An assay to probe Plasmodium falciparum growth, transmission stage formation and early gametocyte development

Nature Protocols

Volumn 10, Issue 8, 2015, Pages 1131-1142

  Brancucci, Nicolas M B ^a   Goldowitz, Ilana ^a   Buchholz, Kathrin ^b   Werling, Kristine ^a   Marti, Matthias ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE;

ARTICLE; ASEXUAL REPRODUCTION; BIOASSAY; CONTROLLED STUDY; CULTURE MEDIUM; FLOW CYTOMETRY; GAMETOCYTE; HUMAN; HUMAN CELL; MICROBIAL GROWTH; NONHUMAN; PARASITE DEVELOPMENT; PARASITE TRANSMISSION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENTIATION; MALARIA FALCIPARUM; PARASITOLOGY; PHYSIOLOGY; PROCEDURES; TRANSMISSION;

PLASMODIUM FALCIPARUM;

FLOW CYTOMETRY; MALARIA, FALCIPARUM; PARASITOLOGY; PLASMODIUM FALCIPARUM;

EID: 84937951556     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2015.072     Document Type: Article

References (44)

1. Alonso, P.L. et al. A research agenda to underpin malaria eradication. PLoS Med. 8, e1000406 (2011
2. Sowunmi, A., Adedeji, A.A., Gbotosho, G.O., Fateye, B.A. &Happi, T.C. Effects of pyrimethamine-sulphadoxine, chloroquine plus chlorpheniramine, and amodiaquine plus pyrimethamine-sulphadoxine on gametocytes during and after treatment of acute, uncomplicated malaria in children. Mem. Inst. Oswaldo Cruz 101, 887-893 (2006
3. Sowunmi, A. &Fateye, B.A. Plasmodium falciparum gametocytaemia in Nigerian children: before, during and after treatment with antimalarial drugs. Trop. Med. Int. Health 8, 783-792 (2003
4. Fehintola, F.A., Balogun, S.T. &Adeoye, S.B. Intermittent preventive treatment during pregnancy with sulphadoxine-pyrimethamine may promote Plasmodium falciparum gametocytogenesis. Med. Princ. Pract. 21, 63-67 (2012
5. Buckling, A., Ranford-Cartwright, L.C., Miles, A. &Read, A.F. Chloroquine increases Plasmodium falciparum gametocytogenesis in vitro. Parasitology 118 (Part 4), 339-346 (1999
6. Price, R. et al. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am. J. Trop. Med. Hyg. 60, 1019-1023 (1999
7. Dechy-Cabaret, O. &Benoit-Vical, F. Effects of antimalarial molecules on the gametocyte stage of Plasmodium falciparum: the debate. J. Med. Chem. 55, 10328-10344 (2012
8. Bell, A.S. et al. Enhanced transmission of drug-resistant parasites to mosquitoes following drug treatment in rodent malaria. PLoS ONE 7, e37172 (2012
9. World Health Organization. WHO Malaria Report 2014. http://www.who.int/malaria/publications/world-malaria-report-2014/en/(2014
10. Buchholz, K. et al. A high-throughput screen targeting malaria transmission stages opens new avenues for drug development. J. Infect. Dis. 203, 1445-1453 (2011
11. Hanson, K.K. et al. Torins are potent antimalarials that block replenishment of Plasmodium liver stage parasitophorous vacuole membrane proteins. Proc. Natl. Acad. Sci. USA 110, E2838-E2847 (2013
12. da Cruz, F.P. et al. Drug screen targeted at Plasmodium liver stages identifies a potent multistage antimalarial drug. J. Infect. Dis. 205, 1278-1286 (2012
13. Kafsack, B.F. et al. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 507, 248-252 (2014
14. Sinha, A. et al. A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 507, 253-257 (2014
15. Coleman, B.I. et al. A Plasmodium falciparum histone deacetylase regulates antigenic variation and gametocyte conversion. Cell Host Microbe 16, 177-186 (2014
16. Brancucci, N.M., Witmer, K., Schmid, C. &Voss, T.S. A var gene upstream element controls protein synthesis at the level of translation initiation in Plasmodium falciparum. PLoS ONE 9, e100183 (2014
17. Mantel, P.Y. &Marti, M. The role of extracellular vesicles in Plasmodium and other protozoan parasites. Cell. Microbiol. 16, 344-354 (2014
18. Regev-Rudzki, N. et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 153, 1120-1133 (2013
19. Carter, R. &Miller, L.H. Evidence for environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bull. World Health Organ. 57 (suppl. 1), 37-52 (1979
20. Dyer, M. &Day, K. Expression of Plasmodium falciparum trimeric G proteins and their involvement in switching to sexual development. Mol. Biochem. Parasitol. 108, 67-78 (2000
21. Peatey, C.L., Dixon, M.W., Gardiner, D.L. &Trenholme, K.R. Temporal evaluation of commitment to sexual development in Plasmodium falciparum. Malar. J. 12, 134 (2013
22. Trager, W. &Gill, G.S. Plasmodium falciparum gametocyte formation in vitro: its stimulation by phorbol diesters and by 8-bromo cyclic adenosine monophosphate. J. Protozool. 36, 451-454 (1989
23. Inselburg, J. Stage-specific inhibitory effect of cyclic AMP on asexual maturation and gametocyte formation of Plasmodium falciparum. J. Parasitol. 69, 592-597 (1983
24. Read, L.K. &Mikkelsen, R.B. Comparison of adenylate cyclase and cAMP-dependent protein kinase in gametocytogenic and nongametocytogenic clones of Plasmodium falciparum. J. Parasitol. 77, 346-352 (1991
25. Chaubey, S., Grover, M. &Tatu, U. Endoplasmic reticulum stress triggers gametocytogenesis in the malaria parasite. J. Biol. Chem. 289, 16662-16674 (2014
26. Carter, L.M. et al. Stress and sex in malaria parasites: why does commitment vary? Evol. Med. Public Health 2013, 135-147 (2013
27. Ankarklev, J., Brancucci, N.M., Goldowitz, I., Mantel, P.Y. &Marti, M. Sex: how malaria parasites get turned on. Curr. Biol. 24, R368-R370 (2014
28. Chevalley, S., Coste, A., Lopez, A., Pipy, B. &Valentin, A. Flow cytometry for the evaluation of anti-plasmodial activity of drugs on Plasmodium falciparum gametocytes. Malar. J. 9, 49 (2010
29. Sanders, N.G., Sullivan, D.J., Mlambo, G., Dimopoulos, G. &Tripathi, A.K. Gametocytocidal screen identifies novel chemical classes with Plasmodium falciparum transmission blocking activity. PLoS ONE 9, e105817 (2014
30. Peatey, C.L., Spicer, T.P., Hodder, P.S., Trenholme, K.R. &Gardiner, D.L. A high-throughput assay for the identification of drugs against late-stage Plasmodium falciparum gametocytes. Mol. Biochem. Parasitol. 180, 127-131 (2011
31. Lelievre, J. et al. Activity of clinically relevant antimalarial drugs on Plasmodium falciparum mature gametocytes in an ATP bioluminescence transmission blocking assay. PLoS ONE 7, e35019 (2012
32. Tanaka, T.Q. et al. A quantitative high throughput assay for identifying gametocytocidal compounds. Mol. Biochem. Parasitol. 188, 20-25 (2013
33. DAlessandro, S. et al. A Plasmodium falciparum screening assay for anti-gametocyte drugs based on parasite lactate dehydrogenase detection. J. Antimicrob. Chemother. 68, 2048-2058 (2013
34. Lucantoni, L., Duffy, S., Adjalley, S.H., Fidock, D.A. &Avery, V.M. Identification of MMV malaria box inhibitors of Plasmodium falciparum early-stage gametocytes using a luciferase-based high-throughput assay. Antimicrob. Agents Chemother. 57, 6050-6062 (2013
35. Wang, Z. et al. A flow cytometry-based quantitative drug sensitivity assay for all Plasmodium falciparum gametocyte stages. PLoS ONE 9, e93825 (2014
36. Silvestrini, F. et al. Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Mol. Biochem. Parasitol. 143, 100-110 (2005
37. Aingaran, M. et al. Host cell deformability is linked to transmission in the human malaria parasite Plasmodium falciparum. Cell. Microbiol. 14, 983-993 (2012
38. Khandelwal, S. &Saxena, R.K. Age-dependent increase in green autofluorescence of blood erythrocytes. J. Biosci. 32, 1139-1145 (2007
39. Elliott, S.R. et al. Antibody recognition of heterologous variant surface antigens after a single Plasmodium falciparum infection in previously naive adults. Am. J. Trop. Med. Hyg. 76, 860-864 (2007
40. Hommel, M. et al. Evaluation of the antigenic diversity of placenta-binding Plasmodium falciparum variants and the antibody repertoire among pregnant women. Infect. Immun. 78, 1963-1978 (2010
41. Zhang, J.H., Chung, T.D. &Oldenburg, K.R. A simple statistical parameter for use in evaluation and validation of high-throughput screening assays. J. Biomol. Screen. 4, 67-73 (1999
42. Moll, K., Ljungstroem, I., Perlmann, H., Scherf, A. &Wahlgren, M. Methods in Malaria Research 6th edn. http://www.mr4.org/Publications/MethodsinMalariaResearch.aspx (MR4/ATCC, 2013
43. Alano, P. et al. Plasmodium falciparum: parasites defective in early stages of gametocytogenesis. Exp. Parasitol. 81, 227-235 (1995
44. Chaal, B.K., Gupta, A.P., Wastuwidyaningtyas, B.D., Luah, Y.H. &Bozdech, Z. Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle. PLoS Pathog. 6, e1000737 (2010