Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1990 Sep;58(9):2745–2749. doi: 10.1128/iai.58.9.2745-2749.1990

Stimulatory effect of staphylococcal leukocidin on phosphoinositide metabolism in rabbit polymorphonuclear leukocytes.

X Wang 1, M Noda 1, I Kato 1
PMCID: PMC313562  PMID: 2167292

Abstract

When rabbit polymorphonuclear leukocytes (PMNs) were incubated with staphylococcal leukocidin (F and S components) in the presence of 32Pi at 37 degrees C, incorporation of 32Pi into phosphatidylinositol 4-phosphate (PIP) and phosphatidylinositol 4,5-bisphosphate (PIP2) occurred after a lag phase of 10 s and reached a maximal level at 60 s of 50- and 30-fold increase, respectively, compared with that of the control in the absence of the toxin. Whereas the amount of 32P radioactivity incorporated in PIP and PIP2 decreased to control levels in a few minutes, 32P incorporation into phosphatidic acid (PA) continuously increased over 3 min. These findings suggested an early activation of phosphoinositide-specific phospholipase C in rabbit PMNs by leukocidin as shown by the rapid breakdown of PIP and PIP2 accompanied by the appearance of PA. The stimulatory effect of leukocidin on some enzymatic activities of the phosphatidylinositol pathway was further investigated by using PMN cell membrane preparations. In the presence of both the F and S components, enhanced 32P incorporation was observed not only in PIP2 and PA but also in PIP. While the F component mainly enhanced 32P incorporation into PIP2 and PA, the S component alone had no effect on 32P incorporation into PIP, PIP2, and PA. The F component alone enhanced conversion of PIP to [32P]PIP2 in the presence of unlabeled PIP and [gamma-32P]ATP, through the activation of PIP kinase. PIP kinase activity was potentiated by the addition of NAD and GTP. Subsequent formation of [32P]PA was also enhanced by the F component, resulting from activation of the phosphoinositide-specific phospholipase C. These results suggested that the F component of staphylococcal leukocidin is responsible for the enhancement of phosphoinositide metabolism in rabbit PMN cell membranes.

Full text

PDF
2745

Images in this article

2747Image
on p.2747
2748Image
on p.2748

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Banga H. S., Walker R. K., Winberry L. K., Rittenhouse S. E. Platelet adenylate cyclase and phospholipase C are affected differentially by ADP-ribosylation. Effects on thrombin-mediated responses. Biochem J. 1988 May 15;252(1):297–300. doi: 10.1042/bj2520297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Gilman A. G. G proteins and dual control of adenylate cyclase. Cell. 1984 Mar;36(3):577–579. doi: 10.1016/0092-8674(84)90336-2. [DOI] [PubMed] [Google Scholar]
  3. Gilman A. G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem. 1987;56:615–649. doi: 10.1146/annurev.bi.56.070187.003151. [DOI] [PubMed] [Google Scholar]
  4. Graber R., Losa G. A. Subcellular localization and kinetic properties of phosphatidylinositol 4,5-bisphosphate phospholipase C and inositol phosphate enzymes from human peripheral blood mononuclear cells. Enzyme. 1989;41(1):17–26. doi: 10.1159/000469046. [DOI] [PubMed] [Google Scholar]
  5. Jolles J., Schrama L. H., Gispen W. H. Calcium-dependent turnover of brain polyphosphoinositides in vitro after prelabelling in vivo. Biochim Biophys Acta. 1981 Oct 23;666(1):90–98. doi: 10.1016/0005-2760(81)90094-1. [DOI] [PubMed] [Google Scholar]
  6. Katada T., Ui M. Direct modification of the membrane adenylate cyclase system by islet-activating protein due to ADP-ribosylation of a membrane protein. Proc Natl Acad Sci U S A. 1982 May;79(10):3129–3133. doi: 10.1073/pnas.79.10.3129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kato I., Noda M. ADP-ribosylation of cell membrane proteins by staphylococcal alpha-toxin and leukocidin in rabbit erythrocytes and polymorphonuclear leukocytes. FEBS Lett. 1989 Sep 11;255(1):59–62. doi: 10.1016/0014-5793(89)81060-9. [DOI] [PubMed] [Google Scholar]
  8. Limor R., Schvartz I., Hazum E., Ayalon D., Naor Z. Effect of guanine nucleotides on phospholipase C activity in permeabilized pituitary cells: possible involvement of an inhibitory GTP-binding protein. Biochem Biophys Res Commun. 1989 Feb 28;159(1):209–215. doi: 10.1016/0006-291x(89)92424-8. [DOI] [PubMed] [Google Scholar]
  9. Matsuoka I., Syoto B., Kurihara K., Kubo S., Syuto B. ADP-ribosylation of specific membrane proteins in pheochromocytoma and primary-cultured brain cells by botulinum neurotoxins type C and D. FEBS Lett. 1987 Jun 1;216(2):295–299. doi: 10.1016/0014-5793(87)80709-3. [DOI] [PubMed] [Google Scholar]
  10. Michell R. H. Polyphosphoinositide breakdown as the initiating reaction in receptor-stimulated inositol phospholipid metabolism. Life Sci. 1983 May 2;32(18):2083–2085. doi: 10.1016/0024-3205(83)90095-4. [DOI] [PubMed] [Google Scholar]
  11. Nishizuka Y. Turnover of inositol phospholipids and signal transduction. Science. 1984 Sep 21;225(4668):1365–1370. doi: 10.1126/science.6147898. [DOI] [PubMed] [Google Scholar]
  12. Noda M., Hirayama T., Kato I., Matsuda F. Crystallization and properties of staphylococcal leukocidin. Biochim Biophys Acta. 1980 Nov 17;633(1):33–44. doi: 10.1016/0304-4165(80)90035-5. [DOI] [PubMed] [Google Scholar]
  13. Noda M., Hirayama T., Matsuda F., Kato I. An early effect of the S component of staphylococcal leukocidin on methylation of phospholipid in various leukocytes. Infect Immun. 1985 Oct;50(1):142–145. doi: 10.1128/iai.50.1.142-145.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Noda M., Kato I., Hirayama T., Matsuda F. Fixation and inactivation of staphylococcal leukocidin by phosphatidylcholine and ganglioside GM1 in rabbit polymorphonuclear leukocytes. Infect Immun. 1980 Aug;29(2):678–684. doi: 10.1128/iai.29.2.678-684.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Noda M., Kato I., Hirayama T., Matsuda F. Mode of action of staphylococcal leukocidin: effects of the S and F components on the activities of membrane-associated enzymes of rabbit polymorphonuclear leukocytes. Infect Immun. 1982 Jan;35(1):38–45. doi: 10.1128/iai.35.1.38-45.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ohta H., Okajima F., Ui M. Inhibition by islet-activating protein of a chemotactic peptide-induced early breakdown of inositol phospholipids and Ca2+ mobilization in guinea pig neutrophils. J Biol Chem. 1985 Dec 15;260(29):15771–15780. [PubMed] [Google Scholar]
  17. Pretlow T. G., 2nd, Luberoff D. E. A new method for separating lymphocytes and granulocytes from human peripheral blood using programmed gradient sedimentation in an isokinetic gradient. Immunology. 1973 Jan;24(1):85–92. [PMC free article] [PubMed] [Google Scholar]
  18. Schwertz D. W., Halverson J. Characterization of phospholipase C-mediated polyphosphoinositide hydrolysis in rat heart ventricles. Arch Biochem Biophys. 1989 Feb 15;269(1):137–147. doi: 10.1016/0003-9861(89)90094-5. [DOI] [PubMed] [Google Scholar]
  19. Smith C. D., Chang K. J. Regulation of brain phosphatidylinositol-4-phosphate kinase by GTP analogues. A potential role for guanine nucleotide regulatory proteins. J Biol Chem. 1989 Feb 25;264(6):3206–3210. [PubMed] [Google Scholar]
  20. Smith C. D., Cox C. C., Snyderman R. Receptor-coupled activation of phosphoinositide-specific phospholipase C by an N protein. Science. 1986 Apr 4;232(4746):97–100. doi: 10.1126/science.3006254. [DOI] [PubMed] [Google Scholar]
  21. Urumow T., Wieland O. H. Stimulation of phosphatidylinositol 4-phosphate phosphorylation in human placenta membranes by GTP gamma S. FEBS Lett. 1986 Oct 27;207(2):253–257. doi: 10.1016/0014-5793(86)81499-5. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES