DNA topoisomerase I from parasitic protozoa: A potential target for chemotherapy

Biochimica et Biophysica Acta - Gene Structure and Expression

Volumn 1759, Issue 3-4, 2006, Pages 117-131

  Reguera, R M ^a   Redondo, C M ^a   Gutierrez de Prado, R ^a   Perez Pertejo Y ^a   Balana Fouce R ^a  

^a UNIVERSITY OF LEÓN   (Spain)

Author keywords

Camptothecin; Cryptosporidium; DNA topoisomerase IB; Indolocarbazole; Parasitic protozoa; Plasmodium; Trypanosomatid

Indexed keywords

1,4 NAPHTHOQUINONE DERIVATIVE; ACRIDINE DERIVATIVE; ANTILEISHMANIAL AGENT; ANTIPROTOZOAL AGENT; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BERBERINE; BERBERINE DERIVATIVE; CAMPTOTHECIN; CAMPTOTHECIN DERIVATIVE; CARBAZOLE DERIVATIVE; CORALYNE; DIMINAZENE ACETURATE; DIOSPYRIN; DNA TOPOISOMERASE; DNA TOPOISOMERASE INHIBITOR; HO 33258; HO 333258; HO 33342; IRINOTECAN; MEGLUMINE ANTIMONATE; NITIDINE; PENTAMIDINE; PROTOZOAL PROTEIN; REBECCAMYCIN; RM 762; STIBOGLUCONATE SODIUM; TOPOTECAN; UNCLASSIFIED DRUG;

CELL DEATH; CLINICAL TRIAL; COST BENEFIT ANALYSIS; CRYPTOSPORIDIOSIS; CYTOLOGY; DNA DETERMINATION; DRUG TARGETING; GENE CONTROL; HUMAN; LEISHMANIASIS; MALARIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTOZOON; QUANTITATIVE STRUCTURE ACTIVITY RELATION; REVIEW; TRYPANOSOMA; TRYPANOSOMIASIS; UNSPECIFIED SIDE EFFECT;

ANIMALS; DNA TOPOISOMERASES, TYPE I; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; NEOPLASMS; PHYLOGENY; PROTOZOA;

MAMMALIA; PROKARYOTA; PROTOZOA;

EID: 33744536418     PISSN: 01674781     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbaexp.2006.03.006     Document Type: Review

References (116)

1. Greenwood B.M., Bojang K., Whitty C.J.M., and Targett G.A.T. Malaria. Lancet 365 (2005) 1487-1498
2. Shlomai J. The structure and replication of kinetoplast DNA. Curr. Mol. Med. 4 (2004) 623-647
3. Kioy D., Jannin J., and Mattock N. Human African trypanosomiasis. Nat. Rev., Microbiol. 2 (2004) 186-187
4. Miles M.A., Feliciangeli M.D., and de Arias A.R. American trypanosomiasis (Chagas' disease) and the role of molecular epidemiology in guiding control strategies. BMJ 326 (2003) 1444-1448
5. Desjeux P. Leishmaniasis: current situation and new perspectives. Comp. Immunol. Microbiol. Infect. Dis. 27 (2004) 305-318
6. May J., and Meyer C.G. Chemoresistance in falciparum malaria. Trends Parasitol. 19 (2003) 432-435
7. Le Bras J., and Durand R. The mechanisms of resistance to antimalarial drugs in Plasmodium falciparum. Fundam. Clin. Pharmacol. 17 (2003) 147-153
8. Ashley E.A., and White N.J. Artemisinin-based combinations. Curr. Opin. Infect. Dis. 18 (2005) 531-536
9. Legros D., Ollivier G., Gastellu-Etchegorry M., Paquet C., Burri C., Jannin J., and Buscher P. Treatment of human African trypanosomiasis-Present situation and needs for research and development. Lancet, Infect. Dis. 2 (2002) 437-440
10. Kennedy P.G. Human African trypanosomiasis of the CNS: current issues and challenges. J. Clin. Invest. 113 (2004) 496-504
11. Mpia B., and Pepin J. Combination of eflornithine and melarsoprol for melarsoprol-resistant Gambian trypanosomiasis. Trop. Med. Int. Health 7 (2002) 775-779
12. Urbina J.A., and Docampo R. Specific chemotherapy of Chagas' disease: controversies and advances. Trends Parasitol. 19 (2003) 495-501
13. Docampo R. Sensitivity of parasites to free radical damage by antiparasitic drugs. Chem. Biol. Interact. 73 (1990) 1-27
14. Croft S.L., and Coombs G.H. Leishmaniasis-Current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol. 19 (2003) 502-508
15. Balaña-Fouce R., Reguera R.M., Cubría J.C., and Ordóñez D. The pharmacology of leishmaniasis. Gen. Pharmacol. 30 (1998) 435-443
16. Bommer W., Eibl H.J., Engel K.R., Kuhlencord A., Sindermann H., Sundar S., and Zappel H. Leishmaniasis-Oral treatment with hexadecylphosphocholine. Wien Klin. Wochenschr. 116 (2004) 24-29
17. Rivas L., Moreno J., Cañavate C., and Alvar J. Virulence and disease in leishmaniasis: what is relevant for the patient?. Trends Parasitol. 20 (2004) 297-301
18. Harms G., and Feldmeier H. The impact of HIV infection on tropical diseases. Infect. Dis. Clin. North Am. 19 (2005) 121-135
19. Burton A. Sharing needles may produce artificial Leishmania cycle. Lancet, Infect. Dis. 1 (2001) 4
20. Champoux J.J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70 (2001) 369-413
21. Wang J.C. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev., Mol. Cell Biol. 3 (2002) 430-440
22. Corbett K.D., and Berger J.M. Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu. Rev. Biophys. Biomol. Struct. 33 (2004) 95-118
23. Wang J.C. DNA topoisomerases. Annu. Rev. Biochem. 65 (1996) 635-692
24. Berger J.M. Structure of DNA topoisomerases. Biochim. Biophys. Acta 1400 (1998) 3-18
25. Cheesman S., McAleese S., Goman M., Johnson D., Horrocks P., Ridley R.G., and Kilbey B. The gene encoding topoisomerase II from Plasmodium falciparum. Nucleic Acids Res. 22 (1994) 2547-2551
26. Strauss P.R., and Wang J.C. The TOP2 gene of Trypanosoma brucei: a single-copy gene that shares extensive homology with other TOP2 genes encoding eukaryotic DNA topoisomerase II. Mol. Biochem. Parasitol. 38 (1990) 141-150
27. Fragoso S.P., and Goldenberg S. Cloning and characterization of the gene encoding Trypanosoma cruzi DNA topoisomerase II. Mol. Biochem. Parasitol. 55 (1992) 127-134
28. Christopher L.J., and Dykstra C.C. Identification of a type II topoisomerase gene from Cryptosporidium parvum. J. Eukaryot. Microbiol. 41 (1994) 28S
29. Das A., Dasgupta A., Sharma S., Ghosh M., Sengupta T., Bandopadhyay S., and Majumder H.K. Characterisation of the gene encoding type II DNA topoisomerase from Leishmania donovani: a key molecular target in antileishmanial therapy. Nucleic Acids Res. 29 (2001) 1844-1851
30. Stewart L., Redinbo M.R., Qiu X., Hol W.G., and Champoux J.J. A model for the mechanism of human topoisomerase I. Science 279 (1998) 1534-1541
31. Champoux J.J. Domains of human topoisomerase I and associated functions. Prog. Nucleic Acid Res. Mol. Biol. 60 (1998) 111-132
32. Stewart L., Ireton G.C., and Champoux J.J. The domain organization of DNA topoisomerase I. J. Biol. Chem. 271 (1996) 7602-7608
33. Redinbo M.R., Stewart L., Kuhn P., Champoux J.J., and Hol W.G. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279 (1998) 1504-1513
34. Ireton G.C., Stewart L., Parker L.H., and Champoux J.J. Expression of human topoisomerase I with a partial deletion of the linker region yields monomeric and dimeric enzymes that respond differently to camptothecin. J. Biol. Chem. 275 (2000) 25820-25830
35. Riou J.F., Gabillot M., Philippe M., Schrevel J., and Riou G. Purification and characterization of Plasmodium berghei DNA topoisomerases I and II: drug action, inhibition of decatenation and relaxation, and stimulation of DNA cleavage. Biochemistry 25 (1986) 1471-1479
36. Tosh K., and Kilbey B. The gene encoding topoisomerase I from the human parasite Plasmodium falciparum. Gene 163 (1995) 151-154
37. Tosh K., Cheesman S., Horrocks P., and Kilbey B. Plasmodium falciparum: stage-related expression of topoisomerase I. Exp. Parasitol. 91 (1999) 126-132
38. Villa H., Otero Marcos A.R., Reguera R.M., Balana-Fouce R., Garcia-Estrada C., Perez-Pertejo Y., Tekwani B.L., Myler P.J., Stuart K.D., Bjornsti M.A., and Ordoñez D. A novel active DNA topoisomerase I in Leishmania donovani. J. Biol. Chem. 278 (2003) 3521-3526
39. Das A., Mandal C., Dasgupta A., Sengupta T., and Majumder H.K. An insight into the active site of a type I topoisomerase from the kinetoplastid protozoan Leishmania donovani. Nucleic Acid. Res. 30 (2002) 794-802
40. Bodley A.L., Chakraborty A.K., Xie S., Burri C., and Shapiro T.A. An unusual type IB topoisomerase from African trypanosomes. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 7344-7539
41. Das B.B., Sen N., Ganguly A., and Majumder H.K. Reconstitution and functional characterization of the unusual bi-subunit type I DNA topoisomerase from Leishmania donovani. FEBS Lett. 565 (2004) 81-88
42. Stewart L., Ireton G.C., and Champoux J.J. Reconstitution of a human topoisomerase I by fragment complementation. J. Mol. Biol. 269 (1997) 355-372
43. Park H., and Sternglanz R. Two separate conserved domains of eukaryotic DNA topoisomerase I bind to each other and reconstitute enzymatic activity. Chromosoma 107 (1998) 211-215
44. Davies D.R., Mushtaq A., Interthal H., Champoux J.J., and Hol W.G. The structure of the transition state of the heterodimeric topoisomerase I of Leishmania donovani as a vanadate complex. J. Mol. Biol. 357 (2006) 1202-1210
45. D'Arpa P., and Liu L.F. Cell cycle-specific and transcription-related phosphorylation of mammalian topoisomerase I. Exp. Cell Res. 217 (1995) 125-131
46. Das B.B., Sen N., Dasgupta S.B., Ganguly A., and Majumder H.K. N-Terminal region of the large subunit of Leishmania donovani bisubunit topoisomerase I is involved in DNA relaxation and interaction with the smaller subunit. J. Biol. Chem. 280 (2005) 16335-16344
47. Wang Z., and Englund P.T. RNA interference of a trypanosome topoisomerase II causes progressive loss of mitochondrial DNA. EMBO J. 20 (2001) 4674-4683
48. Bakshi R.P., and Shapiro T.A. RNA interference of Trypanosoma brucei topoisomerase IB: both subunits are essential. Mol. Biochem. Parasitol. 136 (2004) 249-255
49. Das A., Dasgupta A., Sengupta T., and Majumder H.K. Topoisomerases of kinetoplastid parasites as potential chemotherapeutic targets. Trends Parasitol. 20 (2004) 381-387
50. Broccoli S., Marquis J.F., Papadopoulou B., Olivier M., and Drolet M. Characterization of a Leishmania donovani gene encoding a protein that closely resembles a type IB topoisomerase. Nucleic Acids Res. 27 (1999) 2745-2752
51. Cheng C., Kussie P., Pavletich N., and Shuman S. Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases. Cell 92 (1998) 841-850
52. Stiles J.K., Hicock P.I., Shah P.H., and Meade J.C. Genomic organization, transcription, splicing and gene regulation in Leishmania. Ann. Trop. Med. Parasitol. 93 (1999) 781-807
53. Pourquier P., and Pommier Y. Topoisomerase I-mediated DNA damage. Adv. Cancer Res. 80 (2001) 189-216
54. Desai S.D., Liu L.F., Vazquez-Abad D., and D'Arpa P. Ubiquitin-dependent destruction of topoisomerase I is stimulated by the antitumor drug camptothecin. J. Biol. Chem. 272 (1997) 24159-24164
55. Desai S.D., Li T.K., Rodriguez-Bauman A., Rubin E.H., and Liu L.F. Ubiquitin/26S proteasome-mediated degradation of topoisomerase I as a resistance mechanism to camptothecin in tumor cells. Cancer Res. 61 (2001) 5926-5932
56. Pommier Y. Camptothecins and topoisomerase I: a foot in the door. Targeting the genome beyond topoisomerase I with camptothecins and novel anticancer drugs: importance of DNA replication, repair and cell cycle checkpoints. Curr. Med. Chem. Anticancer Agents 4 (2004) 429-434
57. Cusack Jr. J.C., Liu R., Houston M., Abendroth K., Elliott P.J., Adams J., and Baldwin Jr. A.S. Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systematic nuclear factor-kB inhibition. Cancer Res. 61 (2001) 3535-3540
58. Emmerlich V., Santarius U., Bakker-Grunwald T., and Scholze H. Isolation and subunit composition of the 20S proteasome of Giardia lamblia. Mol. Biochem. Parasitol. 100 (1999) 131-134
59. Yao Y., Toth C.R., Huang L., Wong M.L., Dias P., Burlingame A.L., Coffino P., and Wang C.C. Alpha5 subunit in Trypanosoma brucei proteasome can self-assemble to form a cylinder of four stacked heptamer rings. Biochem. J. 344 (1999) 349-358
60. Diego J.L., Katz J.M., Marshall P., Gutierrez B., Manning J.E., Nussenzweig V., and Gonzalez J. The ubiquitin-proteasome pathway plays an essential role in proteolysis during Trypanosoma cruzi remodeling. Biochemistry 40 (2001) 1053-1062
61. Robertson C.D. The Leishmania mexicana proteasome. Mol. Biochem. Parasitol. 103 (1999) 49-60
62. Hellberg A., Sommer A., and Bruchhaus I. Primary sequence of a putative non-ATPase subunit of the 26S proteasome from Entamoeba histolytica is similar to the human and yeast S2 subunit. Parasitol. Res. 85 (1999) 417-420
63. Certad G., Abrahem A., and Georges E. Cloning and partial characterization of the proteasome S4 ATPase from Plasmodium falciparum. Exp. Parasitol. 93 (1999) 123-131
64. Paugam A., Creuzet C., Dupouy-Camet J., and Roisin M.P. Evidence for the existence of a proteasome in Toxoplasma gondii: intracellular localization and specific peptidase activities. Parasite 8 (2001) 267-273
65. Paugam A., Bulteau A.-L., Dupouy-Camet J., Creuzet C., and Friguet B. Characterization and role of protozoan parasite proteosomes. Trends Parasitol. 19 (2003) 55-59
66. Carlton J.M., et al. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419 (2002) 512-519
67. Berriman M., et al. The genome of the African trypanosome Trypanosoma brucei. Science 309 (2005) 416-422
68. El-Sayed N.M., et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309 (2005) 409-415
69. Ivens A.C., et al. The genome of the kinetoplastid parasite, Leishmania major. Science 309 (2005) 436-442
70. Mao Y., Sun M., Desai S.D., and Liu L.F. SUMO-1 conjugation to topoisomerase I: a possible repair response to topoisomerase-mediated DNA damage. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4046-4051
71. Horie K., Tomida A., Sugimoto Y., Yasugi T., Yoshikawa H., Taketani Y., and Tsuruo T. SUMO-1 conjugation to intact DNA topoisomerase I amplifies cleavable complex formation induced by camptothecin. Oncogene 21 (2002) 7913-7922
72. Mo Y.Y., Yu Y., Shen Z., and Beck W.T. Nucleolar delocalization of human topoisomerase I in response to topotecan correlates with sumoylation of the protein. J. Biol. Chem. 277 (2002) 2958-2964
73. Rodriguez M.S., Dargemont C., and Hay R.T. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276 (2001) 12654-12659
74. Chessman S.J. The topoisomerases of protozoan parasites. Parasitol. Today 16 (2000) 277-281
75. Bakshi R.P., and Shapiro T.A. DNA topoisomerases as targets for antiprotozoal chemotherapy. Mini Rev. Med. Chem. 3 (2003) 597-608
76. Wang J.C. DNA topoisomerases as targets of therapeutics: an overview. Adv. Pharmacol. 29 (1994) 1-19
77. Capranico G., Giaccone G., Zunino F., Garattini S., and D'Incalci M. Development of DNA topoisomerase-related therapeutics: a short perspective of new challenges. Curr. Med. Chem. Anticancer Agents 4 (2004) 335-345
78. Pizzolato J.F., and Saltz L.B. The camptothecins. Lancet 361 (2003) 2235-2242
79. Adams D.J. The impact of tumor physiology on camptothecin-based drug development. Curr. Med. Chem. Anticancer Agents 5 (2005) 1-13
80. Sriram D., Yogeeswari P., Thirumurugan R., and Bal T.R. Camptothecin and its analogues: a review on their chemotherapeutic potential. Nat. Prod. Res. 19 (2005) 393-412
81. Bodley A.L., and Shapiro T.A. Molecular and cytotoxic effects of camptothecin, a topoisomerase I inhibitor, on trypanosomes and Leishmania. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 3726-3730
82. Bodley A.L., Cumming J.N., and Shapiro T.A. Effect of camptothecin, a topoisomerase I inhibitor on Plasmodium falciparum. Biochem. Pharmacol. 55 (1998) 709-711
83. Bodley A.L., Wani M.C., Wall M.E., and Shapiro T.A. Antitrypanosomal activity of camptothecin analogs. Structure-activity correlations. Biochem. Pharmacol. 50 (1995) 937-942
84. Deterding A., Dungey F.A., Thompson K.A., and Steverding D. Anti-trypanosomal activities of DNA topoisomerase inhibitors. Acta Trop. 93 (2005) 311-316
85. Rooseboom M., Commandeur J.N., and Vermeulen N.P. Enzyme-catalyzed activation of anticancer pro-drugs. Pharmacol. Rev. 56 (2004) 53-102
86. Staker B.L., Feese M.D., Cushman M., Pommier Y., Zembower D., Stewart L., and Burgin A.B. Structures of three classes of anticancer agents bound to the human topoisomerase I-DNA covalent complex. J. Med. Chem. 48 (2005) 2336-2345
87. Staker B.L., Hjerrild K., Feese M.D., Behnke C.A., Burgin Jr. A.B., and Stewart L. The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 15387-15392
88. Redinbo M.R., Champoux J.J., and Hol W.G. Structural insights into the function of type IB topoisomerases. Curr. Opin. Struct. Biol. 9 (1999) 29-36
89. Marquis J.F., Hardy I., and Olivier M. Topoisomerase I amino acid substitutions, Gly185Arg and Asp325Glu, confer camptothecin resistance in Leishmania donovani. Antimicrob. Agents Chemother. 49 (2005) 1441-1446
90. Proulx M.E., Desormeaux A., Marquis J.F., Olivier M., and Bergeron M.G. Treatment of visceral leishmaniasis with sterically stabilized liposomes containing camptothecin. Antimicrob. Agents Chemother. 45 (2001) 2623-2627
91. Meng L.H., Liao Z.Y., and Pommier Y. Non-camptothecin DNA topoisomerase I inhibitors in cancer therapy. Curr. Top. Med. Chem. 3 (2003) 305-320
92. Woo M.H., Vance J.R., Marcos A.R., Bailly C., and Bjornsti M.A. Active site mutations in DNA topoisomerase I distinguish the cytotoxic activities of camptothecin and the indolocarbazole, rebeccamycin. J. Biol. Chem. 277 (2002) 3813-3822
93. Antony S., Kohlhagen G., Agama K., Jayaraman M., Cao S., Durrani F.A., Rustum Y.M., Cushman M., and Pommier Y. Cellular topoisomerase I inhibition and antiproliferative activity by MJ-III-65 (NSC 706744), an indenoisoquinoline topoisomerase I poison. Mol. Pharmacol. 67 (2005) 523-530
94. Hazra B., Saha A.K., Ray R., Roy D.K., Sur P., and Banerjee A. Antiprotozoal activity of diospyrin towards Leishmania donovani promastigotes in vitro. Trans. R. Soc. Trop. Med. Hyg. 81 (1987) 738-741
95. Ray S., Hazra B., Mittra B., Das A., and Majumder H.K. Diospyrin, a bisnaphthoquinone: a novel inhibitor of type I DNA topoisomerase of Leishmania donovani. Mol. Pharmacol. 54 (1998) 994-999
96. Syrovets T., Buchele B., Gedig E., Slupsky J.R., and Simmet T. Acetyl-boswellic acids are novel catalytic inhibitors of human topoisomerases I and II. Mol. Pharmacol. 58 (2000) 71-81
97. Chowdhury A.R., Mandal S., Goswami A., Ghosh M., Mandal L., Chakraborty D., Ganguly A., Tripathi G., Mukhopadhyay S., Bandyopadhyay S., and Majumder H.K. Dihydrobetulinic acid induces apoptosis in Leishmania donovani by targeting DNA topoisomerase I and II: implications in antileishmanial therapy. Mol. Med. 9 (2003) 26-36
98. Chakraborty A.K., and Majumder H.K. Mode of action of pentavalent antimonials: specific inhibition of type I DNA topoisomerase of Leishmania donovani. Biochem. Biophys. Res. Commun. 152 (1988) 605-611
99. Walker J., and Saravia N.G. Inhibition of Leishmania donovani promastigote DNA topoisomerase I and human monocyte DNA topoisomerases I and II by antimonial drugs and classical antitopoisomerase agents. J. Parasitol. 90 (2004) 1155-1162
100. Lucumi A., Robledo S., Gama V., and Saravia N.G. Sensitivity of Leishmania viannia panamensis to pentavalent antimony is correlated with the formation of cleavable DNA-protein complexes. Antimicrob. Agents Chemother. 42 (1998) 1990-1995
101. Vennerstrom J., Lovelace J.K., Waits V.B., Hanson W.L., and Klayman D.L. Berberine derivatives as antileishmanial drugs. Antimicrob. Agents Chemother. 34 (1990) 918-921
102. Marquis J.F., Makhey D., LaVoie E.J., and Olivier M. Effects of topoisomerases inhibitors protoberberine on Leishmania donovani growth, macrophage function, and infection. J. Parasitol. 89 (2003) 1048-1052
103. Merschjohann K., Sporer F., Steverding D., and Wink M. In vitro effect of alkaloids on bloodstream forms of Trypanosoma brucei and T. congolense. Planta Med. 67 (2001) 623-627
104. Kinnamon K.E., Poon B.T., Hanson W.L., and Waits V.B. Activity of anticancer compounds against Trypanosoma cruzi-infected mice. Am. J. Trop. Med. Hyg. 58 (1998) 804-806
105. Chen A.Y., Yu C., Gatto B., and Liu L.F. DNA minor groove-binding ligands: a different class of mammalian DNA topoisomerase I inhibitors. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 8131-8135
106. Jean-Moreno V., Rojas R., Goyeneche D., Coombs G.H., and Walker J. Leishmania donovani: differential activities of classical topoisomerase inhibitors and antileishmanials against parasite and host cells at the level of DNA topoisomerase I and in cytotoxicity assays. Exp. Parasitol. 112 (2006) 21-30
107. Baguley B.C., and Ferguson L.R. Mutagenic properties of topoisomerase-targeted drugs. Biochim. Biophys. Acta 1400 (1998) 213-222
108. Pommier Y., Redon C., Rao V.A., Seiler J.A., Sordet O., Takemura H., Antony S., Meng L., Liao Z., Kohlhagen G., Zhang H., and Kohn K.W. Repair of and checkpoint response to topoisomerase I-mediated DNA damage. Mutat. Res. 532 (2003) 173-203
109. McKean P.G., Keen J.K., Smith D.F., and Benson F.E. Identification and characterization of a RAD51 gene from Leishmania major. Mol. Biochem. Parasitol. 15 (2001) 209-216
110. Gallego C., Estevez A.M., Farez E., Ruiz-Perez L.M., and Gonzalez-Pacanowska D. Overexpression of AP endonuclease protects Leishmania major cells against methotrexate induced DNA fragmentation and hydrogen peroxide. Mol. Biochem. Parasitol. 141 (2005) 191-197
111. Burri C., Bodley A.L., and Shapiro T.A. Topoisomerases in Kinetoplastids. Parasitol. Today 12 (1996) 226-231
112. Lee N., Bertholet S., Debrabant A., Muller J., Duncan R., and Nakhasi H.L. Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Differ. 9 (2002) 53-64
113. Sen N., Das B.B., Ganguly A., Mukherjee T., Tripathi G., Bandyopadhyay S., Rakshit S., Sen T., and Majumder H.K. Camptothecin induced mitochondrial dysfunction leading to programmed cell death in unicellular hemoflagellate Leishmania donovani. Cell Death Differ. 11 (2004) 924-936
114. Sen N., Das B.B., Ganguly A., Mukherjee T., Bandyopadhyay S., and Majumder H.K. Camptothecin-induced imbalance in intracellular cation homeostasis regulates programmed cell death in unicellular hemoflagellate Leishmania donovani. J. Biol. Chem. 279 (2004) 52366-52375
115. Podesta D., Garcia-Herreros M.I., Cannata J.J., Stoppani A.O., and Fernández Villamil S.H. Purification and properties of poly(ADP-ribose)polymerase from Crithidia fasciculata. Automodification and poly(ADP-ribosyl)ation of DNA topoisomerase. Mol. Biochem. Parasitol. 135 (2004) 211-219
116. El Sayed N.M., et al. Comparative genomics of Trypanosomatid parasitic protozoa. Science 309 (2005) 404-409