Coxiella burnetii phase I and II variants replicate with similar kinetics in degradative phagolysosome-like compartments of human macrophages

Infection and Immunity

Volumn 78, Issue 8, 2010, Pages 3465-3474

  Howe, Dale ^a   Shannon, Jeffrey G ^a   Winfree, Seth ^b   Dorward, David W ^a   Heinzen, Robert A ^a  

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

^b Laboratory of Intracellular Parasites   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN D; CD63 ANTIGEN; INTERLEUKIN 6; RAB PROTEIN; RAB7 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; CATHEPSIN;

ARTICLE; BACTERIAL GROWTH; CELL TYPE; COXIELLA BURNETII; CYTOKINE RELEASE; DEGRADATION KINETICS; ESCHERICHIA COLI; GENETIC VARIABILITY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOLYSOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; Q FEVER; CELL CULTURE; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHAGOSOME; SECRETION;

CATHEPSINS; CELLS, CULTURED; COXIELLA BURNETII; ESCHERICHIA COLI; HUMANS; INTERLEUKIN-6; MACROPHAGES; PHAGOSOMES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77955300012     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00406-10     Document Type: Article

References (57)

1. Aguilera, M., R. Salinas, E. Rosales, S. Carminati, M. I. Colombo, and W. Beron. 2009. Actin dynamics and Rho GTPases regulate the size and formation of parasitophorous vacuoles containing Coxiella burnetii. Infect. Immun. 77:4609-4620.
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. Amano, K., J. C. Williams, T. F. McCaul, and M. G. Peacock. 1984. Biochemical and immunological properties of Coxiella burnetii cell wall and peptidoglycan-protein complex fractions. J. Bacteriol. 160:982-988.
4. Andoh, M., G. Zhang, K. E. Russell-Lodrigue, H. R. Shive, B. R. Weeks, and J. E. Samuel. 2007. T cells are essential for bacterial clearance, and gamma interferon, tumor necrosis factor alpha, and B cells are crucial for disease development in Coxiella burnetii infection in mice. Infect. Immun. 75:3245-3255. (Pubitemid 47040925)
5. Baca, O. G., E. T. Akporiaye, A. S. Aragon, I. L. Martinez, M. V. Robles, and N. L. Warner. 1981. Fate of phase I and phase II Coxiella burnetii in several macrophage-like tumor cell lines. Infect. Immun. 33:258-266.
6. Beare, P. A., D. Howe, D. C. Cockrell, and R. A. Heinzen. 2007. Efficient method of cloning the obligate intracellular bacterium Coxiella burnetii. Appl. Environ. Microbiol. 73:4048-4054.
7. Beare, P. A., J. E. Samuel, D. Howe, K. Virtaneva, S. F. Porcella, and R. A. Heinzen. 2006. Genetic diversity of the Q fever agent, Coxiella burnetii, assessed by microarray-based whole-genome comparisons. J. Bacteriol. 188:2309-2324.
8. Benoit, M., E. Ghigo, C. Capo, D. Raoult, and J. L. Mege. 2008. The uptake of apoptotic cells drives Coxiella burnetii replication and macrophage polarization: a model for Q fever endocarditis. PLoS Pathog. 4:e1000066.
9. Brennan, R. E., K. Russell, G. Zhang, and J. E. Samuel. 2004. Both inducible nitric oxide synthase and NADPH oxidase contribute to the control of virulent phase I Coxiella burnetii infections. Infect. Immun. 72:6666-6675.
10. Bucci, C., P. Thomsen, P. Nicoziani, J. McCarthy, and B. van Deurs. 2000. Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 11:467-480.
11. Burton, P. R., N. Kordova, and D. Paretsky. 1971. Electron microscopic studies of the rickettsia Coxiella burnetii: entry, lysosomal response, and fate of rickettsial DNA in L-cells. Can. J. Microbiol. 17:143-150.
12. Capo, C., A. Moynault, Y. Collette, D. Olive, E. J. Brown, D. Raoult, and J. L. Mege. 2003. Coxiella burnetii avoids macrophage phagocytosis by interfering with spatial distribution of complement receptor 3. J. Immunol. 170:4217-4225.
13. 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.
14. 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.
15. Creasy, B. M., C. B. Hartmann, F. K. White, and K. L. McCoy. 2007. New assay using fluorogenic substrates and immunofluorescence staining to measure cysteine cathepsin activity in live cell subpopulations. Cytometry 71(Pt A):114-123.
16. Ghigo, E., C. Capo, D. Raoult, and J. L. Mege. 2001. Interleukin-10 stimulates Coxiella burnetii replication in human monocytes through tumor necrosis factor down-modulation: role in microbicidal defect of Q fever. Infect. Immun. 69:2345-2352.
17. Ghigo, E., C. Capo, C. H. Tung, D. Raoult, J. P. Gorvel, and J. L. Mege. 2002. Coxiella burnetii survival in THP-1 monocytes involves the impairment of phagosome maturation: IFN-gamma mediates its restoration and bacterial killing. J. Immunol. 169:4488-4495.
18. Ghigo, E., A. Honstettre, C. Capo, J. P. Gorvel, D. Raoult, and J. L. Mege. 2004. Link between impaired maturation of phagosomes and defective Coxiella burnetii killing in patients with chronic Q fever. J. Infect. Dis. 190:1767-1772.
19. Grieshaber, S., J. A. Swanson, and T. Hackstadt. 2002. Determination of the physical environment within the Chlamydia trachomatis inclusion using ion-selective ratiometric probes. Cell. Microbiol. 4:273-283.
20. Hackstadt, T., M. G. Peacock, P. J. Hitchcock, and R. L. Cole. 1985. Lipopolysaccharide variation in Coxiella burnetii: intrastrain heterogeneity in structure and antigenicity. Infect. Immun. 48:359-365.
21. Heinzen, R. A., T. Hackstadt, and J. E. Samuel. 1999. Developmental biology of Coxiella burnetii. Trends Microbiol. 7:149-154.
22. 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.
23. Honstettre, A., E. Ghigo, A. Moynault, C. Capo, R. Toman, S. Akira, O. Takeuchi, H. Lepidi, D. Raoult, and J. L. Mege. 2004. Lipopolysaccharide from Coxiella burnetii is involved in bacterial phagocytosis, filamentous actin reorganization, and inflammatory responses through Toll-like receptor 4. J. Immunol. 172:3695-3703.
24. Hoover, T. A., D. W. Culp, M. H. Vodkin, J. C. Williams, and H. A. Thompson. 2002. Chromosomal DNA deletions explain phenotypic characteristics of two antigenic variants, phase II and RSA 514 (crazy), of the Coxiella burnetii Nine Mile strain. Infect. Immun. 70:6726-6733.
25. Howe, D., and L. P. Mallavia. 2000. Coxiella burnetii exhibits morphological change and delays phagolysosomal fusion after internalization by J774A.1 cells. Infect. Immun. 68:3815-3821.
26. Howe, D., J. Melnicakova, I. Barak, and R. A. Heinzen. 2003. Maturation of the Coxiella burnetii parasitophorous vacuole requires bacterial protein synthesis but not replication. Cell. Microbiol. 5:469-480.
27. Khavkin, T., and S. S. Tabibzadeh. 1988. Histologic, immunofluorescence, and electron microscopic study of infectious process in mouse lung after intranasal challenge with Coxiella burnetii. Infect. Immun. 56:1792-1799.
28. Kishimoto, R. A., and J. S. Walker. 1976. Interaction between Coxiella burnetii and guinea pig peritoneal macrophages. Infect. Immun. 14:416-421.
29. 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.
30. Lubick, K., M. Radke, and M. Jutila. 2007. Securinine, a GABAA receptor antagonist, enhances macrophage clearance of phase II C. burnetii: comparison with TLR agonists. J. Leukoc. Biol. 82:1062-1069.
31. Luzio, J. P., P. R. Pryor, and N. A. Bright. 2007. Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 8:622-632.
32. Maurin, M., A. M. Benoliel, P. Bongrand, and D. Raoult. 1992. Phagolysosomal alkalinization and the bactericidal effect of antibiotics: the Coxiella burnetii paradigm. J. Infect. Dis. 166:1097-1102.
33. Maurin, M., A. M. Benoliel, P. Bongrand, and D. Raoult. 1992. Phagolysosomes of Coxiella burnetii-infected cell lines maintain an acidic pH during persistent infection. Infect. Immun. 60:5013-5016.
34. Maurin, M., and D. Raoult. 1999. Q fever. Clin. Microbiol. Rev. 12:518-553.
35. 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.
36. Nielsen, E., F. Severin, J. M. Backer, A. A. Hyman, and M. Zerial. 1999. Rab5 regulates motility of early endosomes on microtubules. Nat. Cell Biol. 1:376-382.
37. Omsland, A., D. C. Cockrell, D. Howe, E. R. Fischer, K. Virtaneva, D. E. Sturdevant, S. F. Porcella, and R. A. Heinzen. 2009. Host cell-free growth of the Q fever bacterium Coxiella burnetii. Proc. Natl. Acad. Sci. U. S. A. 106:4430-4434.
38. 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. (Pubitemid 351931257)
39. Pethe, K., D. L. Swenson, S. Alonso, J. Anderson, C. Wang, and D. G. Russell. 2004. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc. Natl. Acad. Sci. U. S. A. 101: 13642-13647.
40. 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.
41. Russell, D. G., B. C. Vanderven, S. Glennie, H. Mwandumba, and R. S. Heyderman. 2009. The macrophage marches on its phagosome: dynamic assays of phagosome function. Nat. Rev. Immunol. 9:594-600.
42. Sauer, J. D., J. G. Shannon, D. Howe, S. F. Hayes, M. S. Swanson, and R. A. Heinzen. 2005. Specificity of Legionella pneumophila and Coxiella burnetii vacuoles and versatility of Legionella pneumophila revealed by coinfection. Infect. Immun. 73:4494-4504.
43. Scott, C. C., R. J. Botelho, and S. Grinstein. 2003. Phagosome maturation: a few bugs in the system. J. Membr. Biol. 193:137-152.
44. Shannon, J. G., D. C. Cockrell, K. Takahashi, G. L. Stahl, and R. A. Heinzen. 2009. Antibody-mediated immunity to the obligate intracellular bacterial pathogen Coxiella burnetii is Fc receptor- and complement-independent. BMC Immunol. 10:26.
45. Shannon, J. G., and R. A. Heinzen. 2007. Infection of human monocytederived macrophages with Coxiella burnetii. Methods Mol. Biol. 431:189-200.
46. Shannon, J. G., D. Howe, and R. A. Heinzen. 2005. Lack of dendritic cell maturation following infection by Coxiella burnetii synthesizing different lipopolysaccharide chemotypes. Ann. N. Y. Acad. Sci. 1063:154-160.
47. Shannon, J. G., D. Howe, and R. A. Heinzen. 2005. Virulent Coxiella burnetii does not activate human dendritic cells: role of lipopolysaccharide as a shielding molecule. Proc. Natl. Acad. Sci. U. S. A. 102:8722-8727.
48. Stein, A., C. Louveau, H. Lepidi, F. Ricci, P. Baylac, B. Davoust, and D. Raoult. 2005. Q fever pneumonia: virulence of Coxiella burnetii pathovars in a murine model of aerosol infection. Infect. Immun. 73:2469-2477.
49. Tujulin, E., B. Lilliehook, A. Macellaro, A. Sjostedt, and L. Norlander. 1999. Early cytokine induction in mouse P388D1 macrophages infected by Coxiella burnetii. Vet. Immunol. Immunopathol. 68:159-168.
50. Vazquez, C. L., and M. I. Colombo. 2010. Coxiella burnetii modulates Beclin 1 and Bcl-2, preventing host cell apoptosis to generate a persistent bacterial infection. Cell Death Differ. 17:421-438.
51. Vishwanath, S., and T. Hackstadt. 1988. Lipopolysaccharide phase variation determines the complement-mediated serum susceptibility of Coxiella burnetii. Infect. Immun. 56:40-44. (Pubitemid 18032125)
52. Voth, D. E., and R. A. Heinzen. 2007. Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell. Microbiol. 9:829-840.
53. Voth, D. E., and R. A. Heinzen. 2009. Sustained activation of Akt and Erk1/2 is required for Coxiella burnetii antiapoptotic activity. Infect. Immun. 77:205-213.
54. 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.
55. Zaidi, N., A. Maurer, S. Nieke, and H. Kalbacher. 2008. Cathepsin D: a cellular roadmap. Biochem. Biophys. Res. Commun. 376:5-9.
56. Zamboni, D. S. 2004. Genetic control of natural resistance of mouse macrophages to Coxiella burnetii infection in vitro: macrophages from restrictive strains control parasitophorous vacuole maturation. Infect. Immun. 72:2395-2399.
57. Zamboni, D. S., R. A. Mortara, E. Freymuller, and M. Rabinovitch. 2002. Mouse resident peritoneal macrophages partially control in vitro infection with Coxiella burnetii phase II. Microbes Infect. 4:591-598.