Multiple plasmodium falciparum erythrocyte membrane protein 1 variants per genome can Bind IgM via Its Fc fragment Fcμ

Infection and Immunity

Volumn 83, Issue 10, 2015, Pages 3972-3981

  Jeppesen, Anine ^a   Ditlev, Sisse Bolm ^a   Soroka, Vladyslav ^a   Stevenson, Liz ^a   Turner, Louise ^a   Dzikowski, Ron ^b   Hviid, Lars ^a   Barfoda, Lea ^a  

^a University of Copenhagen   (Denmark)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN 4 SULFATE; DUFFY BINDING EPSILON PROTEIN; DUFFY BINDING PROTEIN; ERYTHROCYTE MEMBRANE PROTEIN 1; FC MU RECEPTOR; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN M; UNCLASSIFIED DRUG; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ERYTHROCYTE ADHESIVENESS; IN VITRO STUDY; INSECT GENOME; MOUSE; NONHUMAN; PHAGOCYTOSIS; PLACENTA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; ROSETTE FORMATION; GENETICS; GENOME; HUMAN; IMMUNOLOGY; MALARIA FALCIPARUM; PARASITOLOGY; PLASMODIUM FALCIPARUM;

ANTIBODIES, PROTOZOAN; GENOME, PROTOZOAN; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN M; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAN PROTEINS; ROSETTE FORMATION;

EID: 84944463301     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00337-15     Document Type: Article

References (61)

1. Forsgren A, Sjoquist J. 1966. "Protein A" from S. aureus. I. Pseudoimmune reaction with human γ-globulin. J Immunol 97:822-827.
2. Bjorck L, Kronvall G. 1984. Purification and some properties of streptococcal protein G, a novel IgG-binding reagent. J Immunol 133:969-974.
3. Dossett JH, Kronvall G, Williams RC, Jr, Quie PG. 1969. Antiphagocytic effects of staphylococcal protein A. J Immunol 103:1405-1410.
4. Rowe JA, ShafiJ, 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. AmJ Trop Med Hyg 66:692-699.
5. Creasey A, Staalsoe T, Raza A, Arnot D, Rowe JA. 2003. Nonspecific immunoglobulinMbinding and chondroitin sulfate A binding are linked phenotypes of Plasmodium falciparum isolates implicated in malaria during pregnancy. Infect Immun 71:4767-4771. http://dx.doi.org/10.1128/IAI.71.8.4767-4771.2003.
6. alanti A, Staalsoe T, Lavstsen T, Jensen ATR, Sowa MPK, Arnot DE, Hviid L, Theander TG. 2003. Selective upregulation of a single distinctly structured var gene in CSA-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol 49:179-191. http://dx.doi.org/10.1046/j.1365-2958.2003.03570.x.
7. Salanti A, Dahlbäck M, Turner L, Nielsen MA, Barfod L, Magistrado P, Jensen ATR, Lavstsen T, Ofori MF, Marsh K, Hviid L, Theander TG. 2004. Evidence for the involvement of VAR2CSA in pregnancyassociated malaria. J Exp Med 200:1197-1203. http://dx.doi.org/10.1084/jem.20041579.
8. Khunrae P, Dahlbäck M, Nielsen MA, Andersen G, Ditlev SB, Resende M, Pinto VV, Theander TG, Higgins MK, Salanti A. 2010. Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J Mol Biol 397:826-834. http://dx.doi.org/10.1016/j.jmb.2010.01.040.
9. Srivastava A, Gangnard S, Round A, Dechavanne S, Juillerat A, Raynal B, Faure G, Baron B, Ramboarina S, Singh SK, Belrhali H, England P, Lewit-Bentley A, Scherf A, Bentley GA, Gamain B. 2010. Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc Natl Acad SciUS A 107:4884-4889. http://dx.doi.org/10.1073/pnas.1000951107.
10. 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. http://dx.doi.org/10.1038/40888.
11. Vigan-Womas I, Guillotte M, Le Scanf C, Igonet S, Petres S, Juillerat A, Badaut C, Nato F, Schneider A, Lavergne A, Contamin H, Tall A, Baril L, Bentley GA, Mercereau-Puijalon O. 2008. An in vivo/in vitro model of rosetting and autoagglutination mediated by Plasmodium falciparum VarO, a group A var gene encoding a frequent serotype. Infect Immun 76:5565-5580. http://dx.doi.org/10.1128/IAI.00901-08.
12. Vigan-Womas I, Guillotte M, Juillerat A, Vallieres C, Lewit-Bentley A, Tall A, Baril L, Bentley GA, Mercereau-Puijalon O. 2011. Allelic diversity of the Plasmodium falciparum erythrocyte membrane protein 1 entails variant-specific red cell surface epitopes. PLoS One 6:e16544. http://dx.doi.org/10.1371/journal.pone.0016544.
13. Ghumra A, Semblat JP, Ataide R, Kifude C, Adams Y, Claessens A, Anong DN, Bull PC, Fennell C, Arman M, Amambua-Ngwa A, Walther M, Conway DJ, Kassambara L, Doumbo OK, Raza A, Rowe JA. 2012. Induction of strain-transcending antibodies against group A PfEMP1 surface antigens from virulent malaria parasites. PLoS Pathog 8:e1002665. http://dx.doi.org/10.1371/journal.ppat.1002665.
14. Carlson J, Ekre HP, Helmby H, Gysin J, Greenwood BM, Wahlgren M. 1992. Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. AmJ Trop Med Hyg 46:595-602.
15. Stevenson L, Huda P, Jeppesen A, Laursen E, Rowe JA, Craig A, Streicher W, Barfod L, Hviid L. 2015. Investigating the function of Fc-specific binding of IgM to Plasmodium falciparum erythrocyte membrane protein 1 mediating erythrocyte rosetting. Cell Microbiol 17:819-831. http://dx.doi.org/10.1111/cmi.12403.
16. Kyriacou HM, Steen KE, Raza A, Arman M, Warimwe G, Bull PC, Havlik I, Rowe JA. 2007. In vitro inhibition of Plasmodium falciparum rosette formation by curdlan sulphate. Antimicrob Agents Chemother 51:1321-1326. http://dx.doi.org/10.1128/AAC.01216-06.
17. Vigan-Womas I, Guillotte M, Juillerat A, Hessel A, Raynal B, England P, Cohen JH, Bertrand O, Peyrard T, Bentley GA, Lewit-Bentley A, Mercereau-Puijalon O. 2012. Structural basis for the ABO blood-group dependence of Plasmodium falciparum rosetting. PLoS Pathog 8:e1002781. http://dx.doi.org/10.1371/journal.ppat.1002781.
18. Czajkowsky DM, Salanti A, Ditlev SB, Shao Z, Ghumra A, Rowe JA, Pleass RJ. 2010. IgM, FcμRs, and malarial immune evasion. J Immunol 184:4597-4603. http://dx.doi.org/10.4049/jimmunol.1000203.
19. Barfod L, Dalgaard MB, Pleman ST, Ofori MF, Pleass RJ, Hviid L. 2011. Evasion of immunity to Plasmodium falciparum malaria by IgM masking of protective IgG epitopes in infected erythrocyte surface-exposed PfEMP1. Proc Natl Acad Sci U S A 108:12485-12490. http://dx.doi.org/10.1073/pnas.1103708108.
20. Stevenson L, Laursen E, Cowan GJ, Bandoh B, Barfod L, Cavanagh DR, Andersen GR, Hviid L. 2015. α2-Macroglobulin can crosslink multiple Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) molecules and may facilitate adhesion of parasitized erythrocytes. PLoS Pathog 11:e1005022. http://dx.doi.org/10.1371/journal.ppat.1005022.
21. Creasey A, Giha H, Hamad AA, El Hassan IM, Theander TG, Arnot DE. 2004. Eleven years of malaria surveillance in a Sudanese village highlights unexpected variation in individual disease susceptibility and outbreak severity. Parasitology 129:263-271. http://dx.doi.org/10.1017/S0031182004005724.
22. Barfod L, Nielsen MA, Turner L, Dahlbäck M, Jensen ATR, Hviid L, Theander TG, Salanti A. 2006. Baculovirus-expressed constructs induce immunoglobulin G that recognizes VAR2CSA on Plasmodium falciparum- infected erythrocytes. Infect Immun 74:4357-4360. http://dx.doi.org/10.1128/IAI.01617-05.
23. Rask TS, Hansen DA, Theander TG, Pedersen AG, Lavstsen T. 2010. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes-divide and conquer. PLoS Comput Biol 6:e1000933. http://dx.doi.org/10.1371/journal.pcbi.1000933.
24. Berger SS, Turner L, Wang CW, Petersen JE, Kraft M, Lusingu JP, Mmbando B, Marquard AM, Bengtsson DB, Hviid L, Nielsen MA, Theander TG, Lavstsen T. 2013. Plasmodium falciparum expressing domain cassette 5 type PfEMP1 (DC5-PfEMP1) bind PECAM1. PLoS One 8:e69117. http://dx.doi.org/10.1371/journal.pone.0069117.
25. Barfod L, Bernasconi N, Dahlbäck M, Jarrosay D, Andersen PH, Salanti A, Ofori MF, Turner L, Resende M, Nielsen MA, Theander TG, Sallusto F, Lanzavecchia A, Hviid L. 2007. Human pregnancy-associated malariaspecific B cells target polymorphic, conformational epitopes in VAR2CSA. Mol Microbiol 63:335-347. http://dx.doi.org/10.1111/j.1365-2958.2006.05503.x.
26. Barfod L, Dobrilovic T, Magistrado P, Khunrae P, Viwami F, Bruun J, Dahlbäck M, Bernasconi NL, Fried M, John D, Duffy PE, Salanti A, Lanzavecchia A, Lim CT, Ndam NT, Higgins MK, Hviid L. 2010. Chondroitin sulfate A-adhering Plasmodium falciparum-infected erythrocytes express functionally important antibody epitopes shared by multiple variants. J Immunol 185:7553-7561. http://dx.doi.org/10.4049/jimmunol.1002390.
27. Bhasin VK, Trager W. 1984. Gametocyte-forming and nongametocyte- forming clones of Plasmodium falciparum. Am J Trop Med Hyg 33:534-537.
28. Cranmer SL, Magowan C, Liang J, Coppel RL, Cooke BM. 1997. An alternative to serum for cultivation of Plasmodium falciparum in vitro. Trans R Soc Trop Med Hyg 91:363-365. http://dx.doi.org/10.1016/S0035-9203(97)90110-3.
29. Frank M, Dzikowski R, Amulic B, Deitsch K. 2007. Variable switching rates of malaria virulence genes are associated with chromosomal position. Mol Microbiol 64:1486-1498. http://dx.doi.org/10.1111/j.1365-2958.2007.05736.x.
30. Dzikowski R, Deitsch KW. 2008. Active transcription is required for maintenance of epigenetic memory in the malaria parasite Plasmodium falciparum. J Mol Biol 382:288-297. http://dx.doi.org/10.1016/j.jmb.2008.07.015.
31. Fastman Y, Noble R, Recker M, Dzikowski R. 2012. Erasing the epigenetic memory and beginning to switch-the onset of antigenic switching of var genes in Plasmodium falciparum. PLoS One 7:e34168. http://dx.doi.org/10.1371/journal.pone.0034168.
32. Staalsoe T, Nielsen MA, Vestergaard LS, Jensen ATR, Theander TG, Hviid L. 2003. In vitro selection of Plasmodium falciparum 3D7 for expression of variant surface antigens associated with severe malaria in African children. Parasite Immunol 25:421-427. http://dx.doi.org/10.1111/j.1365-3024.2003.00652.x.
33. Bengtsson A, Joergensen L, Rask TS, Olsen RW, Andersen MA, Turner L, Theander TG, Hviid L, Higgins MK, Craig A, Brown A, Jensen AT. 2013. A novel domain cassette identifies Plasmodium falciparum PfEMP1 proteins binding ICAM-1 and is a target of cross-reactive, adhesioninhibitory antibodies. J Immunol 190:240-249. http://dx.doi.org/10.4049/jimmunol.1202578.
34. Dahlbäck M, Lavstsen T, Salanti A, Hviid L, Arnot DE, Theander T, Nielsen MA. 2007. Changes in var gene mRNA levels during erythrocytic development in two phenotypically distinct Plasmodium falciparum parasites. Malar J 6:78. http://dx.doi.org/10.1186/1475-2875-6-78.
35. Wang CW, Lavstsen T, Bengtsson DC, Magistrado PA, Berger SS, Marquard AM, Alifrangis M, Lusingu JP, Theander TG, Turner L. 2012. Evidence for in vitro and in vivo expression of the conserved VAR3 (type 3) Plasmodium falciparum erythrocyte membrane protein 1. Malar J 11:129. http://dx.doi.org/10.1186/1475-2875-11-129.
36. Ghumra A, Semblat J-P, McIntosh RS, Raza A, Rasmussen IB, Braathen R, Johansen F-E, Sandlie I, Mongini PK, Rowe JA, Pleass RJ. 2008. Identification of residues in the Cμ4 domain of polymeric IgM essential for interaction with Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1). J Immunol 181:1988-2000. http://dx.doi.org/10.4049/jimmunol.181.3.1988.
37. Haase RN, Megnekou R, Lundquist M, Ofori MF, Hviid L, Staalsoe T. 2006. Plasmodium falciparum parasites expressing pregnancy-specific variant surface antigens adhere strongly to the choriocarcinoma cell line BeWo. Infect Immun 74:3035-3038. http://dx.doi.org/10.1128/IAI.74.5.3035-3038.2006.
38. Tippett E, Fernandes LA, Rogerson SJ, Jaworowski A. 2007. A novel flow cytometric phagocytosis assay of malaria-infected erythrocytes. J Immunol Methods 325:42-50. http://dx.doi.org/10.1016/j.jim.2007.05.012.
39. Rasti N, Namusoke F, Chene A, Chen Q, Gamain B, Staalsoe T, Klinkert M, Mirembe F, Kironde F, Wahlgren M. 2006. Nonimmune immunoglobulin binding and multiple adhesion characterize P. falciparum- infected erythrocytes of placental origin. Proc Natl Acad Sci U S A 103:13795-13800. http://dx.doi.org/10.1073/pnas.0601519103.
40. Semblat JP, Raza A, Kyes SA, Rowe JA. 2006. Identification of Plasmodium falciparum var1CSA and var2CSA domains that bind IgM natural antibodies. Mol Biochem Parasitol 146:192-197. http://dx.doi.org/10.1016/j.molbiopara.2005.12.007.
41. Jensen ATR, Magistrado PA, Sharp S, Joergensen L, Lavstsen T, Chiucchiuini A, Salanti A, Vestergaard LS, Lusingu JP, Hermsen R, Sauerwein R, Christensen J, Nielsen MA, Hviid L, Sutherland C, Staalsoe T, Theander TG. 2004. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes. J Exp Med 199:1179-1190. http://dx.doi.org/10.1084/jem.20040274.
42. Chen QJ, Heddini A, Barragan A, Fernandez V, Pearce SFA, Wahlgren M. 2000. The semiconserved head structure of Plasmodium falciparum erythrocyte membrane protein 1 mediates binding to multiple independent host receptors. J Exp Med 192:1-9. http://dx.doi.org/10.1084/jem.192.1.1.
43. Flick K, Scholander C, Chen Q, Fernandez V, Pouvelle B, Gysin J, Wahlgren M. 2001. Role of non-immune IgG bound to PfEMP1 in placental malaria. Science 293:2098-2100. http://dx.doi.org/10.1126/science.1062891.
44. Pasternak ND, Dzikowski R. 2009. PfEMP1: an antigen that plays a key role in the pathogenicity and immune evasion of the malaria parasite Plasmodium falciparum. Int J Biochem Cell Biol 41:1463-1466. http://dx.doi.org/10.1016/j.biocel.2008.12.012.
45. Hommel M, David PH, Oligino LD. 1983. Surface alterations of erythrocytes in Plasmodium falciparum malaria. Antigenic variation, antigenic diversity, and the role of the spleen. J Exp Med 157:1137-1148.
46. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, Pinches R, Newbold CI, Miller LH. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82: 101-110. http://dx.doi.org/10.1016/0092-8674(95)90056-X.
47. Su X, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, Ravetch JA, Wellems TE. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82:89-100. http://dx.doi.org/10.1016/0092-8674(95)90055-1.
48. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511. http://dx.doi.org/10.1038/nature01097.
49. Hviid L, Jensen AT. 2015. PfEMP1-a parasite protein family of key importance in Plasmodium falciparum malaria immunity and pathogenesis. Adv Parasitol 88:51-84. http://dx.doi.org/10.1016/bs.apar.2015.02.004.
50. Turner L, Lavstsen T, Berger SS, Wang CW, Petersen JE, Avril M, Brazier AJ, Freeth J, Jespersen JS, Nielsen MA, Magistrado P, Lusingu J, Smith JD, Higgins MK, Theander TG. 2013. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498: 502-505. http://dx.doi.org/10.1038/nature12216.
51. Lau CK, Turner L, Jespersen JS, Lowe ED, Petersen B, Wang CW, Petersen JE, Lusingu J, Theander TG, Lavstsen T, Higgins MK. 2015. Structural conservation despite huge sequence diversity allows EPCR binding by the PfEMP1 family implicated in severe childhood malaria. Cell Host Microbe 17:118-129. http://dx.doi.org/10.1016/j.chom.2014.11.007.
52. Hviid L. 2011. The case for PfEMP1-based vaccines to protect pregnant women against Plasmodium falciparum malaria. Expert Rev Vaccines 10: 1405-1414. http://dx.doi.org/10.1586/erv.11.113.
53. Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, Lanzer M. 1998. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra- erythrocytic development in Plasmodium falciparum. EMBO J 17: 5418-5428. http://dx.doi.org/10.1093/emboj/17.18.5418.
54. Schieck E, Pfahler JM, Sanchez CP, Lanzer M. 2007. Nuclear run-on analysis of var gene expression in Plasmodium falciparum. Mol Biochem Parasitol 153:207-212. http://dx.doi.org/10.1016/j.molbiopara.2007.02.004.
55. Dzikowski R, Frank M, Deitsch K. 2006. Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of anti- gen production. PLoS Pathog 2:e22. http://dx.doi.org/10.1371/journal.ppat.0020022.
56. Dzikowski R, Deitsch KW. 2009. Genetics of antigenic variation in Plasmodium falciparum. Curr Genet 55:103-110. http://dx.doi.org/10.1007/s00294-009-0233-2.
57. Guizetti J, Scherf A. 2013. Silence, activate, poise, and switch! Mechanisms of antigenic variation in Plasmodium falciparum. Cell Microbiol 15:718-726. http://dx.doi.org/10.1111/cmi.12115.
58. Helmby H, Cavelier L, Pettersson U, Wahlgren M. 1993. Rosetting Plasmodium falciparum-infected erythrocytes express unique strainspecific antigens on their surface. Infect Immun 61:284-288.
59. Goel S, Palmkvist M, Moll K, Joannin N, Lara P, Akhouri R, Moradi N, Ojemalm K, Westman M, Angeletti D, Kjellin H, Lehtio J, Blixt O, Idestrom L, Gahmberg CG, Storry JR, Hult AK, Olsson ML, von Heijne G, Nilsson I, Wahlgren M. 2015. RIFINs are adhesins implicated in severe Plasmodium falciparum malaria. Nat Med 21:314-317. http://dx.doi.org/10.1038/nm.3812.
60. Mercereau-Puijalon O, Guillotte M, Vigan-Womas I. 2008. Rosetting in Plasmodium falciparum: a cytoadherence phenotype with multiple actors. Transfus Clin Biol 15:62-71. http://dx.doi.org/10.1016/j.tracli.2008.04.003.
61. Lavstsen T, Salanti A, Jensen ATR, 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. http://dx.doi.org/10.1186/1475-2875-2-27.