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Review

Bacteria Exploit Autophagy For Their Own Benefit

, , &
Pages 3205-3215 | Published online: 11 Oct 2019

References

  • Martinet W, Agostinis P, Vanhoecke B, Dewaele M, De Meyer GR. Autophagy in disease: a double-edged sword with therapeutic potential. Clin Sci (Lond). 2009;116(9):697–712. doi:10.1042/CS2008050819323652
  • Mancias JD, Kimmelman AC. Mechanisms of selective autophagy in normal physiology and cancer. J Mol Biol. 2016;428(9Pt A):1659–1680. doi:10.1016/j.jmb.2016.02.02726953261
  • Kimmelman AC. The dynamic nature of autophagy in cancer. Genes Dev. 2011;25(19):1999–2010. doi:10.1101/gad.1755881121979913
  • Klionsky DJ, Cregg JM, Dunn WA Jr., et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell. 2003;5(4):539–545.14536056
  • Tsukada M, Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 1993;333(1–2):169–174. doi:10.1016/0014-5793(93)80398-e8224160
  • Ohsumi Y. Historical landmarks of autophagy research. Cell Res. 2014;24(1):9–23. doi:10.1038/cr.2013.16924366340
  • Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol. 2010;22(2):124–131. doi:10.1016/j.ceb.2009.11.01420034776
  • Xiong Q, Li W, Li P, Yang M, Wu C, Eichinger L. The role of ATG16 in autophagy and the ubiquitin proteasome system. Cells. 2018;8:1. doi:10.3390/cells8010002
  • Levine B. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell. 2005;120(2):159–162. doi:10.1016/j.cell.2005.01.00515680321
  • Ogawa M, Mimuro H, Yoshikawa Y, Ashida H, Sasakawa C. Manipulation of autophagy by bacteria for their own benefit. Microbiol Immunol. 2011;55(7):459–471. doi:10.1111/j.1348-0421.2011.00343.x21707736
  • Robinson M, Schor S, Barouch-Bentov R, Einav S. Viral journeys on the intracellular highways. Cell Mol Life Sci. 2018;75(20):3693–3714. doi:10.1007/s00018-018-2882-030043139
  • Echavarria-Consuegra L, Smit JM, Reggiori F. Role of autophagy during the replication and pathogenesis of common mosquito-borne flavi- and alphaviruses. Open Biol. 2019;9(3):190009. doi:10.1098/rsob.19005430862253
  • Choi Y, Bowman JW, Jung JU. Autophagy during viral infection – a double-edged sword. Nat Rev Microbiol. 2018;16(6):341–354. doi:10.1038/s41579-018-0003-629556036
  • Niu H, Yamaguchi M, Rikihisa Y. Subversion of cellular autophagy by Anaplasma phagocytophilum. Cell Microbiol. 2008;10(3):593–605. doi:10.1111/j.1462-5822.2007.01068.x17979984
  • Niu H, Xiong Q, Yamamoto A, Hayashi-Nishino M, Rikihisa Y. Autophagosomes induced by a bacterial Beclin 1 binding protein facilitate obligatory intracellular infection. Proc Natl Acad Sci U S A. 2012;109(51):20800–20807. doi:10.1073/pnas.121867410923197835
  • Niu H, Rikihisa Y. Ats-1: a novel bacterial molecule that links autophagy to bacterial nutrition. Autophagy. 2013;9(5):787–788. doi:10.4161/auto.2369323388398
  • Pappas G, Akritidis N, Bosilkovski M, Tsianos E. Brucellosis. N Engl J Med. 2005;352(22):2325–2336. doi:10.1056/NEJMra05057015930423
  • Celli J. Surviving inside a macrophage: the many ways of Brucella. Res Microbiol. 2006;157(2):93–98. doi:10.1016/j.resmic.2005.10.00216364608
  • Pizarro-Cerda J, Meresse S, Parton RG, et al. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun. 1998;66(12):5711–5724.9826346
  • Taguchi Y, Imaoka K, Kataoka M, et al. Yip1A, a novel host factor for the activation of the IRE1 pathway of the unfolded protein response during Brucella infection. PLoS Pathog. 2015;11(3):e1004747. doi:10.1371/journal.ppat.100474725742138
  • Starr T, Child R, Wehrly TD, et al. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe. 2012;11(1):33–45. doi:10.1016/j.chom.2011.12.00222264511
  • Pizarro-Cerda J, Moreno E, Sanguedolce V, Mege JL, Gorvel JP. Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun. 1998;66(5):2387–2392.9573138
  • Arriola Benitez PC, Pesce Viglietti AI, Herrmann CK, et al. Brucella abortus promotes a fibrotic phenotype in hepatic stellate cells, with concomitant activation of the autophagy pathway. Infect Immun. 2018;86:1.
  • Pesce Viglietti AI, Gentilini MV, Arriola Benitez PC, Giambartolomei GH, Delpino MV. B. abortus modulates osteoblast function through the induction of autophagy. Front Cell Infect Microbiol. 2018;8:425. doi:10.3389/fcimb.2018.0002630564561
  • Guo F, Zhang H, Chen C, et al. Autophagy favors Brucella melitensis survival in infected macrophages. Cell Mol Biol Lett. 2012;17(2):249–257. doi:10.2478/s11658-012-0009-422367856
  • Li T, Xu Y, Liu L, et al. Brucella melitensis 16M regulates the effect of AIR domain on inflammatory factors, autophagy, and apoptosis in mouse macrophage through the ROS signaling pathway. PLoS One. 2016;11(12):e0167486. doi:10.1371/journal.pone.016748627907115
  • Pandey A, Lin F, Cabello AL, et al. Activation of host IRE1alpha-dependent signaling axis contributes the intracellular parasitism of Brucella melitensis. Front Cell Infect Microbiol. 2018;8:103. doi:10.3389/fcimb.2018.0002629732320
  • Colombo MI, Gutierrez MG, Romano PS. The two faces of autophagy: Coxiella and Mycobacterium. Autophagy. 2006;2(3):162–164. doi:10.4161/auto.282716874070
  • Escoll P, Rolando M, Buchrieser C. Modulation of host autophagy during bacterial infection: sabotaging host munitions for pathogen nutrition. Front Immunol. 2016;7:81. doi:10.3389/fimmu.2016.0008126973656
  • Steele S, Brunton J, Kawula T. The role of autophagy in intracellular pathogen nutrient acquisition. Front Cell Infect Microbiol. 2015;5:51. doi:10.3389/fcimb.2015.0005126106587
  • Beron W, Gutierrez MG, Rabinovitch M, Colombo MI. Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immun. 2002;70(10):5816–5821. doi:10.1128/iai.70.10.5816-5821.200212228312
  • Gutierrez MG, Vazquez CL, Munafo DB, et al. Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol. 2005;7(7):981–993. doi:10.1111/j.1462-5822.2005.00527.x15953030
  • Vazquez CL, Colombo MI. Coxiella burnetii modulates Beclin 1 and Bcl-2, preventing host cell apoptosis to generate a persistent bacterial infection. Cell Death Differ. 2010;17(3):421–438. doi:10.1038/cdd.2009.12919798108
  • Latomanski EA, Newton HJ. Interaction between autophagic vesicles and the Coxiella-containing vacuole requires CLTC (clathrin heavy chain). Autophagy. 2018;14(10):1710–1725. doi:10.1080/15548627.2018.148380629973118
  • McCaul TF, Williams JC. Developmental cycle of Coxiella burnetii: structure and morphogenesis of vegetative and sporogenic differentiations. J Bacteriol. 1981;147(3):1063–1076.7275931
  • Gutierrez MG, Colombo MI. Autophagosomes: a fast-food joint for unexpected guests. Autophagy. 2005;1(3):179–181. doi:10.4161/auto.1.3.206316874034
  • Baca OG, Li YP, Kumar H. Survival of the Q fever agent Coxiella burnetii in the phagolysosome. Trends Microbiol. 1994;2(12):476–480. doi:10.1016/0966-842x(94)90651-37889323
  • Hackstadt T, Williams JC. Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc Natl Acad Sci U S A. 1981;78(5):3240–3244. doi:10.1073/pnas.78.5.32406942430
  • Heinzen RA, Hackstadt T, Samuel JE. Developmental biology of Coxiella burnettii. Trends Microbiol. 1999;7(4):149–154. doi:10.1016/s0966-842x(99)01475-410217829
  • Newton HJ, Kohler LJ, McDonough JA, et al. A screen of Coxiella burnetii mutants reveals important roles for Dot/Icm effectors and host autophagy in vacuole biogenesis. PLoS Pathog. 2014;10(7):e1004286. doi:10.1371/journal.ppat.100428625080348
  • Kohler LJ, Reed SC, Sarraf SA, Arteaga DD, Newton HJ, Roy CR. Effector protein Cig2 decreases host tolerance of infection by directing constitutive fusion of autophagosomes with the coxiella-containing vacuole. MBio. 2016;7:4.
  • Martinez E, Allombert J, Cantet F, et al. Coxiella burnetii effector CvpB modulates phosphoinositide metabolism for optimal vacuole development. Proc Natl Acad Sci U S A. 2016;113(23):E3260–E3269. doi:10.1073/pnas.152281111327226300
  • Mansilla Pareja ME, Bongiovanni A, Lafont F, Colombo MI. Alterations of the Coxiella burnetii replicative vacuole membrane integrity and interplay with the autophagy pathway. Front Cell Infect Microbiol. 2017;7:112. doi:10.3389/fcimb.2017.0051728484683
  • Al-Younes HM, Brinkmann V, Meyer TF. Interaction of Chlamydia trachomatis serovar L2 with the host autophagic pathway. Infect Immun. 2004;72(8):4751–4762. doi:10.1128/IAI.72.8.4751-4762.200415271937
  • Yasir M, Pachikara ND, Bao X, Pan Z, Fan H. Regulation of chlamydial infection by host autophagy and vacuolar ATPase-bearing organelles. Infect Immun. 2011;79(10):4019–4028. doi:10.1128/IAI.05308-1121807906
  • Ouellette SP, Dorsey FC, Moshiach S, Cleveland JL, Carabeo RA. Chlamydia species-dependent differences in the growth requirement for lysosomes. PLoS One. 2011;6(3):e16783. doi:10.1371/journal.pone.001678321408144
  • Lei W, Li Q, Su S, Bu J, Huang Q, Li Z. Chlamydia trachomatis plasmid-encoded protein pORF5 protects mitochondrial function by inducing mitophagy and increasing HMGB1 expression. Pathog Dis. 2017;75:9. doi:10.1093/femspd/ftx111
  • Oyston PC, Sjostedt A, Titball RW. Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat Rev Microbiol. 2004;2(12):967–978. doi:10.1038/nrmicro104515550942
  • Checroun C, Wehrly TD, Fischer ER, Hayes SF, Celli J. Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc Natl Acad Sci U S A. 2006;103(39):14578–14583. doi:10.1073/pnas.060183810316983090
  • Steele S, Brunton J, Ziehr B, Taft-Benz S, Moorman N, Kawula T. Francisella tularensis harvests nutrients derived via ATG5-independent autophagy to support intracellular growth. PLoS Pathog. 2013;9(8):e1003562. doi:10.1371/journal.ppat.100356223966861
  • Wang YH, Wu JJ, Lei HY. The autophagic induction in Helicobacter pylori-infected macrophage. Exp Biol Med (Maywood). 2009;234(2):171–180. doi:10.3181/0808-RM-25219064937
  • Hu W, Zhang L, Li MX, et al. Vitamin D3 activates the autolysosomal degradation function against Helicobacter pylori through the PDIA3 receptor in gastric epithelial cells. Autophagy. 2019;15(4):707–725. doi:10.1080/15548627.2018.155783530612517
  • Terebiznik MR, Raju D, Vazquez CL, et al. Effect of Helicobacter pylori’s vacuolating cytotoxin on the autophagy pathway in gastric epithelial cells. Autophagy. 2009;5(3):370–379. doi:10.4161/auto.5.3.766319164948
  • Raju D, Hussey S, Ang M, et al. Vacuolating cytotoxin and variants in Atg16L1 that disrupt autophagy promote Helicobacter pylori infection in humans. Gastroenterology. 2012;142(5):1160–1171. doi:10.1053/j.gastro.2012.01.04322333951
  • Yahiro K, Satoh M, Nakano M, et al. Low-density lipoprotein receptor-related protein-1 (LRP1) mediates autophagy and apoptosis caused by Helicobacter pylori VacA. J Biol Chem. 2012;287(37):31104–31115. doi:10.1074/jbc.M112.38749822822085
  • Kim IJ, Lee J, Oh SJ, et al. Helicobacter pylori infection modulates host cell metabolism through VacA-dependent inhibition of mTORC1. Cell Host Microbe. 2018;23(5):583–593 e588. doi:10.1016/j.chom.2018.04.00629746831
  • Lai CH, Huang JC, Cheng HH, et al. Helicobacter pylori cholesterol glucosylation modulates autophagy for increasing intracellular survival in macrophages. Cell Microbiol. 2018;20(12):e12947. doi:10.1111/cmi.1294730151951
  • Zhang L, Hu W, Cho CH, et al. Reduced lysosomal clearance of autophagosomes promotes survival and colonization of Helicobacter pylori. J Pathol. 2018;244(4):432–444. doi:10.1002/path.503329327342
  • Wang YH, Gorvel JP, Chu YT, Wu JJ, Lei HY. Helicobacter pylori impairs murine dendritic cell responses to infection. PLoS One. 2010;5(5):e10844. doi:10.1371/journal.pone.001084420523725
  • Campoy E, Colombo MI. Autophagy in intracellular bacterial infection. Biochim Biophys Acta. 2009;1793(9):1465–1477. doi:10.1016/j.bbamcr.2009.03.00319303905
  • Dubuisson JF, Swanson MS. Mouse infection by Legionella, a model to analyze autophagy. Autophagy. 2006;2(3):179–182. doi:10.4161/auto.283116874080
  • Joshi AD, Swanson MS. Secrets of a successful pathogen: legionella resistance to progression along the autophagic pathway. Front Microbiol. 2011;2:138. doi:10.3389/fmicb.2011.0021521743811
  • Sturgill-Koszycki S, Swanson MS. Legionella pneumophila replication vacuoles mature into acidic, endocytic organelles. J Exp Med. 2000;192(9):1261–1272. doi:10.1084/jem.192.9.126111067875
  • Amer AO, Swanson MS. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol. 2005;7(6):765–778. doi:10.1111/j.1462-5822.2005.00509.x15888080
  • Zhang Y, Yao Y, Qiu X, et al. Listeria hijacks host mitophagy through a novel mitophagy receptor to evade killing. Nat Immunol. 2019;20(4):433–446. doi:10.1038/s41590-019-0324-230804553
  • Lerner TR, de Souza Carvalho-Wodarz C, Repnik U, et al. Lymphatic endothelial cells are a replicative niche for Mycobacterium tuberculosis. J Clin Invest. 2016;126(3):1093–1108. doi:10.1172/JCI8337926901813
  • Fine KL, Metcalfe MG, White E, Virji M, Karls RK, Quinn FD. Involvement of the autophagy pathway in trafficking of Mycobacterium tuberculosis bacilli through cultured human type II epithelial cells. Cell Microbiol. 2012;14(9):1402–1414. doi:10.1111/j.1462-5822.2012.01804.x22519722
  • Scherr N, Honnappa S, Kunz G, et al. Structural basis for the specific inhibition of protein kinase G, a virulence factor of Mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 2007;104(29):12151–12156. doi:10.1073/pnas.070284210417616581
  • Wong D, Bach H, Sun J, Hmama Z, Av-Gay Y. Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H+-ATPase to inhibit phagosome acidification. Proc Natl Acad Sci U S A. 2011;108(48):19371–19376. doi:10.1073/pnas.110920110822087003
  • Zulauf KE, Sullivan JT, Braunstein M. The SecA2 pathway of Mycobacterium tuberculosis exports effectors that work in concert to arrest phagosome and autophagosome maturation. PLoS Pathog. 2018;14(4):e1007011. doi:10.1371/journal.ppat.100701129709019
  • de Chastellier C, Thilo L. Cholesterol depletion in Mycobacterium avium-infected macrophages overcomes the block in phagosome maturation and leads to the reversible sequestration of viable mycobacteria in phagolysosome-derived autophagic vacuoles. Cell Microbiol. 2006;8(2):242–256. doi:10.1111/j.1462-5822.2005.00617.x16441435
  • Lerena MC, Colombo MI. Mycobacterium marinum induces a marked LC3 recruitment to its containing phagosome that depends on a functional ESX-1 secretion system. Cell Microbiol. 2011;13(6):814–835. doi:10.1111/j.1462-5822.2011.01581.x21447143
  • Gerstenmaier L, Pilla R, Herrmann L, et al. The autophagic machinery ensures nonlytic transmission of mycobacteria. Proc Natl Acad Sci U S A. 2015;112(7):E687–692. doi:10.1073/pnas.142331811225646440
  • Atanasova KR, Yilmaz O. Prelude to oral microbes and chronic diseases: past, present and future. Microbes Infect. 2015;17(7):473–483. doi:10.1016/j.micinf.2015.03.00725813714
  • Reyes L, Eiler-Mcmanis E, Rodrigues PH, et al. Deletion of lipoprotein PG0717 in Porphyromonas gingivalis W83 reduces gingipain activity and alters trafficking in and response by host cells. PLoS One. 2013;8(9):e74230. doi:10.1371/journal.pone.007423024069284
  • Dorn BR, Dunn WA Jr., Progulske-Fox A. Invasion of human coronary artery cells by periodontal pathogens. Infect Immun. 1999;67(11):5792–5798.10531230
  • Dorn BR, Dunn WA Jr., Progulske-Fox A. Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect Immun. 2001;69(9):5698–5708. doi:10.1128/iai.69.9.5698-5708.200111500446
  • Lee K, Roberts JS, Choi CH, Atanasova KR, Yilmaz O. Porphyromonas gingivalis traffics into endoplasmic reticulum-rich-autophagosomes for successful survival in human gingival epithelial cells. Virulence. 2018;9(1):845–859. doi:10.1080/21505594.2018.145417129616874
  • Liu J, Wang X, Zheng M, Luan Q. Lipopolysaccharide from Porphyromonas gingivalis promotes autophagy of human gingival fibroblasts through the PI3K/Akt/mTOR signaling pathway. Life Sci. 2018;211:133–139. doi:10.1016/j.lfs.2018.09.02330218719
  • Hagio-Izaki K, Yasunaga M, Yamaguchi M, et al. Lipopolysaccharide induces bacterial autophagy in epithelial keratinocytes of the gingival sulcus. BMC Cell Biol. 2018;19(1):18. doi:10.1186/s12860-018-0168-x30165815
  • Yang F, Kimberlin AN, Elowsky CG, et al. A plant immune receptor degraded by selective autophagy. Mol Plant. 2019;12(1):113–123. doi:10.1016/j.molp.2018.11.01130508598
  • Dong J, Chen W. The role of autophagy in chloroplast degradation and chlorophagy in immune defenses during Pst DC3000 (AvrRps4) infection. PLoS One. 2013;8(8):e73091. doi:10.1371/journal.pone.007309124023671
  • Ustun S, Hafren A, Liu Q, et al. Bacteria exploit autophagy for proteasome degradation and enhanced virulence in plants. Plant Cell. 2018;30(3):668–685. doi:10.1105/tpc.17.0081529500318
  • Pujol C, Klein KA, Romanov GA, et al. Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect Immun. 2009;77(6):2251–2261. doi:10.1128/IAI.00068-0919289509
  • Ustun S, Sheikh A, Gimenez-Ibanez S, Jones A, Ntoukakis V, Bornke F. The proteasome acts as a hub for plant immunity and is targeted by Pseudomonas type III effectors. Plant Physiol. 2016;172(3):1941–1958. doi:10.1104/pp.16.0080827613851
  • Messer JS, Murphy SF, Logsdon MF, et al. The Crohn’s disease: associated ATG16L1 variant and Salmonella invasion. BMJ Open. 2013;3:6. doi:10.1136/bmjopen-2013-002790
  • Travassos LH, Carneiro LA, Ramjeet M, et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat Immunol. 2010;11(1):55–62. doi:10.1038/ni.182319898471
  • Yu HB, Croxen MA, Marchiando AM, et al. Autophagy facilitates Salmonella replication in HeLa cells. MBio. 2014;5(2):e00865–00814. doi:10.1128/mBio.00865-1424618251
  • 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;18(5):527–537. doi:10.1016/j.chom.2015.10.01526567507
  • Owen KA, Casanova JE. Salmonella manipulates autophagy to “serve and protect”. Cell Host Microbe. 2015;18(5):517–519. doi:10.1016/j.chom.2015.10.02026567504
  • Casanova JE. Bacterial autophagy: offense and defense at the host-pathogen interface. Cell Mol Gastroenterol Hepatol. 2017;4(2):237–243.28660242
  • Fedrigo GV, Campoy EM, Di Venanzio G, Colombo MI, Garcia Vescovi E. Serratia marcescens is able to survive and proliferate in autophagic-like vacuoles inside non-phagocytic cells. PLoS One. 2011;6(8):e24054.21901159
  • Di Venanzio G, Stepanenko TM, Garcia Vescovi E. Serratia marcescens ShlA pore-forming toxin is responsible for early induction of autophagy in host cells and is transcriptionally regulated by RcsB. Infect Immun. 2014;82(9):3542–3554.24914224
  • Schnaith A, Kashkar H, Leggio SA, Addicks K, Kronke M, Krut O. Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J Biol Chem. 2007;282(4):2695–2706.17135247
  • Boada-Romero E, Letek M, Fleischer A, Pallauf K, Ramon-Barros C, Pimentel-Muinos FX. TMEM59 defines a novel ATG16L1-binding motif that promotes local activation of LC3. Embo J. 2013;32(4):566–582.23376921
  • Mestre MB, Colombo MI. cAMP and EPAC are key players in the regulation of the signal transduction pathway involved in the alpha-hemolysin autophagic response. PLoS Pathog. 2012;8(5):e1002664.22654658
  • Wang C, Symington JW, Mysorekar IU. ATG16L1 and pathogenesis of urinary tract infections. Autophagy. 2012;8(11):1693–1694.22874553
  • Cadwell K, Liu JY, Brown SL, et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature. 2008;456(7219):259–263.18849966
  • Wang C, Mendonsa GR, Symington JW, et al. Atg16L1 deficiency confers protection from uropathogenic Escherichia coli infection in vivo. Proc Natl Acad Sci U S A. 2012;109(27):11008–11013.22715292
  • Clyne M. Urinary tract infections: autophagy gene mutation confers protection against uropathogenic E. coli infection. Nat Rev Urol. 2012;9(8):410. doi:10.1038/nrurol.2012.140
  • Wang C, Yuan X, Ma E, et al. NOD2 is dispensable for ATG16L1 deficiency-mediated resistance to urinary tract infection. Autophagy. 2014;10(2):331–338. doi:10.4161/auto.2719624384785
  • Symington JW, Wang C, Twentyman J, et al. ATG16L1 deficiency in macrophages drives clearance of uropathogenic E. coli in an IL-1beta-dependent manner. Mucosal Immunol. 2015;8(6):1388–1399. doi:10.1038/mi.2015.725669147
  • Wang C, Bauckman KA, Ross ASB, et al. A non-canonical autophagy-dependent role of the ATG16L1(T300A) variant in urothelial vesicular trafficking and uropathogenic Escherichia coli persistence. Autophagy. 2019;15(3):527–542. doi:10.1080/15548627.2018.153529030335568
  • Bauckman KA, Mysorekar IU. Ferritinophagy drives uropathogenic Escherichia coli persistence in bladder epithelial cells. Autophagy. 2016;12(5):850–863. doi:10.1080/15548627.2016.116017627002654
  • Perry RD, Fetherston JD. Yersinia pestis – etiologic agent of plague. Clin Microbiol Rev. 1997;10(1):35–66.8993858
  • Lukaszewski RA, Kenny DJ, Taylor R, Rees DG, Hartley MG, Oyston PC. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect Immun. 2005;73(11):7142–7150. doi:10.1128/IAI.73.11.7142-7150.200516239508
  • Klein KA, Bliska JB. How Yersinia pestis becomes a foreign obstruction in the digestive system of the macrophage. Autophagy. 2009;5(6):882–883. doi:10.4161/auto.909519550144
  • Moreau K, Lacas-Gervais S, Fujita N, et al. Autophagosomes can support Yersinia pseudotuberculosis replication in macrophages. Cell Microbiol. 2010;12(8):1108–1123. doi:10.1111/j.1462-5822.2010.01456.x20180800
  • Ligeon LA, Moreau K, Barois N, et al. Role of VAMP3 and VAMP7 in the commitment of Yersinia pseudotuberculosis to LC3-associated pathways involving single- or double-membrane vacuoles. Autophagy. 2014;10(9):1588–1602. doi:10.4161/auto.2941125046114