Phylogeography of var gene repertoires reveals fine-scale geospatial clustering of Plasmodium falciparum populations in a highly endemic area

Molecular Ecology

Volumn 24, Issue 2, 2015, Pages 484-497

  Tessema, Sofonias K ^a,b   Monk, Stephanie L ^a,b,f   Schultz, Mark B ^a,b   Tavul, Livingstone ^c   Reeder, John C ^d   Siba, Peter M ^c   Mueller, Ivo ^a,b,e   Barry, Alyssa E ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c PAPUA NEW GUINEA INSTITUTE OF MEDICAL RESEARCH   (Papua New Guinea)

^d BURNET INSTITUTE   (Australia)

^e CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^f MONASH UNIVERSITY   (Australia)

Author keywords

DBL ; genetic diversity; immune evasion; Plasmodium falciparum; population structure; var genes

Indexed keywords

MUGIL; PLASMODIUM FALCIPARUM;

ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; MICROSATELLITE DNA; PROTOZOAL DNA; PROTOZOAL PROTEIN;

ALLELE; BIOLOGICAL MODEL; CLUSTER ANALYSIS; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; MALARIA FALCIPARUM; MOLECULAR GENETICS; PAPUA NEW GUINEA; PARASITOLOGY; PHYLOGEOGRAPHY; PLASMODIUM FALCIPARUM; POPULATION GENETICS;

ALLELES; CLUSTER ANALYSIS; DNA, PROTOZOAN; GENETIC VARIATION; GENETICS, POPULATION; MALARIA, FALCIPARUM; MICROSATELLITE REPEATS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PAPUA NEW GUINEA; PHYLOGEOGRAPHY; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 84920984620     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13033     Document Type: Article

References (65)

1. Albrecht L, Castiñeiras C, Carvalho BO, et al,. (2010) The South American Plasmodium falciparum var gene repertoire is limited, highly shared and possibly lacks several antigenic types. Gene, 453, 37-44.
2. Al-Hamidhi S, Mahdy MA, Idris MA, et al,. (2014) The prospect of malaria elimination in the Arabian Peninsula: a population genetic approach. Infection, Genetics and Evolution, 27C, 25-31.
3. Anderson TJ, Haubold B, Williams JT, et al,. (2000) Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Molecular Biology and Evolution, 17, 1467-1482.
4. Artzy-Randrup Y, Rorick MM, Day K, et al,. (2012) Population structuring of multi-copy, antigen-encoding genes in Plasmodium falciparum. ELife, 1, e00093.
5. Attenborough RD, Alpers MP, (1992) Human Biology in Papua New Guinea: The Small Cosmos. Oxford University Press, Oxford, UK.
6. Avise JC, (2009) Phylogeography: retrospect and prospect. Journal of Biogeography, 36, 3-15.
7. Banu S, Honore N, Saint-Joanis B, et al,. (2002) Are the PE-PGRS proteins of Mycobacterium tuberculosis variable surface antigens? Molecular Microbiology, 44, 9-19.
8. Barry AE, Leliwa-Sytek A, Tavul L, et al,. (2007) Population genomics of the immune evasion (var) genes of Plasmodium falciparum. PLoS Pathogens, 3, e34.
9. Barry AE, Schultz L, Senn N, et al,. (2013) High levels of genetic diversity of Plasmodium falciparum populations in Papua New Guinea despite variable infection prevalence. American Journal of Tropical Medicine and Hygiene, 88, 718-725.
10. Baruch DI, Pasloske BL, Singh HB, et al,. (1995) Cloning the Plasmodium falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell, 82, 77-87.
11. Beeson JG, Chan J-A, Fowkes FJ, (2013) PfEMP1 as a target of human immunity and a vaccine candidate against malaria. Expert Review of Vaccines, 12, 105-108.
12. Bejon P, Turner L, Lavstsen T, et al,. (2011) Serological evidence of discrete spatial clusters of Plasmodium falciparum parasites. PLoS ONE, 6, e21711.
13. Bousema T, Griffin JT, Sauerwein RW, et al,. (2012) Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Medicine, 9, e1001165.
14. Bull PC, Lowe BS, Kortok M, et al,. (1998) Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nature Medicine, 4, 358-360.
15. Bull PC, Kyes S, Buckee CO, et al,. (2007) An approach to classifying sequence tags sampled from Plasmodium falciparum var genes. Molecular and Biochemical Parasitology, 154, 98-102.
16. Bull PC, Buckee CO, Kyes S, et al,. (2008) Plasmodium falciparum antigenic variation. Mapping mosaic var gene sequences onto a network of shared, highly polymorphic sequence blocks. Molecular Microbiology, 68, 1519-1534.
17. Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF, (1988) Human malaria transmission studies in the Anopheles punctulatus Complex in Papua New Guinea-Sporozoite rates, inoculation rates, and sporozoite densities. American Journal of Tropical Medicine and Hygiene, 39, 135-144.
18. Cattani JA, Moir JS, Gibson FD, et al,. (1986) Small-area variations in the epidemiology of malaria in Madang Province. Papua and New Guinea Medical Journal, 29, 11-17.
19. Chao A, (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics, 43, 783-791.
20. Chao A, Chazdon RL, Colwell RK, Shen T-J, (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecology Letters, 8, 148-159.
21. Chen DS, Barry AE, Leliwa-Sytek A, et al,. (2011) A molecular epidemiological study of var gene diversity to characterize the reservoir of Plasmodium falciparum in humans in Africa. PLoS ONE, 6, e16629.
22. Chenet SM, Schneider KA, Villegas L, Escalante AA, (2012) Local population structure of Plasmodium: impact on malaria control and elimination. Malaria Journal, 11, 412.
23. Colwell RK, (2013) EstimateS: Statistical estimation of species richness and shared species from samples: http://purl.oclc.org/estimates.
24. Colwell RK, Chao A, Gotelli NJ, et al,. (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology, 5, 3-21.
25. Cooper RD, Waterson DG, Frances SP, et al,. (2009) Malaria vectors of Papua New Guinea. International Journal for Parasitology, 39, 1495-1501.
26. Cotter C, Sturrock HJW, Hsiang MS, et al,. (2013) The changing epidemiology of malaria elimination: new strategies for new challenges. The Lancet, 382, 900-911.
27. Curry G, Koczberski G, (1998) Migration and Circulation as a way of life for the Wosera Abelam of Papua New Guinea. Asia Pacific Viewpoint, 39, 29-52.
28. Desowitz RS, Spark RA, (1987) Malaria in the Maprik area of the Sepik region, Papua New Guinea: 1957-1984. Transactions of the Royal Society of Tropical Medicine and Hygiene, 81, 175-176.
29. Drummond AJ, Rambaut A, (2007) beast: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
30. Duffy MF, Byrne TJ, Carret C, Ivens A, Brown GV, (2009) Ectopic recombination of a malaria var gene during mitosis associated with an altered var switch rate. Journal of Molecular Biology, 389, 453-469.
31. Edgar RC, (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.
32. Forsyth KP, Anders RF, Cattani JA, Alpers MP, (1989) Small area variation in prevalence of an S-antigen serotype of Plasmodium falciparum in villages of Madang, Papua New Guinea. American Journal of Tropical Medicine and Hygiene, 40, 344-350.
33. Freitas-Junior LH, Bottius E, Pirrit LA, et al,. (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. Falciparum. Nature, 407, 1018-1022.
34. de la Fuente J, Van Den Bussche RA, Garcia-Garcia JC, et al,. (2002) Phylogeography of New World isolates of Anaplasma marginale based on major surface protein sequences. Veterinary Microbiology, 88, 275-285.
35. Gaschen B, Taylor J, Yusim K, et al,. (2002) Diversity considerations in HIV-1 vaccine selection. Science, 296, 2354-2360.
36. Gatei W, Kariuki S, Hawley W, et al,. (2010) Effects of transmission reduction by insecticide-treated bed nets (ITNs) on parasite genetics population structure: I. The genetic diversity of Plasmodium falciparum parasites by microsatellite markers in western Kenya. Malaria Journal, 9, 1-11.
37. Greenwood BM, (1989) The microepidemiology of malaria and its importance to malaria control. Transactions of the Royal Society of Tropical Medicine and Hygiene, 83, 25-29.
38. Hii JLK, Smith T, Mai A, et al,. (1997) Spatial and temporal variation in abundance of Anopheles (Diptera: Culicidae) in a malaria endemic area in Papua New Guinea. Journal of Medical Entomology, 34, 193-205.
39. Holmes EC, (2004) The phylogeography of human viruses. Molecular Ecology, 13, 745-756.
40. Kariuki SK, Njunge J, Muia A, et al,. (2013) Effect of malaria transmission reduction by insecticide-treated bed nets (ITNs) on the genetic diversity of Plasmodium falciparum merozoite surface protein (MSP-1) and circumsporozoite (CSP) in western Kenya. Malaria Journal, 12, 1-10.
41. Kasehagen LJ, Mueller I, McNamara DT, et al,. (2006) Changing patterns of Plasmodium blood-stage infections in the Wosera region of Papua New Guinea monitored by light microscopy and high throughput PCR diagnosis. American Journal of Tropical Medicine and Hygiene, 75, 588-596.
42. Khaireh BA, Assefa A, Guessod HH, et al,. (2013) Population genetics analysis during the elimination process of Plasmodium falciparum in Djibouti. Malaria Journal, 12, 201.
43. Kirkman LA, Deitsch KW, (2012) Antigenic variation and the generation of diversity in malaria parasites. Current Opinion in Microbiology, 15, 456-462.
44. Kraemer SM, Smith JD, (2003) Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. Molecular Microbiology, 50, 1527-1538.
45. Kyes SA, Kraemer SM, Smith JD, (2007) Antigenic variation in Plasmodium falciparum: gene organization and regulation of the var multigene family. Eukaryotic Cell, 6, 1511-1520.
46. Larremore DB, Clauset A, Buckee CO, (2013) A network approach to analyzing highly recombinant malaria parasite genes. PLoS Computational Biology, 9, e1003268.
47. Lavstsen T, Salanti A, Jensen AT, Arnot DE, Theander TG, (2003) Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malaria Journal, 2, 1-14.
48. Lum JK, Kaneko A, Tanabe K, et al,. (2004) Malaria dispersal among islands: human mediated Plasmodium falciparum gene flow in Vanuatu, Melanesia. Acta Tropica, 90, 181-185.
49. Madang Division of Education (2009) Ten Year Provincial Educational Plan 2009-2018. Madang Provincial Adminstration, Division of Education, Madang, Papua New Guinea.
50. Mbogo CM, Mwangangi JM, Nzovu J, et al,. (2003) Spatial and temporal heterogeneity of anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. American Journal of Tropical Medicine and Hygiene, 68, 734-742.
51. Mueller I, Schoepflin S, Smith TA, et al,. (2012) Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proceedings of the National Academy of Sciences, USA, 109, 10030-10035.
52. Muller I, Bockarie M, Alpers M, Smith T, (2003) The epidemiology of malaria in Papua New Guinea. Trends in Parasitology, 19, 253-259.
53. Patel SS, King CL, Mgone CS, Kazura JW, Zimmerman PA, (2004) Glycophorin C (Gerbich antigen blood group) and band 3 polymorphisms in two malaria holoendemic regions of Papua New Guinea. American Journal of Hematology, 75, 1-5.
54. Peters W, (1960) Studies on the epidemiology of malaria in New Guinea. Part I. Holoendemic malaria: the clinical picture. Transactions of the Royal Society of Tropical Medicine and Hygiene, 54, 242-249.
55. 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.
56. Salanti A, Staalsoe T, Lavstsen T, et al,. (2003) Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Molecular Microbiology, 49, 179-191.
57. Sander AF, Lavstsen T, Rask TS, et al. (2014) DNA secondary structures are associated with recombination in major Plasmodium falciparum variable surface antigen gene families. Nucleic Acids Research, 42, 2270-2281.
58. Schultz L, Wapling J, Mueller I, et al,. (2010) Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malaria Journal, 9, 1-13.
59. Smith JD, Chitnis CE, Craig AG, et al,. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell, 82, 101-110.
60. Smith JD, Kyes S, Craig AG, et al,. (1998) Analysis of adhesive domains from the A4VAR Plasmodium falciparum erythrocyte membrane protein-1 identifies a CD36 binding domain. Molecular and Biochemical Parasitology, 97, 133-148.
61. Su XZ, Heatwole VM, Wertheimer SP, et al,. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell, 82, 89-100.
62. Talarico S, Zhang LX, Marrs CF, et al,. (2008) Mycobacterium tuberculosis PE-PGRS16 and PE-PGRS26 genetic polymorphism among clinical isolates. Tuberculosis (Edinb), 88, 283-294.
63. Tanabe K, Mita T, Jombart T, et al,. (2010) Plasmodium falciparum accompanied the human expansion out of Africa. Current Biology, 20, 1283-1288.
64. Wallace RG, Fitch WM, (2008) Influenza A H5N1 immigration is filtered out at some international borders. PLoS ONE, 3, 1-11.
65. WHO (2013) World Malaria Report 2013. 284.