Toward the development of effective transmission-blocking vaccines for malaria

Expert Review of Vaccines

Volumn 14, Issue 5, 2015, Pages 653-680

  Nikolaeva, Daria ^a,b   Draper, Simon J ^a   Biswas, Sumi ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

genome; malaria; membrane feeding assay; Plasmodium falciparum; transmission blocking vaccine

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; IMMUNOGLOBULIN G; MALARIA VACCINE; MONOCLONAL ANTIBODY; SERINE PROTEINASE INHIBITOR; PROTOZOON ANTIBODY; VACCINE;

ANOPHELES; ANTIBODY RESPONSE; ANTIBODY TITER; BORDETELLA PERTUSSIS; CD8+ T LYMPHOCYTE; CHROMOSOME 13; CHROMOSOME 2; CHROMOSOME 4; CHROMOSOME 5; CHROMOSOME 6; CONJUGATION; DISULFIDE BOND; DNA BASE COMPOSITION; GAMETOCYTE; GENE DISRUPTION; GENE DUPLICATION; GENOME; IMMUNE RESPONSE; IMMUNOGENICITY; INNATE IMMUNITY; MALARIA; MALARIA CONTROL; NONHUMAN; PARASITE CLEARANCE; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PARASITE TRANSMISSION; PLASMODIUM; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; ANIMAL; BLOOD; DISEASE TRANSMISSION; DRUG DEVELOPMENT; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOSQUITO; PARASITOLOGY; PREVENTION AND CONTROL; TRENDS;

ANIMALS; ANTIBODIES, PROTOZOAN; CULICIDAE; DISEASE TRANSMISSION, INFECTIOUS; DRUG DISCOVERY; HUMANS; MALARIA; PLASMODIUM; VACCINES;

EID: 84927725516     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.2015.993383     Document Type: Review

References (216)

1. Zhu HM, Li J, Zheng H. [Human natural infection of Plasmodium knowlesi]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 2006;24(1):70-1
2. Ta TH, Hisam S, Lanza M, et al. First case of a naturally acquired human infection with Plasmodium cynomolgi. Malar J 2014; 13(1):68
3. Stow ers A, Carter R. Current developments in malaria transmission-blocking vaccines. Expert Opin Biol Ther 2001;1(4):619-28
4. WHO. World Malaria Report 2012. 2012 [cited 2013]
5. Alonso PL, Tanner M. Public health challenges and prospects for malaria control and elimination. Nat Med 2013;19(2): 150-5
6. Birkett AJ. PATH Malaria Vaccine Initiative (MVI): perspectives on the status of malaria vaccine development. Hum Vaccin 2010; 6(1):139-45
7. Roberts L, Enserink M. Malaria. Did they really say. eradication? Science 2007; 318(5856):1544-5
8. Alonso PL, Brown G, Arevalo-Herrera M, et al. A research agenda to underpin malaria eradication. PLoS Med 2011;8(1):e1000406
9. Moorthy VS, Newman RD, Okwo-Bele JM. Malaria vaccine technology roadmap. Lancet 2013;382(9906):1700-1
10. Birkett AJ, Moorthy VS, Loucq C, et al. Malaria vaccine R&D in the Decade of Vaccines: breakthroughs, challenges and opportunities. Vaccine 2013;31(Suppl 2): B233-43
11. Goodman AL, Draper SJ. Blood-stage malaria vaccines-recent progress and future challenges. Ann Trop Med Parasitol 2010; 104(3):189-211
12. Sinha A, Hughes KR, Modrzynska KK, et al. A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 2014;507(7491):253-7
13. Kafsack BF, Rovira-Graells N, Clark TG, et al. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 2014;507(7491): 248-52
14. Joice R, Nilsson SK, Montgomery J, et al. Plasmodium falciparum transmission stages accumulate in the human bone marrow. Sci Transl Med 2014;6(244):244re5
15. Angrisano F, Tan YH, Sturm A, et al. Malaria parasite colonisation of the mosquito midgut-placing the Plasmodium ookinete centre stage. Int J Parasitol 2012; 42(6):519-27
16. Sinden RE. A biologist's perspective on malaria vaccine development. Hum Vaccin 2010;6(1):3-11
17. Dondorp AM, Nosten F, Yi P, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 2009; 361(5):455-67
18. Ariey F, Witkowski B, Amaratunga C, et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 2014;505(7481):50-5
19. Huff CG, Marchbank DF, Shiroishi T. Changes in infectiousness of malarial gametocytes. II. Analysis of the possible causative factors. Exp Parasitol 1958;7(4): 399-417
20. Gwadz RW. Successful immunization against the sexual stages of Plasmodium gallinaceum. Science 1976;193(4258): 1150-1
21. Carter R, Chen DH. Malaria transmission blocked by immunisation with gametes of the malaria parasite. Nature 1976; 263(5572):57-60
22. Mendis KN, Targett GA. Immunisation against gametes and asexual erythrocytic stages of a rodent malaria parasite. Nature 1979;277(5695):389-91
23. Gwadz RW, Green I. Malaria immunization in Rhesus monkeys. A vaccine effective against both the sexual and asexual stages of Plasmodium knowlesi. J Exp Med 1978; 148(5):1311-23
24. Ponnudurai T, Meuwissen JH, Leeuwenberg AD, et al. The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Trans R Soc Trop Med Hyg 1982;76(2): 242-50
25. Rener J, Graves PM, Carter R, et al. Target antigens of transmission-blocking immunity on gametes of plasmodium falciparum. J Exp Med 1983;158(3):976-81
26. Ranawaka GR, Alejo-Blanco AR, Sinden RE. Characterization of the effector mechanisms of a transmission-blocking antibody upon differentiation of Plasmodium berghei gametocytes into ookinetes in vitro. Parasitology 1994;109(Pt 1):11-17
27. Ranawaka GR, Fleck SL, Blanco AR, et al. Characterization of the modes of action of anti-Pbs21 malaria transmission-blocking immunity: ookinete to oocyst differentiation in vivo. Parasitology 1994;109(Pt 4):403-11
28. Sinden RE, Carter R, Drakeley C, Leroy D. The biology of sexual development of Plasmodium: the design and implementation of transmission-blocking strategies. Malar J 2012;11:70
29. Healer J, McGuinness D, Carter R, Riley E. Transmission-blocking immunity to Plasmodium falciparum in malaria-immune individuals is associated with antibodies to the gamete surface protein Pfs230. Parasitology 1999;119(Pt 5):425-33
30. Graves PM, Carter R, Burkot TR, et al. Antibodies to Plasmodium falciparum gamete surface antigens in Papua New Guinea sera. Parasite Immunol 1988;10(2): 209-18
31. Roeffen W, Mulder B, Teelen K, et al. Association between anti-Pfs48/45 reactivity and P. falciparum transmission-blocking activity in sera from Cameroon. Parasite Immunol 1996;18(2):103-9
32. Tsuboi T, Kaslow DC, Gozar MM, et al. Sequence polymorphism in two novel Plasmodium vivax ookinete surface proteins, Pvs25 and Pvs28, that are malaria transmission-blocking vaccine candidates. Mol Med 1998;4(12):772-82
33. Wu Y, Ellis RD, Shaffer D, et al. Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with montanide ISA 51. PLoS One 2008;3(7):e2636
34. Da DF, Dixit S, Sattabonkot J, et al. Anti-Pfs25 human plasma reduces transmission of Plasmodium falciparum isolates that have diverse genetic backgrounds. Infect Immun 2013;81(6): 1984-9
35. Niederwieser I, Felger I, Beck HP. Limited polymorphism in Plasmodium falciparum sexual-stage antigens. Am J Trop Med Hyg 2001;64(1-2):9-11
36. Williamson KC, Kaslow DC. Strain polymorphism of Plasmodium falciparum transmission-blocking target antigen Pfs230. Mol Biochem Parasitol 1993;62(1):125-7
37. Kumar N, Carter R. Biosynthesis of the target antigens of antibodies blocking transmission of Plasmodium falciparum. Mol Biochem Parasitol 1984;13(3):333-42
38. Vermeulen AN, Ponnudurai T, Beckers PJ, et al. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med 1985;162(5):1460-76
39. Vermeulen AN, van Deursen J, Brakenhoff RH, et al. Characterization of Plasmodium falciparum sexual stage antigens and their biosynthesis in synchronised gametocyte cultures. Mol Biochem Parasitol 1986;20(2):155-63
40. van Dijk MR, Janse CJ, Thompson J, et al. A central role for P48/45 in malaria parasite male gamete fertility. Cell 2001;104(1): 153-64
41. Eksi S, Czesny B, van Gemert GJ, et al. Malaria transmission-blocking antigen, Pfs230, mediates human red blood cell binding to exflagellating male parasites and oocyst production. Mol Microbiol 2006; 61(4):991-8
42. Williamson KC. Pfs230: from malaria transmission-blocking vaccine candidate toward function. Parasite Immunol 2003; 25(7):351-9
43. Carter R, Coulson A, Bhatti S, et al. Predicted disulfide-bonded structures for three uniquely related proteins of Plasmodium falciparum, Pfs230, Pfs48/45 and Pf12. Mol Biochem Parasitol 1995; 71(2):203-10
44. Brooks SR, Williamson KC. Proteolysis of Plasmodium falciparum surface antigen, Pfs230, during gametogenesis. Mol Biochem Parasitol 2000;106(1):77-82
45. Williamson KC, Fujioka H, Aikawa M, Kaslow DC. Stage-specific processing of Pfs230, a Plasmodium falciparum transmission-blocking vaccine candidate. Mol Biochem Parasitol 1996;78(1-2):161-9
46. Eksi S, Stump A, Fanning SL, et al. Targeting and sequestration of truncated Pfs230 in an intraerythrocytic compartment during Plasmodium falciparum gametocytogenesis. Mol Microbiol 2002; 44(6):1507-16
47. Quakyi IA, Carter R, Rener J, et al. The 230-kDa gamete surface protein of Plasmodium falciparum is also a target for transmission-blocking antibodies. J Immunol 1987;139(12):4213-17
48. Williamson KC, Keister DB, Muratova O, Kaslow DC. Recombinant Pfs230, a Plasmodium falciparum gametocyte protein, induces antisera that reduce the infectivity of Plasmodium falciparum to mosquitoes. Mol Biochem Parasitol 1995;75(1):33-42
49. Riley EM, Williamson KC, Greenwood BM, Kaslow DC. Human immune recognition of recombinant proteins representing discrete domains of the Plasmodium falciparum gamete surface protein. Pfs230. Parasite Immunol 1995;17(1):11-19
50. Gerloff DL, Creasey A, Maslau S, Carter R. Structural models for the protein family characterized by gamete surface protein Pfs230 of Plasmodium falciparum. Proc Natl Acad Sci USA 2005;102(38): 13598-603
51. Tachibana M, Wu Y, Iriko H, et al. N-terminal prodomain of Pfs230 synthesized using a cell-free system is sufficient to induce complement-dependent malaria transmission-blocking activity. Clin Vaccine Immunol 2011;18(8):1343-50
52. Farrance CE, Rhee A, Jones RM, et al. A plant-produced Pfs230 vaccine candidate blocks transmission of Plasmodium falciparum. Clin Vaccine Immunol 2011; 18(8):1351-7
53. MacDonald N, Nguyen V, Shimp RL Jr., et al. Antibodies against a yeast expressed Pfs230 protein produced by scalable bioprocesses block mosquito transmission of malaria parasites and function together with antibodies against Pfs25. In The American Society of Tropical Medicine and Hygiene. Washington, DC: 2013; The American Journal of Tropical Medicine and Hygiene
54. Kocken CH, Jansen J, Kaan AM, et al. Cloning and expression of the gene coding for the transmission blocking target antigen Pfs48/45 of Plasmodium falciparum. Mol Biochem Parasitol 1993;61(1):59-68
55. Milek RL, Roeffen WF, Kocken CH, et al. Immunological properties of recombinant proteins of the transmission blocking vaccine candidate, Pfs48/45, of the human malaria parasite Plasmodium falciparum produced in Escherichia coli. Parasite Immunol 1998;20(8):377-85
56. Milek RL, DeVries AA, Roeffen WF, et al. Plasmodium falciparum: heterologous synthesis of the transmission-blocking vaccine candidate Pfs48/45 in recombinant vaccinia virus-infected cells. Exp Parasitol 1998;90(2):165-74
57. Milek RL, Stunnenberg HG, Konings RN. Assembly and expression of a synthetic gene encoding the antigen Pfs48/45 of the human malaria parasite Plasmodium falciparum in yeast. Vaccine 2000;18(14): 1402-11
58. Outchkourov N, Vermunt A, Jansen J, et al. Epitope analysis of the malaria surface antigen pfs48/45 identifies a subdomain that elicits transmission blocking antibodies. J Biol Chem 2007;282(23):17148-56
59. Outchkourov NS, Roeffen W, Kaan A, et al. Correctly folded Pfs48/45 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in mice. Proc Natl Acad Sci USA 2008;105(11): 4301-5
60. Chowdhury DR, Angov E, Kariuki T, Kumar N. A potent malaria transmission blocking vaccine based on codon harmonized full length Pfs48/45 expressed in Escherichia coli. PLoS One 2009;4(7): e6352
61. Jones CS, Luong T, Hannon M, et al. Heterologous expression of the C-terminal antigenic domain of the malaria vaccine candidate Pfs48/45 in the green algae Chlamydomonas reinhardtii. Appl Microbiol Biotechnol 2013;97(5):1987-95
62. Mamedov T, Ghosh A, Jones RM, et al. Production of non-glycosylated recombinant proteins in Nicotiana benthamiana plants by co-expressing bacterial PNGase F. Plant Biotechnol J 2012;10(7):773-82
63. Theisen M, Roeffen W, Singh SK, et al. A multi-stage malaria vaccine candidate targeting both transmission and asexual parasite life-cycle stages. Vaccine 2014; 32(22):2623-30
64. Duffy PE, Pimenta P, Kaslow DC. Pgs28 belongs to a family of epidermal growth factor-like antigens that are targets of malaria transmission-blocking antibodies. J Exp Med 1993;177(2):505-10
65. Hisaeda H, Stowers AW, Tsuboi T, et al. Antibodies to malaria vaccine candidates Pvs25 and Pvs28 completely block the ability of Plasmodium vivax to infect mosquitoes. Infect Immun 2000;68(12): 6618-23
66. Mair GR, Braks JA, Garver LS, et al. Regulation of sexual development of Plasmodium by translational repression. Science 2006;313(5787):667-9
67. Gozar MM, Price VL, Kaslow DC. Saccharomyces cerevisiae-secreted fusion proteins Pfs25 and Pfs28 elicit potent Plasmodium falciparum transmission-blocking antibodies in mice. Infect Immun 1998;66(1):59-64
68. Duffy PE, Kaslow DC. A novel malaria protein, Pfs28, and Pfs25 are genetically linked and synergistic as falciparum malaria transmission-blocking vaccines. Infect Immun 1997;65(3):1109-13
69. Hisaeda H, Collins WE, Saul A, Stowers AW. Antibodies to Plasmodium vivax transmission-blocking vaccine candidate antigens Pvs25 and Pvs28 do not show synergism. Vaccine 2001;20(5-6): 763-70
70. Tomas AM, Margos G, Dimopoulos G, et al. P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J 2001;20(15): 3975-83
71. Baton LA, Ranford-Cartwright LC. Do malaria ookinete surface proteins P25 and P28 mediate parasite entry into mosquito midgut epithelial cells Malar J 2005;4(1): 15
72. Vlachou D, Lycett G, Side-n-Kiamos I, et al. Anopheles gambiae laminin interacts with the P25 surface protein of Plasmodium berghei ookinetes. Mol Biochem Parasitol 2001;112(2):229-37
73. Side-n-Kiamos I, Vlachou D, Margos G, et al. Distinct roles for pbs21 and pbs25 in the in vitro ookinete to oocyst transformation of Plasmodium berghei. J Cell Sci 2000;113(Pt 19):3419-26
74. Saxena AK, Singh K, Su HP, et al. The essential mosquito-stage P25 and P28 proteins from Plasmodium form tile-like triangular prisms. Nat Struct Mol Biol 2006;13(1):90-1
75. Sinden RE, Winger L, Carter EH, et al. Ookinete antigens of Plasmodium berghei: a light and electron-microscope immunogold study of expression of the 21 kDa determinant recognized by a transmission-blocking antibody. Proc R Soc Lond B Biol Sci 1987;230(1261):443-58
76. Winger LA, Tirawanchai N, Nicholas J, et al. Ookinete antigens of Plasmodium berghei. Appearance on the zygote surface of an Mr 21 kD determinant identified by transmission-blocking monoclonal antibodies. Parasite Immunol 1988;10(2): 193-207
77. Kaslow DC, Quakyi IA, Syin C, et al. A vaccine candidate from the sexual stage of human malaria that contains EGF-like domains. Nature 1988;333(6168):74-6
78. Appella E, Weber IT, Blasi F. Structure and function of epidermal growth factor-like regions in proteins. FEBS Lett 1988;231(1): 1-4
79. Saxena AK, Wu Y, Garboczi DN. Plasmodium p25 and p28 surface proteins: potential transmission-blocking vaccines. Eukaryot Cell 2007;6(8):1260-5
80. Stowers AW, Keister DB, Muratova O, Kaslow DC. A region of Plasmodium falciparum antigen Pfs25 that is the target of highly potent transmission-blocking antibodies. Infect Immun 2000;68(10): 5530-8
81. Kaslow DC, Shiloach J. Production, purification and immunogenicity of a malaria transmission-blocking vaccine candidate: TBV25H expressed in yeast and purified using nickel-NTA agarose. Biotechnology (N Y) 1994;12(5):494-9
82. Zou L, Miles AP, Wang J, Stowers AW. Expression of malaria transmission-blocking vaccine antigen Pfs25 in Pichia pastoris for use in human clinical trials. Vaccine 2003; 21(15):1650-7
83. Cheru L, Wu Y, Diouf A, et al. The IC(50) of anti-Pfs25 antibody in membrane-feeding assay varies among species. Vaccine 2010; 28(27):4423-9
84. Cohen J, Nussenzweig V, Nussenzweig R, et al. From the circumsporozoite protein to the RTS, S/AS candidate vaccine. Hum Vaccin 2010;6(1):90-6
85. Wu Y, Przysiecki C, Flanagan E, et al. Sustained high-titer antibody responses induced by conjugating a malarial vaccine candidate to outer-membrane protein complex. Proc Natl Acad Sci USA 2006; 103(48):18243-8
86. Saul A. Mosquito stage, transmission blocking vaccines for malaria. Curr Opin Infect Dis 2007;20(5):476-81
87. Kaslow DC, Bathurst IC, Lensen T, et al. Saccharomyces cerevisiae recombinant Pfs25 adsorbed to alum elicits antibodies that block transmission of Plasmodium falciparum. Infect Immun 1994;62(12): 5576-80
88. Malkin EM, Durbin AP, Diemert DJ, et al. Phase 1 vaccine trial of Pvs25H: a transmission blocking vaccine for Plasmodium vivax malaria. Vaccine 2005; 23(24):3131-8
89. Kumar R, Angov E, Kumar N. Potent Malaria Transmission-Blocking Antibody Responses Elicited by Plasmodium falciparum Pfs25 Expressed in Escherichia coli after Successful Protein Refolding. Infect Immun 2014;82(4):1453-9
90. Tsuboi T, Takeo S, Iriko H, et al. Wheat germ cell-free system-based production of malaria proteins for discovery of novel vaccine candidates. Infect Immun 2008; 76(4):1702-8
91. Miura K, Takashima E, Deng B, et al. Functional comparison of Plasmodium falciparum transmission-blocking vaccine candidates by the standard membrane-feeding assay. Infect Immun 2013;81(12):4377-82
92. Farrance CE, Chichester JA, Musiychuk K, et al. Antibodies to plant-produced Plasmodium falciparum sexual stage protein Pfs25 exhibit transmission blocking activity. Hum Vaccin 2011(7 Suppl):191-8
93. Gregory JA, Li F, Tomosada LM, et al. Algae-produced Pfs25 elicits antibodies that inhibit malaria transmission. PLoS One 2012;7(5):e37179
94. Kubler-Kielb J, Majadly F, Wu Y, et al. Long-lasting and transmission-blocking activity of antibodies to Plasmodium falciparum elicited in mice by protein conjugates of Pfs25. Proc Natl Acad Sci USA 2007;104(1):293-8
95. Gregory JA, Topol AB, Doerner DZ, et al. Alga-produced cholera toxin-Pfs25 fusion proteins as oral vaccines. Appl Environ Microbiol 2013;79(13):3917-25
96. Arakawa T, Komesu A, Otsuki H, et al. Nasal immunization with a malaria transmission-blocking vaccine candidate, Pfs25, induces complete protective immunity in mice against field isolates of Plasmodium falciparum. Infect Immun 2005;73(11):7375-80
97. Shimp RL Jr., Rowe C, Reiter K, et al. Development of a Pfs25-EPA malaria transmission blocking vaccine as a chemically conjugated nanoparticle. Vaccine 2013;31(28):2954-62
98. Qian F, Aebig JA, Reiter K, et al. Enhanced antibody responses to Plasmodium falciparum Pfs28 induced in mice by conjugation to ExoProtein A of Pseudomonas aeruginosa with an improved procedure. Microbes Infect 2009;11(3): 408-12
99. Testing Pfs25-EPA/Alhydrogel as a potential malaria transmission blocking vaccine. Available from: http://clinicaltrials.gov/show/NCT01867463
100. Jones RM, Chichester JA, Mett V, et al. A plant-produced Pfs25 VLP malaria vaccine candidate induces persistent transmission blocking antibodies against Plasmodium falciparum in immunized mice. PLoS One 2013;8(11):e79538
101. Safety and immunogenicity of plant-derived Pfs25 VLP-FhCMB malaria transmission blocking vaccine in healthy adults. Available from: http://clinicaltrials.gov/show/NCT02013687
102. Kaslow DC. Transmission-blocking vaccines. Chem Immunol 2002;80:287-307
103. Goodman AL, Blagborough AM, Biswas S, et al. A viral vectored prime-boost immunization regime targeting the malaria Pfs25 antigen induces transmission-blocking activity. PLoS One 2011;6(12):e29428
104. Biswas S, Li Y, Miura S, et al. Enhancing Antibody Immunogenicity of Transmission-Blocking Malaria Vaccines. In 62nd Annual Meeting: american Society of Tropical Medicine and Hygiene. Washington D.C; 2013; The American Journal of Tropical Medicine and Hygiene
105. Gardner MJ, Hall N, Fung E, et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002;419(6906):498-511
106. Carlton JM, Adams JH, Silva JC, et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 2008;455(7214):757-63
107. Young JA, Fivelman QL, Blair PL, et al. The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol Biochem Parasitol 2005; 143(1):67-79
108. Silvestrini F, Bozdech Z, Lanfrancotti A, et al. Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Mol Biochem Parasitol 2005; 143(1):100-10
109. Lasonder E, Ishihama Y, Andersen JS, et al. Analysis of the Plasmodium falciparum proteome by high-Accuracy mass spectrometry. Nature 2002;419(6906): 537-42
110. Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev 2011;24(2):377-410
111. Xu X, Dong Y, Abraham EG, et al. Transcriptome analysis of Anopheles stephensi-Plasmodium berghei interactions. Mol Biochem Parasitol 2005;142(1):76-87
112. Le Roch KG, Johnson JR, Florens L, et al. Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res 2004;14(11):2308-18
113. Hall N, Karras M, Raine JD, et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 2005; 307(5706):82-6
114. Khan SM, Franke-Fayard B, Mair GR, et al. Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 2005; 121(5):675-87
115. Lal K, Prieto JH, Bromley E, et al. Characterisation of Plasmodium invasive organelles; an ookinete microneme proteome. Proteomics 2009;9(5):1142-51
116. Dinglasan RR, Devenport M, Florens L, et al. The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochem Mol Biol 2009;39(2):125-34
117. Parish LA, Colquhoun DR, Ubaida Mohien C, et al. Ookinete-interacting proteins on the microvillar surface are partitioned into detergent resistant membranes of Anopheles gambiae midguts. J Proteome Res 2011; 10(11):5150-62
118. Templeton TJ, Kaslow DC. Identification of additional members define a Plasmodium falciparum gene superfamily which includes Pfs48/45 and Pfs230. Mol Biochem Parasitol 1999;101(1-2):223-7
119. Thompson J, Janse CJ, Waters AP. Comparative genomics in Plasmodium: a tool for the identification of genes and functional analysis. Mol Biochem Parasitol 2001;118(2):147-54
120. Pradel G. Proteins of the malaria parasite sexual stages: expression, function and potential for transmission blocking strategies. Parasitology 2007;134(Pt.14): 1911-29
121. van Dijk MR, Douradinha B, Franke-Fayard B, et al. Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci USA 2005;102(34):12194-9
122. Ishino T, Chinzei Y, Yuda M. Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Mol Microbiol 2005;58(5): 1264-75
123. Sanders PR, Gilson PR, Cantin GT, et al. Distinct protein classes including novel merozoite surface antigens in Raft-like membranes of Plasmodium falciparum. J Biol Chem 2005;280(48):40169-76
124. Tonkin ML, Arredondo SA, Loveless BC, et al. Structural and biochemical characterization of Plasmodium falciparum 12 (Pf12) reveals a unique interdomain organization and the potential for an antiparallel arrangement with Pf41. J Biol Chem 2013;288(18):12805-17
125. Taechalertpaisarn T, Crosnier C, Bartholdson SJ, et al. Biochemical and functional analysis of two Plasmodium falciparum blood-stage 6-cys proteins: P12 and P41. PLoS One 2012;7(7):e41937
126. van Schaijk BC, van Dijk MR, van de Vegte-Bolmer M, et al. Pfs47, paralog of the male fertility factor Pfs48/45, is a female specific surface protein in Plasmodium falciparum. Mol Biochem Parasitol 2006;149(2):216-22
127. Molina-Cruz A, Garver LS, Alabaster A, et al. The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 2013; 340(6135):984-7
128. Liu Y, Tewari R, Ning J, et al. The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes Dev 2008; 22(8):1051-68
129. Blagborough AM, Sinden RE. Plasmodium berghei HAP2 induces strong malaria transmission-blocking immunity in vivo and in vitro. Vaccine 2009;27(38):5187-94
130. Simon N, Lasonder E, Scheuermayer M, et al. Malaria parasites co-opt human factor H to prevent complement-mediated lysis in the mosquito midgut. Cell Host Microbe 2013;13(1):29-41
131. Carter V, Shimizu S, Arai M, et al. PbSR is synthesized in macrogametocytes and involved in formation of the malaria crystalloids. Mol Microbiol 2008;68(6): 1560-9
132. Saeed S, Carter V, Tremp AZ. Dessens JT. Plasmodium berghei crystalloids contain multiple LCCL proteins. Mol Biochem Parasitol 2010;170(1):49-53
133. Raine JD, Ecker A, Mendoza J, et al. Female inheritance of malarial lap genes is essential for mosquito transmission. PLoS Pathog 2007;3(3):e30
134. Trottein F, Triglia T, Cowman AF. Molecular cloning of a gene from Plasmodium falciparum that codes for a protein sharing motifs found in adhesive molecules from mammals and plasmodia. Mol Biochem Parasitol 1995;74(2):129-41
135. Dessens JT, Beetsma AL, Dimopoulos G, et al. CTRP is essential for mosquito infection by malaria ookinetes. EMBO J 1999;18(22):6221-7
136. Yuda M, Sakaida H, Chinzei Y. Targeted disruption of the plasmodium berghei CTRP gene reveals its essential role in malaria infection of the vector mosquito. J Exp Med 1999;190(11):1711-16
137. Templeton TJ, Kaslow DC, Fidock DA. Developmental arrest of the human malaria parasite Plasmodium falciparum within the mosquito midgut via CTRP gene disruption. Mol Microbiol 2000;36(1):1-9
138. Kaneko O, Templeton TJ, Iriko H, et al. The Plasmodium vivax homolog of the ookinete adhesive micronemal protein. CTRP Parasitol Int 2006;55(3):227-31
139. Li F, Templeton TJ, Popov V, et al. Plasmodium ookinete-secreted proteins secreted through a common micronemal pathway are targets of blocking malaria transmission. J Biol Chem 2004;279(25): 26635-44
140. Nacer A, Underhill A, Hurd H. The microneme proteins CTRP and SOAP are not essential for Plasmodium berghei ookinete to oocyst transformation in vitro in a cell free system. Malar J 2008;7:82
141. Yuda M, Yano K, Tsuboi T, et al. von Willebrand Factor A domain-related protein, a novel microneme protein of the malaria ookinete highly conserved throughout Plasmodium parasites. Mol Biochem Parasitol 2001;116(1):65-72
142. Dessens JT, Side-n-Kiamos I, Mendoza J, et al. SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development. Mol Microbiol 2003;49(2):319-29
143. Ecker A, Bushell ES, Tewari R, Sinden RE. Reverse genetics screen identifies six proteins important for malaria development in the mosquito. Mol Microbiol 2008;70(1): 209-20
144. Ghosh AK, Coppens I, Gårdsvoll H, et al. Plasmodium ookinetes coopt mammalian plasminogen to invade the mosquito midgut. Proc Natl Acad Sci USA 2011; 108(41):17153-8
145. Langer RC, Li F, Popov V, et al. Monoclonal antibody against the Plasmodium falciparum chitinase, PfCHT1, recognizes a malaria transmission-blocking epitope in Plasmodium gallinaceum ookinetes unrelated to the chitinase PgCHT1. Infect Immun 2002;70(3): 1581-90
146. Li F, Patra KP, Vinetz JM. An anti-Chitinase malaria transmission-blocking single-chain antibody as an effector molecule for creating a Plasmodium falciparum-refractory mosquito. J Infect Dis 2005;192(5):878-87
147. Shahabuddin M, Toyoshima T, Aikawa M, Kaslow DC. Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinase by mosquito protease. Proc Natl Acad Sci USA 1993; 90(9):4266-70
148. Tsai YL, Hayward RE, Langer RC, et al. Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect Immun 2001; 69(6):4048-54
149. Dessens JT, Mendoza J, Claudianos C, et al. Knockout of the rodent malaria parasite chitinase pbCHT1 reduces infectivity to mosquitoes. Infect Immun 2001;69(6):4041-7
150. Kaiser K, Camargo N, Coppens I, et al. A member of a conserved Plasmodium protein family with membrane-Attack complex/perforin (MACPF)-like domains localizes to the micronemes of sporozoites. Mol Biochem Parasitol 2004;133(1):15-26
151. Ishino T, Chinzei Y, Yuda M. A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell Microbiol 2005;7(2):199-208
152. Kadota K, Ishino T, Matsuyama T, et al. Essential role of membrane-Attack protein in malarial transmission to mosquito host. Proc Natl Acad Sci USA 2004;101(46): 16310-15
153. Ecker A, Pinto SB, Baker KW, et al. Plasmodium berghei: plasmodium perforin-like protein 5 is required for mosquito midgut invasion in Anopheles stephensi. Exp Parasitol 2007;116(4):504-8
154. Deligianni E, Morgan RN, Bertuccini L, et al. A perforin-like protein mediates disruption of the erythrocyte membrane during egress of Plasmodium berghei male gametocytes. Cell Microbiol 2013;15(8): 1438-55
155. Kariu T, Ishino T, Yano K, et al. CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol Microbiol 2006;59(5):1369-79
156. Sinden RE. A proteomic analysis of malaria biology: integration of old literature and new technologies. Int J Parasitol 2004; 34(13-14):1441-50
157. Sinden RE, Billingsley PF. Plasmodium invasion of mosquito cells: hawk or dove Trends Parasitol 2001;17(5):209-12
158. Dawes EJ, Churcher TS, Zhuang S, et al. Anopheles mortality is both age-And Plasmodium-density dependent: implications for malaria transmission. Malar J 2009;8:228
159. Ramasamy MS, Ramasamy R. Effect of anti-mosquito antibodies on the infectivity of the rodent malaria parasite Plasmodium berghei to Anopheles farauti. Med Vet Entomol 1990;4(2):161-6
160. Lal AA, Schriefer ME, Sacci JB, et al. Inhibition of malaria parasite development in mosquitoes by anti-mosquito-midgut antibodies. Infect Immun 1994;62(1): 316-18
161. Lal AA, Patterson PS, Sacci JB, et al. Anti-mosquito midgut antibodies block development of Plasmodium falciparum and Plasmodium vivax in multiple species of Anopheles mosquitoes and reduce vector fecundity and survivorship. Proc Natl Acad Sci USA 2001;98(9):5228-33
162. Srikrishnaraj KA, Ramasamy R, Ramasamy MS. Antibodies to Anopheles midgut reduce vector competence for Plasmodium vivax malaria. Med Vet Entomol 1995;9(4):353-7
163. Wilkins S, Billingsley PF. Partial characterization of oligosaccharides expressed on midgut microvillar glycoproteins of the mosquito, Anopheles stephensi Liston. Insect Biochem Mol Biol 2001;31(10): 937-48
164. Dinglasan RR, Fields I, Shahabuddin M, et al. Monoclonal antibody MG96 completely blocks Plasmodium yoelii development in Anopheles stephensi. Infect Immun 2003;71(12):6995-7001
165. Lavazec C, Bourgouin C. Mosquito-based transmission blocking vaccines for interrupting Plasmodium development. Microbes Infect 2008;10(8):845-9
166. Bonnet S, Pre-vot G, Jacques JC, et al. Transcripts of the malaria vector Anopheles gambiae that are differentially regulated in the midgut upon exposure to invasive stages of Plasmodium falciparum. Cell Microbiol 2001;3(7):449-58
167. Lavazec C, Bonnet S, Thiery I, et al. cpbAg1 encodes an active carboxypeptidase B expressed in the midgut of Anopheles gambiae. Insect Mol Biol 2005;14(2): 163-74
168. Lavazec C, Boudin C, Lacroix R, et al. Carboxypeptidases B of Anopheles gambiae as targets for a Plasmodium falciparum transmission-blocking vaccine. Infect Immun 2007;75(4):1635-42
169. Dinglasan RR, Kalume DE, Kanzok SM, et al. Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen. Proc Natl Acad Sci USA 2007;104(33):13461-6
170. Armistead JS, Morlais I, Mathias DK, et al. Antibodies to a Single, Conserved Epitope in Anopheles APN1 Inhibit Universal Transmission of Plasmodium falciparum and Plasmodium vivax Malaria. Infect Immun 2014;82(2):818-29
171. Williams AR, Zakutansky SE, Miura K, et al. Immunisation against a serine protease inhibitor reduces intensity of Plasmodium berghei infection in mosquitoes. Int J Parasitol 2013;43(11):869-74
172. Whitten MM, Shiao SH, Levashina EA. Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol 2006;28(4):121-30
173. Dinglasan RR, Jacobs-Lorena M. Flipping the paradigm on malaria transmission-blocking vaccines. Trends Parasitol 2008;24(8):364-70
174. Cirimotich CM, Dong Y, Garver LS, et al. Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol 2010;34(4):387-95
175. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 2009; 139(7):1268-78
176. Tsuboi T, Takeo S, Arumugam TU, et al. The wheat germ cell-free protein synthesis system: a key tool for novel malaria vaccine candidate discovery. Acta Trop 2010; 114(3):171-6
177. Gowda DC, Davidson EA. Protein glycosylation in the malaria parasite. Parasitol Today 1999;15(4):147-52
178. Aguiar JC, LaBaer J, Blair PL, et al. High-throughput generation of P. falciparum functional molecules by recombinational cloning. Genome Res 2004;14(10B):2076-82
179. Mehlin C, Boni E, Buckner FS, et al. Heterologous expression of proteins from Plasmodium falciparum: results from 1000 genes. Mol Biochem Parasitol 2006; 148(2):144-60
180. Vedadi M, Lew J, Artz J, et al. Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms. Mol Biochem Parasitol 2007;151(1):100-10
181. Mu J, Awadalla P, Duan J, et al. Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat Genet 2007;39(1): 126-30
182. Doolan DL, Mu Y, Unal B, et al. Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics 2008;8(22):4680-94
183. Arumugam TU, Ito D, Takashima E, et al. Application of wheat germ cell-free protein expression system for novel malaria vaccine candidate discovery. Expert Rev Vaccines 2014;13(1):75-85
184. Crosnier C, Wanaguru M, McDade B, et al. A library of functional recombinant cell-surface and secreted P. falciparum merozoite proteins. Mol Cell Proteomics 2013;12(12):3976-86
185. Zenonos ZA, Rayner JC, Wright GJ. Towards a comprehensive Plasmodium falciparum merozoite cell surface and secreted recombinant protein library. Malar J 2014;13(1):93
186. Douglas AD, Williams AR, Illingworth JJ, et al. The blood-stage malaria antigen PfRH5 is susceptible to vaccine-inducible cross-strain neutralizing antibody. Nat Commun 2011;2:601
187. Manske M, Miotto O, Campino S, et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 2012 487 7407 375-9
188. Williamson KC, Criscio MD, Kaslow DC. Cloning and expression of the gene for Plasmodium falciparum transmission-blocking target antigen, Pfs230. Mol Biochem Parasitol 1993;58(2):355-8
189. Vincent AA, Fanning S, Caira FC, Williamson KC. Immunogenicity of malaria transmission-blocking vaccine candidate, y230.CA14 following crosslinking in the presence of tetanus toxoid. Parasite Immunol 1999;21(11):573-81
190. Bustamante PJ, Woodruff DC, Oh J, et al. Differential ability of specific regions of Plasmodium falciparum sexual-stage antigen, Pfs230, to induce malaria transmission-blocking immunity. Parasite Immunol 2000;22(8):373-80
191. Fanning SL, Czesny B, Sedegah M, et al. A glycosylphosphatidylinositol anchor signal sequence enhances the immunogenicity of a DNA vaccine encoding Plasmodium falciparum sexual-stage antigen, Pfs230. Vaccine 2003;21(23):3228-35
192. Tachibana M, Sato C, Otsuki H, et al. Plasmodium vivax gametocyte protein Pvs230 is a transmission-blocking vaccine candidate. Vaccine 2012;30(10):1807-12
193. Barr PJ, Green KM, Gibson HL, et al. Recombinant Pfs25 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in experimental animals. J Exp Med 1991; 174(5):1203-8
194. Coban C, Ishii KJ, Stowers AW, et al. Effect of CpG oligodeoxynucleotides on the immunogenicity of Pfs25, a Plasmodium falciparum transmission-blocking vaccine antigen. Infect Immun 2004;72(1):584-8
195. Arakawa T, Tachibana M, Miyata T, et al. Malaria ookinete surface protein-based vaccination via the intranasal route completely blocks parasite transmission in both passive and active vaccination regimens in a rodent model of malaria infection. Infect Immun 2009;77(12):5496-500
196. Miles AP, Zhang Y, Saul A, Stowers AW. Large-scale purification and characterization of malaria vaccine candidate antigen Pvs25H for use in clinical trials. Protein Expr Purif 2002;25(1):87-96
197. Arakawa T, Tsuboi T, Kishimoto A, et al. Serum antibodies induced by intranasal immunization of mice with Plasmodium vivax Pvs25 co-Administered with cholera toxin completely block parasite transmission to mosquitoes. Vaccine 2003;21(23):3143-8
198. Sattabongkot J, Tsuboi T, Hisaeda H, et al. Blocking of transmission to mosquitoes by antibody to Plasmodium vivax malaria vaccine candidates Pvs25 and Pvs28 despite antigenic polymorphism in field isolates. Am J Trop Med Hyg 2003;69(5):536-41
199. Arevalo-Herrera M, Solarte Y, Yasnot MF, et al. Induction of transmission-blocking immunity in Aotus monkeys by vaccination with a Plasmodium vivax clinical grade PVS25 recombinant protein. Am J Trop Med Hyg 2005;73(5 Suppl):32-7
200. Collins WE, Barnwell JW, Sullivan JS, et al. Assessment of transmission-blocking activity of candidate Pvs25 vaccine using gametocytes from chimpanzees. Am J Trop Med Hyg 2006;74(2):215-21
201. Gozar MM, Muratova O, Keister DB, et al. Plasmodium falciparum: immunogenicity of alum-Adsorbed clinical-grade TBV25-28, a yeast-secreted malaria transmission-blocking vaccine candidate. Exp Parasitol 2001;97(2): 61-9
202. Qian F, Wu Y, Muratova O, et al. Conjugating recombinant proteins to Pseudomonas aeruginosa ExoProtein A: a strategy for enhancing immunogenicity of malaria vaccine candidates. Vaccine 2007; 25(20):3923-33
203. Qian F, Rausch KM, Muratova O, et al. Addition of CpG ODN to recombinant Pseudomonas aeruginosa ExoProtein A conjugates of AMA1 and Pfs25 greatly increases the number of responders. Vaccine 2008;26(20):2521-7
204. Kubler-Kielb J, Majadly F, Biesova Z, et al. A bicomponent Plasmodium falciparum investigational vaccine composed of protein-peptide conjugates. Proc Natl Acad Sci USA 2010;107(3):1172-7
205. Miyata T, Harakuni T, Tsuboi T, et al. Plasmodium vivax ookinete surface protein Pvs25 linked to cholera toxin B subunit induces potent transmission-blocking immunity by intranasal as well as subcutaneous immunization. Infect Immun 2010;78(9):3773-82
206. Grifantini R, Finco O, Bartolini E, et al. Multi-plasmid DNA vaccination avoids antigenic competition and enhances immunogenicity of a poorly immunogenic plasmid. Eur J Immunol 1998;28(4): 1225-32
207. Lobo CA, Dhar R, Kumar N. Immunization of mice with DNA-based Pfs25 elicits potent malaria transmission-blocking antibodies. Infect Immun 1999;67(4):1688-93
208. Coban C, Philipp MT, Purcell JE, et al. Induction of Plasmodium falciparum transmission-blocking antibodies in nonhuman primates by a combination of DNA and protein immunizations. Infect Immun 2004;72(1):253-9
209. LeBlanc R, Vasquez Y, Hannaman D, et al. Markedly enhanced immunogenicity of a Pfs25 DNA-based malaria transmission-blocking vaccine by in vivo electroporation. Vaccine 2008;26(2):185-92
210. Kumar R, Nyakundi R, Kariuki T, et al. Functional evaluation of malaria Pfs25 DNA vaccine by in vivo electroporation in olive baboons. Vaccine 2013;31(31):3140-7
211. Kaslow DC, Isaacs SN, Quakyi IA, et al. Induction of Plasmodium falciparum transmission-blocking antibodies by recombinant vaccinia virus. Science 1991; 252(5010):1310-13
212. Tiwari S, Goyal AK, Mishra N, et al. Development and characterization of novel carrier gel core liposomes based transmission blocking malaria vaccine. J Control Release 2009;140(2):157-65
213. Mlambo G, Kumar N, Yoshida S. Functional immunogenicity of baculovirus expressing Pfs25, a human malaria transmission-blocking vaccine candidate antigen. Vaccine 2010;28(43):7025-9
214. Rawlings DJ, Kaslow DC. Adjuvant-dependent immune response to malarial transmission-blocking vaccine candidate antigens. J Exp Med 1992;176(5): 1483-7
215. Gholizadeh S, Basseri HR, Zakeri S, et al. Cloning, expression and transmission-blocking activity of anti-PvWARP, malaria vaccine candidate, in Anopheles stephensi mysorensis. Malar J 2010;9:158
216. Takeo S, Hisamori D, Matsuda S, et al. Enzymatic characterization of the Plasmodium vivax chitinase, a potential malaria transmission-blocking target. Parasitol Int 2009;58(3):243-8