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PMID: 19381014 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Self-regulation of inflammatory cell trafficking in mice by the leukocyte surface apyrase CD39.

The Journal of clinical investigation ·Vol. 119 ·No. 5 ·2009-05-00 ·Pages 1136-49

Hyman MC, Petrovic-Djergovic D, Visovatti SH, Liao H, Yanamadala S, Bouïs D, Su EJ, Lawrence DA, Broekman MJ, Marcus AJ, Pinsky DJ

Abstract

Leukocyte and platelet accumulation at sites of cerebral ischemia exacerbate cerebral damage. The ectoenzyme CD39 on the plasmalemma of endothelial cells metabolizes ADP to suppress platelet accumulation in the ischemic brain. However, the role of leukocyte surface CD39 in regulating monocyte and neutrophil trafficking in this setting is not known. Here we have demonstrated in mice what we believe to be a novel mechanism by which CD39 on monocytes and neutrophils regulates their own sequestration into ischemic cerebral tissue, by catabolizing nucleotides released by injured cells, thereby inhibiting their chemotaxis, adhesion, and transmigration. Bone marrow reconstitution and provision of an apyrase, an enzyme that hydrolyzes nucleoside tri- and diphosphates, each normalized ischemic leukosequestration and cerebral infarction in CD39-deficient mice. Leukocytes purified from Cd39-/- mice had a markedly diminished capacity to phosphohydrolyze adenine nucleotides and regulate platelet reactivity, suggesting that leukocyte ectoapyrases modulate the ambient vascular nucleotide milieu. Dissipation of ATP by CD39 reduced P2X7 receptor stimulation and thereby suppressed baseline leukocyte alphaMbeta2-integrin expression. As alphaMbeta2-integrin blockade reversed the postischemic, inflammatory phenotype of Cd39-/- mice, these data suggest that phosphohydrolytic activity on the leukocyte surface suppresses cell-cell interactions that would otherwise promote thrombosis or inflammation. These studies indicate that CD39 on both endothelial cells and leukocytes reduces inflammatory cell trafficking and platelet reactivity, with a consequent reduction in tissue injury following cerebral ischemic challenge.

MeSH Terms
5'-Nucleotidase/antagonists & inhibitors Adenosine Diphosphate/metabolism Adenosine Triphosphate/metabolism Animals Antibodies, Monoclonal/immunology,pharmacology Antigens, CD/physiology Apyrase/pharmacology,physiology Bone Marrow Transplantation Brain Ischemia/genetics,pathology Cell Line, Tumor Cell Movement/drug effects,physiology Endothelial Cells/metabolism Enzyme Inhibitors/pharmacology Leukocytes/cytology,drug effects,metabolism Macrophage-1 Antigen/immunology,metabolism Macrophages/cytology,drug effects,metabolism Mice Mice, Inbred Strains Mice, Knockout Monocytes/cytology,drug effects,metabolism Neutrophils/cytology,metabolism Platelet Activation/physiology Purinergic P2 Receptor Antagonists RNA Interference Receptors, Purinergic P2/genetics Transplantation Chimera/physiology
Chemicals
Antibodies, Monoclonal Antigens, CD Enzyme Inhibitors Macrophage-1 Antigen Purinergic P2 Receptor Antagonists Receptors, Purinergic P2 Adenosine Diphosphate Adenosine Triphosphate 5'-Nucleotidase Apyrase CD39 antigen
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Hyman Matthew C
Department of Molecular and Integrative Physiology, University of Michigan Medical Center, Ann Arbor, USA. mchyman@umich.edu
Petrovic-Djergovic Danica
Visovatti Scott H
Liao Hui
Yanamadala Sunitha
Bouïs Diane
Su Enming J
Lawrence Daniel A
Broekman M Johan
Marcus Aaron J
Pinsky David J
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Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
1558-8238
Published
2009-05-00
Epub
2009-00-20
Pages
1136-49
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC2673847
Subset
IM
Grants
NHLBI NIH HHS · P01 HL046403 · United States
NHLBI NIH HHS · T32 HL007853 · United States
NHLBI NIH HHS · HL46403 · United States
NINDS NIH HHS · R01 NS041460 · United States
NHLBI NIH HHS · P01HL089407 · United States
NHLBI NIH HHS · HL47073 · United States
NHLBI NIH HHS · R37 HL047073 · United States
NHLBI NIH HHS · HL086676 · United States
NHLBI NIH HHS · R01 HL086676 · United States
NHLBI NIH HHS · R01 HL069448 · United States
NINDS NIH HHS · NS041460 · United States
NHLBI NIH HHS · R01 HL047073 · United States
NHLBI NIH HHS · HL69448 · United States
NHLBI NIH HHS · P01 HL089407 · United States
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