The reticulocyte binding-like proteins of P. knowlesi locate to the micronemes of merozoites and define two new members of this invasion ligand family

Molecular and Biochemical Parasitology

Volumn 165, Issue 2, 2009, Pages 111-121

  Meyer, Esmeralda V S ^a   Semenya, Amma A ^a   Okenu, Daniel M N ^a,b   Dluzewski, Anton R ^c   Bannister, Lawrence H ^d   Barnwell, John W ^e   Galinski, Mary R ^a,f  

^a EMORY UNIVERSITY   (United States)

^b MOREHOUSE SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d ST THOMAS HOSPITAL   (United Kingdom)

^e Division of Parasitic Diseases   (United States)

^f EMORY UNIVERSITY   (United States)

Author keywords

Apicomplexa; Erythrocytes; Malaria; Merozoite invasion; Plasmodium knowlesi; Reticulocyte binding proteins

Indexed keywords

BACTERIAL PROTEIN; BINDING PROTEIN; ERYTHROCYTE BINDING PROTEIN XA; ERYTHROCYTE BINDING PROTEIN XB; LIGAND; RETICULOCYTE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BIOINFORMATICS; CELL ORGANELLE; COMPARATIVE STUDY; ERYTHROCYTE; EXPERIMENTAL STUDY; GENOME; HOST CELL; IMMUNOELECTRON MICROSCOPY; MALARIA; MEROZOITE; MICRONEME; MOLECULAR EVOLUTION; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PLASMODIUM KNOWLESI; PLASMODIUM VIVAX; PRIORITY JOURNAL; PROTEIN ANALYSIS; PSEUDOGENE; RABBIT; SOUTHERN BLOTTING;

ANIMALS; CARRIER PROTEINS; ERYTHROCYTES; GENOME, PROTOZOAN; LIGANDS; MACACA MULATTA; MEROZOITES; MOLECULAR SEQUENCE DATA; ORGANELLES; PHYLOGENY; PLASMODIUM; PLASMODIUM KNOWLESI; PROTEIN BINDING; PROTOZOAN PROTEINS; PSEUDOGENES; RETICULOCYTES; SCHIZONTS;

APICOMPLEXA; ORYCTOLAGUS CUNICULUS; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM VIVAX; SIMIAE;

EID: 62549128614     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2009.01.012     Document Type: Article

References (45)

1. Galinski M.R., Dluzewski A.R., and Barnwell J.W. A mechanistic approach to merozoite invasion of red blood cells: merozoite biogenesis, rupture, and invasion of erythrocytes. In: Sherman I.W. (Ed). Molecular approaches to malaria (2005), ASM Press 113-168
2. Galinski M.R., Medina C.C., Ingravallo P., and Barnwell J.W. A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell 69 7 (1992) 1213-1226
3. Galinski M.R., and Barnwell J.W. Plasmodium vivax: merozoites, invasion of reticulocytes and considerations for malaria vaccine development. Parasitol Today 12 1 (1996) 20-29
4. Galinski M.R., Xu M., and Barnwell J.W. Plasmodium vivax reticulocyte binding protein-2 (PvRBP-2) shares structural features with PvRBP-1 and the Plasmodium yoelii 235 kDa rhoptry protein family. Mol Biochem Parasitol 108 2 (2000) 257-262
5. Rayner J.C., Vargas-Serrato E., Huber C.S., Galinski M.R., and Barnwell J.W. A Plasmodium falciparum homologue of Plasmodium vivax reticulocyte binding protein (PvRBP1) defines a trypsin-resistant erythrocyte invasion pathway. J Exp Med 194 11 (2001) 1571-1581
6. Rayner J.C., Galinski M.R., Ingravallo P., and Barnwell J.W. 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 USA 97 17 (2000) 9648-9653
7. Triglia T., Thompson J., Caruana S.R., Delorenzi M., Speed T., and Cowman A.F. Identification of proteins from Plasmodium falciparum that are homologous to reticulocyte binding proteins in Plasmodium vivax. Infect Immun 69 2 (2001) 1084-1092
8. Taylor H.M., Triglia T., Thompson J., et al. Plasmodium falciparum homologue of the genes for Plasmodium vivax and Plasmodium yoelii adhesive proteins, which is transcribed but not translated. Infect Immun 69 6 (2001) 3635-3645
9. Kaneko O., Mu J., Tsuboi T., Su X., and Torii M. Gene structure and expression of a Plasmodium falciparum 220-kDa protein homologous to the Plasmodium vivax reticulocyte binding proteins. Mol Biochem Parasitol 121 2 (2002) 275-278
10. Okenu D.M., Meyer E.V., Puckett T.C., Rosas-Acosta G., Barnwell J.W., and Galinski M.R. The reticulocyte binding proteins of Plasmodium cynomolgi: a model system for studies of P. vivax. Mol Biochem Parasitol 143 1 (2005) 116-120
11. Rayner J.C., Huber C.S., Galinski M.R., and Barnwell J.W. Rapid evolution of an erythrocyte invasion gene family: the Plasmodium reichenowi reticulocyte binding like (RBL) genes. Mol Biochem Parasitol 133 2 (2004) 287-296
12. Ogun S.A., and Holder A.A. A high molecular mass Plasmodium yoelii rhoptry protein binds to erythrocytes. Mol Biochem Parasitol 76 1-2 (1996) 321-324
13. Keen J.K., Sinha K.A., Brown K.N., and Holder A.A. A gene coding for a high-molecular mass rhoptry protein of Plasmodium yoelii. Mol Biochem Parasitol 65 1 (1994) 171-177
14. Cowman A.F., and Crabb B.S. Invasion of red blood cells by malaria parasites. Cell 124 4 (2006) 755-766
15. Rodriguez M., Lustigman S., Montero E., Oksov Y., and Lobo C.A. PfRH5: a novel reticulocyte-binding family homolog of plasmodium falciparum that binds to the erythrocyte, and an investigation of its receptor. PLoS ONE 3 10 (2008) e3300
16. Rayner J.C., Huber C.S., and Barnwell J.W. Conservation and divergence in erythrocyte invasion ligands: Plasmodium reichenowi EBL genes. Mol Biochem Parasitol 138 2 (2004) 243-247
17. Carlton J.M., Adams J.H., Silva J.C., et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455 7214 (2008) 757-763
18. Triglia T., Duraisingh M.T., Good R.T., and Cowman A.F. Reticulocyte-binding protein homologue 1 is required for sialic acid-dependent invasion into human erythrocytes by Plasmodium falciparum. Mol Microbiol 55 1 (2005) 162-174
19. Duraisingh M.T., Triglia T., Ralph S.A., et al. Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J 22 5 (2003) 1047-1057
20. Gao X., Yeo K.P., Aw S.S., et al. Antibodies targeting the PfRH1 binding domain inhibit invasion of Plasmodium falciparum merozoites. PLoS Pathog 4 7 (2008) e1000104
21. Gaur D., Singh S., Jiang L., Diouf A., and Miller L.H. Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion. Proc Natl Acad Sci USA 104 45 (2007) 17789-17794
22. Hayton K., Gaur D., Liu A., et al. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 4 1 (2008) 40-51
23. Chin W., Contacos P.G., Coatney G.R., and Kimball H.R. A naturally acquired quotidian-type malaria in man transferable to monkeys. Science 149 (1965) 865
24. Fong Y.L., Cadigan F.C., and Coatney G.R. A presumptive case of naturally occurring Plasmodium knowlesi malaria in man in Malaysia. Trans R Soc Trop Med Hyg 65 6 (1971) 839-840
25. Singh B., Kim Sung L., Matusop A., et al. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet 363 9414 (2004) 1017-1024
26. Cox-Singh J., Davis T.M., Lee K.S., et al. Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis 46 2 (2008) 165-171
27. Cox-Singh J., and Singh B. Knowlesi malaria: newly emergent and of public health importance?. Trends Parasitol 24 9 (2008) 406-410
28. Waters A.P., Higgins D.G., and McCutchan T.F. Evolutionary relatedness of some primate models of Plasmodium. Mol Biol Evol 10 4 (1993) 914-923
29. Vargas-Serrato E., Corredor V., and Galinski M.R. Phylogenetic analysis of CSP and MSP-9 gene sequences demonstrates the close relationship of Plasmodium coatneyi to Plasmodium knowlesi. Infect Genet Evol 3 1 (2003) 67-73
30. Johnson J.G., Epstein N., Shiroishi T., and Miller L.H. Factors affecting the ability of isolated Plasmodium knowlesi merozoites to attach to and invade erythrocytes. Parasitology 80 3 (1980) 539-550
31. Pain A., Bohme U., Berry A.E., et al. The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 455 7214 (2008) 799-803
32. Barnwell J.W., Galinski M.R., DeSimone S.G., Perler F., and Ingravallo P. Plasmodium vivax, P. cynomolgi, and P. knowlesi: identification of homologue proteins associated with the surface of merozoites. Exp Parasitol 91 3 (1999) 238-249
33. Eyles D.E., Dunn F.L., Warren M., and Guinn E. Plasmodium coatneyi from the Philippines. J Parasitol 49 (1963) 1038
34. Kyes S., Pinches R., and Newbold C. A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol Biochem Parasitol 105 2 (2000) 311-315
35. Altman J.D., Henner D., Nilsson B., Anderson S., and Kuntz I.D. Intracellular expression of BPTI fusion proteins and single column cleavage/affinity purification by chymotrypsin. Protein Eng 4 5 (1991) 593-600
36. Barnwell J.W., Howard R.J., and Miller L.H. Altered expression of Plasmodium knowlesi variant antigen on the erythrocyte membrane in splenectomized rhesus monkeys. J Immunol 128 1 (1982) 224-226
37. Kumar S., Tamura K., Jakobsen I.B., and Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17 12 (2001) 1244-1245
38. Galinski M.R., and Corredor V. Variant antigen expression in malaria infections: posttranscriptional gene silencing, virulence and severe pathology. Mol Biochem Parasitol 134 1 (2004) 17-25
39. Johnson J.G., Epstein N., Shiroishi T., and Miller L.H. Identification of surface proteins on viable Plasmodium knowlesi merozoites. J Protozool 28 2 (1981) 160-164
40. Escalante A.A., Cornejo O.E., Freeland D.E., et al. A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite. Proc Natl Acad Sci USA 102 6 (2005) 1980-1985
41. Mu J., Joy D.A., Duan J., et al. Host switch leads to emergence of Plasmodium vivax malaria in humans. Mol Biol Evol 22 8 (2005) 1686-1693
42. Oka M., Aikawa M., Freeman R.R., Holder A.A., and Fine E. Ultrastructural localization of protective antigens of Plasmodium yoelii merozoites by the use of monoclonal antibodies and ultrathin cryomicrotomy. Am J Trop Med Hyg 33 3 (1984) 342-346
43. Aikawa M., Miller L.H., Johnson J., and Rabbege J. Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J Cell Biol 77 1 (1978) 72-82
44. Mitchell G.H., and Bannister L.H. Malaria parasite invasion: interactions with the red cell membrane. Crit Rev Oncol Hematol 8 4 (1988) 225-310
45. Adams J.H., Sim B.K., Dolan S.A., Fang X., Kaslow D.C., and Miller L.H. A family of erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci USA 89 15 (1992) 7085-7089