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ARTICLE |

Hepatic Recognition and Catabolism of Serum Glycoproteins FREE

Gilbert Ashwell, MD; Clifford J. Steer, MD
[+] Author Affiliations

Reprint requests to National Institutes of Health, Department of Health and Human Services, Bldg 10, Room 9N-105, Bethesda, MD 20205 (Dr Ashwell).


JAMA. 1981;246(20):2358-2364. doi:10.1001/jama.1981.03320200044026
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Published online

WITH THE exception of albumin, essentially all serum proteins are glycoproteins, that is, proteins to which one or more carbohydrate chains are bound in covalent linkage. The sugars most commonly found in association with proteins are galactose, mannose, N-acetylhexosamine, sialic acid, and fucose. Glucose occurs rarely, if at all, as a normal constituent of circulating proteins.

In general, the carbohydrate moiety may be envisaged as consisting of two domains. The outer, nonreducing terminus is composed of the trisaccharide, sialic acid-galactose-N-acetylglucosamine. Usually, between two and four such terminal triads may be linked glycosidically to the second domain, which is composed of three mannose and two N-acetylglucosamine residues. The structure of a typical, complex carbohydrate chain is illustrated in the Figure. On treatment with neuraminidase, the sialic acid moiety is cleaved to reveal the penultimate galactose moiety as the new, nonreducing termini of the resulting asialoglycoprotein. Fucose, which

REFERENCES

Sharon N, Lis H:  Glycoproteins: Research booming on long-ignored, ubiquitous compounds . Chem Eng News 1981;;59:21-44.
Morell AG, van den Hamer CJA, Scheinberg IH, et al:  Physical and chemical studies on ceruloplasmin: IV. Preparation of radioactive, sialic acid-free ceruloplasmin labeled with tritium on terminal D-galactose residues . J Biol Chem 1966;;241:3745-3749.
Morell AG, Irvine RA, Sternlieb I, et al:  Physical and chemical studies on ceruloplasmin: V. Metabolic studies on sialic acid-free ceruloplasmin in vivo . J Biol Chem 1968;;243:155-159.
Hickman J, Ashwell G, Morell AG, et al:  Physical and chemical studies on ceruloplasmin: VIII. Preparation of N-acetylneuraminic acid -1-14C-labeled ceruloplasmin . J Biol Chem 1970;; 245:759-766.
Van den Hamer CJA, Morell AG, Scheinberg IH, et al:  Physical and chemical studies on ceruloplasmin: XI. The role of galactosyl residues in the clearance of ceruloplasmin from the circulation . J Biol Chem 1970;;245:4397-4402.
Morell AG, Gregoriadis G, Scheinberg IH, et al:  The role of sialic acid in determining the survival of glycoproteins in the circulation . J Biol Chem 1971;;246:1461-1467.
Pricer WE Jr, Ashwell G:  The binding of desialylated glycoproteins by plasma membranes of rat liver . J Biol Chem 1971;;246:4825-4833.
Van Lenten L, Ashwell G:  The binding of desialylated glycoproteins by plasma membranes of rat liver: Development of a quantitative inhibition assay . J Biol Chem 1972;;247:4633-4640.
Ashwell G, Morell AG:  The role of surface carbohydrates in the hepatic recognition and transport of circulating glycoproteins . Adv Enzymol 1974;;41:99-128.
Hudgin RL, Pricer WE Jr, Ashwell G, et al:  The isolation and properties of a rabbit liver binding protein specific for asialoglycoproteins . J Biol Chem 1974;;249:5536-5543.
Kawasaki T, Ashwell G:  Chemical and physical properties of an hepatic membrane protein that specifically binds asialoglycoproteins . J Biol Chem 1976;;251:1296-1302.
Andersen TT, Freytag JW:  Physical characteristics of the rabbit liver galactoside binding protein , abstracted. Fed Proc 1980;;39:1923.
Tanabe T, Pricer WE Jr, Ashwell G:  Subcellular membrane topology and turnover of a rat hepatic binding protein specific for asialoglycoproteins . J Biol Chem 1979;;254:1038-1043.
Sawamura T, Nakada H, Fujii-Kuriyama Y, et al:  Some properties of a binding protein specific for asialoglycoproteins and its distribution in rat liver microsomes . Cell Struc Func 1980;;5:133-146.
Baenziger JU, Maynard Y:  Human hepatic lectin: Physiochemical properties and specificity . J Biol Chem 1980;;255:4607-4613.
Neufeld EF, Ashwell G:  Carbohydrate recognition systems for receptor-mediated pinocytosis , in Lennarz WJ (ed): The Biochemistry of Glycoproteins and Proteoglycans . New York, Plenum Publishing Corp, 1980;, pp 241-266.
Hubbard AL, Wilson G, Ashwell G, et al:  An electron microscope autoradiographic study of the carbohydrate recognition system in rat liver: I. Distribution of 125I-ligands among the liver cell types . J Cell Biol 1979;;83:47-64.
Wall DA, Wilson G, Hubbard AL:  The galactose-specific recognition system of mammalian liver: The route of ligand internalization in rat hepatocytes . Cell 1980;;21:79-93.
Stockert RJ, Haimes HB, Morell AG, et al:  Endocytosis of asialoglycoprotein-enzyme conjugates by hepatocytes . Lab Invest 1980;;43:556-563.
Regoeczi E, Taylor P, Hatton MWC, et al:  Distinction between binding and endocytosis of human asialo-transferrin by the rat liver . Biochem J 1978;;174:171-178.
Hatton MWC, Marz L, Berry LR, et al:  Biand tri-antennary human transferrin glycopeptides and their affinities for the hepatic lectin specific for asialoglycoproteins . Biochem J 1979;; 181:633-638.
Regoeczi E, Chindemi PA, Hatton MWC, et al:  Galactose-specific elimination of human asialotransferrin by the bone marrow in the rabbit . Arch Biochem Biophys 1980;;205:76-84.
Dunn WA, Hubbard AL, Aronson NN Jr:  Low temperature selectively inhibits fusion between pinocytic vesicles and lysosomes during heterophagy of 125I-asialogetuin by the perfused rat liver . J Biol Chem 1980;;255:5971-5978.
Weigel PH, Oka JA:  Temperature dependence of endocytosis mediated by the asialoglycoprotein receptor in isolated hepatocytes: Evidence for two potentially rate-limiting steps . J Biol Chem 1981;;256:2615-2617.
Dunn WA, LaBadie JH, Aronson NN Jr:  Inhibition of 125I-asialofetuin catabolism by leupeptin in the perfused rat liver and in vivo . J Biol Chem 1979;;254:4191-4196.
Kolset SO, Tolleshaug H, Berg T:  The effects of colchicine and cytochalasin B on uptake and degradation of asialoglycoproteins in isolated rat hepatocytes . Exp Cell Res 1979;; 122:159-167.
Tolleshaug H, Abdelnour M, Berg T:  Binding of concanavalin A to isolated hepatocytes and its effect on uptake and degradation of asialofetuin by the cells . Biochem J 1980;:190:697-703.
Tolleshaug H:  Binding and internalization of asialoglycoproteins by isolated rat hepatocytes . Int J Biochem 1981;;13:45-51.
Steer CJ, Ashwell G:  Studies on a mammalian hepatic binding protein specific for asialoglycoproteins: Evidence for receptor recycling in isolated rat hepatocytes . J Biol Chem 1980;; 255:3008-3013.
Pricer WE Jr, Ashwell G:  Subcellular distribution of a mammalian hepatic binding protein specific for asialoglycoproteins . J Biol Chem 1976;;251:7539-7544.
Weigel PH:  Characterization of the asialoglycoprotein receptor on isolated rat hepatocytes . J Biol Chem 1980;;255:6111-6120.
Harford J, Ashwell G:  Immunologic evidence for the transmembrane nature of the rat liver receptor for asialoglycoproteins . Proc Natl Acad Sci USA 1981;;78:1557-1561.
Nakada H, Sawamura T, Tashiro Y:  Biosynthesis and insertion of a hepatic binding protein specific for asialoglycoproteins into endoplasmic reticulum membranes . J Biochem 1981;;89:135-141.
Stockhert RJ, Gärtner U, Morell AG, et al:  Effects of receptor specific antibody on the uptake of desialylated glycoproteins in the isolated perfused rat liver . J Biol Chem 1980;; 255:3830-3831.
Stockert RJ, Howard DJ, Morell AG, et al:  Functional segregation of hepatic receptors for asialoglycoproteins during endocytosis . J Biol Chem 1980;;255:9028-9029.
Marshall JS, Green AM, Pensky J, et al:  Measurement of circulating desialylated glycoproteins and correlation with hepatocellular damage . J Clin Invest 1974;;54:555-562.
Lunney J: Studies on the Regulation of Serum Glycoprotein Homeostasis, thesis. The Johns Hopkins University, Baltimore, 1976.
Marshall JS, Williams S:  Serum inhibitors of desialylated glycoprotein binding to hepatocyte membranes . Biochim Biophys Acta 1978;; 543:41-52.
Arima T, Motoyama Y, Yamamoto T, et al:  Serum glycoproteins in the liver diseases: V. Desialylated glycoproteins in chronic hepatitis . Gastroenterol Jpn 1978;;13:503-506.
Arima T:  Serum glycoproteins in the liver diseases: VIII. Desialylated glycoproteins in the liver cirrhosis . Gastroenterol Jpn 1979;;14:349-352.
Sobue G, Kosaka A:  Asialoglycoproteinemia in a case of primary hepatic cancer . Hepato-Gastroenterol 1980;;27:200-203.
Gärtner U, Stockert RJ, Morell AG, et al:  Modulation of the transport of bilirubin and asialo-orosomucoid during liver regeneration . Hepatology 1981;;1:99-106.
Hickman J, Ashwell G:  Studies on the hepatic binding of asialoglycoproteins in hepatoma tissue and by isolated hepatocytes , in Tager JM, Hooghwinkel HJM, Daems WTH (eds): Enzyme Therapy in Lysosomal Storage Disease . Amsterdam, North-Holland Publishing Co, 1974;, pp 169-172.
Stockert RJ, Becker FF:  Diminished hepatic binding protein for desialylated glycoproteins during chemical hepatocarcinogenesis . Cancer Res 1980;;40:3632-3634.
Furbish FS, Steer CJ, Krett NL, et al:  Uptake and distribution of placental glucocerebrosidase in rat hepatic cells and effects of sequential deglycosylation . Biochim Biophys Acta 1981;;673:425-434.
Fiume L, Mattioli A, Balboni PG, et al:  Enhanced inhibition of virus DNA synthesis in hepatocytes by trifluorothymidine coupled to asialo fetuin . FEBS Lett 1979;;103:47-51.
Fiume L, Mattioli A, Busi C, et al:  Selective inhibition of ectromelia virus DNA synthesis in hepatocytes by adenine-9-β-D-arabinofuranoside (ara-A) and adenine-9-β-D-arabinofuranoside 5′-monophosphate (ara-AMP) conjugated to asialofetuin . FEBS Lett 1980;;116:185-188.
Hickman J, Bose S:  Role of the carbohydrate moiety in determining the survival of interferon in the circulation . J Biol Chem 1977;; 252:8336-8337.
Cawley DB, Simpson DL, Herschman HR:  Asialoglycoprotein receptor mediates the toxic effects of an asialofetuin-diphtheria toxin fragment A conjugate on cultured rat hepatocytes . Proc Natl Acad Sci USA 1981;;78:3383-3387.
Attie AD, Pitman RC, Steinberg D:  Metabolism of native and of lactosylated low-density lipoprotein: Evidence for two pathways for catabolism of exogenous proteins in rat hepatocytes . Proc Natl Acad Sci USA 1980;;77:5923-5927.
Stockert RJ, Morell AG, Scheinberg IH:  Mammalian hepatic lectin . Science 1974;;186:365-366.
Novogrodsky A, Ashwell G:  Lymphocyte mitogenesis induced by a mammalian liver protein that specifically binds desialylated glycoproteins . Proc Natl Acad Sci USA 1977;;77:676-678.
Woodruff JJ, Gesner BM:  The effect of neuraminidase on the fate of transfused lymphocytes . J Exp Med 1969;;129:551-567.
Kolb H, Kolb-Bachofen V, Schlepper-Schafer J:  Cell contacts mediated by D-galactose-specific lectins on liver cells . Biol Cellulaire 1979;;36:301-308.
Kolb H, Vogt D, Herbertz L, et al:  The galactose-specific lectins on rat hepatocytes and kupffer cells have identical binding characteristics . Hoppe Seylers Z Physiol Chem 1980;; 361:1747-1750.
Steer CJ, James SP, Vierling JM, et al:  The selective hepatic uptake of desialylated peripheral blood mononuclear cells in rabbits . Gastroenterology 1980;;79:917-923.
Vierling JM, Steer CJ, Hickman JW, et al:  Cell-mediated cytotoxicity of desialylated human lymphocytes induced by a mitogenic mammalian liver protein . Gastroenterology 1978;; 75:456-461.
Kolb-Bachofen V, Kolb H:  Autoimmune reactions against liver cells by syngeneic neuraminidase-treated lymphocytes . J Immunol 1979;;123:2830-2834.
Krohn KA, Vera DR, Stadalnick RC:  A Complementary radiopharmaceutical and mathematical model for quantitating hepatic binding protein receptors , in Colobetti LG (exec ed): Radiotracers in Biology and Medicine (Receptor Binding Radiotracers , vol 10), Eckelman WC (section ed), to be published.
Neufeld EF, Cantz MJ:  Corrective factors for inborn errors of mucopolysaccharide metabolism . Ann NY Acad Sci 1971;;179:580-587.

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Sharon N, Lis H:  Glycoproteins: Research booming on long-ignored, ubiquitous compounds . Chem Eng News 1981;;59:21-44.
Morell AG, van den Hamer CJA, Scheinberg IH, et al:  Physical and chemical studies on ceruloplasmin: IV. Preparation of radioactive, sialic acid-free ceruloplasmin labeled with tritium on terminal D-galactose residues . J Biol Chem 1966;;241:3745-3749.
Morell AG, Irvine RA, Sternlieb I, et al:  Physical and chemical studies on ceruloplasmin: V. Metabolic studies on sialic acid-free ceruloplasmin in vivo . J Biol Chem 1968;;243:155-159.
Hickman J, Ashwell G, Morell AG, et al:  Physical and chemical studies on ceruloplasmin: VIII. Preparation of N-acetylneuraminic acid -1-14C-labeled ceruloplasmin . J Biol Chem 1970;; 245:759-766.
Van den Hamer CJA, Morell AG, Scheinberg IH, et al:  Physical and chemical studies on ceruloplasmin: XI. The role of galactosyl residues in the clearance of ceruloplasmin from the circulation . J Biol Chem 1970;;245:4397-4402.
Morell AG, Gregoriadis G, Scheinberg IH, et al:  The role of sialic acid in determining the survival of glycoproteins in the circulation . J Biol Chem 1971;;246:1461-1467.
Pricer WE Jr, Ashwell G:  The binding of desialylated glycoproteins by plasma membranes of rat liver . J Biol Chem 1971;;246:4825-4833.
Van Lenten L, Ashwell G:  The binding of desialylated glycoproteins by plasma membranes of rat liver: Development of a quantitative inhibition assay . J Biol Chem 1972;;247:4633-4640.
Ashwell G, Morell AG:  The role of surface carbohydrates in the hepatic recognition and transport of circulating glycoproteins . Adv Enzymol 1974;;41:99-128.
Hudgin RL, Pricer WE Jr, Ashwell G, et al:  The isolation and properties of a rabbit liver binding protein specific for asialoglycoproteins . J Biol Chem 1974;;249:5536-5543.
Kawasaki T, Ashwell G:  Chemical and physical properties of an hepatic membrane protein that specifically binds asialoglycoproteins . J Biol Chem 1976;;251:1296-1302.
Andersen TT, Freytag JW:  Physical characteristics of the rabbit liver galactoside binding protein , abstracted. Fed Proc 1980;;39:1923.
Tanabe T, Pricer WE Jr, Ashwell G:  Subcellular membrane topology and turnover of a rat hepatic binding protein specific for asialoglycoproteins . J Biol Chem 1979;;254:1038-1043.
Sawamura T, Nakada H, Fujii-Kuriyama Y, et al:  Some properties of a binding protein specific for asialoglycoproteins and its distribution in rat liver microsomes . Cell Struc Func 1980;;5:133-146.
Baenziger JU, Maynard Y:  Human hepatic lectin: Physiochemical properties and specificity . J Biol Chem 1980;;255:4607-4613.
Neufeld EF, Ashwell G:  Carbohydrate recognition systems for receptor-mediated pinocytosis , in Lennarz WJ (ed): The Biochemistry of Glycoproteins and Proteoglycans . New York, Plenum Publishing Corp, 1980;, pp 241-266.
Hubbard AL, Wilson G, Ashwell G, et al:  An electron microscope autoradiographic study of the carbohydrate recognition system in rat liver: I. Distribution of 125I-ligands among the liver cell types . J Cell Biol 1979;;83:47-64.
Wall DA, Wilson G, Hubbard AL:  The galactose-specific recognition system of mammalian liver: The route of ligand internalization in rat hepatocytes . Cell 1980;;21:79-93.
Stockert RJ, Haimes HB, Morell AG, et al:  Endocytosis of asialoglycoprotein-enzyme conjugates by hepatocytes . Lab Invest 1980;;43:556-563.
Regoeczi E, Taylor P, Hatton MWC, et al:  Distinction between binding and endocytosis of human asialo-transferrin by the rat liver . Biochem J 1978;;174:171-178.
Hatton MWC, Marz L, Berry LR, et al:  Biand tri-antennary human transferrin glycopeptides and their affinities for the hepatic lectin specific for asialoglycoproteins . Biochem J 1979;; 181:633-638.
Regoeczi E, Chindemi PA, Hatton MWC, et al:  Galactose-specific elimination of human asialotransferrin by the bone marrow in the rabbit . Arch Biochem Biophys 1980;;205:76-84.
Dunn WA, Hubbard AL, Aronson NN Jr:  Low temperature selectively inhibits fusion between pinocytic vesicles and lysosomes during heterophagy of 125I-asialogetuin by the perfused rat liver . J Biol Chem 1980;;255:5971-5978.
Weigel PH, Oka JA:  Temperature dependence of endocytosis mediated by the asialoglycoprotein receptor in isolated hepatocytes: Evidence for two potentially rate-limiting steps . J Biol Chem 1981;;256:2615-2617.
Dunn WA, LaBadie JH, Aronson NN Jr:  Inhibition of 125I-asialofetuin catabolism by leupeptin in the perfused rat liver and in vivo . J Biol Chem 1979;;254:4191-4196.
Kolset SO, Tolleshaug H, Berg T:  The effects of colchicine and cytochalasin B on uptake and degradation of asialoglycoproteins in isolated rat hepatocytes . Exp Cell Res 1979;; 122:159-167.
Tolleshaug H, Abdelnour M, Berg T:  Binding of concanavalin A to isolated hepatocytes and its effect on uptake and degradation of asialofetuin by the cells . Biochem J 1980;:190:697-703.
Tolleshaug H:  Binding and internalization of asialoglycoproteins by isolated rat hepatocytes . Int J Biochem 1981;;13:45-51.
Steer CJ, Ashwell G:  Studies on a mammalian hepatic binding protein specific for asialoglycoproteins: Evidence for receptor recycling in isolated rat hepatocytes . J Biol Chem 1980;; 255:3008-3013.
Pricer WE Jr, Ashwell G:  Subcellular distribution of a mammalian hepatic binding protein specific for asialoglycoproteins . J Biol Chem 1976;;251:7539-7544.
Weigel PH:  Characterization of the asialoglycoprotein receptor on isolated rat hepatocytes . J Biol Chem 1980;;255:6111-6120.
Harford J, Ashwell G:  Immunologic evidence for the transmembrane nature of the rat liver receptor for asialoglycoproteins . Proc Natl Acad Sci USA 1981;;78:1557-1561.
Nakada H, Sawamura T, Tashiro Y:  Biosynthesis and insertion of a hepatic binding protein specific for asialoglycoproteins into endoplasmic reticulum membranes . J Biochem 1981;;89:135-141.
Stockhert RJ, Gärtner U, Morell AG, et al:  Effects of receptor specific antibody on the uptake of desialylated glycoproteins in the isolated perfused rat liver . J Biol Chem 1980;; 255:3830-3831.
Stockert RJ, Howard DJ, Morell AG, et al:  Functional segregation of hepatic receptors for asialoglycoproteins during endocytosis . J Biol Chem 1980;;255:9028-9029.
Marshall JS, Green AM, Pensky J, et al:  Measurement of circulating desialylated glycoproteins and correlation with hepatocellular damage . J Clin Invest 1974;;54:555-562.
Lunney J: Studies on the Regulation of Serum Glycoprotein Homeostasis, thesis. The Johns Hopkins University, Baltimore, 1976.
Marshall JS, Williams S:  Serum inhibitors of desialylated glycoprotein binding to hepatocyte membranes . Biochim Biophys Acta 1978;; 543:41-52.
Arima T, Motoyama Y, Yamamoto T, et al:  Serum glycoproteins in the liver diseases: V. Desialylated glycoproteins in chronic hepatitis . Gastroenterol Jpn 1978;;13:503-506.
Arima T:  Serum glycoproteins in the liver diseases: VIII. Desialylated glycoproteins in the liver cirrhosis . Gastroenterol Jpn 1979;;14:349-352.
Sobue G, Kosaka A:  Asialoglycoproteinemia in a case of primary hepatic cancer . Hepato-Gastroenterol 1980;;27:200-203.
Gärtner U, Stockert RJ, Morell AG, et al:  Modulation of the transport of bilirubin and asialo-orosomucoid during liver regeneration . Hepatology 1981;;1:99-106.
Hickman J, Ashwell G:  Studies on the hepatic binding of asialoglycoproteins in hepatoma tissue and by isolated hepatocytes , in Tager JM, Hooghwinkel HJM, Daems WTH (eds): Enzyme Therapy in Lysosomal Storage Disease . Amsterdam, North-Holland Publishing Co, 1974;, pp 169-172.
Stockert RJ, Becker FF:  Diminished hepatic binding protein for desialylated glycoproteins during chemical hepatocarcinogenesis . Cancer Res 1980;;40:3632-3634.
Furbish FS, Steer CJ, Krett NL, et al:  Uptake and distribution of placental glucocerebrosidase in rat hepatic cells and effects of sequential deglycosylation . Biochim Biophys Acta 1981;;673:425-434.
Fiume L, Mattioli A, Balboni PG, et al:  Enhanced inhibition of virus DNA synthesis in hepatocytes by trifluorothymidine coupled to asialo fetuin . FEBS Lett 1979;;103:47-51.
Fiume L, Mattioli A, Busi C, et al:  Selective inhibition of ectromelia virus DNA synthesis in hepatocytes by adenine-9-β-D-arabinofuranoside (ara-A) and adenine-9-β-D-arabinofuranoside 5′-monophosphate (ara-AMP) conjugated to asialofetuin . FEBS Lett 1980;;116:185-188.
Hickman J, Bose S:  Role of the carbohydrate moiety in determining the survival of interferon in the circulation . J Biol Chem 1977;; 252:8336-8337.
Cawley DB, Simpson DL, Herschman HR:  Asialoglycoprotein receptor mediates the toxic effects of an asialofetuin-diphtheria toxin fragment A conjugate on cultured rat hepatocytes . Proc Natl Acad Sci USA 1981;;78:3383-3387.
Attie AD, Pitman RC, Steinberg D:  Metabolism of native and of lactosylated low-density lipoprotein: Evidence for two pathways for catabolism of exogenous proteins in rat hepatocytes . Proc Natl Acad Sci USA 1980;;77:5923-5927.
Stockert RJ, Morell AG, Scheinberg IH:  Mammalian hepatic lectin . Science 1974;;186:365-366.
Novogrodsky A, Ashwell G:  Lymphocyte mitogenesis induced by a mammalian liver protein that specifically binds desialylated glycoproteins . Proc Natl Acad Sci USA 1977;;77:676-678.
Woodruff JJ, Gesner BM:  The effect of neuraminidase on the fate of transfused lymphocytes . J Exp Med 1969;;129:551-567.
Kolb H, Kolb-Bachofen V, Schlepper-Schafer J:  Cell contacts mediated by D-galactose-specific lectins on liver cells . Biol Cellulaire 1979;;36:301-308.
Kolb H, Vogt D, Herbertz L, et al:  The galactose-specific lectins on rat hepatocytes and kupffer cells have identical binding characteristics . Hoppe Seylers Z Physiol Chem 1980;; 361:1747-1750.
Steer CJ, James SP, Vierling JM, et al:  The selective hepatic uptake of desialylated peripheral blood mononuclear cells in rabbits . Gastroenterology 1980;;79:917-923.
Vierling JM, Steer CJ, Hickman JW, et al:  Cell-mediated cytotoxicity of desialylated human lymphocytes induced by a mitogenic mammalian liver protein . Gastroenterology 1978;; 75:456-461.
Kolb-Bachofen V, Kolb H:  Autoimmune reactions against liver cells by syngeneic neuraminidase-treated lymphocytes . J Immunol 1979;;123:2830-2834.
Krohn KA, Vera DR, Stadalnick RC:  A Complementary radiopharmaceutical and mathematical model for quantitating hepatic binding protein receptors , in Colobetti LG (exec ed): Radiotracers in Biology and Medicine (Receptor Binding Radiotracers , vol 10), Eckelman WC (section ed), to be published.
Neufeld EF, Cantz MJ:  Corrective factors for inborn errors of mucopolysaccharide metabolism . Ann NY Acad Sci 1971;;179:580-587.
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