Abstract
The distribution of the extracellular matrix proteins types III pN-collagen and IV collagen, laminin and tenascin was investigated in fetal, infant, and adult human spleens by using immuno-electron microscopy. The presence of type III pN-collagen was assessed by using an antibody against the aminoterminal propeptide of type III procollagen. All the proteins other than type III pN-collagen were found in reticular fibers throughout development. In the white pulp of the fetus aged 16 gestational weeks, only an occasional type III pN-collagen-containing fibril was present, although type III pN-collagen was abundant in the reticular fibers of the red pulp. Conversely, in adults, most of the reticular fibers of the white pulp, but not of the red pulp, were immunoreactive for type III pN-collagen. Ring fibers, the basement membranes of venous sinuses, were well developed in both infant and adult spleens. The first signs of their formation could be seen as a discontinuous basement membrane, which was immunoreactive for type IV collagen, laminin, and tenascin in the fetus aged 20 gestational weeks. Intracytoplasmic immunoreactivity for all the proteins studied was visible in the mesenchymal cells of the fetus aged 16 gestational weeks and in the reticular cells of the older fetuses, which also showed labeling for type IV collagen and laminin in the endothelial cells. The results suggest that proteins of the extracellular matrix are produced by these stationary cells.
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Apaja-Sarkkinen M, Alavaikko M, Karttunen T, Autio-Harmainen H (1986) Basement membrane proteins in the spleen: immunohistochemical demonstration and relation to reticulin. Histopathology 10:295–302
Aufderheide E, Chiquet-Ehrismann R, Ekblom P (1987) Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme. J Cell Biol 105: 599–608
Barzanji AJ, Emery JL (1978) Germinal centres in the spleens of neonates and stillbirths. Early Hum Dev 1:363–369
Berg TK van den, Ende M van der, Döpp EA, Kraal G, Dijkstra CD (1993) Localization of β1 integrins and their extracellular ligands in human lymphoid tissue. Am J Pathol 143:1098–1110
Burgeson R, Nimni M (1992) Collagen types. Clin Orthop 282:250–272
Burridge K, Fath K (1989) Focal contacts: transmembrane links between the extracellular matrix and the cytoskeleton. Bioessays 10:104–108
Chiquet M (1992) Tenascin: an extracellular matrix protein involved in morphogenesis of epithelial organs. Kidney Int 41: 629–631
Chiquet-Ehrismann R, Mackie E, Pearson C, Sakakura T (1986) Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47:131–139
Dingemans KP, Bergh Weerman MA van den (1990) Rapid contrasting of extracellular elements in thin sections. Ultrastruct Pathol 14:519–527
Drenckhahn D, Wagner J (1986) Stress fibers in the splenic sinus endothelium in situ: Molecular structure, relationship to the extracellular matrix, and contractility. J Cell Biol 102:1738–1747
Dziadek M, Timpl R (1985) Expression of nidogen and laminin in basement membranes during mouse embryogenesis and in teratocarcinoma cells. Dev Biol 111:372–382
Ekblom P (1989) Developmentally regulated conversion of mesenchyme to epithelium. FASEB J 3:2141–2150
End P, Panayotou G, Entwistle A, Waterfield MD, Chiquet M (1982) Tenascin: a modulator of cell growth. Eur J Biochem 209:1041–1051
Fleischmajer R (1986) Collagen fibrillogenesis: a mechanism of structural biology. J Invest Dermatol 87:553–554
Fleischmajer R, Perlish JS, Burgeson RE, Shaikh-Bahai F, Timpl R (1990) Type I and type III collagen interactions during fibrillogenesis. Ann NY Acad Sci 580:161–175
Griffiths G, McDowell A, Back R, Dubochet J (1984) On the preparation of cryosections for immunocytochemistry. J Ultrastruct Res 89:65–78
Hynes R (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11–25
Jaakkola S, Savunen O, Halme T, Uitto J, Peltonen J (1993) Basement membranes during development of human nerve: Schwann cells and perineurial cells display marked changes in their expression profiles for laminin subunits and β1 and β4 integrins. J Neurocytol 22:215–230
Karttunen T, Sormunen R, Risteli L, Risteli J, Autio-Harmainen H (1989) Immunoelectron microscopic localization of laminin, type IV collagen, and type III pN-collagen in reticular fibers of human lymph nodes. J Histochem Cytochem 37:279–286
Klein G, Langegger M, Timpl R, Ekblom P (1988) Role of laminin A chain in the development of epithelial cell polarity. Cell 55:331–341
Kubota S, Tashiro K, Yamada Y (1992) Signaling site of laminin with mitogenic activity. J Biol Chem 267:4285–4288
Leivo I, Vaheri A, Timpl R, Wartiovaara J (1980) Appearance and distribution of collagens and laminin in the early mouse embryo. Dev Biol 76:100–114
Liakka A, Autio-Harmainen H (1992) Distribution of the extracellular matrix proteins tenascin, fibronectin, and vitronectin in fetal, infant, and adult human spleens. J Histochem Cytochem 40:1203–1210
Liakka A, Apaja-Sarkkinen M, Karttunen T, Autio-Harmainen H (1991) Distribution of laminin and types IV and III collagen in fetal, infant and adult human spleens. Cell Tissue Res 263: 245–252
Mark K von der, Mark H von der, Goodman S (1992) Cellular responses to extracellular matrix. Kidney Int 41:632–640
Niemelä O, Risteli L, Parkkinen J, Risteli J (1985) Purification and characterization of the N-terminal propeptide of human type III pro-collagen. Biochem J 232:146–150
Olsen D, Nagayoshi T, Fazio M, Peltonen J, Jaakkola S, Sanborn D, Sasaki T, Kuivaniemi H, Chu M-L, Deutzmann R, Timpl R, Uitto J (1989) Human laminin: cloning and sequence analysis of cDNAs encoding A, B1 and B2 chains, and expression of the corresponding genes in human skin and cultured cells. Lab Invest 60:772–782
Ono K (1930) Untersuchungen über die Entwicklung der menschlichen Milz. Z Zellforsch Mikrosk Anat 10:573–603
Panayotou G, End P, Aumailley M, Timpl R, Engel J (1989) Growth factor like domains in laminin. Cell 56:93–101
Risteli L, Timpl R (1981) Isolation and characterization of pepsin fragments of laminin from human placental and renal basement membranes. Biochem J 193:749–755
Risteli J, Bächinger HP, Engel J, Furthmayr H, Timpl R (1980) 7-S collagen: characterization of unusual basement membrane structure. Eur J Biochem 108:239–250
Romanic AM, Adachi E, Kadler KE, Hojima Y, Prockop DJ (1991) Copolymerization of pNcollagen III and collagen I. J Biol Chem 266:12703–12709
Saito H, Yokoi Y, Watanabe S, Tajima J, Kuroda H, Namihisa T (1988) Reticular meshwork of the spleen in rats studied by electron microscopy. Am J Anat 181:235–252
Simo P, Simon-Assmann P, Bouziges F, Leberquier C, Kedinger M, Ekblom P, Sorokin L (1991) Changes in the expression of laminin during intestinal development. Development 112:477–487
Slot JW, Geuze HJ (1985) A new method of preparing gold probes for multiple-labeling cytochemistry. Eur J Cell Biol 38:87–93
Sormunen R, Eskelinen S, Lehto V-P (1993) Bile canaliculus formation in cultured HEPG2 cells. Lab Invest 68:652–662
Tiitta O, Wahlström T, Paavonen J, Linnala A, Sharma S, Gould VE, Virtanen J (1992) Enhanced tenascin expression in cervical and vulvar koilocytic lesions. Am J Pathol 141:907–913
Timens W (1991) The human spleen and the immune system: not just another lymphoid organ. Res Immunol 142:316–320
Vellguth S, Gaudecker B von, Müller-Hermelink H-K (1985) The development of the human spleen. Ultrastructural studies in fetuses from the 14th to 24th week of gestation. Cell Tissue Res 242:579–592
Weber M (1992) Basement membrane proteins. Kidney Int 41:620–628
Young SL, Chang L-Y, Erickson HP (1994) Tenascin-C in rat lung: distribution, ontogeny and role in branching morphogenesis. Dev Biol 161:615–625
Yurchenco PD, Ruben GC (1987) Basement membrane structure in situ: evidence for lateral associations in the type IV collagen network. J Cell Biol 105:2559–2568
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Liakka, A., Karjalainen, H., Virtanen, I. et al. Immuno-electron-microscopic localization of types III pN-collagen and IV collagen, laminin and tenascin in developing and adult human spleen. Cell Tissue Res 282, 117–127 (1995). https://doi.org/10.1007/BF00319138
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DOI: https://doi.org/10.1007/BF00319138