Identification and classification of the malaria parasite blood developmental stages, using imaging flow cytometry

Methods

Volumn 112, Issue , 2017, Pages 157-166

  Dekel, Elya ^a   Rivkin, Anna ^a   Heidenreich, Meta ^a   Nadav, Yotam ^a   Ofir Birin, Yifat ^a   Porat, Ziv ^a   Regev Rudzki, Neta ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Blood stage; Gametocytes; Imaging flow cytometry; Malaria; Plasmodium falciparum

Indexed keywords

ARTICLE; CELL COUNT; CELL POPULATION; CELL STRUCTURE; CLASSIFICATION; DEVELOPMENTAL STAGE; ERYTHROCYTE; FLOW CYTOMETRY; GAMETOCYTE; IMAGE ANALYSIS; IMAGING FLOW CYTOMETRY; MEASUREMENT ACCURACY; NONHUMAN; PARASITE IDENTIFICATION; PARASITEMIA; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; RELIABILITY; RING STAGE; SCHIZONT; TROPHOZOITE; VALIDATION STUDY; CELL CULTURE; CHEMISTRY; GIEMSA STAIN; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMAGE CYTOMETRY; LIFE CYCLE STAGE; PARASITOLOGY; PHYSIOLOGY; PROCEDURES; STAINING; ULTRASTRUCTURE;

BENZIMIDAZOLE DERIVATIVE; BENZOTHIAZOLE DERIVATIVE; BISBENZIMIDE ETHOXIDE TRIHYDROCHLORIDE; FLUORESCENT DYE; QUINOLINE DERIVATIVE; THIAZOLE ORANGE;

AZURE STAINS; BENZIMIDAZOLES; BENZOTHIAZOLES; CELLS, CULTURED; ERYTHROCYTES; FLOW CYTOMETRY; FLUORESCENT DYES; HUMANS; IMAGE CYTOMETRY; LIFE CYCLE STAGES; PLASMODIUM FALCIPARUM; QUINOLINES; STAINING AND LABELING;

EID: 85003749542     PISSN: 10462023     EISSN: 10959130     Source Type: Journal    
DOI: 10.1016/j.ymeth.2016.06.021     Document Type: Article

References (37)

1. [1] Ménard, R., Tavares, J., Cockburn, I., Markus, M., Zavala, F., Looking under the skin: the first steps in malarial infection and immunity. Nat. Rev. Microbiol., 11, 2013.
2. [2] Angrisano, F., Tan, Y.-H., Sturm, A., McFadden, G.I., Baum, J., Malaria parasite colonisation of the mosquito midgut – placing the Plasmodium ookinete centre stage. Int. J. Parasitol. 42:6 (2012), 519–527.
3. [3] Scheibel, L.W., Adler, A., Trager, W., Tetraethylthiuram disulfide (Antabuse) inhibits the human malaria parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 76:10 (1979), 5303–5307.
4. [4] Adjalley, S.H., Johnston, G.L., Li, T., Eastman, R.T., Ekland, E.H., Eappen, A.G., Richman, A., Sim, B.K.L., Lee, M.C.S., Hoffman, S.L., Fidock, D.A., Plus, P.N.A.S., Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc. Natl. Acad. Sci. 108:47 (2011), E1214–E1223.
5. [5] Garcia, L., Determination of Parasitemia Protocol. 2001 pp. 1–4.
6. [6] Jang, J.W., Kim, J.Y., Yoon, J., Yoon, S.Y., Cho, C.H., Han, E.T., An, S.S.A., Lim, C.S., Flow cytometric enumeration of parasitemia in cultures of Plasmodium falciparum stained with SYBR green I and CD235A. Sci. World. J., 2014, 2014.
7. [7] Corbett, Y., Herrera, L., Gonzalez, J., Cubilla, L., Capson, T.L., Coley, P.D., Kursar, T.A., Romero, L.I., Ortega-Barria, E., A novel DNA-based microfluorimetric method to evaluate antimalarial drug activity. Am. J. Trop. Med. Hyg. 70:2 (2004), 119–124.
8. [8] Smeijsters, L.J., Zijlstra, N.M., Franssen, F.F., Overdulve, J.P., Simple, fast, and accurate fluorometric method to determine drug susceptibility of Plasmodium falciparum in 24-well suspension cultures. Antimicrob. Agents Chemother. 40:4 (1996), 835–838.
9. [9] Hare, J.D., Two-color flow-cytometric analysis of the growth cycle of Plasmodium falciparum in vitro: identification of cell cycle compartments. J. Histochem. Cytochem. 34:12 (1986), 1651–1658.
10. [10] Staalsoe, T., Giha, H.A., Dodoo, D., Theander, T.G., Hviid, L., Detection of antibodies to variant antigens on Plasmodium falciparum-infected erythrocytes by flow cytometry. Cytometry 35:4 (1999), 329–336.
11. [11] Billker, O., Dechamps, S., Tewari, R., Wenig, G., Franke-Fayard, B., Brinkmann, V., Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117:4 (2004), 503–514.
12. [12] Zuba-surma, E.K., Kucia, M., Abdel-latif, A., Lillard, J.W. Jr., Ratajczak, M.Z., The ImageStream System: a key step to a new era in imaging. Folia Histochem. Cytobiol. 45:4 (2007), 279–290.
13. [13] Zuba-Surma, E., Kucia, M., Ratajczak, M., ‘Decoding the Dots’: the ImageStream system (ISS) as a novel and powerful tool for flow cytometric analysis. Open Life Sci. 3:1 (2008), 1–10.
14. [14] Basiji, D.A., Ortyn, W.E., Liang, L., Venkatachalam, V., Morrissey, P., Cellular image analysis and imaging by flow cytometry. Clin. Lab. Med. 27:3 (2007), 653–670.
15. [15] Filby, A., Davies, D., Reporting imaging flow cytometry data for publication: why mask the detail?. Cytom. Part A 81A:8 (2012), 637–642.
16. [16] Grimberg, B.T., Erickson, J.J., Sramkoski, R.M., Jacobberger, J.W., Zimmerman, P.A., Monitoring Plasmodium falciparum growth and development by UV flow cytometry using an optimized Hoechst-thiazole orange staining strategy. Cytom. Part A 73A:6 (2008), 546–554.
17. [17] Franklin, R.M., Brun, R., Grieder, A., Microscopic and flow cytophotometric analysis of parasitemia in cultures of Plasmodium falciparum vitally stained with Hoechst 33342–application to studies of antimalarial agents. Zeitschrift für Parasitenkd 72:2 (1986), 201–212 (Berlin, Ger.).
18. [18] Makler, M.T., Lee, L.G., Thiazole orange: a new dye for Plasmodium species analysis. Cytometry 8:6 (1987), 568–570.
19. [19] Brancucci, N.M.B., Goldowitz, I., Buchholz, K., Werling, K., Marti, M., An assay to probe Plasmodium falciparum growth, transmission stage formation and early gametocyte development. Nat. Protoc. 10:8 (2015), 1131–1142.
20. [20] Jang, J.W., Kim, J.Y., Yoon, J., Yoon, S.Y., Cho, C.H., Han, E.T., An, S.S.A., Lim, C.S., Flow cytometric enumeration of parasitemia in cultures of Plasmodium falciparum stained with SYBR green i and CD235A. Sci. World J., 2014, 2014.
21. [21] Philipp, S., Oberg, H.H., Janssen, O., Leippe, M., Gelhaus, C., Isolation of erythrocytes infected with viable early stages of Plasmodium falciparum by flow cytometry. Cytom. Part A 81A:12 (2012), 1048–1054.
22. [22] Bousema, T., Drakeley, C., Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin. Microbiol. Rev. 24:2 (2011), 377–410.
23. [23] D'Alessandro, S., Silvestrini, F., Dechering, K., Corbett, Y., Parapini, S., Timmerman, M., Galastri, L., Basilico, N., Sauerwein, R., Alano, P., Taramelli, D., A Plasmodium falciparum screening assay for anti-gametocyte drugs based on parasite lactate dehydrogenase detection. J. Antimicrob. Chemother. 68:9 (2013), 2048–2058.
24. [24] Lucantoni, L., Silvestrini, F., Signore, M., Siciliano, G., Eldering, M., Dechering, K.J., Avery, V.M., Alano, P., A simple and predictive phenotypic High Content Imaging assay for Plasmodium falciparum mature gametocytes to identify malaria transmission blocking compounds. Nat. Publ. Gr., 2015, 1–14.
25. [25] Regev-Rudzki, N., Wilson, D.W., Carvalho, T.G., Sisquella, X., Coleman, B.M., Rug, M., Bursac, D., Angrisano, F., Gee, M., Hill, A.F., Baum, J., Cowman, A.F., Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 153:5 (2013), 1120–1133.
26. [26] Vorobjev, I.A., Buchholz, K., Prabhat, P., Ketman, K., Egan, E.S., Marti, M., Duraisingh, M.T., Barteneva, N.S., Optimization of flow cytometric detection and cell sorting of transgenic Plasmodium parasites using interchangeable optical filters. Malar. J., 11(1), 2012, 1.
27. [27] Christian, D.A., Koshy, A.A., Reuter, M.A., Betts, M.R., Boothroyd, J.C., Hunter, A., Use of transgenic parasites and host reporters to dissect Events that promote interleukin-12 production during toxoplasmosis. Infect. Immun. 82:10 (2014), 4056–4067.
28. [28] Bargieri, D.Y., Andenmatten, N., Lagal, V., Thiberge, S., Whitelaw, J.A., Tardieux, I., Meissner, M., Menard, R., Apical membrane antigen 1 mediates apicomplexan parasite attachment but is dispensable for host cell invasion. Nat. Commun., 2013.
29. [29] Gibson-corley, K.N., Bockenstedt, M.M., Li, H., Boggiatto, P.M., Phanse, Y., Petersen, C.A., Bellaire, B.H., Jones, E., An in vitro model of antibody-enhanced killing of the intracellular parasite Leishmania amazonensis. PLoS One 9:9 (2014), 1–8.
30. [30] Lee, Y.Q., Goh, A.S.P., Ch'Ng, J.H., Nosten, F.H., Preiser, P.R., Pervaiz, S., Yadav, S.K., Tan, K.S.W., A high-content phenotypic screen reveals the disruptive potency of quinacrine and 3′,4′-dichlorobenzamil on the digestive vacuole of Plasmodium falciparum. Antimicrob. Agents Chemother. 58:1 (2014), 550–558.
31. [31] Marangon, I., Boggetto, N., Ménard-Moyon, C., Venturelli, E., Béoutis, M.L., Péchoux, C., Luciani, N., Wilhelm, C., Bianco, A., Gazeau, F., Intercellular carbon nanotube translocation assessed by flow cytometry imaging. Nano Lett. 12:9 (2012), 4830–4837.
32. [32] Safeukui, I., Buffet, P.A., Perrot, S., Sauvanet, A., Aussilhou, B., Surface area loss and increased sphericity account for the splenic entrapment of subpopulations of Plasmodium falciparum ring-infected erythrocytes. PLoS One, 8(3), 2013.
33. [33] Carter, L.M., Kafsack, B.F.C., Llinás, M., Mideo, N., Pollitt, L.C., Reece, S.E., Stress and sex in malaria parasites: why does commitment vary?. Evol. Med. Public Health 2013:1 (2013), 135–147.
34. [34] Trager, W., Jensen, J.B., Human malaria parasites in continuous culture. Science 193:4254 (1976), 673–675.
35. [35] George, T.C., Fanning, S.L., Fitzgeral-Bocarsly, P., Medeiros, R.B., Highfill, S., Shimizu, Y., Hall, B.E., Frost, K., Basiji, D., Ortyn, W.E., Morrissey, P.J., Lynch, D.H., Quantitative measurement of nuclear translocation events using similarity analysis of multispectral cellular images obtained in flow. J. Immunol. Methods 311:1–2 (2006), 117–129.
36. [36] Tonkin, C.J., Van Dooren, G.G., Spurck, T.P., Struck, N.S., Good, R.T., Handman, E., Cowman, A.F., McFadden, G.I., Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol. Biochem. Parasitol. 137:1 (2004), 13–21.
37. [37] Marangon, I., Boggetto, N., Ménard-Moyon, C., Luciani, N., Wilhelm, C., Bianco, A., Gazeau, F., Localization and relative quantification of carbon nanotubes in cells with multispectral imaging flow cytometry. J. Vis. Exp.(82), 2013, e50566.