Macrophage cell death in microbial infections

Cellular Microbiology

Volumn 18, Issue 4, 2016, Pages 466-474

  Chow, Seong H ^a   Deo, Pankaj ^a   Naderer, Thomas ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN;

APOPTOSIS; ARTICLE; BACTERIAL INFECTION; BACTERIAL SURVIVAL; CELL DEATH; CELL INVASION; HUMAN; IMMUNE EVASION; INTRACELLULAR SIGNALING; LEISHMANIA; MACROPHAGE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; ANIMAL; COMMUNICABLE DISEASE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL DEATH; COMMUNICABLE DISEASES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; MACROPHAGES;

EID: 84961209950     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12573     Document Type: Article

References (98)

1. Aachoui, Y., Leaf, I.A., Hagar, J.A., Fontana, M.F., Campos, C.G., Zak, D.E., et al. (2013) Caspase-11 protects against bacteria that escape the vacuole. Science 339: 975-978.
2. Abu Khweek, A., Fernandez Davila, N.S., Caution, K., Akhter, A., Abdulrahman, B.A., Tazi, M., et al. (2013) Biofilm-derived Legionella pneumophila evades the innate immune response in macrophages. Front Cell Infect Microbiol 3: 18.
3. Abu-Zant, A., Jones, S., Asare, R., Suttles, J., Price, C., Graham, J., and Kwaik, Y.A. (2007) Anti-apoptotic signalling by the Dot/Icm secretion system of L. pneumophila. Cell Microbiol 9: 246-264.
4. Afonso, L., Borges, V.M., Cruz, H., Ribeiro-Gomes, F.L., DosReis, G.A., Dutra, A.N., et al. (2008) Interactions with apoptotic but not with necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis. J Leukoc Biol 84: 389-396.
5. Akhter, A., Caution, K., Abu Khweek, A., Tazi, M., Abdulrahman, B.A., Abdelaziz, D.H., et al. (2012) Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization. Immunity 37: 35-47.
6. Akhter, A., Gavrilin, M.A., Frantz, L., Washington, S., Ditty, C., Limoli, D., et al. (2009) Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog 5: e1000361.
7. Alonzo, F., III, and Torres, V.J. (2014) The bicomponent pore-forming leucocidins of Staphylococcus aureus. Microbiol Mol Biol Rev 78: 199-230.
8. Banga, S., Gao, P., Shen, X., Fiscus, V., Zong, W.X., Chen, L., and Luo, Z.Q. (2007) Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc Natl Acad Sci U S A 104: 5121-5126.
9. Barry, K.C., Fontana, M.F., Portman, J.L., Dugan, A.S., and Vance, R.E. (2013) IL-1alpha signaling initiates the inflammatory response to virulent Legionella pneumophila in vivo. J Immunol 190: 6329-6339.
10. Bielaszewska, M., Ruter, C., Kunsmann, L., Greune, L., Bauwens, A., Zhang, W., et al. (2013) Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. PLoS Pathog 9: e1003797.
11. Broz, P., Ruby, T., Belhocine, K., Bouley, D.M., Kayagaki, N., Dixit, V.M., and Monack, D.M. (2012) Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490: 288-291.
12. Byrne, B.G., Dubuisson, J.F., Joshi, A.D., Persson, J.J., and Swanson, M.S. (2013) Inflammasome components coordinate autophagy and pyroptosis as macrophage responses to infection. mBio 4: e00620-00612.
13. Carratala, J., and Garcia-Vidal, C. (2010) An update on Legionella. Curr Opin Infect Dis 23: 152-157.
14. Case, C.L., Kohler, L.J., Lima, J.B., Strowig, T., de Zoete, M.R., Flavell, R.A., et al. (2013) Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila. Proc Natl Acad Sci U S A 29: 1851-1856.
15. Cazalet, C., Gomez-Valero, L., Rusniok, C., Lomma, M., Dervins-Ravault, D., Newton, H.J., et al. (2010) Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet 6: e1000851.
16. Chateau, A., and Seifert, H.S. (2015) Neisseria gonorrhoeae survives within and modulates apoptosis and inflammatory cytokine production of human macrophages. Cell Microbiol. DOI: 10.1111/cmi.12529.
17. Chipuk, J.E., McStay, G.P., Bharti, A., Kuwana, T., Clarke, C.J., Siskind, L.J., et al. (2012) Sphingolipid metabolism cooperates with BAK and BAX to promote the mitochondrial pathway of apoptosis. Cell 148: 988-1000.
18. Craven, R.R., Gao, X., Allen, I.C., Gris, D., Wardenburg, J.B., McElvania-TeKippe, E., et al. (2009) Staphylococcus aureus α-hemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells. PLoS One 4: e7446.
19. Creasey, E.A., and Isberg, R.R. (2012) The protein SdhA maintains the integrity of the Legionella-containing vacuole. Proc Natl Acad Sci U S A 28: 3481-3486.
20. Cunha, L.D., Ribeiro, J.M., Fernandes, T.D., Massis, L.M., Khoo, C.A., Moffatt, J.H., et al. (2015) Inhibition of inflammasome activation by Coxiella burnetii type IV secretion system effector IcaA. Nat Commun 6: 10205.
21. Czabotar, P.E., Lessene, G., Strasser, A., and Adams, J.M. (2014) Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol 15: 49-63.
22. DaMata, J.P., Mendes, B.P., Maciel-Lima, K., Menezes, C.A., Dutra, W.O., Sousa, L.P., and Horta, M.F. (2015) Distinct macrophage fates after in vitro infection with different species of Leishmania: induction of apoptosis by Leishmania (Leishmania) amazonensis, but not by Leishmania (Viannia) guyanensis. PLoS One 10: e0141196.
23. Das, S., Ghosh, A.K., Singh, S., Saha, B., Ganguly, A., and Das, P. (2015) Unmethylated CpG motifs in the L. donovani DNA regulate TLR9-dependent delay of programmed cell death in macrophages. J Leukoc Biol 97: 363-378.
24. Du, X., Youle, R.J., FitzGerald, D.J., and Pastan, I. (2010) Pseudomonas exotoxin A-mediated apoptosis is Bak dependent and preceded by the degradation of Mcl-1. Mol Cell Biol 30: 3444-3452.
25. Fukao, T., Tanabe, M., Terauchi, Y., Ota, T., Matsuda, S., Asano, T., et al. (2002) PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat Immunol 3: 875-881.
26. Galluzzi, L., Bravo-San Pedro, J.M., Vitale, I., Aaronson, S.A., Abrams, J.M., Adam, D., et al. (2015) Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ 22: 58-73.
27. Gonzalez-Juarbe, N., Gilley, R.P., Hinojosa, C.A., Bradley, K.M., Kamei, A., Gao, G., et al. (2015) Pore-forming toxins induce macrophage necroptosis during acute bacterial pneumonia. PLoS Pathog 11: e1005337.
28. Greaney, A.J., Leppla, S.H., and Moayeri, M. (2015) Bacterial exotoxins and the inflammasome. Front Immunol 6: 570.
29. Gueirard, P., Laplante, A., Rondeau, C., Milon, G., and Desjardins, M. (2008) Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages. Cell Microbiol 10: 100-111.
30. Hildebrand, J.M., Tanzer, M.C., Lucet, I.S., Young, S.N., Spall, S.K., Sharma, P., et al. (2014) Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. Proc Natl Acad Sci U S A 111: 15072-15077.
31. Holzinger, D., Gieldon, L., Mysore, V., Nippe, N., Taxman, D.J., Duncan, J.A., et al. (2012) Staphylococcus aureus Panton-Valentine leukocidin induces an inflammatory response in human phagocytes via the NLRP3 inflammasome. J Leukoc Biol 92: 1069-1081.
32. Hongo, I., Baba, T., Oishi, K., Morimoto, Y., Ito, T., and Hiramatsu, K. (2009) Phenol-soluble modulin α3 enhances the human neutrophil lysis mediated by Panton-Valentine leukocidin. J Infect Dis 200: 715-722.
33. Huang, J., and Brumell, J.H. (2014) Bacteria-autophagy interplay: a battle for survival. Nat Rev Microbiol 12: 101-114.
34. Jiang, J.H., Davies, J.K., Lithgow, T., Strugnell, R.A., and Gabriel, K. (2011) Targeting of Neisserial PorB to the mitochondrial outer membrane: an insight on the evolution of beta-barrel protein assembly machines. Mol Microbiol 82: 976-987.
35. Jin, J.S., Kwon, S.O., Moon, D.C., Gurung, M., Lee, J.H., Kim, S.I., and Lee, J.C. (2011) Acinetobacter baumannii secretes cytotoxic outer membrane protein A via outer membrane vesicles. PLoS One 6: e17027.
36. Kaparakis-Liaskos, M., and Ferrero, R.L. (2015) Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol 15: 375-387.
37. Kayagaki, N., Stowe, I.B., Lee, B.L., O'Rourke, K., Anderson, K., Warming, S., et al. (2015) Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526: 666-671.
38. Kayagaki, N., Warming, S., Lamkanfi, M., Vande Walle, L., Louie, S., Dong, J., et al. (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479: 117-121.
39. Kebaier, C., Chamberland, R.R., Allen, I.C., Gao, X., Broglie, P.M., Hall, J.D., et al. (2012) Staphylococcus aureus α-hemolysin mediates virulence in a murine model of severe pneumonia through activation of the NLRP3 inflammasome. J Infect Dis 205: 807-817.
40. Kepp, O., Gottschalk, K., Churin, Y., Rajalingam, K., Brinkmann, V., Machuy, N., et al. (2009) Bim and Bmf synergize to induce apoptosis in Neisseria gonorrhoeae infection. PLoS Pathog 5: e1000348.
41. Kitur, K., Parker, D., Nieto, P., Ahn, D.S., Cohen, T.S., Chung, S., et al. (2015) Toxin-induced necroptosis is a major mechanism of Staphylococcus aureus lung damage. PLoS Pathog 11: e1004820.
42. Klingenbeck, L., Eckart, R.A., Berens, C., and Luhrmann, A. (2013) The Coxiella burnetii type IV secretion system substrate CaeB inhibits intrinsic apoptosis at the mitochondrial level. Cell Microbiol 15: 675-687.
43. Kortmann, J., Brubaker, S.W., and Monack, D.M. (2015) Cutting edge: inflammasome activation in primary human macrophages is dependent on flagellin. J Immunol 195: 815-819.
44. Kozjak-Pavlovic, V., Dian-Lothrop, E.A., Meinecke, M., Kepp, O., Ross, K., Rajalingam, K., et al. (2009) Bacterial porin disrupts mitochondrial membrane potential and sensitizes host cells to apoptosis. PLoS Pathog 5: e1000629.
45. Kunsmann, L., Ruter, C., Bauwens, A., Greune, L., Gluder, M., Kemper, B., et al. (2015) Virulence from vesicles: novel mechanisms of host cell injury by Escherichia coli O104:H4 outbreak strain. Sci Rep 5: 13252.
46. Lage, S.L., Buzzo, C.L., Amaral, E.P., Matteucci, K.C., Massis, L.M., Icimoto, M.Y., et al. (2013) Cytosolic flagellin-induced lysosomal pathway regulates inflammasome-dependent and -independent macrophage responses. Proc Natl Acad Sci U S A 110: E3321-3330.
47. Lamkanfi, M., and Dixit, V.M. (2010) Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8: 44-54.
48. Laskay, T., van Zandbergen, G., and Solbach, W. (2008) Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: apoptosis as infection-promoting factor. Immunobiology 213: 183-191.
49. Lawlor, K.E., Khan, N., Mildenhall, A., Gerlic, M., Croker, B.A., D'Cruz, A.A., et al. (2015) RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat Commun 6: 6282.
50. Levinsohn, J.L., Newman, Z.L., Hellmich, K.A., Fattah, R., Getz, M.A., Liu, S., et al. (2012) Anthrax lethal factor cleavage of Nlrp1 is required for activation of the inflammasome. PLoS Pathog 8: e1002638.
51. Losick, V.P., and Isberg, R.R. (2006) NF-kappaB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J Exp Med 203: 2177-2189.
52. Luhrmann, A., Nogueira, C.V., Carey, K.L., and Roy, C.R. (2010) Inhibition of pathogen-induced apoptosis by a Coxiella burnetii type IV effector protein. Proc Natl Acad Sci U S A 107: 18997-19001.
53. MacDonald, I.A., and Kuehn, M.J. (2012) Offense and defense: microbial membrane vesicles play both ways. Res Microbiol 163: 607-618.
54. Martin, C.J., Booty, M.G., Rosebrock, T.R., Nunes-Alves, C., Desjardins, D.M., Keren, I., et al. (2012) Efferocytosis is an innate antibacterial mechanism. Cell Host Microbe 12: 289-300.
55. Massari, P., Gunawardana, J., Liu, X., and Wetzler, L.M. (2010) Meningococcal porin PorB prevents cellular apoptosis in a toll-like receptor 2- and NF-kappaB-independent manner. Infect Immun 78: 994-1003.
56. Melehani, J.H., James, D.B.A., DuMont, A.L., Torres, V.J., and Duncan, J.A. (2015) Staphylococcus aureus leukocidin A/B (LukAB) kills human monocytes via host NLRP3 and ASC when extracellular, but not intracellular. PLoS Pathog 11: e1004970.
57. Menu, P., and Vince, J.E. (2011) The NLRP3 inflammasome in health and disease: the good, the bad and the ugly. Clin Exp Immunol 166: 1-15.
58. Miao, E.A., Leaf, I.A., Treuting, P.M., Mao, D.P., Dors, M., Sarkar, A., et al. (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11: 1136-1142.
59. Michalska, M., and Wolf, P. (2015) Pseudomonas Exotoxin A: optimized by evolution for effective killing. Front Microbiol 6: 963.
60. Molmeret, M., Jones, S., Santic, M., Habyarimana, F., Esteban, M.T., and Kwaik, Y.A. (2010) Temporal and spatial trigger of post-exponential virulence-associated regulatory cascades by Legionella pneumophila after bacterial escape into the host cell cytosol. Environ Microbiol 12: 704-715.
61. Molofsky, A.B., Byrne, B.G., Whitfield, N.N., Madigan, C.A., Fuse, E.T., Tateda, K., and Swanson, M.S. (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203: 1093-1104.
62. Moore, K.J., and Matlashewski, G. (1994) Intracellular infection by Leishmania donovani inhibits macrophage apoptosis. J Immunol 152: 2930-2937.
63. Muller, A., Gunther, D., Brinkmann, V., Hurwitz, R., Meyer, T.F., and Rudel, T. (2000) Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells. EMBO J 19: 5332-5343.
64. Naderer, T., and McConville, M.J. (2008) The Leishmania-macrophage interaction: a metabolic perspective. Cell Microbiol 10: 301-308.
65. Newton, H.J., Ang, D.K., van Driel, I.R., and Hartland, E.L. (2010) Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23: 274-298.
66. Pereira, M.S., Marques, G.G., Dellama, J.E., and Zamboni, D.S. (2011) The Nlrc4 inflammasome contributes to restriction of pulmonary infection by flagellated Legionella spp. that trigger pyroptosis. Front Microbiol 2: 33.
67. Perret, M., Badiou, C., Lina, G., Burbaud, S., Benito, Y., Bes, M., et al. (2012) Cross-talk between Staphylococcus aureus leukocidins-intoxicated macrophages and lung epithelial cells triggers chemokine secretion in an inflammasome-dependent manner. Cell Microbiol 14: 1019-1036.
68. Peters, N.C., Egen, J.G., Secundino, N., Debrabant, A., Kimblin, N., Kamhawi, S., et al. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321: 970-974.
69. Pierini, R., Juruj, C., Perret, M., Jones, C.L., Mangeot, P., Weiss, D.S., and Henry, T. (2012) AIM2/ASC triggers caspase-8-dependent apoptosis in Francisella-infected caspase-1-deficient macrophages. Cell Death Differ 19: 1709-1721.
70. Prates, D.B., Araujo-Santos, T., Luz, N.F., Andrade, B.B., Franca-Costa, J., Afonso, L., et al. (2011) Lutzomyia longipalpis saliva drives apoptosis and enhances parasite burden in neutrophils. J Leukoc Biol 90: 575-582.
71. Price, J.V., and Vance, R.E. (2014) The macrophage paradox. Immunity 41: 685-693.
72. Proto, W.R., Coombs, G.H., and Mottram, J.C. (2013) Cell death in parasitic protozoa: regulated or incidental? Nat Rev Microbiol 11: 58-66.
73. Real, F., Florentino, P.T., Reis, L.C., Ramos-Sanchez, E.M., Veras, P.S., Goto, H., and Mortara, R.A. (2014) Cell-to-cell transfer of Leishmania amazonensis amastigotes is mediated by immunomodulatory LAMP-rich parasitophorous extrusions. Cell Microbiol 16: 1549-1564.
74. Ren, T., Zamboni, D.S., Roy, C.R., Dietrich, W.F., and Vance, R.E. (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18.
75. Ribeiro-Gomes, F.L., Peters, N.C., Debrabant, A., and Sacks, D.L. (2012a) Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-Leishmania response. PLoS Pathog 8: e1002536.
76. Ribeiro-Gomes, F.L., and Sacks, D. (2012b) The influence of early neutrophil-Leishmania interactions on the host immune response to infection. Front Cell Infect Microbiol 2: 59.
77. Robinson, N., McComb, S., Mulligan, R., Dudani, R., Krishnan, L., and Sad, S. (2012) Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat Immunol 13: 954-962.
78. Roca, F.J., and Ramakrishnan, L. (2013) TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 153: 521-534.
79. Ruhland, A., Leal, N., and Kima, P.E. (2007) Leishmania promastigotes activate PI3K/Akt signalling to confer host cell resistance to apoptosis. Cell Microbiol 9: 84-96.
80. Sagulenko, V., Thygesen, S.J., Sester, D.P., Idris, A., Cridland, J.A., Vajjhala, P.R., et al. (2013) AIM2 and NLRP3 inflammasomes activate both apoptotic and pyroptotic death pathways via ASC. Cell Death Differ 20: 1149-1160.
81. Saitoh, T., Fujita, N., Jang, M.H., Uematsu, S., Yang, B.G., Satoh, T., et al. (2008) Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456: 264-268.
82. Scherr, T.D., Hanke, M.L., Huang, O., James, D.B.A., Horswill, A.R., Bayles, K.W., et al. (2015) Staphylococcus aureus biofilms induce macrophage dysfunction through leukocidin AB and alpha-toxin. mBio 6: e01021-01015.
83. Shi, J., Zhao, Y., Wang, K., Shi, X., Wang, Y., Huang, H., et al. (2015) Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526: 660-665.
84. Silke, J., Rickard, J.A., and Gerlic, M. (2015) The diverse role of RIP kinases in necroptosis and inflammation. Nat Immunol 16: 689-697.
85. Spaan, A.N., Vrieling, M., Wallet, P., Badiou, C., Reyes-Robles, T., Ohneck, E.A., et al. (2014) The staphylococcal toxins γ-haemolysin AB and CB differentially target phagocytes by employing specific chemokine receptors. Nat Commun 5: 5438.
86. Speir, M., Vince, J.E., and Naderer, T. (2014) Programmed cell death in Legionella infection. Future Microbiol 9: 107-118.
87. Srivastav, S., Basu Ball, W., Gupta, P., Giri, J., Ukil, A., and Das, P.K. (2014) Leishmania donovani prevents oxidative burst-mediated apoptosis of host macrophages through selective induction of suppressors of cytokine signaling (SOCS) proteins. J Biol Chem 289: 1092-1105.
88. Sun, L., Wang, H., Wang, Z., He, S., Chen, S., Liao, D., et al. (2012) Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148: 213-227.
89. Suzuki, T., Franchi, L., Toma, C., Ashida, H., Ogawa, M., Yoshikawa, Y., et al. (2007) Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog 3: e111.
90. Traven, A., and Naderer, T. (2014) Microbial egress: a hitchhiker's guide to freedom. PLoS Pathog 10: e1004201.
91. Van Opdenbosch, N., Gurung, P., Vande Walle, L., Fossoul, A., Kanneganti, T.D., and Lamkanfi, M. (2014) Activation of the NLRP1b inflammasome independently of ASC-mediated caspase-1 autoproteolysis and speck formation. Nat Commun 5: 3209.
92. van Zandbergen, G., Bollinger, A., Wenzel, A., Kamhawi, S., Voll, R., Klinger, M., et al. (2006) Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci U S A 103: 13837-13842.
93. van Zandbergen, G., Klinger, M., Mueller, A., Dannenberg, S., Gebert, A., Solbach, W., and Laskay, T. (2004) Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 173: 6521-6525.
94. Wanderley, J.L., Moreira, M.E., Benjamin, A., Bonomo, A.C., and Barcinski, M.A. (2006) Mimicry of apoptotic cells by exposing phosphatidylserine participates in the establishment of amastigotes of Leishmania (L) amazonensis in mammalian hosts. J Immunol 176: 1834-1839.
95. Weng, D., Marty-Roix, R., Ganesan, S., Proulx, M.K., Vladimer, G.I., Kaiser, W.J., et al. (2014) Caspase-8 and RIP kinases regulate bacteria-induced innate immune responses and cell death. Proc Natl Acad Sci U S A 111: 7391-7396.
96. Zhu, W., Hammad, L.A., Hsu, F., Mao, Y., and Luo, Z.Q. (2013) Induction of caspase 3 activation by multiple L. pneumophila Dot/Icm substrates. Cell Microbiol 15: 1783-1795.
97. Zhu, W., Tao, L., Quick, M.L., Joyce, J.A., Qu, J.M., and Luo, Z.Q. (2015) Sensing cytosolic RpsL by macrophages induces lysosomal cell death and termination of bacterial infection. PLoS Pathog 11: e1004704.
98. Zielke, R.A., Wierzbicki, I.H., Weber, J.V., Gafken, P.R., and Sikora, A.E. (2014) Quantitative proteomics of the Neisseria gonorrhoeae cell envelope and membrane vesicles for the discovery of potential therapeutic targets. Mol Cell Proteomics 13: 1299-1317.