Structural and immunological correlations between the variable blocks of the var2csa domain DBL6ε from two plasmodium falciparum parasite lines

Journal of Molecular Biology

Volumn 425, Issue 10, 2013, Pages 1697-1711

  Gangnard, Stéphane ^a,b   Badaut, Cyril ^a,b,c   Ramboarina, Stéphanie ^a,b   Baron, Bruno ^a   Ramdani, Tarik ^a,b   Gamain, Benoît ^d,e,f,g   Deloron, Philippe ^c,e,g   Lewit Bentley, Anita ^a,b   Bentley, Graham A ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^d INSERM   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f INSTITUT NATIONAL DE LA TRANSFUSION SANGUINE   (France)

^g Laboratoire d'Excellence GR Ex   (France)

Author keywords

antigenicity; crystal structure; epitopes; PfEMP1; pregnancy associated malaria

Indexed keywords

DUFFY BIND LIKE 6 EPSI PROTEIN; DUFFY BINDING PROTEIN; ERYTHROCYTE MEMBRANE PROTEIN 1; GLYCOSAMINOGLYCAN; IMMUNOGLOBULIN G; UNCLASSIFIED DRUG; VAR2CSA PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CROSS REACTION; HUMAN; NONHUMAN; PLASMODIUM FALCIPARUM; PREGNANT WOMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE;

PLASMODIUM FALCIPARUM;

EID: 84877583949     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.02.014     Document Type: Article

References (45)

1. L.H. Miller, D.I. Baruch, K. Marsh, and O.K. Doumbo The pathogenic basis of malaria Nature 415 2002 673 679
2. A.G. Maier, B.M. Cooke, A.F. Cowman, and L. Tilley Malaria parasite proteins that remodel the host erythrocyte Nat. Rev.; Microbiol. 7 2009 341 354
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
4. 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
5. A. Scherf, J.J. Lopez-Rubio, and L. Riviere Antigenic variation in Plasmodium falciparum Annu. Rev. Microbiol. 62 2008 445 470
6. M. Fried, and P.E. Duffy Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta Science 272 1996 1502 1504
7. B.J. Brabin, C. Romagosa, S. Abdelgalil, C. Menéndez, F.H. Verhoeff, and R. McGready The sick placenta - the role of malaria Placenta 25 2004 359 378
8. A. Salanti, T. Staalsoe, T. Lavstsen, A.T. Jensen, M.P. Sowa, and D.E. Arnot 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
9. N.G. Tuikue Ndam, A. Salanti, G. Bertin, M. Dahlbäck, N. Fievet, and L. Turner High level of var2csa transcription by Plasmodium falciparum isolated from the placenta J. Infect. Dis. 192 2005 331 335
10. N.K. Viebig, B. Gamain, C. Scheidig, C. Lépolard, J. Przyborski, and M. Lanzer A single member of the Plasmodium falciparum var multigene family determines cytoadhesion to the placental receptor chondroitin sulphate A EMBO Rep. 6 2005 775 781
11. N.K. Viebig, E. Levin, S. Dechavanne, S.J. Rogerson, J. Gysin, and J.D. Smith Disruption of var2csa gene impairs placental malaria associated adhesion phenotype PLoS One 2 2007 e910
12. M. Fried, F. Nosten, A. Brockman, B.J. Brabin, and P.E. Duffy Maternal antibodies block malaria Nature 395 1998 851 852
13. C.H. Ricke, T. Staalsoe, K. Koram, B.D. Akanmori, E.M. Riley, and T.G. Theander Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulfate A J. Immunol. 165 2000 3309 3316
14. P.E. Duffy, and M. Fried Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns Infect. Immun. 71 2003 6620 6623
15. J. Guitard, G. Cottrell, N.M. Magnouha, A. Salanti, T. Li, and S. Sow Differential evolution of anti-VAR2CSA-IgG3 in primigravidae and multigravidae pregnant women infected by Plasmodium falciparum Malar. J. 7 2008 10
16. N.G. Tuikue Ndam, A. Salanti, J.Y. Le-Hesran, G. Cottrell, N. Fievet, and L. Turner Dynamics of anti-VAR2CSA immunoglobulin G response in a cohort of Senegalese pregnant women J. Infect. Dis. 193 2006 713 720
17. T.S. Rask, D.A. Hansen, T.G. Theander, A. Gorm Pedersen, and T. Lavstsen Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes - divide and conquer PLoS Comput. Biol. 6 2010 e1000933
18. B. Gamain, A.R. Trimnell, C. Scheidig, A. Scherf, L.H. Miller, and J.D. Smith Identification of multiple chondroitin sulfate A (CSA)-binding domains in the var2CSA gene transcribed in CSA-binding parasites J. Infect. Dis. 191 2005 1010 1013
19. M. Avril, B. Gamain, C. Lépolard, N. Viaud, A. Scherf, and J. Gysin Characterization of anti-var2CSA-PfEMP1 cytoadhesion inhibitory mouse monoclonal antibodies Microbes Infect. 8 2006 2863 2871
20. N. Bir, S.S. Yazdani, M. Avril, C. Layez, J. Gysin, and C.E. Chitnis Immunogenicity of Duffy binding-like domains that bind chondroitin sulfate A and protection against pregnancy-associated malaria Infect. Immun. 74 2006 5955 5963
21. A. Srivastava, S. Gangnard, A. Round, S. Dechavanne, A. Juillerat, and B. Raynal Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA Proc. Natl Acad. Sci. USA 107 2010 4884 4889
22. P. Khunrae, M. Dahlbäck, M.A. Nielsen, G. Andersen, S.B. Ditlev, and M. Resende Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies J. Mol. Biol. 397 2010 826 834
23. J. Bockhorst, F. Lu, J.H. Janes, J. Keebler, B. Gamain, and P. Awadalla Structural polymorphism and diversifying selection on the pregnancy malaria vaccine candidate VAR2CSA Mol. Biochem. Parasitol. 155 2007 103 112
24. C. Badaut, G. Bertin, T. Rustico, N. Fievet, A. Massougbodji, and A. Gaye Towards the rational design of a candidate vaccine against pregnancy associated malaria: conserved sequences of the DBL6ε domain of VAR2CSA PLoS One 5 2010 e11276
25. P.C. Bull, C.O. Buckee, S. Kyes, M.M. Kortok, V. Thathy, and B. Guyah Plasmodium falciparum antigenic variation. Mapping mosaic var gene sequences onto a network of shared, highly polymorphic sequence blocks Mol. Microbiol. 68 2008 1519 1534
26. M.F. Duffy, A. Caragounis, R. Noviyanti, H.M. Kyriacou, E.K. Choong, and K. Boysen Transcribed var genes associated with placental malaria in Malawian women Infect. Immun. 74 2006 4875 4883
27. A.R. Trimnell, S.M. Kraemer, S. Mukherjee, D.J. Phippard, J.H. Janes, and E. Flamoe Global genetic diversity and evolution of var genes associated with placental and severe childhood malaria Mol. Biochem. Parasitol. 148 2006 169 180
28. 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
29. J.G. Beeson, E.J. Mann, T.J. Byrne, A. Caragounis, S.R. Elliott, and G.V. Brown Antigenic differences and conservation among placental Plasmodium falciparum-infected erythrocytes and acquisition of variant-specific and cross-reactive antibodies J. Infect. Dis. 193 2006 721 730
30. A.F. Sander, A. Salanti, T. Lavstsen, M.A. Nielsen, P. Magistrado, and J. Lusingu Multiple var2csa-type PfEMP1 genes located at different chromosomal loci occur in many Plasmodium falciparum isolates PLoS One 4 2009 e6667
31. V.V. Pinto, S.B. Ditlev, K.E. Jensen, M. Resende, M. Dahlbäck, and G. Andersen Differential induction of functional IgG using the Plasmodium falciparum placental malaria vaccine candidate VAR2CSA PLoS One 6 2011 e17942
32. P. Khunrae, J.M. Philip, D.R. Bull, and M.K. Higgins Structural comparison of two CSPG-binding DBL domains from the VAR2CSA protein important in malaria during pregnancy J. Mol. Biol. 393 2009 202 213
33. S.C. Lovell, I.W. Davis, W.B. Arendall 3rd.; P.I. de Bakker, J.M. Word, and M.G. Prisant Structure validation by Cα geometry: φ,ψ and Cβ deviation Proteins 50 2003 437 450
34. 1-varO, the rosetting domain of PfEMP1 from the VarO line of Plasmodium falciparum Mol. Biochem. Parasitol. 170 2010 84 92
35. S.R. Elliott, M.F. Duffy, T.J. Byrne, J.G. Beeson, E.J. Mann, and D.W. Wilson Cross-reactive surface epitopes on chondroitin sulfate A-adherent Plasmodium falciparum-infected erythrocytes are associated with transcription of var2csa Infect. Immun. 73 2005 2848 2856
36. A.V. Oleinikov, E. Rossnagle, S. Francis, T.K. Mutabingwa, M. Fried, and P.E. Duffy Effects of sex, parity, and sequence variation on seroreactivity to candidate pregnancy malaria vaccine antigens J. Infect. Dis. 196 2007 155 164
37. W. Kabsch XDS Acta Crystallogr.; Sect. D: Biol. Crystallogr. 66 2010 125 132
38. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr.; Sect. D: Biol. Crystallogr. 50 1994 760 763
39. C. Vonrhein, E. Blanc, P. Roversi, and G. Bricogne Automated structure solution with autoSHARP Methods Mol. Biol. 364 2007 215 230
40. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr.; Sect. D: Biol. Crystallogr. 60 2004 2126 2132
41. J. Wang Inclusion of weak high-resolution X-ray data for improvement of a group II intron structure Acta Crystallogr.; Sect. D: Biol. Crystallogr. 66 2010 988 1000
42. L. Potterton, S. McNicholas, E. Krissinel, J. Gruber, K. Cowtan, and P. Emsley Developments in the CCP4 molecular-graphics project Acta Crystallogr.; Sect. D: Biol. Crystallogr. 60 2004 2288 2294
43. W.C. Johnson Analyzing protein circular dichroism spectra for accurate secondary structures Proteins 35 1999 307 312
44. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
45. P. Deloron, J. Milet, and C. Badaut Plasmodium falciparum variability and immune evasion proceed from antigenicity of consensus sequences from DBL6ε; generalization to all DBL from VAR2CSA PLoS One 8 2013 e54882