Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine

Cellular Physiology and Biochemistry

Volumn 12, Issue 5-6, 2002, Pages 373-384

  Eda, Shigetoshi ^a   Sherman, Irwin W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Malaria; Phosphatidylserine; Red blood cells

Indexed keywords

CD32 ANTIGEN; CD36 ANTIGEN; CHONDROITIN 4 SULFATE; GLYCEROPHOSPHORYLCHOLINE; INTERCELLULAR ADHESION MOLECULE 1; LIPOCORTIN 5; LIPOSOME; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE; THROMBOSPONDIN;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL ASSAY; CELL SURFACE; CHO CELL; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ERYTHROCYTE ADHESIVENESS; FEMALE; IN VITRO STUDY; MALARIA; MELANOMA CELL; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SCHIZONT; AMELANOTIC MELANOMA; ANIMAL; BLOOD; CELL ADHESION; CELL CULTURE; CHEMISTRY; CONFOCAL MICROSCOPY; ERYTHROCYTE; FLOW CYTOMETRY; GROWTH, DEVELOPMENT AND AGING; HAMSTER; HUMAN; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY;

CRICETINAE; CRICETULUS GRISEUS; PLASMODIUM FALCIPARUM;

ANIMALS; ANNEXIN A5; ANTIGENS, CD36; CELL ADHESION; CHO CELLS; CRICETINAE; ERYTHROCYTES; FLOW CYTOMETRY; HUMANS; LIPOSOMES; MALARIA, FALCIPARUM; MELANOMA, AMELANOTIC; MICROSCOPY, CONFOCAL; PHOSPHATIDYLSERINES; PLASMODIUM FALCIPARUM; THROMBOSPONDINS; TUMOR CELLS, CULTURED;

EID: 0036434149     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000067908     Document Type: Article

References (79)

1. Trigg P, Kondrachine A: The current global malaria situation. In Sherman IW, ed. Malaria: Parasite Biology, Pathogenesis and Protection. Washington, D.C., ASM Press, 1998, pp11-22.
2. Sherman IW, Crandall IE, Guthrie N, Land KM: The sticky secrets of sequestration. Parasitology Today 1995;11:378-384.
3. Aikawa M, Rabbege JR, Udeinya I, Miller LH: Electron microscopy of knobs in Plasmodium falciparum-infected erythrocytes. J Parasitol 1983;69:435-437.
4. Taylor DW, Parra M, Chapman GB, Stearns ME, Rener J, Aikawa M, Uni S, Aley SB, Panton LJ, Howard RJ: Localization of Plasmodium falciparum histidine-rich protein 1 in the erythrocyte skeleton under knobs. Mol Biochem Parasitol 1987;25:165-174.
5. Crabb BS, Cooke BM, Reeder JC, Waller RF, Caruana SR, Davern KM, Wickham ME, Brown GV, Coppel RL, Cowman AF: Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 1997;89:287-296.
6. Biggs BA, Culvenor JG, Ng JS, Kemp DJ, Brown GV: Plasmodium falciparum: Cytoadherence of a knobless clone. Exp Parasitol 1989;69:189-197.
7. Ruangjirachuporn W, Afzelius BA, Paulie S, Wahlgren M, Berzins K, Perlmann P: Cytoadherence of knobby and knobless Plasmodium falciparum-infected erythrocytes. Parasitology 1991;102:325-334.
8. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, Feldman M, Traschi TF, Howard RJ: Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized erythrocytes. Cell 1995;82:77-87.
9. Kyes SA, Rowe JA, Kriek N, Newbold CI: Rifins: A second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc Natl Acad Sci USA 1999;96:9333-9338.
10. Ockenhouse CF, Klotz FW, Tandon NN, Jamieson GA: Sequestrin, a CD36 recognition protein on Plasmodium falciparum malaria-infected erythrocytes identified by anti-idiotype antibodies. Proc Natl Acad Sci USA 1991;88:3175-3179.
11. Waller KL, Nunomura W, Cooke BM, Mohandas N, Coppel RL: Mapping the domains of the cytoadherence ligand Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) that bind to the knob-associated histidine-rich protein (KAHRP). Mol Biochem Parasitol 2002;119:125-129.
12. Miller LH, Hudson-Taylor D, Gamain B, Saul AJ: Definition of the minimal domain of CIDR1α of Plasmodium falciparum PfEMP1 for binding CD36. Mol Biochem Parasitol 2002;120:321-323.
13. Smith JD, Craig AG, Kriek N, Hudson-Taylor D, Kyes S, Fagen T, Pinches R, Baruch DI, Newbold CI, Miller LH: Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: A parasite adhesion trait implicated in cerebral malaria. Proc Natl Acad Sci USA 2000;97:1766-1771.
14. Buffet PA, Gamain B, Scheidig C, Baruch D, Smith JD, Hernandez-Rivas R, Pouvelle B, Oishi S, Fujii N, Fusai T, Parzy D, Miller LH, Gysin J, Scherf A: Plasmodium falciparum domain mediating adhesion to chondroitin sulfate A: A receptor for human placental infection. Proc Natl Acad Sci USA 1999;96:12743-12748.
15. Baruch DI, Gormley JA, Ma C, Howard RJ, Pasloske BL: Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Proc Natl Acad Sci USA 1996;93:3497-3452.
16. Crandall I, Land KM, Sherman IW: Plasmodium falciparum: Pfalhesin and CD36 form an adhesin/receptor pair that is responsible for the pH-dependent portion of cytoadherence/sequestration. Exp Parasitol 1994;78:203-209.
17. Eda S, Lawler J, Sherman IW: Plasmodium falciparum-infected erythrocyte adhesion to the type 3 repeat domain of thrombospondin-1 is mediated by a modified band 3 protein. Mol Biochem Parasitol 1999;100:195-205.
18. Treutiger CJ, Heddini A, Fernandez V, Muller W. A, Wahlgren M: PECAM/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nature Med 1997;3:1405-1408.
19. Ockenhouse CF, Tegoshi T, Maeno Y, Benjamin C, Ho M, Kan K, Thway Y, Win K, Aikawa M, Lobb LL: Human vascular endothelial cell adhesion receptors for Plasmodium falciparum-infected erythrocytes: Roles for endothelial leukocyte adhesion molecule-1 and vascular cell adhesion molecule 1. J Exp Med 1992;176:1183-1189.
20. Senczuk AM, Reeder JC, Kosmala MM, Ho M: Plasmodium falciparum erythrocyte membrane protein 1 functions as a ligand for P-selectin. Blood 2001;98:3132-3135.
21. Ho M, Schollaardt T, Niu X, Looareesuwan S, Patel KD, Kubes P: Characterization of Plasmodium falciparum-infected erythrocyte and P-selectin interaction under flow conditions. Blood 1998;91:4803-4809.
22. 3 on human microvascular endothelial cells. Am J Trop Med Hyg 1998;59:77-79.
23. Beeson JG, Rogerson SJ, Cooke BM, Reeder JC, Chai W, Lawson AM, Molyneux ME, Brown GV: Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 2000;6:86-90.
24. Beeson JG, Brown GV: Pathogenesis of Plasmodium falciparum malaria: The roles of parasite adhesion and antigenic variation. Cell Mol Life Sci 2002;59:258-271.
25. Cooke BM, Berendt AR, Craig AG, MacGregor J, Newbold CI, Nash GB: Rolling and stationary cytoadhesion of red blood cells parasitized by Plasmodium falciparum: Separate roles for ICAM-1, CD36 and thrombospondin. Br J Haematol 1994;87:162-170.
26. Rock EP, Roth EF Jr, Rojas-Corona RR, Sherwood JA, Nagel RL, Howard RJ, Kaul D: Thrombospondin mediates the cytoadherence of Plasmodium falciparum-infected red cells to vascular endothelium in shear flow conditions. Blood 1988;71:71-5.
27. Siano JP, Grady KK, Millet P, Swerlick RA, Wick TM: Plasmodium falciparum: Soluble thrombospondin increases cytoadherence of parasitized erythrocytes to human microvascular endothelium under shear flow conditions. Exp Parasitol 1997;87:69-72.
28. Bevers EM, Comfurius P, Dekkers DWC, Zwaal RFA: Lipid translocation across the plasma membrane of mammalian cells. Biochim Biophys Acta 1999;1439:317-330.
29. Joshi P, Dutta GP, Gupta CM: An intracellular simian malarial parasite (Plasmodium knowlesi) induces stage-dependent alterations in membrane phospholipid organization of its host erythrocyte. Biochem J 1987;246:103-108.
30. Maguire PA, Prudhomme J. Sherman IW: Alterations in erythrocyte membrane phospholipid organization due to intracellular growth of the human malaria parasite, Plasmodium falciparum. Parasitology 1991;102:179-186.
31. Sherman IW, Prudhomme J, Tait JF: Altered membrane phospholipid asymmetry in Plasmodium falciparum-infected erythrocytes. Parasitol Today 1997;13:242-243.
32. Tait JF, Smith C. Phosphatidylserine receptors: Role of CD36 in binding of anionic phospholipid vesicles to monocytic cells. J Biol Chem 1999;274:3048-3054.
33. Manodori AB, Barabino GA, Lubin BH, Kuypers FA: Adherence of phosphatidylserine-exposing erythrocytes to endothelial matrix thrombospondin. Blood 2000;95:1293-1300.
34. Roberts DD, Sherwood JA, Spitalnik SL, Panton LJ, Howard R, Dixit VM, Frazier WA, Miller LH, Ginsburg V: Thrombospondin binds falciparum malaria parasitized erythrocytes and mediate cytoadherence. Nature 1985;318:64-66.
35. Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD: Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science 1989;243:1469-1471.
36. Wood BL, Gibson DF, Tait JF: Increased erythrocyte phosphatidylserine exposure in sickle cell diseases: Flowcytometric measurement and clinical associations. Blood 1996;88:1873-1880.
37. Tait JF, Gibson D, Fujikawa K: Phospholipid binding properties of human placental anticoagulant protein I, a member of the lipocortin family. J Biol Chem 1989;264:7944-7949.
38. Hasler T, Albrecht GR, Van Schravendijk MR, Aguiar JC, Morehead KE, Pasloske BL, Ma C, Barnwell JW, Greenwood B, Howard RJ: An improved microassay for P. falciparum cytoadherence using stable transformations of Chinese hamster ovary cells expressing CD36 or intracellular adhesion molecule-1. Am J Trop Med Hyg 1993;48:332-347.
39. Sherman IW, Valdez E: In vitro cytoadherence of Plasmodium falciparum-infected erythrocytes to melanoma cells: Factors affecting adhesion. Parasitology 1989;98:359-369.
40. Lidholt K, Weinke JL, Kiser CS, Lugemwa FN, Bame KJ, Cheifetz S, Massague J, Lindahl U, Esko JD: A single mutation affects both N-acetylglucosaminyltransferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proc Natl Acad Sci USA 1992;89:2267-2271.
41. Tandon NN, Lipsky RH, Burgress WH, Jamieson GA: Isolation and characterization of platelet glycoprotein IV (CD36). J Biol Chem 1989;264:7570-7575.
42. Lawler JW, Slayter HS, Coligan JE: Isolation and characterization of a high molecular weight glycoprotein from human blood platelets. J Biol Chem 1978;253:8609-8616.
43. Cooke BM, Rogerson SJ, Brown GV, Coppel RL: Adhesion of malaria-infected red blood cell to chondroitin sulfate A under flow conditions. Blood 1996;88:4040-4044.
44. Brendt AR, Simmons DL, Tansley J, Newbold CI, Marsh K: Intercellular adhesion molecule 1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature 1989;341:57-59.
45. Trager W, Jensen JB: Human malaria parasites in continuous culture. Science 1976;193:673-675.
46. Pasvol G, Wilson RJ, Smalley ME, Brown J: Separation of viable schizont-infected cells of Plasmodium falciparum from human blood. Ann Trop Med Parasitol 1978;72:87-88.
47. Dittmer JC, Wells MA: Quantitative and qualitative analysis of lipids and lipid components. Methods Enzymol 1969;14:482-530.
48. 2+ concentration on the in vitro cytoadherence of infected erythrocytes to amelanotic melanoma cells. Exp Parasitol 1991;73:362-368.
49. Aikawa M, Udeinya IJ, Rabbege J, Dayan M, Leech JH, Howard RJ, Miller LH: Structural alteration of the membrane of erythrocytes infected with Plasmodium falciparum. J Protozool 1985;32:424-429.
50. Ginsburg H, Kutner S, Krugliak M, Cabantchik ZI: Characterization of permeation pathways appearing in the host membrane of Plasmodium falciparum infected red blood cells. Mol Biochem Parasitol 1985;14:313-322.
51. Kirk K: Membrane transportation in malaria-infected erythrocyte. Physiol Reviews 2001;81:495-537.
52. Paulitschke M, Nash GB: Membrane rigidity of red blood cells parasitized by different strains of Plasmodium falciparum. J Lab Clin Med 1993;122:581-589.
53. Holz GG Jr: Lipids and the malarial parasite. Bull WHO 1977;55:237-248.
54. Green ML, Xiao L, Lal A: Formation of hydroxyeicosatetraenoic acid from hemozoin-catalyzed oxidation of arachidonic acid. Mol Biochem Parasitol 1997;83:183-188.
55. Yuthavong Y, Wilairat P, Panijpan B, Potiwan C, Beale GH: Alterations in membrane proteins of mouse erythrocytes infected with different species and strains of malaria parasites. Comp Biochem Physiol B: Comparative Biochemistry 1979;63:83-85.
56. Joshi P, Gupta CM: Abnormal membrane phospholipid organization in Plasmodium falciparum-infected human erythrocytes. Br J Haematol 1988;68:255-259.
57. Schwartz RS, Olson JA, Raventos-Suarez C, Yee M. Heath RH, Lubin B, Nagel RL: Altered plasma membrane phospholipid organization in Plasmodium falciparum-infected human erythrocytes. Blood 1987;69:401-407.
58. Van der Schaft PH, Beaumelle B, Vial H, Roelofsen B, Op den Kam JAF, Van Deenen LLM: Phospholipid organization in monkey erythrocytes upon Plasmodium knowlesi infection. Biochim Biophys Acta 1987;901:1-14.
59. Moll GN, Vial HJ, Bevers EM, Ancelin ML, Roelofsen B, Comfurius P, Slotboom AJ, Zwaal RFA, Op den Kamp JAF, Van Deenen LL: Phospholipid asymmetry in the plasma membrane of malaria infected erythrocytes. Biochem Cell Biol 1990;68:579-585.
60. Taverne J, Van Schie R, Playfair J, Reutelingsperger C: Malaria: Phosphatidylserine expression is not increased on the surface of parasitized erythrocytes. Parasitol Today 1995;11:298-299.
61. Simoes AP, Roelofsen B, Op den Kamp JAF: Lipid compartmentalization in erythrocytes parasitized by Plasmodium spp. Parasitol Today 1992;8:18-21.
62. Turrini F, Ginsburg H, Bussolino F, Pescarmona G, Serra MV Arese P: Phagocytosis of Plasmodium falciparum-infected red cells by human monocytes: Involvement of immune and nonimmune determinants and dependence on parasite developmental stage. Blood 1992;80:801-808.
63. Facer CA, Agiostratidou G: High levels of antiphospholipid antibodies in uncomplicated and severe Plasmodium falciparum and P. vivax malaria. Clin Exp Immunol 1994;95:304-309.
64. Arduini A, Stern A, Stroto S, Belfiglio M, Mancinelli G, Scurti R, Federici G: Effect of oxidative stress on membrane phospholipid and protein in human erythrocytes. Arch Biochem Biophys 1989;273, 112-120.
65. Bergmann WL, Dressler V, Haest CWM, Deuticke B: Crosslinking of Sh-groups in the erythrocyte membrane enhances transbilayer reolientation of phospholipids. Evidence for a limited access of phospholipids to the reorientation sites. Biochim Biophys Acta 1984;769:390-398.
66. Halbhuber KJ, Stibenz D. Meyer HW, Zimmerman N, Linss W, Oehring H, Brox D: Membrane skeleton alteration-a factor promoting IgG receptor expression in the erythrocyte membrane. Biochim Biophys Acta 1987;46:S88-S92.
67. Tait JF, Gibson D: Measurement of membrane phospholipid asymmetry in normal and sickle-cell erythrocytes by means of annexin V binding. J Lab Clin Med 1994;123:741-748.
68. Kuypers FA, Lewis RA, Hua M, Schott MA, Discher D, Ernst JD, Lubin BH: Detection of altered membrane phospholipid asymmetry in subpopulations of human red blood cells using fluoroscently labeled annexin V. Blood 1996;87:1179-1187.
69. Yashar VB-B, Barenholz Y, Hy-Am E, Rachmilewitz EA, Eldor A: Phosphatidylserine in the outer leaflet of red blood cells from thalassemia patients may explain the chronic hypercoagulable state and thrombotic episode. Am J Hematol 1993;44:63-65.
70. Wilson MJ, Richter-Lowney K, Daleke DL: Hyperglycemia induces a loss of phospholipid asymmetry in human erythrocytes. Biochemistry 1993;32:11302-11310.
71. Beppu M, Ando K, Kikugawa K: Poly-N-acetyllactosaminyl saccharide chains of band 3 as determinants for anti-band 3 autoantibody binding to senescent and oxidized erythrocytes. Cell Mol Biol 1996;42:1007-1024.
72. Telci A, Cakatay U, Salman S, Satman I, Sivas A: Oxidative protein damage in early stage Type 1 diabetic patients. Diabetes Res Clin Pract 2000;50:213-223.
73. Aydin A, Orhan H, Sayal A, Ozata M, Sahin G, Isimer A: Oxidative stress and nitric oxide related parameters in type II diabetes mellitus: Effects of glycemic control. Clin Biochem 2001;34:65-70.
74. Savill J, Fadok V: Corpse clearance defines the meaning of cell death. Nature 2000;407:784-788.
75. Newbold C, Warn P, Black G, Berendt A, Craig A, Snow B, Msobo M, Peshu N, Marsh K: Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am J Trop Med Hyg 1997;57:389-398.
76. Hillery CA, Scott JP, Du, MC: The carboxy-terminal cell binding domain of thrombospondin is essential for sickle red blood cell adhesion. Blood 1999;94:302-309.
77. Setty BN, Kulkarni S, Stuart MJ: Role of erythrocyte phosphatidylserine in sickle red cell-endothelial adhesion. Blood 2002;99:1564-1571.
78. Lucas, JZ, Sherman, IW: Plasmodium falciparum: Thrombospondin mediates parasitized erythrocyte band 3-related adhesin binding. Exp Parasitol 1998;89:78-85.
79. Yamaguchi A, Yamamoto N, Akamatsu N, Saito TC, Kaneda M, Umeda M, Tanoue K: PS-liposome and ox-LDL bind to different sites of the immunodominant domain (#155-183) of CD36: A study with GS95, a new anti-CD36 monoclonal antibody. Thromb Res 2000;97:317-326.