Platelet microparticles: A new player in malaria parasite cytoadherence to human brain endothelium

FASEB Journal

Volumn 23, Issue 10, 2009, Pages 3449-3458

  Faille, Dorothée ^a,b   Combes, Valéry ^a   Mitchell, Andrew J ^c   Fontaine, Albin ^b   Juhan Vague, Irène ^d   Alessi, Marie Christine ^d   Chimini, Giovanna ^c   Fusaï, Thierry ^b   Grau, Georges E ^a  

^a University of Sydney   (Australia)

^b SERVICE DE SANTÉ DES ARMÉES   (France)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Antigen transfer; Internalization; Microvessels; Neuroinflammation; Pathogenesis; Vesiculation

Indexed keywords

CD31 ANTIGEN; CD36 ANTIGEN; ERYTHROCYTE MEMBRANE PROTEIN 1; MONOCLONAL ANTIBODY; THROMBOCYTE ANTIGEN; TRYPSIN;

ARTICLE; BINDING AFFINITY; BLOOD BRAIN BARRIER; BRAIN ENDOTHELIUM; BRAIN MALARIA; CELL INTERACTION; ENDOTHELIUM; ERYTHROCYTE; ERYTHROCYTE ADHESIVENESS; ERYTHROCYTE MEMBRANE; HUMAN; HUMAN CELL; NONHUMAN; PATHOGENESIS; PHENOTYPE; PLASMODIUM FALCIPARUM; PLATELET MICROPARTICLE; PRIORITY JOURNAL; PROTEIN VARIANT;

PLASMODIUM FALCIPARUM;

EID: 70349666551     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-135822     Document Type: Article

References (53)

1. Newton, C. R., and Krishna, S. (1998) Severe falciparum malaria in children: current understanding of pathophysiology and supportive treatment. Pharmacol. Ther. 79, 1-53
2. Idro, R., Jenkins, N. E., and Newton, C. R. (2005) Pathogenesis, clinical features, and neurological outcome of cerebral malaria. Lancet Neurol. 4, 827-840 (Pubitemid 41619438)
3. Silamut, K., Phu, N. H., Whitty, C., Turner, G. D., Louwrier, K., Mai, N. T., Simpson, J. A., Hien, T. T., and White, N. J. (1999) A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am. J. Pathol. 155, 395-410 (Pubitemid 29370390)
4. Patnaik, J. K., Das, B. S., Mishra, S. K., Mohanty, S., Satpathy, S. K., and Mohanty, D. (1994) Vascular clogging, mononuclear cell margination, and enhanced vascular permeability in the pathogenesis of human cerebral malaria. Am. J. Trop. Med. Hyg. 51, 642-647 (Pubitemid 24378561)
5. Porta, J., Carota, A., Pizzolato, G. P., Wildi, E., Widmer, M. C., Margairaz, C., and Grau, G. E. (1993) Immunopathological changes in human cerebral malaria. Clin. Neuropathol. 12, 142-146 (Pubitemid 23176558)
6. Grau, G. E., Mackenzie, C. D., Carr, R. A., Redard, M., Pizzolato, G., Allasia, C., Cataldo, C., Taylor, T. E., and Molyneux, M. E. (2003) Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J. Infect. Dis. 187, 461-466 (Pubitemid 36184587)
7. Yipp, B. G., Baruch, D. I., Brady, C., Murray, A. G., Looareesuwan, S., Kubes, P., and Ho, M. (2003) Recombinant PfEMP1 peptide inhibits and reverses cytoadherence of clinical Plasmodium falciparum isolates in vivo. Blood 101, 331-337 (Pubitemid 36025927)
8. Rogerson, S. J., Chaiyaroj, S. C., Ng, K., Reeder, J. C., and Brown, G. V. (1995) Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes. J. Exp. Med. 182, 15-20
9. Treutiger, C. J., Heddini, A., Fernandez, V., Muller, W. A., and Wahlgren, M. (1997) PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nat. Med. 3, 1405-1408 (Pubitemid 28011044)
10. Ho, M., and White, N. J. (1999) Molecular mechanisms of cytoadherence in malaria. Am. J. Physiol. 276, C1231-1242
11. Ringwald, P., Peyron, F., Lepers, J. P., Rabarison, P., Rakotomalala, C., Razanamparany, M., Rabodonirina, M., Roux, J., and Le Bras, J. (1993) Parasite virulence factors during falciparum malaria: rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infect. Immun. 61, 5198-5204 (Pubitemid 23353898)
12. Carlson, J., Nash, G. B., Gabutti, V., al-Yaman, F., and Wahlgren, M. (1994) Natural protection against severe Plasmodium falciparum malaria due to impaired rosette formation. Blood 84, 3909-3914
13. Rowe, A., Obeiro, J., Newbold, C. I., and Marsh, K. (1995) Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect. Immun. 63, 2323-2326
14. Fernandez, V., Treutiger, C. J., Nash, G. B., and Wahlgren, M. (1998) Multiple adhesive phenotypes linked to rosetting binding of erythrocytes in Plasmodium falciparum malaria. Infect. Immun. 66, 2969-2975 (Pubitemid 28261810)
15. Hunt, N. H., and Grau, G. E. (2003) Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol. 24, 491-499 (Pubitemid 37088152)
16. Pain, A., Ferguson, D. J., Kai, O., Urban, B. C., Lowe, B., Marsh, K., and Roberts, D. J. (2001) Platelet-mediated clumping of Plasmodium falciparum-infected erythrocytes is a common adhesive phenotype and is associated with severe malaria. Proc. Natl. Acad. Sci. U. S. A. 98, 1805-1810 (Pubitemid 32165579)
17. Chotivanich, K., Sritabal, J., Udomsangpetch, R., Newton, P., Stepniewska, K. A., Ruangveerayuth, R., Looareesuwan, S., Roberts, D. J., and White, N. J. (2004) Platelet-induced autoagglutination of Plasmodium falciparum-infected red blood cells and disease severity in Thailand. J. Infect. Dis. 189, 1052-1055 (Pubitemid 38373098)
18. Wassmer, S. C., Lepolard, C., Traore, B., Pouvelle, B., Gysin, J., and Grau, G. E. (2004) Platelets reorient Plasmodium falciparuminfected erythrocyte cytoadhesion to activated endothelial cells. J. Infect. Dis. 189, 180-189 (Pubitemid 38147240)
19. Wassmer, S. C., Combes, V., Candal, F. J., Juhan-Vague, I., and Grau, G. E. (2006) Platelets potentiate brain endothelial alterations induced by Plasmodium falciparum. Infect. Immun. 74, 645-653 (Pubitemid 43023120)
20. Von Zur Muhlen, C., Sibson, N. R., Peter, K., Campbell, S. J., Wilainam, P., Grau, G. E., Bode, C., Choudhury, R. P., and Anthony, D. C. (2008) A contrast agent recognizing activated platelets reveals murine cerebral malaria pathology undetectable by conventional MRI. J. Clin. Invest. 118, 1198-1207
21. Grau, G. E., Pointaire, P., Piguet, P. F., Vesin, C., Rosen, H., Stamenkovic, I., Takei, F., and Vassalli, P. (1991) Late administration of monoclonal antibody to leukocyte function-antigen 1 abrogates incipient murine cerebral malaria. Eur. J. Immunol. 21, 2265-2267
22. Sun, G., Chang, W. L., Li, J., Berney, S. M., Kimpel, D., and van der Heyde, H. C. (2003) Inhibition of platelet adherence to brain microvasculature protects against severe Plasmodium berghei malaria. Infect. Immun. 71, 6553-6561 (Pubitemid 37337715)
23. Grau, G. E., Tacchini-Cottier, F., Vesin, C., Milon, G., Lou, J. N., Piguet, P. F., and Juillard, P. (1993) TNF-induced microvascular pathology: active role for platelets and importance of the LFA-1/ICAM-1 interaction. Eur. Cytokine Netw. 4, 415-419 (Pubitemid 24062019)
24. Van der Heyde, H. C., Gramaglia, I., Sun, G., and Woods, C. (2005) Platelet depletion by anti-CD41 (αIIb) mAb injection early but not late in the course of disease protects against Plasmodium berghei pathogenesis by altering the levels of pathogenic cytokines. Blood 105, 1956-1963 (Pubitemid 40731778)
25. Hugel, B., Martinez, M. C., Kunzelmann, C., and Freyssinet, J. M. (2005) Membrane microparticles: two sides of the coin. Physiology (Bethesda) 20, 22-27 (Pubitemid 40363367)
26. Nomura, S., Tandon, N. N., Nakamura, T., Cone, J., Fukuhara, S., and Kambayashi, J. (2001) High-shear-stress-induced activation of platelets and microparticles enhances expression of cell adhesion molecules in THP-1 and endothelial cells. Atherosclerosis 158, 277-287 (Pubitemid 32913636)
27. Barry, O. P., Pratico, D., Savani, R. C., and FitzGerald, G. A. (1998) Modulation of monocyte-endothelial cell interactions by platelet microparticles. J. Clin. Invest. 102, 136-144 (Pubitemid 28323840)
28. Salanova, B., Choi, M., Rolle, S., Wellner, M., Luft, F. C., and Kettritz, R. (2007) β2-Integrins and acquired glycoprotein IIb/IIIa (GPIIb/IIIa) receptors cooperate in NF-κB activation of human neutrophils. J. Biol. Chem. 282, 27960-27969 (Pubitemid 47529545)
29. Combes, V., Taylor, T. E., Juhan-Vague, I., Mege, J. L., Mwenechanya, J., Tembo, M., Grau, G. E., and Molyneux, M. E. (2004) Circulating endothelial microparticles in Malawian children with severe falciparum malaria complicated with coma. JAMA 291, 2542-2544 (Pubitemid 38702769)
30. Combes, V., Coltel, N., Alibert, M., van Eck, M., Raymond, C., Juhan-Vague, I., Grau, G. E., and Chimini, G. (2005) ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am. J. Pathol. 166, 295-302 (Pubitemid 40051681)
31. Piguet, P. F., Kan, C. D., and Vesin, C. (2002) Thrombocytopenia in an animal model of malaria is associated with an increased caspase-mediated death of thrombocytes. Apoptosis 7, 91-98
32. Diamant, M., Tushuizen, M. E., Sturk, A., and Nieuwland, R. (2004) Cellular microparticles: new players in the field of vascular disease? Eur. J. Clin. Invest. 34, 392-401 (Pubitemid 38859560)
33. Fried, M., and Duffy, P. E. (1996) Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272, 1502-1504 (Pubitemid 26200005)
34. Trager, W., and Jensen, J. B. (1976) Human malaria parasites in continuous culture. Science 193, 673-675
35. Jensen, J. B. (1978) Concentration from continuous culture of erythrocytes infected with trophozoites and schizonts of Plasmodium falciparum. Am. J. Trop. Med. Hyg. 27, 1274-1276
36. Dorovini-Zis, K., Prameya, R., and Bowman, P. D. (1991) Culture and characterization of microvascular endothelial cells derived from human brain. Lab. Invest. 64, 425-436
37. Tocchetti, E. V., Flower, R. L., and Lloyd, J. V. (2001) Assessment of in vitro-generated platelet microparticles using a modified flow cytometric strategy. Thromb. Res. 103, 47-55
38. Leech, J. H., Barnwell, J. W., Miller, L. H., and Howard, R. J. (1984) Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J. Exp. Med. 159, 1567-1575 (Pubitemid 14117068)
39. Bjerknes, R., and Bassoe, C. F. (1984) Phagocyte C3-mediated attachment and internalization: flow cytometric studies using a fluorescence quenching technique. Blut 49, 315-323 (Pubitemid 14006786)
40. Lou, J., Lucas, R., and Grau, G. E. (2001) Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans. Clin. Microbiol. Rev. 14, 810-820, table of contents (Pubitemid 32979632)
41. Wassmer, S. C., Taylor, T., Maclennan, C. A., Kanjala, M., Mukaka, M., Molyneux, M. E., and Grau, G. E. (2008) Platelet-induced clumping of Plasmodium falciparum-infected erythrocytes from Malawian patients with cerebral malaria - possible modulation in vivo by thrombocytopenia. J. Infect. Dis. 197, 72-78 (Pubitemid 351263469)
42. Steiner, M. (1987) Platelet surface glycosaminoglycans are an effective shield for distinct platelet receptors. Biochim. Biophys. Acta 931, 286-293
43. Mack, M., Kleinschmidt, A., Bruhl, H., Klier, C., Nelson, P. J., Cihak, J., Plachy, J., Stangassinger, M., Erfle, V., and Schlondorff, D. (2000) Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat. Med. 6, 769-775 (Pubitemid 30469425)
44. Del Conde, I., Shrimpton, C. N., Thiagarajan, P., and Lopez, J. A. (2005) Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 106, 1604-1611 (Pubitemid 41208572)
45. Flaumenhaft, R. (2006) Formation and fate of platelet microparticles. Blood Cells Mol. Dis. 36, 182-187
46. Birts, C. N., Barton, C. H., and Wilton, D. C. (2008) A catalytically independent physiological function for human acute phase protein group IIA phospholipase A2: cellular uptake facilitates cell debris removal. J. Biol. Chem. 283, 5034-5045
47. Pradhan, D., Williamson, P., and Schlegel, R. A. (1994) Phosphatidylserine vesicles inhibit phagocytosis of erythrocytes with a symmetric transbilayer distribution of phospholipids. Mol. Membr. Biol. 11, 181-187
48. Setty, B. N., and Betal, S. G. (2008) Microvascular endothelial cells express a phosphatidylserine receptor: a functionally active receptor for phosphatidylserine-positive erythrocytes. Blood 111, 905-914
49. Manodori, A. B., Barabino, G. A., Lubin, B. H., and Kuypers, F. A. (2000) Adherence of phosphatidylserine-exposing erythrocytes to endothelial matrix thrombospondin. Blood 95, 1293-1300
50. Fajardo, L. F. (1973) Letter: malarial parasites in mammalian platelets. Nature 243, 298-299
51. McMorran, B. J., Marshall, V. M., de Graaf, C., Drysdale, K. E., Shabbar, M., Smyth, G. K., Corbin, J. E., Alexander, W. S., and Foote, S. J. (2009) Platelets kill intraerythrocytic malarial parasites and mediate survival to infection. Science 323, 797-800
52. Sinauridze, E. I., Kireev, D. A., Popenko, N. Y., Pichugin, A. V., Panteleev, M. A., Krymskaya, O. V., and Ataullakhanov, F. I. (2007) Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb. Haemost. 97, 425-434
53. Nomura, S., Inami, N., and Iwasaka, T. (2007) Differences in functional roles between activated platelets and platelet-derived microparticles. Thromb. Haemost. 98, 1143-1144 (Pubitemid 350091147)