Virulence factors perforate the pathogen-containing vacuole to signal efferocytosis

Atluri, 2011, Interactions of the human pathogenic Brucella species with their hosts, Annu. Rev. Microbiol., 65, 523, 10.1146/annurev-micro-090110-102905 Barquero-Calvo, 2007, Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection, PLoS One, 2, e631, 10.1371/journal.pone.0000631 Burton, 2014, Disparate impact of oxidative host defenses determines the fate of Salmonella during systemic infection in mice, Cell Host Microbe, 15, 72, 10.1016/j.chom.2013.12.006 Conlan, 1996, Neutrophils prevent extracellular colonization of the liver microvasculature by Salmonella Typhimurium, Infect. Immun., 64, 1043, 10.1128/iai.64.3.1043-1047.1996 Cookson, 2001, Pro-inflammatory programmed cell death, Trends Microbiol., 9, 113, 10.1016/S0966-842X(00)01936-3 Cummings, 2006, In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted, Mol. Microbiol., 61, 795, 10.1111/j.1365-2958.2006.05271.x de Barsy, 2011, Identification of a Brucella spp. secreted effector specifically interacting with human small GTPase Rab2, Cell. Microbiol., 13, 1044, 10.1111/j.1462-5822.2011.01601.x de Jong, 2008, Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system, Mol. Microbiol., 70, 1378, 10.1111/j.1365-2958.2008.06487.x Dunlap, 1992, A “safe-site” for Salmonella Typhimurium is within splenic polymorphonuclear cells, Microb. Pathog., 13, 181, 10.1016/0882-4010(92)90019-K Fadok, 2001, Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts, J. Biol. Chem., 276, 1071, 10.1074/jbc.M003649200 Fink, 2019, Pillars article: Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 2006. 8: 1812–1825, J. Immunol., 202, 1913 Franchi, 2006, Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in Salmonella-infected macrophages, Nat. Immunol., 7, 576, 10.1038/ni1346 Grant, 2012, Attenuated Salmonella Typhimurium lacking the pathogenicity island-2 type 3 secretion system grow to high bacterial numbers inside phagocytes in mice, PLoS Pathog, 8, 10.1371/journal.ppat.1003070 Hensel, 1995, Simultaneous identification of bacterial virulence genes by negative selection, Science, 269, 400, 10.1126/science.7618105 Herb, 2021, Reactive oxygen species: not omnipresent but important in many locations, Front. Cell Dev. Biol., 9, 716406, 10.3389/fcell.2021.716406 Hiyoshi, 2018, Mechanisms to evade the phagocyte respiratory burst arose by convergent evolution in typhoidal Salmonella serovars, Cell Rep, 22, 1787, 10.1016/j.celrep.2018.01.016 Hong, 2000, Identification of genes required for chronic persistence of Brucella abortus in mice, Infect. Immun., 68, 4102, 10.1128/IAI.68.7.4102-4107.2000 Ikari, 1983, New synthetic inhibitor to the alternative complement pathway, Immunology, 49, 685 Jorgensen, 2016, Pyroptosis triggers pore-induced intracellular traps (PITs) that capture bacteria and lead to their clearance by efferocytosis, J. Exp. Med., 213, 2113, 10.1084/jem.20151613 Knodler, 2014, Quantitative assessment of cytosolic Salmonella in epithelial cells, PLoS One, 9, 10.1371/journal.pone.0084681 LaRock, 2015, Salmonellae interactions with host processes, Nat. Rev. Microbiol., 13, 191, 10.1038/nrmicro3420 Li, 2017, Brucella rough mutant induce macrophage death via activating IRE1alpha pathway of endoplasmic reticulum stress by enhanced T4SS secretion, Front. Cell. Infect. Microbiol., 7, 422, 10.3389/fcimb.2017.00422 Mack, 2001, Expression and characterization of the chemokine receptors CCR2 and CCR5 in mice, J. Immunol., 166, 4697, 10.4049/jimmunol.166.7.4697 Marchesini, 2011, In search of Brucella abortus type IV secretion substrates: screening and identification of four proteins translocated into host cells through VirB system, Cell. Microbiol., 13, 1261, 10.1111/j.1462-5822.2011.01618.x Matsuda, 2019, Salmonella enterica effectors SifA, SpvB, SseF, SseJ, and SteA contribute to type III secretion system 1-independent inflammation in a streptomycin-pretreated mouse model of colitis, Infect. Immun., 87, e00872-18, 10.1128/IAI.00872-18 Meunier, 2015, Quantification of cytosolic versus vacuolar Salmonella in primary macrophages by differential permeabilization, J. Vis. Exp., 101 Miao, 2006, Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf, Nat. Immunol., 7, 569, 10.1038/ni1344 Monack, 1996, Salmonella Typhimurium invasion induces apoptosis in infected macrophages, Proc. Natl. Acad. Sci. USA, 93, 9833, 10.1073/pnas.93.18.9833 Myeni, 2013, Brucella modulates secretory trafficking via multiple type IV secretion effector proteins, PLoS Pathog, 9, 10.1371/journal.ppat.1003556 Pei, 2008, Cytotoxicity in macrophages infected with rough Brucella mutants is type IV secretion system dependent, Infect. Immun., 76, 30, 10.1128/IAI.00379-07 Richter-Dahlfors, 1997, Murine salmonellosis studied by confocal microscopy: Salmonella Typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo, J. Exp. Med., 186, 569, 10.1084/jem.186.4.569 Rolán, 2007, Mice lacking components of adaptive immunity show increased Brucella abortus virB mutant colonization, Infect. Immun., 75, 2965, 10.1128/IAI.01896-06 Stauffer, 2018, EzColocalization: an ImageJ plugin for visualizing and measuring colocalization in cells and organisms, Sci. Rep., 8, 15764, 10.1038/s41598-018-33592-8 Sun, 2007, Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium, J. Biol. Chem., 282, 33897, 10.1074/jbc.C700181200 Terwagne, 2013, Innate immune recognition of flagellin limits systemic persistence of Brucella, Cell. Microbiol., 15, 942, 10.1111/cmi.12088 Thurston, 2012, Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion, Nature, 482, 414, 10.1038/nature10744 Tian, 2020, A rough Brucella mutant induced macrophage death depends on secretion activity of T4SS, but not on cellular Txnip- and caspase-2-mediated signaling pathway, Vet. Microbiol., 244, 108648, 10.1016/j.vetmic.2020.108648 van der Velden, 2000, Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype Typhimurium, Infect. Immun., 68, 5702, 10.1128/IAI.68.10.5702-5709.2000 Vance, 2009, Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system, Cell Host Microbe, 6, 10, 10.1016/j.chom.2009.06.007 Vazquez-Torres, 2000, Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase, Science, 287, 1655, 10.1126/science.287.5458.1655 Wangdi, 2014, The Vi capsular polysaccharide enables Salmonella enterica serovar typhi to evade microbe-guided neutrophil chemotaxis, PLoS Pathog, 10, 10.1371/journal.ppat.1004306 Zhang, 2009, Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils, Immunity, 31, 761, 10.1016/j.immuni.2009.09.016