Visceral leishmaniasis: Experimental models for drug discovery

Indian Journal of Medical Research

Volumn 133, Issue 1, 2011, Pages 27-39

  Gupta, Suman ^a   Nishi, ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

Chemotherapeutic models; Primates; Rodents; Screening assays; Visceral leishmaniasis

Indexed keywords

ALKALINE PHOSPHATASE; AMPHOTERICIN B; ANTILEISHMANIAL AGENT; BETA GALACTOSIDASE; BETA LACTAMASE; CHLORAMPHENICOL ACETYLTRANSFERASE; FIREFLY LUCIFERASE; GREEN FLUORESCENT PROTEIN; MILTEFOSINE; VACCINE; ANTIPROTOZOAL AGENT; PROTOZOAL PROTEIN;

AMASTIGOTE; BAGG ALBINO MOUSE; CHEMOTHERAPY; COLORIMETRY; DOG; DRUG ACTIVITY; DRUG RESEARCH; DRUG SCREENING; GERMFREE ANIMAL; HAMSTER; HAPLORHINI; HIGH THROUGHPUT SCREENING; IC 50; IMMUNOLOGY; IN VITRO STUDY; LEISHMANIA; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; NONHUMAN; PARASITE CULTIVATION; PROMASTIGOTE; PROTEIN EXPRESSION; REPORTER GENE; REVIEW; RODENT; VACCINATION; VISCERAL LEISHMANIASIS; ANIMAL; CLINICAL TRIAL (TOPIC); DRUG DEVELOPMENT; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; METHODOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIPROTOZOAL AGENTS; CLINICAL TRIALS AS TOPIC; DRUG DISCOVERY; DRUG EVALUATION, PRECLINICAL; GENES, REPORTER; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; PROTOZOAN PROTEINS;

EID: 79851498525     PISSN: 09715916     EISSN: 09715916     Source Type: Journal    
DOI: None     Document Type: Review

References (99)

1. World Health Organization. The leishmaniases and Leishmania/HIV co-infections. Geneva, Switzerland: World Health Organization; 2002.
2. Bhatnagar S, Guru PY, Katiyar JC, Srivastava R, Mukherjee A, Akhtar M S, et al. Exploration of antileishmanial activity in heterocycles; results of their in vivo and in vitro bioevaluations. Indian J Med Res 1989; 89: 439-444.
3. Croft SL. In vitro screens in the experimental chemotherapy of Leishmaniasis and trypanosomiasis. Parasitol Today 1986; 2: 64-69.
4. Neal RA. Leishmania major: culture media, mouse strains, and promastigote virulence and infectivity. Exp Parasitol 1984; 57: 269-273.
5. Peters W, Evans DA, Lanham SM. Importance of parasite identification in case of leishmaniasis. J R Soc Med 1983; 76: 540-542.
6. Croft SL, Seifert K, Yardley V. Current scenario of drug development for 1eishmaniasis. Indian J Med Res 2006; 123: 399-410.
7. Jackson JE, Tally JD, Tang DB. An in vitro micro method for drug sensitivity testing of leishmania. Am J Trop Med Hyg 1989; 41: 318-330.
8. Callahan HL, Portal AC, Devereaux R, Grogl M. An Axenic amastigote system for drug screening. Antimicrob Agents Chemother 1997; 41: 818-822.
9. Ephros M, Bitnun A, Shaked P, Waldman E, Zilberstein D. Stage-specific activity of pentavalent antimony against Leishmania donovani axenic amastigotes. Antimicrob Agents Chemother 1999; 43: 278-282.
10. Sereno D, Cordeiro da Silva A, Mathieu-Daude F, Ouaissi A. Advances and perspectives in Leishmania cell based drug-screening procedures. Parasitol Int 2007; 56: 3-7.
11. Sereno D, Lemesre JL. Use of an enzymatic micro method to quantify amastigote stage of Leishmania amazonensis in vitro. Parasitol Res 1997; 83: 401-403.
12. Ganguly S, Bandyopadhyay S, Sarkar A, Chatterjee M. Development of a semi automated colorimetric assay for screening anti-leishmanial agents. J Microbiol Methods 2005; 66: 78-86.
13. Sereno D, Alegre AM, Silvester R, Vergnes B, Ouaissi A. In vitro antileishmanial activity of nicotinamide. Antimicrob Agents Chemother 2005; 49: 808-812.
14. Vergnes B, Vanhille L, Ouaissi A, Sereno D. Stage specific antileishmanial activity of an inhibitor of SIR2 histone deacetylase. Acta Trop 2005; 94: 107-115.
15. Sereno D, Roy G, Lemesre JL, Papadopoulou B, Ouellette M. DNA transformation of Leishmania infantum axenic amastigotes and their use in drug screening. Antimicrob Agents Chemother 2001; 45: 1168-1173.
16. Shimonya O, Jaffe CL. Rapid fluorescent assay for screening drugs on Leishmania amastigotes. J Microbiol Methods 2008; 75: 196-200.
17. Escobar P, Matu S, Marques C, Croft SL. Sensitivities of Leishmania species to hexadecylphosphocholine (miltefosine), ET-18-OCH (3) (edelfosine) and amphotericin B. Acta Trop 2002; 81: 151-157.
18. Yardley V, Croft SL, De Donker S, Dujardin JC, Siddhartha K, Miranda C, et al. The sensitivity of clinical isolates of Leishmania from Peru and Nepal to Miltefosine. Am J Trop Med Hyg 2005; 73: 272-275.
19. Neal RA, Croft SL. An in-vitro system for determining the activity of compounds against the intracellular amastigote form of Leishmania donovani. J Antimicrob Chemother 1984; 14: 463-475.
20. Berman JD. Leishmania tropica: quantitation of in vitro activity of antileishmanial agents by Giemsa staining, viability and 3H-formycin B incorporation. J Parasitol 1984; 70: 561-562.
21. Berman JD, Lee LS. Activity of antileishmanial agents against amastigotes inhuman monocyte-derived macrophages and in mouser peritoneal macrophages. J Parasitol 1984; 70: 220-225.
22. Berman JD, Wyler DJ. An in vitro model for investigation of chemotherapeutic agents in leishmaniasis. J Infect Dis 1980; 142: 83-86.
23. Looker DL, Martinez S, Horton JM, Marr JJ. Growth of Leishmania donovani amastigotes in the continuous human macrophages cell line U937: Studies on drug efficacy and metabolism. J Infect Dis 1986; 154: 323-327.
24. Gebre-Hiwot A, Tadesse G, Croft SL, Frommel D. An in vitro model for screening antileishmanial drugs: the human leukaemia monocyte cell line, THP1. Acta Trop 1992; 51: 237-245.
25. Seifert K, Croft SL. In vitro and in vivo interactions between miltefosine and other antileishmanial drugs. Antimicrob Agents Chemother 2006; 50: 73-79.
26. Monte-Alegre A, Ouaissi A, Sereno D. Leishmania amastigotes as targets for drug screening. Kinetoplastid Biol Dis 2006; 5: 6.
27. Changsen C, Franzblau SG, Palittapongarnpim P. Improved green fluorescent protein reporter gene-based micro plate screening for anti tuberculosis compounds by utilizing an acetamidase promoter. Antimicrob Agents chemother 2003; 47: 3682-3687.
28. Dorsky DI, Wells M, Harrington RD: Detection of HIV-I infection with a green fluorescent protein reporter system. J Acquir Immune Defic Syndr Hum Retroviral 1996; 13: 308-313.
29. Buckner FS, Verlinde CLMJ, La Flamme AC, Van Voorhis WC. Efficient technique for screening drugs for activity against Trypanosoma cruzi using parasites expressing β-galactosidase. Antimicrob Agents Chemother 1996; 40: 2592-2597.
30. Naylor LH. Reporter gene technology: the future looks bright. Biochem Pharmacol 1999; 58: 749-757.
31. Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ. Primary structure of the Aequorea victoria green - fluorescent protein. Gene 1992; 111: 229-233.
32. Tsien RY. The green fluorescent protein. Annu Rev Biochem 1998; 67: 509-44.
33. Kain SR. Green fluorescent protein (GFP): applications in cell-based assays for drug discovery. Drug Discov Today 1999; 77: 57-64.
34. Debrabant A, Ghedin E, Dwyer DM. Dissection of the functional domains of the Leishmania surface membrane 3'-nucleotidase/nuclease, a unique member of the class I nuclease family. J Biol Chem 2000; 275: 16366-16372.
35. Ha DS, Schwarz JK, Turco SJ, Beverley SM. Use of the green fluorescent protein as a marker in transfected Leishmania. Mol Biochem Parasitol 1996; 77: 57-64.
36. Singh N, Dube A. Fluorescent leishmania: application to anti-leishmanial drug testing. Am J Trop Med Hyg 2004; 71: 400-2.
37. Mehta SR, Huang R, Yang M, Zhang XQ, Kolli B, Chang KP, et al. Real-time in vivo green fluorescent protein imaging of a murine leishmaniasis model as a new tool for leishmania vaccine and drug discovery. Clinical Vacc Immunol 2008; 15: 1764-1770.
38. Roy G, Dumas C, Sereno D, Wu Y, Singh AK, Tremblay MJ, et al. Episomal and stable expression of the luciferase reporter gene for quantifying Leishmania spp. infections in macrophages and in animal models. Mol Biochem Parasitol 2000; 110: 195-206.
39. Okuno T, Goto Y, Matsumoto Y, Otsuka H, Matsumoto Y. Applications of recombinant Leishmania amazonensis expressing egfp or the beta-galactosidase gene for drug screening and histopathological analysis. Exp Anim 2003; 52: 109-118.
40. Dube A, Singh N, Sundar S, Singh N. Refractoriness to the treatment of sodium stibogluconate in Indian kala-azar field isolates persists in in vitro and in vivo experimental models. Parasitol Res 2005; 96: 216-223.
41. Chan MMY, Bulinski JC, Chang KP, Fong DA. Micro plate assay for Leishmania amazonensis promastigotes expressing multimeric green fluorescent protein. Parasitol Res 2003; 89: 266-271.
42. Singh N, Gupta R, Jaiswal AK, Sundar S. Dube A. Transgenic Leishmania donovani clinical isolates expressing green fluorescent protein constitutively for rapid and reliable ex vivo drug screening. J Antimicrob Chemother 2009; 64: 370-374.
43. Seeber F, Boothroyd JC. Escherichia coli beta-galactosidase as an in vitro and in vivo reporter enzyme and stable transfection marker in the intracellular protozoan parasite Toxoplasma gondii. Gene 1996; 169: 39-45.
44. Campbell RE. Realization of β-lactamase as a versatile fluorogenic reporter. Trends Biotechnol 2005; 22: 208-211.
45. Buckner FS, Wilson AJ. Colorimetric assay for screening compounds against leishmania amastigotes grown in macrophages. Am J Trop Med Hyg 2005; 72: 600-605.
46. Zlokearnik G, Negulescu PA, Knapp TE, Mere L, Burres N, Feng L. Quantification of transcriptional and clonal selection of single living cells with β-lactamase as reporter. Science 1998; 279: 84-88.
47. Mandal S, Maharjan M, Ganguly S, Chatterjee M, Singh S, Buckner FS, et al. High throughput screening of amastigotes of Leishmania donovani clinical isolates against drugs using colorimetric β-lactamase assay. Indian J Exp Biol 2009; 47: 475-479.
48. Welsh S, Kay SA. Reporter gene expression for monitoring gene transfer. Curr Opin Biotechnol 1997; 8: 617-622.
49. Jacobs WR, Barletta RG, Udani R, Chan J, Kalkut G, Sonse G. Rapid assessment of drug susceptibilities of Mycobacterium tuberculosis by means of Luciferase Reporter Phages. Science 1993; 260: 819-822.
50. Gould SJ, Subramani S. Firefly luciferase as a tool in molecular and cell biology. Anal Biochem 1988; 175: 5-13.
51. Valdivia RH, Falkow S. Probing bacterial gene expression within host cells. Trends Microbiol 1997; 5: 360-333.
52. Ashutosh, Gupta S, Ramesh, Sundar S, Goyal N. Use of Leishmania donovani field isolates expressing the luciferase reporter gene in in vitro drug screening. Antimicrob Agents Chemother 2005; 49: 3776-3783.
53. Pandey S, Suryawanshi SN, Nishi, Goyal N, Gupta S. Chemotherapy of Leishmaniasis Part V: Synthesis and in vitro bio evaluation of novel pyridinone derivatives. Euro J Med Chem 2006; 42: 669-674.
54. Gupta L, Talwar A, Nishi, Palne S, Gupta S, Chauhan, PM. Synthesis of marine alkaloid: 8, 9-dihydrocoscinamide B and its analogues as novel class of antileishmanial agents. Bioorg Med Chem Lett 2007; 17: 4075-4079.
55. Sunduru N, Nishi, Palne S, Chauhan PMS, Gupta S. Synthesis and antileishmanial activity of novel 2,4,6-trisubstituted pyrimidines and 1,3,5-triazines. Europ J Med Chem 2009; 44: 2473-2481.
56. Lang T, Goyard S, Lebastard M, Milon G. Bioluminescent Leishmania expressing luciferase for rapid and high throughput screening of drugs acting on amastigote-harbouring macrophages and for quantitative real-time monitoring of parasitism features in living mice. Cell Microbiol 2005; 7: 383-392.
57. Kutzleb R, Schweyen RJ, Kaudewitz F. Extra chromosomal inheritance of paromomycin resistance in Saccharomyces cerevisiae. Mol Genet Genomics 1973; 125: 91-98.
58. Denise H, Coombs GH, Mottram JC. Generation of Leishmania mutants lacking antibiotic resistance genes using a versatile hit-and-run targeting strategy. FEMS Microbiol Lett 2004; 235: 89-94.
59. Grover GS, Turner BA, Parker CN, Meier J, Lala DS, Lee PH. Multiplexing nuclear receptors for agonist identification in a cell based reporter gene high-throughput screen. J Biomol Screen 2003; 8: 239-246.
60. Young KH, Wang Y, Bender C, Ajit S, Ramirez F, Gilbert A, et al. Yeast-based screening for inhibitors of RGS proteins. Methods Enzymol 2004; 389: 277-301.
61. http://en.wikipedia.org/wiki/z_factor, accessed on....
62. Siqueira-Neto J, Song O-R, Oh H, Sohn J-H, Yang G, Jiyoun N, et al. Antileishmanial high-throughput drug screening reveals drug candidates with new scaffolds. PLoS Negl Trop Dis 2010; 4: e675.
63. Hommel M, Jaffe CL, Travi B, Milon G. Experimental models for leishmaniasis and for testing anti-leishmanial vaccines. Ann Trop Med Parasitol 1995; 89 (Suppl. 1): 55-73.
64. Croft SL, DavidsonRN, Thornton EA. Liposomal amphotericin B in the treatment ofvisceral leishmaniasis. J Antimicrob Chemother 1991; 28: 111-118.
65. Murray HW, Brooks EB, De Vecchio JL, Heinzel FP. Immuno-enhancement combined with amphotericin B as treatment for experimental visceral leishmaniasis. Antimicrob Agents Chemother 2003; 47: 2513-2517.
66. Louis J, Gumy A, Voigt H, Rocken M, Launois P. Experimental cutaneous leishmaniasis: a powerful models to study in vivo the mechanisms underlying genetic differences in Th subset differentiation. Eur J Dermatol 2002; 12: 316-318.
67. Courret N, Lang T, Milon G, Antoine JC. Intradermal inoculations of low doses of Leishmania major and Leishmania amazonensis metacyclic promastigotes induce different immuno-parasitic processes and status of protection in BALB/c mice. Int J Parasitol 2003; 33: 1373-1383.
68. Bradley DJ. Letter. Genetic control of natural resistance to Leishmania donovani. Nature 1974; 250: 353-354.
69. Blackwell JM. Genetic susceptibility to leishmanial infections: studies in mice and man. Parasitology 1996; 112: S67-S74.
70. Liew FY, O'Donnell CA. Immunology of leishmaniasis. Adv Parasitol 1993; 32: 161-259.
71. Bradley DJ, Kirkley J. Variation in susceptibility of mouse strains to Leishmania donovani infection. Trans R Soc Trop Med Hyg 1972; 66: 527-528.
72. Fulton JD, Joyner LP. Infection by Leishmania donovani in the cotton rat. J Gen Microbiol 1948; 2: 103-109.
73. Mikhail JW, Mansour NS. Mystromys albicaudatus, the African white-tailed rat, as an experimental host for Leishmania donovani. J Parasitol 1973; 59: 1085-1087.
74. McKinney LA, Hendricks LD. Experimental infection of Mystromys albicaudatus with Leishmania braziliensis: pathology. Am J Trop Med Hyg 1980; 29: 753-760.
75. Nolan TJ, Farell JP. Experimental infections of the multi-mammate rat (Mastomys natalensis) with Leishmania donovani and Leishmania major. Am J Trop Med Hyg 1987; 36: 264-269.
76. Dwivedi SN, Guru PY, Bhagat RC, Shankhdhar V, Sen AB. Comparative susceptibility of Mastomys natalensis and golden hamsters (Mesocricetus auratus) to Leishmania donovani. Presented in the symposium on Fifth National Congress of Parasitology, 1983, June 25-27, Tirupati, India.
77. Smyly HJ, Young LW. The experimental transmission of leishmaniasis to animals. Proc Soc Exp Bio Med 1924; 21: 354-356.
78. Farrell JP. Leishmania donovani: acquired resistance to visceral leishmaniasis in the golden hamster. Exp Parasitol 1976; 40: 89-94.
79. Gifawesen C, Farrell JP. Comparison of T-cell responses in self-limiting versus progressive visceral Leishmania donovani infections in golden hamsters. Infect Immun 1989; 57: 3091-3096.
80. Stauber LA, Franchino EM, Grun J. An eight day method for screening of compounds against Leishmania donovani in the golden hamster. J Protozool 1958; 5: 269-273.
81. Mikhail JW, Mansour NS. Leishmania donovani: therapeutic and prophylactic action of antimony dextran glycoside (RL-712) in the golden hamster. Exp Parasitol 1975; 37: 348-352.
82. Hanson WL, Chapman WL, Jr., Kinnamon KE. Testing of drugs for antileishmanial activity in golden hamsters infected with Leishmania donovani. Int J Parasitol 1977; 7: 443-447.
83. Gupta S, Zehra K, Nigam V, Katiyar JC. Antileishmanial drug testing: Appraisal on existing techniques. Indian J Parasitol 1992; 16: 1-7.
84. Beveridge E. Chemotherapy of leishmaniasis. In: Schnitzer, RJ, Hawking, F, editors. Experimental chemotherapy. vol.1 New York: Academic Press, 1963. p. 257-280.
85. Gupta S, Tiwari S. Leishmania donovani infected inbred Golden Hamster as experimental model for visceral leishmaniasis. J Parasitic Dis 2000; 24: 211-213.
86. Dea-Ayuela MA, Rama-Iniguez S, Alunda JM, Bolas-Fernandez F. Setting new immuno-biological parameters in the hamster model of visceral leishmaniasis for in vivo testing of antileishmanial compounds. Vet Res Commun 2007; 31: 703-717.
87. De Oliveira CI, Teixeira MJ, Gomes R, Barral A, Brodskyn C. Animal models for infectious diseases caused by parasites: Leishmaniasis. Drug Dis Today: Dis Mod 2004; 1: 81-86.
88. Chapman WL, Hanson WL Jr, Waits VB, Kinnamon KE. Antileishmanial activity of selected compounds in dogs experimentally infected with Leishmania donovani. Rev Inst Med Trop Sao Paulo 1979; 21: 189-193.
89. Rioux JA, Golvan YJ, Croset H, Houin R. Leishmaniases in the Mediterranean "Midi": results of an ecologic survey. Bull Soc Pathol Exot Filiales 1969; 62: 332-333.
90. Keenan CM, Hendricks LD, Lightner L, Webster HK, Johnson AJ. Visceral leishmaniasis in the German shepherd dog. I. Infection, clinical disease, and clinical pathology. Vet Pathol 1984; 21: 74-79.
91. Abranches P, Santos-Gomes G, Rachamim N, Campino L, Schnur LF, Jaffe CL. An experimental model for canine visceral leishmaniasis. Parasite Immunol 1991; 13: 537-550.
92. Chapman WL, Jr, Hanson WL, Hendricks LD. Toxicity and efficacy of the antileishmanial drug meglumine antimoniate in the owl monkey (Aotus trivirgatus). J Parasitol 1983; 69: 1176-1177.
93. Chapman WL, Jr., Hanson WL. Visceral leishmaniasis in the squirrel monkey (Saimiri sciurea). J Parasitol 1981; 67: 740-741.
94. Anuradha, Pal A, Zehra K, Katiyar JC, Sethi N, Bhatia G, et al. The Indian langur: preliminary report of a new nonhuman primate host for visceral leishmaniasis. Bull World Health Organ 1992; 70: 63-72.
95. Dube A, Srivastava JK, Sharma P, Chaturvedi A, Katiyar JC, Naik S. Leishmania donovani: cellular and humoral immune responses in Indian languor monkey Presbytis entellus. Acta Trop 1999; 73: 37-48.
96. Dube A, Sharma P, Shrivastava JK, Mishra A, Katiyar JC. Vaccination of languor monkeys (Presbytus entellus) against Leishmania donovani with autoclaved L major plus BCG. Parasitology 1998; 116: 219-222.
97. Misra A, Dube A, Shrivastava B, Sharma P, Shrivastava JK, Katiyar JC. Successful vaccination against Leishmania donovani infection in Indian languor using alum-precipitated autoclaved Leishmania major with BCG. Vaccine 2001; 19: 3485-3492.
98. Kamau SW, Grimm F, Hehl AB. Expression of green fluorescent protein as a marker for effect of antileishmanial compounds in vitro. Antimicrob Agents Chemother 2001; 45: 3654-3656.
99. Garg R, Dube A. Animal models for vaccine studies for visceral leishmaniasis Indian J Med Res 2006; 123: 439-454.