ZIP8 Regulates Host Defense through Zinc-Mediated Inhibition of NF-κB

Cell Reports

Volumn 3, Issue 2, 2013, Pages 386-400

  Liu, Ming Jie ^a   Bao, Shengying ^a   Gálvez Peralta, Marina ^c   Pyle, Charlie J ^a   Rudawsky, Andrew C ^a   Pavlovicz, Ryan E ^b   Killilea, David W ^d   Li, Chenglong ^b   Nebert, Daniel W ^c   Wewers, Mark D ^a   Knoell, Daren L ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^d CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN ZIP8; UNCLASSIFIED DRUG; ZINC TRANSPORTER;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; FIBROBLAST; HUMAN; IN VITRO STUDY; INNATE IMMUNITY; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ZINC DEFICIENCY; ZINC METABOLISM;

ANIMALS; BASE SEQUENCE; BINDING SITES; CATION TRANSPORT PROTEINS; CELLS, CULTURED; HEK293 CELLS; HUMANS; I-KAPPA B KINASE; INFLAMMATION; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTIONAL ACTIVATION; ZINC;

BACTERIA (MICROORGANISMS); MUS;

EID: 84874232263     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.01.009     Document Type: Article

References (54)

1. Abraham E., Singer M. Mechanisms of sepsis-induced organ dysfunction. Crit. Care Med. 2007, 35:2408-2416.
2. Aiba I., Hossain A., Kuo M.T. Elevated GSH level increases cadmium resistance through down-regulation of Sp1-dependent expression of the cadmium transporter ZIP8. Mol. Pharmacol. 2008, 74:823-833.
3. Angus D.C., Linde-Zwirble W.T., Lidicker J., Clermont G., Carcillo J., Pinsky M.R. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 2001, 29:1303-1310.
4. Aydemir T.B., Liuzzi J.P., McClellan S., Cousins R.J. Zinc transporter ZIP8 (SLC39A8) and zinc influence IFN-gamma expression in activated human T cells. J. Leukoc. Biol. 2009, 86:337-348.
5. Banerjee A., Gerondakis S. Coordinating TLR-activated signaling pathways in cells of the immune system. Immunol. Cell Biol. 2007, 85:420-424.
6. Banerjee A., Gugasyan R., McMahon M., Gerondakis S. Diverse Toll-like receptors utilize Tpl2 to activate extracellular signal-regulated kinase (ERK) in hemopoietic cells. Proc. Natl. Acad. Sci. USA 2006, 103:3274-3279.
7. Bao S., Liu M.J., Lee B., Besecker B., Lai J.P., Guttridge D.C., Knoell D.L. Zinc modulates the innate immune response in vivo to polymicrobial sepsis through regulation of NF-kappaB. Am. J. Physiol. Lung Cell. Mol. Physiol. 2010, 298:L744-L754.
8. Begum N.A., Kobayashi M., Moriwaki Y., Matsumoto M., Toyoshima K., Seya T. Mycobacterium bovis BCG cell wall and lipopolysaccharide induce a novel gene, BIGM103, encoding a 7-TM protein: identification of a new protein family having Zn-transporter and Zn-metalloprotease signatures. Genomics 2002, 80:630-645.
9. Besecker B., Bao S., Bohacova B., Papp A., Sadee W., Knoell D.L. The human zinc transporter SLC39A8 (Zip8) is critical in zinc-mediated cytoprotection in lung epithelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294:L1127-L1136.
10. Besecker B.Y., Exline M.C., Hollyfield J., Phillips G., Disilvestro R.A., Wewers M.D., Knoell D.L. A comparison of zinc metabolism, inflammation, and disease severity in critically ill infected and noninfected adults early after intensive care unit admission. Am. J. Clin. Nutr. 2011, 93:1356-1364.
11. Boone D.L., Turer E.E., Lee E.G., Ahmad R.C., Wheeler M.T., Tsui C., Hurley P., Chien M., Chai S., Hitotsumatsu O., et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 2004, 5:1052-1060.
12. Brooks W.A., Santosham M., Naheed A., Goswami D., Wahed M.A., Diener-West M., Faruque A.S., Black R.E. Effect of weekly zinc supplements on incidence of pneumonia and diarrhoea in children younger than 2 years in an urban, low-income population in Bangladesh: randomised controlled trial. Lancet 2005, 366:999-1004.
13. Burns K., Janssens S., Brissoni B., Olivos N., Beyaert R., Tschopp J. Inhibition of interleukin 1 receptor/Toll-like receptor signaling through the alternatively spliced, short form of MyD88 is due to its failure to recruit IRAK-4. J. Exp. Med. 2003, 197:263-268.
14. Caulfield L.E., de Onis M., Blössner M., Black R.E. Undernutrition as an underlying cause of child deaths associated with diarrhea, pneumonia, malaria, and measles. Am. J. Clin. Nutr. 2004, 80:193-198.
15. Chiao P.J., Miyamoto S., Verma I.M. Autoregulation of I kappa B alpha activity. Proc. Natl. Acad. Sci. USA 1994, 91:28-32.
16. Cousins R.J., Leinart A.S. Tissue-specific regulation of zinc metabolism and metallothionein genes by interleukin 1. FASEB J. 1988, 2:2884-2890.
17. Cui J., Zhu L., Xia X., Wang H.Y., Legras X., Hong J., Ji J., Shen P., Zheng S., Chen Z.J., Wang R.F. NLRC5 negatively regulates the NF-kappaB and type I interferon signaling pathways. Cell 2010, 141:483-496.
18. Gaetke L.M., McClain C.J., Talwalkar R.T., Shedlofsky S.I. Effects of endotoxin on zinc metabolism in human volunteers. Am. J. Physiol. 1997, 272:E952-E956.
19. Gálvez-Peralta M., He L., Jorge-Nebert L.F., Wang B., Miller M.L., Eppert B.L., Afton S., Nebert D.W. ZIP8 zinc transporter: indispensable role for both multiple-organ organogenesis and hematopoiesis in utero. PLoS One 2012, 7:e36055.
20. Girijashanker K., He L., Soleimani M., Reed J.M., Li H., Liu Z., Wang B., Dalton T.P., Nebert D.W. Slc39a14 gene encodes ZIP14, a metal/bicarbonate symporter: similarities to the ZIP8 transporter. Mol. Pharmacol. 2008, 73:1413-1423.
21. Haase H., Rink L. Signal transduction in monocytes: the role of zinc ions. Biometals 2007, 20:579-585.
22. Haase H., Rink L. Functional significance of zinc-related signaling pathways in immune cells. Annu. Rev. Nutr. 2009, 29:133-152.
23. Hambidge K.M., Krebs N.F. Zinc deficiency: a special challenge. J. Nutr. 2007, 137:1101-1105.
24. Hayden M.S., Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008, 132:344-362.
25. Hotchkiss R.S., Karl I.E. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 2003, 348:138-150.
26. Jeon K.I., Jeong J.Y., Jue D.M. Thiol-reactive metal compounds inhibit NF-kappa B activation by blocking I kappa B kinase. J. Immunol. 2000, 164:5981-5989.
27. Johnson G.L., Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002, 298:1911-1912.
28. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
29. Kehl-Fie T.E., Skaar E.P. Nutritional immunity beyond iron: a role for manganese and zinc. Curr. Opin. Chem. Biol. 2010, 14:218-224.
30. King J.C., Shames D.M., Woodhouse L.R. Zinc homeostasis in humans. J. Nutr. 2000, 130(5S, Suppl):1360S-1366S.
31. 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.
32. Knoell D.L., Julian M.W., Bao S., Besecker B., Macre J.E., Leikauf G.D., DiSilvestro R.A., Crouser E.D. Zinc deficiency increases organ damage and mortality in a murine model of polymicrobial sepsis. Crit. Care Med. 2009, 37:1380-1388.
33. Kobayashi K., Hernandez L.D., Galán J.E., Janeway C.A., Medzhitov R., Flavell R.A. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 2002, 110:191-202.
34. Li Q., Van Antwerp D., Mercurio F., Lee K.F., Verma I.M. Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 1999, 284:321-325.
35. Lichten L.A., Cousins R.J. Mammalian zinc transporters: nutritional and physiologic regulation. Annu. Rev. Nutr. 2009, 29:153-176.
36. Liew F.Y., Xu D., Brint E.K., O'Neill L.A. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 2005, 5:446-458.
37. Lin W., Chai J., Love J., Fu D. Selective electrodiffusion of zinc ions in a Zrt-, Irt-like protein, ZIPB. J. Biol. Chem. 2010, 285:39013-39020.
38. Liuzzi J.P., Lichten L.A., Rivera S., Blanchard R.K., Aydemir T.B., Knutson M.D., Ganz T., Cousins R.J. Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc. Natl. Acad. Sci. USA 2005, 102:6843-6848.
39. Martin G.S., Mannino D.M., Eaton S., Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 2003, 348:1546-1554.
40. Nishida K., Hasegawa A., Nakae S., Oboki K., Saito H., Yamasaki S., Hirano T. Zinc transporter Znt5/Slc30a5 is required for the mast cell-mediated delayed-type allergic reaction but not the immediate-type reaction. J. Exp. Med. 2009, 206:1351-1364.
41. Parrillo J.E. Pathogenetic mechanisms of septic shock. N. Engl. J. Med. 1993, 328:1471-1477.
42. Prasad A.S., Beck F.W., Bao B., Fitzgerald J.T., Snell D.C., Steinberg J.D., Cardozo L.J. Zinc supplementation decreases incidence of infections in the elderly: effect of zinc on generation of cytokines and oxidative stress. Am. J. Clin. Nutr. 2007, 85:837-844.
43. Rink L., Haase H. Zinc homeostasis and immunity. Trends Immunol. 2007, 28:1-4.
44. Rudolph D., Yeh W.C., Wakeham A., Rudolph B., Nallainathan D., Potter J., Elia A.J., Mak T.W. Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice. Genes Dev. 2000, 14:854-862.
45. Ruland J. Return to homeostasis: downregulation of NF-κB responses. Nat. Immunol. 2011, 12:709-714.
46. Sobocinski P.Z., Canterbury W.J., Mapes C.A., Dinterman R.E. Involvement of hepatic metallothioneins in hypozincemia associated with bacterial infection. Am. J. Physiol. 1978, 234:E399-E406.
47. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
48. Thomas L. Germs. N. Engl. J. Med. 1972, 287:553-555.
49. 2 transporter expression. Biochem. Biophys. Res. Commun. 2011, 410:289-294.
50. Warren H.S. Strategies for the treatment of sepsis. N. Engl. J. Med. 1997, 336:952-953.
51. Waterfield M., Jin W., Reiley W., Zhang M., Sun S.C. IkappaB kinase is an essential component of the Tpl2 signaling pathway. Mol. Cell. Biol. 2004, 24:6040-6048.
52. Wong H.R., Shanley T.P., Sakthivel B., Cvijanovich N., Lin R., Allen G.L., Thomas N.J., Doctor A., Kalyanaraman M., Tofil N.M., et al. Genome-level expression profiles in pediatric septic shock indicate a role for altered zinc homeostasis in poor outcome. Physiol. Genomics 2007, 30:146-155. Genomics of Pediatric SIRS/Septic Shock Investigators.
53. Xu G., Lo Y.C., Li Q., Napolitano G., Wu X., Jiang X., Dreano M., Karin M., Wu H. Crystal structure of inhibitor of κB kinase β. Nature 2011, 472:325-330.
54. Yu M., Lee W.W., Tomar D., Pryshchep S., Czesnikiewicz-Guzik M., Lamar D.L., Li G., Singh K., Tian L., Weyand C.M., Goronzy J.J. Regulation of T cell receptor signaling by activation-induced zinc influx. J. Exp. Med. 2011, 208:775-785.