Functional analysis of monoclonal antibodies against the Plasmodium falciparum PfEMP1-VarO adhesin
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  • 作者:Micheline Guillotte ; Farida Nato ; Alexandre Juillerat ; Audrey Hessel…
  • 关键词:Malaria ; Rosetting ; PfEMP1 adhesin ; Monoclonal antibodies (mAbs) ; Rosette ; disrupting antibodies ; Epitopes ; Antigenicity
  • 刊名:Malaria Journal
  • 出版年:2016
  • 出版时间:December 2016
  • 年:2016
  • 卷:15
  • 期:1
  • 全文大小:4,748 KB
  • 参考文献:1.Milner DA, Lee JJ, Frantzreb C, Whitten RO, Kamiza S, Carr RA, et al. Quantitative assessment of multiorgan sequestration of parasites in fatal pediatric cerebral malaria. J Infect Dis. 2015;212:1317–21.PubMed CrossRef
    2.Schofield L. Intravascular infiltrates and organ-specific inflammation in malaria pathogenesis. Immunol Cell Biol. 2007;85:130–7.PubMed CrossRef
    3.Kraemer SM, Smith JD. A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol. 2006;9:374–80.PubMed CrossRef
    4.Smith JD, Subramanian G, Gamain B, Baruch DI, Miller LH. Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol Biochem Parasitol. 2000;110:293–310.PubMed CrossRef
    5.Lavstsen T, Salanti A, Jensen AT, Arnot DE, Theander TG. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J. 2003;2:27.PubMed PubMedCentral CrossRef
    6.Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes—divide and conquer. PLoS Comput Biol. 2010;6:e1000933.PubMed PubMedCentral CrossRef
    7.Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet. 1990;336:1457–60.PubMed CrossRef
    8.Treutiger CJ, Hedlund I, Helmby H, Carlson J, Jepson A, Twumasi P, et al. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am J Trop Med Hyg. 1992;46:503–10.PubMed
    9.Rowe A, Obeiro J, Newbold CI, Marsh K. Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun. 1995;63:2323–6.PubMed PubMedCentral
    10.Doumbo OK, Thera MA, Kone AK, Raza A, Tempest LJ, Lyke KE, et al. High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am J Trop Med Hyg. 2009;81:987–93.PubMed PubMedCentral CrossRef
    11.Hviid L, Jensen AT. PfEMP1—a parasite protein family of key importance in Plasmodium falciparum malaria immunity and pathogenesis. Adv Parasitol. 2015;88:51–84.PubMed CrossRef
    12.Le Scanf C, Vigan-Womas I, Contamin H, Guillotte M, Bischoff E, Mercereau-Puijalon O. Rosetting is associated with increased Plasmodium falciparum in vivo multiplication rate in the Saimiri sciureus monkey. Microbes Infect. 2008;10:447–51.PubMed CrossRef
    13.Vigan-Womas I, Guillotte M, Le Scanf C, Igonet S, Petres S, Juillerat A, et al. 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. 2008;76:5565–80.PubMed PubMedCentral CrossRef
    14.Albrecht L, Moll K, Blomqvist K, Normark J, Chen Q, Wahlgren M. Var gene transcription and PfEMP1 expression in the rosetting and cytoadhesive Plasmodium falciparum clone FCR3S1.2. Malar J. 2011;10:17.PubMed PubMedCentral CrossRef
    15.Ghumra A, Semblat JP, Ataide R, Kifude C, Adams Y, Claessens A, et al. Induction of strain-transcending antibodies against Group A PfEMP1 surface antigens from virulent malaria parasites. PLoS Pathog. 2012;8:e1002665.PubMed PubMedCentral CrossRef
    16.Scholander C, Treutiger CJ, Hultenby K, Wahlgren M. Novel fibrillar structure confers adhesive property to malaria-infected erythrocytes. Nat Med. 1996;2:204–8.PubMed CrossRef
    17.Clough B, Atilola FA, Black J, Pasvol G. Plasmodium falciparum: the importance of IgM in the rosetting of parasite-infected erythrocytes. Exp Parasitol. 1998;89:129–32.PubMed CrossRef
    18.Rowe JA, Shafi J, Kai OK, Marsh K, Raza A. 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. 2002;66:692–9.PubMed
    19.Luginbuhl A, Nikolic M, Beck HP, Wahlgren M, Lutz HU. 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. 2007;75:1771–7.PubMed PubMedCentral CrossRef
    20.Vigan-Womas I, Guillotte M, Juillerat A, Hessel A, Raynal B, England P, et al. Structural basis for the ABO blood-group dependence of Plasmodium falciparum rosetting. PLoS Pathog. 2012;8:e1002781.PubMed PubMedCentral CrossRef
    21.Stevenson L, Huda P, Jeppesen A, Laursen E, Rowe JA, Craig A, et al. Investigating the function of Fc-specific binding of IgM to Plasmodium falciparum erythrocyte membrane protein 1 mediating erythrocyte rosetting. Cell Microbiol. 2015;17:819–31.PubMed CrossRef
    22.Stevenson L, Laursen E, Cowan GJ, Bandoh B, Barfod L, Cavanagh DR, et al. Alpha2-macroglobulin can crosslink multiple Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) molecules and may facilitate adhesion of parasitized erythrocytes. PLoS Pathog. 2015;11:e1005022.PubMed PubMedCentral CrossRef
    23.Rowe JA, Moulds JM, Newbold CI, Miller LH. P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature. 1997;388:292–5.PubMed CrossRef
    24.Barragan A, Spillmann D, Kremsner PG, Wahlgren M, Carlson J. Plasmodium falciparum: molecular background to strain-specific rosette disruption by glycosaminoglycans and sulfated glycoconjugates. Exp Parasitol. 1999;91:133–43.PubMed CrossRef
    25.Mercereau-Puijalon O, Guillotte M, Vigan-Womas I. Rosetting in Plasmodium falciparum: a cytoadherence phenotype with multiple actors. Transfus Clin Biol. 2008;15:62–71.PubMed CrossRef
    26.Ghumra A, Khunrae P, Ataide R, Raza A, Rogerson SJ, Higgins MK, et al. Immunisation with recombinant PfEMP1 domains elicits functional rosette-inhibiting and phagocytosis-inducing antibodies to Plasmodium falciparum. PLoS One. 2011;6:e16414.PubMed PubMedCentral CrossRef
    27.Juillerat A, Igonet S, Vigan-Womas I, Guillotte M, Gangnard S, Faure G, et al. Biochemical and biophysical characterisation of DBL1alpha1-varO, the rosetting domain of PfEMP1 from the VarO line of Plasmodium falciparum. Mol Biochem Parasitol. 2010;170:84–92.PubMed CrossRef
    28.Juillerat A, Lewit-Bentley A, Guillotte M, Gangnard S, Hessel A, Baron B, et al. 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. 2011;108:5243–8.PubMed PubMedCentral CrossRef
    29.Vigan-Womas I, Lokossou A, Guillotte M, Juillerat A, Bentley G, Garcia A, et al. The humoral response to Plasmodium falciparum VarO rosetting variant and its association with protection against malaria in Beninese children. Malar J. 2010;9:267.PubMed PubMedCentral CrossRef
    30.Vigan-Womas I, Guillotte M, Juillerat A, Vallieres C, Lewit-Bentley A, Tall A, et al. Allelic diversity of the Plasmodium falciparum erythrocyte membrane protein 1 entails variant-specific red cell surface epitopes. PLoS One. 2011;6:e16544.PubMed PubMedCentral CrossRef
    31.Vigan-Womas I, Guillotte M, Mercereau-Puijalon O. Plasmodium falciparum rosette formation assay. Bio-protocol. 2013;3:e 412. http://​www.​bio-protocol.​org/​e412 .
    32.Guillotte M, Vigan-Womas I, Mercereau-Puijalon O. Plasmodium falciparum rosette disruption assay. Bio-protocol. 2013;3:e411. http://​www.​bio-protocol.​org/​e411 .
    33.Guillotte M, Juillerat A, Igonet S, Hessel A, Petres S, Crublet E, et al. Immunogenicity of the Plasmodium falciparum PfEMP1-VarO adhesin: induction of surface-reactive and rosette-disrupting antibodies to VarO infected erythrocytes. PLoS One. 2015;10:e0134292.PubMed PubMedCentral CrossRef
    34.Nato F, Reich K, Lhopital S, Rouyre S, Geoffroy C, Mazie JC, et al. Production and characterization of neutralizing and non neutralizing monoclonal antibodies against listeriolysin O. Infect Immun. 1991;59:4641–6.PubMed PubMedCentral
    35.Décret n° 2013-118 du 1er février 2013 relatif à la protection des animaux utilisés à des fins scientifiques. http://​www.​legifrance.​gouv.​fr/​eli/​decret/​2013/​2/​1/​AGRG1231951D/​jo/​texte .
    36.Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. https://​www.​infrafrontier.​eu/​procedures/​animal-welfare-and-ethics/​ .
    37.Le Scanf C, Fandeur T, Morales-Betoulle ME, Mercereau-Puijalon O. Plasmodium falciparum: altered expressions of erythrocyte membrane-associated antigens during antigenic variation. Exp Parasitol. 1997;85:135–48.PubMed CrossRef
    38.Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, Sahlen A, et al. Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med. 1998;187:15–23.PubMed PubMedCentral CrossRef
    39.Heddini A, Pettersson F, Kai O, Shafi J, Obiero J, Chen Q, et al. Fresh isolates from children with severe Plasmodium falciparum malaria bind to multiple receptors. Infect Immun. 2001;69:5849–56.PubMed PubMedCentral CrossRef
    40.Wahlgren M, Carlson J, Helmby H, Hedlund I, Treutiger CJ. Molecular mechanisms and biological importance of Plasmodium falciparum erythrocyte rosetting. Mem Inst Oswaldo Cruz. 1992;87(Suppl 3):323–9.PubMed CrossRef
    41.Goel S, Palmkvist M, Moll K, Joannin N, Lara P, Akhouri RR, et al. RIFINs are adhesins implicated in severe Plasmodium falciparum malaria. Nat Med. 2015;21:314–7.PubMed CrossRef
    42.Niang M, Bei AK, Madnani KG, Pelly S, Dankwa S, Kanjee U, et al. STEVOR is a Plasmodium falciparum erythrocyte binding protein that mediates merozoite invasion and rosetting. Cell Host Microbe. 2014;16:81–93.PubMed PubMedCentral CrossRef
    43.Mancio-Silva L, Mota MM. A mediator for malaria stickiness in A versus O blood. Nat Med. 2015;21:307–8.PubMed CrossRef
    44.Lennartz F, Bengtsson A, Olsen RW, Joergensen L, Brown A, Remy L, et al. Mapping the binding site of a cross-reactive Plasmodium falciparum PfEMP1 monoclonal antibody inhibitory of ICAM-1 binding. J Immunol. 2015;195:3273–83.PubMed PubMedCentral CrossRef
    45.Angeletti D, Albrecht L, Blomqvist K, Quintana Mdel P, Akhter T, Bachle SM, et al. Plasmodium falciparum rosetting epitopes converge in the SD3-loop of PfEMP1-DBL1alpha. PLoS One. 2012;7:e50758.PubMed PubMedCentral CrossRef
    46.Angeletti D, Sandalova T, Wahlgren M, Achour A. Binding of subdomains 1/2 of PfEMP1-DBL1alpha to heparan sulfate or heparin mediates Plasmodium falciparum rosetting. PLoS One. 2015;10:e0118898.PubMed PubMedCentral CrossRef
    47.Albrecht L, Angeletti D, Moll K, Blomqvist K, Valentini D, D’Alexandri FL, et al. B-cell epitopes in NTS-DBL1alpha of PfEMP1 recognized by human antibodies in rosetting Plasmodium falciparum. PLoS One. 2014;9:e113248.PubMed PubMedCentral CrossRef
    48.Carlson J, Ekre HP, Helmby H, Gysin J, Greenwood BM, Wahlgren M. Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. Am J Trop Med Hyg. 1992;46:595–602.PubMed
    49.Rowe A, Berendt AR, Marsh K, Newbold CI. Plasmodium falciparum: a family of sulphated glycoconjugates disrupts erythrocyte rosettes. Exp Parasitol. 1994;79:506–16.PubMed CrossRef
    50.Barragan A, Kremsner PG, Wahlgren M, Carlson J. Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun. 2000;68:2971–5.PubMed PubMedCentral CrossRef
    51.Kyriacou HM, Steen KE, Raza A, Arman M, Warimwe G, Bull PC, et al. In vitro inhibition of Plasmodium falciparum rosette formation by curdlan sulfate. Antimicrob Agents Chemother. 2007;51:1321–6.PubMed PubMedCentral CrossRef
    52.Blomqvist K, Albrecht L, Quintana Mdel P, Angeletti D, Joannin N, Chene A, et al. A sequence in subdomain 2 of DBL1alpha of Plasmodium falciparum erythrocyte membrane protein 1 induces strain transcending antibodies. PLoS One. 2013;8:e52679.PubMed PubMedCentral CrossRef
  • 作者单位:Micheline Guillotte (1) (2)
    Farida Nato (3)
    Alexandre Juillerat (4) (5)
    Audrey Hessel (1) (4)
    Françoise Marchand (3)
    Anita Lewit-Bentley (4) (5)
    Graham A. Bentley (4) (5)
    Inès Vigan-Womas (1) (2) (6)
    Odile Mercereau-Puijalon (1) (2)

    1. Institut Pasteur, Unité d’Immunologie Moléculaire des Parasites, 25-28 rue du Dr ROUX, 75015, Paris, France
    2. URA CNRS 2581, 25-28 rue du Dr ROUX, 75015, Paris, France
    3. Institut Pasteur, Plate-forme de Production de Protéines recombinantes et d’Anticorps (PF5), 25-28 rue du Dr ROUX, 75015, Paris, France
    4. Institut Pasteur, Unité d’Immunologie Structurale, 25-28 rue du Dr ROUX, 75015, Paris, France
    5. CNRS URA 2185, 25-28 rue du Dr ROUX, 75015, Paris, France
    6. Institut Pasteur de Madagascar, Unité d’Immunologie des Maladies Infectieuses, BP 1274, Antananarivo 101, Madagascar
  • 刊物主题:Parasitology; Infectious Diseases; Tropical Medicine;
  • 出版者:BioMed Central
  • ISSN:1475-2875
文摘
Background Rosetting, namely the capacity of the Plasmodium falciparum-infected red blood cells to bind uninfected RBCs, is commonly observed in African children with severe malaria. Rosetting results from specific interactions between a subset of variant P. falciparum erythrocyte membrane protein 1 (PfEMP1) adhesins encoded by var genes, serum components and RBC receptors. Rosette formation is a redundant phenotype, as there exists more than one var gene encoding a rosette-mediating PfEMP1 in each genome and hence a diverse array of underlying interactions. Moreover, field diversity creates a large panel of rosetting-associated serotypes and studies with human immune sera indicate that surface-reacting antibodies are essentially variant-specific. To gain better insight into the interactions involved in rosetting and map surface epitopes, a panel of monoclonal antibodies (mAbs) was investigated.

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