assmann P (1987) Mesenchymedependent differentiation of epithelial progenitor cells in the gut. J Pediatr Gastroenterol Nutr 6:14–23
Hahn U (1988) Extracellular matrix proteins in small intestinal cell cultures. Scand J Gastroenterol 23:[Suppl 151] 70–78
Havenith MG, Arends JW, Simon R, Volovics A, Wiggers T, Bosman FT (1988) Type-IV collagen immunoreactivity in colorectal cancer. Prognostic value of basement membrane deposition. Cancer 62:2207–2211
Hay ED (1981) Extracellular matrix. J Cell Biol 91:205–223
Iozzo RV (1984) Proteoglycans and neoplastic-mesenchymal cell interactions. Human Pathol 15:2–10
Iozzo RV (1984) Biosynthesis of heparan sulfate proteoglycan by human colon carcinoma cells and its localization at the cell surface. J Cell Biol 99:403–417
Kedinger M, Simon-Assmann P, Bouziges F, Haffen K (1988) Epithelial-mesenchymal interactions in intestinal epithelial differentiation. Scand J Gastroenterol 23: [Suppl 151] 62–69
Kemeny E, Fillit HM, Damle S, Mahabir R, Kefalides NA, Gregory JD, Antonovych T, Sabnis S, Zabriskie JB (1988) Monoclonal antibodies to heparan sulfate proteoglycan: development and application to the study of normal tissue and pathologic human kidney biopsies. Connect Tissue Res 18:9–25
Lacroix B, Kedinger M, Simon-Assmann P, Haffen K (1984) Effects of human fetal gastroenteric mesenchymal cells on some developmental aspects of animal gut endoderm. Differentiation 28:129–135
Lebenthal E, Lee PC (1983) Interactions of determinants in the ontogeny of the gastrointestinal tract: a unified concept. Pediatr Res 17:19–24
Leblond CP, Inoue S (1989) Structure, composition and assembly of basement membrane. Am J Anat 185:367–390
Levy P, Picard J, Bruel A (1981) Sulfatation of heparan sulfate in isolated rat intestinal epithelial cells. FEBS Lett 131:257–261
Ménard D (1989) Growth-promoting factors and the development of the human gut. In: Lebenthal E (ed) Human gastrointestinal development. Raven Press, New York, pp 123–149
Ménard D, Arsenault P, Pothier P (1988) Biologic effects of epidermal growth factor in human fetal jejunum. Gastroenterology 94:656–663
Quaroni A, Isselbacher K, Ruoslahti E (1978) Fibronectin synthesis by epithelial cells of rat small intestine. Proc Natl Acad Sci USA 75:5548–5552
Rodriguez-Boulan E, Nelson WJ (1989) Morphogenesis of the polarized epithelial phenotype. Science 245:718–725
Sanders EJ (1987) The roles of epithelial-mesenchymal cell interactions in developmental processes. Biochem Cell Biol 66:530–540
Schoen RC, Bentley KL, Klebe RJ (1982) Monoclonal antibody against human fibronectin which inhibits cell attachment. Hybridoma 1:99–108
Sebastio G, Hunziker W, O'Neill B, Malo C, Ménard D, Auricchio S, Semenza G (1987) The biosynthesis of intestinal sucraseisomaltase in human embryo is most likely controlled at the level of transcription. Biochem Biophys Res Commun 149:830–839
Semenza G, Sebastio G, Hunziker W, Malo C, Ménard D, Auricchio S (1988) Biosynthesis of human small intestinal sucraseisomaltase. In: Lentze MJ, Sterchi EE (eds) Brush border membranes. Thieme, Stuttgart New York, pp 43–51
Senior PV, Crithley Dr, Beck F, Walker RA, Varley JM (1988) The localization of laminin mRNA and protein in the postimplantation embryo and placenta of the mouse: an in situ hybridization and immunocytochemical study. Development 104:431–446
Simon-Assmann PM, Kedinger M, Grenier JF, Haffen K (1982) Control of brush border enzymes by dexamethasone in the fetal rat intestine cultured in vitro. J Pediatr Gastroenterol Nutr 1:257–265
Simon-Assmann P, Lacroix B, Kedinger M, Haffen K (1986) Maturation of brush border hydrolases in human fetal intestine maintained in organ culture. Early Hum Dev 13:65–74
Simon-Assmann P, Kedinger M, Haffen K (1986) Immunocytochemical localization of extracellular-matrix proteins in relation to rat intestinal morphogenesis. Differentiation 32:59–66
Simon-Assmann P, Bouziges F, Arnold C, Haffen K, Kedinger M (1988) Epithelial-mesenchymal interactions in the production of basement membrane components in the gut. Development 102:339–347
Simon-Assmann P, Bouziges F, Vigny M, Kedinger M (1989) Origin and deposition of basement membrane heparan sulfate proteoglycan in the developing intestine. J Cell Biol 109:1837–1848
Timpl R, Dziadek M (1986) Structure, development, and molecular pathology of basement membranes. Int Rev Exp Pathol 29:1–112
Weiser MM, Ryzowics S, Soroka Cj, Albini B (1989) Synthesis of intestinal basement membrane. Immunol Invest 18:417–430
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Beaulieu, JF., Vachon, P.H. & Chartrand, S. Immunolocalization of extracellular matrix components during organogenesis in the human small intestine. Anat Embryol 183, 363–369 (1991). https://doi.org/10.1007/BF00196837
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DOI: https://doi.org/10.1007/BF00196837