Abstract
The cells responsible for the clearance of collagen were studied in cod. Cod collagen labelled with the lysosomal trap-label 125I-tyramine cellobiose was cleared from the circulation with a t1/2 of 15 min. 1 h After injection 75%, 17% and 8% of the label were recovered in the heart, liver and blood, respectively. 24 h After administration of collagen labelled conventionally with 125I to allow escape of labelled degradation product from the site of uptake, 80% of the label had left the heart, signifying degradation. When collagen was tagged with 125I-tyramine cellobiose, heart-associated radioactivity did not decrease after 24 h, indicating intralysosomal degradation. Fluorescence microscopy revealed that i.v. injected fluorescently-labelled collagen accumulated in discrete vesicles of cells lining the endocardial blood space of both atrium and ventricle. Conventional and immuno-electron microscopy showed that these cells contained numerous coated pits and vesicles reflecting active endocytosis, and that ligand lined the limiting membrane of early endosomes. Intravenously injected 2 μm latex accumulated mainly in kidney. We conclude that the population of non-macrophagic endocardial cells are important for the turnover of collagen in cod. These cells therefore resemble sinusoidal endothelial cells of salmon kidney and mammalian liver.
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Aschoff L (1924) Das Reticulo-Endotheliale System. Ergebnisse d inn Med 26:1–118
Dan C, Wake K (1985) Modes of endocytosis of latex particles in sinusoidal endothelial and Kupffer cells of normal and perfused rat liver. Exp Cell Res 158:75–78
Ferguson HW (1975) Phagocytosis by the endocardial lining cells of the atrium of plaice (Pleuronectes platessa). J Comp Pathol 85:561–569
Fraser JRE (1989) Hyaluronan: sources, turnover and metabolism. In: Lindh E, Thorell JI (eds) Clinical impact of bone and connective tissue markers. Academic Press, London, pp 31–49
Griffiths G, McDowall A, Back R, Dubochet J (1984) On the preparation of sections for immunocytochemistry. J Ultrastruct Res 89:65–78
Hellevik T, Bondevik A, Smedsrød B (1993) Intracellular trafficking of endocytosed collagen in rat liver endothelial cells. In: Wisse E, Knook DL (eds) Cells of the Hepatic Sinusoid, vol 4. Kupffer Cell Foundation, Leiden, pp 431–433
Laakso T, Smedsrød B (1987) Cellular distribution in rat liver of intravenously administered polyacryl starch and chondroitin sulfate microparticles. Int J Pharmacol 36:253–262
Leknes IL (1980) Ultrastructure of atrial endocardium and myocardium in three species of gadidae (Teleostei). Cell Tissue Res 248:1–10
Leknes IL (1981) Ultrahistochemical studies on the moderately electron dense bodies in teleostean endocardial cells. Histochemistry 72:211–214
Lewis MS, Piez KA (1964) Characterization of collagen of the skin of the dogfish shark, Squalus acanthias. J Biol Chem 239:3336–3340
Marzi I, Zhong Z, Lemasters JJ, Thurman RG (1989) Evidence that graft survival is not related to parenchymal cell viability in rat liver transplantation: the importance of nonparenchymal cells. Transplantation 48:463–468
McDowell EM, Trumph BF (1976) Histologic fixatives suitable for diagnostic light and electron microscopy. Arch Pathol Lab Med 100:405–414
Melkko J, Hellevik T, Risteli L, Risteli J, Smedsrød B (1994) Clearance of NH2-terminal propeptides of types I and III procollagen is a physiological function of the scavenger receptor in liver endothelial cells. J Exp Med 179:405–412
Nishida J, McDonnell D, Krasovich MA, Ekataksin W, McCuskey RS (1993) Effects of interleukin-1α on hepatic phagocytic cells and sinusoidal microcirculation. In: Knook DL, Wisse E (eds) Cells of the Hepatic Sinusoid, vol 4. Kupffer Cell Foundation, Leiden, pp 148–151
Pereira CA, Steffan A-M, Kirn A (1984) Kupffer and endothelial liver cell damage renders A/J mice susceptible to mouse hepatitis virus type 3. Virus Res 1:557–563
Pittman RC, Carew TE, Glass CK, Green SR, Taylor CA Jr, Attie AD (1983) A radioiodinated intracellularly trapped ligand for determining the sites of plasma protein degradation in vivo. Biochem J 212:791–800
Praaning-van Dalen DP, Brouwer A, Knook DL (1981) Clearance capacity of rat liver Kupffer, endothelial and parenchymal cells. Gastroenterology 81:1036–1044
Rabinovitch M (1968) Phagocytosis: The engulfment stage. Sem Hematol 5:134–155
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Scoazec J-Y, Feldman G (1990) Both macrophages and endothelial cells of the human hepatic sinusoid express the CD4 molecule, a receptor for the human immunodeficiency virus. Hepatology 12:505–510
Slot JW, Geuze (1985) A novel method to make gold probes for multiple labelling cytochemistry. Eur J Cell Biol 38:87–93
Smedsrød B (1988) Aminoterminal propeptide of type III procollagen is cleared from the circulation by receptor-mediated endocytosis in liver endothelial cells. Collagen Related Research 8:375–388
Smedsrød B, Johansson S, Pertoft H (1985) Studies in vivo and in vitro on the uptake and degradation of soluble alpha 1 (I) chains in rat liver endothelial and Kupffer cells. Biochem J 228:415–424
Smedsrød B, Malmgren M, Ericsson J, Laurent TC (1988) Morphological studies on endocytosis of chondroitin sulphate proteoglycan by rat liver endothelial cells. Cell Tissue Res 253:39–45
Smedsrød B, Pertoft H, Gustafson S, Laurent TC (1990) Scavenger functions of the liver endothelial cell. Biochem J 266:313–327
Smedsrød B, Gjøen T, Sveinbjørnsson B, Berg T (1993) Catabolism of circulating collagen in the Atlantic salmon (Salmo salar). J Fish Biol 42:279–291
Steffan AM, Gendrault JL, McCuskey RS, McCuskey PA, Kirn A (1986) Phagocytosis, an unrecognized property of murine liver endothelial cells. Hepatology 6:830–836
Steffan AM, Lafon M-E, Gendrault J-L, Schweitzer C, Royer C, Jaeck D, Arnaud J-P, Schmitt M-P, Aubertin A-M, Kirn A (1992) Primary cultures of endothelial cells from the human liver sinusoid are permissive for human immunodeficiency virus type 1. Proc Natl Acad Sci USA 89:1582–1586
Sætersdal TS, Justesen N-P, Kronstad AW (1974) Ultrastructure and innervation of the teleostean atrium. J Mol Cell Cardiol 6:415–437
Tokuyasu KT (1986) Application of cryoultramicrotomy to immunocytochemistry. J Micrsc 143:139–149
van Furth R, Cohn ZA, Hirsch IG, Spector WG, Langevoort HL (1972) The mononuclear phagocyte system: A new classification of macrophages, monocytes and their precursor cells. Bull WHO 46:845–852
Wisse E (1970) An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids. J Ultrastruct Res 31:125–150
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Smedsrød, B., Olsen, R. & Sveinbjørnsson, B. Circulating collagen is catabolized by endocytosis mainly by endothelial cells of endocardium in cod (Gadus morhua). Cell Tissue Res 280, 39–48 (1995). https://doi.org/10.1007/BF00304509
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DOI: https://doi.org/10.1007/BF00304509