The Coxiella burnetii parasitophorous vacuole

Advances in Experimental Medicine and Biology

Volumn 984, Issue , 2012, Pages 141-169

  Ghigo, Eric ^a   Colombo, María I ^b   Heinzen, Robert A ^c  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b Instituto de Histologia y Embriologia   (Argentina)

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

Author keywords

Autophagy; Endosome; Integrin; Lipopolysaccharide; Lysosome; Macrophage; Monocyte; Parasitophorous vacuole; Phase variation; Secretory pathway

Indexed keywords

CYTOKINE; INTEGRIN; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR;

ACIDITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BIOGENESIS; CELL MATURATION; CELL MIGRATION; CELL STRUCTURE; CELL VACUOLE; COXIELLA BURNETII; CYTOLOGY; CYTOSKELETON; EPITHELIUM CELL; HOST CELL; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INTRACELLULAR TRANSPORT; MACROPHAGE; MICROBIAL ACTIVITY; MONONUCLEAR PHAGOCYTE; NONHUMAN; PARASITOPHOROUS VACUOLE; PHAGOCYTOSIS; PRIORITY JOURNAL; Q FEVER; SECRETORY PATHWAY; TROPHOBLAST;

ANIMALS; COXIELLA BURNETII; HUMANS; LYSOSOMES; MONONUCLEAR PHAGOCYTE SYSTEM; PHAGOSOMES; VACUOLES;

BACTERIA (MICROORGANISMS); COXIELLA BURNETII; EUKARYOTA;

EID: 84863739064     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-4315-1_8     Document Type: Article

References (153)

1. 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
2. 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
3. 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
4. Akporiaye ET, Stefanovich D, Tsosie V, Baca G (1990) Coxiella burnetii fails to stimulate human neutrophil superoxide anion production. Acta Virol 34:64-70
5. Alonso A, Garcia-Del Portillo F (2004) Hijacking of eukaryotic functions by intracellular bacterial pathogens. Int Microbiol 7:181-191
6. Amano K, Williams JC (1984) Chemical and immunological characterization of lipopolysaccharides from phase I and phase II Coxiella burnetii . J Bacteriol 160:994-1002
7. 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
8. Aragon AS, Pereira HA, Baca OG (1995) A cationic antimicrobial peptide enhances the infectivity of Coxiella burnetii . Acta Virol 39:223-226
9. 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
10. 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
11. 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
12. 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
13. Baca OG, Klassen DA, Aragon AS (1993a) Entry of Coxiella burnetii into host cells. Acta Virol 37:143-155
14. 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
15. Baca OG, Li YP, Kumar H (1994) Survival of the Q fever agent Coxiella burnetii in the phagolysosome. Trends Microbiol 2:476-480
16. Barry AO, Mege JL, Ghigo E (2011) Hijacked phagosomes and leukocyte activation: an intimate relationship. J Leukoc Biol 89:373-382
17. 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
18. 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
19. 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
20. Beare PA, Sandoz KM, Omsland A, Rockey DD, Heinzen RA (2011) Advances in genetic manipulation of obligate intracellular bacterial pathogens. Front Microbiol. 2:97
21. 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
22. 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
23. 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
24. Blander JM, Medzhitov R (2004) Regulation of phagosome maturation by signals from toll-like receptors. Science 304:1014-1018
25. 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
26. 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
27. 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
28. Bucci C, Thomsen P, Nicoziani P, Mccarthy J, Van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11:467-480
29. Burnet FM, Freeman M (1937) Experimental studies on the virus of "Q" fever. Med J Aust 2:299-305
30. 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
31. Burton PR, Stueckemann J, Paretsky D (1975) Electron microscopy studies of the limiting layers of the rickettsia Coxiella burneti . J Bacteriol 122:316-324
32. 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
33. 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
34. 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
35. 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
36. 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
37. 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 a v b 3 integrin and CR3. J Immunol 163:6078-6085
38. 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
39. Chen C, Banga S, Mertens K, Weber MM, Gorbaslieva I, Tan Y, Luo ZQ, Samuel JE (2010) Largescale identi fication and translocation of type IV secretion substrates by Coxiella burnetii . Proc Natl Acad Sci U S A 107:21755-21760
40. Coleman SA, Fischer ER, Howe D, Mead DJ, Heinzen RA (2004) Temporal analysis of Coxiella burnetii morphological differentiation. J Bacteriol 186:7344-7352
41. Cooke RA (2008) Q fever. Was Edward Derrick's contribution undervalued? Med J Aust 189:660-662
42. Cossart P, Roy CR (2010) manipulation of host membrane machinery by bacterial pathogens. Curr Opin Cell Biol 22:547-554
43. Cossart P, Sansonetti PJ (2004) Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242-248
44. Cox HR (1938) A filter-passing infectious agent isolated from ticks. III. Description of organism and cultivation experiments. Public Health Rep 53:2270-2276
45. Cox HR (1939) Sudies of a filter-passing infectious agent isolated from ticks. V. Further attempts to cultivate in cell-free media. Suggested classi fication. Public Health Rep 54:1822-1827
46. 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
47. 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
48. Deretic V, Levine B (2009) Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5:527-549
49. Derrick EH (1937) "Q" fever, a new fever entity: clinical features, diagnosis, and laboratory investigation. Med J Aust 2:281-299
50. Desjardins M, Celis JE, Van Meer G, Dieplinger H, Jahraus A, Grif fiths G, Huber LA (1994) Molecular characterization of phagosomes. J Biol Chem 269:32194-321200
51. 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
52. 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
53. 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
54. 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
55. Grieshaber SS, Grieshaber NA, Miller N, Hackstadt T (2006) Chlamydia trachomatis causes centrosomal defects resulting in chromosomal segregation abnormalities. Traf fic 7:940-949
56. 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
57. Haas A (2007) The phagosome: compartment with a license to kill. Traf fic 8:311-330
58. Hackstadt T (1988) Steric hindrance of antibody binding to surface proteins of Coxiella burnetti by phase I lipopolysaccharide. Infect Immun 56:802-807
59. 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
60. 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
61. 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
62. Handley J, Paretsky D, Stueckemann J (1967) Electron microscopic observations of Coxiella burnetii in the guinea pig. J Bacteriol 94:263-267
63. 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
64. Henry RM, Hoppe AD, Joshi N, Swanson JA (2004) The uniformity of phagosome maturation in macrophages. J Cell Biol 164:185-194
65. Hill J, Samuel JE (2011) Coxiella burnetii acid phosphatase inhibits the release of reactive oxygen intermediates in polymorphonuclear leukocytes. Infect Immun 79:414-420
66. Hinrichs DJ, Jerrells TR (1976) In vitro evaluation of immunity to Coxiella burnetii . J Immunol 117:996-1003
67. 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
68. Holden DW (2002) Traf ficking of the Salmonella vacuole in macrophages. Traf fic 3:161-169
69. 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
70. 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, fi lamentous actin reorganization, and in flammatory responses through Toll-like receptor 4. J Immunol 172:3695-3703
71. 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
72. 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
73. 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
74. Howe D, Barrows LF, Lindstrom NM, Heinzen RA (2002) Nitric oxide inhibits Coxiella burnetii replication and parasitophorous vacuole maturation. Infect Immun 70:5140-5147
75. 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
76. 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
77. 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
78. Hu C, mayadas-Norton T, Tanaka K, Chan J, Salgame P (2000) Mycobacterium tuberculosis infection in complement receptor 3-de ficient mice. J Immunol 165:2596-2602
79. Hussain SK, Broederdorf LJ, Shama UM, Voth DE (2010) Host kinase activity is required for Coxiella burnetii parasitophorous vacuole formation. Front Microbiol 1:137
80. 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
81. Khavkin T, Tabibzadeh SS (1988) Histologic, immuno fluorescence, and electron microscopic study of infectious process in mouse lung after intranasal challenge with Coxiella burnetii . Infect Immun 56:1792-1799
82. Koster FT, Williams JC, Goodwin JS (1985) Cellular immunity in Q fever: speci fic lymphocyte unresponsiveness in Q fever endocarditis. J Infect Dis 152:1283-1289
83. 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
84. Lem L, Riethof DA, Scidmore-Carlson M, Grif fiths 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
85. Li YP, Curley G, Lopez M, Chavez M, Glew R, Aragon A, Kumar H, Baca OG (1996) Proteintyrosine phosphatase activity of Coxiella burnetii that inhibits human neutrophils. Acta Virol 40:263-272
86. 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
87. 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
88. Luzio JP, Pryor PR, Bright NA (2007) Lysosomes: fusion and function. Nat Rev Mol Cell Biol 8:622-632
89. Luzio JP, Parkinson MD, Gray SR, Bright NA (2009) The delivery of endocytosed cargo to lysosomes. Biochem Soc Trans 37:1019-1021
90. 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
91. 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
92. 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
93. 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
94. 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
95. Meghari S, Honstettre A, Lepidi H, Ryffel B, Raoult D, Mege JL (2005) TLR2 is necessary to in flammatory response in Coxiella burnetii infection. Ann N Y Acad Sci 1063:161-166
96. 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
97. 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
98. 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
99. Newton HJ, Ang DK, Van Driel IR, Hartland EL (2010) Molecular pathogenesis of infections caused by Legionella pneumophila . Clin Microbiol Rev 23:274-298
100. 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
101. Oh YK, Swanson JA (1996) Different fates of phagocytosed particles after delivery into macrophage lysosomes. J Cell Biol 132:585-593
102. 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
103. 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
104. Ormsbee RA (1952) The growth of Coxiella burnetii in embryonated eggs. J Bacteriol 63:73-86
105. 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
106. 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
107. Patil S, Jedsadayanmata A, Wencel-Drake JD, Wang W, Knezevic I, Lam SC (1999) Identi fication 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 membraneproximal region of the beta(3) cytoplasmic tail. J Biol Chem 274:28575-28583
108. 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
109. 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
110. Rohde K, Yates RM, Purdy GE, Russell DG (2007) Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 219:37-54
111. 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
112. Romano PS, Gutierrez MG, Beron W, Rabinovitch M, Colombo MI (2007) The autophagic pathway is actively modulated by phase II Coxiella burnetii to ef ficiently replicate in the host cell. Cell Microbiol 9:891-909
113. Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12:697-715
114. 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
115. Sauer JD, Shannon JG, Howe D, Hayes SF, Swanson MS, Heinzen RA (2005) Speci ficity of Legionella pneumophila and Coxiella burnetii vacuoles and versatility of Legionella pneumophila revealed by coinfection. Infect Immun 73:4494-4504
116. 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
117. Scott CC, Botelho RJ, Grinstein S (2003) Phagosome maturation: a few bugs in the system. J Membr Biol 193:137-152
118. 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
119. 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
120. 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 complementindependent. BMC Immunol 10:26
121. 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
122. Siemsen DW, Kirpotina LN, Jutila ma, Quinn MT (2009) Inhibition of the human neutrophil NADPH oxidase by Coxiella burnetii . Microbes Infect 11:671-679
123. 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
124. Stuart LM, Ezekowitz RA (2005) Phagocytosis: elegant complexity. Immunity 22:539-550
125. 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
126. Tsang AW, Oestergaard K, Myers JT, Swanson JA (2000) Altered membrane trafficking in activated bone marrow-derived macrophages. J Leukoc Biol 68:487-494
127. 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
128. Underhill DM (2004) Toll-like receptors and microbes take aim at each other. Curr Opin Immunol 16:483-487
129. 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
130. 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
131. Vishwanath S, Hackstadt T (1988) Lipopolysaccharide phase variation determines the complementmediated serum susceptibility of Coxiella burnetii . Infect Immun 56:40-44
132. Voth DE, Heinzen RA (2007) Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii . Cell Microbiol 9:829-840
133. Voth DE, Heinzen RA (2009a) Coxiella type IV secretion and cellular microbiology. Curr Opin Microbiol 12:74-80
134. Voth DE, Heinzen RA (2009b) Sustained activation of Akt and Erk1/2 is required for Coxiella burnetii antiapoptotic activity. Infect Immun 77:205-213
135. 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
136. 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 in fluence Dot/Icm-mediated secretion. J Bacteriol 191:4232-4242
137. 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
138. Weber SS, Ragaz C, Hilbi H (2009) Pathogen traf ficking pathways and host phosphoinositide metabolism. Mol Microbiol 71:1341-1352
139. 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
140. Weiss E (1973) Growth and physiology of rickettsiae. Bacteriol Rev 37:259-283
141. Weiss E, Moulder JW (1984) Order I. Rickettsiales Gieszczkiewicz 1939, 25 AL . The Williams & Wilkens Co., Baltimore
142. Wesolowski J, Paumet F (2010) SNARE motif: a common motif used by pathogens to manipulate membrane fusion. Virulence 1:319-324
143. 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
144. 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
145. Yates RM, Russell DG (2005) Phagosome maturation proceeds independently of stimulation of toll-like receptors 2 and 4. Immunity 23:409-417
146. Zaidi N, maurer A, Nieke S, Kalbacher H (2008) Cathepsin D: a cellular roadmap. Biochem Biophys Res Commun 376:5-9
147. 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
148. Zamboni DS, Rabinovitch M (2003) Nitric oxide partially controls Coxiella burnetii phase II infection in mouse primary macrophages. Infect Immun 71:1225-1233
149. 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
150. 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
151. 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-in flammatory cytokines and resistance to infection. J Biol Chem 279:54405-54415
152. Zerial M, Mcbride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107-117
153. Zoppino FC, Militello RD, Slavin I, Alvarez C, Colombo MI (2010) Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traf fic 11:1246-1261