Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 46, 2010, Pages 20138-20143

  Juliano, Jonathan J ^a   Porter, Kimberly ^b   Mwapasa, Victor ^c   Sem, Rithy ^d   Rogers, William O ^e   Ariey, Frédéric ^f   Wongsrichanaiai, Chansuda ^e   Read, Andrew ^g,h   Meshnick, Steven R ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c UNIVERSITY OF MALAWI   (Malawi)

^d National Center for Parasitology Entomology and Malaria Control   (Cambodia)

^e Naval Medical Research Unit 2 Pacific   (United States)

^f INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

^g PENNSYLVANIA STATE UNIVERSITY   (United States)

^h NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Next generation sequencing; Plasmodium falciparum

Indexed keywords

MSP1 PROTEIN; MSP2 PROTEIN; PROTOZOAL PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ANTIMALARIAL DRUG RESISTANCE; CLINICAL ARTICLE; CONFERENCE PAPER; ECOLOGY; ENDEMIC DISEASE; FEMALE; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HOST; HUMAN; MALARIA FALCIPARUM; MASSIVELY PARALLEL PYROSEQUENCING; MICROBIAL DIVERSITY; MIXED INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PYROSEQUENCING; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALIA; PLASMODIUM FALCIPARUM;

EID: 78650529458     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1007068107     Document Type: Article

References (50)

1. World Health Organization (2008) World Malaria Report 2008 (World Health Organization, Geneva).
2. Bell AS, de Roode JC, Sim D, Read AF (2006) Within-host competition in genetically diverse malaria infections: Parasite virulence and competitive success. Evolution 60: 1358-1371.
3. Liu S, Mu J, Jiang H, Su XZ (2008) Effects of Plasmodium falciparum mixed infections on in vitro antimalarial drug tests and genotyping. Am J Trop Med Hyg 79:178-184.
4. Mideo N, et al. (2008) Understanding and predicting strain-specific patterns of pathogenesis in the rodent malaria Plasmodium chabaudi. Am Nat 172:214-238.
5. Wargo AR, Huijben S, de Roode JC, Shepherd J, Read AF (2007) Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc Natl Acad Sci USA 104:19914-19919.
6. Hastings IM (2003) Malaria control and the evolution of drug resistance: an intriguing link. Trends Parasitol 19:70-73.
7. Hastings IM, D'Alessandro U (2000) Modelling a predictable disaster: The rise and spread of drug-resistantmalaria. Parasitol Today 16:340-347.
8. Huijben S, et al. (2010) Chemotherapy, within-host ecology and fitness of drug resistant malaria parasites. Evolution, 10.1111/j.1558-5646.2010.01068.x.
9. Talisuna AO, Okello PE, Erhart A, Coosemans M, D'Alessandro U (2007) Intensity of malaria transmission and the spread of Plasmodium falciparum resistant malaria: A review of epidemiologic field evidence. Am J Trop Med Hyg 77(6 suppl)170-180.
10. Juliano JJ, et al. (2009) Misclassification of drug failure in Plasmodium falciparum clinical trials in southeast Asia. J Infect Dis 200:624-628.
11. Greenhouse B, et al. (2006) Validation of microsatellite markers for use in genotyping polyclonal Plasmodium falciparum infections. Am J Trop Med Hyg 75:836-842.
12. Kwiek JJ, et al. (2007) Estimating true antimalarial efficacy by heteroduplex tracking assay in patients with complex Plasmodium falciparum infections. Antimicrob Agents Chemother 51:521-527.
13. Juliano JJ, Gadalla N, Sutherland CJ, Meshnick SR (2010) The perils of PCR: Can we accurately 'correct' antimalarial trials? Trends Parasitol 26:119-124.
14. Juliano JJ, Taylor SM, Meshnick SR (2009) Polymerase chain reaction adjustment in antimalarial trials: Molecular malarkey? J Infect Dis 200:5-7.
15. World Health Organization (2008) Methods and Techniques for Clinical Trials on Antimalarial Drug Efficacy: Genotyping to Identify Parasite Populations (World Health Organization, Geneva).
16. Juliano JJ, Kwiek JJ, Cappell K, Mwapasa V, Meshnick SR (2007) Minority-variant pfcrt K76T mutations and chloroquine resistance, Malawi. Emerg Infect Dis 13:872-877.
17. Hastings IM, Nsanzabana C, Smith TA (2010) A comparison of methods to detect and quantify the markers of antimalarial drug resistance. Am J Trop Med Hyg 83:489-495.
18. Tanabe K, et al. (2002) In vitro recombination during PCR of Plasmodium falciparum DNA: A potential pitfall in molecular population genetic analysis. Mol Biochem Parasitol 122:211-216.
19. Ferreira MU, et al. (1998) Allelic diversity at the merozoite surface protein-1 locus of Plasmodium falciparum in clinical isolates from the southwestern Brazilian Amazon. Am J Trop Med Hyg 59:474-480.
20. Ngrenngarmlert W, et al. (2005) Measuring allelic heterogeneity in Plasmodium falciparum by a heteroduplex tracking assay. Am J Trop Med Hyg 72:694-701.
21. Felger I, et al. (1997) Sequence diversity and molecular evolution of the merozoite surface antigen 2 of Plasmodium falciparum. J Mol Evol 45:154-160.
22. Huse SM, Huber JA, Morrison HG, Sogin ML, Welch DM (2007) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8:R143.
23. Magurran AE (2004) Measuring Biological Diversity (Blackwell Science, Malden, MA).
24. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379-391.
25. Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating and comparing incidence based species accumulation curves. Ecology 85:2717-2727.
26. Chao A (1989) Estimating population size for sparse data in capture-recapture experiments. Biometrics 45:427-438.
27. Snounou G, Beck HP (1998) The use of PCR genotyping in the assessment of recrudescence or reinfection after antimalarial drug treatment. Parasitol Today 14:462-467.
28. Day KP, Koella JC, Nee S, Gupta S, Read AF (1992) Population genetics and dynamics of Plasmodium falciparum: An ecological view. Parasitology 104(suppl):S35-S52.
29. Read AF, Taylor LH (2001) The ecology of genetically diverse infections. Science 292: 1099-1102.
30. Bruce MC, et al. (2000) Cross-species interactions between malaria parasites in humans. Science 287:845-848.
31. Daubersies P, et al. (1996) Rapid turnover of Plasmodium falciparum populations in asymptomatic individuals living in a high transmission area. Am J Trop Med Hyg 54:18-26.
32. Mercereau-Puijalon O (1996) Revisiting host/parasite interactions: molecular analysis of parasites collected during longitudinal and cross-sectional surveys in humans. Parasite Immunol 18:173-180.
33. Talisuna AO, et al. (2004) Two mutations in dihydrofolate reductase combined with one in the dihydropteroate synthase gene predict sulphadoxine-pyrimethamine parasitological failure in Ugandan children with uncomplicated falciparum malaria. Infect Genet Evol 4:321-327.
34. Harrington WE, et al. (2009) Competitive facilitation of drug-resistant Plasmodium falciparum malaria parasites in pregnant women who receive preventive treatment. Proc Natl Acad Sci USA 106:9027-9032.
35. Hoffmann C, et al. (2007) DNA bar coding and pyrosequencing to identify rare HIV drug resistance mutations. Nucleic Acids Res 35:e91.
36. Wang C, Mitsuya Y, Gharizadeh B, Ronaghi M, Shafer RW (2007) Characterization of mutation spectra with ultra-deep pyrosequencing: Application to HIV-1 drug resistance. Genome Res 17:1195-1201.
37. Rozera G,et al. (2009) Massively parallel pyrosequencing highlights minority variantsin the HIV-1 envquasispecies deriving from lymphomonocyte sub-populations. Retrovirology 6:15.
38. Mitsuya Y, et al. (2008) Minority human immunodeficiency virus type 1 variants in antiretroviral-naive persons with reverse transcriptase codon 215 revertant mutations. J Virol 82:10747-10755.
39. Archer J, et al. (2009) Detection of low-frequency pretherapy chemokine (CXC motif) receptor 4 (CXCR4)-using HIV-1 with ultra-deep pyrosequencing. Aids 23:1209-1218.
40. Rogers WO, et al. (2009) Failure of artesunate-mefloquine combination therapy for uncomplicated Plasmodium falciparum malaria in southern Cambodia. Malar J 8:10.
41. Mayengue PI, et al. (2004) Submicroscopic Plasmodium falciparum infections and multiplicity of infection in matched peripheral, placental and umbilical cord blood samples from Gabonese women. Trop Med Int Health 9:949-958.
42. Lahr DJ, Katz LA (2009) Reducing the impact of PCR-mediated recombination in molecular evolution and environmental studies using a new-generation high-fidelity DNA polymerase. Biotechniques 47:857-866.
43. Kaneko O, Kimura M, Kawamoto F, Ferreira MU, Tanabe K (1997) Plasmodium falciparum: Allelic variation in the merozoite surface protein 1 gene in wild isolates from southern Vietnam. Exp Parasitol 86:45-57.
44. Williams R, et al. (2006) Amplification of complex gene libraries by emulsion PCR. Nat Methods 3:545-550.
45. Schoepflin S, et al. (2009) Comparison of Plasmodium falciparum allelic frequency distribution in different endemic settings by high-resolution genotyping. Malar J 8:250.
46. Hook EB, Regal RR (1995) Capture-recapture methods in epidemiology: methods and limitations. Epidemiol Rev 17:243-264.
47. Kalilani L, et al. (2007) A randomized controlled pilot trial of azithromycin or artesunate added to sulfadoxine-pyrimethamine as treatment for malaria in pregnant women. PLoS ONE 2:e1166.
48. Tsibris AM, et al. (2009) Quantitative deep sequencing reveals dynamic HIV-1 escape and large population shifts during CCR5 antagonist therapy in vivo. PLoSONE 4:e5683.
49. Keating KA, Quinn JF (1998) Estimating species richness: The Michaelis-Menten model revisited. Oikos 81:411-416.
50. Wei SG, et al. (2010) Comparative performance of species-richness estimators using data from a subtropical forest tree community. Ecol Res 25:93-101.