A scalable assessment of Plasmodium falciparum transmission in the standard membrane-feeding assay, using transgenic parasites expressing green fluorescent protein-luciferase

Journal of Infectious Diseases

Volumn 210, Issue 9, 2014, Pages 1456-1463

  Stone, Will J R ^a   Churcher, Thomas S ^c   Graumans, Wouter ^a   Van Gemert, Geert Jan ^a   Vos, Martijn W ^a,b   Lanke, Kjerstin H W ^a   Van De Vegte Bolmer, Marga G ^a   Siebelink Stoter, Rianne ^a   Dechering, Koen J ^b   Vaughan, Ashley M ^e   Camargo, Nelly ^e   Kappe, Stefan H I ^e   Sauerwein, Robert W ^a,b   Bousema, Teun ^a,d  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Current affiliation: TropIQ Health Sciences   (Netherlands)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Anopheles; Infectivity; Luminescence; Malaria; Mosquito feeding assay; Mosquitoes; Oocysts; P. falciparum; SMFA; Transmission reducing activity

Indexed keywords

GREEN FLUORESCENT PROTEIN; LUCIFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANOPHELES GAMBIAE; ANOPHELES STEPHENSI; ARTICLE; BIOASSAY; CONTROLLED STUDY; INFECTION RATE; LUMINESCENCE; MICROSCOPY; NONHUMAN; OOCYST; PARASITE TRANSMISSION; PLASMODIUM FALCIPARUM; PREVALENCE; PRIORITY JOURNAL; STANDARD MEMBRANE FEEDING ASSAY; TRANSGENIC ORGANISM; TRANSMISSION REDUCING ACTIVITY; ANIMAL; ANOPHELES; DIAGNOSTIC USE; FEMALE; GENETICS; HUMAN; MALARIA FALCIPARUM; PARASITOLOGY; PHYSIOLOGY; TRANSMISSION;

ANIMALS; ANOPHELES; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MALARIA, FALCIPARUM; MICROSCOPY; ORGANISMS, GENETICALLY MODIFIED; PLASMODIUM FALCIPARUM;

EID: 84922031896     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu271     Document Type: Article

References (25)

1. World Health Organization. World malaria report. Geneva: WHO, 2013.
2. Griffin JT, Hollingsworth TD, Okell LC, et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med 2010; 7:e1000324.
3. Moonen B, Cohen JM, Snow RW, et al. Operational strategies to achieve and maintain malaria elimination. Lancet 2010; 376:1592-603.
4. Vannice K, Brown G, Akanmori B, Moorthy V. MALVAC 2012 scientific forum: accelerating development of second-generation malaria vaccines. Malar J 2012; 11:372.
5. Churcher TS, Blagborough AM, Delves M, et al. Measuring the blockade of malaria transmission - An analysis of the Standard Membrane Feeding Assay. Int J Parasitol 2012; 42:1037-44.
6. van der Kolk M, de Vlas SJ, Saul A, van de Vegte-bolmer M, Eling WM, Sauerwein W. Evaluation of the standard membrane feeding assay (SMFA) for the determination of malaria transmission-reducing activity using empirical data. Parasitology 2005; 130:13-22.
7. Delves M, Sinden R. A semi-automated method for counting fluorescent malaria oocysts increases the throughput of transmission blocking studies. Malar J 2010; 9:35.
8. Bell AS, Ranford-Cartwright LC. A real-time PCR assay for quantifying Plasmodium falciparum infections in the mosquito vector. Int J Parasitol 2004; 34:795-802.
9. Miura K, Deng B, Tullo G, et al. Qualification of standard membrane-feeding assay with Plasmodium falciparum malaria and potential improvements for future assays. PLoS One 2013; 8:e57909.
10. Janse CJ, Franke-Fayard B, Mair GR, et al. High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol Biochem Parasitol 2006; 145:60-70.
11. Delves MJ, Ramakrishnan C, Blagborough AM, Leroy D, Wells TNC, Sinden RE. A high-throughput assay for the identification of malarial transmission-blocking drugs and vaccines. Int J Parasitol 2012; 42:999-1006.
12. Vaughan AM, Mikolajczak SA, Camargo N, et al. A transgenic Plasmodium falciparum NF54 strain that expresses GFP-luciferase throughout the parasite life cycle. Mol Biochem Parasitol 2012; 186:143-7.
13. Ponnudurai T, Lensen AHW, Leeuwenberg ADEM, Meuwissen JHET. Cultivation of fertile Plasmodium falciparum gametocytes in semiautomated systems. 1. Static cultures. Trans R Soc Trop Med Hyg 1982; 76:812-8.
14. Ponnudurai T, Lensen AHW, Van Gemert GJA, Bensink MPE, Bolmer M, Meuwissen JHET. Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology 1989; 98:165-73.
15. Feldmann AM, Ponnudurai T. Selection of Anopheles stephensi for refractoriness and susceptibility to Plasmodium falciparum. Med Vet Entomol 1989; 3:41-52.
16. Vermeulen AN, Ponnudurai T, Beckers PJ, Verhave JP, Smits MA, Meuwissen JH. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med 1985; 162:1460-76.
17. Roeffen W, Teelen K, van As J, vd Vegte-Bolmer M, Eling W, Sauerwein R. Plasmodium falciparum: production and characterization of rat monoclonal antibodies specific for the sexual-stage Pfs48/45 antigen. Exp Parasitol 2001; 97:45-9.
18. Saeed M, Roeffen W, Alexander N, Drakeley CJ, Targett GAT, Sutherland CJ. Plasmodium falciparum antigens on the surface of the gametocyte-infected erythrocyte. PLoS One 2008; 3:e2280.
19. Molina-Cruz A, Garver LS, Alabaster A, et al. The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 2013; 340:984-7.
20. Bolker BM, Brooks ME, Clark CJ, et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 2009; 24:127-35.
21. Medley GF, Sinden RE, Fleck S, Billingsley PF, Tirawanchap N, Rodriguez MH. Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 1993; 106:441-9.
22. van der Kolk M, de Vlas SJ, Sauerwein RW. Reduction and enhancement of Plasmodium falciparum transmission by endemic human sera. Int J Parasitol 2006; 36:1091-5.
23. World Health Organization. Measures of efficacy of anti-malaria interventions against malaria transmission. WHO technical series. Geneva: WHO, 2010.
24. Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun 2012; 3. http://dx.doi.org/10.1038/ncomms2241. doi:10.1038/ncomms2241.
25. Bousema T, Churcher TS, Morlais I, Dinglasan RR. Can field-based mosquito feeding assays be used for evaluating transmission-blocking interventions? Trends Parasitol 2013; 29:53-9.