Development and Validation of a Luminescence-based, Medium-Throughput Assay for Drug Screening in Schistosoma mansoni

PLoS Neglected Tropical Diseases

Volumn 9, Issue 1, 2015, Pages

  Lalli, Cristiana ^a   Guidi, Alessandra ^a   Gennari, Nadia ^b   Altamura, Sergio ^b   Bresciani, Alberto ^b   Ruberti, Giovina ^a  

^a CNR   (Italy)

^b IRBM   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

10 [2 (DIETHYLAMINO)ETHYL] 9(10H) ACRIDINONE (2 THIAZOLIDINYLIDENE)HYDRAZONE; ADENOSINE TRIPHOSPHATE; ANTIINFECTIVE AGENT; ANTIPARASITIC AGENT; AURANOFIN; DISULFIRAM; GAMBOGIC ACID; MENADIONE; OLTIPRAZ; OXAMNIQUINE; PARTHENOLIDE; PLUMBAGIN; PRAZIQUANTEL; SANGUINARINE; THONZONIUM; UNCLASSIFIED DRUG; ANTISCHISTOSOMAL AGENT;

ADULT; ANIMAL MODEL; ARTICLE; BIOASSAY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG SCREENING; FEMALE; FLUORESCENCE MICROSCOPY; LD 50; LIMIT OF QUANTITATION; LIQUID CHROMATOGRAPHY; LUMINESCENCE BASED ASSAY; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PARASITE VIABILITY; REPRODUCIBILITY; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SENSITIVITY ANALYSIS; ANIMAL; DRUG DEVELOPMENT; DRUG EFFECTS; LUMINESCENCE; METABOLISM; PROCEDURES;

ADENOSINE TRIPHOSPHATE; ANIMALS; DRUG DISCOVERY; FEMALE; LUMINESCENT MEASUREMENTS; MICE; SCHISTOSOMA MANSONI; SCHISTOSOMICIDES;

EID: 84922241656     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003484     Document Type: Article

References (46)

1. Nwaka S, Hudson A, (2006) Innovative lead discovery strategies for tropical diseases. Nat Rev Drug Discov 5: 941–955. doi: 10.1038/nrd2144
2. Crompton DWT, Peters P and Savioli L (2010) Working to overcome the global impact of neglected tropical diseases first WHO report on neglected tropical diseases 2010. World Health Org.
3. Gray DJ, McManus DP, Li Y, Williams GM, Bergquist R, et al. (2010) Schistosomiasis elimination: lessons from the past guide the future. Lancet Infect Dis 10: 733–736. doi: 10.1016/S1473-3099(10)70099-2 20705513
4. Pica-Mattoccia L, Cioli D, (2004) Sex- and stage-related sensitivity of Schistosoma mansoni to in vivo and in vitro praziquantel treatment. Int J Parasitol 34: 527–533. doi: 10.1016/j.ijpara.2003.12.003 15013742
5. Sabah AA, Fletcher C, Webbe G, Doenhoff MJ, (1986) Schistosoma mansoni: chemotherapy of infections of different ages. Exp Parasitol 61: 294–303. doi: 10.1016/0014-4894(86)90184-0 3086114
6. Gonnert R, Andrews P, (1977) Praziquantel, a new board-spectrum antischistosomal agent. Z Parasitenkd 52: 129–150. doi: 10.1007/BF00389899 410178
7. Dabo A, Doucoure B, Koita O, Diallo M, Kouriba B, et al. (2000) Reinfection with Schistosoma haematobium and mansoni despite repeated praziquantel office treatment in Niger, Mali. Med Trop (Mars) 60: 351–355.
8. Fallon PG, Doenhoff MJ, (1994) Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. Am J Trop Med Hyg 51: 83–88. 8059919
9. Ismail M, Botros S, Metwally A, William S, Farghally A, et al. (1999) Resistance to praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. Am J Trop Med Hyg 60: 932–935. 10403323
10. Gryseels B, Mbaye A, De Vlas SJ, Stelma FF, Guisse F, et al. (2001) Are poor responses to praziquantel for the treatment of Schistosoma mansoni infections in Senegal due to resistance? An overview of the evidence. Trop Med Int Health 6: 864–873. doi: 10.1046/j.1365-3156.2001.00811.x 11703840
11. Cioli D, Botros SS, Wheatcroft-Francklow K, Mbaye A, Southgate V, et al. (2004) Determination of ED50 values for praziquantel in praziquantel-resistant and -susceptible Schistosoma mansoni isolates. Int J Parasitol 34: 979–987. doi: 10.1016/j.ijpara.2004.05.001 15217737
12. Melman SD, Steinauer ML, Cunningham C, Kubatko LS, Mwangi IN, et al. (2009) Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl Trop Dis 3: e504. doi: 10.1371/journal.pntd.0000504 19688043
13. Cioli D, Pica-Mattoccia L, Basso A, Guidi A, (2014) Schistosomiasis control: praziquantel forever? Mol Biochem Parasitol 195: 23–29. doi: 10.1016/j.molbiopara.2014.06.002 24955523
14. Mansour NR, Bickle QD, (2010) Comparison of microscopy and Alamar blue reduction in a larval based assay for schistosome drug screening. PLoS Negl Trop Dis 4: e795. doi: 10.1371/journal.pntd.0000795 20706580
15. Peak E, Chalmers IW, Hoffmann KF, (2010) Development and validation of a quantitative, high-throughput, fluorescent-based bioassay to detect schistosoma viability. PLoS Negl Trop Dis 4: e759. doi: 10.1371/journal.pntd.0000759 20668553
16. Singh R. PM, Heskia I., Xu F., McKerrow J. and Caffrey C.R. (2009) Automated image-based phenotypic screening for high-throughput drug discovery. Proc 22nd IEEE Int Symp Comput-Based Med Syst.
17. Lee H, Moody-Davis A, Saha U, Suzuki BM, Asarnow D, et al. (2012) Quantification and clustering of phenotypic screening data using time-series analysis for chemotherapy of schistosomiasis. BMC genomics 13 Suppl 1: S4. doi: 10.1186/1471-2164-13-S1-S4 22369037
18. Asarnow DE, Singh R, (2013) Segmenting the etiological agent of schistosomiasis for high-content screening. IEEE Trans Med Imaging 32: 1007–1018. doi: 10.1109/TMI.2013.2247412 23428618
19. Paveley RA, Mansour NR, Hallyburton I, Bleicher LS, Benn AE, et al. (2012) Whole organism high-content screening by label-free, image-based Bayesian classification for parasitic diseases. PLoS Negl Trop Dis 6: e1762. doi: 10.1371/journal.pntd.0001762 22860151
20. Brink LH, McLaren DJ, Smithers SR, (1977) Schistosoma mansoni: a comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology 74: 73–86. doi: 10.1017/S0031182000047545 320543
21. Protasio AV, Dunne DW, Berriman M, (2013) Comparative study of transcriptome profiles of mechanical- and skin-transformed Schistosoma mansoni schistosomula. PLoS Negl Trop Dis 7: e2091. doi: 10.1371/journal.pntd.0002091 23516644
22. Nare B, Smith JM, Prichard RK, (1991) Differential effects of oltipraz and its oxy-analogue on the viability of Schistosoma mansoni and the activity of glutathione S-transferase. Biochem Pharmacol 42: 1287–1292. doi: 10.1016/0006-2952(91)90267-9 1888337
23. Zhang SM, Coultas KA, (2013) Identification of plumbagin and sanguinarine as effective chemotherapeutic agents for treatment of schistosomiasis. Int J Parasitol Drugs Drug Resist 3: 28–34. doi: 10.1016/j.ijpddr.2012.12.001 23641325
24. Wang X, Chen W, (2012) Gambogic acid is a novel anti-cancer agent that inhibits cell proliferation, angiogenesis and metastasis. Anticancer Agents Med Chem 12: 994–1000. doi: 10.2174/187152012802650066 22339063
25. Zhang JH, Chung TD, Oldenburg KR, (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 4: 67–73. doi: 10.1177/108705719900400206 10838414
26. van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, et al. (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86: 125–139. doi: 10.1016/S0001-706X(03)00029-9 12745133
27. Keiser J, (2010) In vitro and in vivo trematode models for chemotherapeutic studies. Parasitology 137: 589–603. doi: 10.1017/S0031182009991739 19961653
28. Sykes ML, Avery VM, (2009) A luciferase based viability assay for ATP detection in 384-well format for high throughput whole cell screening of Trypanosoma brucei brucei bloodstream form strain 427. Parasit Vectors 2: 54. doi: 10.1186/1756-3305-2-54 19909542
29. Debnath A, Parsonage D, Andrade RM, He C, Cobo ER, et al. (2012) A high-throughput drug screen for Entamoeba histolytica identifies a new lead and target. Nat Med 18: 956–960. doi: 10.1038/nm.2758 22610278
30. Derbyshire ER, Prudencio M, Mota MM, Clardy J, (2012) Liver-stage malaria parasites vulnerable to diverse chemical scaffolds. Proc Natl Acad Sci U S A 109: 8511–8516. doi: 10.1073/pnas.1118370109 22586124
31. Caffrey CR, Steverding D, Swenerton RK, Kelly B, Walshe D, et al. (2007) Bis-acridines as lead antiparasitic agents: structure-activity analysis of a discrete compound library in vitro. Antimicrob Agents Chemother 51: 2164–2172. doi: 10.1128/AAC.01418-06 17371810
32. Manneck T, Braissant O, Haggenmuller Y, Keiser J, (2011) Isothermal microcalorimetry to study drugs against Schistosoma mansoni. J Clin Microbiol 49: 1217–1225. doi: 10.1128/JCM.02382-10 21270220
33. Marxer M, Ingram K, Keiser J, (2012) Development of an in vitro drug screening assay using Schistosoma haematobium schistosomula. Parasit Vectors 5: 165. doi: 10.1186/1756-3305-5-165 22876861
34. Paveley RA, Bickle QD, (2013) Automated imaging and other developments in whole-organism anthelmintic screening. Parasite Immunol 35: 302–313. doi: 10.1111/pim.12037 23581722
35. Mahady GB, Beecher CW, (1994) Quercetin-induced benzophenanthridine alkaloid production in suspension cell cultures of Sanguinaria canadensis. Planta Med 60: 553–557. doi: 10.1055/s-2006-959570 7809211
36. Chaturvedi MM, Kumar A, Darnay BG, Chainy GB, Agarwal S, et al. (1997) Sanguinarine (pseudochelerythrine) is a potent inhibitor of NF-kappaB activation, IkappaBalpha phosphorylation, and degradation. J Biol Chem 272: 30129–30134. doi: 10.1074/jbc.272.48.30129 9374492
37. Ahmad N, Gupta S, Husain MM, Heiskanen KM, Mukhtar H, (2000) Differential antiproliferative and apoptotic response of sanguinarine for cancer cells versus normal cells. Clin Cancer Res 6: 1524–1528. 10778985
38. Pelizzaro-Rocha KJ, Tiuman TS, Izumi E, Ueda-Nakamura T, Dias Filho BP, et al. (2010) Synergistic effects of parthenolide and benznidazole on Trypanosoma cruzi. Phytomedicine 18: 36–39. doi: 10.1016/j.phymed.2010.09.005 21035317
39. Godinho LS, Aleixo de Carvalho LS, Barbosa de Castro CC, Dias MM, Pinto Pde F, et al. (2014) Anthelmintic activity of crude extract and essential oil of Tanacetum vulgare (Asteraceae) against adult worms of Schistosoma mansoni. ScientificWorldJournal 2014: 460342. doi: 10.1155/2014/460342 24672320
40. Borkosky S, Ponce de Leon S, Juarez G, Sierra MG, Bardon A, (2009) Molluscicidal sesquiterpene lactones from species of the tribe Vernonieae (Compositae). Chem Biodivers 6: 513–519. doi: 10.1002/cbdv.200800156 19353532
41. Seed JL, Pratt MC, Bennett JL, (1979) The effects of chronic disulfiram treatment on mice infected with Schistosoma mansoni. Am J Trop Med Hyg 28: 508–514. 572149
42. Hill DE, Fetterer RH, (1997) The effect of disulfiram on egg shell formation in adult Trichuris muris. J Parasitol 83: 938–942. doi: 10.2307/3284293 9379303
43. Scheibel LW, Adler A, Trager W, (1979) Tetraethylthiuram disulfide (Antabuse) inhibits the human malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A 76: 5303–5307. doi: 10.1073/pnas.76.10.5303 388434
44. Nash T, Rice WG, (1998) Efficacies of zinc-finger-active drugs against Giardia lamblia. Antimicrob Agents Chemother 42: 1488–1492. 9624499
45. Bouma MJ, Snowdon D, Fairlamb AH, Ackers JP, (1998) Activity of disulfiram (bis(diethylthiocarbamoyl)disulphide) and ditiocarb (diethyldithiocarbamate) against metronidazole-sensitive and -resistant Trichomonas vaginalis and Tritrichomonas foetus. J Antimicrob Chemother 42: 817–820. doi: 10.1093/jac/42.6.817 10052908
46. Paget T, Maroulis S, Mitchell A, Edwards MR, Jarroll EL, et al. (2004) Menadione kills trophozoites and cysts of Giardia intestinalis. Microbiology 150: 1231–1236. doi: 10.1099/mic.0.26836-0 15133085