A small library of chalcones induce liver cancer cell death through Akt phosphorylation inhibition.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
16 07 2020
Historique:
received: 18 10 2017
accepted: 26 06 2020
entrez: 18 7 2020
pubmed: 18 7 2020
medline: 22 12 2020
Statut: epublish

Résumé

Hepatocellular carcinoma (HCC) ranks as the fifth most common and the second deadliest cancer worldwide. HCC is extremely resistant to the conventional chemotherapeutics. Hence, it is vital to develop new treatment options. Chalcones were previously shown to have anticancer activities in other cancer types. In this study, 11 chalcones along with quercetin, papaverin, catechin, Sorafenib and 5FU were analyzed for their bioactivities on 6 HCC cell lines and on dental pulp stem cells (DPSC) which differentiates into hepatocytes, and is used as a model for untransformed control cells. 3 of the chalcones (1, 9 and 11) were selected for further investigation due to their high cytotoxicity against liver cancer cells and compared to the other clinically established compounds. Chalcones did not show significant bioactivity ([Formula: see text]) on dental pulp stem cells. Cell cycle analysis revealed that these 3 chalcone-molecules induced SubG1/G1 arrest. Akt protein phosphorylation was inhibited by these molecules in PTEN deficient, drug resistant, mesenchymal like Mahlavu cells leading to the activation of p21 and the inhibition of NF[Formula: see text]B-p65 transcription factor. Hence the chalcones induced apoptotic cell death pathway through NF[Formula: see text]B-p65 inhibition. On the other hand, these molecules triggered p21 dependent activation of Rb protein and thereby inhibition of cell cycle and cell growth in liver cancer cells. Involvement of PI3K/Akt pathway hyperactivation was previously described in survival of liver cancer cells as carcinogenic event. Therefore, our results indicated that these chalcones can be considered as candidates for liver cancer therapeutics particularly when PI3K/Akt pathway involved in tumor development.

Identifiants

pubmed: 32678233
doi: 10.1038/s41598-020-68775-9
pii: 10.1038/s41598-020-68775-9
pmc: PMC7367369
doi:

Substances chimiques

Antineoplastic Agents 0
Chalcones 0
Proto-Oncogene Proteins c-akt EC 2.7.11.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

11814

Références

Ferlay, J. et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127, 2893–917 (2010). https://doi.org/10.1002/ijc.25516 .
Farazi, P. A. & DePinho, R. A. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat. Rev. Cancer 6, 674–87. https://doi.org/10.1038/nrc1934 (2006).
doi: 10.1038/nrc1934 pubmed: 16929323
Aravalli, R. N., Steer, C. J. & Cressman, E. N. K. Molecular mechanisms of hepatocellular carcinoma. Hepatology (Baltimore, Md.) 48, 2047–63. https://doi.org/10.1002/hep.22580 (2008).
doi: 10.1002/hep.22580
Wei, Z., Doria, C. & Liu, Y. Targeted therapies in the treatment of advanced hepatocellular carcinoma. Clin. Med. Insights Oncol. 7, 87–102. https://doi.org/10.4137/CMO.S7633 (2013).
doi: 10.4137/CMO.S7633 pubmed: 23761989 pmcid: 3667684
Adnane, L., Trail, P. A., Taylor, I. & Wilhelm, S. M. Sorafenib (BAY 43–9006, Nexavar), a dual-action inhibitor that targets RAF/MEK/ERK pathway in tumor cells and tyrosine kinases VEGFR/PDGFR in tumor vasculature. Methods Enzymol. 407, 597–612. https://doi.org/10.1016/S0076-6879(05)07047-3 (2006).
doi: 10.1016/S0076-6879(05)07047-3 pubmed: 16757355
Durmaz, I. et al. Liver cancer cells are sensitive to Lanatoside C induced cell death independent of their PTEN status. Phytomedicine 23, 42–51. https://doi.org/10.1016/j.phymed.2015.11.012 (2016).
doi: 10.1016/j.phymed.2015.11.012 pubmed: 26902406
Bhaskar, P. T. & Hay, N. The two TORCs and Akt. Dev. Cell 12, 487–502. https://doi.org/10.1016/j.devcel.2007.03.020 (2007).
doi: 10.1016/j.devcel.2007.03.020 pubmed: 17419990
Engelman, J. . A. . Targeting PI3K signalling in cancer: opportunities, challenges and limitations.. Nat. Rev. Cancer 9, 550–562. https://doi.org/10.1038/nrc2664 (2009).
doi: 10.1038/nrc2664 pubmed: 19629070
McCubrey, J. A. et al. Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR cascade inhibitors: how mutations can result in therapy resistance and how to overcome resistance. Oncotarget 3, 1068–111 (2012). https://doi.org/10.18632/oncotarget.659 .
Peyrou, M., Bourgoin, L. & Foti, M. PTEN in liver diseases and cancer. World J. Gastroenterol. 16, 4627–33 (2010).
doi: 10.3748/wjg.v16.i37.4627
Carnero, A., Blanco-Aparicio, C., Renner, O., Link, W. & Leal, J. F. M. The PTEN/PI3K/AKT signalling pathway in cancer, therapeutic implications. Curr. Cancer Drug Targets 8, 187–98 (2008).
doi: 10.2174/156800908784293659
Liu, P., Cheng, H., Roberts, T. M. & Zhao, J. J. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat. Rev. Drug Discov. 8, 627–44. https://doi.org/10.1038/nrd2926 (2009).
doi: 10.1038/nrd2926 pubmed: 19644473 pmcid: 3142564
Buontempo, F. et al. Inhibition of Akt signaling in hepatoma cells induces apoptotic cell death independent of Akt activation status. Investig. New Drugs 29, 1303–13. https://doi.org/10.1007/s10637-010-9486-3 (2011).
doi: 10.1007/s10637-010-9486-3 pubmed: 20628892
Ameta, K., Gupta, V. & Gaur, R. The Biochemistry of Chalcones: Chalcones: Synthesis and Biological Evaluation by Dr. K. L. Ameta (2011-03-24): Amazon.co.uk: Books (Lambert Academic Publishing, 2011).
Di Carlo, G., Mascolo, N., Izzo, A. A. & Capasso, F. Flavonoids: old and new aspects of a class of natural therapeutic drugs. Life Sci. 65, 337–53 (1999).
doi: 10.1016/S0024-3205(99)00120-4
Canela, M.-D. et al. Antivascular and antitumor properties of the tubulin-binding chalcone TUB091. Oncotarget (2016). https://doi.org/10.18632/oncotarget.9527 .
Martel-frachet, V. et al. IPP51 , a chalcone acting as a microtubule inhibitor with in vivo antitumor activity against bladder carcinoma. Oncotarget 6 (2015). https://doi.org/10.18632/oncotarget.4144 .
Amslinger, S. The tunable functionality of alpha, beta-unsaturated carbonyl compounds enables their differential application in biological systems. ChemMedChem 5, 351–6. https://doi.org/10.1002/cmdc.200900499 (2010).
doi: 10.1002/cmdc.200900499 pubmed: 20112330
Mahapatra, D. K., Bharti, S. K. & Asati, V. Anti-cancer chalcones: Structural and molecular target perspectives. Eur. J. Med. Chem. 98, 69–114. https://doi.org/10.1016/j.ejmech.2015.05.004 (2015).
doi: 10.1016/j.ejmech.2015.05.004 pubmed: 26005917
Borrelli, S. et al. New class of squalene-based releasable nanoassemblies of paclitaxel, podophyllotoxin, camptothecin and epothilone A. Eur. J. Med. Chem. 85, 179–90. https://doi.org/10.1016/j.ejmech.2014.07.035 (2014).
doi: 10.1016/j.ejmech.2014.07.035 pubmed: 25084144
Borrelli, S. et al. Self-assembled squalene-based fluorescent heteronanoparticles.. ChemPlusChem 80, 47–49. https://doi.org/10.1002/cplu.201402239 (2015).
doi: 10.1002/cplu.201402239
Calogero, F. et al. 9-Fluorenone-2-carboxylic acid as a scaffold for tubulin interacting compounds. ChemPlusChem 78, 663–669. https://doi.org/10.1002/cplu.201300036 (2013).
doi: 10.1002/cplu.201300036 pubmed: 31986630
Christodoulou, M. S. et al. Quinazolinecarboline alkaloid evodiamine as scaffold for targeting topoisomerase I and sirtuins. Bioorg. Med. Chem. 21, 6920–8. https://doi.org/10.1016/j.bmc.2013.09.030 (2013).
doi: 10.1016/j.bmc.2013.09.030
Christodoulou, M. S. et al. Synthesis and biological evaluation of imidazolo[2,1-b]benzothiazole derivatives, as potential p53 inhibitors. Bioorg. Med. Chem. 19, 1649–57. https://doi.org/10.1016/j.bmc.2011.01.039 (2011).
doi: 10.1016/j.bmc.2011.01.039
Christodoulou, M. S. et al. Camptothecin-7-yl-methanthiole: semisynthesis and biological evaluation. ChemMedChem 7, 2134–43. https://doi.org/10.1002/cmdc.201200322 (2012).
doi: 10.1002/cmdc.201200322 pubmed: 23086693
Christodoulou, M. S. et al. 4-(1,2-diarylbut-1-en-1-yl)isobutyranilide derivatives as inhibitors of topoisomerase II. Eur. J. Med. Chem. https://doi.org/10.1016/j.ejmech.2016.03.090 (2016).
Christodoulou, M. S., Liekens, S., Kasiotis, K. M. & Haroutounian, S. A. Novel pyrazole derivatives: synthesis and evaluation of anti-angiogenic activity. Bioorg. Med. Chem. 18, 4338–50. https://doi.org/10.1016/j.bmc.2010.04.076 (2010).
doi: 10.1016/j.bmc.2010.04.076
Christodoulou, M. S. et al. Boehmeriasin A as new lead compound for the inhibition of topoisomerases and SIRT2. Eur. J. Med. Chem. 92, 766–75. https://doi.org/10.1016/j.ejmech.2015.01.038 (2015).
doi: 10.1016/j.ejmech.2015.01.038 pubmed: 25626146
Christodoulou, M. S. et al. Synthesis and biological evaluation of novel tamoxifen analogues. Bioorg. Med. Chem. 21, 4120–31. https://doi.org/10.1016/j.bmc.2013.05.012 (2013).
doi: 10.1016/j.bmc.2013.05.012
Christodoulou, M. S. et al. Click reaction as a tool to combine pharmacophores: the case of vismodegib. ChemPlusChem 80, 938–943. https://doi.org/10.1002/cplu.201402435 (2015).
doi: 10.1002/cplu.201402435 pubmed: 31973263
Fumagalli, G. et al. Cyclopamine-paclitaxel-containing nanoparticles: internalization in cells detected by confocal and super-resolution microscopy. ChemPlusChem 80, 1380–1383. https://doi.org/10.1002/cplu.201500156 (2015).
doi: 10.1002/cplu.201500156 pubmed: 31973361
Marucci, C. et al. Synthesis of pironetin-dumetorine hybrids as tubulin binders. Eur. J. Org. Chem. 2016, 2029–2036. https://doi.org/10.1002/ejoc.201600130 (2016).
doi: 10.1002/ejoc.201600130
Ikeda, et al. Multipotent cells from the human third molar: feasibility of cell-based therapy for liver disease. Differentiation 76, 495–505. https://doi.org/10.1111/j.1432-0436.2007.00245.x (2008).
doi: 10.1111/j.1432-0436.2007.00245.x pubmed: 18093227
Ohkoshi, S., Hara, H., Hirono, H., Watanabe, K. & Hasegawa, K. Regenerative medicine using dental pulp stem cells for liver diseases. World J. Gastrointest. Pharmacol. Ther. 8, 1–6. https://doi.org/10.4292/wjgpt.v8.i1.1 (2017).
doi: 10.4292/wjgpt.v8.i1.1 pubmed: 28217369 pmcid: 5292602
Kim, D.-C. et al. Induction of growth inhibition and apoptosis in human uterine leiomyoma cells by isoliquiritigenin. Reprod. Sci. 15, 552–8. https://doi.org/10.1177/1933719107312681 (2008).
doi: 10.1177/1933719107312681
Viatour, P., Merville, M.-P., Bours, V. & Chariot, A. Phosphorylation of NF-[Formula: see text] and [Formula: see text] proteins: implications in cancer and inflammation. Trends Biochem. Sci. 30, 43–52. https://doi.org/10.1016/j.tibs.2004.11.009 (2005).
doi: 10.1016/j.tibs.2004.11.009 pubmed: 15653325
He, W. et al. Anticancer cardamonin analogs suppress the activation of NF-kappaB pathway in lung cancer cells. Mol. Cell. Biochem. 389, 25–33. https://doi.org/10.1007/s11010-013-1923-0 (2014).
doi: 10.1007/s11010-013-1923-0 pubmed: 24390014
Dan, H. C. et al. Akt-dependent regulation of NF-κB is controlled by mTOR and Raptor in association with IKK. Genes Dev. 22, 1490–500. https://doi.org/10.1101/gad.1662308 (2008).
doi: 10.1101/gad.1662308
Lu, S., Ren, C., Liu, Y. & Epner, D. E. PI3K-Akt signaling is involved in the regulation of p21(WAF/CIP) expression and androgen-independent growth in prostate cancer cells. Int. J. Oncol. 28, 245–51 (2006).
pubmed: 16328002
Tsatsanis, C. & Spandidos, D. A. The role of oncogenic kinases in human cancer (review). Int. J. Mol. Med. 5, 583–90 (2000).
pubmed: 10812005
Rakoff-Nahoum, S. Why cancer and inflammation?. Yale J. Biol. Med. 79, 123–30 (2006).
pubmed: 17940622
Rueden, C. T. et al. Imagej 2: Imagej for the next generation of scientific image data. BMC Bioinform. 18, 529. https://doi.org/10.1186/s12859-017-1934-z (2017).
doi: 10.1186/s12859-017-1934-z pubmed: 29187165 pmcid: 5708080

Auteurs

Irem Durmaz Sahin (ID)

School of Medicine, Koc University, 34450, Istanbul, Turkey. irsahin@ku.edu.tr.

Michael S Christodoulou (MS)

DISFARM, Sezione di Chimica Generale e Organica "A. Marchesini" Universitádegli Studi di Milano, via Venezian 21, 20133, Milano, Italy.

Ece Akhan Guzelcan (EA)

CanSyL, Graduate School of Informatics, Middle East Technical University, 06800, Ankara, Turkey.

Altay Koyas (A)

CanSyL, Graduate School of Informatics, Middle East Technical University, 06800, Ankara, Turkey.

Cigdem Karaca (C)

Faculty of Dentistry, Department of Oral and Maxillofacial Surgery, Hacettepe University, 06230, Ankara, Turkey.

Daniele Passarella (D)

Department of Chemistry, Universitá degli Studi di Milano, Via Golgi 19, 20133, Milano, Italy.

Rengul Cetin-Atalay (R)

CanSyL, Graduate School of Informatics, Middle East Technical University, 06800, Ankara, Turkey.

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