Structural basis for the ABO blood-group dependence of plasmodium falciparum rosetting

PLoS Pathogens

Volumn 8, Issue 7, 2012, Pages 33-

  Vigan Womas, Inès ^a,b   Guillotte, Micheline ^a,b   Juillerat, Alexandre ^a,b   Hessel, Audrey ^a,b   Raynal, Bertrand ^a,b   England, Patrick ^a,b   Cohen, Jacques H ^c   Bertrand, Olivier ^d   Peyrard, Thierry ^d   Bentley, Graham A ^a,b   Lewit Bentley, Anita ^a,b   Mercereau Puijalon, Odile ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^d INSTITUT NATIONAL DE LA TRANSFUSION SANGUINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; HEPARIN; PROTEIN; PROTEIN CIDR1 GAMMA; PROTEIN DBL1 ALPHA1; RECOMBINANT PROTEIN; TRISACCHARIDE; UNCLASSIFIED DRUG; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ARTICLE; BINDING SITE; BLOOD GROUP A; BLOOD GROUP ABO SYSTEM; BLOOD GROUP B; BLOOD GROUP O; CELLULAR PARAMETERS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA POLYMORPHISM; ERYTHROCYTE FUNCTION AND CHARACTERISTICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PROTEIN BINDING; ROSETTING; SITE DIRECTED MUTAGENESIS; SURFACE PLASMON RESONANCE; AMINO ACID SEQUENCE; BLOOD; CHEMISTRY; ERYTHROCYTE; GENETICS; HUMAN; IMMUNE ADHERENCE; IMMUNOLOGY; MALARIA FALCIPARUM; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; ROSETTE FORMATION; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

PLASMODIUM FALCIPARUM;

ABO BLOOD-GROUP SYSTEM; AMINO ACID SEQUENCE; ANTIBODIES, PROTOZOAN; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; ERYTHROCYTES; HUMANS; IMMUNE ADHERENCE REACTION; MALARIA, FALCIPARUM; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PLASMODIUM FALCIPARUM; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; ROSETTE FORMATION;

EID: 84864612921     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002781     Document Type: Article

References (72)

1. Boren T, Falk P, Roth KA, Larson G, Normark S, (1993) Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262: 1892-1895.
2. Hutson AM, Atmar RL, Graham DY, Estes MK, (2002) Norwalk virus infection and disease is associated with ABO histo-blood group type. J Infect Dis 185: 1335-1337.
3. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, et al. (2003) Human susceptibility and resistance to Norwalk virus infection. Nat Med 9: 548-553.
4. Marionneau S, Ruvoen N, Le Moullac-Vaidye B, Clement M, Cailleau-Thomas A, et al. (2002) Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122: 1967-1977.
5. Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS, (2003) Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 278: 14112-14120.
6. Swerdlow DL, Mintz ED, Rodriguez M, Tejada E, Ocampo C, et al. (1994) Severe life-threatening cholera associated with blood group O in Peru: implications for the Latin American epidemic. J Infect Dis 170: 468-472.
7. Fry AE, Griffiths MJ, Auburn S, Diakite M, Forton JT, et al. (2008) Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum Mol Genet 17: 567-576.
8. Lell B, May J, Schmidt-Ott RJ, Lehman LG, Luckner D, et al. (1999) The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin Infect Dis 28: 794-799.
9. Rowe JA, Handel IG, Thera MA, Deans AM, Lyke KE, et al. (2007) Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci U S A 104: 17471-17476.
10. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, et al. (1990) Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336: 1457-1460.
11. Doumbo OK, Thera MA, Kone AK, Raza A, Tempest LJ, et al. (2009) High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am J Trop Med Hyg 81: 987-993.
12. Rowe A, Obeiro J, Newbold CI, Marsh K, (1995) Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun 63: 2323-2326.
13. Barragan A, Kremsner PG, Wahlgren M, Carlson J, (2000) Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun 68: 2971-2975.
14. Carlson J, Wahlgren M, (1992) Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med 176: 1311-1317.
15. Chotivanich KT, Udomsangpetch R, Pipitaporn B, Angus B, Suputtamongkol Y, et al. (1998) Rosetting characteristics of uninfected erythrocytes from healthy individuals and malaria patients. Ann Trop Med Parasitol 92: 45-56.
16. Udomsangpetch R, Todd J, Carlson J, Greenwood BM, (1993) The effects of hemoglobin genotype and ABO blood group on the formation of rosettes by Plasmodium falciparum-infected red blood cells. Am J Trop Med Hyg 48: 149-153.
17. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, et al. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82: 89-100.
18. Kraemer SM, Smith JD, (2006) A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 9: 374-380.
19. Lavstsen T, Salanti A, Jensen AT, Arnot DE, Theander TG, (2003) Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J 2: 27.
20. Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T, (2010) Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes-divide and conquer. PLoS Comput Biol 6: e1000933.
21. Smith JD, Subramanian G, Gamain B, Baruch DI, Miller LH, (2000) Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol Biochem Parasitol 110: 293-310.
22. Kraemer SM, Kyes SA, Aggarwal G, Springer AL, Nelson SO, et al. (2007) Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics 8: 45.
23. Rowe JA, Moulds JM, Newbold CI, Miller LH, (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388: 292-295.
24. Vigan-Womas I, Guillotte M, Le Scanf C, Igonet S, Petres S, et al. (2008) An in vivo and in vitro model of Plasmodium falciparum rosetting and autoagglutination mediated by varO, a group A var gene encoding a frequent serotype. Infect Immun 76: 5565-5580.
25. Vigan-Womas I, Guillotte M, Juillerat A, Vallieres C, Lewit-Bentley A, et al. (2011) Allelic diversity of the Plasmodium falciparum erythrocyte membrane protein 1 entails variant-specific red cell surface epitopes. PLoS One 6: e16544.
26. Albrecht L, Moll K, Blomqvist K, Normark J, Chen Q, et al. (2011) var gene transcription and PfEMP1 expression in the rosetting and cytoadhesive Plasmodium falciparum clone FCR3S1.2. Malar J 10: 17.
27. Juillerat A, Lewit-Bentley A, Guillotte M, Gangnard S, Hessel A, et al. (2011) Structure of a Plasmodium falciparum PfEMP1 rosetting domain reveals a role for the N-terminal segment in heparin-mediated rosette inhibition. Proc Natl Acad Sci U S A 108: 5243-5248.
28. Klein MM, Gittis AG, Su HP, Makobongo MO, Moore JM, et al. (2008) The cysteine-rich interdomain region from the highly variable plasmodium falciparum erythrocyte membrane protein-1 exhibits a conserved structure. PLoS Pathog 4: e1000147.
29. Clough B, Atilola FA, Black J, Pasvol G, (1998) Plasmodium falciparum: the importance of IgM in the rosetting of parasite-infected erythrocytes. Exp Parasitol 89: 129-132.
30. Luginbuhl A, Nikolic M, Beck HP, Wahlgren M, Lutz HU, (2007) Complement factor D, albumin, and immunoglobulin G anti-band 3 protein antibodies mimic serum in promoting rosetting of malaria-infected red blood cells. Infect Immun 75: 1771-1777.
31. Somner EA, Black J, Pasvol G, (2000) Multiple human serum components act as bridging molecules in rosette formation by Plasmodium falciparum-infected erythrocytes. Blood 95: 674-682.
32. Treutiger CJ, Scholander C, Carlson J, McAdam KP, Raynes JG, et al. (1999) Rouleaux-forming serum proteins are involved in the rosetting of Plasmodium falciparum-infected erythrocytes. Exp Parasitol 93: 215-224.
33. Rogerson SJ, Katundu P, Molyneux ME, (2000) Rosette formation by clinical isolates of Plasmodium falciparum in serum-free medium. Trans R Soc Trop Med Hyg 94: 461-462.
34. Rowe JA, Rogerson SJ, Raza A, Moulds JM, Kazatchkine MD, et al. (2000) Mapping of the region of complement receptor (CR) 1 required for Plasmodium falciparum rosetting and demonstration of the importance of CR1 in rosetting in field isolates. J Immunol 165: 6341-6346.
35. Rowe JA, Shafi J, Kai OK, Marsh K, Raza A, (2002) Nonimmune IgM, but not IgG binds to the surface of Plasmodium falciparum-infected erythrocytes and correlates with rosetting and severe malaria. Am J Trop Med Hyg 66: 692-699.
36. Scholander C, Treutiger CJ, Hultenby K, Wahlgren M, (1996) Novel fibrillar structure confers adhesive property to malaria-infected erythrocytes. Nat Med 2: 204-208.
37. Juillerat A, Igonet S, Vigan-Womas I, Guillotte M, Gangnard S, et al. (2010) Biochemical and biophysical characterisation of DBL1alpha1-varO, the rosetting domain of PfEMP1 from the VarO line of Plasmodium falciparum. Mol Biochem Parasitol 170: 84-92.
38. Chen Q, Heddini A, Barragan A, Fernandez V, Pearce SF, et al. (2000) The semiconserved head structure of Plasmodium falciparum erythrocyte membrane protein 1 mediates binding to multiple independent host receptors. J Exp Med 192: 1-10.
39. Morgan WTJ, Watkins WM, (2000) Unravelling the biochemical basis of blood group ABO and Lewis antigenic specificity. Glycoconj J 17: 501-530.
40. Brookes E, Demeler B, Rocco M, (2010) Developments in the US-SOMO bead modeling suite: new features in the direct residue-to-bead method, improved grid routines, and influence of accessible surface area screening. Macromol Biosci 10: 746-753.
41. Garcia de la Torre J, Huertas ML, Carrasco B, (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys J 78: 719-730.
42. Fandeur T, Le Scanf C, Bonnemains B, Slomianny C, Mercereau-Puijalon O, (1995) Immune pressure selects for Plasmodium falciparum parasites presenting distinct red blood cell surface antigens and inducing strain-specific protection in Saimiri sciureus monkeys. J Exp Med 181: 283-295.
43. Janes JH, Wang CP, Levin-Edens E, Vigan-Womas I, Guillotte M, et al. (2011) Investigating the host binding signature on the Plasmodium falciparum PfEMP1 protein family. PLoS Pathog 7: e1002032.
44. Clausen H, Hakomori S, (1989) ABH and related histo-blood group antigens; immunochemical differences in carrier isotypes and their distribution. Vox Sang 56: 1-20.
45. Fujii H, Yoshida A, (1980) Multiple components of blood group A and B antigens in human erythrocyte membranes and their difference between A1 and A2 status. Proc Natl Acad Sci U S A 77: 2951-2954.
46. Svensson L, Rydberg L, de Mattos LC, Henry SM, (2009) Blood group A(1) and A(2) revisited: an immunochemical analysis. Vox Sang 96: 56-61.
47. Higgins MK, (2008) The structure of a chondroitin sulfate-binding domain important in placental malaria. J Biol Chem 283: 21842-21846.
48. Singh K, Gitti RK, Diouf A, Zhou H, Gowda DC, et al. (2010) Subdomain 3 of Plasmodium falciparum VAR2CSA DBL3x is identified as a minimal chondroitin sulfate A-binding region. J Biol Chem 285: 24855-24862.
49. Singh K, Gittis AG, Nguyen P, Gowda DC, Miller LH, et al. (2008) Structure of the DBL3x domain of pregnancy-associated malaria protein VAR2CSA complexed with chondroitin sulfate A. Nat Struct Mol Biol 15: 932-938.
50. Singh SK, Hora R, Belrhali H, Chitnis CE, Sharma A, (2006) Structural basis for Duffy recognition by the malaria parasite Duffy-binding-like domain. Nature 439: 741-744.
51. Tolia NH, Enemark EJ, Sim BK, Joshua-Tor L, (2005) Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 122: 183-193.
52. Bull PC, Berriman M, Kyes S, Quail MA, Hall N, et al. (2005) Plasmodium falciparum variant surface antigen expression patterns during malaria. PLoS Pathog 1: e26.
53. Warimwe GM, Keane TM, Fegan G, Musyoki JN, Newton CR, et al. (2009) Plasmodium falciparum var gene expression is modified by host immunity. Proc Natl Acad Sci U S A 106: 21801-21806.
54. Normark J, Nilsson D, Ribacke U, Winter G, Moll K, et al. (2007) PfEMP1-DBL1alpha amino acid motifs in severe disease states of Plasmodium falciparum malaria. Proc Natl Acad Sci U S A 104: 15835-15840.
55. Batchelor JD, Zahm JA, Tolia NH, (2011) Dimerization of Plasmodium vivax DBP is induced upon receptor binding and drives recognition of DARC. Nat Struct Mol Biol 18: 908-914.
56. Khunrae P, Dahlback M, Nielsen MA, Andersen G, Ditlev SB, et al. (2010) Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J Mol Biol 397: 826-834.
57. Srivastava A, Gangnard S, Round A, Dechavanne S, Juillerat A, et al. (2010) Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc Natl Acad Sci U S A 107: 4884-4889.
58. Moore RE, (1955) Distribution of blood factors, ABO, MN and Rh in a group of American Negroes. Am J Phys Anthropol 13: 121-128.
59. Mourant AE, Kopec AC, Domaniewska-Sobczak K, (1978) Blood groups and diseases: a study of associations of diseases with blood groups and other polymorphisms Oxford; New York Oxford University Press.
60. Reed TE, (1968) Distributions and tests of independence of seven blood group systems in a large multiracial sample from California. Am J Hum Genet 20: 142-150.
61. Hult AK, Olsson ML, (2010) Many genetically defined ABO subgroups exhibit characteristic flow cytometric patterns. Transfusion 50: 308-323.
62. Safeukui I, Correas JM, Brousse V, Hirt D, Deplaine G, et al. (2008) Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Blood 112: 2520-2528.
63. Nato F, Mazie JC, Fournier JM, Slizewicz B, Sagot N, et al. (1991) Production of polyclonal and monoclonal antibodies against group A, B, and C capsular polysaccharides of Neisseria meningitidis and preparation of latex reagents. J Clin Microbiol 29: 1447-1452.
64. Kabsch W, (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132.
65. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
66. Vonrhein C, Blanc E, Roversi P, Bricogne G, (2007) Automated structure solution with autoSHARP. Methods Mol Biol 364: 215-230.
67. Emsley P, Lohkamp B, Scott WG, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
68. Potterton L, McNicholas S, Krissinel E, Gruber J, Cowtan K, et al. (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 60: 2288-2294.
69. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, et al. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 19: 1639-1662.
70. Schuck P, Perugini MA, Gonzales NR, Howlett GJ, Schubert D, (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys J 82: 1096-1111.
71. Weiss M, (2001) Global Indicators of X-ray data quality. J Appl Cryst 34: 130-135.
72. Johnson WC, (1999) Analyzing protein circular dichroism spectra for accurate secondary structures. Proteins 35: 307-312.