Utilizing Genome-Wide mRNA Profiling to Identify the Cytotoxic Chemotherapeutic Mechanism of Triazoloacridone C-1305 as Direct Microtubule Stabilization - Publication - Bridge of Knowledge

Your account

login

Search

Utilizing Genome-Wide mRNA Profiling to Identify the Cytotoxic Chemotherapeutic Mechanism of Triazoloacridone C-1305 as Direct Microtubule Stabilization

Abstract

Rational drug design and in vitro pharmacology profiling constitute the gold standard in drug development pipelines. Problems arise, however, because this process is often dicult due to limited information regarding the complete identification of a molecule’s biological activities. The increasing aordability of genome-wide next-generation technologies now provides an excellent opportunity to understand a compound’s diverse eects on gene regulation. Here, we used an unbiased approach in lung and colon cancer cell lines to identify the early transcriptomic signatures of C-1305 cytotoxicity that highlight the novel pathways responsible for its biological activity. Our results demonstrate that C-1305 promotes direct microtubule stabilization as a part of its mechanism of action that leads to apoptosis. Furthermore, we show that C-1305 promotes G2 cell cycle arrest by modulating gene expression. The results indicate that C-1305 is the first microtubule stabilizing agent that also is a topoisomerase II inhibitor. This study provides a novel approach and methodology for delineating the antitumor mechanisms of other putative anticancer drug candidates.

Citations

  • 5

    CrossRef

  • 0

    Web of Science

  • 6

    Scopus

Authors (16)

Cite as

Full text

download paper
downloaded 37 times
Publication version
Accepted or Published Version
License
Creative Commons: CC-BY open in new tab

Keywords

Details

Category:
Articles
Type:
artykuły w czasopismach
Published in:
Cancers no. 12,
ISSN: 2072-6694
Language:
English
Publication year:
2020
Bibliographic description:
Króliczewski, J., Bartoszewska S., Dudkowska M., Janiszewska D., Biernatowska A., Crossman D., Krzymiński K., Wysocka m., Romanowska A., Bagiński M., Markuszewski M., Ochocka R., Collawn J., Sikorski A., Sikora E., Bartoszewski R.: Utilizing Genome-Wide mRNA Profiling to Identify the Cytotoxic Chemotherapeutic Mechanism of Triazoloacridone C-1305 as Direct Microtubule Stabilization// Cancers -Vol. 12,iss. 4 (2020), s.864-
DOI:
Digital Object Identifier (open in new tab) 10.3390/cancers12040864
Bibliography: test
  1. Bowes, J.; Brown, A.J.; Hamon, J.; Jarolimek, W.; Sridhar, A.; Waldron, G.; Whitebread, S. Reducing safety-related drug attrition: the use of in vitro pharmacological profiling. Nat. Rev. Drug Discov. 2012, 11, 909-922. [CrossRef] [PubMed] open in new tab
  2. Bartoszewski, R.; Sikorski, A.F. Editorial focus: understanding off-target effects as the key to successful RNAi therapy. Cell. Mol. Biol. Lett. 2019, 24, 69. [CrossRef] [PubMed] open in new tab
  3. Shapiro, E.; Biezuner, T.; Linnarsson, S. Single-cell sequencing-based technologies will revolutionize whole-organism science. Nat. Rev. Genet. 2013, 14, 618-630. [CrossRef] [PubMed] open in new tab
  4. Wu, H.J.; Wang, C.; Wu, S.X. Single-Cell Sequencing for Drug Discovery and Drug Development. Curr. Top. Med. Chem. 2017, 17, 1769-1777. [CrossRef] open in new tab
  5. Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol. 2007, 35, 495-516. [CrossRef] open in new tab
  6. Cholody, W.M.; Martelli, S.; Konopa, J. 8-Substituted 5-[(aminoalkyl)amino]-6H-v-triazolo[4,5,1-de]acridin- 6-ones as potential antineoplastic agents. Synthesis and biological activity. J. Med. Chem. 1990, 33, 2852-2856. [CrossRef] open in new tab
  7. Kusnierczyk, H.; Cholody, W.M.; Paradziej-Lukowicz, J.; Radzikowski, C.; Konopa, J. Experimental antitumor activity and toxicity of the selected triazolo-and imidazoacridinones. Arch. Immunol. Ther. Exp. (Warsz) 1994, 42, 415-423.
  8. Lemke, K.; Poindessous, V.; Skladanowski, A.; Larsen, A.K. The antitumor triazoloacridone C-1305 is a topoisomerase II poison with unusual properties. Mol. Pharmacol. 2004, 66, 1035-1042. [CrossRef] open in new tab
  9. Bram, E.E.; Ifergan, I.; Grimberg, M.; Lemke, K.; Skladanowski, A.; Assaraf, Y.G. C421 allele-specific ABCG2 gene amplification confers resistance to the antitumor triazoloacridone C-1305 in human lung cancer cells. Biochem. Pharmacol. 2007, 74, 41-53. [CrossRef] open in new tab
  10. Capps, D.B.; Dunbar, J.; Kesten, S.R.; Shillis, J.; Werbel, L.M.; Plowman, J.; Ward, D.L. 2-(aminoalkyl)-5- nitropyrazolo[3,4,5-kl]acridines, a new class of anticancer agents. J. Med. Chem. 1992, 35, 4770-4778. [CrossRef] open in new tab
  11. Bartoszewski, R.; Gebert, M.; Janaszak-Jasiecka, A.; Cabaj, A.; Kroliczewski, J.; Bartoszewska, S.; Sobolewska, A.; Crossman, D.K.; Ochocka, R.; Kamysz, W.; et al. Genome-wide mRNA profiling identifies RCAN1 and GADD45A as regulators of the transitional switch from pro-survival to apoptosis during ER stress. FEBS J. 2019. [CrossRef] open in new tab
  12. Bartoszewska, S.; Cabaj, A.; Dabrowski, M.; Collawn, J.F.; Bartoszewski, R. miR-34c-5p modulates X-box-binding protein 1 (XBP1) expression during the adaptive phase of the unfolded protein response. FASEB J. 2019, 33, 11541-11554. [CrossRef] open in new tab
  13. Xi, B.A.; Wang, T.X.; Li, N.; Ouyang, W.; Zhang, W.; Wu, J.Y.; Xu, X.; Wang, X.B.; Abassi, Y.A. Functional Cardiotoxicity Profiling and Screening Using the xCELLigence RTCA Cardio System. Jala 2011, 16, 415-421. [CrossRef] [PubMed] open in new tab
  14. Moniri, M.R.; Young, A.; Reinheimer, K.; Rayat, J.; Dai, L.J.; Warnock, G.L. Dynamic assessment of cell viability, proliferation and migration using real time cell analyzer system (RTCA). Cytotechnology 2015, 67, 379-386. [CrossRef] [PubMed] open in new tab
  15. Wesierska-Gadek, J.; Schloffer, D.; Gueorguieva, M.; Uhl, M.; Skladanowski, A. Increased susceptibility of poly(ADP-ribose) polymerase-1 knockout cells to antitumor triazoloacridone C-1305 is associated with permanent G2 cell cycle arrest. Cancer Res. 2004, 64, 4487-4497. [CrossRef] [PubMed] open in new tab
  16. Gazdar, A.F.; Gao, B.N.; Minna, J.D. Lung cancer cell lines: Useless artifacts or invaluable tools for medical science? Lung Cancer 2010, 68, 309-318. [CrossRef] open in new tab
  17. Ben-Ari Fuchs, S.; Lieder, I.; Stelzer, G.; Mazor, Y.; Buzhor, E.; Kaplan, S.; Bogoch, Y.; Plaschkes, I.; Shitrit, A.; Rappaport, N.; et al. GeneAnalytics: An Integrative Gene Set Analysis Tool for Next Generation Sequencing, RNAseq and Microarray Data. OMICS 2016, 20, 139-151. [CrossRef] open in new tab
  18. Chen, E.Y.; Tan, C.M.; Kou, Y.; Duan, Q.; Wang, Z.; Meirelles, G.V.; Clark, N.R.; Ma'ayan, A. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinform. 2013, 14, 128. [CrossRef] open in new tab
  19. Liao, Y.; Wang, J.; Jaehnig, E.J.; Shi, Z.; Zhang, B. WebGestalt 2019: gene set analysis toolkit with revamped UIs and APIs. Nucleic Acids Res. 2019, 47, W199-W205. [CrossRef] open in new tab
  20. Shibue, T.; Suzuki, S.; Okamoto, H.; Yoshida, H.; Ohba, Y.; Takaoka, A.; Taniguchi, T. Differential contribution of Puma and Noxa in dual regulation of p53-mediated apoptotic pathways. Embo J. 2006, 25, 4952-4962. [CrossRef] open in new tab
  21. Marciniak, S.J.; Yun, C.Y.; Oyadomari, S.; Novoa, I.; Zhang, Y.H.; Jungreis, R.; Nagata, K.; Harding, H.P.; Ron, D. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 2004, 18, 3066-3077. [CrossRef] [PubMed] open in new tab
  22. Jauhiainen, A.; Thomsen, C.; Strombom, L.; Grundevik, P.; Andersson, C.; Danielsson, A.; Andersson, M.K.; Nerman, O.; Rorkvist, L.; Stahlberg, A.; et al. Distinct cytoplasmic and nuclear functions of the stress induced protein DDIT3/CHOP/GADD153. PLoS ONE 2012, 7, e33208. [CrossRef] [PubMed] open in new tab
  23. Chen, H.C.; Kanai, M.; Inoue-Yamauchi, A.; Tu, H.C.; Huang, Y.; Ren, D.; Kim, H.; Takeda, S.; Reyna, D.E.; Chan, P.M.; et al. An interconnected hierarchical model of cell death regulation by the BCL-2 family. Nat. Cell. Biol. 2015, 17, 1270-1281. [CrossRef] [PubMed] open in new tab
  24. Salvador, J.M.; Brown-Clay, J.D.; Fornace, A.J. Gadd45 in Stress Signaling, Cell Cycle Control, and Apoptosis. Adv. Exp. Med. Biol. 2013, 793, 1-19. [CrossRef] open in new tab
  25. Ren, D.; Tu, H.-C.; Kim, H.; Wang, G.X.; Bean, G.R.; Takeuchi, O.; Jeffers, J.R.; Zambetti, G.P.; Hsieh, J.J.D.; Cheng, E.H.Y. BID, BIM, and PUMA Are Essential for Activation of the BAX-and BAK-Dependent Cell Death Program. Science 2010, 330, 1390. [CrossRef] open in new tab
  26. Scott, F.L.; Stec, B.; Pop, C.; Dobaczewska, M.K.; Lee, J.J.; Monosov, E.; Robinson, H.; Salvesen, G.S.; Schwarzenbacher, R.; Riedl, S.J. The Fas-FADD death domain complex structure unravels signalling by receptor clustering. Nature 2009, 457, 1019-1022. [CrossRef] open in new tab
  27. Kuribayashi, K.; Finnberg, N.; Jeffers, J.R.; Zambetti, G.P.; El-Deiry, W.S. The relative contribution of pro-apoptotic p53-target genes in the triggering of apoptosis following DNA damage in vitro and in vivo. Cell Cycle 2011, 10, 2380-2389. [CrossRef] open in new tab
  28. Shrestha, R.L.; Conti, D.; Tamura, N.; Braun, D.; Ramalingam, R.A.; Cieslinski, K.; Ries, J.; Draviam, V.M. Aurora-B kinase pathway controls the lateral to end-on conversion of kinetochore-microtubule attachments in human cells. Nat. Commun. 2017, 8, 150. [CrossRef] open in new tab
  29. Pouwels, J.; Kukkonen, A.M.; Lan, W.; Daum, J.R.; Gorbsky, G.J.; Stukenberg, T.; Kallio, M.J. Shugoshin 1 plays a central role in kinetochore assembly and is required for kinetochore targeting of Plk1. Cell Cycle 2007, 6, 1579-1585. [CrossRef] open in new tab
  30. Jackman, M.; Lindon, C.; Nigg, E.A.; Pines, J. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat. Cell. Biol. 2003, 5, 143-148. [CrossRef] open in new tab
  31. Zhu, C.; Zhao, J.; Bibikova, M.; Leverson, J.D.; Bossy-Wetzel, E.; Fan, J.-B.; Abraham, R.T.; Jiang, W. Functional Analysis of Human Microtubule-based Motor Proteins, the Kinesins and Dyneins, in Mitosis/Cytokinesis Using RNA Interference. Mol. Biol. Cell 2005, 16, 3187-3199. [CrossRef] [PubMed] open in new tab
  32. Rapley, J.; Nicolas, M.; Groen, A.; Regue, L.; Bertran, M.T.; Caelles, C.; Avruch, J.; Roig, J. The NIMA-family kinase Nek6 phosphorylates the kinesin Eg5 at a novel site necessary for mitotic spindle formation. J. Cell. Sci. 2008, 121, 3912-3921. [CrossRef] [PubMed] open in new tab
  33. van Heesbeen, R.G.H.P.; Tanenbaum, M.E.; Medema, R.H. Balanced Activity of Three Mitotic Motors Is Required for Bipolar Spindle Assembly and Chromosome Segregation. Cell Rep. 2014, 8, 948-956. [CrossRef] [PubMed] open in new tab
  34. Huang, Y.; Yao, Y.; Xu, H.Z.; Wang, Z.G.; Lu, L.; Dai, W. Defects in chromosome congression and mitotic progression in KIF18A-deficient cells are partly mediated through impaired functions of CENP-E. Cell Cycle 2009, 8, 2643-2649. [CrossRef] open in new tab
  35. Tanenbaum, M.E.; Macurek, L.; van der Vaart, B.; Galli, M.; Akhmanova, A.; Medema, R.H. A Complex of Kif18b and MCAK Promotes Microtubule Depolymerization and Is Negatively Regulated by Aurora Kinases. Curr. Biol. 2011, 21, 1356-1365. [CrossRef] open in new tab
  36. Tokai, N.; Fujimoto-Nishiyama, A.; Toyoshima, Y.; Yonemura, S.; Tsukita, S.; Inoue, J.; Yamamota, T. Kid, a novel kinesin-like DNA binding protein, is localized to chromosomes and the mitotic spindle. Embo J. 1996, 15, 457-467. [CrossRef] open in new tab
  37. Bourhis, E.; Lingel, A.; Phung, Q.; Fairbrother, W.J.; Cochran, A.G. Phosphorylation of a borealin dimerization domain is required for proper chromosome segregation. Biochemistry 2009, 48, 6783-6793. [CrossRef] open in new tab
  38. Vong, Q.P.; Cao, K.; Li, H.Y.; Iglesias, P.A.; Zheng, Y. Chromosome alignment and segregation regulated by ubiquitination of survivin. Science 2005, 310, 1499-1504. [CrossRef] open in new tab
  39. Cheng, Y.-M.; Tsai, C.-C.; Hsu, Y.-C. Sulforaphane, a Dietary Isothiocyanate, Induces G2/M Arrest in Cervical Cancer Cells through CyclinB1 Downregulation and GADD45β/CDC2 Association. Int. J. Mol. Sci. 2016, 17, 1530. [CrossRef] open in new tab
  40. Bellanger, S.; de Gramont, A.; Sobczak-Thepot, J. Cyclin B2 suppresses mitotic failure and DNA re-replication in human somatic cells knocked down for both cyclins B1 and B2. Oncogene 2007, 26, 7175-7184. [CrossRef] open in new tab
  41. Kraft, C.; Herzog, F.; Gieffers, C.; Mechtler, K.; Hagting, A.; Pines, J.; Peters, J.M. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. Embo J. 2003, 22, 6598-6609. [CrossRef] [PubMed] open in new tab
  42. Lukasova, E.; Kovar ik, A.; Bac ikova, A.; Falk, M.; Kozubek, S. Loss of lamin B receptor is necessary to induce cellular senescence. Biochem. J. 2017, 474, 281-300. [CrossRef] [PubMed] open in new tab
  43. Liao, H.; Winkfein, R.J.; Mack, G.; Rattner, J.B.; Yen, T.J. CENP-F is a protein of the nuclear matrix that assembles onto kinetochores at late G2 and is rapidly degraded after mitosis. J. Cell. Biol. 1995, 130, 507-518. [CrossRef] [PubMed] open in new tab
  44. Hung, L.Y.; Chen, H.L.; Chang, C.W.; Li, B.R.; Tang, T.K. Identification of a novel microtubule-destabilizing motif in CPAP that binds to tubulin heterodimers and inhibits microtubule assembly. Mol. Biol. Cell. 2004, 15, 2697-2706. [CrossRef] [PubMed] open in new tab
  45. Cheeseman, I.M.; Hori, T.; Fukagawa, T.; Desai, A. KNL1 and the CENP-H/I/K complex coordinately direct kinetochore assembly in vertebrates. Mol. Biol. Cell. 2008, 19, 587-594. [CrossRef] [PubMed] open in new tab
  46. McKinley, K.L.; Sekulic, N.; Guo, L.Y.; Tsinman, T.; Black, B.E.; Cheeseman, I.M. The CENP-L-N Complex Forms a Critical Node in an Integrated Meshwork of Interactions at the Centromere-Kinetochore Interface. Mol. Cell. 2015, 60, 886-898. [CrossRef] [PubMed] open in new tab
  47. Bancroft, J.; Auckland, P.; Samora, C.P.; McAinsh, A.D. Chromosome congression is promoted by CENP-Q- and CENP-E-dependent pathways. J. Cell. Sci. 2015, 128, 171-184. [CrossRef] open in new tab
  48. Wang, Z.; Liu, Y.; Zhang, P.; Zhang, W.; Wang, W.; Curr, K.; Wei, G.; Mao, J.H. FAM83D promotes cell proliferation and motility by downregulating tumor suppressor gene FBXW7. Oncotarget 2013, 4, 2476-2486. [CrossRef] open in new tab
  49. Pe'er, T.; Lahmi, R.; Sharaby, Y.; Chorni, E.; Noach, M.; Vecsler, M.; Zlotorynski, E.; Steen, H.; Steen, J.A.; Tzur, A. Gas2l3, a novel constriction site-associated protein whose regulation is mediated by the APC/C Cdh1 complex. PLoS ONE 2013, 8, e57532. [CrossRef] open in new tab
  50. Li, C.; Zhang, Y.; Yang, Q.; Ye, F.; Sun, S.Y.; Chen, E.S.; Liou, Y.C. NuSAP modulates the dynamics of kinetochore microtubules by attenuating MCAK depolymerisation activity. Sci. Rep. 2016, 6, 18773. [CrossRef] open in new tab
  51. Kellogg, E.H.; Howes, S.; Ti, S.C.; Ramirez-Aportela, E.; Kapoor, T.M.; Chacon, P.; Nogales, E. Near-atomic cryo-EM structure of PRC1 bound to the microtubule. Proc. Natl. Acad. Sci. USA 2016, 113, 9430-9439. [CrossRef] [PubMed] open in new tab
  52. Welburn, J.P.; Grishchuk, E.L.; Backer, C.B.; Wilson-Kubalek, E.M.; Yates, J.R., 3rd; Cheeseman, I.M. The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev. Cell 2009, 16, 374-385. [CrossRef] [PubMed] open in new tab
  53. Rubin, C.I.; Atweh, G.F. The role of stathmin in the regulation of the cell cycle. J. Cell. Biochem. 2004, 93, 242-250. [CrossRef] [PubMed] open in new tab
  54. Polyak, K.; Xia, Y.; Zweier, J.L.; Kinzler, K.W.; Vogelstein, B. A model for p53-induced apoptosis. Nature 1997, 389, 300-305. [CrossRef] open in new tab
  55. Seillier, M.; Peuget, S.; Gayet, O.; Gauthier, C.; N'Guessan, P.; Monte, M.; Carrier, A.; Iovanna, J.L.; Dusetti, N.J. TP53INP1, a tumor suppressor, interacts with LC3 and ATG8-family proteins through the LC3-interacting region (LIR) and promotes autophagy-dependent cell death. Cell Death Differ. 2012, 19, 1525-1535. [CrossRef] [PubMed] open in new tab
  56. Hemavathy, K.; Guru, S.C.; Harris, J.; Chen, J.D.; Ip, Y.T. Human Slug is a repressor that localizes to sites of active transcription. Mol. Cell. Biol. 2000, 20, 5087-5095. [CrossRef] open in new tab
  57. Khoury-Haddad, H.; Guttmann-Raviv, N.; Ipenberg, I.; Huggins, D.; Jeyasekharan, A.D.; Ayoub, N. PARP1-dependent recruitment of KDM4D histone demethylase to DNA damage sites promotes double-strand break repair. Proc. Natl. Acad. Sci. USA 2014, 111, E728-E737. [CrossRef] open in new tab
  58. Zhu, L.; Chen, L. Progress in research on paclitaxel and tumor immunotherapy. Cell. Mol. Biol. Lett. 2019, 24, 40. [CrossRef] open in new tab
  59. Snyder, J.P.; Nettles, J.H.; Cornett, B.; Downing, K.H.; Nogales, E. The binding conformation of Taxol in beta-tubulin: A model based on electron crystallographic density. Proc. Natl. Acad. Sci. USA 2001, 98, 5312-5316. [CrossRef] open in new tab
  60. Farce, A.; Loge, C.; Gallet, S.; Lebegue, N.; Carato, P.; Chavatte, P.; Berthelot, P.; Lesieur, D. Docking study of ligands into the colchicine binding site of tubulin. J. Enzyme. Inhib. Med. Chem. 2004, 19, 541-547. [CrossRef] open in new tab
  61. Pettersen, E.F.; Goddard, T.D.; Huang, C.C.; Couch, G.S.; Greenblatt, D.M.; Meng, E.C.; Ferrin, T.E. UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25, 1605-1612. [CrossRef] [PubMed] open in new tab
  62. Nogales, E.; Wolf, S.G.; Downing, K.H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 1998, 391, 199-203. [CrossRef] [PubMed] open in new tab
  63. Irwin, J.J.; Shoichet, B.K. ZINC-A free database of commercially available compounds for virtual screening. J. Chem. Inf. Model. 2005, 45, 177-182. [CrossRef] [PubMed] open in new tab
  64. Shoffner, S.K.; Schnell, S. Estimation of the lag time in a subsequent monomer addition model for fibril elongation. Phys. Chem. Chem. Phys. 2016, 18, 21259-21268. [CrossRef] [PubMed] open in new tab
  65. Martel-Frachet, V.; Keramidas, M.; Nurisso, A.; DeBonis, S.; Rome, C.; Coll, J.L.; Boumendjel, A.; Skoufias, D.A.; Ronot, X. IPP51, a chalcone acting as a microtubule inhibitor with in vivo antitumor activity against bladder carcinoma. Oncotarget 2015, 6, 14669-14686. [CrossRef] [PubMed] open in new tab
  66. Risinger, A.L.; Li, J.; Bennett, M.J.; Rohena, C.C.; Peng, J.; Schriemer, D.C.; Mooberry, S.L. Taccalonolide binding to tubulin imparts microtubule stability and potent in vivo activity. Cancer Res. 2013, 73, 6780-6792. [CrossRef] [PubMed] open in new tab
  67. Mu, Y.; Liu, Y.; Li, L.; Tian, C.; Zhou, H.; Zhang, Q.; Yan, B. The Novel Tubulin Polymerization Inhibitor MHPT Exhibits Selective Anti-Tumor Activity against Rhabdomyosarcoma In Vitro and In Vivo. PLOS ONE 2015, 10, e0121806. [CrossRef] open in new tab
  68. Augustin, E.; Mos-Rompa, A.; Skwarska, A.; Witkowski, J.M.; Konopa, J. Induction of G2/M phase arrest and apoptosis of human leukemia cells by potent antitumor triazoloacridinone C-1305. Biochem. Pharmacol. 2006, 72, 1668-1679. [CrossRef] open in new tab
  69. Wahl, A.F.; Donaldson, K.L.; Fairchild, C.; Lee, F.Y.; Foster, S.A.; Demers, G.W.; Galloway, D.A. Loss of normal p53 function confers sensitization to Taxol by increasing G2/M arrest and apoptosis. Nat. Med. 1996, 2, 72-79. [CrossRef] open in new tab
  70. Horwitz, S.B. Taxol (paclitaxel): mechanisms of action. Ann. Oncol. 1994, 5 Suppl 6, S3-6. open in new tab
  71. Bollag, D.M.; Mcqueney, P.A.; Zhu, J.; Hensens, O.; Koupal, L.; Liesch, J.; Goetz, M.; Lazarides, E.; Woods, C.M. Epothilones, a New Class of Microtubule-Stabilizing Agents with a Taxol-Like Mechanism of Action. Cancer Res. 1995, 55, 2325-2333. [PubMed]
  72. Blajeski, A.L.; Phan, V.A.; Kottke, T.J.; Kaufmann, S.H. G(1) and G(2) cell-cycle arrest following microtubule depolymerization in human breast cancer cells. J. Clin. Investig. 2002, 110, 91-99. [CrossRef] [PubMed] open in new tab
  73. Lemke, K.; Wojciechowski, M.; Laine, W.; Bailly, C.; Colson, P.; Baginski, M.; Larsen, A.K.; Skladanowski, A. Induction of unique structural changes in guanine-rich DNA regions by the triazoloacridone C-1305, a topoisomerase II inhibitor with antitumor activities. Nucleic Acids Res. 2005, 33, 6034-6047. [CrossRef] [PubMed] open in new tab
  74. Koba, M.; Konopa, J. Interactions of antitumor triazoloacridinones with DNA. Acta. Biochim. Pol. 2007, 54, 297-306. [CrossRef] [PubMed] open in new tab
  75. Wang, J.C. Cellular roles of DNA topoisomerases: A molecular perspective. Nat. Rev. Mol. Cell. Biol. 2002, 3, 430-440. [CrossRef] [PubMed] open in new tab
  76. Pawlowska, M.; Augustin, E.; Mazerska, Z. CYP3A4 overexpression enhances apoptosis induced by anticancer agent imidazoacridinone C-1311, but does not change the metabolism of C-1311 in CHO cells. Acta. Pharmacol. Sin. 2014, 35, 98-112. [CrossRef] [PubMed] open in new tab
  77. Niemira, M.; Dastych, J.; Mazerska, Z. Pregnane X receptor dependent up-regulation of CYP2C9 and CYP3A4 in tumor cells by antitumor acridine agents, C-1748 and C-1305, selectively diminished under hypoxia. Biochem. Pharmacol. 2013, 86, 231-241. [CrossRef] open in new tab
  78. Augustin, E.; Skwarska, A.; Weryszko, A.; Pelikant, I.; Sankowska, E.; Borowa-Mazgaj, B. The antitumor compound triazoloacridinone C-1305 inhibits FLT3 kinase activity and potentiates apoptosis in mutant FLT3-ITD leukemia cells. Acta Pharm. Sin. 2015, 36, 385-399. [CrossRef] open in new tab
  79. Kanai, M.; Tong, W.M.; Sugihara, E.; Wang, Z.Q.; Fukasawa, K.; Miwa, M. Involvement of poly(ADP-Ribose) polymerase 1 and poly(ADP-Ribosyl)ation in regulation of centrosome function. Mol. Cell. Biol. 2003, 23, 2451-2462. [CrossRef] open in new tab
  80. Giannakakou, P.; Sackett, D.L.; Ward, Y.; Webster, K.R.; Blagosklonny, M.V.; Fojo, T. p53 is associated with cellular microtubules and is transported to the nucleus by dynein. Nat. Cell Biol. 2000, 2, 709-717. [CrossRef] open in new tab
  81. Contadini, C.; Monteonofrio, L.; Virdia, I.; Prodosmo, A.; Valente, D.; Chessa, L.; Musio, A.; Fava, L.L.; Rinaldo, C.; Di Rocco, G.; et al. p53 mitotic centrosome localization preserves centrosome integrity and works as sensor for the mitotic surveillance pathway. Cell. Death. Dis. 2019, 10. [CrossRef] [PubMed] open in new tab
  82. Slade, D. Mitotic functions of poly(ADP-ribose) polymerases. Biochem. Pharmacol. 2019, 167, 33-43. [CrossRef] [PubMed] open in new tab
  83. Galmarini, C.M.; Kamath, K.; Vanier-Viornery, A.; Hervieu, V.; Peiller, E.; Falette, N.; Puisieux, A.; Jordan, M.A.; Dumontet, C. Drug resistance associated with loss of p53 involves extensive alterations in microtubule composition and dynamics. Br. J. Cancer 2003, 88, 1793-1799. [CrossRef] [PubMed] open in new tab
  84. Topcul, M.; Ceti, N.I.; Ozbas Turan, S.; Kolusayin Ozar, M.O. In vitro cytotoxic effect of PARP inhibitor alone and in combination with nabpaclitaxel on triplenegative and luminal A breast cancer cells. Oncol. Rep. 2018, 40, 527-535. [CrossRef] open in new tab
  85. Lu, Y.; Liu, Y.; Pang, Y.; Pacak, K.; Yang, C. Double-barreled gun: Combination of PARP inhibitor with conventional chemotherapy. Pharmacol. Ther. 2018, 188, 168-175. [CrossRef] open in new tab
  86. Solary, E.; Leteurtre, F.; Paull, K.D.; Scudiero, D.; Hamel, E.; Pommier, Y. Dual inhibition of topoisomerase II and tubulin polymerization by azatoxin, a novel cytotoxic agent. Biochem. Pharmacol. 1993, 45, 2449-2456. [CrossRef] open in new tab
  87. Yi, J.M.; Zhang, X.F.; Huan, X.J.; Song, S.S.; Wang, W.; Tian, Q.T.; Sun, Y.M.; Chen, Y.; Ding, J.; Wang, Y.Q.; et al. Dual targeting of microtubule and topoisomerase II by alpha-carboline derivative YCH337 for tumor proliferation and growth inhibition. Oncotarget 2015, 6, 8960-8973. [CrossRef] open in new tab
  88. Hevener, K.; Verstak, T.A.; Lutat, K.E.; Riggsbee, D.L.; Mooney, J.W. Recent developments in topoisomerase-targeted cancer chemotherapy. Acta Pharm. Sin. B 2018, 8, 844-861. [CrossRef] open in new tab
  89. Cozens, A.L.; Yezzi, M.J.; Kunzelmann, K.; Ohrui, T.; Chin, L.; Eng, K.; Finkbeiner, W.E.; Widdicombe, J.H.; Gruenert, D.C. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am. J. Respir. Cell. Mol. Biol. 1994, 10, 38-47. [CrossRef] open in new tab
  90. Dobin, A.; Davis, C.A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T.R. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013, 29, 15-21. [CrossRef] open in new tab
  91. Trapnell, C.; Williams, B.A.; Pertea, G.; Mortazavi, A.; Kwan, G.; van Baren, M.J.; Salzberg, S.L.; Wold, B.J.; Pachter, L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28, 511. [CrossRef] [PubMed] open in new tab
  92. Anders, S.; Pyl, P.T.; Huber, W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 2015, 31, 166-169. [CrossRef] [PubMed] open in new tab
  93. Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [CrossRef] [PubMed] open in new tab
  94. Larionov, A.; Krause, A.; Miller, W. A standard curve based method for relative real time PCR data processing. BMC Bioinform. 2005, 6, 62. [CrossRef] open in new tab
  95. Bartoszewski, R.; Hering, A.; Marszall, M.; Stefanowicz Hajduk, J.; Bartoszewska, S.; Kapoor, N.; Kochan, K.; Ochocka, R. Mangiferin has an additive effect on the apoptotic properties of hesperidin in Cyclopia sp. tea extracts. PLoS ONE 2014, 9, e92128. [CrossRef] open in new tab
  96. SwissDock. Available online: www.swissdock.ch/docking# (accessed on 25 March 2020). open in new tab
  97. Grosdidier, A.; Zoete, V.; Michielin, O. EADock: docking of small molecules into protein active sites with a multiobjective evolutionary optimization. Proteins 2007, 67, 1010-1025. [CrossRef] open in new tab
  98. Hanwell, M.D.; Curtis, D.E.; Lonie, D.C.; Vandermeersch, T.; Zurek, E.; Hutchison, G.R. Avogadro: an advanced semantic chemical editor, visualization, and analysis platform. J. Cheminform. 2012, 4, 17. [CrossRef] open in new tab
  99. Prota, A.E.; Danel, F.; Bachmann, F.; Bargsten, K.; Buey, R.M.; Pohlmann, J.; Reinelt, S.; Lane, H.; Steinmetz, M.O. The novel microtubule-destabilizing drug BAL27862 binds to the colchicine site of tubulin with distinct effects on microtubule organization. J. Mol. Biol. 2014, 426, 1848-1860. [CrossRef] open in new tab
  100. Shelanski, M.L.; Gaskin, F.; Cantor, C.R. Microtubule assembly in the absence of added nucleotides. Proc. Natl. Acad. Sci. USA 1973, 70, 765-768. [CrossRef] open in new tab
  101. Kavallaris, M.; Tait, A.S.; Walsh, B.J.; He, L.; Horwitz, S.B.; Norris, M.D.; Haber, M. Multiple microtubule alterations are associated with Vinca alkaloid resistance in human leukemia cells. Cancer Res. 2001, 61, 5803-5809. open in new tab
  102. Kruskal, W.H.; Wallis, W.A. Use of Ranks in One-Criterion Variance Analysis. J. Am. Stat. Assoc. 1952, 47, 583-621. [CrossRef] open in new tab
  103. Dunn, O.J. Multiple Comparisons Using Rank Sums. Technometrics 1964, 6, 241. [CrossRef] open in new tab
  104. Gene Expression Omnibus (GEO). Available online: www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc= GSE143649 (accessed on 25 March 2020). open in new tab
  105. © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). open in new tab
Sources of funding:
Verified by:
Gdańsk University of Technology

seen 122 times

Recommended for you

Novel chalcone-derived pyrazoles as potential therapeutic agents for the treatment of non-small cell lung cancer

2022

Triazoloacridone C-1305 impairs XBP1 splicing by acting as a potential IRE1α endoribonuclease inhibitor

  • S. Bartoszewska,
  • J. Króliczewski,
  • D. Crossman
  • + 4 authors
2021

DNA-damaging imidazoacridinone C-1311 induces autophagy followed by irreversible growth arrest and senescence in human lung cancer cells

2013

Increased cytotoxicity of an unusual DNA topoisomerase II inhibitor compound C-1305 toward HeLa cells with downregulated PARP-1 activity results from re-activation of the p53 pathway and modulation of mitotic checkpoints

2010
Meta Tags