IL-4 Induces Metallothionein 3- and SLC30A4-Dependent Increase in Intracellular Zn2+ that Promotes Pathogen Persistence in Macrophages

Cell Reports

Volumn 16, Issue 12, 2016, Pages 3232-3246

  Subramanian Vignesh, Kavitha ^a   Landero Figueroa, Julio A ^b   Porollo, Aleksey ^c   Divanovic, Senad ^c   Caruso, Joseph A ^b   Deepe, George S ^a,d  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 4; METALLOTHIONEIN III; STAT6 PROTEIN; ZINC ION; CATION TRANSPORT PROTEIN; GROWTH INHIBITOR; NERVE PROTEIN; SLC30A4 PROTEIN, HUMAN; ZINC;

ANIMAL CELL; ARTICLE; CELL EXPANSION; CELL LEVEL; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ZINC HOMEOSTASIS; ANIMAL; HISTOPLASMOSIS; IMMUNOLOGY; MACROPHAGE; MACROPHAGE ACTIVATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; CATION TRANSPORT PROTEINS; HISTOPLASMOSIS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERLEUKIN-4; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; NERVE TISSUE PROTEINS; ZINC;

EID: 84991327486     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.08.057     Document Type: Article

References (35)

1. Allendoerfer, R., Deepe, G.S. Jr., Intrapulmonary response to Histoplasma capsulatum in gamma interferon knockout mice. Infect. Immun. 65 (1997), 2564–2569.
2. Balce, D.R., Li, B., Allan, E.R., Rybicka, J.M., Krohn, R.M., Yates, R.M., Alternative activation of macrophages by IL-4 enhances the proteolytic capacity of their phagosomes through synergistic mechanisms. Blood 118 (2011), 4199–4208.
3. Citiulo, F., Jacobsen, I.D., Miramón, P., Schild, L., Brunke, S., Zipfel, P., Brock, M., Hube, B., Wilson, D., Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog., 8, 2012, e1002777.
4. Ding, Z.C., Ni, F.Y., Huang, Z.X., Neuronal growth-inhibitory factor (metallothionein-3): structure-function relationships. FEBS J. 277 (2010), 2912–2920.
5. El Chartouni, C., Schwarzfischer, L., Rehli, M., Interleukin-4 induced interferon regulatory factor (Irf) 4 participates in the regulation of alternative macrophage priming. Immunobiology 215 (2010), 821–825.
6. 2+ in cells. Metallomics 6 (2014), 301–315.
7. Gocheva, V., Wang, H.W., Gadea, B.B., Shree, T., Hunter, K.E., Garfall, A.L., Berman, T., Joyce, J.A., IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 24 (2010), 241–255.
8. Gruber, K., Maywald, M., Rosenkranz, E., Haase, H., Plumakers, B., Rink, L., Zinc deficiency adversely influences interleukin-4 and interleukin-6 signaling. J. Biol. Regul. Homeost. Agents 27 (2013), 661–671.
9. Haase, H., Rink, L., Zinc signals and immune function. Biofactors 40 (2014), 27–40.
10. Haase, H., Ober-Blöbaum, J.L., Engelhardt, G., Hebel, S., Heit, A., Heine, H., Rink, L., Zinc signals are essential for lipopolysaccharide-induced signal transduction in monocytes. J. Immunol. 181 (2008), 6491–6502.
11. Harris, J., De Haro, S.A., Master, S.S., Keane, J., Roberts, E.A., Delgado, M., Deretic, V., T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity 27 (2007), 505–517.
12. Hennigar, S.R., Kelleher, S.L., TNFα Post-Translationally Targets ZnT2 to Accumulate Zinc in Lysosomes. J. Cell. Physiol. 230 (2015), 2345–2350.
13. Hood, M.I., Skaar, E.P., Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10 (2012), 525–537.
14. Jacob, C., Maret, W., Vallee, B.L., Control of zinc transfer between thionein, metallothionein, and zinc proteins. Proc. Natl. Acad. Sci. U S A 95 (1998), 3489–3494.
15. Kahnert, A., Seiler, P., Stein, M., Bandermann, S., Hahnke, K., Mollenkopf, H., Kaufmann, S.H., Alternative activation deprives macrophages of a coordinated defense program to Mycobacterium tuberculosis. Eur. J. Immunol. 36 (2006), 631–647.
16. Lee, S.J., Koh, J.Y., Roles of zinc and metallothionein-3 in oxidative stress-induced lysosomal dysfunction, cell death, and autophagy in neurons and astrocytes. Mol. Brain, 3, 2010, 30.
17. Leopold Wager, C.M., Wormley, F.L. Jr., Classical versus alternative macrophage activation: the Ying and the Yang in host defense against pulmonary fungal infections. Mucosal Immunol. 7 (2014), 1023–1035.
18. Li, Y., Maret, W., Human metallothionein metallomics. J. Anal. At. Spectrom. 23 (2008), 1055–1062.
19. 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., et al. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11 (2012), 227–239.
20. McCormick, N.H., Kelleher, S.L., ZnT4 provides zinc to zinc-dependent proteins in the trans-Golgi network critical for cell function and Zn export in mammary epithelial cells. Am. J. Physiol. Cell Physiol. 303 (2012), C291–C297.
21. McKim, J.M. Jr., Choudhuri, S., Klaassen, C.D., In vitro degradation of apo-, zinc-, and cadmium-metallothionein by cathepsins B, C, and D. Toxicol. Appl. Pharmacol. 116 (1992), 117–124.
22. Mosser, D.M., The many faces of macrophage activation. J. Leukoc. Biol. 73 (2003), 209–212.
23. Mosser, D.M., Edwards, J.P., Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8 (2008), 958–969.
24. Müller, S., Faulhaber, A., Sieber, C., Pfeifer, D., Hochberg, T., Gansz, M., Deshmukh, S.D., Dauth, S., Brix, K., Saftig, P., et al. The endolysosomal cysteine cathepsins L and K are involved in macrophage-mediated clearance of Staphylococcus aureus and the concomitant cytokine induction. FASEB J. 28 (2014), 162–175.
25. Murray, P.J., Allen, J.E., Biswas, S.K., Fisher, E.A., Gilroy, D.W., Goerdt, S., Gordon, S., Hamilton, J.A., Ivashkiv, L.B., Lawrence, T., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41 (2014), 14–20.
26. Newman, S.L., Gootee, L., Colony-stimulating factors activate human macrophages to inhibit intracellular growth of Histoplasma capsulatum yeasts. Infect. Immun. 60 (1992), 4593–4597.
27. Palmiter, R.D., Huang, L., Efflux and compartmentalization of zinc by members of the SLC30 family of solute carriers. Pflugers Arch. 447 (2004), 744–751.
28. Rivera-Marrero, C.A., Stewart, J., Shafer, W.M., Roman, J., The down-regulation of cathepsin G in THP-1 monocytes after infection with Mycobacterium tuberculosis is associated with increased intracellular survival of bacilli. Infect. Immun. 72 (2004), 5712–5721.
29. Subramanian Vignesh, K., Deepe, G.S. Jr., Immunological orchestration of zinc homeostasis: The battle between host mechanisms and pathogen defenses. Arch. Biochem. Biophys., 2016, 10.1016/j.abb.2016.02.020 Published online February 4, 2016.
30. Subramanian Vignesh, K., Landero Figueroa, J.A., Porollo, A., Caruso, J.A., Deepe, G.S. Jr., Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. Immunity 39 (2013), 697–710.
31. Subramanian Vignesh, K., Landero Figueroa, J.A., Porollo, A., Caruso, J.A., Deepe, G.S. Jr., Zinc sequestration: arming phagocyte defense against fungal attack. PLoS Pathog., 9, 2013, e1003815.
32. Szymczak, W.A., Deepe, G.S. Jr., The CCL7-CCL2-CCR2 axis regulates IL-4 production in lungs and fungal immunity. J. Immunol. 183 (2009), 1964–1974.
33. Teigelkamp, S., Bhardwaj, R.S., Roth, J., Meinardus-Hager, G., Karas, M., Sorg, C., Calcium-dependent complex assembly of the myeloic differentiation proteins MRP-8 and MRP-14. J. Biol. Chem. 266 (1991), 13462–13467.
34. Verma, A., Kroetz, D.N., Tweedle, J.L., Deepe, G.S. Jr., Type II cytokines impair host defense against an intracellular fungal pathogen by amplifying macrophage generation of IL-33. Mucosal Immunol. 8 (2015), 380–389.
35. Weiss, G., Bogdan, C., Hentze, M.W., Pathways for the regulation of macrophage iron metabolism by the anti-inflammatory cytokines IL-4 and IL-13. J. Immunol. 158 (1997), 420–425.