Erythrocyte membrane alterations in Plasmodium falciparum malaria sequestration

Current Opinion in Hematology

Volumn 4, Issue 2, 1997, Pages 148-154

  Oh, S Steven ^a   Chishti, Athar H ^a   Palek, Jiri ^a   Liu, Shih Chun ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL MEMBRANE PROTEIN; ERYTHROCYTE BAND 3 PROTEIN; ERYTHROCYTE BAND 4.1 PROTEIN; HISTIDINE; MEMBRANE RECEPTOR; SPECTRIN;

BRAIN MALARIA; CYTOSKELETON; ERYTHROCYTE ADHESIVENESS; ERYTHROCYTE MEMBRANE; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; MALARIA; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SHORT SURVEY;

EID: 0030910143     PISSN: 10656251     EISSN: None     Source Type: Journal    
DOI: 10.1097/00062752-199704020-00012     Document Type: Short Survey

References (67)

1. Warrell DA: Pathophysiology of severe falciparum malaria in man. Parasitology 1987, 94(suppl):S53-76.
2. Pongponratn E, Riganti M, Pupoowong B, Aikawa M: Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study. Am J Trop Med Hyg 1991, 44:168-175.
3. Pasloske BL, Howard, RJ: Malaria, the red cell, and the endothelium. Annu Rev Med 1994, 45:283-295.
4. Macpherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA: Human cerebral malaria: a quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol 1985, 119:385-401.
5. Berendt AR, Turner GDH, Newbold Cl: Cerebral malaria: the sequestration hypothesis. Parasitol Today 1994, 10:412-414.
6. Gormley JA, Howard RJ, Taraschi TF: Trafficking of malarial proteins to the host cell cytoplasm and erythrocyte surface membrane involves multiple pathways. J Cell Biol 1992, 119:1481-1495.
7. Deitsch KW, Wellems TE: Membrane modifications in erythrocytes parasitized by Plasmodium falciparum. Mol Biochem Parasitol 1996, 76:1-10. Plasmodium falciparum-induced internal and external modifications of host erythrocytes including the erythrocyte membrane modifications are broadly reviewed.
8. Aikawa M, Iseki M, Barnwell J, Taylor D, Oo MM, Howard R: The pathology of human cerebral malaria. Am J Trop Med Hyg 1990, 43:30-37.
9. Miller LH, Good MF, Milon G: Malaria pathogenesis. Science 1994, 264:1878-1883.
10. Luse SA, Miller LH: Plasmodium falciparum malaria: ultrastructure of parasitized erythrocytes in cardiac vessels. Am J Trop Med Hyg 1971, 20:655-660.
11. Gruenberg J, Allred DR, Sherman IW: Scanning electron microscope-analysis of the protrusions (knobs) present on the surface of Plasmodium falciparum-infected erythrocytes. J Cell Biol 1983, 97:795-802.
12. Trager W, Rudzinski MA, Bradbury PC: The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infections in man. Bull WHO 1966, 35:883-885.
13. Aikawa M, Brown A, Smith CD, Tegoshi T, Howard RJ, Hasler TH, Ito Y, Perry G, Collins WE, Webster K: A primate model for human cerebral malaria: Plasmodium coatneyi-infected rhesus monkeys. Am J Trop Med Hyg 1992, 46:391-397.
14. Kawai S, Aikawa M, Kano S, Suzuki M: A primate model for severe human malaria with cerebral involvement: Plasmodium coatneyiinfected Mecaca fuscata. Am J Trop Med Hyg 1993, 48:630-636.
15. Kawai S, Kano S, Suzuki M: Rosette formation by Plasmodium coatneyi-infected erythrocytes of the Japanese macaque (Macaca fuscata). Am J Trop Med Hyg 1995, 53:295-299. Electron microscopic examination revealed that knobs present on the surface of P. coatneyi-infected erythrocytes appear to mediate interactions with adjacent uninfected erythrocytes to form rosettes. Protruding ends of these knobs attached to the membranes of uninfected erythrocytes.
16. Fujioka H, Millet P, Maeno Y, Nakazawa S, Ito Y, Howard RJ, Collins WE, Aikawa M: A nonhuman primate model for human cerebral malaria: rhesus monkeys experimentally infected with Plasmodium fragile. Exp Parasitol 1994, 78:371-376.
17. Sherman IW, Crandall I, Smith H: Membrane proteins involved in the adherence of Plasmodium felciparum-infected erythrocytes to the endothelium. Biol Cell 1992, 74:161-178.
18. Udeinya IJ, Graves PM, Carter R, Aikawa M, Miller LH: Plasmodium falciparum: effect of time in continuous culture on binding to human endothelial cells and amelanotlc melanoma cells. Exp Parasitol 1983, 56:207-214.
19. Udomsangpetch R, Aikawa M, Berzins K, Wahlgre M, Perlmann P: Cytoadherence of knobless Plasmodium falciparum-infected erythrocytes and its inhibition by a human monoclonal antibody. Nature 1989, 338:763-765.
20. Biggs BA, Culvenor JG, Ng JS, Kemp DJ, Brown, GV: Plasmodium falciparum: cytoadherence of a knobless clone. Exp Parasitol 1989, 69:189-197.
21. 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.
22. Crandall I, Guthrie N, Demers D, Sherman IW: Plasmodium falciparum: CD36 dependent cytoadherence of rosetting of infected erythrocytes is modulated by knobs. Cell Adhes Commun 1994, 2:503-510.
23. Crandall I, Sherman IW: The human anion transport protein, band 3, contains a CD36-like binding domain for Plasmodium falciparum infected erythrocytes. Parasitology 1996, 112:261-267. A murine monoclonal antibody raised against P. falciparum-infected erythrocytes seems to recognize a CD36-like region in band 3 and enhanced cytoadherence but blocked resetting of infected erythrocytes. This region in band 3 (residues 476 through 485 in the external loop 2) may be involved in rosetting.
24. Chishti AH, Andrabi KI, Derick LH, Palek J, Liu S-C: Isolation of skeleton-associated knobs from human red blood cells infected with malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 1992, 52:283-287.
25. Baruch DI, Pasloske BL, Singh HB, Bi S, Ma SC, Feldman M, Taraschi TF, Howard RJ: Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 1995, 82:77-87. The cloning of two related PfEMP1 genes from the Malayan Camp parasite strain is described. Multiple forms of the PfEMP1 gene are apparent in this parasite strain.
26. Su X-z, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, Ravetch JA, Wellems TE: The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 1995, 82:89-100. A family of var genes that encode extremely diverse P. falciparum proteins (PfEMP1 family) is identified and characterized in detail. On the basis of hybridization with exon I and exon II probes, 50 to 150 var genes were estimated on multiple parasite chromosomes.
27. Smith JD, Chitnis CE, Craig AG, Robers DJ, Hudson-Taylor DE, Peterson DS, Pinches R, Newbold Cl, Miller LH: Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 1995, 82:101-110. Expression of variant surface antigens is shown to correlate with expression of individual members of a large, multigene family named var. Each var gene contains copies of a motif that has been shown to bind diverse host ligands.
28. Sharma DY, Kilejian A: Structure of the knob protein (KP) gene of Plasmodium falciparum. Mol Biochem Parasitol 1987, 26:11-16.
29. Pologe LG, Pavlovec A, Shio H, Ravetech JV: Primary structure and subcellular localization of the knob-associated histidine-rich protein of Plasmodium falciparum. Proc Natl Acad Sci U S A 1987, 84:7139-7143.
30. Leech JH, Barnwell JW, Aikawa M, Miller LH, Howard RJ: Plasmodium falciparum malaria: association of knobs on the surface of infected erythrocytes with a histidine-rich protein and the erythrocyte skeleton. J Cell Biol 1984, 98:1256-1264.
31. Chishti AH, Palek J, Fisher D, Azim AC, Yi SJ, Liu SC: In vitro reconstruction of knob present on the surface of P. falciparum-infected human red blood cells. Blood Suppl I 1995, 86:470a.
32. Pasloske BL, Baruch DI, van Schravendijk MR, Handunnetti SM, Aikawa M, Fujioka H, Taraschi TF, Gormley JA, Howard RJ: Cloning and characterization of a Plasmodium falciparum gene encoding a novel high-molecular weight host membrane-associated protein, PfEMP3. Mol Biochem Parasitol 1993, 59:59-72.
33. Pasloske BL, Baruch DI, Ma C, Taraschi TF, Gormely JA, Howard RJ: PfEMP3 and HRP1: co-expressed genes localized to chromosome 2 of Plasmodium falciparum. Gene 1994, 144:131-136.
34. Taylor DW, Parra M, Chapman GB, Stearns ME, Rener J, Aikawa M, Uni S, Aley SB, Panton U, Howard RJ: Localization of Plasmodium falciparum histidine-rich protein 1 in the erythrocyte skeleton under knobs. Mol Biochem Parasitol 1987, 25:165-174.
35. Kilejian A, Rashid MA, Aikawa M, Aji T, Yang YF: Selective association of a fragment of the knob protein with spectrin, actin and the red cell membrane. Mol Biochem Parasitol 1991, 44:175-181.
36. Kant R, Sharma YD: Allelic forms of the knob associated histidine-rich protein gene of Plasmodium falciparum. FEBS Lett 1996, 380:147-151. The KAHRP gene cloned from two Indian isolates of P. falciparum showed major sequence differences in the C-terminus repeat domain. However, the biologically important domains, such as the spectrin-actin binding region, remained highly conserved.
37. Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV: Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes. J Exp Med 1995, 182:15-20.
38. Robert C, Pouvelle B, Meyer P, Muanza K, Fujioka H, Aikawa M, Scherf A, Gysin J: Chondroitin-4-sulfate (proteoglycan), a receptor for Plasmodium falciparum-infected erythrocyte adherence on brain microvascular endothelial cells. Res Immunol 1995, 146:383-393.
39. Howard RJ, Lyons JA, Uni S, Saul AJ, Aley SB, Klotz F, Panton LJ, Sherwood JA, Marsh K, Aikawa M, Rock EP: Transport of an Mr approx. 300,000 Plasmodium falciparum protein (PfEMP2) from the intraerythrocytic asexual parasite to the host cell membrane. J Cell Biol 1987, 104:1269-1280.
40. Coppel RL, Lustigman S, Murray L, Anders RF: MESA is a P. falciparum phosphoprotein associated with the erythrocyte membrane skeleton. Mol Biochem Parasitol 1988, 31:223-231.
41. 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.
42. Cradall I, Collins WE, Gysin J, Sherman IR: Synthetic peptides based on motifs present in human band 3 protein inhibit cytoadherence/sequestration of the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A 1993, 90:4703-4707.
43. Helmby H, Cavelier L, Pettersson U, Wahlgren M: Rosetting Plasmodium falciparum-infected erythrocytes express unique strain-specific antigens on their surface. Infect Immun 1993, 61:284-268.
44. Carlson J, Holmquist G, Taylor DW, Perlmann P, Wahlgre M: Antibodies to a histidine-rich protein (PfHRP1) disrupt spontaneously formed Plasmodium falciparum erythrocyte rosettes. Proc Natl Acad Sci U S A 1990, 87:2511-2515.
45. Magowan C, Coppel RL, Lau AOT, Moronne MM, Tchernia G, Mohandas N: Role of the Plasmodium falciparum mature-parasite-infected erythrocyte surface antigene (MESA/PfEMP-2) in malarial infection of erythrocytes. Blood 1995, 88:3196-3204. Describes the invasion, differentiation, and multiplication of MESA-positive and MESA-negative parasites in normal and protein 4.1-deficient erythrocytes as well as the cytoadherent capacity of these parasitized cells. Findings suggest that MESA binding to protein 4.1 plays a major role in intraerythrocytic parasite viability. MESA, however, was not involved in cytoadherence.
46. Land KM, Sherman IW, Gysin J, Crandall IE: Anti-adhesive antibodies and peptides as potential therapeutics for Plasmodium falciparum malaria. Parasitol Today 1995, 11:19-23. Properties of antiadhesive peptides modeled on exofacial regions of band 3 and antibodies raised against these peptides are reviewed in the context of antiadhesion therapy for P. falciparum malaria.
47. Crandall I, Sherman IW: Plasmodium falciparum (human malaria)-induced modifications in human erythrocyte band 3 protein. Parasitology 1991, 102:335-340.
48. Gardner JP, Pinches RA, Roberts DJ, Newbold CI: Variant antigens and endothelial receptor adhesion in Plasmodium falciparum. Proc Natl Acad Sci U S A 1996, 93:3503-3508.
49. 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 intracellular adhesion molecule 1. Proc Natl Acad Sci U S A 1996, 93:3497-3502. Binding of PfEMP1 expressed on the surface of adherent erythrocytes to CD36, thrombospondin, and ICAM-1 is directly demonstrated. Binding of PfEMP1 to particular host cell receptors correlated with the binding phenotype of the parasitized erythrocytes from which PfEMP1 was extracted. It was found that CD36-and thrombospondm-binding domains were distinct entities located on a single PfEMP1 molecule.
50. Leech JH, Barnwell JW, Miller LH, Howard RJ: Identification of a strainspecific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J Exp Med 1984, 159:1567-1575.
51. Aley SB, Sherwood JA, Howard RJ: Knob-positive and knob-negative Plasmodium falciparum differ in expression of a strain-specific malarial antigen on the surface of infected erythrocytes. J Exp Med 1984, 160:1585-1590.
52. Howard RJ, Barnwell JW, Rock EP, Neequaye J, Ofori AD, Maloy WL, Lyon JA, Saul A: Two approximately 300 kilodalton Plasmodium falciparum proteins at the surface membrane of infected erythrocytes. Mol Biochem Parasitol 1988, 27:207-223.
53. Howard RJ, Gilladoga AD: Molecular studies related to the pathogenesis of cerebral malaria. Blood 1989, 74:2603-2618.
54. Liu SC, Yi SJ, Bell CE, Fisher D, Oh SS, Palek J, Chishti AH: Interaction of cytoadherence-associated proteins in malaria-parasitized erythrocyte. Blood Suppl I 1996, 88:277a.
55. Winograd E, Greenan JRT, Sherman IW: Expression of senescent antigen on erythrocytes with a knobby variant of the human malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A 1987, 84:1931-1935.
56. Winograd E, Sherman IW: Characterization of a modified red cell membrane protein expressed on erythrocytes infected with the human malaria parasite Plasmodium falciparum: possible role as a cytoadherent mediating protein. J Cell Biol 1989, 108:23-30.
57. Crandall I, Sherman IW: Cytoadherence-related neoantigens on Plasmodium falciparum (human malaria)-infected human erythrocytes result from the exposure of normally cryptic regions of the band 3 protein. Parasitology 1994, 108:257-267.
58. Crandall I, Sherman IW: Antibodies to synthetic peptides based on band 3 motifs react specifically with Plasmodium falciparum (human malaria)-infected erythrocytes and block cytoadherence. Parasitology 1994, 108:389-396.
59. Guthrie N, Bird DM, Crandall I, Sherman IW: Plasmodium falciparum: the adherence of erythrocytes infected with human malaria can be mimicked using pfalhesin-coated microspheres. Cell Adhes Commun 1995, 3:407-417.
60. Guthrie N, Crandall IE, Marini S, Fasciglione GF, Sherman IW: Monoclonal antibodies that react with human band 3 residues 542-555 recognize different conformations of this protein in uninfected and Plasmodium falciparum infected erythrocytes. Mol Cell Biochem 1995, 144:117-123. Two monoclonal antibodies that recognize a common peptide sequence were shown to have different binding properties, which were attributed to different conformations of the peptide sequence. It is suggested that changes in the surface topography of human band 3 protein may modulate the adherent property of P. falciparum-infected erythrocytes.
61. Tanner MJA, Martin PG, High S: The complete amino acid sequence of the human erythrocyte membrane anion-transport protein deduced from the cDNA sequence. Biochem J 1988, 256:703-712.
62. Lux SE, John KM, Kopito RR, Lodish HF: Cloning and characterization of band 3, the human erythrocyte anion-exchange protein (AE1). Proc Natl Acad Sci U S A 1989, 86:9089-9093.
63. Kay MMB, Marchalonis JJ, Hughes J, Watanabe K, Schluter SF: Definition of a physiologic aging autoantigen by using synthetic peptides of membrane protein band 3: localization of the active antigenic sites. Proc Natl Acad Sci U S A 1990, 87:5734-5738.
64. Wang DN, Sarabia VE, Reithmeier RAF, Kuhlbrandt W: Three-dimensional map of the dimeric membrane domain of the human erythrocyte anion exchanger, band 3. EMBO J 1994, 13:3230-3235.
65. Crandall I, Guthrie N, Sherman IW: Plasmodium falciparum: sera of individuals living in a malaria-endemic region recognize peptide motifs of the human erythrocyte anion transport protein. Am J Trop Med Hyg 1995, 52:450-455. Sera from individuals living in the Gambia showed strong reactivity with decapeptides patterned on the human band 3 sequence and P. falciparum-infected erythrocytes but failed to react with native band 3. A number of cryptic exofacial regions of band 3, which become surface exposed in infected erythrocytes, are suggested.
66. Gardner JP, Pinches RA, Roberts DJ, Newbold CI: Variant antigens and endothelial receptor adhesion in Plasmodium falciparum. Proc Natl Acad Sci U S A 1996, 93:3503-3508. Sequence-specific proteases and surface-labeling techniques were used to dissect the role of defined antigenic variants in binding of P. felciparum-infected erythrocytes to particular receptors. A single infected erythrocyte bound to ICAM-1, CD36, and thrombospondin. Binding to ICAM-1 and CD36 occurred in a variant-specific manner, whereas binding to thrombospondin was a constant property of infected erythrocytes. The study suggests that PfEMP1 and a yet unidentified surface receptor (presumably band 3) are involved in cytoadherence.
67. White NJ, Olliaro PL: Strategies for the prevention of antimalarial drug resistance: rationale for combination chemotherapy for malaria. Parasitol Today 1996, 12:399-401.