The Novel Dual Topoisomerase Inhibitor P8-D6 Shows Anti-myeloma Activity
Journal
Molecular cancer therapeutics
ISSN: 1538-8514
Titre abrégé: Mol Cancer Ther
Pays: United States
ID NLM: 101132535
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
received:
05
02
2021
revised:
04
10
2021
accepted:
28
10
2021
pubmed:
3
11
2021
medline:
31
3
2022
entrez:
2
11
2021
Statut:
ppublish
Résumé
P8-D6 is a novel dual inhibitor of human topoisomerase I (TOP1) and II (TOP2) with broad pro-apoptotic antitumor activity. NCI-60 screening revealed markedly improved cytotoxicity of P8-D6 against solid and leukemia cell lines compared with other single and dual topoisomerase inhibitors, for example, irinotecan, doxorubicin, or pyrazoloacridine. In this study, we investigated the capacity of P8-D6 to inhibit myeloma cell growth
Identifiants
pubmed: 34725192
pii: 1535-7163.MCT-21-0119
doi: 10.1158/1535-7163.MCT-21-0119
doi:
Substances chimiques
1-(5,8-dihydroxy-1,4-dioxo-1,4-dihydronaphthalen-2-yl)-4-methylpent-3-en-1-yl (E)-2-(4-(3-oxo-3-(3-(trifluoromethoxy)phenyl)prop-1-en-1-yl)phenoxy)acetate
0
Naphthalenes
0
Topoisomerase II Inhibitors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
70-78Informations de copyright
©2021 American Association for Cancer Research.
Références
Pommier Y, Sun Y, Huang S-y, Nitiss JL. Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat Rev Mol Cell Biol. 2016;17:703–21.
Pommier Y. Drugging topoisomerases: lessons and challenges. ACS Chem Biol. 2013;8:82–95.
Perrin D, van Hille B, Barret JM, Kruczynski A, Etievant C, Imbert T, et al. 11782, a novel epipodophylloid non-intercalating dual catalytic inhibitor of topoisomerases I and II with an original mechanism of action. Biochem Pharmacol. 2000;59:807–19.
Adjei AA, Charron M, Rowinsky EK, Svingen PA, Miller J, Reid JM, et al. Effect of pyrazoloacridine (NSC 366140) on DNA topoisomerases I and II. Clin Cancer Res. 1998;4:683–91.
Poddevin B, Riou JF, Lavelle F, Pommier Y. Dual topoisomerase I and II inhibition by intoplicine (RP-60475), a new antitumor agent in early clinical trials. Mol Pharmacol. 1993;44:767–74.
Mistry P, Stewart AJ, Dangerfield W, Baker M, Liddle C, Bootle D, et al. In vitro and in vivo characterization of XR11576, a novel, orally active, dual inhibitor of topoisomerase I and II. Anticancer Drugs. 2002;13:15–28.
Rao VA, Agama K, Holbeck S, Pommier Y. Batracylin (NSC 320846), a dual inhibitor of DNA topoisomerases I and II induces histone gamma-H2AX as a biomarker of DNA damage. Cancer Res. 2007;67:9971–9.
Marzi L, Sun Y, Huang SN, James A, Difilippantonio S, Pommier Y. The indenoisoquinoline LMP517: a novel antitumor agent targeting both TOP1 and TOP2. Mol Cancer Ther. 2020;19:1589–97.
Brangi M, Litman T, Ciotti M, Nishiyama K, Kohlhagen G, Takimoto C, et al. Camptothecin resistance: role of the ATP-binding cassette (ABC), mitoxantrone-resistance half-transporter (MXR), and potential for glucuronidation in MXR-expressing cells. Cancer Res. 1999;59:5938–46.
Lefevre D, Riou JF, Ahomadegbe JC, Zhou DY, Benard J, Riou G. Study of molecular markers of resistance to m-AMSA in a human breast cancer cell line. Decrease of topoisomerase II and increase of both topoisomerase I and acidic glutathione S transferase. Biochem Pharmacol. 1991;41:1967–79.
Ramaswamy B, Mrozek E, Kuebler JP, Bekaii-Saab T, Kraut EH. Phase II trial of pyrazoloacridine (NSC#366140) in patients with metastatic breast cancer. Invest New Drugs. 2011;29:347–51.
Abigerges D, Armand JP, Chabot GG, Bruno R, Bissery MC, Bayssas M, et al. Phase I and pharmacology study of intoplicine (RP 60475; NSC 645008), novel topoisomerase I and II inhibitor, in cancer patients. Anticancer Drugs. 1996;7:166–74.
de Jonge MJ, Kaye S, Verweij J, Brock C, Reade S, Scurr M, et al. Phase I and pharmacokinetic study of XR11576, an oral topoisomerase I and II inhibitor, administered on days 1–5 of a 3-weekly cycle in patients with advanced solid tumours. Br J Cancer. 2004;91:1459–65.
Baglini E, Salerno S, Barresi E, Robello M, Da Settimo F, Taliani S, et al. Multiple topoisomerase I (TopoI), topoisomerase II (TopoII) and tyrosyl-DNA phosphodiesterase (TDP) inhibitors in the development of anticancer drugs. Eur J Pharm Sci. 2021;156:105594.
Shitara K, Bang YJ, Iwasa S, Sugimoto N, Ryu MH, Sakai D, et al. Trastuzumab deruxtecan in previously treated HER2-positive gastric cancer. N Engl J Med. 2020;382:2419–30.
Syed YY. Sacituzumab govitecan: first approval. Drugs. 2020;80:1019–25.
Meier C, Steinhauer TN, Koczian F, Plitzko B, Jarolim K, Girreser U, et al. A dual topoisomerase inhibitor of intense pro-apoptotic and antileukemic nature for cancer treatment. ChemMedChem. 2017;12:347–52.
Aichinger G, Lichtenberger FB, Steinhauer TN, Florkemeier I, Del Favero G, Clement B, et al. The aza-analogous benzo[c]phenanthridine P8-D6 acts as a dual topoisomerase I and II poison, thus exhibiting potent genotoxic properties. Molecules. 2020;25:1524.
Cowan AJ, Allen C, Barac A, et al. Global burden of multiple myeloma: a systematic analysis for the global burden of disease study 2016. JAMA Oncol. 2018;4:1221–7.
Kawano Y, Moschetta M, Manier S, Glavey S, Gorgun GT, Roccaro AM, et al. Targeting the bone marrow microenvironment in multiple myeloma. Immunol Rev. 2015;263:160–72.
Kristinsson SY, Anderson WF, Landgren O. Improved long-term survival in multiple myeloma up to the age of 80 years. Leukemia. 2014;28:1346–8.
Takeshita T, Wu W, Koike A, Fukuda M, Ohta T. Perturbation of DNA repair pathways by proteasome inhibitors corresponds to enhanced chemosensitivity of cells to DNA damage-inducing agents. Cancer Chemother Pharmacol. 2009;64:1039–46.
Guerrant W, Patil V, Canzoneri JC, Oyelere AK. Dual targeting of histone deacetylase and topoisomerase II with novel bifunctional inhibitors. J Med Chem. 2012;55:1465–77.
Beksac M, Balli S, Akcora Yildiz D. Drug targeting of genomic instability in multiple myeloma. Front Genet. 2020;11:228.
Peipp M, Lammerts van Bueren JJ, Schneider-Merck T, Bleeker WW, Dechant M, Beyer T, et al. Antibody fucosylation differentially impacts cytotoxicity mediated by NK and PMN effector cells. Blood. 2008;112:2390–9.
Burger R, Guenther A, Bakker F, Schmalzing M, Bernand S, Baum W, et al. Gp130 and ras mediated signaling in human plasma cell line INA-6: a cytokine-regulated tumor model for plasmacytoma. Hematol J. 2001;2:42–53.
Meister S, Schubert U, Neubert K, Herrmann K, Burger R, Gramatzki M, et al. Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Res. 2007;67:1783–92.
Klausz K, Cieker M, Kellner C, Rosner T, Otte A, Krohn S, et al. Fc-engineering significantly improves the recruitment of immune effector cells by anti-ICAM-1 antibody MSH-TP15 for myeloma therapy. Haematologica. 2021;106:1857–66.
Hu J, Wen PY, Abrey LE, Fadul CE, Drappatz J, Salem N, et al. A phase II trial of oral gimatecan for recurrent glioblastoma. J Neurooncol. 2013;111:347–53.
LoRusso P, Wozniak AJ, Polin L, Capps D, Leopold WR, Werbel LM, et al. Antitumor efficacy of PD115934 (NSC 366140) against solid tumors of mice. Cancer Res. 1990;50:4900–5.
Bissery MC, Nguyen CH, Bisagni E, Vrignaud P, Lavelle F. Antitumor activity of intoplicine (RP 60475, NSC 645008), a new benzo-pyrido-indole: evaluation against solid tumors and leukemias in mice. Invest New Drugs. 1993;11:263–77.
Von Hoff DD, Burris HA 3rd, Eckardt J, Rothenberg M, Fields SM, Chen SF, et al. Preclinical and phase I trials of topoisomerase I inhibitors. Cancer Chemother Pharmacol. 1994;34:S41–5.
Yano H, Kayukawa S, Iida S, Nakagawa C, Oguri T, Sanda T, et al. Overexpression of carboxylesterase-2 results in enhanced efficacy of topoisomerase I inhibitor, irinotecan (CPT-11), for multiple myeloma. Cancer Sci. 2008;99:2309–14.
Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev. 2001;46:3–26.
Zebothsen I, Girreser U, Clement B. Metabolism of cytostatically active 6-aminobenzo[c]phenanthridines by human and porcine hepatic microsomes and recombinant cytochrome P450 enzymes. Xenobiotica. 2006;36:581–95.
Ali AS, Gronberg M, Langer SW, Ladekarl M, Hjortland GO, Vestermark LW, et al. Intravenous versus oral etoposide: efficacy and correlation to clinical outcome in patients with high-grade metastatic gastroenteropancreatic neuroendocrine neoplasms (WHO G3). Med Oncol. 2018;35:47.
Devriese LA, Witteveen PE, Mergui-Roelvink M, Smith DA, Lewis LD, Mendelson DS, et al. Pharmacodynamics and pharmacokinetics of oral topotecan in patients with advanced solid tumours and impaired renal function. Br J Clin Pharmacol. 2015;80:253–66.
Bastasch M, Panella TJ, Kretzschmer SL, Graham D, Mayo M, Williamson S. Phase II trial of pyrazoloacridine in advanced non-small cell carcinoma of the lung–a kansas cancer institute and thompson cancer survival center study. Invest New Drugs. 2002;20:339–42.
Delord J-P, Bennouna J, Dieras V, Campone M, Lefresne F, Aslanis V, et al. First-in-man study of tafluposide, a novel inhibitor of topoisomerase I and II. Mol Cancer Ther. 2007;6:A138.
van Gijn R, ten Bokkel Huinink WW, Rodenhuis S, Vermorken JB, van Tellingen O, Rosing H, et al. Topoisomerase I/II inhibitor intoplicine administered as a 24 h infusion: phase I and pharmacologic study. Anticancer Drugs. 1999;10:17–23.
Barret JM, Kruczynski A, Etievant C, Hill BT. Synergistic effects of F 11782, a novel dual inhibitor of topoisomerases I and II, in combination with other anticancer agents. Cancer Chemother Pharmacol. 2002;49:479–86.
Lin CP, Ban Y, Lyu YL, Liu LF. Proteasome-dependent processing of topoisomerase I-DNA adducts into DNA double strand breaks at arrested replication forks. J Biol Chem. 2009;284:28084–92.
Cusack JC, Liu R, Houston M, Abendroth K, Elliott PJ, Adams J, et al. Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-κB inhibition. Cancer Res. 2001;61:3535–40.
Kummar S, Chen A, Ji J, Zhang Y, Reid JM, Ames M, et al. Phase I study of PARP inhibitor ABT-888 in combination with topotecan in adults with refractory solid tumors and lymphomas. Cancer Res. 2011;71:5626–34.
LoRusso PM, Li J, Burger A, Heilbrun LK, Sausville EA, Boerner SA, et al. Phase I safety, pharmacokinetic, and pharmacodynamic study of the Poly(ADP-ribose) polymerase (PARP) inhibitor veliparib (ABT-888) in combination with irinotecan in patients with advanced solid tumors. Clin Cancer Res. 2016;22:3227–37.
Murai J, Zhang Y, Morris J, Ji J, Takeda S, Doroshow JH, et al. Rationale for Poly(ADP-ribose) polymerase (PARP) inhibitors in combination therapy with camptothecins or temozolomide based on PARP trapping versus catalytic inhibition. J Pharmacol Exp Ther. 2014;349:408–16.
Bowman KJ, Newell DR, Calvert AH, Curtin NJ. Differential effects of the poly (ADP-ribose) polymerase (PARP) inhibitor NU1025 on topoisomerase I and II inhibitor cytotoxicity in L1210 cells in vitro. Br J Cancer. 2001;84:106–12.
Voorhees PM, Gasparetto C, Moore DT, Winans D, Orlowski RZ, Hurd DD. Final results of a phase 1 study of vorinostat, pegylated liposomal doxorubicin, and bortezomib in relapsed or refractory multiple myeloma. Clin Lymphoma Myeloma Leuk. 2017;17:424–32.
Aggarwal C, Cohen RB, Yu E, Hwang W-T, Bauml JM, Alley E, et al. Etirinotecan pegol (NKTR-102) in third-line treatment of patients with metastatic or recurrent non–small-cell lung cancer: results of a phase II study. Clin Lung Cancer. 2018;19:157–62.
Perez EA, Awada A, O'Shaughnessy J, Rugo HS, Twelves C, Im S-A, et al. Etirinotecan pegol (NKTR-102) versus treatment of physician's choice in women with advanced breast cancer previously treated with an anthracycline, a taxane, and capecitabine (BEACON): a randomised, open-label, multicentre, phase 3 trial. Lancet Oncol. 2015;16:1556–68.
Lenz H-J, Philip P, Saunders M, Kolevska T, Mukherjee K, Samuel L, et al. Randomized study of etirinotecan pegol versus irinotecan as second-line treatment for metastatic colorectal cancer. Cancer Chemother Pharmacol. 2017;80:1161–9.
Rustin G, Vergote I, Micha JP, Duska LR, Reed N, Bendell J, et al. A multicenter, open-label, expanded phase 2 study to evaluate the safety and efficacy of etirinotecan pegol, a polymer conjugate of irinotecan, in women with recurrent platinum-resistant or refractory ovarian cancer. Gynecol Oncol. 2017;147:276–82.
Nagpal S, Recht CK, Bertrand S, Thomas RP, Ajlan A, Pena J, et al. Phase II pilot study of single-agent etirinotecan pegol (NKTR-102) in bevacizumab-resistant high grade glioma. J Neurooncol. 2015;123:277–82.
Ri M, Suzuki K, Iida S, Hatake K, Chou T, Taniwaki M, et al. A phase I/II study for dose-finding, and to investigate the safety, pharmacokinetics and preliminary efficacy of NK012, an SN-38-incorporating macromolecular polymeric micelle, in patients with multiple myeloma. Intern Med. 2018;57:939–46.