Macrophage and epithelial cell H-ferritin expression regulates renal inflammation

Kidney International

Volumn 88, Issue 1, 2015, Pages 95-108

  Bolisetty, Subhashini ^a   Zarjou, Abolfazl ^a   Hull, Travis D ^a   Traylor, Amie M ^a   Perianayagam, Anjana ^a   Joseph, Reny ^a   Kamal, Ahmed I ^a   Arosio, Paolo ^b   Soares, Miguel P ^c   Jeney, Viktoria ^d,e   Balla, Jozsef ^d,e   George, James F ^a   Agarwal, Anupam ^a,f  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF BRESCIA   (Italy)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^d UNIVERSITY OF DEBRECEN   (Hungary)

^e INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^f BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Acute kidney injury; Ferritin; Fibrosis; Inflammation; Macrophage polarization

Indexed keywords

CHEMOKINE; FERRITIN; HEME OXYGENASE 1; APOFERRITIN; CCL2 PROTEIN, MOUSE; COLONY STIMULATING FACTOR 1; INTERLEUKIN 10; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL ISOLATION; CONTROLLED STUDY; IN VITRO STUDY; KIDNEY FIBROSIS; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; KIDNEY TUBULE EPITHELIUM; MACROPHAGE; MALE; MONOCYTE; MOUSE; NEPHRITIS; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TRANSGENIC MOUSE; URETER OBSTRUCTION; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; COMPLICATION; CYTOLOGY; DEFICIENCY; DISEASE MODEL; EPITHELIUM CELL; FIBROSIS; GENE EXPRESSION; GENETICS; KIDNEY; MACROPHAGE ACTIVATION; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOFERRITINS; CELLS, CULTURED; CHEMOKINE CCL2; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FIBROSIS; GENE EXPRESSION; HEME OXYGENASE-1; INTERLEUKIN-10; INTERLEUKIN-6; KIDNEY; KIDNEY TUBULES, PROXIMAL; MACROPHAGE ACTIVATION; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELOID CELLS; NEPHRITIS; RNA, MESSENGER; URETERAL OBSTRUCTION;

EID: 84934441179     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2015.102     Document Type: Article

References (85)

1. Liu Y. Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 2006; 69: 213-217.
2. Strutz F, Neilson EG. New insights into mechanisms of fibrosis in immune renal injury. Springer Semin Immunopathol. 2003; 24: 459-476.
3. Zeisberg M, Neilson EG. Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol 2010; 21: 1819-1834.
4. Aksu U, Demirci C, Ince C. The pathogenesis of acute kidney injury and the toxic triangle of oxygen, reactive oxygen species and nitric oxide. Contrib Nephrol 2011; 174: 119-128.
5. Sharfuddin AA, Molitoris BA. Pathophysiology of ischemic acute kidney injury. Nat Rev Nephrol 2011; 7: 189-200.
6. Basile DP, Anderson MD, Sutton TA. Pathophysiology of acute kidney injury. Compr Physiol 2012; 2: 1303-1353.
7. Kinsey GR, Okusa MD. Role of leukocytes in the pathogenesis of acute kidney injury. Crit Care 2012; 16: 214.
8. Furuichi K, Kaneko S, Wada T. Chemokine/chemokine receptor-mediated inflammation regulates pathologic changes from acute kidney injury to chronic kidney disease. Clin Exp Nephrol 2009; 13: 9-14.
9. Jang HS, Kim JI, Han SJ et al. The recruitment and subsequent proliferation of bone marrow-derived cells in postischemic kidney are important to the progression of fibrosis. Am J Physiol Renal Physiol 2014; 306: F1451-F1461.
10. Koyner JL, Sher Ali R, Murray PT. Antioxidants. Do they have a place in the prevention or therapy of acute kidney injury? Nephron Exp Nephrol 2008; 109: e109-e117.
11. Heyman SN, Rosen S, Rosenberger C. A role for oxidative stress. Contrib Nephrol 2011; 174: 138-148.
12. Nath KA. Heme oxygenase-1: a provenance for cytoprotective pathways in the kidney and other tissues. Kidney Int 2006; 70: 432-443.
13. Lee DW, Faubel S, Edelstein CL. Cytokines in acute kidney injury (AKI). Clin Nephrol 2011; 76: 165-173.
14. Akcay A, Nguyen Q, Edelstein CL. Mediators of inflammation in acute kidney injury. Mediat Inflamm 2009; 2009: 137072.
15. Kinsey GR, Li L, Okusa MD. Inflammation in acute kidney injury. Nephron Exp Nephrol 2008; 109: e102-e107.
16. Nath KA. Heme oxygenase-1 and acute kidney injury. Curr Opin Nephrol Hypertens 2014; 23: 17-24.
17. Wei Q, Hill WD, Su Y et al. Heme oxygenase-1 induction contributes to renoprotection by G-CSF during rhabdomyolysis-associated acute kidney injury. Am J Physiol Renal Physiol 2011; 301: F162-F170.
18. Bolisetty S, Traylor AM, Kim J et al. Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J Am Soc Nephrol 2010; 21: 1702-1712.
19. Shiraishi F, Curtis LM, Truong L et al. Heme oxygenase-1 gene ablation or expression modulates cisplatin-induced renal tubular apoptosis. Am J Physiol Renal Physiol 2000; 278: F726-F736.
20. Agarwal A, Balla J, Alam J et al. Induction of heme oxygenase in toxic renal injury: a protective role in cisplatin nephrotoxicity in the rat. Kidney Int 1995; 48: 1298-1307.
21. Nath KA, Balla G, Vercellotti GM et al. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 1992; 90: 267-270.
22. Zarjou A, Bolisetty S, Joseph R et al. Proximal tubule H-ferritin mediates iron trafficking in acute kidney injury. J Clin Invest 2013; 123: 4423-4434.
23. Gozzelino R, Soares MP. Coupling heme and iron metabolism via ferritin H chain. Antioxid Redox Signal 2014; 20: 1754-1769.
24. Zhang MZ, Yao B, Yang S et al. CSF-1 signaling mediates recovery from acute kidney injury. J Clin Invest 2012; 122: 4519-4532.
25. Winterberg PD, Wang Y, Lin KM et al. Reactive oxygen species and IRF1 stimulate IFNalpha production by proximal tubules during ischemic AKI. Am J Physiol Renal Physiol 2013; 305: F164-F172.
26. Anders HJ, Vielhauer V, Schlondorff D. Chemokines and chemokine receptors are involved in the resolution or progression of renal disease. Kidney Int 2003; 63: 401-415.
27. Li L, Okusa MD. Macrophages, dendritic cells, and kidney ischemiareperfusion injury. Semin Nephrol 2010; 30: 268-277.
28. Alikhan MA, Ricardo SD. Mononuclear phagocyte system in kidney disease and repair. Nephrology (Carlton) 2013; 18: 81-91.
29. Williams TM, Little MH, Ricardo SD. Macrophages in renal development, injury, and repair. Semin Nephrol 2010; 30: 255-267.
30. Cao Q, Wang Y, Harris DC. Pathogenic and protective role of macrophages in kidney disease. Am J Physiol Renal Physiol 2013; 305: F3-11.
31. Eardley KS, Zehnder D, Quinkler M et al. The relationship between albuminuria, MCP-1/CCL2, and interstitial macrophages in chronic kidney disease. Kidney Int 2006; 69: 1189-1197.
32. Lim AK, Tesch GH. Inflammation in diabetic nephropathy. Mediat Inflamm 2012; 2012: 146154.
33. Yang N, Isbel NM, Nikolic-Paterson DJ et al. Local macrophage proliferation in human glomerulonephritis. Kidney Int 1998; 54: 143-151.
34. Chaves LD, Mathew L, Shakaib M et al. Contrasting effects of systemic monocyte/macrophage and CD4+ T cell depletion in a reversible ureteral obstruction mouse model of chronic kidney disease. Clin Dev Immunol 2013; 2013: 836989.
35. Henderson NC, Mackinnon AC, Farnworth SL et al. Galectin-3 expression and secretion links macrophages to the promotion of renal fibrosis. Am J Pathol 2008; 172: 288-298.
36. Ko GJ, Boo CS, Jo SK et al. Macrophages contribute to the development of renal fibrosis following ischaemia/reperfusion-induced acute kidney injury. Nephrol Dial Transplant 2008; 23: 842-852.
37. Machida Y, Kitamoto K, Izumi Y et al. Renal fibrosis in murine obstructive nephropathy is attenuated by depletion of monocyte lineage, not dendritic cells. J Pharmacol Sci 2010; 114: 464-473.
38. Lee S, Huen S, Nishio H et al. Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 2011; 22: 317-326.
39. Nishida M, Okumura Y, Fujimoto S et al. Adoptive transfer of macrophages ameliorates renal fibrosis in mice. Biochem Biophys Res Commun 2005; 332: 11-16.
40. Martinez FO, Sica A, Mantovani A et al. Macrophage activation and polarization. Front Biosci 2008; 13: 453-461.
41. Mantovani A, Biswas SK, Galdiero MR et al. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 2013; 229: 176-185.
42. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122: 787-795.
43. Cassetta L, Cassol E, Poli G. Macrophage polarization in health and disease. Scientific World J 2011; 11: 2391-2402.
44. Biswas SK, Mantovani A. Orchestration of metabolism by macrophages. Cell Metab 2012; 15: 432-437.
45. Sierra-Filardi E, Vega MA, Sanchez-Mateos P et al. Heme oxygenase-1 expression in M-CSF-polarized M2 macrophages contributes to LPSinduced IL-10 release. Immunobiology 2010; 215: 788-795.
46. Durante W. Protective role of heme oxygenase-1 against inflammation in atherosclerosis. Front Biosci (Landmark Ed) 2011; 16: 2372-2388.
47. Paine A, Eiz-Vesper B, Blasczyk R et al. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 2010; 80: 1895-1903.
48. Hull TD, Agarwal A, George JF. The mononuclear phagocyte system in homeostasis and disease: a role for heme oxygenase-1. Antioxid Redox Signal 2014; 20: 1770-1788.
49. Li L, Huang L, Sung SS et al. The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemia-reperfusion injury. Kidney Int 2008; 74: 1526-1537.
50. Sunderkotter C, Nikolic T, Dillon MJ et al. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 2004; 172: 4410-4417.
51. Tacke F, Randolph GJ. Migratory fate and differentiation of blood monocyte subsets. Immunobiology 2006; 211: 609-618.
52. Nahrendorf M, Swirski FK. Monocyte and macrophage heterogeneity in the heart. Circ Res 2013; 112: 1624-1633.
53. Davies LC, Jenkins SJ, Allen JE et al. Tissue-resident macrophages. Nat Immunol 2013; 14: 986-995.
54. Kawakami T, Lichtnekert J, Thompson LJ et al. Resident renal mononuclear phagocytes comprise five discrete populations with distinct phenotypes and functions. J Immunol 2013; 191: 3358-3372.
55. Kie JH, Kapturczak MH, Traylor A et al. Heme oxygenase-1 deficiency promotes epithelial-mesenchymal transition and renal fibrosis. J Am Soc Nephrol 2008; 19: 1681-1691.
56. Kim J, Zarjou A, Traylor AM et al. In vivo regulation of the heme oxygenase-1 gene in humanized transgenic mice. Kidney Int 2012; 82: 278-291.
57. Ferreira C, Bucchini D, Martin ME et al. Early embryonic lethality of H ferritin gene deletion in mice. J Biol Chem 2000; 275: 3021-3024.
58. Chovatiya R, Medzhitov R. Stress, inflammation, and defense of homeostasis. Mol Cell 2014; 54: 281-288.
59. Biswas SK, Chittezhath M, Shalova IN et al. Macrophage polarization and plasticity in health and disease. Immunol Res 2012; 53: 11-24.
60. Hume DA. Applications of myeloid-specific promoters in transgenic mice support in vivo imaging and functional genomics but do not support the concept of distinct macrophage and dendritic cell lineages or roles in immunity. J Leukoc Biol 2011; 89: 525-538.
61. Levi S, Arosio P. Mitochondrial ferritin. Int J Biochem Cell Biol 2004; 36: 1887-1889.
62. Drysdale J, Arosio P, Invernizzi R et al. Mitochondrial ferritin: a new player in iron metabolism. Blood Cells Mol Dis 2002; 29: 376-383.
63. Linsenmayer TF, Cai CX, Millholland JM et al. Nuclear ferritin in corneal epithelial cells: tissue-specific nuclear transport and protection from UV-damage. Prog Retin Eye Res 2005; 24: 139-159.
64. Surguladze N, Patton S, Cozzi A et al. Characterization of nuclear ferritin and mechanism of translocation. Biochem J 2005; 388: 731-740.
65. Thompson KJ, Fried MG, Ye Z et al. Regulation, mechanisms and proposed function of ferritin translocation to cell nuclei. J Cell Sci 2002; 115: 2165-2177.
66. Harrison PM, Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1996; 1275: 161-203.
67. Gozzelino R, Andrade BB, Larsen R et al. Metabolic adaptation to tissue iron overload confers tolerance to malaria. Cell Host Microbe 2012; 12: 693-704.
68. Rosario C, Zandman-Goddard G, Meyron-Holtz EG et al. The hyperferritinemic syndrome: macrophage activation syndrome, Still's disease, septic shock and catastrophic antiphospholipid syndrome. BMC Med 2013; 11: 185.
69. Recalcati S, Invernizzi P, Arosio P et al. New functions for an iron storage protein: the role of ferritin in immunity and autoimmunity. J Autoimmun 2008; 30: 84-89.
70. Morikawa K, Oseko F, Morikawa S. H-and L-rich ferritins suppress antibody production, but not proliferation, of human B lymphocytes in vitro. Blood 1994; 83: 737-743.
71. Hann HW, Stahlhut MW, Lee S et al. Effects of isoferritins on human granulocytes. Cancer 1989; 63: 2492-2496.
72. Gray CP, Franco AV, Arosio P et al. Immunosuppressive effects of melanoma-derived heavy-chain ferritin are dependent on stimulation of IL-10 production. Int J Cancer 2001; 92: 843-850.
73. Davis CL, Kausz AT, Zager RA et al. Acute renal failure after cardiopulmonary bypass in related to decreased serum ferritin levels. J Am Soc Nephrol 1999; 10: 2396-2402.
74. Ruddell RG, Hoang-Le D, Barwood JM et al. Ferritin functions as a proinflammatory cytokine via iron-independent protein kinase C zeta/ nuclear factor kappaB-regulated signaling in rat hepatic stellate cells. Hepatology 2009; 49: 887-900.
75. Dai Y, Zhang W, Wen J et al. A2B adenosine receptor-mediated induction of IL-6 promotes CKD. J Am Soc Nephrol 2011; 22: 890-901.
76. Pesce JT, Ramalingam TR, Mentink-Kane MM et al. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathogen 2009; 5: e1000371.
77. Meng XM, Nikolic-Paterson DJ, Lan HY. Inflammatory processes in renal fibrosis. Nat Rev Nephrol 2014; 10: 493-503.
78. Vernon MA, Mylonas KJ, Hughes J. Macrophages and renal fibrosis. Semin Nephrol 2010; 30: 302-317.
79. LeBleu VS, Taduri G, O'Connell J et al. Origin and function of myofibroblasts in kidney fibrosis. Nat Med 2013; 19: 1047-1053.
80. Kalantar-Zadeh K, Don BR, Rodriguez RA et al. Serum ferritin is a marker of morbidity and mortality in hemodialysis patients. Am J Kidney Dis 2001; 37: 564-572.
81. Rambod M, Kovesdy CP, Kalantar-Zadeh K. Combined high serum ferritin and low iron saturation in hemodialysis patients: the role of inflammation. Clin J Am Soc Nephrol 2008; 3: 1691-1701.
82. Darshan D, Vanoaica L, Richman L et al. Conditional deletion of ferritin H in mice induces loss of iron storage and liver damage. Hepatology 2009; 50: 852-860.
83. Zarjou A, Yang S, Abraham E et al. Identification of a microRNA signature in renal fibrosis: role of miR-21. Am J Physiol Renal Physiol 2011; 301: F793-F801.
84. Hull TD, Bolisetty S, DeAlmeida AC et al. Heme oxygenase-1 expression protects the heart from acute injury caused by inducible Cre recombinase. Lab Invest 2013; 93: 868-879.
85. Moon JJ, Chu HH, Hataye J et al. Tracking epitope-specific T cells. Nat Protoc 2009; 4: 565-581.