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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Nov 1;89(21):10242–10246. doi: 10.1073/pnas.89.21.10242

CD22-mediated stimulation of T cells regulates T-cell receptor/CD3-induced signaling.

A Aruffo 1, S B Kanner 1, D Sgroi 1, J A Ledbetter 1, I Stamenkovic 1
PMCID: PMC50314  PMID: 1438211

Abstract

Interaction between B lymphocytes and other cell types is mediated in part by the B-cell adhesion molecule CD22. Recent work has suggested one of the T-cell ligands of B cells to be CD45RO, an isoform of the receptor-linked phosphotyrosine phosphatase CD45. Here we demonstrate direct interaction between CD22 and several isoforms of CD45, including CD45RO, and propose that the interaction may participate in regulation of lymphocyte signaling. Cross-linking of CD3 and CD22 T-cell ligands with anti-CD3 antibody and soluble CD22 is shown to block anti-CD3-induced intracellular calcium increase and to inhibit tyrosine phosphorylation of phospholipase C gamma 1. These effects are consistent with those observed upon coligation of CD3 and CD45 with antibody, providing support to the possibility that ligand-mediated stimulation of CD45 may result in modulation of substrate phosphorylation and lymphocyte activation.

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Selected References

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  1. Akbar A. N., Terry L., Timms A., Beverley P. C., Janossy G. Loss of CD45R and gain of UCHL1 reactivity is a feature of primed T cells. J Immunol. 1988 Apr 1;140(7):2171–2178. [PubMed] [Google Scholar]
  2. Aruffo A., Kolanus W., Walz G., Fredman P., Seed B. CD62/P-selectin recognition of myeloid and tumor cell sulfatides. Cell. 1991 Oct 4;67(1):35–44. doi: 10.1016/0092-8674(91)90570-o. [DOI] [PubMed] [Google Scholar]
  3. Aruffo A., Stamenkovic I., Melnick M., Underhill C. B., Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell. 1990 Jun 29;61(7):1303–1313. doi: 10.1016/0092-8674(90)90694-a. [DOI] [PubMed] [Google Scholar]
  4. Bartlett W. C., McCann J., Shepherd D. M., Roy M., Noelle R. J. Cognate interactions between helper T cells and B cells. IV. Requirements for the expression of effector phase activity by helper T cells. J Immunol. 1990 Dec 15;145(12):3956–3962. [PubMed] [Google Scholar]
  5. Cantley L. C., Auger K. R., Carpenter C., Duckworth B., Graziani A., Kapeller R., Soltoff S. Oncogenes and signal transduction. Cell. 1991 Jan 25;64(2):281–302. doi: 10.1016/0092-8674(91)90639-g. [DOI] [PubMed] [Google Scholar]
  6. Cantrell D. A., Davies A. A., Crumpton M. J. Activators of protein kinase C down-regulate and phosphorylate the T3/T-cell antigen receptor complex of human T lymphocytes. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8158–8162. doi: 10.1073/pnas.82.23.8158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Charbonneau H., Tonks N. K., Walsh K. A., Fischer E. H. The leukocyte common antigen (CD45): a putative receptor-linked protein tyrosine phosphatase. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7182–7186. doi: 10.1073/pnas.85.19.7182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clark E. A., Ledbetter J. A. Leukocyte cell surface enzymology: CD45 (LCA, T200) is a protein tyrosine phosphatase. Immunol Today. 1989 Jul;10(7):225–228. doi: 10.1016/0167-5699(89)90257-0. [DOI] [PubMed] [Google Scholar]
  9. Downward J., Graves J. D., Warne P. H., Rayter S., Cantrell D. A. Stimulation of p21ras upon T-cell activation. Nature. 1990 Aug 23;346(6286):719–723. doi: 10.1038/346719a0. [DOI] [PubMed] [Google Scholar]
  10. Fischer E. H., Charbonneau H., Tonks N. K. Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes. Science. 1991 Jul 26;253(5018):401–406. doi: 10.1126/science.1650499. [DOI] [PubMed] [Google Scholar]
  11. Granja C., Lin L. L., Yunis E. J., Relias V., Dasgupta J. D. PLC gamma 1, a possible mediator of T cell receptor function. J Biol Chem. 1991 Sep 5;266(25):16277–16280. [PubMed] [Google Scholar]
  12. Hoffman S., Edelman G. M. Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5762–5766. doi: 10.1073/pnas.80.18.5762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kanner S. B., Damle N. K., Blake J., Aruffo A., Ledbetter J. A. CD2/LFA-3 ligation induces phospholipase-C gamma 1 tyrosine phosphorylation and regulates CD3 signaling. J Immunol. 1992 Apr 1;148(7):2023–2029. [PubMed] [Google Scholar]
  14. Kanner S. B., Deans J. P., Ledbetter J. A. Regulation of CD3-induced phospholipase C-gamma 1 (PLC gamma 1) tyrosine phosphorylation by CD4 and CD45 receptors. Immunology. 1992 Mar;75(3):441–447. [PMC free article] [PubMed] [Google Scholar]
  15. Kanner S. B., Kavanagh T. J., Grossmann A., Hu S. L., Bolen J. B., Rabinovitch P. S., Ledbetter J. A. Sulfhydryl oxidation down-regulates T-cell signaling and inhibits tyrosine phosphorylation of phospholipase C gamma 1. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):300–304. doi: 10.1073/pnas.89.1.300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kanner S. B., Reynolds A. B., Parsons J. T. Tyrosine phosphorylation of a 120-kilodalton pp60src substrate upon epidermal growth factor and platelet-derived growth factor receptor stimulation and in polyomavirus middle-T-antigen-transformed cells. Mol Cell Biol. 1991 Feb;11(2):713–720. doi: 10.1128/mcb.11.2.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Koretzky G. A., Picus J., Thomas M. L., Weiss A. Tyrosine phosphatase CD45 is essential for coupling T-cell antigen receptor to the phosphatidyl inositol pathway. Nature. 1990 Jul 5;346(6279):66–68. doi: 10.1038/346066a0. [DOI] [PubMed] [Google Scholar]
  18. Kupfer A., Singer S. J. Cell biology of cytotoxic and helper T cell functions: immunofluorescence microscopic studies of single cells and cell couples. Annu Rev Immunol. 1989;7:309–337. doi: 10.1146/annurev.iy.07.040189.001521. [DOI] [PubMed] [Google Scholar]
  19. Kupfer A., Swain S. L., Janeway C. A., Jr, Singer S. J. The specific direct interaction of helper T cells and antigen-presenting B cells. Proc Natl Acad Sci U S A. 1986 Aug;83(16):6080–6083. doi: 10.1073/pnas.83.16.6080. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Künemund V., Jungalwala F. B., Fischer G., Chou D. K., Keilhauer G., Schachner M. The L2/HNK-1 carbohydrate of neural cell adhesion molecules is involved in cell interactions. J Cell Biol. 1988 Jan;106(1):213–223. doi: 10.1083/jcb.106.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lai C., Brow M. A., Nave K. A., Noronha A. B., Quarles R. H., Bloom F. E., Milner R. J., Sutcliffe J. G. Two forms of 1B236/myelin-associated glycoprotein, a cell adhesion molecule for postnatal neural development, are produced by alternative splicing. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4337–4341. doi: 10.1073/pnas.84.12.4337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ledbetter J. A., Gilliland L. K., Schieven G. L. The interaction of CD4 with CD3/Ti regulates tyrosine phosphorylation of substrates during T cell activation. Semin Immunol. 1990 Mar;2(2):99–106. [PubMed] [Google Scholar]
  23. Ledbetter J. A., Rose L. M., Spooner C. E., Beatty P. G., Martin P. J., Clark E. A. Antibodies to common leukocyte antigen p220 influence human T cell proliferation by modifying IL 2 receptor expression. J Immunol. 1985 Sep;135(3):1819–1825. [PubMed] [Google Scholar]
  24. Ledbetter J. A., Schieven G. L., Uckun F. M., Imboden J. B. CD45 cross-linking regulates phospholipase C activation and tyrosine phosphorylation of specific substrates in CD3/Ti-stimulated T cells. J Immunol. 1991 Mar 1;146(5):1577–1583. [PubMed] [Google Scholar]
  25. Linsley P. S., Brady W., Urnes M., Grosmaire L. S., Damle N. K., Ledbetter J. A. CTLA-4 is a second receptor for the B cell activation antigen B7. J Exp Med. 1991 Sep 1;174(3):561–569. doi: 10.1084/jem.174.3.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Linsley P. S., Clark E. A., Ledbetter J. A. T-cell antigen CD28 mediates adhesion with B cells by interacting with activation antigen B7/BB-1. Proc Natl Acad Sci U S A. 1990 Jul;87(13):5031–5035. doi: 10.1073/pnas.87.13.5031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ostergaard H. L., Shackelford D. A., Hurley T. R., Johnson P., Hyman R., Sefton B. M., Trowbridge I. S. Expression of CD45 alters phosphorylation of the lck-encoded tyrosine protein kinase in murine lymphoma T-cell lines. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8959–8963. doi: 10.1073/pnas.86.22.8959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Park D. J., Rho H. W., Rhee S. G. CD3 stimulation causes phosphorylation of phospholipase C-gamma 1 on serine and tyrosine residues in a human T-cell line. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5453–5456. doi: 10.1073/pnas.88.12.5453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pingel J. T., Thomas M. L. Evidence that the leukocyte-common antigen is required for antigen-induced T lymphocyte proliferation. Cell. 1989 Sep 22;58(6):1055–1065. doi: 10.1016/0092-8674(89)90504-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pulido R., Sánchez-Madrid F. Biochemical nature and topographic localization of epitopes defining four distinct CD45 antigen specificities. Conventional CD45, CD45R, 180 kDa (UCHL1) and 220/205/190 kDa. J Immunol. 1989 Sep 15;143(6):1930–1936. [PubMed] [Google Scholar]
  31. Rabinovitch P. S., June C. H., Grossmann A., Ledbetter J. A. Heterogeneity among T cells in intracellular free calcium responses after mitogen stimulation with PHA or anti-CD3. Simultaneous use of indo-1 and immunofluorescence with flow cytometry. J Immunol. 1986 Aug 1;137(3):952–961. [PubMed] [Google Scholar]
  32. Reuter G., Schauer R., Szeiki C., Kamerling J. P., Vliegenthart J. F. A detailed study of the periodate oxidation of sialic acids in glycoproteins. Glycoconj J. 1989;6(1):35–44. doi: 10.1007/BF01047888. [DOI] [PubMed] [Google Scholar]
  33. Sanders V. M., Snyder J. M., Uhr J. W., Vitetta E. S. Characterization of the physical interaction between antigen-specific B and T cells. J Immunol. 1986 Oct 15;137(8):2395–2404. [PubMed] [Google Scholar]
  34. Secrist J. P., Karnitz L., Abraham R. T. T-cell antigen receptor ligation induces tyrosine phosphorylation of phospholipase C-gamma 1. J Biol Chem. 1991 Jul 5;266(19):12135–12139. [PubMed] [Google Scholar]
  35. Siegel J. N., Klausner R. D., Rapp U. R., Samelson L. E. T cell antigen receptor engagement stimulates c-raf phosphorylation and induces c-raf-associated kinase activity via a protein kinase C-dependent pathway. J Biol Chem. 1990 Oct 25;265(30):18472–18480. [PubMed] [Google Scholar]
  36. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  37. Stamenkovic I., Seed B. The B-cell antigen CD22 mediates monocyte and erythrocyte adhesion. Nature. 1990 May 3;345(6270):74–77. doi: 10.1038/345074a0. [DOI] [PubMed] [Google Scholar]
  38. Stamenkovic I., Sgroi D., Aruffo A. CD22 binds to alpha-2,6-sialyltransferase-dependent epitopes on COS cells. Cell. 1992 Mar 20;68(6):1003–1004. doi: 10.1016/0092-8674(92)90071-j. [DOI] [PubMed] [Google Scholar]
  39. Stamenkovic I., Sgroi D., Aruffo A., Sy M. S., Anderson T. 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):1133–1144. doi: 10.1016/0092-8674(91)90036-x. [DOI] [PubMed] [Google Scholar]
  40. Streuli M., Hall L. R., Saga Y., Schlossman S. F., Saito H. Differential usage of three exons generates at least five different mRNAs encoding human leukocyte common antigens. J Exp Med. 1987 Nov 1;166(5):1548–1566. doi: 10.1084/jem.166.5.1548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Terry L. A., Brown M. H., Beverley P. C. The monoclonal antibody, UCHL1, recognizes a 180,000 MW component of the human leucocyte-common antigen, CD45. Immunology. 1988 Jun;64(2):331–336. [PMC free article] [PubMed] [Google Scholar]
  42. Thomas M. L. The leukocyte common antigen family. Annu Rev Immunol. 1989;7:339–369. doi: 10.1146/annurev.iy.07.040189.002011. [DOI] [PubMed] [Google Scholar]
  43. Tonks N. K., Charbonneau H., Diltz C. D., Fischer E. H., Walsh K. A. Demonstration that the leukocyte common antigen CD45 is a protein tyrosine phosphatase. Biochemistry. 1988 Nov 29;27(24):8695–8701. doi: 10.1021/bi00424a001. [DOI] [PubMed] [Google Scholar]
  44. Trowbridge I. S. CD45. A prototype for transmembrane protein tyrosine phosphatases. J Biol Chem. 1991 Dec 15;266(35):23517–23520. [PubMed] [Google Scholar]
  45. Van de Velde H., von Hoegen I., Luo W., Parnes J. R., Thielemans K. The B-cell surface protein CD72/Lyb-2 is the ligand for CD5. Nature. 1991 Jun 20;351(6328):662–665. doi: 10.1038/351662a0. [DOI] [PubMed] [Google Scholar]
  46. Weiss A., Koretzky G., Schatzman R. C., Kadlecek T. Functional activation of the T-cell antigen receptor induces tyrosine phosphorylation of phospholipase C-gamma 1. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5484–5488. doi: 10.1073/pnas.88.13.5484. [DOI] [PMC free article] [PubMed] [Google Scholar]

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