CD36-mediated nonopsonic phagocytosis of erythrocytes infected with stage I and IIA gametocytes of Plasmodium falciparum

Infection and Immunity

Volumn 71, Issue 1, 2003, Pages 393-400

  Smith, Todd G ^a   Serghides, Lena ^a   Patel, Samir N ^a   Febbraio, Maria ^b   Silverstein, Roy L ^b   Kain, Kevin C ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALITRETINOIN; CD36 ANTIGEN; MONOCLONAL ANTIBODY; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTAGLANDIN J2; RETINOID X RECEPTOR; TRYPSIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; GAMETOCYTE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTERNALIZATION; MALARIA; MICROSCOPY; MONOCYTE; MOUSE; NONHUMAN; PARASITE TRANSMISSION; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD36; CELLS, CULTURED; ERYTHROCYTES; HUMANS; MACROPHAGES, PERITONEAL; MALARIA, FALCIPARUM; MICE; MONOCYTES; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; TRANSCRIPTION FACTORS; TRYPSIN; UP-REGULATION;

EID: 0037220515     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.1.393-400.2003     Document Type: Article

References (56)

1. Aikawa, M., M. Iseki, J. W. Barnwell, D. Taylor, M. M. Oo, and R. J. Howard. 1990. The pathology of human cerebral malaria. Am. J. Trop. Med. Hyg. 43:30-37.
2. Aitman, T. J., L. D. Cooper, P. J. Norsworthy, F. N. Wahid, J. K. Gray, B. R. Curtis, P. M. McKeigue, D. Kwiatkowski, B. M. Greenwood, R. W. Snow, A. V. Hill, and J. Scott. 2000. Malaria susceptibility and CD36 mutation. Nature 405:1015-1016.
3. Anonymous. 1999. Malaria, 1982-1997. W. H. O. Wkly. Epidemiol. Rec. 74:265-270.
4. Baker, D. A., O. Daramola, M. V. MeCrossan, J. Harmer, and G. A. T. Targett. 1994. Subcellular localization of Pfsl6, a Plasmodium falciparum gametocyte antigen. Parasitology 108:129-137.
5. Barnwell, J. W., and M. R. Galinski. 1998. Invasion of vertebrate cells: erythrocytes, p. 93-120. In I. W. Sherman (ed.), Malaria: Parasite Biology, Pathogenesis, and Protection. ASM Press, Washington, D.C.
6. Baruch, D. I., J. A. Gormley, C. Ma, R. J. Howard, and B. L. Pasloske. 1996. Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intracellular adhesion molecule 1. Proc. Natl. Acad. Sci. USA 93:3497-3502.
7. Baruch, D. I., X. C. Ma, H. B. Singh, X. Bi, B. L. Pasloske, and R. J. Howard. 1997. Identification of a region of PfEMP1 that mediates adherence of Plasmadium falciparum infected erythrocytes to CD36: Conserved function with variant sequence. Blood 90:3766-3775.
8. Beeson, J. G., S. J. Rogerson, B. M. Cooke, J. C. Reeder, W. Chai, A. M. Lawson, M. E. Molyneux, and G. V. Brown. 2000. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat. Med. 6:86-90.
9. Berendt, A. R., D. Simmons, J. Tansey, C. K. Newbold, and K. Marsh. 1989. Intercellular adhesion molecule 1 (ICAM-1) is an endothelial cytoadherence receptor for Plasmodium falciparum. Nature 341:57-59.
10. Bouharoun-Tayoun, H., C. Oeuvray, F. Lunel, and P. Druilhe. 1995. Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J. Exp. Med. 182:409-418.
11. Bruce, M. C., D. A. Baker, P. Alano, N. C. Rogers, P. M. Graves, G. A. Targett, and R. Carter. 1990. Sequence coding for a sexual stage specific protein of Plasmodium falciparum. Nucleic Acids Res. 18:3637.
12. Bruce, M. C., N. C. Carter, K. Nakamura, M. Aikawa, and R. Carter. 1994. Cellular location and temporal expression of the Plasmodium falciparum sexual stage antigen Pfsl6. Mol. Biochem. Parasitol. 65:11-22.
13. Carter, R., and P. M. Graves. 1988. Gametocytes, p. 253-305. In W. H. Wernsdorfer and I. A. McGregor (ed.), Malaria: Principles and Practice of Malariology. Churchill Livingstone, Edinburgh, Scotland.
14. Carter, R., L. C. Ranford-Cartwright, and P. Alano. 1993. The culture and preparation of gametocytes of Plasmyodium falciparum for immunochemical, molecular, and mosquito infectivity studies, p. 67-88. In J. E. Hyde (ed.), Methods in Molecular Biology, Vol. 21. Protocols in Molecular Parasitology. Humana Press, Totawa, N.J.
15. Celada, A., A. Cruchaud, and L. H. Perrin. 1983. Phagocytosis of Plasmodium falciparum-parasitized erythrocytes by human polymorphonuclear leukocytes. J. Parasitol. 69:49-53.
16. Chiayaroj, S. C., P. Angkasekwinai, A. Buranakiti, S. Looareesuwan, S. J. Rogerson, and G. V. Brown. 1996. Cytoadherence characteristics of Plasmodium falciparum isolates from Thailand: Evidence for chondroitin sulfate as a cytoadherence receptor. Am. J. Trop. Med. Hyg. 55:76-80.
17. Cooke, B. M., C. L. Nicoll, D. I. Baruch, and R. L. Coppel. 1998. A recombinant peptide based on PfEMP-1 blocks and reverses adhesion of malariainfected red blood cells to CD36 under flow. Mol. Microbiol. 30:83-90.
18. Day, K. P., R. E. Hayward, and M. Dyer. 1998. The biology of Plasmodium falciparum transmission stages. Parasitology 116:S95-S109.
19. Deitsch, K. W., and T. E. Wellems. 1996. Membrane modifications in erythrocytes parasitized by Plasmodium falciparum. Mol. Biochem. Parasitol, 76: 1-10.
20. Febbraio, M., N. A. Abumrad, D. P. Hajjar, K. Sharma, W. Cheng, S. F. A. Pearce, and R. L. Silverstein. 1999. A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J. Biol. Chem. 274:19055-19062.
21. Ferrante, A., L. Kumaratilake, C. M. Rzepczyk, and J.-M. Dayer. 1990. Killing of Plasmodium falciparum by cytokine-activated effector cells (neutrophils and macrophages). Immunol. Lett. 25:179-188.
22. Hayward, R. E., B. Tiwari, K. P. Piper, D. I. Baruch, and K. P. Day. 1999. Virulence and transmission success of the malarial parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 96:4563-4568.
23. Healer, J., A. Graszynski, and E. Riley. 1999. Phagocytosis does not play a major role in naturally acquired transmission-blocking immunity to Plasmodium falciparum malaria. Infect. Immun. 67:2334-2339.
24. Kaslow, D. C. 1998. Acquired immunity to sexual stages, p. 457-466. In I. W. Sherman (ed.), Malaria: Parasite Biology, Pathogenesis, and Protection. ASM Press, Washington, D.C.
25. Kersten, S., B. Desvergne, and W. Wahli. 2000. Roles of PPARs in health and disease. Nature 405:421-424.
26. Lensen, A., L. Mulder, T. Tchuinkam, L. Willemsen, W. Eling, and R. Sauerwein. 1998. Mechanisms that reduce transmission of Plasmodium falciparum malaria in semiimmune and nonimmune persons. J. Infect. Dis. 177:1358-1363.
27. Lensen, A. H. W., M. Bolmer-Van de Vegte, G. J. Van Gemert, W. M. C. Eling, and R. W. Sauerwein. 1997. Leukocytes in a Plasmodium falciparum-infected blood meal reduce transmission of malaria to Anopheles mosquitoes. Infect. Immun. 65:3834-3837.
28. McGilvray, I. D., L. Serghides, A. Kapus, O. D. Rotstein, and K. C. Kain. 2000. Non-opsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitised erythrocytes: A role of CD36 in malarial clearance. Blood 96:3231-3240.
29. Miller, L. H., M. F. Good, and G. Milon. 1994. Malaria pathogenesis. Science 264:1878-1883.
30. Miller, L. H., D. I. Baruch, K. Marsh, and O. K. Doumbo. 2002. The pathogenic basis of malaria. Nature 415:673-679.
31. Newbold, C. I., G. Warn, A. Black, A. Berendt, A. Craig, B. Snow, M. Msobo, N. Peshu, and K. Marsh. 1997. Receptor-specific adhesion and clinical disease in Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 57:389-398.
32. Ockenhouse, C. F., and J. D. Chulay. 1988. Plasmodium falciparum sequestration: OKM5 antigen (CD36) mediates cytoadherence of parasitized erythrocytes to a myelo-monocytic cell line. J. Infect. Dis. 157:584-588.
33. Ockenhouse, C. F., M. Ho, N. N. Tandon, G. A. Van Seventer, S. Shaw, N. J. White, G. A. Jamieson, J. D. Chulay, and H. K. Webster. 1991. Molecular basis of sequestration in severe and uncomplicated Plasmodium falciparum malaria: Differential adhesion of infected erythrocytes to CD36 and ICAM-1. J. Infect. Dis. 164:163-169.
34. Ockenhouse, C. F., C. Magowan, and J. D. Chulay. 1989. Activation of monocytes and platelets by monoclonal antibodies or malaria-infected erythrocytes binding to the CD36 surface receptor in vitro. J. Clin. Investig. 84:468-475.
35. Oquendo, P., E. Hundt, J. Lawler, and B. Seed. 1989. CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell 58: 95-101.
36. Roberts, D. D., J. A. Sherwood, S. L. Spitalnik, L. J. Panton, R. J. Howard, V. M. Dixit, W. A. Frazier, L. H. Miller, and V. Grinsburg. 1985. Thrombospondin binds falciparum parasitized erythrocytes and may mediate cytoadherence. Nature 318:64-66.
37. Rogers, N. J., B. S. Hall, J. Obiero, G. A. T. Targett, and C. J. Sutherland. 2000. A model for sequestration of the transmission stages of Plasmodium falciparum: Adhesion of gametocyte-infected erythrocytes to human bone marrow cells. Infect. Immun. 68:3455-3462.
38. Savill, J., N. Hogg, Y. Ren, and C. Haslett. 1992. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Investig. 90:1513-1522.
39. Serghides, L., I. C. Crandall, E. Hull, and K. C. Kain. 1998. The Plasmodium falciparum-CD36 interaction is modified by a single amino acid substitution in CD36. Blood 92:1814-1819.
40. Serghides, L., and K. C. Kain. 2001. PPARγ-RXR agonists increase CD36-dependent phagocytosis of Plasmodium falciparum-parasitized erythrocytes and decrease malaria-induced TNFα secretion by monocytes/macrophages. J. Immunol. 166:6742-6748.
41. Serghides, L., and K. C. Kain. 2002. Mechanism of vitamin A-induced protection in falciparum malaria. Lancet 359:1404-1406.
42. 3 on human microvascular endothelial cells. Am. J. Trop. Med. Hyg. 59:77-79.
43. Sinden, R. E., and M. E. Smalley. 1976. Gametocytes of Plasmodium falciparum: Phagocytosis by leucocytes in vivo and in vitro. Trans. R. Soc. Trop. Med. Hyg. 70:344-345.
44. Smalley, M. E. 1976. Plasmodium falciparum gametocytogenesis in vitro. Nature 264:271-272.
45. Smalley, M. E., S. Abdalla, and J. Brown. 1980. The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans. R. Soc. Trop. Med. Hyg. 75:103-105.
46. Smith, T. G., P. Lourenco, R. Carter, D. Walliker, and L. C. Ranford-Cartwright. 2000. Commitment to sexual differentiation in the human malaria parasite, Plasmodium falciparum. Parasitology 121:127-133.
47. Taylor, L. H., and A. F. Read. 1997. Why so few transmission stages? Reproductive restraint by malaria parasites. Parasitol. Today 13:135-140.
48. Tontonoz, P., L. Nagy, J. G. Alvarez, V. A. Thomazy, and R. M. Evans. 1998. PPARγ promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93:241-252.
49. Trager, W., and J. B. Jensen. 1976. Human malaria parasites in continuous culture. Science 193:673-677.
50. Trubowitz, S., and B. Mazek. 1968. Plasmodium falciparum: Phagocytosis by polymorphonuclear leukocytes. Science 162:273-274.
51. Turner, G. D., H. Morrison, and M. Jones. 1994. An immunohistochemical study of the pathology of fatal malaria. Am. J. Pathol. 145:1057-1069.
52. Turrini, F., H. Ginsburg, F. Bussolino, G. P. Pescarmona, M. V. Serra, and P. Arese. 1992. Phagocytosis of Plasmodium falciparum-infected human red blood cells by human monocytes: Involvement of immune and non-immune determinants and dependence on parasite developmental stage. Blood 80: 801-808.
53. Walliker, D., I. A. Quakyi, T. E. Wellems, T. F. McCutchan, A. Szarfman, W. T. London, L. M. Corcoran, T. R. Burkot, and R. Carter. 1987. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236:1661-1666.
54. West, S. A., T. G. Smith, and A. F. Read. 2000. Sex allocation and population structure in apicomplexan (protozoa) parasites. Proc. R. Soc. Lond. B 267: 257-263.
55. West, S. A., T. G. Smith, S. R. Lee, and A. F. Read. 2002. Fertility insurance and the sex ratios of malaria and related haemospororin blood parasites. J. Parasitol. 88:258-263.
56. Wozencraft, A. O., H. M. Dockrell, J. Taverne, G. A. T. Targett, and J. H. L. Playfair. 1984. Killing of human malaria parasites by macrophage secretory products. Infect. Immun. 43:664-669.