Structure-Guided Identification of a Family of Dual Receptor-Binding PfEMP1 that Is Associated with Cerebral Malaria

Cell Host and Microbe

Volumn 21, Issue 3, 2017, Pages 403-414

  Lennartz, Frank ^a   Adams, Yvonne ^b,c   Bengtsson, Anja ^b,c   Olsen, Rebecca W ^b,c   Turner, Louise ^b,c   Ndam, Nicaise T ^d,e   Ecklu Mensah, Gertrude ^b,c,f   Moussiliou, Azizath ^e   Ofori, Michael F ^f   Gamain, Benoit ^g   Lusingu, John P ^h   Petersen, Jens E V ^b,c   Wang, Christian W ^b,c   Nunes Silva, Sofia ^g   Jespersen, Jakob S ^b,c   Lau, Clinton K Y ^a   Theander, Thor G ^b,c   Lavstsen, Thomas ^b,c   Hviid, Lars ^b,c   Higgins, Matthew K ^a   Jensen, Anja T R ^b,c   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Rigshospitalet   (Denmark)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^e UNIVERSITY OF ABOMEY CALAVI   (Benin)

^f University of Ghana   (Ghana)

^g hôpital Robert Debré et Institut national de la transfusion sanguine   (France)

^h NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (Tanzania)

Author keywords

cerebral malaria; EPCR; ICAM 1; PfEMP1; Plasmodium falciparum

Indexed keywords

ENDOTHELIAL PROTEIN C RECEPTOR; ERYTHROCYTE MEMBRANE PROTEIN 1; INTERCELLULAR ADHESION MOLECULE 1; CELL SURFACE RECEPTOR; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; LEUKOCYTE ANTIGEN; PROCR PROTEIN, HUMAN; PROTEIN BINDING; PROTOZOAL PROTEIN; VIRULENCE FACTOR;

ARTICLE; CEREBRAL MALARIA; GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; SEQUENCE ANALYSIS; BIOLOGY; CELL ADHESION; CHEMISTRY; DNA SEQUENCE; GENETICS; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; SMALL ANGLE SCATTERING; SURFACE PLASMON RESONANCE; X RAY CRYSTALLOGRAPHY;

ANTIGENS, CD; CELL ADHESION; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; GENOME, PROTOZOAN; INTERCELLULAR ADHESION MOLECULE-1; MALARIA, CEREBRAL; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAN PROTEINS; RECEPTORS, CELL SURFACE; SCATTERING, SMALL ANGLE; SEQUENCE ANALYSIS, DNA; SURFACE PLASMON RESONANCE; VIRULENCE FACTORS;

EID: 85014755683     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.02.009     Document Type: Article

References (48)

1. Avril, M., Tripathi, A.K., Brazier, A.J., Andisi, C., Janes, J.H., Soma, V.L., Sullivan, D.J. Jr., Bull, P.C., Stins, M.F., Smith, J.D., A restricted subset of var genes mediates adherence of Plasmodium falciparum-infected erythrocytes to brain endothelial cells. Proc. Natl. Acad. Sci. USA 109 (2012), E1782–E1790.
2. Avril, M., Bernabeu, M., Benjamin, M., Brazier, A.J., Smith, J.D., Interaction between endothelial protein C receptor and intercellular adhesion molecule 1 to mediate binding of Plasmodium falciparum-infected erythrocytes to endothelial cells. MBio, 7, 2016 e00615-16.
3. Band, G., Rockett, K.A., Spencer, C.C., Kwiatkowski, D.P., Malaria Genomic Epidemiology Network. A novel locus of resistance to severe malaria in a region of ancient balancing selection. Nature 526 (2015), 253–257.
4. Bengtsson, A., Joergensen, L., Rask, T.S., Olsen, R.W., Andersen, M.A., Turner, L., Theander, T.G., Hviid, L., Higgins, M.K., Craig, A., 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.
5. Bernabeu, M., Danziger, S.A., Avril, M., Vaz, M., Babar, P.H., Brazier, A.J., Herricks, T., Maki, J.N., Pereira, L., Mascarenhas, A., et al. Severe adult malaria is associated with specific PfEMP1 adhesion types and high parasite biomass. Proc. Natl. Acad. Sci. USA 113 (2016), E3270–E3279.
6. Birbeck, G.L., Molyneux, M.E., Kaplan, P.W., Seydel, K.B., Chimalizeni, Y.F., Kawaza, K., Taylor, T.E., Blantyre Malaria Project Epilepsy Study (BMPES) of neurological outcomes in retinopathy-positive paediatric cerebral malaria survivors: a prospective cohort study. Lancet Neurol. 9 (2010), 1173–1181.
7. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Sharff, A., Smart, O.S., Vonrhein, C., and Womack, T.O. (2016). BUSTER version 2.10.2 (Global Phasing).
8. Claessens, A., Adams, Y., Ghumra, A., Lindergard, G., Buchan, C.C., Andisi, C., Bull, P.C., Mok, S., Gupta, A.P., Wang, C.W., 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. USA 109 (2012), E1772–E1781.
9. Cunnington, A.J., Riley, E.M., Walther, M., Stuck in a rut? Reconsidering the role of parasite sequestration in severe malaria syndromes. Trends Parasitol. 29 (2013), 585–592.
10. Dondorp, A.M., Fanello, C.I., Hendriksen, I.C., Gomes, E., Seni, A., Chhaganlal, K.D., Bojang, K., Olaosebikan, R., Anunobi, N., Maitland, K., et al., AQUAMAT group. Artesunate versus quinine in the treatment of severe falciparum malaria in African children (AQUAMAT): an open-label, randomised trial. Lancet 376 (2010), 1647–1657.
11. Doumbo, O.K., Thera, M.A., Koné, A.K., Raza, A., Tempest, L.J., Lyke, K.E., Plowe, C.V., Rowe, J.A., High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am. J. Trop. Med. Hyg. 81 (2009), 987–993.
12. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
13. Evans, P.R., Murshudov, G.N., How good are my data and what is the resolution?. Acta Crystallogr. D Biol. Crystallogr. 69 (2013), 1204–1214.
14. Goel, S., Palmkvist, M., Moll, K., Joannin, N., Lara, P., Akhouri, R.R., Moradi, N., Öjemalm, K., Westman, M., Angeletti, D., et al. RIFINs are adhesins implicated in severe Plasmodium falciparum malaria. Nat. Med. 21 (2015), 314–317.
15. Howell, D.P., Levin, E.A., Springer, A.L., Kraemer, S.M., Phippard, D.J., Schief, W.R., Smith, J.D., Mapping a common interaction site used by Plasmodium falciparum Duffy binding-like domains to bind diverse host receptors. Mol. Microbiol. 67 (2008), 78–87.
16. Hsieh, F.L., Turner, L., Bolla, J.R., Robinson, C.V., Lavstsen, T., Higgins, M.K., The structural basis for CD36 binding by the malaria parasite. Nat. Commun., 7, 2016, 12837.
17. Hviid, L., Jensen, A.T., PfEMP1—a parasite protein family of key importance in Plasmodium falciparum malaria immunity and pathogenesis. Adv. Parasitol. 88 (2015), 51–84.
18. Idro, R., Jenkins, N.E., Newton, C.R., Pathogenesis, clinical features, and neurological outcome of cerebral malaria. Lancet Neurol. 4 (2005), 827–840.
19. Janes, J.H., Wang, C.P., Levin-Edens, E., Vigan-Womas, I., Guillotte, M., Melcher, M., Mercereau-Puijalon, O., Smith, J.D., Investigating the host binding signature on the Plasmodium falciparum PfEMP1 protein family. PLoS Pathog., 7, 2011, e1002032.
20. Jensen, A.T., Magistrado, P., Sharp, S., Joergensen, L., Lavstsen, T., Chiucchiuini, A., Salanti, A., Vestergaard, L.S., Lusingu, J.P., Hermsen, R., 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.
21. Jespersen, J.S., Wang, C.W., Mkumbaye, S.I., Minja, D.T., Petersen, B., Turner, L., Petersen, J.E., Lusingu, J.P., Theander, T.G., Lavstsen, T., Plasmodium falciparum var genes expressed in children with severe malaria encode CIDRα1 domains. EMBO Mol. Med. 8 (2016), 839–850.
22. Kim, J.H., Singvall, J., Schwarz-Linek, U., Johnson, B.J., Potts, J.R., Höök, M., BBK32, a fibronectin binding MSCRAMM from Borrelia burgdorferi, contains a disordered region that undergoes a conformational change on ligand binding. J. Biol. Chem. 279 (2004), 41706–41714.
23. Kwong, P.D., Wyatt, R., Robinson, J., Sweet, R.W., Sodroski, J., Hendrickson, W.A., Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393 (1998), 648–659.
24. Lau, C.K., Turner, L., Jespersen, J.S., Lowe, E.D., Petersen, B., Wang, C.W., Petersen, J.E., Lusingu, J., Theander, T.G., Lavstsen, T., Higgins, M.K., Structural conservation despite huge sequence diversity allows EPCR binding by the PfEMP1 family implicated in severe childhood malaria. Cell Host Microbe 17 (2015), 118–129.
25. Lavstsen, T., Turner, L., Saguti, F., Magistrado, P., Rask, T.S., Jespersen, J.S., Wang, C.W., Berger, S.S., Baraka, V., Marquard, A.M., et al. Plasmodium falciparum erythrocyte membrane protein 1 domain cassettes 8 and 13 are associated with severe malaria in children. Proc. Natl. Acad. Sci. USA 109 (2012), E1791–E1800.
26. Lusingu, J.P., Vestergaard, L.S., Mmbando, B.P., Drakeley, C.J., Jones, C., Akida, J., Savaeli, Z.X., Kitua, A.Y., Lemnge, M.M., Theander, T.G., Malaria morbidity and immunity among residents of villages with different Plasmodium falciparum transmission intensity in North-Eastern Tanzania. Malar. J., 3, 2004, 26.
27. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., Read, R.J., Phaser crystallographic software. J. Appl. Cryst. 40 (2007), 658–674.
28. Menschikowski, M., Hagelgans, A., Eisenhofer, G., Siegert, G., Regulation of endothelial protein C receptor shedding by cytokines is mediated through differential activation of MAP kinase signaling pathways. Exp. Cell Res. 315 (2009), 2673–2682.
29. Miotto, O., Amato, R., Ashley, E.A., MacInnis, B., Almagro-Garcia, J., Amaratunga, C., Lim, P., Mead, D., Oyola, S.O., Dhorda, M., et al. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat. Genet. 47 (2015), 226–234.
30. Mkumbaye, S.I., Wang, C.W., Lyimo, E., Jespersen, J.S., Manjurano, A., Mosha, J., Kavishe, R.A., Mwakalinga, S.B., Minja, D.T., Lusingu, J.P., et al. The severity of Plasmodium falciparum infection is associated with transcript levels of var genes encoding EPCR-binding PfEMP1. Infect. Immun., 2017, 10.1128/IAI.00841-16 Published online January 30, 2017.
31. Moxon, C.A., Heyderman, R.S., Wassmer, S.C., Dysregulation of coagulation in cerebral malaria. Mol. Biochem. Parasitol. 166 (2009), 99–108.
32. Moxon, C.A., Wassmer, S.C., Milner, D.A. Jr., Chisala, N.V., Taylor, T.E., Seydel, K.B., Molyneux, M.E., Faragher, B., Esmon, C.T., Downey, C., 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.
33. Murshudov, G.N., Skubák, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F., Vagin, A.A., REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 355–367.
34. Newbold, C., Warn, P., Black, G., Berendt, A., Craig, A., Snow, B., Msobo, M., Peshu, N., Marsh, K., Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am. J. Trop. Med. Hyg. 57 (1997), 389–398.
35. Niang, M., Bei, A.K., Madnani, K.G., Pelly, S., Dankwa, S., Kanjee, U., Gunalan, K., Amaladoss, A., Yeo, K.P., Bob, N.S., et al. STEVOR is a Plasmodium falciparum erythrocyte binding protein that mediates merozoite invasion and rosetting. Cell Host Microbe 16 (2014), 81–93.
36. Ochola, L.B., Siddondo, B.R., Ocholla, H., Nkya, S., Kimani, E.N., Williams, T.N., Makale, J.O., Liljander, A., Urban, B.C., Bull, P.C., et al. Specific receptor usage in Plasmodium falciparum cytoadherence is associated with disease outcome. PLoS ONE, 6, 2011, e14741.
37. Oleinikov, A.V., Amos, E., Frye, I.T., Rossnagle, E., Mutabingwa, T.K., Fried, M., Duffy, P.E., 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.
38. Petersen, J.E., Bouwens, E.A., Tamayo, I., Turner, L., Wang, C.W., Stins, M., Theander, T.G., Hermida, J., Mosnier, L.O., Lavstsen, T., Protein C system defects inflicted by the malaria parasite protein PfEMP1 can be overcome by a soluble EPCR variant. Thromb. Haemost. 114 (2015), 1038–1048.
39. Rask, T.S., Hansen, D.A., Theander, T.G., Gorm Pedersen, A., Lavstsen, T., Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes—divide and conquer. PLoS Comput. Biol., 6, 2010, e1000933.
40. Robinson, B.A., Welch, T.L., Smith, J.D., 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.
41. Rogerson, S.J., Tembenu, R., Dobaño, C., Plitt, S., Taylor, T.E., Molyneux, M.E., Cytoadherence characteristics of Plasmodium falciparum-infected erythrocytes from Malawian children with severe and uncomplicated malaria. Am. J. Trop. Med. Hyg. 61 (1999), 467–472.
42. Rowe, J.A., Moulds, J.M., Newbold, C.I., Miller, L.H., P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388 (1997), 292–295.
43. Seydel, K.B., Kampondeni, S.D., Valim, C., Potchen, M.J., Milner, D.A., Muwalo, F.W., Birbeck, G.L., Bradley, W.G., Fox, L.L., Glover, S.J., et al. Brain swelling and death in children with cerebral malaria. N. Engl. J. Med. 372 (2015), 1126–1137.
44. Silamut, K., Phu, N.H., Whitty, C., Turner, G.D., Louwrier, K., Mai, N.T., Simpson, J.A., Hien, T.T., White, N.J., A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am. J. Pathol. 155 (1999), 395–410.
45. Storm, J., Craig, A.G., Pathogenesis of cerebral malaria—inflammation and cytoadherence. Front. Cell. Infect. Microbiol., 4, 2014, 100.
46. Theisen, M., Soe, S., Jessing, S.G., Okkels, L.M., Danielsen, S., Oeuvray, C., Druilhe, P., Jepsen, S., Identification of a major B-cell epitope of the Plasmodium falciparum glutamate-rich protein (GLURP), targeted by human antibodies mediating parasite killing. Vaccine 19 (2000), 204–212.
47. Turner, G.D., Morrison, H., Jones, M., Davis, T.M., Looareesuwan, S., Buley, I.D., Gatter, K.C., Newbold, C.I., Pukritayakamee, S., Nagachinta, B., 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.
48. Turner, L., Lavstsen, T., Berger, S.S., Wang, C.W., Petersen, J.E., Avril, M., Brazier, A.J., Freeth, J., Jespersen, J.S., Nielsen, M.A., et al. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498 (2013), 502–505.