Decreased capacity of immune cells to cause tissue injury mediates kidney ischemic preconditioning

J Immunol. 2006 Jun 1;176(11):7015-20. doi: 10.4049/jimmunol.176.11.7015.

Abstract

Ischemic preconditioning (IP) is a well-established phenomenon, and the underlying mechanisms of IP are thought to involve adaptive changes within the injured tissue. Because one of the main functions of immune cells is to harbor memory, we hypothesized that circulating immune cells could mediate IP by responding to an initial ischemia reperfusion injury (IRI) and then mediate decreased injury after a second IRI event. C57BL/6 mice underwent 30 min of bilateral renal clamping or sham operation. At 5 days after ischemia, purified leukocytes from spleen were adoptively transferred into T cell-deficient (nu/nu) mice. After 1 wk, these mice underwent 30 min of renal IRI. The nu/nu mice receiving leukocytes from ischemic wild-type mice had significantly reduced renal injury compared with nu/nu mice receiving leukocytes from sham-operated, wild-type mice. Infiltration of neutrophil and macrophage in postischemic kidney did not correlate with the protection. No difference in kidney C3d or IgG deposition was detected between groups. Given that inducible NO synthase (iNOS) has been implicated in IP, leukocytes from ischemic or sham-operated, iNOS-deficient mice were transferred into nu/nu mice. Effects similar to those of wild-type transfer of ischemic leukocytes were demonstrated; thus, iNOS was not mediating the IP effect of leukocytes. This is the first evidence that immune cells are primed after renal IRI and thereby lose the capacity to cause kidney injury during a second episode of IRI. This finding may also be relevant for elucidating the mechanisms underlying cross-talk between injured kidney and distant organs.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Cell Movement / genetics
  • Cell Movement / immunology
  • Complement C3d / metabolism
  • Hemoglobins / metabolism
  • Immunoglobulin G / metabolism
  • Ischemic Preconditioning*
  • Kidney / blood supply*
  • Kidney / enzymology
  • Kidney / immunology*
  • Leukocyte Transfusion
  • Lymphopenia / enzymology
  • Lymphopenia / genetics*
  • Lymphopenia / immunology*
  • Macrophages / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Nude
  • Neutrophil Infiltration / genetics
  • Neutrophil Infiltration / immunology
  • Nitric Oxide Synthase Type II / physiology
  • Reperfusion Injury / enzymology
  • Reperfusion Injury / genetics
  • Reperfusion Injury / immunology
  • Reperfusion Injury / prevention & control
  • Spleen / cytology
  • Spleen / transplantation

Substances

  • Hemoglobins
  • Immunoglobulin G
  • Complement C3d
  • Nitric Oxide Synthase Type II