Table of Contents Author Guidelines Submit a Manuscript
Enzyme Research
Volume 2011, Article ID 518258, 8 pages
http://dx.doi.org/10.4061/2011/518258
Review Article

Trypanosome Prereplication Machinery: A Potential New Target for an Old Problem

Laboratório Especial de Toxinologia Aplicada (LETA) Center for Applied Toxinology (CAT/CEPID), Instituto Butantan, Avenida Vital Brasil 1500, 05503-000 São Paulo, SP, Brazil

Received 15 December 2010; Revised 16 March 2011; Accepted 30 March 2011

Academic Editor: Ariel M. Silber

Copyright © 2011 Simone Guedes Calderano et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Pepin, “Combination therapy for sleeping sickness: a wake-up call,” Journal of Infectious Diseases, vol. 195, no. 3, pp. 311–313, 2007. View at Google Scholar · View at Scopus
  2. G. Russomando, M. M. C. De Tomassone, I. De Guillen et al., “Treatment of congenital chagas' disease diagnosed and followed up by the polymerase chain reaction,” American Journal of Tropical Medicine and Hygiene, vol. 59, no. 3, pp. 487–491, 1998. View at Google Scholar · View at Scopus
  3. A. R. Vago, L. O. Andrade, A. A. Leite et al., “Genetic characterization of Trypanosoma cruzi directly from tissues of patients with chronic chagas disease: differential distribution of genetic types into diverse organs,” American Journal of Pathology, vol. 156, no. 5, pp. 1805–1809, 2000. View at Google Scholar · View at Scopus
  4. E. Magnus, T. Vervoort, and N. Van Meirvenne, “A card-agglutination test with stained trypanosomes (C.A.T.T.) for the serological diagnosis of T. b. gambiense trypanosomiasis,” Annales de la Societe Belge de Medecine Tropicale, vol. 58, no. 3, pp. 169–176, 1978. View at Google Scholar · View at Scopus
  5. E. S. Umezawa, S. F. Bastos, M. E. Camargo et al., “Evaluation of recombinant antigens for serodiagnosis of Chagas' disease in South and Central America,” Journal of Clinical Microbiology, vol. 37, no. 5, pp. 1554–1560, 1999. View at Google Scholar · View at Scopus
  6. A. C. Pastini, S. R. Iglesias, V. C. Carricarte, M. E. Guerin, D. O. Sanchez, and A. C. Frasch, “Immunoassay with recombinant Trypanosoma cruzi antigens potentially useful for screening donated blood and diagnosing Chagas disease,” Clinical Chemistry, vol. 40, no. 10, pp. 1893–1897, 1994. View at Google Scholar · View at Scopus
  7. M. S. Leguizamón, G. Russomando, A. Luquetti et al., “Long-lasting antibodies detected by a trans-sialidase inhibition assay of sera from parasite-free, serologically cured chagasic patients,” Journal of Infectious Diseases, vol. 175, no. 5, pp. 1272–1275, 1997. View at Google Scholar · View at Scopus
  8. A. J. Duggan and M. P. Hutchinson, “Sleeping sickness in Europeans: a review of 109 cases,” Journal of Tropical Medicine and Hygiene, vol. 69, no. 6, pp. 124–131, 1966. View at Google Scholar · View at Scopus
  9. F. Checchi, J. A. N. Filipe, D. T. Haydon, D. Chandramohan, and F. Chappuis, “Estimates of the duration of the early and late stage of gambiense sleeping sickness,” BMC Infectious Diseases, vol. 8, article 16, 2008. View at Publisher · View at Google Scholar · View at PubMed
  10. M. Odiit, F. Kansiime, and J. C. K. Enyaru, “Duration of symptoms and case fatality of sleeping sickness caused by Trypanosoma brucei rhodesiense in Tororo, Uganda,” East African Medical Journal, vol. 74, no. 12, pp. 792–795, 1997. View at Google Scholar · View at Scopus
  11. E. M. Fèvre, P. G. Coleman, S. C. Welburn, and I. Maudlin, “Reanalyzing the 1900–1920 sleeping sickness epidemic in Uganda,” Emerging Infectious Diseases, vol. 10, no. 4, pp. 567–573, 2004. View at Google Scholar · View at Scopus
  12. J. C. P. Dias, “The treatment of Chagas disease (South American trypanosomiasis),” Annals of Internal Medicine, vol. 144, no. 10, pp. 772–774, 2006. View at Google Scholar · View at Scopus
  13. R. Docampo and S. N. J. Moreno, “Free radical metabolism of antiparasitic agents,” Federation Proceedings, vol. 45, no. 10, pp. 2471–2476, 1986. View at Google Scholar · View at Scopus
  14. B. Enanga, M. R. Ariyanayagam, M. L. Stewart, and M. P. Barrett, “Activity of megazol, a trypanocidal nitroimidazole, is associated with DNA damage,” Antimicrobial Agents and Chemotherapy, vol. 47, no. 10, pp. 3368–3370, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. W. Apt, “Current and developing therapeutic agents in the treatment of Chagas disease,” Drug design, development and therapy, vol. 4, pp. 243–253, 2010. View at Google Scholar
  16. M. P. Barrett, D. W. Boykin, R. Brun, and R. R. Tidwell, “Human African trypanosomiasis: pharmacological re-engagement with a neglected disease,” British Journal of Pharmacology, vol. 152, no. 8, pp. 1155–1171, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. B. J. Berger, N. S. Carter, and A. H. Fairlamb, “Polyamine and pentamidine metabolism in African trypanosomes,” Acta Tropica, vol. 54, no. 3-4, pp. 215–224, 1993. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Hanau, M. Rippa, M. Bertelli, F. Dallocchio, and M. P. Barrett, “6-Phosphogluconate dehydrogenase from Trypanosoma brucei. Kinetic analysis and inhibition by trypanocidal drugs,” European Journal of Biochemistry, vol. 240, no. 3, pp. 592–599, 1996. View at Google Scholar · View at Scopus
  19. C. Burri and R. Brun, “Eflornithine for the treatment of human African trypanosomiasis,” Parasitology Research, vol. 90, no. 1, pp. S49–S52, 2003. View at Google Scholar · View at Scopus
  20. S. R. Meshnick, R. W. Grady, S. H. Blobstein, and A. Cerami, “Porphyrin-induced lysis of Trypanosoma brucei: a role for zinc,” Journal of Pharmacology and Experimental Therapeutics, vol. 207, no. 3, pp. 1041–1050, 1978. View at Google Scholar · View at Scopus
  21. A. J. Romanha, S. L. de Castro, M. N. C. Soeiro et al., “In vitro and in vivo experimental models for drug screening and development for Chagas disease,” Memorias do Instituto Oswaldo Cruz, vol. 105, no. 2, pp. 233–238, 2010. View at Google Scholar · View at Scopus
  22. A. Liendo, K. Lazardi, and J. A. Urbina, “In-vitro antiproliferative effects and mechanism of action of the bis-triazole D0870 and its £(-) enantiomer against Trypanosoma cruzi,” Journal of Antimicrobial Chemotherapy, vol. 41, no. 2, pp. 197–205, 1998. View at Google Scholar · View at Scopus
  23. J. H. Ansede, M. Anbazhagan, R. Brun, J. D. Easterbrook, J. E. Hall, and D. W. Boykin, “O-alkoxyamidine prodrugs of furamidine: in vitro transport and microsomal metabolism as indicators of in vivo efficacy in a mouse model of Trypanosoma brucei rhodesiense infection,” Journal of Medicinal Chemistry, vol. 47, no. 17, pp. 4335–4338, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. P. D. De Melo Godoy, L. A. Nogueira-Junior, L. S. Paes et al., “Trypanosome prereplication machinery contains a single functional Orc1/Cdc6 protein, which is typical of archaea,” Eukaryotic Cell, vol. 8, no. 10, pp. 1592–1603, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. S. P. Bell and A. Dutta, “DNA replication in eukaryotic cells,” Annual Review of Biochemistry, vol. 71, pp. 333–374, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. B. Stillman, “Origin recognition and the chromosome cycle,” FEBS Letters, vol. 579, no. 4, pp. 877–884, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. J. F. X. Diffley, “DNA replication: building the perfect switch,” Current Biology, vol. 11, no. 9, pp. R367–R370, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Labib and J. F. X. Diffley, “Is the MCM2–7 complex the eukaryotic DNA replication fork helicase?” Current Opinion in Genetics and Development, vol. 11, no. 1, pp. 64–70, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. S. P. Bell and B. Stillman, “ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex,” Nature, vol. 357, no. 6374, pp. 128–134, 1992. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. B. P. Duncker, I. N. Chesnokov, and B. J. McConkey, “The origin recognition complex protein family,” Genome biology, vol. 10, no. 3, p. 214, 2009. View at Google Scholar · View at Scopus
  31. A. F. Neuwald, L. Aravind, J. L. Spouge, and E. V. Koonin, “AAA: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes,” Genome Research, vol. 9, no. 1, pp. 27–43, 1999. View at Google Scholar · View at Scopus
  32. J. P. Erzberger and J. M. Berger, “Evolutionary relationships and structural mechanisms of AAA+ proteins,” Annual Review of Biophysics and Biomolecular Structure, vol. 35, pp. 93–114, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. L. H. Hartwell, “Sequential function of gene products relative to DNA synthesis in the yeast cell cycle,” Journal of Molecular Biology, vol. 104, no. 4, pp. 803–817, 1976. View at Google Scholar · View at Scopus
  34. C. Speck and B. Stillman, “Cdc6 ATPase activity regulates ORC·Cdc6 stability and the selection of specific DNA sequences as origins of DNA replication,” Journal of Biological Chemistry, vol. 282, no. 16, pp. 11705–11714, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. M. Lei and B. K. Tye, “Initiating DNA synthesis: from recruiting to activating the MCM complex,” Journal of Cell Science, vol. 114, no. 8, pp. 1447–1454, 2001. View at Google Scholar · View at Scopus
  36. S. Chen, M. A. De Vries, and S. P. Bell, “Orc6 is required for dynamic recruitment of Cdt1 during repeated Mcm2–7 loading,” Genes and Development, vol. 21, no. 22, pp. 2897–2907, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. C. Evrin, P. Clarke, J. Zech et al., “A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 48, pp. 20240–20245, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. J. C. W. Randell, J. L. Bowers, H. K. Rodríguez, and S. P. Bell, “Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2–7 helicase,” Molecular Cell, vol. 21, no. 1, pp. 29–39, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. V. Tsakraklides and S. P. Bell, “Dynamics of pre-replicative complex assembly,” Journal of Biological Chemistry, vol. 22, pp. 877–884, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. M. De Felice, L. Esposito, B. Pucci et al., “Modular organization of a Cdc6-like protein from the crenarchaeon Sulfolobus solfataricus,” Biochemical Journal, vol. 381, no. 3, pp. 645–653, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. M. De Felice, L. Esposito, B. Pucci, M. De Falco, M. Rossi, and F. M. Pisani, “A CDC6-like factor from the archaea Sulfolobus solfataricus promotes binding of the mini-chromosome maintenance complex to DNA,” Journal of Biological Chemistry, vol. 279, no. 41, pp. 43008–43012, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. M. De Felice, L. Esposito, M. Rossi, and F. M. Pisani, “Biochemical characterization of two Cdc6/ORC1-like proteins from the crenarchaeon Sulfolobus solfataricus,” Extremophiles, vol. 10, no. 1, pp. 61–70, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. N. M. El-Sayed, P. J. Myler, D. C. Bartholomeu et al., “The genome sequence of Trypanosoma cruzi, etiologic agent of chagas disease,” Science, vol. 309, no. 5733, pp. 409–415, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. J. E. Walker, M. Saraste, M. J. Runswick, and N. J. Gay, “Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold,” The EMBO Journal, vol. 1, no. 8, pp. 945–951, 1982. View at Google Scholar · View at Scopus
  45. B. Guenther, R. Onrust, A. Sali, M. O'Donnell, and J. Kuriyan, “Crystal structure of the δ' subunit of the clamp-loader complex of E. coli DNA polymerase III,” Cell, vol. 91, no. 3, pp. 335–345, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. L. Janin, “ATPase inhibitors of heat-shock protein 90, second season,” Drug Discovery Today, vol. 15, no. 9-10, pp. 342–353, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. A. I. Roca and M. M. Cox, “RecA protein: structure, function, and role in recombinational DNA repair,” Progress in Nucleic Acid Research and Molecular Biology, vol. 56, pp. 129–223, 1997. View at Google Scholar · View at Scopus
  48. D. A. Ostrov, J. A. Hernández Prada, P. E. Corsino, K. A. Finton, N. Le, and T. C. Rowe, “Discovery of novel DNA gyrase inhibitors by high-throughput virtual screening,” Antimicrobial Agents and Chemotherapy, vol. 51, no. 10, pp. 3688–3698, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. D. Aiello, M. H. Barnes, E. E. Biswas et al., “Discovery, characterization and comparison of inhibitors of Bacillus anthracis and Staphylococcus aureus replicative DNA helicases,” Bioorganic and Medicinal Chemistry, vol. 17, no. 13, pp. 4466–4476, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. P. Csermely, T. Schnaider, C. Soti, Z. Prohászka, and G. Nardai, “The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review,” Pharmacology and Therapeutics, vol. 79, no. 2, pp. 129–168, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. W. B. Pratt, Y. Morishima, and Y. Osawa, “The Hsp90 chaperone machinery regulates signaling by modulating ligand binding clefts,” Journal of Biological Chemistry, vol. 283, no. 34, pp. 22885–22889, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. L. Whitesell and S. L. Lindquist, “HSP90 and the chaperoning of cancer,” Nature Reviews Cancer, vol. 5, no. 10, pp. 761–772, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. A. Kamal, L. Thao, J. Sensintaffar et al., “A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors,” Nature, vol. 425, no. 6956, pp. 407–410, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. JI. S. Hahn, “The Hsp90 chaperone machinery: from structure to drug development,” BMB Reports, vol. 42, no. 10, pp. 623–630, 2009. View at Google Scholar · View at Scopus
  55. L. Whitesell, E. G. Mimnaugh, B. De Costa, C. E. Myers, and L. M. Neckers, “Inhibition of heat shock protein HSP90-pp60(v-src) heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 18, pp. 8324–8328, 1994. View at Google Scholar · View at Scopus
  56. R. C. Schnur and M. L. Corman, “Preparation of 17-amino-22-(4'-azido-3'125-iodophenacyl)-17- demethoxygeldanamycin (1): an ansamycin for photoaffinity labeling,” Journal of Labelled Compounds and Radiopharmaceuticals, vol. 34, no. 6, pp. 529–535, 1994. View at Publisher · View at Google Scholar · View at Scopus
  57. P. Miller, R. C. Schnur, E. Barbacci, M. P. Moyer, and J. D. Moyer, “Binding of benzoquinoid ansamycins to p100 correlates with their ability to deplete the erbB2 gene product p185,” Biochemical and Biophysical Research Communications, vol. 201, no. 3, pp. 1313–1319, 1994. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. S. M. Roe, C. Prodromou, R. O'Brien, J. E. Ladbury, P. W. Piper, and L. H. Pearl, “Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin,” Journal of Medicinal Chemistry, vol. 42, no. 2, pp. 260–266, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. H. W. Boucher, G. H. Talbot, J. S. Bradley et al., “Bad bugs, no drugs: no ESKAPE! an update from the Infectious Diseases Society of America,” Clinical Infectious Diseases, vol. 48, no. 1, pp. 1–12, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. J. Z. Sexton, T. J. Wigle, Q. He et al., “Novel inhibitors of E. coli RecA ATPase activity,” Current Chemical Genomics, vol. 4, no. 1, pp. 34–42, 2010. View at Publisher · View at Google Scholar · View at PubMed
  61. G. Scholefield, J.-W. Veening, and H. Murray, “DnaA and ORC: more than DNA replication initiators,” Trends in Cell Biology, vol. 21, no. 3, pp. 188–194, 2011. View at Publisher · View at Google Scholar · View at PubMed