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Abstract

Coxiella burnetii is a bacterial intracellular parasite of eucaryotic cells that replicates within a membrane-bound compartment, or “parasitophorous vacuole” (PV). With the exception of human macrophages/monocytes, the consensus model of PV trafficking in host cells invokes endolysosomal maturation culminating in lysosome fusion. C. burnetii resists the degradative functions of the vacuole while at the same time exploiting the acidic pH for metabolic activation. While at first glance the mature PV resembles a large phagolysosome, an increasing body of evidence indicates the vacuole is in fact a specialized compartment that is actively modified by the pathogen. Adding to the complexity of PV biogenesis is new data showing vacuole engagement with autophagic and early secretory pathways. In this chapter, we review current knowledge of PV nature and development, and discuss disparate data related to the ultimate maturation state of PV harboring virulent or avirulent C. burnetii lipopolysaccharide phase variants in human mononuclear phagocytes.

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References

  • Agramonte-Hevia J, Gonzalez-Arenas A, Barrera D, Velasco-Velazquez M (2002) Gram-negative bacteria and phagocytic cell interaction mediated by complement receptor 3. FEMS Immunol Med Microbiol 34:255–266

    PubMed  CAS  Google Scholar 

  • Aguilera M, Salinas R, Rosales E, Carminati S, Colombo MI, Beron W (2009) Actin dynamics and Rho GTPases regulate the size and formation of parasitophorous vacuoles containing Coxiella burnetii. Infect Immun 77:4609–4620

    PubMed  CAS  Google Scholar 

  • Akporiaye ET, Rowatt JD, Aragon AA, Baca OG (1983) Lysosomal response of a murine macrophage-like cell line persistently infected with Coxiella burnetii. Infect Immun 40:1155–1162

    PubMed  CAS  Google Scholar 

  • Akporiaye ET, Stefanovich D, Tsosie V, Baca G (1990) Coxiella burnetii fails to stimulate human neutrophil superoxide anion production. Acta Virol 34:64–70

    PubMed  CAS  Google Scholar 

  • Alonso A, Garcia-Del Portillo F (2004) Hijacking of eukaryotic functions by intracellular bacterial pathogens. Int Microbiol 7:181–191

    PubMed  Google Scholar 

  • Amano K, Williams JC (1984) Chemical and immunological characterization of lipopolysaccharides from phase I and phase II Coxiella burnetii. J Bacteriol 160:994–1002

    PubMed  CAS  Google Scholar 

  • Amano K, Williams JC, Mccaul TF, Peacock MG (1984) Biochemical and immunological properties of Coxiella burnetii cell wall and peptidoglycan-protein complex fractions. J Bacteriol 160:982–988

    PubMed  CAS  Google Scholar 

  • Aragon AS, Pereira HA, Baca OG (1995) A cationic antimicrobial peptide enhances the infectivity of Coxiella burnetii. Acta Virol 39:223–226

    PubMed  CAS  Google Scholar 

  • Ariel BM, Khavkin TN, Amosenkova NI (1973) Interaction between Coxiellae burnetii and the cells in experimental Q-rickettsiosis. Histologic and electron microscope studies. Pathol Microbiol 39:412–423

    CAS  Google Scholar 

  • Baca OG, Akporiaye ET, Aragon AS, Martinez IL, Robles MV, Warner NL (1981) Fate of phase I and phase II Coxiella burnetii in several macrophage-like tumor cell lines. Infect Immun 33:258–266

    PubMed  CAS  Google Scholar 

  • Baca O, Akporiaye ET, Rowatt JD (1984) Possible biochemical adaptations of Coxiella burnetii for survival within phagocytes: effects of antibody. In: Leive L, Schlessinger D (eds) Microbiology 1984. ASM Press, Washington, DC

    Google Scholar 

  • Baca OG, Scott TO, Akporiaye ET, Deblassie R, Crissman HA (1985) Cell cycle distribution patterns and generation times of L929 fibroblast cells persistently infected with Coxiella burnetii. Infect Immun 47:366–369

    PubMed  CAS  Google Scholar 

  • Baca OG, Klassen DA, Aragon AS (1993a) Entry of Coxiella burnetii into host cells. Acta Virol 37:143–155

    PubMed  CAS  Google Scholar 

  • Baca OG, Roman MJ, Glew RH, Christner RF, Buhler JE, Aragon AS (1993b) Acid phosphatase activity in Coxiella burnetii: a possible virulence factor. Infect Immun 61:4232–4239

    PubMed  CAS  Google Scholar 

  • Baca OG, Li YP, Kumar H (1994) Survival of the Q fever agent Coxiella burnetii in the phagolysosome. Trends Microbiol 2:476–480

    PubMed  CAS  Google Scholar 

  • Barry AO, Mege JL, Ghigo E (2011) Hijacked phagosomes and leukocyte activation: an intimate relationship. J Leukoc Biol 89:373–382

    PubMed  CAS  Google Scholar 

  • Beare PA, Samuel JE, Howe D, Virtaneva K, Porcella SF, Heinzen RA (2006) Genetic diversity of the Q fever agent, Coxiella burnetii, assessed by microarray-based whole-genome comparisons. J Bacteriol 188:2309–2324

    PubMed  CAS  Google Scholar 

  • Beare PA, Howe D, Cockrell DC, Omsland A, Hansen B, Heinzen RA (2009a) Characterization of a Coxiella burnetii ftsZ mutant generated by Himar1 transposon mutagenesis. J Bacteriol 191:1369–1381

    PubMed  CAS  Google Scholar 

  • Beare PA, Unsworth N, Andoh M, Voth DE, Omsland A, Gilk SD, Williams KP, Sobral BW, Kupko JJ 3rd, Porcella SF, Samuel JE, Heinzen RA (2009b) Comparative genomics reveal extensive transposon-mediated genomic plasticity and diversity among potential effector proteins within the genus Coxiella. Infect Immun 77:642–656

    PubMed  CAS  Google Scholar 

  • Beare PA, Sandoz KM, Omsland A, Rockey DD, Heinzen RA (2011) Advances in genetic manipulation of obligate intracellular bacterial pathogens. Front Microbiol. 2:97

    Google Scholar 

  • Bekker LG, Freeman S, Murray PJ, Ryffel B, Kaplan G (2001) TNF-alpha controls intracellular mycobacterial growth by both inducible nitric oxide synthase-dependent and inducible nitric oxide synthase-independent pathways. J Immunol 166:6728–6734

    PubMed  CAS  Google Scholar 

  • Ben Amara A, Ghigo E, Le Priol Y, Lepolard C, Salcedo SP, Lemichez E, Bretelle F, Capo C, Mege JL (2010) Coxiella burnetii, the agent of Q fever, replicates within trophoblasts and induces a unique transcriptional response. PLoS One 5:e15315

    PubMed  CAS  Google Scholar 

  • Beron W, Gutierrez MG, Rabinovitch M, Colombo MI (2002) Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immun 70:5816–5821

    PubMed  CAS  Google Scholar 

  • Blander JM, Medzhitov R (2004) Regulation of phagosome maturation by signals from toll-like receptors. Science 304:1014–1018

    PubMed  CAS  Google Scholar 

  • Blauer F, Groscurth P, Schneemann M, Schoedon G, Schaffner A (1995) Modulation of the antilisterial activity of human blood-derived macrophages by activating and deactivating cytokines. J Interferon Cytokine Res 15:105–114

    PubMed  CAS  Google Scholar 

  • Brennan RE, Russell K, Zhang G, Samuel JE (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

    PubMed  CAS  Google Scholar 

  • Briggs HL, Pul N, Seshadri R, Wilson MJ, Tersteeg C, Russell-Lodrigue KE, Andoh M, Baumler AJ, Samuel JE (2008) Limited role for iron regulation in Coxiella burnetii pathogenesis. Infect Immun 76:2189–2201

    PubMed  CAS  Google Scholar 

  • Bucci C, Thomsen P, Nicoziani P, Mccarthy J, Van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11:467–480

    PubMed  CAS  Google Scholar 

  • Burnet FM, Freeman M (1937) Experimental studies on the virus of “Q” fever. Med J Aust 2:299–305

    Google Scholar 

  • Burton PR, Kordova N, Paretsky D (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

    PubMed  CAS  Google Scholar 

  • Burton PR, Stueckemann J, Paretsky D (1975) Electron microscopy studies of the limiting layers of the rickettsia Coxiella burneti. J Bacteriol 122:316–324

    PubMed  CAS  Google Scholar 

  • Burton PR, Stueckemann J, Welsh RM, Paretsky D (1978) Some ultrastructural effects of persistent infections by the rickettsia Coxiella burnetii in mouse L cells and green monkey kidney (Vero) cells. Infect Immun 21:556–566

    PubMed  CAS  Google Scholar 

  • Caldwell HD, Wood H, Crane D, Bailey R, Jones RB, Mabey D, Maclean I, Mohammed Z, Peeling R, Roshick C, Schachter J, Solomon AW, Stamm WE, Suchland RJ, Taylor L, West SK, Quinn TC, Belland RJ, Mcclarty G (2003) Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J Clin Invest 111:1757–1769

    PubMed  CAS  Google Scholar 

  • Campoy EM, Zoppino FC, Colombo MI (2011) The early secretory pathway contributes to the growth of the Coxiella-replicative niche. Infect Immun 79:402–413

    PubMed  CAS  Google Scholar 

  • Capo C, Zaffran Y, Zugun F, Houpikian P, Raoult D, Mege JL (1996a) Production of interleukin-10 and transforming growth factor beta by peripheral blood mononuclear cells in Q fever endocarditis. Infect Immun 64:4143–4147

    PubMed  CAS  Google Scholar 

  • Capo C, Zugun F, Stein A, Tardei G, Lepidi H, Raoult D, Mege JL (1996b) Upregulation of tumor necrosis factor alpha and interleukin-1 beta in Q fever endocarditis. Infect Immun 64:1638–1642

    PubMed  CAS  Google Scholar 

  • Capo C, Lindberg FP, Meconi S, Zaffran Y, Tardei G, Brown EJ, Raoult D, Mege JL (1999) Subversion of monocyte functions by Coxiella burnetii: impairment of the cross-talk between αvβ3 integrin and CR3. J Immunol 163:6078–6085

    PubMed  CAS  Google Scholar 

  • Capo C, Moynault A, Collette Y, Olive D, Brown EJ, Raoult D, Mege JL (2003) Coxiella burnetii avoids macrophage phagocytosis by interfering with spatial distribution of complement receptor 3. J Immunol 170:4217–4225

    PubMed  CAS  Google Scholar 

  • Chen C, Banga S, Mertens K, Weber MM, Gorbaslieva I, Tan Y, Luo ZQ, Samuel JE (2010) Large-scale identification and translocation of type IV secretion substrates by Coxiella burnetii. Proc Natl Acad Sci U S A 107:21755–21760

    PubMed  CAS  Google Scholar 

  • Coleman SA, Fischer ER, Howe D, Mead DJ, Heinzen RA (2004) Temporal analysis of Coxiella burnetii morphological differentiation. J Bacteriol 186:7344–7352

    PubMed  CAS  Google Scholar 

  • Cooke RA (2008) Q fever. Was Edward Derrick’s contribution undervalued? Med J Aust 189:660–662

    PubMed  Google Scholar 

  • Cossart P, Roy CR (2010) Manipulation of host membrane machinery by bacterial pathogens. Curr Opin Cell Biol 22:547–554

    PubMed  CAS  Google Scholar 

  • Cossart P, Sansonetti PJ (2004) Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242–248

    PubMed  CAS  Google Scholar 

  • Cox HR (1938) A filter-passing infectious agent isolated from ticks. III. Description of organism and cultivation experiments. Public Health Rep 53:2270–2276

    Google Scholar 

  • Cox HR (1939) Sudies of a filter-passing infectious agent isolated from ticks. V. Further attempts to cultivate in cell-free media. Suggested classification. Public Health Rep 54:1822–1827

    Google Scholar 

  • Dellacasagrande J, Capo C, Raoult D, Mege JL (1999) IFN-gamma-mediated control of Coxiella burnetii survival in monocytes: the role of cell apoptosis and TNF. J Immunol 162:2259–2265

    PubMed  CAS  Google Scholar 

  • Denison AM, Massung RF, Thompson HA (2007) Analysis of the O-antigen biosynthesis regions of phase II isolates of Coxiella burnetii. FEMS Microbiol Lett 267:102–107

    PubMed  CAS  Google Scholar 

  • Deretic V, Levine B (2009) Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5:527–549

    PubMed  CAS  Google Scholar 

  • Derrick EH (1937) “Q” fever, a new fever entity: clinical features, diagnosis, and laboratory investigation. Med J Aust 2:281–299

    Google Scholar 

  • Desjardins M, Celis JE, Van Meer G, Dieplinger H, Jahraus A, Griffiths G, Huber LA (1994) Molecular characterization of phagosomes. J Biol Chem 269:32194–321200

    PubMed  CAS  Google Scholar 

  • Ghigo E, Capo C, Tung CH, Raoult D, Gorvel JP, Mege JL (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

    PubMed  CAS  Google Scholar 

  • Ghigo E, Honstettre A, Capo C, Gorvel JP, Raoult D, Mege JL (2004) Link between impaired maturation of phagosomes and defective Coxiella burnetii killing in patients with chronic Q fever. J Infect Dis 190:1767–1772

    PubMed  CAS  Google Scholar 

  • Ghigo E, Capo C, Raoult D, Mege JL (2006) Intracellular life of Coxiella burnetii in macrophages: insight Into Q fever. Curr Immunol Rev 2:225–232

    CAS  Google Scholar 

  • Grieshaber S, Swanson JA, Hackstadt T (2002) Determination of the physical environment within the Chlamydia trachomatis inclusion using ion-selective ratiometric probes. Cell Microbiol 4:273–283

    PubMed  CAS  Google Scholar 

  • Grieshaber SS, Grieshaber NA, Miller N, Hackstadt T (2006) Chlamydia trachomatis causes centrosomal defects resulting in chromosomal segregation abnormalities. Traffic 7:940–949

    PubMed  CAS  Google Scholar 

  • Gutierrez MG, Vazquez CL, Munafo DB, Zoppino FC, Beron W, Rabinovitch M, Colombo MI (2005) Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol 7:981–993

    PubMed  CAS  Google Scholar 

  • Haas A (2007) The phagosome: compartment with a license to kill. Traffic 8:311–330

    PubMed  CAS  Google Scholar 

  • Hackstadt T (1988) Steric hindrance of antibody binding to surface proteins of Coxiella burnetti by phase I lipopolysaccharide. Infect Immun 56:802–807

    PubMed  CAS  Google Scholar 

  • Hackstadt T, Williams JC (1981) Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc Natl Acad Sci U S A 78:3240–3244

    PubMed  CAS  Google Scholar 

  • Hackstadt T, Williams JC (1984) Metabolic adaptations of Coxiella burnetii to intraphagolysosomal growth. In: Lieve L, Schlessinger D (eds) Microbiology 1984. ASM Press, Washington, DC

    Google Scholar 

  • Hackstadt T, Peacock MG, Hitchcock PJ, Cole RL (1985) Lipopolysaccharide variation in Coxiella burnetii: intrastrain heterogeneity in structure and antigenicity. Infect Immun 48:359–365

    PubMed  CAS  Google Scholar 

  • Handley J, Paretsky D, Stueckemann J (1967) Electron microscopic observations of Coxiella burnetii in the guinea pig. J Bacteriol 94:263–267

    PubMed  CAS  Google Scholar 

  • Heinzen RA, Scidmore MA, Rockey DD, Hackstadt T (1996) Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect Immun 64:796–809

    PubMed  CAS  Google Scholar 

  • Henry RM, Hoppe AD, Joshi N, Swanson JA (2004) The uniformity of phagosome maturation in macrophages. J Cell Biol 164:185–194

    PubMed  CAS  Google Scholar 

  • Hill J, Samuel JE (2011) Coxiella burnetii acid phosphatase inhibits the release of reactive oxygen intermediates in polymorphonuclear leukocytes. Infect Immun 79:414–420

    PubMed  CAS  Google Scholar 

  • Hinrichs DJ, Jerrells TR (1976) In vitro evaluation of immunity to Coxiella burnetii. J Immunol 117:996–1003

    PubMed  CAS  Google Scholar 

  • Hirsch CS, Ellner JJ, Russell DG, Rich EA (1994) Complement receptor-mediated uptake and tumor necrosis factor-alpha-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J Immunol 152:743–753

    PubMed  CAS  Google Scholar 

  • Holden DW (2002) Trafficking of the Salmonella vacuole in macrophages. Traffic 3:161–169

    PubMed  CAS  Google Scholar 

  • Honstettre A, Imbert G, Ghigo E, Gouriet F, Capo C, Raoult D, Mege JL (2003) Dysregulation of cytokines in acute Q fever: role of interleukin-10 and tumor necrosis factor in chronic evolution of Q fever. J Infect Dis 187:956–962

    PubMed  CAS  Google Scholar 

  • Honstettre A, Ghigo E, Moynault A, Capo C, Toman R, Akira S, Takeuchi O, Lepidi H, Raoult D, Mege JL (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

    PubMed  CAS  Google Scholar 

  • Hoover TA, Culp DW, Vodkin MH, Williams JC, Thompson HA (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

    PubMed  CAS  Google Scholar 

  • Houde M, Bertholet S, Gagnon E, Brunet S, Goyette G, Laplante A, Princiotta MF, Thibault P, Sacks D, Desjardins M (2003) Phagosomes are competent organelles for antigen cross-presentation. Nature 425:402–406

    PubMed  CAS  Google Scholar 

  • Howe D, Mallavia LP (2000) Coxiella burnetii exhibits morphological change and delays phagolysosomal fusion after internalization by J774A.1 cells. Infect Immun 68:3815–3821

    PubMed  CAS  Google Scholar 

  • Howe D, Barrows LF, Lindstrom NM, Heinzen RA (2002) Nitric oxide inhibits Coxiella burnetii replication and parasitophorous vacuole maturation. Infect Immun 70:5140–5147

    PubMed  CAS  Google Scholar 

  • Howe D, Melnicakova J, Barak I, Heinzen RA (2003) Maturation of the Coxiella burnetii parasitophorous vacuole requires bacterial protein synthesis but not replication. Cell Microbiol 5:469–480

    PubMed  CAS  Google Scholar 

  • Howe D, Shannon JG, Winfree S, Dorward DW, Heinzen RA (2010) Coxiella burnetii phase I and II variants replicate with similar kinetics in degradative phagolysosome-like compartments of human macrophages. Infect Immun 78:3465–3474

    PubMed  CAS  Google Scholar 

  • Hu H, Sosnovsky G, Swartz HM (1992) Simultaneous measurements of the intra- and extra-cellular oxygen concentration in viable cells. Biochim Biophys Acta 1112:161–166

    PubMed  CAS  Google Scholar 

  • Hu C, Mayadas-Norton T, Tanaka K, Chan J, Salgame P (2000) Mycobacterium tuberculosis infection in complement receptor 3-deficient mice. J Immunol 165:2596–2602

    PubMed  CAS  Google Scholar 

  • Hussain SK, Broederdorf LJ, Shama UM, Voth DE (2010) Host kinase activity is required for Coxiella burnetii parasitophorous vacuole formation. Front Microbiol 1:137

    PubMed  Google Scholar 

  • Izzo AA, Marmion BP (1993) Variation in interferon-gamma responses to Coxiella burnetii antigens with lymphocytes from vaccinated or naturally infected subjects. Clin Exp Immunol 94:507–515

    PubMed  CAS  Google Scholar 

  • Khavkin T, Tabibzadeh SS (1988) Histologic, immunofluorescence, and electron microscopic study of infectious process in mouse lung after intranasal challenge with Coxiella burnetii. Infect Immun 56:1792–1799

    PubMed  CAS  Google Scholar 

  • Koster FT, Williams JC, Goodwin JS (1985) Cellular immunity in Q fever: specific lymphocyte unresponsiveness in Q fever endocarditis. J Infect Dis 152:1283–1289

    PubMed  CAS  Google Scholar 

  • Kumar Y, Valdivia RH (2008) Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds. Cell Host Microbe 4:159–169

    PubMed  CAS  Google Scholar 

  • Lem L, Riethof DA, Scidmore-Carlson M, Griffiths GM, Hackstadt T, Brodsky FM (1999) Enhanced interaction of HLA-DM with HLA-DR in enlarged vacuoles of hereditary and infectious lysosomal diseases. J Immunol 162:523–532

    PubMed  CAS  Google Scholar 

  • Li YP, Curley G, Lopez M, Chavez M, Glew R, Aragon A, Kumar H, Baca OG (1996) Protein-tyrosine phosphatase activity of Coxiella burnetii that inhibits human neutrophils. Acta Virol 40:263–272

    PubMed  CAS  Google Scholar 

  • Lubick K, Radke M, Jutila M (2007) Securinine, a GABAA receptor antagonist, enhances macrophage clearance of phase II C. burnetii: comparison with TLR agonists. J Leukoc Biol 82:1062–1069

    PubMed  CAS  Google Scholar 

  • Luhrmann A, Nogueira CV, Carey KL, Roy CR (2010) Inhibition of pathogen-induced apoptosis by a Coxiella burnetii type IV effector protein. Proc Natl Acad Sci U S A 107:18997–19001

    PubMed  CAS  Google Scholar 

  • Luzio JP, Pryor PR, Bright NA (2007) Lysosomes: fusion and function. Nat Rev Mol Cell Biol 8:622–632

    PubMed  CAS  Google Scholar 

  • Luzio JP, Parkinson MD, Gray SR, Bright NA (2009) The delivery of endocytosed cargo to lysosomes. Biochem Soc Trans 37:1019–1021

    PubMed  CAS  Google Scholar 

  • Mahapatra S, Ayoubi P, Shaw EI (2010) Coxiella burnetii Nine Mile II proteins modulate gene expression of monocytic host cells during infection. BMC Microbiol 10:244

    PubMed  Google Scholar 

  • Maurin M, Benoliel AM, Bongrand P, Raoult D (1992a) Phagolysosomal alkalinization and the bactericidal effect of antibiotics: the Coxiella burnetii paradigm. J Infect Dis 166:1097–1102

    PubMed  CAS  Google Scholar 

  • Maurin M, Benoliel AM, Bongrand P, Raoult D (1992b) Phagolysosomes of Coxiella burnetii-infected cell lines maintain an acidic pH during persistent infection. Infect Immun 60:5013–5016

    PubMed  CAS  Google Scholar 

  • Meconi S, Jacomo V, Boquet P, Raoult D, Mege JL, Capo C (1998) Coxiella burnetii induces reorganization of the actin cytoskeleton in human monocytes. Infect Immun 66:5527–5533

    PubMed  CAS  Google Scholar 

  • Meconi S, Capo C, Remacle-Bonnet M, Pommier G, Raoult D, Mege JL (2001) Activation of protein tyrosine kinases by Coxiella burnetii: role in actin cytoskeleton reorganization and bacterial phagocytosis. Infect Immun 69:2520–2526

    PubMed  CAS  Google Scholar 

  • Meghari S, Honstettre A, Lepidi H, Ryffel B, Raoult D, Mege JL (2005) TLR2 is necessary to inflammatory response in Coxiella burnetii infection. Ann N Y Acad Sci 1063:161–166

    PubMed  Google Scholar 

  • Meresse S, Steele-Mortimer O, Finlay BB, Gorvel JP (1999a) The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J 18:4394–4403

    PubMed  CAS  Google Scholar 

  • Meresse S, Steele-Mortimer O, Moreno E, Desjardins M, Finlay B, Gorvel JP (1999b) Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat Cell Biol 1:183–188

    Google Scholar 

  • Moos A, Hackstadt T (1987) Comparative virulence of intra- and interstrain lipopolysaccharide variants of Coxiella burnetii in the guinea pig model. Infect Immun 55:1144–1150

    PubMed  CAS  Google Scholar 

  • Newton HJ, Ang DK, Van Driel IR, Hartland EL (2010) Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23:274–298

    PubMed  CAS  Google Scholar 

  • Ochoa-Reparaz J, Sentissi J, Trunkle T, Riccardi C, Pascual DW (2007) Attenuated Coxiella burnetii phase II causes a febrile response in gamma interferon knockout and Toll-like receptor 2 knockout mice and protects against reinfection. Infect Immun 75:5845–5858

    PubMed  CAS  Google Scholar 

  • Oh YK, Swanson JA (1996) Different fates of phagocytosed particles after delivery into macrophage lysosomes. J Cell Biol 132:585–593

    PubMed  CAS  Google Scholar 

  • Omsland A, Cockrell DC, Howe D, Fischer ER, Virtaneva K, Sturdevant DE, Porcella SF, Heinzen RA (2009) Host cell-free growth of the Q fever bacterium Coxiella burnetii. Proc Natl Acad Sci U S A 106:4430–4434

    PubMed  CAS  Google Scholar 

  • Omsland A, Gilk SD, Shannon JG, Beare PA, Voth DE, Howe D, Cockrell DC, Heinzen RA (2010) Exploring the cause of human Q fever: recent advances in Coxiella burnetii research. In: Georgiev V (ed) National Institute of Allergy and Infectious Diseases: Intramural Research, vol 3. Springer, New York

    Google Scholar 

  • Ormsbee RA (1952) The growth of Coxiella burnetii in embryonated eggs. J Bacteriol 63:73–86

    PubMed  CAS  Google Scholar 

  • Pan X, Luhrmann A, Satoh A, Laskowski-Arce MA, Roy CR (2008) Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320:1651–1654

    PubMed  CAS  Google Scholar 

  • Park DR, Skerrett SJ (1996) IL-10 enhances the growth of Legionella pneumophila in human mononuclear phagocytes and reverses the protective effect of IFN-gamma: differential responses of blood monocytes and alveolar macrophages. J Immunol 157:2528–2538

    PubMed  CAS  Google Scholar 

  • Patil S, Jedsadayanmata A, Wencel-Drake JD, Wang W, Knezevic I, Lam SC (1999) Identification of a talin-binding site in the integrin beta(3) subunit distinct from the NPLY regulatory motif of post-ligand binding functions. The talin n-terminal head domain interacts with the membrane-proximal region of the beta(3) cytoplasmic tail. J Biol Chem 274:28575–28583

    PubMed  CAS  Google Scholar 

  • Ren Q, Robertson SJ, Howe D, Barrows LF, Heinzen RA (2003) Comparative DNA microarray analysis of host cell transcriptional responses to infection by Coxiella burnetii or Chlamydia trachomatis. Ann N Y Acad Sci 990:701–713

    PubMed  CAS  Google Scholar 

  • Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735–749

    PubMed  CAS  Google Scholar 

  • Rohde K, Yates RM, Purdy GE, Russell DG (2007) Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 219:37–54

    PubMed  CAS  Google Scholar 

  • Roman MJ, Coriz PD, Baca OG (1986) A proposed model to explain persistent infection of host cells with Coxiella burnetii. J Gen Microbiol 132:1415–1422

    PubMed  CAS  Google Scholar 

  • Romano PS, Gutierrez MG, Beron W, Rabinovitch M, Colombo MI (2007) The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell Microbiol 9:891–909

    PubMed  CAS  Google Scholar 

  • Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12:697–715

    PubMed  CAS  Google Scholar 

  • Santic M, Molmeret M, Abu Kwaik Y (2005) Maturation of the Legionella pneumophila-containing phagosome into a phagolysosome within gamma interferon-activated macrophages. Infect Immun 73:3166–3171

    PubMed  CAS  Google Scholar 

  • Sauer JD, Shannon JG, Howe D, Hayes SF, Swanson MS, Heinzen RA (2005) Specificity of Legionella pneumophila and Coxiella burnetii vacuoles and versatility of Legionella pneumophila revealed by coinfection. Infect Immun 73:4494–4504

    PubMed  CAS  Google Scholar 

  • Schaible UE, Schlesinger PH, Steinberg TH, Mangel WF, Kobayashi T, Russell DG (1999) Parasitophorous vacuoles of Leishmania mexicana acquire macromolecules from the host cell cytosol via two independent routes. J Cell Sci 112:681–693

    PubMed  CAS  Google Scholar 

  • Scott CC, Botelho RJ, Grinstein S (2003) Phagosome maturation: a few bugs in the system. J Membr Biol 193:137–152

    PubMed  CAS  Google Scholar 

  • Seshadri R, Paulsen IT, Eisen JA, Read TD, Nelson KE, Nelson WC, Ward NL, Tettelin H, Davidsen TM, Beanan MJ, Deboy RT, Daugherty SC, Brinkac LM, Madupu R, Dodson RJ, Khouri HM, Lee KH, Carty HA, Scanlan D, Heinzen RA, Thompson HA, Samuel JE, Fraser CM, Heidelberg JF (2003) Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci U S A 100:5455–5460

    PubMed  CAS  Google Scholar 

  • Shannon JG, Howe D, Heinzen RA (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

    PubMed  CAS  Google Scholar 

  • Shannon JG, Cockrell DC, Takahashi K, Stahl GL, Heinzen RA (2009) Antibody-mediated immunity to the obligate intracellular bacterial pathogen Coxiella burnetii is Fc receptor- and complement-independent. BMC Immunol 10:26

    PubMed  Google Scholar 

  • Sidhu GS, Singh AK, Sundarrajan RN, Sundar SV, Maheshwari RK (1999) Role of vacuolar H(+)-ATPase in interferon-induced inhibition of viral glycoprotein transport. J Interferon Cytokine Res 19:1297–1303

    PubMed  CAS  Google Scholar 

  • Siemsen DW, Kirpotina LN, Jutila MA, Quinn MT (2009) Inhibition of the human neutrophil NADPH oxidase by Coxiella burnetii. Microbes Infect 11:671–679

    PubMed  CAS  Google Scholar 

  • Stein A, Louveau C, Lepidi H, Ricci F, Baylac P, Davoust B, Raoult D (2005) Q fever pneumonia: virulence of Coxiella burnetii pathovars in a murine model of aerosol infection. Infect Immun 73:2469–2477

    PubMed  CAS  Google Scholar 

  • Stuart LM, Ezekowitz RA (2005) Phagocytosis: elegant complexity. Immunity 22:539–550

    PubMed  CAS  Google Scholar 

  • Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S (2005) Macrophage receptors and immune recognition. Annu Rev Immunol 23:901–944

    PubMed  CAS  Google Scholar 

  • Tsang AW, Oestergaard K, Myers JT, Swanson JA (2000) Altered membrane trafficking in activated bone marrow-derived macrophages. J Leukoc Biol 68:487–494

    PubMed  CAS  Google Scholar 

  • Tujulin E, Macellaro A, Lilliehook B, Norlander L (1998) Effect of endocytosis inhibitors on Coxiella burnetii interaction with host cells. Acta Virol 42:125–131

    PubMed  CAS  Google Scholar 

  • Underhill DM (2004) Toll-like receptors and microbes take aim at each other. Curr Opin Immunol 16:483–487

    PubMed  CAS  Google Scholar 

  • Vazquez CL, Colombo MI (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

    PubMed  CAS  Google Scholar 

  • Via LE, Fratti RA, Mcfalone M, Pagan-Ramos E, Deretic D, Deretic V (1998) Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111:897–905

    PubMed  CAS  Google Scholar 

  • Vishwanath S, Hackstadt T (1988) Lipopolysaccharide phase variation determines the complement-mediated serum susceptibility of Coxiella burnetii. Infect Immun 56:40–44

    PubMed  CAS  Google Scholar 

  • Voth DE, Heinzen RA (2007) Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell Microbiol 9:829–840

    PubMed  CAS  Google Scholar 

  • Voth DE, Heinzen RA (2009a) Coxiella type IV secretion and cellular microbiology. Curr Opin Microbiol 12:74–80

    PubMed  CAS  Google Scholar 

  • Voth DE, Heinzen RA (2009b) Sustained activation of Akt and Erk1/2 is required for Coxiella burnetii antiapoptotic activity. Infect Immun 77:205–213

    PubMed  CAS  Google Scholar 

  • Voth DE, Howe D, Heinzen RA (2007) Coxiella burnetii inhibits apoptosis in human THP-1 cells and monkey primary alveolar macrophages. Infect Immun 75:4263–4271

    PubMed  CAS  Google Scholar 

  • Voth DE, Howe D, Beare PA, Vogel JP, Unsworth N, Samuel JE, Heinzen RA (2009) The Coxiella burnetii ankyrin repeat domain-containing protein family is heterogeneous, with C-terminal truncations that influence Dot/Icm-mediated secretion. J Bacteriol 191:4232–4242

    PubMed  CAS  Google Scholar 

  • Voth DE, Beare PA, Howe D, Sharma UM, Samoilis G, Cockrell DC, Omsland A, Heinzen RA (2011) The Coxiella burnetii cryptic plasmid is enriched in genes encoding type IV secretion system substrates. J Bacteriol 193:1493–1503

    PubMed  CAS  Google Scholar 

  • Weber SS, Ragaz C, Hilbi H (2009) Pathogen trafficking pathways and host phosphoinositide metabolism. Mol Microbiol 71:1341–1352

    PubMed  CAS  Google Scholar 

  • Weisburg WG, Dobson ME, Samuel JE, Dasch GA, Mallavia LP, Baca O, Mandelco L, Sechrest JE, Weiss E, Woese CR (1989) Phylogenetic diversity of the Rickettsiae. J Bacteriol 171:4202–4206

    PubMed  CAS  Google Scholar 

  • Weiss E (1973) Growth and physiology of rickettsiae. Bacteriol Rev 37:259–283

    PubMed  CAS  Google Scholar 

  • Weiss E, Moulder JW (1984) Order I. Rickettsiales Gieszczkiewicz 1939, 25AL. The Williams & Wilkens Co., Baltimore

    Google Scholar 

  • Wesolowski J, Paumet F (2010) SNARE motif: a common motif used by pathogens to manipulate membrane fusion. Virulence 1:319–324

    PubMed  Google Scholar 

  • West MA, Wallin RP, Matthews SP, Svensson HG, Zaru R, Ljunggren HG, Prescott AR, Watts C (2004) Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305:1153–1157

    PubMed  CAS  Google Scholar 

  • Williams JC, Peacock MG, Mccaul TF (1981) Immunological and biological characterization of Coxiella burnetii, phases I and II, separated from host components. Infect Immun 32:840–851

    PubMed  CAS  Google Scholar 

  • Yates RM, Russell DG (2005) Phagosome maturation proceeds independently of stimulation of toll-like receptors 2 and 4. Immunity 23:409–417

    PubMed  CAS  Google Scholar 

  • Zaidi N, Maurer A, Nieke S, Kalbacher H (2008) Cathepsin D: a cellular roadmap. Biochem Biophys Res Commun 376:5–9

    PubMed  CAS  Google Scholar 

  • Zamboni DS (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

    PubMed  CAS  Google Scholar 

  • Zamboni DS, Rabinovitch M (2003) Nitric oxide partially controls Coxiella burnetii phase II infection in mouse primary macrophages. Infect Immun 71:1225–1233

    PubMed  CAS  Google Scholar 

  • Zamboni DS, Rabinovitch M (2004) Phagocytosis of apoptotic cells increases the susceptibility of macrophages to infection with Coxiella burnetii Phase II through down-modulation of nitric oxide production. Infect Immun 72:2075–2080

    PubMed  CAS  Google Scholar 

  • Zamboni DS, Mortara RA, Freymuller E, Rabinovitch M (2002) Mouse resident peritoneal macrophages partially control in vitro infection with Coxiella burnetii phase II. Microbes Infect 4:591–598

    PubMed  Google Scholar 

  • Zamboni DS, Campos MA, Torrecilhas AC, Kiss K, Samuel JE, Golenbock DT, Lauw FN, Roy CR, Almeida IC, Gazzinelli RT (2004) Stimulation of toll-like receptor 2 by Coxiella burnetii is required for macrophage production of pro-inflammatory cytokines and resistance to infection. J Biol Chem 279:54405–54415

    PubMed  CAS  Google Scholar 

  • Zerial M, Mcbride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117

    PubMed  CAS  Google Scholar 

  • Zoppino FC, Militello RD, Slavin I, Alvarez C, Colombo MI (2010) Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 11:1246–1261

    PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Dale Howe and Stacy Gilk for critical reading of the manuscript. This research was supported by the CNRS (E. G.), the Agencia Nacional de Promoción Científica y Tecnológica and SECTyP (Universidad Nacional de Cuyo) (M. I. C.) and the Intramural Research Program of the National Institutes of Health, National Institute of Allergy and Infectious Diseases (R. A. H.)

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Ghigo, E., Colombo, M.I., Heinzen, R.A. (2012). The Coxiella burnetii Parasitophorous Vacuole. In: Toman, R., Heinzen, R., Samuel, J., Mege, JL. (eds) Coxiella burnetii: Recent Advances and New Perspectives in Research of the Q Fever Bacterium. Advances in Experimental Medicine and Biology, vol 984. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4315-1_8

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