Home LiteratureArticle Details
PMID: 19129795 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Compartmentalization of neutrophils in the kidney and lung following acute ischemic kidney injury.

Kidney international ·Vol. 75 ·No. 7 ·2009-04-00 ·Pages 689-98

Awad AS, Rouse M, Huang L, Vergis AL, Reutershan J, Cathro HP, Linden J, Okusa MD

Abstract

During renal ischemia-reperfusion, local and distant tissue injury is caused by an influx of neutrophils into the affected tissues. Here we measured the kinetics of margination and transmigration of neutrophils in vivo in the kidney and lungs following renal ischemia-reperfusion. After bilateral renal injury, kidney neutrophil content increased threefold at 24 h. The neutrophils were found primarily in the interstitium and to a lesser degree marginated to the vascular endothelium. These interstitial neutrophils had significantly lower levels of intracellular IFN-gamma, IL-4, IL-6, and IL-10 a tendency for decreased amounts of IL-4 and TNF-alpha compared to the marginated neutrophils. Localization of the neutrophils to the kidney interstitium was confirmed by high resolution microscopy and these sites of transmigration were directly associated with areas of increased vascular permeability. Activation of the adenosine 2A receptor significantly decreased both kidney neutrophil transmigration by about half and vascular permeability by about a third. After unilateral renal ischemia-reperfusion, the unclipped kidney and lungs did not accumulate interstitial neutrophils or have increased vascular permeability despite a marked increase of neutrophil margination in the lungs. Our findings suggest there is a sequential recruitment and transmigration of neutrophils from the vasculature into the kidney interstitium at the site of tissue injury following renal ischemia-reperfusion.

MeSH Terms
Animals Capillary Permeability Cytokines/analysis Endothelium, Vascular Extracellular Fluid Kidney Kidney Diseases/immunology Kinetics Lung Diseases/immunology Mice Mice, Inbred C57BL Neutrophil Infiltration Receptor, Adenosine A2A/metabolism Reperfusion Injury/immunology
Chemicals
Cytokines Receptor, Adenosine A2A
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Awad Alaa S
Division of Nephrology, Department of Medicine, University of Virginia Health System, Charlottesville, VA 22908, USA. awad@virginia.edu
Rouse Michael
Huang Liping
Vergis Amy L
Reutershan Jörg
Cathro Helen P
Linden Joel
Okusa Mark D
References (30)
30 references, click to expand
  1. Acute renal failure in the new millennium: time to consider combination therapy.
    Semin Nephrol. 2000 Jan;20(1):4-19 PMID: 10651214
  2. Selective sphingosine 1-phosphate 1 receptor activation reduces ischemia-reperfusion injury in mouse kidney.
    Am J Physiol Renal Physiol. 2006 Jun;290(6):F1516-24 PMID: 16403835
  3. Postischemic renal injury is mediated by neutrophils and leukotrienes.
    Am J Physiol. 1989 May;256(5 Pt 2):F794-802 PMID: 2541628
  4. Neutrophils accentuate ischemia-reperfusion injury in isolated perfused rat kidneys.
    Am J Physiol. 1988 Oct;255(4 Pt 2):F728-35 PMID: 2845813
  5. Inhibition by adenosine of reactive oxygen metabolite production by human polymorphonuclear leucocytes.
    Biochem J. 1985 Apr 15;227(2):669-74 PMID: 4004786
  6. Human neutrophils produce interferon gamma upon stimulation by interleukin-12.
    Lab Invest. 2004 Oct;84(10):1363-71 PMID: 15220936
  7. Blocking the immune response in ischemic acute kidney injury: the role of adenosine 2A agonists.
    Nat Clin Pract Nephrol. 2006 Aug;2(8):432-44 PMID: 16932478
  8. Renal protection from ischemia mediated by A2A adenosine receptors on bone marrow-derived cells.
    J Clin Invest. 2003 Sep;112(6):883-91 PMID: 12975473
  9. Refining predictive models in critically ill patients with acute renal failure.
    J Am Soc Nephrol. 2002 May;13(5):1350-7 PMID: 11961023
  10. The monoclonal antibody TER-119 recognizes a molecule associated with glycophorin A and specifically marks the late stages of murine erythroid lineage.
    Br J Haematol. 2000 May;109(2):280-7 PMID: 10848813
  11. Adenosine; a physiologic modulator of superoxide anion generation by human neutrophils. Adenosine acts via an A2 receptor on human neutrophils.
    J Immunol. 1985 Aug;135(2):1366-71 PMID: 2989364
  12. IL-4 production by human polymorphonuclear neutrophils.
    J Leukoc Biol. 2000 Jul;68(1):125-30 PMID: 10914499
  13. Renal ischemia-reperfusion injury and adenosine 2A receptor-mediated tissue protection: the role of CD4+ T cells and IFN-gamma.
    J Immunol. 2006 Mar 1;176(5):3108-14 PMID: 16493070
  14. Renal ischemia/reperfusion leads to macrophage-mediated increase in pulmonary vascular permeability.
    Kidney Int. 1999 Jun;55(6):2362-7 PMID: 10354283
  15. Neutrophils accentuate renal cold ischemia-reperfusion injury. Dose-dependent protective effect of a platelet-activating factor receptor antagonist.
    J Pharmacol Exp Ther. 1997 Feb;280(2):786-94 PMID: 9023292
  16. A(2A) adenosine receptor-mediated inhibition of renal injury and neutrophil adhesion.
    Am J Physiol Renal Physiol. 2000 Nov;279(5):F809-18 PMID: 11053040
  17. Adenosine: a physiological modulator of superoxide anion generation by human neutrophils.
    J Exp Med. 1983 Oct 1;158(4):1160-77 PMID: 6311934
  18. Sequential recruitment of neutrophils into lung and bronchoalveolar lavage fluid in LPS-induced acute lung injury.
    Am J Physiol Lung Cell Mol Physiol. 2005 Nov;289(5):L807-15 PMID: 15951336
  19. Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury.
    J Clin Invest. 1996 Feb 15;97(4):1056-63 PMID: 8613529
  20. The role of neutrophils in acute renal failure.
    Semin Nephrol. 1998 Sep;18(5):498-504 PMID: 9754602
  21. Alpha-melanocyte-stimulating hormone inhibits lung injury after renal ischemia/reperfusion.
    Am J Respir Crit Care Med. 2004 Mar 15;169(6):749-56 PMID: 14711793
  22. Neutrophil-mediated post-ischemic tubular leakage in the rat kidney.
    Kidney Int. 1989 Oct;36(4):555-61 PMID: 2811061
  23. In vivo vascular leakage assay.
    Methods Mol Med. 2004;98:191-8 PMID: 15064440
  24. Measles virus infection of rhesus macaques affects neutrophil expression of IL-12 and IL-10.
    Viral Immunol. 2003;16(3):369-79 PMID: 14583151
  25. Distant effects of experimental renal ischemia/reperfusion injury.
    J Am Soc Nephrol. 2003 Jun;14(6):1549-58 PMID: 12761255
  26. Inflammatory cells in ischemic acute renal failure.
    Kidney Int. 2004 Aug;66(2):486-91 PMID: 15253694
  27. Adenosine A2A receptor activation attenuates inflammation and injury in diabetic nephropathy.
    Am J Physiol Renal Physiol. 2006 Apr;290(4):F828-37 PMID: 16332931
  28. Alpha-melanocyte-stimulating hormone protects against renal injury after ischemia in mice and rats.
    J Clin Invest. 1997 Mar 15;99(6):1165-72 PMID: 9077523
  29. NKT cell activation mediates neutrophil IFN-gamma production and renal ischemia-reperfusion injury.
    J Immunol. 2007 May 1;178(9):5899-911 PMID: 17442974
  30. Capsular polysaccharide of Cryptococcus neoformans induces proinflammatory cytokine release by human neutrophils.
    Infect Immun. 1996 Aug;64(8):2897-903 PMID: 8757810
Article Info
Journal
Kidney international
Abbr.
Kidney Int
ISSN
1523-1755
Published
2009-04-00
Epub
2009-00-07
Pages
689-98
Language
English
Region
United States
NLM ID
0323470
PMCID
PMC2656389
Subset
IM
Grants
NIDDK NIH HHS · R00 DK077444 · United States
NIDDK NIH HHS · R01 DK062324-06 · United States
NIDDK NIH HHS · R01 DK062324 · United States
NIDDK NIH HHS · R00 DK077444-04 · United States
NIDDK NIH HHS · DK58413 · United States
NHLBI NIH HHS · P01 HL073361 · United States
NHLBI NIH HHS · HL37942 · United States
NIDDK NIH HHS · R41 DK058413 · United States
NIDDK NIH HHS · R41 DK058413-01 · United States
NIDDK NIH HHS · K99 DK077444 · United States
NIDDK NIH HHS · DK62324 · United States
NIDDK NIH HHS · 1K99DK077444-01 · United States
NIDDK NIH HHS · R01 DK056223-08 · United States
NIDDK NIH HHS · DK56223 · United States
NIDDK NIH HHS · K99 DK077444-01A1 · United States
NIDDK NIH HHS · K99 DK077444-02 · United States
NIDDK NIH HHS · R01 DK056223 · United States
NHLBI NIH HHS · 1 P01 HL073361 · United States
NHLBI NIH HHS · P01 HL073361-059001 · United States
NHLBI NIH HHS · R01 HL037942-22 · United States
NIDDK NIH HHS · R44 DK058413 · United States
NIDDK NIH HHS · R00 DK077444-03 · United States
NHLBI NIH HHS · R01 HL037942 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com