Chapter 40 : Strategies Used by Bacteria to Grow in Macrophages

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

Preview this chapter:
Zoom in

Strategies Used by Bacteria to Grow in Macrophages, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819194/9781555819187_Chap40-1.gif /docserver/preview/fulltext/10.1128/9781555819194/9781555819187_Chap40-2.gif


Intracellular bacterial pathogens cause a wide range of diseases and significantly contribute to the morbidity and mortality associated with infectious diseases worldwide ( ) ( Table 1 ). These bacteria use several different strategies to replicate in host cells and influence host processes such as membrane trafficking, signaling pathways, metabolism, cell death, and survival ( ). Broadly, intracellular bacteria colonize two topologically distinct regions of the host cell and are divided into cytosolic and intravacuolar bacteria according to their intracellular lifestyle. However, most intracellular bacterial pathogens have unique intracellular life cycles with features strikingly different from one another ( Fig. 1 ). It should also be noted that intravacuolar pathogens gain access to the host cytosol to some extent, and that cytosolic bacteria might spend an underestimated part of their intracellular life cycle within membrane-bound compartments ( ).

Citation: Mitchell G, Chen C, Portnoy D. 2017. Strategies Used by Bacteria to Grow in Macrophages, p 701-725. In Gordon S (ed), Myeloid Cells in Health and Disease. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MCHD-0012-2015
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Lifestyles of intracellular bacterial pathogens. (1) escapes a late endosome (LE)-like vacuole in a T6SS-dependent manner. Following replication in the cytosol, may retranslocate to a membrane-bound compartment resembling an autolysosome. (2) escapes the phagolysosomal pathway using the T2SS (Sec) effectors LLO and PLCs. replicates rapidly in the cytosol and hijacks the host actin polymerization machinery to move within and between cells. (3) escapes into the cytosol in a T3SS-dependent manner. performs actin-based motility and promotes host cell fusion. (4) is adapted to the phagolysosomal pathway and resides in a spacious phagolysosomal-like compartment. The Dot/Icm system (T4SS) is required for recruiting the autophagosomal marker LC3 and for vacuole biogenesis. (5) arrests phagosome maturation at the early endosome (EE) stage in a T7SS-dependent manner. (6) and segregate from the endocytic route at the EE stage, recruit ER-derived vesicles, and form ribosome-studded specialized vacuoles in a T4SS-dependent manner. (7) e segregates from the endocytic route and forms a unique inclusion vacuole by recruiting Golgi-derived vesicles. e effectors promote Golgi fragmentation and generate actin filaments around the inclusion. is found in two different forms: the nonreplicating infectious elementary body (EB) and the intracytoplasmic replicative reticulate body (RB). T2SS and T3SS effectors are thought to be involved in the intracellular life cycle of . (8) replicates in an LE-like compartment that excludes lysosomal degradation enzymes. The -containing vacuole migrates to the microtubule-organizing center and forms -induced filaments (Sif) along microtubules in a T3SS-dependent manner.

Citation: Mitchell G, Chen C, Portnoy D. 2017. Strategies Used by Bacteria to Grow in Macrophages, p 701-725. In Gordon S (ed), Myeloid Cells in Health and Disease. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MCHD-0012-2015
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Fauci AS,, Morens DM . 2012. The perpetual challenge of infectious diseases. N Engl J Med 366 : 454461.[PubMed] [CrossRef]
2. Price JV,, Vance RE . 2014. The macrophage paradox. Immunity 41 : 685693.[PubMed] [CrossRef]
3. Dumler JS,, Choi KS,, Garcia-Garcia JC,, Barat NS,, Scorpio DG,, Garyu JW,, Grab DJ,, Bakken JS . 2005. Human granulocytic anaplasmosis and Anaplasma phagocytophilum . Emerg Infect Dis 11 : 18281834.[PubMed] [CrossRef]
4. Franco MP,, Mulder M,, Gilman RH,, Smits HL . 2007. Human brucellosis. Lancet Infect Dis 7 : 775786.[CrossRef]
5. Piggott JA,, Hochholzer L . 1970. Human melioidosis. A histopathologic study of acute and chronic melioidosis. Arch Pathol 90 : 101111.[PubMed]
6. Grayston JT,, Aldous MB,, Easton A,, Wang SP,, Kuo CC,, Campbell LA,, Altman J . 1993. Evidence that Chlamydia pneumoniae causes pneumonia and bronchitis. J Infect Dis 168 : 12311235.[PubMed] [CrossRef]
7. Gross RJ,, Rowe B,, Easton JA . 1973. Neonatal meningitis caused by Citrobacter koseri . J Clin Pathol 26 : 138139.[PubMed] [CrossRef]
8. Maurin M,, Raoult D . 1999. Q fever. Clin Microbiol Rev 12 : 518553.[PubMed]
9. Dumler JS,, Madigan JE,, Pusterla N,, Bakken JS . 2007. Ehrlichioses in humans: epidemiology, clinical presentation, diagnosis, and treatment. Clin Infect Dis 45(Suppl 1): S45S51.[PubMed] [CrossRef]
10. Sjöstedt A . 2007. Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann N Y Acad Sci 1105 : 129.[PubMed] [CrossRef]
11. Phin N,, Parry-Ford F,, Harrison T,, Stagg HR,, Zhang N,, Kumar K,, Lortholary O,, Zumla A,, Abubakar I . 2014. Epidemiology and clinical management of Legionnaires’ disease. Lancet Infect Dis 14 : 10111021.[CrossRef]
12. Hof H . 2003. History and epidemiology of listeriosis. FEMS Immunol Med Microbiol 35 : 199202.[CrossRef]
13. Daniel TM . 2006. The history of tuberculosis. Respir Med 100 : 18621870.[PubMed] [CrossRef]
14. Prescott JF . 1991. Rhodococcus equi: an animal and human pathogen. Clin Microbiol Rev 4 : 2034.[PubMed]
15. Harrell GT . 1949. Rocky Mountain spotted fever. Medicine (Baltimore) 28 : 333370.[PubMed] [CrossRef]
16. Blaser MJ,, Newman LS . 1982. A review of human salmonellosis: I. Infective dose. Rev Infect Dis 4 : 10961106.[PubMed] [CrossRef]
17. Thi EP,, Lambertz U,, Reiner NE . 2012. Sleeping with the enemy: how intracellular pathogens cope with a macrophage lifestyle. PLoS Pathog 8 : e1002551. doi:10.1371/journal.ppat.1002551. [PubMed] [CrossRef]
18. Ray K,, Marteyn B,, Sansonetti PJ,, Tang CM . 2009. Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat Rev Microbiol 7 : 333340.[PubMed] [CrossRef]
19. Alix E,, Mukherjee S,, Roy CR . 2011. Subversion of membrane transport pathways by vacuolar pathogens. J Cell Biol 195 : 943952.[PubMed] [CrossRef]
20. Fredlund J,, Enninga J . 2014. Cytoplasmic access by intracellular bacterial pathogens. Trends Microbiol 22 : 128137.[PubMed] [CrossRef]
21. Birmingham CL,, Canadien V,, Kaniuk NA,, Steinberg BE,, Higgins DE,, Brumell JH . 2008. Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 451 : 350354.[PubMed] [CrossRef]
22. Checroun C,, Wehrly TD,, Fischer ER,, Hayes SF,, Celli J . 2006. Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc Natl Acad Sci U S A 103 : 1457814583.[PubMed] [CrossRef]
23. Plüddemann A,, Mukhopadhyay S,, Gordon S . 2011. Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry. Immunol Rev 240 : 1124.[PubMed] [CrossRef]
24. Murray PJ,, Wynn TA . 2011. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 11 : 723737.[PubMed] [CrossRef]
25. Flannagan RS,, Cosío G,, Grinstein S . 2009. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7 : 355366.[PubMed] [CrossRef]
26. Broz P,, Monack DM . 2013. Newly described pattern recognition receptors team up against intracellular pathogens. Nat Rev Immunol 13 : 551565.[PubMed] [CrossRef]
27. Kawai T,, Akira S . 2006. TLR signaling. Cell Death Differ 13 : 816825.[PubMed] [CrossRef]
28. Strober W,, Murray PJ,, Kitani A,, Watanabe T . 2006. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat Rev Immunol 6 : 920.[PubMed] [CrossRef]
29. Keestra AM,, Winter MG,, Auburger JJ,, Frässle SP,, Xavier MN,, Winter SE,, Kim A,, Poon V,, Ravesloot MM,, Waldenmaier JF,, Tsolis RM,, Eigenheer RA,, Bäumler AJ . 2013. Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature 496 : 233237.[PubMed] [CrossRef]
30. von Moltke J,, Ayres JS,, Kofoed EM,, Chavarría-Smith J,, Vance RE . 2013. Recognition of bacteria by inflammasomes. Annu Rev Immunol 31 : 73106.[PubMed] [CrossRef]
31. Vanaja SK,, Rathinam VA,, Fitzgerald KA . 2015. Mechanisms of inflammasome activation: recent advances and novel insights. Trends Cell Biol 25 : 308315.[PubMed] [CrossRef]
32. Hornung V,, Ablasser A,, Charrel-Dennis M,, Bauernfeind F,, Horvath G,, Caffrey DR,, Latz E,, Fitzgerald KA . 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458 : 514518.[PubMed] [CrossRef]
33. Fernandes-Alnemri T,, Yu JW,, Datta P,, Wu J,, Alnemri ES . 2009. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458 : 509513.[PubMed] [CrossRef]
34. Fernandes-Alnemri T,, Yu JW,, Juliana C,, Solorzano L,, Kang S,, Wu J,, Datta P,, McCormick M,, Huang L,, McDermott E,, Eisenlohr L,, Landel CP,, Alnemri ES . 2010. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis . Nat Immunol 11 : 385393.[PubMed] [CrossRef]
35. Jones JW,, Kayagaki N,, Broz P,, Henry T,, Newton K,, O’Rourke K,, Chan S,, Dong J,, Qu Y,, Roose-Girma M,, Dixit VM,, Monack DM . 2010. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis . Proc Natl Acad Sci U S A 107 : 97719776.[PubMed] [CrossRef]
36. Rathinam VA,, Jiang Z,, Waggoner SN,, Sharma S,, Cole LE,, Waggoner L,, Vanaja SK,, Monks BG,, Ganesan S,, Latz E,, Hornung V,, Vogel SN,, Szomolanyi-Tsuda E,, Fitzgerald KA . 2010. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol 11 : 395402.[PubMed] [CrossRef]
37. Sauer JD,, Witte CE,, Zemansky J,, Hanson B,, Lauer P,, Portnoy DA . 2010. Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7 : 412419.[PubMed] [CrossRef]
38. Tsuchiya K,, Hara H,, Kawamura I,, Nomura T,, Yamamoto T,, Daim S,, Dewamitta SR,, Shen Y,, Fang R,, Mitsuyama M . 2010. Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes . J Immunol 185 : 11861195.[PubMed] [CrossRef]
39. Warren SE,, Armstrong A,, Hamilton MK,, Mao DP,, Leaf IA,, Miao EA,, Aderem A . 2010. Cutting edge: cytosolic bacterial DNA activates the inflammasome via Aim2. J Immunol 185 : 818821.[PubMed] [CrossRef]
40. Ishikawa H,, Barber GN . 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455 : 674678.[PubMed] [CrossRef]
41. Zhong B,, Yang Y,, Li S,, Wang YY,, Li Y,, Diao F,, Lei C,, He X,, Zhang L,, Tien P,, Shu HB . 2008. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29 : 538550.[PubMed] [CrossRef]
42. Ishikawa H,, Ma Z,, Barber GN . 2009. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461 : 788792.[PubMed] [CrossRef]
43. Sauer JD,, Sotelo-Troha K,, von Moltke J,, Monroe KM,, Rae CS,, Brubaker SW,, Hyodo M,, Hayakawa Y,, Woodward JJ,, Portnoy DA,, Vance RE . 2011. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect Immun 79 : 688694.[PubMed] [CrossRef]
44. Burdette DL,, Monroe KM,, Sotelo-Troha K,, Iwig JS,, Eckert B,, Hyodo M,, Hayakawa Y,, Vance RE . 2011. STING is a direct innate immune sensor of cyclic di-GMP. Nature 478 : 515518.[PubMed] [CrossRef]
45. Sun L,, Wu J,, Du F,, Chen X,, Chen ZJ . 2013. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339 : 786791.[PubMed] [CrossRef]
46. Wu J,, Sun L,, Chen X,, Du F,, Shi H,, Chen C,, Chen ZJ . 2013. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339 : 826830.[PubMed] [CrossRef]
47. Zhang Y,, Yeruva L,, Marinov A,, Prantner D,, Wyrick PB,, Lupashin V,, Nagarajan UM . 2014. The DNA sensor, cyclic GMP-AMP synthase, is essential for induction of IFN-β during Chlamydia trachomatis infection. J Immunol 193 : 23942404.[PubMed] [CrossRef]
48. Hansen K,, Prabakaran T,, Laustsen A,, Jørgensen SE,, Rahbæk SH,, Jensen SB,, Nielsen R,, Leber JH,, Decker T,, Horan KA,, Jakobsen MR,, Paludan SR . 2014. Listeria monocytogenes induces IFNβ expression through an IFI16-, cGAS- and STING-dependent pathway. EMBO J 33 : 16541666.[PubMed] [CrossRef]
49. Watson RO,, Bell SL,, MacDuff DA,, Kimmey JM,, Diner EJ,, Olivas J,, Vance RE,, Stallings CL,, Virgin HW,, Cox JS . 2015. The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy. Cell Host Microbe 17 : 811819.[PubMed] [CrossRef]
50. Zhang Z,, Yuan B,, Bao M,, Lu N,, Kim T,, Liu YJ . 2011. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12 : 959965.[PubMed] [CrossRef]
51. Parvatiyar K,, Zhang Z,, Teles RM,, Ouyang S,, Jiang Y,, Iyer SS,, Zaver SA,, Schenk M,, Zeng S,, Zhong W,, Liu ZJ,, Modlin RL,, Liu YJ,, Cheng G . 2012. The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol 13 : 11551161.[PubMed] [CrossRef]
52. Unterholzner L,, Keating SE,, Baran M,, Horan KA,, Jensen SB,, Sharma S,, Sirois CM,, Jin T,, Latz E,, Xiao TS,, Fitzgerald KA,, Paludan SR,, Bowie AG . 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11 : 9971004.[PubMed] [CrossRef]
53. Auerbuch V,, Brockstedt DG,, Meyer-Morse N,, O’Riordan M,, Portnoy DA . 2004. Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes . J Exp Med 200 : 527533.[PubMed] [CrossRef]
54. O’Connell RM,, Saha SK,, Vaidya SA,, Bruhn KW,, Miranda GA,, Zarnegar B,, Perry AK,, Nguyen BO,, Lane TF,, Taniguchi T,, Miller JF,, Cheng G . 2004. Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med 200 : 437445.[PubMed] [CrossRef]
55. Robinson N,, McComb S,, Mulligan R,, Dudani R,, Krishnan L,, Sad S . 2012. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat Immunol 13 : 954962.[PubMed] [CrossRef]
56. Nagarajan UM,, Prantner D,, Sikes JD,, Andrews CW Jr,, Goodwin AM,, Nagarajan S,, Darville T . 2008. Type I interferon signaling exacerbates Chlamydia muridarum genital infection in a murine model. Infect Immun 76 : 46424648.[PubMed] [CrossRef]
57. Qiu H,, Fan Y,, Joyee AG,, Wang S,, Han X,, Bai H,, Jiao L,, Van Rooijen N,, Yang X . 2008. Type I IFNs enhance susceptibility to Chlamydia muridarum lung infection by enhancing apoptosis of local macrophages. J Immunol 181 : 20922102.[PubMed] [CrossRef]
58. Desvignes L,, Wolf AJ,, Ernst JD . 2012. Dynamic roles of type I and type II IFNs in early infection with Mycobacterium tuberculosis . J Immunol 188 : 62056215.[PubMed] [CrossRef]
59. Manca C,, Tsenova L,, Freeman S,, Barczak AK,, Tovey M,, Murray PJ,, Barry C III,, Kaplan G . 2005. Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J Interferon Cytokine Res 25 : 694701.[PubMed] [CrossRef]
60. Dorhoi A,, Yeremeev V,, Nouailles G,, Weiner J III,, Jörg S,, Heinemann E,, Oberbeck-Müller D,, Knaul JK,, Vogelzang A,, Reece ST,, Hahnke K,, Mollenkopf HJ,, Brinkmann V,, Kaufmann SH . 2014. Type I IFN signaling triggers immunopathology in tuberculosis-susceptible mice by modulating lung phagocyte dynamics. Eur J Immunol 44 : 23802393.[PubMed] [CrossRef]
61. Manzanillo PS,, Shiloh MU,, Portnoy DA,, Cox JS . 2012. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11 : 469480.[PubMed] [CrossRef]
62. Huynh KK,, Grinstein S . 2007. Regulation of vacuolar pH and its modulation by some microbial species. Microbiol Mol Biol Rev 71 : 452462.[PubMed] [CrossRef]
63. Quinn MT,, Gauss KA . 2004. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J Leukoc Biol 76 : 760781.[PubMed] [CrossRef]
64. Minakami R,, Sumimotoa H . 2006. Phagocytosis-coupled activation of the superoxide-producing phagocyte oxidase, a member of the NADPH oxidase (Nox) family. Int J Hematol 84 : 193198.[PubMed] [CrossRef]
65. Fang FC . 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2 : 820832.[PubMed] [CrossRef]
66. Cellier MF,, Courville P,, Campion C . 2007. Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 9 : 16621670.[PubMed] [CrossRef]
67. Huang J,, Brumell JH . 2014. Bacteria-autophagy interplay: a battle for survival. Nat Rev Microbiol 12 : 101114.[PubMed] [CrossRef]
68. Mizushima N,, Yoshimori T,, Ohsumi Y . 2011. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27 : 107132.[PubMed] [CrossRef]
69. Bestebroer J,, V’kovski P,, Mauthe M,, Reggiori F . 2013. Hidden behind autophagy: the unconventional roles of ATG proteins. Traffic 14 : 10291041.[PubMed] [CrossRef]
70. Kim DH,, Sarbassov DD,, Ali SM,, King JE,, Latek RR,, Erdjument-Bromage H,, Tempst P,, Sabatini DM . 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110 : 163175.[CrossRef]
71. Hosokawa N,, Hara T,, Kaizuka T,, Kishi C,, Takamura A,, Miura Y,, Iemura S,, Natsume T,, Takehana K,, Yamada N,, Guan JL,, Oshiro N,, Mizushima N . 2009. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20 : 19811991.[PubMed] [CrossRef]
72. He C,, Klionsky DJ . 2009. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43 : 6793.[PubMed] [CrossRef]
73. Parzych KR,, Klionsky DJ . 2014. An overview of autophagy: morphology, mechanism, and regulation. Antioxid Redox Signal 20 : 460473.[PubMed] [CrossRef]
74. Hanna RA,, Quinsay MN,, Orogo AM,, Giang K,, Rikka S,, Gustafsson AB . 2012. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem 287 : 1909419104.[PubMed] [CrossRef]
75. Liu L,, Feng D,, Chen G,, Chen M,, Zheng Q,, Song P,, Ma Q,, Zhu C,, Wang R,, Qi W,, Huang L,, Xue P,, Li B,, Wang X,, Jin H,, Wang J,, Yang F,, Liu P,, Zhu Y,, Sui S,, Chen Q . 2012. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol 14 : 177185.[PubMed] [CrossRef]
76. Novak I,, Kirkin V,, McEwan DG,, Zhang J,, Wild P,, Rozenknop A,, Rogov V,, Löhr F,, Popovic D,, Occhipinti A,, Reichert AS,, Terzic J,, Dötsch V,, Ney PA,, Dikic I . 2010. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11 : 4551.[PubMed] [CrossRef]
77. Boyle KB,, Randow F . 2013. The role of ‘eat-me’ signals and autophagy cargo receptors in innate immunity. Curr Opin Microbiol 16 : 339348.[PubMed] [CrossRef]
78. Yoshikawa Y,, Ogawa M,, Hain T,, Yoshida M,, Fukumatsu M,, Kim M,, Mimuro H,, Nakagawa I,, Yanagawa T,, Ishii T,, Kakizuka A,, Sztul E,, Chakraborty T,, Sasakawa C . 2009. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol 11 : 12331240.[PubMed] [CrossRef]
79. Mostowy S,, Sancho-Shimizu V,, Hamon MA,, Simeone R,, Brosch R,, Johansen T,, Cossart P . 2011. p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J Biol Chem 286 : 2698726995.[PubMed] [CrossRef]
80. Zheng YT,, Shahnazari S,, Brech A,, Lamark T,, Johansen T,, Brumell JH . 2009. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J Immunol 183 : 59095916.[PubMed] [CrossRef]
81. von Muhlinen N,, Thurston T,, Ryzhakov G,, Bloor S,, Randow F . 2010. NDP52, a novel autophagy receptor for ubiquitin-decorated cytosolic bacteria. Autophagy 6 : 288289.[PubMed] [CrossRef]
82. Wild P,, Farhan H,, McEwan DG,, Wagner S,, Rogov VV,, Brady NR,, Richter B,, Korac J,, Waidmann O,, Choudhary C,, Dötsch V,, Bumann D,, Dikic I . 2011. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333 : 228233.[PubMed] [CrossRef]
83. Chong A,, Wehrly TD,, Child R,, Hansen B,, Hwang S,, Virgin HW,, Celli J . 2012. Cytosolic clearance of replication-deficient mutants reveals Francisella tularensis interactions with the autophagic pathway. Autophagy 8 : 13421356.[PubMed] [CrossRef]
84. Cheong H,, Lindsten T,, Wu J,, Lu C,, Thompson CB . 2011. Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc Natl Acad Sci U S A 108 : 1112111126.[PubMed] [CrossRef]
85. Nishida Y,, Arakawa S,, Fujitani K,, Yamaguchi H,, Mizuta T,, Kanaseki T,, Komatsu M,, Otsu K,, Tsujimoto Y,, Shimizu S . 2009. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461 : 654658.[PubMed] [CrossRef]
86. Grishchuk Y,, Ginet V,, Truttmann AC,, Clarke PG,, Puyal J . 2011. Beclin 1-independent autophagy contributes to apoptosis in cortical neurons. Autophagy 7 : 11151131.[PubMed] [CrossRef]
87. Choi J,, Park S,, Biering SB,, Selleck E,, Liu CY,, Zhang X,, Fujita N,, Saitoh T,, Akira S,, Yoshimori T,, Sibley LD,, Hwang S,, Virgin HW . 2014. The parasitophorous vacuole membrane of Toxoplasma gondii is targeted for disruption by ubiquitin-like conjugation systems of autophagy. Immunity 40 : 924935.[PubMed] [CrossRef]
88. Mestre MB,, Fader CM,, Sola C,, Colombo MI . 2010. Alpha-hemolysin is required for the activation of the autophagic pathway in Staphylococcus aureus-infected cells. Autophagy 6 : 110125.[PubMed] [CrossRef]
89. Sanjuan MA,, Dillon CP,, Tait SW,, Moshiach S,, Dorsey F,, Connell S,, Komatsu M,, Tanaka K,, Cleveland JL,, Withoff S,, Green DR . 2007. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450 : 12531257.[PubMed] [CrossRef]
90. Henault J,, Martinez J,, Riggs JM,, Tian J,, Mehta P,, Clarke L,, Sasai M,, Latz E,, Brinkmann MM,, Iwasaki A,, Coyle AJ,, Kolbeck R,, Green DR,, Sanjuan MA . 2012. Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity 37 : 986997.[PubMed] [CrossRef]
91. Martinez J,, Almendinger J,, Oberst A,, Ness R,, Dillon CP,, Fitzgerald P,, Hengartner MO,, Green DR . 2011. Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci U S A 108 : 1739617401.[PubMed] [CrossRef]
92. Huang J,, Canadien V,, Lam GY,, Steinberg BE,, Dinauer MC,, Magalhaes MA,, Glogauer M,, Grinstein S,, Brumell JH . 2009. Activation of antibacterial autophagy by NADPH oxidases. Proc Natl Acad Sci U S A 106 : 62266231.[PubMed] [CrossRef]
93. Gong L,, Cullinane M,, Treerat P,, Ramm G,, Prescott M,, Adler B,, Boyce JD,, Devenish RJ . 2011. The Burkholderia pseudomallei type III secretion system and BopA are required for evasion of LC3-associated phagocytosis. PLoS One 6 : e17852. doi:10.1371/journal.pone.0017852. [CrossRef]
94. Cullinane M,, Gong L,, Li X,, Lazar-Adler N,, Tra T,, Wolvetang E,, Prescott M,, Boyce JD,, Devenish RJ,, Adler B . 2008. Stimulation of autophagy suppresses the intracellular survival of Burkholderia pseudomallei in mammalian cell lines. Autophagy 4 : 744753.[PubMed] [CrossRef]
95. Lamkanfi M,, Dixit VM . 2010. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8 : 4454.[PubMed] [CrossRef]
96. Ashida H,, Mimuro H,, Ogawa M,, Kobayashi T,, Sanada T,, Kim M,, Sasakawa C . 2011. Cell death and infection: a double-edged sword for host and pathogen survival. J Cell Biol 195 : 931942.[PubMed] [CrossRef]
97. Rudel T,, Kepp O,, Kozjak-Pavlovic V . 2010. Interactions between bacterial pathogens and mitochondrial cell death pathways. Nat Rev Microbiol 8 : 693705.[PubMed] [CrossRef]
98. Sridharan H,, Upton JW . 2014. Programmed necrosis in microbial pathogenesis. Trends Microbiol 22 : 199207.[PubMed] [CrossRef]
99. Kaiser WJ,, Upton JW,, Long AB,, Livingston-Rosanoff D,, Daley-Bauer LP,, Hakem R,, Caspary T,, Mocarski ES . 2011. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471 : 368372.[PubMed] [CrossRef]
100. Holler N,, Zaru R,, Micheau O,, Thome M,, Attinger A,, Valitutti S,, Bodmer JL,, Schneider P,, Seed B,, Tschopp J . 2000. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 1 : 489495.[PubMed] [CrossRef]
101. Mocarski ES,, Upton JW,, Kaiser WJ . 2011. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat Rev Immunol 12 : 7988.[CrossRef]
102. Miao EA,, Leaf IA,, Treuting PM,, Mao DP,, Dors M,, Sarkar A,, Warren SE,, Wewers MD,, Aderem A . 2010. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11 : 11361142.[PubMed] [CrossRef]
103. Ross TM . 2001. Using death to one’s advantage: HIV modulation of apoptosis. Leukemia 15 : 332341.[PubMed] [CrossRef]
104. Early J,, Fischer K,, Bermudez LE . 2011. Mycobacterium avium uses apoptotic macrophages as tools for spreading. Microb Pathog 50 : 132139.[PubMed] [CrossRef]
105. Cornelis GR . 2006. The type III secretion injectisome. Nat Rev Microbiol 4 : 811825.[PubMed] [CrossRef]
106. Blocker AJ,, Deane JE,, Veenendaal AK,, Roversi P,, Hodgkinson JL,, Johnson S,, Lea SM . 2008. What’s the point of the type III secretion system needle? Proc Natl Acad Sci U S A 105 : 65076513.[PubMed] [CrossRef]
107. Valdivia RH . 2008. Chlamydia effector proteins and new insights into chlamydial cellular microbiology. Curr Opin Microbiol 11 : 5359.[PubMed] [CrossRef]
108. Ho TD,, Starnbach MN . 2005. The Salmonella enterica serovar Typhimurium-encoded type III secretion systems can translocate Chlamydia trachomatis proteins into the cytosol of host cells. Infect Immun 73 : 905911.[PubMed] [CrossRef]
109. Subtil A,, Delevoye C,, Balañá ME,, Tastevin L,, Perrinet S,, Dautry-Varsat A . 2005. A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates. Mol Microbiol 56 : 16361647.[PubMed] [CrossRef]
110. Pennini ME,, Perrinet S,, Dautry-Varsat A,, Subtil A . 2010. Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis . PLoS Pathog 6 : e1000995. doi:10.1371/journal.ppat.1000995. [CrossRef]
111. da Cunha M,, Milho C,, Almeida F,, Pais SV,, Borges V,, Maurício R,, Borrego MJ,, Gomes JP,, Mota LJ . 2014. Identification of type III secretion substrates of Chlamydia trachomatis using Yersinia enterocolitica as a heterologous system. BMC Microbiol 14 : 40. doi:10.1186/1471-2180-14-40. [CrossRef]
112. Christie PJ,, Cascales E . 2005. Structural and dynamic properties of bacterial type IV secretion systems (review). Mol Membr Biol 22 : 5161.[CrossRef]
113. Vogel JP,, Andrews HL,, Wong SK,, Isberg RR . 1998. Conjugative transfer by the virulence system of Legionella pneumophila . Science 279 : 873876.[PubMed] [CrossRef]
114. O’Callaghan D,, Cazevieille C,, Allardet-Servent A,, Boschiroli ML,, Bourg G,, Foulongne V,, Frutos P,, Kulakov Y,, Ramuz M . 1999. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis . Mol Microbiol 33 : 12101220.[PubMed] [CrossRef]
115. Sadosky AB,, Wiater LA,, Shuman HA . 1993. Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun 61 : 53615373.[PubMed]
116. Berger KH,, Merriam JJ,, Isberg RR . 1994. Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol Microbiol 14 : 809822.[PubMed] [CrossRef]
117. Carey KL,, Newton HJ,, Lührmann 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. [CrossRef]
118. Liu H,, Bao W,, Lin M,, Niu H,, Rikihisa Y . 2012. Ehrlichia type IV secretion effector ECH0825 is translocated to mitochondria and curbs ROS and apoptosis by upregulating host MnSOD. Cell Microbiol 14 : 10371050.[PubMed] [CrossRef]
119. Lin M,, den Dulk-Ras A,, Hooykaas PJ,, Rikihisa Y . 2007. Anaplasma phagocytophilum AnkA secreted by type IV secretion system is tyrosine phosphorylated by Abl-1 to facilitate infection. Cell Microbiol 9 : 26442657.[PubMed] [CrossRef]
120. Rikihisa Y,, Lin M . 2010. Anaplasma phagocytophilum and Ehrlichia chaffeensis type IV secretion and Ank proteins. Curr Opin Microbiol 13 : 5966.[PubMed] [CrossRef]
121. Kudryashev M,, Wang RY,, Brackmann M,, Scherer S,, Maier T,, Baker D,, DiMaio F,, Stahlberg H,, Egelman EH,, Basler M . 2015. Structure of the type VI secretion system contractile sheath. Cell 160 : 952962.[PubMed] [CrossRef]
122. Coulthurst SJ . 2013. The Type VI secretion system—a widespread and versatile cell targeting system. Res Microbiol 164 : 640654.[PubMed] [CrossRef]
123. Pezoa D,, Blondel CJ,, Silva CA,, Yang HJ,, Andrews-Polymenis H,, Santiviago CA,, Contreras I . 2014. Only one of the two type VI secretion systems encoded in the Salmonella enterica serotype Dublin genome is involved in colonization of the avian and murine hosts. Vet Res 45 : 2. doi:10.1186/1297-9716-45-2. [CrossRef]
124. Mulder DT,, Cooper CA,, Coombes BK . 2012. Type VI secretion system-associated gene clusters contribute to pathogenesis of Salmonella enterica serovar Typhimurium. Infect Immun 80 : 19962007.[PubMed] [CrossRef]
125. Blondel CJ,, Jiménez JC,, Leiva LE,, Alvarez SA,, Pinto BI,, Contreras F,, Pezoa D,, Santiviago CA,, Contreras I . 2013. The type VI secretion system encoded in Salmonella pathogenicity island 19 is required for Salmonella enterica serotype Gallinarum survival within infected macrophages. Infect Immun 81 : 12071220.[PubMed] [CrossRef]
126. Bansal-Mutalik R,, Nikaido H . 2014. Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. Proc Natl Acad Sci U S A 111 : 49584963.[PubMed] [CrossRef]
127. Abdallah AM,, Gey van Pittius NC,, Champion PA,, Cox J,, Luirink J,, Vandenbroucke-Grauls CM,, Appelmelk BJ,, Bitter W . 2007. Type VII secretion—mycobacteria show the way. Nat Rev Microbiol 5 : 883891.[PubMed] [CrossRef]
128. Bitter W,, Houben EN,, Bottai D,, Brodin P,, Brown EJ,, Cox JS,, Derbyshire K,, Fortune SM,, Gao LY,, Liu J,, Gey van Pittius NC,, Pym AS,, Rubin EJ,, Sherman DR,, Cole ST,, Brosch R . 2009. Systematic genetic nomenclature for type VII secretion systems. PLoS Pathog 5 : e1000507. doi:10.1371/journal.ppat.1000507. [CrossRef]
129. Pallen MJ . 2002. The ESAT-6/WXG100 superfamily—and a new Gram-positive secretion system? Trends Microbiol 10 : 209212.[CrossRef]
130. Brodin P,, Majlessi L,, Marsollier L,, de Jonge MI,, Bottai D,, Demangel C,, Hinds J,, Neyrolles O,, Butcher PD,, Leclerc C,, Cole ST,, Brosch R . 2006. Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 74 : 8898.[PubMed] [CrossRef]
131. Pym AS,, Brodin P,, Majlessi L,, Brosch R,, Demangel C,, Williams A,, Griffiths KE,, Marchal G,, Leclerc C,, Cole ST . 2003. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat Med 9 : 533539.[PubMed] [CrossRef]
132. Ekiert DC,, Cox JS . 2014. Structure of a PE-PPE-EspG complex from Mycobacterium tuberculosis reveals molecular specificity of ESX protein secretion. Proc Natl Acad Sci U S A 111 : 1475814763.[PubMed] [CrossRef]
133. van der Wel N,, Hava D,, Houben D,, Fluitsma D,, van Zon M,, Pierson J,, Brenner M,, Peters PJ . 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129 : 12871298.[PubMed] [CrossRef]
134. Méresse S,, Steele-Mortimer O,, Moreno E,, Desjardins M,, Finlay B,, Gorvel JP . 1999. Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat Cell Biol 1 : E183E188.[PubMed]
135. Vogel JP,, Isberg RR . 1999. Cell biology of Legionella pneumophila . Curr Opin Microbiol 2 : 3034.[CrossRef]
136. Pizarro-Cerdá J,, Méresse S,, Parton RG,, van der Goot G,, Sola-Landa A,, Lopez-Goñi 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 : 57115724.[PubMed]
137. 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 : 545556.[PubMed] [CrossRef]
138. Franco IS,, Shuman HA,, Charpentier X . 2009. The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell Microbiol 11 : 14351443.[PubMed] [CrossRef]
139. Nagai H,, Kagan JC,, Zhu X,, Kahn RA,, Roy CR . 2002. A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295 : 679682.[PubMed] [CrossRef]
140. Neunuebel MR,, Chen Y,, Gaspar AH,, Backlund PS Jr,, Yergey A,, Machner MP . 2011. De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila . Science 333 : 453456.[PubMed] [CrossRef]
141. Neunuebel MR,, Machner MP . 2012. The taming of a Rab GTPase by Legionella pneumophila . Small GTPases 3 : 2833.[PubMed] [CrossRef]
142. Derré I,, Isberg RR . 2004. Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect Immun 72 : 30483053.[PubMed] [CrossRef]
143. Kagan JC,, Roy CR . 2002. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 4 : 945954.[PubMed] [CrossRef]
144. Scidmore MA,, Fischer ER,, Hackstadt T . 1996. Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J Cell Biol 134 : 363374.[PubMed] [CrossRef]
145. Heuer D,, Rejman Lipinski A,, Machuy N,, Karlas A,, Wehrens A,, Siedler F,, Brinkmann V,, Meyer TF . 2009. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457 : 731735.[PubMed] [CrossRef]
146. Boleti H,, Benmerah A,, Ojcius DM,, Cerf-Bensussan N,, Dautry-Varsat A . 1999. Chlamydia infection of epithelial cells expressing dynamin and Eps15 mutants: clathrin-independent entry into cells and dynamin-dependent productive growth. J Cell Sci 112 : 14871496.[PubMed]
147. 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 : 1332613331.[PubMed] [CrossRef]
148. Mehra A,, Zahra A,, Thompson V,, Sirisaengtaksin N,, Wells A,, Porto M,, Köster S,, Penberthy K,, Kubota Y,, Dricot A,, Rogan D,, Vidal M,, Hill DE,, Bean AJ,, Philips JA . 2013. Mycobacterium tuberculosis type VII secreted effector EsxH targets host ESCRT to impair trafficking. PLoS Pathog 9 : e1003734. doi:10.1371/journal.ppat.1003734. [CrossRef]
149. 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 U S A 108 : 1937119376.[PubMed] [CrossRef]
150. Xu L,, Shen X,, Bryan A,, Banga S,, Swanson MS,, Luo ZQ . 2010. Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector. PLoS Pathog 6 : e1000822. doi:10.1371/journal.ppat.1000822. [CrossRef]
151. Fratti RA,, Chua J,, Vergne I,, Deretic V . 2003. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A 100 : 54375442.[PubMed] [CrossRef]
152. Vergne I,, Chua J,, Lee HH,, Lucas M,, Belisle J,, Deretic V . 2005. Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis . Proc Natl Acad Sci U S A 102 : 40334038.[PubMed] [CrossRef]
153. Fratti RA,, Backer JM,, Gruenberg J,, Corvera S,, Deretic V . 2001. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 154 : 631644.[PubMed] [CrossRef]
154. Philips JA . 2008. Mycobacterial manipulation of vacuolar sorting. Cell Microbiol 10 : 24082415.[PubMed] [CrossRef]
155. Alix E,, Mukherjee S,, Roy CR . 2011. Subversion of membrane transport pathways by vacuolar pathogens. J Cell Biol 195 : 943952.[PubMed] [CrossRef]
156. Steele-Mortimer O,, Méresse S,, Gorvel JP,, Toh BH,, Finlay BB . 1999. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1 : 3349.[PubMed] [CrossRef]
157. Steele-Mortimer O . 2008. The Salmonella-containing vacuole: moving with the times. Curr Opin Microbiol 11 : 3845.[PubMed] [CrossRef]
158. 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 : 561573.[PubMed] [CrossRef]
159. Newton HJ,, Kohler LJ,, McDonough JA,, Temoche-Diaz M,, Crabill E,, Hartland EL,, Roy CR . 2014. A screen of Coxiella burnetii mutants reveals important roles for Dot/Icm effectors and host autophagy in vacuole biogenesis. PLoS Pathog 10 : e1004286. doi:10.1371/journal.ppat.1004286. [CrossRef]
160. 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 : 661670.[PubMed] [CrossRef]
161. Thurston TL,, Wandel MP,, von Muhlinen N,, Foeglein A,, Randow F . 2012. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482 : 414418.[PubMed] [CrossRef]
162. Paz I,, Sachse M,, Dupont N,, Mounier J,, Cederfur C,, Enninga J,, Leffler H,, Poirier F,, Prevost MC,, Lafont F,, Sansonetti P . 2010. Galectin-3, a marker for vacuole lysis by invasive pathogens. Cell Microbiol 12 : 530544.[PubMed] [CrossRef]
163. Perrin AJ,, Jiang X,, Birmingham CL,, So NS,, Brumell JH . 2004. Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr Biol 14 : 806811.[PubMed] [CrossRef]
164. Creasey EA,, Isberg RR . 2014. Maintenance of vacuole integrity by bacterial pathogens. Curr Opin Microbiol 17 : 4652.[PubMed] [CrossRef]
165. Kumar Y,, Valdivia RH . 2009. Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 5 : 593601.[PubMed] [CrossRef]
166. Radtke AL,, O’Riordan MX . 2008. Homeostatic maintenance of pathogen-containing vacuoles requires TBK1-dependent regulation of aquaporin-1. Cell Microbiol 10 : 21972207.[PubMed] [CrossRef]
167. Meunier E,, Dick MS,, Dreier RF,, Schürmann N,, Kenzelmann Broz D,, Warming S,, Roose-Girma M,, Bumann D,, Kayagaki N,, Takeda K,, Yamamoto M,, Broz P . 2014. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 509 : 366370.[PubMed] [CrossRef]
168. Kumar Y,, Valdivia RH . 2008. Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds. Cell Host Microbe 4 : 159169.[PubMed] [CrossRef]
169. Méresse S,, Unsworth KE,, Habermann A,, Griffiths G,, Fang F,, Martínez-Lorenzo MJ,, Waterman SR,, Gorvel JP,, Holden DW . 2001. Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella . Cell Microbiol 3 : 567577.[PubMed] [CrossRef]
170. Jorgensen I,, Bednar MM,, Amin V,, Davis BK,, Ting JP,, McCafferty DG,, Valdivia RH . 2011. The Chlamydia protease CPAF regulates host and bacterial proteins to maintain pathogen vacuole integrity and promote virulence. Cell Host Microbe 10 : 2132.[PubMed] [CrossRef]
171. Wasylnka JA,, Bakowski MA,, Szeto J,, Ohlson MB,, Trimble WS,, Miller SI,, Brumell JH . 2008. Role for myosin II in regulating positioning of Salmonella-containing vacuoles and intracellular replication. Infect Immun 76 : 27222735.[PubMed] [CrossRef]
172. Dumont A,, Boucrot E,, Drevensek S,, Daire V,, Gorvel JP,, Poüs C,, Holden DW,, Méresse S . 2010. SKIP, the host target of the Salmonella virulence factor SifA, promotes kinesin-1-dependent vacuolar membrane exchanges. Traffic 11 : 899911.[PubMed] [CrossRef]
173. Beuzón CR,, Méresse S,, Unsworth KE,, Ruíz-Albert J,, Garvis S,, Waterman SR,, Ryder TA,, Boucrot E,, Holden DW . 2000. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19 : 32353249.[PubMed] [CrossRef]
174. Cheng W,, Yin K,, Lu D,, Li B,, Zhu D,, Chen Y,, Zhang H,, Xu S,, Chai J,, Gu L . 2012. Structural insights into a unique Legionella pneumophila effector LidA recognizing both GDP and GTP bound Rab1 in their active state. PLoS Pathog 8 : e1002528. doi:10.1371/journal.ppat.1002528. [CrossRef]
175. Brumell JH,, Tang P,, Zaharik ML,, Finlay BB . 2002. Disruption of the Salmonella-containing vacuole leads to increased replication of Salmonella enterica serovar Typhimurium in the cytosol of epithelial cells. Infect Immun 70 : 32643270.[PubMed] [CrossRef]
176. Hilbi H,, Weber S,, Finsel I . 2011. Anchors for effectors: subversion of phosphoinositide lipids by Legionella . Front Microbiol 2 : 91. doi:10.3389/fmicb.2011.00091. [CrossRef]
177. 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. [CrossRef]
178. 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]
179. Nawabi P,, Catron DM,, Haldar K . 2008. Esterification of cholesterol by a type III secretion effector during intracellular Salmonella infection. Mol Microbiol 68 : 173185.[PubMed] [CrossRef]
180. Flieger A,, Neumeister B,, Cianciotto NP . 2002. Characterization of the gene encoding the major secreted lysophospholipase A of Legionella pneumophila and its role in detoxification of lysophosphatidylcholine. Infect Immun 70 : 60946106.[PubMed] [CrossRef]
181. Creasey EA,, Isberg RR . 2012. The protein SdhA maintains the integrity of the Legionella-containing vacuole. Proc Natl Acad Sci U S A 109 : 34813486.[PubMed] [CrossRef]
182. Ruiz-Albert J,, Yu XJ,, Beuzón CR,, Blakey AN,, Galyov EE,, Holden DW . 2002. Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol Microbiol 44 : 645661.[PubMed] [CrossRef]
183. Watson RO,, Manzanillo PS,, Cox JS . 2012. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150 : 803815