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PMID: 9636173 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Masking and unmasking of the sialic acid-binding lectin activity of CD22 (Siglec-2) on B lymphocytes.

Razi N, Varki A

Abstract

CD22 is a B cell-restricted glycoprotein involved in signal transduction and modulation of cellular activation. It is also an I-type lectin (now designated Siglec-2), whose extracellular domain can specifically recognize alpha2-6-linked sialic acid (Sia) residues. This activity is postulated to mediate intercellular adhesion and/or to act as a coreceptor in antigen-induced B cell activation. However, studies with recombinant CD22 indicate that the lectin function can be inactivated by expression of alpha2-6-linked Sia residues on the same cell surface. To explore whether this masking phenomenon affects native CD22 on B cells, we first developed a probe to detect the lectin activity of recombinant CD22 expressed on Chinese hamster ovary cells (which have no endogenous alpha2-6-linked Sia residues). This probe is inactive against CD22-positive B lymphoma cells and Epstein-Barr virus-transformed lymphoblasts which express high levels of alpha2-6-linked Sia residues. Enzymatic desialylation unmasks the CD22 lectin activity, indicating that endogenous Sia residues block the CD22 lectin-binding site. Truncation of the side chains of cell surface Sia residues by mild periodate oxidation (known to abrogate Sia recognition by CD22) also had this unmasking effect, indicating that the effects of desialylation are not due to a loss of negative charge. Normal resting B cells from human peripheral blood gave similar findings. However, the lectin is partially unmasked during in vitro activation of these cells. Thus, the lectin activity of CD22 is restricted by endogenous sialylation in resting B cells and may be transiently unmasked during in vivo activation, perhaps to modulate intercellular or intracellular interactions at this critical stage in the humoral response.

MeSH Terms
Animals Antigens, CD/genetics,metabolism Antigens, Differentiation, B-Lymphocyte/genetics,metabolism B-Lymphocytes/metabolism,virology Binding Sites CHO Cells Cell Adhesion Molecules/genetics,metabolism Cell Transformation, Viral Cricetinae Herpesvirus 4, Human Humans Lectins/metabolism N-Acetylneuraminic Acid/metabolism Recombinant Proteins/metabolism Sialic Acid Binding Ig-like Lectin 2
Chemicals
Antigens, CD Antigens, Differentiation, B-Lymphocyte CD22 protein, human Cell Adhesion Molecules Lectins Recombinant Proteins Sialic Acid Binding Ig-like Lectin 2 N-Acetylneuraminic Acid
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Razi N
Glycobiology Program, University of California, San Diego Cancer Center, Divisions of Hematology-Oncology and Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0687, USA.
Varki A
References (55)
55 references, click to expand
  1. 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
  2. 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
  3. CD22, a B cell-specific receptor, mediates adhesion and signal transduction.
    J Immunol. 1993 Jun 1;150(11):4715-8 PMID: 8496586
  4. 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
  5. Association of CD22 with the B cell antigen receptor.
    Eur J Immunol. 1993 Jun;23(6):1358-63 PMID: 7684686
  6. Sialyltransferase: a novel acute-phase reactant.
    Comp Biochem Physiol B. 1993 May;105(1):29-33 PMID: 7684961
  7. Structural study of the sugar chains of human leukocyte common antigen CD45.
    Biochemistry. 1993 Nov 30;32(47):12694-704 PMID: 8251489
  8. How B and T cells talk to each other.
    Nature. 1994 Feb 3;367(6462):425-8 PMID: 8107800
  9. Cytokine-induced beta-galactoside alpha-2,6-sialyltransferase in human endothelial cells mediates alpha 2,6-sialylation of adhesion molecules and CD22 ligands.
    J Biol Chem. 1994 Apr 8;269(14):10637-43 PMID: 8144653
  10. Sialylation of the B lymphocyte molecule CD22 by alpha 2,6-sialyltransferase is implicated in the regulation of CD22-mediated adhesion.
    J Biol Chem. 1994 Apr 22;269(16):11783-6 PMID: 8163475
  11. Differential expression of five sialyltransferase genes in human tissues.
    J Biol Chem. 1994 Jul 8;269(27):17872-8 PMID: 8027041
  12. 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):549-62 PMID: 8034751
  13. Sialoadhesin, a macrophage sialic acid binding receptor for haemopoietic cells with 17 immunoglobulin-like domains.
    EMBO J. 1994 Oct 3;13(19):4490-503 PMID: 7925291
  14. Integrin-mediated cell adhesion: the extracellular face.
    J Biol Chem. 1994 Oct 14;269(41):25235-8 PMID: 7929213
  15. Regulation of B cell:T cell interactions: potential involvement of an endogenous B cell sialidase.
    Immunol Invest. 1994 Nov;23(6-7):393-411 PMID: 7851958
  16. Modifications of cell surface sialic acids modulate cell adhesion mediated by sialoadhesin and CD22.
    Glycoconj J. 1994 Dec;11(6):576-85 PMID: 7696861
  17. Identification of the ligand-binding domains of CD22, a member of the immunoglobulin superfamily that uniquely binds a sialic acid-dependent ligand.
    J Exp Med. 1995 Apr 1;181(4):1581-6 PMID: 7535343
  18. Characterization of sialyloligosaccharide binding by recombinant soluble and native cell-associated CD22. Evidence for a minimal structural recognition motif and the potential importance of multisite binding.
    J Biol Chem. 1995 Mar 31;270(13):7523-32 PMID: 7706299
  19. CD22-mediated cell adhesion to cytokine-activated human endothelial cells. Positive and negative regulation by alpha 2-6-sialylation of cellular glycoproteins.
    J Biol Chem. 1995 Mar 31;270(13):7533-42 PMID: 7706300
  20. Binding of human plasma sialoglycoproteins by the B cell-specific lectin CD22. Selective recognition of immunoglobulin M and haptoglobin.
    J Biol Chem. 1995 Mar 31;270(13):7543-50 PMID: 7706301
  21. Characterization of CD33 as a new member of the sialoadhesin family of cellular interaction molecules.
    Blood. 1995 Apr 15;85(8):2005-12 PMID: 7718872
  22. Constitutive endocytosis and degradation of CD22 by human B cells.
    J Immunol. 1995 May 1;154(9):4466-75 PMID: 7722303
  23. Regulation of CD45 engagement by the B-cell receptor CD22.
    Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):4026-30 PMID: 7537381
  24. I-type lectins.
    J Biol Chem. 1995 Jun 16;270(24):14243-6 PMID: 7782275
  25. Phosphotyrosine-dependent association between CD22 and protein tyrosine phosphatase 1C.
    Eur J Immunol. 1995 Jun;25(6):1573-9 PMID: 7542197
  26. A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP.
    Science. 1995 Jul 14;269(5221):242-4 PMID: 7618087
  27. Hematopoietic cell phosphatase is recruited to CD22 following B cell antigen receptor ligation.
    J Biol Chem. 1995 Sep 1;270(35):20305-8 PMID: 7657601
  28. Ig domains 1 and 2 of murine CD22 constitute the ligand-binding domain and bind multiple sialylated ligands expressed on B and T cells.
    J Immunol. 1995 Oct 1;155(7):3368-76 PMID: 7561031
  29. The amino-terminal immunoglobulin-like domain of sialoadhesin contains the sialic acid binding site. Comparison with CD22.
    J Biol Chem. 1995 Nov 3;270(44):26184-91 PMID: 7592823
  30. CD22 associates with protein tyrosine phosphatase 1C, Syk, and phospholipase C-gamma(1) upon B cell activation.
    J Exp Med. 1996 Feb 1;183(2):547-60 PMID: 8627166
  31. Characterization of terminal sialic acid linkages on human thymocytes. Correlation between lectin-binding phenotype and sialyltransferase expression.
    J Biol Chem. 1996 May 3;271(18):10793-9 PMID: 8631891
  32. Transcription of the beta-galactoside alpha 2,6-sialyltransferase gene in B lymphocytes is directed by a separate and distinct promoter.
    Glycobiology. 1996 Apr;6(3):271-9 PMID: 8724135
  33. A single N-linked glycosylation site is implicated in the regulation of ligand recognition by the I-type lectins CD22 and CD33.
    J Biol Chem. 1996 Aug 2;271(31):18803-9 PMID: 8702538
  34. Hyperresponsive B cells in CD22-deficient mice.
    Science. 1996 Nov 1;274(5288):798-801 PMID: 8864124
  35. Carbohydrate recognition systems: functional triads in cell-cell interactions.
    Curr Opin Struct Biol. 1996 Oct;6(5):679-91 PMID: 8913692
  36. Sialic acid 9-O-acetylation on murine erythroleukemia cells affects complement activation, binding to I-type lectins, and tissue homing.
    J Biol Chem. 1996 Dec 6;271(49):31526-32 PMID: 8940168
  37. CD22 regulates thymus-independent responses and the lifespan of B cells.
    Nature. 1996 Dec 19-26;384(6610):634-7 PMID: 8967951
  38. The Sialoadhesins--a family of sialic acid-dependent cellular recognition molecules within the immunoglobulin superfamily.
    Glycoconj J. 1996 Dec;13(6):913-26 PMID: 8981082
  39. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice.
    Immunity. 1996 Dec;5(6):551-62 PMID: 8986715
  40. Sialic acid specificity of myelin-associated glycoprotein binding.
    J Biol Chem. 1997 Jan 10;272(2):1248-55 PMID: 8995428
  41. The role of CD40 ligand in costimulation and T-cell activation.
    Immunol Rev. 1996 Oct;153:85-106 PMID: 9010720
  42. CD22 is a negative regulator of B-cell receptor signalling.
    Curr Biol. 1997 Feb 1;7(2):133-43 PMID: 9016707
  43. Regulation of myelin-associated glycoprotein binding by sialylated cis-ligands.
    J Neurochem. 1997 Apr;68(4):1753-63 PMID: 9084450
  44. Distribution of lymphocyte subsets in bone marrow and peripheral blood is associated with haptoglobin type. Binding of haptoglobin to the B-cell lectin CD22.
    Eur J Clin Chem Clin Biochem. 1997 Mar;35(3):199-205 PMID: 9127741
  45. CD22, a B lymphocyte-specific adhesion molecule that regulates antigen receptor signaling.
    Annu Rev Immunol. 1997;15:481-504 PMID: 9143697
  46. Tuning antigen receptor signaling by CD22: integrating cues from antigens and the microenvironment.
    Immunity. 1997 May;6(5):509-17 PMID: 9175829
  47. Binding specificities of the sialoadhesin family of I-type lectins. Sialic acid linkage and substructure requirements for binding of myelin-associated glycoprotein, Schwann cell myelin protein, and sialoadhesin.
    J Biol Chem. 1997 Jul 4;272(27):16889-95 PMID: 9201997
  48. Cloning and characterization of a sialidase from the murine histocompatibility-2 complex: low levels of mRNA and a single amino acid mutation are responsible for reduced sialidase activity in mice carrying the Neu1a allele.
    Glycobiology. 1997 Oct;7(7):975-86 PMID: 9363440
  49. Siglecs: a family of sialic-acid binding lectins.
    Glycobiology. 1998 Feb;8(2):v PMID: 9498912
  50. Sialoadhesin, myelin-associated glycoprotein and CD22 define a new family of sialic acid-dependent adhesion molecules of the immunoglobulin superfamily.
    Curr Biol. 1994 Nov 1;4(11):965-72 PMID: 7533044
  51. Transcriptional regulation of the liver beta-galactoside alpha 2,6-sialyltransferase by glucocorticoids.
    J Biol Chem. 1990 Oct 15;265(29):17849-53 PMID: 2211665
  52. 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
  53. 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
  54. Human Golgi beta-galactoside alpha-2,6-sialyltransferase generates a group of sialylated B lymphocyte differentiation antigens.
    Eur J Immunol. 1992 Nov;22(11):2777-81 PMID: 1425905
  55. 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
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1998-06-23
Pages
7469-74
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC22653
Subset
IM
Grants
NIGMS NIH HHS · R01 GM032373 · United States
NIGMS NIH HHS · R37 GM032373 · United States
NIGMS NIH HHS · GM32373 · United States
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