Close kinship within multiple-genotype malaria parasite infections

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1738, 2012, Pages 2589-2598

  Nkhoma, Standwell C ^a,b   Nair, Shalini ^a   Cheeseman, Ian H ^a   Rohr Allegrini, Cherise ^c   Singlam, Sittaporn ^d   Nosten, François ^d,e   Anderson, Tim J C ^a  

^a SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^b UNIVERSITY OF MALAWI   (Malawi)

^c TEXAS DEPARTMENT OF STATE HEALTH SERVICES   (United States)

^d SHOKLO MALARIA RESEARCH UNIT   (Thailand)

^e MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Dilution cloning; Inbreeding; Multiple clone infection; Plasmodium falciparum; Relatedness

Indexed keywords

PLASMODIUM FALCIPARUM;

ANIMAL; ARTICLE; CLASSIFICATION; DISEASE TRANSMISSION; GENE FREQUENCY; GENETICS; GENOTYPE; HAPLOTYPE; HUMAN; ISOLATION AND PURIFICATION; MALARIA FALCIPARUM; MALAWI; MIXED INFECTION; PARASITOLOGY; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; SPOROZOITE; THAILAND;

ANIMALS; CHILD, PRESCHOOL; COINFECTION; GENE FREQUENCY; GENOTYPE; HAPLOTYPES; HUMANS; MALARIA, FALCIPARUM; MALAWI; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SPOROZOITES; THAILAND;

EID: 84987722638     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.0113     Document Type: Article

References (50)

1. Anderson, T. J. et al. 2000 Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol. Biol. Evol. 17, 1467–1482.
2. Arnot, D. E. 2002 The influence of the genetic complexity of Plasmodium falciparum infections on the epidemiology of malaria. Trans. R. Soc. Trop. Med. Hyg. 96(Suppl. 1), S131–S136. (doi:10.1016/S0035-9203(02)90064-7)
3. Magesa, S. M., Mdira, K. Y., Babiker, H. A., Alifrangis, M., Farnert, A., Simonsen, P. E., Bygbjerg, I. C., Walliker, D. & Jakobsen, P. H. 2002 Diversity of Plasmodium falciparum clones infecting children living in a holoendemic area in north-eastern Tanzania. Acta Trop. 84, 83–92. (doi:10.1016/S0001-706X(02)00179-1)
4. Vafa, M., Troye-Blomberg, M., Anchang, J., Garcia, A. & Migot-Nabias, F. 2008 Multiplicity of Plasmodium falciparum infection in asymptomatic children in Senegal: relation to transmission, age and erythrocyte variants. Malar. J. 7, 17. (doi:10.1186/1475-2875-7-17)
5. Ford, A. F. & Schall, J. J. 2011 Relative clonal proportions over time in mixed-genotype infections of the lizard malaria parasite Plasmodium mexicanum. Int. J. Parasitol. 41, 731–738. (doi:10.1016/j.ijpara.2011.01.010)
6. Lee, K. S., Divis, P. C., Zakaria, S. K., Matusop, A., Julin, R. A., Conway, D. J., Cox-Singh, J. & Singh, B. 2011 Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Pathogens 7, e1002015. (doi:10.1371/journal.ppat.1002015)
7. de Roode, J. C. et al. 2005 Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl Acad. Sci. USA 102, 7624–7628. (doi:10.1073/ pnas.0500078102)
8. Wargo, A. R., Huijben, S., de Roode, J. C., Shepherd, J. & Read, A. F. 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. (doi:10.1073/pnas.0707766104)
9. Antao, T. & Hastings, I. M. 2011 Environmental, pharmacological and genetic influences on the spread of drug-resistant malaria. Proc. R. Soc. B 278, 1705–1712. (doi:10.1098/rspb.2010.1907)
10. Reece, S. E., Drew, D. R. & Gardner, A. 2008 Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453, 609–614. (doi:10.1038/nature06954)
11. Read, A. F. & Taylor, L. H. 2001 The ecology of genetically diverse infections. Science 292, 1099–1102. (doi:10.1126/science.1059410)
12. Hill, W. G. & Babiker, H. A. 1995 Estimation of numbers of malaria clones in blood samples. Proc. R. Soc. Lond. B 262, 249–257. (doi:10.1098/rspb.1995.0203)
13. Rosenberg, R., Wirtz, R. A., Schneider, I. & Burge, R. 1990 An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Trans.R.Soc.Trop.Med.Hyg.84, 209–212. (doi:10.1016/0035-9203(90)90258-G)
14. Beier, J. C. 1998 Malaria parasite development in mosquitoes. Annu. Rev. Entomol. 43, 519–543. (doi:10.1146/annurev.ento.43.1.519)
15. Read, A. F., Day, T. & Huijben, S. 2011 The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy. Proc. Natl Acad. Sci. USA 108(Suppl. 2), 10871–10877. (doi:10.1073/pnas.1100299108)
16. Juliano, J. J., Porter, K., Mwapasa, V., Sem, R., Rogers, W. O., Ariey, F., Wongsrichanalai, C., Read, A. & Meshnick, S. R. 2010 Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing. Proc. Natl Acad. Sci. USA 107, 20138–20143. (doi:10.1073/pnas.1007068107)
17. Druilhe, P., Daubersies, P., Patarapotikul, J., Gentil, C., Chene, L., Chongsuphajaisiddhi, T., Mellouk, S. & Langsley, G. 1998 A primary malarial infection is composed of a very wide range of genetically diverse but related parasites. J. Clin. Invest. 101, 2008–2016. (doi:10.1172/JCI119890)
18. Conway, D. J., Greenwood, B. M. & McBride, J. S. 1991 The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology 103, 1–6. (doi:10.1017/S0031182000059217)
19. Sutton, P. L., Neyra, V., Hernandez, J. N. & Branch, O. H. 2009 Plasmodium falciparum and Plasmodium vivax infections in the Peruvian Amazon: propagation of complex, multiple allele-type infections without super-infection. Am. J. Trop. Med. Hyg. 81, 950–960. (doi:10.4269/ajtmh.2009.09-0132)
20. Mzilahowa, T., McCall, P. J. & Hastings, I. M. 2007 ‘Sexual’ population structure and genetics of the malaria agent P. falciparum. PLoS ONE 2, e613. (doi:10.1371/journal.pone.0000613)
21. Kazembe, L. N., Kleinschmidt, I., Holtz, T. H. & Sharp, B. L. 2006 Spatial analysis and mapping of malaria risk in Malawi using point-referenced prevalence of infection data. Int. J. Health. Geogr. 5, 41. (doi:10.1186/1476-072X-5-41)
22. Luxemburger, C., Thwai, K. L., White, N. J., Webster, H. K., Kyle, D. E., Maelankirri, L., Chongsuphajaisiddhi, T. & Nosten, F. 1996 The epidemiology of malaria in a Karen population on the western border of Thailand. Trans. R. Soc. Trop. Med. Hyg. 90, 105–111. (doi:10.1016/S0035-9203(96)90102-9)
23. Anderson, T. J., Su, X. Z., Bockarie, M., Lagog, M. & Day, K. P. 1999 Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology 119, 113–125. (doi:10.1017/S0031182099004552)
24. Brockman, A., Paul, R. E., Anderson, T. J., Hackford, I., Phaiphun, L., Looareesuwan, S., Nosten, F. & Day, K. P. 1999 Application of genetic markers to the identification of recrudescent Plasmodium falciparum infections on the northwestern border of Thailand. Am. J. Trop. Med. Hyg. 60, 14–21.
25. Makler, M. T., Ries, J. M., Williams, J. A., Bancroft, J. E., Piper, R. C., Gibbins, B. L. & Hinrichs, D. J. 1993 Parasite lactate dehydrogenase as an assay for Plasmodium falciparum drug sensitivity. Am. J. Trop. Med. Hyg. 48, 739–741.
26. Anderson, T. J., Williams, J. T., Nair, S., Sudimack, D., Barends, M., Jaidee, A., Price, R. N. & Nosten, F. 2010 Inferred relatedness and heritability in malaria parasites. Proc. R. Soc. B 277, 2531–2540. (doi:10.1098/rspb.2010.0196)
27. Recker, M., Buckee, C. O., Serazin, A., Kyes, S., Pinches, R., Christodoulou, Z., Springer, A. L., Gupta, S. & Newbold, C. I. 2011 Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern. PLoS Pathogens 7, e1001306. (doi:10.1371/journal.ppat.1001306)
28. Daubersies, P., Sallenave-Sales, S., Magne, S., Trape, J. F., Contamin, H., Fandeur, T., Rogier, C., Mercereau-Puijalon, O. & Druilhe, P. 1996 Rapid turnover of Plasmodium falciparum populations in asymptomatic individuals living in a high transmission area. Am. J. Trop. Med. Hyg. 54, 18–26.
29. Bruce, M. C., Galinski, M. R., Barnwell, J. W., Donnelly, C. A., Walmsley, M., Alpers, M. P., Walliker, D. & Day, K. P. 2000 Genetic diversity and dynamics of Plasmodium falciparum and P. vivax populations in multiply infected children with asymptomatic malaria infections in Papua New Guinea. Parasitology 121, 257–272. (doi:10.1017/ S0031182099006356)
30. Farnert, A. 2008 Plasmodium falciparum population dynamics: only snapshots in time? Trends Parasitol. 24, 340–344. (doi:10.1016/j.pt.2008.04.008)
31. Contamin, H., Fandeur, T., Rogier, C., Bonnefoy, S., Konate, L., Trape, J. F. & Mercereau-Puijalon, O. 1996 Different genetic characteristics of Plasmodium falciparum isolates collected during successive clinical malaria episodes in Senegalese children. Am. J. Trop. Med. Hyg. 54, 632–643.
32. Kun, J. F., Missinou, M. A., Lell, B., Sovric, M., Knoop, H., Bojowald, B., Dangelmaier, O. & Kremsner, P. G. 2002 New emerging Plasmodium falciparum genotypes in children during the transition phase from asymptomatic parasitemia to malaria. Am. J. Trop. Med. Hyg. 66, 653–658.
33. Portugal, S. et al. 2011 Host-mediated regulation of superinfection in malaria. Nat. Med. 17, 732–737. (doi:10.1038/nm.2368)
34. Mayor, A., Saute, F., Aponte, J. J., Almeda, J., Gomez-Olive, F. X., Dgedge, M. & Alonso, P. L. 2003 Plasmodium falciparum multiple infections in Mozambique, its relation to other malariological indices and to prospective risk of malaria morbidity. Trop. Med. Int. Health 8, 3–11. (doi:10.1046/j.1365-3156.2003.00968.x)
35. Prugnolle, F., Durand, P., Jacob, K., Razakandrainibe, F., Arnathau, C., Villarreal, D., Rousset, F., de Meeus, T. & Renaud, F. 2008 A comparison of Anopheles gambiae and Plasmodium falciparum genetic structure over space and time. Microbes Infect. 10, 269–275. (doi:10.1016/j. micinf.2007.12.021)
36. Broman, K. W. 2005 The genomes of recombinant inbred lines. Genetics 169, 1133–1146. (doi:10.1534/genetics.104.035212)
37. Walliker, D., Quakyi, I. A., Wellems, T. E., McCutchan, T. F., Szarfman, A., London, W. T., Corcoran, L. M., Burkot, T. R. & Carter, R. 1987 Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236, 1661–1666. (doi:10.1126/science.3299700)
38. Walker-Jonah, A., Dolan, S. A., Gwadz, R. W., Panton, L. J. & Wellems, T. E. 1992 An RFLP map of the Plasmodium falciparum genome, recombination rates and favored linkage groups in a genetic cross. Mol. Biochem. Parasitol. 51, 313–320. (doi:10.1016/0166-6851(92) 90081-T)
39. Freitas-Junior, L. H., Bottius, E., Pirrit, L. A., Deitsch, K. W., Scheidig, C., Guinet, F., Nehrbass, U., Wellems, T. E. & Scherf, A. 2000 Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407, 1018–1022. (doi:10.1038/35039531)
40. Hill, W. G., Babiker, H. A., Ranford-Cartwright, L. C. & Walliker, D. 1995 Estimation of inbreeding coefficients from genotypic data on multiple alleles, and application to estimation of clonality in malaria parasites. Genet. Res. 65, 53–61. (doi:10.1017/S0016672300033000)
41. Hastings, I. M., Nsanzabana, C. & Smith, T. A. 2010 A comparison of methods to detect and quantify the markers of antimalarial drug resistance. Am. J. Trop. Med. Hyg. 83, 489–495. (doi:10.4269/ajtmh.2010.10-0072)
42. Huijben, S., Sim, D. G., Nelson, W. A. & Read, A. F. 2011 The fitness of drug-resistant malaria parasites in a rodent model: multiplicity of infection. J. Evol. Biol. 24, 2410–2422. (doi:10.1111/j.1420-9101.2011.02369.x)
43. Buckling, A. & Brockhurst, M. A. 2008 Kin selection and the evolution of virulence. Heredity 100, 484–488. (doi:10.1038/sj.hdy.6801093)
44. Vardo-Zalik, A. M. & Schall, J. J. 2008 Clonal diversity within infections and the virulence of a malaria parasite, Plasmodium mexicanum. Parasitology 135, 1363–1372. (doi:10.1017/S0031182008004964)
45. West, S. A., Reece, S. E. & Read, A. F. 2001 Evolution of gametocyte sex ratios in malaria and related api-complexan (protozoan) parasites. Trends Parasitol. 17, 525–531. (doi:10.1016/S1471-4922(01)02058-X)
46. Bell, A. S., de Roode, J. C., Sim, D. & Read, A. F. 2006 Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 1358–1371. (doi:10.1554/05-611.1)
47. Conway, D. J. 2007 Molecular epidemiology of malaria. Clin. Microbiol. Rev. 20, 188–204. (doi:10.1128/CMR. 00021-06)
48. Annan, Z. et al. 2007 Population genetic structure of Plasmodium falciparum in the two main African vectors, Anopheles gambiae and Anopheles funestus. Proc. Natl Acad. Sci. USA 104, 7987–7992. (doi:10.1073/pnas.0702715104)
49. Anderson, T., Nkhoma, S., Ecker, A. & Fidock, D. 2011 How can we identify parasite genes that underlie antimalarial drug resistance? Pharmacogenomics 12, 59–85. (doi:10.2217/pgs.10.165)
50. Riehle, M. M. et al. 2006 Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312, 577–579. (doi:10.1126/science.1124153)