Home LiteratureArticle Details
PMID: 8034751 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Natural ligands of the B cell adhesion molecule CD22 beta can be masked by 9-O-acetylation of sialic acids.

The Journal of cell biology ·Vol. 126 ·No. 2 ·1994-07-00 ·Pages 549-62

Sjoberg ER, Powell LD, Klein A, Varki A

Abstract

CD22 beta is a B cell-restricted phosphoprotein expressed on the surface of mature resting B cells. It mediates interactions with other cells partly or exclusively via recognition of alpha 2-6-linked sialic acids on glycoconjugates. The sialylated N-linked oligosaccharides recognized best by CD22 beta are common to many glycoproteins, suggesting that additional regulatory mechanisms may exist. Since the exocyclic side chain of sialic acid is required for recognition, we explored the effects of a naturally occurring modification of the side chain, 9-O-acetylation. Semisynthetic N-linked oligosaccharides terminating with 9-O-acetylated, alpha 2-6-linked sialic acids showed markedly reduced binding to CD22 beta relative to their non-O-acetylated counterparts. Murine lymphoid cells were probed for natural CD22 beta ligands that might be O-acetylated using recombinant soluble forms of CD22 beta (CD22 beta Rg) and influenza C esterase (CHE-Fc, which specifically removes 9-O-acetyl esters from sialic acids). By flow cytometry analysis, CD22 beta Rg binding to splenic B cells and a subset of T cells was increased by pretreatment with CHE-Fc, indicating that some potential CD22 beta ligands are naturally "masked" by 9-O-acetylation. Unmasking of these CD22 beta ligands by removal of 9-O-acetyl esters from intact splenocytes substantially increases their CD22 beta-dependent adhesion in an in vitro adhesion assay. Probing of murine lymphoid tissue sections by CD22 beta Rg and CHE-Fc treatment demonstrates regionally restricted and differentially expressed patterns of distribution between masked and unmasked ligands. For example, lymph node-associated follicular B cells express high levels of CD22 beta ligands, none of which are masked by 9-O-acetylation. In contrast, the ligands on lymph node-associated dendritic cells are almost completely masked by 9-O-acetylation, suggesting that masking may regulate interactions between CD22 beta-positive B cells and dendritic cells. In the thymus, only medullary cells express CD22 beta ligands, and a significant portion of these are masked by 9-O-acetylation, particularly at the cortical-medullary junction. Thus, 9-O-acetylation of sialic acids on immune cells is in a position to negatively regulate CD22 beta adhesion events in a manner depending on both cell type and tissue localization.

MeSH Terms
Acetylation Acetylesterase Animals Antigens, CD/metabolism Antigens, Differentiation, B-Lymphocyte/metabolism B-Lymphocytes/chemistry Carboxylic Ester Hydrolases/metabolism Cell Adhesion/physiology Cell Adhesion Molecules/metabolism Dendritic Cells/chemistry Glycoproteins/analysis,metabolism Lectins Ligands Lymph Nodes/chemistry,cytology Mice Neuraminic Acids/metabolism Oligosaccharides/chemical synthesis,metabolism Sialic Acid Binding Ig-like Lectin 2 Sialic Acids/metabolism Spleen/cytology T-Lymphocytes/chemistry Thymus Gland/chemistry
Chemicals
Antigens, CD Antigens, Differentiation, B-Lymphocyte Cd22 protein, mouse Cell Adhesion Molecules Glycoproteins Lectins Ligands Neuraminic Acids Oligosaccharides Sialic Acid Binding Ig-like Lectin 2 Sialic Acids Carboxylic Ester Hydrolases Acetylesterase sialate O-acetylesterase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sjoberg E R
Glycobiology Program, University of California, San Diego Cancer Center, La Jolla 92093-0063.
Powell L D
Klein A
Varki A
References (47)
47 references, click to expand
  1. Synthesis of 9-O-acetyl- and 4,9-di-O-acetyl derivatives of the methyl ester of N-acetyl-beta-D-neuraminic acid methylglycoside. Their use as models in periodate oxidation studies.
    Hoppe Seylers Z Physiol Chem. 1975 Oct;356(10):1575-83 PMID: 174994
  2. The oligosaccharide binding specificities of CD22 beta, a sialic acid-specific lectin of B cells.
    J Biol Chem. 1994 Apr 8;269(14):10628-36 PMID: 8144652
  3. Sialylation of glycoprotein oligosaccharides N-linked to asparagine. Enzymatic characterization of a Gal beta 1 to 3(4)GlcNAc alpha 2 to 3 sialyltransferase and a Gal beta 1 to 4GlcNAc alpha 2 to 6 sialyltransferase from rat liver.
    J Biol Chem. 1982 Nov 25;257(22):13845-53 PMID: 7142180
  4. Glycolipids of murine lymphocyte subpopulations. Structural characterization of thymus gangliosides.
    J Biol Chem. 1983 May 10;258(9):5893-8 PMID: 6853556
  5. The release and purification of sialic acids from glycoconjugates: methods to minimize the loss and migration of O-acetyl groups.
    Anal Biochem. 1984 Feb;137(1):236-47 PMID: 6731802
  6. Determination of the sialylation pattern of human fibrinogen glycopeptides with fast atom bombardment.
    Biochemistry. 1984 Dec 18;23(26):6389-92 PMID: 6529554
  7. Sialylation of glycoprotein oligosaccharides with N-acetyl-, N-glycolyl-, and N-O-diacetylneuraminic acids.
    J Biol Chem. 1985 Jul 25;260(15):8838-49 PMID: 4019457
  8. HD39 (B3), a B lineage-restricted antigen whose cell surface expression is limited to resting and activated human B lymphocytes.
    J Immunol. 1986 Jun 15;136(12):4470-9 PMID: 3086431
  9. Amplification of human B cell activation by a monoclonal antibody to the B cell-specific antigen CD22, Bp 130/140.
    J Immunol. 1987 Jan 1;138(1):98-103 PMID: 3097151
  10. Branch specificity of bovine colostrum CMP-sialic acid: Gal beta 1----4GlcNAc-R alpha 2----6-sialyltransferase. Sialylation of bi-, tri-, and tetraantennary oligosaccharides and glycopeptides of the N-acetyllactosamine type.
    J Biol Chem. 1987 Feb 15;262(5):2025-33 PMID: 3546284
  11. Migration of O-acetyl groups in N,O-acetylneuraminic acids.
    Eur J Biochem. 1987 Feb 2;162(3):601-7 PMID: 3830159
  12. Selective inactivation of influenza C esterase: a probe for detecting 9-O-acetylated sialic acids.
    Science. 1987 Jun 5;236(4806):1293-5 PMID: 3589663
  13. Role of the CD22 human B cell antigen in B cell triggering by anti-immunoglobulin.
    J Immunol. 1988 Mar 15;140(6):1791-5 PMID: 3257985
  14. Alterations of acyl-neuraminic acids on T-lymphocytes in cases of melanoma.
    Klin Wochenschr. 1988 Jun 15;66(12):540-4 PMID: 3262185
  15. Conformational analysis of the sialyl alpha(2----3/6)N-acetyllactosamine structural element occurring in glycoproteins, by two-dimensional NOE 1H-NMR spectroscopy in combination with energy calculations by hard-sphere exo-anomeric and molecular mechanics force-field with hydrogen-bonding potential.
    Eur J Biochem. 1989 Jan 2;178(3):727-39 PMID: 2912732
  16. Lymphocyte homing.
    Adv Immunol. 1989;44:313-78 PMID: 2646861
  17. The B-cell antigen CD22 mediates monocyte and erythrocyte adhesion.
    Nature. 1990 May 3;345(6270):74-7 PMID: 1691828
  18. Biosynthesis and turnover of O-acetyl and N-acetyl groups in the gangliosides of human melanoma cells.
    J Biol Chem. 1990 Aug 5;265(22):13091-103 PMID: 2198284
  19. Adhesion receptors of the immune system.
    Nature. 1990 Aug 2;346(6283):425-34 PMID: 1974032
  20. cDNA cloning of the B cell membrane protein CD22: a mediator of B-B cell interactions.
    J Exp Med. 1991 Jan 1;173(1):137-46 PMID: 1985119
  21. Accessory cells in normal human and rodent lymph nodes: morphology, phenotype, and functional implications.
    Curr Top Pathol. 1990;84 ( Pt 1):193-218 PMID: 2292194
  22. [Change in acylneuraminic acid content of T-lymphocytes and in plasma in breast cancer].
    Klin Wochenschr. 1991 Jan 4;69(1):5-9 PMID: 2016848
  23. Regulation of human B-cell activation and adhesion.
    Annu Rev Immunol. 1991;9:97-127 PMID: 1910693
  24. The B lymphocyte adhesion molecule CD22 interacts with leukocyte common antigen CD45RO on T cells and alpha 2-6 sialyltransferase, CD75, on B cells.
    Cell. 1991 Sep 20;66(6):1133-44 PMID: 1717156
  25. CD45. A prototype for transmembrane protein tyrosine phosphatases.
    J Biol Chem. 1991 Dec 15;266(35):23517-20 PMID: 1836211
  26. The HB-6, CDw75, and CD76 differentiation antigens are unique cell-surface carbohydrate determinants generated by the beta-galactoside alpha 2,6-sialyltransferase.
    J Cell Biol. 1992 Jan;116(2):423-35 PMID: 1730763
  27. Diversity in the sialic acids.
    Glycobiology. 1992 Feb;2(1):25-40 PMID: 1550987
  28. Conformational analysis of sialyloligosaccharides.
    Carbohydr Res. 1991 Sep 30;218:27-54 PMID: 1802388
  29. Cell cycle-dependent regulation of CDw75 (beta-galactoside alpha-2,6-sialyltransferase) on human B lymphocytes.
    Eur J Immunol. 1992 May;22(5):1149-55 PMID: 1577059
  30. Purification and characterization of the nuclear cytidine 5'-monophosphate N-acetylneuraminic acid synthetase from rat liver.
    J Biol Chem. 1992 May 5;267(13):9257-63 PMID: 1577759
  31. Structural and immunological characterization of O-acetylated GD2. Evidence that GD2 is an acceptor for ganglioside O-acetyltransferase in human melanoma cells.
    J Biol Chem. 1992 Aug 15;267(23):16200-11 PMID: 1644805
  32. Identification and characterization of the murine homologue of CD22, a B lymphocyte-restricted adhesion molecule.
    J Immunol. 1992 Oct 15;149(8):2641-9 PMID: 1401903
  33. CDw 60 antibodies bind to acetylated forms of ganglioside GD3.
    Biochem Biophys Res Commun. 1992 Sep 30;187(3):1343-9 PMID: 1417810
  34. CD22-mediated stimulation of T cells regulates T-cell receptor/CD3-induced signaling.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10242-6 PMID: 1438211
  35. Tyrosine phosphorylation of CD22 during B cell activation.
    Science. 1992 Nov 6;258(5084):1001-4 PMID: 1279802
  36. Enhanced interaction of L-selectin with the high endothelial venule ligand via selectively oxidized sialic acids.
    Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1068-72 PMID: 7679216
  37. Chromosome mapping and organization of the human beta-galactoside alpha 2,6-sialyltransferase gene. Differential and cell-type specific usage of upstream exon sequences in B-lymphoblastoid cells.
    J Biol Chem. 1993 Feb 25;268(6):4355-61 PMID: 7786324
  38. CD22, a B cell-specific immunoglobulin superfamily member, is a sialic acid-binding lectin.
    J Biol Chem. 1993 Apr 5;268(10):7011-8 PMID: 8463234
  39. Natural ligands of the B cell adhesion molecule CD22 beta carry N-linked oligosaccharides with alpha-2,6-linked sialic acids that are required for recognition.
    J Biol Chem. 1993 Apr 5;268(10):7019-27 PMID: 8463235
  40. CD22 associates with the human surface IgM-B-cell antigen receptor complex.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3236-40 PMID: 8475064
  41. Immunological memory.
    Annu Rev Immunol. 1993;11:49-77 PMID: 8476570
  42. Cell-specific expression of human beta-galactoside alpha 2,6-sialyltransferase transcripts differing in the 5' untranslated region.
    Eur J Biochem. 1993 Apr 1;213(1):467-75 PMID: 8477718
  43. Kinetic and spatial interrelationships between ganglioside glycosyltransferases and O-acetyltransferase(s) in human melanoma cells.
    J Biol Chem. 1993 May 15;268(14):10185-96 PMID: 8486686
  44. 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):10197-206 PMID: 8486687
  45. The same epitope on CD22 of B lymphocytes mediates the adhesion of erythrocytes, T and B lymphocytes, neutrophils, and monocytes.
    J Immunol. 1993 Jun 1;150(11):4719-32 PMID: 7684411
  46. CDw60 glycolipid antigens of human leukocytes: structural characterization and cellular distribution.
    Blood. 1993 Sep 15;82(6):1776-86 PMID: 8400232
  47. The nature of sialic acids in human lymphocytes.
    Biochim Biophys Acta. 1982 Feb 2;714(2):351-5 PMID: 6976798
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.126.2.549
Published
1994-07-00
Pages
549-62
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2200033
Subset
IM
Grants
NCI NIH HHS · KO1 CA01649 · United States
NIGMS NIH HHS · R01GM32373 · United States
External Links
PubMed source DOI: 10.1083/jcb.126.2.549 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2