Macrophage Migration Inhibitory Factor Release by Macrophages after Ingestion of Plasmodium chabaudi-Infected Erythrocytes: Possible Role in the Pathogenesis of Malarial Anemia

doi:10.1128/IAI.68.4.2259-2267.2000

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Infection and Immunity, April 2000, p. 2259-2267, Vol. 68, No. 4
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Macrophage Migration Inhibitory Factor Release by Macrophages after Ingestion of Plasmodium chabaudi-Infected Erythrocytes: Possible Role in the Pathogenesis of Malarial Anemia

James A. Martiney,¹^,^* Barbara Sherry,¹ Christine N. Metz,² Marisol Espinoza,¹ Angel S. Ferrer,¹ Thierry Calandra,²^, Hal E. Broxmeyer,³ and Richard Bucala²

Laboratory of Cytokine Biology¹ and Laboratory of Medical Biochemistry,² The Picower Institute for Medical Research, Manhasset, New York 11030, and Department of Microbiology and Immunology and The Walther Oncology Center, Indiana University School of Medicine, Indianapolis, Indiana 46202³

Received 24 August 1999/Returned for modification 7 October 1999/Accepted 13 January 2000

Human falciparum malaria, caused by Plasmodium falciparum infection, results in 1 to 2 million deaths per year, mostly childrenunder the age of 5 years. The two main causes of death are severeanemia and cerebral malaria. Malarial anemia is characterizedby parasite red blood cell (RBC) destruction and suppression oferythropoiesis (the mechanism of which is unknown) in the presenceof a robust host erythropoietin response. The production of ahost-derived erythropoiesis inhibitor in response to parasiteproducts has been implicated in the pathogenesis of malarial anemia.The identity of this putative host factor is unknown, but antibodyneutralization studies have ruled out interleukin-1 $beta$ , tumor necrosisfactor alpha, and gamma interferon while injection of interleukin-12protects susceptible mice against lethal P. chabaudi infection.In this study, we report that ingestion of P. chabaudi-infectederythrocytes or malarial pigment (hemozoin) induces the releaseof macrophage migration inhibitory factor (MIF) from macrophages.MIF, a proinflammatory mediator and counter-regulator of glucocorticoidaction, inhibits erythroid (BFU-E), multipotential (CFU-GEMM),and granulocyte-macrophage (CFU-GM) progenitor-derived colonyformation. MIF was detected in the sera of P. chabaudi-infectedBALB/c mice, and circulating levels correlated with disease severity.Liver MIF immunoreactivity increased concomitant with extensivepigment and parasitized RBC deposition. Finally, MIF was elevatedthree- to fourfold in the spleen and bone marrow of P. chabaudi-infectedmice with active disease, as compared to early disease, or ofuninfected controls. In summary, the present results suggest thatMIF may be a host-derived factor involved in the pathophysiologyof malariaanemia.

^* Corresponding author. Mailing address: Forchheimer 520 Department of Pathology, Albert Einstein College of Medicine, 1300Morris Park Ave., Bronx, NY 10461. Phone: (718) 430-2048. Fax:(718) 430-2140. E-mail: martiney{at}freewweb.com.

Present address: Division of Infectious Diseases, Department of Internal Medicine, BH-19.111, CHUV, CH-1011 Lausanne,Switzerland.

Infection and Immunity, April 2000, p. 2259-2267, Vol. 68, No. 4
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

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