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. 1992 Aug;60(8):3452–3455. doi: 10.1128/iai.60.8.3452-3455.1992

Infection of macrophages with Legionella pneumophila induces phosphorylation of a 76-kilodalton protein.

Y Yamamoto 1, T W Klein 1, H Shinomiya 1, M Nakano 1, H Friedman 1
PMCID: PMC257337  PMID: 1639515

Abstract

Infection of peritoneal macrophages from susceptible A/J mice with Legionella pneumophila induced phosphorylation of a 76-kDa protein. The phosphorylation occurred when macrophages were infected with a virulent strain of L. pneumophila but did not occur when they were infected with an avirulent strain or with other bacteria such as either Pseudomonas aeruginosa or Salmonella typhimurium. Also, no phosphorylation of this protein was observed when macrophages were stimulated with either lipopolysaccharide or phorbol myristate acetate. However, phosphorylation did occur in macrophages infected with a virulent strain of L. pneumophila and treated with either erythromycin to inhibit growth or with cytochalasin D to inhibit uptake of L. pneumophila by macrophages. These results support the view that phosphorylation of this protein occurs during the early phases of interaction between L. pneumophila and macrophages. The role of this specific protein in the recognition, intracellular uptake, and growth of L. pneumophila in permissive macrophages remains to be clarified.

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Selected References

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

  1. Baldwin T. J., Brooks S. F., Knutton S., Manjarrez Hernandez H. A., Aitken A., Williams P. H. Protein phosphorylation by protein kinase C in HEp-2 cells infected with enteropathogenic Escherichia coli. Infect Immun. 1990 Mar;58(3):761–765. doi: 10.1128/iai.58.3.761-765.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bangsborg J. M., Cianciotto N. P., Hindersson P. Nucleotide sequence analysis of the Legionella micdadei mip gene, encoding a 30-kilodalton analog of the Legionella pneumophila Mip protein. Infect Immun. 1991 Oct;59(10):3836–3840. doi: 10.1128/iai.59.10.3836-3840.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Catrenich C. E., Johnson W. Virulence conversion of Legionella pneumophila: a one-way phenomenon. Infect Immun. 1988 Dec;56(12):3121–3125. doi: 10.1128/iai.56.12.3121-3125.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chaplin D. D., Wedner H. J., Parker C. W. Protein phosphorylation in human peripheral blood lymphocytes: mitogen-induced increases in protein phosphorylation in intact lymphocytes. J Immunol. 1980 May;124(5):2390–2398. [PubMed] [Google Scholar]
  5. Cohen P. The role of protein phosphorylation in neural and hormonal control of cellular activity. Nature. 1982 Apr 15;296(5858):613–620. doi: 10.1038/296613a0. [DOI] [PubMed] [Google Scholar]
  6. Elliott J. A., Winn W. C., Jr Treatment of alveolar macrophages with cytochalasin D inhibits uptake and subsequent growth of Legionella pneumophila. Infect Immun. 1986 Jan;51(1):31–36. doi: 10.1128/iai.51.1.31-36.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Evans S. W., Rennick D., Farrar W. L. Identification of a signal-transduction pathway shared by haematopoietic growth factors with diverse biological specificity. Biochem J. 1987 Jun 15;244(3):683–691. doi: 10.1042/bj2440683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Friedman H., Widen R., Klein T., Searls L., Cabrian K. Legionella pneumophila-induced blastogenesis of murine lymphoid cells in vitro. Infect Immun. 1984 Jan;43(1):314–319. doi: 10.1128/iai.43.1.314-319.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Horwitz M. A., Silverstein S. C. Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest. 1980 Sep;66(3):441–450. doi: 10.1172/JCI109874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hunter T. A thousand and one protein kinases. Cell. 1987 Sep 11;50(6):823–829. doi: 10.1016/0092-8674(87)90509-5. [DOI] [PubMed] [Google Scholar]
  11. Krebs E. G., Beavo J. A. Phosphorylation-dephosphorylation of enzymes. Annu Rev Biochem. 1979;48:923–959. doi: 10.1146/annurev.bi.48.070179.004423. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Morrison D. C., Rudbach J. A. Endotoxin-cell-membrane interactions leading to transmembrane signaling. Contemp Top Mol Immunol. 1981;8:187–218. doi: 10.1007/978-1-4684-3917-5_6. [DOI] [PubMed] [Google Scholar]
  14. Morrison D. C., Ryan J. L. Bacterial endotoxins and host immune responses. Adv Immunol. 1979;28:293–450. doi: 10.1016/s0065-2776(08)60802-0. [DOI] [PubMed] [Google Scholar]
  15. Pontremoli S., Melloni E., Michetti M., Sparatore B., Salamino F., Sacco O., Horecker B. L. Phosphorylation and proteolytic modification of specific cytoskeletal proteins in human neutrophils stimulated by phorbol 12-myristate 13-acetate. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3604–3608. doi: 10.1073/pnas.84.11.3604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Saha A. K., Dowling J. N., Mukhopadhyay N. K., Glew R. H. Legionella micdadei protein kinase catalyzes phosphorylation of tubulin and phosphatidylinositol. J Bacteriol. 1989 Sep;171(9):5103–5110. doi: 10.1128/jb.171.9.5103-5110.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Shawver L. K., Pierce G. F., Kawahara R. S., Deuel T. F. Platelet-derived growth factor induces phosphorylation of a 64-kDa nuclear protein. J Biol Chem. 1989 Jan 15;264(2):1046–1050. [PubMed] [Google Scholar]
  18. Shinomiya H., Hirata H., Nakano M. Purification and characterization of the 65-kDa protein phosphorylated in murine macrophages by stimulation with bacterial lipopolysaccharide. J Immunol. 1991 May 15;146(10):3617–3625. [PubMed] [Google Scholar]
  19. Suzuki K., Koshio O., Ishida-Okawara A., Shibata M., Yamakawa Y., Tagawa M., Ota H., Kuramoto A., Mizuno S. Localization of chemotactic activity and 64 kD protein phosphorylation for human polymorphonuclear leukocytes in N-terminus of the chemotactic protein LUCT/IL-8. Biochem Biophys Res Commun. 1989 Sep 29;163(3):1298–1305. doi: 10.1016/0006-291x(89)91119-4. [DOI] [PubMed] [Google Scholar]
  20. Vildé J. L., Dournon E., Rajagopalan P. Inhibition of Legionella pneumophila multiplication within human macrophages by antimicrobial agents. Antimicrob Agents Chemother. 1986 Nov;30(5):743–748. doi: 10.1128/aac.30.5.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Weiel J. E., Hamilton T. A., Adams D. O. LPS induces altered phosphate labeling of proteins in murine peritoneal macrophages. J Immunol. 1986 Apr 15;136(8):3012–3018. [PubMed] [Google Scholar]
  22. Yamamoto M., Nishimura J., Ideguchi H., Ibayashi H. Specific phosphorylation of 22-kD proteins by various inducers for granuloid differentiation in myeloid leukemic cells. Leuk Res. 1988;12(1):71–80. doi: 10.1016/s0145-2126(98)80011-8. [DOI] [PubMed] [Google Scholar]
  23. Yamamoto Y., Klein T. W., Newton C. A., Widen R., Friedman H. Growth of Legionella pneumophila in thioglycolate-elicited peritoneal macrophages from A/J mice. Infect Immun. 1988 Feb;56(2):370–375. doi: 10.1128/iai.56.2.370-375.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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