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Published in: Pediatric Nephrology 4/2019

01-04-2019 | Review

The role of macrophages during acute kidney injury: destruction and repair

Authors: Hwa I. Han, Lauren B. Skvarca, Eugenel B. Espiritu, Alan J. Davidson, Neil A. Hukriede

Published in: Pediatric Nephrology | Issue 4/2019

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Abstract

Acute kidney injury (AKI) is defined by a rapid decline in renal function. Regardless of the initial cause of injury, the influx of immune cells is a common theme during AKI. While an inflammatory response is critical for the initial control of injury, a prolonged response can negatively affect tissue repair. In this review, we focus on the role of macrophages, from early inflammation to resolution, during AKI. These cells serve as the innate defense system by phagocytosing cellular debris and pathogenic molecules and bridge communication with the adaptive immune system by acting as antigen-presenting cells and secreting cytokines. While many immune cells function to initiate inflammation, macrophages play a complex role throughout AKI. This complexity is driven by their functional plasticity: the ability to polarize from a “pro-inflammatory” phenotype to a “pro-reparative” phenotype. Importantly, experimental and translational studies indicate that macrophage polarization opens the possibility to generate novel therapeutics to promote repair during AKI. A thorough understanding of the biological roles these phagocytes play during both injury and repair is necessary to understand the limitations while furthering the therapeutic application.
Literature
1.
go back to reference Jang HR, Rabb H (2015) Immune cells in experimental acute kidney injury. Nat Rev Nephrol 11:88–101CrossRefPubMed Jang HR, Rabb H (2015) Immune cells in experimental acute kidney injury. Nat Rev Nephrol 11:88–101CrossRefPubMed
3.
go back to reference Varol C, Mildner A, Jung S (2015) Macrophages: development and tissue specialization. Annu Rev Immunol 33:643–675CrossRefPubMed Varol C, Mildner A, Jung S (2015) Macrophages: development and tissue specialization. Annu Rev Immunol 33:643–675CrossRefPubMed
5.
go back to reference Mescher AL (2017) Macrophages and fibroblasts during inflammation and tissue repair in models of organ regeneration. Regeneration (Oxf) 4:39–53CrossRef Mescher AL (2017) Macrophages and fibroblasts during inflammation and tissue repair in models of organ regeneration. Regeneration (Oxf) 4:39–53CrossRef
6.
go back to reference Liang H, Xu F, Wen XJ, Liu HZ, Wang HB, Zhong JY, Yang CX, Zhang B (2017) Interleukin-33 signaling contributes to renal fibrosis following ischemia reperfusion. Eur J Pharmacol 812:18–27CrossRefPubMed Liang H, Xu F, Wen XJ, Liu HZ, Wang HB, Zhong JY, Yang CX, Zhang B (2017) Interleukin-33 signaling contributes to renal fibrosis following ischemia reperfusion. Eur J Pharmacol 812:18–27CrossRefPubMed
7.
go back to reference Stifano G, Affandi AJ, Mathes AL, Rice LM, Nakerakanti S, Nazari B, Lee J, Christmann RB, Lafyatis R (2014) Chronic toll-like receptor 4 stimulation in skin induces inflammation, macrophage activation, transforming growth factor beta signature gene expression, and fibrosis. Arthritis Res Ther 16:R136CrossRefPubMedPubMedCentral Stifano G, Affandi AJ, Mathes AL, Rice LM, Nakerakanti S, Nazari B, Lee J, Christmann RB, Lafyatis R (2014) Chronic toll-like receptor 4 stimulation in skin induces inflammation, macrophage activation, transforming growth factor beta signature gene expression, and fibrosis. Arthritis Res Ther 16:R136CrossRefPubMedPubMedCentral
8.
go back to reference van Furth R, Cohn ZA, Hirsch JG, Humphrey JH, Spector WG, Langevoort HL (1972) The mononuclear phagocyte system: a new classification of macrophages, monocytes, and their precursor cells. Bull World Health Organ 46:845–852PubMedPubMedCentral van Furth R, Cohn ZA, Hirsch JG, Humphrey JH, Spector WG, Langevoort HL (1972) The mononuclear phagocyte system: a new classification of macrophages, monocytes, and their precursor cells. Bull World Health Organ 46:845–852PubMedPubMedCentral
9.
go back to reference Davidson AJ, Zon LI (2004) The ‘definitive’ (and ‘primitive’) guide to zebrafish hematopoiesis. Oncogene 23:7233–7246CrossRefPubMed Davidson AJ, Zon LI (2004) The ‘definitive’ (and ‘primitive’) guide to zebrafish hematopoiesis. Oncogene 23:7233–7246CrossRefPubMed
10.
go back to reference Gentek R, Molawi K, Sieweke MH (2014) Tissue macrophage identity and self-renewal. Immunol Rev 262:56–73CrossRefPubMed Gentek R, Molawi K, Sieweke MH (2014) Tissue macrophage identity and self-renewal. Immunol Rev 262:56–73CrossRefPubMed
11.
go back to reference Conger J (1997) Hemodynamic factors in acute renal failure. Adv Ren Replace Ther 4:25–37PubMed Conger J (1997) Hemodynamic factors in acute renal failure. Adv Ren Replace Ther 4:25–37PubMed
12.
go back to reference Brooks DP (1996) Role of endothelin in renal function and dysfunction. Clin Exp Pharmacol Physiol 23:345–348CrossRefPubMed Brooks DP (1996) Role of endothelin in renal function and dysfunction. Clin Exp Pharmacol Physiol 23:345–348CrossRefPubMed
15.
go back to reference Ysebaert DK, De Greef KE, Vercauteren SR, Ghielli M, Verpooten GA, Eyskens EJ, De Broe ME (2000) Identification and kinetics of leukocytes after severe ischaemia/reperfusion renal injury. Nephrol Dial Transplant 15:1562–1574CrossRefPubMed Ysebaert DK, De Greef KE, Vercauteren SR, Ghielli M, Verpooten GA, Eyskens EJ, De Broe ME (2000) Identification and kinetics of leukocytes after severe ischaemia/reperfusion renal injury. Nephrol Dial Transplant 15:1562–1574CrossRefPubMed
17.
go back to reference Chauhan P, Sodhi A, Shrivastava A (2009) Cisplatin primes murine peritoneal macrophages for enhanced expression of nitric oxide, proinflammatory cytokines, TLRs, transcription factors and activation of MAP kinases upon co-incubation with L929 cells. Immunobiology 214:197–209CrossRefPubMed Chauhan P, Sodhi A, Shrivastava A (2009) Cisplatin primes murine peritoneal macrophages for enhanced expression of nitric oxide, proinflammatory cytokines, TLRs, transcription factors and activation of MAP kinases upon co-incubation with L929 cells. Immunobiology 214:197–209CrossRefPubMed
18.
go back to reference Zhang MZ, Yao B, Yang S, Jiang L, Wang S, Fan X, Yin H, Wong K, Miyazawa T, Chen J, Chang I, Singh A, Harris RC (2012) CSF-1 signaling mediates recovery from acute kidney injury. J Clin Invest 122:4519–4532CrossRefPubMedPubMedCentral Zhang MZ, Yao B, Yang S, Jiang L, Wang S, Fan X, Yin H, Wong K, Miyazawa T, Chen J, Chang I, Singh A, Harris RC (2012) CSF-1 signaling mediates recovery from acute kidney injury. J Clin Invest 122:4519–4532CrossRefPubMedPubMedCentral
19.
20.
go back to reference Gottlieb RA (2011) Cell death pathways in acute ischemia/reperfusion injury. J Cardiovasc Pharmacol Ther 16:233–238CrossRefPubMed Gottlieb RA (2011) Cell death pathways in acute ischemia/reperfusion injury. J Cardiovasc Pharmacol Ther 16:233–238CrossRefPubMed
21.
go back to reference Lee S, Huen S, Nishio H, Nishio S, Lee HK, Choi BS, Ruhrberg C, Cantley LG (2011) Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 22:317–326CrossRefPubMedPubMedCentral Lee S, Huen S, Nishio H, Nishio S, Lee HK, Choi BS, Ruhrberg C, Cantley LG (2011) Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 22:317–326CrossRefPubMedPubMedCentral
23.
go back to reference Kroner A, Greenhalgh AD, Zarruk JG, Passos Dos Santos R, Gaestel M, David S (2014) TNF and increased intracellular iron alter macrophage polarization to a detrimental M1 phenotype in the injured spinal cord. Neuron 83:1098–1116CrossRefPubMed Kroner A, Greenhalgh AD, Zarruk JG, Passos Dos Santos R, Gaestel M, David S (2014) TNF and increased intracellular iron alter macrophage polarization to a detrimental M1 phenotype in the injured spinal cord. Neuron 83:1098–1116CrossRefPubMed
24.
go back to reference Huen SC, Huynh L, Marlier A, Lee Y, Moeckel GW, Cantley LG (2015) GM-CSF promotes macrophage alternative activation after renal ischemia/reperfusion injury. J Am Soc Nephrol 26:1334–1345CrossRefPubMed Huen SC, Huynh L, Marlier A, Lee Y, Moeckel GW, Cantley LG (2015) GM-CSF promotes macrophage alternative activation after renal ischemia/reperfusion injury. J Am Soc Nephrol 26:1334–1345CrossRefPubMed
25.
go back to reference de Gaetano M, Crean D, Barry M, Belton O (2016) M1- and M2-type macrophage responses are predictive of adverse outcomes in human atherosclerosis. Front Immunol 7:275CrossRefPubMedPubMedCentral de Gaetano M, Crean D, Barry M, Belton O (2016) M1- and M2-type macrophage responses are predictive of adverse outcomes in human atherosclerosis. Front Immunol 7:275CrossRefPubMedPubMedCentral
26.
go back to reference Klinkert K, Whelan D, Clover AJP, Leblond AL, Kumar AHS, Caplice NM (2017) Selective M2 macrophage depletion leads to prolonged inflammation in surgical wounds. Eur Surg Res 58:109–120CrossRefPubMed Klinkert K, Whelan D, Clover AJP, Leblond AL, Kumar AHS, Caplice NM (2017) Selective M2 macrophage depletion leads to prolonged inflammation in surgical wounds. Eur Surg Res 58:109–120CrossRefPubMed
27.
go back to reference Melgar-Lesmes P, Edelman ER (2015) Monocyte-endothelial cell interactions in the regulation of vascular sprouting and liver regeneration in mouse. J Hepatol 63:917–925CrossRefPubMedPubMedCentral Melgar-Lesmes P, Edelman ER (2015) Monocyte-endothelial cell interactions in the regulation of vascular sprouting and liver regeneration in mouse. J Hepatol 63:917–925CrossRefPubMedPubMedCentral
28.
go back to reference Lee H, Liao JJ, Graeler M, Huang MC, Goetzl EJ (2002) Lysophospholipid regulation of mononuclear phagocytes. Biochim Biophys Acta 1582:175–177CrossRefPubMed Lee H, Liao JJ, Graeler M, Huang MC, Goetzl EJ (2002) Lysophospholipid regulation of mononuclear phagocytes. Biochim Biophys Acta 1582:175–177CrossRefPubMed
30.
go back to reference Saha S, Aranda E, Hayakawa Y, Bhanja P, Atay S, Brodin NP, Li J, Asfaha S, Liu L, Tailor Y, Zhang J, Godwin AK, Tome WA, Wang TC, Guha C, Pollard JW (2016) Macrophage-derived extracellular vesicle-packaged WNTs rescue intestinal stem cells and enhance survival after radiation injury. Nat Commun 7:13096CrossRefPubMedPubMedCentral Saha S, Aranda E, Hayakawa Y, Bhanja P, Atay S, Brodin NP, Li J, Asfaha S, Liu L, Tailor Y, Zhang J, Godwin AK, Tome WA, Wang TC, Guha C, Pollard JW (2016) Macrophage-derived extracellular vesicle-packaged WNTs rescue intestinal stem cells and enhance survival after radiation injury. Nat Commun 7:13096CrossRefPubMedPubMedCentral
31.
go back to reference Long ME, Eddy WE, Gong KQ, Lovelace-Macon LL, McMahan RS, Charron J, Liles WC, Manicone AM (2017) MEK1/2 inhibition promotes macrophage reparative properties. J Immunol 198:862–872CrossRefPubMed Long ME, Eddy WE, Gong KQ, Lovelace-Macon LL, McMahan RS, Charron J, Liles WC, Manicone AM (2017) MEK1/2 inhibition promotes macrophage reparative properties. J Immunol 198:862–872CrossRefPubMed
32.
go back to reference Lin SL, Li B, Rao S, Yeo EJ, 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 USA 107:4194–4199CrossRefPubMed Lin SL, Li B, Rao S, Yeo EJ, 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 USA 107:4194–4199CrossRefPubMed
33.
go back to reference Lech M, Grobmayr R, Ryu M, Lorenz G, Hartter I, Mulay SR, Susanti HE, Kobayashi KS, Flavell RA, Anders HJ (2014) Macrophage phenotype controls long-term AKI outcomes—kidney regeneration versus atrophy. J Am Soc Nephrol 25:292–304CrossRefPubMed Lech M, Grobmayr R, Ryu M, Lorenz G, Hartter I, Mulay SR, Susanti HE, Kobayashi KS, Flavell RA, Anders HJ (2014) Macrophage phenotype controls long-term AKI outcomes—kidney regeneration versus atrophy. J Am Soc Nephrol 25:292–304CrossRefPubMed
34.
go back to reference Wang S, Zhang C, Li J, Niyazi S, Zheng L, Xu M, Rong R, Yang C, Zhu T (2017) Erythropoietin protects against rhabdomyolysis-induced acute kidney injury by modulating macrophage polarization. Cell Death Dis 8:e2725CrossRefPubMedPubMedCentral Wang S, Zhang C, Li J, Niyazi S, Zheng L, Xu M, Rong R, Yang C, Zhu T (2017) Erythropoietin protects against rhabdomyolysis-induced acute kidney injury by modulating macrophage polarization. Cell Death Dis 8:e2725CrossRefPubMedPubMedCentral
35.
go back to reference Chiba T, Skrypnyk NI, Skvarca LB, Penchev R, Zhang KX, Rochon ER, Fall JL, Paueksakon P, Yang H, Alford CE, Roman BL, Zhang MZ, Harris R, Hukriede NA, de Caestecker MP (2016) Retinoic acid Signaling coordinates macrophage-dependent injury and repair after AKI. J Am Soc Nephrol 27:495–508CrossRefPubMed Chiba T, Skrypnyk NI, Skvarca LB, Penchev R, Zhang KX, Rochon ER, Fall JL, Paueksakon P, Yang H, Alford CE, Roman BL, Zhang MZ, Harris R, Hukriede NA, de Caestecker MP (2016) Retinoic acid Signaling coordinates macrophage-dependent injury and repair after AKI. J Am Soc Nephrol 27:495–508CrossRefPubMed
36.
go back to reference Geng Y, Zhang L, Fu B, Zhang J, Hong Q, Hu J, Li D, Luo C, Cui S, Zhu F, Chen X (2014) Mesenchymal stem cells ameliorate rhabdomyolysis-induced acute kidney injury via the activation of M2 macrophages. Stem Cell Res Ther 5:80CrossRefPubMedPubMedCentral Geng Y, Zhang L, Fu B, Zhang J, Hong Q, Hu J, Li D, Luo C, Cui S, Zhu F, Chen X (2014) Mesenchymal stem cells ameliorate rhabdomyolysis-induced acute kidney injury via the activation of M2 macrophages. Stem Cell Res Ther 5:80CrossRefPubMedPubMedCentral
37.
go back to reference Bagnis C, Beaufils H, Jacquiaud C, Adabra Y, Jouanneau C, Le Nahour G, Jaudon MC, Bourbouze R, Jacobs C, Deray G (2001) Erythropoietin enhances recovery after cisplatin-induced acute renal failure in the rat. Nephrol Dial Transplant 16:932–938CrossRefPubMed Bagnis C, Beaufils H, Jacquiaud C, Adabra Y, Jouanneau C, Le Nahour G, Jaudon MC, Bourbouze R, Jacobs C, Deray G (2001) Erythropoietin enhances recovery after cisplatin-induced acute renal failure in the rat. Nephrol Dial Transplant 16:932–938CrossRefPubMed
38.
go back to reference Eirin A, Zhu XY, Puranik AS, Tang H, McGurren KA, van Wijnen AJ, Lerman A, Lerman LO (2017) Mesenchymal stem cell-derived extracellular vesicles attenuate kidney inflammation. Kidney Int 92:114–124CrossRefPubMedPubMedCentral Eirin A, Zhu XY, Puranik AS, Tang H, McGurren KA, van Wijnen AJ, Lerman A, Lerman LO (2017) Mesenchymal stem cell-derived extracellular vesicles attenuate kidney inflammation. Kidney Int 92:114–124CrossRefPubMedPubMedCentral
39.
go back to reference Tanaka K, Tanabe K, Nishii N, Takiue K, Sugiyama H, Wada J (2017) Sustained Tubulointerstitial inflammation in kidney with severe leptospirosis. Intern Med 56:1179–1184CrossRefPubMedPubMedCentral Tanaka K, Tanabe K, Nishii N, Takiue K, Sugiyama H, Wada J (2017) Sustained Tubulointerstitial inflammation in kidney with severe leptospirosis. Intern Med 56:1179–1184CrossRefPubMedPubMedCentral
40.
go back to reference Rubio-Navarro A, Carril M, Padro D, Guerrero-Hue M, Tarin C, Samaniego R, Cannata P, Cano A, Villalobos JM, Sevillano AM, Yuste C, Gutierrez E, Praga M, Egido J, Moreno JA (2016) CD163-macrophages are involved in rhabdomyolysis-induced kidney injury and may be detected by MRI with targeted gold-coated iron oxide nanoparticles. Theranostics 6:896–914CrossRefPubMedPubMedCentral Rubio-Navarro A, Carril M, Padro D, Guerrero-Hue M, Tarin C, Samaniego R, Cannata P, Cano A, Villalobos JM, Sevillano AM, Yuste C, Gutierrez E, Praga M, Egido J, Moreno JA (2016) CD163-macrophages are involved in rhabdomyolysis-induced kidney injury and may be detected by MRI with targeted gold-coated iron oxide nanoparticles. Theranostics 6:896–914CrossRefPubMedPubMedCentral
41.
go back to reference Gutierrez E, Egido J, Rubio-Navarro A, Buendia I, Blanco Colio LM, Toldos O, Manzarbeitia F, de Lorenzo A, Sanchez R, Ortiz A, Praga M, Moreno JA (2012) Oxidative stress, macrophage infiltration and CD163 expression are determinants of long-term renal outcome in macrohematuria-induced acute kidney injury of IgA nephropathy. Nephron Clin Pract 121:c42–c53CrossRefPubMed Gutierrez E, Egido J, Rubio-Navarro A, Buendia I, Blanco Colio LM, Toldos O, Manzarbeitia F, de Lorenzo A, Sanchez R, Ortiz A, Praga M, Moreno JA (2012) Oxidative stress, macrophage infiltration and CD163 expression are determinants of long-term renal outcome in macrohematuria-induced acute kidney injury of IgA nephropathy. Nephron Clin Pract 121:c42–c53CrossRefPubMed
42.
go back to reference Barkhordari K, Karimi A, Shafiee A, Soltaninia H, Khatami MR, Abbasi K, Yousefshahi F, Haghighat B, Brown V (2011) Effect of pentoxifylline on preventing acute kidney injury after cardiac surgery by measuring urinary neutrophil gelatinase-associated lipocalin. J Cardiothorac Surg 19:6–8 Barkhordari K, Karimi A, Shafiee A, Soltaninia H, Khatami MR, Abbasi K, Yousefshahi F, Haghighat B, Brown V (2011) Effect of pentoxifylline on preventing acute kidney injury after cardiac surgery by measuring urinary neutrophil gelatinase-associated lipocalin. J Cardiothorac Surg 19:6–8
43.
go back to reference Tasanarong A, Duangchana S, Sumransurp S, Homvises B, Satdhabudha O (2013) Prophylaxis with erythropoietin versus placebo reduces acute kidney injury and neutrophil gelatinase-associated lipocalin in patients undergoing cardiac surgery: a randomized, double-blind controlled trial. BMC Nephrol 14:136CrossRefPubMedPubMedCentral Tasanarong A, Duangchana S, Sumransurp S, Homvises B, Satdhabudha O (2013) Prophylaxis with erythropoietin versus placebo reduces acute kidney injury and neutrophil gelatinase-associated lipocalin in patients undergoing cardiac surgery: a randomized, double-blind controlled trial. BMC Nephrol 14:136CrossRefPubMedPubMedCentral
44.
go back to reference Oh SW, Chin HJ, Chae DW, Na KY (2012) Erythropoietin improves long-term outcomes in patients with acute kidney injury after coronary artery bypass grafting. J Korean Med Sci 27:506–511CrossRefPubMedPubMedCentral Oh SW, Chin HJ, Chae DW, Na KY (2012) Erythropoietin improves long-term outcomes in patients with acute kidney injury after coronary artery bypass grafting. J Korean Med Sci 27:506–511CrossRefPubMedPubMedCentral
45.
go back to reference Kim JE, Song SW, Kim JY, Lee HJ, Chung KH, Shim YH (2016) Effect of a single bolus of erythropoietin on Renoprotection in patients undergoing thoracic aortic surgery with moderate hypothermic circulatory arrest. Ann Thorac Surg 101:690–696CrossRefPubMed Kim JE, Song SW, Kim JY, Lee HJ, Chung KH, Shim YH (2016) Effect of a single bolus of erythropoietin on Renoprotection in patients undergoing thoracic aortic surgery with moderate hypothermic circulatory arrest. Ann Thorac Surg 101:690–696CrossRefPubMed
46.
go back to reference Cagli K, Ulas MM, Ozisik K, Kale A, Bakuy V, Emir M, Balci M, Topbas M, Sener E, Tasdemir O (2005) The intraoperative effect of pentoxifylline on the inflammatory process and leukocytes in cardiac surgery patients undergoing cardiopulmonary bypass. Perfusion 20:45–51CrossRefPubMed Cagli K, Ulas MM, Ozisik K, Kale A, Bakuy V, Emir M, Balci M, Topbas M, Sener E, Tasdemir O (2005) The intraoperative effect of pentoxifylline on the inflammatory process and leukocytes in cardiac surgery patients undergoing cardiopulmonary bypass. Perfusion 20:45–51CrossRefPubMed
47.
go back to reference Wang ZY, Zhang Q, Liao ZJ, Han CM, Lv GZ, Luo CQ, Chen J, Yang SX, Yang XD, Liu Q (2008) Effect of recombinant human granulocyte-macrophage colony stimulating factor on wound healing in patients with deep partial thickness burn. Zhonghua Shao Shang Za Zhi 24:107–110PubMed Wang ZY, Zhang Q, Liao ZJ, Han CM, Lv GZ, Luo CQ, Chen J, Yang SX, Yang XD, Liu Q (2008) Effect of recombinant human granulocyte-macrophage colony stimulating factor on wound healing in patients with deep partial thickness burn. Zhonghua Shao Shang Za Zhi 24:107–110PubMed
48.
49.
go back to reference el Nahas AM (1991) The role of growth hormone and insulin-like growth factor-I in experimental renal growth and scarring. Am J Kidney Dis 17:677–679CrossRefPubMed el Nahas AM (1991) The role of growth hormone and insulin-like growth factor-I in experimental renal growth and scarring. Am J Kidney Dis 17:677–679CrossRefPubMed
50.
go back to reference Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interf Cytokine Res 29:313–326CrossRef Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interf Cytokine Res 29:313–326CrossRef
51.
go back to reference Amann B, Tinzmann R, Angelkort B (2003) ACE inhibitors improve diabetic nephropathy through suppression of renal MCP-1. Diabetes Care 26:2421–2425CrossRefPubMed Amann B, Tinzmann R, Angelkort B (2003) ACE inhibitors improve diabetic nephropathy through suppression of renal MCP-1. Diabetes Care 26:2421–2425CrossRefPubMed
52.
go back to reference Mercalli A, Calavita I, Dugnani E, Citro A, Cantarelli E, Nano R, Melzi R, Maffi P, Secchi A, Sordi V, Piemonti L (2013) Rapamycin unbalances the polarization of human macrophages to M1. Immunology 140:179–190CrossRefPubMedPubMedCentral Mercalli A, Calavita I, Dugnani E, Citro A, Cantarelli E, Nano R, Melzi R, Maffi P, Secchi A, Sordi V, Piemonti L (2013) Rapamycin unbalances the polarization of human macrophages to M1. Immunology 140:179–190CrossRefPubMedPubMedCentral
53.
go back to reference Wingert RA, Davidson AJ (2008) The zebrafish pronephros: a model to study nephron segmentation. Kidney Int 73:1120–1127CrossRefPubMed Wingert RA, Davidson AJ (2008) The zebrafish pronephros: a model to study nephron segmentation. Kidney Int 73:1120–1127CrossRefPubMed
54.
57.
go back to reference Cianciolo Cosentino C, Skrypnyk NI, Brilli LL, Chiba T, Novitskaya T, Woods C, West J, Korotchenko VN, McDermott L, Day BW, Davidson AJ, Harris RC, de Caestecker MP, Hukriede NA (2013) Histone deacetylase inhibitor enhances recovery after AKI. J Am Soc Nephrol 24:943–953CrossRefPubMedPubMedCentral Cianciolo Cosentino C, Skrypnyk NI, Brilli LL, Chiba T, Novitskaya T, Woods C, West J, Korotchenko VN, McDermott L, Day BW, Davidson AJ, Harris RC, de Caestecker MP, Hukriede NA (2013) Histone deacetylase inhibitor enhances recovery after AKI. J Am Soc Nephrol 24:943–953CrossRefPubMedPubMedCentral
58.
go back to reference Humphreys BD, Czerniak S, DiRocco DP, Hasnain W, Cheema R, Bonventre JV (2011) Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci USA 108:9226–9231CrossRefPubMed Humphreys BD, Czerniak S, DiRocco DP, Hasnain W, Cheema R, Bonventre JV (2011) Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci USA 108:9226–9231CrossRefPubMed
59.
go back to reference Yin W, Naini SM, Chen G, Hentschel DM, Humphreys BD, Bonventre JV (2016) Mammalian target of rapamycin mediates kidney injury molecule 1-dependent tubule injury in a surrogate model. J Am Soc Nephrol 27:1943–1957CrossRefPubMed Yin W, Naini SM, Chen G, Hentschel DM, Humphreys BD, Bonventre JV (2016) Mammalian target of rapamycin mediates kidney injury molecule 1-dependent tubule injury in a surrogate model. J Am Soc Nephrol 27:1943–1957CrossRefPubMed
60.
go back to reference Cirio MC, de Groh ED, de Caestecker MP, Davidson AJ, Hukriede NA (2014) Kidney regeneration: common themes from the embryo to the adult. Pediatr Nephrol 29:553–564CrossRefPubMed Cirio MC, de Groh ED, de Caestecker MP, Davidson AJ, Hukriede NA (2014) Kidney regeneration: common themes from the embryo to the adult. Pediatr Nephrol 29:553–564CrossRefPubMed
61.
go back to reference Hentschel DM, Park KM, Cilenti L, Zervos AS, Drummond I, Bonventre JV (2005) Acute renal failure in zebrafish: a novel system to study a complex disease. Am J Physiol Renal Physiol 288:F923–F929CrossRefPubMed Hentschel DM, Park KM, Cilenti L, Zervos AS, Drummond I, Bonventre JV (2005) Acute renal failure in zebrafish: a novel system to study a complex disease. Am J Physiol Renal Physiol 288:F923–F929CrossRefPubMed
62.
go back to reference deGroh ED, Swanhart LM, Cosentino CC, Jackson RL, Dai W, Kitchens CA, Day BW, Smithgall TE, Hukriede NA (2010) Inhibition of histone deacetylase expands the renal progenitor cell population. J Am Soc Nephrol 21:794–802CrossRef deGroh ED, Swanhart LM, Cosentino CC, Jackson RL, Dai W, Kitchens CA, Day BW, Smithgall TE, Hukriede NA (2010) Inhibition of histone deacetylase expands the renal progenitor cell population. J Am Soc Nephrol 21:794–802CrossRef
63.
go back to reference Skrypnyk NI, Sanker S, Brilli-Skvarca L, Novitskaya T, Woods C, Chiba T, Patel K, Goldberg ND, McDermott L, Vinson PN, Calcutt MW, Huryn DM, Vernetti LA, Vogt A, Hukriede N, de Caestecker MP (2015) Delayed treatment with PTBA analogs reduces post injury renal fibrosis after kidney injury. Am J Physiol Renal Physiol 310:F705–F716CrossRefPubMedPubMedCentral Skrypnyk NI, Sanker S, Brilli-Skvarca L, Novitskaya T, Woods C, Chiba T, Patel K, Goldberg ND, McDermott L, Vinson PN, Calcutt MW, Huryn DM, Vernetti LA, Vogt A, Hukriede N, de Caestecker MP (2015) Delayed treatment with PTBA analogs reduces post injury renal fibrosis after kidney injury. Am J Physiol Renal Physiol 310:F705–F716CrossRefPubMedPubMedCentral
64.
go back to reference Sanker S, Cirio MC, Vollmer LL, Goldberg ND, McDermott LA, Hukriede NA, Vogt A (2013) Development of high-content assays for kidney progenitor cell expansion in transgenic zebrafish. J Biomol Screen 18:1193–1202CrossRefPubMed Sanker S, Cirio MC, Vollmer LL, Goldberg ND, McDermott LA, Hukriede NA, Vogt A (2013) Development of high-content assays for kidney progenitor cell expansion in transgenic zebrafish. J Biomol Screen 18:1193–1202CrossRefPubMed
65.
go back to reference Ellett F, Lieschke GJ (2010) Zebrafish as a model for vertebrate hematopoiesis. Curr Opin Pharmacol 10:563–570CrossRefPubMed Ellett F, Lieschke GJ (2010) Zebrafish as a model for vertebrate hematopoiesis. Curr Opin Pharmacol 10:563–570CrossRefPubMed
66.
go back to reference Murayama E, Kissa K, Zapata A, Mordelet E, Briolat V, Lin HF, Handin RI, Herbomel P (2006) Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25:963–975CrossRefPubMed Murayama E, Kissa K, Zapata A, Mordelet E, Briolat V, Lin HF, Handin RI, Herbomel P (2006) Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25:963–975CrossRefPubMed
67.
go back to reference Yu T, Guo W, Tian Y, Xu J, Chen J, Li L, Wen Z (2017) Distinct regulatory networks control the development of macrophages of different origins in zebrafish. Blood 129:509–519CrossRefPubMed Yu T, Guo W, Tian Y, Xu J, Chen J, Li L, Wen Z (2017) Distinct regulatory networks control the development of macrophages of different origins in zebrafish. Blood 129:509–519CrossRefPubMed
68.
go back to reference Henry KM, Loynes CA, Whyte MK, Renshaw SA (2013) Zebrafish as a model for the study of neutrophil biology. J Leukoc Biol 94:633–642CrossRefPubMed Henry KM, Loynes CA, Whyte MK, Renshaw SA (2013) Zebrafish as a model for the study of neutrophil biology. J Leukoc Biol 94:633–642CrossRefPubMed
69.
go back to reference Hall C, Flores MV, Storm T, Crosier K, Crosier P (2007) The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish. BMC Dev Biol 7:42CrossRefPubMedPubMedCentral Hall C, Flores MV, Storm T, Crosier K, Crosier P (2007) The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish. BMC Dev Biol 7:42CrossRefPubMedPubMedCentral
70.
go back to reference Ellett F, Pase L, Hayman JW, Andrianopoulos A, Lieschke GJ (2011) mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117:e49–e56CrossRefPubMedPubMedCentral Ellett F, Pase L, Hayman JW, Andrianopoulos A, Lieschke GJ (2011) mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117:e49–e56CrossRefPubMedPubMedCentral
71.
72.
go back to reference Wu J, Choi TY, Shin D (2017) tomm22 knockdown-mediated hepatocyte damages elicit both the formation of hybrid hepatocytes and biliary conversion to hepatocytes in zebrafish larvae. Gene Expr 17:237–249CrossRefPubMedPubMedCentral Wu J, Choi TY, Shin D (2017) tomm22 knockdown-mediated hepatocyte damages elicit both the formation of hybrid hepatocytes and biliary conversion to hepatocytes in zebrafish larvae. Gene Expr 17:237–249CrossRefPubMedPubMedCentral
73.
go back to reference Nguyen-Chi M, Laplace-Builhe B, Travnickova J, Luz-Crawford P, Tejedor G, Phan QT, Duroux-Richard I, Levraud JP, Kissa K, Lutfalla G, Jorgensen C, Djouad F (2015) Identification of polarized macrophage subsets in zebrafish. Elife 4:e07288. https://doi.org/10.7554/eLife.07288 Nguyen-Chi M, Laplace-Builhe B, Travnickova J, Luz-Crawford P, Tejedor G, Phan QT, Duroux-Richard I, Levraud JP, Kissa K, Lutfalla G, Jorgensen C, Djouad F (2015) Identification of polarized macrophage subsets in zebrafish. Elife 4:e07288. https://​doi.​org/​10.​7554/​eLife.​07288
74.
go back to reference Chen L, Sha ML, Li D, Zhu YP, Wang XJ, Jiang CY, Xia SJ, Shao Y (2017) Relaxin abrogates renal interstitial fibrosis by regulating macrophage polarization via inhibition of Toll-like receptor 4 signaling. Oncotarget 8:21044–21053PubMedPubMedCentral Chen L, Sha ML, Li D, Zhu YP, Wang XJ, Jiang CY, Xia SJ, Shao Y (2017) Relaxin abrogates renal interstitial fibrosis by regulating macrophage polarization via inhibition of Toll-like receptor 4 signaling. Oncotarget 8:21044–21053PubMedPubMedCentral
77.
go back to reference Zhang MZ, Wang X, Wang Y, Niu A, Wang S, Zou C, Harris RC (2017) IL-4/IL-13-mediated polarization of renal macrophages/dendritic cells to an M2a phenotype is essential for recovery from acute kidney injury. Kidney Int 91:375–386CrossRefPubMed Zhang MZ, Wang X, Wang Y, Niu A, Wang S, Zou C, Harris RC (2017) IL-4/IL-13-mediated polarization of renal macrophages/dendritic cells to an M2a phenotype is essential for recovery from acute kidney injury. Kidney Int 91:375–386CrossRefPubMed
78.
go back to reference Chen X, Wang CC, Song SM, Wei SY, Li JS, Zhao SL, Li B (2015) The administration of erythropoietin attenuates kidney injury induced by ischemia/reperfusion with increased activation of Wnt/beta-catenin signaling. J Formos Med Assoc 114:430–437CrossRefPubMed Chen X, Wang CC, Song SM, Wei SY, Li JS, Zhao SL, Li B (2015) The administration of erythropoietin attenuates kidney injury induced by ischemia/reperfusion with increased activation of Wnt/beta-catenin signaling. J Formos Med Assoc 114:430–437CrossRefPubMed
79.
go back to reference Wang Y, Chang J, Yao B, Niu A, Kelly E, Breeggemann MC, Abboud Werner SL, Harris RC, Zhang MZ (2015) Proximal tubule-derived colony stimulating factor-1 mediates polarization of renal macrophages and dendritic cells, and recovery in acute kidney injury. Kidney Int 88:1274–1282CrossRefPubMedPubMedCentral Wang Y, Chang J, Yao B, Niu A, Kelly E, Breeggemann MC, Abboud Werner SL, Harris RC, Zhang MZ (2015) Proximal tubule-derived colony stimulating factor-1 mediates polarization of renal macrophages and dendritic cells, and recovery in acute kidney injury. Kidney Int 88:1274–1282CrossRefPubMedPubMedCentral
80.
go back to reference Susnik N, Sorensen-Zender I, Rong S, von Vietinghoff S, Lu X, Rubera I, Tauc M, Falk CS, Alexander WS, Melk A, Haller H, Schmitt R (2014) Ablation of proximal tubular suppressor of cytokine signaling 3 enhances tubular cell cycling and modifies macrophage phenotype during acute kidney injury. Kidney Int 85:1357–1368.CrossRefPubMed Susnik N, Sorensen-Zender I, Rong S, von Vietinghoff S, Lu X, Rubera I, Tauc M, Falk CS, Alexander WS, Melk A, Haller H, Schmitt R (2014) Ablation of proximal tubular suppressor of cytokine signaling 3 enhances tubular cell cycling and modifies macrophage phenotype during acute kidney injury. Kidney Int 85:1357–1368.CrossRefPubMed
Metadata
Title
The role of macrophages during acute kidney injury: destruction and repair
Authors
Hwa I. Han
Lauren B. Skvarca
Eugenel B. Espiritu
Alan J. Davidson
Neil A. Hukriede
Publication date
01-04-2019
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Nephrology / Issue 4/2019
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-017-3883-1

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