Skip to main content
Top
Published in: Malaria Journal 1/2014

Open Access 01-12-2014 | Research

Distinct patterns of diversity, population structure and evolution in the AMA1 genes of sympatric Plasmodium falciparum and Plasmodium vivax populations of Papua New Guinea from an area of similarly high transmission

Authors: Alicia Arnott, Johanna Wapling, Ivo Mueller, Paul A Ramsland, Peter M Siba, John C Reeder, Alyssa E Barry

Published in: Malaria Journal | Issue 1/2014

Login to get access

Abstract

Background

As Plasmodium falciparum and Plasmodium vivax co-exist in most malaria-endemic regions outside sub-Saharan Africa, malaria control strategies in these areas must target both species in order to succeed. Population genetic analyses can predict the effectiveness of interventions including vaccines, by providing insight into patterns of diversity and evolution. The aim of this study was to investigate the population genetics of leading malaria vaccine candidate AMA1 in sympatric P. falciparum and P. vivax populations of Papua New Guinea (PNG), an area of similarly high prevalence (Pf = 22.3 to 38.8%, Pv = 15.3 to 31.8%).

Methods

A total of 72 Pfama1 and 102 Pvama1 sequences were collected from two distinct areas, Madang and Wosera, on the highly endemic PNG north coast.

Results

Despite a greater number of polymorphic sites in the AMA1 genes of P. falciparum (Madang = 52; Wosera = 56) compared to P. vivax (Madang = 36, Wosera = 34), the number of AMA1 haplotypes, haplotype diversity (Hd) and recombination (R) was far lower for P. falciparum (Madang = 12, Wosera = 20; Hd ≤0.92, R ≤45.8) than for P. vivax (Madang = 50, Wosera = 38; Hd = 0.99, R = ≤70.9). Balancing selection was detected only within domain I of AMA1 for P. vivax, and in both domains I and III for P. falciparum.

Conclusions

Higher diversity in the genes encoding P. vivax AMA1 than in P. falciparum AMA1 in this highly endemic area has important implications for development of AMA1-based vaccines in PNG and beyond. These results also suggest a smaller effective population size of P. falciparum compared to P. vivax, a finding that warrants further investigation. Differing patterns of selection on the AMA1 genes indicate that critical antigenic sites may differ between the species, highlighting the need for independent investigations of these two leading vaccine candidates.
Appendix
Available only for authorised users
Literature
1.
go back to reference Genton B, D'Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Muller I: Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med. 2008, 5: e127-PubMedCentralCrossRefPubMed Genton B, D'Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Muller I: Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med. 2008, 5: e127-PubMedCentralCrossRefPubMed
2.
go back to reference Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM: Vivax malaria: neglected and not benign. Am J Trop Med Hyg. 2007, 77: 79-87.PubMedCentralPubMed Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM: Vivax malaria: neglected and not benign. Am J Trop Med Hyg. 2007, 77: 79-87.PubMedCentralPubMed
3.
go back to reference Barcus MJ, Basri H, Picarima H, Manyakori C, Sekartuti , Elyazar I, Bangs MJ, Maguire JD, Baird JK: Demographic risk factors for severe and fatal vivax and falciparum malaria among hospital admissions in northeastern Indonesian Papua. Am J Trop Med Hyg. 2007, 77: 984-991.PubMed Barcus MJ, Basri H, Picarima H, Manyakori C, Sekartuti , Elyazar I, Bangs MJ, Maguire JD, Baird JK: Demographic risk factors for severe and fatal vivax and falciparum malaria among hospital admissions in northeastern Indonesian Papua. Am J Trop Med Hyg. 2007, 77: 984-991.PubMed
4.
go back to reference Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, Karyana M, Lampah DA, Price RN: Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua. Indonesia PLoS Med. 2008, 5: e128-CrossRefPubMed Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, Karyana M, Lampah DA, Price RN: Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua. Indonesia PLoS Med. 2008, 5: e128-CrossRefPubMed
5.
go back to reference Guerra CA, Howes RE, Patil AP, Gething PW, Van Boeckel TP, Temperley WH, Kabaria CW, Tatem AJ, Manh BH, Elyazar IR, Baird JK, Snow RW, Hay SI: The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl Trop Dis. 2010, 4: e774-PubMedCentralCrossRefPubMed Guerra CA, Howes RE, Patil AP, Gething PW, Van Boeckel TP, Temperley WH, Kabaria CW, Tatem AJ, Manh BH, Elyazar IR, Baird JK, Snow RW, Hay SI: The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl Trop Dis. 2010, 4: e774-PubMedCentralCrossRefPubMed
6.
go back to reference Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, Gueye CS, Fullman N, Gosling RD, Feachem RG: The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet. 2013, 382: 900-911.CrossRefPubMed Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, Gueye CS, Fullman N, Gosling RD, Feachem RG: The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet. 2013, 382: 900-911.CrossRefPubMed
8.
go back to reference Neafsey DE, Galinsky K, Jiang RH, Young L, Sykes SM, Saif S, Gujja S, Goldberg JM, Young S, Zeng Q, Chapman SB, Dash AP, Anvikar AR, Sutton PL, Birren BW, Escalante AA, Barnwell JW, Carlton JM: The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat Genet. 2012, 44: 1046-1050.PubMedCentralCrossRefPubMed Neafsey DE, Galinsky K, Jiang RH, Young L, Sykes SM, Saif S, Gujja S, Goldberg JM, Young S, Zeng Q, Chapman SB, Dash AP, Anvikar AR, Sutton PL, Birren BW, Escalante AA, Barnwell JW, Carlton JM: The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat Genet. 2012, 44: 1046-1050.PubMedCentralCrossRefPubMed
9.
go back to reference Khim N, Benedet C, Kim S, Kheng S, Siv S, Leang R, Lek S, Muth S, Chea N, Chuor CM, Duong S, Kerleguer A, Tor P, Chim P, Canier L, Witkowski B, Taylor WR, Menard D: G6PD deficiency in Plasmodium falciparum and Plasmodium vivax malaria-infected Cambodian patients. Malar J. 2013, 12: 171-PubMedCentralCrossRefPubMed Khim N, Benedet C, Kim S, Kheng S, Siv S, Leang R, Lek S, Muth S, Chea N, Chuor CM, Duong S, Kerleguer A, Tor P, Chim P, Canier L, Witkowski B, Taylor WR, Menard D: G6PD deficiency in Plasmodium falciparum and Plasmodium vivax malaria-infected Cambodian patients. Malar J. 2013, 12: 171-PubMedCentralCrossRefPubMed
10.
go back to reference Orjuela-Sanchez P, Sa JM, Brandi MC, Rodrigues PT, Bastos MS, Amaratunga C, Duong S, Fairhurst RM, Ferreira MU: Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, Western Cambodia. Exp Parasitol. 2013, 134: 318-326.PubMedCentralCrossRefPubMed Orjuela-Sanchez P, Sa JM, Brandi MC, Rodrigues PT, Bastos MS, Amaratunga C, Duong S, Fairhurst RM, Ferreira MU: Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, Western Cambodia. Exp Parasitol. 2013, 134: 318-326.PubMedCentralCrossRefPubMed
11.
go back to reference Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, Escalante AA, Ouattara A, Traore K, Niangaly A, Djimde AA, Doumbo OK, Plowe CV: Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci Transl Med. 2009, 1: 2ra5-PubMedCentralCrossRefPubMed Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, Escalante AA, Ouattara A, Traore K, Niangaly A, Djimde AA, Doumbo OK, Plowe CV: Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci Transl Med. 2009, 1: 2ra5-PubMedCentralCrossRefPubMed
12.
go back to reference Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP: Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000, 17: 1467-1482.CrossRefPubMed Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP: Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000, 17: 1467-1482.CrossRefPubMed
13.
go back to reference Tanabe K, Mita T, Jombart T, Eriksson A, Horibe S, Palacpac N, Ranford-Cartwright L, Sawai H, Sakihama N, Ohmae H, Nakamura M, Ferreira MU, Escalante AA, Prugnolle F, Bjorkman A, Farnert A, Kaneko A, Horii T, Manica A, Kishino H, Balloux F: Plasmodium falciparum accompanied the human expansion out of Africa. Curr Biol. 2010, 20: 1283-1289.CrossRefPubMed Tanabe K, Mita T, Jombart T, Eriksson A, Horibe S, Palacpac N, Ranford-Cartwright L, Sawai H, Sakihama N, Ohmae H, Nakamura M, Ferreira MU, Escalante AA, Prugnolle F, Bjorkman A, Farnert A, Kaneko A, Horii T, Manica A, Kishino H, Balloux F: Plasmodium falciparum accompanied the human expansion out of Africa. Curr Biol. 2010, 20: 1283-1289.CrossRefPubMed
14.
go back to reference Ferreira MU, Karunaweera ND, da Silva-Nunes M, da Silva NS, Wirth DF, Hartl DL: Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. J Infect Dis. 2007, 195: 1218-1226.CrossRefPubMed Ferreira MU, Karunaweera ND, da Silva-Nunes M, da Silva NS, Wirth DF, Hartl DL: Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. J Infect Dis. 2007, 195: 1218-1226.CrossRefPubMed
15.
go back to reference Imwong M, Nair S, Pukrittayakamee S, Sudimack D, Williams JT, Mayxay M, Newton PN, Kim JR, Nandy A, Osorio L, Carlton JM, White NJ, Day NP, Anderson TJ: Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int J Parasitol. 2007, 37: 1013-1022.CrossRefPubMed Imwong M, Nair S, Pukrittayakamee S, Sudimack D, Williams JT, Mayxay M, Newton PN, Kim JR, Nandy A, Osorio L, Carlton JM, White NJ, Day NP, Anderson TJ: Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int J Parasitol. 2007, 37: 1013-1022.CrossRefPubMed
16.
go back to reference Taylor JE, Pacheco MA, Bacon DJ, Beg MA, Machado RL, Fairhurst RM, Herrera S, Kim JY, Menard D, Povoa MM, Villegas L, Mulyanto , Snounou G, Cui L, Zeyrek FY, Escalante AA: The evolutionary history of Plasmodium vivax as inferred from mitochondrial genomes: parasite genetic diversity in the Americas. Mol Biol Evol. 2013, 30: 2050-2064.PubMedCentralCrossRefPubMed Taylor JE, Pacheco MA, Bacon DJ, Beg MA, Machado RL, Fairhurst RM, Herrera S, Kim JY, Menard D, Povoa MM, Villegas L, Mulyanto , Snounou G, Cui L, Zeyrek FY, Escalante AA: The evolutionary history of Plasmodium vivax as inferred from mitochondrial genomes: parasite genetic diversity in the Americas. Mol Biol Evol. 2013, 30: 2050-2064.PubMedCentralCrossRefPubMed
17.
go back to reference Prugnolle F, Rougeron V, Becquart P, Berry A, Makanga B, Rahola N, Arnathau C, Ngoubangoye B, Menard S, Willaume E, Ayala FJ, Fontenille D, Ollomo B, Durand P, Paupy C, Renaud F: Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc Natl Acad Sci USA. 2013, 110: 8123-8128.PubMedCentralCrossRefPubMed Prugnolle F, Rougeron V, Becquart P, Berry A, Makanga B, Rahola N, Arnathau C, Ngoubangoye B, Menard S, Willaume E, Ayala FJ, Fontenille D, Ollomo B, Durand P, Paupy C, Renaud F: Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc Natl Acad Sci USA. 2013, 110: 8123-8128.PubMedCentralCrossRefPubMed
18.
go back to reference Liu W, Li Y, Shaw KS, Learn GH, Plenderleith LJ, Malenke JA, Sundararaman SA, Ramirez MA, Crystal PA, Smith AG, Bibollet-Ruche F, Ayouba A, Locatelli S, Esteban A, Mouacha F, Guichet E, Butel C, Ahuka-Mundeke S, Inogwabini BI, Ndjango JB, Speede S, Sanz CM, Morgan DB, Gonder MK, Kranzusch PJ, Walsh PD, Georgiev AV, Muller MN, Piel AK, Stewart FA: African origin of the malaria parasite Plasmodium vivax. Nat Commun. 2014, 5: 3346-PubMedCentralPubMed Liu W, Li Y, Shaw KS, Learn GH, Plenderleith LJ, Malenke JA, Sundararaman SA, Ramirez MA, Crystal PA, Smith AG, Bibollet-Ruche F, Ayouba A, Locatelli S, Esteban A, Mouacha F, Guichet E, Butel C, Ahuka-Mundeke S, Inogwabini BI, Ndjango JB, Speede S, Sanz CM, Morgan DB, Gonder MK, Kranzusch PJ, Walsh PD, Georgiev AV, Muller MN, Piel AK, Stewart FA: African origin of the malaria parasite Plasmodium vivax. Nat Commun. 2014, 5: 3346-PubMedCentralPubMed
19.
go back to reference Arnott A, Barry AE, Reeder JC: Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Malar J. 2012, 11: 14-PubMedCentralCrossRefPubMed Arnott A, Barry AE, Reeder JC: Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Malar J. 2012, 11: 14-PubMedCentralCrossRefPubMed
20.
21.
go back to reference Barry AE, Schultz L, Buckee CO, Reeder JC: Contrasting population structures of the genes encoding ten leading vaccine-candidate antigens of the human malaria parasite, Plasmodium falciparum. PLoS One. 2009, 4: e8497-PubMedCentralCrossRefPubMed Barry AE, Schultz L, Buckee CO, Reeder JC: Contrasting population structures of the genes encoding ten leading vaccine-candidate antigens of the human malaria parasite, Plasmodium falciparum. PLoS One. 2009, 4: e8497-PubMedCentralCrossRefPubMed
22.
go back to reference Takala SL, Plowe CV: Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming 'vaccine resistant malaria'. Parasite Immunol. 2009, 31: 560-573.PubMedCentralCrossRefPubMed Takala SL, Plowe CV: Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming 'vaccine resistant malaria'. Parasite Immunol. 2009, 31: 560-573.PubMedCentralCrossRefPubMed
23.
go back to reference Arevalo-Herrera M, Chitnis C, Herrera S: Current status of Plasmodium vivax vaccine. Hum Vaccin. 2010, 6: 124-132.CrossRefPubMed Arevalo-Herrera M, Chitnis C, Herrera S: Current status of Plasmodium vivax vaccine. Hum Vaccin. 2010, 6: 124-132.CrossRefPubMed
24.
go back to reference Pacheco MA, Poe AC, Collins WE, Lal AA, Tanabe K, Kariuki SK, Udhayakumar V, Escalante AA: A comparative study of the genetic diversity of the 42kDa fragment of the merozoite surface protein 1 in Plasmodium falciparum and P. vivax. Infect Genet Evol. 2007, 7: 180-187.PubMedCentralCrossRefPubMed Pacheco MA, Poe AC, Collins WE, Lal AA, Tanabe K, Kariuki SK, Udhayakumar V, Escalante AA: A comparative study of the genetic diversity of the 42kDa fragment of the merozoite surface protein 1 in Plasmodium falciparum and P. vivax. Infect Genet Evol. 2007, 7: 180-187.PubMedCentralCrossRefPubMed
25.
go back to reference Chenet SM, Pacheco MA, Bacon DJ, Collins WE, Barnwell JW, Escalante AA: The evolution and diversity of a low complexity vaccine candidate, merozoite surface protein 9 (MSP-9), in Plasmodium vivax and closely related species. Infect Genet Evol. 2013, 20: 239-248.PubMedCentralCrossRefPubMed Chenet SM, Pacheco MA, Bacon DJ, Collins WE, Barnwell JW, Escalante AA: The evolution and diversity of a low complexity vaccine candidate, merozoite surface protein 9 (MSP-9), in Plasmodium vivax and closely related species. Infect Genet Evol. 2013, 20: 239-248.PubMedCentralCrossRefPubMed
26.
go back to reference Remarque EJ, Faber BW, Kocken CH, Thomas AW: Apical membrane antigen 1: a malaria vaccine candidate in review. Trends Parasitol. 2008, 24: 74-84.CrossRefPubMed Remarque EJ, Faber BW, Kocken CH, Thomas AW: Apical membrane antigen 1: a malaria vaccine candidate in review. Trends Parasitol. 2008, 24: 74-84.CrossRefPubMed
27.
go back to reference Gentil F, Bargieri DY, Leite JA, Francoso KS, Patricio MB, Espindola NM, Vaz AJ, Palatnik-de-Sousa CB, Rodrigues MM, Costa FT, Soares IS: A recombinant vaccine based on domain II of Plasmodium vivax Apical Membrane Antigen 1 induces high antibody titres in mice. Vaccine. 2010, 28: 6183-6190.CrossRefPubMed Gentil F, Bargieri DY, Leite JA, Francoso KS, Patricio MB, Espindola NM, Vaz AJ, Palatnik-de-Sousa CB, Rodrigues MM, Costa FT, Soares IS: A recombinant vaccine based on domain II of Plasmodium vivax Apical Membrane Antigen 1 induces high antibody titres in mice. Vaccine. 2010, 28: 6183-6190.CrossRefPubMed
28.
go back to reference Moon SU, Na BK, Kang JM, Kim JY, Cho SH, Park YK, Sohn WM, Lin K, Kim TS: Genetic polymorphism and effect of natural selection at domain I of apical membrane antigen-1 (AMA-1) in Plasmodium vivax isolates from Myanmar. Acta Trop. 2010, 114: 71-75.CrossRefPubMed Moon SU, Na BK, Kang JM, Kim JY, Cho SH, Park YK, Sohn WM, Lin K, Kim TS: Genetic polymorphism and effect of natural selection at domain I of apical membrane antigen-1 (AMA-1) in Plasmodium vivax isolates from Myanmar. Acta Trop. 2010, 114: 71-75.CrossRefPubMed
29.
go back to reference Mardani A, Keshavarz H, Heidari A, Hajjaran H, Raeisi A, Khorramizadeh MR: Genetic diversity and natural selection at the domain I of apical membrane antigen-1 (AMA-1) of Plasmodium falciparum in isolates from Iran. Exp Parasitol. 2012, 130: 456-462.CrossRefPubMed Mardani A, Keshavarz H, Heidari A, Hajjaran H, Raeisi A, Khorramizadeh MR: Genetic diversity and natural selection at the domain I of apical membrane antigen-1 (AMA-1) of Plasmodium falciparum in isolates from Iran. Exp Parasitol. 2012, 130: 456-462.CrossRefPubMed
31.
go back to reference Sheehy SH, Duncan CJ, Elias SC, Biswas S, Collins KA, O'Hara GA, Halstead FD, Ewer KJ, Mahungu T, Spencer AJ, Miura K, Poulton ID, Dicks MD, Edwards NJ, Berrie E, Moyle S, Colloca S, Cortese R, Gantlett K, Long CA, Lawrie AM, Gilbert SC, Doherty T, Nicosia A, Hill AV, Draper SJ: Phase Ia clinical evaluation of the safety and immunogenicity of the Plasmodium falciparum blood-stage antigen AMA1 in ChAd63 and MVA vaccine vectors. PLoS One. 2012, 7: e31208-PubMedCentralCrossRefPubMed Sheehy SH, Duncan CJ, Elias SC, Biswas S, Collins KA, O'Hara GA, Halstead FD, Ewer KJ, Mahungu T, Spencer AJ, Miura K, Poulton ID, Dicks MD, Edwards NJ, Berrie E, Moyle S, Colloca S, Cortese R, Gantlett K, Long CA, Lawrie AM, Gilbert SC, Doherty T, Nicosia A, Hill AV, Draper SJ: Phase Ia clinical evaluation of the safety and immunogenicity of the Plasmodium falciparum blood-stage antigen AMA1 in ChAd63 and MVA vaccine vectors. PLoS One. 2012, 7: e31208-PubMedCentralCrossRefPubMed
32.
go back to reference Biswas S, Dicks MD, Long CA, Remarque EJ, Siani L, Colloca S, Cottingham MG, Holder AA, Gilbert SC, Hill AV, Draper SJ: Transgene optimization, immunogenicity and in vitro efficacy of viral vectored vaccines expressing two alleles of Plasmodium falciparum AMA1. PLoS One. 2011, 6: e20977-PubMedCentralCrossRefPubMed Biswas S, Dicks MD, Long CA, Remarque EJ, Siani L, Colloca S, Cottingham MG, Holder AA, Gilbert SC, Hill AV, Draper SJ: Transgene optimization, immunogenicity and in vitro efficacy of viral vectored vaccines expressing two alleles of Plasmodium falciparum AMA1. PLoS One. 2011, 6: e20977-PubMedCentralCrossRefPubMed
33.
go back to reference Bai T, Becker M, Gupta A, Strike P, Murphy VJ, Anders RF, Batchelor AH: Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. Proc Natl Acad Sci USA. 2005, 102: 12736-12741.PubMedCentralCrossRefPubMed Bai T, Becker M, Gupta A, Strike P, Murphy VJ, Anders RF, Batchelor AH: Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. Proc Natl Acad Sci USA. 2005, 102: 12736-12741.PubMedCentralCrossRefPubMed
34.
go back to reference Yap A, Azevedo MF, Gilson PR, Weiss GE, O'Neill MT, Wilson DW, Crabb BS, Cowman AF: Conditional expression of apical membrane antigen 1 in Plasmodium falciparum shows it is required for erythrocyte invasion by merozoites. Cell Microbiol. 2014, 16: 642-656.PubMedCentralCrossRefPubMed Yap A, Azevedo MF, Gilson PR, Weiss GE, O'Neill MT, Wilson DW, Crabb BS, Cowman AF: Conditional expression of apical membrane antigen 1 in Plasmodium falciparum shows it is required for erythrocyte invasion by merozoites. Cell Microbiol. 2014, 16: 642-656.PubMedCentralCrossRefPubMed
35.
go back to reference Cortes A, Mellombo M, Mueller I, Benet A, Reeder JC, Anders RF: Geographical structure of diversity and differences between symptomatic and asymptomatic infections for Plasmodium falciparum vaccine candidate AMA1. Infect Immun. 2003, 71: 1416-1426.PubMedCentralCrossRefPubMed Cortes A, Mellombo M, Mueller I, Benet A, Reeder JC, Anders RF: Geographical structure of diversity and differences between symptomatic and asymptomatic infections for Plasmodium falciparum vaccine candidate AMA1. Infect Immun. 2003, 71: 1416-1426.PubMedCentralCrossRefPubMed
36.
go back to reference Osier FH, Weedall GD, Verra F, Murungi L, Tetteh KK, Bull P, Faber BW, Remarque E, Thomas A, Marsh K, Conway DJ: Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Infect Immun. 2010, 78: 4625-4633.PubMedCentralCrossRefPubMed Osier FH, Weedall GD, Verra F, Murungi L, Tetteh KK, Bull P, Faber BW, Remarque E, Thomas A, Marsh K, Conway DJ: Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Infect Immun. 2010, 78: 4625-4633.PubMedCentralCrossRefPubMed
37.
go back to reference Cortes A, Mellombo M, Masciantonio R, Murphy VJ, Reeder JC, Anders RF: Allele specificity of naturally acquired antibody responses against Plasmodium falciparum apical membrane antigen 1. Infect Immun. 2005, 73: 422-430.PubMedCentralCrossRefPubMed Cortes A, Mellombo M, Masciantonio R, Murphy VJ, Reeder JC, Anders RF: Allele specificity of naturally acquired antibody responses against Plasmodium falciparum apical membrane antigen 1. Infect Immun. 2005, 73: 422-430.PubMedCentralCrossRefPubMed
38.
go back to reference Mugyenyi CK, Elliott SR, McCallum FJ, Anders RF, Marsh K, Beeson JG: Antibodies to polymorphic invasion-inhibitory and non-inhibitory epitopes of Plasmodium falciparum apical membrane antigen 1 in human malaria. PLoS One. 2013, 8: e68304-PubMedCentralCrossRefPubMed Mugyenyi CK, Elliott SR, McCallum FJ, Anders RF, Marsh K, Beeson JG: Antibodies to polymorphic invasion-inhibitory and non-inhibitory epitopes of Plasmodium falciparum apical membrane antigen 1 in human malaria. PLoS One. 2013, 8: e68304-PubMedCentralCrossRefPubMed
39.
go back to reference Mufalo BC, Gentil F, Bargieri DY, Costa FT, Rodrigues MM, Soares IS: Plasmodium vivax apical membrane antigen-1: comparative recognition of different domains by antibodies induced during natural human infection. Microbes Infect. 2008, 10: 1266-1273.CrossRefPubMed Mufalo BC, Gentil F, Bargieri DY, Costa FT, Rodrigues MM, Soares IS: Plasmodium vivax apical membrane antigen-1: comparative recognition of different domains by antibodies induced during natural human infection. Microbes Infect. 2008, 10: 1266-1273.CrossRefPubMed
40.
go back to reference Dias S, Somarathna M, Manamperi A, Escalante AA, Gunasekera AM, Udagama PV: Evaluation of the genetic diversity of domain II of Plasmodium vivax Apical Membrane Antigen 1 (PvAMA-1) and the ensuing strain-specific immune responses in patients from Sri Lanka. Vaccine. 2011, 29: 7491-7504.CrossRefPubMed Dias S, Somarathna M, Manamperi A, Escalante AA, Gunasekera AM, Udagama PV: Evaluation of the genetic diversity of domain II of Plasmodium vivax Apical Membrane Antigen 1 (PvAMA-1) and the ensuing strain-specific immune responses in patients from Sri Lanka. Vaccine. 2011, 29: 7491-7504.CrossRefPubMed
41.
go back to reference Rodrigues MH, Rodrigues KM, Oliveira TR, Comodo AN, Rodrigues MM, Kocken CH, Thomas AW, Soares IS: Antibody response of naturally infected individuals to recombinant Plasmodium vivax apical membrane antigen-1. Int J Parasitol. 2005, 35: 185-192.CrossRefPubMed Rodrigues MH, Rodrigues KM, Oliveira TR, Comodo AN, Rodrigues MM, Kocken CH, Thomas AW, Soares IS: Antibody response of naturally infected individuals to recombinant Plasmodium vivax apical membrane antigen-1. Int J Parasitol. 2005, 35: 185-192.CrossRefPubMed
42.
go back to reference Barbedo MB, Ricci R, Jimenez MC, Cunha MG, Yazdani SS, Chitnis CE, Rodrigues MM, Soares IS: Comparative recognition by human IgG antibodies of recombinant proteins representing three asexual erythrocytic stage vaccine candidates of Plasmodium vivax. Mem Inst Oswaldo Cruz. 2007, 102: 335-339.CrossRefPubMed Barbedo MB, Ricci R, Jimenez MC, Cunha MG, Yazdani SS, Chitnis CE, Rodrigues MM, Soares IS: Comparative recognition by human IgG antibodies of recombinant proteins representing three asexual erythrocytic stage vaccine candidates of Plasmodium vivax. Mem Inst Oswaldo Cruz. 2007, 102: 335-339.CrossRefPubMed
43.
44.
go back to reference Kennedy MC, Wang J, Zhang Y, Miles AP, Chitsaz F, Saul A, Long CA, Miller LH, Stowers AW: In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect Immun. 2002, 70: 6948-6960.PubMedCentralCrossRefPubMed Kennedy MC, Wang J, Zhang Y, Miles AP, Chitsaz F, Saul A, Long CA, Miller LH, Stowers AW: In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect Immun. 2002, 70: 6948-6960.PubMedCentralCrossRefPubMed
45.
go back to reference Kocken CH, Withers-Martinez C, Dubbeld MA, van der Wel A, Hackett F, Valderrama A, Blackman MJ, Thomas AW: High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect Immun. 2002, 70: 4471-4476.PubMedCentralCrossRefPubMed Kocken CH, Withers-Martinez C, Dubbeld MA, van der Wel A, Hackett F, Valderrama A, Blackman MJ, Thomas AW: High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect Immun. 2002, 70: 4471-4476.PubMedCentralCrossRefPubMed
46.
go back to reference Dodoo D, Atuguba F, Bosomprah S, Ansah NA, Ansah P, Lamptey H, Egyir B, Oduro AR, Gyan B, Hodgson A, Koram KA: Antibody levels to multiple malaria vaccine candidate antigens in relation to clinical malaria episodes in children in the Kasena-Nankana district of Northern Ghana. Malar J. 2011, 10: 108-PubMedCentralCrossRefPubMed Dodoo D, Atuguba F, Bosomprah S, Ansah NA, Ansah P, Lamptey H, Egyir B, Oduro AR, Gyan B, Hodgson A, Koram KA: Antibody levels to multiple malaria vaccine candidate antigens in relation to clinical malaria episodes in children in the Kasena-Nankana district of Northern Ghana. Malar J. 2011, 10: 108-PubMedCentralCrossRefPubMed
47.
go back to reference Stanisic DI, Richards JS, McCallum FJ, Michon P, King CL, Schoepflin S, Gilson PR, Murphy VJ, Anders RF, Mueller I, Beeson JG: Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infect Immun. 2009, 77: 1165-1174.PubMedCentralCrossRefPubMed Stanisic DI, Richards JS, McCallum FJ, Michon P, King CL, Schoepflin S, Gilson PR, Murphy VJ, Anders RF, Mueller I, Beeson JG: Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infect Immun. 2009, 77: 1165-1174.PubMedCentralCrossRefPubMed
48.
go back to reference Ord RL, Tami A, Sutherland CJ: ama1 genes of sympatric Plasmodium vivax and P. falciparum from Venezuela differ significantly in genetic diversity and recombination frequency. PLoS One. 2008, 3: e3366-PubMedCentralCrossRefPubMed Ord RL, Tami A, Sutherland CJ: ama1 genes of sympatric Plasmodium vivax and P. falciparum from Venezuela differ significantly in genetic diversity and recombination frequency. PLoS One. 2008, 3: e3366-PubMedCentralCrossRefPubMed
49.
go back to reference Mueller I, Kaiok J, Reeder JC, Cortes A: The population structure of Plasmodium falciparum and Plasmodium vivax during an epidemic of malaria in the Eastern Highlands of Papua New Guinea. Am J Trop Med Hyg. 2002, 67: 459-464.PubMed Mueller I, Kaiok J, Reeder JC, Cortes A: The population structure of Plasmodium falciparum and Plasmodium vivax during an epidemic of malaria in the Eastern Highlands of Papua New Guinea. Am J Trop Med Hyg. 2002, 67: 459-464.PubMed
50.
go back to reference Mueller I, Genton B, Betuela I, Alpers MP: Vaccines against malaria: perspectives from Papua New Guinea. Hum Vaccin. 2010, 6: 17-20.CrossRefPubMed Mueller I, Genton B, Betuela I, Alpers MP: Vaccines against malaria: perspectives from Papua New Guinea. Hum Vaccin. 2010, 6: 17-20.CrossRefPubMed
51.
go back to reference Arnott A, Mueller I, Ramsland PA, Siba PM, Reeder JC, Barry AE: Global population structure of the genes encoding the malaria vaccine candidate, Plasmodium vivax apical membrane antigen 1 (PvAMA1). PLoS Negl Trop Dis. 2013, 7: e2506-PubMedCentralCrossRefPubMed Arnott A, Mueller I, Ramsland PA, Siba PM, Reeder JC, Barry AE: Global population structure of the genes encoding the malaria vaccine candidate, Plasmodium vivax apical membrane antigen 1 (PvAMA1). PLoS Negl Trop Dis. 2013, 7: e2506-PubMedCentralCrossRefPubMed
52.
go back to reference Figtree M, Pasay CJ, Slade R, Cheng Q, Cloonan N, Walker J, Saul A: Plasmodium vivax synonymous substitution frequencies, evolution and population structure deduced from diversity in AMA 1 and MSP 1 genes. Mol Biochem Parasitol. 2000, 108: 53-66.CrossRefPubMed Figtree M, Pasay CJ, Slade R, Cheng Q, Cloonan N, Walker J, Saul A: Plasmodium vivax synonymous substitution frequencies, evolution and population structure deduced from diversity in AMA 1 and MSP 1 genes. Mol Biochem Parasitol. 2000, 108: 53-66.CrossRefPubMed
53.
go back to reference Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, Kiniboro B, Buckee CO, Tavul L, Siba PM, Reeder JC, Barry AE: Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malar J. 2010, 9: 336-PubMedCentralCrossRefPubMed Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, Kiniboro B, Buckee CO, Tavul L, Siba PM, Reeder JC, Barry AE: Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malar J. 2010, 9: 336-PubMedCentralCrossRefPubMed
54.
go back to reference Arnott A, Barnadas C, Senn N, Siba P, Mueller I, Reeder JC, Barry AE: High genetic diversity of Plasmodium vivax on the north coast of Papua New Guinea. Am J Trop Med Hyg. 2013, 89: 188-194.PubMedCentralCrossRefPubMed Arnott A, Barnadas C, Senn N, Siba P, Mueller I, Reeder JC, Barry AE: High genetic diversity of Plasmodium vivax on the north coast of Papua New Guinea. Am J Trop Med Hyg. 2013, 89: 188-194.PubMedCentralCrossRefPubMed
55.
go back to reference Barry AE, Schultz L, Senn N, Nale J, Kiniboro B, Siba PM, Mueller I, Reeder JC: High levels of genetic diversity of Plasmodium falciparum populations in Papua New Guinea despite variable infection prevalence. Am J Trop Med Hyg. 2013, 88: 718-725.PubMedCentralCrossRefPubMed Barry AE, Schultz L, Senn N, Nale J, Kiniboro B, Siba PM, Mueller I, Reeder JC: High levels of genetic diversity of Plasmodium falciparum populations in Papua New Guinea despite variable infection prevalence. Am J Trop Med Hyg. 2013, 88: 718-725.PubMedCentralCrossRefPubMed
56.
go back to reference Koepfli C, Timinao L, Antao T, Barry AE, Siba P, Mueller I, Felger I: A large reservoir and little population structure in the South Pacific. PLoS One. 2013, 8: e66041-PubMedCentralCrossRefPubMed Koepfli C, Timinao L, Antao T, Barry AE, Siba P, Mueller I, Felger I: A large reservoir and little population structure in the South Pacific. PLoS One. 2013, 8: e66041-PubMedCentralCrossRefPubMed
57.
go back to reference Pinard R, de Winter A, Sarkis GJ, Gerstein MB, Tartaro KR, Plant RN, Egholm M, Rothberg JM, Leamon JH: Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing. BMC Genomics. 2006, 7: 216-PubMedCentralCrossRefPubMed Pinard R, de Winter A, Sarkis GJ, Gerstein MB, Tartaro KR, Plant RN, Egholm M, Rothberg JM, Leamon JH: Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing. BMC Genomics. 2006, 7: 216-PubMedCentralCrossRefPubMed
58.
go back to reference Havryliuk T, Orjuela-Sanchez P, Ferreira MU: Plasmodium vivax: microsatellite analysis of multiple-clone infections. Exp Parasitol. 2008, 120: 330-336.CrossRefPubMed Havryliuk T, Orjuela-Sanchez P, Ferreira MU: Plasmodium vivax: microsatellite analysis of multiple-clone infections. Exp Parasitol. 2008, 120: 330-336.CrossRefPubMed
59.
go back to reference Karunaweera ND, Ferreira MU, Hart DL, Wirth DF: Fourteen polymorphic microsatellite DNA markers for the human malaria parasite Plasmodium vivax. Mol Ecol Notes. 2007, 7: 172-175.CrossRef Karunaweera ND, Ferreira MU, Hart DL, Wirth DF: Fourteen polymorphic microsatellite DNA markers for the human malaria parasite Plasmodium vivax. Mol Ecol Notes. 2007, 7: 172-175.CrossRef
60.
go back to reference Duan J, Mu J, Thera MA, Joy D, Kosakovsky Pond SL, Diemert D, Long C, Zhou H, Miura K, Ouattara A, Dolo A, Doumbo O, Su XZ, Miller L: Population structure of the genes encoding the polymorphic Plasmodium falciparum apical membrane antigen 1: implications for vaccine design. Proc Natl Acad Sci USA. 2008, 105: 7857-7862.PubMedCentralCrossRefPubMed Duan J, Mu J, Thera MA, Joy D, Kosakovsky Pond SL, Diemert D, Long C, Zhou H, Miura K, Ouattara A, Dolo A, Doumbo O, Su XZ, Miller L: Population structure of the genes encoding the polymorphic Plasmodium falciparum apical membrane antigen 1: implications for vaccine design. Proc Natl Acad Sci USA. 2008, 105: 7857-7862.PubMedCentralCrossRefPubMed
61.
go back to reference Wang X, Mu J, Li G, Chen P, Guo X, Fu L, Chen L, Su X, Wellems TE: Decreased prevalence of the Plasmodium falciparum chloroquine resistance transporter 76T marker associated with cessation of chloroquine use against P. falciparum malaria in Hainan, People's Republic of China. Am J Trop Med Hyg. 2005, 72: 410-414.PubMed Wang X, Mu J, Li G, Chen P, Guo X, Fu L, Chen L, Su X, Wellems TE: Decreased prevalence of the Plasmodium falciparum chloroquine resistance transporter 76T marker associated with cessation of chloroquine use against P. falciparum malaria in Hainan, People's Republic of China. Am J Trop Med Hyg. 2005, 72: 410-414.PubMed
62.
go back to reference Cheng Q, Saul A: Sequence analysis of the apical membrane antigen I (AMA-1) of Plasmodium vivax. Mol Biochem Parasitol. 1994, 65: 183-187.CrossRefPubMed Cheng Q, Saul A: Sequence analysis of the apical membrane antigen I (AMA-1) of Plasmodium vivax. Mol Biochem Parasitol. 1994, 65: 183-187.CrossRefPubMed
64.
go back to reference Ntumngia FB, McHenry AM, Barnwell JW, Cole-Tobian J, King CL, Adams JH: Genetic variation among Plasmodium vivax isolates adapted to non-human primates and the implication for vaccine development. Am J Trop Med Hyg. 2009, 80: 218-227.PubMedCentralPubMed Ntumngia FB, McHenry AM, Barnwell JW, Cole-Tobian J, King CL, Adams JH: Genetic variation among Plasmodium vivax isolates adapted to non-human primates and the implication for vaccine development. Am J Trop Med Hyg. 2009, 80: 218-227.PubMedCentralPubMed
65.
go back to reference Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739.PubMedCentralCrossRefPubMed Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739.PubMedCentralCrossRefPubMed
66.
go back to reference Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009, 25: 1451-1452.CrossRefPubMed Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009, 25: 1451-1452.CrossRefPubMed
67.
go back to reference Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986, 3: 418-426.PubMed Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986, 3: 418-426.PubMed
68.
go back to reference Hurlbert SH: The non-concept of species diversity: a critique and alternative parameters. Ecology. 1971, 52: 577-586.CrossRef Hurlbert SH: The non-concept of species diversity: a critique and alternative parameters. Ecology. 1971, 52: 577-586.CrossRef
69.
go back to reference Goudet J: FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered. 1995, 86: 485-486. Goudet J: FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered. 1995, 86: 485-486.
70.
go back to reference Glaubitz JC: CONVERT: a user friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes. 2004, 4: 309-310.CrossRef Glaubitz JC: CONVERT: a user friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes. 2004, 4: 309-310.CrossRef
71.
go back to reference Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, Nickerson DA, Kruglyak L: Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol. 2004, 2: e286-PubMedCentralCrossRefPubMed Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, Nickerson DA, Kruglyak L: Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol. 2004, 2: e286-PubMedCentralCrossRefPubMed
72.
go back to reference Hudson RR: Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987, 50: 245-250.CrossRefPubMed Hudson RR: Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987, 50: 245-250.CrossRefPubMed
73.
go back to reference Lewontin RC: The interaction of selection and linkage. I. General considerations; heterotic models. Genetics. 1964, 49: 49-67.PubMedCentralPubMed Lewontin RC: The interaction of selection and linkage. I. General considerations; heterotic models. Genetics. 1964, 49: 49-67.PubMedCentralPubMed
74.
go back to reference Hill WG, Robertson A: Linkage disequilibrium in finite populations. Theor Appl Genet. 1968, 38: 226-231.CrossRefPubMed Hill WG, Robertson A: Linkage disequilibrium in finite populations. Theor Appl Genet. 1968, 38: 226-231.CrossRefPubMed
75.
go back to reference Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES: TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007, 23: 2633-2635.CrossRefPubMed Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES: TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007, 23: 2633-2635.CrossRefPubMed
76.
go back to reference Mueller JC: Linkage disequilibrium for different scales and applications. Brief Bioinform. 2004, 5: 355-364.CrossRefPubMed Mueller JC: Linkage disequilibrium for different scales and applications. Brief Bioinform. 2004, 5: 355-364.CrossRefPubMed
77.
go back to reference Coley AM, Gupta A, Murphy VJ, Bai T, Kim H, Foley M, Anders RF, Batchelor AH: Structure of the malaria antigen AMA1 in complex with a growth-inhibitory antibody. PLoS Pathog. 2007, 3: 1308-1319.PubMed Coley AM, Gupta A, Murphy VJ, Bai T, Kim H, Foley M, Anders RF, Batchelor AH: Structure of the malaria antigen AMA1 in complex with a growth-inhibitory antibody. PLoS Pathog. 2007, 3: 1308-1319.PubMed
78.
go back to reference Srinivasan P, Beatty WL, Diouf A, Herrera R, Ambroggio X, Moch JK, Tyler JS, Narum DL, Pierce SK, Boothroyd JC, Haynes JD, Miller LH: Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc Natl Acad Sci USA. 2011, 108: 13275-13280.PubMedCentralCrossRefPubMed Srinivasan P, Beatty WL, Diouf A, Herrera R, Ambroggio X, Moch JK, Tyler JS, Narum DL, Pierce SK, Boothroyd JC, Haynes JD, Miller LH: Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc Natl Acad Sci USA. 2011, 108: 13275-13280.PubMedCentralCrossRefPubMed
79.
go back to reference Dutta S, Lee SY, Batchelor AH, Lanar DE: Structural basis of antigenic escape of a malaria vaccine candidate. Proc Natl Acad Sci USA. 2007, 104: 12488-12493.PubMedCentralCrossRefPubMed Dutta S, Lee SY, Batchelor AH, Lanar DE: Structural basis of antigenic escape of a malaria vaccine candidate. Proc Natl Acad Sci USA. 2007, 104: 12488-12493.PubMedCentralCrossRefPubMed
80.
go back to reference Dutta S, Dlugosz LS, Drew DR, Ge X, Ababacar D, Rovira YI, Moch JK, Shi M, Long CA, Foley M, Beeson JG, Anders RF, Miura K, Haynes JD, Batchelor AH: Overcoming antigenic diversity by enhancing the immunogenicity of conserved epitopes on the malaria vaccine candidate apical membrane antigen-1. PLoS Pathog. 2013, 9: e1003840-PubMedCentralCrossRefPubMed Dutta S, Dlugosz LS, Drew DR, Ge X, Ababacar D, Rovira YI, Moch JK, Shi M, Long CA, Foley M, Beeson JG, Anders RF, Miura K, Haynes JD, Batchelor AH: Overcoming antigenic diversity by enhancing the immunogenicity of conserved epitopes on the malaria vaccine candidate apical membrane antigen-1. PLoS Pathog. 2013, 9: e1003840-PubMedCentralCrossRefPubMed
81.
go back to reference Collins CR, Withers-Martinez C, Bentley GA, Batchelor AH, Thomas AW, Blackman MJ: Fine mapping of an epitope recognized by an invasion-inhibitory monoclonal antibody on the malaria vaccine candidate apical membrane antigen 1. J Biol Chem. 2007, 282: 7431-7441.CrossRefPubMed Collins CR, Withers-Martinez C, Bentley GA, Batchelor AH, Thomas AW, Blackman MJ: Fine mapping of an epitope recognized by an invasion-inhibitory monoclonal antibody on the malaria vaccine candidate apical membrane antigen 1. J Biol Chem. 2007, 282: 7431-7441.CrossRefPubMed
82.
go back to reference Kasehagen LJ, Mueller I, McNamara DT, Bockarie MJ, Kiniboro B, Rare L, Lorry K, Kastens W, Reeder JC, Kazura JW, Zimmerman PA: Changing patterns of Plasmodium blood-stage infections in the Wosera region of Papua New Guinea monitored by light microscopy and high throughput PCR diagnosis. Am J Trop Med Hyg. 2006, 75: 588-596.PubMedCentralPubMed Kasehagen LJ, Mueller I, McNamara DT, Bockarie MJ, Kiniboro B, Rare L, Lorry K, Kastens W, Reeder JC, Kazura JW, Zimmerman PA: Changing patterns of Plasmodium blood-stage infections in the Wosera region of Papua New Guinea monitored by light microscopy and high throughput PCR diagnosis. Am J Trop Med Hyg. 2006, 75: 588-596.PubMedCentralPubMed
83.
go back to reference Riley EM, Stewart VA: Immune mechanisms in malaria: new insights in vaccine development. Nat Med. 2013, 19: 168-178.CrossRefPubMed Riley EM, Stewart VA: Immune mechanisms in malaria: new insights in vaccine development. Nat Med. 2013, 19: 168-178.CrossRefPubMed
84.
go back to reference Richards JS, Beeson JG: The future for blood-stage vaccines against malaria. Immunol Cell Biol. 2009, 87: 377-390.CrossRefPubMed Richards JS, Beeson JG: The future for blood-stage vaccines against malaria. Immunol Cell Biol. 2009, 87: 377-390.CrossRefPubMed
85.
go back to reference Ferreira MU, da Silva NM, Wunderlich G: Antigenic diversity and immune evasion by malaria parasites. Clin Diagn Lab Immunol. 2004, 11: 987-995.PubMedCentralPubMed Ferreira MU, da Silva NM, Wunderlich G: Antigenic diversity and immune evasion by malaria parasites. Clin Diagn Lab Immunol. 2004, 11: 987-995.PubMedCentralPubMed
86.
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: 1505-1512.PubMedCentralPubMed Polley SD, Conway DJ: Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics. 2001, 158: 1505-1512.PubMedCentralPubMed
87.
go back to reference Lal AA, Hughes MA, Oliveira DA, Nelson C, Bloland PB, Oloo AJ, Hawley WE, Hightower AW, Nahlen BL, Udhayakumar V: Identification of T-cell determinants in natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in an adult population exposed to malaria. Infect Immun. 1996, 64: 1054-1059.PubMedCentralPubMed Lal AA, Hughes MA, Oliveira DA, Nelson C, Bloland PB, Oloo AJ, Hawley WE, Hightower AW, Nahlen BL, Udhayakumar V: Identification of T-cell determinants in natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in an adult population exposed to malaria. Infect Immun. 1996, 64: 1054-1059.PubMedCentralPubMed
88.
go back to reference Udhayakumar V, Kariuki S, Kolczack M, Girma M, Roberts JM, Oloo AJ, Nahlen BL, Lal AA: Longitudinal study of natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in a holoendemic region of malaria in western Kenya: Asembo Bay Cohort Project VIII. Am J Trop Med Hyg. 2001, 65: 100-107.PubMed Udhayakumar V, Kariuki S, Kolczack M, Girma M, Roberts JM, Oloo AJ, Nahlen BL, Lal AA: Longitudinal study of natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in a holoendemic region of malaria in western Kenya: Asembo Bay Cohort Project VIII. Am J Trop Med Hyg. 2001, 65: 100-107.PubMed
89.
go back to reference Cui L, Escalante AA, Imwong M, Snounou G: The genetic diversity of Plasmodium vivax populations. Trends Parasitol. 2003, 19: 220-226.CrossRefPubMed Cui L, Escalante AA, Imwong M, Snounou G: The genetic diversity of Plasmodium vivax populations. Trends Parasitol. 2003, 19: 220-226.CrossRefPubMed
90.
go back to reference Yung AP, Bennett NM: Chloroquine-resistant falciparum malaria in Papua New Guinea. Med J Aust. 1976, 2: 320-321.PubMed Yung AP, Bennett NM: Chloroquine-resistant falciparum malaria in Papua New Guinea. Med J Aust. 1976, 2: 320-321.PubMed
91.
go back to reference Grimmond TR, Donovan KO, Riley ID: Chloroquine resistant malaria in Papua New Guinea. P N G Med J. 1976, 19: 184-185.PubMed Grimmond TR, Donovan KO, Riley ID: Chloroquine resistant malaria in Papua New Guinea. P N G Med J. 1976, 19: 184-185.PubMed
92.
go back to reference Rieckmann KH, Davis DR, Hutton DC: Plasmodium vivax resistance to chloroquine?. Lancet. 1989, 2: 1183-1184.CrossRefPubMed Rieckmann KH, Davis DR, Hutton DC: Plasmodium vivax resistance to chloroquine?. Lancet. 1989, 2: 1183-1184.CrossRefPubMed
93.
go back to reference Whitby M, Wood G, Veenendaal JR, Rieckmann K: Chloroquine-resistant Plasmodium vivax. Lancet. 1989, 2: 1395-CrossRefPubMed Whitby M, Wood G, Veenendaal JR, Rieckmann K: Chloroquine-resistant Plasmodium vivax. Lancet. 1989, 2: 1395-CrossRefPubMed
94.
go back to reference Koepfli C, Ross A, Kiniboro B, Smith TA, Zimmerman PA, Siba P, Mueller I, Felger I: Multiplicity and diversity of Plasmodium vivax infections in a highly endemic region in Papua New Guinea. PLoS Negl Trop Dis. 2011, 5: e1424-PubMedCentralCrossRefPubMed Koepfli C, Ross A, Kiniboro B, Smith TA, Zimmerman PA, Siba P, Mueller I, Felger I: Multiplicity and diversity of Plasmodium vivax infections in a highly endemic region in Papua New Guinea. PLoS Negl Trop Dis. 2011, 5: e1424-PubMedCentralCrossRefPubMed
Metadata
Title
Distinct patterns of diversity, population structure and evolution in the AMA1 genes of sympatric Plasmodium falciparum and Plasmodium vivax populations of Papua New Guinea from an area of similarly high transmission
Authors
Alicia Arnott
Johanna Wapling
Ivo Mueller
Paul A Ramsland
Peter M Siba
John C Reeder
Alyssa E Barry
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2014
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-13-233

Other articles of this Issue 1/2014

Malaria Journal 1/2014 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 discusses last year's major advances in heart failure and cardiomyopathies.