Changes in var gene mRNA levels during erythrocytic development in two phenotypically distinct Plasmodium falciparum parasites

Malaria Journal

Volumn 6, Issue , 2007, Pages

  Dahlbäck, Madeleine ^a,b   Lavstsen, Thomas ^a,b   Salanti, Ali ^a,b   Hviid, Lars ^a,b   Arnot, David E ^a,b,c   Theander, Thor G ^a,b   Nielsen, Morten A ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Rigshospitalet   (Denmark)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN 4 SULFATE; COMPLEMENTARY DNA; DBL5 EPSILON PROTEIN; GENE PRODUCT; IMMUNOGLOBULIN G; MEMBRANE ANTIGEN; MESSENGER RNA; PLASMODIUM FALCIPARUM ERYTHROCYTE MEMBRANE PROTEIN 1; UNCLASSIFIED DRUG; VAR PROTEIN; VAR2CSA PROTEIN; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; PROTOZOAL PROTEIN;

ARTICLE; CELL CYCLE; CELL INVASION; CELL MATURATION; CONTROLLED STUDY; DISEASE COURSE; DNA SYNTHESIS; ERYTHROCYTE; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; IMMUNOGLOBULIN BLOOD LEVEL; INFECTION; MALARIA; MALE; NONHUMAN; PARASITE; PHENOTYPE; PLASMODIUM FALCIPARUM; PREGNANT WOMAN; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; ANIMAL; CLASSIFICATION; CULTURE TECHNIQUE; GENE; GENETICS; HOSPITALIZATION; MALARIA FALCIPARUM; METABOLISM; PATHOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; CULTURE TECHNIQUES; GENES, PROTOZOAN; HUMANS; MALARIA, FALCIPARUM; PHENOTYPE; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PROTOZOAN PROTEINS; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; TRANSCRIPTION, GENETIC;

EID: 34447095947     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-6-78     Document Type: Article

References (47)

1. Parasite sequestration in Plasmodium falciparum malaria: spleen and antibody modulation of cytoadherence of infected erythrocytes. PH David M Hommel LH Miller IJ Udeinya LD Oligino, Proc Natl Acad Sci USA 1983 80 5075 5079 6348780 10.1073/pnas.80.16.5075
2. Roles of surface antigens on malaria-infected red blood cells in evasion of immunity. RJ Howard JW Barnwell, Contemp Top Immunobiol 1984 12 127 200 6365440
3. Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. CF Ockenhouse NN Tandon C Magowan GA Jamieson JD Chulay, Science 1989 243 1469 1471 10.1126/science.2467377 2467377
4. Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. DD Roberts JA Sherwood SL Spitalnik LJ Panton RJ Howard VM Dixit WA Frazier LH Miller V Ginsburg, Nature 1985 318 64 66 10.1038/318064a0 2414670
5. Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. AR Berendt DL Simmons J Tansey CI Newbold K Marsh, Nature 1989 341 57 59 10.1038/341057a0 2475784
6. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. M Fried PE Duffy, Science 1996 272 1502 1504 10.1126/science.272.5267. 1502 8633247
7. Cloning the Plasmodium falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. DI Baruch BL Pasloske HB Singh XH Bi XC Ma M Feldman TF Taraschi RJ Howard, Cell 1995 82 77 87 10.1016/0092-8674(95)90054-3 7541722
8. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. XZ Su VM Heatwole SP Wertheimer F Guinet JA Herrfeldt DS Peterson JA Ravetch TE Wellems, Cell 1995 82 89 100 10.1016/0092-8674(95)90055-1 7606788
9. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. JD Smith CE Chitnis AG Craig DJ Roberts DE Hudson-Taylor DS Peterson R Pinches CI Newbold LH Miller, Cell 1995 82 101 110 10.1016/0092-8674(95)90056-X 7606775
10. Genome sequence of the human malaria parasite Plasmodium falciparum. MJ Gardner N Hall E Fung O White M Berriman RW Hyman JM Carlton A Pain KE Nelson S Bowman IT Paulsen K James JA Eisen K Rutherford SL Salzberg A Craig S Kyes MS Chan V Nene SJ Shallom B Suh J Peterson S Angiuoli M Pertea J Allen J Selengut D Haft MW Mather AB Vaidya DMA Martin AH Fairlamb MJ Fraunholz DS Roos SA Ralph GI McFadden LM Cummings GM Subramanian C Mungall JC Venter DJ Carucci SL Hoffman C Newbold RW Davis CM Fraser B Barrell, Nature 2002 419 498 511 10.1038/nature01097 12368864
11. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. T Lavstsen A Salanti ATR Jensen DE Arnot TG Theander, Malaria Journal 2003 2 27 14565852 10.1186/1475-2875-2-27
12. Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. SM Kraemer JD Smith, Mol Microbiol 2003 50 1527 1538 10.1046/j.1365-2958.2003. 03814.x 14651636
13. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. K Marsh L Otoo RJ Hayes DC Carson BM Greenwood, Trans R Soc Trop Med Hyg 1989 83 293 303 10.1016/0035-9203(89)90478-1 2694458
14. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. PC Bull BS Lowe M Kortok CS Molyneux CI Newbold K Marsh, Nat Med 1998 4 358 360 10.1038/nm0398-358 9500614
15. Malaria-induced acquisition of antibodies to Plasmodium falciparum variant surface antigens. MF Ofori D Dodoo T Staalsoe JAL Kurtzhals K Koram TG Theander BD Akanmori L Hviid, Infect Immun 2002 70 2982 2988 12010988 10.1128/IAI.70.6.2982-2988.2002
16. Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of Newborns. PE Duffy M Fried, Infect Immun 2003 71 6620 6623 14573685 10.1128/IAI.71.11.6620-6623.2003
17. Variant surface antigen-specific IgG and protection against clinical consequences of pregnancy-associated Plasmodium falciparum malaria. T Staalsoe CE Shulman JN Bulmer K Kawuondo K Marsh L Hviid, Lancet 2004 363 283 289 10.1016/S0140-6736(03)15386-X 14751701
18. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. A Salanti T Staalsoe T Lavstsen ATR Jensen MPK Sowa DE Arnot L Hviid TG Theander, Mol Microbiol 2003 49 179 191 10.1046/j.1365-2958.2003.03570.x 12823820
19. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. A Salanti M Dahlback L Turner MA Nielsen L Barfod P Magistrado ATR Jensen T Lavstsen MF Ofori K Marsh L Hviid TG Theander, J Exp Med 2004 200 1197 1203 10.1084/jem.20041579 15520249
20. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes. ATR Jensen P Magistrado S Sharp L Joergensen T Lavstsen A Chiucciuini A Salanti LS Vestergaard JP Lusingu R Hermsen R Sauerwein J Christensen MA Nielsen L Hviid C Sutherland T Staalsoe TG Theander, Journal of Experimental Medicine 2004 199 1179 1190 10.1084/jem.20040274 15123742
21. IgG antibody reactivity to a Group A PfEMP1 and protection from Plasmodium falciparum malaria. PA Magistrado J Lusingu LS Vestergaard M Lemnge T Lavstsen L Turner L Hviid AT Jensen TG Theander, Infect Immun 2007 75 2415 2420 10.1128/IAI.00951-06 17283085
22. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. A Scherf R Hernandez-Rivas P Buffet E Bottius C Benatar B Pouvelle J Gysin M Lanzer, EMBO J 1998 17 5418 5426 9736619 10.1093/emboj/17.18.5418
23. Developmental selection of var gene expression in Plasmodium falciparum. QJ Chen V Fernandez A Sundstrom M Schlichtherle S Datta P Hagblom M Wahlgren, Nature 1998 394 392 395 10.1038/28660 9690477
24. A simple RNA analysismethod shows var and rif multigene family expression patterns in Plasmodium falciparum. S Kyes R Pinches C Newbold, Mol Biochem Parasitol 2000 105 311 315 10.1016/S0166-6851(99)00193-0 10693754
25. A well-conserved Plasmodium falciparum var gene shows an unusual stage-specific transcript pattern. SA Kyes Z Christodoulou A Raza P Horrocks R Pinches JA Rowe CI Newbold, Mol Microbiol 2003 48 1339 1348 10.1046/j.1365-2958. 2003.03505.x 12787360
26. Multiple var gene transcripts are expressed in Plasmodium falciparum infected erythrocytes selected for adhesion. R Noviyanti GV Brown ME Wickham MF Duffy AF Cowman JC Reeder, Mol Biochem Parasitol 2001 114 227 237 10.1016/S0166-6851(01)00266-3 11378202
27. Transcription of multiple var genes by individual, trophozoite-stage Plasmodium falciparum cells expressing a chondroitin sulphate A binding phenotype. MF Duffy GV Brown W Basuki EO Krejany R Noviyanti AF Cowman JC Reeder, Mol Microbiol 2002 43 1285 1293 10.1046/j.1365-2958.2002.02822.x 11918813
28. Human malaria parasites in continuous culture. W Trager JB Jensen, Science 1976 193 673 675 10.1126/science.781840 781840
29. Detection of antibodies to variant antigens on Plasmodium falciparum-infected erythrocytes by flow cytometry. T Staalsoe HA Giha D Dodoo TG Theander L Hviid, Cytometry 1999 35 329 336 10.1002/(SICI)1097-0320(19990401) 35:4<329::AID-CYTO5>3.0.CO;2-Y 10213198
30. 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. CH Ricke T Staalsoe K Koram BD Akanmori EM Riley TG Theander L Hviid, J Immunol 2000 165 3309 3316 10975848
31. Separation of malaria-infected erythrocytes from whole blood: use of a selective high-gradient magnetic separation technique. F Paul S Roath D Melville DC Warhurst JO Osisanya, Lancet 1981 2 70 71 10.1016/S0140-6736(81)90414-1 6113443
32. PlasmoDB - The Plasmodium Genome Resource. http://www.plasmodb.org
33. Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of antigen production. R Dzikowski M Frank K Deitsch, PLoS Pathog 2006 2 e22 16518466 10.1371/journal.ppat.0020022
34. A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. TS Voss J Healer AJ Marty MF Duffy JK Thompson JG Beeson JC Reeder BS Crabb AF Cowman, Nature 2006 439 1004 1008 16382237
35. Are Plasmodium falciparum parasites present in peripheral blood genetically the same as those sequestered in the tissues? EG Dembo HT Phiri J Montgomery ME Molyneux SJ Rogerson, Am J Trop Med Hyg 2006 74 730 732 16687670
36. A study of var gene transcription in vitro using universal var gene primers. HM Taylor SA Kyes D Harris N Kriek CI Newbold, Mol Biochem Parasitol 2000 105 13 23 10.1016/S0166-6851(99)00159-0 10613695
37. Plasmodium falciparum var gene expression is developmentally controlled at the level of RNA polymerase II-mediated transcription initiation. S Kyes Z Christodoulou R Pinches N Kriek P Horrocks C Newbold, Mol Microbiol 2007 63 1237 1247 10.1111/j.1365-2958.2007.05587.x 17257309
38. Broad analysis reveals a consistent pattern of var gene transcription in Plasmodium falciparum repeatedly selected for a defined adhesion phenotype. MF Duffy TJ Byrne SR Elliott DW Wilson SJ Rogerson JG Beeson R Noviyanti GV Brown, Mol Microbiol 2005 56 774 788 10.1111/j.1365-2958.2005.04577.x 15819631
39. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium faiciparum. MT Duraisingh TS Voss AJ Marty MF Duffy RT Good JK Thompson LH Freitas-Junior A Scherf BS Crabb AF Cowman, Cell 2005 121 13 24 10.1016/j.cell.2005.01.036 15820675
40. Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations. SA Ralph C Scheidig-Benatar A Scherf, Proc Natl Acad Sci USA 2005 102 5414 5419 15797990 10.1073/pnas.0408883102
41. Identification of nuclear proteins that interact differentially with Plasmodium falciparum var gene promoters. TS Voss M Kaestli D Vogel S Bopp HP Beck, Mol Microbiol 2003 48 1593 1607 10.1046/j.1365-2958.2003.03528.x 12791141
42. The 3D7var5.2 (var COMMON) type var gene family is commonly expressed in non-placental Plasmodium falciparum malaria. G Winter QJ Chen K Flick P Kremsner V Fernandez M Wahlgren, Mol Biochem Parasitol 2003 127 179 191 10.1016/S0166-6851(03)00004-5 12672527
43. A silenced Plasmodium falciparum var promoter can be activated in vivo through spontaneous deletion of a silencing element in the intron. L Gannoun-Zaki A Jost JB Mu KW Deitsch TE Wellems, Eukaryot Cell 2005 4 490 492 15701812 10.1128/EC.4.2.490-492.2005
44. Strict pairing of var promoters and introns is required for var gene silencing in the malaria parasite Plasmodium falciparum. M Frank R Dzikowski D Costantini B Amulic E Berdougo K Deitsch, J Biol Chem 2006 281 9942 9952 10.1074/jbc.M513067200 16455655
45. Variantantigens and endothelial receptor adhesion in Plasmodium falciparum. JP Gardner RA Pinches DJ Roberts CI Newbold, Proc Natl Acad Sci USA 1996 93 3503 3508 8622966 10.1073/pnas.93.8.3503
46. Targeted mutagenesis of Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) disrupts cytoadherence of malaria-infected red blood cells. JG Waterkeyn ME Wickham KM Davern BM Cooke RL Coppel JC Reeder JG Culvenor RF Waller AF Cowman, EMBO J 2000 19 2813 2823 10856227 10.1093/emboj/19.12.2813
47. Characterization of the pathway for transport of the cytoadherence- mediating protein, PfEMP1, to the host cell surface in malaria parasite-infected erythrocytes. N Kriek L Tilley P Horrocks R Pinches BC Elford DJP Ferguson K Lingelbach CI Newbold, Mol Microbiol 2003 50 1215 1227 10.1046/j.1365-2958.2003. 03784.x 14622410