Inhibition of DNA topoisomerase I activity and induction of apoptosis by thiazacridine derivatives

Toxicology and Applied Pharmacology

Volumn 268, Issue 1, 2013, Pages 37-46

  Barros, Francisco W A ^a   Bezerra, Daniel P ^b   Ferreira, Paulo M P ^c   Cavalcanti, Bruno C ^a   Silva, Teresinha G ^d   Pitta, Marina G R ^d   de Lima, Maria do C A ^d   Galdino, Suely L ^d   Pitta, Ivan da R ^d   Costa Lotufo, Letícia V ^a   Moraes, Manoel O ^a   Burbano, Rommel R ^e   Guecheva, Temenouga N ^f   Henriques, João A P ^f   Pessoa, Cláudia ^a  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^c FEDERAL UNIVERSITY OF PIAUÍ   (Brazil)

^d FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^e FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^f FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Acridine; Apoptosis; DNA topoisomerase I; Thiazacridine; Thiazolidine

Indexed keywords

ACRIDINE; CASPASE 3; CASPASE 7; CYTOTOXIC AGENT; DNA TOPOISOMERASE; ETHIDIUM; PHOSPHATIDYLSERINE; THIAZACRIDINE DERIVATIVE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL MEMBRANE DEPOLARIZATION; CELL PROLIFERATION; COLON CARCINOMA; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENOTOXICITY; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; SACCHAROMYCES CEREVISIAE;

ACRIDINES; APOPTOSIS; CASPASES; CELL LINE, TUMOR; CELL SURVIVAL; COLONIC NEOPLASMS; COMET ASSAY; DNA FRAGMENTATION; DNA TOPOISOMERASES, TYPE I; HUMANS; MICROSCOPY, FLUORESCENCE; SACCHAROMYCES CEREVISIAE; TELOMERASE; THIAZOLIDINEDIONES;

EID: 84873886660     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.01.010     Document Type: Article

References (54)

1. Attia S.M. Mutagenicity of some topoisomerase II-interactive agents. Saudi Pharm. J. 2008, 17:1-24.
2. Attia, S.M., in press. Molecular cytogenetic evaluation of the mechanism of genotoxic potential of amsacrine and nocodazole in mouse bone marrow cells. J. Appl. Toxicol. doi:10.1002/jat.1753.
3. Barros C.D., Amato A.A., de Oliveira T.B., Iannini K.B., Silva A.L., Silva T.G., Leite E.S., Hernandes M.Z., Lima M.C.A., Galdino S.L., Neves F.A., Pitta I.R. Synthesis and anti-inflammatory activity of new arylidene-thiazolidine-2,4-diones as PPAR ligands. Bioorg. Med. Chem. 2010, 18:3805-3811.
4. Barros F.W., Silva T.G., Pitta M.G.R., Bezerra D.P., Costa-Lotufo L.V., de Moraes M.O., Pessoa C., de Moura M.A., de Abreu F.C., de Lima M.D., Galdino S.L., Pitta I.R., Goulart M.O. Synthesis and cytotoxic activity of new acridine-thiazolidine derivatives. Bioorg. Med. Chem. 2012, 20:3533-3539.
5. Belmont P., Bosson J., Godet T., Tiano M. Acridine and acridone derivatives, anticancer properties and synthetic methods: where are we now?. Anticancer Agents Med. Chem. 2007, 7:139-169.
6. Bender M.A., Awa A.A., Brooks A.L., Evans H.J., Groer P.G., Littlefield L.G., Pereira C., Preston R.J., Wachholz B.W. Current status of cytogenetic procedures to detect and quantify previous exposures to radiation. Mutat. Res. 1988, 196:103-159.
7. Berthold F. Isolation of human monocytes by ficoll density gradient centrifugation. Blut 1981, 3:367-371.
8. Blasiak J., Gloc E., Drzewoski J., Wozniak K., Zadrozny M., Skórski T., Pertynski T. Free radical scavengers can differentially modulate the genotoxicity of amsacrine in normal and cancer cells. Mutat. Res. 2003, 535:25-34.
9. Brown M.G., Lawce H.J. Peripheral blood cytogenetic methods. The AGT Cytogenetics Laboratory Manual 1997, 77-171. Lippincott-Raven Publishers, Philadelphia. M.J. Barch, T. Knutsen, J.L. Spurbeck (Eds.).
10. Burke D., Dawson D., Stearns T. Methods in Yeast Genetics 2000, Cold Spring Harbor, Laboratory Press, New York.
11. Castillo-González D., Cabrera-Pérez M.A., Pérez-González M., Helguera A.M., Durán-Martínez A. Prediction of telomerase inhibitory activity for acridinic derivatives based on chemical structure. Eur. J. Med. Chem. 2009, 44:4826-4840.
12. Cavalcanti B.C., Sombra C.M.L., Oliveira J.H.H.L., Berlinck R.G.S., Moraes M.O., Pessoa C. Cytotoxicity and genotoxicity of ingenamine G isolated from the Brazilian marine sponge Pachychalina alcaloidifera. Comp. Biochem. Physiol. C 2008, 147:409-415.
13. Fan T.J., Han L.H., Cong R.S., Liang J. Caspase family proteases and apoptosis. Acta Biochim. Biophys. Sin. 2005, 37:719-727.
14. Gao S., Xu Y.M., Valeriote F.A., Gunatilaka A.A. Pierreiones A-D, solid tumour selective pyranoisoflavones and other cytotoxic constituents from Antheroporum pierrei. J. Nat. Prod. 2011, 74:852-856.
15. Gorman A.M., Samali A., McGowan A.J., Cotter T.G. Use of flow cytometry techniques in studying mechanisms of apoptosis in leukemic cells. Cytometry 1997, 29:97-105.
16. Guo C., Gasparian A.V., Zhuang Z., Bosykh D.A., Komar A.A., Gudkov A.V., Gurova K.V. 9-Aminoacridine-based anticancer drugs target the PI3K/AKT/mTOR, NF-kappaB and p53 pathways. Oncogene 2009, 28:1151-1161.
17. Hartmann J.T., Lipp H.P. Camptothecin and podophyllotoxin derivatives: inhibitors of topoisomerase I and II-mechanisms of action, pharmacokinetics and toxicity profile. Drug Saf. 2006, 29:209-230.
18. Hartmann A., Speit G. The contribution of cytotoxicity to DNA effects in the single cell gel test (comet assay). Toxicol. Lett. 1997, 90:183-188.
19. Hsiang Y.H., Lihou M.G., Liu L.F. Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res. 1989, 49:5077-5082.
20. Hutchins D., Steel C.M. Phytohaemagglutinin-induced proliferation of human T lymphocytes: differences between neonate and adults in accessory cell requirements. Clin. Exp. Immunol. 1983, 52:355-364.
21. Kao-Shan C.S., Micetich K., Zwelling L.A., Whang-Peng J. Cytogenetic effects of amsacrine on human lymphocytes in vivo and in vitro. Cancer Treat. Rep. 1984, 68:989-997.
22. Ketron A.C., Denny W.A., Graves D.E., Osheroff N. Amsacrine as a topoisomerase II poison: importance of drug-DNA interactions. Biochemistry 2012, 51:1730-1739.
23. Kitazumi I., Tsukahara M. Regulation of DNA fragmentation: the role of caspases and phosphorylation. FEBS J. 2011, 278:427-441.
24. Kolokythas G., Pouli N., Marakos P., Pratsinis H., Kletsas D. Design, synthesis and antiproliferative activity of some new azapyranoxanthenone aminoderivatives. Eur. J. Med. Chem. 2006, 41:71-79.
25. Kothakota S., Azuma T., Reinhard C., Klippel A., Tang J., Chu K., McGarry T.J., Kirschner M.W., Koths K., Kwiatkowski D.J., Williams L.T. Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 1997, 278:294-298.
26. Lansdorp P.M. Telomere length and proliferation potential of hematopoietic stem cells. J. Cell Sci. 1995, 108:1-6.
27. Lansdorp P.M., Verwoerd N.P., van de Rijke F.M., Dragowska V., Little M.T., Dirks R.W., Raap H.J. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 1996, 5:685-691.
28. 2 checkpoint proteins with cisplatin. Anticancer Res. 1998, 18:4057-4066.
29. Los M., Burek C.J., Stroh C., Benedyk K., Hug H., Mackiewicz A. Anticancer drugs of tomorrow: apoptotic pathways as target for drug design. Drug Discov. Today 2003, 8:67-77.
30. McGahon A.J., Martin S.J., Bissonnette R.P., Mahboubi A., Shi Y., Mogil R.J., Nishioka W.K., Green D.R. The end of the (cell) line: methods for the study of apoptosis in vitro. Methods Cell Biol. 1995, 46:153-185.
31. Miao Z.H., Player A., Shankavaram U., Wang Y.H., Zimonjic D.B., Lorenzi P.L., Liao Z.Y., Liu H., Shimura T., Zhang H.L., Meng L.H., Zhang Y.W., Kawasaki E.S., Popescu N.C., Aladjem M.I., Goldstein D.J., Weinstein J.N., Pommier Y. Nonclassic functions of human topoisomerase I: genome-wide and pharmacologic analyses. Cancer Res. 2007, 67:8752-8761.
32. Moorhead P.S., Nomell P.C., Mellman W.J., Battips D.M., Hungerford D.A. Chromosome preparations of leukocytes cultured from human peripheral blood. Exp. Cell Res. 1960, 20:613-616.
33. Moukharskaya J., Verschraegen C. Topoisomerase 1 inhibitors and cancer therapy. Hematol. Oncol. Clin. North Am. 2012, 26:507-525.
34. Mourão R.H., Silva T.G., Soares A.L., Vieira E.S., Santos J.N., Lima M.C., Lima V.L., Galdino S.L., Barbe J., Pitta I.R. Synthesis and biological activity of novel acridinylidene and benzylidene thiazolidinediones. Eur. J. Med. Chem. 2005, 40:1129-1133.
35. Nicoletti I., Magliorati G., Pagliacci M.C., Grignani F., Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 1991, 139:271-279.
36. Nishi Y., Miyakawa Y., Kato K. Chromosome aberrations induced by pyrolysates of carbohydrates in Chinese hamster V79 cells. Mutat. Res. 1989, 227:117-123.
37. Oppegard L.M., Ougolkov A.V., Luchini D.N., Schoon R.A., Goodell J.R., Kaur H., Billadeau D.D., Ferguson D.M., Hiasa H. Novel acridine-based compounds that exhibit an anti-pancreatic cancer activity are catalytic inhibitors of human topoisomerase II. Eur. J. Pharmacol. 2009, 602:223-229.
38. Pommier Y., Pourquier P., Fan Y., Strumberg D. Mechanism of action of eukaryotic DNA topoisomerase I and drugs targeted to the enzyme. Biochim. Biophys. Acta 1998, 1400:83-105.
39. Pommier Y., Leo E., Zhang H., Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol. 2010, 17:421-433.
40. Poon S.S., Martens U.M., Ward R.K., Lansdorp P.M. Telomere length measurements using digital fluorescence microscopy. Cytometry 1999, 36:267-278.
41. Potmesil M. Camptothecins: from bench research to hospital wards. Cancer Res. 1994, 54:1431-1439.
42. Preston R.J., San Sebastian J.R., McFee A.F. The in vitro human lymphocyte assay for assessing the clastogenicity of chemical agents. Mutat. Res. 1987, 189:175-183.
43. Schultz D.R., Harrington W.J. Apoptosis: programmed cell death at molecular level. Semin. Arthritis Rheum. 2003, 32:345-369.
44. Sebestik J., Hlavacek J., Stibor I. A role of the 9-aminoacridines and their conjugates in a life science. Curr. Protein Pept. Sci. 2007, 8:471-483.
45. Sebolt J.S., Scavone S.V., Pinter C.D., Hamelehle K.L., Von Hoff D.D., Jackson R.C. Pyrazoloacridines, a new class of anticancer agents with selectivity against solid tumours in vitro. Cancer Res. 1987, 47:4299-4304.
46. Silva T.G., Barbosa F.S.V., Brandão S.S.F., Lima M.C.A., Galdino S.L., Pitta I.R., Barbe J. Synthesis and structural elucidation of new benzylidene imidazolidines and acridinylidene thiazolidines. Heterocycl. Commun. 2001, 7:523-528.
47. Singh N.P., Mccoy M.T., Tice R.R., Schneider E.L.A. Single technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 1988, 175:184-191.
48. Speit G., Hartmann A. The comet assay (single-cell gel test). A sensitive genotoxicity test for the detection of DNA damage and repair. Methods Mol. Biol. 1999, 113:203-212.
49. Stewart L., Redinbo M.R., Qiu X., Hol W.G., Champoux J.J. A model for the mechanism of human topoisomerase I. Science 1998, 279:1534-1541.
50. Sureda F.X., Escubedo E., Gabriel C., Comas J., Camarasa J., Camins A. Mitochondrial membrane potential measurement in rat cerebellar neurons by flow cytometry. Cytometry 1997, 28:74-80.
51. Thale Z., Johnson T., Tenney K., Wenzel P.J., Lobkovsky E., Clardy J., Media J., Pietraszkiewicz H., Valeriote F.A., Crews P. Structures and cytotoxic properties of sponge-derived bisannulated acridines. J. Org. Chem. 2002, 67:9384-9391.
52. Vermes I., Haanen C., Steffens-Nakken H., Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods 1995, 184:39-51.
53. Vos S.M., Tretter E.M., Schmidt B.H., Berger J.M. All tangled up: how cells direct, manage and exploit topoisomerase function. Nat. Rev. Mol. Cell Biol. 2011, 12:827-841.
54. Wojcik A., Sauer K., Zolzer F., Bauch T., Muller W.U. Analysis of DNA damage recovery processes in the adaptive response to ionizing radiation in human lymphocytes. Mutagenesis 1996, 11:291-297.