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Infection and Immunity, March 2007, p. 1116-1128, Vol. 75, No. 3
0019-9567/07/$08.00+0     doi:10.1128/IAI.00902-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Functional Characterization of the Plasmodium falciparum and P. berghei Homologues of Macrophage Migration Inhibitory Factor{triangledown}

Kevin D. Augustijn,1 Robert Kleemann,2 Joanne Thompson,3 Teake Kooistra,2 Carina E. Crawford,3 Sarah E. Reece,3 Arnab Pain,4 Arjan H. G. Siebum,5 Chris J. Janse,1 and Andrew P Waters1*

Department of Parasitology, LUMC, Albinusdreef 2, 2333 ZA, Leiden, The Netherlands,1 Vascular and Metabolic Diseases, TNO-Quality of Life, Zernikedreef 9, 2333 CK, Leiden, The Netherlands,2 Institute of Immunology and Infection Research, Kings Buildings, Ashworth Laboratories, West Mains Road, EH9 3JT Edinburgh, United Kingdom,3 The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA Cambridge, Cambridge, United Kingdom,4 Leiden Institute of Chemistry, Gorlaeus Laboratories, Einsteinweg 55, 2333 CC, Leiden, The Netherlands5

Received 7 June 2006/ Returned for modification 16 August 2006/ Accepted 3 December 2006

Macrophage migration inhibitory factor (MIF) is a mammalian cytokine that participates in innate and adaptive immune responses. Homologues of mammalian MIF have been discovered in parasite species infecting mammalian hosts (nematodes and malaria parasites), which suggests that the parasites express MIF to modulate the host immune response upon infection. Here we report the first biochemical and genetic characterization of a Plasmodium MIF (PMIF). Like human MIF, histidine-tagged purified recombinant PMIF shows tautomerase and oxidoreductase activities (although the activities are reduced compared to those of histidine-tagged human MIF) and efficiently inhibits AP-1 activity in human embryonic kidney cells. Furthermore, we found that Plasmodium berghei MIF is expressed in both a mammalian host and a mosquito vector and that, in blood stages, it is secreted into the infected erythrocytes and released upon schizont rupture. Mutant P. berghei parasites lacking PMIF were able to complete the entire life cycle and exhibited no significant changes in growth characteristics or virulence features during blood stage infection. However, rodent hosts infected with knockout parasites had significantly higher numbers of circulating reticulocytes. Our results suggest that PMIF is produced by the parasite to influence host immune responses and the course of anemia upon infection.

* Corresponding author. Mailing address: Department of Parasitology, LUMC, Albinusdreef 2, Room P4-35, 2333 ZA Leiden, The Netherlands. Phone: 31-71 5265069. Fax: 31-71 5266907. E-mail: waters{at}lumc.nl.

{triangledown} Published ahead of print on 11 December 2006.

Editor: J. F. Urban, Jr.

Infection and Immunity, March 2007, p. 1116-1128, Vol. 75, No. 3
0019-9567/07/$08.00+0     doi:10.1128/IAI.00902-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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