Sustained activation of Akt and Erk1/2 is required for Coxiella burnetii antiapoptotic activity

Infection and Immunity

Volumn 77, Issue 1, 2009, Pages 205-213

  Voth, Daniel E ^a,c   Heinzen, Robert A ^a,b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN C JUN; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; COXIELLA BURNETII; CYTOKINE PRODUCTION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; Q FEVER; RNA SYNTHESIS; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL LINE; CERCOPITHECUS AETHIOPS; COXIELLA BURNETII; HUMANS; MACROPHAGES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; ONCOGENE PROTEIN V-AKT; PHOSPHORYLATION; TIME FACTORS;

EID: 58449089569     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01124-08     Document Type: Article

References (48)

1. Abu-Zant, A., S. Jones, R. Asare, J. Suttles, C. Price, J. Graham, and Y. A. Kwaik. 2007. Anti-apoptotic signalling by the Dot/Icm secretion system of L. pneumophila. Cell. Microbiol. 9:246-264.
2. Akporiaye, E. T., J. D. Rowatt, A. A. Aragon, and O. G. Baca. 1983. Lysosomal response of a murine macrophage-like cell line persistently infected with Coxiella burnetii. Infect. Immun. 40:1155-1162.
3. Banga, S., P. Gao, X. Shen, V. Fiscus, W. X. Zong, L. Chen, and Z. Q. Luo. 2007. Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc. Natl. Acad. Sci. USA 104:5121-5126.
4. Bhavsar, A. P., J. A. Guttman, and B. B. Finlay. 2007. Manipulation of host-cell pathways by bacterial pathogens. Nature 449:827-834.
5. Buchholz, K. R., and R. S. Stephens. 2007. The extracellular signal-regulated kinase/mitogen-activated protein kinase pathway induces the inflammatory factor interleukin-8 following Chlamydia trachomatis infection. Infect. Immun. 75:5924-5929.
6. Cockrell, D. C., P. A. Beare, E. R. Fischer, D. Howe, and R. A. Heinzen. 2008. A method for purifying obligate intracellular Coxiella burnetii that employs digitonin lysis of host cells. J. Microbiol. Methods 72:321-325.
7. Coleman, S. A., E. R. Fischer, D. Howe, D. J. Mead, and R. A. Heinzen. 2004. Temporal analysis of Coxiella burnetii morphological differentiation. J. Bacteriol. 186:7344-7352.
8. Cuenda, A., and S. Rousseau. 2007. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta 1773:1358-1375.
9. Dellacasagrande, J., C. Capo, D. Raoult, and J. L. Mege. 1999. IFN-gamma-mediated control of Coxiella burnetii survival in monocytes: the role of cell apoptosis and TNF. J. Immunol. 162:2259-2265.
10. Dellacasagrande, J., E. Ghigo, D. Raoult, C. Capo, and J. L. Mege. 2002. IFN-gamma-induced apoptosis and microbicidal activity in monocytes harboring the intracellular bacterium Coxiella burnetii require membrane TNF and homotypic cell adherence. J. Immunol. 169:6309-6315.
11. Dhiman, R., M. Raje, and S. Majumdar. 2007. Differential expression of NF-κB in mycobacteria infected THP-1 affects apoptosis. Biochim. Biophys. Acta 1770:649-658.
12. Faherty, C. S., and A. T. Maurelli. 2008. Staying alive: bacterial inhibition of apoptosis during infection. Trends Microbiol. 16:173-180.
13. Frödin, M., and S. Gammeltoft. 1999. Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol. Cell. Endocrinol. 151:65-77.
14. Hackstadt, T., and J. C. Williams. 1981. Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc. Natl. Acad. Sci. USA 78:3240-3244.
15. Heinzen, R. A., T. Hackstadt, and J. E. Samuel. 1999. Developmental biology of Coxiella burnetii. Trends Microbiol. 7:149-154.
16. Heinzen, R. A., M. A. Scidmore, D. D. Rockey, and T. Hackstadt. 1996. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect. Immun. 64:796-809.
17. Howe, D., and R. A. Heinzen. 2006. Coxiella burnetii inhabits a cholesterolrich vacuole and influences cellular cholesterol metabolism. Cell. Microbiol. 8:496-507.
18. Howie, H. L., S. L. Shiflett, and M. So. 2008. Extracellular signal-regulated kinase activation by Neisseria gonorrhoeae downregulates epithelial cell proapoptotic proteins Bad and Bim. Infect. Immun. 76:2715-2721.
19. Hybiske, K., and R. S. Stephens. 2008. Exit strategies of intracellular pathogens. Nat. Rev. Microbiol. 6:99-110.
20. Jin, Z., and W. S. El-Deiry. 2005. Overview of cell death signaling pathways. Cancer Biol. Ther. 4:139-163.
21. Knodler, L. A., B. B. Finlay, and O. Steele-Mortimer. 2005. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J. Biol. Chem. 280:9058-9064.
22. Loeuillet, C., F. Martinon, C. Perez, M. Munoz, M. Thome, and P. R. Meylan. 2006. Mycobacterium tuberculosis subverts innate immunity to evade specific effectors. J. Immunol. 177:6245-6255.
23. Losick, V. P., and R. R. Isberg. 2006. NF-κB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J. Exp. Med. 203:2177-2189.
24. Luhrmann, A., and C. R. Roy. 2007. Coxiella burnetii inhibits activation of host cell apoptosis through a mechanism that involves preventing cytochrome c release from mitochondria. Infect. Immun. 75:5282-5289.
25. Maiti, D., A. Bhattacharyya, and J. Basu. 2001. Lipoarabinomannan from Mycobacterium tuberculosis promotes macrophage survival by phosphorylating Bad through a phosphatidylinositol 3-kinase/Akt pathway. J. Biol. Chem. 276:329-333.
26. Manning, B. D., and L. C. Cantley. 2007. AKT/PKB signaling: navigating downstream. Cell 129:1261-1274.
27. Maurin, M., and D. Raoult. 1999. Q fever. Clin. Microbiol. Rev. 12:518-553.
28. McCubrey, J. A., L. S. Steelman, S. L. Abrams, J. T. Lee, F. Chang, F. E. Bertrand, P. M. Navolanic, D. M. Terrian, R. A. Franklin, A. B. D'Assoro, J. L. Salisbury, M. C. Mazzarino, F. Stivala, and M. Libra. 2006. Roles of the RAF/MEK/ERK and PI3K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv. Enzyme Regul. 46:249-279.
29. McCubrey, J. A., L. S. Steelman, W. H. Chappell, S. L. Abrams, E. W. Wong, F. Chang, B. Lehmann, D. M. Terrian, M. Milella, A. Tafuri, F. Stivala, M. Libra, J. Basecke, C. Evangelisti, A. M. Martelli, and R. A. Franklin. 2007. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation, and drug resistance. Biochim. Biophys. Acta 1773:1263-1284.
30. Mimuro, H., T. Suzuki, S. Nagai, G. Rieder, M. Suzuki, T. Nagai, Y. Fujita, K. Nagamatsu, N. Ishijima, S. Koyasu, R. Haas, and C. Sasakawa. 2007. Helicobacter pylori dampens gut epithelial self-renewal by inhibiting apoptosis, a bacterial strategy to enhance colonization of the stomach. Cell Host Microbe. 2:250-263.
31. Miyairi, I., and G. I. Byrne. 2006. Chlamydia and programmed cell death. Curr. Opin. Microbiol. 9:102-108.
32. Moos, A., and T. Hackstadt. 1987. Comparative virulence of intra- and interstrain lipopolysaccharide variants of Coxiella burnetii in the guinea pig model. Infect. Immun. 55:1144-1150.
33. Mynott, T. L., B. Crossett, and S. R. Prathalingam. 2002. Proteolytic inhibition of Salmonella enterica serovar Typhimurium-induced activation of the mitogen-activated protein kinases ERK and JNK in cultured human intestinal cells. Infect. Immun. 70:86-95.
34. Nishina, H., T. Wada, and T. Katada. 2004. Physiological roles of SAPK/JNK signaling pathway. J. Biochem. 136:123-126.
35. Pan, X., A. Luhrmann, A. Satoh, M. A. Laskowski-Arce, and C. R. Roy. 2008. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320:1651-1654.
36. Roach, S. K., and J. S. Schorey. 2002. Differential regulation of the mitogen-activated protein kinases by pathogenic and nonpathogenic mycobacteria. Infect. Immun. 70:3040-3052.
37. Romano, P. S., M. G. Gutierrez, W. Beron, M. Rabinovitch, and M. I. Colombo. 2007. The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell. Microbiol. 9:891-909.
38. Schmitt, E., M. Gehrmann, M. Brunet, G. Multhoff, and C. Garrido. 2007. Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J. Leukoc. Biol. 81:15-27.
39. Shannon, J. G., and R. A. Heinzen. 2008. Infection of human monocyte-derived macrophages with Coxiella burnetii. Methods Mol. Biol. 431:189-200.
40. Takeda, K., T. Noguchi, I. Naguro, and H. Ichijo. 2008. Apoptosis signal-regulating kinase 1 in stress and immune response. Annu. Rev. Pharmacol. Toxicol. 48:199-225.
41. Tapinos, N., and A. Rambukkana. 2005. Insights into regulation of human Schwann cell proliferation by Erk1/2 via a MEK-independent and p56Lck-dependent pathway from leprosy bacilli. Proc. Natl. Acad. Sci. USA 102:9188-9193.
42. Tse, H. M., S. I. Josephy, E. D. Chan, D. Fouts, and A. M. Cooper. 2002. Activation of the mitogen-activated protein kinase signaling pathway is instrumental in determining the ability of Mycobacterium avium to grow in murine macrophages. J. Immunol. 168:825-833.
43. Tsurutani, J., K. A. West, J. Sayyah, J. J. Gills, and P. A. Dennis. 2005. Inhibition of the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin pathway but not the MEK/ERK pathway attenuates laminin-mediated small cell lung cancer cellular survival and resistance to imatinib mesylate or chemotherapy. Cancer Res. 65:8423-8432.
44. Verbeke, P., L. Welter-Stahl, S. Ying, J. Hansen, G. Hacker, T. Darville, and D. M. Ojcius. 2006. Recruitment of Bad by the Chlamydia trachomatis vacuole correlates with host cell survival. PLoS Pathog. 2:e45.
45. Voth, D. E., and R. A. Heinzen. 2007. Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell. Microbiol. 9:829-840.
46. Voth, D. E., D. Howe, and R. A. Heinzen. 2007. Coxiella burnetii inhibits apoptosis in human THP-1 cells and monkey primary alveolar macrophages. Infect. Immun. 75:4263-4271.
47. Welsh, C. T., J. T. Summersgill, and R. D. Miller. 2004. Increases in c-Jun N-terminal kinase/stress-activated protein kinase and p38 activity in monocyte-derived macrophages following the uptake of Legionella pneumophila. Infect. Immun. 72:1512-1518.
48. Zhu, H., H. O. Fearnhead, and G. M. Cohen. 1995. An ICE-like protease is a common mediator of apoptosis induced by diverse stimuli in human monocytic THP.1 cells. FEBS Lett. 374:303-308.