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. 1997 Jun 1;324(Pt 2):673–680. doi: 10.1042/bj3240673

Selective binding of N-acetylglucosamine to the chicken hepatic lectin.

L Burrows 1, S T Iobst 1, K Drickamer 1
PMCID: PMC1218481  PMID: 9182733

Abstract

Among Ca2+-dependent (C-type) animal lectins, the chicken hepatic lectin (CHL) is unique in displaying almost complete selectivity for N-acetylglucosamine over other monosaccharide ligands. The crystal structures of the carbohydrate-recognition domain (CRD) from serum mannose-binding protein (MBP) and of a complex between the CRD from liver MBP and the methyl glycoside of N-acetylglucosamine were used to model the binding site in CHL. Substitution of portions of CHL into the MBP framework did not substantially increase selectivity. A bacterial expression system for the CRD of CHL was developed so that specific residues predicted to be near the 2-acetamido substituent of N-acetylglucosamine could be altered by site-directed mutagenesis. The results indicate that the ligand is bound to CHL in the same orientation as it binds to liver MBP. A tyrosine and a valine residue that probably contact the the N-acetyl group have been identified. These results, together with studies of ligand-binding selectivity, suggest that these residues form part of a binding pocket for the N-acetyl group, which confers selective binding of N-acetylglucosamine.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beavil A. J., Edmeades R. L., Gould H. J., Sutton B. J. Alpha-helical coiled-coil stalks in the low-affinity receptor for IgE (Fc epsilon RII/CD23) and related C-type lectins. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):753–757. doi: 10.1073/pnas.89.2.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Childs R. A., Feizi T., Yuen C. T., Drickamer K., Quesenberry M. S. Differential recognition of core and terminal portions of oligosaccharide ligands by carbohydrate-recognition domains of two mannose-binding proteins. J Biol Chem. 1990 Dec 5;265(34):20770–20777. [PubMed] [Google Scholar]
  3. Drickamer K. Complete amino acid sequence of a membrane receptor for glycoproteins. Sequence of the chicken hepatic lectin. J Biol Chem. 1981 Jun 10;256(11):5827–5839. [PubMed] [Google Scholar]
  4. Drickamer K. Engineering galactose-binding activity into a C-type mannose-binding protein. Nature. 1992 Nov 12;360(6400):183–186. doi: 10.1038/360183a0. [DOI] [PubMed] [Google Scholar]
  5. Drickamer K. Evolution of Ca(2+)-dependent animal lectins. Prog Nucleic Acid Res Mol Biol. 1993;45:207–232. [PubMed] [Google Scholar]
  6. Drickamer K., Taylor M. E. Biology of animal lectins. Annu Rev Cell Biol. 1993;9:237–264. doi: 10.1146/annurev.cb.09.110193.001321. [DOI] [PubMed] [Google Scholar]
  7. Fornstedt N., Porath J. Characterization studies on a new lectin found in seeds of Vicia ervilia. FEBS Lett. 1975 Sep 15;57(2):187–191. doi: 10.1016/0014-5793(75)80713-7. [DOI] [PubMed] [Google Scholar]
  8. GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ghrayeb J., Kimura H., Takahara M., Hsiung H., Masui Y., Inouye M. Secretion cloning vectors in Escherichia coli. EMBO J. 1984 Oct;3(10):2437–2442. doi: 10.1002/j.1460-2075.1984.tb02151.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Holland E. C., Drickamer K. Signal recognition particle mediates the insertion of a transmembrane protein which has a cytoplasmic NH2 terminus. J Biol Chem. 1986 Jan 25;261(3):1286–1292. [PubMed] [Google Scholar]
  11. Hsueh E. C., Holland E. C., Carrera G. M., Jr, Drickamer K. The rat liver asialoglycoprotein receptor polypeptide must be inserted into a microsome to achieve its active conformation. J Biol Chem. 1986 Apr 15;261(11):4940–4947. [PubMed] [Google Scholar]
  12. Ichikawa Y., Lee R. T., Lee Y. C. Synthesis of N-acetylglucosamine derivatives as probes for specificity of chicken hepatic lectin. Glycoconj J. 1990;7(4):335–348. doi: 10.1007/BF01073377. [DOI] [PubMed] [Google Scholar]
  13. Iobst S. T., Drickamer K. Selective sugar binding to the carbohydrate recognition domains of the rat hepatic and macrophage asialoglycoprotein receptors. J Biol Chem. 1996 Mar 22;271(12):6686–6693. doi: 10.1074/jbc.271.12.6686. [DOI] [PubMed] [Google Scholar]
  14. Iobst S. T., Wormald M. R., Weis W. I., Dwek R. A., Drickamer K. Binding of sugar ligands to Ca(2+)-dependent animal lectins. I. Analysis of mannose binding by site-directed mutagenesis and NMR. J Biol Chem. 1994 Jun 3;269(22):15505–15511. [PubMed] [Google Scholar]
  15. Kawasaki T., Ashwell G. Isolation and characterization of an avian hepatic binding protein specific for N-acetylglucosamine-terminated glycoproteins. J Biol Chem. 1977 Sep 25;252(18):6536–6543. [PubMed] [Google Scholar]
  16. Kronis K. A., Carver J. P. Specificity of isolectins of wheat germ agglutinin for sialyloligosaccharides: a 360-MHz proton nuclear magnetic resonance binding study. Biochemistry. 1982 Jun 22;21(13):3050–3057. doi: 10.1021/bi00256a003. [DOI] [PubMed] [Google Scholar]
  17. Kuhlenschmidt T. B., Lee Y. C. Specificity of chicken liver carbohydrate binding protein. Biochemistry. 1984 Jul 31;23(16):3569–3575. doi: 10.1021/bi00311a001. [DOI] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. Lee R. T., Ichikawa Y., Fay M., Drickamer K., Shao M. C., Lee Y. C. Ligand-binding characteristics of rat serum-type mannose-binding protein (MBP-A). Homology of binding site architecture with mammalian and chicken hepatic lectins. J Biol Chem. 1991 Mar 15;266(8):4810–4815. [PubMed] [Google Scholar]
  20. Lee R. T., Rice K. G., Rao N. B., Ichikawa Y., Barthel T., Piskarev V., Lee Y. C. Binding characteristics of N-acetylglucosamine-specific lectin of the isolated chicken hepatocytes: similarities to mammalian hepatic galactose/N-acetylgalactosamine-specific lectin. Biochemistry. 1989 Oct 17;28(21):8351–8358. doi: 10.1021/bi00447a013. [DOI] [PubMed] [Google Scholar]
  21. Loeb J. A., Drickamer K. The chicken receptor for endocytosis of glycoproteins contains a cluster of N-acetylglucosamine-binding sites. J Biol Chem. 1987 Mar 5;262(7):3022–3029. [PubMed] [Google Scholar]
  22. Mellow T. E., Halberg D., Drickamer K. Endocytosis of N-acetylglucosamine-containing glycoproteins by rat fibroblasts expressing a single species of chicken liver glycoprotein receptor. J Biol Chem. 1988 Apr 15;263(11):5468–5473. [PubMed] [Google Scholar]
  23. Mullin N. P., Hall K. T., Taylor M. E. Characterization of ligand binding to a carbohydrate-recognition domain of the macrophage mannose receptor. J Biol Chem. 1994 Nov 11;269(45):28405–28413. [PubMed] [Google Scholar]
  24. Ng K. K., Drickamer K., Weis W. I. Structural analysis of monosaccharide recognition by rat liver mannose-binding protein. J Biol Chem. 1996 Jan 12;271(2):663–674. doi: 10.1074/jbc.271.2.663. [DOI] [PubMed] [Google Scholar]
  25. Quesenberry M. S., Drickamer K. Determination of the minimum carbohydrate-recognition domain in two C-type animal lectins. Glycobiology. 1991 Dec;1(6):615–621. doi: 10.1093/glycob/1.6.615. [DOI] [PubMed] [Google Scholar]
  26. Quesenberry M. S., Drickamer K. Role of conserved and nonconserved residues in the Ca(2+)-dependent carbohydrate-recognition domain of a rat mannose-binding protein. Analysis by random cassette mutagenesis. J Biol Chem. 1992 May 25;267(15):10831–10841. [PubMed] [Google Scholar]
  27. Saleque S., Ruiz N., Drickamer K. Expression and characterization of a carbohydrate-binding fragment of rat aggrecan. Glycobiology. 1993 Apr;3(2):185–190. doi: 10.1093/glycob/3.2.185. [DOI] [PubMed] [Google Scholar]
  28. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sikder S. K., Kabat E. A., Steer C. J., Ashwell G. The binding site of chicken hepatic lectin. J Biol Chem. 1983 Oct 25;258(20):12520–12525. [PubMed] [Google Scholar]
  30. Staros J. V. N-hydroxysulfosuccinimide active esters: bis(N-hydroxysulfosuccinimide) esters of two dicarboxylic acids are hydrophilic, membrane-impermeant, protein cross-linkers. Biochemistry. 1982 Aug 17;21(17):3950–3955. doi: 10.1021/bi00260a008. [DOI] [PubMed] [Google Scholar]
  31. Verrey F., Drickamer K. Determinants of oligomeric structure in the chicken liver glycoprotein receptor. Biochem J. 1993 May 15;292(Pt 1):149–155. doi: 10.1042/bj2920149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Weis W. I., Crichlow G. V., Murthy H. M., Hendrickson W. A., Drickamer K. Physical characterization and crystallization of the carbohydrate-recognition domain of a mannose-binding protein from rat. J Biol Chem. 1991 Nov 5;266(31):20678–20686. [PubMed] [Google Scholar]
  33. Weis W. I., Drickamer K., Hendrickson W. A. Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature. 1992 Nov 12;360(6400):127–134. doi: 10.1038/360127a0. [DOI] [PubMed] [Google Scholar]
  34. Weis W. I., Drickamer K. Structural basis of lectin-carbohydrate recognition. Annu Rev Biochem. 1996;65:441–473. doi: 10.1146/annurev.bi.65.070196.002301. [DOI] [PubMed] [Google Scholar]
  35. Wright C. S. Crystallographic elucidation of the saccharide binding mode in wheat germ agglutinin and its biological significance. J Mol Biol. 1980 Aug 15;141(3):267–291. doi: 10.1016/0022-2836(80)90181-3. [DOI] [PubMed] [Google Scholar]
  36. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983 Jun 1;133(1):17–21. doi: 10.1111/j.1432-1033.1983.tb07424.x. [DOI] [PubMed] [Google Scholar]

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