Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Comparison of allele frequencies of Plasmodium falciparum merozoite antigens in malaria infections sampled in different years in a Kenyan population

Authors: Lynette Isabella Ochola-Oyier, John Okombo, Njoroge Wagatua, Jacob Ochieng, Kevin K. Tetteh, Greg Fegan, Philip Bejon, Kevin Marsh

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

Plasmodium falciparum merozoite antigens elicit antibody responses in malaria-endemic populations, some of which are clinically protective, which is one of the reasons why merozoite antigens are the focus of malaria vaccine development efforts. Polymorphisms in several merozoite antigen-encoding genes are thought to arise as a result of selection by the human immune system.

Methods

The allele frequency distribution of 15 merozoite antigens over a two-year period, 2007 and 2008, was examined in parasites obtained from children with uncomplicated malaria. In the same population, allele frequency changes pre- and post-anti-malarial treatment were also examined. Any gene which showed a significant shift in allele frequencies was also assessed longitudinally in asymptomatic and complicated malaria infections.

Results

Fluctuating allele frequencies were identified in codons 147 and 148 of reticulocyte-binding homologue (Rh) 5, with a shift from HD to YH haplotypes over the two-year period in uncomplicated malaria infections. However, in both the asymptomatic and complicated malaria infections YH was the dominant and stable haplotype over the two-year and ten-year periods, respectively. A logistic regression analysis of all three malaria infection populations between 2007 and 2009 revealed, that the chance of being infected with the HD haplotype decreased with time from 2007 to 2009 and increased in the uncomplicated and asymptomatic infections.

Conclusion

Rh5 codons 147 and 148 showed heterogeneity at both an individual and population level and may be under some degree of immune selection.
Appendix
Available only for authorised users
Literature
1.
go back to reference Garrigan D, Hedrick PW. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution. 2003;57:1707–22.CrossRefPubMed Garrigan D, Hedrick PW. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution. 2003;57:1707–22.CrossRefPubMed
2.
go back to reference Tennessen JA, Blouin MS. Balancing selection at a frog antimicrobial peptide locus: fluctuating immune effector alleles? Mol Biol Evol. 2008;25:2669–80.CrossRefPubMedPubMedCentral Tennessen JA, Blouin MS. Balancing selection at a frog antimicrobial peptide locus: fluctuating immune effector alleles? Mol Biol Evol. 2008;25:2669–80.CrossRefPubMedPubMedCentral
3.
go back to reference Hughes AL. Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Mol Biol Evol. 1992;9:381–93.PubMed Hughes AL. Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Mol Biol Evol. 1992;9:381–93.PubMed
4.
go back to reference Polley SD, Conway DJ. Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics. 2001;158:1505–12.PubMedPubMedCentral Polley SD, Conway DJ. Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics. 2001;158:1505–12.PubMedPubMedCentral
5.
go back to reference Verra F, Chokejindachai W, Weedall GD, Polley SD, Mwangi TW, Marsh K, et al. Contrasting signatures of selection on the Plasmodium falciparum erythrocyte binding antigen gene family. Mol Biochem Parasitol. 2006;149:182–90.CrossRefPubMed Verra F, Chokejindachai W, Weedall GD, Polley SD, Mwangi TW, Marsh K, et al. Contrasting signatures of selection on the Plasmodium falciparum erythrocyte binding antigen gene family. Mol Biochem Parasitol. 2006;149:182–90.CrossRefPubMed
6.
go back to reference Polley SD, Tetteh KKA, Lloyd JM, Akpogheneta OJ, Greenwood BM, Bojang KA, et al. Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J Infect Dis. 2007;195:279–87.CrossRefPubMed Polley SD, Tetteh KKA, Lloyd JM, Akpogheneta OJ, Greenwood BM, Bojang KA, et al. Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J Infect Dis. 2007;195:279–87.CrossRefPubMed
7.
go back to reference Tetteh KKA, Stewart LB, Ochola LI, Amambua-Ngwa A, Thomas AW, Marsh K, et al. Prospective identification of malaria parasite genes under balancing selection. PLoS ONE. 2009;4:e5568.CrossRefPubMedPubMedCentral Tetteh KKA, Stewart LB, Ochola LI, Amambua-Ngwa A, Thomas AW, Marsh K, et al. Prospective identification of malaria parasite genes under balancing selection. PLoS ONE. 2009;4:e5568.CrossRefPubMedPubMedCentral
8.
go back to reference Ochola LI, Tetteh KKA, Stewart LB, Riitho V, Marsh K, Conway DJ. Allele frequency based and polymorphism-versus-divergence indices of balancing selection in a new filtered set of polymorphic genes in Plasmodium falciparum. Mol Biol Evol. 2010;27:2344–51.CrossRefPubMedPubMedCentral Ochola LI, Tetteh KKA, Stewart LB, Riitho V, Marsh K, Conway DJ. Allele frequency based and polymorphism-versus-divergence indices of balancing selection in a new filtered set of polymorphic genes in Plasmodium falciparum. Mol Biol Evol. 2010;27:2344–51.CrossRefPubMedPubMedCentral
9.
go back to reference Rayner JC, Tran TM, Corredor V, Huber CS, Barnwell JW, Galinski MR. Dramatic difference in diversity between Plasmodium falciparum and Plasmodium vivax reticulocyte binding-like genes. Am J Trop Med Hyg. 2005;72:666–74.PubMed Rayner JC, Tran TM, Corredor V, Huber CS, Barnwell JW, Galinski MR. Dramatic difference in diversity between Plasmodium falciparum and Plasmodium vivax reticulocyte binding-like genes. Am J Trop Med Hyg. 2005;72:666–74.PubMed
10.
go back to reference Reiling L, Richards JS, Fowkes FJI, Barry AE, Triglia T, Chokejindachai W, et al. Evidence that the erythrocyte invasion ligand PfRh2 is a target of protective immunity against Plasmodium falciparum malaria. J Immunol. 2010;185:6157–67.CrossRefPubMed Reiling L, Richards JS, Fowkes FJI, Barry AE, Triglia T, Chokejindachai W, et al. Evidence that the erythrocyte invasion ligand PfRh2 is a target of protective immunity against Plasmodium falciparum malaria. J Immunol. 2010;185:6157–67.CrossRefPubMed
11.
go back to reference Osier FH, Weedall GD, Verra F, Murungi L, Tetteh KK, Bull P, et al. Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Infect Immun. 2010;78:4625–33.CrossRefPubMedPubMedCentral Osier FH, Weedall GD, Verra F, Murungi L, Tetteh KK, Bull P, et al. Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Infect Immun. 2010;78:4625–33.CrossRefPubMedPubMedCentral
12.
13.
go back to reference Tham WH, Wilson DW, Reiling L, Chen L, Beeson JG, Cowman AF. Antibodies to reticulocyte binding protein-like homologue 4 inhibit invasion of Plasmodium falciparum into human erythrocytes. Infect Immun. 2009;77:2427–35.CrossRefPubMedPubMedCentral Tham WH, Wilson DW, Reiling L, Chen L, Beeson JG, Cowman AF. Antibodies to reticulocyte binding protein-like homologue 4 inhibit invasion of Plasmodium falciparum into human erythrocytes. Infect Immun. 2009;77:2427–35.CrossRefPubMedPubMedCentral
14.
go back to reference Crewther PE, Matthew ML, Flegg RH, Anders RF. Protective immune responses to apical membrane antigen 1 of Plasmodium chabaudi involve recognition of strain-specific epitopes. Infect Immun. 1996;64:3310–7.PubMedPubMedCentral Crewther PE, Matthew ML, Flegg RH, Anders RF. Protective immune responses to apical membrane antigen 1 of Plasmodium chabaudi involve recognition of strain-specific epitopes. Infect Immun. 1996;64:3310–7.PubMedPubMedCentral
15.
go back to reference Lyon JA, Angov E, Fay MP, Sullivan JS, Girourd AS, Robinson SJ, et al. Protection induced by Plasmodium falciparum MSP1 (42) is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PLoS ONE. 2008;3:e2830.CrossRefPubMedPubMedCentral Lyon JA, Angov E, Fay MP, Sullivan JS, Girourd AS, Robinson SJ, et al. Protection induced by Plasmodium falciparum MSP1 (42) is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PLoS ONE. 2008;3:e2830.CrossRefPubMedPubMedCentral
16.
go back to reference Conway DJ, Greenwood BM, McBride JS. Longitudinal study of Plasmodium falciparum polymorphic antigens in a malaria-endemic population. Infect Immun. 1992;60:1122–7.PubMedPubMedCentral Conway DJ, Greenwood BM, McBride JS. Longitudinal study of Plasmodium falciparum polymorphic antigens in a malaria-endemic population. Infect Immun. 1992;60:1122–7.PubMedPubMedCentral
17.
go back to reference Genton B, Betuela I, Felger I, Al-Yaman F, Anders RF, Saul A, et al. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. J Infect Dis. 2002;185:820–7.CrossRefPubMed Genton B, Betuela I, Felger I, Al-Yaman F, Anders RF, Saul A, et al. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. J Infect Dis. 2002;185:820–7.CrossRefPubMed
18.
go back to reference Healer J, Murphy V, Hodder AN, Masciantonio R, Gemmill AW, Anders RF, et al. Allelic polymorphisms in apical membrane antigen-1 are responsible for evasion of antibody-mediated inhibition in Plasmodium falciparum. Mol Microbiol. 2004;52:159–68.CrossRefPubMed Healer J, Murphy V, Hodder AN, Masciantonio R, Gemmill AW, Anders RF, et al. Allelic polymorphisms in apical membrane antigen-1 are responsible for evasion of antibody-mediated inhibition in Plasmodium falciparum. Mol Microbiol. 2004;52:159–68.CrossRefPubMed
19.
go back to reference Ouattara A, Takala-Harrison S, Thera MA, Coulibaly D, Niangaly A, Saye R, et al. Molecular basis of allele-specific efficacy of a blood-stage malaria vaccine: vaccine development implications. J Infect Dis. 2013;207:511–9.CrossRefPubMedPubMedCentral Ouattara A, Takala-Harrison S, Thera MA, Coulibaly D, Niangaly A, Saye R, et al. Molecular basis of allele-specific efficacy of a blood-stage malaria vaccine: vaccine development implications. J Infect Dis. 2013;207:511–9.CrossRefPubMedPubMedCentral
20.
go back to reference Takahata N, Nei M. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics. 1990;24:967–78. Takahata N, Nei M. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics. 1990;24:967–78.
21.
go back to reference Babiker HA, Satti G, Walliker D. Genetic changes in the population of Plasmodium falciparum in a Sudanese village over a three-year period. Am J Trop Med Hyg. 1995;53:7–15.PubMed Babiker HA, Satti G, Walliker D. Genetic changes in the population of Plasmodium falciparum in a Sudanese village over a three-year period. Am J Trop Med Hyg. 1995;53:7–15.PubMed
22.
go back to reference Ferreira MU, Liu Q, Zhou M, Kimura M, Kaneko O, Van Thien H, et al. Stable patterns of allelic diversity at the merozoite surface protein-1 locus of Plasmodium falciparum in clinical isolates from southern Vietnam. J Eukaryot Microbiol. 1998;45:131–6.CrossRefPubMed Ferreira MU, Liu Q, Zhou M, Kimura M, Kaneko O, Van Thien H, et al. Stable patterns of allelic diversity at the merozoite surface protein-1 locus of Plasmodium falciparum in clinical isolates from southern Vietnam. J Eukaryot Microbiol. 1998;45:131–6.CrossRefPubMed
23.
go back to reference Sallenave-Sales S, Ferreira-da-Cruz MF, Faria CP, Cerruti C Jr, Daniel-Ribeiro CT, Zalis MG. Plasmodium falciparum: limited genetic diversity of MSP-2 in isolates circulating in Brazilian endemic areas. Exp Parasitol. 2003;103:127–35.CrossRefPubMed Sallenave-Sales S, Ferreira-da-Cruz MF, Faria CP, Cerruti C Jr, Daniel-Ribeiro CT, Zalis MG. Plasmodium falciparum: limited genetic diversity of MSP-2 in isolates circulating in Brazilian endemic areas. Exp Parasitol. 2003;103:127–35.CrossRefPubMed
24.
go back to reference Orjuela-Sánchez P, Da Silva-Nunes M, Da Silva NS, Scopel KKG, Gonçalves RM, Malafronte RS, et al. Population dynamics of genetically diverse Plasmodium falciparum lineages: community-based prospective study in rural Amazonia. Parasitology. 2009;136:1097–105.CrossRefPubMedPubMedCentral Orjuela-Sánchez P, Da Silva-Nunes M, Da Silva NS, Scopel KKG, Gonçalves RM, Malafronte RS, et al. Population dynamics of genetically diverse Plasmodium falciparum lineages: community-based prospective study in rural Amazonia. Parasitology. 2009;136:1097–105.CrossRefPubMedPubMedCentral
25.
go back to reference Xangsayarath P, Kaewthamasorn M, Yahata K, Nakazawa S, Sattabongkot J, Udomsangpetch R, et al. Positive diversifying selection on the Plasmodium falciparum surf4.1 gene in Thailand. Trop. Med Health. 2012;40:79–89. Xangsayarath P, Kaewthamasorn M, Yahata K, Nakazawa S, Sattabongkot J, Udomsangpetch R, et al. Positive diversifying selection on the Plasmodium falciparum surf4.1 gene in Thailand. Trop. Med Health. 2012;40:79–89.
26.
go back to reference Kaewthamasorn M, Yahata K, Alexandre JSF, Xangsayarath P, Nakazawa S, Torii M, et al. Stable allele frequency distribution of the polymorphic region of SURFIN(4.2) in Plasmodium falciparum isolates from Thailand. Parasitol Int. 2012;61:317–23.CrossRefPubMed Kaewthamasorn M, Yahata K, Alexandre JSF, Xangsayarath P, Nakazawa S, Torii M, et al. Stable allele frequency distribution of the polymorphic region of SURFIN(4.2) in Plasmodium falciparum isolates from Thailand. Parasitol Int. 2012;61:317–23.CrossRefPubMed
27.
go back to reference Pratt-Riccio LR, Perce-da-Silva Dde S, Lima-Junior JC, Theisen M, Santos F, Daniel-Ribeiro CT, de Oliveira-Ferreira J, Banic DM. Genetic polymorphisms in the glutamate-rich protein of Plasmodium falciparum field isolates from a malaria-endemic area of Brazil. Mem Inst Oswaldo Cruz. 2013;108:523–8.CrossRefPubMedPubMedCentral Pratt-Riccio LR, Perce-da-Silva Dde S, Lima-Junior JC, Theisen M, Santos F, Daniel-Ribeiro CT, de Oliveira-Ferreira J, Banic DM. Genetic polymorphisms in the glutamate-rich protein of Plasmodium falciparum field isolates from a malaria-endemic area of Brazil. Mem Inst Oswaldo Cruz. 2013;108:523–8.CrossRefPubMedPubMedCentral
28.
go back to reference Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature. 1999;400:667–71.CrossRefPubMed Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature. 1999;400:667–71.CrossRefPubMed
29.
go back to reference Tiffin P, Hacker R, Gaut BS. Population genetic evidence for rapid changes in intraspecific diversity and allelic cycling of a specialist defense gene in Zea. Genetics. 2004;168:425–34.CrossRefPubMedPubMedCentral Tiffin P, Hacker R, Gaut BS. Population genetic evidence for rapid changes in intraspecific diversity and allelic cycling of a specialist defense gene in Zea. Genetics. 2004;168:425–34.CrossRefPubMedPubMedCentral
30.
go back to reference Forsyth KP, Anders RF, Cattani JA, Alpers MP. Small area variation in prevalence of an S-antigen serotype of Plasmodium falciparum in villages of Madang, Papua New Guinea. Am J Trop Med Hyg. 1989;40:344–50.PubMed Forsyth KP, Anders RF, Cattani JA, Alpers MP. Small area variation in prevalence of an S-antigen serotype of Plasmodium falciparum in villages of Madang, Papua New Guinea. Am J Trop Med Hyg. 1989;40:344–50.PubMed
31.
go back to reference Eisen DP, Wang L, Jouin H, Murhandarwati EEH, Black CG, Mercereau-Puijalon O, et al. Antibodies elicited in adults by a primary Plasmodium falciparum blood-stage infection recognize different epitopes compared with immune individuals. Malar J. 2007;6:86.CrossRefPubMedPubMedCentral Eisen DP, Wang L, Jouin H, Murhandarwati EEH, Black CG, Mercereau-Puijalon O, et al. Antibodies elicited in adults by a primary Plasmodium falciparum blood-stage infection recognize different epitopes compared with immune individuals. Malar J. 2007;6:86.CrossRefPubMedPubMedCentral
32.
go back to reference Borrmann S, Sasi P, Mwai L, Bashraheil M, Abdallah A, Muriithi S, et al. Declining responsiveness of Plasmodium falciparum infections to artemisinin-based combination treatments on the Kenyan coast. PLoS ONE. 2011;6:e26005.CrossRefPubMedPubMedCentral Borrmann S, Sasi P, Mwai L, Bashraheil M, Abdallah A, Muriithi S, et al. Declining responsiveness of Plasmodium falciparum infections to artemisinin-based combination treatments on the Kenyan coast. PLoS ONE. 2011;6:e26005.CrossRefPubMedPubMedCentral
33.
go back to reference O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, Newton CR, Marsh K. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet. 2008;372:1555–62.CrossRefPubMedPubMedCentral O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, Newton CR, Marsh K. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet. 2008;372:1555–62.CrossRefPubMedPubMedCentral
34.
go back to reference Scott JAG, Bauni E, Moisi JC, Ojal J, Gatakaa H, Nyundo C, et al. Profile: the Kilifi health and demographic surveillance system (KHDSS). Int J Epidemiol. 2012;41:650–7.CrossRefPubMedPubMedCentral Scott JAG, Bauni E, Moisi JC, Ojal J, Gatakaa H, Nyundo C, et al. Profile: the Kilifi health and demographic surveillance system (KHDSS). Int J Epidemiol. 2012;41:650–7.CrossRefPubMedPubMedCentral
35.
go back to reference Bereczky S, Mårtensson A, Gil JP, Färnert A. Rapid DNA extraction from archive blood spots on filter paper for genotyping of Plasmodium falciparum. Am J Trop Med Hyg. 2005;72:249–51.PubMed Bereczky S, Mårtensson A, Gil JP, Färnert A. Rapid DNA extraction from archive blood spots on filter paper for genotyping of Plasmodium falciparum. Am J Trop Med Hyg. 2005;72:249–51.PubMed
37.
go back to reference Marsh K, Forster D, Waruiru C, Mwangi I, Winstanley M, Marsh V, et al. Indicators of life-threatening malaria in African children. N Engl J Med. 1995;332:1399–404.CrossRefPubMed Marsh K, Forster D, Waruiru C, Mwangi I, Winstanley M, Marsh V, et al. Indicators of life-threatening malaria in African children. N Engl J Med. 1995;332:1399–404.CrossRefPubMed
38.
go back to reference Kulldorff M. SaTScan—Software for the spatial, temporal, and space-time scan statistics. Boston: Harvard Medical School and Harvard Pilgrim Health Care; 2010. Kulldorff M. SaTScan—Software for the spatial, temporal, and space-time scan statistics. Boston: Harvard Medical School and Harvard Pilgrim Health Care; 2010.
39.
go back to reference Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, et al. Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med. 2010;7:e1000304.CrossRefPubMedPubMedCentral Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, et al. Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med. 2010;7:e1000304.CrossRefPubMedPubMedCentral
40.
go back to reference Ochola-Oyier LI, Okombo J, Mwai L, Kiara SM, Pole L, Tetteh KK, et al. The MSPDBL2 codon 591 polymorphism is associated with lumefantrine in vitro drug responses in Plasmodium falciparum isolates from Kilifi, Kenya. Antimicrob Agents Chemother. 2015;59:1770–5.CrossRefPubMedPubMedCentral Ochola-Oyier LI, Okombo J, Mwai L, Kiara SM, Pole L, Tetteh KK, et al. The MSPDBL2 codon 591 polymorphism is associated with lumefantrine in vitro drug responses in Plasmodium falciparum isolates from Kilifi, Kenya. Antimicrob Agents Chemother. 2015;59:1770–5.CrossRefPubMedPubMedCentral
41.
go back to reference Lopez-Perez M, Villasis E, Machado RL, Póvoa MM, Vinetz JM, Blair S, et al. Plasmodium falciparum field isolates from South America use an atypical red blood cell invasion pathway associated with invasion ligand polymorphisms. PLoS ONE. 2012;7:e47913.CrossRefPubMedPubMedCentral Lopez-Perez M, Villasis E, Machado RL, Póvoa MM, Vinetz JM, Blair S, et al. Plasmodium falciparum field isolates from South America use an atypical red blood cell invasion pathway associated with invasion ligand polymorphisms. PLoS ONE. 2012;7:e47913.CrossRefPubMedPubMedCentral
42.
go back to reference Jennings CV, Ahouidi AD, Zilversmit M, Bei AK, Rayner J, Sarr O, et al. Molecular analysis of erythrocyte invasion in Plasmodium falciparum isolates from Senegal. Infect Immun. 2007;75:3531–8.CrossRefPubMedPubMedCentral Jennings CV, Ahouidi AD, Zilversmit M, Bei AK, Rayner J, Sarr O, et al. Molecular analysis of erythrocyte invasion in Plasmodium falciparum isolates from Senegal. Infect Immun. 2007;75:3531–8.CrossRefPubMedPubMedCentral
43.
go back to reference Ahouidi AD, Bei AK, Neafsey DE, Sarr O, Volkman S, Milner D, et al. Population genetic analysis of large sequence polymorphisms in Plasmodium falciparum blood-stage antigens. Infect Genet Evol. 2010;10:200–6.CrossRefPubMedPubMedCentral Ahouidi AD, Bei AK, Neafsey DE, Sarr O, Volkman S, Milner D, et al. Population genetic analysis of large sequence polymorphisms in Plasmodium falciparum blood-stage antigens. Infect Genet Evol. 2010;10:200–6.CrossRefPubMedPubMedCentral
44.
go back to reference Bai T, Becker M, Gupta A, Strike P, Murphy VJ, Anders RF, et al. Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. Proc Natl Acad Sci USA. 2005;102:12736–41.CrossRefPubMedPubMedCentral Bai T, Becker M, Gupta A, Strike P, Murphy VJ, Anders RF, et al. Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. Proc Natl Acad Sci USA. 2005;102:12736–41.CrossRefPubMedPubMedCentral
45.
go back to reference Hayton K, Gaur D, Liu A, Takahashi J, Henschen B, Singh S, et al. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe. 2008;4:40–51.CrossRefPubMedPubMedCentral Hayton K, Gaur D, Liu A, Takahashi J, Henschen B, Singh S, et al. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe. 2008;4:40–51.CrossRefPubMedPubMedCentral
46.
go back to reference Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature. 2012;487:375.CrossRefPubMedPubMedCentral Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature. 2012;487:375.CrossRefPubMedPubMedCentral
47.
go back to reference Bustamante LY, Bartholdson SJ, Crosnier C, Campos MG, Wanaguru M, Nguon C, et al. A full-length recombinant Plasmodium falciparum PfRH5 protein induces inhibitory antibodies that are effective across common PfRH5 genetic variants. Vaccine. 2013;31:373–9.CrossRefPubMedPubMedCentral Bustamante LY, Bartholdson SJ, Crosnier C, Campos MG, Wanaguru M, Nguon C, et al. A full-length recombinant Plasmodium falciparum PfRH5 protein induces inhibitory antibodies that are effective across common PfRH5 genetic variants. Vaccine. 2013;31:373–9.CrossRefPubMedPubMedCentral
48.
go back to reference Polley SD, Chokejindachai W, Conway DJ. Allele frequency-based analyses robustly map sequence sites under balancing selection in a malaria vaccine candidate antigen. Genetics. 2003;165:555–61.PubMedPubMedCentral Polley SD, Chokejindachai W, Conway DJ. Allele frequency-based analyses robustly map sequence sites under balancing selection in a malaria vaccine candidate antigen. Genetics. 2003;165:555–61.PubMedPubMedCentral
50.
go back to reference Mwangi TW, Ross A, Snow RW, Marsh K. Case definitions of clinical malaria under different transmission conditions in Kilifi District, Kenya. J Infect Dis. 2005;191:1932–9.CrossRefPubMedPubMedCentral Mwangi TW, Ross A, Snow RW, Marsh K. Case definitions of clinical malaria under different transmission conditions in Kilifi District, Kenya. J Infect Dis. 2005;191:1932–9.CrossRefPubMedPubMedCentral
51.
go back to reference Patel SD, Ahouidi AD, Bei AK, Dieye TN, Mboup S, Harrison SC, et al. Plasmodium falciparum merozoite surface antigen, PfRH5, elicits detectable levels of invasion-inhibiting antibodies in humans. J Infect Dis. 2013;208:1679–81.CrossRefPubMedPubMedCentral Patel SD, Ahouidi AD, Bei AK, Dieye TN, Mboup S, Harrison SC, et al. Plasmodium falciparum merozoite surface antigen, PfRH5, elicits detectable levels of invasion-inhibiting antibodies in humans. J Infect Dis. 2013;208:1679–81.CrossRefPubMedPubMedCentral
52.
go back to reference Wright KE, Hjerrild KA, Bartlett J, Douglas AD, Jin J, Brown RE, et al. Structure of malaria invasion protein RH5 with erythrocyte basigin and blocking antibodies. Nature. 2014;515:427–30.CrossRefPubMedPubMedCentral Wright KE, Hjerrild KA, Bartlett J, Douglas AD, Jin J, Brown RE, et al. Structure of malaria invasion protein RH5 with erythrocyte basigin and blocking antibodies. Nature. 2014;515:427–30.CrossRefPubMedPubMedCentral
53.
go back to reference Douglas AD, Williams AR, Illingworth JJ, Kamuyu G, Biswas S, Goodman AL, et al. The blood-stage malaria antigen PfRH5 is susceptible to vaccine-inducible cross-strain neutralizing antibody. Nat Commun. 2011;2:601.CrossRefPubMedPubMedCentral Douglas AD, Williams AR, Illingworth JJ, Kamuyu G, Biswas S, Goodman AL, et al. The blood-stage malaria antigen PfRH5 is susceptible to vaccine-inducible cross-strain neutralizing antibody. Nat Commun. 2011;2:601.CrossRefPubMedPubMedCentral
54.
go back to reference Tran TM, Ongoiba A, Coursen J, Crosnier C, Diouf A, Huang CY, et al. Naturally acquired antibodies specific for Plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria. J Infect Dis. 2014;209:789–98.CrossRefPubMedPubMedCentral Tran TM, Ongoiba A, Coursen J, Crosnier C, Diouf A, Huang CY, et al. Naturally acquired antibodies specific for Plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria. J Infect Dis. 2014;209:789–98.CrossRefPubMedPubMedCentral
55.
go back to reference Smit-McBride Z, Moya A, Ayala FJ. Linkage disequilibrium in natural and experimental populations of Drosophila melanogaster. Genetics. 1998;120:1043–51. Smit-McBride Z, Moya A, Ayala FJ. Linkage disequilibrium in natural and experimental populations of Drosophila melanogaster. Genetics. 1998;120:1043–51.
56.
go back to reference da Silva J, Coetzer M, Nedellec R, Pastore C, Mosier DE. Fitness epistasis and constraints on adaptation in a human immunodeficiency virus type 1 protein region. Genetics. 2010;85:293–303.CrossRef da Silva J, Coetzer M, Nedellec R, Pastore C, Mosier DE. Fitness epistasis and constraints on adaptation in a human immunodeficiency virus type 1 protein region. Genetics. 2010;85:293–303.CrossRef
57.
go back to reference Baum J, Maier AG, Good RT, Simpson KM, Cowman AF. Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog. 2005;1:e37.CrossRefPubMedPubMedCentral Baum J, Maier AG, Good RT, Simpson KM, Cowman AF. Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog. 2005;1:e37.CrossRefPubMedPubMedCentral
Metadata
Title
Comparison of allele frequencies of Plasmodium falciparum merozoite antigens in malaria infections sampled in different years in a Kenyan population
Authors
Lynette Isabella Ochola-Oyier
John Okombo
Njoroge Wagatua
Jacob Ochieng
Kevin K. Tetteh
Greg Fegan
Philip Bejon
Kevin Marsh
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1304-8

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.