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Quantification of Plasmodium falciparum malaria from complex infections in the Peruvian Amazon using quantitative PCR of the merozoite surface protein 1, block 2 (PfMSP1-B2): in vitro dynamics reveal density-dependent interactions

Published online by Cambridge University Press:  20 February 2012

THOMAS M. ZERVOS ,
JEAN N. HERNANDEZ ,
PATRICK L. SUTTON  and
ORALEE H. BRANCH
THOMAS M. ZERVOS
Affiliation:
Department of Medical Parasitology, New York University School of Medicine, 341 E 25th St, OPH, New York, NY 10010, USA
JEAN N. HERNANDEZ
Affiliation:
Universidad Nacional de la Amazonia Peruana, Laboratorio de Investigaciones Productos Naturales Anti-Parasitarios, Iquitos, Peru
PATRICK L. SUTTON
Affiliation:
Department of Medical Parasitology, New York University School of Medicine, 341 E 25th St, OPH, New York, NY 10010, USA
ORALEE H. BRANCH*
Affiliation:
Department of Medical Parasitology, New York University School of Medicine, 341 E 25th St, OPH, New York, NY 10010, USA
*
*Corresponding author: Department of Medical Parasitology, New York University School of Medicine, 341 E 25th St, OPH, New York, NY 10010, USA. Tel: +011 212 263 4364. Fax: +011 212 263 8116. E-mail: OraLee.Branch@nyumc.org
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Summary

The majority of Plasmodium falciparum field isolates are defined as complex infections because they contain multiple genetically distinct clones. Studying interactions between clones in complex infections in vivo and in vitro could elucidate important phenomena in malaria infection, transmission and treatment. Using quantitative PCR (qPCR) of the P. falciparum merozoite surface protein 1, block 2 (PfMSP1-B2), we provide a sensitive and efficient genotyping method. This is important for epidemiological studies because it makes it possible to study genotype-specific growth dynamics. We compared 3 PfMSP1-B2 genotyping methods by analysing 79 field isolates from the Peruvian Amazon. In vivo observations from other studies using these techniques led to the hypothesis that clones within complex infections interact. By co-culturing clones with different PfMSP1-B2 genotypes, and measuring parasitaemia using qPCR, we found that suppression of clonal expansion was a factor of the collective density of all clones present in a culture. PfMSP1-B2 qPCR enabled us to find in vitro evidence for parasite-parasite interactions and could facilitate future investigations of growth trends in naturally occurring complex infections.

Keywords

Plasmodium falciparummerozoite surface protein 1block 2quantitative PCRdensity regulation
Type
Research Article
Information
Parasitology , Volume 139 , Issue 6 , May 2012 , pp. 701 - 708
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Bei, A. K., Membi, C. D., Rayner, J. C., Mubi, M., Ngasala, B., Sultan, A. A., Premji, Z. and Duraisingh, M. T. (2007). Variant merozoite protein expression is associated with erythrocyte invasion phenotypes in Plasmodium falciparum isolates from Tanzania. Molecular and Biochemical Parasitology 153, 66–71. doi: S0166-6851(07)00034-5 [pii] 10.1016/j.molbiopara.2007.01.007.CrossRefGoogle ScholarPubMed
Bell, A. S., de Roode, J. C., Sim, D. and Read, A. F. (2006). Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 1358–1371.Google ScholarPubMed
Branch, O. H., Casapia, M. W., Gamboa, D. V., Hernandez, J. N., Alava, F. F., Roncal, N., Alvarez, E., Perez, E. J. and Gotuzzo, E. (2005). Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in recently emerged, hypoendemic Peruvian Amazon community. Malaria Journal 4(27), 1–16.CrossRefGoogle ScholarPubMed
Branch, O. H., Sutton, P. L., Barnes, C., Castro, J. C., Hussin, J., Awadalla, P. and Hijar, G. (2011). Plasmodium falciparum genetic diversity maintained and amplified over 5 years of a low transmission endemic in the Peruvian Amazon. Molecular Biology and Evolution 28, 1973–1986.CrossRefGoogle ScholarPubMed
Branch, O. H., Takala, S., Kariuki, S., Nahlen, I. B., Kolczak, M. K. and Lal, A. A. (2001). Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infection and Immunity 69, 7783–7792.CrossRefGoogle ScholarPubMed
Bremermann, H. J. and Pickering, J. (1983). A game-theoretical model of parasite virulence. Journal of Theoretical Biology 100, 411–426. doi: 0022-5193(83)90438-1.CrossRefGoogle ScholarPubMed
Bruce, M. C., Galinski, M. R., Barnwell, J. W., Donnelly, C. A., Walmsley, M., Alpers, M. P., Walliker, D. and 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.CrossRefGoogle ScholarPubMed
Certa, U., Rotmann, D., Matile, H. and Reber-Liske, R. (1987). A naturally occurring gene encoding the major surface antigen precursor p190 of Plasmodium falciparum lacks tripeptide repeats. EMBO Journal 6, 4137–4142.CrossRefGoogle ScholarPubMed
Cheesman, S. J., de Roode, J. C., Read, A. F. and Carter, R. (2003). Real-time quantitative PCR for analysis of genetically mixed infections of malaria parasites: technique validation and applications. Molecular and Biochemical Parasitology 131, 83–91.CrossRefGoogle ScholarPubMed
Chenet, S. M., Branch, O. H., Escalante, A. A., Lucas, C. M. and Bacon, D. J. (2008). Genetic diversity of vaccine candidate antigens in Plasmodium falciparum isolates from the Amazon basin of Peru. Malaria Journal 27, 1–11. doi: 10.1186/1475-2875-7-93Google Scholar
Colborn, J. M., Koita, O. A., Cisse, O., Bagayoko, M. W., Guthrie, E. J. and Krogstad, D. J. (2006). Identifying and quantifying genotypes in polyclonal infections due to single species. Emerging Infectious Diseases 12, 475–482.CrossRefGoogle ScholarPubMed
de Roode, J. C., Culleton, R., Bell, A. S. and Read, A. F. (2004). Competitive release of drug resistance following drug treatment of mixed Plasmodium chabaudi infections. Malaria Journal 3, 1–6. doi: 10.1186/1475-2875-3-33CrossRefGoogle ScholarPubMed
de Roode, J. C., Pansini, R., Cheesman, S. J., Helinski, M. E., Huijben, S., Wargo, A. R., Bell, A. S., Chan, B. H., Walliker, D. and Read, A. F. (2005). Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences, USA 102, 7624–7628. doi: 0500078102 [pii] 10.1073/pnas.0500078102.CrossRefGoogle ScholarPubMed
Dyer, M. and Day, K. P. (2003). Regulation of the rate of asexual growth and commitment to sexual development by diffusible factors from in vitro cultures of Plasmodium falciparum. The American Journal of Tropical Medicine and Hygiene 68, 403–409.CrossRefGoogle ScholarPubMed
Falk, N., Maire, N., Sama, W., Owusu-Agyei, , Smith, T., Beck, Hans-Peter. and Felger, I. (2006). Comparison of PCR-RFLP and Genescan-based genotyping for analyzing infection dynamics of Plasmodium falciparum. The American Journal of Tropical Medicine and Hygiene 74, 944–950.CrossRefGoogle ScholarPubMed
Farnert, A., Arez, A. P., Babiker, H. A., Beck, H. P., Benito, A., Bjorkman, A., Bruce, M. C., Conway, D. J., Day, K. P., Henning, L., Mercereau-Puijalon, O., Ranford-Cartwright, L. C., Rubio, J. M., Snounou, G., Walliker, D., Zwetyenga, J. and do Rosario, V. E. (2001). Genotyping of Plasmodium falciparum infections by PCR: a comparative multicentre study. Transactions of the Royal Society of Tropical Medicine and Hygiene 95(2), 225–232.CrossRefGoogle ScholarPubMed
Farnert, A., Lebbad, M., Faraja, L. and Rooth, I. (2008). Extensive dynamics of Plasmodium falciparum densities, stages and genotyping profiles. Malaria Journal 7, 1–5. doi: 1475-2875-7-241 [pii] 10.1186/1475-2875-7-241.CrossRefGoogle ScholarPubMed
Goodyer, I. D., Johnson, J., Eisenthal, R. and Hayes, D. J. (1994). Purification of mature-stage Plasmodium falciparum by gelatine flotation. Annals of Tropical Medicine and Parasitology 88, 209–211.CrossRefGoogle ScholarPubMed
Harrington, W. E., Mutabingwa, T. K., Muehlenbachs, A., Sorensen, B., Bolla, M. C., Fried, M. and Duffy, P. E. (2009). Competitive facilitation of drug-resistant Plasmodium falciparum malaria parasites in pregnant women who receive preventive treatment. Proceedings of the National Academy of Sciences, USA 106, 9027–9032. doi: 0901415106 [pii] 10.1073/pnas.0901415106.CrossRefGoogle ScholarPubMed
Hellriegel, B. (1992). Modelling the immune response to malaria with ecological concepts: short-term behaviour against long-term equilibrium. Proceedings of the Royal Societyof London, B 250, 249–256. doi: 10.1098/rspb.1992.0156.Google ScholarPubMed
Huijben, S., Sim, D. G., Nelson, W. A. and Read, A. F. (2011). The fitness of drug-resistant malaria parasites in a rodent model: multiplicity of infection. Journal of Evolutionary Biology 24, 2410–2422. doi: 10.1111/j.1420-9101.2011.02369.x.CrossRefGoogle Scholar
Lambros, C. and Vanderberg, J. P. (1979). Synchronization of Plasmodium falciparum erythrocytic stages in culture. The Journal of Parasitology 65, 418–420.CrossRefGoogle ScholarPubMed
Liljander, A., Bejon, P., Mwacharo, J., Kai, O., Ogada, E., Peshu, N., Marsh, K. and Farnert, A. (2011). Clearance of asymptomatic P. falciparum Infections Interacts with the number of clones to predict the risk of subsequent malaria in Kenyan children. PLoS One 6, e16940. doi: 10.1371/journal.pone.0016940.CrossRefGoogle ScholarPubMed
Liljander, A., Wiklund, L., Falk, N., Kweku, M., Martensson, A., Felger, I. and Farnert, A. (2009). Optimization and validation of multi-coloured capillary electrophoresis for genotyping of Plasmodium falciparum merozoite surface proteins (msp1 and 2). Malaria Journal 8, 1–14. doi: 1475-2875-8-78 [pii] 10.1186/1475-2875-8-78.CrossRefGoogle ScholarPubMed
McBride, J. S. and Heidrich, H. G. (1987). Fragments of the polymorphic Mr 185,000 glycoprotein from the surface of isolated Plasmodium falciparum merozoites form an antigenic complex. Molecular and Biochemical Parasitology 23, 71–84. doi: 0166-6851(87)90189-7.CrossRefGoogle Scholar
Mosquera, J. and Adler, F. R. (1998). Evolution of virulence: a unified framework for COInfection and superinfection. Journal of Theoretical Biology 195, 293–313. doi: S0022-5193(98)90793-7 [pii] 10.1006/jtbi.1998.0793.CrossRefGoogle ScholarPubMed
Mutai, B. K. and Waitumbi, J. N. (2010). Apoptosis stalks Plasmodium falciparum maintained in continuous culture condition. Malaria Journal 9 (Suppl. 3) 1–9. doi: 1475-2875-9-S3-S6 [pii] 10.1186/1475-2875-9-S3-S6.CrossRefGoogle ScholarPubMed
Orjuela-Sanchez, P., Da Silva-Nunes, M., Da Silva, N. S., Scopel, K. K., Goncalves, R. M., Malafronte, R. S. and Ferreira, M. U. (2009). Population dynamics of genetically diverse Plasmodium falciparum lineages: community-based prospective study in rural Amazonia. Parasitology 136, 1097–1105. doi: 10.1017/S0031182009990539.CrossRefGoogle ScholarPubMed
Robert, F., Ntoumi, F., Angel, G., Candito, D., Rogier, C., Fandeur, T., Sarthou, J. L. and Mercereau-Puijalon, O. (1996). Extensive genetic diversity of Plasmodium falciparum isolates collected from patients with severe malaria in Dakar, Senegal. Transactions of the Royal Society of Tropical Medicine and Hygiene 190, 704–711.CrossRefGoogle Scholar
Sutton, P. L., Clark, E. H., Silva, C. and Branch, O. H. (2010). The Plasmodium falciparum merozoite surface protein-1 19 KD antibody response in the Peruvian Amazon predominantly targets the non-allele specific, shared sites of this antigen. Malaria Journal 9, 1–11. doi: 1475-2875-9-3 [pii]10.1186/1475-2875-9-3CrossRefGoogle Scholar
Sutton, P. L., Neyra, V., Hernandez, J. N. and Branch, O. H. (2009). Plasmodium falciparum and Plasmodium vivax infections in the Peruvian Amazon: propagation of complex, multiple allele-type infections without super-infection. The American Journal of Tropical Medicine and Hygiene 81, 950–960. doi: 81/6/950 [pii] 10.4269/ajtmh.2009.09-0132.CrossRefGoogle ScholarPubMed
Smith, T., Felger, I., Kitua, A., Tanner, M. and Beck, H. P. (1999). Dynamics of multiple Plasmodium falciparum infections in infants in a highly endemic area of Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene, 93 (Suppl 1), 35–39.CrossRefGoogle Scholar
Tanabe, K., Mackay, M., Goman, M. and Scaife, J. G. (1987). Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum. Journal of Molecular Biology 195, 273–287.CrossRefGoogle Scholar
Tang, J., Hu, M., Lee, S. and Roblin, R. (2000). A polymerase chain reaction based method for detecting Mycoplasma/Acholeplasma contaminants in cell culture. Journal of Microbiological Methods 39, 121–126. doi: S0167-7012(99)00107-4.CrossRefGoogle ScholarPubMed
Taylor, L. H., Walliker, D. and Read, A. F. (1997). Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proceedings of the Royal Society of London, B 264, 927–935. doi: 10.1098/rspb.1997.0128.CrossRefGoogle ScholarPubMed
Torres, K. J., Clark, E. H., Hernandez, J. N., Soto-Cornejo, K. E., Gamboa, D. and Branch, O. H. (2008). Antibody response dynamics to the Plasmodium falciparum conserved vaccine candidate antigen, merozoite surface protein-1 C-terminal 19kD (MSP1–19kD), in Peruvians exposed to hypoendemic malaria transmission. Malaria Journal 7, 1–11. doi: 1475-2875-7-173 [pii] 10.1186/1475-2875-7-173.CrossRefGoogle Scholar
Trager, W. and Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–675.CrossRefGoogle ScholarPubMed
Trager, W. and Jensen, J. B. (1997). Continuous culture of Plasmodium falciparum: its impact on malaria research. International Journal for Parasitology 27, 989–1006. doi: S0020751997000805.CrossRefGoogle ScholarPubMed