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

Malaria Journal

Volumn 13, Issue 1, 2014, Pages

  Arnott, Alicia ^a,c,d   Wapling, Johanna ^a   Mueller, Ivo ^b,c,d   Ramsland, Paul A ^a,d,e,f   Siba, Peter M ^g   Reeder, John C ^a,e   Barry, Alyssa E ^c,d  

^a BURNET INSTITUTE   (Australia)

^b CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f CURTIN UNIVERSITY   (Australia)

^g PAPUA NEW GUINEA INSTITUTE OF MEDICAL RESEARCH   (Papua New Guinea)

Author keywords

AMA1; Malaria vaccine; Papua New Guinea; Plasmodium falciparum; Plasmodium vivax; Population genetics

Indexed keywords

MALARIA VACCINE; APICAL MEMBRANE ANTIGEN I, PLASMODIUM; MEMBRANE PROTEIN; PARASITE ANTIGEN; PROTOZOAL DNA; PROTOZOAL PROTEIN;

AMA1 GENE; ARTICLE; BACTERIAL GENE; BALANCING SELECTION; EFFECTIVE POPULATION SIZE; HAPLOTYPE; MALARIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PAPUA NEW GUINEA; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; POPULATION GENETICS; POPULATION STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ENDEMIC DISEASE; EPIDEMIOLOGY; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; MALARIA, FALCIPARUM; MALARIA, VIVAX; MOLECULAR GENETICS; PARASITOLOGY; PROTEIN CONFORMATION;

ANTIGENS, PROTOZOAN; DNA, PROTOZOAN; ENDEMIC DISEASES; GENETIC VARIATION; MALARIA, FALCIPARUM; MALARIA, VIVAX; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PAPUA NEW GUINEA; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PROTEIN CONFORMATION; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 84902072353     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-13-233     Document Type: Article

References (94)

1. Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. Genton B, D'Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Muller I, PLoS Med 2008 5 127
2. Vivax malaria: neglected and not benign. Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM, Am J Trop Med Hyg 2007 77 79 87
3. Demographic risk factors for severe and fatal vivax and falciparum malaria among hospital admissions in northeastern Indonesian Papua. Barcus MJ, Basri H, Picarima H, Manyakori C, Sekartuti, Elyazar I, Bangs MJ, Maguire JD, Baird JK, Am J Trop Med Hyg 2007 77 984 991 (Pubitemid 351837852)
4. Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua. Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, Karyana M, Lampah DA, Price RN, Indonesia PLoS Med 2008 5 128
5. The international limits and population at risk of Plasmodium vivax transmission in 2009. 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, PLoS Negl Trop Dis 2010 4 774
6. The changing epidemiology of malaria elimination: new strategies for new challenges. Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, Gueye CS, Fullman N, Gosling RD, Feachem RG, Lancet 2013 382 900 911
7. Relapse. White NJ, Imwong M, Adv Parasitol 2012 80 113 150
8. The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. 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, Nat Genet 2012 44 1046 1050
9. G6PD deficiency in Plasmodium falciparum and Plasmodium vivax malaria-infected Cambodian patients. 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, Malar J 2013 12 171
10. Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, Western Cambodia. Orjuela-Sanchez P, Sa JM, Brandi MC, Rodrigues PT, Bastos MS, Amaratunga C, Duong S, Fairhurst RM, Ferreira MU, Exp Parasitol 2013 134 318 326
11. Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, Escalante AA, Ouattara A, Traore K, Niangaly A, Djimde AA, Doumbo OK, Plowe CV, Sci Transl Med 2009 1 2ra5
12. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. 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, Mol Biol Evol 2000 17 1467 1482
13. Plasmodium falciparum accompanied the human expansion out of Africa. 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, Curr Biol 2010 20 1283 1289
14. Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. Ferreira MU, Karunaweera ND, da Silva-Nunes M, da Silva NS, Wirth DF, Hartl DL, J Infect Dis 2007 195 1218 1226 (Pubitemid 46543456)
15. Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. 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, Int J Parasitol 2007 37 1013 1022 (Pubitemid 46887595)
16. The evolutionary history of Plasmodium vivax as inferred from mitochondrial genomes: parasite genetic diversity in the Americas. 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, Mol Biol Evol 2013 30 2050 2064
17. Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. 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, Proc Natl Acad Sci USA 2013 110 8123 8128
18. African origin of the malaria parasite Plasmodium vivax. 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, et al. Nat Commun 2014 5 3346
19. Understanding the population genetics of Plasmodium vivax is essential for malaria control and elimination. Arnott A, Barry AE, Reeder JC, Malar J 2012 11 14
20. A review of malaria vaccine clinical projects based on the WHO rainbow table. Schwartz L, Brown GV, Genton B, Moorthy VS, Malar J 2012 11 11
21. Contrasting population structures of the genes encoding ten leading vaccine-candidate antigens of the human malaria parasite, Plasmodium falciparum. Barry AE, Schultz L, Buckee CO, Reeder JC, PLoS One 2009 4 8497
22. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming 'vaccine resistant malaria'. Takala SL, Plowe CV, Parasite Immunol 2009 31 560 573
23. Current status of Plasmodium vivax vaccine. Arevalo-Herrera M, Chitnis C, Herrera S, Hum Vaccin 2010 6 124 132
24. A comparative study of the genetic diversity of the 42kDa fragment of the merozoite surface protein 1 in Plasmodium falciparum and P. vivax. Pacheco MA, Poe AC, Collins WE, Lal AA, Tanabe K, Kariuki SK, Udhayakumar V, Escalante AA, Infect Genet Evol 2007 7 180 187 (Pubitemid 46172945)
25. The evolution and diversity of a low complexity vaccine candidate, merozoite surface protein 9 (MSP-9), in Plasmodium vivax and closely related species. Chenet SM, Pacheco MA, Bacon DJ, Collins WE, Barnwell JW, Escalante AA, Infect Genet Evol 2013 20 239 248
26. Apical membrane antigen 1: a malaria vaccine candidate in review. Remarque EJ, Faber BW, Kocken CH, Thomas AW, Trends Parasitol 2008 24 74 84
27. A recombinant vaccine based on domain II of Plasmodium vivax Apical Membrane Antigen 1 induces high antibody titres in mice. Gentil F, Bargieri DY, Leite JA, Francoso KS, Patricio MB, Espindola NM, Vaz AJ, Palatnik-de-Sousa CB, Rodrigues MM, Costa FT, Soares IS, Vaccine 2010 28 6183 6190
28. Genetic polymorphism and effect of natural selection at domain I of apical membrane antigen-1 (AMA-1) in Plasmodium vivax isolates from Myanmar. Moon SU, Na BK, Kang JM, Kim JY, Cho SH, Park YK, Sohn WM, Lin K, Kim TS, Acta Trop 2010 114 71 75
29. Genetic diversity and natural selection at the domain I of apical membrane antigen-1 (AMA-1) of Plasmodium falciparum in isolates from Iran. Mardani A, Keshavarz H, Heidari A, Hajjaran H, Raeisi A, Khorramizadeh MR, Exp Parasitol 2012 130 456 462
30. Plasmodium vivax: who cares? Galinski MR, Barnwell JW, Malar J 2008 7 Suppl 1 9
31. Phase Ia clinical evaluation of the safety and immunogenicity of the Plasmodium falciparum blood-stage antigen AMA1 in ChAd63 and MVA vaccine vectors. 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, PLoS One 2012 7 31208
32. Transgene optimization, immunogenicity and in vitro efficacy of viral vectored vaccines expressing two alleles of Plasmodium falciparum AMA1. Biswas S, Dicks MD, Long CA, Remarque EJ, Siani L, Colloca S, Cottingham MG, Holder AA, Gilbert SC, Hill AV, Draper SJ, PLoS One 2011 6 20977
33. Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. Bai T, Becker M, Gupta A, Strike P, Murphy VJ, Anders RF, Batchelor AH, Proc Natl Acad Sci USA 2005 102 12736 12741 (Pubitemid 41279435)
34. Conditional expression of apical membrane antigen 1 in Plasmodium falciparum shows it is required for erythrocyte invasion by merozoites. Yap A, Azevedo MF, Gilson PR, Weiss GE, O'Neill MT, Wilson DW, Crabb BS, Cowman AF, Cell Microbiol 2014 16 642 656
35. Geographical structure of diversity and differences between symptomatic and asymptomatic infections for Plasmodium falciparum vaccine candidate AMA1. Cortes A, Mellombo M, Mueller I, Benet A, Reeder JC, Anders RF, Infect Immun 2003 71 1416 1426 (Pubitemid 36254328)
36. Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Osier FH, Weedall GD, Verra F, Murungi L, Tetteh KK, Bull P, Faber BW, Remarque E, Thomas A, Marsh K, Conway DJ, Infect Immun 2010 78 4625 4633
37. Allele specificity of naturally acquired antibody responses against Plasmodium falciparum apical membrane antigen 1. Cortes A, Mellombo M, Masciantonio R, Murphy VJ, Reeder JC, Anders RF, Infect Immun 2005 73 422 430 (Pubitemid 40041135)
38. Antibodies to polymorphic invasion-inhibitory and non-inhibitory epitopes of Plasmodium falciparum apical membrane antigen 1 in human malaria. Mugyenyi CK, Elliott SR, McCallum FJ, Anders RF, Marsh K, Beeson JG, PLoS One 2013 8 68304
39. Plasmodium vivax apical membrane antigen-1: comparative recognition of different domains by antibodies induced during natural human infection. Mufalo BC, Gentil F, Bargieri DY, Costa FT, Rodrigues MM, Soares IS, Microbes Infect 2008 10 1266 1273
40. 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. Dias S, Somarathna M, Manamperi A, Escalante AA, Gunasekera AM, Udagama PV, Vaccine 2011 29 7491 7504
41. Antibody response of naturally infected individuals to recombinant Plasmodium vivax apical membrane antigen-1. Rodrigues MH, Rodrigues KM, Oliveira TR, Comodo AN, Rodrigues MM, Kocken CH, Thomas AW, Soares IS, Int J Parasitol 2005 35 185 192 (Pubitemid 40248713)
42. Comparative recognition by human IgG antibodies of recombinant proteins representing three asexual erythrocytic stage vaccine candidates of Plasmodium vivax. Barbedo MB, Ricci R, Jimenez MC, Cunha MG, Yazdani SS, Chitnis CE, Rodrigues MM, Soares IS, Mem Inst Oswaldo Cruz 2007 102 335 339 (Pubitemid 46869331)
43. Specificity of the protective antibody response to apical membrane antigen 1. Hodder AN, Crewther PE, Anders RF, Infect Immun 2001 69 3286 3294 (Pubitemid 32332227)
44. 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. Kennedy MC, Wang J, Zhang Y, Miles AP, Chitsaz F, Saul A, Long CA, Miller LH, Stowers AW, Infect Immun 2002 70 6948 6960 (Pubitemid 35387930)
45. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Kocken CH, Withers-Martinez C, Dubbeld MA, van der Wel A, Hackett F, Valderrama A, Blackman MJ, Thomas AW, Infect Immun 2002 70 4471 4476 (Pubitemid 34790958)
46. Antibody levels to multiple malaria vaccine candidate antigens in relation to clinical malaria episodes in children in the Kasena-Nankana district of Northern Ghana. Dodoo D, Atuguba F, Bosomprah S, Ansah NA, Ansah P, Lamptey H, Egyir B, Oduro AR, Gyan B, Hodgson A, Koram KA, Malar J 2011 10 108
47. Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Stanisic DI, Richards JS, McCallum FJ, Michon P, King CL, Schoepflin S, Gilson PR, Murphy VJ, Anders RF, Mueller I, Beeson JG, Infect Immun 2009 77 1165 1174
48. ama1 genes of sympatric Plasmodium vivax and P. falciparum from Venezuela differ significantly in genetic diversity and recombination frequency. Ord RL, Tami A, Sutherland CJ, PLoS One 2008 3 3366
49. The population structure of Plasmodium falciparum and Plasmodium vivax during an epidemic of malaria in the Eastern Highlands of Papua New Guinea. Mueller I, Kaiok J, Reeder JC, Cortes A, Am J Trop Med Hyg 2002 67 459 464 (Pubitemid 35403158)
50. Vaccines against malaria: perspectives from Papua New Guinea. Mueller I, Genton B, Betuela I, Alpers MP, Hum Vaccin 2010 6 17 20
51. Global population structure of the genes encoding the malaria vaccine candidate, Plasmodium vivax apical membrane antigen 1 (PvAMA1). Arnott A, Mueller I, Ramsland PA, Siba PM, Reeder JC, Barry AE, PLoS Negl Trop Dis 2013 7 2506
52. Plasmodium vivax synonymous substitution frequencies, evolution and population structure deduced from diversity in AMA 1 and MSP 1 genes. Figtree M, Pasay CJ, Slade R, Cheng Q, Cloonan N, Walker J, Saul A, Mol Biochem Parasitol 2000 108 53 66 (Pubitemid 30236315)
53. Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, Kiniboro B, Buckee CO, Tavul L, Siba PM, Reeder JC, Barry AE, Malar J 2010 9 336
54. High genetic diversity of Plasmodium vivax on the north coast of Papua New Guinea. Arnott A, Barnadas C, Senn N, Siba P, Mueller I, Reeder JC, Barry AE, Am J Trop Med Hyg 2013 89 188 194
55. High levels of genetic diversity of Plasmodium falciparum populations in Papua New Guinea despite variable infection prevalence. Barry AE, Schultz L, Senn N, Nale J, Kiniboro B, Siba PM, Mueller I, Reeder JC, Am J Trop Med Hyg 2013 88 718 725
56. A large reservoir and little population structure in the South Pacific. Koepfli C, Timinao L, Antao T, Barry AE, Siba P, Mueller I, Felger I, PLoS One 2013 8 66041
57. Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing. Pinard R, de Winter A, Sarkis GJ, Gerstein MB, Tartaro KR, Plant RN, Egholm M, Rothberg JM, Leamon JH, BMC Genomics 2006 7 216
58. Plasmodium vivax: microsatellite analysis of multiple-clone infections. Havryliuk T, Orjuela-Sanchez P, Ferreira MU, Exp Parasitol 2008 120 330 336
59. Fourteen polymorphic microsatellite DNA markers for the human malaria parasite Plasmodium vivax. Karunaweera ND, Ferreira MU, Hart DL, Wirth DF, Mol Ecol Notes 2007 7 172 175 (Pubitemid 46046618)
60. Population structure of the genes encoding the polymorphic Plasmodium falciparum apical membrane antigen 1: implications for vaccine design. 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, Proc Natl Acad Sci USA 2008 105 7857 7862 (Pubitemid 351872728)
61. 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. Wang X, Mu J, Li G, Chen P, Guo X, Fu L, Chen L, Su X, Wellems TE, Am J Trop Med Hyg 2005 72 410 414 (Pubitemid 41278849)
62. Sequence analysis of the apical membrane antigen I (AMA-1) of Plasmodium vivax. Cheng Q, Saul A, Mol Biochem Parasitol 1994 65 183 187 (Pubitemid 24232828)
63. Sequencher® version 5.0 sequence analysis software. Gene Codes Corporation, Ann Arbor, MI, USA http://www.genecodes.com
64. Genetic variation among Plasmodium vivax isolates adapted to non-human primates and the implication for vaccine development. Ntumngia FB, McHenry AM, Barnwell JW, Cole-Tobian J, King CL, Adams JH, Am J Trop Med Hyg 2009 80 218 227
65. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 2731 2739
66. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Librado P, Rozas J, Bioinformatics 2009 25 1451 1452
67. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Nei M, Gojobori T, Mol Biol Evol 1986 3 418 426 (Pubitemid 16010523)
68. The non-concept of species diversity: a critique and alternative parameters. Hurlbert SH, Ecology 1971 52 577 586
69. FSTAT (Version 1.2): a computer program to calculate F-statistics. Goudet J, J Hered 1995 86 485 486
70. CONVERT: a user friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Glaubitz JC, Mol Ecol Notes 2004 4 309 310 (Pubitemid 38689019)
71. Population history and natural selection shape patterns of genetic variation in 132 genes. Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, Nickerson DA, Kruglyak L, PLoS Biol 2004 2 286
72. Estimating the recombination parameter of a finite population model without selection. Hudson RR, Genet Res 1987 50 245 250 (Pubitemid 18042123)
73. The interaction of selection and linkage. I. General considerations; heterotic models. Lewontin RC, Genetics 1964 49 49 67
74. Linkage disequilibrium in finite populations. Hill WG, Robertson A, Theor Appl Genet 1968 38 226 231
75. TASSEL: software for association mapping of complex traits in diverse samples. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES, Bioinformatics 2007 23 2633 2635 (Pubitemid 350048371)
76. Linkage disequilibrium for different scales and applications. Mueller JC, Brief Bioinform 2004 5 355 364
77. Structure of the malaria antigen AMA1 in complex with a growth-inhibitory antibody. Coley AM, Gupta A, Murphy VJ, Bai T, Kim H, Foley M, Anders RF, Batchelor AH, PLoS Pathog 2007 3 1308 1319 (Pubitemid 47510283)
78. Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Srinivasan P, Beatty WL, Diouf A, Herrera R, Ambroggio X, Moch JK, Tyler JS, Narum DL, Pierce SK, Boothroyd JC, Haynes JD, Miller LH, Proc Natl Acad Sci USA 2011 108 13275 13280
79. Structural basis of antigenic escape of a malaria vaccine candidate. Dutta S, Lee SY, Batchelor AH, Lanar DE, Proc Natl Acad Sci USA 2007 104 12488 12493 (Pubitemid 47206165)
80. Overcoming antigenic diversity by enhancing the immunogenicity of conserved epitopes on the malaria vaccine candidate apical membrane antigen-1. 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, PLoS Pathog 2013 9 1003840
81. Fine mapping of an epitope recognized by an invasion-inhibitory monoclonal antibody on the malaria vaccine candidate apical membrane antigen 1. Collins CR, Withers-Martinez C, Bentley GA, Batchelor AH, Thomas AW, Blackman MJ, J Biol Chem 2007 282 7431 7441 (Pubitemid 47093640)
82. Changing patterns of Plasmodium blood-stage infections in the Wosera region of Papua New Guinea monitored by light microscopy and high throughput PCR diagnosis. Kasehagen LJ, Mueller I, McNamara DT, Bockarie MJ, Kiniboro B, Rare L, Lorry K, Kastens W, Reeder JC, Kazura JW, Zimmerman PA, Am J Trop Med Hyg 2006 75 588 596 (Pubitemid 46941260)
83. Immune mechanisms in malaria: new insights in vaccine development. Riley EM, Stewart VA, Nat Med 2013 19 168 178
84. The future for blood-stage vaccines against malaria. Richards JS, Beeson JG, Immunol Cell Biol 2009 87 377 390
85. Antigenic diversity and immune evasion by malaria parasites. Ferreira MU, da Silva NM, Wunderlich G, Clin Diagn Lab Immunol 2004 11 987 995 (Pubitemid 39540833)
86. Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Polley SD, Conway DJ, Genetics 2001 158 1505 1512 (Pubitemid 32783136)
87. 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. Lal AA, Hughes MA, Oliveira DA, Nelson C, Bloland PB, Oloo AJ, Hawley WE, Hightower AW, Nahlen BL, Udhayakumar V, Infect Immun 1996 64 1054 1059 (Pubitemid 26065590)
88. 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. Udhayakumar V, Kariuki S, Kolczack M, Girma M, Roberts JM, Oloo AJ, Nahlen BL, Lal AA, Am J Trop Med Hyg 2001 65 100 107 (Pubitemid 32744213)
89. The genetic diversity of Plasmodium vivax populations. Cui L, Escalante AA, Imwong M, Snounou G, Trends Parasitol 2003 19 220 226 (Pubitemid 36588596)
90. Chloroquine-resistant falciparum malaria in Papua New Guinea. Yung AP, Bennett NM, Med J Aust 1976 2 320 321
91. Chloroquine resistant malaria in Papua New Guinea. Grimmond TR, Donovan KO, Riley ID, P N G Med J 1976 19 184 185 (Pubitemid 8111126)
92. Plasmodium vivax resistance to chloroquine? Rieckmann KH, Davis DR, Hutton DC, Lancet 1989 2 1183 1184 (Pubitemid 19275451)
93. Chloroquine-resistant Plasmodium vivax. Whitby M, Wood G, Veenendaal JR, Rieckmann K, Lancet 1989 2 1395 (Pubitemid 20003003)
94. Multiplicity and diversity of Plasmodium vivax infections in a highly endemic region in Papua New Guinea. Koepfli C, Ross A, Kiniboro B, Smith TA, Zimmerman PA, Siba P, Mueller I, Felger I, PLoS Negl Trop Dis 2011 5 1424