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Brief Report - Basic Science

Targeted interplay between bacterial pathogens and host autophagy

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Pages 1620-1633 | Received 15 May 2017, Accepted 01 Mar 2019, Published online: 25 Mar 2019

References

  • Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature. 2011 Jan;469:323–335.
  • Randow F, Youle RJ. Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe. 2014 Apr;15:403–411.
  • Gomes LC, Dikic I. Autophagy in antimicrobial immunity. Mol Cell. 2014 Apr;54:224–233.
  • Mostowy S, Cossart P. Bacterial autophagy: restriction or promotion of bacterial replication? Trends Cell Biol. 2012 Jun;22:283–291.
  • Virgin HW, Levine B. Autophagy genes in immunity. Nat Immunol. 2009 May;10:461–470.
  • Heath RJ, Goel G, Baxt LA, et al. RNF166 determines recruitment of adaptor proteins during antibacterial autophagy. Cell Rep. 2016 Nov;17:2183–2194.
  • Tumbarello DA, Manna PT, Allen M, et al. The autophagy receptor TAX1BP1 and the molecular motor myosin VI are required for clearance of salmonella typhimurium by autophagy. PLoS Pathog. 2015 Oct;11:e1005174.
  • Verlhac P, Grégoire IP, Azocar O, et al. Autophagy receptor NDP52 regulates pathogen-containing autophagosome maturation. Cell Host Microbe. 2015 Apr;17:515–525.
  • Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000 Nov;19:5720–5728.
  • Birgisdottir ÅB, Lamark T, Johansen T. The LIR motif - crucial for selective autophagy. J Cell Sci. 2013 Aug;126:3237–3247.
  • Khaminets A, Behl C, Dikic I. Ubiquitin-dependent and independent signals in selective autophagy. Trends Cell Biol. 2016 Jan;26:6–16.
  • von Muhlinen N, Akutsu M, Ravenhill BJ, et al. LC3C, bound selectively by a noncanonical LIR motif in NDP52, is required for antibacterial autophagy. Mol Cell. 2012 Nov;48:329–342.
  • Wild P, Farhan H, McEwan DG, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science. 2011 Jul;333:228–233.
  • Pankiv S, Clausen TH, Lamark T, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007 Aug;282:24131–24145.
  • 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;9:985–995.
  • Mandell MA, Jain A, Arko-Mensah J, et al. TRIM proteins regulate autophagy and can target autophagic substrates by direct recognition. Dev Cell. 2014 Aug;30:394–409.
  • Veljanovski V, Batoko H. Selective autophagy of non-ubiquitylated targets in plants: looking for cognate receptor/adaptor proteins. Front Plant Sci. 2014 Jun;5:308.
  • Kim B-W, Kwon DH, Song HK. Structure biology of selective autophagy receptors. BMB Rep. 2016;49:73–80.
  • Kwon DH, Song HK A structural view of xenophagy, a battle between host and microbes. Mol. Cells. 2018 Jan;41:27–34.
  • von Muhlinen N, Thurston T, Ryzhakov G, et al. NDP52, a novel autophagy receptor for ubiquitin-decorated cytosolic bacteria. Autophagy. 2010 Feb;6:288–289.
  • Schille S, Crauwels P, Bohn R, et al. LC3-associated phagocytosis in microbial pathogenesis. Int J Med Microbiol. 2017 Nov. pii: S1438-4221(17)30283-7.
  • Huang J, Brumell JH. Bacteria-autophagy interplay: a battle for survival. Nat Rev Microbiol. 2014 Feb;12:101–114.
  • Choy A, Roy CR. Autophagy and bacterial infection: an evolving arms race. Trends Microbiol. 2013 Sep;21:451–456.
  • Ogawa M, Yoshikawa Y, Kobayashi T, et al. A Tecpr1-dependent selective autophagy pathway targets bacterial pathogens. Cell Host Microbe. 2011 May;9:376–389.
  • Ogawa M, Yoshimori T, Suzuki T, et al. Escape of intracellular Shigella from autophagy. Science. 2005 Feb;307:727–731.
  • Choy A, Dancourt J, Mugo B, et al. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science. 2012 Nov;338:1072–1076.
  • Heinzen RA, Scidmore MA, Rockey DD, et al. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect Immun. 1996 Mar;64:796–809.
  • Winchell CG, Graham JG, Kurten RC, et al. Coxiella burnetii type IV secretion-dependent recruitment of macrophage autophagosomes. Infect Immun. 2014 Jun;82:2229–2238.
  • Scheidel J, Amstein L, Ackermann J, et al. In silico knockout studies of xenophagic capturing of salmonella. PLoS Comput Biol. 2016 Dec;12:e1005200.
  • Cui T, Li W, Liu L, et al. Uncovering new pathogen-host protein-protein interactions by pairwise structure similarity. PLoS ONE. 2016 Jan;11:e0147612.
  • Dyer MD, Murali TM, Sobral BW. Computational prediction of host-pathogen protein-protein interactions. Bioinformatics. 2007 Jul;23:i159–66.
  • Garamszegi S, Franzosa EA, Xia Y. Signatures of pleiotropy, economy and convergent evolution in a domain-resolved map of human-virus protein-protein interaction networks. PLoS Pathog. 2013 Dec;9:e1003778.
  • Budak G, Eren Ozsoy O, Aydin Son Y, et al. Reconstruction of the temporal signaling network in Salmonella-infected human cells. Front Microbiol. 2015 Jul;6:730.
  • Fiskin E, Bionda T, Dikic I, et al. Global analysis of host and bacterial ubiquitinome in response to salmonella typhimurium infection. Mol Cell. 2016 Jun;62:967–981.
  • Hartford OM, Wann ER, Höök M, et al. Identification of residues in the Staphylococcus aureus fibrinogen-binding MSCRAMM clumping factor A (ClfA) that are important for ligand binding. J Biol Chem. 2001 Jan;276:2466–2473.
  • Ganesh VK, Rivera JJ, Smeds E, et al. A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog. 2008 Nov;4:e1000226.
  • Higgins J, Loughman A, van Kessel KPM, et al. Clumping factor A of Staphylococcus aureus inhibits phagocytosis by human polymorphonuclear leucocytes. FEMS Microbiol Lett. 2006 May;258:290–296.
  • Haiko J, Westerlund-Wikström B. The role of the bacterial flagellum in adhesion and virulence. Biology (Basel). 2013 Oct;2:1242–1267.
  • Cemma M, Kim PK, Brumell JH. The ubiquitin-binding adaptor proteins p62/SQSTM1 and NDP52 are recruited independently to bacteria-associated microdomains to target Salmonella to the autophagy pathway. Autophagy. 2011 Mar;7:341–345.
  • Ellinghaus D, Zhang H, Zeissig S, et al. Association between variants of PRDM1 and NDP52 and Crohn’s disease, based on exome sequencing and functional studies. Gastroenterology. 2013 Aug;145:339–347.
  • Vignal C, Singer E, Peyrin-Biroulet L, et al. How NOD2 mutations predispose to Crohn’s disease? Microbes Infect. 2007 Apr;9:658–663.
  • Hampe J, Franke A, Rosenstiel P, et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet. 2007 Feb;39:207–211.
  • Rioux JD, Xavier RJ, Taylor KD, et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet. 2007 May;39:596–604.
  • Galson DL, Roodman GD. Pathobiology of paget’s disease of bone. J Bone Metab. 2014 May;21:85–98.
  • Servera E, Sancho J, Bañuls P, et al. Bulbar impairment score predicts noninvasive volume-cycled ventilation failure during an acute lower respiratory tract infection in ALS. J Neurol Sci. 2015 Nov;358:87–91.
  • Angelakis E, Patrick G, Peloni JM, et al. Orientia tsutsugamushi in lung of patient with acute respiratory distress syndrome, France, 2013. Emerging Infect. Dis. 2015 Feb;21:373–375.
  • Chen L, Zheng D, Liu B, et al. VFDB 2016: hierarchical and refined dataset for big data analysis–10 years on. Nucleic Acids Res. 2016 Jan;44:D694–7.
  • Atilano ML, Pereira PM, Vaz F, et al. Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the drosophila innate immune system. Elife. 2014 Apr;3:e02277.
  • Jan AT. Outer membrane vesicles (OMVs) of gram-negative bacteria: A perspective update. Front Microbiol. 2017 Jun;8:1053.
  • Bai J, Kim SI, Ryu S, et al. Identification and characterization of outer membrane vesicle-associated proteins in Salmonella enterica serovar Typhimurium. Infect Immun. 2014 Oct;82:4001–4010.
  • Galka F, Wai SN, Kusch H, et al. Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun. 2008 May;76:1825–1836.
  • Liu Q, Yi J, Liang K, et al. Salmonella Choleraesuis outer membrane vesicles: proteomics and immunogenicity. J Basic Microbiol. 2017 Jul;852–861.
  • Fábrega M-J, Rodríguez-Nogales A, Garrido-Mesa J, et al. Intestinal anti-inflammatory effects of outer membrane vesicles from Escherichia coli Nissle 1917 in DSS-experimental colitis in mice. Front Microbiol. 2017 Jul;8:1274.
  • Cañas M-A, Giménez R, Fábrega M-J, et al. Outer membrane vesicles from the probiotic Escherichia coli Nissle 1917 and the commensal ECOR12 enter intestinal epithelial cells via clathrin-dependent endocytosis and elicit differential effects on DNA damage. PLoS ONE. 2016 Aug;11:e0160374.
  • Aguilera L, Toloza L, Giménez R, et al. Proteomic analysis of outer membrane vesicles from the probiotic strain Escherichia coli Nissle 1917. Proteomics. 2014 Feb;14:222–229.
  • Zakharzhevskaya NB, Vanyushkina AA, Altukhov IA, et al. Outer membrane vesicles secreted by pathogenic and nonpathogenic Bacteroides fragilis represent different metabolic activities. Sci Rep. 2017 Jul;7:5008.
  • Leppla SH. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc Natl Acad Sci USA. 1982 May;79:3162–3166.
  • Romagnoli A, Etna MP, Giacomini E, et al. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy. 2012 Sep;8:1357–1370.
  • Chen D, Zhong Q. A tethering coherent protein in autophagosome maturation. Autophagy. 2012 Jun;8:985–986.
  • Michaux C, Holmqvist E, Vasicek E, et al. RNA target profiles direct the discovery of virulence functions for the cold-shock proteins CspC and CspE. Proc Natl Acad Sci USA. 2017 Jun;114:6824–6829.
  • Eggleson KK, Duffin KL, Goldberg DE. Identification and characterization of falcilysin, a metallopeptidase involved in hemoglobin catabolism within the malaria parasite plasmodium falciparum. J Biol Chem. 1999 Nov;274:32411–32417.
  • Dabonné S, Moallic C, Sine J-P, et al. Cloning, expression and characterization of a 46.5-kDa metallopeptidase from Bacillus halodurans H4 sharing properties with the pitrilysin family. Biochim Biophys Acta. 2005 Aug;1725:136–143.
  • Kimura Y, Ikuta K, Kimura T, et al. Nardilysin regulates inflammation, metaplasia, and tumors in murine stomach. Sci Rep. 2017 Feb;7:43052.
  • Castanheira S, García-Del Portillo F. Salmonella populations inside host cells. Front Cell Infect Microbiol. 2017 Oct;7:432.
  • Knodler LA, Nair V, Steele-Mortimer O. Quantitative assessment of cytosolic Salmonella in epithelial cells. PLoS ONE. 2014 Jan;9:e84681.
  • Ji Y, McLandsborough L, Kondagunta A, et al. C5a peptidase alters clearance and trafficking of group A streptococci by infected mice. Infect Immun. 1996 Feb;64:503–510.
  • Nakagawa I, Amano A, Mizushima N, et al. Autophagy defends cells against invading group A Streptococcus. Science. 2004 Nov;306:1037–1040.
  • Knodler LA, Vallance BA, Celli J, et al. Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci USA. 2010 Oct;107:17733–17738.
  • Kirkin V, Lamark T, Sou Y-S, et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell. 2009 Feb;33:505–516.
  • Brown D. Antibiotic resistance breakers: can repurposed drugs fill the antibiotic discovery void? Nat Rev Drug Discov. 2015 Dec;14:821–832.
  • The UniProt Consortium. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 2017 Jan;45:D158–D169.
  • Peabody MA, Laird MR, Vlasschaert C, et al. PSORTdb: expanding the bacteria and archaea protein subcellular localization database to better reflect diversity in cell envelope structures. Nucleic Acids Res. 2016 Jan;44:D663–8.
  • Jadhav TS, Wooten MW, Wooten MC. Mining the TRAF6/p62 interactome for a selective ubiquitination motif. BMC Proc. 2011 May;5(Suppl 2):S4.
  • Kim B-W, Hong SB, Kim JH, et al. Structural basis for recognition of autophagic receptor NDP52 by the sugar receptor galectin-8. Nat Commun. 2013;4:1613.
  • Jacomin A-C, Samavedam S, Promponas V, et al. iLIR database: A web resource for LIR motif-containing proteins in eukaryotes. Autophagy. 2016 Oct;12:1945–1953.
  • Kalvari I, Tsompanis S, Mulakkal NC, et al. iLIR: A web resource for prediction of Atg8-family interacting proteins. Autophagy. 2014 May;10:913–925.
  • van der Lee R, Buljan M, Lang B, et al. Classification of intrinsically disordered regions and proteins. Chem Rev. 2014 Jul;114:6589–6631.
  • Korcsmaros T, Dunai ZA, Vellai T, et al. Teaching the bioinformatics of signaling networks: an integrated approach to facilitate multi-disciplinary learning. Brief. Bioinformatics. 2013 Sep;14:618–632.
  • Bader S, Kühner S, Gavin A-C. Interaction networks for systems biology. FEBS Lett. 2008 Apr;582:1220–1224.
  • Raghavachari B, Tasneem A, Przytycka TM, et al. DOMINE: a database of protein domain interactions. Nucleic Acids Res. 2008 Jan;36:D656–61.
  • Dinkel H, Van Roey K, Michael S, et al. The eukaryotic linear motif resource ELM: 10 years and counting. Nucleic Acids Res. 2014 Jan;42:D259–66.
  • Türei D, Földvári-Nagy L, Fazekas D, et al. Autophagy regulatory network - a systems-level bioinformatics resource for studying the mechanism and regulation of autophagy. Autophagy. 2015;11:155–165.
  • Kubisch J, Türei D, Földvári-Nagy L, et al. Complex regulation of autophagy in cancer - integrated approaches to discover the networks that hold a double-edged sword. Semin Cancer Biol. 2013 Aug;23:252–261.
  • Remm M, Storm CE, Sonnhammer EL. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol. 2001 Dec;314:1041–1052.
  • Mészáros B, Simon I, Dosztányi Z. Prediction of protein binding regions in disordered proteins. PLoS Comput Biol. 2009 May;5:e1000376.
  • Dosztányi Z, Csizmók V, Tompa P, et al. The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J Mol Biol. 2005 Apr;347:827–839.
  • Jones P, Binns D, Chang H-Y, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014 May;30:1236–1240.
  • Hoiseth SK, Stocker BAD. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature. 1981;291(5812):238–239.
  • Hautefort I, Proenca MJ, Hinton JCD Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl. Environ. Microbiol. Dec 2003;69 (12):7480–7491.
  • Sambrook J, Russell D. Molecular cloning: A laboratory manual. 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2001.
  • Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Pnas. 2000 June;6:6640–6645.
  • Gemski P, Stocker BAD. Transduction by bacteriophage P22 in nonsmooth mutants of Salmonella typhimurium. Genet Mol Biol. 1967 May;93(5):1588–1597.
  • Cherepanov PP, Wackernagel W. Gene disruption in Escherichia coli: tcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene. 1995 May;158(1):9–14.