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. 1996 Oct 15;24(20):4003–4008. doi: 10.1093/nar/24.20.4003

Molecular cloning of the cDNA encoding a murine sialic acid-specific 9-O-acetylesterase and RNA expression in cells of hematopoietic and non-hematopoietic origin.

A Stoddart 1, Y Zhang 1, C J Paige 1
PMCID: PMC146199  PMID: 8918804

Abstract

We describe the isolation of a cDNA encoding a murine sialic acid-specific 9-O-acetylesterase as well as its expression pattern in cells of both hematopoietic and non-hematopoietic origin. This enzyme catalyzes the removal of O-acetyl ester groups from position 9 of the parent sialic acid N-acetylneuraminic acid. The cDNA is 2105 nt in length and encodes a protein of 541 amino acids with a predicted molecular weight of 61 kDa, not including oligosaccharides linked to eight potential N-glycosylation sites. The cDNA encoding the acetylesterase displays a widespread distribution in various cell lines and tissues. Expression studies of B lineage cell lines and primary fetal liver cells revealed a developmentally regulated expression pattern in cells of hematopoietic origin. Given the importance of 9-O-acetylation of sialic acids, the cloning of the cDNA encoding a sialic acid-specific 9-O-acetylesterase will be helpful in understanding further the regulation of this post-translational modification and the biological consequences thereof.

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Selected References

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  1. Bergman Y., Stewart S. J., Levy S., Levy R. Biosynthesis, glycosylation, and in vitro translation of the human T cell antigen Leu-4. J Immunol. 1983 Oct;131(4):1876–1881. [PubMed] [Google Scholar]
  2. Blum A. S., Barnstable C. J. O-acetylation of a cell-surface carbohydrate creates discrete molecular patterns during neural development. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8716–8720. doi: 10.1073/pnas.84.23.8716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brady G., Iscove N. N. Construction of cDNA libraries from single cells. Methods Enzymol. 1993;225:611–623. doi: 10.1016/0076-6879(93)25039-5. [DOI] [PubMed] [Google Scholar]
  4. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  5. Brenner S. The molecular evolution of genes and proteins: a tale of two serines. Nature. 1988 Aug 11;334(6182):528–530. doi: 10.1038/334528a0. [DOI] [PubMed] [Google Scholar]
  6. Butor C., Diaz S., Varki A. High level O-acetylation of sialic acids on N-linked oligosaccharides of rat liver membranes. Differential subcellular distribution of 7- and 9-O-acetyl groups and of enzymes involved in their regulation. J Biol Chem. 1993 May 15;268(14):10197–10206. [PubMed] [Google Scholar]
  7. Butor C., Higa H. H., Varki A. Structural, immunological, and biosynthetic studies of a sialic acid-specific O-acetylesterase from rat liver. J Biol Chem. 1993 May 15;268(14):10207–10213. [PubMed] [Google Scholar]
  8. Cumano A., Paige C. J., Iscove N. N., Brady G. Bipotential precursors of B cells and macrophages in murine fetal liver. Nature. 1992 Apr 16;356(6370):612–615. doi: 10.1038/356612a0. [DOI] [PubMed] [Google Scholar]
  9. Diaz S., Higa H. H., Hayes B. K., Varki A. O-acetylation and de-O-acetylation of sialic acids. 7- and 9-o-acetylation of alpha 2,6-linked sialic acids on endogenous N-linked glycans in rat liver Golgi vesicles. J Biol Chem. 1989 Nov 15;264(32):19416–19426. [PubMed] [Google Scholar]
  10. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  11. Fleischer B. Mechanism of glycosylation in the Golgi apparatus. J Histochem Cytochem. 1983 Aug;31(8):1033–1040. doi: 10.1177/31.8.6345657. [DOI] [PubMed] [Google Scholar]
  12. Hayes B. K., Varki A. O-acetylation and de-O-acetylation of sialic acids. Sialic acid esterases of diverse evolutionary origins have serine active sites and essential arginine residues. J Biol Chem. 1989 Nov 15;264(32):19443–19448. [PubMed] [Google Scholar]
  13. Herrler G., Reuter G., Rott R., Klenk H. D., Schauer R. N-acetyl-9-O-acetylneuraminic acid, the receptor determinant for influenza C virus, is a differentiation marker on chicken erythrocytes. Biol Chem Hoppe Seyler. 1987 May;368(5):451–454. doi: 10.1515/bchm3.1987.368.1.451. [DOI] [PubMed] [Google Scholar]
  14. Herrler G., Rott R., Klenk H. D., Müller H. P., Shukla A. K., Schauer R. The receptor-destroying enzyme of influenza C virus is neuraminate-O-acetylesterase. EMBO J. 1985 Jun;4(6):1503–1506. doi: 10.1002/j.1460-2075.1985.tb03809.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Higa H. H., Diaz S., Varki A. Biochemical and genetic evidence for distinct membrane-bound and cytosolic sialic acid O-acetyl-esterases: serine-active-site enzymes. Biochem Biophys Res Commun. 1987 May 14;144(3):1099–1108. doi: 10.1016/0006-291x(87)91425-2. [DOI] [PubMed] [Google Scholar]
  16. Higa H. H., Manzi A., Varki A. O-acetylation and de-O-acetylation of sialic acids. Purification, characterization, and properties of a glycosylated rat liver esterase specific for 9-O-acetylated sialic acids. J Biol Chem. 1989 Nov 15;264(32):19435–19442. [PubMed] [Google Scholar]
  17. Kamerling J. P., Schauer R., Shukla A. K., Stoll S., Van Halbeek H., Vliegenthart J. F. Migration of O-acetyl groups in N,O-acetylneuraminic acids. Eur J Biochem. 1987 Feb 2;162(3):601–607. doi: 10.1111/j.1432-1033.1987.tb10681.x. [DOI] [PubMed] [Google Scholar]
  18. Kee B. L., Cumano A., Iscove N. N., Paige C. J. Stromal cell independent growth of bipotent B cell--macrophage precursors from murine fetal liver. Int Immunol. 1994 Mar;6(3):401–407. doi: 10.1093/intimm/6.3.401. [DOI] [PubMed] [Google Scholar]
  19. Kelm S., Schauer R., Manuguerra J. C., Gross H. J., Crocker P. R. Modifications of cell surface sialic acids modulate cell adhesion mediated by sialoadhesin and CD22. Glycoconj J. 1994 Dec;11(6):576–585. doi: 10.1007/BF00731309. [DOI] [PubMed] [Google Scholar]
  20. Kincade P. W., Lee G., Watanabe T., Sun L., Scheid M. P. Antigens displayed on murine B lymphocyte precursors. J Immunol. 1981 Dec;127(6):2262–2268. [PubMed] [Google Scholar]
  21. Levine J. M., Beasley L., Stallcup W. B. Localization of a neurectoderm-associated cell surface antigen in the developing and adult rat. Brain Res. 1986 Jun;392(1-2):211–222. doi: 10.1016/0165-3806(86)90247-6. [DOI] [PubMed] [Google Scholar]
  22. Liang P., Pardee A. B. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992 Aug 14;257(5072):967–971. doi: 10.1126/science.1354393. [DOI] [PubMed] [Google Scholar]
  23. Marshall R. D. Glycoproteins. Annu Rev Biochem. 1972;41:673–702. doi: 10.1146/annurev.bi.41.070172.003325. [DOI] [PubMed] [Google Scholar]
  24. Paige C. J., Gisler R. H., McKearn J. P., Iscove N. N. Differentiation of murine B cell precursors in agar culture. Frequency, surface marker analysis and requirements for growth of clonable pre-B cells. Eur J Immunol. 1984 Nov;14(11):979–987. doi: 10.1002/eji.1830141104. [DOI] [PubMed] [Google Scholar]
  25. Paige C. J., Kincade P. W., Ralph P. Murine B cell leukemia line with inducible surface immunoglobulin expression. J Immunol. 1978 Aug;121(2):641–647. [PubMed] [Google Scholar]
  26. 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]
  27. Schauer R. Sialic acids: metabolism of O-acetyl groups. Methods Enzymol. 1987;138:611–626. doi: 10.1016/0076-6879(87)38055-3. [DOI] [PubMed] [Google Scholar]
  28. Sjoberg E. R., Powell L. D., Klein A., Varki A. Natural ligands of the B cell adhesion molecule CD22 beta can be masked by 9-O-acetylation of sialic acids. J Cell Biol. 1994 Jul;126(2):549–562. doi: 10.1083/jcb.126.2.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Troy F. A., 2nd Polysialylation: from bacteria to brains. Glycobiology. 1992 Feb;2(1):5–23. doi: 10.1093/glycob/2.1.5. [DOI] [PubMed] [Google Scholar]
  30. Varki A. Diversity in the sialic acids. Glycobiology. 1992 Feb;2(1):25–40. doi: 10.1093/glycob/2.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Varki A., Muchmore E., Diaz S. A sialic acid-specific O-acetylesterase in human erythrocytes: possible identity with esterase D, the genetic marker of retinoblastomas and Wilson disease. Proc Natl Acad Sci U S A. 1986 Feb;83(4):882–886. doi: 10.1073/pnas.83.4.882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vlasak R., Luytjes W., Spaan W., Palese P. Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4526–4529. doi: 10.1073/pnas.85.12.4526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Zimmer G., Suguri T., Reuter G., Yu R. K., Schauer R., Herrler G. Modification of sialic acids by 9-O-acetylation is detected in human leucocytes using the lectin property of influenza C virus. Glycobiology. 1994 Jun;4(3):343–349. doi: 10.1093/glycob/4.3.343. [DOI] [PMC free article] [PubMed] [Google Scholar]

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