The role of PfEMP1 adhesion domain classification in Plasmodium falciparum pathogenesis research

Molecular and Biochemical Parasitology

Volumn 195, Issue 2, 2014, Pages 82-87

  Smith, Joseph D ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Antigenic variation; Malaria; Pathogenesis; Plasmodium falciparum; Var

Indexed keywords

ERYTHROCYTE MEMBRANE PROTEIN 1; CELL SURFACE RECEPTOR; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAL PROTEIN;

ARTICLE; BINDING AFFINITY; CELL ADHESION; CELL MEMBRANE; CYSTEINE RICH INTERDOMAIN REGION; DISEASE SEVERITY; GENE SEQUENCE; GENETIC RECOMBINATION; MALARIA FALCIPARUM; MOLECULAR PATHOLOGY; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; TROPISM; ANIMAL; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PARASITOLOGY; PATHOGENICITY; PROTEIN TERTIARY STRUCTURE;

PLASMODIUM FALCIPARUM;

ANIMALS; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; RECEPTORS, CELL SURFACE;

EID: 84906791161     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2014.07.006     Document Type: Review

References (51)

1. L.H. Miller, D.I. Baruch, K. Marsh, and O.K. Doumbo The pathogenic basis of malaria Nature 415 2002 673 679 (Pubitemid 34136400)
2. N.J. White, G.D. Turner, N.P. Day, and A.M. Dondorp Lethal malaria: Marchiafava and Bignami were right J Infect Dis 208 2013 192 198
3. S.M. Kraemer, and J.D. Smith A family affair: var genes, PfEMP1 binding, and malaria disease Curr Opin Microbiol 9 2006 374 380 (Pubitemid 44108717)
4. M.J. Gardner, N. Hall, E. Fung, O. White, M. Berriman, and R.W. Hyman et al. Genome sequence of the human malaria parasite Plasmodium falciparum Nature 419 2002 498 511
5. S.M. Kraemer, S.A. Kyes, G. Aggarwal, A.L. Springer, S.O. Nelson, and Z. Christodoulou et al. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates BMC Genomics 8 2007 45
6. T.S. Rask, D.A. Hansen, T.G. Theander, P.A. Gorm, and T. Lavstsen Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes - divide and conquer PLoS Comput Biol 6 2010 e1000933
7. A. Salanti, T. Staalsoe, T. Lavstsen, A.T. Jensen, M.P. Sowa, and D.E. Arnot et al. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria Mol Microbiol 49 2003 179 191 (Pubitemid 36792013)
8. J. Montgomery, F.A. Mphande, M. Berriman, A. Pain, S.J. Rogerson, and T.E. Taylor et al. Differential var gene expression in the organs of patients dying of falciparum malaria Mol Microbiol 65 2007 959 967 (Pubitemid 47221074)
9. B.A. Robinson, T.L. Welch, and J.D. Smith Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome Mol Microbiol 47 2003 1265 1278 (Pubitemid 36307850)
10. M. Fried, and P.E. Duffy Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta Science 272 1996 1502 1504 (Pubitemid 26200005)
11. J.D. Smith, G. Subramanian, B. Gamain, D.I. Baruch, and L.H. Miller Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family Mol Biochem Parasitol 110 2000 293 310
12. D.I. Baruch, B.L. Pasloske, H.B. Singh, X. Bi, X.C. Ma, and M. Feldman et al. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes Cell 82 1995 77 87
13. J.D. Smith, C.E. Chitnis, A.G. Craig, D.J. Roberts, D.E. Hudson-Taylor, and D.S. Peterson et al. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes Cell 82 1995 101 110
14. X.Z. Su, V.M. Heatwole, S.P. Wertheimer, F. Guinet, J.A. Herrfeldt, and D.S. Peterson et al. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes Cell 82 1995 89 100
15. C.E. Chitnis, and L.H. Miller Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion J Exp Med 180 1994 497 506 (Pubitemid 24224126)
16. B.K. Sim, C.E. Chitnis, K. Wasniowska, T.J. Hadley, and L.H. Miller Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum Science 264 1994 1941 1944 (Pubitemid 24245642)
17. J.A. Rowe, A. Claessens, R.A. Corrigan, and M. Arman Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications Expert Rev Mol Med 11 2009 e16
18. D.I. Baruch, X.C. Ma, H.B. Singh, X. Bi, B.L. Pasloske, and R.J. Howard Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence Blood 90 1997 3766 3775 (Pubitemid 27473450)
19. J.D. Smith, S. Kyes, A.G. Craig, T. Fagan, D. Hudson-Taylor, and L.H. Miller et al. Analysis of adhesive domains from the A4VAR Plasmodium falciparum erythrocyte membrane protein-1 identifies a CD36 binding domain Mol Biochem Parasitol 97 1998 133 148 (Pubitemid 28558708)
20. J.D. Smith, A.G. Craig, N. Kriek, D. Hudson-Taylor, S. Kyes, and T. Fagen et al. Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: a parasite adhesion trait implicated in cerebral malaria Proc Natl Acad Sci U S A 97 2000 1766 1771 (Pubitemid 30118517)
21. J.A. Rowe, J.M. Moulds, C.I. Newbold, and L.H. Miller P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1 Nature 388 1997 292 295 (Pubitemid 27317975)
22. T. Lavstsen, A. Salanti, A.T. Jensen, D.E. Arnot, and T.G. Theander Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions Malar J 2 2003 27
23. L. Turner, T. Lavstsen, S.S. Berger, C.W. Wang, J.E. Petersen, and M. Avril et al. Severe malaria is associated with parasite binding to endothelial protein C receptor Nature 498 2013 502 505
24. A.T. Jensen, P. Magistrado, S. Sharp, L. Joergensen, T. Lavstsen, and A. Chiucchiuini et al. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes J Exp Med 199 2004 1179 1190 (Pubitemid 38620255)
25. H.M. Kyriacou, G.N. Stone, R.J. Challis, A. Raza, K.E. Lyke, and M.A. Thera et al. Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia Mol Biochem Parasitol 150 2006 211 218 (Pubitemid 44691950)
26. G.M. Warimwe, T.M. Keane, G. Fegan, J.N. Musyoki, C.R. Newton, and A. Pain et al. Plasmodium falciparum var gene expression is modified by host immunity Proc Natl Acad Sci U S A 106 2009 21801 21806
27. A. Ghumra, J.P. Semblat, R. Ataide, C. Kifude, Y. Adams, and A. Claessens et al. Induction of strain-transcending antibodies against Group A PfEMP1 surface antigens from virulent malaria parasites PLoS Pathog 8 2012 e1002665
28. J. Carlson, H. Helmby, A.V. Hill, D. Brewster, B.M. Greenwood, and M. Wahlgren Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies Lancet 336 1990 1457 1460
29. F. Prugnolle, P. Durand, B. Ollomo, L. Duval, F. Ariey, and C. Arnathau et al. A fresh look at the origin of Plasmodium falciparum, the most malignant malaria agent PLoS Pathog 7 2011 e1001283
30. S.M. Kraemer, and J.D. Smith Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family Mol Microbiol 50 2003 1527 1538 (Pubitemid 38010450)
31. B.C. Urban, D.J. Ferguson, A. Pain, N. Willcox, M. Plebanski, and J.M. Austyn et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells Nature 400 1999 73 77 (Pubitemid 29315113)
32. M. Avril, A.K. Tripathi, A.J. Brazier, C. Andisi, J.H. Janes, and V.L. Soma et al. A restricted subset of var genes mediates adherence of Plasmodium falciparum-infected erythrocytes to brain endothelial cells Proc Natl Acad Sci U S A 109 2012 E1782 E1790
33. J.H. Janes, C.P. Wang, E. Levin-Edens, I. Vigan-Womas, M. Guillotte, and M. Melcher et al. Investigating the host binding signature on the Plasmodium falciparum PfEMP1 protein family PLoS Pathog 7 2011 e1002032
34. B.M. Cooke, A.R. Berendt, A.G. Craig, J. MacGregor, C.I. Newbold, and G.B. Nash Rolling and stationary cytoadhesion of red blood cells parasitized by Plasmodium falciparum: separate roles for ICAM-1, CD36 and thrombospondin Br J Haematol 87 1994 162 170 (Pubitemid 24207016)
35. L.B. Ochola, B.R. Siddondo, H. Ocholla, S. Nkya, E.N. Kimani, and T.N. Williams et al. Specific Receptor Usage in Plasmodium falciparum Cytoadherence Is Associated with Disease Outcome PLoS ONE 6 2011 e14741
36. G.D. Turner, H. Morrison, M. Jones, T.M. Davis, S. Looareesuwan, and I.D. Buley 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 145 1994 1057 1069 (Pubitemid 24345654)
37. A. Bengtsson, L. Joergensen, T.S. Rask, R.W. Olsen, M.A. Andersen, and L. Turner et al. A novel domain cassette identifies Plasmodium falciparum PfEMP1 proteins binding ICAM-1 and is a target of cross-reactive, adhesion-inhibitory antibodies J Immunol 190 2013 240 249
38. D.P. Howell, E.A. Levin, A.L. Springer, S.M. Kraemer, D.J. Phippard, and W.R. Schief et al. Mapping a common interaction site used by Plasmodium falciparum Duffy binding-like domains to bind diverse host receptors Mol Microbiol 67 2008 78 87 (Pubitemid 350231136)
39. A.V. Oleinikov, E. Amos, I.T. Frye, E. Rossnagle, T.K. Mutabingwa, and M. Fried et al. High throughput functional assays of the variant antigen PfEMP1 reveal a single domain in the 3D7 Plasmodium falciparum genome that binds ICAM1 with high affinity and is targeted by naturally acquired neutralizing antibodies PLoS Pathog 5 2009 e1000386
40. C.D. Jun, C.V. Carman, S.D. Redick, M. Shimaoka, H.P. Erickson, and T.A. Springer Ultrastructure and function of dimeric, soluble intercellular adhesion molecule-1 (ICAM-1) J Biol Chem 276 2001 29019 29027
41. R.L. Silverstein, and M. Febbraio CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior Sci Signal 2 2009 re3
42. A. Claessens, Y. Adams, A. Ghumra, G. Lindergard, C.C. Buchan, and C. Andisi et al. A subset of group A-like var genes encodes the malaria parasite ligands for binding to human brain endothelial cells Proc Natl Acad Sci U S A 109 2012 E1772 E1781
43. T. Lavstsen, L. Turner, F. Saguti, P. Magistrado, T.S. Rask, and J.S. Jespersen et al. Plasmodium falciparum erythrocyte membrane protein 1 domain cassettes 8 and 13 are associated with severe malaria in children Proc Natl Acad Sci U S A 109 2012 E1791 E1800
44. M. Avril, A.J. Brazier, M. Melcher, S. Sampath, and J.D. Smith DC8 and DC13 var genes associated with severe malaria bind avidly to diverse endothelial cells PLoS Pathog 9 2013 e1003430
45. S.P. Davis, K. Lee, M.R. Gillrie, L. Roa, M. Amrein, and M. Ho CD36 recruits alpha(5)beta(1) integrin to promote cytoadherence of P. falciparum-infected erythrocytes PLoS Pathog 9 2013 e1003590
46. E.A. Bouwens, F. Stavenuiter, and L.O. Mosnier Mechanisms of anticoagulant and cytoprotective actions of the protein C pathway J Thromb Haemost 11 Suppl. 1 2013 242 253
47. C.A. Moxon, S.C. Wassmer, D.A. Milner Jr., N.V. Chisala, T.E. Taylor, and K.B. Seydel et al. Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children Blood 122 2013 842 851
48. Z. Laszik, A. Mitro, F.B. Taylor Jr., G. Ferrell, and C.T. Esmon Human protein C receptor is present primarily on endothelium of large blood vessels: implications for the control of the protein C pathway Circulation 96 1997 3633 3640 (Pubitemid 27513443)
49. A.J. Cunnington, M. Walther, and E.M. Riley Piecing together the puzzle of severe malaria Sci Transl Med 5 2013 211ps18
50. M.M. Rorick, T.S. Rask, E.B. Baskerville, K.P. Day, and M. Pascual Homology blocks of Plasmodium falciparum var genes and clinically distinct forms of severe malaria in a local population BMC Microbiol 13 2013 244
51. G.M. Warimwe, G. Fegan, J.N. Musyoki, C.R. Newton, M. Opiyo, and G. Githinji et al. Prognostic indicators of life-threatening malaria are associated with distinct parasite variant antigen profiles Sci Transl Med 4 2012 129ra45