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PMID: 25266072 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Vascular-resident CD169-positive monocytes and macrophages control neutrophil accumulation in the kidney with ischemia-reperfusion injury.

Journal of the American Society of Nephrology : JASN ·Vol. 26 ·No. 4 ·2015-04-00 ·Pages 896-906

Karasawa K, Asano K, Moriyama S, Ushiki M, Monya M, Iida M, Kuboki E, Yagita H, Uchida K, Nitta K, Tanaka M

Abstract

Monocytes and kidney-resident macrophages are considered to be involved in the pathogenesis of renal ischemia-reperfusion injury (IRI). Several subsets of monocytes and macrophages are localized in the injured tissue, but the pathologic roles of these cells are not fully understood. Here, we show that CD169(+) monocytes and macrophages have a critical role in preventing excessive inflammation in IRI by downregulating intercellular adhesion molecule-1 (ICAM-1) expression on vascular endothelial cells. Mice depleted of CD169(+) cells showed enhanced endothelial ICAM-1 expression and developed irreversible renal damage associated with infiltration of a large number of neutrophils. The perivascular localization of CD169(+) monocytes and macrophages indicated direct interaction with blood vessels, and coculture experiments showed that the direct interaction of CD169(+) cell-depleted peripheral blood leukocytes augments the expression levels of ICAM-1 on endothelial cells. Notably, the transfer of Ly6C(lo) monocytes into CD169(+) cell-depleted mice rescued the mice from lethal renal injury and normalized renal ICAM-1 expression levels, indicating that the Ly6C(lo) subset of CD169(+) monocytes has a major role in the regulation of inflammation. Our findings highlight the previously unknown role of CD169(+) monocytes and macrophages in the maintenance of vascular homeostasis and provide new approaches to the treatment of renal IRI.

Keywords
acute renal failure immunology and pathology ischemia-reperfusion macrophages
MeSH Terms
Acute Kidney Injury/immunology Animals Endothelial Cells/metabolism Endothelium, Vascular/metabolism Intercellular Adhesion Molecule-1/metabolism Kidney/blood supply,immunology Male Mice, Inbred C57BL Phagocytes/physiology Reperfusion Injury/immunology Sialic Acid Binding Ig-like Lectin 1/analysis
Chemicals
Sialic Acid Binding Ig-like Lectin 1 Siglec1 protein, mouse Intercellular Adhesion Molecule-1
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Karasawa Kazunori
Laboratory of Immune Regulation, School of Life Science, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan; Department of Medicine, Kidney Center, Tokyo Women's Medical University, Tokyo, Japan;
Asano Kenichi
Laboratory of Immune Regulation, School of Life Science, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan; Japan Science and Technology Agency, PRESTO, Saitama, Japan; and.
Moriyama Shigetaka
Laboratory of Immune Regulation, School of Life Science, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan;
Ushiki Mikiko
Laboratory of Immune Regulation, School of Life Science, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan;
Monya Misa
Laboratory of Immune Regulation, School of Life Science, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan;
Iida Mayumi
Laboratory of Immune Regulation, School of Life Science, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan;
Kuboki Erika
Laboratory of Immune Regulation, School of Life Science, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan;
Yagita Hideo
Department of Immunology, Juntendo University School of Medicine, Tokyo, Japan.
Uchida Keiko
Department of Medicine, Kidney Center, Tokyo Women's Medical University, Tokyo, Japan;
Nitta Kosaku
Department of Medicine, Kidney Center, Tokyo Women's Medical University, Tokyo, Japan;
Tanaka Masato
Laboratory of Immune Regulation, School of Life Science, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan; mtanaka@toyaku.ac.jp.
References (46)
46 references, click to expand
  1. Codon-improved Cre recombinase (iCre) expression in the mouse.
    Genesis. 2002 Jan;32(1):19-26 PMID: 11835670
  2. Fractalkine receptor (CX3CR1) inhibition is protective against ischemic acute renal failure in mice.
    Am J Physiol Renal Physiol. 2008 Jan;294(1):F264-71 PMID: 18003857
  3. Blood monocytes consist of two principal subsets with distinct migratory properties.
    Immunity. 2003 Jul;19(1):71-82 PMID: 12871640
  4. Hematopoiesis: an evolving paradigm for stem cell biology.
    Cell. 2008 Feb 22;132(4):631-44 PMID: 18295580
  5. Fate mapping analysis reveals that adult microglia derive from primitive macrophages.
    Science. 2010 Nov 5;330(6005):841-5 PMID: 20966214
  6. Macrophage Wnt7b is critical for kidney repair and regeneration.
    Proc Natl Acad Sci U S A. 2010 Mar 2;107(9):4194-9 PMID: 20160075
  7. Identification of thrombospondin 1 (TSP-1) as a novel mediator of cell injury in kidney ischemia.
    J Clin Invest. 2005 Dec;115(12):3451-9 PMID: 16294224
  8. Monocyte chemoattractant protein-1 contributes to gut homeostasis and intestinal inflammation by composition of IL-10-producing regulatory macrophage subset.
    J Immunol. 2010 Mar 1;184(5):2671-6 PMID: 20107182
  9. CSF-1 signaling mediates recovery from acute kidney injury.
    J Clin Invest. 2012 Dec;122(12):4519-32 PMID: 23143303
  10. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2.
    Nat Immunol. 2006 Mar;7(3):311-7 PMID: 16462739
  11. Ischemia and reperfusion--from mechanism to translation.
    Nat Med. 2011 Nov 07;17(11):1391-401 PMID: 22064429
  12. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes.
    Immunity. 2013 Apr 18;38(4):792-804 PMID: 23601688
  13. Kupffer cell heterogeneity: functional properties of bone marrow derived and sessile hepatic macrophages.
    Blood. 2007 Dec 1;110(12):4077-85 PMID: 17690256
  14. Update on mechanisms of ischemic acute kidney injury.
    J Am Soc Nephrol. 2006 Jun;17(6):1503-20 PMID: 16707563
  15. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens.
    J Clin Invest. 2007 Aug;117(8):2268-78 PMID: 17657313
  16. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C- monocytes.
    Nat Immunol. 2011 Jul 03;12(8):778-85 PMID: 21725321
  17. Renal ischemia-reperfusion injury and adenosine 2A receptor-mediated tissue protection: role of macrophages.
    Am J Physiol Renal Physiol. 2005 Apr;288(4):F722-31 PMID: 15561971
  18. CD169⁺ macrophages provide a niche promoting erythropoiesis under homeostasis and stress.
    Nat Med. 2013 Apr;19(4):429-36 PMID: 23502962
  19. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis.
    Immunity. 2013 Jan 24;38(1):79-91 PMID: 23273845
  20. Pathophysiology of ischaemia-reperfusion injury.
    J Pathol. 2000 Feb;190(3):255-66 PMID: 10685060
  21. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network.
    J Exp Med. 2009 Dec 21;206(13):3089-100 PMID: 19995948
  22. Chemokine receptor CCR1 regulates inflammatory cell infiltration after renal ischemia-reperfusion injury.
    J Immunol. 2008 Dec 15;181(12):8670-6 PMID: 19050287
  23. Mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80. Identification of resident macrophages in renal medullary and cortical interstitium and the juxtaglomerular complex.
    J Exp Med. 1983 May 1;157(5):1704-9 PMID: 6854206
  24. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions.
    J Exp Med. 2007 Nov 26;204(12):3037-47 PMID: 18025128
  25. Ontogeny of the hematopoietic system.
    Annu Rev Immunol. 2007;25:745-85 PMID: 17201678
  26. A lineage of myeloid cells independent of Myb and hematopoietic stem cells.
    Science. 2012 Apr 6;336(6077):86-90 PMID: 22442384
  27. CCR2 signaling contributes to ischemia-reperfusion injury in kidney.
    J Am Soc Nephrol. 2003 Oct;14(10):2503-15 PMID: 14514728
  28. Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis.
    J Exp Med. 2005 Jun 6;201(11):1761-9 PMID: 15928200
  29. Cellular pathophysiology of ischemic acute kidney injury.
    J Clin Invest. 2011 Nov;121(11):4210-21 PMID: 22045571
  30. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells.
    Immunity. 2012 Dec 14;37(6):1076-90 PMID: 23219392
  31. Bone marrow-specific deficiency of nuclear receptor Nur77 enhances atherosclerosis.
    Circ Res. 2012 Feb 3;110(3):428-38 PMID: 22194623
  32. Role of neutrophil NADPH oxidase in the mechanism of tumor necrosis factor-alpha -induced NF-kappa B activation and intercellular adhesion molecule-1 expression in endothelial cells.
    J Biol Chem. 2002 Feb 1;277(5):3404-11 PMID: 11729200
  33. Intravascular danger signals guide neutrophils to sites of sterile inflammation.
    Science. 2010 Oct 15;330(6002):362-6 PMID: 20947763
  34. Novel subset of CD8{alpha}+ dendritic cells localized in the marginal zone is responsible for tolerance to cell-associated antigens.
    J Immunol. 2009 Apr 1;182(7):4127-36 PMID: 19299710
  35. CD169-positive macrophages dominate antitumor immunity by crosspresenting dead cell-associated antigens.
    Immunity. 2011 Jan 28;34(1):85-95 PMID: 21194983
  36. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus.
    BMC Dev Biol. 2001;1:4 PMID: 11299042
  37. Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal.
    Cell. 2013 Apr 11;153(2):362-75 PMID: 23582326
  38. Macrophage diversity in renal injury and repair.
    J Clin Invest. 2008 Nov;118(11):3522-30 PMID: 18982158
  39. The renal mononuclear phagocytic system.
    J Am Soc Nephrol. 2012 Feb;23(2):194-203 PMID: 22135312
  40. Langerhans cells renew in the skin throughout life under steady-state conditions.
    Nat Immunol. 2002 Dec;3(12):1135-41 PMID: 12415265
  41. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure.
    Science. 2013 Jan 11;339(6116):161-6 PMID: 23307733
  42. Distinct macrophage phenotypes contribute to kidney injury and repair.
    J Am Soc Nephrol. 2011 Feb;22(2):317-26 PMID: 21289217
  43. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion.
    Mol Cell Biol. 2000 Jun;20(11):4106-14 PMID: 10805752
  44. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior.
    Science. 2007 Aug 3;317(5838):666-70 PMID: 17673663
  45. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche.
    J Exp Med. 2011 Feb 14;208(2):261-71 PMID: 21282381
  46. Mouse macrophage hemagglutinin (sheep erythrocyte receptor) with specificity for sialylated glycoconjugates characterized by a monoclonal antibody.
    J Exp Med. 1989 Apr 1;169(4):1333-46 PMID: 2926328
Article Info
Journal
Journal of the American Society of Nephrology : JASN
Abbr.
J Am Soc Nephrol
ISSN
1533-3450
Published
2015-04-00
Epub
2014-00-29
Pages
896-906
Language
English
Region
United States
NLM ID
9013836
PMCID
PMC4378108
Subset
IM
Corrections
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