Salmonella employs multiple mechanisms to subvert the TLR-inducible zinc-mediated antimicrobial response of human macrophages

FASEB Journal

Volumn 30, Issue 5, 2016, Pages 1901-1912

  Kapetanovic, Ronan ^a,b   Bokil, Nilesh J ^a,b   Achard, Maud E S ^a   Ong, Cheryl Lynn Y ^a   Peters, Kate M ^a   Stocks, Claudia J ^a,b   Phan, Minh Duy ^a   Monteleone, Mercedes ^a,b   Schroder, Kate ^a,b   Irvine, Katharine M ^a,b   Saunders, Bernadette M ^c   Walker, Mark J ^a   Stacey, Katryn J ^a   McEwan, Alastair G ^a   Schembri, Mark A ^a   Sweet, Matthew J ^a,b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b IMB Centre for Inflammation and Disease Research   (Australia)

^c UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

Bacterial pathogens; Innate immunity; Metal ions; Trafficking pathways

Indexed keywords

COPPER; ZINC; BACTERIAL PROTEIN; BACTERIAL RNA; MESSENGER RNA; SPI1 PROTEIN, SALMONELLA; TOLL LIKE RECEPTOR;

ARTICLE; BACTERIAL CLEARANCE; BACTERIAL IMMUNITY; BACTERIUM MUTANT; CELLULAR STRESS RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ESCHERICHIA COLI; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNE EVASION; INNATE IMMUNITY; MACROPHAGE; MASS SPECTROMETRY; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA PATHOGENICITY ISLAND 1; SIGNAL TRANSDUCTION; CELL CULTURE; CELL LINE; CHEMISTRY; CYTOPLASM VESICLE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SALMONELLA;

BACTERIAL PROTEINS; CELL LINE; CELLS, CULTURED; COPPER; CYTOPLASMIC VESICLES; GENE EXPRESSION REGULATION, BACTERIAL; MACROPHAGES; RNA, BACTERIAL; RNA, MESSENGER; SALMONELLA; SALMONELLA TYPHIMURIUM; TOLL-LIKE RECEPTORS; ZINC;

EID: 84966340121     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201500061     Document Type: Article

References (64)

1. Sweet, M. J., and Bokil, N. J. (2010) The role of monocytes and macrophages innate immunity: Macrophage anti-microbial pathways. In Regulation of Innate Immune Function (Marsh, C. B., Tridandapani, S., and and Piper, M. G., eds.), pp. 1-31, Research Signpost, Trivandrum, India
2. Flannagan, R. S., Cosío, G., and Grinstein, S. (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7,355-366
3. Nairz, M., Schroll, A., Sonnweber, T., and Weiss, G. (2010) The struggle for iron - a metal at the host-pathogen interface. Cell. Microbiol. 12, 1691-1702
4. Schaible, U. E., and Kaufmann, S. H. (2004) Iron and microbial infection. Nat. Rev. Microbiol. 2, 946-953
5. Hodgkinson, V., and Petris, M. J. (2012) Copper homeostasis at the host-pathogen interface. J. Biol. Chem. 287, 13549-13555
6. Hood, M. I., and Skaar, E. P. (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10, 525-537
7. Samanovic, M. I., Ding, C., Thiele, D. J., and Darwin, K. H. (2012) Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe 11, 106-115
8. Stafford,S.L.,Bokil,N.J.,Achard,M.E.,Kapetanovic,R.,Schembri, M. A., McEwan, A. G., and Sweet, M. J. (2013) Metal ions in macrophage antimicrobial pathways: emerging roles for zinc and copper. Biosci. Rep. 33, pii: e00049
9. Behnsen, J., Perez-Lopez, A., Nuccio, S. P., and Raffatellu, M. (2015) Exploiting host immunity: the Salmonella paradigm. Trends Immunol. 36,112-120
10. Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., Jones, J. L., and Griffin, P. M. (2011) Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17,7-15
11. Majowicz, S. E., Musto, J., Scallan, E., Angulo, F. J., Kirk, M., O'Brien, S. J., Jones, T. F., Fazil, A., and Hoekstra, R. M.; International Collaboration on Enteric Disease 'Burden of Illness' Studies (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50, 882-889
12. Wardlaw, T., Salama, P., Brocklehurst, C., Chopra, M., and Mason, E. (2010) Diarrhoea: why children are still dying and what can be done. Lancet 375,870-872
13. Bhandari, N., Mazumder, S., Taneja, S., Dube, B., Agarwal, R. C., Mahalanabis, D., Fontaine, O., Black, R. E., and Bhan, M. K. (2008) Effectiveness of zinc supplementation plus oral rehydration salts compared with oral rehydration salts alone as a treatment for acute diarrhea in a primary care setting: a cluster randomized trial. Pediatrics 121, e1279-e1285
14. Lukacik, M., Thomas, R. L., and Aranda, J. V. (2008) A meta-analysis of the effects of oral zinc in the treatment of acute and persistent diarrhea. Pediatrics 121,326-336
15. Bhutta, Z. A., Black, R. E., Brown, K. H., Gardner, J. M., Gore, S., Hidayat, A., Khatun, F., Martorell, R., Ninh, N. X., Penny, M. E., Rosado, J. L., Roy, S. K., Ruel, M., Sazawal, S., and Shankar, A. (1999) Prevention of diarrhea and pneumonia by zinc supplementation in children in developing countries: pooled analysis of randomized controlled trials. Zinc Investigators' Collaborative Group. J. Pediatr. 135,689-697
16. Valavi, E., Hakimzadeh, M., Shamsizadeh, A., Aminzadeh, M., and Alghasi, A. (2011) The efficacy of zinc supplementation on outcome of children with severe pneumonia. A randomized double-blind placebo-controlled clinical trial. Indian J. Pediatr. 78, 1079-1084
17. Prasad, A. S. (2012) Discovery of human zinc deficiency: 50 years later. J. Trace Elem. Med. Biol. 26, 66-69
18. Prasad, A. S. (2008) Zinc in human health: effect of zinc on immune cells. Mol. Med. 14, 353-357
19. Bao, S., Liu, M. J., Lee, B., Besecker, B., Lai, J. P., Guttridge, D. C., and Knoell, D. L. (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
20. Knoell, D. L., Julian, M. W., Bao, S., Besecker, B., Macre, J. E., Leikauf, G. D., DiSilvestro, R. A., and Crouser, E. D. (2009) Zinc deficiency increases organ damage and mortality in a murine model of polymicrobial sepsis. Crit. Care Med. 37,1380-1388
21. Nowak, J. E., Harmon, K., Caldwell, C. C., and Wong, H. R. (2012) Prophylactic zinc supplementation reduces bacterial load and improves survival in a murine model of sepsis. Pediatr. Crit. Care Med. 13, e323-329
22. Liu, M. J., Bao, S., Gálvez-Peralta, M., Pyle, C. J., Rudawsky, A. C., Pavlovicz, R. E., Killilea, D. W., Li, C., Nebert, D. W., Wewers, M. D., and Knoell, D. L. (2013) ZIP8 regulates host defense through zincmediated inhibition of NF-kB. Cell Rep. 3, 386-400
23. Haase, H., Ober-Blöbaum, J. L., Engelhardt, G., Hebel, S., Heit, A., Heine, H., and Rink, L. (2008) Zinc signals are essential for lipopolysaccharide-induced signal transduction in monocytes. J. Immunol. 181, 6491-6502
24. Brieger, A., Rink, L., and Haase, H. (2013) Differential regulation of TLR-dependent MyD88 and TRIF signaling pathways by free zinc ions. J. Immunol. 191, 1808-1817
25. McDevitt,C.A.,Ogunniyi,A.D.,Valkov,E.,Lawrence,M.C.,Kobe, B., McEwan, A. G., and Paton, J. C. (2011) A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog. 7, e1002357
26. Eijkelkamp, B. A., Morey, J. R., Ween, M. P., Ong, C. L., McEwan, A. G., Paton, J. C., and McDevitt, C. A. (2014) Extracellular zinc competitively inhibits manganese uptake and compromises oxidative stress management in Streptococcus pneumoniae. PLoS One 9,e89427
27. Ong, C. L., Walker, M. J., and McEwan, A. G. (2015) Zinc disrupts central carbon metabolism and capsule biosynthesis in Streptococcus pyogenes. Sci. Rep. 5, 10799
28. Ong, C. L., Gillen, C. M., Barnett, T. C., Walker, M. J., and McEwan, A. G. (2014) An antimicrobial role for zinc in innate immune defense against group A streptococcus. J. Infect. Dis. 209, 1500-1508
29. Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I.,Wang,C.,Tailleux,L.,Tilleul,S.,Charrière, G. M., Waddell, S. J., Foti, M., Lugo-Villarino, G., Gao, Q., Maridonneau-Parini, I., Butcher, P. D., Castagnoli, P. R., Gicquel, B., de Chastellier, C., and Neyrolles, O. (2011) Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10, 248-259
30. Mayer,L.S.,Uciechowski,P.,Meyer,S.,Schwerdtle,T.,Rink,L.,and Haase, H. (2014) Differential impact of zinc deficiency on phagocytosis, oxidative burst, and production of pro-inflammatory cytokines by human monocytes. Metallomics 6, 1288-1295
31. Subramanian Vignesh, K., Landero Figueroa, J. A., Porollo, A., Caruso, J. A., and Deepe, G. S., Jr. (2013) Granulocyte macrophagecolony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. Immunity 39,697-710
32. Diaz-Ochoa,V.E.,Jellbauer,S.,Klaus,S.,andRaffatellu,M.(2014) Transition metal ions at the crossroads of mucosal immunity and microbial pathogenesis. Front. Cell. Infect. Microbiol. 4, 2
33. Hoiseth, S. K., and Stocker, B. A. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291,238-239
34. Galán, J. E., and Curtiss III, R. (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 86, 6383-6387
35. Blattner, F. R., Plunkett III, G., Bloch, C. A., Perna, N. T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J. D., Rode, C. K., Mayhew, G. F., Gregor, J., Davis, N. W., Kirkpatrick, H. A., Goeden, M. A., Rose, D. J., Mau, B., and Shao, Y. (1997) The complete genome sequence of Escherichia coli K-12. Science 277, 1453-1462
36. Totsika, M., Beatson, S. A., Sarkar, S., Phan, M. D., Petty, N. K., Bachmann, N., Szubert, M., Sidjabat, H. E., Paterson, D. L., Upton, M., and Schembri, M. A. (2011) Insights into a multidrug resistant Escherichia coli pathogen of the globally disseminated ST131 lineage: genome analysis and virulence mechanisms. PLoS One 6, e26578
37. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97, 6640-6645
38. Wang, R. F., and Kushner, S. R. (1991) Construction of versatile lowcopy-number vectors for cloning, sequencing and geneexpression in Escherichia coli. Gene 100, 195-199
39. Allsopp, L. P., Beloin, C., Ulett, G. C., Valle, J., Totsika, M., Sherlock, O., Ghigo, J. M., and Schembri, M. A. (2012) Molecular characterization of UpaB and UpaC, two new autotransporter proteins of uropathogenic Escherichia coli CFT073. Infect. Immun. 80, 321-332
40. Phan, M. D., Peters, K. M., Sarkar, S., Lukowski, S. W., Allsopp, L. P., Gomes Moriel, D., Achard, M. E., Totsika, M., Marshall, V. M., Upton, M., Beatson, S. A., and Schembri, M. A. (2013) The serum resistome of a globally disseminated multidrug resistant uropathogenic Escherichia coli clone. PLoS Genet. 9, e1003834
41. Bokil, N. J., Totsika, M., Carey, A. J., Stacey, K. J., Hancock, V., Saunders, B. M., Ravasi, T., Ulett, G. C., Schembri, M. A., and Sweet, M. J. (2011) Intramacrophage survival of uropathogenic Escherichia coli: differences between diverse clinical isolates and between mouse and human macrophages. Immunobiology 216,1164-1171
42. Lundberg, U., Vinatzer, U., Berdnik, D., von Gabain, A., and Baccarini, M. (1999) Growth phase-regulated induction of Salmonella-induced macrophage apoptosis correlates with transient expression of SPI-1 genes. J. Bacteriol. 181, 3433-3437
43. Monack, D. M., Raupach, B., Hromockyj, A. E., and Falkow, S. (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93, 9833-9838
44. Achard, M. E., Stafford, S. L., Bokil, N. J., Chartres, J., Bernhardt, P. V., Schembri, M. A., Sweet, M. J., and McEwan, A. G. (2012) Copper redistribution in murine macrophages in response to Salmonella infection. Biochem. J. 444, 51-57
45. Gee, K. R., Zhou, Z. L., Qian, W. J., and Kennedy, R. (2002) Detection and imaging of zinc secretion from pancreatic beta-cells using a new fluorescent zinc indicator. J. Am. Chem. Soc. 124,776-778
46. Coyle, P., Zalewski, P. D., Philcox, J. C., Forbes, I. J., Ward, A. D., Lincoln, S. F., Mahadevan, I., and Rofe, A. M. (1994) Measurement of zinc in hepatocytes by using a fluorescent probe, zinquin: relationship tometallothionein and intracellular zinc. Biochem. J. 303, 781-786
47. Schroder, K., Irvine, K. M., Taylor, M. S., Bokil, N. J., Le Cao, K. A., Masterman, K. A., Labzin, L. I., Semple, C. A., Kapetanovic, R., Fairbairn, L., Akalin, A., Faulkner, G. J., Baillie, J. K., Gongora, M., Daub, C. O., Kawaji, H., McLachlan, G. J., Goldman, N., Grimmond, S. M., Carninci, P., Suzuki, H., Hayashizaki, Y., Lenhard, B., Hume, D. A., and Sweet, M. J. (2012) Conservation and divergence in Tolllike receptor 4-regulated gene expression in primary human versus mouse macrophages. Proc. Natl. Acad. Sci. USA 109, E944-E953
48. Yamamoto, K., and Ishihama, A. (2005) Transcriptional response of Escherichia coli to external zinc. J. Bacteriol. 187, 6333-6340
49. Rensing, C., Mitra, B., and Rosen, B. P. (1997) The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc. Natl. Acad. Sci. USA 94, 14326-14331
50. Dieye, Y., Ameiss, K., Mellata, M., and Curtiss III, R. (2009) The Salmonella Pathogenicity Island (SPI) 1 contributes more than SPI2 to the colonization of the chicken by Salmonella enterica serovar Typhimurium. BMC Microbiol. 9, 3
51. Giacomodonato, M. N., Uzzau, S., Bacciu, D., Caccuri, R., Sarnacki, S. H., Rubino, S., and Cerquetti, M. C. (2007) SipA, SopA, SopB, SopD and SopE2 effector proteins of Salmonella enterica serovar Typhimurium are synthesized at late stages of infection in mice. Microbiology 153,1221-1228
52. Brawn, L. C., Hayward, R. D., and Koronakis, V. (2007) Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe 1,63-75
53. Pérez, J. M., Pradeñas, G. A., Navarro, C. A., Henríquez, D. R., Pichuantes, S. E., and Vásquez, C. C. (2006) Geobacillus stearothermophilus LV cadA gene mediates resistance to cadmium, lead and zinc in zntA mutants of Salmonella entérica serovar Typhimurium. Biol. Res. 39,661-668
54. Miller, E. W., Zeng, L., Domaille, D. W., and Chang, C. J. (2006) Preparation and use of Coppersensor-1, a synthetic fluorophore for live-cell copper imaging. Nat. Protoc. 1, 824-827
55. Liu, J. Z., Jellbauer, S., Poe, A. J., Ton, V., Pesciaroli, M., Kehl-Fie, T. E., Restrepo, N. A., Hosking, M. P., Edwards, R. A., Battistoni, A., Pasquali, P., Lane, T. E., Chazin, W. J., Vogl, T., Roth, J., Skaar, E. P., and Raffatellu, M. (2012) Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11, 227-239
56. Cerasi,M.,Liu,J.Z.,Ammendola,S.,Poe,A.J.,Petrarca,P.,Pesciaroli, M., Pasquali, P., Raffatellu, M., and Battistoni, A. (2014) The ZupT transporter plays an important role in zinc homeostasis and contributes to Salmonella enterica virulence. Metallomics 6, 845-853
57. Wagner, D., Maser, J., Lai, B., Cai, Z., Barry III, C. E., Höner Zu Bentrup, K., Russell, D. G., and Bermudez, L. E. (2005) Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomalsystem.J. Immunol. 174,1491-1500
58. Stähler, F. N., Odenbreit, S., Haas, R., Wilrich, J., Van Vliet, A. H., Kusters, J. G., Kist, M., and Bereswill, S. (2006) The novel Helicobacter pylori CznABC metal efflux pump is required for cadmium, zinc, and nickel resistance, urease modulation, and gastric colonization. Infect. Immun. 74, 3845-3852
59. Van der Heijden, J., and Finlay, B. B. (2012) Type III effectormediated processes in Salmonella infection. Future Microbiol. 7, 685-703
60. Zhou, D., Chen, L. M., Hernandez, L., Shears, S. B., and Galán, J. E. (2001) A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 39, 248-259
61. Kitamura, H., Morikawa, H., Kamon, H., Iguchi, M., Hojyo, S., Fukada, T., Yamashita, S., Kaisho, T., Akira, S., Murakami, M., and Hirano, T. (2006) Toll-like receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat. Immunol. 7, 971-977
62. Dineley, K. E., Votyakova, T. V., and Reynolds, I. J. (2003) Zinc inhibition of cellular energy production: implications for mitochondria and neurodegeneration. J. Neurochem. 85, 563-570
63. Irving, H., and Williams, R. J. P. (1953) The stability of transitionmetal complexes. J. Chem. Soc.3192-3210
64. Xu, F. F., and Imlay, J. A. (2012) Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli. Appl. Environ. Microbiol. 78, 3614-3621