Inverse agonist of estrogen-related receptor γ controls Salmonella typhimurium infection by modulating host iron homeostasis

Nature Medicine

Volumn 20, Issue 4, 2014, Pages 419-424

  Kim, Don Kyu ^a   Jeong, Jae Ho ^a,b   Lee, Ji Min ^a   Kim, Kwang Soo ^a,b   Park, Seung Hwan ^b   Kim, Yong Deuk ^a   Koh, Minseob ^c   Shin, Minsang ^a   Jung, Yoon Seok ^a   Kim, Hyung Seok ^b   Lee, Tae Hoon ^a   Oh, Byung Chul ^d   Kim, Jae Il ^e,f   Park, Hwan Tae ^g   Jeong, Won Il ^h   Lee, Chul Ho ⁱ   Park, Seung Bum ^c   Min, Jung Joon ^a,b   Jung, Sook In ^a,b   Choi, Seok Yong ^b   Choy, Hyon E ^a,b   Choi, Hueng Sik ^a   more..

^a Chonnam National University   (South Korea)

^b Chonnam National University Medical School   (South Korea)

^c Seoul National University   (South Korea)

^d Gachon University College of Medicine   (South Korea)

^e Gwangju Institute of Science and Technology (GIST)   (South Korea)

^f AnyGen Jeonnam NanoBioResearch Center   (South Korea)

^g Dong A University   (South Korea)

^h Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

ⁱ Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RELATED RECEPTOR GAMMA; FERRITIN; GAMMA INTERFERON; GSK 5182; HEPCIDIN; HORMONE RECEPTOR STIMULATING AGENT; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; IRON; JANUS KINASE 2; MATRIPTASE; MATRIPTASE 2; NALIDIXIC ACID; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; STAT3 PROTEIN; STEROID RECEPTOR; TRANSFERRIN RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CELL STRAIN CACO 2; FERRITIN BLOOD LEVEL; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; INTERNALIZATION; INTESTINE LOOP; IRON BLOOD LEVEL; IRON HOMEOSTASIS; IRON METABOLISM; LIVER; MACROPHAGE; MESENTERY LYMPH NODE; MICROBIAL COLONIZATION; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SIGNAL TRANSDUCTION; SPLEEN;

BACTERIA (MICROORGANISMS); MUS; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

ANIMALS; CATION TRANSPORT PROTEINS; HEPATOCYTES; HEPCIDINS; HOMEOSTASIS; INTERLEUKIN-6; IRON; LIVER; MACROPHAGES; MICE; RECEPTORS, ESTROGEN; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

EID: 84898042156     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3483     Document Type: Article

References (26)

1. Ganz, T. Hepcidin-a peptide hormone at the interface of innate immunity and iron metabolism. Curr. Top. Microbiol. Immunol. 306, 183-198 (2006).
2. Nemeth, E. et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306, 2090-2093 (2004).
3. Ganz, T. Hepcidin and iron regulation, 10 years later. Blood 117, 4425-4433 (2011).
4. Chlosta, S. et al. The iron efflux protein ferroportin regulates the intracellular growth of Salmonella enterica. Infect. Immun. 74, 3065-3067 (2006).
5. Nairz, M. et al. The co-ordinated regulation of iron homeostasis in murine macrophages limits the availability of iron for intracellular Salmonella typhimurium. Cell. Microbiol. 9, 2126-2140 (2007).
6. Paradkar, P.N. et al. Iron depletion limits intracellular bacterial growth in macrophages. Blood 112, 866-874 (2008).
7. Wagner, D. et al. Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J. Immunol. 174, 1491-1500 (2005).
8. Collins, H.L. Withholding iron as a cellular defence mechanism-friend or foe? Eur. J. Immunol. 38, 1803-1806 (2008).
9. Kim, D.K. et al. Estrogen-related receptor γ (ERRγ) is a novel transcriptional regulator of phosphatidic acid phosphatase, LIPIN1, and inhibits hepatic insulin signaling. J. Biol. Chem. 286, 38035-38042 (2011).
10. Kim, D.K. et al. Orphan nuclear receptor estrogen-related receptor γ (ERRγ) is key regulator of hepatic gluconeogenesis. J. Biol. Chem. 287, 21628-21639 (2012).
11. Kim, D.K. et al. Estrogen-related receptor γ controls hepatic CB1 receptor-mediated CYP2E1 expression and oxidative liver injury by alcohol. Gut 62, 1044-1054 (2013).
12. Kim, D.K. et al. Inverse agonist of nuclear receptor ERRγ mediates antidiabetic effect through inhibition of hepatic gluconeogenesis. Diabetes 62, 3093-3102 (2013).
13. Wang, L. et al. Selective modulation of TLR4-activated inflammatory responses by altered iron homeostasis in mice. J. Clin. Invest. 119, 3322-3328 (2009).
14. Wang, L. et al. Attenuated inflammatory responses in hemochromatosis reveal a role for iron in the regulation of macrophage cytokine translation. J. Immunol. 181, 2723-2731 (2008).
15. Giguère, V. Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr. Rev. 29, 677-696 (2008).
16. Chao, E.Y. et al. Structure-guided synthesis of tamoxifen analogs with improved selectivity for the orphan ERRγ. Bioorg. Med. Chem. Lett. 16, 821-824 (2006).
17. Kenakin, T. Principles: receptor theory in pharmacology. Trends Pharmacol. Sci. 25, 186-192 (2004).
18. Fritsche, G., Nairz, M., Libby, S.J., Fang, F.C. & Weiss, G. Slc11a1 (Nramp1) impairs growth of Salmonella enterica serovar Typhimurium in macrophages via stimulation of lipocalin-2 expression. J. Leukoc. Biol. 92, 353-359 (2012).
19. Barton, C.H., Biggs, T.E., Baker, S.T., Bowen, H. & Atkinson, P.G. Nramp1: a link between intracellular iron transport and innate resistance to intracellular pathogens. J. Leukoc. Biol. 66, 757-762 (1999).
20. Park, C.H., Valore, E.V., Waring, A.J. & Ganz, T. Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J. Biol. Chem. 276, 7806-7810 (2001).
21. Alaynick, W.A. et al. ERRγ directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab. 6, 13-24 (2007).
22. Rangwala, S.M. et al. Estrogen-related receptor γ is a key regulator of muscle mitochondrial activity and oxidative capacity. J. Biol. Chem. 285, 22619-22629 (2010).
23. Nairz, M. et al. Nitric oxide-mediated regulation of ferroportin-1 controls macrophage iron homeostasis and immune function in Salmonella infection. J. Exp. Med. 210, 855-873 (2013).
24. Byun, J.S., Suh, Y.G., Yi, H.S., Lee, Y.S. & Jeong, W.I. Activation of Toll-like receptor 3 attenuates alcoholic liver injury by stimulating Kupffer cells and stellate cells to produce interleukin-10 in mice. J. Hepatol. 58, 342-349 (2013).
25. Min, J.J. et al. Noninvasive real-time imaging of tumors and metastases using tumor-targeting light-emitting Escherichia coli. Mol. Imaging Biol. 10, 54-61 (2008).
26. Min, J.J., Nguyen, V.H., Kim, H.J., Hong, Y. & Choy, H.E. Quantitative bioluminescence imaging of tumor-targeting bacteria in living animals. Nat. Protoc. 3, 629-636 (2008).