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Host Receptors in Malaria Merozoite Invasion

  • Chapter
Malaria: Drugs, Disease and Post-genomic Biology

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 295))

Abstract

The clinical manifestations of Plasmodium falciparum malaria are directly linked to the blood stage of the parasite life cycle. At the blood stage, the circulating merozoites invade erythrocytes via a specific invasion pathway often identified with its dependence or independence on sialic acid residues of the host receptor. The invasion process involves multiple receptor-ligand interactions that mediate a complex series of events in a period of approximately 1 min. Although the mechanism by which merozoites invade erythrocytes is not fully understood, recent advances have put a new perspective on the importance of developing a multivalent blood stage-malaria vaccine. In this review, we highlight the role of currently identified host invasion receptors in blood-stage malaria. cr]2005|Springer-Verlag Berlin Heidelberg

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References

  • Adams JH, Blair PL, Kaneko O, Peterson DS (2001) An expanding ebl family of Plasmodium falciparum. Trends Parasitol 17:297–299

    Article  PubMed  CAS  Google Scholar 

  • Aikawa M, Miller LH, Johnson J, Rabbege J (1978) Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J Cell Biol 77:72–82

    Article  PubMed  CAS  Google Scholar 

  • Akaki M, Nagayasu E, Nakano Y, Aikawa M (2002) Surface charge of Plasmodium falciparum merozoites as revealed by atomic force microscopy with surface potential spectroscopy. Parasitol Res 88:16–20

    Article  PubMed  CAS  Google Scholar 

  • Auffray I, Marfatia S, de Jong K, Lee G, Huang CH, Paszty C, Tanner MJ, Mohandas N, Chasis JA (2001) Glycophorin A dimerization and band 3 interaction during erythroid membrane biogenesis: in vivo studies in human glycophorin A transgenic mice. Blood 97:2872–2878

    Article  PubMed  CAS  Google Scholar 

  • Bannister L, Mitchell G (2003) The ins, outs and roundabouts of malaria. Trends Parasitol 19:209–213

    Article  PubMed  Google Scholar 

  • Bannister LH, Butcher GA, Dennis ED, Mitchell GH (1975) Structure and invasive behaviour of Plasmodium knowlesi merozoites in vitro. Parasitology 71:483–491

    Article  PubMed  CAS  Google Scholar 

  • Bannister LH, Dluzewski AR (1990) The ultrastructure of red cell invasion in malaria infections: a review. Blood Cells 16:257–292

    PubMed  CAS  Google Scholar 

  • Baum J, Pinder M, Conway DJ (2003) Erythrocyte invasion phenotypes of Plasmodium falciparum in The Gambia. Infect Immun 71:1856–1863

    Article  PubMed  CAS  Google Scholar 

  • Bergman LW, Kaiser K, Fujioka H, Coppens I, Daly TM, Fox S, Matuschewski K, Nussenzweig V, Kappe SH (2003) Myosin A tail domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. J Cell Sci 116:39–49

    Article  PubMed  CAS  Google Scholar 

  • Binks RH, Conway DJ (1999) The major allelic dimorphisms in four Plasmodium falciparum merozoite proteins are not associated with alternative pathways of erythrocyte invasion. Mol Biochem Parasitol 103:123–127.

    Article  PubMed  CAS  Google Scholar 

  • Bray RS (1958) The susceptibility of Liberians to the Madagascar strain of Plasmodium vivax. J Parasitol 44:371–373

    Article  PubMed  CAS  Google Scholar 

  • Breguet G, Ney R, Grimm W, Hope SL, Kirk RL, Blake NM, Narendra IB, Toha A (1982) Genetic survey of an isolated community in Bali, Indonesia. I. Blood groups, serum proteins and hepatitis B serology. Hum Hered 32:52–61

    Article  PubMed  CAS  Google Scholar 

  • Bruce LJ, Ring SM, Anstee DJ, Reid ME, Wilkinson S, Tanner MJ (1995) Changes in the blood group Wright antigens are associated with a mutation at amino acid 658 in human erythrocyte band 3: a site of interaction between band 3 and glycophorin A under certain conditions. Blood 85:541–547.

    PubMed  CAS  Google Scholar 

  • Buchanan DI, Sinclair M, Sanger R, Gavin J, Teesdale P (1976) An Alberta Cree Indian with a rare Duffy antibody, anti-Fy 3. Vox Sang 30:114–121

    Article  PubMed  CAS  Google Scholar 

  • Camus D, Hadley TJ (1985) A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 230:553–556

    Article  PubMed  CAS  Google Scholar 

  • Cantor EM, Lombo TB, Cepeda A, Espinosa AM, Barrero CA, Guzman F, Gunturiz ML, Urquiza M, Ocampo M, Patarroyo ME, Patarroyo MA (2001) Plasmodium vivax: functional analysis of a highly conserved PvRBP-1 protein region. Mol Biochem Parasitol 117:229–234.

    Article  PubMed  CAS  Google Scholar 

  • Carter R, Walliker D (1975) New observations on the malaria parasites of rodents of the Central African Republic — Plasmodium vinckei petteri subsp. nov. and Plasmodium chabaudi Landau, 1965. Ann Trop Med Parasitol 69:187–196

    PubMed  CAS  Google Scholar 

  • Casey JR, Reithmeier RA (1991) Analysis of the oligomeric state of Band 3, the anion transport protein of the human erythrocyte membrane, by size exclusion high performance liquid chromatography. Oligomeric stability and origin of heterogeneity. J Biol Chem 266:15726–15737

    PubMed  CAS  Google Scholar 

  • Chambers EJ, Bloomberg GB, Ring SM, Tanner MJ (1999) Structural studies on the effects of the deletion in the red cell anion exchanger (band 3, AE1) associated with South East Asian ovalocytosis. J Mol Biol 285:1289–1307

    Article  PubMed  CAS  Google Scholar 

  • Chandanayingyong D, Bejrachandra S, Metaseta P, Pongsataporn S (1979) Further study of Rh, Kell, Duffy, P, MN, Lewis and Gerbiech blood groups of the Thais. Southeast Asian J Trop Med Public Health 10:209–211

    PubMed  CAS  Google Scholar 

  • Chaudhuri A, Polyakova J, Zbrzezna V, Williams K, Gulati S, Pogo AO (1993) Cloning of glycoprotein D cDNA, which encodes the major subunit of the Duffy blood group system and the receptor for the Plasmodium vivax malaria parasite. Proc Natl Acad Sci U S A 90:10793–10797

    Article  PubMed  CAS  Google Scholar 

  • Chaudhuri A, Zbrzezna V, Johnson C, Nichols M, Rubinstein P, Marsh WL, Pogo AO (1989) Purification and characterization of an erythrocyte membrane protein complex carrying Duffy blood group antigenicity. Possible receptor for Plasmodium vivax and Plasmodium knowlesi malaria parasite. J Biol Chem 264:13770–13774

    PubMed  CAS  Google Scholar 

  • Chishti AH, Palek J, Fisher D, Maalouf GJ, Liu SC (1996) Reduced invasion and growth of Plasmodium falciparum into elliptocytic red blood cells with a combined defficiency of protein 4.1, glycophorin C, and p55. Blood 87:3462–3469

    PubMed  CAS  Google Scholar 

  • Chitnis CE (2001) Molecular insights into receptors used by malaria parasites for erythrocyte invasion. Curr Opin Hematol 8:85–91

    Article  PubMed  CAS  Google Scholar 

  • Chitnis CE, Chaudhuri A, Horuk R, Pogo AO, Miller LH (1996) The domain on the Duffy blood group antigen for binding Plasmodium vivax and P. knowlesi malarial parasites to erythrocytes. J Exp Med 184:1531–1536

    Article  PubMed  CAS  Google Scholar 

  • Chitnis CE, Miller LH (1994) Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion. J Exp Med 180:497–506

    Article  PubMed  CAS  Google Scholar 

  • Clough B, Paulitschke M, Nash GB, Bayley PM, Anstee DJ, Wilson RJ, Pasvol G, Gratzer WB (1995) Mechanism of regulation of malarial invasion by extraerythrocytic ligands. Mol Biochem Parasitol 69:19–27

    Article  PubMed  CAS  Google Scholar 

  • Colfen H, Boulter JM, Harding SE, Watts A (1998) Ultracentrifugation studies on the transmembrane domain of the human erythrocyte anion transporter band 3 in the detergent C12E8. Eur Biophys J 27:651–655

    Article  PubMed  CAS  Google Scholar 

  • Cooke BM, Mohandas N, Coppel RL (2004) Malaria and the red blood cell membrane. Semin Hematol 41:173–188

    Article  PubMed  Google Scholar 

  • Cowman AF, Baldi DL, Healer J, Mills KE, O’Donnell RA, Reed MB, Triglia T, Wickham ME, Crabb BS (2000) Functional analysis of proteins involved in Plasmodium falciparum merozoite invasion of red blood cells. FEBS Lett 476:84–88

    Article  PubMed  CAS  Google Scholar 

  • Crabb BS, Cooke BM, Reeder JC, Waller RF, Caruana SR, Davern KM, Wickham ME, Brown GV, Coppel RL, Cowman AF (1997) Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89:287–296

    Article  PubMed  CAS  Google Scholar 

  • Crandall I, Sherman IW (1994) 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 108:257–267

    PubMed  Google Scholar 

  • Darbonne WC, Rice GC, Mohler MA, Apple T, Hebert CA, Valente AJ, Baker JB (1991) Red blood cells are a sink for interleukin 8, a leukocyte chemotaxin. J Clin Invest 88:1362–1369

    Article  PubMed  CAS  Google Scholar 

  • Dolan SA, Miller LH, Wellems TE (1990) Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciparum. J Clin Invest 86:618–624

    Article  PubMed  CAS  Google Scholar 

  • Dolan SA, Proctor JL, Alling DW, Okubo Y, Wellems TE, Miller LH (1994) Glycophorin B as an EBA-175 independent Plasmodium falciparum receptor of human erythrocytes. Mol Biochem Parasitol 64:55–63

    Article  PubMed  CAS  Google Scholar 

  • Duraisingh MT, Maier AG, Triglia T, Cowman AF (2003) Erythrocyte-binding antigen 175 mediates invasion in Plasmodium falciparum utilizing sialic acid-dependent and-independent pathways. Proc Natl Acad Sci U S A 100:4796–4801

    Article  PubMed  CAS  Google Scholar 

  • Duraisingh MT, Triglia T, Ralph SA, Rayner JC, Barnwell JW, McFadden GI, Cowman AF (2003) Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J 22:1047–1057

    Article  PubMed  CAS  Google Scholar 

  • Dvorak JA, Miller LH, Whitehouse WC, Shiroishi T (1975) Invasion of erythrocytes by malaria merozoites. Science 187:748–750

    Article  PubMed  CAS  Google Scholar 

  • Dzandu JK, Deh ME, Wise GE (1985) A re-examination of the effects of chymotrypsin and trypsin on the erythrocyte membrane surface topology. Biochem Biophys Res Commun 126:50–58

    Article  PubMed  CAS  Google Scholar 

  • Eylar EH, Madoff MA, Brody OV, Oncley JL (1962) The contribution of sialic acid to the surface charge of the erythrocyte. J Biol Chem 237:1992–2000

    PubMed  CAS  Google Scholar 

  • Fortin A, Stevenson MM, Gros P (2002) Susceptibility to malaria as a complex trait: big pressure from a tiny creature. Hum Mol Genet 11:2469–2478

    Article  PubMed  CAS  Google Scholar 

  • Fujinaga J, Tang XB, Casey JR (1999) Topology of the membrane domain of human erythrocyte anion exchange protein, AE1. J Biol Chem 274:6626–6633

    Article  PubMed  CAS  Google Scholar 

  • Furthmayr H (1978) Glycophorins A, B, and C: a family of sialoglycoproteins. Isolation and preliminary characterization of trypsin derived peptides. J Supramol Struct 9:79–95

    Article  PubMed  CAS  Google Scholar 

  • Galinski MR, Medina CC, Ingravallo P, Barnwell JW (1992) A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell 69:1213–1226

    Article  PubMed  CAS  Google Scholar 

  • Gallup JL, Sachs JD (2001) The economic burden of malaria. Am J Trop Med Hyg 64:85–96

    PubMed  CAS  Google Scholar 

  • Ghosh A, Edwards MJ, Jacobs-Lorena M (2000) The journey of the malaria parasite in the mosquito: hopes for the new century. Parasitol Today 16:196–201

    Article  PubMed  CAS  Google Scholar 

  • Gilberger TW, Thompson JK, Reed MB, Good RT, Cowman AF (2003a) The cytoplasmic domain of the Plasmodium falciparum ligand EBA-175 is essential for invasion but not protein trafficking. J Cell Biol 162:317–327

    Article  PubMed  CAS  Google Scholar 

  • Gilberger TW, Thompson JK, Triglia T, Good RT, Duraisingh MT, Cowman AF (2003b) A novel erythrocyte binding antigen-175 paralogue from Plasmodium falciparum defines a new trypsin-resistant receptor on human erythrocytes. J Biol Chem 278:14480–14486

    Article  PubMed  CAS  Google Scholar 

  • Goel VK, Li X, Chen H, Liu SC, Chishti AH, Oh SS (2003) Band 3 is a host receptor binding merozoite surface protein 1 during the Plasmodium falciparum invasion of erythrocytes. Proc Natl Acad Sci U S A 100:5164–5169

    Article  PubMed  CAS  Google Scholar 

  • Gratzer WB, Dluzewski AR (1993) The red blood cell and malaria parasite invasion. Semin Hematol 30:232–247

    PubMed  CAS  Google Scholar 

  • Hadley TJ, Klotz FW, Pasvol G, Haynes JD, McGinniss MH, Okubo Y, Miller LH (1987) Falciparum malaria parasites invade erythrocytes that lack glycophorin A and B (MkMk). Strain differences indicate receptor heterogeneity and two pathways for invasion. J Clin Invest 80:1190–1193

    Article  PubMed  CAS  Google Scholar 

  • Hassoun H, Hanada T, Lutchman M, Sahr KE, Palek J, Hanspal M, Chishti AH (1998) Complete deficiency of glycophorin A in red blood cells from mice with targeted inactivation of the band 3 (AE1) gene. Blood 91:2146–2151

    PubMed  CAS  Google Scholar 

  • Haynes JD, Dalton JP, Klotz FW, McGinniss MH, Hadley TJ, Hudson DE, Miller LH (1988) Receptor-like specificity of a Plasmodium knowlesi malarial protein that binds to Duffy antigen ligands on erythrocytes. J Exp Med 167:1873–1881

    Article  PubMed  CAS  Google Scholar 

  • Holding PA, Snow RW (2001) Impact of Plasmodium falciparum malaria on performance and learning: review of the evidence. Am J Trop Med Hyg 64:68–75

    PubMed  CAS  Google Scholar 

  • Hood AT, Fabry ME, Costantini F, Nagel RL, Shear HL (1996) Protection from lethal malaria in transgenic mice expressing sickle hemoglobin. Blood 87:1600–1603

    PubMed  CAS  Google Scholar 

  • Horuk R, Chitnis CE, Darbonne WC, Colby TJ, Rybicki A, Hadley TJ, Miller LH (1993) Areceptor for the malarial parasite Plasmodium vivax: the erythrocyte chemokine receptor. Science 261:1182–1184

    Article  PubMed  CAS  Google Scholar 

  • Jakobsen PH, Heegaard PM, Koch C, Wasniowska K, Lemnge MM, Jensen JB, Sim BK (1998) Identification of an erythrocyte binding peptide from the erythrocyte binding antigen, EBA-175, which blocks parasite multiplication and induces peptide blocking antibodies. Infect Immun 66:4203–4207

    PubMed  CAS  Google Scholar 

  • Jarolim P, Palek J, Amato D, Hassan K, Sapak P, Nurse GT, Rubin HL, Zhai S, Sahr KE, Liu SC (1991) Deletion in erythrocyte band 3 gene in malaria-resistant Southeast Asian ovalocytosis. Proc Natl Acad Sci U S A 88:11022–11026

    Article  PubMed  CAS  Google Scholar 

  • Jarra W, Brown KN (1989) Invasion of mature and immature erythrocytes of CBA/Ca mice by a cloned line of Plasmodium chabaudi chabaudi. Parasitology 2:157–163

    Google Scholar 

  • Jones GL, Edmundson HM (1991) Plasmodium falciparum polypeptides interacting with human red cell membranes show high affinity binding to Band-3. Biochim Biophys Acta 1097:71–76

    PubMed  CAS  Google Scholar 

  • Kain KC, Orlandi PA, Haynes JD, Sim KL, Lanar DE (1993) Evidence for two-stage binding by the 175-kD erythrocyte binding antigen of Plasmodium falciparum. J Exp Med 178:1497–1505

    Article  PubMed  CAS  Google Scholar 

  • Kaneko O, Fidock DA, Schwartz OM, Miller LH (2000) Disruption of the C-terminal region of EBA-175 in the Dd2/Nm clone of Plasmodium falciparum does not affect erythrocyte invasion. Mol Biochem Parasitol 110:135–146

    Article  PubMed  CAS  Google Scholar 

  • Kaneko O, Mu J, Tsuboi T, Su X, Torii M (2002) Gene structure and expression of a Plasmodium falciparum 220-kDa protein homologous to the Plasmodium vivax reticulocyte binding proteins. Mol Biochem Parasitol 121:275–278

    Article  PubMed  CAS  Google Scholar 

  • Kappe SH, Buscaglia CA, Bergman LW, Coppens I, Nussenzweig V (2004) Apicomplexan gliding motility and host cell invasion: overhauling the motor model. Trends Parasitol 20:13–16

    Article  PubMed  CAS  Google Scholar 

  • Kappe SH, Kaiser K, Matuschewski K (2003) The Plasmodium sporozoite journey: a rite of passage. Trends Parasitol 19:135–143

    Article  PubMed  Google Scholar 

  • Khan SM, Jarra W, Preiser PR (2001) The 235 kDa rhoptry protein of Plasmodium (yoelii) yoelii: function at the junction. Mol Biochem Parasitol 117:1–10

    Article  PubMed  CAS  Google Scholar 

  • Klotz FW, Chulay JD, Daniel W, Miller LH (1987) Invasion of mouse erythrocytes by the human malaria parasite, Plasmodium falciparum. J Exp Med 165:1713–1718

    Article  PubMed  CAS  Google Scholar 

  • Kuma H, Abe Y, Askin D, Bruce LJ, Hamasaki T, Tanner MJ, Hamasaki N (2002) Molecular basis and functional consequences of the dominant effects of the mutant band 3 on the structure of normal band 3 in Southeast Asian ovalocytosis. Biochemistry 41:3311–3320

    Article  PubMed  CAS  Google Scholar 

  • Kushwaha A, Perween A, Mukund S, Majumdar S, Bhardwaj D, Chowdhury NR, Chauhan VS (2002) Amino terminus of Plasmodium falciparum acidic basic repeat antigen interacts with the erythrocyte membrane through band 3 protein. Mol Biochem Parasitol 122:45–54.

    Article  PubMed  CAS  Google Scholar 

  • Ladda R, Aikawa M, Sprinz H (1969) Penetration of erythrocytes by merozoites of mammalian and avian malarial parasites. J Parasitol 55:633–644

    Article  PubMed  CAS  Google Scholar 

  • Langreth SG, Jensen JB, Reese RT, Trager W (1978) Fine structure of human malaria in vitro. J Protozool 25:443–452

    PubMed  CAS  Google Scholar 

  • Li X, Chen H, Oo TH, Daly TM, Bergman LW, Liu SC, Chishti AH, Oh SS (2004) A coligand complex anchors Plasmodium falciparum merozoites to the erythrocyte invasion receptor band 3. J Biol Chem 279:5765–5771

    Article  PubMed  CAS  Google Scholar 

  • Liu SC, Palek J, Yi SJ, Nichols PE, Derick LH, Chiou SS, Amato D, Corbett JD, Cho MR, Golan DE (1995) Molecular basis of altered red blood cell membrane properties in Southeast Asian ovalocytosis: role of the mutant band 3 protein in band 3 oligomerization and retention by the membrane skeleton. Blood 86:349–358

    PubMed  CAS  Google Scholar 

  • Lobo CA, Rodriguez M, Reid M, Lustigman S (2003) Glycophorin C is the receptor for the Plasmodium falciparum erythrocyte binding ligand PfEBP-2 (baebl). Blood 101:4628–4631

    Article  PubMed  CAS  Google Scholar 

  • Luo H, Chaudhuri A, Zbrzezna V, He Y, Pogo AO (2000) Deletion of the murine Duffy gene (Dfy) reveals that the Duffy receptor is functionally redundant. Mol Cell Biol 20:3097–3101

    Article  PubMed  CAS  Google Scholar 

  • Maier AG, Duraisingh MT, Reeder JC, Patel SS, Kazura JW, Zimmerman PA, Cowman AF (2003) Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9:87–92

    Article  PubMed  CAS  Google Scholar 

  • Mallinson G, Soo KS, Schall TJ, Pisacka M, Anstee DJ (1995) Mutations in the erythrocyte chemokine receptor (Duffy) gene: the molecular basis of the Fya/Fyb antigens and identification of a deletion in the Duffy gene of an apparently healthy individual with the Fy(a-b-) phenotype. Br J Haematol 90:823–829

    Article  PubMed  CAS  Google Scholar 

  • Mason SJ, Miller LH, Shiroishi T, Dvorak JA, McGinniss MH (1977) The Duffy blood group determinants: their role in the susceptibility of human and animal erythrocytes to Plasmodium knowlesi malaria. Br J Haematol 36:327–335

    Article  PubMed  CAS  Google Scholar 

  • Mayer DC, Kaneko O, Hudson-Taylor DE, Reid ME, Miller LH (2001) Characterization of a Plasmodium falciparum erythrocyte-binding protein paralogous to EBA-175. Proc Natl Acad Sci U S A 98:5222–5227

    Article  PubMed  CAS  Google Scholar 

  • Mayer DC, Mu JB, Feng X, Su XZ, Miller LH (2002) Polymorphism in a Plasmodium falciparum erythrocyte-binding ligand changes its receptor specificity. J ExpMed 196:1523–1528

    Article  CAS  Google Scholar 

  • Mayer DC, Mu JB, Kaneko O, Duan J, Su XZ, Miller LH (2004) Polymorphism in the Plasmodium falciparum erythrocyte-binding ligand JESEBL/EBA-181 alters its receptor specificity. Proc Natl Acad Sci U S A 101:2518–2523

    Article  PubMed  CAS  Google Scholar 

  • McPherson RA, Donald DR, Sawyer WH, Tilley L (1993) Proteolytic digestion of band 3 at an external site alters the erythrocyte membrane organisation and may facilitate malarial invasion. Mol Biochem Parasitol 62:233–242

    Article  PubMed  CAS  Google Scholar 

  • Meissner M, Schluter D, Soldati D (2002) Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298:837–840

    Article  PubMed  CAS  Google Scholar 

  • Mgone CS, Koki G, Paniu MM, Kono J, Bhatia KK, Genton B, Alexander ND, Alpers MP (1996) Occurrence of the erythrocyte band 3 (AE1) gene deletion in relation to malaria endemicity in Papua New Guinea. Trans R Soc Trop Med Hyg 90:228–231

    Article  PubMed  CAS  Google Scholar 

  • Michon P, Woolley I, Wood EM, Kastens W, Zimmerman PA, Adams JH (2001) Duffynull promoter heterozygosity reduces DARC expression and abrogates adhesion of the P. vivax ligand required for blood-stage infection. FEBS Lett 495:111–114

    Article  PubMed  CAS  Google Scholar 

  • Miller LH, Aikawa M, Johnson JG, Shiroishi T (1979) Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J Exp Med 149:172–184

    Article  PubMed  CAS  Google Scholar 

  • Miller LH, Haynes JD, McAuliffe FM, Shiroishi T, Durocher JR, McGinniss MH (1977) Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi. J Exp Med 146:277–281

    Article  PubMed  CAS  Google Scholar 

  • Miller LH, Hudson D, Haynes JD (1988) Identification of Plasmodium knowlesi erythrocyte binding proteins. Mol Biochem Parasitol 31:217–222

    Article  PubMed  CAS  Google Scholar 

  • Miller LH, Hudson D, Rener J, Taylor D, Hadley TJ, Zilberstein D (1983) A monoclonal antibody to rhesus erythrocyte band 3 inhibits invasion by malaria (Plasmodium knowlesi) merozoites. J Clin Invest 72:1357–1364

    Article  PubMed  CAS  Google Scholar 

  • Miller LH, Mason SJ, Clyde DF, McGinniss MH (1976) The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295:302–304

    Article  PubMed  CAS  Google Scholar 

  • Miller LH, Mason SJ, Dvorak JA, McGinniss MH, Rothman IK (1975) Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189:561–563

    Article  PubMed  CAS  Google Scholar 

  • Mitchell GH, Hadley TJ, McGinniss MH, Klotz FW, Miller LH (1986) Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors. Blood 67:1519–1521

    PubMed  CAS  Google Scholar 

  • Mohandas N, Winardi R, Knowles D, Leung A, Parra M, George E, Conboy J, Chasis J (1992) Molecular basis for membrane rigidity of hereditary ovalocytosis. A novel mechanism involving the cytoplasmic domain of band 3. J Clin Invest 89:686–692

    Article  PubMed  CAS  Google Scholar 

  • Mons B (1990) Preferential invasion of malarial merozoites into young red blood cells. Blood Cells 16:299–312

    PubMed  CAS  Google Scholar 

  • Mota MM, Hafalla JC, Rodriguez A (2002) Migration through host cells activates Plasmodium sporozoites for infection. Nat Med 8:1318–1322

    Article  PubMed  CAS  Google Scholar 

  • Mota MM, Rodriguez A (2002) Invasion of mammalian host cells by Plasmodium sporozoites. Bioessays 24:149–156

    Article  PubMed  Google Scholar 

  • Nagel RL, Roth EF, Jr. (1989) Malaria and red cell genetic defects. Blood 74:1213–1221

    PubMed  CAS  Google Scholar 

  • Narum DL, Fuhrmann SR, Luu T, Sim BK (2002) A novel Plasmodium falciparum erythrocyte binding protein-2 (EBP2/BAEBL) involved in erythrocyte receptor binding. Mol Biochem Parasitol 119:159–168

    Article  PubMed  CAS  Google Scholar 

  • Narum DL, Haynes JD, Fuhrmann S, Moch K, Liang H, Hoffman SL, Sim BK (2000) Antibodies against the Plasmodium falciparum receptor binding domain of EBA-175 block invasion pathways that do not involve sialic acids. Infect Immun 68:1964–1966.

    Article  PubMed  CAS  Google Scholar 

  • Nigg EA, Bron C, Girardet M, Cherry RJ (1980) Band 3-glycophorin A association in erythrocyte membrane demonstrated by combining protein diffusion measurements with antibody-induced cross-linking. Biochemistry 19:1887–1893

    Article  PubMed  CAS  Google Scholar 

  • Ogun SA, Holder AA (1996) A high molecular mass Plasmodium yoelii rhoptry protein binds to erythrocytes. Mol Biochem Parasitol 76:321–324

    Article  PubMed  CAS  Google Scholar 

  • Ogun SA, Scott-Finnigan TJ, Narum DL, Holder AA (2000) Plasmodium yoelii: effects of red blood cell modification and antibodies on the binding characteristics of the 235-kDa rhoptry protein. Exp Parasitol 95:187–195

    Article  PubMed  CAS  Google Scholar 

  • Oh SS, Chishti AH, Palek J, Liu SC (1997) Erythrocyte membrane alterations in Plasmodium falciparum malaria sequestration. Curr Opin Hematol 4:148–154

    Article  PubMed  CAS  Google Scholar 

  • Oh SS, Voigt S, Fisher D, Yi SJ, LeRoy PJ, Derick LH, Liu SC, Chishti AH (2000) Plasmodium falciparum erythrocyte membrane protein 1 is anchored to the spectrin-actin junction and knob associated histidine-rich protein in the erythrocyte skeleton. Mol Biochem Parasitol 108:237–247

    Article  PubMed  CAS  Google Scholar 

  • Okoye VC, Bennett V (1985) Plasmodium falciparum malaria: band 3 as a possible receptor during invasion of human erythrocytes. Science 227:169–171

    Article  PubMed  CAS  Google Scholar 

  • Okoyeh JN, Pillai CR, Chitnis CE (1999) Plasmodium falciparum field isolates commonly use erythrocyte invasion pathways that are independent of sialic acid residues of glycophorin A. Infect Immun 67:5784–5791

    PubMed  CAS  Google Scholar 

  • Orlandi PA, Klotz FW, Haynes JD (1992) A malaria invasion receptor, the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum recognizes the terminal Neu5Ac(alpha 2-3)Gal-sequences of glycophorin A. J Cell Biol 116:901–909

    Article  PubMed  CAS  Google Scholar 

  • Pasloske BL, Howard RJ (1994) Malaria, the red cell, and the endothelium. Annu Rev Med 45:283–295

    Article  PubMed  CAS  Google Scholar 

  • Pasvol G (1984) Receptors on red cells for Plasmodium falciparum and their interaction with merozoites. Philos Trans R Soc Lond B Biol Sci 307:189–200

    Article  PubMed  CAS  Google Scholar 

  • Pasvol G, Anstee D, Tanner MJ (1984) Glycophorin C and the invasion of red cells by Plasmodium falciparum. Lancet 1:907–908

    Article  PubMed  CAS  Google Scholar 

  • Pasvol G, Chasis JA, Mohandas N, Anstee DJ, Tanner MJ, Merry AH (1989) Inhibition of malarial parasite invasion by monoclonal antibodies against glycophorin A correlates with reduction in red cell membrane deformability. Blood 74:1836–1843

    PubMed  CAS  Google Scholar 

  • Pasvol G, Wainscoat JS, Weatherall DJ (1982) Erythrocytes deficiency in glycophorin resist invasion by the malarial parasite Plasmodium falciparum. Nature 297:64–66

    Article  PubMed  CAS  Google Scholar 

  • Pasvol G, Weatherall DJ, Wilson RJ (1980) The increased susceptibility of young red cells to invasion by the malarial parasite Plasmodium falciparum. Br J Haematol 45:285–295

    Article  PubMed  CAS  Google Scholar 

  • Perkins ME (1984) Binding of glycophorins to Plasmodium falciparum merozoites. Mol Biochem Parasitol 10:67–78

    Article  PubMed  CAS  Google Scholar 

  • Peters LL, Jindel HK, Gwynn B, Korsgren C, John KM, Lux SE, Mohandas N, Cohen CM, Cho MR, Golan DE, Brugnara C (1999) Mild spherocytosis and altered red cell ion transport in protein 4. 2-null mice. J Clin Invest 103:1527–1537

    Article  PubMed  CAS  Google Scholar 

  • Poole J (2000) Red cell antigens on band 3 and glycophorin A. Blood Rev 14:31–43.

    Article  PubMed  CAS  Google Scholar 

  • Popov M, Tam LY, Li J, Reithmeier RA (1997) Mapping the ends of transmembrane segments in a polytopic membrane protein. Scanning N-glycosylation mutagenesis of extracytosolic loops in the anion exchanger, band 3. J Biol Chem 272:18325–18332

    Article  PubMed  CAS  Google Scholar 

  • Preiser P, Kaviratne M, Khan S, Bannister L, Jarra W (2000) The apical organelles of malaria merozoites: host cell selection, invasion, host immunity and immune evasion. Microbes Infect 2:1461–1477

    Article  PubMed  CAS  Google Scholar 

  • Preiser PR, Khan S, Costa FT, Jarra W, Belnoue E, Ogun S, Holder AA, Voza T, Landau I, Snounou G, Renia L (2002) Stage-specific transcription of distinct repertoires of a multigene family during Plasmodium life cycle. Science 295:342–345

    Article  PubMed  CAS  Google Scholar 

  • Ranjan A, Chitnis CE (1999) Mapping regions containing binding residues within functional domains of Plasmodium vivax and Plasmodium knowlesi erythrocyte-binding proteins. Proc Natl Acad Sci U S A 96:14067–14072

    Article  PubMed  CAS  Google Scholar 

  • Ravindranath Y, Goyette G, Jr., Johnson RM (1994) Southeast Asian ovalocytosis in an African-American family. Blood 84:2823–2824

    PubMed  CAS  Google Scholar 

  • Rayner JC, Galinski MR, Ingravallo P, Barnwell JW (2000) Two Plasmodium falciparum genes express merozoite proteins that are related to Plasmodium vivax and Plasmodium yoelii adhesive proteins involved in host cell selection and invasion. Proc Natl Acad Sci U S A 97:9648–9653

    Article  PubMed  CAS  Google Scholar 

  • Rayner JC, Vargas-Serrato E, Huber CS, Galinski MR, Barnwell JW (2001) A Plasmodium falciparum homologue of Plasmodium vivax reticulocyte binding protein (PvRBP1) defines a trypsin-resistant erythrocyte invasion pathway. J Exp Med 194:1571–1581

    Article  PubMed  CAS  Google Scholar 

  • Reed MB, Caruana SR, Batchelor AH, Thompson JK, Crabb BS, Cowman AF (2000) Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proc Natl Acad Sci U S A 97:7509–7514

    Article  PubMed  CAS  Google Scholar 

  • Reid ME, Lomas-Francis C (1997) The blood group antigen facts book. Academic Press, New York, NY.

    Google Scholar 

  • Rodriguez LE, Urquiza M, Ocampo M, Suarez J, Curtidor H, Guzman F, Vargas LE, Trivinos M, Rosas M, Patarroyo ME (2000) Plasmodium falciparum EBA-175 kDa protein peptides which bind to human red blood cells. Parasitology 120:225–235.

    Article  PubMed  CAS  Google Scholar 

  • Rogers ME, Williams DT, Niththyananthan R, Rampling MW, Heslop KE, Johnston DG (1992) Decrease in erythrocyte glycophorin sialic acid content is associated with increased erythrocyte aggregation in human diabetes. Clin Sci (Lond) 82:309–313

    CAS  Google Scholar 

  • Roggwiller E, Betoulle ME, Blisnick T, Braun Breton C (1996) A role for erythrocyte band 3 degradation by the parasite gp76 serine protease in the formation of the parasitophorous vacuole during invasion of erythrocytes by Plasmodium falciparum. Mol Biochem Parasitol 82:13–24

    Article  PubMed  CAS  Google Scholar 

  • Sachs J, Malaney P (2002) The economic and social burden of malaria. Nature 415:680–685

    Article  PubMed  CAS  Google Scholar 

  • Sanger R, Race RR, Jack J (1955) The Duffy blood groups of New York negroes: the phenotype Fy (a-b-). Br J Haematol 1:370–374

    Article  PubMed  CAS  Google Scholar 

  • Shear HL (1993) Transgenic and mutant animal models to study mechanisms of protection of red cell genetic defects against malaria. Experientia 49:37–42

    Article  PubMed  CAS  Google Scholar 

  • Sherman IW, Eda S, Winograd E (2003) Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes Infect 5:897–909

    Article  PubMed  CAS  Google Scholar 

  • Shimizu Y, Ao H, Soemantri A, Tiwawech D, Settheetham-Ishida W, Kayame OW, Kimura M, Nishioka T, Ishida T (2000) Sero-and molecular typing of Duffy blood group in Southeast Asians and Oceanians. Hum Biol 72:511–518

    PubMed  CAS  Google Scholar 

  • Sibley LD (2004) Intracellular parasite invasion strategies. Science 304:248–253

    Article  PubMed  CAS  Google Scholar 

  • Sim BK, Carter JM, Deal CD, Holland C, Haynes JD, Gross M (1994) Plasmodium falciparum: further characterization of a functionally active region of the merozoite invasion ligand EBA-175. Exp Parasitol 78:259–268

    Article  PubMed  CAS  Google Scholar 

  • Sim BK, Chitnis CE, Wasniowska K, Hadley TJ, Miller LH (1994) Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 264:1941–1944

    Article  PubMed  CAS  Google Scholar 

  • Sim BK, Orlandi PA, Haynes JD, Klotz FW, Carter JM, Camus D, Zegans ME, Chulay JD (1990) Primary structure of the 175 K Plasmodium falciparum erythrocyte binding antigen and identification of a peptide which elicits antibodies that inhibit malaria merozoite invasion. J Cell Biol 111:1877–1884

    Article  PubMed  CAS  Google Scholar 

  • Sinden RE, Billingsley PF (2001) Plasmodium invasion of mosquito cells: hawk or dove? Trends Parasitol 17:209–212

    Article  PubMed  CAS  Google Scholar 

  • Singh B, Kim Sung L, Matusop A, Radhakrishnan A, Shamsul SS, Cox-Singh J, Thomas A, Conway DJ (2004) A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet 363:1017–1024

    Article  PubMed  Google Scholar 

  • Soubes SC, Reid ME, Kaneko O, Miller LH (1999) Search for the sialic acid-independent receptor on red blood cells for invasion by Plasmodium falciparum. Vox Sang 76:107–114

    Article  PubMed  CAS  Google Scholar 

  • Soubes SC, Wellems TE, Miller LH (1997) Plasmodium falciparum: A high proportion of parasites from a population of the Dd2 strain are able to invade erythrocytes by an alternative pathway. Exp Parasitol 86:79–83

    Article  PubMed  CAS  Google Scholar 

  • Southgate CD, Chishti AH, Mitchell B, Yi SJ, Palek J (1996) Targeted disruption of the murine erythroid band 3 gene results in spherocytosis and severe haemolytic anaemia despite a normal membrane skeleton. Nat Genet 14:227–230

    Article  PubMed  CAS  Google Scholar 

  • Swardson-Olver CJ, Dawson TC, Burnett RC, Peiper SC, Maeda N, Avery AC (2002) Plasmodium yoelii uses the murine Duffy antigen receptor for chemokines as a receptor for normocyte invasion and an alternative receptor for reticulocyte invasion. Blood 99:2677–2684

    Article  PubMed  CAS  Google Scholar 

  • Takeshima Y, Sofro AS, Suryantoro P, Narita N, Matsuo M (1994) Twenty seven nucleotide deletion within exon 11 of the erythrocyte band 3 gene in Indonesian ovalocytosis. Jpn J Hum Genet 39:181–185

    Article  PubMed  CAS  Google Scholar 

  • Tanner MJ, Bruce L, Martin PG, Rearden DM, Jones GL (1991) Melanesian hereditary ovalocytes have a deletion in red cell band 3. Blood 78:2785–2786

    PubMed  CAS  Google Scholar 

  • Taylor HM, Triglia T, Thompson J, Sajid M, Fowler R, Wickham ME, Cowman AF, Holder AA (2001) Plasmodium falciparum homologue of the genes for Plasmodium vivax and Plasmodium yoelii adhesive proteins, which is transcribed but not translated. Infect Immun 69:3635–3645

    Article  PubMed  CAS  Google Scholar 

  • Tournamille C, Colin Y, Cartron JP, Le Van Kim C (1995) Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Genet 10:224–228

    Article  PubMed  CAS  Google Scholar 

  • Triglia T, Thompson J, Caruana SR, Delorenzi M, Speed T, Cowman AF (2001) Identification of proteins from Plasmodium falciparum that are homologous to reticulocyte binding proteins in Plasmodium vivax. Infect Immun 69:1084–1092

    Article  PubMed  CAS  Google Scholar 

  • Vince JW, Sarabia VE, Reithmeier RA (1997) Self-association of Band 3, the human erythrocyte anion exchanger, in detergent solution. Biochim Biophys Acta 1326:295–306

    Article  PubMed  CAS  Google Scholar 

  • Voigt S, Hanspal M, LeRoy PJ, Zhao PS, Oh SS, Chishti AH, Liu SC (2000) The cytoadherence ligand Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) binds to the P. falciparum knob-associated histidine-rich protein (KAHRP) by electrostatic interactions. Mol Biochem Parasitol 110:423–428

    Article  PubMed  CAS  Google Scholar 

  • Waller KL, Cooke BM, Nunomura W, Mohandas N, Coppel RL (1999) Mapping the binding domains involved in the interaction between the Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and the cytoadherence ligand P. falciparum erythrocyte membrane protein 1 (PfEMP1). Journal of Biological Chemistry 274:23808–23813

    Article  PubMed  CAS  Google Scholar 

  • Wertheimer SP, Barnwell JW (1989) Plasmodium vivax interaction with the human Duffy blood group glycoprotein: identification of a parasite receptor-like protein. Exp Parasitol 69:340–350

    Article  PubMed  CAS  Google Scholar 

  • WHO (2001) The world health report 2001, Annex Table 3: Burden of disease in disability-adjusted life years (DALYs) by cause, sex and mortality stratum in WHO Regions, estimates for 2000. WHO, Geneva Switzerland

    Google Scholar 

  • WHO (2004) Fact Sheet No. 94: Malaria. WHO, Geneva Switzerland

    Google Scholar 

  • Wilson RJ (1990) Biochemistry of red cell invasion. Blood Cells 16:237–252; discussion 253-236

    PubMed  CAS  Google Scholar 

  • Young MD, Eyles DE, Burgess RW, Jeffery GM (1955) Experimental testing of the immunity of Negroes to Plasmodium vivax. J Parasitol 41:315–318

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Steck TL (1975) Isolation and characterization of band 3, the predominant polypeptide of the human erythrocyte membrane. J Biol Chem 250:9170–9175

    PubMed  CAS  Google Scholar 

  • Zhang D, Kiyatkin A, Bolin JT, Low PS (2000) Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood 96:2925–2933

    PubMed  CAS  Google Scholar 

  • Zimmerman PA, Patel SS, Maier AG, Bockarie MJ, Kazura JW (2003) Erythrocyte polymorphisms and malaria parasite invasion in Papua New Guinea. Trends Parasitol 19:250–252

    Article  PubMed  Google Scholar 

  • Zimmerman PA, Woolley I, Masinde GL, Miller SM, McNamara DT, Hazlett F, Mgone CS, Alpers MP, Genton B, Boatin BA, Kazura JW (1999) Emergence of FY*A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proc Natl Acad Sci U S A 96:13973–13977

    Article  PubMed  CAS  Google Scholar 

  • Zuckerman A (1958) Blood loss and replacement in plasmodial infections. II. Plasmodium vinckei in untreated weanling and mature rats. J Infect Dis 103:205–224

    PubMed  CAS  Google Scholar 

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Oh, S.S., Chishti, A.H. (2005). Host Receptors in Malaria Merozoite Invasion. In: Compans, R.W., et al. Malaria: Drugs, Disease and Post-genomic Biology. Current Topics in Microbiology and Immunology, vol 295. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-29088-5_8

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