Macrophage-mediated injury and repair after ischemic kidney injury

Pediatric Nephrology

Volumn 30, Issue 2, 2015, Pages 199-209

  Huen, Sarah C ^a   Cantley, Lloyd G ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acute kidney injury; Ischemia reperfusion; Macrophage activation; Repair

Indexed keywords

CLODRONIC ACID; GAMMA INTERFERON;

CELL PHAGOCYTOSIS; CELL THERAPY; HISTORY; HUMAN; IMMUNOREGULATION; IN VIVO STUDY; INNATE IMMUNITY; KIDNEY FIBROSIS; KIDNEY ISCHEMIA; MACROPHAGE; MACROPHAGE ACTIVATION; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; TISSUE REPAIR; TRANSCRIPTION REGULATION; ACUTE KIDNEY FAILURE; ANIMAL; IMMUNOLOGY;

ACUTE KIDNEY INJURY; ANIMALS; HUMANS; MACROPHAGES; REPERFUSION INJURY;

EID: 84924064923     PISSN: 0931041X     EISSN: 1432198X     Source Type: Journal    
DOI: 10.1007/s00467-013-2726-y     Document Type: Review

References (72)

1. Sutton TA, Mang HE, Campos SB, Sandoval RM, Yoder MC, Molitoris BA (2003) Injury of the renal microvascular endothelium alters barrier function after ischemia. Am J Physiol Renal Physiol 285:F191-F198
2. Li L, Huang L, Sung S-SJ, Lobo PI, Brown MG, Gregg RK, Engelhard VH, Okusa MD (2007) NKT cell activation mediates neutrophil IFN-gamma production and renal ischemia-reperfusion injury. J Immunol 178:5899-5911
3. Kaufmann SHE (2008) Immunology's foundation: the 100-year anniversary of the Nobel Prize to Paul Ehrlich and Elie Metchnikoff. Nat Immunol 9:705-712
4. Pollard JW(2009) Trophic macrophages in development and disease. Nat Rev Immunol 9:259-270
5. Wynn TA, Chawla A, Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496:445-455
6. Shi C, Pamer EG (2011) Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11:762-774
7. Satpathy AT, Wu X, Albring JC, Murphy KM (2012) Re (de) fining the dendritic cell lineage. Nat Immunol 13:1145-1154
8. Kawakami T, Lichtnekert J, Thompson LJ, Karna P, Bouabe H, Hohl TM, Heinecke JW, Ziegler SF, Nelson PJ, Duffield JS (2013) Resident renal mononuclear phagocytes comprise five discrete populations with distinct phenotypes and functions. J Immunol 191: 3358-3372
9. Bradford BM, Sester DP, Hume DA, Mabbott NA (2011) Defining the anatomical localisation of subsets of the murine mononuclear phagocyte system using integrin alpha X (Itgax, CD11c) and colony stimulating factor 1 receptor (Csf1r, CD115) expression fails to discriminate dendritic cells from macrophages. Immunobiology 216:1228-1237
10. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23-35
11. Rauch I, Müller M, Decker T (2013) The regulation of inflammation by interferons and their STATs. JAK-STAT 2:e23820
12. Medzhitov R, Janeway C (2000) Innate immune recognition: mechanisms and pathways. Immunol Rev 173:89-97
13. Zhang X,Mosser DM (2008)Macrophage activation by endogenous danger signals. J Pathol 214:161-178
14. Mosser DM (2003) The many faces of macrophage activation. J Leukoc Biol 73:209-212
15. Lawrence T, Natoli G (2011) Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 11:750-761
16. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A, Gherardi RK, Chazaud B (2007) Inflammatorymonocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204:1057-1069
17. Martinez FO, Helming L, Gordon S (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27:451-483
18. Takeda K, Tanaka T, Shi W, Matsumoto M, Minami M, Kashiwamura S, Nakanishi K, Yoshida N, Kishimoto T, Akira S (1996) Essential role of Stat6 in IL-4 signalling. Nature 380:627-630
19. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Red Eagle A, Vats D, Brombacher F, Ferrante AW, Chawla A (2007) Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447:1116-1120
20. Liao X, Sharma N, Kapadia F, Zhou G, Lu Y, Hong H, Paruchuri K, Mahabeleshwar GH, Dalmas E, Venteclef N, Flask CA, Kim J, Doreian BW, Lu KQ, Kaestner KH, Hamik A, Clément K, Jain MK (2011) Krüppel-like factor 4 regulates macrophage polarization. J Clin Invest 121:2736-2749
21. Szanto A, Balint BL, Nagy ZS, Barta E, Dezso B, Pap A, Szeles L, Poliska S, Oros M, Evans RM, Barak Y, Schwabe J, Nagy L (2010) STAT6 transcription factor is a facilitator of the nuclear receptor PPARγ-regulated gene expression in macrophages and dendritic cells. Immunity 33:699-712
22. Huang JT, Welch JS, Ricote M, Binder CJ, Willson TM, Kelly C, Witztum JL, Funk CD, Conrad D, Glass CK (1999) Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature 400:378-382
23. Lehtonen A, Veckman V, Nikula T, Lahesmaa R, Kinnunen L, Matikainen S, Julkunen I (2005) Differential expression of IFN regulatory factor 4 gene in human monocyte-derived dendritic cells and macrophages. J Immunol 175:6570-6579
24. Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, Miyake T, Matsushita K, Okazaki T, Saitoh T, Honma K, Matsuyama T, Yui K, Tsujimura T, Standley DM, Nakanishi K, Nakai K, Akira S (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol 11:936-944
25. Morris SM(2009) Recent advances in argininemetabolism: roles and regulation of the arginases. Br J Pharmacol 157:922-930
26. highregulatory phenotype in macrophages. J Immunol 185:2044-2050
27. Fadok VA, Bratton DL, Konowal A, Freed PW,Westcott JY, Henson PM (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/ paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101:890-898
28. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677-686
29. Sica A,Mantovani A (2012)Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122:787-795
30. Lichtnekert J, Kawakami T, Parks WC, Duffield JS (2013) Changes in macrophage phenotype as the immune response evolves. Curr Opin Pharmacol 13:555-564
31. Li L, Huang L, Sung S-SJ, Vergis AL, Rosin DL, Rose CE, Lobo PI, Okusa MD (2008) The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemiareperfusion injury. Kidney Int 74:1526-1537
32. Furuichi K, Wada T, Iwata Y, Kitagawa K, Kobayashi K-I, Hashimoto H, Ishiwata Y, Asano M, Wang H, Matsushima K, Takeya M, Kuziel WA, Mukaida N, Yokoyama H (2003) CCR2 signaling contributes to ischemia-reperfusion injury in kidney. J Am Soc Nephrol 14:2503-2515
33. Furuichi K, Gao J-L, Murphy PM (2006) Chemokine receptor CX3CR1 regulates renal interstitial fibrosis after ischemiareperfusion injury. Am J Pathol 169:372-387
34. Furuichi K, Gao J-L, Horuk R, Wada T, Kaneko S, Murphy PM (2008) Chemokine receptor CCR1 regulates inflammatory cell infiltration after renal ischemia-reperfusion injury. J Immunol 181:8670-8676
35. Ko GJ, Linfert D, Jang HR, Higbee E,Watkins T, Cheadle C, LiuM, Racusen L, Grigoryev DN, Rabb H (2012) Transcriptional analysis of infiltrating T cells in kidney ischemia-reperfusion injury reveals a pathophysiological role for CCR5. Am J Physiol Renal Physiol 302: F762-F773
36. Day Y-J, Huang L, Ye H, Linden J, Okusa MD (2005) Renal ischemia-reperfusion injury and adenosine 2A receptor-mediated tissue protection: role of macrophages. Am J Physiol Renal Physiol 288:F722-F731
37. Jo S-K, Sung S-A, ChoW-Y, Go K-J, Kim H-K (2006) Macrophages contribute to the initiation of ischaemic acute renal failure in rats. Nephrol Dial Transplant 21:1231-1239
38. Lee S, Huen S, Nishio H, Nishio S, Lee HK, Choi B-S, Ruhrberg C, Cantley LG (2011) Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 22:317-326
39. Vinuesa E, Hotter G, Jung M, Herrero-Fresneda I, Torras J, Sola A (2008) Macrophage involvement in the kidney repair phase after ischaemia/reperfusion injury. J Pathol 214:104-113
40. Ferenbach DA, Sheldrake TA, Dhaliwal K, Kipari TMJ, Marson LP, Kluth DC, Hughes J (2012) Macrophage/monocyte depletion by clodronate, but not diphtheria toxin, improves renal ischemia/ reperfusion injury in mice. Kidney Int 82:928-933
41. Lu L, Faubel S, He Z, Andres-Hernando A, Jani A, Kedl R, Edelstein CL (2012) Depletion of macrophages and dendritic cells in ischemic acute kidney injury. Am J Nephrol 35:181-190
42. Li L, Okusa MD (2010) Macrophages, Dendritic Cells, and Kidney Ischemia-Reperfusion Injury. Semin Nephrol 30:268-277
43. Bajwa A, Huang L, Ye H, Dondeti K, Song S, Rosin DL, Lynch KR, Lobo PI, Li L, Okusa MD (2012) Dendritic cell sphingosine 1-phosphate receptor-3 regulates Th1-Th2 polarity in kidney ischemia-reperfusion injury. J Immunol 189:2584-2596
44. Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315-424
45. Leemans JC, Stokman G, Claessen N, Rouschop KM, Teske GJD, Kirschning CJ, Akira S, van der Poll T, Weening JJ, Florquin S (2005) Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J Clin Invest 115:2894-2903
46. Wu H, Chen G, Wyburn KR, Yin J, Bertolino P, Eris JM, Alexander SI, Sharland AF, Chadban SJ (2007) TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 117: 2847-2859
47. Lech M, Avila-Ferrufino A, Allam R, Segerer S, Khandoga A, Krombach F, Garlanda C, Mantovani A, Anders H-J (2009) Resident dendritic cells prevent postischemic acute renal failure by help of single Ig IL-1 receptor-related protein. J Immunol 183:4109-4118
48. Li L, Huang L, Ye H, Song SP, Bajwa A, Lee SJ, Moser EK, Jaworska K, Kinsey GR, Day YJ, Linden J, Lobo PI, Rosin DL, Okusa MD (2012) Dendritic cells tolerized with adenosine AAR agonist attenuate acute kidney injury. J Clin Invest 122:3931-3942
49. Jang H-S, Kim J, Park Y-K, Park KM(2008) Infiltrated macrophages contribute to recovery after ischemic injury but not to ischemic preconditioning in kidneys. Transplantation 85:447-455
50. Lin S-L, Li B, Rao S, Yeo E-J, Hudson TE, Nowlin BT, Pei H, Chen L, Zheng JJ, Carroll TJ, Pollard JW, McMahon AP, Lang RA, Duffield JS (2010) Macrophage Wnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci U S A 107:4194-4199
51. AlikhanMA, Jones CV,Williams TM, Beckhouse AG, Fletcher AL, Kett MM, Sakkal S, Samuel CS, Ramsay RG, Deane JA, Wells CA, LittleMH, Hume DA, Ricardo SD (2011) Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses. Am J Pathol 179:1243-1256
52. Menke J, Iwata Y, RabacalWA, Basu R, YeungYG, Humphreys BD, Wada T, Schwarting A, Stanley ER, Kelley VR (2009) CSF-1 signals directly to renal tubular epithelial cells to mediate repair in mice. J Clin Invest 119:2330-2342
53. Yokota N, Burne-Taney M, Racusen L, Rabb H (2003) Contrasting roles for STAT4 and STAT6 signal transduction pathways in murine renal ischemia-reperfusion injury. Am J Physiol Renal Physiol 285: F319-F325
54. Huen SC, Cantley LG (2011) Renal Tubular Cells Induce Early Pro-Inflammatory and Late Alternative Activation in Macrophages [Abstract] Poster presented at American Society of Nephrology Kidney Week J Am Soc Nephrol 22:367A
55. Eguchi J, Kong X, Tenta M, Wang X, Kang S, Rosen ED (2013) Interferon regulatory factor 4 regulates obesity-induced inflammation through regulation of adipose tissue macrophage polarization. Diabetes 62:3394-3403
56. Lassen S, LechM, Römmele C, Mittruecker H-W, Mak TW, Anders H-J (2010) Ischemia reperfusion induces IFN regulatory factor 4 in renal dendritic cells, which suppresses postischemic inflammation and prevents acute renal failure. J Immunol 185:1976-1983
57. Sutton TA, Hato T, Mai E, Yoshimoto M, Kuehl S, Anderson M, Mang H, Plotkin Z, Chan RJ, Dagher PC (2013) p53 is renoprotective after ischemic kidney injury by reducing inflammation. J Am Soc Nephrol 24:113-124
58. Pesce JT, Ramalingam TR, Mentink-Kane MM, Wilson MS, El Kasmi KC, Smith AM, Thompson RW, Cheever AW, Murray PJ, Wynn TA (2009) Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog 5:e1000371
59. Miller SB, Martin DR, Kissane J, Hammerman MR (1992) Insulinlike growth factor I accelerates recovery from ischemic acute tubular necrosis in the rat. Proc Natl Acad Sci U S A 89:11876-11880
60. Schmidt IM, Hall IE, Kale S, Lee S, He CH, Lee Y, Chupp GL, Moeckel GW, Lee CG, Elias JA, Parikh CR, Cantley LG (2013) Chitinase-like protein Brp-39/YKL-40 modulates the renal response to ischemic injury and predicts delayed allograft function. J Am Soc Nephrol 24:309-319
61. Ferenbach DA, Nkejabega NCJ, McKay J, Choudhary AK, Vernon MA, Beesley MF, Clay S, Conway BC, Marson LP, Kluth DC, Hughes J (2011) The induction of macrophage hemeoxygenase-1 is protective during acute kidney injury in aging mice. Kidney Int 79: 966-976
62. Ferenbach DA, Ramdas V, Spencer N, Marson L, Anegon I, Hughes J, Kluth DC (2010) Macrophages expressing heme oxygenase-1 improve renal function in ischemia/reperfusion injury. Mol Ther 18: 1706-1713
63. Jung M, Sola A, Hughes J, Kluth DC, Vinuesa E, Viñas JL, Pérez-Ladaga A, Hotter G (2012) Infusion of IL-10-expressing cells protects against renal ischemia through induction of lipocalin-2. Kidney Int 81:969-982
64. Mori K, Lee HT, Rapoport D, Drexler IR, Foster K, Yang J, Schmidt-Ott KM, Chen X, Li JY, Weiss S, Mishra J, Cheema FH, Markowitz G, Suganami T, Sawai K, Mukoyama M, Kunis C, D'Agati V, Devarajan P, Barasch J (2005) Endocytic delivery of lipocalinsiderophore-iron complex rescues the kidney from ischemiareperfusion injury. J Clin Invest 115:610-621
65. Ranganathan PV, Jayakumar C, Ramesh G (2013) Netrin-1-treated macrophages protect the kidney against ischemia-reperfusion injury and suppress inflammation by inducing M2 polarization. Am J Physiol Renal Physiol 304:F948-F957
66. Sean Eardley K, Cockwell P (2005) Macrophages and progressive tubulointerstitial disease. Kidney Int 68:437-455
67. Ko GJ, Boo C-S, Jo S-K, Cho WY, Kim HK (2008) Macrophages contribute to the development of renal fibrosis following ischaemia/ reperfusion-induced acute kidney injury. Nephrol Dial Transplant 23: 842-852
68. Duffield JS, Lupher M, Thannickal VJ, Wynn TA (2013) Host responses in tissue repair and fibrosis. Annu Rev Pathol Mech Dis 8:241-276
69. Boor P, Ostendorf T, Floege J (2010) Renal fibrosis: novel insights into mechanisms and therapeutic targets. Nat Rev Nephrol 6:643-656
70. Huen SC, Moeckel GW, Cantley LG (2013) Macrophage-specific deletion of transforming growth factor-β1 does not prevent renal fibrosis after severe ischemia-reperfusion or obstructive injury. Am J Physiol Renal Physiol 305:F477-F484
71. Campanholle G,Mittelsteadt K, Nakagawa S, Kobayashi A, Lin S-L, Gharib SA, Heinecke JW, Hamerman JA, AltemeierWA, Duffield JS (2013) TLR-2/TLR-4 TREM-1 signaling pathway is dispensable in inflammatory myeloid cells during sterile kidney injury. PLoS ONE 8:e68640
72. Castaño AP, Lin S-L, Surowy T, Nowlin BT, Turlapati SA, Patel T, Singh A, Li S, Lupher ML, Duffield JS (2009) Serum amyloid P inhibits fibrosis through Fc gamma R-dependent monocyte-macrophage regulation in vivo. Sci Transl Med 1:5ra13