CD36 selection of 3D7 Plasmodium falciparum associated with severe childhood malaria results in reduced VAR4 expression

Malaria Journal

Volumn 7, Issue , 2008, Pages

  Magistrado, Pamela A ^a   Staalsoe, Trine ^b   Theander, Thor G ^a   Hviid, Lars ^b   Jensen, Anja T R ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; PROTEIN VAR 4; UNCLASSIFIED DRUG; VIRUS PROTEIN; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; MEMBRANE ANTIGEN; PARASITE ANTIGEN; PRIMER DNA; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC STABILITY; GENETIC TRANSCRIPTION; HUMAN; MALARIA; PHENOTYPE; PLASMODIUM FALCIPARUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ADOLESCENT; ADULT; ANIMAL; BLOOD; CELL ADHESION; CHEMISTRY; CHILD; CHO CELL; CRICETULUS; ERYTHROCYTE; GENE EXPRESSION PROFILING; GENETICS; HAMSTER; METABOLISM; METHODOLOGY; MIDDLE AGED; PARASITOLOGY; PRESCHOOL CHILD; SEROTYPING;

ADOLESCENT; ADULT; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, CD36; ANTIGENS, PROTOZOAN; ANTIGENS, SURFACE; CELL ADHESION; CHILD; CHILD, PRESCHOOL; CHO CELLS; CRICETINAE; CRICETULUS; DNA PRIMERS; ERYTHROCYTES; GENE EXPRESSION PROFILING; HUMANS; MIDDLE AGED; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEROTYPING;

EID: 54849439939     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-7-204     Document Type: Article

References (53)

1. Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. DI Baruch JA Gormely C Ma RJ Howard BL Pasloske, Proc Natl Acad Sci USA 1996 93 3497 3502 8622965 10.1073/pnas.93.8.3497
2. Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. Q Chen A Barragan V Fernandez A Sundstrom M Schlichtherle A Sahlen J Carlson S Datta M Wahlgren, J Exp Med 1998 187 15 23 9419207 10.1084/jem.187.1.15
3. The semiconserved head structure of Plasmodium falciparum erythrocyte membrane protein 1 mediates binding to multiple independent host receptors. Q Chen A Heddini A Barragan V Fernandez SF Pearce M Wahlgren, J Exp Med 2000 192 1 10 10880521 10.1084/jem.192.1.1
4. Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: a parasite adhesion trait implicated in cerebral malaria. JD Smith AG Craig N Kriek D Hudson-Taylor S Kyes T Fagen R Pinches DI Baruch CI Newbold LH Miller, Proc Natl Acad Sci USA 2000 97 1766 1771 10677532 10.1073/pnas.040545897
5. The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by P. falciparum erythrocyte membrane protein 1. JC Reeder AF Cowman KM Davern JG Beeson JK Thompson SJ Rogerson GV Brown, Proc Natl Acad Sci USA 1999 96 5198 5202 10220443 10.1073/pnas.96.9.5198
6. Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence. DI Baruch XC Ma HB Singh X Bi BL Pasloske RJ Howard, Blood 1997 90 3766 3775 9345064
7. P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. JA Rowe JM Moulds CI Newbold LH Miller, Nature 1997 388 292 295 10.1038/40269 9230440
8. Plasmodium falciparum domain mediating adhesion to chondroitin sulfate A: a receptor for human placental infection. PA Buffet B Gamain C Scheidig D Baruch JD Smith R Hernandez-Rivas B Pouvelle S Oishi N Fujii T Fusai D Parzy LH Miller J Gysin A Scherf, Proc Natl Acad Sci USA 1999 96 12743 12748 10535993 10.1073/pnas.96.22.12743
9. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. DJ Roberts AG Craig AR Berendt R Pinches G Nash K Marsh CI Newbold, Nature 1992 357 689 692 10.1038/357689a0 1614515
10. Antigenic variation in Plasmodium falciparum. BA Biggs L Gooze K Wycherley W Wollish B Southwell JH Leech GV Brown, Proc Natl Acad Sci USA 1991 88 9171 9174 1924380 10.1073/pnas.88.20.9171
11. In vivo switching between variant surface antigens in human Plasmodium falciparum infection. T Staalsoe AA Hamad L Hviid IM Elhassan DE Arnot TG Theander, J Infect Dis 2002 186 719 722 10.1086/342390 12195363
12. Malaria-induced acquisition of antibodies to Plasmodium falciparum variant surface antigens. MF Ofori D Dodoo T Staalsoe JA Kurtzhals K Koram TG Theander BD Akanmori L Hviid, Infect Immun 2002 70 2982 2988 12010988 10.1128/IAI.70.6.2982-2988.2002
13. Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children. D Dodoo T Staalsoe H Giha JA Kurtzhals BD Akanmori K Koram S Dunyo FK Nkrumah L Hviid TG Theander, Infect Immun 2001 69 3713 3718 11349035 10.1128/IAI.69.6.3713-3718. 2001
14. Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants. K Marsh RJ Howard, Science 1986 231 150 153 10.1126/science.2417315 2417315
15. 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
16. 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
17. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. DI Baruch BL Pasloske HB Singh X Bi XC Ma M Feldman TF Taraschi RJ Howard, Cell 1995 82 77 87 10.1016/0092-8674(95)90054-3 7541722
18. 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
19. 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
20. 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
21. The var genes of Plasmodium falciparum are located in the subtelomeric region of most chromosomes. JP Rubio JK Thompson AF Cowman, EMBO J 1996 15 4069 4077 8670911
22. Expression of var genes located within polymorphic subtelomeric domains of Plasmodium falciparum chromosomes. K Fischer P Horrocks M Preuss J Wiesner S Wunsch AA Camargo M Lanzer, Mol Cell Biol 1997 17 3679 3686 9199301
23. 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
24. Developmental selection of var gene expression in Plasmodium falciparum. Q Chen V Fernandez A Sundstrom M Schlichtherle S Datta P Hagblom M Wahlgren, Nature 1998 394 392 395 10.1038/28660 9690477
25. 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
26. 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
27. In vitro selection of Plasmodium falciparum 3D7 for expression of variant surface antigens associated with severe malaria in African children. T Staalsoe MA Nielsen LS Vestergaard AT Jensen TG Theander L Hviid, Parasite Immunol 2003 25 421 427 10.1111/j.1365-3024.2003.00652.x 14651589
28. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes. AT Jensen P Magistrado S Sharp L Joergensen T Lavstsen A Chiucchiuini A Salanti LS Vestergaard JP Lusingu R Hermsen R Sauerwein J Christensen MA Nielsen L Hviid C Sutherland T Staalsoe TG Theander, J Exp Med 2004 199 1179 1190 15123742 10.1084/jem.20040274
29. Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia. HM Kyriacou GN Stone RJ Challis A Raza KE Lyke MA Thera AK Koné OK Doumbo CV Plowe JA Rowe, Mol Biochem Parasitol 2006 150 211 218 16996149 10.1016/j.molbiopara. 2006.08.005
30. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. T Lavstsen A Salanti AT Jensen DE Arnot TG Theander, Malar J 2003 2 27 14565852 10.1186/1475-2875-2-27
31. Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome. BA Robinson TL Welch JD Smith, Mol Microbiol 2003 47 1265 1278 10.1046/j.1365-2958.2003.03378.x 12603733
32. Plasmodium falciparum antigenic variation: Relationships between in vivo selection, acquired antibody response, and disease severity. PC Bull A Pain FM Ndungu SM Kinyanjui DJ Roberts CI Newbold K Marsh, J Infects Dis 2005 192 1119 1126 10.1086/432761
33. 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
34. Concentration from continuous culture of erythrocytes infected with trophozoites and schizonts of Plasmodium falciparum. JB Jensen, Am J Trop Med Hyg 1978 27 1274 1276 365006
35. Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and nonsevere malaria and is modified by acquired immunity. MA Nielsen T Staalsoe JA Kurtzhals BQ Goka D Dodoo M Alifrangis TG Theander BD Akanmori L Hviid, J Immunol 2002 168 3444 3450 11907103
36. Insecticide-treated bed nets reduce plasma antibody levels and limit the repertoire of antibodies to Plasmodium falciparum variant surface antigens. N Askjaer C Maxwell W Chambo T Staalsoe MA Nielsen L Hviid C Curtis TG Theander, Clin Diagn Lab Immunol 2001 8 1289 1291 11687480 10.1128/CDLI.8.6.1289-1291.2001
37. 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
38. 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 AT Jensen MP Sowa DE Arnot L Hviid TG Theander, Mol Microbiol 2003 49 179 191 10.1046/j.1365-2958. 2003.03570.x 12823820
39. A non-sense mutation in Cd36 gene is associated with protection from severe malaria. A Pain BC Urban O Kai C Casals-Pascual J Shafi K Marsh DJ Roberts, Lancet 2001 357 1502 1503 10.1016/S0140-6736(00)04662-6 11377606
40. Clinical correlates of in vitro Plasmodium falciparum cytoadherence. M Ho B Singh S Looareesuwan TM Davis D Bunnag NJ White, Infect Immun 1991 59 873 878 1997437
41. Malaria susceptibility and CD36 mutation. TJ Aitman LD Cooper PJ Norsworthy FN Wahid JK Gray BR Curtis PM McKeigue D Kwiatkowski BM Greenwood RW Snow AV Hill J Scott, Nature 2000 405 1015 1016 10.1038/35016636 10890433
42. Association of severe noncerebral Plasmodium falciparum malaria in Brazil with expressed PfEMP1 DBL1 alpha sequences lacking cysteine residues. K Kirchgatter HA Portillo, Mol Med 2002 8 16 23 11984002
43. Receptor-specific adhesion and clinical disease in Plasmodium falciparum. C Newbold P Warn G Black A Berendt A Craig B Snow M Msobo N Peshu K Marsh, Am J Trop Med Hyg 1997 57 389 398 9347951
44. 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. GD Turner H Morrison M Jones TM Davis S Looareesuwan ID Buley KC Gatter CI Newbold S Pukritayakamee B Nagachinta NJ White AR Berendt, Am J Pathol 1994 145 1057 1069 7526692
45. A high frequency African coding polymorphism in the N-terminal domain of ICAM-1 predisposing to cerebral malaria in Kenya. D Fernandez-Reyes AG Craig SA Kyes N Peshu RW Snow AR Berendt K Marsh CI Newbold, Hum Mol Genet 1997 6 1357 1360 10.1093/hmg/6.8.1357 9259284
46. 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 5428 9736619 10.1093/emboj/17.18.5418
47. A simple RNA analysis method 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
48. Transcriptome analysis of antigenic variation in Plasmodium falciparum - var silencing is not dependent on antisense RNA. SA Ralph E Bischoff D Mattei O Sismeiro M-A Dillies G Guigon J-Y Coppee PH David A Scherf, Genome Biology 2005 6 R93 16277748 10.1186/gb-2005-6-11-r93
49. 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
50. Changes in var gene mRNA levels during erythrocytic development in two phenotypically distinct Plasmodium falciparum parasites. M Dahlbäck T Lavstsen A Salanti L Hviid DE Arnot TG Theander MA Nielsen, Malaria J 2007 6 78 10.1186/1475-2875-6-78
51. Variable var transition rates underlie antigenic variation in malaria. P Horrocks R Pinches Z Christodoulou SA Kyes CI Newbold, Proc Natl Acad Sci USA 2004 101 11129 11134 15256597 10.1073/pnas.0402347101
52. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. DJ Roberts AG Craig AR Berendt R Pinches G Nash K Marsh CI Newbold, Nature 1992 357 689 692 10.1038/357689a0 1614515
53. Variable switching rates of malaria virulence genes are associated with chromosomal position. M Frank R Dzikowski B Amulic K Deitsch, Mol Microbiol 2007 64 1486 1498 10.1111/j.1365-2958.2007.05736.x 17555435