The role of vitamin D in regulating the iron-hepcidin-ferroportin axis in monocytes

Journal of Clinical and Translational Endocrinology

Volumn 1, Issue 1, 2014, Pages

  Zughaier, Susu M ^a,c   Alvarez, Jessica A ^a   Sloan, John H ^b   Konrad, Robert J ^b   Tangpricha, Vin ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Anemia of inflammation; Chronic kidney disease; Ferroportin; Hepcidin; IL 1b; IL 6; Macrophage; NRAMP1; Vitamin D

Indexed keywords

CALCITRIOL; COLECALCIFEROL; FERROPORTIN; HEPCIDIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; IRON; LIPOPOLYSACCHARIDE; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; PARATHYROID HORMONE; VITAMIN D;

ADULT; ANEMIA; ARTICLE; BLOOD SAMPLING; CHRONIC KIDNEY DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; HUMAN; HUMAN TISSUE; HYPERTENSION; IN VITRO STUDY; IN VIVO STUDY; IRON METABOLISM; MACROPHAGE; MACROPHAGE CULTURE; MALE; MONOCYTE; PILOT STUDY; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; STUDY DESIGN; VITAMIN SUPPLEMENTATION;

EID: 84901468319     PISSN: None     EISSN: 22146237     Source Type: Journal    
DOI: 10.1016/j.jcte.2014.01.003     Document Type: Article

References (69)

1. Mallbris L O'Brien KP Hulthen A Sandstedt B Cowland JB Borregaard N et al. Neutrophil gelatinase-associated lipoc alin is a marker for dysregulated keratinocyte differentiation in human skin. Exp Dermatol 2002 11 6):584e91.
2. LaClair RE Hellman RN Karp SL Kraus M Ofner S Li Q et al. Preva lence of calcidiol deficiency in CKD: A cross-sectional study across latitudes in the United States. Am J Kidney Dis 2005;45(6):1026e33.
3. Alvarez JA Law J Coakley KE Zughaier SM Hao L Shahid Salles K et al. Highdose cholecalciferol reduces parathyroid hormone in patients with early chronic kidney disease: A pilot randomized double-blind placebo-controlled trial. Am J Clin Nutr 2012;96(3):672e9. PMCID: 3417221.
4. Wasse H Huang R Long Q Zhao Y Singapuri S McKinnon W et al. Very highdose cholecalciferol and arteriovenous fistula maturation in ESRD: A randomized double-blind placebo-controll ed pilot study. J Vasc Access 2013;0(0):0.
5. Chandra P Binongo JN Ziegler TR Schlanger LE Wang W Someren JT et al. Cholecalciferol (vitamin D3) therapy and vitamin D insuffic iency in patients with chronic kidney disease: A randomized controlled pilot study. Endocr Pract 2008;14(1):10e7. PMCID: 2654595.
6. Judd SE Tangpricha V. Vitamin D therapy and cardiovascular health. Curr Hypertens Rep 2011;13(3):187e91.
7. Ullah MI Uwaifo GI Nicholas WC Koch CA. Does Vitamin D deficiency cause hypertension Current evidence from clinical studies and potential mechan isms. Int J Endocrinol 2010;2010:1e11.
8. Carvalho C Isakova T Collerone G Olbina G Wolf M Westerman M et al. Hepcidin and disordered mineral metabolism in chronic kidney disease. Clin Nephrol 2011;76(2):90e8.
9. Perlstein TS Pande R Berliner N Vanasse GJ. Prevalence of 25-hydroxyvitamin D deficiency in subgroups of elderly persons with anemia: Association with anemia of inflam mation. Blood 2011;117(10):2800e6.
10. Icardi A Paoletti E De Nicola L Mazzaferro S Russo R Cozzolino M. Renal anaemia and EPO hyporesponsiveness associated with vitamin D deficiency: The po tential role of inflammation. Nephrol Dial Transplant 2013;28(7): 1672e9.
11. Ganz T. Hepcidin and iron regulation 10 years later. Blood 2011;117(17): 4425e33. PMCID: 3099567.
12. Sun CC Vaja V Babitt JL Lin HY. Targeting the hepcidin-ferroportin axis to develop new treatment strategies for anemia of chronic disease and anemia of inflammation. Am J Hematol 2012;87(4):392e400. P MCID: 3653431.
13. Ganz T Nemeth E. Hepcidin and disorders of iron metabolism. Annu Rev Med 2011;62:347e60.
14. Ganz T. Macrophages and systemic iron homeostasis. J Innate Immun 2012;4(5e6):446e53.
15. Zaritsky J Young B Gales B Wang HJ Rastogi A Westerman M et al. Reduction of serum hepcidin by hemodialysis in pediatric and adult patients. Clin J Am Soc Nephrol 2010;5(6):1010e4. PMCI D: 2879302.
16. Babitt JL Lin HY. Molecular mechanisms of hepcidin regulation: Implications for the anemia of CKD. Am J Kidney Dis 2010;55(4):726e41. PMCID: 2905036.
17. Ganz T Olbina G Girelli D Nemeth E Westerman M. Immunoassay for human serum hepcidin. Blood 2008;112(10):4292e7.
18. Nemeth E Rivera S Gabayan V Keller C Taudor f S Pedersen BK et al. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest 2004;113(9):1271e6. PMCID: 398432.
19. Lee P Peng H Gelbart T Wang L Beutler E. Regulation of hepcidin transcription by interleukin-1 and interleukin-6. Proc Natl Acad Sci U S A 2005;102(6):1906e10. PMCID: 548537.
20. Wrighti ng DM Andrews NC. Interleukin-6 induces hepcidin expression through STAT3. Blood 2006;108(9):3204e9. PMCID: 1895528.
21. Pigeon C Ilyin G Courselaud B Leroyer P Turlin B B rissot P 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):7811e9.
22. Park CH Valore EV Waring AJ Ganz T. Hepcidin a urinary antimicrobial peptide synthesized in the liver. J Biol Chem 2001;276(11):7806e10.
23. Krause A Neitz S Magert HJ Sc hulz A Forssmann WG Schulz-Knappe P et al. LEAP-1 a novel highly disulfide-bonded human peptide exhibits antimicrobial activity.FEBS Lett 2000 480 2e3):147e50.
24. Zaritsky J Young B Wang HJ Westerman M Olbina G Nemeth E et al. Hepcidinea potential novel biomarker for iron status in chronic kidney disease. Clin J Am Soc Nephrol 2009;4(6):1051e6. PMCID: 2689881.
25. Cabrera AR Cuneo KC Desjardins A Sampson JH McSherry F Herndon 2nd JE et al. Concurrent stereotactic radiosurgery and bevacizumab in recurrent malignant gliomas: A prospective trial. Int J Radiat Oncol Biol Phys 2013;86(5): 873e9.
26. Roig EA Richer E Canonne-Hergaux F Gros P Cellier MF. Regulation of NRAMP1 gene expression by 1alpha,25-dihydroxy-vitamin D(3) in HL-60 phagocytes. J Leukoc Biol 2002;71(5):890e904.
27. Rodrigues PN Gomes SS Neves JV Gomes-Pereira S Correia-Neves M Nunes-Alves C et al. Mycobacteria-induced anaemia revisited: A molecular approach reveals the involvement of NRAMP1 and lipocalin-2 but not of hepcidin. Immunobiology 2011;216(10):1127e34.
28. Nemeth E Tuttle MS Powelson J Vaughn MB Donovan A Ward DM et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004;306(5704):2090e3.
29. De Domenico I Ward DM Langelier C Vaugh n MB Nemeth E Sundquist WI et al. The molecular mechanism of hepcidin-mediated ferroportin downregulation. Mol Biol Cell 2007;18(7):2569e78. PMCID: 1924807.
30. Cellier M Shustik C Dalton W Rich E Hu J Malo D et al. Expression of the human NRAMP1 gene in professional primary phagocytes: Studies in blood cells and in HL-60 promyelocytic leukemia. J Leukoc Biol 1997;61(1):96e105.
31. Zughaier SM Tzeng YL Zimmer SM Datta A Carlson RW Stephens DS. Neisseria meningitidis lipooligosaccharide structure-dependent activation of the macrophage CD14/Toll-like receptor 4 pathway. Infect I mmun 2004;72(1): 371e80.
32. Zughaier SM. Neisseria meningitidis capsular polysaccharides induce inflammatory responses via TLR2 and TLR4-MD-2. J Leukoc Biol 2011;89(3):469e80. PMCID: 3040465.
33. Zughaier SM Zimmer SM Datta A Carlson RW Stephens DS. Differential induction of the toll-like receptor 4-MyD88-dependent and-independent signaling pathways by endotoxins. Infect Immun 2005;73(5):2940e50.
34. Leclercq A Houard X Philippe M Ollivier V Sebbag U Meilhac O et al. Involvement of intraplaque hemorrhage in atherothrombosis evolution via neutrophil protease enrichm ent. J Leukoc Biol 2007;82(6):1420e9.
35. Levey AS Coresh J Greene T Stevens LA Zhang YL Hendriksen S et al. Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann Intern Med 2006;145(4):247e54.
36. Alvarez JA Zughaier SM Law J Hao L Wasse H Ziegler TR et a l. Effects of high-dose cholecalciferol on serum markers of inflammation and immunity in patients with early chronic kidney disease. Eur J Clin Nutr 2013;67(3):264e9.
37. Wang J Pantopoulos K. Re gulation of cellular iron metabolism. Biochem J 2011;434(3):365e81. PMCID: 3048577.
38. Bell SJ. The effect of VitaminD3 on hepcidin and IL-8 expression in monocytes. J Hematol 2013;2(1):1e7.
39. Bacchetta J Zaritsky JJ Sea JL Chun RF Lisse TS Zavala K et al. Suppression of iron-regulatory hepcidin by vitamin D. J Am Soc Nephrol 2014;25:564e72.
40. Layoun A Santos MM. Bacterial cell wall constituents induce hepcidin expression in macrophages through MyD88 signaling. Inflammation 2012;35(4):1500e6.
41. Wang L Harrington L Tre bicka E Shi HN Kagan JC Hong CC et al. Selective modulation of TLR4-activated inflammatory responses by altered iron homeostasis in mice. J Clin Invest 2009;119(11):3322e8. PMCID: 2769199.
42. Theurl I Theurl M Seifert M Mair S Nairz M Rumpold H et al. Autocrine formation of hepcidin induces iron retention in human monocytes. Blood 2008;111(4):2392e9.
43. ] Ramezani A Raj DS. The gut microbiome kidney disease and targeted interventions. J Am Soc Nephrol 2013. PMCID: 24231662.
44. McCarley P. The KDOQI clinical practice guidelines and clinical practice r ecommendations for treating anemia in patients with chronic kidney disease: Implications for nurses. Nephrol Nurs J 2006 33 4):423e6. 45; quiz 7e8.
45. Malyszko J Malyszko JS Bachorzewska-Gajewska H Poniatowski B Dobrzycki S Mysliwiec M. Neutrophil gelatinase-associated lipocalin is a new and sensitive marker of kidney function in chronic kidney disease patients and renal allograft recipients. Transplant Proc 2009;41(1):158e61.
46. Malyszko J Bachorzewska-Gajewska H Sitniewska E Malyszko JS Poniatowski B Dobrzycki S. Serum neutrophil gelatinase-associated lipocalin as a marker of renal function in non-diab etic patients with stage 2-4 chronic kidney disease. Ren Fail 2008;30(6):625e8.
47. Pecoits-Filho R Barany P Lindholm B Heimburger O Stenvinkel P. Interleukin-6 is an independent pr edictor of mortality in patients starting dialysis treatment. Nephrol Dial Transplant 2002;17(9):1684e8.
48. Wang FD Zhou DB Li SL Wang X Zhang JP Duan MH et al. Effect of reco mbinant human erythropoietin on hepcidin mRNA expression in patients with multiple myeloma. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2011;19(2): 390e4.
49. Zughaier SM Shafer WM Stephens DS. Antimicrobial p eptides and endotoxin inhibit cytokine and nitric oxide release but amplify respiratory burst response in human and murine macrophages. Cell Microbiol 2005;7(9):1251e62.
50. Valenti L Dongiovanni P Mot ta BM Swinkels DW Bonara P Rametta R et al. Serum hepcidin and macrophage iron correlate with MCP-1 release and vascular damage in patients with metabolic syndrome alterations. Arterioscler Thromb Vasc Biol 2011;31( 3):683e90.
51. Zhang Y Leung DY Richers BN Liu Y Remigio LK Riches DW et al. Vitamin D inhibits monocyte/macrophage proinflammatory cytokine production by targetingMAPK phosphatase-1. J Immunol 2012;188(5):2127e35. PMCID: 3368346.
52. Chen Y Liu W Sun T Huang Y Wang Y Deb DK et al. 1,25-dihydroxyvitamin D promotes negative feedback regulation of TLR signaling via targeting microRNA-155-SOCS1 in macrophages. J Immunol 2013;190(7):3687e95. PMCID: 3608760.
53. Katsushima F Takahashi A Sakamoto N Kanno Y Abe K Ohira H. Expression of micro-RNAs in pe ripheral blood mononuclear cells from primary biliary cirrhosis patients. Hepatol Res; 2013. http://dx.doi.org/10.1111/hepr.12198.
54. Wang H Peng W Ouyang X Li W Dai Y. Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Transl Res 2012;160(3):198e206.
55. Leng RX Pan HF Qin WZ Chen GM Ye DQ. Role of microRNA-155 in autoimmunity. Cytokine Growth Factor Rev 2011;22(3):141e7.
56. Wang G Tam LS Li EK Kwan BC Chow KM Luk CC et al. Serum and urinary cell-free MiR-146a and MiR-155 in patients with systemic lupus erythematosus. J Rheumatol 2010;37(12):2516e22.
57. Li YC Chen Y Liu W Thadhani R. MicroRNA-med iated mechanism of vitamin D regulation of innate immune response. J Steroid Biochem Mol Biol 2013. http://dx.doi.org/10.1016/j.jsbmb.2013.09.014.
58. Chen NK Chong TW Loh HL Lim KH Gan VH Wang M et al. Negative regulatory responses to metabolically triggered inflammation impair renal epithelial immunity in diabetes mellitus. J Mol Med (Berl) 2013;91(5):587e98. PMCID: 3644409.
59. Jo EK. Innate immunity to mycobacteria: Vitamin D and autophagy. Cell Microbiol 2010;12(8):1026e35.
60. Yuk JM Shin DM Lee HM Yang CS Jin HS Kim KK et al. Vitamin D3 induces autophagy in human monocytes/macrophages via cathelicidin. Cell Host Microbe 2009;6(3):231e43.
61. Campbell GR Spector SA. Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog 2012;8(5):e1002689. PMCID: 3349755. [62] Campbell GR Spector SA. Toll-like receptor 8 ligands activate a vitamin D mediated autophagic response that inhibits human immunodeficiency virus type 1. PLoS Pathog 2012;8(11):e1003017. PMCID: 3499571.
62. Zughaier S Karna P Stephens D Aneja R. Potent anti-inflammatory activity of novel microtubule-modulating brominated noscapine analogs. PLoS One 2010;5(2):e9165. PMCID: 2820095.
63. Vecchi C Montosi G Zhang K Lamberti I Duncan SA Kaufman RJ et al. ER stress controls iron metabolism through induction of hepcidin. Science 2009;325(5942):877e80. PMCID: 2923557.
64. Riek AE Oh J Bernal-Mizrachi C. 125(OH)(2) vitamin D suppresses macrophage migration and reverses atherogenic cholesterol metabolism in type 2 diabetic patients. J Steroid Biochem Mol Biol 2013 136 309 e12.
65. Riek AE Oh J Sprague JE Timpson A de las Fuentes L Bernal-Mizrachi L et al. Vitamin D suppression of endoplasmic reticulum stress promotes an antiatherogenic monocyte/macrophage phenotype in type 2 di abetic patients. J Biol Chem 2012;287(46):38482e94. PMCID: 3493893.
66. Atkinson MA Melamed ML Kumar J Roy CN Miller 3rd ER Furth SL et al. Vitamin D race and risk for anemia in children. J Pediatr 2014;164:153e8. e1.
67. Astor BC Muntner P Levin A Eustace JA Coresh J. Association of kidney function with anemia: The Third National Health and Nutrition Examination Survey (1988-1994). Arch Intern Med 2002;162(12):1401e8.
68. Goicoechea M Vazquez MI Ruiz MA Gomez-Campdera F Perez-Garcia R Valderrabano F. Intravenous calci triol improves anaemia and reduces the need for erythropoietin in haemodialysis patients. Nephron 1998;78(1): 23e7.
69. Albitar S Genin R Fen-Chong M Serveaux MO Schohn D Chuet C. High-dose alfacalcidol improves anaemia in patients on haemodialysis. Nephrol Dial Transplant 1997;12(3):514e8.