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Relationship between tenascin and α-smooth muscle actin expression in the developing human small intestinal mucosa

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Abstract

The expression of tenascin (Tn) and α-smooth muscle actin (α-SMA) was analyzed in the developing and adult human small intestine by means of double immunofluorescent staining with specific antibodies. By 7 weeks of gestation, the gut anlage has a simple tubular shape and is formed of a stratified undifferentiated epithelium surrounded by a poorly organized mesenchyme. Both Tn and α-SMA were found exclusively at the periphery of the tissue, corresponding to the presumptive muscularis propria. By 9 weeks, villus rudiments had formed but Tn and α-SMA remained restricted to the muscularis propria. Tn was first detected in the mesenchyme at 11 weeks. By 13 weeks, a preferential distribution of Tn in the subepithelial region of the mesenchyme was readily observed while α-SMA was still absent. From this stage to 20 weeks, Tn gradually concentrated in this region that, as determined by α-SMA detection, corresponded to the future muscularis mucosa area. As shown by double staining of Tn and α-SMA, deposition of Tn also preceded the appearance of the other α-SMA-expressing cells in the mucosa. These observations suggest that Tn could have a role in the differentiation of intestinal contractile cells.

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References

  • Akiyama SK, Nagata K, Yamada KM (1990) Cell surface receptors for extracellular matrix components. Biochim Biophys Acta 1031:91–110

    Google Scholar 

  • Arey LB (1965) Developmental anatomy. A textbook and laboratory manual of embryology. Saunders, Philadelphia

    Google Scholar 

  • 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

    Google Scholar 

  • Beaulieu J-F (1992) Differential expression of the VLA family of integrins along the crypt-villus axis in the human small intestine. J Cell Sci 102:427–436

    Google Scholar 

  • Beaulieu J-F, Nichols B, Quaroni A (1989) Posttranslational regulation of sucrase-isomaltase expression in intestinal crypt and villus cells. J Biol Chem 264:20000–20011

    Google Scholar 

  • Beaulieu J-F, Vachon PH, Chartrand S (1991) Immunolocalization of extracellular matrix components during organogenesis in the human small intestine. Anat Embryol 183:363–369

    Google Scholar 

  • Beaulieu J-F, Millane G, Calvert R (1992) Developmental expression of two antigens associated with mouse intestinal crypts. Dev Dynamics 193:325–331

    Google Scholar 

  • Beaulieu J-F, Jutras S, Kusakabe M, Perreault N (1993) Expression of tenascin in the developing human small intestine. Biochim Biophys Res Commun 192:1086–1092

    Google Scholar 

  • Bissell MJ, Barcellos-Hoff MH (1987) The influence of extracellular matrix on gene expression: is structure the message? J Cell Sci 58 [Suppl 8]:327–343

    Google Scholar 

  • Bustamante S, Koldovsky O (1981) Synopsis of development of the main morphological structures of the human gastrointestinal tract. In: Lebenthal E (ed) Textbook in gastroenterology and nutrition in infancy. Raven Press, New York pp 49–55

    Google Scholar 

  • Chiquet M (1992) Tenascin — an extracellular matrix protein involved in morphogenesis of epithelial organs. Kidney Int 41:629–631

    Google Scholar 

  • Chiquet M, Fambrough DM (1984) Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol 98:1926–1936

    Google Scholar 

  • Chiquet-Ehrismann R (1991) Anti-adhesive molecules of the extracellular matrix. Curr Opin Cell Biol 3:800–804

    Google Scholar 

  • Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T (1986) Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47:131–139

    Google Scholar 

  • Chiquet-Ehrismann R, Matsuoka Y, Hofer U, Spring J, Bernasconi C, Chiquet M (1991) Tenascin variants: differential binding to fibronectin and distinct distribution in cell culture and tissues. Cell Regul 2:927–938

    Google Scholar 

  • Colony PC (1983) Successive phases of human fetal intestinal development. In: Kretchmer N, Minkows A (eds) Nutritional adaptation of the gastrointestinal tract. Raven Press, New York Vevey, pp 3–28

    Google Scholar 

  • Colony Moxey P, Trier JS (1978) Specialized cell types in the human fetal small intestine. Anat Rec 191:269–286

    Google Scholar 

  • Crossin KL, Hoffman S, Grumet M, Thiery JP, Edelman GM (1986) Site-restricted expression of cytotactin during development of the chicken embryo. J Cell Biol 102:1917–1930

    Google Scholar 

  • Edelman GM (1992) Morphoregulation. Dev Dynamics 193:2–10

    Google Scholar 

  • Edelman GM, Jones FS (1992) Cytotactin: a morphoregulatory molecule and a target for regulation by homeobox gene products. Trends Biochem. Sci. 17:228–232

    Google Scholar 

  • Erickson HP, Bourdon MA (1989) Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors. Annu Rev Cell Biol 5:71–92

    Google Scholar 

  • Gabella G (1987) Structure of muscles and nerves in the gastrointestinal tract. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven Press, New York, pp 335–381

    Google Scholar 

  • Grand R, Watkins JB, Torti FM (1976) Development of the human gastrointestinal tract. Gastroenterology 70:790–810

    Google Scholar 

  • Gröschel-Stewart U, Rakousky C, Franke R, Peleg I, Kahane I, Eldor A, Muhlrad A (1985) Immunohistochemical studies with antibodies to myosins from the cytoplasm and plasma membrane fraction of human blood platelets. Cell Tissue Res 241:399–404

    Google Scholar 

  • Gulcher JR, Nies DE, Marton LS, Stefansson K (1989) An alternatively spliced region of the human hexabranchion contains a repeat of potential N-glycosylation sites. Proc Natl Acad Sci USA 86:1588–1592

    Google Scholar 

  • Hartman AL, Sawtell NM, Lessard JL (1989) Expression of actin isoforms in developing rat intestinal epithelium. J Histochem Cytochem 37:1225–1233

    Google Scholar 

  • Hay ED (1981) Extracellular matrix. J Cell Biol 91:205–223

    Google Scholar 

  • Hemler ME (1990) VLA proteins in the integrin family: structures, functions, and their role on leucocytes. Annu Rev Immunol 8:365–400

    Google Scholar 

  • Joyce NC, Haire MF, Palade GE (1987) Morphologic and biochemical evidence for a contractile cell network within the rat intestinal mucosa. Gastroenterology 92:68–81

    Google Scholar 

  • Jutras S, Beaulieu J-F (1992) Expression of tenascin in the developing human small intestine. Gastroenterology 102:A559

    Google Scholar 

  • Kedinger M, Simon-Assmann P, Bouziges F, Arnold C, Alexander E, Haffen K (1990) Smooth muscle actin expression during rat gut development and induction in fetal skin fibroblastic cells associated with intestinal embryonic epithelium. Differentiation 43:87–97

    Google Scholar 

  • Mackie EJ, Thesleff I, Chiquet-Ehrismann R (1987) Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105:2569–2579

    Google Scholar 

  • Matsuoka Y, Spring J, Ballmer-Hofer K, Hofer U, Chiquet-Ehrismann R (1990) Differential expression of tenascin splicing variants in the chick gizzard and in cell culture. Cell Differ Dev 32:417–424

    Google Scholar 

  • McDonald JA (1989) Matrix regulation of cell shape and gene expression. Curr Opin Cell Biol 1:995–999

    Google Scholar 

  • McHugh KM, Lessard JL (1988) The developmental expression of the rat α-vascular and γ-enteric smooth muscle isoactins: isolation and characterization of a rat γ-enteric actin cDNA. Mol Cell Biol 8:5224–5231

    Google Scholar 

  • Ménard D (1989) Growth promoting factors and the development of the human gut. In: Lebenthal E (ed) Human intestinal development. Raven Press, New York, pp 123–150

    Google Scholar 

  • Ménard D, Calvert R (1991) Fetal and postnatal development of the small and large intestine: patterns and regulation. In: Morisset J, Solomon TE (eds) Growth of the gastrointestinal tract: gastrointestinal hormones and growth factors. CRC Press, Boca Raton, pp 159–174

    Google Scholar 

  • Natali PG, Zardi L (1989) Tenascin: a hexameric adhesive glycoprotein. Int J Cancer S4:66–68

    Google Scholar 

  • Natali PG, Nicotra MR, Bigotti A, Castellani P, Risso AM, Zardi L (1991) Comparative analysis of the expression of the extracellular matrix protein tenascin in normal human fetal, adult and tumor tissues. Int J Cancer 47:811–816

    Google Scholar 

  • Oike Y, Hiraiwa H, Kawakatsu H, Nishikai M, Okinaka T, Suzuki T, Okada A, Yatani R, Sakakura T (1990) Isolation and characterization of human fibroblast tenascin. An extracellular matrix glycoprotein of interest for developmental studies. Int J Dev Biol 34:309–317

    Google Scholar 

  • Patten BM (1946) Human embryology. Blakiston, Philadelphia

    Google Scholar 

  • Probstmeier R, Martini R, Tacke R, Schachner M (1990a) Expression of the adhesion molecules L1, N-CAM and J1/tenascin during development of the murine small intestine. Differentiation 44:42–55

    Google Scholar 

  • Probstmeier R, Martini R, Schachner M (1990b) Expression of J1/tenascin in the crypt-villus unit of adult mouse small intestine: implication for its role in epithelial cell shedding. Development 109:313–321

    Google Scholar 

  • Rong PM, Ziller C, Pena-Melian A, LeDouarin NM (1987) A monoclonal antibody specific for avian early myogenic cells and differentiated muscle. Dev Biol 122:338–353

    Google Scholar 

  • Ruoslahti E (1991) Integrins. J Clin Invest 87:1–5

    Google Scholar 

  • Sage EH, Bornstein P (1991) Extracellular proteins that modulate cell-matrix interactions. SPARC, tenascin and thrombospondin. J Biol Chem 266:14831–14834

    Google Scholar 

  • Sakakura T, Kusano I (1991) Tenascin in tissue perturbation repair. Acta Pathol Jpn 41:247–258

    Google Scholar 

  • Sapino AP, Dietrich PY, Skalli O, Widgren S, Gabbiani G (1989) Colonic pericryptal fibroblasts. Differentiation pattern in embryogenesis and phenotypic modulation in epithelial proliferative lesions. Virchows Arch [A] 415:551–557

    Google Scholar 

  • Simon-Assmann P, Kedinger M, Haffen K (1986) Immunocytochemical localization of extracellular-matrix proteins in relation to rat intestinal morphogenesis. Differentiation 32:59–66

    Google Scholar 

  • Siri A, Carnemolla B, Saginati M, Leprini A, Casari G, Baralle F, Zardi L (1991) Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucleic Acid Res 19:525–531

    Google Scholar 

  • Skalli O, Vandekerckhove J, Gabbiani G (1987) Actin-isoform pattern as a marker of normal or pathological smooth-muscle and fibroblastic tissues. Differentiation 33:232–238

    Google Scholar 

  • Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G (1986) A monoclonal antibody against α-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol 103:2787–2796

    Google Scholar 

  • Spring J, Beck K, Chiquet-Ehrismann R (1989) Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell 58:325–334

    Google Scholar 

  • Thomas JO, Kornberg RD (1975) An octamer of histone in chromatin and free in solution. Proc Natl Acad Sci USA 72:2626–2630

    Google Scholar 

  • Timpl R (1989) Structure and biological activity of basement membrane proteins. Eur J Biochem 180:487–502

    Google Scholar 

  • Timpl R, Dziadek M (1986) Structure, development, and molecular pathology of basement membranes. Int Rev Exp Pathol 29:1–112

    Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets. Procedures and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Google Scholar 

  • Vachon PH, Durand J, Beaulieu J-F (1993) Basement membrane formation and redistribution of the β1 integrins in a human intestinal co-culture system. Anat Rec 236:567–576

    Google Scholar 

  • Yurchenco PD, Schittny JC (1990) Molecular architecture of basement membranes. FASEB J 4:1577–1590

    Google Scholar 

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Beaulieu, JF., Jutras, S., Durand, J. et al. Relationship between tenascin and α-smooth muscle actin expression in the developing human small intestinal mucosa. Anat Embryol 188, 149–158 (1993). https://doi.org/10.1007/BF00186248

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