Role of the hepcidin-ferroportin axis in pathogen-mediated intracellular iron sequestration in human phagocytic cells

Blood Advances

Volumn 2, Issue 10, 2018, Pages 1089-1100

  Abreu, Rodrigo ^a   Quinn, Frederick ^a   Giri, Pramod K ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRITIN; FERROPORTIN; HEPCIDIN; INTERLEUKIN 6; IRON; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9;

ARTICLE; BOVINE TUBERCULOSIS; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INFECTIOUS AGENT; INTRACELLULAR SIGNALING; IRON HOMEOSTASIS; LISTERIOSIS; MACROPHAGE; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 85053842610     PISSN: 24739529     EISSN: 24739537     Source Type: Journal    
DOI: 10.1182/bloodadvances.2017015255     Document Type: Article

References (41)

1. Braun V, Killmann H. Bacterial solutions to the iron-supply problem. Trends Biochem Sci. 1999;24(3):104-109.
2. Drakesmith H, Prentice AM. Hepcidin and the iron-infection axis. Science. 2012;338(6108):768-772.
3. Boelaert JR, Vandecasteele SJ, Appelberg R, Gordeuk VR. The effect of the host’s iron status on tuberculosis. J Infect Dis. 2007;195(12):1745-1753.
4. McDermid JM, Jaye A, Schim van der Loeff MF, et al. Elevated iron status strongly predicts mortality in West African adults with HIV infection. J Acquir Immune Defic Syndr. 2007;46(4):498-507.
5. Sazawal S, Black RE, Ramsan M, et al. Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial. Lancet. 2006;367(9505):133-143.
6. Ganz T, Nemeth E. Hepcidin and disorders of iron metabolism. Annu Rev Med. 2011;62:347-360.
7. Pigeon C, Ilyin G, Courselaud B, et al. A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem. 2001;276(11):7811-7819.
8. Roy CN, Mak HH, Akpan I, Losyev G, Zurakowski D, Andrews NC. Hepcidin antimicrobial peptide transgenic mice exhibit features of the anemia of inflammation. Blood. 2007;109(9):4038-4044.
9. Nicolas G, Bennoun M, Porteu A, et al. Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc Natl Acad Sci USA. 2002;99(7): 4596-4601.
10. Rivera S, Liu L, Nemeth E, Gabayan V, Sorensen OE, Ganz T. Hepcidin excess induces the sequestration of iron and exacerbates tumor-associated anemia. Blood. 2005;105(4):1797-1802.
11. Peyssonnaux C, Zinkernagel AS, Datta V, Lauth X, Johnson RS, Nizet V. TLR4-dependent hepcidin expression by myeloid cells in response to bacterial pathogens. Blood. 2006;107(9):3727-3732.
12. Janeway CA Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002;20(1):197-216.
13. Nemeth E, Rivera S, Gabayan V, et al. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest. 2004;113(9):1271-1276.
14. Rodriguez R, Jung C-L, Gabayan V, et al. Hepcidin induction by pathogens and pathogen-derived molecules is strongly dependent on interleukin-6. Infect Immun. 2014;82(2):745-752.
15. Ganz T. Hepcidin, a key regulator of iron metabolism and mediator of anemia of inflammation. Blood. 2003;102(3):783-788.
16. Nemeth E, Valore EV, Territo M, Schiller G, Lichtenstein A, Ganz T. Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood. 2003;101(7):2461-2463.
17. Kemna E, Pickkers P, Nemeth E, van der Hoeven H, Swinkels D. Time-course analysis of hepcidin, serum iron, and plasma cytokine levels in humans injected with LPS. Blood. 2005;106(5):1864-1866.
18. Guida C, Altamura S, Klein FA, et al. A novel inflammatory pathway mediating rapid hepcidin-independent hypoferremia. Blood. 2015;125(14): 2265-2275.
19. Choi JA, Lim YJ, Cho SN, et al. Mycobacterial HBHA induces endoplasmic reticulum stress-mediated apoptosis through the generation of reactive oxygen species and cytosolic Ca21 in murine macrophage RAW 264.7 cells. Cell Death Dis. 2013;4(12):e957.
20. Hauf N, Goebel W, Fiedler F, Sokolovic Z, Kuhn M. Listeria monocytogenes infection of P388D1 macrophages results in a biphasic NF-kappaB (RelA/p50) activation induced by lipoteichoic acid and bacterial phospholipases and mediated by IkappaBalpha and IkappaBbeta degradation. Proc Natl Acad Sci USA. 1997;94(17):9394-9399.
21. ATCC: THP-1 (ATCC TIB-202) product datasheet. https://www.atcc.org/products/all/TIB-202.aspx. Accessed 31 July 2017.
22. Sil P, Hayes CP, Reaves BJ, et al. P2Y6 receptor antagonist MRS2578 inhibits neutrophil activation and aggregated neutrophil extracellular trap formation induced by gout-associated monosodium urate crystals. J Immunol. 2017;198(1):428-442.
23. Delirezh N, Shojaeefar E, Parvin P, Asadi B. Comparison the effects of two monocyte isolation methods, plastic adherence and magnetic activated cell sorting methods, on phagocytic activity of generated dendritic cells. Cell J. 2013;15(3):218-223.
24. Rey-Giraud F, Hafner M, Ries CH. In vitro generation of monocyte-derived macrophages under serum-free conditions improves their tumor promoting functions. PLoS One. 2012;7(8):e42656.
25. Ross SL, Tran L, Winters A, et al. Molecular mechanism of hepcidin-mediated ferroportin internalization requires ferroportin lysines, not tyrosines or JAK-STAT. Cell Metab. 2012;15(6):905-917.
26. Sasu B, Haniu M, Boone TC, et al. Hepcidin, hepcidin antagonists and methods of use. https://patents.google.com/patent/US20060269572A1/en. Accessed 31 July 2017.
27. Nakamura K, Kawakami T, Yamamoto N, et al. Activation of the NLRP3 inflammasome by cellular labile iron. Exp Hematol. 2016;44(2):116-124.
28. Schwandner R, Dziarski R, Wesche H, Rothe M, Kirschning CJ. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J Biol Chem. 1999;274(25):17406-17409.
29. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol. 2005;17(1):1-14.
30. MacKenzie EL, Iwasaki K, Tsuji Y. Intracellular iron transport and storage: from molecular mechanisms to health implications. Antioxid Redox Signal. 2008;10(6):997-1030.
31. Wrighting DM, Andrews NC. Interleukin-6 induces hepcidin expression through STAT3. Blood. 2006;108(9):3204-3209.
32. Hirao Y, Kanda T, Aso Y, Mitsuhashi M, Kobayashi I. Interleukin-8—an early marker for bacterial infection. Lab Med. 2000;31(1):39-44.
33. Kawasumi H, Gono T, Kawaguchi Y, et al. IL-6, IL-8, and IL-10 are associated with hyperferritinemia in rapidly progressive interstitial lung disease with polymyositis/dermatomyositis. Biomed Res Int. 2014;2014:815245.
34. Basu J, Shin DM, Jo EK. Mycobacterial signaling through toll-like receptors. Front Cell Infect Microbiol. 2012;2:145.
35. Nemeth E, Tuttle MS, Powelson J, et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science. 2004; 306(5704):2090-2093.
36. Yeh KY, Yeh M, Glass J. Hepcidin regulation of ferroportin 1 expression in the liver and intestine of the rat. Am J Physiol Gastrointest Liver Physiol. 2004; 286(3):G385-G394.
37. Yin S, Cao W. Toll-like receptor signaling induces Nrf2 pathway activation through p62-triggered Keap1 degradation. Mol Cell Biol. 2015;35(15): 2673-2683.
38. Harada N, Kanayama M, Maruyama A, et al. Nrf2 regulates ferroportin 1-mediated iron efflux and counteracts lipopolysaccharide-induced ferroportin 1 mRNA suppression in macrophages. Arch Biochem Biophys. 2011;508(1):101-109.
39. Kerkhoff AD, Meintjes G, Burton R, Vogt M, Wood R, Lawn SD. Relationship between blood concentrations of hepcidin and anemia severity, mycobacterial burden, and mortality among patients with HIV-associated tuberculosis. J Infect Dis. 2016;213(1):61-70.
40. Andriopoulos B Jr, Corradini E, Xia Y, et al. BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nat Genet. 2009;41(4): 482-487.
41. Wu X, Yung LM, Cheng WH, et al. Hepcidin regulation by BMP signaling in macrophages is lipopolysaccharide dependent. PLoS One. 2012;7(9): e44622.