Abstract
Exposure to oxidants such as hydrogen peroxide (H2O2) and gamma-ray irradiation has been recently shown to trigger tyrosine phosphorylation in B cells as does cross-linking surface immunoglobulin (sIg) by antigens or anti-immunoglobulins. We studied the mechanism by which H2O2 induced tyrosine phosphorylation in B cells and compared it with the mechanism utilized by sIg. Both anti-immunoglobulin M (anti-IgM) and H2O2 induced tyrosine phosphorylation through protein tyrosine kinase (PTK) activation. However, the tyrosine phosphorylation caused by H2O2 but not that induced by anti-IgM, was modulated by agents affecting cellular thiols and glutathione contents including dithiothreitol, 2-mercaptoethanol, and buthionine sulphoximine. Moreover, the tyrosine phosphorylation caused by the oxidant but not that induced by anti-IgM was markedly augmented by two inflammatory cytokines, tumour necrosis factor-alpha and interleukin-1 alpha, although these agents by themselves did not stimulate PTK activity nor induce tyrosine phosphorylation. These findings demonstrate that oxidative stress but not surface IgM (sIgM) ligation triggers tyrosine phosphorylation through a mechanism that is sensitive to cellular thiols and these inflammatory cytokines.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bauskin A. R., Alkalay I., Ben-Neriah Y. Redox regulation of a protein tyrosine kinase in the endoplasmic reticulum. Cell. 1991 Aug 23;66(4):685–696. doi: 10.1016/0092-8674(91)90114-e. [DOI] [PubMed] [Google Scholar]
- Bernier M., Laird D. M., Lane M. D. Insulin-activated tyrosine phosphorylation of a 15-kilodalton protein in intact 3T3-L1 adipocytes. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1844–1848. doi: 10.1073/pnas.84.7.1844. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burkhardt A. L., Brunswick M., Bolen J. B., Mond J. J. Anti-immunoglobulin stimulation of B lymphocytes activates src-related protein-tyrosine kinases. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7410–7414. doi: 10.1073/pnas.88.16.7410. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gold M. R., Matsuuchi L., Kelly R. B., DeFranco A. L. Tyrosine phosphorylation of components of the B-cell antigen receptors following receptor crosslinking. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3436–3440. doi: 10.1073/pnas.88.8.3436. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Griffith O. W. Depletion of glutathione by inhibition of biosynthesis. Methods Enzymol. 1981;77:59–63. doi: 10.1016/s0076-6879(81)77011-3. [DOI] [PubMed] [Google Scholar]
- Guy G. R., Cairns J., Ng S. B., Tan Y. H. Inactivation of a redox-sensitive protein phosphatase during the early events of tumor necrosis factor/interleukin-1 signal transduction. J Biol Chem. 1993 Jan 25;268(3):2141–2148. [PubMed] [Google Scholar]
- Hutchcroft J. E., Harrison M. L., Geahlen R. L. Association of the 72-kDa protein-tyrosine kinase PTK72 with the B cell antigen receptor. J Biol Chem. 1992 Apr 25;267(12):8613–8619. [PubMed] [Google Scholar]
- Hutchcroft J. E., Harrison M. L., Geahlen R. L. B lymphocyte activation is accompanied by phosphorylation of a 72-kDa protein-tyrosine kinase. J Biol Chem. 1991 Aug 15;266(23):14846–14849. [PubMed] [Google Scholar]
- Kharbanda S., Yuan Z. M., Rubin E., Weichselbaum R., Kufe D. Activation of Src-like p56/p53lyn tyrosine kinase by ionizing radiation. J Biol Chem. 1994 Aug 12;269(32):20739–20743. [PubMed] [Google Scholar]
- Kärenlampi S. O., Eisen H. J., Hankinson O., Nebert D. W. Effects of cytochrome P1-450 inducers on the cell-surface receptors for epidermal growth factor, phorbol 12,13-dibutyrate, or insulin of cultured mouse hepatoma cells. J Biol Chem. 1983 Sep 10;258(17):10378–10383. [PubMed] [Google Scholar]
- 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]
- Lander H. M., Levine D. M., Novogrodsky A. Stress stimuli-induced lymphocyte activation. Cell Immunol. 1992 Nov;145(1):146–155. doi: 10.1016/0008-8749(92)90319-k. [DOI] [PubMed] [Google Scholar]
- Law D. A., Gold M. R., DeFranco A. L. Examination of B lymphoid cell lines for membrane immunoglobulin-stimulated tyrosine phosphorylation and src-family tyrosine kinase mRNA expression. Mol Immunol. 1992 Jul-Aug;29(7-8):917–926. doi: 10.1016/0161-5890(92)90130-p. [DOI] [PubMed] [Google Scholar]
- Nakamura K., Hori T., Sato N., Sugie K., Kawakami T., Yodoi J. Redox regulation of a src family protein tyrosine kinase p56lck in T cells. Oncogene. 1993 Nov;8(11):3133–3139. [PubMed] [Google Scholar]
- Oetken C., von Willebrand M., Autero M., Ruutu T., Andersson L. C., Mustelin T. Phenylarsine oxide augments tyrosine phosphorylation in hematopoietic cells. Eur J Haematol. 1992 Oct;49(4):208–214. doi: 10.1111/j.1600-0609.1992.tb00048.x. [DOI] [PubMed] [Google Scholar]
- Schick M. R., Levy S. The TAPA-1 molecule is associated on the surface of B cells with HLA-DR molecules. J Immunol. 1993 Oct 15;151(8):4090–4097. [PubMed] [Google Scholar]
- Schick M. R., Nguyen V. Q., Levy S. Anti-TAPA-1 antibodies induce protein tyrosine phosphorylation that is prevented by increasing intracellular thiol levels. J Immunol. 1993 Aug 15;151(4):1918–1925. [PubMed] [Google Scholar]
- Schieven G. L., Kirihara J. M., Burg D. L., Geahlen R. L., Ledbetter J. A. p72syk tyrosine kinase is activated by oxidizing conditions that induce lymphocyte tyrosine phosphorylation and Ca2+ signals. J Biol Chem. 1993 Aug 5;268(22):16688–16692. [PubMed] [Google Scholar]
- Schieven G. L., Kirihara J. M., Myers D. E., Ledbetter J. A., Uckun F. M. Reactive oxygen intermediates activate NF-kappa B in a tyrosine kinase-dependent mechanism and in combination with vanadate activate the p56lck and p59fyn tyrosine kinases in human lymphocytes. Blood. 1993 Aug 15;82(4):1212–1220. [PubMed] [Google Scholar]
- Schieven G. L., Mittler R. S., Nadler S. G., Kirihara J. M., Bolen J. B., Kanner S. B., Ledbetter J. A. ZAP-70 tyrosine kinase, CD45, and T cell receptor involvement in UV- and H2O2-induced T cell signal transduction. J Biol Chem. 1994 Aug 12;269(32):20718–20726. [PubMed] [Google Scholar]
- Staal F. J., Anderson M. T., Staal G. E., Herzenberg L. A., Gitler C., Herzenberg L. A. Redox regulation of signal transduction: tyrosine phosphorylation and calcium influx. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3619–3622. doi: 10.1073/pnas.91.9.3619. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamanashi Y., Kakiuchi T., Mizuguchi J., Yamamoto T., Toyoshima K. Association of B cell antigen receptor with protein tyrosine kinase Lyn. Science. 1991 Jan 11;251(4990):192–194. doi: 10.1126/science.1702903. [DOI] [PubMed] [Google Scholar]