3,426
Views
60
CrossRef citations to date
0
Altmetric
Basic Research Paper

Ferritinophagy drives uropathogenic Escherichia coli persistence in bladder epithelial cells

&
Pages 850-863 | Received 10 Aug 2015, Accepted 25 Feb 2016, Published online: 22 Mar 2016

References

  • Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol 2010; 7:653-60; PMID:21139641; http://dx.doi.org/10.1038/nrurol.2010.190
  • Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015; 13:269-84; PMID:25853778; http://dx.doi.org/10.1038/nrmicro3432
  • Barber AE, Norton JP, Spivak AM, Mulvey MA. Urinary tract infections: current and emerging management strategies. Clin Infect Dis 2013; 57:719-24; PMID:23645845; http://dx.doi.org/10.1093/cid/cit284
  • Wang C, Symington JW, Mysorekar IU. ATG16L1 and pathogenesis of urinary tract infections. Autophagy 2012; 8:1693-4; PMID:22874553; http://dx.doi.org/10.4161/auto.21600
  • Wang C, Mendonsa GR, Symington JW, Zhang Q, Cadwell K, Virgin HW, Mysorekar IU. Atg16L1 deficiency confers protection from uropathogenic Escherichia coli infection in vivo. Proc Natl Acad Sci USA 2012; 109:11008-13; PMID:22715292; http://dx.doi.org/10.1073/pnas.1203952109
  • Yep A, McQuade T, Kirchhoff P, Larsen M, Mobley HL. Inhibitors of TonB function identified by a high-throughput screen for inhibitors of iron acquisition in uropathogenic Escherichia coli CFT073. MBio 2014; 5:e01089-1013; PMID:24570372; http://dx.doi.org/10.1128/mBio.01089-13
  • Garcia EC, Brumbaugh AR, Mobley HL. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect Immun 2011; 79:1225-35; PMID:21220482; http://dx.doi.org/10.1128/IAI.01222-10
  • Gao Q, Wang X, Xu H, Xu Y, Ling J, Zhang D, Gao S, Liu X. Roles of iron acquisition systems in virulence of extraintestinal pathogenic Escherichia coli: salmochelin and aerobactin contribute more to virulence than heme in a chicken infection model. BMC Microbiol 2012; 12:143; PMID:22817680; http://dx.doi.org/10.1186/1471-2180-12-143
  • Subashchandrabose S, Mobley HL. Back to the metal age: battle for metals at the host-pathogen interface during urinary tract infection. Metallomics 2015; 7(6):935-42; PMID:25677827; http://dx.doi.org/10.1039/c4mt00329b
  • Wiles TJ, Kulesus RR, Mulvey MA. Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol 2008; 85:11-19; PMID:18482721; http://dx.doi.org/10.1016/j.yexmp.2008.03.007
  • Hagan EC, Mobley HL. Haem acquisition is facilitated by a novel receptor Hma and required by uropathogenic Escherichia coli for kidney infection. Mol Microbiol 2009; 71:79-91; PMID:19019144; http://dx.doi.org/10.1111/j.1365-2958.2008.06509.x
  • Hagan EC, Lloyd AL, Rasko DA, Faerber GJ, Mobley HL. Escherichia coli global gene expression in urine from women with urinary tract infection. PLoS Pathog 2010; 6:e1001187; PMID:21085611; http://dx.doi.org/10.1371/journal.ppat.1001187
  • Shields-Cutler RR, Crowley JR, Hung CS, Stapleton AE, Aldrich CC, Marschall J, Henderson JP. Human urinary composition controls Siderocalin's antibacterial activity. J Biol Chem 2015; 290(26):15949-60; PMID:25861985; http://dx.doi.org/10.1074/jbc.M115.645812
  • Brumbaugh AR, Smith SN, Mobley HL. Immunization with the yersiniabactin receptor, FyuA, protects against pyelonephritis in a murine model of urinary tract infection. Infect Immun 2013; 81:3309-16; PMID:23798537; http://dx.doi.org/10.1128/IAI.00470-13
  • Silva B, Faustino P. An overview of molecular basis of iron metabolism regulation and the associated pathologies. Biochim Biophys Acta 2015; 1852:1347-59; PMID:25843914; http://dx.doi.org/10.1016/j.bbadis.2015.03.011
  • Richardson DR, Lane DJ, Becker EM, Huang ML, Whitnall M, Suryo Rahmanto Y, Sheftel AD, Ponka P. Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol. Proc Natl Acad Sci USA 2010; 107:10775-82; PMID:20495089; http://dx.doi.org/10.1073/pnas.0912925107
  • Lunova M, Goehring C, Kuscuoglu D, Mueller K, Chen Y, Walther P, Deschemin JC, Vaulont S, Haybaeck J, Lackner C, et al. Hepcidin knockout mice fed with iron-rich diet develop chronic liver injury and liver fibrosis due to lysosomal iron overload. J Hepatol 2014; 61:633-641; PMID:24816174; http://dx.doi.org/10.1016/j.jhep.2014.04.034
  • Kurz T, Terman A, Gustafsson B, Brunk UT. Lysosomes in iron metabolism, ageing and apoptosis. Histochem Cell Biol 2008; 129:389-406; PMID:18259769; http://dx.doi.org/10.1007/s00418-008-0394-y
  • Kurz T, Eaton JW, Brunk UT. The role of lysosomes in iron metabolism and recycling. Int J Biochem Cell Biol 2011; 43:1686-97; PMID:21907822; http://dx.doi.org/10.1016/j.biocel.2011.08.016
  • De Domenico I, Vaughn MB, Li L, Bagley D, Musci G, Ward DM, Kaplan J. Ferroportin-mediated mobilization of ferritin iron precedes ferritin degradation by the proteasome. EMBO J 2006; 25:5396-404 PMID:17082767; http://dx.doi.org/10.1038/sj.emboj.7601409
  • Bauckman KA, Haller E, Flores I, Nanjundan M. Iron modulates cell survival in a Ras- and MAPK-dependent manner in ovarian cells. Cell Death Dis 2013; 4:e592; PMID:23598404; http://dx.doi.org/10.1038/cddis.2013.87
  • Bauckman K, Haller E, Taran N, Rockfield S, Ruiz-Rivera A, Nanjundan M. Iron alters cell survival in a mitochondria-dependent pathway in ovarian cancer cells. Biochem J 2015; 466:401-13; PMID:25697096; http://dx.doi.org/10.1042/BJ20140878
  • Mancias JD, Wang X, Gygi SP, Harper JW, Kimmelman AC. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 2014; 509:105-9; PMID:24695223; http://dx.doi.org/10.1038/nature13148
  • Dowdle WE, Nyfeler B, Nagel J, Elling RA, Liu S, Triantafellow E, Menon S, Wang Z, Honda A, Pardee G, et al. Selective VPS34 inhibitor blocks autophagy and uncovers a role for NCOA4 in ferritin degradation and iron homeostasis in vivo. Nat Cell Biol 2014; 16:1069-79; PMID:25327288; http://dx.doi.org/10.1038/ncb3053
  • Bauckman KA, Owusu-Boaitey N, Mysorekar IU. Selective autophagy: Xenophagy. Methods 2014; 75:120-7; PMID:25497060; http://dx.doi.org/10.1016/j.ymeth.2014.12.005
  • Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
  • Oppenheimer SJ. Iron and infection: the clinical evidence. Acta Paediatr Scand Suppl 1989; 361:53-62; PMID:2485586
  • Ala A, Schilsky ML. Inherited metabolic liver disease. Curr Opin Gastroenterol 2004; 20:198-207; PMID:15703644; http://dx.doi.org/10.1097/00001574-200405000-00004
  • Straud S, Zubovych I, De Brabander JK, Roth MG. Inhibition of iron uptake is responsible for differential sensitivity to V-ATPase inhibitors in several cancer cell lines. PloS One 2010; 5:e11629; PMID:20661293; http://dx.doi.org/10.1371/journal.pone.0011629
  • Dayani PN, Bishop MC, Black K, Zeltzer PM. Desferoxamine (DFO)–mediated iron chelation: rationale for a novel approach to therapy for brain cancer. J Neuro-Oncol 2004; 67:367-77; PMID:15164994; http://dx.doi.org/10.1023/B:NEON.0000024238.21349.37
  • Allen GF, Toth R, James J, Ganley IG. Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep 2013; 14:1127-135; PMID:24176932; http://dx.doi.org/10.1038/embor.2013.168
  • Mysorekar IU, Hultgren SJ. Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc Natl Acad Sci USA 2006; 103:14170-5; PMID:16968784; http://dx.doi.org/10.1073/pnas.0602136103
  • Knowles LM, Zewe J, Malik G, Parwani AV, Gingrich JR, Pilch J. CLT1 targets bladder cancer through integrin alpha5beta1 and CLIC3. Mol Cancer Res 2013; 11:194-203; PMID:23204394; http://dx.doi.org/10.1158/1541-7786.MCR-12-0300
  • Terman A, Kurz T. Lysosomal iron, iron chelation, and cell death. Antioxid Redox Signal 2013; 18:888-98; PMID:22909065; http://dx.doi.org/10.1089/ars.2012.4885
  • Morse D, Lin L, Choi AM, Ryter SW. Heme oxygenase-1, a critical arbitrator of cell death pathways in lung injury and disease. Free Radic Biol Med 2009; 47:1-12; PMID:19362144; http://dx.doi.org/10.1016/j.freeradbiomed.2009.04.007
  • Khan MI, Mohammad A, Patil G, Naqvi SA, Chauhan LK, Ahmad I. Induction of ROS, mitochondrial damage and autophagy in lung epithelial cancer cells by iron oxide nanoparticles. Biomaterials 2012; 33:1477-1488; PMID:22098780; http://dx.doi.org/10.1016/j.biom-aterials.2011.10.080
  • Chen G, Jing CH, Liu PP, Ruan D, Wang L. Induction of autophagic cell death in the rat brain caused by iron. Am J Med Sci 2013; 345:369-374; PMID:23187302; http://dx.doi.org/10.1097/MAJ.0b0-13e318271c031
  • Tait SW, Ichim G, Green DR. Die another way–non-apoptotic mechanisms of cell death. J Cell Sci 2014; 127:2135-2144; PMID:24833670; http://dx.doi.org/10.1242/jcs.093575
  • Symington JW, Wang C, Twentyman J, Owusu-Boaitey N, Schwendener R, Núñez G, Schilling JD, Mysorekar IU. ATG16L1 deficiency in macrophages drives clearance of uropathogenic E. coli in an IL-1beta-dependent manner. Mucosal Immunol 2015; 8(6):1388-99; PMID:25669147; http://dx.doi.org/10.1038/mi.2015.7
  • Schaale K, Peters KM, Murthy AM, Fritzsche AK, Phan MD, Totsika M, Robertson AA, Nichols KB, Cooper MA, Stacey KJ, et al. Strain- and host species-specific inflammasome activation, IL-1beta release, and cell death in macrophages infected with uropathogenic Escherichia coli. Mucosal Immunol 2015; 9(1):124-36; PMID:25993444; http://dx.doi.org/10.1038/mi.2015.44
  • Nagamatsu K, Hannan TJ, Guest RL, Kostakioti M, Hadjifrangiskou M, Binkley J, Dodson K, Raivio TL, Hultgren SJ. Dysregulation of Escherichia coli alpha-hemolysin expression alters the course of acute and persistent urinary tract infection. Proc Natl Acad Sci USA 2015; 112:E871-80; PMID:25675528; http://dx.doi.org/10.1073/pnas.1500374112
  • Boyle KB, Randow F. The role of ‘eat-me’ signals and autophagy cargo receptors in innate immunity. Curr Opin Microbiol 2013; 16:339-48; PMID:23623150; http://dx.doi.org/10.1016/j.mib.2013.03.010
  • Anderson CP, Shen M, Eisenstein RSm Lei bold EA. Mammalian iron metabolism and its control by iron regulatory proteins. Biochim Biophys Acta 2012; 1823:1468-83; PMID:22610083; http://dx.doi.org/10.1016/j.bbamcr.2012.05.010
  • Goodall M, Thorburn A. Identifying specific receptors for cargo-mediated autophagy. Cell Res 2014; 24:783-4; PMID:24797431; http://dx.doi.org/10.1038/cr.2014.56
  • Zukor H, Song W, Liberman A, Mui J, Vali H, Fillebeen C, Pantopoulos K, Wu TD, Guerquin-Kern JL, Schipper HM. HO-1-mediated macroautophagy: a mechanism for unregulated iron deposition in aging and degenerating neural tissues. J Neurochem 2009; 109:776-91; PMID:19250338; http://dx.doi.org/10.1111/j.1471-4159.2009.06007.x
  • Sakaida I, Kyle ME, Farber JL. Autophagic degradation of protein generates a pool of ferric iron required for the killing of cultured hepatocytes by an oxidative stress. Mol Pharmacol 1990; 37:435-42; PMID:2314391
  • Pullarkat V, Meng Z, Donohue C, Yamamoto VN, Tomassetti S, Bhatia R, Krishnan A, Forman SJ, Synold TW. Iron chelators induce autophagic cell death in multiple myeloma cells. Leuk Res 2014; 38:988-96; PMID:24998390; http://dx.doi.org/10.1016/j.leukres.2014.06.005
  • Chen CW, Chen TY, Tsai KL, Lin CL, Yokoyama KK, Lee WS, Chiueh CC, Hsu C. Inhibition of autophagy as a therapeutic strategy of iron-induced brain injury after hemorrhage. Autophagy 2012; 8:1510-20; PMID:22909970; http://dx.doi.org/10.4161/auto.21289
  • Soundravally R, Agieshkumar B, Daisy M, Sherin J, Cleetus CC. Ferritin levels predict severe dengue. Infection 2015; 43:13-19; PMID:25354733; http://dx.doi.org/10.1007/s15010-014-0683-4
  • Pandey R, Rodriguez GM. A ferritin mutant of Mycobacterium tuberculosis is highly susceptible to killing by antibiotics and is unable to establish a chronic infection in mice. Infect Immun 2012; 80:3650-9; PMID:22802345; http://dx.doi.org/10.1128/IAI.00229-12
  • Vardhan H, Bhengraj AR, Jha R, Singh Mittal A. Chlamydia trachomatis alters iron-regulatory protein-1 binding capacity and modulates cellular iron homeostasis in HeLa-229 cells. J Biomed Biotechnol 2009; 2009:342032; PMID:19688112; http://dx.doi.org/10.1155/2009/342032
  • Mittra B, Andrews NW. IRONy OF FATE: role of iron-mediated ROS in Leishmania differentiation. Trends Parasitol 2013; 29:489-96; PMID:23948431; http://dx.doi.org/10.1016/j.pt.2013.07.007
  • do Nascimento PR, Martins DR, Monteiro GR, Queiroz PV, Freire-Neto FP, Queiroz JW, Morais Lima AL, Jeronimo SM. Association of pro-inflammatory cytokines and iron regulatory protein 2 (IRP2) with Leishmania burden in canine visceral leishmaniasis. PloS One 2013; 8:e73873; PMID:24146743; http://dx.doi.org/10.1371/journal.pone.0073873
  • Mava Y, Ambe JP, Bello M, Watila I, Nottidge VA. Urinary tract infection in febrile children with sickle cell anaemia. West Afr J Med 2011; 30:268-72; PMID:22669831
  • Christopher GW. Escherichia coli bacteremia, meningitis, and hemochromatosis. Arch Intern Med 1985; 145:1908; PMID:3899040; http://dx.doi.org/10.1001/archinte.1985.00360100178031
  • Gordon S, Trinchieri G. Innate resistance and inflammation. Curr Opin Immunol 2009; 21:1-2; PMID:19223161; http://dx.doi.org/10.1016/j.coi.2009.02.001
  • Biasiotto G, Di Lorenzo D, Archetti S, Zanella I. Iron and neurodegeneration: is ferritinophagy the link? Mol Neurobiol 2015; 1-33; PMID:26468157; http://dx.doi.org/10.1007/s12035-015-9473-y
  • Kong XY, Nesset CK, Damme M, Løberg EM, Lübke T, Mæhlen J, Andersson KB, Lorenzo PI, Roos N, Thoresen GH, et al. Loss of lysosomal membrane protein NCU-G1 in mice results in spontaneous liver fibrosis with accumulation of lipofuscin and iron in Kupffer cells. Dis Model Mech 2014; 7:351-62; PMID:24487409; http://dx.doi.org/10.1242/dmm.014050
  • Dikshit N, Bist P, Fenlon SN, Pulloor NK, Chua CE, Scidmore MA, Carlyon JA, Tang BL, Chen SL, Sukumaran B. Intracellular uropathogenic E. coli exploits host Rab35 for iron acquisition and survival within urinary bladder cells. PLoS Pathog 2015; 11:e1005083; PMID:26248231; http://dx.doi.org/10.1371/journal.ppat.1005083
  • Puigserver, P. Part I Chapter 6: Signaling Transduction and Regulation of Cell Metabolism. (Hoffman R, Benz E, Silverstein L, Heslop H, Weitz J, Anastasi J, eds.) In Hematology: Basic Principles and Practices, 6th Edition. Philadelphia: Churchill Livingstone, 2012: 55–65.
  • Matsumoto T. Urinary tract infections in the elderly. Curr Urol Rep 2001; 2:330-3; PMID:12084261; http://dx.doi.org/10.1007/s11934-001-0073-1
  • Arshad M, Seed PC. Urinary tract infections in the infant. Clin Perinatol 2015; 42:17-28 vii; PMID:25677994; http://dx.doi.org/10.1016/j.clp.2014.10.003
  • Collard KJ. Iron homeostasis in the neonate. Pediatrics 2009; 123:1208-16; PMID:19336381; http://dx.doi.org/10.1542/peds.2008-1047
  • Pfrimer K, Micheletto RF, Marchini JS, Padovan GJ, Moriguti JC, Ferriolli E. Impact of aging on urinary excretion of iron and zinc. Nutr Metab Insights 2014; 7:47-50; PMID:24932105; http://dx.doi.org/10.4137/NMI.S12977
  • Detweiler K, Mayers D, Fletcher SG. Bacteruria and Urinary Tract Infections in the Elderly. Urol Clin North Am 2015; 42:561-8; PMID:26475952; http://dx.doi.org/10.1016/j.ucl.2015.07.002
  • Bishop BL, Duncan MJ, Song J, Li G, Zaas D, Abraham SN. Cyclic AMP-regulated exocytosis of Escherichia coli from infected bladder epithelial cells. Nat Med 2007; 13:625-30; PMID:17417648; http://dx.doi.org/10.1038/nm1572

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.