1,040
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

Inhibition mechanism of naphthylphenylamine derivatives acting on the CDC25B dual phosphatase and analysis of the molecular processes involved in the high cytotoxicity exerted by one selected derivative in melanoma cells

, , , , , , , , , & show all
Pages 1866-1878 | Received 29 Jul 2020, Accepted 31 Aug 2020, Published online: 29 Sep 2020

References

  • Diaz-Moralli S, Tarrado-Castellarnau M, Miranda A, Cascante M. Targeting cell cycle regulation in cancer therapy. Pharmacol Ther 2013;138:255–71.
  • Manchado E, Guillamot M, Malumbres M. Killing cells by targeting mitosis. Cell Death Differ 2012;19:369–77.
  • Malumbres M, Barbacid M. Mammalian cyclin-dependent kinases. Trends Biochem Sci 2005;30:630–41.
  • Nilsson I, Hoffmann I. Cell cycle regulation by the Cdc25 phosphatase family. Prog Cell Cycle Res 2000;4:107–14.
  • Aressy B, Ducommun B. Cell cycle control by the CDC25 phosphatases. Anticancer Agents Med Chem 2008;8:818–24.
  • Boudolf V, Inze D, De Veylder L. What if higher plants lack a CDC25 phosphatase? Trends Plant Sci 2006;11:474–9.
  • Mailand N, Podtelejnikov AV, Groth A, et al. Regulation of G(2)/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J 2002;21:5911–20.
  • Sur S, Agrawal DK. Phosphatases and kinases regulating CDC25 activity in the cell cycle: clinical implications of CDC25 overexpression and potential treatment strategies. Mol Cell Biochem 2016;416:33–46.
  • Crncec A, Hochegger H. Triggering mitosis. FEBS Lett 2019;593:2868–88.
  • Lee G, White LS, Hurov KE, et al. Response of small intestinal epithelial cells to acute disruption of cell division through CDC25 deletion. Proc Natl Acad Sci USA 2009;106:4701–6.
  • Kristjánsdóttir K, Rudolph J. Cdc25 phosphatases and cancer. Chem Biol 2004;11:1043–51.
  • Al-Matouq J, Holmes TR, Hansen LA. CDC25B and CDC25C overexpression in nonmelanoma skin cancer suppresses cell death. Mol Carcinog 2019;58:1691–700.
  • Tang L, Li G, Tron VA, et al. Expression of cell cycle regulators in human cutaneous malignant melanoma. Melanoma Res 1999;9:148–54.
  • Cerchia C, Lavecchia A. Small molecule drugs and targeted therapy for melanoma: current strategies and future directions. Curr Med Chem 2017;24:2312–44.
  • Brezak MC, Valette A, Quaranta M, et al. IRC-083864, a novel bis quinone inhibitor of CDC25 phosphatases active against human cancer cells. Int J Cancer 2009;124:1449–56.
  • Lavecchia A, Di Giovanni C, Pesapane A, et al. Discovery of new inhibitors of Cdc25b dual specificity phosphatases by structure-based virtual screening. J Med Chem 2012;55:4142–58.
  • Capasso A, Cerchia C, Di Giovanni C, et al. Ligand-based chemoinformatic discovery of a novel small molecule inhibitor targeting Cdc25 dual specificity phosphatases and displaying in vitro efficacy against melanoma cells. Oncotarget 2015;6:40202–22.
  • Cerchia C, Nasso R, Mori M, et al. Discovery of novel naphthylphenylketone and naphthylphenylamine derivatives as cell division cycle 25B (CDC25B) phosphatase inhibitors: design, synthesis, inhibition mechanism, and in vitro efficacy against melanoma cell lines. J Med Chem 2019;62:7089–110.
  • Brezak MC, Quaranta M, Contour-Galcera MO, et al. Inhibition of human tumor cell growth in vivo by an orally bioavailable inhibitor of CDC25 phosphatases. Mol Cancer Ther 2005;4:1378–87.
  • Brezak MC, Quaranta M, Mondesert O, et al. A novel synthetic inhibitor of CDC25 phosphatases: BN82002. Cancer Res 2004;64:3320–5.
  • Brenner AK, Reikvam H, Lavecchia A, Bruserud O. Therapeutic targeting the cell division cycle 25 (CDC25) phosphatases in human acute myeloid leukemia - The possibility to target several kinases through inhibition of the various CDC25 isoforms. Molecules 2014;19:18414–47.
  • Contour-Galcera MO, Lavergne O, Brezak MC, et al. Synthesis of small molecule CDC25 phosphatases inhibitors. Bioorg Med Chem Lett 2004;14:5809–12.
  • Lavecchia A, Coluccia A, Di Giovanni C, Novellino E. Cdc25B phosphatase inhibitors in cancer therapy: latest developments, trends and medicinal chemistry perspective. Anticancer Agents Med Chem 2008;8:843–56.
  • Lavecchia A, Di Giovanni C, Novellino E. Inhibitors of Cdc25 phosphatases as anticancer agents: a patent review. Expert Opin Ther Patents 2010;20:405–25.
  • Lavecchia A, Di Giovanni C, Novellino E. CDC25 phosphatase inhibitors: an update. Mini Rev Med Chem 2012;12:62–73.
  • Lavecchia A, Cosconati S, Limongelli V, Novellino E. Modeling of Cdc25B dual specificity protein phosphatase inhibitors: docking of ligands and enzymatic inhibition mechanism. Chem Med Chem 2006;1:540–50.
  • He R, Zeng LF, He Y, et al. Small molecule tools for functional interrogation of protein tyrosine phosphatases. FEBS J 2013;280:731–50.
  • Huber-Villaume S, Revelant G, Sibille E, et al. 2-(Thienothiazolylimino)-1,3-thiazolidin-4-ones inhibit cell division cycle 25 A phosphatase. Bioorg Med Chem 2016;24:2920–8.
  • Bana E, Sibille E, Valente S, et al. A novel coumarin-quinone derivative SV37 inhibits CDC25 phosphatases, impairs proliferation, and induces cell death. Mol Carcinog 2015;54:229–41.
  • Albano F, Arcucci A, Granato G, et al. Markers of mitochondrial dysfunction during the diclofenac-induced apoptosis in melanoma cell lines. Biochimie 2013;95:934–45.
  • Gelzo M, Granato G, Albano F, et al. Evaluation of cytotoxic effects of 7-dehydrocholesterol on melanoma cells. Free Radic Biol Med 2014;70:129–40.
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248–54.
  • Arcucci A, Ruocco MR, Albano F, et al. Analysis of extracellular superoxide dismutase and Akt in ascending aortic aneurysm with tricuspid or bicuspid aortic valve. Eur J Histochem 2014;58:2383.
  • Arcucci A, Ruocco MR, Amatruda N, et al. Analysis of extracellular superoxide dismutase in fibroblasts from patients with systemic sclerosis. J Biol Regul Homeost Agents 2011;25:647–54.
  • Rudolph J. Cdc25 phosphatases: structure, specificity, and mechanism. Biochemistry 2007;46:3595–604.
  • DiPaola RS. To arrest or not to G(2)-M Cell-cycle arrest (Commentary re: Tyagi AK et al. Silibinin strongly synergizes human prostate carcinoma DU145 cells to doxorubicin-induced growth inhibition, G(2)-M arrest, and apoptosis Clin Cancer Res 2002;8:3512–9). Clin Cancer Res 2002;8:3311–4.
  • Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 2007;8:729–40.
  • Degterev A, Boyce M, Yuan J. A decade of caspases. Oncogene 2003;22:8543–67.
  • Wolter KG, Hsu YT, Smith CL, et al. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 1997;139:1281–92.
  • Morgan DO. Principles of CDK regulation. Nature 1995;374:131–4.
  • Yamaura M, Mitsushita J, Furuta S, et al. NADPH oxidase 4 contributes to transformation phenotype of melanoma cells by regulating G2-M cell cycle progression. Cancer Res 2009;69:2647–54.
  • Zacksenhaus E, Liu JC, Granieri L, et al. CDC25 as a common therapeutic target for triple-negative breast cancer - the challenges ahead . Mol Cell Oncol 2018;5:e1481814.
  • Ryan KM. p53 and autophagy in cancer: guardian of the genome meets guardian of the proteome. Eur J Cancer 2011;47:44–50.
  • Agrawal SN, Dhruv K, Meshram S. p53: the guardian of genome, apoptosis, and its role in carcinogenesis. Eur J Biomed Pharm Sci 2017;4:161–6.
  • Wang Z, Sun Y. Targeting p53 for novel anticancer therapy. Transl Oncol 2010;3:1–12.
  • Dalvai M, Mondesert O, Bourdon JC, et al. Cdc25B is negatively regulated by p53 through Sp1 and NF-Y transcription factors. Oncogene 2011;30:2282–8.
  • St Clair S, Giono L, Varmeh-Ziaie S, et al. DNA damage-induced downregulation of Cdc25C is mediated by p53 via two independent mechanisms: one involves direct binding to the cdc25C promoter. Mol Cell 2004;16:725–36.
  • Ihle MA, Fassunke J, Konig K, et al. Comparison of high resolution melting analysis, pyrosequencing, next generation sequencing and immunohistochemistry to conventional Sanger sequencing for the detection of p.V600E and non-p.V600E BRAF mutations. BMC Cancer 2014;14:13.
  • Colombino M, Capone M, Lissia A, et al. BRAF/NRAS mutation frequencies among primary tumors and metastases in patients with melanoma. J Clin Oncol 2012;30:2522–9.
  • Sullivan RJ, Flaherty KT. Resistance to BRAF-targeted therapy in melanoma. Eur J Cancer 2013;49:1297–304.
  • Ascierto PA, McArthur GA, Dréno B, et al. Cobimetinib combined with vemurafenib in advanced BRAF (V600)-mutant melanoma (coBRIM): updated efficacy results from a randomised, double-blind, phase 3 trial. Lancet Oncol 2016;17:1248–60.
  • Ruocco MR, Avagliano A, Granato G, et al. Metabolic flexibility in melanoma: a potential therapeutic target. Semin Cancer Biol 2019;59:187–207.
  • Acquaviva J, Smith DL, Jimenez JP, et al. Overcoming acquired BRAF inhibitor resistance in melanoma via targeted inhibition of Hsp90 with ganetespib. Mol Cancer Ther 2014;13:353–63.
  • Gopal YN, Deng W, Woodman SE, et al. Basal and treatment-induced activation of AKT mediates resistance to cell death by AZD6244 (ARRY-142886) in Braf-mutant human cutaneous melanoma cells. Cancer Res 2010;70:8736–47.
  • Perna D, Karreth FA, Rust AG, et al. BRAF inhibitor resistance mediated by the AKT pathway in an oncogenic BRAF mouse melanoma model. Proc Natl Acad Sci USA 2015;112:E536–45.
  • Holmes TR, Dindu S, Hansen LA. Aberrant localization of signaling proteins in skin cancer: implications for treatment. Mol Carcinog 2019;58:1631–9.