Differing Patterns of Selection and Geospatial Genetic Diversity within Two Leading Plasmodium vivax Candidate Vaccine Antigens

PLoS Neglected Tropical Diseases

Volumn 8, Issue 4, 2014, Pages

  Parobek, Christian M ^a,b   Bailey, Jeffrey A ^c,d   Hathaway, Nicholas J ^c,d   Socheat, Duong ^e   Rogers, William O ^f   Juliano, Jonathan J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e National Malaria Center   (Cambodia)

^f Naval Medical Research Unit 2   (Cambodia)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; MALARIA VACCINE; MEROZOITE SURFACE PROTEIN 1; PARASITE ANTIGEN;

ANTIGEN MEDIATED CLONAL SELECTION; ARTICLE; CAMBODIAN; CLINICAL ARTICLE; DNA POLYMORPHISM; DNA SEQUENCE; GENE AMPLIFICATION; GENE FREQUENCY; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; HUMAN; MALARIA FALCIPARUM; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PARASITE ISOLATION; PHYLOGENETIC TREE; PLASMODIUM VIVAX MALARIA; POLYMERASE CHAIN REACTION; POPULATION GENETIC STRUCTURE; PROTEIN DOMAIN;

BIOSTATISTICS; CAMBODIA; DNA, PROTOZOAN; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MALARIA VACCINES; MEROZOITE SURFACE PROTEIN 1; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYLOGEOGRAPHY; PLASMODIUM VIVAX; PROTOZOAN PROTEINS; SELECTION, GENETIC;

EID: 84901255670     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002796     Document Type: Article

References (105)

1. Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, et al. (2009) Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 9: 555-566 doi:10.1016/S1473-3099(09)70177-X.
2. Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, et al. (2008) Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med 5: e128 doi:10.1371/journal.pmed.0050128.
3. Price RN, Douglas NM, Anstey NM, (2009) New developments in Plasmodium vivax malaria: severe disease and the rise of chloroquine resistance. Curr Opin Infect Dis 22: 430-435 doi:10.1097/QCO.0b013e32832f14c1.
4. Marfurt J, de Monbrison F, Brega S, Barbollat L, Müller I, et al. (2008) Molecular markers of in vivo Plasmodium vivax resistance to amodiaquine plus sulfadoxine-pyrimethamine: mutations in pvdhfr and pvmdr1. J Infect Dis 198: 409-417 doi:10.1086/589882.
5. Greenwood B, Targett G, (2009) Do we still need a malaria vaccine? Parasite Immunol 31: 582-586 doi:10.1111/j.1365-3024.2009.01140.x.
6. Baird JK, (2013) Evidence and Implications of Mortality Associated with Acute Plasmodium vivax Malaria. Clin Microbiol Rev 26: 36-57 doi:10.1128/CMR.00074-12.
7. PATH Malaria Vaccine Initiative (2011) Staying the course? Malaria research and development in a time of economic uncertainty.
8. Arévalo-Herrera M, Chitnis C, Herrera S, (2010) Current status of Plasmodium vivax vaccine. Hum Vaccin 6: 124-132.
9. Espinosa AM, Sierra AY, Barrero CA, Cepeda LA, Cantor EM, et al. (2003) Expression, polymorphism analysis, reticulocyte binding and serological reactivity of two Plasmodium vivax MSP-1 protein recombinant fragments. Vaccine 21: 1033-1043.
10. Collins WE, Kaslow DC, Sullivan JS, Morris CL, Galland GG, et al. (1999) Testing the efficacy of a recombinant merozoite surface protein (MSP-1(19) of Plasmodium vivax in Saimiri boliviensis monkeys. Am J Trop Med Hyg 60: 350-356.
11. Blackman MJ, Heidrich HG, Donachie S, McBride JS, Holder AA, (1990) A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J Exp Med 172: 379-382.
12. Guevara Patiño JA, Holder AA, McBride JS, Blackman MJ, (1997) Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies. J Exp Med 186: 1689-1699.
13. Udhayakumar V, Anyona D, Kariuki S, Shi YP, Bloland PB, et al. (1995) Identification of T and B Cell Epitopes Recognized by Humans in the C- Terminal 42-kDa Domain of the Plasmodium Falciparum Merozoite Surface Protein (MSP)-1. J Immunol 154: 6022-6030.
14. Nwuba RI, Sodeinde O, Anumudu CI, Omosun YO, Odaibo AB, et al. (2002) The Human Immune Response to Plasmodium falciparum Includes Both Antibodies That Inhibit Merozoite Surface Protein 1 Secondary Processing and Blocking Antibodies. Infect Immun 70: 5328-5331 doi:10.1128/IAI.70.9.5328-5331.2002.
15. Sultan AA, (1999) Molecular mechanisms of malaria sporozoite motility and invasion of host cells. Int Microbiol Off J Span Soc Microbiol 2: 155-160.
16. Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, et al. (2011) First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med 365: 1863-1875 doi:10.1056/NEJMoa1102287.
17. Takala SL, Plowe CV, (2009) Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming "vaccine resistant malaria.". Parasite Immunol 31: 560-573 doi:10.1111/j.1365-3024.2009.01138.x.
18. Thera MA, Doumbo OK, Coulibaly D, Laurens MB, Ouattara A, et al. (2011) A field trial to assess a blood-stage malaria vaccine. N Engl J Med 365: 1004-1013 doi:10.1056/NEJMoa1008115.
19. Genton B, Betuela I, Felger I, Al-Yaman F, Anders RF, et al. (2002) 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 185: 820-827 doi:10.1086/339342.
20. Pattaradilokrat S, Cheesman SJ, Carter R, (2007) Linkage Group Selection: Towards Identifying Genes Controlling Strain Specific Protective Immunity in Malaria. PLoS ONE 2: e857 doi:10.1371/journal.pone.0000857.
21. Martinelli A, Cheesman S, Hunt P, Culleton R, Raza A, et al. (2005) A genetic approach to the de novo identification of targets of strain-specific immunity in malaria parasites. Proc Natl Acad Sci U S A 102: 814-819 doi:10.1073/pnas.0405097102.
22. Enosse S, Dobaño C, Quelhas D, Aponte JJ, Lievens M, et al. (2006) RTS,S/AS02A malaria vaccine does not induce parasite CSP T cell epitope selection and reduces multiplicity of infection. PLoS Clin Trials 1: e5 doi:10.1371/journal.pctr.0010005.
23. Kumkhaek C, Phra-ek K, Rénia L, Singhasivanon P, Looareesuwan S, et al. (2005) Are Extensive T Cell Epitope Polymorphisms in the Plasmodium falciparum Circumsporozoite Antigen, a Leading Sporozoite Vaccine Candidate, Selected by Immune Pressure? J Immunol 175: 3935-3939.
24. Alloueche A, Milligan P, Conway DJ, Pinder M, Bojang K, et al. (2003) Protective Efficacy of the Rts,s/as02 Plasmodium Falciparum Malaria Vaccine Is Not Strain Specific. Am J Trop Med Hyg 68: 97-101.
25. Kumkhaek C, Phra-Ek K, Rénia L, Singhasivanon P, Looareesuwan S, et al. (2005) Are extensive T cell epitope polymorphisms in the Plasmodium falciparum circumsporozoite antigen, a leading sporozoite vaccine candidate, selected by immune pressure? J Immunol Baltim Md 1950 175: 3935-3939.
26. Abdulla S, Salim N, Machera F, Kamata R, Juma O, et al. (2013) Randomized, controlled trial of the long term safety, immunogenicity and efficacy of RTS,S/AS02(D) malaria vaccine in infants living in a malaria-endemic region. Malar J 12: 11 doi:10.1186/1475-2875-12-11.
27. Olotu A, Fegan G, Wambua J, Nyangweso G, Awuondo KO, et al. (2013) Four-Year Efficacy of RTS,S/AS01E and Its Interaction with Malaria Exposure. N Engl J Med 368: 1111-1120 doi:10.1056/NEJMoa1207564.
28. Lin JT, Juliano JJ, Kharabora O, Sem R, Lin F-C, et al. (2012) Individual Plasmodium vivax msp1 Variants within Polyclonal P. vivax Infections Display Different Propensities for Relapse. J Clin Microbiol 50: 1449-1451 doi:10.1128/JCM.06212-11.
29. Rogers WO, Sem R, Tero T, Chim P, Lim P, et al. (2009) Failure of artesunate-mefloquine combination therapy for uncomplicated Plasmodium falciparum malaria in southern Cambodia. Malar J 8: 10 doi:10.1186/1475-2875-8-10.
30. Givens MB, Lin JT, Lon C, Gosi P, Char MC, et al. (2014) Development of a Capillary Electrophoresis-Based Heteroduplex Tracking Assay To Measure In-Host Genetic Diversity of Initial and Recurrent Plasmodium vivax Infections in Cambodia. J Clin Microbiol 52: 298-301 doi:10.1128/JCM.02274-13.
31. Ngrenngarmlert W, Kwiek JJ, Kamwendo DD, Ritola K, Swanstrom R, et al. (2005) Measuring Allelic Heterogeneity in Plasmodium Falciparum by a Heteroduplex Tracking Assay. Am J Trop Med Hyg 72: 694-701.
32. Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, et al. (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407: 513-516 doi:10.1038/35035083.
33. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359 doi:10.1038/nmeth.1923.
34. Colwell RK, Mao CX, Chang J, (2004) INTERPOLATING, EXTRAPOLATING, AND COMPARING INCIDENCE-BASED SPECIES ACCUMULATION CURVES. Ecology 85: 2717-2727 doi:10.1890/03-0557.
35. Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, et al. (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5: 3-21 doi:10.1093/jpe/rtr044.
36. Kang J-M, Ju H-L, Kang Y-M, Lee D-H, Moon S-U, et al. (2012) Genetic polymorphism and natural selection in the C-terminal 42 kDa region of merozoite surface protein-1 among Plasmodium vivax Korean isolates. Malar J 11: 206 doi:10.1186/1475-2875-11-206.
37. Librado P, Rozas J, (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinforma Oxf Engl 25: 1451-1452 doi:10.1093/bioinformatics/btp187.
38. Hudson RR, (1987) Estimating the recombination parameter of a finite population model without selection. Genet Res 50: 245-250.
39. McDonald JH, Kreitman M, (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652-654 doi:10.1038/351652a0.
40. Jongwutiwes S, Buppan P, Kosuvin R, Seethamchai S, Pattanawong U, et al. (2011) Plasmodium knowlesi Malaria in humans and macaques, Thailand. Emerg Infect Dis 17: 1799-1806 doi:10.3201/eid1710.110349.
41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739 doi:10.1093/molbev/msr121.
42. Hughes AL, (2004) The evolution of amino acid repeat arrays in Plasmodium and other organisms. J Mol Evol 59: 528-535 doi:10.1007/s00239-004-2645-4.
43. Nei M, Gojobori T, (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
44. Excoffier L, Laval G, Schneider S, (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinforma Online 1: 47-50.
45. Paradis E, Claude J, Strimmer K, (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20: 289-290 doi:10.1093/bioinformatics/btg412.
46. Bérard S, Nicolas F, Buard J, Gascuel O, Rivals E, (2006) A fast and specific alignment method for minisatellite maps. Evol Bioinforma Online 2: 303-320.
47. Bérard S, Rivals E, (2003) Comparison of minisatellites. J Comput Biol J Comput Mol Cell Biol 10: 357-372 doi:10.1089/10665270360688066.
48. Tamura K, Nei M, Kumar S, (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101: 11030-11035 doi:10.1073/pnas.0404206101.
49. Desper R, Gascuel O, (2002) Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J Comput Biol J Comput Mol Cell Biol 9: 687-705 doi:10.1089/106652702761034136.
50. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
51. Hudson RR, (2000) A new statistic for detecting genetic differentiation. Genetics 155: 2011-2014.
52. Hamady M, Lozupone C, Knight R, (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17-27 doi:10.1038/ismej.2009.97.
53. Bandelt HJ, Forster P, Röhl A, (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37-48.
54. Jongwutiwes S, Putaporntip C, Hughes AL, (2010) Bottleneck effects on vaccine-candidate antigen diversity of malaria parasites in Thailand. Vaccine 28: 3112-3117 doi:10.1016/j.vaccine.2010.02.062.
55. Putaporntip C, Jongwutiwes S, Sakihama N, Ferreira MU, Kho W-G, et al. (2002) Mosaic organization and heterogeneity in frequency of allelic recombination of the Plasmodium vivax merozoite surface protein-1 locus. Proc Natl Acad Sci U S A 99: 16348-16353 doi:10.1073/pnas.252348999.
56. Thakur A, Alam MT, Sharma YD, (2008) Genetic diversity in the C-terminal 42 kDa region of merozoite surface protein-1 of Plasmodium vivax (PvMSP-1(42)) among Indian isolates. Acta Trop 108: 58-63 doi:10.1016/j.actatropica.2008.08.011.
57. Han E-T, Wang Y, Lim CS, Cho JH, Chai J-Y, (2011) Genetic diversity of the malaria vaccine candidate merozoite surface protein 1 gene of Plasmodium vivax field isolates in Republic of Korea. Parasitol Res 109: 1571-1576 doi:10.1007/s00436-011-2413-5.
58. Zeyrek FY, Tachibana S-I, Yuksel F, Doni N, Palacpac N, et al. (2010) Limited polymorphism of the Plasmodium vivax merozoite surface protein 1 gene in isolates from Turkey. Am J Trop Med Hyg 83: 1230-1237 doi:10.4269/ajtmh.2010.10-0353.
59. Weedall GD, Conway DJ, (2010) Detecting signatures of balancing selection to identify targets of anti-parasite immunity. Trends Parasitol 26: 363-369 doi:10.1016/j.pt.2010.04.002.
60. Tajima F, (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
61. Chenet SM, Tapia LL, Escalante AA, Durand S, Lucas C, et al. (2012) Genetic diversity and population structure of genes encoding vaccine candidate antigens of Plasmodium vivax. Malar J 11: 68 doi:10.1186/1475-2875-11-68.
62. Hudson RR, Slatkin M, Maddison WP, (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132: 583-589.
63. Carneiro MO, Russ C, Ross MG, Gabriel SB, Nusbaum C, et al. (2012) Pacific biosciences sequencing technology for genotyping and variation discovery in human data. BMC Genomics 13: 375 doi:10.1186/1471-2164-13-375.
64. Lim CS, Tazi L, Ayala FJ, (2005) Plasmodium vivax: recent world expansion and genetic identity to Plasmodium simium. Proc Natl Acad Sci U S A 102: 15523-15528 doi:10.1073/pnas.0507413102.
65. Henry-Halldin CN, Sepe D, Susapu M, McNamara DT, Bockarie M, et al. (2011) High-throughput molecular diagnosis of circumsporozoite variants VK210 and VK247 detects complex Plasmodium vivax infections in malaria endemic populations in Papua New Guinea. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 11: 391-398 doi:10.1016/j.meegid.2010.11.010.
66. Dias S, Wickramarachchi T, Sahabandu I, Escalante AA, Udagama PV, (2013) Population genetic structure of the Plasmodium vivax circumsporozoite protein (Pvcsp) in Sri Lanka. Gene 518: 381-387 doi:10.1016/j.gene.2013.01.003.
67. Hernández-Martínez MÁ, Escalante AA, Arévalo-Herrera M, Herrera S, (2011) Antigenic diversity of the Plasmodium vivax circumsporozoite protein in parasite isolates of Western Colombia. Am J Trop Med Hyg 84: 51-57 doi:10.4269/ajtmh.2011.09-0785.
68. Patil A, Orjuela-Sánchez P, da Silva-Nunes M, Ferreira MU, (2010) Evolutionary dynamics of the immunodominant repeats of the Plasmodium vivax malaria-vaccine candidate circumsporozoite protein (CSP). Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 10: 298-303 doi:10.1016/j.meegid.2010.01.006.
69. Santos-Ciminera PD, Alecrim M das GC, Roberts DR, Quinnan GV Jr, (2007) Molecular epidemiology of Plasmodium vivax in the State of Amazonas, Brazil. Acta Trop 102: 38-46 doi:10.1016/j.actatropica.2007.02.013.
70. Lopez AC, Ortiz A, Coello J, Sosa-Ochoa W, Torres REM, et al. (2012) Genetic diversity of Plasmodium vivax and Plasmodium falciparum in Honduras. Malar J 11: 391 doi:10.1186/1475-2875-11-391.
71. Cerami C, Kwakye-Berko F, Nussenzweig V, (1992) Binding of malarial circumsporozoite protein to sulfatides [Gal(3-SO4)beta 1-Cer] and cholesterol-3-sulfate and its dependence on disulfide bond formation between cysteines in region II. Mol Biochem Parasitol 54: 1-12.
72. Sinnis P, Clavijo P, Fenyö D, Chait BT, Cerami C, et al. (1994) Structural and functional properties of region II-plus of the malaria circumsporozoite protein. J Exp Med 180: 297-306.
73. Seth RK, Bhat AA, Rao DN, Biswas S, (2010) Acquired immune response to defined Plasmodium vivax antigens in individuals residing in northern India. Microbes Infect 12: 199-206 doi:10.1016/j.micinf.2009.12.006.
74. Tetteh KKA, Stewart LB, Ochola LI, Amambua-Ngwa A, Thomas AW, et al. (2009) Prospective Identification of Malaria Parasite Genes under Balancing Selection. PLoS ONE 4: e5568 doi:10.1371/journal.pone.0005568.
75. Charlesworth J, Eyre-Walker A, (2008) The McDonald-Kreitman Test and Slightly Deleterious Mutations. Mol Biol Evol 25: 1007-1015 doi:10.1093/molbev/msn005.
76. Blackman MJ, Whittle H, Holder AA, (1991) Processing of thePlasmodium falciparum major merozoite surface protein-1: identification of a 33-kilodalton secondary processing product which is shed prior to erythrocyte invasion. Mol Biochem Parasitol 49: 35-44 doi:10.1016/0166-6851(91)90128-S.
77. Arnot DE, Barnwell JW, Tam JP, Nussenzweig V, Nussenzweig RS, et al. (1985) Circumsporozoite protein of Plasmodium vivax: gene cloning and characterization of the immunodominant epitope. Science 230: 815-818 doi:10.1126/science.2414847.
78. Arevalo-Herrera M, Roggero MA, Gonzalez JM, Vergara J, Corradin G, et al. (1998) Mapping and comparison of the B cell epitopes recognized on the Plasmodium vivax circumsporozoite protein by immune Colombians and immunized Aotus monkeys. Ann Trop Med Parasitol 92: 539-551 doi:10.1080/00034989859230.
79. Herrera S, Escobar P, Plata Cde, Avila GI, Corradin G, et al. (1992) Human recognition of T cell epitopes on the Plasmodium vivax circumsporozoite protein. J Immunol 148: 3986-3990.
80. Hughes AL, (1991) Circumsporozoite protein genes of malaria parasites (Plasmodium spp.): evidence for positive selection on immunogenic regions. Genetics 127: 345-353.
81. Nardin E, Clavijo P, Mons B, Belkum Avan, Ponnudurai T, et al. (1991) T cell epitopes of the circumsporozoite protein of Plasmodium vivax. Recognition by lymphocytes of a sporozoite-immunized chimpanzee. J Immunol 146: 1674-1678.
82. Bowman NM, Congdon S, Mvalo T, Patel JC, Escamilla V, et al. (2013) Comparative population structure of Plasmodium falciparum circumsporozoite protein NANP repeat lengths in Lilongwe, Malawi. Sci Rep 3: 1990 doi:10.1038/srep01990.
83. Escalante AA, Lal AA, Ayala FJ, (1998) Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum. Genetics 149: 189-202.
84. Rich SM, Hudson RR, Ayala FJ, (1997) Plasmodium falciparum antigenic diversity: Evidence of clonal population structure. Proc Natl Acad Sci U S A 94: 13040-13045.
85. Hartl DL, (2004) The origin of malaria: mixed messages from genetic diversity. Nat Rev Microbiol 2: 15-22 doi:10.1038/nrmicro795.
86. Ferreira MU, Hartl DL, (2007) Plasmodium falciparum: Worldwide sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-2 (MSP-2). Exp Parasitol 115: 32-40 doi:10.1016/j.exppara.2006.05.003.
87. Pacheco MA, Poe AC, Collins WE, Lal AA, Tanabe K, et al. (2007) A comparative study of the genetic diversity of the 42 kDa fragment of the merozoite surface protein 1 in Plasmodium falciparum and P. vivax. Infect Genet Evol 7: 180-187 doi:10.1016/j.meegid.2006.08.002.
88. Bailey JA, Mvalo T, Aragam N, Weiser M, Congdon S, et al. (2012) Use of Massively Parallel Pyrosequencing to Evaluate the Diversity of and Selection on Plasmodium falciparum csp T-Cell Epitopes in Lilongwe, Malawi. J Infect Dis 206: 580-587 doi:10.1093/infdis/jis329.
89. Jalloh A, Jalloh M, Matsuoka H, (2009) T-cell epitope polymorphisms of the Plasmodium falciparum circumsporozoite protein among field isolates from Sierra Leone: age-dependent haplotype distribution? Malar J 8: 120 doi:10.1186/1475-2875-8-120.
90. Gandhi K, Thera MA, Coulibaly D, Traoré K, Guindo AB, et al. (2012) Next generation sequencing to detect variation in the Plasmodium falciparum circumsporozoite protein. Am J Trop Med Hyg 86: 775-781 doi:10.4269/ajtmh.2012.11-0478.
91. Weedall GD, Preston BMJ, Thomas AW, Sutherland CJ, Conway DJ, (2007) Differential evidence of natural selection on two leading sporozoite stage malaria vaccine candidate antigens. Int J Parasitol 37: 77-85 doi:10.1016/j.ijpara.2006.09.001.
92. Zárate S, Pond SLK, Shapshak P, Frost SDW, (2007) Comparative Study of Methods for Detecting Sequence Compartmentalization in Human Immunodeficiency Virus Type 1. J Virol 81: 6643-6651 doi:10.1128/JVI.02268-06.
93. Arnott A, Mueller I, Ramsland PA, Siba PM, Reeder JC, et al. (2013) Global Population Structure of the Genes Encoding the Malaria Vaccine Candidate, Plasmodium vivax Apical Membrane Antigen 1 (PvAMA1). PLoS Negl Trop Dis 7: e2506 doi:10.1371/journal.pntd.0002506.
94. Barry AE, Schultz L, Buckee CO, Reeder JC, (2009) Contrasting population structures of the genes encoding ten leading vaccine-candidate antigens of the human malaria parasite, Plasmodium falciparum. PloS One 4: e8497 doi:10.1371/journal.pone.0008497.
95. Boulanger N, Charoenvit Y, Krettli A, Betschart B, (1995) Developmental changes in the circumsporozoite proteins of Plasmodium berghei and P. gallinaceum in their mosquito vectors. Parasitol Res 81: 58-65.
96. Posthuma G, Meis JF, Verhave JP, Hollingdale MR, Ponnudurai T, et al. (1988) Immunogold localization of circumsporozoite protein of the malaria parasite Plasmodium falciparum during sporogony in Anopheles stephensi midguts. Eur J Cell Biol 46: 18-24.
97. Golenda CF, Starkweather WH, Wirtz RA, (1990) The distribution of circumsporozoite protein (CS) in Anopheles stephensi mosquitoes infected with Plasmodium falciparum malaria. J Histochem Cytochem Off J Histochem Soc 38: 475-481.
98. WHO World Malaria Report (2011). Available: http://www.who.int/malaria/publications/atoz/9789241564403/en/index.html.
99. Foley DH, Klein TA, Lee I-Y, Kim M-S, Wilkerson RC, et al. (2011) Mosquito species composition and Plasmodium vivax infection rates on Baengnyeong-do (island), Republic of Korea. Korean J Parasitol 49: 313-316 doi:10.3347/kjp.2011.49.3.313.
100. Yoo D-H, Shin E-H, Park M-Y, Kim HC, Lee D-K, et al. (2013) Mosquito species composition and Plasmodium vivax infection rates for Korean army bases near the demilitarized zone in the Republic of Korea, 2011. Am J Trop Med Hyg 88: 24-28 doi:10.4269/ajtmh.2012.11-0755.
101. Adak T, Singh OP, Das MK, Wattal S, Nanda N, (2005) Comparative susceptibility of three important malaria vectors Anopheles stephensi, Anopheles fluviatilis, and Anopheles sundaicus to Plasmodium vivax. J Parasitol 91: 79-82 doi:10.1645/GE-3514.
102. Marrelli MT, Honório NA, Flores-Mendoza C, Lourenço-de-Oliveira R, Marinotti O, et al. (1999) Comparative susceptibility of two members of the Anopheles oswaldoi complex, An. oswaldoi and An. konderi, to infection by Plasmodium vivax. Trans R Soc Trop Med Hyg 93: 381-384.
103. Joshi D, Choochote W, Park M-H, Kim J-Y, Kim T-S, et al. (2009) The susceptibility of Anopheles lesteri to infection with Korean strain of Plasmodium vivax. Malar J 8: 42 doi:10.1186/1475-2875-8-42.
104. Da Silva ANM, Santos CCB, Lacerda RN, Machado RLD, Póvoa MM, (2006) Susceptibility of Anopheles aquasalis and an. darlingi to Plasmodium vivax VK210 and VK247. Mem Inst Oswaldo Cruz 101: 547-550.
105. Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, et al. (2009) Extreme Polymorphism in a Vaccine Antigen and Risk of Clinical Malaria: Implications for Vaccine Development. Sci Transl Med 1: 2ra5 doi:10.1126/scitranslmed.3000257.