Variations in human liver fucosyltransferase activities in hepatobiliary diseases
Corresponding Author
Maryvonne Jezequel-Cuer
Laboratoire de Biochimie A, Hôpital Bichat, Paris and CNRS SDI 6210, Châtenay-Malabry
Laboratoire de Biochimie A, C.H.U. Bichat-Claude Bernard, 46 Rue Henri Huchard, 75877 Paris Cedex 18, FranceSearch for more papers by this authorJean-François Flejou
Laboratoire d'Anatomie et de Cytologie Pathologiques, Hôpital Beaujon, Clichy and INSERM U 239 Faculté de Médecine X. Bichat, Paris, France
Search for more papers by this authorGeneviève Durand
Laboratoire de Biochimie A, Hôpital Bichat, Paris and CNRS SDI 6210, Châtenay-Malabry
Search for more papers by this authorCorresponding Author
Maryvonne Jezequel-Cuer
Laboratoire de Biochimie A, Hôpital Bichat, Paris and CNRS SDI 6210, Châtenay-Malabry
Laboratoire de Biochimie A, C.H.U. Bichat-Claude Bernard, 46 Rue Henri Huchard, 75877 Paris Cedex 18, FranceSearch for more papers by this authorJean-François Flejou
Laboratoire d'Anatomie et de Cytologie Pathologiques, Hôpital Beaujon, Clichy and INSERM U 239 Faculté de Médecine X. Bichat, Paris, France
Search for more papers by this authorGeneviève Durand
Laboratoire de Biochimie A, Hôpital Bichat, Paris and CNRS SDI 6210, Châtenay-Malabry
Search for more papers by this authorAbstract
ABSTRACT— The hyperfucosylation of a number of glycoconjugates observed in liver diseases involves the action of several specific fucosyltransferases (F.T.) notably responsible for synthesizing histo-blood group antigens. We determined the activities of α3, α2 and α3/4 F.T. in 35 liver biopsy samples from patients with fatty liver, alcoholic or post-hepatic liver cirrhosis, primary or secondary biliary cirrhosis, acute hepatitis or a normal liver. F.T. activities were measured by transfer of GDP [14C] fucose to asialotransferrin for α3 F.T, to phenyl β-D-galactoside for α2 F.T. and to 2′ fucosyllactose for α3/4 F.T. The diseased liver extracts showed an early increase in non-Le gene-associated α3 F.T. activity (p = 0.001), which was related to the number of steatosic hepatocytes and the degree of intralobular inflammatory infiltration. Overexpression of this α3 F.T. provides an explanation for the strong expression of 3-fucosyl lactosamine structures described in several hepatobiliary diseases. α2 F.T. levels were significantly elevated in the two groups of liver cirrhosis and acute hepatitis (p = 0.05), but not enough to consider α2 F.T. as a sensitive feature of mesenchymal cell injury. All Lewis-positive biopsies displaying biliary alterations showed increased Le gene-encoded α3/4 F.T. activity (p = 0.001), which was related to the intensity of neoductular proliferation. Elevated levels of α3/4 F.T may be a very early sign of biliary regeneration.
References
- 1 Montreuil J. Primary structure of glycoprotein glycans. Basis for the molecular biology of glycoproteins. Adv Carbohydr Chem Biochem 1980: 37: 157–223.
- 2 Wierusezski Jm, Fournet B., Konan D., Biou D., Durand G. 400 MHz1H-NMR spectroscopy of fucosylated tetrasialyl oligosaccharides isolated from normal and cirrhotic alpha 1-acid glycoprotein. FEBS Lett 1988: 288: 390–394.
- 3 Yamamoto FI, Clausen H., White T., Marken J., Hakomori SI. Molecular genetic basis of the histo-blood group ABO system. Nature 1990: 345: 229–233.
- 4 Rouger PH, Poupon R., Gane P., Mallissen B., Darnis F., Salmon CH. Expression of blood group antigens including HLA markers in human adult liver. Tissue Antigens 1986: 27: 78–86.
- 5 Rhodes JM, Hubscher S., Black R., Elias E., Savage A. Lectin histochemistry of the liver in biliary disease, following transplantation and in cholangiocarcinoma. J Hepatol 1988: 6: 277–282.
- 6 Okada Y., Jinno K., Moriwaki S. et al. Blood group antigens in the intrahepatic biliary tree. I: Distribution in the normal liver. J Hepatol 1988: 6: 63–70.
- 7
Okada Y.,
Jinno K.,
Moriwakis et al.
Expression of ABH and Lewis blood group antigens in combined hepatocellular cholangiocarcinoma.
Cancer
1987: 60: 345–352.
10.1002/1097-0142(19870801)60:3<345::AID-CNCR2820600311>3.0.CO;2-T CAS PubMed Web of Science® Google Scholar
- 8 Oriol R. Genetic control of the fucosylation of ABH precursor chains. Evidence for new epistatic interactions in different cells and tissues. J Immunogenet 1990: 17: 235–245.
- 9 Watkins WM, Greenwell P., Yates AD, Johnson PH. Regulation of expression of carbohydrate blood group antigens. Biochimie 1988: 70: 1597–1611.
- 10 Biou D., Chanton P., Konan D., N'Guyen H., Feger J., Durand G. Microheterogeneity of the carbohydrate moiety of human alpha 1-acid glycoprotein in two benign liver diseases: alcoholic cirrhosis and acute hepatitis. Clin Chim Acta 1989: 186: 59–66.
- 11 Campion B., Leger D., Wieruszeski JM, Montreuil J., Spik G. Presence of fucosylated triantennary, tetraantennary and pentaantennary glycans in transferrin synthesized by the human hepatocarcinoma cell line Hep G2. Eur J Biochem 1989: 184: 405–413.
- 12 Yamashita K., Koide N., Endo T., Iwaki Y., Kobata A. Altered glycosylation of serum transferrin of patients with hepatocellular carcinoma. J Biol Chem 1989: 264: 2415–2423.
- 13 Okada Y., Shimoe T., Muguruma M. et al. Hepatocellular expression of a novel glycoprotein with sialylated difucosyl Lex activity in the active inflammatory lesions of chronic liver disease. Am J Pathol 1988: 130: 384–392.
- 14 Mollicone R., Bara J., Le Pendu J., Oriol R. Immunohistologic pattern of type 1 (Lea, Leb) and type 2 (X, Y, H) blood group-related antigens in the human pyloric and duodenal mucosae. Lab Invest 1985: 53: 219–227.
- 15 Finne J., Burger M., Prieels JP. Enzymatic basis for a lectin-resistant phenotype: increase in a fucosyltransferase in mouse melanoma cells. J Cell Biol 1982: 92: 277–282.
- 16 Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976: 72: 248–254.
- 17 Beyer TA, Rearick JI, Paulson JC, Prieels JP, Sadler JE, Hill RL. Biosynthesis of mammalian glycoproteins: glycosylation pathways in the synthesis of the non-reducing terminal sequences. J Biol Chem 1979: 254: 12531–12541.
- 18 White WJ, Schray KJ, Alhadeff JA. Studies on the catalytic residues at the active site of human liver a L fucosidase. Biochim Biophys Acta 1985: 829: 303–310.
- 19 Skacel P. O., Watkins WM Fucosyltransferase expression in human platelets and leucocytes. Glycoconj J 1987: 4: 267–272.
- 20 Johnson PH, Watkins WM. Separation of an α-3-L-fucosyltransferase from the blood-group-Le-gene-specified α-3/4-L fucosyltransferase in human milk. Biochem Soc Trans 1982: 10: 445–446.
- 21 Zar JH. Biostatistical analysis. Englewood NH: Prentice-Hall Inc, 1984: 122–149.
- 22 Dorland L., Haverkamp J., Schut BI et al. The structure of the asialocarbohydrate units of human serotransferrin as proven by 360 MHz proton magnetic resonance spectroscopy. FEBS Lett 1977: 77: 15–20.
- 23 Mollicone R., Gibaud A., François A., Ratcliffe M., Oriol R. Acceptor specificity and tissue distribution of three human α3-fucosyltransferases. Eur J Biochem 1990: 191: 169–176.
- 24 Johnson PH, Skacel O. P., Greenwell P., Watkins WM. Presence of human α3-L-fucosyltransferase in the white cells of an individual who lacks this enzyme in serum. Biochem Soc Trans 1988: 17: 133–134.
- 25 Le Pendu J., Cartron JP, Lemieux RU, Oriol R. The presence of at least two different H-blood-group related β-D-gal α2-L fucosyltransferases in human serum and the genetics of blood group H substances. Am J Hum Genet 1985: 37: 749–760.
- 26 Johnson PH, Watkins WM. Purification of α-3-L fucosyltransferase from human liver. In: Lis Sharon, Kahane Duksin, eds. Xth International Symposium on Glycoconjugates, Proceedings, Jerusalem 1989: 214–215.
- 27 Tamagawa H., Iwakura K., Amano A., Shizukuishi S., Tsunemitsu A. Substrate specificity of fucosyltransferase purified from human parotid saliva. J Dent Res 1987: 66: 756–760.
- 28 Kessel D., Sykes E., Henderson M. Glycosyltransferase levels in tumors metastatic to liver and in uninvolved liver tissue. J Natl Cancer Inst 1977: 59: 29–32.
- 29 Iizuka S., Yoshida A. Tissue-dependent expression of two α1–2 fucosyltransferases specified by the H and Se genes. Enzyme 1987: 37: 159–163.
- 30 Howie AJ, Brown G. Effect of neuraminidase on the expression of the 3-fucosyl-N-acetyllactosamine antigen in human tissues. J Clin Pathol 1985: 38: 409–416.
- 31 Hutchinson WL, Du MQ, Johnson PJ, Williams R. Fucosyltransferases: differential plasma and tissue alterations in hepatocellular carcinoma and cirrhosis. Hepatology 1991: 13: 683–688.
- 32 Chang S., Duerr B., Serif G. An epimerase-reductase in L-fucose synthesis. J Biol Chem 1988: 263: 1693–1697.
- 33 Mezey E. Alcoholic liver disease. In: H. Popper, F. Schaffner, eds. Progress in liver diseases, Vol VII. New York: Grune and Stratton, 1982: 555–557.
- 34 Woloski BMR, Fuller GM, Jamieson JC, Gospodarek E. Studies on the effect of the hepatocyte stimulating factor on galactose β1–4 N acetylglucosamine α2–6 sialyltransferase in cultured hepatocytes. Biochim Biophys Acta 1986: 885: 185–191.
- 35 Mackiewicz A., Kushner I. Interferon β2/B-cell stimulating factor 2/Interleukin 6 affects glycosylation of acute phase proteins in human hepatoma cell lines. Scand J Immunol 1989: 29: 265–271.
- 36 Rajan VP, Larsen RD, Ajmeva S., Ernst LK, Lowe JB. A cloned human DNA restriction fragment determines expression of a GDP-L-Fucose: β-D-galactoside 2-α-L-fucosyl-transferase in transfected cells. J Biol Chem 1989: 264: 11158–11167.
- 37 Uchida T., Peters RL. The nature and origin of proliferated bile ductules in alcoholic liver disease. Am J Clin Pathol 1983: 79: 326–333.
- 38 Nakanuma Y., Sasaki M. Expression of blood group related antigens in the intrahepatic biliary tree and hepatocytes in normal livers and various hepatobiliary diseases. Hepatology 1989: 10: 174–178.
- 39 Michalopoulos GK. Liver regeneration: molecular mechanisms of growth control. FASEB J 1990: 4: 176–187.
- 40 Kinoshita T., Tashiro K., Nakamura T. Marked increase of HGF mRNA in non parenchymal liver cells of rats treated with hepatotoxins. Biochem Biophys Res Commun 1989: 165: 1229–1234.
