Home LiteratureArticle Details
PMID: 18395207 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Frequent recombination events generate diversity within the multi-copy variant antigen gene families of Plasmodium falciparum.

International journal for parasitology ·Vol. 38 ·No. 10 ·2008-08-00 ·Pages 1099-109

Frank M, Kirkman L, Costantini D, Sanyal S, Lavazec C, Templeton TJ, Deitsch KW

Abstract

The human malaria parasite Plasmodium falciparum utilises a mechanism of antigenic variation to avoid the antibody response of its human host and thereby generates a long-term, persistent infection. This process predominantly results from systematic changes in expression of the primary erythrocyte surface antigen, a parasite-produced protein called PfEMP1 that is encoded by a repertoire of over 60 var genes in the P. falciparum genome. var genes exhibit extensive sequence diversity, both within a single parasite's genome as well as between different parasite isolates, and thus provide a large repertoire of antigenic determinants to be alternately displayed over the course of an infection. Whilst significant work has recently been published documenting the extreme level of diversity displayed by var genes found in natural parasite populations, little work has been done regarding the mechanisms that lead to sequence diversification and heterogeneity within var genes. In the course of producing transgenic lines from the original NF54 parasite isolate, we cloned and characterised a parasite line, termed E5, which is closely related to but distinct from 3D7, the parasite used for the P. falciparum genome nucleotide sequencing project. Analysis of the E5 var gene repertoire, as well as that of the surrounding rif and stevor multi-copy gene families, identified examples of frequent recombination events within these gene families, including an example of a duplicative transposition which indicates that recombination events play a significant role in the generation of diversity within the antigen encoding genes of P. falciparum.

MeSH Terms
Animals Antigenic Variation Antigens, Protozoan/genetics Base Sequence Cloning, Organism Erythrocytes/parasitology Gene Conversion Genes, Protozoan/immunology Genotype Humans Molecular Sequence Data Plasmodium falciparum/genetics,immunology Polymerase Chain Reaction/methods Protozoan Proteins/genetics
Chemicals
Antigens, Protozoan Protozoan Proteins erythrocyte membrane protein 1, Plasmodium falciparum
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Frank Matthias
Department of Microbiology and Immunology, Weill Medical College of Cornell University, 1300 York Avenue, Box 62, New York, NY 10021, USA.
Kirkman Laura
Costantini Daniel
Sanyal Sohini
Lavazec Catherine
Templeton Thomas J
Deitsch Kirk W
References (53)
53 references, click to expand
  1. Antigenic variation in Babesia bovis occurs through segmental gene conversion of the ves multigene family, within a bidirectional locus of active transcription.
    Mol Microbiol. 2006 Jan;59(2):402-14 PMID: 16390438
  2. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes.
    Cell. 1995 Jul 14;82(1):101-10 PMID: 7606775
  3. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites.
    Cell. 2005 Apr 8;121(1):25-36 PMID: 15820676
  4. Antibodies to Plasmodium falciparum rifin proteins are associated with rapid parasite clearance and asymptomatic infections.
    Infect Immun. 2003 Nov;71(11):6229-33 PMID: 14573641
  5. Var gene diversity in Plasmodium falciparum is generated by frequent recombination events.
    Mol Biochem Parasitol. 2000 Oct;110(2):391-7 PMID: 11071291
  6. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria.
    Mol Microbiol. 2003 Jul;49(1):179-91 PMID: 12823820
  7. Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome.
    Nat Genet. 2007 Jan;39(1):126-30 PMID: 17159981
  8. Chloroquine sensitivity of isolates of Plasmodium falciparum adapted to in vitro culture.
    Trop Geogr Med. 1981 Mar;33(1):50-4 PMID: 7018038
  9. A central role for Plasmodium falciparum subtelomeric regions in spatial positioning and telomere length regulation.
    EMBO J. 2002 Feb 15;21(4):815-24 PMID: 11847128
  10. A genetic screen for improved plasmid segregation reveals a role for Rep20 in the interaction of Plasmodium falciparum chromosomes.
    EMBO J. 2002 Mar 1;21(5):1231-9 PMID: 11867551
  11. Genome variation and evolution of the malaria parasite Plasmodium falciparum.
    Nat Genet. 2007 Jan;39(1):120-5 PMID: 17159978
  12. Population genomics of the immune evasion (var) genes of Plasmodium falciparum.
    PLoS Pathog. 2007 Mar;3(3):e34 PMID: 17367208
  13. Sympatric Plasmodium falciparum isolates from Venezuela have structured var gene repertoires.
    Malar J. 2003 Apr 11;2:7 PMID: 12737636
  14. Malaria pathogenesis.
    Science. 1994 Jun 24;264(5167):1878-83 PMID: 8009217
  15. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes.
    Cell. 1995 Jul 14;82(1):77-87 PMID: 7541722
  16. Activation, silencing and mutually exclusive expression within the var gene family of Plasmodium falciparum.
    Int J Parasitol. 2006 Aug;36(9):975-85 PMID: 16797552
  17. A study of var gene transcription in vitro using universal var gene primers.
    Mol Biochem Parasitol. 2000 Jan 5;105(1):13-23 PMID: 10613695
  18. A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria.
    Nature. 2006 Feb 23;439(7079):1004-8 PMID: 16382237
  19. Hypervariability within the Rifin, Stevor and Pfmc-2TM superfamilies in Plasmodium falciparum.
    Nucleic Acids Res. 2006;34(22):6696-707 PMID: 17148488
  20. Variable switching rates of malaria virulence genes are associated with chromosomal position.
    Mol Microbiol. 2007 Jun;64(6):1486-98 PMID: 17555435
  21. Molecular analysis of recrudescent parasites in a Plasmodium falciparum drug efficacy trial in Gabon.
    Trans R Soc Trop Med Hyg. 1997 Nov-Dec;91(6):719-24 PMID: 9509189
  22. Genetic diversity of the DBLalpha region in Plasmodium falciparum var genes among Asia-Pacific isolates.
    Mol Biochem Parasitol. 2002 Mar;120(1):117-26 PMID: 11849711
  23. Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites.
    EMBO Rep. 2007 Oct;8(10):959-65 PMID: 17762879
  24. Mechanisms of antigenic variation in African trypanosomes.
    Behring Inst Mitt. 1997 Mar;(99):1-15 PMID: 9303197
  25. Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum.
    Nature. 2000 Oct 26;407(6807):1018-22 PMID: 11069183
  26. Pregnancy-associated malaria and the prospects for syndrome-specific antimalaria vaccines.
    J Exp Med. 2004 Nov 1;200(9):1093-7 PMID: 15520241
  27. Evidence that Plasmodium falciparum chromosome end clusters are cross-linked by protein and are the sites of both virulence gene silencing and activation.
    Mol Microbiol. 2006 Oct;62(1):72-83 PMID: 16942599
  28. Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome.
    Mol Microbiol. 2003 Mar;47(5):1265-78 PMID: 12603733
  29. Analysis of Plasmodium falciparum PfEMP-1/var genes suggests that recombination rearranges constrained sequences.
    Mol Biochem Parasitol. 1999 Jul 30;102(1):167-77 PMID: 10477185
  30. Plasmodium falciparum: isolation of large numbers of parasite clones from infected blood samples.
    Exp Parasitol. 1996 Jun;83(1):147-9 PMID: 8654543
  31. Strict pairing of var promoters and introns is required for var gene silencing in the malaria parasite Plasmodium falciparum.
    J Biol Chem. 2006 Apr 14;281(15):9942-52 PMID: 16455655
  32. Genome wide gene amplifications and deletions in Plasmodium falciparum.
    Mol Biochem Parasitol. 2007 Sep;155(1):33-44 PMID: 17599553
  33. Recombination hotspots and population structure in Plasmodium falciparum.
    PLoS Biol. 2005 Oct;3(10):e335 PMID: 16144426
  34. Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family.
    Mol Microbiol. 2003 Dec;50(5):1527-38 PMID: 14651636
  35. Genome sequence of the human malaria parasite Plasmodium falciparum.
    Nature. 2002 Oct 3;419(6906):498-511 PMID: 12368864
  36. Recognition of variant Rifin antigens by human antibodies induced during natural Plasmodium falciparum infections.
    Infect Immun. 2002 Dec;70(12):7013-21 PMID: 12438381
  37. The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae.
    Mol Microbiol. 2005 Oct;58(2):510-9 PMID: 16194236
  38. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes.
    J Exp Med. 2004 May 3;199(9):1179-90 PMID: 15123742
  39. Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum.
    Science. 2002 Oct 4;298(5591):216-8 PMID: 12364807
  40. Genomic representation of var gene sequences in Plasmodium falciparum field isolates from different geographic regions.
    Mol Biochem Parasitol. 1997 Aug;87(2):235-8 PMID: 9247936
  41. Alterations in local chromatin environment are involved in silencing and activation of subtelomeric var genes in Plasmodium falciparum.
    Mol Microbiol. 2007 Oct;66(1):139-50 PMID: 17725559
  42. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions.
    Malar J. 2003 Sep 10;2:27 PMID: 14565852
  43. Large deletions result from breakage and healing of P. falciparum chromosomes.
    Cell. 1988 Dec 2;55(5):869-74 PMID: 3056622
  44. Expression switching in the stevor and Pfmc-2TM superfamilies in Plasmodium falciparum.
    Mol Microbiol. 2007 Jun;64(6):1621-34 PMID: 17555442
  45. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates.
    BMC Genomics. 2007 Feb 07;8:45 PMID: 17286864
  46. Genetic analysis of the human malaria parasite Plasmodium falciparum.
    Science. 1987 Jun 26;236(4809):1661-6 PMID: 3299700
  47. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria.
    J Exp Med. 2004 Nov 1;200(9):1197-203 PMID: 15520249
  48. Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of antigen production.
    PLoS Pathog. 2006 Mar;2(3):e22 PMID: 16518466
  49. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum.
    Cell. 2005 Apr 8;121(1):13-24 PMID: 15820675
  50. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand.
    Trans R Soc Trop Med Hyg. 1999 Jul-Aug;93(4):369-74 PMID: 10674079
  51. Gene conversion: a mechanism for generation of heterogeneity in the tprK gene of Treponema pallidum during infection.
    Mol Microbiol. 2004 Jun;52(6):1579-96 PMID: 15186410
  52. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes.
    Cell. 1995 Jul 14;82(1):89-100 PMID: 7606788
  53. A genome-wide map of diversity in Plasmodium falciparum.
    Nat Genet. 2007 Jan;39(1):113-9 PMID: 17159979
Article Info
Journal
International journal for parasitology
Abbr.
Int J Parasitol
ISSN
0020-7519
Published
2008-08-00
Epub
2008-00-29
Pages
1099-109
Language
English
Region
England
NLM ID
0314024
PMCID
PMC2441941
Subset
IM
Grants
NIAID NIH HHS · R01 AI052390 · United States
NIAID NIH HHS · T32 AI007613 · United States
NIAID NIH HHS · R01 AI052390-07 · United States
NIAID NIH HHS · AI 54580 · United States
NIAID NIH HHS · AI 07613 · United States
NIAID NIH HHS · R01 AI054580 · United States
NIAID NIH HHS · AI 52390 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]