Abstract
Phosphatidylinositol-specific phospholipase C (PIPLC) from Bacillus thuringiensis, which cleaves phosphatidylinositol or glycosylphosphatidylinositol on the external cell surface to generate a second messenger for intracellular signal transduction (S. Rahman et al., FEBS Lett. 303:193-196, 1992), was found to preferentially promote the generation of alloantigen-specific cytotoxic T lymphocytes in mixed leukocyte culture. PIPLC affected an early stage of cytotoxic T-lymphocyte activation in culture, and there was no evidence of any soluble cellular mediators of this PIPLC action. PIPLC neither enhanced overall cell proliferation nor noticeably promoted interleukin-2 and -4 production in mixed leukocyte culture. The relative population size of Ly-2+ T cells was increased, however, in a late mixed leukocyte culture with PIPLC. In addition, PIPLC enhanced an anti-CD3 monoclonal antibody-induced early increase in [Ca2+]i. These results suggest a new parasite (bacterium)-oriented mechanism for enhancing antigen-driven host cytotoxic T-lymphocyte immunity which does not include promotion of interleukin-2 production.
Full Text
The Full Text of this article is available as a PDF (201.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Diaz-Laviada I., Larrodera P., Nieto J. L., Cornet M. E., Diaz-Meco M. T., Sanchez M. J., Guddal P. H., Johansen T., Haro A., Moscat J. Mechanism of inhibition of adenylate cyclase by phospholipase C-catalyzed hydrolysis of phosphatidylcholine. Involvement of a pertussis toxin-sensitive G protein and protein kinase C. J Biol Chem. 1991 Jan 15;266(2):1170–1176. [PubMed] [Google Scholar]
- Doery H. M., Magnusson B. J., Gulasekharam J., Pearson J. E. The properties of phospholipase enzymes in staphylococcal toxins. J Gen Microbiol. 1965 Aug;40(2):283–296. doi: 10.1099/00221287-40-2-283. [DOI] [PubMed] [Google Scholar]
- Dustin M. L., Selvaraj P., Mattaliano R. J., Springer T. A. Anchoring mechanisms for LFA-3 cell adhesion glycoprotein at membrane surface. 1987 Oct 29-Nov 4Nature. 329(6142):846–848. doi: 10.1038/329846a0. [DOI] [PubMed] [Google Scholar]
- Farrar J. J., Benjamin W. R., Hilfiker M. L., Howard M., Farrar W. L., Fuller-Farrar J. The biochemistry, biology, and role of interleukin 2 in the induction of cytotoxic T cell and antibody-forming B cell responses. Immunol Rev. 1982;63:129–166. doi: 10.1111/j.1600-065x.1982.tb00414.x. [DOI] [PubMed] [Google Scholar]
- Ferguson M. A., Williams A. F. Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. Annu Rev Biochem. 1988;57:285–320. doi: 10.1146/annurev.bi.57.070188.001441. [DOI] [PubMed] [Google Scholar]
- Grammer S. F., Ishioka G. Y., Chesnut R. W. Studies on the capacity of B cells as well as T cells to serve as accessory cells for the activation of herpes simplex virus-specific cytolytic T cells. J Immunol. 1988 Mar 15;140(6):2016–2022. [PubMed] [Google Scholar]
- Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
- Ikezawa H., Nakabayashi T., Suzuki K., Nakajima M., Taguchi T., Taguchi R. Complete purification of phosphatidylinositol-specific phospholipase C from a strain of Bacillus thuringiensis. J Biochem. 1983 Jun;93(6):1717–1719. doi: 10.1093/oxfordjournals.jbchem.a134315. [DOI] [PubMed] [Google Scholar]
- Ikezawa H., Yamanegi M., Taguchi R., Miyashita T., Ohyabu T. Studies on phosphatidylinositol phosphodiesterase (phospholipase C type) of Bacillus cereus. I. purification, properties and phosphatase-releasing activity. Biochim Biophys Acta. 1976 Nov 19;450(2):154–164. [PubMed] [Google Scholar]
- Isobe K., Kollias G., Kolsto A. B., Grosveld F. T cell independent Thy-1 allo-antibody response with the use of transgenic mice. J Immunol. 1986 Oct 1;137(7):2089–2092. [PubMed] [Google Scholar]
- Isobe K., Nakashima I. Homotypic aggregation of murine T lymphocytes induced by anti-Thy-1 monoclonal antibodies. Immunology. 1991 Jun;73(2):159–164. [PMC free article] [PubMed] [Google Scholar]
- Jamshedur Rahman S. M., Pu M. V., Zhang Y. H., Hamaguchi M., Iwamoto T., Taguchi R., Ikezawa H., Isobe K., Yoshida T., Nakashima I. Delivery of an accessory signal for cell activation by exogenous phosphatidylinositol-specific phospholipase C. FEBS Lett. 1992 Jun 1;303(2-3):193–196. doi: 10.1016/0014-5793(92)80517-k. [DOI] [PubMed] [Google Scholar]
- Kido N., Nakashima I., Kato N. Correlation between strong adjuvanticity of Klebsiella O3 lipopolysaccharide and its ability to induce interleukin-1 secretion. Cell Immunol. 1984 May;85(2):477–486. doi: 10.1016/0008-8749(84)90260-0. [DOI] [PubMed] [Google Scholar]
- Leo O., Foo M., Sachs D. H., Samelson L. E., Bluestone J. A. Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1374–1378. doi: 10.1073/pnas.84.5.1374. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Low M. G., Kincade P. W. Phosphatidylinositol is the membrane-anchoring domain of the Thy-1 glycoprotein. Nature. 1985 Nov 7;318(6041):62–64. doi: 10.1038/318062a0. [DOI] [PubMed] [Google Scholar]
- Low M. G. The glycosyl-phosphatidylinositol anchor of membrane proteins. Biochim Biophys Acta. 1989 Dec 6;988(3):427–454. doi: 10.1016/0304-4157(89)90014-2. [DOI] [PubMed] [Google Scholar]
- Mengaud J., Braun-Breton C., Cossart P. Identification of phosphatidylinositol-specific phospholipase C activity in Listeria monocytogenes: a novel type of virulence factor? Mol Microbiol. 1991 Feb;5(2):367–372. doi: 10.1111/j.1365-2958.1991.tb02118.x. [DOI] [PubMed] [Google Scholar]
- Nagase F., Ueda K., Kawashima K., Jamshedur Rahman S. M., Isobe K., Yoshida T., Hasegawa Y., Ando K., Iwamoto T., Nagura E. Development of host-dependent high-grade tumor-specific immunity through a novel mechanism triggered by the Lyt-2+ tumor-specific T cell clone (K7L) that induces temporal growth of L1210 leukemia-K7L-variant. J Immunol. 1987 Apr 1;138(7):2359–2365. [PubMed] [Google Scholar]
- Nakashima I., Kato N. Non-specific stimulation of immunoglobulin synthesis in mice by capsular polysaccharide of Klebsiella pneumoniae. Immunology. 1974 Aug;27(2):179–193. [PMC free article] [PubMed] [Google Scholar]
- Nakashima I., Kobayashi T., Kato N. Alterations in the antibody response to bovine serum albumin by capsular polysaccharide of Klebsiella pneumoniae. J Immunol. 1971 Oct;107(4):1112–1121. [PubMed] [Google Scholar]
- Nakashima I., Mizoguchi K., Kato N., Nagase F., Isobe K., Saito M., Suzuki K. Control of primary IgM antibody responses to H-2 alloantigens by antigen-bearing live B lymphocytes. Eur J Immunol. 1982 Sep;12(9):713–719. doi: 10.1002/eji.1830120904. [DOI] [PubMed] [Google Scholar]
- Nakashima I., Nagase F., Matsuura A., Kato N. Adjuvant actions of polyclonal lymphocyte activators. II. Comparison and characterization of their actions in initiation and potentiation of immune responses to T-dependent and T-independent soluble antigens. Cell Immunol. 1980 Feb;49(2):360–371. doi: 10.1016/0008-8749(80)90037-4. [DOI] [PubMed] [Google Scholar]
- Nakashima I., Pu M. Y., Hamaguchi M., Iwamoto T., Rahman S. M., Zhang Y. H., Kato M., Ohkusu K., Katano Y., Yoshida T. Pathway of signal delivery to murine thymocytes triggered by co-crosslinking CD3 and Thy-1 for cellular DNA fragmentation and growth inhibition. J Immunol. 1993 Oct 1;151(7):3511–3520. [PubMed] [Google Scholar]
- Nakashima I., Yoshida T., Zhang Y. H., Pu M. Y., Taguchi R., Ikezawa H., Isobe K., Iwamoto T., Kato M., Lwin T. T cell maturation stage-linked heterogeneity of the glycosylphosphatidylinositol membrane anchor of Thy-1. Immunobiology. 1992 Sep;185(5):466–474. doi: 10.1016/s0171-2985(11)80088-4. [DOI] [PubMed] [Google Scholar]
- Nakashima I., Zhang Y. H., Rahman S. M., Yoshida T., Isobe K., Ding L. N., Iwamoto T., Hamaguchi M., Ikezawa H., Taguchi R. Evidence of synergy between Thy-1 and CD3/TCR complex in signal delivery to murine thymocytes for cell death. J Immunol. 1991 Aug 15;147(4):1153–1162. [PubMed] [Google Scholar]
- Ohta M., Nakashima I., Kato N. Adjuvant action of bacterial lipopolysaccharide in induction of delayed-type hypersensitivity to protein antigens. Cell Immunol. 1982 Jan 1;66(1):111–120. doi: 10.1016/0008-8749(82)90162-9. [DOI] [PubMed] [Google Scholar]
- Presky D. H., Low M. G., Shevach E. M. Role of phosphatidylinositol-anchored proteins in T cell activation. J Immunol. 1990 Feb 1;144(3):860–868. [PubMed] [Google Scholar]
- Rinchik E. M., Amos D. B. A mutation in a non-MHC murine cell surface antigen detectable by cytotoxic T lymphocytes. J Immunol. 1986 Mar 15;136(6):1992–1998. [PubMed] [Google Scholar]
- Robinson P. J., Millrain M., Antoniou J., Simpson E., Mellor A. L. A glycophospholipid anchor is required for Qa-2-mediated T cell activation. Nature. 1989 Nov 2;342(6245):85–87. doi: 10.1038/342085a0. [DOI] [PubMed] [Google Scholar]
- Robinson P. J. Phosphatidylinositol membrane anchors and T-cell activation. Immunol Today. 1991 Jan;12(1):35–41. doi: 10.1016/0167-5699(91)90110-F. [DOI] [PubMed] [Google Scholar]
- Rock K. L., Yeh E. T., Gramm C. F., Haber S. I., Reiser H., Benacerraf B. TAP, a novel T cell-activating protein involved in the stimulation of MHC-restricted T lymphocytes. J Exp Med. 1986 Feb 1;163(2):315–333. doi: 10.1084/jem.163.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rozengurt E., Rodriguez-Pena M., Smith K. A. Phorbol esters, phospholipase C, and growth factors rapidly stimulate the phosphorylation of a Mr 80,000 protein in intact quiescent 3T3 cells. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7244–7248. doi: 10.1073/pnas.80.23.7244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stiernberg J., Low M. G., Flaherty L., Kincade P. W. Removal of lymphocyte surface molecules with phosphatidylinositol-specific phospholipase C: effects on mitogen responses and evidence that ThB and certain Qa antigens are membrane-anchored via phosphatidylinositol. J Immunol. 1987 Jun 1;138(11):3877–3884. [PubMed] [Google Scholar]
- Taguchi R., Asahi Y., Ikezawa H. Purification and properties of phosphatidylinositol-specific phospholipase C of Bacillus thuringiensis. Biochim Biophys Acta. 1980 Jul 14;619(1):48–57. [PubMed] [Google Scholar]
- Taguchi R., Ikezawa H. Phosphatidyl inositol-specific phospholipase C from Clostridium novyi type A. Arch Biochem Biophys. 1978 Feb;186(1):196–201. doi: 10.1016/0003-9861(78)90480-0. [DOI] [PubMed] [Google Scholar]
- Zhang Y. H., Isobe K., Nagase F., Lwin T., Kato M., Hamaguchi M., Yokochi T., Nakashima I. Glycyrrhizin as a promoter of the late signal transduction for interleukin-2 production by splenic lymphocytes. Immunology. 1993 Aug;79(4):528–534. [PMC free article] [PubMed] [Google Scholar]
