Chapter 23 : Contrasting Lifestyles Within the Host Cell

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Contrasting Lifestyles Within the Host Cell, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819286/9781555819279_Chap23-1.gif /docserver/preview/fulltext/10.1128/9781555819286/9781555819279_Chap23-2.gif


Bacterial pathogens that adopt an intracellular lifestyle often avoid many challenges that are faced by their extracellular counterparts. However, upon entering the host cell, they have a new set of trials with which to contend. Upon phagocytic uptake or entry by receptor-mediated endocytosis, they immediately traffic to a degradative subcellular compartment. Successful intracellular pathogens have adopted different strategies to avoid trafficking of their initial phagosome along the endocytic pathway to fusion with the lysosome, a subcellular compartment that has specifically evolved to degrade them. In this chapter, we will compare the different molecular mechanisms employed by four intracellular pathogens that have adopted distinct vacuolar niches and lifestyles. Many vacuolar pathogens alter their initial phagosomal compartment to stall or exit the endocytic pathway and thereby avoid elimination. Yet a few species require at least some interaction with lysosomes for completion of their infectious cycle. In this chapter, we will compare the strategies employed by and to avoid lysosomal fusion with those of , whose vacuole interacts with lysosomes transiently, and , a bacterium adapted to growth in a compartment that closely resembles a terminal phagolysosome.

Citation: Case E, Samuel J. 2016. Contrasting Lifestyles Within the Host Cell, p 667-692. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0014-2015
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Endosomal trafficking is coordinated by exchanges of lipids and Rab-GTPases. The normal endosomal pathway is illustrated here with major regulatory factors highlighted at each step. After uptake of a cargo, the phagosome fuses with early endosomes, acquiring Rab5, its effector EEA1, and VPS34, which coordinate the change in lipid profile of the endosomal membrane. Soon after, the compartment fuses with late endosomes, and Rab5 is exchanged for Rab7 and its effector RILP. LAMP and V-ATPases are also characteristic of the late endosome. Finally, the late endosome fuses with lysosomes, at which point the compartment is fully matured and highly degradative.

Citation: Case E, Samuel J. 2016. Contrasting Lifestyles Within the Host Cell, p 667-692. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0014-2015
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Intracellular pathogens have evolved distinct trafficking pathways to arrive within their ideal replicative niche. Intracellular trafficking pathways are shown for (Mtb), (Chl), (Br), and (Cb). Key regulatory factors, such as Rab-GTPases, lipids, and bacterial factors are shown. sis fuses with early endosomes (EE) but inhibits fusion with late endosomes (LE) and replicates in a compartment (MCP) that is stalled at an early point along the endocytic pathway. Chl traffics away from the endosomal pathway and escapes to replicate in a Golgi-associated Inclusion. Br allows EE and LE fusion as well as limited lysosomal fusion before trafficking to the ER to replicate in rBCVs (replicative -containing vacuoles). Cb interacts with EE, autophagosomes, and LE and allows lysosomal fusion to arrive in the CCV (-containing vacuole), which resembles a terminal phagolysosome.

Citation: Case E, Samuel J. 2016. Contrasting Lifestyles Within the Host Cell, p 667-692. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0014-2015
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Fredlund J,, Enninga J . 2014. Cytoplasmic access by intracellular bacterial pathogens. Trends Microbiol 22 : 128 137.[PubMed] [CrossRef]
2. Gomes LC,, Dikic I . 2014. Autophagy in antimicrobial immunity. Mol Cell 54 : 224 233.[PubMed] [CrossRef]
3. Kinchen JM,, Ravichandran KS . 2008. Phagosome maturation: going through the acid test. Nat Rev Mol Cell Biol 9 : 781 795.[PubMed] [CrossRef]
4. Vieira OV,, Botelho RJ,, Rameh L,, Brachmann SM,, Matsuo T,, Davidson HW,, Schreiber A,, Backer JM,, Cantley LC,, Grinstein S . 2001. Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J Cell Biol 155 : 19 25.[PubMed] [CrossRef]
5. Di Paolo G,, De Camilli P . 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature 443 : 651 657.[PubMed] [CrossRef]
6. Simonsen A,, Lippe R,, Christoforidis S,, Gaullier J-M,, Brech A,, Callaghan J,, Toh B-H,, Murphy C,, Zerial M,, Stenmark H . 1998. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394 : 494 498.[PubMed] [CrossRef]
7. Hackam DJ,, Rotstein OD,, Zhang W-J,, Demaurex N,, Woodside M,, Tsai O,, Grinstein S . 1997. Regulation of phagosomal acidification: differential targeting of Na +/H +exchangers, Na +/K +-ATPases, and vacuolar-type H +-ATPases. J Biol Chem 272 : 29810 29820.[PubMed] [CrossRef]
8. Kinchen JM,, Ravichandran KS . 2010. Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464 : 778 782.[PubMed] [CrossRef]
9. Poteryaev D,, Datta S,, Ackema K,, Zerial M,, Spang A . 2010. Identification of the switch in early-to-late endosome transition. Cell 141 : 497 508.[PubMed] [CrossRef]
10. Huynh KK,, Eskelinen EL,, Scott CC,, Malevanets A,, Saftig P,, Grinstein S . 2007. LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J 26 : 313 324.[PubMed] [CrossRef]
11. Harrison RE,, Bucci C,, Vieira OV,, Schroer TA,, Grinstein S . 2003. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol 23 : 6494 6506.[PubMed] [CrossRef]
12. Flannagan RS,, Jaumouillé V,, Grinstein S . 2012. The cell biology of phagocytosis. Annu Rev Pathol 7 : 61 98.[PubMed] [CrossRef]
13. Jabado N,, Jankowski A,, Dougaparsad S,, Picard V,, Grinstein S,, Gros P . 2000. Natural resistance to intracellular infections: natural resistance–associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J Exp Med 192 : 1237 1248.[PubMed] [CrossRef]
14. Yates RM,, Hermetter A,, Russell DG . 2005. The kinetics of phagosome maturation as a function of phagosome/lysosome fusion and acquisition of hydrolytic activity. Traffic 6 : 413 420.[PubMed] [CrossRef]
15. Zumla A,, Raviglione M,, Hafner R,, von Reyn CF . 2013. Tuberculosis. N Engl J Med 368 : 745 755.[PubMed] [CrossRef]
16. Forrellad MA,, Klepp LI,, Gioffre A,, Sabio y Garcia J,, Morbidoni HR,, de la Paz Santangelo M,, Cataldi AA,, Bigi F . 2013. Virulence factors of the Mycobacterium tuberculosis complex. Virulence 4 : 3 66.[PubMed] [CrossRef]
17. Matteelli A,, Roggi A,, Carvalho AC . 2014. Extensively drug-resistant tuberculosis: epidemiology and management. Clin Epidemiol 6 : 111 118.[PubMed] [CrossRef]
18. Vergne I,, Chua J,, Singh SB,, Deretic V . 2004. Cell biology of Mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol 20 : 367 394.[PubMed] [CrossRef]
19. Cambier CJ,, Falkow S,, Ramakrishnan L . 2014. Host evasion and exploitation schemes of Mycobacterium tuberculosis . Cell 159 : 1497 1509.[PubMed] [CrossRef]
20. Clemens DL,, Horwitz MA . 1995. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181 : 257 270.[CrossRef]
21. Via LE,, Deretic D,, Ulmer RJ,, Hibler NS,, Huber LA,, Deretic V . 1997. Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by Rab5 and Rab7. J Biol Chem 272 : 13326 13331.[PubMed] [CrossRef]
22. Kang BK,, Schlesinger LS . 1998. Characterization of mannose receptor-dependent phagocytosis mediated by Mycobacterium tuberculosis lipoarabinomannan. Infect Immun 66 : 2769 2777.[PubMed]
23. Ernst JD . 1998. Macrophage receptors for Mycobacterium tuberculosis . Infect Immun 66 : 1277 1281.[PubMed]
24. Gatfield J,, Pieters J . 2000. Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288 : 1647 1650.[PubMed] [CrossRef]
25. Clemens DL,, Lee BY,, Horwitz MA . 2000. Mycobacterium tuberculosis and Legionella pneumophila phagosomes exhibit arrested maturation despite acquisition of Rab7. Infect Immun 68 : 5154 5166.[PubMed] [CrossRef]
26. Clemens DL,, Lee BY,, Horwitz MA . 2000. Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal fate. Infect Immun 68 : 2671 2684.[PubMed] [CrossRef]
27. Vergne I,, Chua J,, Deretic V . 2003. Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca 2+/calmodulin-PI3K hVPS34 cascade. J Exp Med 198 : 653 659.[PubMed] [CrossRef]
28. Malik ZA,, Denning GM,, Kusner DJ . 2000. Inhibition of Ca(2+) signaling by Mycobacterium tuberculosis is associated with reduced phagosome-lysosome fusion and increased survival within human macrophages. J Exp Med 191 : 287 302.[PubMed] [CrossRef]
29. Fratti RA,, Chua J,, Deretic V . 2003. Induction of p38 mitogen-activated protein kinase reduces early endosome autoantigen 1 (EEA1) recruitment to phagosomal membranes. J Biol Chem 278 : 46961 46967.[PubMed] [CrossRef]
30. Cavalli V,, Vilbois F,, Corti M,, Marcote MJ,, Tamura K,, Karin M,, Arkinstall S,, Gruenberg J . 2001. The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol Cell 7 : 421 432.[CrossRef]
31. Fratti RA,, Chua J,, Vergne I,, Deretic V . 2003. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci USA 100 : 5437 5442.[PubMed] [CrossRef]
32. Indrigo J,, Hunter RL Jr,, Actor JK . 2003. Cord factor trehalose 6,6′-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiology 149 : 2049 2059.[PubMed] [CrossRef]
33. Sun J,, Wang X,, Lau A,, Liao TY,, Bucci C,, Hmama Z . 2010. Mycobacterial nucleoside diphosphate kinase blocks phagosome maturation in murine RAW 264.7 macrophages. PLoS One 5 : e8769. doi:10.1371/journal.pone.0008769. [CrossRef]
34. Wong D,, Bach H,, Sun J,, Hmama Z,, Av-Gay Y . 2011. Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H +-ATPase to inhibit phagosome acidification. Proc Natl Acad Sci USA 108 : 19371 19376.[PubMed] [CrossRef]
35. Miller BH,, Fratti RA,, Poschet JF,, Timmins GS,, Master SS,, Burgos M,, Marletta MA,, Deretic V . 2004. Mycobacteria inhibit nitric oxide synthase recruitment to phagosomes during macrophage infection. Infect Immun 72 : 2872 2878.[PubMed] [CrossRef]
36. Davis AS,, Vergne I,, Master SS,, Kyei GB,, Chua J,, Deretic V . 2007. Mechanism of inducible nitric oxide synthase exclusion from mycobacterial phagosomes. PLoS Pathog 3 : e186. [PubMed] [CrossRef]
37. Vergne I,, Fratti RA,, Hill PJ,, Chua J,, Belisle J,, Deretic V . 2004. Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol Biol Cell 15 : 751 760.[PubMed] [CrossRef]
38. Clemens DL,, Horwitz MA . 1996. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J Exp Med 184 : 1349 1355.[PubMed] [CrossRef]
39. Chauhan R,, Mande SC . 2001. Characterization of the Mycobacterium tuberculosis H37Rv alkyl hydroperoxidase AhpC points to the importance of ionic interactions in oligomerization and activity. Biochem J 354 : 209 215.[PubMed] [CrossRef]
40. Master SS,, Springer B,, Sander P,, Boettger EC,, Deretic V,, Timmins GS . 2002. Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages. Microbiology 148 : 3139 3144.[PubMed] [CrossRef]
41. Heym B,, Stavropoulos E,, Honore N,, Domenech P,, Saint-Joanis B,, Wilson TM,, Collins DM,, Colston MJ,, Cole ST . 1997. Effects of overexpression of the alkyl hydroperoxide reductase AhpC on the virulence and isoniazid resistance of Mycobacterium tuberculosis . Infect Immun 65 : 1395 1401.[PubMed]
42. Li Z,, Kelley C,, Collins F,, Rouse D,, Morris S . 1998. Expression of katG in Mycobacterium tuberculosis is associated with its growth and persistence in mice and guinea pigs. J Infect Dis 177 : 1030 1035.[PubMed] [CrossRef]
43. Hu Y,, Coates AR . 2009. Acute and persistent Mycobacterium tuberculosis infections depend on the thiol peroxidase TpX. PLoS One 4 : e5150. [PubMed] [CrossRef]
44. Piddington DL,, Fang FC,, Laessig T,, Cooper AM,, Orme IM,, Buchmeier NA . 2001. Cu,Zn superoxide dismutase of Mycobacterium tuberculosis contributes to survival in activated macrophages that are generating an oxidative burst. Infect Immun 69 : 4980 4987.[PubMed] [CrossRef]
45. Stewart GR,, Newton SM,, Wilkinson KA,, Humphreys IR,, Murphy HN,, Robertson BD,, Wilkinson RJ,, Young DB . 2005. The stress-responsive chaperone alpha-crystallin 2 is required for pathogenesis of Mycobacterium tuberculosis . Mol Microbiol 55 : 1127 1137.[PubMed] [CrossRef]
46. Vandal OH,, Roberts JA,, Odaira T,, Schnappinger D,, Nathan CF,, Ehrt S . 2009. Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. J Bacteriol 191 : 625 631.[PubMed] [CrossRef]
47. Johnson NB,, Hayes LD,, Brown K,, Hoo EC,, Ethier KA , Centers for Disease Control and Prevention . 2014. CDC National Health Report: leading causes of morbidity and mortality and associated behavioral risk and protective factors: United States, 2005-2013. MMWR Surveill Summ 63( Suppl 4) : 3 27.[PubMed]
48. Hahn DL,, Schure A,, Patel K,, Childs T,, Drizik E,, Webley W . 2012. Chlamydia pneumoniae-specific IgE is prevalent in asthma and is associated with disease severity. PLoS One 7 : e35945. doi:10.1371/journal.pone.0035945. [PubMed] [CrossRef]
49. Honarmand H . 2013. Atherosclerosis induced by Chlamydophila pneumoniae: a controversial theory. Interdisc Perspect Infect Dis 2013 : 941392. [PubMed] [CrossRef]
50. Harkinezhad T,, Geens T,, Vanrompay D . 2009. Chlamydo-philapsittaci infections in birds: a review with emphasis on zoonotic consequences. Vet Microbiol 135 : 68 77.[PubMed] [CrossRef]
51. Clifton DR,, Fields KA,, Grieshaber SS,, Dooley CA,, Fischer ER,, Mead DJ,, Carabeo RA,, Hackstadt T . 2004. A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. Proc Natl Acad Sci USA 101 : 10166 10171.[PubMed] [CrossRef]
52. Hybiske K,, Stephens RS . 2007. Mechanisms of host cell exit by the intracellular bacterium Chlamydia . Proc Natl Acad Sci USA 104 : 11430 11435.[PubMed] [CrossRef]
53. Clifton DR,, Dooley CA,, Grieshaber SS,, Carabeo RA,, Fields KA,, Hackstadt T . 2005. Tyrosine phosphorylation of the chlamydial effector protein Tarp is species specific and not required for recruitment of actin. Infect Immun 73 : 3860 3868.[PubMed] [CrossRef]
54. Jewett TJ,, Fischer ER,, Mead DJ,, Hackstadt T . 2006. Chlamydial TARP is a bacterial nucleator of actin. Proc Natl Acad Sci USA 103 : 15599 15604.[PubMed] [CrossRef]
55. 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] [CrossRef]
56. Hackstadt T,, Rockey D,, Heinzen R,, Scidmore M . 1996. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J 15 : 964 977.[PubMed]
57. Hackstadt T,, Scidmore MA,, Rockey DD . 1995. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc Natl Acad Sci USA 92 : 4877 4881.[PubMed] [CrossRef]
58. Damiani MT,, Gambarte Tudela J,, Capmany A . 2014. Targeting eukaryotic Rab proteins: a smart strategy for chlamydial survival and replication. Cell Microbiol 16 : 1329 1338.[PubMed] [CrossRef]
59. Bastidas RJ,, Elwell CA,, Engel JN,, Valdivia RH . 2013. Chlamydial intracellular survival strategies. Cold Spring Harbor Perspect Med 3 : a010256. [PubMed] [CrossRef]
60. Scidmore MA,, Fischer ER,, Hackstadt T . 2003. Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect Immun 71 : 973 984.[PubMed] [CrossRef]
61. 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]
62. Schramm N,, Bagnell CR,, Wyrick PB . 1996. Vesicles containing Chlamydia trachomatis serovar L2 remain above pH 6 within HEC-1B cells. Infect Immun 64 : 1208 1214.[PubMed]
63. Ouellette SP,, Dorsey FC,, Moshiach S,, Cleveland JL,, Carabeo RA . 2011. Chlamydia species-dependent differences in the growth requirement for lysosomes. PLoS One 6 : e16783. doi:10.1371/journal.pone.0016783. [PubMed] [CrossRef]
64. Carabeo RA,, Dooley CA,, Grieshaber SS,, Hackstadt T . 2007. Rac interacts with Abi-1 and WAVE2 to promote an Arp2/3-dependent actin recruitment during chlamydial invasion. Cell Microbiol 9 : 2278 2288.[PubMed] [CrossRef]
65. Lane BJ,, Mutchler C,, Al Khodor S,, Grieshaber SS,, Carabeo RA . 2008. Chlamydial entry involves TARP binding of guanine nucleotide exchange factors. PLoS Pathog 4 : e1000014. doi:10.1371/journal.ppat.1000014. [PubMed] [CrossRef]
66. Belland RJ,, Scidmore MA,, Crane DD,, Hogan DM,, Whitmire W,, McClarty G,, Caldwell HD . 2001. Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Proc Natl Acad Sci USA 98 : 13984 13989.[PubMed] [CrossRef]
67. Thalmann J,, Janik K,, May M,, Sommer K,, Ebeling J,, Hofmann F,, Genth H,, Klos A . 2010. Actin re-organization induced by Chlamydia trachomatis serovar D: evidence for a critical role of the effector protein CT166 targeting Rac. PLoS One 5 : e9887. doi:10.1371/journal.pone.0009887. [CrossRef]
68. Hower S,, Wolf K,, Fields KA . 2009. Evidence that CT694 is a novel Chlamydia trachomatis T3S substrate capable of functioning during invasion or early cycle development. Mol Microbiol 72 : 1423 1437.[PubMed] [CrossRef]
69. Grieshaber SS,, Grieshaber NA,, Hackstadt T . 2003. Chlamydia trachomatis uses host cell dynein to traffic to the microtubule-organizing center in a p50 dynamitin-independent process. J Cell Sci 116 : 3793 3802.[PubMed] [CrossRef]
70. Mital J,, Miller NJ,, Fischer ER,, Hackstadt T . 2010. Specific chlamydial inclusion membrane proteins associate with active Src family kinases in microdomains that interact with the host microtubule network. Cell Microbiol 12 : 1235 1249.[PubMed] [CrossRef]
71. Campbell S,, Richmond SJ,, Yates PS . 1989. The effect of Chlamydia trachomatis infection on the host cell cytoskeleton and membrane compartments. J Gen Microbiol 135 : 2379 2386.[PubMed] [CrossRef]
72. Lutter EI,, Barger AC,, Nair V,, Hackstadt T . 2013. Chlamydia trachomatis inclusion membrane protein CT228 recruits elements of the myosin phosphatase pathway to regulate release mechanisms. Cell Rep 3 : 1921 1931.[PubMed] [CrossRef]
73. Elwell CA,, Engel JN . 2012. Lipid acquisition by intracellular Chlamydiae . Cell Microbiol 14 : 1010 1018.[PubMed] [CrossRef]
74. Rockey DD,, Fischer ER,, Hackstadt T . 1996. Temporal analysis of the developing Chlamydia psittaci inclusion by use of fluorescence and electron microscopy. Infect Immun 64 : 4269 4278.[PubMed]
75. Wolf K,, Hackstadt T . 2001. Sphingomyelin trafficking in Chlamydia pneumoniae-infected cells. Cell Microbiol 3 : 145 152.[PubMed] [CrossRef]
76. Moore ER,, Fischer ER,, Mead DJ,, Hackstadt T . 2008. The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles. Traffic 9 : 2130 2140.[PubMed] [CrossRef]
77. Derre I,, Swiss R,, Agaisse H . 2011. The lipid transfer protein CERT interacts with the Chlamydia inclusion protein IncD and participates to ER- Chlamydia inclusion membrane contact sites. PLoS Pathog 7 : e1002092. doi:10.1371/journal.ppat.1002092. [CrossRef]
78. Elwell CA,, Jiang S,, Kim JH,, Lee A,, Wittmann T,, Hanada K,, Melancon P,, Engel JN . 2011. Chlamydia trachomatis co-opts GBF1 and CERT to acquire host sphingomyelin for distinct roles during intracellular development. PLoS Pathog 7 : e1002198. doi:10.1371/journal.ppat.1002198. [CrossRef]
79. Carabeo RA,, Mead DJ,, Hackstadt T . 2003. Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci 100 : 6771 6776.[PubMed] [CrossRef]
80. Beatty WL . 2008. Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect Immun 76 : 2872 2881.[PubMed] [CrossRef]
81. Moorhead AM,, Jung JY,, Smirnov A,, Kaufer S,, Scidmore MA . 2010. Multiple host proteins that function in phosphatidylinositol-4-phosphate metabolism are recruited to the chlamydial inclusion. Infect Immun 78 : 1990 2007.[PubMed] [CrossRef]
82. Beatty WL . 2006. Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis . J Cell Sci 119 : 350 359.[PubMed] [CrossRef]
83. Kumar Y,, Cocchiaro J,, Valdivia RH . 2006. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr Biol 16 : 1646 1651.[PubMed] [CrossRef]
84. Rzomp KA,, Scholtes LD,, Briggs BJ,, Whittaker GR,, Scidmore MA . 2003. Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect Immun 71 : 5855 5870.[PubMed] [CrossRef]
85. Brumell JH,, Scidmore MA . 2007. Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol Mol Biol Rev 71 : 636 652.[PubMed] [CrossRef]
86. Rzomp KA,, Moorhead AR,, Scidmore MA . 2006. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect Immun 74 : 5362 5373.[PubMed] [CrossRef]
87. Cortes C,, Rzomp KA,, Tvinnereim A,, Scidmore MA,, Wizel B . 2007. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect Immun 75 : 5586 5596.[PubMed] [CrossRef]
88. Capmany A,, Leiva N,, Damiani MT . 2011. Golgi-associated Rab14, a new regulator for Chlamydia trachomatis infection outcome. Commun Integr Biol 4 : 590 593.[PubMed] [CrossRef]
89. Rejman Lipinski A,, Heymann J,, Meissner C,, Karlas A,, Brinkmann V,, Meyer TF,, Heuer D . 2009. Rab6 and Rab11 regulate Chlamydia trachomatis development and golgin-84-dependent Golgi fragmentation. PLoS Pathog 5 : e1000615. doi:10.1371/journal.ppat.1000615. [PubMed] [CrossRef]
90. Ouellette SP,, Carabeo RA . 2010. A functional slow recycling pathway of transferrin is required for growth of Chlamydia . Front Microbiol 1 : 112. [PubMed] [CrossRef]
91. Robertson DK,, Gu L,, Rowe RK,, Beatty WL . 2009. Inclusion biogenesis and reactivation of persistent Chlamydia trachomatis requires host cell sphingolipid biosynthesis. PLoS Pathog 5 : e1000664. doi:10.1371/journal.ppat.1000664. [PubMed] [CrossRef]
92. Matsumoto A,, Bessho H,, Uehira K,, Suda T . 1991. Morphological studies of the association of mitochondria with chlamydial inclusions and the fusion of chlamydial inclusions. J Electron Microsc 40 : 356 363.[PubMed]
93. Peterson EM,, de la Maza LM . 1988. Chlamydia parasitism: ultrastructural characterization of the interaction between the chlamydial cell envelope and the host cell. J Bacteriol 170 : 1389 1392.[PubMed]
94. Derre I,, Pypaert M,, Dautry-Varsat A,, Agaisse H . 2007. RNAi screen in Drosophila cells reveals the involvement of the Tom complex in Chlamydia infection. PLoS Pathog 3 : 1446 1458. doi:10.1371/journal.ppat.003015. [PubMed]
95. McClarty G,, Tipples G . 1991. In situ studies on incorporation of nucleic acid precursors into Chlamydia trachomatis DNA. J Bacteriol 173 : 4922 4931.[PubMed]
96. McClarty G,, Fan H . 1993. Purine metabolism by intracellular Chlamydia psittaci . J Bacteriol 175 : 4662 4669.[PubMed]
97. Bannantine JP,, Griffiths RS,, Viratyosin W,, Brown WJ,, Rockey DD . 2000. A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell Microbiol 2 : 35 47.[PubMed] [CrossRef]
98. Dehoux P,, Flores R,, Dauga C,, Zhong G,, Subtil A . 2011. Multi-genome identification and characterization of Chlamydiae-specific type III secretion substrates: the Inc proteins. BMC Genomics 12 : 109. [PubMed] [CrossRef]
99. Franco MP,, Mulder M,, Gilman RH,, Smits HL . 2007. Human brucellosis. Lancet Infect Dis 7 : 775 786.[PubMed] [CrossRef]
100. Bossi P,, Tegnell A,, Baka A,, Van Loock F,, Hendriks J,, Werner A,, Maidhof H,, Gouvras G . 2004. Bichat guidelines for the clinical management of brucellosis and bioterrorism-related brucellosis. Euro Surveill 9 : E15 E16. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=506. [PubMed]
101. Seleem MN,, Boyle SM,, Sriranganathan N . 2010. Brucellosis: a re-emerging zoonosis. Vet Microbiol 140 : 392 398.[PubMed] [CrossRef]
102. Gomez G,, Adams LG,, Rice-Ficht A,, Ficht TA . 2013. Host- Brucella interactions and the Brucella genome as tools for subunit antigen discovery and immunization against brucellosis. Front Cell Infect Microbiol 3 : 17. [PubMed] [CrossRef]
103. von Bargen K,, Gorvel JP,, Salcedo SP . 2012. Internal affairs: investigating the Brucella intracellular lifestyle. FEMS Microbiol Rev 36 : 533 562.[PubMed] [CrossRef]
104. Pizarro-Cerda J,, Meresse S,, Parton RG,, van der Goot G,, Sola-Landa A,, Lopez-Goni I,, Moreno E,, Gorvel JP . 1998. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun 66 : 5711 5724.[PubMed]
105. Starr T,, Child R,, Wehrly TD,, Hansen B,, Hwang S,, Lopez-Otin C,, Virgin HW,, Celli J . 2012. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 11 : 33 45.[PubMed] [CrossRef]
106. Starr T,, Ng TW,, Wehrly TD,, Knodler LA,, Celli J . 2008. Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment. Traffic 9 : 678 694.[PubMed] [CrossRef]
107. Boschiroli ML,, Ouahrani-Bettache S,, Foulongne V,, Michaux-Charachon S,, Bourg G,, Allardet-Servent A,, Cazevieille C,, Lavigne JP,, Liautard JP,, Ramuz M,, O’Callaghan D . 2002. Type IV secretion and Brucella virulence. Vet Microbiol 90 : 341 348.[PubMed] [CrossRef]
108. Celli J,, de Chastellier C,, Franchini DM,, Pizarro-Cerda J,, Moreno E,, Gorvel JP . 2003. Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 198 : 545 556.[PubMed] [CrossRef]
109. Comerci DJ,, Martinez-Lorenzo MJ,, Sieira R,, Gorvel JP,, Ugalde RA . 2001. Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell Microbiol 3 : 159 168.[PubMed] [CrossRef]
110. Pei J,, Kahl-McDonagh M,, Ficht TA . 2014. Brucella dissociation is essential for macrophage egress and bacterial dissemination. Front Cell Infect Microbiol 4 : 23. [PubMed] [CrossRef]
111. Qin QM,, Pei J,, Ancona V,, Shaw BD,, Ficht TA,, de Figueiredo P . 2008. RNAi screen of endoplasmic reticulum-associated host factors reveals a role for IRE1α in supporting Brucella replication. PLoS Pathog 4 : e1000110. doi:10.1371/journal.ppat.1000110. [PubMed] [CrossRef]
112. Naroeni A,, Porte F . 2002. Role of cholesterol and the ganglioside GM(1) in entry and short-term survival of Brucella suis in murine macrophages. Infect Immun 70 : 1640 1644.[PubMed] [CrossRef]
113. Guzman-Verri C,, Chaves-Olarte E,, von Eichel-Streiber C,, Lopez-Goni I,, Thelestam M,, Arvidson S,, Gorvel JP,, Moreno E . 2001. GTPases of the Rho subfamily are required for Brucella abortus internalization in nonprofessional phagocytes: direct activation of Cdc42. J Biol Chem 276 : 44435 44443.[PubMed] [CrossRef]
114. Pei J,, Turse JE,, Ficht TA . 2008. Evidence of Brucella abortus OPS dictating uptake and restricting NF-kappaB activation in murine macrophages. Microbes Infect 10 : 582 590.[PubMed] [CrossRef]
115. Pei J,, Ficht TA . 2004. Brucella abortus rough mutants are cytopathic for macrophages in culture. Infect Immun 72 : 440 450.[PubMed] [CrossRef]
116. Porte F,, Naroeni A,, Ouahrani-Bettache S,, Liautard JP . 2003. Role of the Brucella suis lipopolysaccharide O antigen in phagosomal genesis and in inhibition of phagosome-lysosome fusion in murine macrophages. Infect Immun 71 : 1481 1490.[PubMed] [CrossRef]
117. Rittig MG,, Kaufmann A,, Robins A,, Shaw B,, Sprenger H,, Gemsa D,, Foulongne V,, Rouot B,, Dornand J . 2003. Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes. J Leukoc Biol 74 : 1045 1055.[PubMed] [CrossRef]
118. Martin-Martin AI,, Vizcaino N,, Fernandez-Lago L . 2010. Cholesterol, ganglioside GM1 and class A scavenger receptor contribute to infection by Brucella ovis and Brucella canis in murine macrophages. Microbes Infect 12 : 246 251.[PubMed] [CrossRef]
119. Hong PC,, Tsolis RM,, Ficht TA . 2000. Identification of genes required for chronic persistence of Brucella abortus in mice. Infect Immun 68 : 4102 4107.[PubMed] [CrossRef]
120. Sieira R,, Comerci DJ,, Sanchez DO,, Ugalde RA . 2000. A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular multiplication. J Bacteriol 182 : 4849 4855.[PubMed] [CrossRef]
121. Arellano-Reynoso B,, Lapaque N,, Salcedo S,, Briones G,, Ciocchini AE,, Ugalde R,, Moreno E,, Moriyon I,, Gorvel JP . 2005. Cyclic beta-1,2-glucan is a Brucella virulence factor required for intracellular survival. Nat Immunol 6 : 618 625.[PubMed] [CrossRef]
122. Roop RM 2nd,, Gaines JM,, Anderson ES,, Caswell CC,, Martin DW . 2009. Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host. Med Microbiol Immunol 198 : 221 238.[PubMed] [CrossRef]
123. Valderas MW,, Alcantara RB,, Baumgartner JE,, Bellaire BH,, Robertson GT,, Ng WL,, Richardson JM,, Winkler ME,, Roop RM 2nd . 2005. Role of HdeA in acid resistance and virulence in Brucella abortus 2308. Vet Microbiol 107 : 307 312.[PubMed] [CrossRef]
124. Endley S,, McMurray D,, Ficht TA . 2001. Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection. J Bacteriol 183 : 2454 2462.[PubMed] [CrossRef]
125. Bandara AB,, Contreras A,, Contreras-Rodriguez A,, Martins AM,, Dobrean V,, Poff-Reichow S,, Rajasekaran P,, Sriranganathan N,, Schurig GG,, Boyle SM . 2007. Brucella suis urease encoded by ure1 but not ure2 is necessary for intestinal infection of BALB/c mice. BMC Microbiol 7 : 57. [PubMed] [CrossRef]
126. Jimenez de Bagues MP,, Dudal S,, Dornand J,, Gross A . 2005. Cellular bioterrorism: how Brucella corrupts macrophage physiology to promote invasion and proliferation. Clin Immunol 114 : 227 238.[PubMed] [CrossRef]
127. Gee JM,, Valderas MW,, Kovach ME,, Grippe VK,, Robertson GT,, Ng WL,, Richardson JM,, Winkler ME,, Roop RM 2nd . 2005. The Brucella abortus Cu,Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infect Immun 73 : 2873 2880.[PubMed] [CrossRef]
128. Haine V,, Dozot M,, Dornand J,, Letesson JJ,, De Bolle X . 2006. NnrA is required for full virulence and regulates several Brucella melitensis denitrification genes. J Bacteriol 188 : 1615 1619.[PubMed] [CrossRef]
129. Loisel-Meyer S,, Jimenez de Bagues MP,, Basseres E,, Dornand J,, Kohler S,, Liautard JP,, Jubier-Maurin V . 2006. Requirement of norD for Brucella suis virulence in a murine model of in vitro and in vivo infection. Infect Immun 74 : 1973 1976.[PubMed] [CrossRef]
130. Steele KH,, Baumgartner JE,, Valderas MW,, Roop RM 2nd . 2010. Comparative study of the roles of AhpC and KatE as respiratory antioxidants in Brucella abortus 2308. J Bacteriol 192 : 4912 4922.[PubMed] [CrossRef]
131. Manterola L,, Moriyon I,, Moreno E,, Sola-Landa A,, Weiss DS,, Koch MH,, Howe J,, Brandenburg K,, Lopez-Goni I . 2005. The lipopolysaccharide of Brucella abortus BvrS/BvrR mutants contains lipid A modifications and has higher affinity for bactericidal cationic peptides. J Bacteriol 187 : 5631 5639.[PubMed] [CrossRef]
132. Pizarro-Cerda J,, Moreno E,, Sanguedolce V,, Mege JL,, Gorvel JP . 1998. Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66 : 2387 2392.[PubMed]
133. Smith JA,, Khan M,, Magnani DD,, Harms JS,, Durward M,, Radhakrishnan GK,, Liu YP,, Splitter GA . 2013. Brucella induces an unfolded protein response via TcpB that supports intracellular replication in macrophages. PLoS Pathog 9 : e1003785. doi:10.1371/journal.ppat.1003785. [PubMed] [CrossRef]
134. Fugier E,, Salcedo SP,, de Chastellier C,, Pophillat M,, Muller A,, Arce-Gorvel V,, Fourquet P,, Gorvel JP . 2009. The glyceraldehyde-3-phosphate dehydrogenase and the small GTPase Rab 2 are crucial for Brucella replication. PLoS Pathog 5 : e1000487. doi:10.1371/journal.ppat.1000487. [PubMed] [CrossRef]
135. de Barsy M,, Jamet A,, Filopon D,, Nicolas C,, Laloux G,, Rual JF,, Muller A,, Twizere JC,, Nkengfac B,, Vandenhaute J,, Hill DE,, Salcedo SP,, Gorvel JP,, Letesson JJ,, De Bolle X . 2011. Identification of a Brucella spp. secreted effector specifically interacting with human small GTPase Rab2. Cell Microbiol 13 : 1044 1058.[PubMed] [CrossRef]
136. Nkengfac B,, Pouyez J,, Bauwens E,, Vandenhaute J,, Letesson JJ,, Wouters J,, De Bolle X . 2012. Structural analysis of Brucella abortus RicA substitutions that do not impair interaction with human Rab2 GTPase. BMC Biochem 13 : 16. [PubMed] [CrossRef]
137. de Barsy M,, Mirabella A,, Letesson JJ,, De Bolle X . 2012. A Brucella abortus cstA mutant is defective for association with endoplasmic reticulum exit sites and displays altered trafficking in HeLa cells. Microbiology 158 : 2610 2618.[PubMed] [CrossRef]
138. Myeni S,, Child R,, Ng TW,, Kupko JJ 3rd,, Wehrly TD,, Porcella SF,, Knodler LA,, Celli J . 2013. Brucella modulates secretory trafficking via multiple type IV secretion effector proteins. PLoS Pathog 9 : e1003556. doi:10.1371/journal.ppat.1003556. [CrossRef]
139. Celli J,, Salcedo SP,, Gorvel JP . 2005. Brucella coopts the small GTPase Sar1 for intracellular replication. Proc Natl Acad Sci USA 102 : 1673 1678.[PubMed] [CrossRef]
140. van Schaik EJ,, Chen C,, Mertens K,, Weber MM,, Samuel JE . 2013. Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii . Nat Rev Microbiol 11 : 561 573.[PubMed] [CrossRef]
141. Enserink M . 2010. Infectious diseases. Questions abound in Q-fever explosion in the Netherlands. Science 327 : 266 267.[PubMed]
142. White B,, Brooks T,, Seaton RA . 2013. Q fever in military and paramilitary personnel in conflict zones: case report and review. Travel Med Infect Dis 11 : 134 137.[PubMed] [CrossRef]
143. Coleman SA,, Fischer ER,, Howe D,, Mead DJ,, Heinzen RA . 2004. Temporal analysis of Coxiella burnetii morphological differentiation. J Bacteriol 186 : 7344 7352.[PubMed] [CrossRef]
144. 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] [CrossRef]
145. Baca OG,, Klassen DA,, Aragon AS . 1993. Entry of Coxiella burnetii into host cells. Acta Virol 37 : 143 155.[PubMed]
146. 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]
147. Beare PA,, Gilk SD,, Larson CL,, Hill J,, Stead CM,, Omsland A,, Cockrell DC,, Howe D,, Voth DE,, Heinzen RA . 2011. Dot/Icm type IVB secretion system requirements for Coxiella burnetii growth in human macrophages. MBio 2 : e00175-00111. doi:10.1128/mBio.00175-11. [CrossRef]
148. Carey KL,, Newton HJ,, Luhrmann A,, Roy CR . 2011. The Coxiella burnetii Dot/Icm system delivers a unique repertoire of type IV effectors into host cells and is required for intracellular replication. PLoS Pathog 7 : e1002056. doi:10.1371/journal.ppat.1002056. [PubMed] [CrossRef]
149. 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 alphavbeta3 integrin and CR3. J Immunol 163 : 6078 6085.[PubMed]
150. Dellacasagrande J,, Ghigo E,, Machergui-El S Hammami,, Toman R,, Raoult D,, Capo C,, Mege J-L . 2000. Alpha vbeta 3 integrin and bacterial lipopolysaccharide are involved in Coxiella burnetii-stimulated production of tumor necrosis factor by human monocytes. Infect Immun 68 : 5673 5678.[PubMed] [CrossRef]
151. Russell-Lodrigue KE,, Zhang GQ,, McMurray DN,, Samuel JE . 2006. Clinical and pathologic changes in a guinea pig aerosol challenge model of acute Q fever. Infect Immun 74 : 6085 6091.[PubMed] [CrossRef]
152. 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] [CrossRef]
153. 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] [CrossRef]
154. Howe D,, Melnicâakova J,, Barâak I,, Heinzen RA . 2003. Fusogenicity of the Coxiella burnetii parasitophorous vacuole. Ann N Y Acad Sci 990 : 556 562.[PubMed] [CrossRef]
155. Larson CL,, Beare PA,, Voth DE,, Howe D,, Cockrell DC,, Bastidas RJ,, Valdivia RH,, Heinzen RA . 2015. Coxiella burnetii effector proteins that localize to the parasitophorous vacuole membrane promote intracellular replication. Infect Immun 83 : 661 670.[PubMed] [CrossRef]
156. Howe D,, Melnicâakovâa J,, Barâak I,, Heinzen RA . 2003. Maturation of the Coxiella burnetii parasitophorous vacuole requires bacterial protein synthesis but not replication. Cell Microbiol 5 : 469 480.[PubMed] [CrossRef]
157. Flannagan RS,, Cosio G,, Grinstein S . 2009. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7 : 355 366.[PubMed] [CrossRef]
158. Oh YK,, Alpuche-Aranda C,, Berthiaume E,, Jinks T,, Miller SI,, Swanson JA . 1996. Rapid and complete fusion of macrophage lysosomes with phagosomes containing Salmonella typhimurium . Infect Immun 64 : 3877 3883.[PubMed]
159. Swanson MS,, Fernandez-Moreira E . 2002. A microbial strategy to multiply in macrophages: the pregnant pause. Traffic 3 : 170 177.[PubMed] [CrossRef]
160. Levine B,, Mizushima N,, Virgin HW . 2011. Autophagy in immunity and inflammation. Nature 469 : 323 335.[PubMed] [CrossRef]
161. 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] [CrossRef]
162. 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] [CrossRef]
163. Criscitiello MF,, Dickman MB,, Samuel JE,, de Figueiredo P . 2013. Tripping on acid: trans-kingdom perspectives on biological acids in immunity and pathogenesis. PLoS Pathog 9 : e1003402. doi:10.1371/journal.ppat.1003402. [CrossRef]
164. Mertens K,, Lantsheer L,, Ennis DG,, Samuel JE . 2008. Constitutive SOS expression and damage-inducible AddAB-mediated recombinational repair systems for Coxiella burnetii as potential adaptations for survival within macrophages. Mol Microbiol 69 : 1411 1426.[PubMed] [CrossRef]
165. 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] [CrossRef]
166. Heinzen RA,, Frazier ME,, Mallavia LP . 1992. Coxiella burnetii superoxide dismutase gene: cloning, sequencing, and expression in Escherichia coli . Infect Immun 60 : 3814 3823.[PubMed]
167. 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 USA 100 : 5455 5460.[PubMed] [CrossRef]
168. 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] [CrossRef]
169. Roman MJ,, Crissman HA,, Samsonoff WA,, Hechemy KE,, Baca OG . 1991. Analysis of Coxiella burnetii isolates in cell culture and the expression of parasite-specific antigens on the host membrane surface. Acta Virol 35 : 503 510.[PubMed]
170. 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] [CrossRef]
171. Hussain SK,, Broederdorf LJ,, Sharma UM,, Voth DE . 2011. Host kinase activity is required for Coxiella burnetii parasitophorous vacuole formation. Front Microbiol 1 : 137. [PubMed]
172. 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] [CrossRef]
173. Martinez E,, Cantet F,, Fava L,, Norville I,, Bonazzi M . 2014. Identification of OmpA, a Coxiella burnetti protein involved in host cell invasion, by multi-phenotypic high-content screening. PLoS Pathog 10 : p.e.1004013. [PubMed]

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error