Innate Immune Recognition: An Issue More Complex Than Expected
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
31334134
PubMed Central
PMC6616152
DOI
10.3389/fcimb.2019.00241
Knihovny.cz E-zdroje
- Klíčová slova
- Francisella tularensis, innate immune recognition, intracellular replication, phagocytosis, signaling pathways,
- MeSH
- alarminy genetika imunologie MeSH
- bakteriální proteiny genetika imunologie MeSH
- fagocytóza genetika MeSH
- Francisella tularensis genetika imunologie patogenita MeSH
- interakce hostitele a patogenu genetika imunologie MeSH
- lidé MeSH
- makrofágy imunologie mikrobiologie MeSH
- PAMP struktury imunologie metabolismus MeSH
- přirozená imunita * MeSH
- receptory buněčného povrchu genetika imunologie MeSH
- receptory rozpoznávající vzory genetika imunologie MeSH
- regulace genové exprese MeSH
- signální transdukce MeSH
- tularemie genetika imunologie mikrobiologie MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- alarminy MeSH
- bakteriální proteiny MeSH
- PAMP struktury MeSH
- receptory buněčného povrchu MeSH
- receptory rozpoznávající vzory MeSH
Primary interaction of an intracellular bacterium with its host cell is initiated by activation of multiple signaling pathways in response to bacterium recognition itself or as cellular responses to stress induced by the bacterium. The leading molecules in these processes are cell surface membrane receptors as well as cytosolic pattern recognition receptors recognizing pathogen-associated molecular patterns or damage-associated molecular patterns induced by the invading bacterium. In this review, we demonstrate possible sequences of events leading to recognition of Francisella tularensis, present findings on known mechanisms for manipulating cell responses to protect Francisella from being killed, and discuss newly published data from the perspective of early stages of host-pathogen interaction.
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Abdel-Nour M., Tsalikis J., Kleinman D., Girardin S. E. (2014). The emerging role of mTOR signalling in antibacterial immunity. Immunol. Cell Biol. 92, 346–353. 10.1038/icb.2014.3 PubMed DOI
Abplanalp A. L., Morris I. R., Parida B. K., Teale J. M., Berton M. T. (2009). TLR-dependent control of Francisella tularensis infection and host inflammatory responses. PLoS ONE 4:e7920. 10.1371/journal.pone.0007920 PubMed DOI PMC
Akimana C., Al-Khodor S., Abu Kwaik Y. (2010). Host factors required for modulation of phagosome biogenesis and proliferation of Francisella tularensis within the Cytosol. PLoS ONE 5:e11025. 10.1371/journal.pone.0011025 PubMed DOI PMC
Akimana C., Kwaik Y. A. (2011). Francisella-arthropod vector interaction and its role in patho-adaptation to infect mammals. Front. Microbiol. 2:34. 10.3389/fmicb.2011.00034 PubMed DOI PMC
Akira S. (2003). Toll-like receptor signaling. J. Biol. Chem. 278, 38105–38108. 10.1074/jbc.R300028200 PubMed DOI
Almine J. F., O'Hare C. A. J., Dunphy G., Haga I. R., Naik R. J., Atrih A., et al. . (2017). IFI16 and cGAS cooperate in the activation of STING during DNA sensing in human keratinocytes. Nat. Commun. 8:14392. 10.1038/ncomms14392 PubMed DOI PMC
Atianand M. K., Duffy E. B., Shah A., Kar S., Malik M., Harton J. A. (2011). Francisella tularensis reveals a disparity between human and mouse NLRP3 inflammasome activation. J. Biol. Chem. 286, 39033–39042. 10.1074/jbc.M111.244079 PubMed DOI PMC
Bakshi C. S., Malik M., Regan K., Melendez J. A., Metzger D. W., Pavlov V. M., et al. . (2006). Superoxide dismutase B gene (sodB)-deficient mutants of Francisella tularensis demonstrate hypersensitivity to oxidative stress and attenuated virulence. J. Bacteriol. 188, 6443–6448. 10.1128/JB.00266-06 PubMed DOI PMC
Balagopal A., MacFarlane A. S., Mohapatra N., Soni S., Gunn J. S., Schlesinger L. S. (2006). Characterization of the receptor-ligand pathways important for entry and survival of Francisella tularensis in human macrophages. Infect. Immun. 74, 5114–5125. 10.1128/IAI.00795-06 PubMed DOI PMC
Bamburg J. R. (1999). Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15, 185–230. 10.1146/annurev.cellbio.15.1.185 PubMed DOI
Bandyopadhyay S., Long M. E., Allen L.-A. H. (2014). Differential expression of microRNAs in Francisella tularensis-infected human macrophages: miR-155-dependent downregulation of MyD88 inhibits the inflammatory response. PLoS ONE 9:e109525. 10.1371/journal.pone.0109525 PubMed DOI PMC
Banerjee I., Behl B., Mendonca M., Shrivastava G., Russo A. J., Menoret A., et al. . (2018). Gasdermin D restrains type I interferon response to cytosolic DNA by disrupting ionic homeostasis. Immunity. 49, 413–426.e5. 10.1016/j.immuni.2018.07.006 PubMed DOI PMC
Barel M., Charbit A. (2014). Detection of the interaction between host and bacterial proteins: eukaryotic nucleolin interacts with Francisella elongation factor Tu. Methods Mol. Biol. 1197, 123–139. 10.1007/978-1-4939-1261-2_7 PubMed DOI
Barel M., Harduin-Lepers A., Portier L., Slomianny M. C., Charbit A. (2016). Host glycosylation pathways and the unfolded protein response contribute to the infection by Francisella. Cell. Microbiol. 18, 1763–1781. 10.1111/cmi.12614 PubMed DOI
Barel M., Hovanessian A. G., Meibom K., Briand J. P., Dupuis M., Charbit A. (2008). A novel receptor - ligand pathway for entry of Francisella tularensis in monocyte-like THP-1 cells: interaction between surface nucleolin and bacterial elongation factor Tu. BMC Microbiol. 8:145. 10.1186/1471-2180-8-145 PubMed DOI PMC
Barel M., Meibom K., Charbit A. (2010). Nucleolin, a shuttle protein promoting infection of human monocytes by Francisella tularensis. PLoS ONE 5:e14193. 10.1371/journal.pone.0014193 PubMed DOI PMC
Barel M., Meibom K., Dubail I., Botella J., Charbit A. (2012). Francisella tularensis regulates the expression of the amino acid transporter SLC1A5 in infected THP-1 human monocytes. Cell. Microbiol. 14, 1769–1783. 10.1111/j.1462-5822.2012.01837.x PubMed DOI
Barel M., Ramond E., Gesbert G., Charbit A. (2015). The complex amino acid diet of Francisella in infected macrophages. Front. Cell. Infect. Microbiol. 5:9. 10.3389/fcimb.2015.00009 PubMed DOI PMC
Bar-Haim E., Gat O., Markel G., Cohen H., Shafferman A., Velan B. (2008). Interrelationship between dendritic cell trafficking and Francisella tularensis dissemination following airway infection. PLoS Pathog. 4:e1000211. 10.1371/journal.ppat.1000211 PubMed DOI PMC
Barker J. R., Chong A., Wehrly T. D., Yu J. J., Rodriguez S. A., Liu J., et al. . (2009). The Francisella tularensis pathogenicity island encodes a secretion system that is required for phagosome escape and virulence. Mol. Microbiol. 74, 1459–1470. 10.1111/j.1365-2958.2009.06947.x PubMed DOI PMC
Barker J. R., Koestler B. J., Carpenter V. K., Burdette D. L., Waters C. M., Vance R. E., et al. . (2013). STING-dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. mBio 4, e00018–e00013. 10.1128/mBio.00018-13 PubMed DOI PMC
Ben Nasr A., Haithcoat J., Masterson J. E., Gunn J. S., Eaves-Pyles T., Klimpel G. R. (2006). Critical role for serum opsonins and complement receptors CR3 (CD11b/CD18) and CR4 (CD11c/CD18) in phagocytosis of Francisella tularensis by human dendritic cells (DC): uptake of Francisella leads to activation of immature DC and intracellular survival of the bacteria. J. Leukoc. Biol. 80, 774–786. 10.1189/jlb.1205755 PubMed DOI
Ben Nasr A., Klimpel G. R. (2008). Subversion of complement activation at the bacterial surface promotes serum resistance and opsonophagocytosis of Francisella tularensis. J. Leukoc. Biol. 84, 77–85. 10.1189/jlb.0807526 PubMed DOI
Blasius A. L., Beutler B. (2010). Intracellular toll-like receptors. Immunity 32, 305–315. 10.1016/j.immuni.2010.03.012 PubMed DOI
Bourdonnay E., Henry T. (2016). Catch me if you can. eLife 5:e14721. 10.7554/eLife.14721 PubMed DOI PMC
Bradburne C. E., Verhoeven A. B., Manyam G. C., Chaudhry S. A., Chang E. L., Thach D. C., et al. . (2013). Temporal transcriptional response during infection of type II alveolar epithelial cells with Francisella tularensis live vaccine strain (LVS) supports a general host suppression and bacterial uptake by macropinocytosis. J. Biol. Chem. 288, 10780–10791. 10.1074/jbc.M112.362178 PubMed DOI PMC
Brandwein D., Wang Z. (2017). Interaction between Rho GTPases and 14-3-3 Proteins. Int. J. Mol. Sci. 18:E2148. 10.3390/ijms18102148 PubMed DOI PMC
Brock S. R., Parmely M. J. (2017). Francisella tularensis confronts the complement system. Front. Cell. Infect. Microbiol. 7:523. 10.3389/fcimb.2017.00523 PubMed DOI PMC
Brodmann M., Dreier R. F., Broz P., Basler M. (2017). Francisella requires dynamic type VI secretion system and ClpB to deliver effectors for phagosomal escape. Nat. Commun. 8:15853. 10.1038/ncomms15853 PubMed DOI PMC
Bröms J. E., Lavander M., Sjöstedt A. (2009). A conserved alpha-helix essential for a type VI secretion-like system of Francisella tularensis. J. Bacteriol. 191, 2431–2446. 10.1128/JB.01759-08 PubMed DOI PMC
Bröms J. E., Meyer L., Sun K., Lavander M., Sjöstedt A. (2012). Unique substrates secreted by the type VI secretion system of Francisella tularensis during intramacrophage infection. PLoS ONE 7:e50473. 10.1371/journal.pone.0050473 PubMed DOI PMC
Bröms J. E., Sjöstedt A., Lavander M. (2010). The role of the Francisella Tularensis pathogenicity island in type VI secretion, intracellular survival, and modulation of host cell signaling. Front. Microbiol. 1:136. 10.3389/fmicb.2010.00136 PubMed DOI PMC
Bronner D. N., Abuaita B. H., Chen X., Fitzgerald K. A., Nuñez G., He Y., et al. . (2015). Endoplasmic reticulum stress activates the inflammasome via NLRP3- and Caspase-2-driven mitochondrial damage. Immunity 43, 451–462. 10.1016/j.immuni.2015.08.008 PubMed DOI PMC
Bulua A. C., Simon A., Maddipati R., Pelletier M., Park H., Kim K.-Y., et al. . (2011). Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J. Exp. Med. 208, 519–533. 10.1084/jem.20102049 PubMed DOI PMC
Burdette D. L., Monroe K. M., Sotelo-Troha K., Iwig J. S., Eckert B., Hyodo M., et al. . (2011). STING is a direct innate immune sensor of cyclic di-GMP. Nature 478, 515–518. 10.1038/nature10429 PubMed DOI PMC
Butchar J. P., Cremer T. J., Clay C. D., Gavrilin M. A., Wewers M. D., Marsh C. B., et al. . (2008). Microarray analysis of human monocytes infected with Francisella tularensis identifies new targets of host response subversion. PLoS ONE 3:e2924. 10.1371/journal.pone.0002924 PubMed DOI PMC
Calfon M., Zeng H., Urano F., Till J. H., Hubbard S. R., Harding H. P., et al. . (2002). IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92–96. 10.1038/415092a PubMed DOI
Case E. D. R., Chong A., Wehrly T. D., Hansen B., Child R., Hwang S., et al. . (2014). The Francisella O-antigen mediates survival in the macrophage cytosol via autophagy avoidance. Cell. Microbiol. 16, 862–877. 10.1111/cmi.12246 PubMed DOI PMC
Challacombe J. F., Petersen J. M., Gallegos-Graves L. V., Hodge D., Pillai S., Kuske C. R. (2017a). Correction for Challacombe et al., whole-genome relationships among francisella bacteria of diverse origins define new species and provide specific regions for detection. Appl. Environ. Microbiol. 83:e00174-17. 10.1128/AEM.00174-17 PubMed DOI PMC
Challacombe J. F., Petersen J. M., Gallegos-Graves L. V., Hodge D., Pillai S., Kuske C. R. (2017b). Whole-genome relationships among Francisella bacteria of diverse origins define new species and provide specific regions for detection. Appl. Environ. Microbiol. 83:e02589-16. 10.1128/AEM.02589-16 PubMed DOI PMC
Checroun C., Wehrly T. D., Fischer E. R., Hayes S. F., Celli J. (2006). Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc. Natl. Acad. Sci. U.S.A. 103, 14578–14583. 10.1073/pnas.0601838103 PubMed DOI PMC
Chen F., Cui G., Wang S., Nair M. K. M., He L., Qi X., et al. . (2017). Outer membrane vesicle-associated lipase FtlA enhances cellular invasion and virulence in Francisella tularensis LVS. Emerg. Microbes Infect. 6:e66. 10.1038/emi.2017.53 PubMed DOI PMC
Chong A., Wehrly T. D., Child R., Hansen B., Hwang S., Virgin H. W., et al. . (2012). Cytosolic clearance of replication-deficient mutants reveals Francisella tularensis interactions with the autophagic pathway. Autophagy 8, 1342–1356. 10.4161/auto.20808 PubMed DOI PMC
Chong A., Wehrly T. D., Nair V., Fischer E. R., Barker J. R., Klose K. E., et al. . (2008). The early phagosomal stage of Francisella tularensis determines optimal phagosomal escape and Francisella pathogenicity island protein expression. Infect. Immun. 76, 5488–5499. 10.1128/IAI.00682-08 PubMed DOI PMC
Clemens D. L., Horwitz M. A. (2007). Uptake and intracellular fate of Francisella tularensis in human macrophages. Ann. N. Y. Acad. Sci. U.S.A. 1105, 160–186. 10.1196/annals.1409.001 PubMed DOI
Clemens D. L., Lee B.-Y., Horwitz M. A. (2004). Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infect. Immun. 72, 3204–3217. 10.1128/IAI.72.6.3204-3217.2004 PubMed DOI PMC
Clemens D. L., Lee B.-Y., Horwitz M. A. (2005). Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect. Immun. 73, 5892–5902. 10.1128/IAI.73.9.5892-5902.2005 PubMed DOI PMC
Clemens D. L., Lee B.-Y., Horwitz M. A. (2018). The Francisella type VI secretion system. Front. Cell. Infect. Microbiol. 8:121. 10.3389/fcimb.2018.00121 PubMed DOI PMC
Cole L. E., Shirey K. A., Barry E., Santiago A., Rallabhandi P., Elkins K. L., et al. . (2007). Toll-like receptor 2-mediated signaling requirements for Francisella tularensis live vaccine strain infection of murine macrophages. Infect. Immun. 75, 4127–4137. 10.1128/IAI.01868-06 PubMed DOI PMC
Collazo C. M., Sher A., Meierovics A. I., Elkins K. L. (2006). Myeloid differentiation factor-88 (MyD88) is essential for control of primary in vivo Francisella tularensis LVS infection, but not for control of intra-macrophage bacterial replication. Microbes Infect. Inst. Pasteur 8, 779–790. 10.1016/j.micinf.2005.09.014 PubMed DOI
Conlan J. W., Chen W., Bosio C. M., Cowley S. C., Elkins K. L. (2011). Infection of mice with Francisella as an immunological model. Curr. Protoc. Immunol. Ed. John E Coligan Al Chapter 19, Unit 19.14. 10.1002/0471142735.im1914s93 PubMed DOI PMC
Crane D. D., Bauler T. J., Wehrly T. D., Bosio C. M. (2014). Mitochondrial ROS potentiates indirect activation of the AIM2 inflammasome. Front. Microbiol. 5:438. 10.3389/fmicb.2014.00438 PubMed DOI PMC
Craven R. R., Hall J. D., Fuller J. R., Taft-Benz S., Kawula T. H. (2008). Francisella tularensis invasion of lung epithelial cells. Infect. Immun. 76, 2833–2842. 10.1128/IAI.00043-08 PubMed DOI PMC
Cremer T. J., Fatehchand K., Shah P., Gillette D., Patel H., Marsh R. L., et al. . (2012). MiR-155 induction by microbes/microbial ligands requires NF-κB-dependent de novo protein synthesis. Front. Cell. Infect. Microbiol. 2:73. 10.3389/fcimb.2012.00073 PubMed DOI PMC
Cremer T. J., Ravneberg D. H., Clay C. D., Piper-Hunter M. G., Marsh C. B., Elton T. S., et al. . (2009). MiR-155 induction by F. novicida but not the virulent F. tularensis results in SHIP down-regulation and enhanced pro-inflammatory cytokine response. PLoS ONE 4:e8508. 10.1371/journal.pone.0008508 PubMed DOI PMC
Dai S., Rajaram M. V. S., Curry H. M., Leander R., Schlesinger L. S. (2013). Fine tuning inflammation at the front door: macrophage complement receptor 3-mediates phagocytosis and immune suppression for Francisella tularensis. PLoS Pathog. 9:e1003114. 10.1371/journal.ppat.1003114 PubMed DOI PMC
De Zoete M. R., Palm N. W., Zhu S., Flavell R. A. (2014). Inflammasomes. Cold Spring Harb. Perspect. Biol. 6:a016287. 10.1101/cshperspect.a016287 PubMed DOI PMC
Deguine J., Barton G. M. (2014). MyD88: a central player in innate immune signaling. F1000prime Rep. 6:97. 10.12703/P6-97 PubMed DOI PMC
Dotson R. J., Rabadi S. M., Westcott E. L., Bradley S., Catlett S. V., Banik S., et al. . (2013). Repression of inflammasome by Francisella tularensis during early stages of infection. J. Biol. Chem. 288, 23844–23857. 10.1074/jbc.M113.490086 PubMed DOI PMC
Dowling J. K., Mansell A. (2016). Toll-like receptors: the swiss army knife of immunity and vaccine development. Clin. Transl. Immunol. 5:e85. 10.1038/cti.2016.22 PubMed DOI PMC
Dueñas A. I., Aceves M., Orduña A., Díaz R., Sánchez Crespo M., García-Rodríguez C. (2006). Francisella tularensis LPS induces the production of cytokines in human monocytes and signals via Toll-like receptor 4 with much lower potency than E. coli LPS. Int. Immunol. 18, 785–795. 10.1093/intimm/dxl015 PubMed DOI
Duffy E. B., Periasamy S., Hunt D., Drake J. R., Harton J. A. (2016). FcγR mediates TLR2- and Syk-dependent NLRP3 inflammasome activation by inactivated Francisella tularensis LVS immune complexes. J. Leukoc. Biol. 100, 1335–1347. 10.1189/jlb.2A1215-555RR PubMed DOI PMC
Duncan D. D., Vogler A. J., Wolcott M. J., Li F., Sarovich D. S., Birdsell D. N., et al. . (2013). Identification and typing of Francisella tularensis with a highly automated genotyping assay. Lett. Appl. Microbiol. 56, 128–134. 10.1111/lam.12022 PubMed DOI
Dziarski R., Kashyap D. R., Gupta D. (2012). Mammalian peptidoglycan recognition proteins kill bacteria by activating two-component systems and modulate microbiome and inflammation. Microb. Drug Resist. Larchmt. N. 18, 280–285. 10.1089/mdr.2012.0002 PubMed DOI PMC
Edwards D. C., Sanders L. C., Bokoch G. M., Gill G. N. (1999). Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1, 253–259. 10.1038/12963 PubMed DOI
Edwards M. W., Aultman J. A., Harber G., Bhatt J. M., Sztul E., Xu Q., et al. . (2013). Role of mTOR downstream effector signaling molecules in Francisella tularensis internalization by murine macrophages. PLoS ONE 8:e83226. 10.1371/journal.pone.0083226 PubMed DOI PMC
Fabrik I., Link M., Putzova D., Plzakova L., Lubovska Z., Philimonenko V., et al. . (2018). The early dendritic cell signaling induced by virulent Francisella tularensis strain occurs in phases and involves the activation of extracellular signal-regulated kinases (ERKs) and p38 in the later stage. Mol. Cell. Proteomics MCP 17, 81–94. 10.1074/mcp.RA117.000160 PubMed DOI PMC
Fernandes-Alnemri T., Yu J. W., Datta P., Wu J., Alnemri E. S. (2009). AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458, 509–513. 10.1038/nature07710 PubMed DOI PMC
Fernandes-Alnemri T., Yu J. W., Juliana C., Solorzano L., Kang S., Wu J., et al. . (2010). The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat. Immunol. 11, 385–393. 10.1038/ni.1859 PubMed DOI PMC
Filippi-Chiela E. C., Viegas M. S., Thomé M. P., Buffon A., Wink M. R., Lenz G. (2016). Modulation of autophagy by calcium signalosome in human disease. Mol. Pharmacol. 90, 371–384. 10.1124/mol.116.105171 PubMed DOI
Forestal C. A., Malik M., Catlett S. V., Savitt A. G., Benach J. L., Sellati T. J., et al. . (2007). Francisella tularensis has a significant extracellular phase in infected mice. J. Infect. Dis. 196, 134–137. 10.1086/518611 PubMed DOI
Fortier A. H., Slayter M. V., Ziemba R., Meltzer M. S., Nacy C. A. (1991). Live vaccine strain of Francisella tularensis: infection and immunity in mice. Infect. Immun. 59, 2922–2928. PubMed PMC
Franchi L., Warner N., Viani K., Nuñez G. (2009). Function of Nod-like receptors in microbial recognition and host defense. Immunol. Rev. 227, 106–128. 10.1111/j.1600-065X.2008.00734.x PubMed DOI PMC
Franz K. M., Kagan J. C. (2017). Innate immune receptors as competitive determinants of cell fate. Mol Cell. 66, 750–760. 10.1016/j.molcel.2017.05.009 PubMed DOI PMC
García-García E., Rosales C. (2002). Signal transduction during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 72, 1092–1108. 10.1189/jlb.72.6.1092 PubMed DOI
Gardner B. M., Pincus D., Gotthardt K., Gallagher C. M., Walter P. (2013). Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb. Perspect. Biol. 5:a013169. 10.1101/cshperspect.a013169 PubMed DOI PMC
Gaudet R. G., Bradfield C. J., MacMicking J. D. (2016). Evolution of cell-autonomous effector mechanisms in macrophages versus non-immune Cells. Microbiol. Spectr. 4. 10.1128/microbiolspec.MCHD-0050-2016 PubMed DOI PMC
Gavrilin M. A., Bouakl I. J., Knatz N. L., Duncan M. D., Hall M. W., Gunn J. S., et al. . (2006). Internalization and phagosome escape required for Francisella to induce human monocyte IL-1beta processing and release. Proc. Natl. Acad. Sci. U.S.A. 103, 141–146. 10.1073/pnas.0504271103 PubMed DOI PMC
Gavrilin M. A., Wewers M. D. (2011). Francisella recognition by inflammasomes: differences between mice and men. Front. Microbiol. 2:11. 10.3389/fmicb.2011.00011 PubMed DOI PMC
Gay N. J., Symmons M. F., Gangloff M., Bryant C. E. (2014). Assembly and localization of Toll-like receptor signalling complexes. Nat. Rev. Immunol. 14, 546–558. 10.1038/nri3713 PubMed DOI
Geier H., Celli J. (2011). Phagocytic receptors dictate phagosomal escape and intracellular proliferation of Francisella tularensis. Infect. Immun. 79, 2204–2214. 10.1128/IAI.01382-10 PubMed DOI PMC
Ghosh R., Wang L., Wang E. S., Perera B. G. K., Igbaria A., Morita S., et al. . (2014). Allosteric inhibition of the IRE1α RNase preserves cell viability and function during endoplasmic reticulum stress. Cell 158, 534–548. 10.1016/j.cell.2014.07.002 PubMed DOI PMC
Golovliov I., Baranov V., Krocova Z., Kovarova H., Sjöstedt A. (2003). An attenuated strain of the facultative intracellular bacterium Francisella tularensis can escape the phagosome of monocytic cells. Infect. Immun. 71, 5940–5950. 10.1128/IAI.71.10.5940-5950.2003 PubMed DOI PMC
Gordon S. (2002). Pattern recognition receptors: doubling up for the innate immune response. Cell 111, 927–930. 10.1016/S0092-8674(02)01201-1 PubMed DOI
Granucci F., Foti M., Ricciardi-Castagnoli P. (2005). Dendritic cell biology. Adv. Immunol. 88, 193–233. 10.1016/S0065-2776(05)88006-X PubMed DOI
Green M. F., Anderson K. A., Means A. R. (2011). Characterization of the CaMKKβ-AMPK signaling complex. Cell. Signal. 23, 2005–2012. 10.1016/j.cellsig.2011.07.014 PubMed DOI PMC
Gründler T., Quednau N., Stump C., Orian-Rousseau V., Ishikawa H., Wolburg H., et al. . (2013). The surface proteins InlA and InlB are interdependently required for polar basolateral invasion by Listeria monocytogenes in a human model of the blood-cerebrospinal fluid barrier. Microbes Infect. Inst. Pasteur. 15, 291–301. 10.1016/j.micinf.2012.12.005 PubMed DOI
Gunnell M. K., Robison R. A., Adams B. J. (2016). Natural selection in virulence genes of Francisella tularensis. J Mol Evol. 82, 264–78. 10.1007/s00239-016-9743-y PubMed DOI
Hagar J. A., Powell D. A., Aachoui Y., Ernst R. K., Miao E. A. (2013). Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341, 1250–1253. 10.1126/science.1240988 PubMed DOI PMC
Hajishengallis G., Lambris J. D. (2010). Crosstalk pathways between Toll-like receptors and the complement system. Trends Immunol. 31, 154–163. 10.1016/j.it.2010.01.002 PubMed DOI PMC
Hajishengallis G., Lambris J. D. (2016). More than complementing Tolls: complement-Toll-like receptor synergy and crosstalk in innate immunity and inflammation. Immunol. Rev. 274, 233–244. 10.1111/imr.12467 PubMed DOI PMC
Hajjar A. M., Harvey M. D., Shaffer S. A., Goodlett D. R., Sjöstedt A., Edebro H., et al. . (2006). Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infect. Immun. 74, 6730–6738. 10.1128/IAI.00934-06 PubMed DOI PMC
Harrison R. A., Lachmann P. J. (1980). The physiological breakdown of the third component of human complement. Mol. Immunol. 17, 9–20. 10.1016/0161-5890(80)90119-4 PubMed DOI
Härtlova A., Link M., Balounova J., Benesova M., Resch U., Straskova A., et al. . (2014). Quantitative proteomics analysis of macrophage-derived lipid rafts reveals induction of autophagy pathway at the early time of Francisella tularensis LVS Infection. J. Proteome Res. 13, 796–804. 10.1021/pr4008656 PubMed DOI
He Y., Hara H., Núñez G. (2016). Mechanism and regulation of NLRP3 inflammasome activation. Trends Biochem. Sci. 41, 1012–1021. 10.1016/j.tibs.2016.09.002 PubMed DOI PMC
Henry T., Brotcke A., Weiss D. S., Thompson L. J., Monack D. M. (2007). Type I interferon signaling is required for activation of the inflammasome during Francisella infection. J. Exp. Med. 204, 987–994. 10.1084/jem.20062665 PubMed DOI PMC
Hetz C., Papa F. R. (2018). The unfolded protein response and cell fate control. Mol. Cell 69, 169–181. 10.1016/j.molcel.2017.06.017 PubMed DOI
Hidmark A., von Saint Paul A., Dalpke A. H. (2012). Cutting edge: TLR13 is a receptor for bacterial RNA. J. Immunol. Baltim. 189, 2717–2721. 10.4049/jimmunol.1200898 PubMed DOI
Høyer-Hansen M., Bastholm L., Szyniarowski P., Campanella M., Szabadkai G., Farkas T., et al. . (2007). Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25, 193–205. 10.1016/j.molcel.2006.12.009 PubMed DOI
Hrstka R., Krocova Z., Cerny J., Vojtesek B., Macela A., Stulik J. (2007). Francisella tularensis strain LVS resides in MHC II-positive autophagic vacuoles in macrophages. Folia Microbiol. 52, 631–636. 10.1007/BF02932193 PubMed DOI
Huang M. T.-H., Mortensen B. L., Taxman D. J., Craven R. R., Taft-Benz S., Kijek T. M., et al. (2010). Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis. J. Immunol. Baltim. 1950 185, 5476–5485. 10.4049/jimmunol.1002154 PubMed DOI PMC
Hurley R. L., Anderson K. A., Franzone J. M., Kemp B. E., Means A. R., Witters L. A. (2005). The Ca2+/Calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J. Biol. Chem. 280, 29060–29066. 10.1074/jbc.M503824200 PubMed DOI
Ishikawa H., Barber G. N. (2008). STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455, 674–678. 10.1038/nature07317 PubMed DOI PMC
Ishikawa H., Ma Z., Barber G. N. (2009). STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788–792. 10.1038/nature08476 PubMed DOI PMC
Jacobs A. T., Ignarro L. J. (2001). Lipopolysaccharide-induced expression of interferon-beta mediates the timing of inducible nitric-oxide synthase induction in RAW 264.7 macrophages. J. Biol. Chem. 276, 47950–47957. 10.1074/jbc.M106639200 PubMed DOI
Janeway C. A. (1989). Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54 (Pt 1), 1–13. 10.1101/SQB.1989.054.01.003 PubMed DOI
Janssens S., Pulendran B., Lambrecht B. N. (2014). Emerging functions of the unfolded protein response in immunity. Nat. Immunol. 15, 910–919. 10.1038/ni.2991 PubMed DOI PMC
Jessop F., Schwarz B., Heitmann E., Buntyn R., Wehrly T., Bosio C. M. (2018). Temporal manipulation of mitochondrial function by virulent Francisella tularensis to limit inflammation and control cell death. Infect. Immun. 86:e00044-18. 10.1128/IAI.00044-18 PubMed DOI PMC
Jin L., Hill K. K., Filak H., Mogan J., Knowles H., Zhang B., et al. (2011). MPYS is required for IRF3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers c-di-AMP and c-di-GMP. J. Immunol. Baltim. 187, 2595–2601. 10.4049/jimmunol.1100088 PubMed DOI PMC
Jones J. W., Kayagaki N., Broz P., Henry T., Newton K., O'Rourke K., et al. . (2010). Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. U.S.A. 107, 9771–9776. 10.1073/pnas.1003738107 PubMed DOI PMC
Jones R. G., Pearce E. J. (2017). MenTORing immunity: mTOR signaling in the development and function of tissue-resident immune cells. Immunity 46, 730–742. 10.1016/j.immuni.2017.04.028 PubMed DOI PMC
Jønsson K. L., Laustsen A., Krapp C., Skipper K. A., Thavachelvam K., Hotter D., et al. . (2017). IFI16 is required for DNA sensing in human macrophages by promoting production and function of cGAMP. Nat. Commun. 8:14391. 10.1038/ncomms14391 PubMed DOI PMC
Kagan J. C., Su T., Horng T., Chow A., Akira S., Medzhitov R. (2008). TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat. Immunol. 9:361–368. 10.1038/ni1569 PubMed DOI PMC
Kanneganti T. D., Lamkanfi M., Kim Y. G., Chen G., Park J. H., Franchi L., et al. . (2007). Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 26, 433–443. 10.1016/j.immuni.2007.03.008 PubMed DOI
Katz J., Zhang P., Martin M., Vogel S. N., Michalek S. M. (2006). Toll-like receptor 2 is required for inflammatory responses to Francisella tularensis LVS. Infect. Immun. 74, 2809–2816. 10.1128/IAI.74.5.2809-2816.2006 PubMed DOI PMC
Kaufman R. J., Malhotra J. D. (2014). Calcium trafficking integrates endoplasmic reticulum function with mitochondrial bioenergetics. Biochim. Biophys. Acta 1843, 2233–2239. 10.1016/j.bbamcr.2014.03.022 PubMed DOI PMC
Kawai T., Akira S. (2009). The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 21, 317–337. 10.1093/intimm/dxp017 PubMed DOI PMC
Kerr M. C., Teasdale R. D. (2009). Defining macropinocytosis. Traffic Cph. Den. 10, 364–371. 10.1111/j.1600-0854.2009.00878.x PubMed DOI
Kitchens R. L. (2000). Role of CD14 in cellular recognition of bacterial lipopolysaccharides. Chem. Immunol. 74, 61–82. 10.1159/000058750 PubMed DOI
Kopp E. B., Medzhitov R. (1999). The Toll-receptor family and control of innate immunity. Curr. Opin. Immunol. 11, 13–18. 10.1016/S0952-7915(99)80003-X PubMed DOI
Krocova Z., Härtlova A., Souckova D., Zivna L., Kroca M., Rudolf E., et al. . (2008). Interaction of B cells with intracellular pathogen Francisella tularensis. Microb. Pathog. 45, 79–85. 10.1016/j.micpath.2008.01.010 PubMed DOI
Krocova Z., Macela A., Kubelkova K. (2017). Innate immune recognition: implications for the interaction of Francisella tularensis with the host immune system. Front. Cell. Infect. Microbiol. 7:446. 10.3389/fcimb.2017.00446 PubMed DOI PMC
Kumar H., Kawai T., Akira S. (2009). Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 388, 621–625. 10.1016/j.bbrc.2009.08.062 PubMed DOI
Lai X.-H., Sjöstedt A. (2003). Delineation of the molecular mechanisms of Francisella tularensis-induced apoptosis in murine macrophages. Infect. Immun. 71, 4642–4646. 10.1128/IAI.71.8.4642-4646.2003 PubMed DOI PMC
Lai X. H., Golovliov I., Sjöstedt A. (2001). Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infect. Immun. 69, 4691–4694. 10.1128/IAI.69.7.4691-4694.2001 PubMed DOI PMC
Lamkanfi M., Kanneganti T. D., Franchi L., Núñez G. (2007). Caspase-1 inflammasomes in infection and inflammation. J. Leukoc. Biol. 82, 220–225. 10.1189/jlb.1206756 PubMed DOI
Laplante M., Sabatini D. M. (2009). mTOR signaling at a glance. J. Cell Sci. 122, 3589–3594. 10.1242/jcs.051011 PubMed DOI PMC
Laplante M., Sabatini D. M. (2012). mTOR signaling in growth control and disease. Cell 149, 274–293. 10.1016/j.cell.2012.03.017 PubMed DOI PMC
Laplante M., Sabatini D. M. (2013). Regulation of mTORC1 and its impact on gene expression at a glance. J. Cell Sci. 126, 1713–1719. 10.1242/jcs.125773 PubMed DOI PMC
Larson M. A., Nalbantoglu U., Sayood K., Zentz E. B., Cer R. Z., Iwen P. C., et al. . (2016). Reclassification of Wolbachia persica as Francisella persica comb. nov. and emended description of the family Francisellaceae. Int. J. Syst. Evol. Microbiol. 66, 1200–1205. 10.1099/ijsem.0.000855 PubMed DOI
Larsson P., Oyston P. C. F., Chain P., Chu M. C., Duffield M., Fuxelius H.-H., et al. . (2005). The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat. Genet. 37, 153–159. 10.1038/ng1499 PubMed DOI
Law H. T., Lin A. E. J., Kim Y., Quach B., Nano F. E., Guttman J. A. (2011). Francisella tularensis uses cholesterol and clathrin-based endocytic mechanisms to invade hepatocytes. Sci. Rep. 1:192. 10.1038/srep00192 PubMed DOI PMC
Lee A. S. (2005). The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods San Diego Calif 35, 373–381. 10.1016/j.ymeth.2004.10.010 PubMed DOI
Levine B., Mizushima N., Virgin H. W. (2011). Autophagy in immunity and inflammation. Nature 469, 323–335. 10.1038/nature09782 PubMed DOI PMC
Li H., Nookala S., Bina X. R., Bina J. E., Re F. (2006). Innate immune response to Francisella tularensis is mediated by TLR2 and caspase-1 activation. J. Leukoc. Biol. 80, 766–773. 10.1189/jlb.0406294 PubMed DOI
Li X.-D., Chen Z. J. (2012). Sequence specific detection of bacterial 23S ribosomal RNA by TLR13. eLife 1:e00102. 10.7554/eLife.00102 PubMed DOI PMC
Lindemann S. R., McLendon M. K., Apicella M. A., Jones B. D. (2007). An in vitro model system used to study adherence and invasion of Francisella tularensis live vaccine strain in nonphagocytic cells. Infect. Immun. 75, 3178–3182. 10.1128/IAI.01811-06 PubMed DOI PMC
Lindgren M., Eneslätt K., Bröms J. E., Sjöstedt A. (2013). Importance of PdpC, IglC, IglI, and IglG for modulation of a host cell death pathway induced by Francisella tularensis. Infect. Immun. 81, 2076–2084. 10.1128/IAI.00275-13 PubMed DOI PMC
Linke M., Fritsch S. D., Sukhbaatar N., Hengstschläger M., Weichhart T. (2017). mTORC1 and mTORC2 as regulators of cell metabolism in immunity. FEBS Lett. 591, 3089–3103. 10.1002/1873-3468.12711 PubMed DOI PMC
Liu X., Zhang Z., Ruan J., Pan Y., Magupalli V. G., Wu H., et al. . (2016). Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535, 153–158. 10.1038/nature18629 PubMed DOI PMC
Long M. E., Lindemann S. R., Rasmussen J. A., Jones B. D., Allen L.-A. H. (2013). Disruption of Francisella tularensis Schu S4 iglI, iglJ, and pdpC genes results in attenuation for growth in human macrophages and in vivo virulence in mice and reveals a unique phenotype for pdpC. Infect. Immun. 81, 850–861. 10.1128/IAI.00822-12 PubMed DOI PMC
Ludu J. S., de Bruin O. M., Duplantis B. N., Schmerk C. L., Chou A. Y., Elkins K. L., et al. . (2008). The Francisella pathogenicity island protein PdpD is required for full virulence and associates with homologues of the type VI secretion system. J. Bacteriol. 190, 4584–4595. 10.1128/JB.00198-08 PubMed DOI PMC
Lugrin J., Martinon F. (2018). The AIM2 inflammasome: Sensor of pathogens and cellular perturbations. Immunol Rev. 281, 99–114. 10.1111/imr.12618 PubMed DOI
Luo S., Mao C., Lee B., Lee A. S. (2006). GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol. Cell. Biol. 26, 5688–5697. 10.1128/MCB.00779-06 PubMed DOI PMC
Ma T., Li J., Xu Y., Yu C., Xu T., Wang H., et al. . (2015). Atg5-independent autophagy regulates mitochondrial clearance and is essential for iPSC reprogramming. Nat. Cell Biol. 17, 1379–1387. 10.1038/ncb3256 PubMed DOI
MacMicking J. D. (2012). Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat. Rev. Immunol. 12, 367–382. 10.1038/nri3210 PubMed DOI PMC
Mahawar M., Atianand M. K., Dotson R. J., Mora V., Rabadi S. M., Metzger D. W., et al. . (2012). Identification of a novel Francisella tularensis factor required for intramacrophage survival and subversion of innate immune response. J. Biol. Chem. 287, 25216–25229. 10.1074/jbc.M112.367672 PubMed DOI PMC
Man S. M., Karki R., Malireddi R. K. S., Neale G., Vogel P., Yamamoto M., et al. . (2015). The transcription factor IRF1 and guanylate-binding proteins target activation of the AIM2 inflammasome by Francisella infection. Nat. Immunol. 16, 467–475. 10.1038/ni.3118 PubMed DOI PMC
Man S. M., Karki R., Sasai M., Place D. E., Kesavardhana S., Temirov J., et al. . (2016). IRGB10 liberates bacterial ligands for sensing by the AIM2 and Caspase-11-NLRP3 inflammasomes. Cell 167, 382–396.e17. 10.1016/j.cell.2016.09.012 PubMed DOI PMC
Mariathasan S., Weiss D. S., Dixit V. M., Monack D. M. (2005). Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J. Exp. Med. 202, 1043–1049. 10.1084/jem.20050977 PubMed DOI PMC
Marié I., Durbin J. E., Levy D. E. (1998). Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17, 6660–6669. 10.1093/emboj/17.22.6660 PubMed DOI PMC
Martinon F., Chen X., Lee A. H., Glimcher L. H. (2010). TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11, 411–418. 10.1038/ni.1857 PubMed DOI PMC
McCaffrey R. L., Schwartz J. T., Lindemann S. R., Moreland J. G., Buchan B. W., Jones B. D., et al. . (2010). Multiple mechanisms of NADPH oxidase inhibition by type A and type B Francisella tularensis. J. Leukoc. Biol. 88, 791–805. 10.1189/jlb.1209811 PubMed DOI PMC
McCaig W. D., Koller A., Thanassi D. G. (2013). Production of outer membrane vesicles and outer membrane tubes by Francisella novicida. J. Bacteriol. 195, 1120–1132. 10.1128/JB.02007-12 PubMed DOI PMC
McCracken J. M., Kinkead L. C., McCaffrey R. L., Allen L.-A. H. (2016). Francisella tularensis modulates a distinct subset of regulatory factors and sustains mitochondrial integrity to impair human neutrophil apoptosis. J. Innate Immun. 8, 299–313. 10.1159/000443882 PubMed DOI PMC
Medina E. A., Morris I. R., Berton M. T. (2010). Phosphatidylinositol 3-kinase activation attenuates the TLR2-mediated macrophage proinflammatory cytokine response to Francisella tularensis live vaccine strain. J. Immunol. Baltim. 1950 185, 7562–7572. 10.4049/jimmunol.0903790 PubMed DOI
Medzhitov R. (2009). Approaching the asymptote: 20 years later. Immunity 30, 766–775. 10.1016/j.immuni.2009.06.004 PubMed DOI
Melillo A. A., Bakshi C. S., Melendez J. A. (2010). Francisella tularensis antioxidants harness reactive oxygen species to restrict macrophage signaling and cytokine production. J. Biol. Chem. 285, 27553–27560. 10.1074/jbc.M110.144394 PubMed DOI PMC
Meunier E., Broz P. (2016). Interferon-inducible GTPases in cell autonomous and innate immunity. Cell. Microbiol. 18, 168–180. 10.1111/cmi.12546 PubMed DOI
Meunier E., Wallet P., Dreier R. F., Costanzo S., Anton L., Rühl S., et al. . (2015). Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with Francisella novicida. Nat. Immunol. 16, 476–484. 10.1038/ni.3119 PubMed DOI PMC
Modlin R. L., Brightbill H. D., Godowski P. J. (1999). The toll of innate immunity on microbial pathogens. N. Engl. J. Med. 340, 1834–1835. 10.1056/NEJM199906103402312 PubMed DOI
Mohapatra N. P., Soni S., Rajaram M. V. S., Dang P. M. C., Reilly T. J., El-Benna J., et al. . (2010). Francisella acid phosphatases inactivate the NADPH oxidase in human phagocytes. J. Immunol. Baltim. 184, 5141–5150. 10.4049/jimmunol.0903413 PubMed DOI PMC
Möller G. (1999). Receptors for innate pathogen defence in insects are normal activation receptors for specific immune responses in mammals. Scand. J. Immunol. 50, 341–347. 10.1046/j.1365-3083.1999.00605.x PubMed DOI
Moretti J., Blander J. M. (2014). Insights into phagocytosis-coupled activation of pattern recognition receptors and inflammasomes. Curr. Opin. Immunol. 26, 100–110. 10.1016/j.coi.2013.11.003 PubMed DOI PMC
Moretti J., Blander J. M. (2017). Cell-autonomous stress responses in innate immunity. J. Leukoc. Biol. 101, 77–86. 10.1189/jlb.2MR0416-201R PubMed DOI PMC
Moretti J., Blander J. M. (2018). Detection of a vita-PAMP STINGs cells into reticulophagy. Autophagy 14, 1102–1104. 10.1080/15548627.2018.1441471 PubMed DOI PMC
Moretti J., Roy S., Bozec D., Martinez J., Chapman J. R., Ueberheide B., et al. . (2017). STING senses microbial viability to orchestrate stress-mediated autophagy of the endoplasmic reticulum. Cell 171, 809–823.e13. 10.1016/j.cell.2017.09.034 PubMed DOI PMC
Moriyama K., Lida K., Yahara I. (1996). Phosphorylation of Ser-3 of cofilin regulates its essential function on actin. Genes Cells 1, 73–86. 10.1046/j.1365-2443.1996.05005.x PubMed DOI
Mourao-Sa D., Roy S., Blander J. M. (2013). Vita-PAMPs: signatures of microbial viability. Adv. Exp. Med. Biol. 785, 1–8. 10.1007/978-1-4614-6217-0_1 PubMed DOI
Muñoz-Wolf N., Lavelle E. C. (2016). Innate immune receptors. Methods Mol. Biol. 1417, 1–43. 10.1007/978-1-4939-3566-6_1 PubMed DOI
Muzio M., Mantovani A. (2000). Toll-like receptors. Microbes Infect. 2, 251–255. 10.1016/S1286-4579(00)00303-8 PubMed DOI
Nakahira K., Haspel J. A., Rathinam V. A. K., Lee S. J., Dolinay T., Lam H. C., et al. . (2011). Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12, 222–230. 10.1038/ni.1980 PubMed DOI PMC
Nano F. E., Zhang N., Cowley S. C., Klose K. E., Cheung K. K. M., Roberts M. J., et al. . (2004). A Francisella tularensis pathogenicity island required for intramacrophage growth. J. Bacteriol. 186, 6430–6436. 10.1128/JB.186.19.6430-6436.2004 PubMed DOI PMC
Okan N. A., Kasper D. L. (2013). The atypical lipopolysaccharide of Francisella. Carbohydr. Res. 378, 79–83. 10.1016/j.carres.2013.06.015 PubMed DOI PMC
Oldenburg M., Krüger A., Ferstl R., Kaufmann A., Nees G., Sigmund A., et al. . (2012). TLR13 recognizes bacterial 23S rRNA devoid of erythromycin resistance-forming modification. Science 337, 1111–1115. 10.1126/science.1220363 PubMed DOI
Pandey S., Kawai T., Akira S. (2014). Microbial sensing by Toll-like receptors and intracellular nucleic acid sensors. Cold Spring Harb. Perspect. Biol. 7:a016246. 10.1101/cshperspect.a016246 PubMed DOI PMC
Park J. H., Ko R., Lee S. Y. (2017). Reciprocal regulation of TLR2-mediated IFN-β production by SHP2 and Gsk3β. Sci. Rep. 7:6807. 10.1038/s41598-017-07316-3 PubMed DOI PMC
Parsa K. V. L., Butchar J. P., Rajaram M. V. S., Cremer T. J., Tridandapani S. (2008). The tyrosine kinase Syk promotes phagocytosis of Francisella through the activation of Erk. Mol. Immunol. 45, 3012–3021. 10.1016/j.molimm.2008.01.011 PubMed DOI PMC
Parsa K. V. L., Ganesan L. P., Rajaram M. V. S., Gavrilin M. A., Balagopal A., Mohapatra N. P., et al. . (2006). Macrophage pro-inflammatory response to Francisella novicida infection is regulated by SHIP. PLoS Pathog. 2:e71. 10.1371/journal.ppat.0020071 PubMed DOI PMC
Phillips N. J., Schilling B., McLendon M. K., Apicella M. A., Gibson B. W. (2004). Novel modification of lipid A of Francisella tularensis. Infect. Immun. 72, 5340–5348. 10.1128/IAI.72.9.5340-5348.2004 PubMed DOI PMC
Pierini L. M. (2006). Uptake of serum-opsonized Francisella tularensis by macrophages can be mediated by class A scavenger receptors. Cell. Microbiol. 8, 1361–1370. 10.1111/j.1462-5822.2006.00719.x PubMed DOI
Pillich H., Loose M., Zimmer K. P., Chakraborty T. (2016). Diverse roles of endoplasmic reticulum stress sensors in bacterial infection. Mol. Cell. Pediatr. 3:9. 10.1186/s40348-016-0037-7 PubMed DOI PMC
Plzakova L., Krocova Z., Kubelkova K., Macela A. (2015). Entry of Francisella tularensis into murine B cells: the role of B cell receptors and complement receptors. PLoS ONE 10:e0132571. 10.1371/journal.pone.0132571 PubMed DOI PMC
Proctor R. A., White J. D., Ayala E., Canonico P. G. (1975). Phagocytosis of Francisella tularensis by Rhesus monkey peripheral leukocytes. Infect. Immun. 11, 146–151. PubMed PMC
Prunier C., Prudent R., Kapur R., Sadoul K., Lafanechère L. (2017). LIM kinases: cofilin and beyond. Oncotarget 8, 41749–41763. 10.18632/oncotarget.16978 PubMed DOI PMC
Putzova D., Panda S., Härtlova A., Stulík J., Gekara N. O. (2017). Subversion of innate immune responses by Francisella involves the disruption of TRAF3 and TRAF6 signalling complexes. Cell. Microbiol. 19 10.1111/cmi.12769 PubMed DOI
Rajaram M. V., Ganesan L. P., Parsa K. V., Butchar J. P., Gunn J. S., Tridandapani S. (2006). Akt/protein kinase B modulates macrophage inflammatory response to Francisella infection and confers a survival advantage in mice. J. Immunol. 177, 6317–6324. 10.4049/jimmunol.177.9.6317 PubMed DOI
Rajaram M. V. S., Butchar J. P., Parsa K. V. L., Cremer T. J., Amer A., Schlesinger L. S., et al. . (2009). Akt and SHIP modulate Francisella escape from the phagosome and induction of the Fas-mediated death pathway. PLoS ONE 4:e7919. 10.1371/journal.pone.0007919 PubMed DOI PMC
Ramond E., Gesbert G., Guerrera I. C., Chhuon C., Dupuis M., Rigard M., et al. . (2015). Importance of host cell arginine uptake in Francisella phagosomal escape and ribosomal protein amounts. Mol. Cell. Proteomics MCP 14, 870–881. 10.1074/mcp.M114.044552 PubMed DOI PMC
Randow F., MacMicking J. D., James L. C. (2013). Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 340, 701–706. 10.1126/science.1233028 PubMed DOI PMC
Rathinam V. A. K., Jiang Z., Waggoner S. N., Sharma S., Cole L. E., Waggoner L., et al. . (2010). The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11, 395–402. 10.1038/ni.1864 PubMed DOI PMC
Riedl S. J., Salvesen G. S. (2007). The apoptosome: signalling platform of cell death. Nat. Rev. Mol. Cell Biol. 8, 405–413. 10.1038/nrm2153 PubMed DOI
Robert C. B., Thomson M., Vercellone A., Gardner F., Ernst R. K., Larrouy-Maumus G., et al. . (2017). Mass spectrometry analysis of intact Francisella bacteria identifies lipid A structure remodeling in response to acidic pH stress. Biochimie 141, 16–20. 10.1016/j.biochi.2017.08.008 PubMed DOI
Roberts L. M., Ledvina H. E., Sempowski G. D., Frelinger J. A. (2014). TLR2 signaling is required for the innate, but not adaptive response to LVS clpB. Front. Immunol. 5:426 10.3389/fimmu.2014.00426 PubMed DOI PMC
Rodionova I. V. (1976). [Catalase activity in the agent of tularemia]. Zh. Mikrobiol. Epidemiol. Immunobiol 60–63. PubMed
Rodriguez A. R., Yu J. J., Navara C., Chambers J. P., Guentzel M. N., Arulanandam B. P. (2016). Contribution of FcεRI-associated vesicles to mast cell-macrophage communication following Francisella tularensis infection. Innate Immun. 22, 567–574. 10.1177/1753425916663639 PubMed DOI
Rosadini C. V., Kagan J. C. (2017). Early innate immune responses to bacterial LPS. Curr. Opin. Immunol. 44, 14–19. 10.1016/j.coi.2016.10.005 PubMed DOI PMC
Roy C. R., Salcedo S. P., Gorvel J. P. E. (2006). Pathogen-endoplasmic-reticulum interactions: in through the out door. Nat. Rev. Immunol. 6, 136–147. 10.1038/nri1775 PubMed DOI PMC
Royet J., Gupta D., Dziarski R. (2011). Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nat. Rev. Immunol. 11, 837–851. 10.1038/nri3089 PubMed DOI
Russo B. C., Brown M. J., Nau G. J. (2013). MyD88-dependent signaling prolongs survival and reduces bacterial burden during pulmonary infection with virulent Francisella tularensis. Am. J. Pathol. 183, 1223–1232. 10.1016/j.ajpath.2013.06.013 PubMed DOI PMC
Saleiro D., Platanias L. C. (2015). Intersection of mTOR and STAT signaling in immunity. Trends Immunol. 36, 21–29. 10.1016/j.it.2014.10.006 PubMed DOI PMC
Sander L. E., Davis M. J., Boekschoten M. V., Amsen D., Dascher C. C., Ryffel B., et al. . (2011). Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474, 385–389. 10.1038/nature10072 PubMed DOI PMC
Santic M., Abu Kwaik Y. (2013). Nutritional virulence of Francisella tularensis. Front. Cell. Infect. Microbiol. 3:112. 10.3389/fcimb.2013.00112 PubMed DOI PMC
Santic M., Akimana C., Asare R., Kouokam J. C., Atay S., Kwaik Y. A. (2009). Intracellular fate of Francisella tularensis within arthropod-derived cells. Environ. Microbiol. 11, 1473–1481. 10.1111/j.1462-2920.2009.01875.x PubMed DOI
Santic M., Molmeret M., Klose K. E., Abu Kwaik Y. (2006). Francisella tularensis travels a novel, twisted road within macrophages. Trends Microbiol. 14, 37–44. 10.1016/j.tim.2005.11.008 PubMed DOI
Sato M., Hata N., Asagiri M., Nakaya T., Taniguchi T., Tanaka N. (1998a). Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 441, 106–110. 10.1016/S0014-5793(98)01514-2 PubMed DOI
Sato M., Tanaka N., Hata N., Oda E., Taniguchi T. (1998b). Involvement of the IRF family transcription factor IRF-3 in virus-induced activation of the IFN-beta gene. FEBS Lett. 425, 112–116. 10.1016/S0014-5793(98)00210-5 PubMed DOI
Schilling B., McLendon M. K., Phillips N. J., Apicella M. A., Gibson B. W. (2007). Characterization of lipid A acylation patterns in Francisella tularensis, Francisella novicida, and Francisella philomiragia using multiple-stage mass spectrometry and matrix-assisted laser desorption/ionization on an intermediate vacuum source linear ion trap. Anal. Chem. 79, 1034–1042. 10.1021/ac061654e PubMed DOI PMC
Schulert G. S., Allen L. A. H. (2006). Differential infection of mononuclear phagocytes by Francisella tularensis: role of the macrophage mannose receptor. J. Leukoc. Biol. 80, 563–571. 10.1189/jlb.0306219 PubMed DOI PMC
Schwartz J. T., Barker J. H., Long M. E., Kaufman J., McCracken J., Allen L. A. H. (2012). Natural IgM mediates complement-dependent uptake of Francisella tularensis by human neutrophils via CR1 and CR3 in nonimmune serum. J. Immunol. Baltim. 189, 3064–3077. 10.4049/jimmunol.1200816 PubMed DOI PMC
Sjöstedt A., Tärnvik A., Sandström G. (1996). Francisella tularensis: host-parasite interaction. FEMS Immunol. Med. Microbiol. 13, 181–184. 10.1111/j.1574-695X.1996.tb00233.x PubMed DOI
Skyberg J. A., Lacey C. A. (2017). Hematopoietic MyD88 and IL-18 are essential for IFN-γ-dependent restriction of type A Francisella tularensis infection. J. Leukoc. Biol. 102, 1441–1450. 10.1189/jlb.4A0517-179R PubMed DOI PMC
Spidlova P., Stulik J. (2017). Francisella tularensis type VI secretion system comes of age. Virulence 8, 628–631. 10.1080/21505594.2016.1278336 PubMed DOI PMC
Stack J., Doyle S. L., Connolly D. J., Reinert L. S., O'Keeffe K. M., McLoughlin R. M., et al. . (2014). TRAM is required for TLR2 endosomal signaling to type I IFN induction. J. Immunol. Baltim. 193, 6090–6102. 10.4049/jimmunol.1401605 PubMed DOI PMC
Steele S., Brunton J., Ziehr B., Taft-Benz S., Moorman N., Kawula T. (2013). Francisella tularensis harvests nutrients derived via ATG5-independent autophagy to support intracellular growth. PLoS Pathog. 9:e1003562. 10.1371/journal.ppat.1003562 PubMed DOI PMC
Steele S., Radlinski L., Taft-Benz S., Brunton J., Kawula T. H. (2016). Trogocytosis-associated cell to cell spread of intracellular bacterial pathogens. eLife 5:e10625. 10.7554/eLife.10625 PubMed DOI PMC
Stevenson T. C., Cywes-Bentley C., Moeller T. D., Weyant K. B., Putnam D., Chang Y.-F., et al. . (2018). Immunization with outer membrane vesicles displaying conserved surface polysaccharide antigen elicits broadly antimicrobial antibodies. Proc. Natl. Acad. Sci. U.S.A. 115, E3106–E3115. 10.1073/pnas.1718341115 PubMed DOI PMC
Storek K. M., Gertsvolf N. A., Ohlson M. B., Monack D. M. (2015). cGAS and Ifi204 cooperate to produce type I IFNs in response to Francisella infection. J. Immunol. Baltim. 194, 3236–3245. 10.4049/jimmunol.1402764 PubMed DOI PMC
Swanson J. A., Hoppe A. D. (2004). The coordination of signaling during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 76, 1093–1103. 10.1189/jlb.0804439 PubMed DOI
Tamilselvam B., Daefler S. (2008). Francisella targets cholesterol-rich host cell membrane domains for entry into macrophages. J. Immunol. 180, 8262–8271. 10.4049/jimmunol.180.12.8262 PubMed DOI
Tao J., Zhou X., Jiang Z. (2016). cGAS-cGAMP-STING: The three musketeers of cytosolic DNA sensing and signaling. IUBMB Life 68, 858–870. 10.1002/iub.1566 PubMed DOI
Tapping R. I., Tobias P. S. (2000). Soluble CD14-mediated cellular responses to lipopolysaccharide. Chem. Immunol. 74, 108–121. 10.1159/000058751 PubMed DOI
Tärnvik A., Berglund L. (2003). Tularaemia. Eur. Respir. J. 21, 361–373. 10.1183/09031936.03.00088903 PubMed DOI
Telepnev M., Golovliov I., Sjöstedt A. (2005). Francisella tularensis LVS initially activates but subsequently down-regulates intracellular signaling and cytokine secretion in mouse monocytic and human peripheral blood mononuclear cells. Microb. Pathog. 38, 239–247. 10.1016/j.micpath.2005.02.003 PubMed DOI
Tjelle T. E., Lovdal T., Berg T. (2000). Phagosome dynamics and function. BioEssays News Rev. Mol. Cell. Dev. Biol. 22, 255–263. 10.1002/(SICI)1521-1878(200003)22:3<255::AID-BIES7>3.0.CO;2-R PubMed DOI
Triantafilou M., Gamper F. G. J., Haston R. M., Mouratis M. A., Morath S., Hartung T., et al. . (2006). Membrane sorting of toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281, 31002–31011. 10.1074/jbc.M602794200 PubMed DOI
Triantafilou M., Miyake K., Golenbock D. T., Triantafilou K. (2002). Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 115, 2603–2611. PubMed
Vanaja S. K., Rathinam V. A. K., Fitzgerald K. A. (2015). Mechanisms of inflammasome activation: recent advances and novel insights. Trends Cell Biol. 25, 308–315. 10.1016/j.tcb.2014.12.009 PubMed DOI PMC
Walsh M. C., Lee J., Choi Y. (2015). Tumor necrosis factor receptor- associated factor 6 (TRAF6) regulation of development, function, and homeostasis of the immune system. Immunol. Rev. 266, 72–92. 10.1111/imr.12302 PubMed DOI PMC
Walter P., Ron D. (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081–1086. 10.1126/science.1209038 PubMed DOI
Wehrly T. D., Chong A., Virtaneva K., Sturdevant D. E., Child R., Edwards J. A., et al. . (2009). Intracellular biology and virulence determinants of Francisella tularensis revealed by transcriptional profiling inside macrophages. Cell. Microbiol. 11, 1128–1150. 10.1111/j.1462-5822.2009.01316.x PubMed DOI PMC
Weichhart T., Hengstschläger M., Linke M. (2015). Regulation of innate immune cell function by mTOR. Nat. Rev. Immunol. 15, 599–614. 10.1038/nri3901 PubMed DOI PMC
Wickstrum J. R., Bokhari S. M., Fischer J. L., Pinson D. M., Yeh H.-W., Horvat R. T., et al. . (2009). Francisella tularensis induces extensive caspase-3 activation and apoptotic cell death in the tissues of infected mice. Infect. Immun. 77, 4827–4836. 10.1128/IAI.00246-09 PubMed DOI PMC
Xia P., Wang S., Gao P., Gao G., Fan Z. (2016). DNA sensor cGAS-mediated immune recognition. Protein Cell 7, 777–791. 10.1007/s13238-016-0320-3 PubMed DOI PMC
Yu J.-J., Raulie E. K., Murthy A. K., Guentzel M. N., Klose K. E., Arulanandam B. P. (2008). The presence of infectious extracellular Francisella tularensis subsp. novicida in murine plasma after pulmonary challenge. Eur. J. Clin. Microbiol. Infect. Dis. 27, 323–325. 10.1007/s10096-007-0434-x PubMed DOI
Zanoni I., Ostuni R., Marek L. R., Barresi S., Barbalat R., Barton G. M., et al. . (2011). CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147, 868–880. 10.1016/j.cell.2011.09.051 PubMed DOI PMC
Zhang J., Randall M. S., Loyd M. R., Dorsey F. C., Kundu M., Cleveland J. L., et al. . (2009). Mitochondrial clearance is regulated by Atg7-dependent and -independent mechanisms during reticulocyte maturation. Blood 114, 157–164. 10.1182/blood-2008-04-151639 PubMed DOI PMC
Zhang Z., Long Q., Xie J. (2012). Roles of peptidoglycan recognition protein (PGRP) in immunity and implications for novel anti-infective measures. Crit. Rev. Eukaryot. Gene Expr. 22, 259–268. 10.1615/CritRevEukarGeneExpr.v22.i3.90 PubMed DOI
Zhao G.-N., Jiang D. S., Li H. (2015). Interferon regulatory factors: at the crossroads of immunity, metabolism, and disease. Biochim. Biophys. Acta 1852, 365–378. 10.1016/j.bbadis.2014.04.030 PubMed DOI
Zhao H., Gonzalezgugel E., Cheng L., Richbourgh B., Nie L., Liu C. (2015). The roles of interferon-inducible p200 family members IFI16 and p204 in innate immune responses, cell differentiation and proliferation. Genes Dis. 2, 46–56. 10.1016/j.gendis.2014.10.003 PubMed DOI PMC
Zhou R., Yazdi A. S., Menu P., Tschopp J. (2011). A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221–225. 10.1038/nature09663 PubMed DOI
Zogaj X., Wyatt G. C., Klose K. E. (2012). Cyclic di-GMP stimulates biofilm formation and inhibits virulence of Francisella novicida. Infect. Immun. 80, 4239–4247. 10.1128/IAI.00702-12 PubMed DOI PMC
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