Two functional reticulocyte binding-like (RBL) invasion ligands of zoonotic Plasmodium knowlesi exhibit differential adhesion to monkey and human erythrocytes

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Semenya, Amma A ^a,b   Tran, Tuan M ^a,d   Meyer, Esmeralda Vs ^a   Barnwell, John W ^b   Galinski, Mary R ^a,c  

^a EMORY UNIVERSITY   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Adhesion; Binding protein; Erythrocyte; Invasion ligand; Malaria; Merozoite; Plasmodium knowlesi; RBLs; Reticulocyte

Indexed keywords

BINDING PROTEIN; CHYMOTRYPSIN; CYSTEINE; NORMOCYTE BINDING PROTEIN; RETICULOCYTE BINDING LIKE INVASION PROTEIN; SIALIDASE; TRYPSIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; ERYTHROCYTE; HAPLORHINI; HYLOBATIDAE; MEROZOITE; NONHUMAN; PLASMODIUM KNOWLESI; PLASMODIUM KNOWLESI MALARIA; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RHESUS MONKEY;

AMINO ACID SEQUENCE; ANIMALS; ASIA, SOUTHEASTERN; BINDING SITES; CELL ADHESION; CERCOPITHECUS AETHIOPS; CLONING, MOLECULAR; COS CELLS; ERYTHROCYTES; GENE EXPRESSION; HUMANS; MACACA MULATTA; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PLASMODIUM KNOWLESI; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT;

EID: 84863498214     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-228     Document Type: Article

References (45)

1. World Health Organization, World Malaria Report World Health Organization Press, Geneva 2011
2. World Health Organization Regional Office for the Western Pacific, Informal consultation on the public health importance of Plasmodium knowlesi World Health Organization Press, Kuching, Sarawak, Malaysia 2011
3. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Singh B, Kim Sung L, Matusop A, Radhakrishnan A, Shamsul SS, Cox-Singh J, Thomas A, Conway DJ, Lancet 2004 363 1017 1024 10.1016/S0140- 6736(04)15836-4 15051281 (Pubitemid 38410774)
4. Knowlesi malaria: newly emergent and of public health importance? Cox-Singh J, Singh B, Trends Parasitol 2008 24 406 410 10.1016/j.pt.2008.06.001 18678527
5. Monkey malaria kills four humans. Galinski MR, Barnwell JW, Trends Parasitol 2009 25 200 204 10.1016/j.pt.2009.02.002 19345613
6. Malaria parasite invasion: interactions with the red cell membrane. Mitchell GH, Bannister LH, Crit Rev Oncol Hematol 1988 8 225 310 3064934
7. Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. Aikawa M, Miller LH, Johnson J, Rabbege J, J Cell Biol 1978 77 72 82 10.1083/jcb.77.1.72 96121 (Pubitemid 8321757)
8. Processing of a major parasite surface glycoprotein during the ultimate stages of differentiation in Plasmodium knowlesi. David PH, Hadley TJ, Aikawa M, Miller LH, Mol Biochem Parasitol 1984 11 267 282 6749183 (Pubitemid 14082595)
9. Multistage multiantigen heterologous prime boost vaccine for Plasmodium knowlesi malaria provides partial protection in rhesus macaques. Rogers WO, Baird JK, Kumar A, Tine JA, Weiss W, Aguiar JC, Gowda K, Gwadz R, Kumar S, Gold M, Hoffman SL, Infect Immun 2001 69 5565 5572 10.1128/IAI.69.9.5565-5572.2001 11500430 (Pubitemid 32786492)
10. Merozoite invasion of red blood cells. Galinski MR, Dluzewski AR, Barnwell JW, Molecular Approaches to Malaria ASM Press, Washington, DC, Sherman IW, 2005 113 168
11. Invasion of erythrocytes by malaria merozoites. Dvorak JA, Miller LH, Whitehouse WC, Shiroishi T, Science 1975 187 748 750 10.1126/science.803712 803712
12. A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Galinski MR, Medina CC, Ingravallo P, Barnwell JW, Cell 1992 69 1213 1226 10.1016/0092-8674(92)90642-P 1617731
13. Invasion of host cells by malaria parasites: a tale of two protein families. Iyer J, Gruner AC, Renia L, Snounou G, Preiser PR, Mol Microbiol 2007 65 231 249 10.1111/j.1365-2958.2007.05791.x 17630968 (Pubitemid 47052720)
14. Invasion of red blood cells by malaria parasites. Cowman AF, Crabb BS, Cell 2006 124 755 766 10.1016/j.cell.2006.02.006 16497586 (Pubitemid 43261450)
15. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, Crabtree J, Angiuoli SV, Merino EF, Amedeo P, Cheng Q, Coulson RM, Crabb BS, Del Portillo HA, Essien K, Feldblyum TV, Fernandez-Becerra C, Gilson PR, Gueye AH, Guo X, Kanga S, Kooij TW, Korsinczky M, Meyer EV, Nene V, Paulsen I, White O, Ralph SA, Ren Q, Sargeant TJ, Salzberg SL, Stoeckert CJ, Sullivan SA, Yamamoto MM, Hoffman SL, Wortman JR, Gardner MJ, Galinski MR, Barnwell JW, Fraser-Liggett CM, Nature 2008 455 757 763 10.1038/nature07327 18843361
16. Plasmodium vivax: Merozoites, invasion of reticulocytes and considerations for malaria vaccine development. Galinski MR, Barnwell JW, Parasitol Today 1996 12 20 29 10.1016/0169-4758(96)80641-7 15275304 (Pubitemid 26029528)
17. Erythrocyte and reticulocyte binding-like proteins of Plasmodium falciparum. Tham WH, Healer J, Cowman AF, Trends Parasitol 2011 1 23 30 10.1016/j.pt.2011.10.002
18. Rapid evolution of an erythrocyte invasion gene family: the Plasmodium reichenowi Reticulocyte Binding Like (RBL) genes. Rayner JC, Huber CS, Galinski MR, Barnwell JW, Mol Biochem Parasitol 2004 133 287 296 10.1016/j.molbiopara. 2003.10.017 14698440 (Pubitemid 38032876)
19. The reticulocyte binding proteins of Plasmodium cynomolgi: a model system for studies of P. vivax. Okenu DM, Meyer EV, Puckett TC, Rosas-Acosta G, Barnwell JW, Galinski MR, Mol Biochem Parasitol 2005 143 116 120 10.1016/j.molbiopara.2005.04.010 15990180 (Pubitemid 41039037)
20. The reticulocyte binding-like proteins of P. knowlesi locate to the micronemes of merozoites and define two new members of this invasion ligand family. Meyer EV, Semenya AA, Okenu DM, Dluzewski AR, Bannister LH, Barnwell JW, Galinski MR, Mol Biochem Parasitol 2009 165 111 121 10.1016/j.molbiopara.2009. 01.012 19428658
21. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Carlton JM, Angiuoli SV, Suh BB, Kooij TW, Pertea M, Silva JC, Ermolaeva MD, Allen JE, Selengut JD, Koo HL, Peterson JD, Pop M, Kosack DS, Shumway MF, Bidwell SL, Shallom SJ, van Aken SE, Riedmuller SB, Feldblyum TV, Cho JK, Quackenbush J, Sedegah M, Shoaibi A, Cummings LM, Florens L, Yates JR, Raine JD, Sinden RE, Harris MA, Cunningham DA, Preiser PR, Bergman LW, Vaidya AB, van Lin LH, Janse CJ, Waters AP, Smith HO, White OR, Salzberg SL, Venter JC, Fraser CM, Hoffman SL, Gardner MJ, Carucci DJ, Nature 2002 419 512 519 10.1038/nature01099 12368865
22. Antibodies targeting the PfRH1 binding domain inhibit invasion of Plasmodium falciparum merozoites. Gao X, Yeo KP, Aw SS, Kuss C, Iyer JK, Genesan S, Rajamanonmani R, Lescar J, Bozdech Z, Preiser PR, PLoS Pathog 2008 4 1000104 10.1371/journal.ppat.1000104 18617995
23. Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion. Gaur D, Singh S, Jiang L, Diouf A, Miller LH, Proc Natl Acad Sci U S A 2007 104 17789 17794 10.1073/pnas.0708772104 17971435 (Pubitemid 350210913)
24. Plasmodium falciparum merozoite invasion is inhibited by antibodies that target the PfRh2a and b binding domains. Triglia T, Chen L, Lopaticki S, Dekiwadia C, Riglar DT, Hodder AN, Ralph SA, Baum J, Cowman AF, PLoS Pathog 2011 7 1002075 10.1371/journal.ppat.1002075 21698217
25. PfRH5: a novel reticulocyte-binding family homolog of Plasmodium falciparum that binds to the erythrocyte, and an investigation of its receptor. Rodriguez M, Lustigman S, Montero E, Oksov Y, Lobo CA, PLoS One 2008 3 3300 10.1371/journal.pone.0003300 18827878
26. Plasmodium falciparum reticulocyte binding-like homologue protein 2 (PfRH2) is a key adhesive molecule involved in erythrocyte invasion. Sahar T, Reddy KS, Bharadwaj M, Pandey AK, Singh S, Chitnis CE, Gaur D, PLoS One 2011 6 17102 10.1371/journal.pone.0017102 21386888
27. Reticulocyte binding protein homologues are key adhesins during erythrocyte invasion by Plasmodium falciparum. Triglia T, Tham WH, Hodder A, Cowman AF, Cell Microbiol 2009 11 1671 1687 10.1111/j.1462-5822.2009.01358.x 19614665
28. Reticulocyte and erythrocyte binding-like proteins function cooperatively in invasion of human erythrocytes by malaria parasites. Lopaticki S, Maier AG, Thompson J, Wilson DW, Tham WH, Triglia T, Gout A, Speed TP, Beeson JG, Healer J, Cowman AF, Infect Immun 2011 79 1107 1117 10.1128/IAI.01021-10 21149582
29. Protein synthesis in vitro by cryopreserved Plasmodium falciparum. Diggs C, Joseph K, Flemmings B, Snodgrass R, Hines F, AmJTrop Med Hyg 1975 24 760 763
30. The cryopreservation of blood cells for clinical use. Meryman HT, Prog Hematol 1979 11 193 227 118482
31. Altered expression of Plasmodium knowlesi variant antigen on the erythrocyte membrane in splenectomized rhesus monkeys. Barnwell JW, Howard RJ, Miller LH, J Immunol 1982 128 224 226 6172478 (Pubitemid 12207445)
32. Rosas-Acosta G, Identification of erythrocyte binding regions within the reticulocyte binding proteins of Plasmodium vivax New York University, 1998
33. Structural characterization of the erythrocyte binding domain of the reticulocyte binding protein homologue family of Plasmodium yoelii. Gruber A, Gunalan K, Ramalingam JK, Manimekalai MS, Gruber G, Preiser PR, Infect Immun 2011 79 2880 2888 10.1128/IAI.01326-10 21482683
34. Reticulocyte-binding protein homologue 5-an essential adhesin involved in invasion of human erythrocytes by Plasmodium falciparum. Baum J, Chen L, Healer J, Lopaticki S, Boyle M, Triglia T, Ehlgen F, Ralph SA, Beeson JG, Cowman AF, Int J Parasitol 2009 39 371 380 10.1016/j.ijpara.2008.10.006 19000690
35. Mapping a common interaction site used by Plasmodium falciparum Duffy binding-like domains to bind diverse host receptors. Howell DP, Levin EA, Springer AL, Kraemer SM, Phippard DJ, Schief WR, Smith JD, Mol Microbiol 2008 67 78 87 18047571 (Pubitemid 350231136)
36. Conserved residues in the Plasmodium vivax Duffy-binding protein ligand domain are critical for erythrocyte receptor recognition. VanBuskirk KM, Sevova E, Adams JH, Proc Natl Acad Sci U S A 2004 101 15754 15759 10.1073/pnas. 0405421101 15498870 (Pubitemid 39473560)
37. Mapping binding residues in the Plasmodium vivax domain that binds Duffy antigen during red cell invasion. Hans D, Pattnaik P, Bhattacharyya A, Shakri AR, Yazdani SS, Sharma M, Choe H, Farzan M, Chitnis CE, Mol Microbiol 2005 55 1423 1434 10.1111/j.1365-2958.2005.04484.x 15720551 (Pubitemid 40342070)
38. 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. Rayner JC, Galinski MR, Ingravallo P, Barnwell JW, Proc Natl Acad Sci U S A 2000 97 9648 9653 10.1073/pnas.160469097 10920203 (Pubitemid 30650830)
39. A Plasmodium falciparum homologue of Plasmodium vivax reticulocyte binding protein (PvRBP1) defines a trypsin-resistant erythrocyte invasion pathway. Rayner JC, Vargas-Serrato E, Huber CS, Galinski MR, Barnwell JW, J Exp Med 2001 194 1571 1581 10.1084/jem.194.11.1571 11733572 (Pubitemid 33126808)
40. Plasmodium falciparum reticulocyte binding-like homologue protein 2 (PfRH2) is a key adhesive molecule involved in erythrocyte invasion. Sahar T, Reddy KS, Bharadwaj M, Pandey AK, Singh S, Chitnis CE, Gaur D, PLoS One 2011 6 17102 10.1371/journal.pone.0017102 21386888
41. Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Cox-Singh J, Davis TM, Lee KS, Shamsul SS, Matusop A, Ratnam S, Rahman HA, Conway DJ, Singh B, Clin Infect Dis 2008 46 165 171 10.1086/524888 18171245 (Pubitemid 351269152)
42. Infection of the squirrel monkey Saimiri sciureus, with Plasmodium knowlesi. Collins WE, Contacos PG, Chin W, Trans R Soc Trop Med Hyg 1978 72 662 663 10.1016/0035-9203(78)90030-5 104412 (Pubitemid 9065876)
43. Additional observations on the sporozoite transmission of Plasmodium knowlesi to monkeys. Collins WE, Sullivan JS, Nace D, Williams T, Williams A, Galland GG, Barnwell JW, J Parasitol 2004 90 866 867 10.1645/GE-3348RN 15357085 (Pubitemid 39128749)
44. Plasmodium knowlesi in the marmoset (Callithrix jacchus). Langhorne J, Cohen S, Parasitology 1979 78 67 76 10.1017/S0031182000048599 33359 (Pubitemid 9105870)
45. Plasmodium knowlesi malaria in children. Barber BE, William T, Jikal M, Jilip J, Dhararaj P, Menon J, Yeo TW, Anstey NM, Emerg Infect Dis 2011 17 814 820 10.3201/eid1705.101489 21529389