Correction: Wu et al., "Salmonella utilizes zinc to subvert antimicrobial host defense of macrophages via modulation of NF-κB signaling" [Infection and Immunity, 85, 12, (2017), (e00418-17)] doi: 10.1128/IAI.00418-17;Salmonella utilizes zinc to subvert antimicrobial host defense of macrophages via modulation of NF-κB signaling

Infection and Immunity

Volumn 85, Issue 12, 2017, Pages

  Wu, Aimin ^a,b   Tymoszuk, Piotr ^a   Haschka, David ^a   Heeke, Simon ^a   Dichtl, Stefanie ^a   Petzer, Verena ^a   Seifert, Markus ^a   Hilbe, Richard ^a   Sopper, Sieghart ^a   Talasz, Heribert ^a   Bumann, Dirk ^c   Lass Flörl, Cornelia ^a   Theurl, Igor ^a   Zhang, Keying ^b   Weiss, Guenter ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b SICHUAN AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Macrophages; NADPH oxidase; NF B; Nitric oxide synthase; Salmonella; Zinc

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; METALLOTHIONEIN I; METALLOTHIONEIN II; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ZINC; METALLOTHIONEIN; NOS2 PROTEIN, MOUSE; RELA PROTEIN, MOUSE; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIAL CLEARANCE; BACTERIAL GROWTH; BACTERIAL IMMUNITY; BACTERIAL SURVIVAL; CELL INVASION; CELL VIABILITY; CONTROLLED STUDY; EXTRACELLULAR SPACE; GENE DELETION; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNE RESPONSE; INFECTION CONTROL; INTRACELLULAR SIGNALING; MACROPHAGE; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAW 264.7 CELL LINE; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMISTRY; CYTOPLASM; DRUG EFFECT; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CYTOPLASM; MACROPHAGES; METALLOTHIONEIN; MICE; MICROBIAL VIABILITY; NITRIC OXIDE SYNTHASE TYPE II; RAW 264.7 CELLS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; ZINC;

EID: 85032432501     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00881-17     Document Type: Erratum

References (55)

1. Botella H, Peyron P, Levillain F, Poincloux R, Poquet Y, Brandli I, Wang C, Tailleux L, Tilleul S, Charriere GM, Waddell SJ, Foti M, Lugo-Villarino G, Gao Q, Maridonneau-Parini I, Butcher PD, Castagnoli PR, Gicquel B, de Chastellier C, Neyrolles O. 2011. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10:248-259. https://doi.org/10.1016/j.chom.2011.08.006
2. Weiss G, Schaible UE. 2015. Macrophage defense mechanisms against intracellular bacteria. Immunol Rev 264:182-203. https://doi.org/10.1111/imr.12266
3. Nairz M, Fritsche G, Brunner P, Talasz H, Hantke K, Weiss G. 2008. Interferon-gamma limits the availability of iron for intramacrophage Salmonella Typhimurium. Eur J Immunol 38:1923-1936. https://doi.org/ 10.1002/eji.200738056
4. Hood MI, Skaar EP. 2012. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10:525-537. https://doi.org/ 10.1038/nrmicro2836
5. Porcheron G, Garenaux A, Proulx J, Sabri M, Dozois CM. 2013. Iron, copper, zinc, and manganese transport and regulation in pathogenic enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence. Front Cell Infect Microbiol 3:90. https://doi.org/10.3389/fcimb.2013.00090
6. Carver PL. 2013. Metal ions and infectious diseases. An overview from the clinic. Met Ions Life Sci 13:1-28. https://doi.org/10.1007/978-94-007-7500-8_1
7. Drakesmith H, Prentice AM. 2012. Hepcidin and the iron-infection axis. Science 338:768-772. https://doi.org/10.1126/science.1224577
8. Ganz T, Nemeth E. 2015. Iron homeostasis in host defence and inflammation. Nat Rev Immunol 15:500-510. https://doi.org/10.1038/nri3863
9. Soares MP, Weiss G. 2015. The Iron Age of host-microbe interactions. EMBO Rep 16:1482-1500. https://doi.org/10.15252/embr.201540558
10. Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M, Kehl-Fie TE, Restrepo NA, Hosking MP, Edwards RA, Battistoni A, Pasquali P, Lane TE, Chazin WJ, Vogl T, Roth J, Skaar EP, Raffatellu M. 2012. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11:227-239. https://doi.org/10.1016/j.chom.2012.01.017
11. Haase H, Rink L. 2014. Multiple impacts of zinc on immune function. Metallomics 6:1175-1180. https://doi.org/10.1039/c3mt00353a
12. Subramanian Vignesh K, Landero Figueroa JA, Porollo A, Caruso JA, Deepe GS, Jr. 2013. Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. Immunity 39:697-710. https://doi.org/10.1016/j.immuni.2013.09.006
13. Wagner D, Maser J, Lai B, Cai Z, Barry CE, III, Honer Zu Bentrup K, Russell DG, Bermudez LE. 2005. Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatiscontaining phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J Immunol 174: 1491-1500. https://doi.org/10.4049/jimmunol.174.3.1491
14. Van Ho A, Ward DM, Kaplan J. 2002. Transition metal transport in yeast. Annu Rev Microbiol 56:237-261. https://doi.org/10.1146/annurev.micro.56.012302.160847
15. Weiss G, Carver PL. Role of divalent metals in infectious disease susceptibility and outcome. Clin Microbiol Infect, in press
16. Nairn BL, Lonergan ZR, Wang J, Braymer JJ, Zhang Y, Calcutt MW, Lisher JP, Gilston BA, Chazin WJ, de Crecy-Lagard V, Giedroc DP, Skaar EP. 2016. The response of Acinetobacter baumannii to zinc starvation. Cell Host Microbe 19:826-836. https://doi.org/10.1016/j.chom.2016.05.007
17. Soofi S, Cousens S, Iqbal SP, Akhund T, Khan J, Ahmed I, Zaidi AKM, Bhutta ZA. 2013. Effect of provision of daily zinc and iron with several micronutrients on growth and morbidity among young children in Pakistan: a cluster-randomised trial. Lancet 382:29-40. https://doi.org/ 10.1016/S0140-6736(13)60437-7
18. Zackular JP, Moore JL, Jordan AT, Juttukonda LJ, Noto MJ, Nicholson MR, Crews JD, Semler MW, Zhang Y, Ware LB, Washington MK, Chazin WJ, Caprioli RM, Skaar EP. 2016. Dietary zinc alters the microbiota and decreases resistance to Clostridium difficile infection. Nat Med 22: 1330-1334. https://doi.org/10.1038/nm.4174
19. Prasad AS, Beck FW, Kaplan J, Chandrasekar PH, Ortega J, Fitzgerald JT, Swerdlow P. 1999. Effect of zinc supplementation on incidence of infections and hospital admissions in sickle cell disease (SCD). Am J Hematol 61:194-202
20. Man SM, Ekpenyong A, Tourlomousis P, Achouri S, Cammarota E, Hughes K, Rizzo A, Ng G, Wright JA, Cicuta P, Guck JR, Bryant CE. 2014. Actin polymerization as a key innate immune effector mechanism to control Salmonella infection. Proc Natl Acad Sci U S A 111:17588-17593. https://doi.org/10.1073/pnas.1419925111
21. Behnsen J, Perez-Lopez A, Nuccio S-P, Raffatellu M. 2015. Exploiting host immunity: the Salmonella paradigm. Trends Immunol 36:112-120. https://doi.org/10.1016/j.it.2014.12.003
22. Andrews-Polymenis HL, Baumler AJ, McCormick BA, Fang FC. 2010. Taming the elephant: Salmonella biology, pathogenesis, and prevention. Infect Immun 78:2356-2369. https://doi.org/10.1128/IAI.00096-10
23. Nairz M, Schleicher U, Schroll A, Sonnweber T, Theurl I, Ludwiczek S, Talasz H, Brandacher G, Moser PL, Muckenthaler MU, Fang FC, Bogdan C, Weiss G. 2013. Nitric oxide-mediated regulation of ferroportin-1 controls macrophage iron homeostasis and immune function in Salmonella infection. J Exp Med 210:855-873. https://doi.org/10.1084/jem.20121946
24. Nairz M, Ferring-Appel D, Casarrubea D, Sonnweber T, Viatte L, Schroll A, Haschka D, Fang FC, Hentze MW, Weiss G, Galy B. 2015. Iron regulatory proteins mediate host resistance to Salmonella infection. Cell Host Microbe 18:254-261. https://doi.org/10.1016/j.chom.2015.06.017
25. Fang FC. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99: 2818-2825. https://doi.org/10.1172/JCI119473
26. van der Heijden J, Bosman ES, Reynolds LA, Finlay BB. 2014. Direct measurement of oxidative and nitrosative stress dynamics in Salmonella inside macrophages. Proc Natl Acad Sci U S A 112:560-565. https://doi.org/10.1073/pnas.1414569112
27. Fang FC. 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2:820-832. https://doi.org/10.1038/nrmicro1004
28. Burton NA, Schürmann N, Casse O, Steeb AK, Claudi B, Zankl J, Schmidt A, Bumann D. 2014. Disparate impact of oxidative host defenses determines the fate of Salmonella during systemic infection in mice. Cell Host Microbe 15:72-83. https://doi.org/10.1016/j.chom.2013.12.006
29. Chakravortty D, Hansen-Wester I, Hensel M. 2002. Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med 195:1155-1166. https://doi.org/10.1084/jem.20011547
30. Haraga A, Ohlson MB, Miller SI. 2008. Salmonellae interplay with host cells. Nat Rev Microbiol 6:53-66. https://doi.org/10.1038/nrmicro1788
31. De Groote MA, Ochsner UA, Shiloh MU, Nathan C, McCord JM, Dinauer MC, Libby SJ, Vazquez-Torres A, Xu Y, Fang FC. 1997. Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci U S A 94:13997-14001. https://doi.org/10.1073/pnas.94.25.13997
32. Cerasi M, Ammendola S, Battistoni A. 2013. Competition for zinc binding in the host-pathogen interaction. Front Cell Infect Microbiol 3:108. https://doi.org/10.3389/fcimb.2013.00108
33. Palacios O, Atrian S, Capdevila M. 2011. Zn-and Cu-thioneins: a functional classification for metallothioneins? J Biol Inorg Chem 16:991-1009. https://doi.org/10.1007/s00775-011-0827-2
34. Cho Y-E, Lomeda R-AR, Ryu S-H, Lee J-H, Beattie JH, Kwun I-S. 2007. Cellular Zn depletion by metal ion chelators (TPEN, DTPA and chelex resin) and its application to osteoblastic MC3T3-E1 cells. Nutr Res Pract 1:29-35. https://doi.org/10.4162/nrp.2007.1.1.29
35. DiDonato JA, Mercurio F, Karin M. 2012. NF-kappaB and the link between inflammation and cancer. Immunol Rev 246:379-400. https://doi.org/10.1111/j.1600-065X.2012.01099.x
36. Fang FC. 2011. Antimicrobial actions of reactive oxygen species. mBio 2:e00141-11. https://doi.org/10.1128/mBio.00141-11
37. Shiloh MU, Nathan CF. 2000. Reactive nitrogen intermediates and the pathogenesis of Salmonella and mycobacteria. Curr Opin Microbiol 3:35-42. https://doi.org/10.1016/S1369-5274(99)00048-X
38. Cichon MA, Radisky DC. 2014. ROS-induced epithelial-mesenchymal transition in mammary epithelial cells is mediated by NF-kB-dependent activation of Snail. Oncotarget 5:2827-2838. https://doi.org/10.18632/ oncotarget.1940
39. Liu J, Du L. 2015. PERK pathway is involved in oxygen-glucose-serum deprivation-induced NF-kB activation via ROS generation in spinal cord astrocytes. Biochem Biophys Res Commun 467:197-203. https://doi.org/ 10.1016/j.bbrc.2015.10.007
40. von Bulow V, Dubben S, Engelhardt G, Hebel S, Plumakers B, Heine H, Rink L, Haase H. 2007. Zinc-dependent suppression of TNF-alpha production is mediated by protein kinase A-induced inhibition of Raf-1, I kappa B kinase beta, and NF-kappa B. J Immunol 179:4180-4186. https://doi.org/10.4049/jimmunol.179.6.4180
41. Haase H, Ober-Blobaum JL, Engelhardt G, Hebel S, Heit A, Heine H, Rink L. 2008. Zinc signals are essential for lipopolysaccharide-induced signal transduction in monocytes. J Immunol 181:6491-6502. https://doi.org/ 10.4049/jimmunol.181.9.6491
42. Liu M-J, Bao S, Galvez-Peralta M, Pyle CJ, Rudawsky AC, Pavlovicz RE, Killilea DW, Li C, Nebert DW, Wewers MD, Knoell DL. 2013. ZIP8 regulates host defense through zinc-mediated inhibition of NF-kappaB. Cell Rep 3:386-400. https://doi.org/10.1016/j.celrep.2013.01.009
43. Brieger A, Rink L, Haase H. 2013. Differential regulation of TLRdependent MyD88 and TRIF signaling pathways by free zinc ions. J Immunol 191:1808-1817. https://doi.org/10.4049/jimmunol.1301261
44. Bao S, Liu M-J, Lee B, Besecker B, Lai J-P, Guttridge DC, Knoell DL. 2010. Zinc modulates the innate immune response in vivo to polymicrobial sepsis through regulation of NF-kappaB. Am J Physiol Lung Cell Mol Physiol 298:L744-L754. https://doi.org/10.1152/ajplung.00368.2009
45. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP, Ma A. 2000. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 289:2350-2354. https://doi.org/10.1126/ science.289.5488.2350
46. Prasad AS, Bao B, Beck FWJ, Sarkar FH. 2011. Zinc-suppressed inflammatory cytokines by induction of A20-mediated inhibition of nuclear factor-kappaB. Nutrition 27:816-823. https://doi.org/10.1016/j.nut.2010.08.010
47. Coyle P, Philcox JC, Carey LC, Rofe AM. 2002. Metallothionein: the multipurpose protein. Cell Mol Life Sci 59:627-647. https://doi.org/10.1007/s00018-002-8454-2
48. Zhou Z, Wang L, Song Z, Saari JT, McClain CJ, Kang YJ. 2004. Abrogation of nuclear factor-kappaB activation is involved in zinc inhibition of lipopolysaccharide-induced tumor necrosis factor-alpha production and liver injury. Am J Pathol 164:1547-1556. https://doi.org/10.1016/S0002-9440(10)63713-3
49. Thone F, Schwanhausser B, Becker D, Ballmaier M, Bumann D. 2007. FACS-isolation of Salmonella-infected cells with defined bacterial load from mouse spleen. J Microbiol Methods 71:220-224. https://doi.org/10.1016/j.mimet.2007.08.016
50. Barat S, Willer Y, Rizos K, Claudi B, Maze A, Schemmer AK, Kirchhoff D, Schmidt A, Burton N, Bumann D. 2012. Immunity to intracellular Salmonella depends on surface-associated antigens. PLoS Pathog 8:e1002966. https://doi.org/10.1371/journal.ppat.1002966
51. Nairz M, Schroll A, Haschka D, Dichtl S, Sonnweber T, Theurl I, Theurl M, Lindner E, Demetz E, Aßhoff M, Bellmann-Weiler R, Müller R, Gerner RR, Moschen AR, Baumgartner N, Moser PL, Talasz H, Tilg H, Fang FC, Weiss G. 2015. Lipocalin-2 ensures host defense against Salmonella Typhimurium by controlling macrophage iron homeostasis and immune response. Eur J Immunol 45:3073-3086. https://doi.org/10.1002/eji.201545569
52. Theurl I, Mattle V, Seifert M, Mariani M, Marth C, Weiss G. 2006. Dysregulated monocyte iron homeostasis and erythropoietin formation in patients with anemia of chronic disease. Blood 107:4142-4148. https:// doi.org/10.1182/blood-2005-08-3364
53. Cho SW, Kim S, Kim JM, Kim J-S. 2013. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31:230-232. https://doi.org/10.1038/nbt.2507
54. Ran FA, Hsu PD, Lin C-Y, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380-1389. https://doi.org/10.1016/j.cell.2013.08.021
55. Sanjana NE, Shalem O, Zhang F. 2014. Improved vectors and genomewide libraries for CRISPR screening. Nat Methods 11:783-784. https:// doi.org/10.1038/nmeth.3047