Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival

Immunity

Volumn 39, Issue 4, 2013, Pages 697-710

  SubramanianVignesh, Kavitha ^a,b   LanderoFigueroa, Julio A ^a   Porollo, Aleksey ^b   Caruso, Joseph A ^a   Deepe, George S ^b,c  

^a UNIVERSITY OF CINCINNATI   (United States)

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

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; METALLOTHIONEIN; PROTEOME; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STAT3 PROTEIN; STAT5 PROTEIN; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMICROBIAL ACTIVITY; ARTICLE; CELL LYSATE; CONTROLLED STUDY; FLOW CYTOMETRY; FUNGUS; GENE SILENCING; GOLGI COMPLEX; HISTOPLASMA CAPSULATUM; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; NUTRIENT; PHAGOCYTE; PRIORITY JOURNAL;

ANIMALS; CATION TRANSPORT PROTEINS; GENE EXPRESSION REGULATION; GOLGI APPARATUS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HISTOPLASMA; HISTOPLASMOSIS; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; METALLOTHIONEIN; MICE; MICE, TRANSGENIC; NADPH OXIDASE; PHAGOSOMES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; SUPEROXIDES; ZINC;

EID: 84885706533     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.09.006     Document Type: Article

References (43)

1. Appelberg R. Macrophage nutriprive antimicrobial mechanisms. J.Leukoc. Biol. 2006, 79:1117-1128.
2. Beyersmann D. Homeostasis and cellular functions of zinc. Materialwiss. Werkstofftech. 2002, 33:764-769.
3. Bhattacharya S., Stout B.A., Bates M.E., Bertics P.J., Malter J.S. Granulocyte macrophage colony-stimulating factor and interleukin-5 activate STAT5 and induce CIS1 mRNA in human peripheral blood eosinophils. Am. J. Respir. Cell Mol. Biol. 2001, 24:312-316.
4. Bishop G.M., Dringen R., Robinson S.R. Zinc stimulates the production of toxic reactive oxygen species (ROS) and inhibits glutathione reductase in astrocytes. Free Radic. Biol. Med. 2007, 42:1222-1230.
5. Botella H., Peyron P., Levillain F., Poincloux R., Poquet Y., Brandli I., Wang C., Tailleux L., Tilleul S., Charrière G.M., et al. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 2011, 10:248-259.
6. Cao J., Bobo J.A., Liuzzi J.P., Cousins R.J. Effects of intracellular zinc depletion on metallothionein and ZIP2 transporter expression and apoptosis. J.Leukoc. Biol. 2001, 70:559-566.
7. Coyle P., Philcox J.C., Carey L.C., Rofe A.M. Metallothionein: the multipurpose protein. Cell. Mol. Life Sci. 2002, 59:627-647.
8. DeCoursey T.E., Morgan D., Cherny V.V. The voltage dependence of NADPH oxidase reveals why phagocytes need proton channels. Nature 2003, 422:531-534.
9. Deepe G.S., Gibbons R., Woodward E. Neutralization of endogenous granulocyte-macrophage colony-stimulating factor subverts the protective immune response to Histoplasma capsulatum. J.Immunol. 1999, 163:4985-4993.
10. Dröse S., Brandt U. Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol. 2012, 748:145-169.
11. Eide D.J. Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 2006, 1763:711-722.
12. Falnoga I., Zelenik Pevec A., Šlejkovec Z., Žnidarič M.T., Zajc I., Mlakar S.J., Marc J. Arsenic trioxide (ATO) influences the gene expression of metallothioneins in human glioblastoma cells. Biol. Trace Elem. Res. 2012, 149:331-339.
13. Fang F.C. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J.Clin. Invest. 1997, 99:2818-2825.
14. Fraker P.J., Gershwin M.E., Good R.A., Prasad A. Interrelationships between zinc and immune function. Fed. Proc. 1986, 45:1474-1479.
15. Gloire G., Legrand-Poels S., Piette J. NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem. Pharmacol. 2006, 72:1493-1505.
16. Heizmann C.W., Cox J.A. New perspectives on S100 proteins: a multi-functional Ca(2+)-, Zn(2+)- and Cu(2+)-binding protein family. Biometals 1998, 11:383-397.
17. Hirano T., Murakami M., Fukada T., Nishida K., Yamasaki S., Suzuki T. Roles of zinc and zinc signaling in immunity: zinc as an intracellular signaling molecule. Adv. Immunol. 2008, 97:149-176.
18. Howard D.H. Intracellular behavior of Histoplasma capsulatum. J.Bacteriol. 1964, 87:33-38.
19. Kauppinen T.M., Higashi Y., Suh S.W., Escartin C., Nagasawa K., Swanson R.A. Zinc triggers microglial activation. J.Neurosci. 2008, 28:5827-5835.
20. Kehl-Fie T.E., Chitayat S., Hood M.I., Damo S., Restrepo N., Garcia C., Munro Kim A., Chazin Walter J., Skaar Eric P. Nutrient Metal Sequestration by Calprotectin Inhibits Bacterial Superoxide Defense, Enhancing Neutrophil Killing of Staphylococcus aureus. Cell Host Microbe 2011, 10:158-164.
21. Kitamura H., Morikawa H., Kamon H., Iguchi M., Hojyo S., Fukada T., Yamashita S., Kaisho T., Akira S., Murakami M., Hirano T. Toll-like receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat. Immunol. 2006, 7:971-977.
22. Korndörfer I.P., Brueckner F., Skerra A. The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting alpha-helices can determine specific association of two EF-hand proteins. J.Mol. Biol. 2007, 370:887-898.
23. Lee D.K., Carrasco J., Hidalgo J., Andrews G.K. Identification of a signal transducer and activator of transcription (STAT) binding site in the mouse metallothionein-I promoter involved in interleukin-6-induced gene expression. Biochem. J. 1999, 337:59-65.
24. 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 2012, 11:227-239.
25. Maret W. The function of zinc metallothionein: a link between cellular zinc and redox state. J.Nutr. 2000, 130(Suppl):1455S-1458S.
26. McCormick N., Velasquez V., Finney L., Vogt S., Kelleher S.L. X-ray fluorescence microscopy reveals accumulation and secretion of discrete intracellular zinc pools in the lactating mouse mammary gland. PLoS ONE 2010, 5:e11078.
27. McDevitt C.A., Ogunniyi A.D., Valkov E., Lawrence M.C., Kobe B., McEwan A.G., Paton J.C. A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog. 2011, 7:e1002357.
28. Minakami R., Sumimotoa H. Phagocytosis-coupled activation of the superoxide-producing phagocyte oxidase, a member of the NADPH oxidase (nox) family. Int. J. Hematol. 2006, 84:193-198.
29. Mosser D.M. The many faces of macrophage activation. J.Leukoc. Biol. 2003, 73:209-212.
30. Muijsers R.B., van Den Worm E., Folkerts G., Beukelman C.J., Koster A.S., Postma D.S., Nijkamp F.P. Apocynin inhibits peroxynitrite formation by murine macrophages. Br. J. Pharmacol. 2000, 130:932-936.
31. Nairz M., Fritsche G., Brunner P., Talasz H., Hantke K., Weiss G. Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium. Eur. J. Immunol. 2008, 38:1923-1936.
32. Nauseef W.M. How human neutrophils kill and degrade microbes: an integrated view. Immunol. Rev. 2007, 219:88-102.
33. Newman S.L., Gootee L. Colony-stimulating factors activate human macrophages to inhibit intracellular growth of Histoplasma capsulatum yeasts. Infect. Immun. 1992, 60:4593-4597.
34. Novak U., Mui A., Miyajima A., Paradiso L. Formation of STAT5-containing DNA binding complexes in response to colony-stimulating factor-1 and platelet-derived growth factor. J.Biol. Chem. 1996, 271:18350-18354.
35. Palmiter R.D., Huang L. Efflux and compartmentalization of zinc by members of the SLC30 family of solute carriers. Pflugers Arch. 2004, 447:744-751.
36. Santoni V., Molloy M., Rabilloud T. Membrane proteins and proteomics: un amour impossible?. Electrophoresis 2000, 21:1054-1070.
37. Simon A.R., Rai U., Fanburg B.L., Cochran B.H. Activation of the JAK-STAT pathway by reactive oxygen species. Am. J. Physiol. 1998, 275:C1640-C1652.
38. Tomat E., Lippard S.J. Imaging mobile zinc in biology. Curr. Opin. Chem. Biol. 2010, 14:225-230.
39. Walkup G.K., Burdette S.C., Lippard S.J., Tsien R.Y. A new cell-permeable fluorescent probe for Zn2+. J.Am. Chem. Soc. 2000, 122:5644-5645.
40. Weisbart R.H., Kwan L., Golde D.W., Gasson J.C. Human GM-CSF primes neutrophils for enhanced oxidative metabolism in response to the major physiological chemoattractants. Blood 1987, 69:18-21.
41. White J.K., Stewart A., Popoff J.F., Wilson S., Blackwell J.M. Incomplete glycosylation and defective intracellular targeting of mutant solute carrier family 11 member 1 (Slc11a1). Biochem. J. 2004, 382:811-819.
42. Winters M.S., Chan Q., Caruso J.A., Deepe G.S. Metallomic analysis of macrophages infected with Histoplasma capsulatum reveals a fundamental role for zinc in host defenses. J.Infect. Dis. 2010, 202:1136-1145.
43. Zwilling B.S., Kuhn D.E., Wikoff L., Brown D., Lafuse W. Role of iron in Nramp1-mediated inhibition of mycobacterial growth. Infect. Immun. 1999, 67:1386-1392.