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Macrophage heterogeneity and renin-angiotensin system disorders

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Abstract

Macrophages are heterogeneous innate immune cells which are important in both the maintenance of tissue homeostasis and its disruption, by promoting tissue inflammation and fibrosis. The renin-angiotensin system is central to the pathophysiology of a large suite of diseases, which are driven in part by large amounts of tissue inflammation and fibrosis. Here, we review recent advances in understanding macrophage heterogeneity in origin and function, and how these may lead to new insights into the pathogenesis of these chronic diseases.

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References

  1. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538–1543. doi:10.1038/nn2014

    Article  CAS  PubMed  Google Scholar 

  2. Arnold CE, Gordon P, Barker RN, Wilson HM (2015) The activation status of human macrophages presenting antigen determines the efficiency of Th17 responses. Immunobiology 220:10–19. doi:10.1016/j.imbio.2014.09.022

    Article  CAS  PubMed  Google Scholar 

  3. Atlas SA (2007) The renin-angiotensin aldosterone system: pathophysiological role and pharmacologic inhibition. J Manag Care Pharm 13:9–20. doi:10.18553/jmcp.2007.13.s8-b.9

    PubMed  Google Scholar 

  4. Bain CC, Bravo-Blas A, Scott CL, Gomez Perdiguero E, Geissmann F, Henri S, Malissen B, Osborne LC, Artis D, Mowat AM (2014) Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol 15:929–937. doi:10.1038/ni.2967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Benigni A, Cassis P, Remuzzi G (2010) Angiotensin II revisited: new roles in inflammation, immunology and aging. EMBO Mol Med 2:247–257. doi:10.1002/emmm.201000080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Binger KJ, Gebhardt M, Heinig M, Rintisch C, Schroeder A, Neuhofer W, Hilgers K, Manzel A, Schwartz C, Kleinewietfeld M, Voelkl J, Schatz V, Linker RA, Lang F, Voehringer D, Wright MD, Hubner N, Dechend R, Jantsch J, Titze J, Muller DN (2015) High salt reduces the activation of IL-4- and IL-13-stimulated macrophages. J Clin Invest 125:4223–4238. doi:10.1172/JCI80919

    Article  PubMed  PubMed Central  Google Scholar 

  7. Brown AS, Yang C, Fung KY, Bachem A, Bourges D, Bedoui S, Hartland EL, van Driel IR (2016) Cooperation between monocyte-derived cells and lymphoid cells in the acute response to a bacterial lung pathogen. PLoS Pathog 12:e1005691. doi:10.1371/journal.ppat.1005691

    Article  PubMed  PubMed Central  Google Scholar 

  8. Bush E, Maeda N, Kuziel WA, Dawson TC, Wilcox JN, DeLeon H, Taylor WR (2000) CC chemokine receptor 2 is required for macrophage infiltration and vascular hypertrophy in angiotensin II-induced hypertension. Hypertension 36:360–363

    Article  CAS  PubMed  Google Scholar 

  9. Cao Q, Harris DC, Wang Y (2015) Macrophages in kidney injury, inflammation, and fibrosis. Physiology (Bethesda) 30:183–194. doi:10.1152/physiol.00046.2014

    CAS  Google Scholar 

  10. Chan CT, Moore JP, Budzyn K, Guida E, Diep H, Vinh A, Jones ES, Widdop RE, Armitage JA, Sakkal S, Ricardo SD, Sobey CG, Drummond GR (2012) Reversal of vascular macrophage accumulation and hypertension by a CCR2 antagonist in deoxycorticosterone/salt-treated mice. Hypertension 60:1207–1212. doi:10.1161/HYPERTENSIONAHA.112.201251

    Article  CAS  PubMed  Google Scholar 

  11. Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, Cyrus N, Brokowski CE, Eisenbarth SC, Phillips GM, Cline GW, Phillips AJ, Medzhitov R (2014) Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 513:559–563. doi:10.1038/nature13490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Crowley SD, Song YS, Sprung G, Griffiths R, Sparks M, Yan M, Burchette JL, Howell DN, Lin EE, Okeiyi B, Stegbauer J, Yang Y, Tharaux PL, Ruiz P (2010) A role for angiotensin II type 1 receptors on bone marrow-derived cells in the pathogenesis of angiotensin II-dependent hypertension. Hypertension 55:99–108. doi:10.1161/HYPERTENSIONAHA.109.144964

    Article  CAS  PubMed  Google Scholar 

  13. Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER (2002) Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99:111–120

    Article  CAS  PubMed  Google Scholar 

  14. De Ciuceis C, Amiri F, Brassard P, Endemann DH, Touyz RM, Schiffrin EL (2005) Reduced vascular remodeling, endothelial dysfunction, and oxidative stress in resistance arteries of angiotensin II-infused macrophage colony-stimulating factor-deficient mice: evidence for a role in inflammation in angiotensin-induced vascular injury. Arterioscler Thromb Vasc Biol 25:2106–2113. doi:10.1161/01.ATV.0000181743.28028.57

    Article  CAS  PubMed  Google Scholar 

  15. Deliyanti D, Miller AG, Tan G, Binger KJ, Samson AL, Wilkinson-Berka JL (2012) Neovascularization is attenuated with aldosterone synthase inhibition in rats with retinopathy. Hypertension 59:607–613. doi:10.1161/HYPERTENSIONAHA.111.188136

    Article  CAS  PubMed  Google Scholar 

  16. Ensan S, Li A, Besla R, Degousee N, Cosme J, Roufaiel M, Shikatani EA, El-Maklizi M, Williams JW, Robins L, Li C, Lewis B, Yun TJ, Lee JS, Wieghofer P, Khattar R, Farrokhi K, Byrne J, Ouzounian M, Zavitz CC, Levy GA, Bauer CM, Libby P, Husain M, Swirski FK, Cheong C, Prinz M, Hilgendorf I, Randolph GJ, Epelman S, Gramolini AO, Cybulsky MI, Rubin BB, Robbins CS (2016) Self-renewing resident arterial macrophages arise from embryonic CX3CR1(+) precursors and circulating monocytes immediately after birth. Nat Immunol 17:159–168. doi:10.1038/ni.3343

    Article  CAS  PubMed  Google Scholar 

  17. Epelman S, Lavine KJ, Beaudin AE, Sojka DK, Carrero JA, Calderon B, Brija T, Gautier EL, Ivanov S, Satpathy AT, Schilling JD, Schwendener R, Sergin I, Razani B, Forsberg EC, Yokoyama WM, Unanue ER, Colonna M, Randolph GJ, Mann DL (2014) Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40:91–104. doi:10.1016/j.immuni.2013.11.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Epelman S, Lavine KJ, Randolph GJ (2014) Origin and functions of tissue macrophages. Immunity 41:21–35. doi:10.1016/j.immuni.2014.06.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Erblich B, Zhu L, Etgen AM, Dobrenis K, Pollard JW (2011) Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS One 6:e26317. doi:10.1371/journal.pone.0026317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Geissmann F, Gordon S, Hume DA, Mowat AM, Randolph GJ (2010) Unravelling mononuclear phagocyte heterogeneity. Nat Rev Immunol 10:453–460. doi:10.1038/nri2784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330:841–845. doi:10.1126/science.1194637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gordon S, Martinez FO (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32:593–604. doi:10.1016/j.immuni.2010.05.007

    Article  CAS  PubMed  Google Scholar 

  23. Gordy C, Pua H, Sempowski GD, He YW (2011) Regulation of steady-state neutrophil homeostasis by macrophages. Blood 117:618–629. doi:10.1182/blood-2010-01-265959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gosselin D, Link VM, Romanoski CE, Fonseca GJ, Eichenfield DZ, Spann NJ, Stender JD, Chun HB, Garner H, Geissmann F, Glass CK (2014) Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159:1327–1340. doi:10.1016/j.cell.2014.11.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hume DA, MacDonald KP (2012) Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 119:1810–1820. doi:10.1182/blood-2011-09-379214

    Article  CAS  PubMed  Google Scholar 

  26. Italiani P, Boraschi D (2014) From monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation. Front Immunol 5:514. doi:10.3389/fimmu.2014.00514

    Article  PubMed  PubMed Central  Google Scholar 

  27. Jantsch J, Binger KJ, Muller DN, Titze J (2014) Macrophages in homeostatic immune function. Front Physiol 5:146. doi:10.3389/fphys.2014.00146

    Article  PubMed  PubMed Central  Google Scholar 

  28. Jantsch J, Schatz V, Friedrich D, Schroder A, Kopp C, Siegert I, Maronna A, Wendelborn D, Linz P, Binger KJ, Gebhardt M, Heinig M, Neubert P, Fischer F, Teufel S, David JP, Neufert C, Cavallaro A, Rakova N, Kuper C, Beck FX, Neuhofer W, Muller DN, Schuler G, Uder M, Bogdan C, Luft FC, Titze J (2015) Cutaneous Na+ storage strengthens the antimicrobial barrier function of the skin and boosts macrophage-driven host defense. Cell Metab 21:493–501. doi:10.1016/j.cmet.2015.02.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kim KW, Williams JW, Wang YT, Ivanov S, Gilfillan S, Colonna M, Virgin HW, Gautier EL, Randolph GJ (2016) MHC II+ resident peritoneal and pleural macrophages rely on IRF4 for development from circulating monocytes. J Exp Med 213:1951–1959. doi:10.1084/jem.20160486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kratz M, Coats BR, Hisert KB, Hagman D, Mutskov V, Peris E, Schoenfelt KQ, Kuzma JN, Larson I, Billing PS, Landerholm RW, Crouthamel M, Gozal D, Hwang S, Singh PK, Becker L (2014) Metabolic dysfunction drives a mechanistically distinct proinflammatory phenotype in adipose tissue macrophages. Cell Metab 20:614–625. doi:10.1016/j.cmet.2014.08.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N, Hussell T, Feldmann M, Udalova IA (2011) IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol 12:231–238. doi:10.1038/ni.1990

    Article  CAS  PubMed  Google Scholar 

  32. Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, Jung S, Amit I (2014) Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159:1312–1326. doi:10.1016/j.cell.2014.11.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ley K, Laudanna C, Cybulsky MI, Nourshargh S (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7:678–689. doi:10.1038/nri2156

    Article  CAS  PubMed  Google Scholar 

  34. Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117:175–184. doi:10.1172/JCI29881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Marko L, Henke N, Park JK, Spallek B, Qadri F, Balogh A, Apel IJ, Oravecz-Wilson KI, Choi M, Przybyl L, Binger KJ, Haase N, Wilck N, Heuser A, Fokuhl V, Ruland J, Lucas PC, McAllister-Lucas LM, Luft FC, Dechend R, Muller DN (2014) Bcl10 mediates angiotensin II-induced cardiac damage and electrical remodeling. Hypertension 64:1032–1039. doi:10.1161/HYPERTENSIONAHA.114.03900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Marko L, Kvakan H, Park JK, Qadri F, Spallek B, Binger KJ, Bowman EP, Kleinewietfeld M, Fokuhl V, Dechend R, Muller DN (2012) Interferon-gamma signaling inhibition ameliorates angiotensin II-induced cardiac damage. Hypertension 60:1430–1436. doi:10.1161/HYPERTENSIONAHA.112.199265

    Article  CAS  PubMed  Google Scholar 

  37. Mitchell GF (2014) Arterial stiffness and hypertension: chicken or egg? Hypertension 64:210–214. doi:10.1161/HYPERTENSIONAHA.114.03449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, Locati M, Mantovani A, Martinez FO, Mege JL, Mosser DM, Natoli G, Saeij JP, Schultze JL, Shirey KA, Sica A, Suttles J, Udalova I, van Ginderachter JA, Vogel SN, Wynn TA (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41:14–20. doi:10.1016/j.immuni.2014.06.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Murray PJ, Wynn TA (2011) Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 11:723–737. doi:10.1038/nri3073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Nicoletti A, Heudes D, Mandet C, Hinglais N, Bariety J, Michel JB (1996) Inflammatory cells and myocardial fibrosis: spatial and temporal distribution in renovascular hypertensive rats. Cardiovasc Res 32:1096–1107

    Article  CAS  PubMed  Google Scholar 

  41. Nishida M, Fujinaka H, Matsusaka T, Price J, Kon V, Fogo AB, Davidson JM, Linton MF, Fazio S, Homma T, Yoshida H, Ichikawa I (2002) Absence of angiotensin II type 1 receptor in bone marrow-derived cells is detrimental in the evolution of renal fibrosis. J Clin Invest 110:1859–1868. doi:10.1172/JCI15045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Okabe Y, Medzhitov R (2016) Tissue biology perspective on macrophages. Nat Immunol 17:9–17. doi:10.1038/ni.3320

    Article  CAS  PubMed  Google Scholar 

  43. Ozawa Y, Kobori H, Suzaki Y, Navar LG (2007) Sustained renal interstitial macrophage infiltration following chronic angiotensin II infusions. Am J Physiol Renal Physiol 292:F330–F339. doi:10.1152/ajprenal.00059.2006

    Article  CAS  PubMed  Google Scholar 

  44. Perdiguero EG, Geissmann F (2016) The development and maintenance of resident macrophages. Nat Immunol 17:2–8. doi:10.1038/ni.3341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Pollard JW (2009) Trophic macrophages in development and disease. Nat Rev Immunol 9:259–270. doi:10.1038/nri2528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ransohoff RM (2016) A polarizing question: do M1 and M2 microglia exist? Nat Neurosci 19:987–991. doi:10.1038/nn.4338

    Article  CAS  PubMed  Google Scholar 

  47. Ricardo SD, van Goor H, Eddy AA (2008) Macrophage diversity in renal injury and repair. J Clin Invest 118:3522–3530. doi:10.1172/JCI36150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Schiwon M, Weisheit C, Franken L, Gutweiler S, Dixit A, Meyer-Schwesinger C, Pohl JM, Maurice NJ, Thiebes S, Lorenz K, Quast T, Fuhrmann M, Baumgarten G, Lohse MJ, Opdenakker G, Bernhagen J, Bucala R, Panzer U, Kolanus W, Grone HJ, Garbi N, Kastenmuller W, Knolle PA, Kurts C, Engel DR (2014) Crosstalk between sentinel and helper macrophages permits neutrophil migration into infected uroepithelium. Cell 156:456–468. doi:10.1016/j.cell.2014.01.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336:86–90. doi:10.1126/science.1219179

    Article  CAS  PubMed  Google Scholar 

  50. Scott CL, Zheng F, De Baetselier P, Martens L, Saeys Y, De Prijck S, Lippens S, Abels C, Schoonooghe S, Raes G, Devoogdt N, Lambrecht BN, Beschin A, Guilliams M (2016) Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells. Nat Commun 7:10321. doi:10.1038/ncomms10321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Shi C, Pamer EG (2011) Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11:762–774. doi:10.1038/nri3070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Shklovskaya E, O'Sullivan BJ, Ng LG, Roediger B, Thomas R, Weninger W, Fazekas de St Groth B (2011) Langerhans cells are precommitted to immune tolerance induction. Proc Natl Acad Sci U S A 108:18049–18054. doi:10.1073/pnas.1110076108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Stamatiades EG, Tremblay ME, Bohm M, Crozet L, Bisht K, Kao D, Coelho C, Fan X, Yewdell WT, Davidson A, Heeger PS, Diebold S, Nimmerjahn F, Geissmann F (2016) Immune monitoring of trans-endothelial transport by kidney-resident macrophages. Cell 166:991–1003. doi:10.1016/j.cell.2016.06.058

    Article  CAS  PubMed  Google Scholar 

  54. Steinman RM (1991) The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9:271–296. doi:10.1146/annurev.iy.09.040191.001415

    Article  CAS  PubMed  Google Scholar 

  55. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, Frezza C, Bernard NJ, Kelly B, Foley NH, Zheng L, Gardet A, Tong Z, Jany SS, Corr SC, Haneklaus M, Caffrey BE, Pierce K, Walmsley S, Beasley FC, Cummins E, Nizet V, Whyte M, Taylor CT, Lin H, Masters SL, Gottlieb E, Kelly VP, Clish C, Auron PE, Xavier RJ, O'Neill LA (2013) Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature 496:238–242. doi:10.1038/nature11986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Wenzel P, Knorr M, Kossmann S, Stratmann J, Hausding M, Schuhmacher S, Karbach SH, Schwenk M, Yogev N, Schulz E, Oelze M, Grabbe S, Jonuleit H, Becker C, Daiber A, Waisman A, Munzel T (2011) Lysozyme M-positive monocytes mediate angiotensin II-induced arterial hypertension and vascular dysfunction. Circulation 124:1370–1381. doi:10.1161/CIRCULATIONAHA.111.034470

    Article  CAS  PubMed  Google Scholar 

  57. Wilkinson-Berka JL, Heine R, Tan G, Cooper ME, Hatzopoulos KM, Fletcher EL, Binger KJ, Campbell DJ, Miller AG (2010) RILLKKMPSV influences the vasculature, neurons and glia, and (pro)renin receptor expression in the retina. Hypertension 55:1454–1460. doi:10.1161/HYPERTENSIONAHA.109.148221

    Article  CAS  PubMed  Google Scholar 

  58. Wilkinson-Berka JL, Tan G, Binger KJ, Sutton L, McMaster K, Deliyanti D, Perera G, Campbell DJ, Miller AG (2011) Aliskiren reduces vascular pathology in diabetic retinopathy and oxygen-induced retinopathy in the transgenic (mRen-2)27 rat. Diabetologia 54:2724–2735. doi:10.1007/s00125-011-2239-9

    Article  CAS  PubMed  Google Scholar 

  59. Wynn TA (2008) Cellular and molecular mechanisms of fibrosis. J Pathol 214:199–210. doi:10.1002/path.2277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wynn TA, Barron L (2010) Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis 30:245–257. doi:10.1055/s-0030-1255354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Wynn TA, Vannella KM (2016) Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44:450–462. doi:10.1016/j.immuni.2016.02.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Zeyda M, Wernly B, Demyanets S, Kaun C, Hammerle M, Hantusch B, Schranz M, Neuhofer A, Itariu BK, Keck M, Prager G, Wojta J, Stulnig TM (2013) Severe obesity increases adipose tissue expression of interleukin-33 and its receptor ST2, both predominantly detectable in endothelial cells of human adipose tissue. Int J Obes 37:658–665. doi:10.1038/ijo.2012.118

    Article  CAS  Google Scholar 

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Acknowledgements

KJB is supported by a National Health and Medical Research Council of Australia Early Career Fellowship (APP1037633).

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KJB and MDW wrote the manuscript.

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  1. Department of Immunology, Monash University, Prahran, Victoria, Australia

    Mark D. Wright

  2. Department of Biochemistry and Molecular Biology, Bio21 Institute of Molecular Science and Biotechnology, University of Melbourne, Parkville, Victoria, Australia

    Katrina J. Binger

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Correspondence to Katrina J. Binger.

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This article is part of the special issue on macrophages in tissue homeostasis in Pflügers Archiv – European Journal of Physiology

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Wright, M.D., Binger, K.J. Macrophage heterogeneity and renin-angiotensin system disorders. Pflugers Arch - Eur J Physiol 469, 445–454 (2017). https://doi.org/10.1007/s00424-017-1940-z

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