Abstract
The glycosylation of the acute phase glycoprotein alpha 1-acid glycoprotein (AGP) in human sera is subject to marked changes during acute inflammation as a result of the cytokine-induced hepatic acute phase reaction. The changes described thus far comprise alterations in the type of branching of the carbohydrate structures as revealed by increased reactivity of AGP with concanavalin A. We now report on acute inflammation-induced increases in alpha 1-->3-fucosylated AGP molecules, as detected by the reactivity of AGP towards the fucose- binding Aleuria aurantia lectin (AAL) in crossed affino- immunoelectrophoresis of human sera. Laparotomy of women, for the removal of benign tumors of the uterus, was used as a model for the development of the hepatic acute phase response. Hugh increases were detected in the amounts of strongly AAL-reactive fractions of AGP, presumably containing three or more fucosylated N-acetyllactosamine units. At least part of these Lewis X-type glycans (Gal beta 1-->[Fuc alpha 1-->3]GlcNAc-R) appeared to be substituted also with an alpha 2-- >3-linked sialic acid residue. This was revealed by the laparotomy- induced abundant staining of AGP with an antisialyl Lewis X monoclonal antibody (CSLEX-1) on blots of sodium dodecyl sulfate-polyacrylamide gels containing AGP isolated from the sera of a patient at various days after operation. It is concluded that acute inflammation induces a strong increase in sialyl Lewis X-substituted AGP molecules that persists at a high level throughout the inflammatory period. We postulate that these changes represent a physiological feedback response on the interaction between leukocytes and inflamed endothelium, which is mediated via sialylated Lewis X structures and the selectin endothelial-leukocyte adhesion molecule 1.
Full Text
The Full Text of this article is available as a PDF (1.2 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bennett M., Schmid K. Immunosuppression by human plasma alpha 1-acid glycoprotein: importance of the carbohydrate moiety. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6109–6113. doi: 10.1073/pnas.77.10.6109. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bierhuizen M. F., De Wit M., Govers C. A., Ferwerda W., Koeleman C., Pos O., Van Dijk W. Glycosylation of three molecular forms of human alpha 1-acid glycoprotein having different interactions with concanavalin A. Variations in the occurrence of di-, tri-, and tetraantennary glycans and the degree of sialylation. Eur J Biochem. 1988 Aug 1;175(2):387–394. doi: 10.1111/j.1432-1033.1988.tb14208.x. [DOI] [PubMed] [Google Scholar]
- Biou D., Konan D., Féger J., Agneray J., Leroy Y., Cardon P., Fournet B., Durand G. Alterations in the carbohydrate moiety of alpha-1-acid glycoprotein purified from human cirrhotic ascitic fluid. Biochim Biophys Acta. 1987 Jul 7;913(3):308–312. doi: 10.1016/0167-4838(87)90140-3. [DOI] [PubMed] [Google Scholar]
- Bog-Hansen T. C. Crossed immuno-affinoelectrophoresis. An analytical method to predict the result of affinity chromatography. Anal Biochem. 1973 Dec;56(2):480–488. doi: 10.1016/0003-2697(73)90215-7. [DOI] [PubMed] [Google Scholar]
- Bories P. N., Feger J., Benbernou N., Rouzeau J. D., Agneray J., Durand G. Prevalence of tri- and tetraantennary glycans of human alpha 1-acid glycoprotein in release of macrophage inhibitor of interleukin-1 activity. Inflammation. 1990 Jun;14(3):315–323. doi: 10.1007/BF00915815. [DOI] [PubMed] [Google Scholar]
- Cardon P., Parente J. P., Leroy Y., Montreuil J., Fournet B. Separation of sialyl-oligosaccharides by high-performance liquid chromatography. Application to the analysis of mono-, di-, tri- and tetrasialyl-oligosaccharides obtained by hydrazinolysis of alpha 1-acid glycoprotein. J Chromatogr. 1986 Mar 28;356(1):135–146. doi: 10.1016/s0021-9673(00)91473-0. [DOI] [PubMed] [Google Scholar]
- Castell J. V., Gómez-Lechón M. J., David M., Fabra R., Trullenque R., Heinrich P. C. Acute-phase response of human hepatocytes: regulation of acute-phase protein synthesis by interleukin-6. Hepatology. 1990 Nov;12(5):1179–1186. doi: 10.1002/hep.1840120517. [DOI] [PubMed] [Google Scholar]
- Chandrasekaran E. V., Davila M., Nixon D., Mendicino J. Structures of the oligosaccharide chains of two forms of alpha 1-acid glycoprotein purified from liver metastases of lung, colon, and breast tumors. Cancer Res. 1984 Apr;44(4):1557–1567. [PubMed] [Google Scholar]
- Chia D., Terasaki P. I., Suyama N., Galton J., Hirota M., Katz D. Use of monoclonal antibodies to sialylated Lewisx and sialylated Lewisa for serological tests of cancer. Cancer Res. 1985 Jan;45(1):435–437. [PubMed] [Google Scholar]
- Costello M., Fiedel B. A., Gewurz H. Inhibition of platelet aggregation by native and desialised alpha-1 acid glycoprotein. Nature. 1979 Oct 25;281(5733):677–678. doi: 10.1038/281677a0. [DOI] [PubMed] [Google Scholar]
- Diabaté S., Geyer R., Stirm S. Structure of the major oligosaccharides in the fusion glycoprotein of Newcastle disease virus. Eur J Biochem. 1984 Mar 1;139(2):329–336. doi: 10.1111/j.1432-1033.1984.tb08011.x. [DOI] [PubMed] [Google Scholar]
- Fournet B., Montreuil J., Strecker G., Dorland L., Haverkamp J., Vliegenthart F. G., Binette J. P., Schmid K. Determination of the primary structures of 16 asialo-carbohydrate units derived from human plasma alpha 1-acid glycoprotein by 360-MHZ 1H NMR spectroscopy and permethylation analysis. Biochemistry. 1978 Nov 28;17(24):5206–5214. doi: 10.1021/bi00617a021. [DOI] [PubMed] [Google Scholar]
- Fukushima K., Hirota M., Terasaki P. I., Wakisaka A., Togashi H., Chia D., Suyama N., Fukushi Y., Nudelman E., Hakomori S. Characterization of sialosylated Lewisx as a new tumor-associated antigen. Cancer Res. 1984 Nov;44(11):5279–5285. [PubMed] [Google Scholar]
- Kannagi R., Fukushi Y., Tachikawa T., Noda A., Shin S., Shigeta K., Hiraiwa N., Fukuda Y., Inamoto T., Hakomori S. Quantitative and qualitative characterization of human cancer-associated serum glycoprotein antigens expressing fucosyl or sialyl-fucosyl type 2 chain polylactosamine. Cancer Res. 1986 May;46(5):2619–2626. [PubMed] [Google Scholar]
- Kaplan H. A., Woloski B. M., Hellman M., Jamieson J. C. Studies on the effect of inflammation on rat liver and serum sialyltransferase. Evidence that inflammation causes release of Gal beta 1 leads to 4GlcNAc alpha 2 leads to 6 sialyltransferase from liver. J Biol Chem. 1983 Oct 10;258(19):11505–11509. [PubMed] [Google Scholar]
- Koj A., Dubin A., Kasperczyk H., Bereta J., Gordon A. H. Changes in the blood level and affinity to concanavalin A of rat plasma glycoproteins during acute inflammation and hepatoma growth. Biochem J. 1982 Sep 15;206(3):545–553. doi: 10.1042/bj2060545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lasky L. A. Lectin cell adhesion molecules (LEC-CAMs): a new family of cell adhesion proteins involved with inflammation. J Cell Biochem. 1991 Feb;45(2):139–146. doi: 10.1002/jcb.240450204. [DOI] [PubMed] [Google Scholar]
- Lejeune P. J., Mallet B., Farnarier C., Kaplanski S. Changes in serum level and affinity for concanavalin A of human alpha 1-proteinase inhibitor in severe burn patients: relationship to natural killer cell activity. Biochim Biophys Acta. 1989 Feb 24;990(2):122–127. doi: 10.1016/s0304-4165(89)80022-4. [DOI] [PubMed] [Google Scholar]
- Macher B. A., Holmes E. H., Swiedler S. J., Stults C. L., Srnka C. A. Human alpha 1-3 fucosyltransferases. Glycobiology. 1991 Dec;1(6):577–584. doi: 10.1093/glycob/1.6.577. [DOI] [PubMed] [Google Scholar]
- Mackiewicz A., Schultz D., Mathison J., Ganapathi M., Kushner I. Effect of cytokines on glycosylation of acute phase proteins in human hepatoma cell lines. Clin Exp Immunol. 1989 Jan;75(1):70–75. [PMC free article] [PubMed] [Google Scholar]
- Nicollet I., Lebreton J. P., Fontaine M., Hiron M. Evidence for alpha-1-acid glycoprotein populations of different pI values after concanavalin A affinity chromatography. Study of their evolution during inflammation in man. Biochim Biophys Acta. 1981 Apr 28;668(2):235–245. doi: 10.1016/0005-2795(81)90031-3. [DOI] [PubMed] [Google Scholar]
- Okada Y., Shimoe T., Muguruma M., Usumoto R., Tsuji T., Jinno K., Moriwaki S., Shin S., Hakomori S. Hepatocellular expression of a novel glycoprotein with sialylated difucosyl Lex activity in the active inflammatory lesions of chronic liver disease. Am J Pathol. 1988 Feb;130(2):384–392. [PMC free article] [PubMed] [Google Scholar]
- Pos O., Moshage H. J., Yap S. H., Snieders J. P., Aarden L. A., van Gool J., Boers W., Brugman A. M., van Dijk W. Effects of monocytic products, recombinant interleukin-1, and recombinant interleukin-6 on glycosylation of alpha 1-acid glycoprotein: studies with primary human hepatocyte cultures and rats. Inflammation. 1989 Aug;13(4):415–427. doi: 10.1007/BF00914925. [DOI] [PubMed] [Google Scholar]
- Pos O., Oostendorp R. A., van der Stelt M. E., Scheper R. J., Van Dijk W. Con A-nonreactive human alpha 1-acid glycoprotein (AGP) is more effective in modulation of lymphocyte proliferation than Con A-reactive AGP serum variants. Inflammation. 1990 Apr;14(2):133–141. doi: 10.1007/BF00917452. [DOI] [PubMed] [Google Scholar]
- Pos O., van der Stelt M. E., Wolbink G. J., Nijsten M. W., van der Tempel G. L., van Dijk W. Changes in the serum concentration and the glycosylation of human alpha 1-acid glycoprotein and alpha 1-protease inhibitor in severely burned persons: relation to interleukin-6 levels. Clin Exp Immunol. 1990 Dec;82(3):579–582. doi: 10.1111/j.1365-2249.1990.tb05493.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shimizu Y., Shaw S., Graber N., Gopal T. V., Horgan K. J., Van Seventer G. A., Newman W. Activation-independent binding of human memory T cells to adhesion molecule ELAM-1. Nature. 1991 Feb 28;349(6312):799–802. doi: 10.1038/349799a0. [DOI] [PubMed] [Google Scholar]
- Skacel P. O., Edwards A. J., Harrison C. T., Watkins W. M. Enzymic control of the expression of the X determinant (CD15) in human myeloid cells during maturation: the regulatory role of 6-sialytransferase. Blood. 1991 Sep 15;78(6):1452–1460. [PubMed] [Google Scholar]
- Springer T. A., Lasky L. A. Cell adhesion. Sticky sugars for selectins. Nature. 1991 Jan 17;349(6306):196–197. doi: 10.1038/349196a0. [DOI] [PubMed] [Google Scholar]
- Thompson S., Cantwell B. M., Cornell C., Turner G. A. Abnormally-fucosylated haptoglobin: a cancer marker for tumour burden but not gross liver metastasis. Br J Cancer. 1991 Aug;64(2):386–390. doi: 10.1038/bjc.1991.314. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thompson S., Guthrie D., Turner G. A. Fucosylated forms of alpha-1-antitrypsin that predict unresponsiveness to chemotherapy in ovarian cancer. Br J Cancer. 1988 Nov;58(5):589–593. doi: 10.1038/bjc.1988.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walz G., Aruffo A., Kolanus W., Bevilacqua M., Seed B. Recognition by ELAM-1 of the sialyl-Lex determinant on myeloid and tumor cells. Science. 1990 Nov 23;250(4984):1132–1135. doi: 10.1126/science.1701275. [DOI] [PubMed] [Google Scholar]
- Wieruszeski J. M., Fournet B., Konan D., Biou D., Durand G. 400-MHz 1H-NMR spectroscopy of fucosylated tetrasialyl oligosaccharides isolated from normal and cirrhotic alpha 1-acid glycoprotein. FEBS Lett. 1988 Oct 10;238(2):390–394. doi: 10.1016/0014-5793(88)80518-0. [DOI] [PubMed] [Google Scholar]
- Woloski B. M., Fuller G. M., Jamieson J. C., Gospodarek E. Studies on the effect of the hepatocyte-stimulating factor on galactose-beta 1----4-N-acetylglucosamine alpha 2----6-sialyltransferase in cultured hepatocytes. Biochim Biophys Acta. 1986 Feb 21;885(2):185–191. doi: 10.1016/0167-4889(86)90087-x. [DOI] [PubMed] [Google Scholar]
- Zhou Q., Moore K. L., Smith D. F., Varki A., McEver R. P., Cummings R. D. The selectin GMP-140 binds to sialylated, fucosylated lactosaminoglycans on both myeloid and nonmyeloid cells. J Cell Biol. 1991 Oct;115(2):557–564. doi: 10.1083/jcb.115.2.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van Dijk W., Boers W., Sala M., Lasthuis A. M., Mookerjea S. Activity and secretion of sialyltransferase in primary monolayer cultures of rat hepatocytes cultured with and without dexamethasone. Biochem Cell Biol. 1986 Feb;64(2):79–84. doi: 10.1139/o86-014. [DOI] [PubMed] [Google Scholar]
- van Dijk W., Pos O., van der Stelt M. E., Moshage H. J., Yap S. H., Dente L., Baumann P., Eap C. B. Inflammation-induced changes in expression and glycosylation of genetic variants of alpha 1-acid glycoprotein. Studies with human sera, primary cultures of human hepatocytes and transgenic mice. Biochem J. 1991 Jun 1;276(Pt 2):343–347. doi: 10.1042/bj2760343. [DOI] [PMC free article] [PubMed] [Google Scholar]
