Comparison of a high-throughput high-content intracellular Leishmania donovani assay with an axenic amastigote assay

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 7, 2013, Pages 2913-2922

  De Rycker, Manu ^a   Hallyburton, Irene ^a   Thomas, John ^a   Campbell, Lorna ^a   Wyllie, Susan ^a   Joshi, Dhananjay ^a,b   Cameron, Scott ^a   Gilbert, Ian H ^a   Wyatt, Paul G ^a   Frearson, Julie A ^a,c   Fairlamb, Alan H ^a   Gray, David W ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b Advinus Therapeutics Private Limited Bangalore   (India)

^c BioFocus DPI   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; ANTILEISHMANIAL AGENT; ATOVAQUONE; KETOCONAZOLE; MILTEFOSINE; NIFURTIMOX; PAROMOMYCIN; PENTAMIDINE; STIBOGLUCONATE SODIUM;

AMASTIGOTE; ARTICLE; AXENIC AMASTIGOTE ASSAY; BIOASSAY; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG ACTIVITY; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; INTERMETHOD COMPARISON; INTRAMACROPHAGE ASSAY; LEISHMANIA DONOVANI; LEISHMANIASIS; MICROSCOPY; PRIORITY JOURNAL;

ANTIPROTOZOAL AGENTS; AXENIC CULTURE; CELL LINE; DRUG DISCOVERY; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; MACROPHAGES; PARASITIC SENSITIVITY TESTS;

EID: 84879030428     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02398-12     Document Type: Article

References (53)

1. World Health Organization. 2010. Control of the leishmaniases. World Health Organ. Tech. Rep. Ser. 2010:xii-xiii; 1-186; back cover.
2. Singh N, Kumar M, Singh RK. 2012. Leishmaniasis: current status of available drugs and new potential drug targets. Asian Pac. J. Trop. Med. 5:485-497.
3. Burchmore RJ, Barrett MP. 2001. Life in vacuoles-nutrient acquisition by Leishmania amastigotes. Int. J. Parasitol. 31:1311-1320. (Pubitemid 32868711)
4. Kima PE. 2007. The amastigote forms of Leishmania are experts at exploiting host cell processes to establish infection and persist. Int. J. Parasitol. 37:1087-1096. (Pubitemid 47042032)
5. Bodley AL, McGarry MW, Shapiro TA. 1995. Drug cytotoxicity assay for African trypanosomes and Leishmania species. J. Infect. Dis. 172:1157-1159.
6. Mikus J, Steverding D. 2000. A simple colorimetric method to screen drug cytotoxicity against Leishmania using the dye Alamar blue. Parasitol. Int. 48:265-269.
7. Nolan LL, Bouchard B. 1991. A rapid in vitro system for screening the effect of experimental compounds on nonadhering cell lines. Curr. Microbiol. 23:277-279.
8. Siqueira-Neto JL, Song OR, Oh H, Sohn JH, Yang G, Nam J, Jang J, Cechetto J, Lee CB, Moon S, Genovesio A, Chatelain E, Christophe T, Freitas-Junior LH. 2010. Antileishmanial high-throughput drug screening reveals drug candidates with new scaffolds. PLoS Negl. Trop. Dis. 4:e675. doi:10.1371/journal.pntd. 0000675.
9. St George S, Bishop JV, Titus RG, Selitrennikoff CP. 2006. Novel compounds active against Leishmania major. Antimicrob. Agents Chemother. 50:474-479. (Pubitemid 43190955)
10. Sharlow ER, Close D, Shun T, Leimgruber S, Reed R, Mustata G, Wipf P, Johnson J, O'Neil M, Grogl M, Magill AJ, Lazo JS. 2009. Identification of potent chemotypes targeting Leishmania major using a highthroughput, low-stringency, computationally enhanced, small molecule screen. PLoS Negl. Trop. Dis. 3:e540. doi:10.1371/journal.pntd.0000540.
11. Debrabant A, Joshi MB, Pimenta PF, Dwyer DM. 2004. Generation of Leishmania donovani axenic amastigotes: their growth and biological characteristics. Int. J. Parasitol. 34:205-217. (Pubitemid 38229824)
12. Bates PA. 1993. Axenic culture of Leishmania amastigotes. Parasitol. Today 9:143-146. (Pubitemid 23080764)
13. Gupta N, Goyal N, Rastogi AK. 2001. In vitro cultivation and characterization of axenic amastigotes of Leishmania. Trends Parasitol. 17:150-153. (Pubitemid 32422185)
14. Teixeira MC, de Jesus Santos R, Sampaio RB, Pontes-de-Carvalho L, dos Santos WL. 2002. A simple and reproducible method to obtain large numbers of axenic amastigotes of different Leishmania species. Parasitol. Res. 88:963-968. (Pubitemid 35216481)
15. Callahan HL, Portal AC, Devereaux R, Grogl M. 1997. An axenic amastigote system for drug screening. Antimicrob. Agents Chemother. 41:818-822. (Pubitemid 27150538)
16. Monte-Alegre A, Ouaissi A, Sereno D. 2006. Leishmania amastigotes as targets for drug screening. Kinetoplastid Biol. Dis. 5:6.
17. Shimony O, Jaffe CL. 2008. Rapid fluorescent assay for screening drugs on Leishmania amastigotes. J. Microbiol. Methods 75:196-200.
18. Holzer TR, McMaster WR, Forney JD. 2006. Expression profiling by whole-genome interspecies microarray hybridization reveals differential gene expression in procyclic promastigotes, lesion-derived amastigotes, and axenic amastigotes in Leishmania mexicana. Mol. Biochem. Parasitol. 146:198-218. (Pubitemid 43356361)
19. Pescher P, Blisnick T, Bastin P, Spath GF. 2011. Quantitative proteome profiling informs on phenotypic traits that adapt Leishmania donovani for axenic and intracellular proliferation. Cell Microbiol. 13:978-991.
20. Vermeersch M, da Luz RI, Tote K, Timmermans JP, Cos P, Maes L. 2009. In vitro susceptibilities of Leishmania donovani promastigote and amastigote stages to antileishmanial reference drugs: practical relevance of stage-specific differences. Antimicrob. Agents Chemother. 53:3855-3859.
21. Li Q., Zhao Y, Ni B, Yao C, Zhou Y, Xu W, Wang Z, Qiao Z. 2008. Comparison of the expression profiles of promastigotes and axenic amastigotes in Leishmania donovani using serial analysis of gene expression. Parasitol. Res. 103:821-828.
22. Sereno D, Cordeiro da Silva A, Mathieu-Daude F, Ouaissi A. 2007. Advances and perspectives in Leishmania cell based drug-screening procedures. Parasitol. Int. 56:3-7.
23. Buckner FS, Wilson AJ. 2005. Colorimetric assay for screening compounds against Leishmania amastigotes grown in macrophages. Am. J. Trop. Med. Hyg. 72:600-605. (Pubitemid 41278830)
24. Lang T, Goyard S, Lebastard M, Milon G. 2005. Bioluminescent Leishmania expressing luciferase for rapid and high throughput screening of drugs acting on amastigote-harboring macrophages and for quantitative real-time monitoring of parasitism features in living mice. Cell. Microbiol. 7:383-392. (Pubitemid 40277918)
25. Mandal S, Maharjan M, Ganguly S, Chatterjee M, Singh S, Buckner FS, Madhubala R. 2009. High-throughput screening of amastigotes of Leishmania donovani clinical isolates against drugs using a colorimetric betalactamase assay. Indian J. Exp. Biol. 47:475-479.
26. De Muylder G, Ang KK, Chen S, Arkin MR, Engel JC, McKerrow JH. 2011. A screen against Leishmania intracellular amastigotes: comparison to a promastigote screen and identification of a host cell-specific hit. PLoS Negl. Trop. Dis. 5:e1253. doi:10.1371/journal.pntd.0001253.
27. Siqueira-Neto JL, Moon S, Jang J, Yang G, Lee C, Moon HK, Chatelain E, Genovesio A, Cechetto J, Freitas-Junior LH. 2012. An image-based high-content screening assay for compounds targeting intracellular Leishmania donovani amastigotes in human macrophages. PLoS Negl. Trop. Dis. 6:e1671. doi:10.1371/journal.pntd.0001671.
28. Brenk R, Schipani A, James D, Krasowski A, Gilbert IH, Frearson J, Wyatt PG. 2008. Lessons learnt from assembling screening libraries for drug discovery for neglected diseases. Chem Med Chem 3:435-444.
29. Goyard S, Segawa H, Gordon J, Showalter M, Duncan R, Turco SJ, Beverley SM. 2003. An in vitro system for developmental and genetic studies of Leishmania donovani phosphoglycans. Mol. Biochem. Parasitol. 130:31-42. (Pubitemid 37205159)
30. Gaur U, Showalter M, Hickerson S, Dalvi R, Turco SJ, Wilson ME, Beverley SM. 2009. Leishmania donovani lacking the Golgi GDP-Man transporter LPG2 exhibit attenuated virulence in mammalian hosts. Exp. Parasitol. 122:182-191.
31. 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. (Pubitemid 29278954)
32. Seifert K, Escobar P, Croft SL. 2010. In vitro activity of anti-leishmanial drugs against Leishmania donovani is host cell dependent. J. Antimicrob. Chemother. 65:508-511.
33. Wang MZ, Zhu X, Srivastava A, Liu Q, Sweat JM, Pandharkar T, Stephens CE, Riccio E, Parman T, Munde M, Mandal S, Madhubala R, Tidwell RR, Wilson WD, Boykin DW, Hall JE, Kyle DE, Werbovetz KA. 2010. Novel arylimidamides for treatment of visceral leishmaniasis. Antimicrob. Agents Chemother. 54:2507-2516.
34. Yardley V, Croft SL. 2000. A comparison of the activities of three amphotericin B lipid formulations against experimental visceral and cutaneous leishmaniasis. Int. J. Antimicrob. Agents 13:243-248. (Pubitemid 30072740)
35. Gupta S. 2011. Visceral leishmaniasis: experimental models for drug discovery. Indian J. Med. Res. 133:27-39.
36. Sereno D, Cavaleyra M, Zemzoumi K, Maquaire S, Ouaissi A, Lemesre JL. 1998. Axenically grown amastigotes of Leishmania infantum used as an in vitro model to investigate the pentavalent antimony mode of action. Antimicrob. Agents Chemother. 42:3097-3102. (Pubitemid 28553724)
37. Auwerx J. 1991. The human leukemia cell line, THP-1: a multifaceted model for the study of monocyte-macrophage differentiation. Experientia 47:22-31.
38. Gebre-Hiwot A, Tadesse G, Croft SL, Frommel D. 1992. An in vitro model for screening antileishmanial drugs: the human leukaemia monocyte cell line, THP-1. Acta Trop. 51:237-245.
39. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, Tada K. 1980. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. cancer 26:171-176. (Pubitemid 10086416)
40. Fernandez O, Diaz-Toro Y, Valderrama L, Ovalle C, Valderrama M, Castillo H, Perez M, Saravia NG. 2012. Novel approach to in vitro drug susceptibility assessment of clinical strains of Leishmania spp. J. Clin. Microbiol. 50:2207-2211.
41. Rogers PD, Stiles JK, Chapman SW, Cleary JD. 2000. Amphotericin B induces expression of genes encoding chemokines and cell adhesion molecules in the human monocytic cell line THP-1. J. Infect. Dis. 182:1280-1283.
42. Gao Y, Deng K, Cao Z, Graziani EI, Gilbert AM, Koehn FE, Wood A, Doherty P, Walsh FS. 2010. Amphotericin B, identified from a natural product screen, antagonizes CNS inhibitors to promote axon growth via activation of an Akt pathway in neurons. J. Neurochem. 113:1331-1342.
43. Manning BD, Cantley LC. 2007. AKT/PKB signaling: navigating downstream. Cell 129:1261-1274. (Pubitemid 46962095)
44. Osorio Y, Travi BL, Renslo AR, Peniche AG, Melby PC. 2011. Identification of small molecule lead compounds for visceral leishmaniasis using a novel ex vivo splenic explant model system. PLoS Negl. Trop. Dis. 5:e962. doi:10.1371/journal.pntd.0000962.
45. Sereno D, Lemesre JL. 1997. Axenically cultured amastigote forms as an in vitro model for investigation of antileishmanial agents. Antimicrob. Agents Chemother. 41:972-976. (Pubitemid 27194170)
46. Carrio J, de Colmenares M, Riera C, Gallego M, Arboix M, Portus M. 2000. Leishmania infantum: stage-specific activity of pentavalent antimony related with the assay conditions. Exp. Parasitol. 95:209-214.
47. Ephros M, Bitnun A, Shaked P, Waldman E, Zilberstein D. 1999. Stage-specific activity of pentavalent antimony against Leishmania donovani axenic amastigotes. Antimicrob. Agents Chemother. 43:278-282. (Pubitemid 29079158)
48. Shaked-Mishan P, Ulrich N, Ephros M, Zilberstein D. 2001. Novel intracellular SbV reducing activity correlates with antimony susceptibility in Leishmania donovani. J. Biol. Chem. 276:3971-3976.
49. Mookerjee Basu J, Mookerjee A, Sen P, Bhaumik S, Banerjee S, Naskar K, Choudhuri SK, Saha B, Raha S, Roy S. 2006. Sodium antimony gluconate induces generation of reactive oxygen species and nitric oxide via phosphoinositide 3-kinase and mitogen-activated protein kinase activation in Leishmania donovani-infected macrophages. Antimicrob. Agents Chemother. 50:1788-1797.
50. Rochette A, Raymond F, Corbeil J, Ouellette M, Papadopoulou B. 2009. Whole-genome comparative RNA expression profiling of axenic and intracellular amastigote forms of Leishmania infantum. Mol. Biochem. Parasitol. 165:32-47.
51. De Rycker M, O'Neill S, Joshi D, Campbell L, Gray DW, Fairlamb AH. 2012. A static-cidal assay for Trypanosoma brucei to aid hit prioritization for progression into drug discovery programmes. PLoS Negl. Trop. Dis. 6:e1932. doi:10.1371/journal.pntd.0001932.
52. Freitas-Junior LH, Chatelain E, Kim HA, Siqueira-Neto JL. 2012. Visceral leishmaniasis treatment: what do we have, what do we need and how to deliver it? Int. J. Parasitol. Drugs Drug Resist. 2:11-19.
53. Bradley DJ, Kirkley J. 1977. Regulation of Leishmania populations within the host. I. the variable course of Leishmania donovani infections in mice. Clin. Exp. Immunol. 30:119-129. (Pubitemid 8249312)