Macrophages target Listeria monocytogenes by two discrete non-canonical autophagy pathways

References

• Galluzzi L, Baehrecke EH, Ballabio A, et al. Molecular definitions of autophagy and related processes. EMBO J. 2017;36(13):1811–1836.
   PubMed Web of Science ®Google Scholar
• Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013 Oct;13(10):722–737.
   PubMed Web of Science ®Google Scholar
• Dupont N, Nascimbeni AC, Morel E, et al. Molecular mechanisms of noncanonical autophagy. Int Rev Cell Mol Biol. 2017;328:1–23.
   PubMed Web of Science ®Google Scholar
• Herb M, Gluschko A, Schramm M. LC3-associated phagocytosis - The highway to hell for phagocytosed microbes. Semin Cell Dev Biol. 2020 May;101:68–76.
   PubMed Web of Science ®Google Scholar
• Cemma M, Grinstein S, Brumell JH. Autophagy proteins are not universally required for phagosome maturation. Autophagy. 2016 Sep;12(9):1440–1446.
   PubMed Web of Science ®Google Scholar
• Ray K, Marteyn B, Sansonetti PJ, et al. Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat Rev Microbiol. 2009 May;7(5):333–340.
   PubMed Web of Science ®Google Scholar
• Tattoli I, Sorbara MT, Yang C, et al. Listeria phospholipases subvert host autophagic defenses by stalling pre-autophagosomal structures. EMBO J. 2013 Nov 27;32(23):3066–3078.
   PubMed Web of Science ®Google Scholar
• Yoshikawa Y, Ogawa M, Hain T, et al. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol. 2009 Oct;11(10):1233–1240.
   PubMed Web of Science ®Google Scholar
• Mitchell G, Ge L, Huang Q, et al. Avoidance of autophagy mediated by PlcA or ActA is required for Listeria monocytogenes growth in macrophages. Infect Immun. 2015 May;83(5):2175–2184.
   PubMed Web of Science ®Google Scholar
• Gluschko A, Herb M, Wiegmann K, et al. The beta2 Integrin Mac-1 induces protective LC3-Associated phagocytosis of Listeria monocytogenes. Cell Host Microbe. 2018 Mar 14;23(3):324–337 e5.
   PubMed Web of Science ®Google Scholar
• Herb M, Gluschko A, Schramm M. LC3-associated phagocytosis initiated by integrin ITGAM-ITGB2/Mac-1 enhances immunity to Listeria monocytogenes. Autophagy. 2018;14(8):1462–1464.
   PubMed Web of Science ®Google Scholar
• Meyer-Morse N, Robbins JR, Rae CS, et al. Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection. PLoS One. 2010 Jan 6;5(1):e8610.
   PubMed Web of Science ®Google Scholar
• Mitchell G, Cheng MI, Chen C, et al. Listeria monocytogenes triggers noncanonical autophagy upon phagocytosis, but avoids subsequent growth-restricting xenophagy. Proc Natl Acad Sci U S A. 2018 Jan 9;115(2):E210–E217.
   PubMed Web of Science ®Google Scholar
• Huang J, Canadien V, Lam GY, et al. Activation of antibacterial autophagy by NADPH oxidases. Proc Natl Acad Sci U S A. 2009 Apr 14;106(15):6226–6231.
   PubMed Web of Science ®Google Scholar
• Martinez J, Malireddi RK, Lu Q, et al. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat Cell Biol. 2015 Jul;17(7):893–906.
   PubMed Web of Science ®Google Scholar
• Osborne SE, Brumell JH, Listeriolysin O. from bazooka to Swiss army knife. Philos Trans R Soc London Ser B. 2017 Aug 5;372:1726.
   Web of Science ®Google Scholar
• Flannagan RS, Heit B, Heinrichs DE. Antimicrobial mechanisms of macrophages and the immune evasion strategies of Staphylococcus aureus. Pathogens. 2015 Nov 27;4(4):826–868.
   PubMed Web of Science ®Google Scholar
• Lee AS, de Lencastre H, Garau J, et al. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Primers. 2018 May 31;4(1):18033.
   PubMed Web of Science ®Google Scholar
• Birmingham CL, Smith AC, Bakowski MA, et al. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem. 2006 Apr 21;281(16):11374–11383.
   PubMed Web of Science ®Google Scholar
• Dupont N, Lacas-Gervais S, Bertout J, et al. Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe. 2009 [ 2009 Aug 20];6(2):137–149.
   PubMed Web of Science ®Google Scholar
• Gogoi M, Shreenivas MM, Chakravortty D. Hoodwinking the Big-Eater to Prosper: the Salmonella-macrophage paradigm. J Innate Immun. 2019;11(3):289–299.
   PubMed Web of Science ®Google Scholar
• Owen KA, Meyer CB, Bouton AH, et al. Activation of focal adhesion kinase by Salmonella suppresses autophagy via an Akt/mTOR signaling pathway and promotes bacterial survival in macrophages. PLoS Pathog. 2014;10(6):e1004159.
   PubMed Web of Science ®Google Scholar
• Ganesan R, Hos NJ, Gutierrez S, et al. Salmonella Typhimurium disrupts Sirt1/AMPK checkpoint control of mTOR to impair autophagy. PLoS Pathog. 2017;13(2):e1006227.
   PubMed Web of Science ®Google Scholar
• Hos NJ, Fischer J, Hos D, et al. TRIM21 is targeted for Chaperone-Mediated Autophagy during Salmonella typhimurium infection. J Immunol. 2020;205(9):2456–2467.
   PubMed Web of Science ®Google Scholar
• Ashida H, Kim M, Sasakawa C. Manipulation of the host cell death pathway by Shigella. Cell Microbiol. 2014;16(12):1757–1766.
   PubMed Web of Science ®Google Scholar
• Meunier E, Broz P. Quantification of cytosolic vs. vacuolar Salmonella in primary macrophages by differential permeabilization. J Vis Exp. 2015 Jul;28(101):e52960.
   Google Scholar
• Herb M, Schramm M. Functions of ROS in macrophages and antimicrobial immunity. Antioxidants (Basel). 2021 Feb 19;10(2).
   PubMedGoogle Scholar
• Pamer EG. Immune responses to Listeria monocytogenes. Nat Rev Immunol. 2004 Oct;4(10):812–823.
   PubMed Web of Science ®Google Scholar
• Kusnadi A, Park SH, Yuan R, et al. The cytokine TNF promotes transcription factor SREBP activity and binding to inflammatory genes to activate macrophages and limit tissue repair. Immunity. 2019 Aug 20;51(2):241–257 e9.
   PubMed Web of Science ®Google Scholar
• Zhou QD, Chi X, Lee MS, et al. Interferon-mediated reprogramming of membrane cholesterol to evade bacterial toxins. Nat Immunol. 2020 Jul;21(7):746–755.
   PubMed Web of Science ®Google Scholar
• Price JV, Russo D, Ji DX, et al. IRG1 and inducible nitric oxide synthase act redundantly with other interferon-gamma-induced factors to restrict intracellular replication of Legionella pneumophila. mBio. 2019 Nov 12;10(6). DOI:https://doi.org/10.1128/mBio.02629-19.
   Web of Science ®Google Scholar
• Thurston TL, Wandel MP, von Muhlinen N, et al. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature. 2012 Jan 15;482(7385):414–418.
   PubMed Web of Science ®Google Scholar
• Ravenhill BJ, Boyle KB, von Muhlinen N, et al. The Cargo Receptor NDP52 initiates selective autophagy by recruiting the ULK complex to cytosol-invading bacteria. Mol Cell. 2019 Apr 18;74(2):320–329 e6.
   PubMed Web of Science ®Google Scholar
• Chauhan S, Kumar S, Jain A, et al. TRIMs and galectins globally cooperate and TRIM16 and Galectin-3 co-direct autophagy in endomembrane damage homeostasis. Dev Cell. 2016 [ 2016 Oct];39(1):13–27.
   PubMed Web of Science ®Google Scholar
• Hong M-H, Weng IC, Li F-Y, et al. Intracellular galectins sense cytosolically exposed glycans as danger and mediate cellular responses. J Biomed Sci. 2021 [ 2021 Mar 4];28(1):16.
   PubMed Web of Science ®Google Scholar
• Kreibich S, Emmenlauer M, Fredlund J, et al. Autophagy proteins promote repair of endosomal membranes damaged by the Salmonella Type Three Secretion System 1. Cell Host Microbe. 2015 Nov 11;18(5):527–537.
   PubMed Web of Science ®Google Scholar
• Weng I-C, Chen H-L, Lo T-H, et al. Cytosolic galectin-3 and −8 regulate antibacterial autophagy through differential recognition of host glycans on damaged phagosomes. Glycobiology. 2018;28(6):392–405.
   PubMed Web of Science ®Google Scholar
• Birmingham CL, Canadien V, Kaniuk NA, et al. Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature. 2008 Jan 17;451(7176):350–354.
   PubMed Web of Science ®Google Scholar
• Johansen T, Lamark T. Selective autophagy: ATG8 family proteins, LIR motifs and cargo receptors.J Mol Biol. 2020 [ 2020 Jan 3];432(1):80–103.
   PubMed Web of Science ®Google Scholar
• Florey O, Gammoh N, Kim SE, et al. V-ATPase and osmotic imbalances activate endolysosomal LC3 lipidation. Autophagy. 2015;11(1):88–99.
   PubMed Web of Science ®Google Scholar
• Heckmann BL, Teubner BJW, Tummers B, et al. LC3-Associated endocytosis facilitates β-Amyloid clearance and mitigates neurodegeneration in Murine Alzheimer’s disease. Cell. 2019 Jul 25;178(3):536–551. e14.
   PubMed Web of Science ®Google Scholar
• Sanjuan MA, Dillon CP, Tait SW, et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature. 2007 Dec 20;450(7173):1253–1257.
   PubMed Web of Science ®Google Scholar
• Lam GY, Cemma M, Muise AM, et al. Host and bacterial factors that regulate LC3 recruitment to Listeria monocytogenes during the early stages of macrophage infection. Autophagy. 2013 Jul;9(7):985–995.
   PubMed Web of Science ®Google Scholar
• Orecchioni M, Ghosheh Y, Pramod AB, et al. Macrophage polarization: different gene signatures in M1(LPS+) vs. Classically and M2(LPS-) vs. Alternatively activated macrophages [Review]. Front Immunol. 2019 [ 2019 May 24];10(1084):1084.
   PubMed Web of Science ®Google Scholar
• Herb M, Farid A, Gluschko A, et al. Highly efficient transfection of primary macrophages with in vitro transcribed mRNA. J Vis Exp. 2019 Nov;9(153):e60143.
   Google Scholar
• Schramm M, Herz J, Haas A, et al. Acid sphingomyelinase is required for efficient phago-lysosomal fusion. Cell Microbiol. 2008 Sep;10(9):1839–1853.
   PubMed Web of Science ®Google Scholar