Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

Alterations of Protein Expression in Macrophages in Response to Candida albicans Infection

  • Shin, Yu-Kyong (Department of Biochemistry, Yonsei Proteome Research Center and Biomedical Proteome Research Center, Yonsei University) ;
  • Kim, Ki-Young (Department of Biochemistry, Yonsei Proteome Research Center and Biomedical Proteome Research Center, Yonsei University) ;
  • Paik, Young-Ki (Department of Biochemistry, Yonsei Proteome Research Center and Biomedical Proteome Research Center, Yonsei University)
  • Received : 2005.06.21
  • Accepted : 2005.07.08
  • Published : 2005.10.31
⟨ Previous Next ⟩

Abstract

Although macrophages are an important first line of cellular defense, they are unable to effectively kill phagocytosed C. albicans. To determine the physiological basis of this inability, we investigated the alterations of macrophage proteins caused by C. albicans infection. Since the formation of C. albicans hyphae caused cell death, proteins were prepared 3 h after infection and examined by two-dimensional gel electrophoresis (2-DE). The most prominent changes were in glycolytic enzymes, which could have caused energy depletion of the infected cells. Also changed were proteins involved in maintenance of cellular integrity and NO production. Treatment of the macrophages with either cytochalasin D or taxol did not alter their inability to kill C. albicans. Our results indicate that multiple factors contribute to cell death as the pathogenic form of C. albicans becomes fully active inside macrophage cells.

Keywords

Acknowledgement

Supported by : Ministry of Health and Welfare

References

  1. Chinen, T., Qureshi, M. H., Koguchi, Y., and Kawakami, K. (1999) Candida albicans suppresses nitric oxide (NO) production by interferon-gamma (IFN-gamma) and lipopolysaccharide (LPS)-stimulated murine peritoneal macrophages. Clin. Exp. Immunol. 115, 491-497 https://doi.org/10.1046/j.1365-2249.1999.00822.x
  2. Cho, S. H., Cho, J. J., Kim, I. S., Vliagoftis, H., Metcalfe, D. D., et al. (1998) Identification and characterization of the inducible murine mast cell gene, imc-415. Biochem. Biophys. Res. Commun. 252, 123-127 https://doi.org/10.1006/bbrc.1998.9609
  3. Cho, Y. M., Bae, S. H., Choi, B. K., Cho, S. Y., Song, C. W., et al. (2003) Differential expression of the liver proteome in senescence accelerated mice. Proteomics 3, 1883-1894 https://doi.org/10.1002/pmic.200300562
  4. Choi, B. K., Chitwood, D. J., and Paik, Y. K. (2003) Proteomic changes during disturbance of cholesterol metabolism by azacoprostane treatment in Caenorhabditis elegans. Mol. Cell. Proteomics 2, 1086-1095 https://doi.org/10.1074/mcp.M300036-MCP200
  5. Delauney, A. J., Hu, C. A., Kishor, P. B., and Verma, D. P. (1993) Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J. Biol. Chem. 268, 18673-18678
  6. Ding, A. H., Nathan, C. F., and Stuehr, D. J. (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141, 2407-2412
  7. Filler, S. G., Swerdloff, J. N., Hobbs, C., and Luckett, P. M. (1995) Penetration and damage of endothelial cells by Candida albicans. Infect. Immun. 63, 976-983
  8. Glockzin, S., von Knethen, A., Scheffner, M., and Brune, B. (1999) Activation of the cell death program by nitric oxide involves inhibition of the proteasome. J. Biol. Chem. 274, 19581-19586 https://doi.org/10.1074/jbc.274.28.19581
  9. Gorg, A., Weiss, W., and Dunn, M. J. (2004) Current twodimensional electrophoresis technology for proteomics. Proteomics 4, 3665-3685 https://doi.org/10.1002/pmic.200401031
  10. Handyside, A. H. and Hunter, S. (1984) A rapid procedure for visualising the inner cell mass and trophectoderm nuclei of mouse blastocysts in situ using polynucleotide-specific fluorochromes. J. Exp. Zool. 231, 429-434 https://doi.org/10.1002/jez.1402310317
  11. Hattori, Y., Campbell, E. B., and Gross, S. S. (1994) Argininosuccinate synthetase mRNA and activity are induced by immunostimulants in vascular smooth muscle. Role in the regeneration or arginine for nitric oxide synthesis. J. Biol. Chem. 269, 9405-9408
  12. Henry-Stanley, M. J., Garni, R. M., and Wells, C. L. (2004) Adaptation of FUN-1 and Calcofluor white stains to assess the ability of viable and nonviable yeast to adhere to and be internalized by cultured mammalian cells. J. Microbiol. Methods 59, 289-292 https://doi.org/10.1016/j.mimet.2004.07.001
  13. Hirano, S., Rees, R. S., Yancy, S. L., Welsh, M. J., Remick, D. G., et al. (2004) Endothelial barrier dysfunction caused by LPS correlates with phosphorylation of HSP27 in vivo. Cell. Biol. Toxicol. 20, 1-4 https://doi.org/10.1023/B:CBTO.0000021019.50889.aa
  14. Ishii, T., Yamada, M., Sato, H., Matsue, M., Taketani, S., et al. (1993) Cloning and characterization of a 23-kDa stressinduced mouse peritoneal macrophage protein. J. Biol. Chem. 268, 18633-18636
  15. Kaposzta, R., Marodi, L., Hollinshead, M., Gordon, S., and da Silva, R. P. (1999) Rapid recruitment of late endosomes and lysosomes in mouse macrophages ingesting Candida albicans. J. Cell. Sci. 112, 3237-3348
  16. Lo, H. J., Johler, J. R., Domenico, B. D., Loebenberg, D., Cacciapuoti, A., et al. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90, 939-949 https://doi.org/10.1016/S0092-8674(00)80358-X
  17. Lodish, H., Berk, A., Zipursky, S. L., Matsudaira, P., Baltimore, D., et al. (1999) Molecular Cell Biology, 4th ed., p. 763, p. 807
  18. Loisel, T. P., Boujemaa, R., Pantaloni, D., and Carlier, M. F. (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613-616 https://doi.org/10.1038/44183
  19. Lorenz, M. C. and Fink, G. R. (2001) The glyoxylate cycle is required for fungal virulence. Nature 412, 83-86 https://doi.org/10.1038/35083594
  20. Moncada, S., Palmer, R. M., and Higgs, E. A. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109-142
  21. Negrutskii, B. S. and El'skaya, A. V. (1998) Eukaryotic translation elongation factor 1 alpha: structure, expression, functions, and possible role in aminoacyl-tRNA channeling. Prog. Nucleic Acid Res. Mol. Biol. 60, 47-78 https://doi.org/10.1016/S0079-6603(08)60889-2
  22. Noh, E. J., Kang, S. W., Shin, Y. J., Kim, D. C., Park, I. S., et al. (2002) Characterization of mycoplasma arginine deiminase expressed in E. coli and its inhibitory regulation of nitric oxide synthesis. Mol. Cells 13, 137-143
  23. Otsu, M., Urade, R., Kito, M., Omura, F., and Kikuchi, M. (1995) A possible role of ER-60 protease in the degradation of misfolded proteins in the endoplasmic reticulum. J. Biol. Chem. 270, 14958-14961 https://doi.org/10.1074/jbc.270.25.14958
  24. Park, K. S., Kang, K. C., Kim, K. Y., Jeong, P. Y., Kim, J. H., et al. (2001) HWY-289, a novel semi-synthetic protoberberine derivative with multiple target sites in Candida albicans. J. Antimicrob. Chemother. 47, 513-519 https://doi.org/10.3349/ymj.2006.47.4.513
  25. Rabilloud, T. (2002) Two-dimensional gel electrophoresis in proteomics: old, old fashioned, but it still climbs up the mountains. Proteomics 2, 3-10 https://doi.org/10.1002/1615-9861(200201)2:1<3::AID-PROT3>3.0.CO;2-R
  26. Rikihisa, Y., Zhang, Y., and Park, J. (1994) Inhibition of infection of macrophages with Ehrlichia risticii by cytochalasins, monodansylcadaverine, and taxol. Infect. Immun. 62, 5126-5132
  27. Robinson, J. M. and Badwey, J. A. (2002) Rapid association of cytoskeletal remodeling proteins with the developing phagosomes of human neutrophils. Histochem. Cell. Biol. 118, 117-125
  28. Romani, L. (2000) Innate and adaptive immunity in Candida albicans infections and saprophytism. J. Leukoc. Biol. 68, 175-179
  29. Schroppel, K., Kryk, M., Herrmann, M., Leberer, E., Rollinghoff, M., et al. (2001) Suppression of type 2 NO-synthase activity in macrophages by Candida albicans. Int. J. Med. Microbiol. 290, 659-668 https://doi.org/10.1016/S1438-4221(01)80003-5
  30. Shevchenko, A., Jensen, O. N., Podtelejnikov, A. V., Sagliocco, F., Wilm, M., et al. (1996) Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. USA 93, 14440-14445
  31. Torosantucci, A., Chiani, P., and Cassone, A. (2000) Differential chemokine response of human monocytes to yeast and hyphal forms of Candida albicans and its relation to the beta- 1,6 glucan of the fungal cell wall. J. Leukoc. Biol. 68, 923-932
  32. Utaisincharoen, P., Tangthawornchaikul, N., Kespichayawattana, W., Anuntagool, N., Chaisuriya, P., et al. (2000) Kinetic studies of the production of nitric oxide (NO) and tumour necrosis factor-alpha (TNF-alpha) in macrophages stimulated with Burkholderia pseudomallei endotoxin. Clin. Exp. Immunol. 122, 324-329 https://doi.org/10.1046/j.1365-2249.2000.01386.x
  33. Vonk, A. G., Wieland, C. W., Netea, M. G., and Kullberg, B. J. (2002) Phagocytosis and intracellular killing of Candida albicans blastoconidia by neutrophils and macrophages: a comparison of different microbiological test systems. J. Microbiol. Methods 49, 55-62 https://doi.org/10.1016/S0167-7012(01)00348-7