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 Blood, 21 May 2009, Vol. 113, No. 21, pp. 5254-5265.
Prepublished online as a Blood First Edition Paper on March 4, 2009; DOI 10.1182/blood-2008-09-180794.

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PHAGOCYTES, GRANULOCYTES, AND MYELOPOIESIS

Neutrophils phagocytose activated platelets in vivo: a phosphatidylserine, P-selectin, and β2 integrin–dependent cell clearance program

Norma Maugeri1, Patrizia Rovere-Querini1, Virgilio Evangelista2, Cesare Covino1, Annalisa Capobianco1, Maria T. S. Bertilaccio1, Antonio Piccoli2, Licia Totani2, Domenico Cianflone1, Attilio Maseri1, and Angelo A. Manfredi1

1 H San Raffaele Scientific Institute and University Vita-Salute San Raffaele, Milan; and 2 Laboratory of Vascular Biology and Pharmacology, Consorzio Mario Negri Sud, Santa Maria Imbaro, Italy

Activated platelets express ligands, which are recognized by counterreceptors on neutrophils. Here, we show that the ensuing cell-to-cell interaction programs neutrophil phagocytic function, resulting in activated platelet clearance. Neutrophils that have internalized platelets circulate in the blood of patients with acute myocardial infarction, and the extent of platelet clearance correlates with expression of platelet activation, including P-selectin. Activated platelets injected intravenously in experimental animals are detectable in circulating neutrophils 60 minutes after, and within 3 hours, more than 70% circulating neutrophils have internalized platelets. Platelet clearance comprises 2 events: adhesion to neutrophils, which requires divalent cations and depends on P-selectin, on the P-selectin glycoprotein ligand-1 (PSGL-1), and on the CD11b/CD18 β2 integrin; and internalization, which is abrogated by the phosphatidylserine-binding protein annexin A5. Adhesion to platelets causes neutrophil degranulation and is blocked by antibodies specific for P-selectin and PSGL-1, either in a synthetic medium in vitro or in the whole blood, therefore in the presence of a physiologic array of plasma cofactors and opsonins. The data suggest that the interaction between circulating platelets and neutrophils influences innate immune functions, possibly contributing to regulate vascular inflammation.


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