Adhesive proteins of the malaria parasite

Current Opinion in Microbiology

Volumn 1, Issue 4, 1998, Pages 472-481

  Coppel, Ross L ^a   Brown, Graham V ^b   Nussenzweig, Victor ^c  

^a MONASH UNIVERSITY   (Australia)

^b ROYAL MELBOURNE HOSPITAL   (Australia)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; CELL ADHESION; ERYTHROCYTE; GENETICS; LIVER; MALARIA; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PATHOGENICITY; PLASMODIUM; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; CELL ADHESION; CELL ADHESION MOLECULES; ERYTHROCYTES; LIVER; MALARIA; MOLECULAR SEQUENCE DATA; PLASMODIUM; PROTOZOAN PROTEINS;

EID: 0032130220     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(98)80068-4     Document Type: Article

References (84)

1. Sinnis P: The malaria sporozoite journey into the liver. Infect Agents Dis 1996, 5:182-189.
2. Greenwood BM: What can be expected from malaria vaccines? In Malaria Vaccine Development: A Multi-immune Response Approach. Edited by Hoffman SL. Washington DC: American Society for Microbiology; 1996:277-301.
3. Nussenzweig RS, Zavala F: A malaria vaccine based on a sporozoite antigen. N Eng J Med 1997, 336:128-130.
4. Stoute JA, Slaoui M, Heppner DG, Momin P, Kester KE, Desmons P, Wellde BT, Garcon N, Krzych U, Marchand M et al.: A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. N Engl J Med 1997, 336:86-91. The first successful human trial of a pre-erythrocytic malaria vaccine. Incorporation of a powerful adjuvant enhanced antibody levels against the circumsporozoite protein and protection.
5. Sim BKL, Chitnis CE, Wasnioska K, Hadley TJ, Miller LH: Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 1994, 264:1941-1944.
6. Sinnis P, Sim BKL: Cell invasion by vertebrate stages of Plasmodium. Trends Microbiol 1997, 5:52-58.
7. Galinski MR, Barnwell JW: Plasmodium vivax - merozoites, invasion of reticulocytes and considerations for malaria vaccine development Parasitol Today 1996, 12:20-29.
8. Kappe S, Noe A, Fraser T, Blair P, Adams J: A family of chimeric erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci USA 1998, 95:1230-1235. A novel family of proteins involved in adhesion to red blood cells during invasion. Their role in invasion still needs to be determined.
9. Nussenzweig V, Nussenzweig RS: Rationale for the development of an engineered sporozoite malaria vaccine. Adv Immunol 1989, 45:283-334.
10. Hoffman SL, Franke ED, Holingdale MR, Druilhe P: Attacking the infected hepatocyte. In Malaria Vaccine Development; A Multiimmune Response Approach. Edited by Hoffman SL. Washington DC: American Society for Microbiology; 1996:35-75.
11. Van Dijk MR, Janse CJ, Waters AP: Expression of a Plasmodium gene introduced into subtelomeric regions of Plasmodium berghei chromosomes. Science 1996, 271:662-665.
12. Wu YM, Kirkman LA, Wellems TE: Transformation of Plasmodium falciparum malaria parasites by homologous integration of plasmids that confer resistance to pyrimethamine. Proc Natl Acad Sci USA 1996, 93:1130-1134.
13. Crabb BS, Cowman AF: Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum. Proc Natl Acad Sci USA 1996, 93:7289-7294.
14. Menard R, Sultan AA, Cortes C, Altszuler R, Vandijk MR, Janse CJ, Waters AP, Nussenzweig RS, Nussenzweig V: Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature 1997, 385:336-340. This paper demonstrates the lack of development of sporozoites inside oocysts in mosquito midguts when the circumsporozoite protein is missing. Mechanism unknown.
15. Sidjanski SP, Vanderberg JP, Sinnis P: Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum. Mol Biochem Parasitol 1997, 90:33-41. Evidence suggesting that sporozoite invasion of Anopheles salivary glands is receptor mediated and that one of the ligands is contained within a conserved region of the circumsporozoite protein.
16. Cerami C, Frevert U, Sinnis P, Takacs B, Nussenzweig V: Rapid clearance of malaria circumsporozoite protein (CS) by hepatocytes. J Exp Med 1994, 179:695-701.
17. Stewart MJ, Nawrot RJ, Schulman S, Vanderberg JP: Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infect Immun 1986, 51:859-864.
18. McCutchan TF, Kissinger JC, Touray MG, Rogers MG, Li J, Sullivan M, Braga EM, Krettli AU, Miller LH: Comparison of circumsporozoite proteins from avian and mammalian malarias: biological and phylogenetic implications. Proc Natl Acad Sci USA 1996, 93:11889-11894.
19. Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V: Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 1993, 177:1287-1298.
20. Frevert U, Sinnis P, Esko JD, Nussenzweig V: Cell surface glycosaminoglycans are not obligatory for Plasmodium berghei sporozoite invasion in vitro. Mol Biochem Parasitol 1996, 76:257-266.
21. Lyon M, Deaken JA, Gallagher JT: Liver heparan sulfate structure. J Biol Chem 1994, 269:11208-11215.
22. Briones MRS, Tsuji M, Nussenzweig V: The large difference in infectivity for mice of Plasmodium berghei and Plasmodium yoelii sporozoites cannot be correlated with their ability to enter into hepatocytes. Mol Biochem Parasitol 1996, 77:7-17.
23. Sinnis P, Willnow TE, Briones MRS, Herz J, Nussenzweig V: Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes. J Exp Med 1996, 184:945-954.
24. Mahley RW, Ji Z, Brecht WJ, Miranda RD, He D: Role of heparan sulfate proteoglycans and the LDL receptor-related protein in remnant lipoprotein metabolism. Annals New York Acad Sci 1994, 737:39-52.
25. Shakibaei M, Frevert U: Dual interaction of the malaria circumsporozoite protein with the low density lipoprotein receptor-related protein (LRP) and heparan sulfate proteoglycans. J Exp Med 1996, 184:1699-1711.
26. Ying P, Shakibaei M, Patankar MS, Clavijo P, Beavis RC, Clark GF, Freverl U: The malaria circumsporozoite protein - interaction of the conserved regions I and II-plus with heparin-like oligosaccharides in heparan sulfate. Exp Parasitol 1997, 85:168-182.
27. Van Pelt J, Kleuskens J, Hollingdale MR, Verhave JP, Ponnudurai T, Meuwissen J, Yap SH: Identification of plasma membrane proteins involved in the hepatocyte invasion of Plasmodium falciparum sporozoites. Mol Biochem Parasitol 1991, 44:225-232.
28. Dobrowolski J, Sibley L: Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 1996, 84:933-939.
29. Sultan A, Thathy V, Frevert U, Robson K, Crisanti A, Nussenzweig V, Nussenzweig R, Menard R: TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 1997, 90:511-522. Use of targeted gene disruption provides an important insight into the requirement for TRAP to allow sporozoites to move and infect the salivary glands of mosquitoes and the liver cells of the mammalian host.
30. Robson KJ, Hall JR, Jennings MW, Harris TJ, Marsh K, Newbold CI, Tate VE, Weatherall DJ: A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 1988, 335:79-82.
31. Rogers WO, Rogers MD, Hedstrom RC, Hoffman SL: Characterization of the gene encoding sporozoite surface protein 2, a protective Plasmodium yoelii sporozoite antigen. Mol Biochem Parasitol 1992, 53:45-51.
32. Muller HM, Reckman I, Hollingdale MR, H B, Robson KJ, Crisanti H: Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. EMBO J 1993, 12:2881-2889.
33. Colombatti A, Bonaldo P, Doliana R: Type A molecules: Interacting domains found in several non-fibrillar collagens and in other extracellular matrix proteins. Matrix 1993, 13:297-306.
34. Lee JO, Rieu P, Arnaout MA, Liddington R: Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18). Cell 1995, 80:631-638.
35. Dobrowolski JM, Niesman IR, Sibley LD: Actin in the parasite Toxoplasma gondii is encoded by a single copy gene, act1, and exists primarily in a globular form. Cell Motil Cytoskeleton 1997, 37:253-262.
36. Dobrowolski JM, Carruthers VB, Sibley LD: Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol Microbiol 1997, 26:163-173.
37. Dubremetz JF: Host cell invasion by Toxoplasma gondii. Trends Microbiol 1998, 6:27-30.
38. Entzeroth R, Kerckhoff H, Konig A: Microneme secretion in Coccidia: confocal laser scanning and electron microscope study of Sarcocystis muris in cell culture. Eur J Cell Biol 1992, 59:405-413.
39. Fidock DA, Bottius E, Brahimi K, Moelans IIMD, Aikawa M, Konings RNH, Certa U, Olafsson P, Kaidoh T, Asavanich A et al.: Cloning and characterization of a novel Plasmodium falciparum sporozoite surface antigen, STARP. Mol Biochem Parasitol 1994, 64:219-232.
40. Fidock DA, Pasquetto V, Gras H, Badell E, Eling W, Ballou WR, Belghiti J, Tartar A, Druilhe P: Plasmodium falciparum sporozoite invasion is inhibited by naturally acquired or experimentally induced polyclonal antibodies to the STARP antigen. Eur J Immunol 1997, 27:2502-2513.
41. Trottein F, Triglia T, Cowman AF: Molecular cloning of a gene from Plasmodium falciparum that codes for a protein sharing motifs found in adhesive molecules from mammals and plasmodia. Mol Biochem Parasitol 1995, 74:129-141.
42. Leech JH, Barnwell JW, Miller LH, Howard RJ: Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J Exp Med 1984, 159:1567-1575.
43. Chaiyaroj SC, Coppel RL, Novakovic S, Brown GV: Multiple ligands for cytoadherence can be present simultaneously on the surface of Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci USA 1994, 91:10805-10808.
44. Marsh K, Howard RJ: Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants. Science 1986, 231:150-153.
45. Bull P, Lowe B, Kortor M, Molyneux C, Newbold C, Marsh K: Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med 1998, 4:358-360. Evidence for the strain-specific nature of the anti-PfEMP1 response. This paper proposes that infecting strains are those that express a variant not previously encountered by the patient.
46. Roberts DJ, Craig AG, Berendt AR, Pinches R, Nash G, Marsh K, Newbold CI: Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 1992, 357:689-692.
47. Baruch DI, Pasloske BL, Singh HB, Bi XH, Ma XC, 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.
48. Su XZ, 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.
49. Smith JD, Chitnis CE, Craig AG, Roberts 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 infested erythrocytes. Cell 1995, 82:101-110.
50. Adams JH, Sim BK, Dolan SA, Fang X, Kaslow DC, Miller LH: A family of erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci USA 1992, 89:7085-7089.
51. Crabb B, 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. Important study clarifying the role of accessory proteins in augmenting intercellular adhesion of PfEMP1, particularly in strengthening its resistance to detachment by shear forces in the circulation.
52. Rubio JP, Thompson JK, Cowman AF: The var genes of Plasmodium falciparum are located in the subtelomeric region of most chromosomes. EMBO J 1996, 15:4069-4077.
53. Cooke BM, Berendt AR, Craig AG, MacGregor J, Newbold CI, Nash GB: Rolling and stationary cytoadhesion of red blood cells parasitised by Plasmodium falciparum: separate roles for ICAM-1, CD36 and Thrombospondin. Brit J Haematol 1994, 87:162-170.
54. Treutiger C, Heddini A, Fernandez V, Mulle W, Wählgren M: PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nat Med 1997, 3:1405-1408. The latest receptor for cytoadherence, and the third member of the immunoglobulin superfamily, is identified. Its role and importance in clinical disease remain to be elucidated.
55. Fried M, Duffy PE: Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 1996, 272:1502-1504.
56. Baruch D, Ma X, Singh H, Bi X, Pasloske B, Howard R: Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence. Blood 1997, 90:3766-3775. The CD36-binding domain of FfEMP1 is now known, and recombinant fragments can act as competitive blockers. Can efficient blockade of CD36 adhesion lead to a better clinical outcome?
57. Turner GDH, Morrison H, Jones M, Davis TME, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B et al.: An immunohistochemical study of the pathology of fatal malaria - evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol 1994, 145:1057-1069.
58. McCormick C, Craig A, Roberts D, Newbold C, Berendt A: Intercellular adhesion molecule-1 and CD36 synergise to mediate adherece of Plasmodium falciparum-infected erythrocytes to human microvascular endothelial cells. J Clin Invest 1997, 100:2521-2529. An attempt to tease apart the complex interplay of multiple receptor-ligand interactions in cytoadherence clearly demonstrates that enhanced binding occurs when multiple receptors are involved.
59. 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. The largest clinical study performed and the best evidence for assigning a specific receptor-ligand interaction to severe clinical disease, suggested to be PfEMP1-ICAM-1.
60. Fischer K, Horrocks P, Preuss M, Wiesner J, Wunsch S, Camargo AA, Lanzer M: Expression of var genes located within polymorphic subtelomeric domains of Plasmodium falciparum chromosomes. Mol Cell Biol 1997, 17:3679-3686. The location of expressed var genes is determined and the importance of the subtelomeric location is reinforced.
61. Hernandez-Rivas R, Mattei D, Sterkers Y, Peterson DS, Wellems TE, Schert A: Expressed var genes are found in Plasmodium falciparum subtelomeric regions. Mol Cell Biol 1997, 17:604-611.
62. Wahlgren M, Fernandez V, Scholander C, Carlson J: Resetting, Parasitol Today 1994, 10:73-79.
63. Ringwald P, Peyron F, Lepers JP, Rabarison P, Rakotomalala C, Razanamparany M, Rabodonirina M, Roux J, Lebras J: Parasite virulence factors during falciparum malaria: rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infect Immun 1993, 61:5198-5204.
64. Carlson J, Helmby H, Hill AVS, Brewster D, Greenwood BM, Wählgren M: Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 1990, 336:1457-1460.
65. Rowe A, Obeiro J, Newbold CI, Marsh K: Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun 1995, 63:2323-2326.
66. Al-Yaman F, Genton B, Mokela D, Raiko A, Kati S, Rogerson S, Reeder J, Alpers M: Human cerebral malaria: lack of significant association between erythrocyte rosetting and disease severity. Trans R Soc Trop Med Hyg 1995, 89:55-58.
67. Udomsangpetch R, Thanikkul K, Pukrittayakamee S, White NJ: Rosette formation by Plasmodium vivax. Trans Roy Soc Trop Med Hyg 1995, 89:635-637.
68. Clough B, Atilola F, Pasvoi G: The role of rosetting in the multiplication of Plasmodium falciparum: rosette formation neither enhances nor targets parasite invasion into uninfected red cells. Br J Haematol 1998, 100:99-104.
69. Kaul DK, Roth EJ, Nagel RL, Howard RJ, Handunnetti SM: Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 1991, 78:812-819.
70. Bouharoun-Tayoun H, Attanath P, Sabchareon A, Chongsuphajaisiddhi T, Druilhe P: Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J Exp Med 1990, 172:1633-1641.
71. Rowe JA, Moulds JM, Newbold Cl, Miller LH: P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement receptor 1. Nature 1997, 388:292-295. An important study identifying complement receptor 1 (CR 1) as a rosetting receptor and demonstrating that red cells bearing a common CR1 polymorphism are less able to form rosettes.
72. Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, Sahlen A, Carlson J, Datta S, Wahlgren M: Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med 1998, 187:15-23. The resetting receptor likely to be found in heparin-sensitive rosettes is identified in this paper.
73. Oquendo P, Hundt E, Lawler J, Seed B: CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell 1989, 58:95-101.
74. 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, 93:3497-3502.
75. Berendt AR, McDowall A, Craig AG, Bates PA, Sternberg MJE, Marsh K, Newbold CI, Hogg N: The binding site on ICAM-1 for Plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1 binding site. Cell 1992, 68:71-81.
76. Berendt AR, Simmons DL, Tansey J, Newbold CI, Marsh K: Intracellular adhesion molecule 1 is an endothelial cell adhesion molecule for Plasmodium falciparum. Nature 1989, 341:57-59.
77. 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.
78. Ockenhouse CF, Tegoshi T, Maeno Y, Benjamin C, Ho M, Kan KE, Thway Y, Win K, Aikawa M, Lobb RR: 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.
79. 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.
80. Crandall I, Collins WE, Gysin J, Sherman IW: Synthetic peptides based on motifs present in human band 3 protein inhibit cytoadherence/sequestration of the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci USA 1993, 90:4703-4707.
81. 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.
82. Handunnetti SM, van Schravendijk MR, Hasler T, Barnwell JW, Greenwalt DE, Howard RJ: Involvement of CD36 on erythrocytes as a rosetting receptor for Plasmodium falciparum-infected erythrocytes. Blood 1992, 80:2097-2104.
83. Helmby H, Cavelier L, Pettersson U, Wahlgren M: Rosetting Plasmodium falciparum-infected erythrocytes express unique strain-specific antigens on their surface. Infect Immun 1993, 61:284-288.
84. Carlson J, Wählgren M: Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med 1992, 176:1311-1317.