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Original Research

In vitro to Clinical Translation of Combinatorial Effects of Doxorubicin and Abemaciclib in Rb-Positive Triple Negative Breast Cancer: A Systems-Based Pharmacokinetic/Pharmacodynamic Modeling Approach

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Pages 87-105 | Published online: 18 Feb 2021

References

  • PodoF, BuydensLM, DeganiH, et al. Triple-negative breast cancer: present challenges and new perspectives. Mol Oncol. 2010;4(3):209–229.20537966
  • SiegelRL, MillerKD, JemalA. Cancer statistics, 2018.. CA Cancer J Clin. 2018;68(1):7–30. doi:10.3322/caac.2144229313949
  • BenderRJ, Mac GabhannF, SchönbachC. Expression of VEGF and semaphorin genes define subgroups of triple negative breast cancer. PLoS One. 2013;8(5):e61788. doi:10.1371/journal.pone.006178823667446
  • FleisherB, ClarkeC, Ait-OudhiaS. Current advances in biomarkers for targeted therapy in triple-negative breast cancer.. Breast Cancer (Dove Medical Press). 2016;8:183–197. doi:10.2147/BCTT.S11465927785100
  • RugoHS, OlopadeOI, DeMicheleA, YauC. Adaptive randomization of veliparib–carboplatin treatment in breast cancer. N Engl J Med. 2016;375(1):23–34. doi:10.1056/NEJMoa151374927406347
  • SikovWM, BerryDA, PerouCM, et al. Impact of the Addition of carboplatin and/or bevacizumab to neoadjuvant once-per-week paclitaxel followed by dose-dense doxorubicin and cyclophosphamide on pathologic complete response rates in stage ii to iii triple-negative breast cancer: CALGB 40603 (alliance). J Clin Oncol. 2014.
  • LiedtkeC, MazouniC, HessKR, et al. Response to Neoadjuvant Therapy and Long-Term Survival in Patients With Triple-Negative Breast Cancer. J Clin Oncol. 2008;26(8):1275–1281.18250347
  • KhouriMG, DouglasPS, MackeyJR, et al. Cancer therapy-induced cardiac toxicity in early breast cancer: addressing the unresolved issues. Circulation. 2012;126(23):2749–2763.23212997
  • GabizonA, ShmeedaH, BarenholzY. Pharmacokinetics of pegylated liposomal Doxorubicin: review of animal and human studies. Clin Pharmacokinet. 2003;42(5):419–436.12739982
  • CharroisGJR, AllenTM. Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer. Biochimica Et Biophysica Acta. 2004;1663(1–2):167–177. doi:10.1016/j.bbamem.2004.03.00615157619
  • O’BrienME, WiglerN, InbarM, et al. Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl(CAELYX™/Doxil®) versus conventional doxorubicin for first-line treatment of metastatic breast cancer. Ann Oncol. 2004;15(3):440–449. doi:10.1093/annonc/mdh09714998846
  • TacarO, SriamornsakP, DassCR. Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems. J Pharm Pharmacol. 2013;65(2):157–170. doi:10.1111/j.2042-7158.2012.01567.x23278683
  • RobinsonTJW, LiuJC, VizeacoumarF, et al. RB1 status in triple negative breast cancer cells dictates response to radiation treatment and selective therapeutic drugs. PLoS One. 2013;8(11):e78641. doi:10.1371/journal.pone.007864124265703
  • ChristowitzC, DavisT, IsaacsA, van NiekerkG, HattinghS, EngelbrechtA-M. Mechanisms of doxorubicin-induced drug resistance and drug resistant tumour growth in a murine breast tumour model. BMC Cancer. 2019;19(1):757. doi:10.1186/s12885-019-5939-z31370818
  • LangeCA, YeeD. Killing the second messenger: targeting loss of cell cycle control in endocrine-resistant breast cancer. Endocr Relat Cancer. 2011;18(4):C19–24. doi:10.1530/ERC-11-011221613412
  • LeeE-R, KimJ-Y, KangY-J, et al. Interplay between PI3K/Akt and MAPK signaling pathways in DNA-damaging drug-induced apoptosis. Biochimica Et Biophysica Acta. 2006;1763(9):958–968. doi:10.1016/j.bbamcr.2006.06.00616905201
  • O’BrienN, ConklinD, BeckmannR, et al. Preclinical Activity of Abemaciclib Alone or in Combination with Antimitotic and Targeted Therapies in Breast Cancer. Mol Cancer Ther. 2018;17(5):897–907. doi:10.1158/1535-7163.MCT-17-029029483214
  • McClendonAK, DeanJL, RivadeneiraDB, et al. CDK4/6 inhibition antagonizes the cytotoxic response to anthracycline therapy. Cell Cycle. 2012;11(14):2747–2755. doi:10.4161/cc.2112722751436
  • LiuC-Y, LauK-Y, Hsu-C-C, et al. Combination of palbociclib with enzalutamide shows in vitro activity in RB proficient and androgen receptor positive triple negative breast cancer cells. PLoS One. 2017;12(12):e0189007. doi:10.1371/journal.pone.018900729261702
  • RobertsPJ, BisiJE, StrumJC, et al. Multiple Roles of Cyclin-Dependent Kinase 4/6 Inhibitors in Cancer Therapy. JNCI. 2012;104(6):476–487. doi:10.1093/jnci/djs00222302033
  • MurphyCG, DicklerMN. The Role of CDK4/6 Inhibition in Breast Cancer. The Oncologist. 2015;20(5):483–490. doi:10.1634/theoncologist.2014-044325876993
  • TateSC, CaiS, AjamieRT, et al. Semi-mechanistic pharmacokinetic/pharmacodynamic modeling of the antitumor activity of LY2835219, a new cyclin-dependent kinase 4/6 inhibitor, in mice bearing human tumor xenografts. Clin Cancer Res. 2014;20(14):3763–3774. doi:10.1158/1078-0432.CCR-13-284624850847
  • YiSY, AhnJS, UhmJE, et al. Favorable response to doxorubicin combination chemotherapy does not yield good clinical outcome in patients with metastatic breast cancer with triple-negative phenotype. BMC Cancer. 2010;10(1):527. doi:10.1186/1471-2407-10-52720920367
  • ZhangN, FuJ-N, ChouT-C. Synergistic combination of microtubule targeting anticancer fludelone with cytoprotective panaxytriol derived from panax ginseng against MX-1 cells in vitro: experimental design and data analysis using the combination index method. Am J Cancer Res. 2016;6(1):97–104.27073727
  • ChouT-C. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 2010;70(2):440–446. doi:10.1158/0008-5472.CAN-09-194720068163
  • InaoT, KotaniH, IidaY, et al. Different sensitivities of senescent breast cancer cells to immune cell-mediated cytotoxicity. Cancer Sci. 2019;110(9):2690–2699. doi:10.1111/cas.1411631250942
  • HouJ-G, JeonB-M, YunY-J, CuiC-H, KimS-C. Ginsenoside Rh2 Ameliorates Doxorubicin-Induced Senescence Bystander Effect in Breast Carcinoma Cell MDA-MB-231 and Normal Epithelial Cell MCF-10A. Int J Mol Sci. 2019;20(5):1244. doi:10.3390/ijms20051244
  • JacksonJG, Pereira-SmithOM. Primary and compensatory roles for RB family members at cell cycle gene promoters that are deacetylated and downregulated in doxorubicin-induced senescence of breast cancer cells. Mol Cell Biol. 2006;26(7):2501–2510. doi:10.1128/MCB.26.7.2501-2510.200616537896
  • PatnaikA, RosenLS, TolaneySM, et al. Efficacy and Safety of Abemaciclib, an Inhibitor of CDK4 and CDK6, for Patients with Breast Cancer, Non–Small Cell Lung Cancer, and Other Solid Tumors. Cancer Discov. 2016;6(7):740–753. doi:10.1158/2159-8290.CD-16-009527217383
  • Verzenio© (abemaciclib) application number 208716Orig1s000; 2020[Multi-Discipline Review] Available from:https://www.accessdata.fda.gov/drugsatfda_docs/nda/2017/208716Orig1s000MultidisciplineR.pdf.
  • GreeneRF, CollinsJM, JenkinsJF, SpeyerJL, MyersCE. Plasma pharmacokinetics of adriamycin and adriamycinol: implications for the design of in vitro experiments and treatment protocols.. Cancer Res. 1983;43(7):3417–3421.6850648
  • LiangS, BrundageRC, JacobsonPA, BlaesA, KirsteinMN. Pharmacokinetic–pharmacodynamic modelling of acute N-terminal pro B-type natriuretic peptide after doxorubicin infusion in breast cancer. Br J Clin Pharmacol. 2016;82(3):773–783. doi:10.1111/bcp.1298927128712
  • GabizonA, CataneR, UzielyB, et al. Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes.. Cancer Res. 1994;54(4):987–992.8313389
  • Janssen. DOXIL (Doxorubicin HCl Liposome Injection) for Intravenous Infusion; 2013.
  • UzielyB. Doxorubicin Hydrochloride for Injection, USP. Kalamazoo, MI: Edited by Company PU; 2003.
  • KayK, DolcyK, BiesR, ShahDK. Estimation of Solid Tumor Doubling Times from Progression-Free Survival Plots Using a Novel Statistical Approach. AAPS J. 2019;21(2):27. doi:10.1208/s12248-019-0302-530737615
  • GolshanM, CirrincioneCT, SikovWM, et al. Impact of Neoadjuvant Chemotherapy in Stage II–III Triple Negative Breast Cancer on Eligibility for Breast-conserving Surgery and Breast Conservation Rates. Ann surg. 2004;1663(1–2):434–439. doi:10.1093/jnci/92.3.205
  • Organization WH. WHO Handbook for Reporting Results of Cancer Treatment. Geneva: World Health Organization; 1979.
  • AsgharUS, BarrAR, CuttsR, et al. Single-Cell Dynamics Determines Response to CDK4/6 Inhibition in Triple-Negative Breast Cancer. Clin Cancer Res. 2017;23(18):5561–5572. doi:10.1158/1078-0432.CCR-17-036928606920
  • EissaIH, MetwalyAM, BelalA, et al. Discovery and antiproliferative evaluation of new quinoxalines as potential DNA intercalators and topoisomerase II inhibitors. Arch Pharm. 2019;352(11):e1900123.
  • MathWorks®. Simbiology® User’s Guide (R2020a); 2020.
  • Perez-BlancoJS, Santos-BuelgaD, Hernández-RivasJM, MartínA, GarcíaMJ. Population pharmacokinetics of doxorubicin and doxorubicinol in patients diagnosed with non-Hodgkin’s lymphoma. Br J Clin Pharmacol. 2016;82(6):1517–1527. doi:10.1111/bcp.1307027447545
  • HsuL-F. Investigation of the Discriminatory Ability of Pharmacokinetic Metrics for the Bioequivalence Assessment of PEGylated Liposomal Doxorubicin. Pharm Res. 2018;35(5):106. doi:10.1007/s11095-018-2387-429564719
  • BhowmikS, BhowmickS, MaitiK, et al. Two multicenter Phase I randomized trials to compare the bioequivalence and safety of a generic doxorubicin hydrochloride liposome injection with Doxil® or Caelyx® in advanced ovarian cancer.. Cancer Chemother Pharmacol. 2018;82(3):521–532. doi:10.1007/s00280-018-3643-329995186
  • TateSC, SykesAK, KulanthaivelP, ChanEM, TurnerPK, CronierDM. A Population Pharmacokinetic and Pharmacodynamic Analysis of Abemaciclib in a Phase I Clinical Trial in Cancer Patients. Clin Pharmacokinet. 2018;57(3):335–344. doi:10.1007/s40262-017-0559-828540640
  • KnudsenES, HutchesonJ, VailP, WitkiewiczAK. Biological specificity of CDK4/6 inhibitors: dose response relationship, in vivo signaling, and composite response signature. Oncotarget. 2017;8(27):43678–43691. doi:10.18632/oncotarget.1843528620137
  • NeophytouC, BoutsikosP, PapageorgisP. Molecular Mechanisms and Emerging Therapeutic Targets of Triple-Negative Breast Cancer Metastasis. Front Oncol. 2018;8:31. doi:10.3389/fonc.2018.0003129520340
  • KnudsenES, WangJYJ. Targeting the RB-pathway in Cancer Therapy. Clin Cancer Res. 2010;16(4):1094. doi:10.1158/1078-0432.CCR-09-078720145169
  • MartinJM, GoldsteinLJ. Profile of abemaciclib and its potential in the treatment of breast cancer. OncoTargets Therapy. 2018;11:5253–5259. doi:10.2147/OTT.S14924530214230
  • DeanJL, ThangavelC, McClendonAK, ReedCA, KnudsenES. Therapeutic CDK4/6 inhibition in breast cancer: key mechanisms of response and failure. Oncogene. 2010;29(28):4018–4032. doi:10.1038/onc.2010.15420473330
  • LlanosS, MegiasD, Blanco-AparicioC, et al. Lysosomal trapping of palbociclib and its functional implications. Oncogene. 2019;38(20):3886–3902. doi:10.1038/s41388-019-0695-830692638
  • CostaRLB, GradisharWJ. Triple-Negative Breast Cancer: current Practice and Future Directions. J Oncol Pract. 2017;13(5):301–303. doi:10.1200/JOP.2017.02333328489982
  • GolshanM, CirrincioneCT, SikovWM, et al. Impact of neoadjuvant chemotherapy in stage II-III triple negative breast cancer on eligibility for breast-conserving surgery and breast conservation rates: surgical results from CALGB 40603 (Alliance). Ann Surg. 2015;262(3):434–439.26222764
  • AllisonSE, ChenY, PetrovicN, et al. Activation of ALDH1A1 in MDA-MB-468 breast cancer cells that over-express CYP2J2 protects against paclitaxel-dependent cell death mediated by reactive oxygen species. Biochem Pharmacol. 2017;143:79–89.28756208
  • ZhangY, YangND, ZhouF, et al. Epigallocatechin-3-gallate induces non-apoptotic cell death in human cancer cells via ROS-mediated lysosomal membrane permeabilization. PLoS One. 2012;7(10):e46749.23056433
  • VurusanerB, PoliG, BasagaH. Tumor suppressor genes and ROS: complex networks of interactions. Free Radic Biol Med. 2012;52(1):7–18.22019631
  • HanahanD, WeinbergRA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674.21376230
  • GubernA, JoaquinM, MarquesM, et al. The N-terminal phosphorylation of RB by p38 bypasses its inactivation by cdks and prevents proliferation in cancer cells. Mol Cell. 2016;64(1):25–36.27642049
  • ZhangY, GaoY, ZhaoL, et al. Mitogen-activated protein kinase p38 and retinoblastoma protein signalling is required for DNA damage-mediated formation of senescence-associated heterochromatic foci in tumour cells. FEBS J. 2013;280(18):4625–4639.23859194
  • ZhangX, KimJ, RuthazerR, et al. The HBP1 transcriptional repressor participates in RAS-induced premature senescence. Mol Cell Biol. 2006;26(22):8252–8266.16966377
  • ReinhardtHC, AslanianAS, LeesJA, YaffeMB. p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell. 2007;11(2):175–189.17292828
  • Bar-OnO, ShapiraM, HershkoDD. Differential effects of doxorubicin treatment on cell cycle arrest and Skp2 expression in breast cancer cells. Anticancer Drugs. 2007;18(10):1113–1121.17893511
  • ForoodiF, DuivenvoordenWC, SinghG. Interactions of doxycycline with chemotherapeutic agents in human breast adenocarcinoma MDA-MB-231 cells. Anticancer Drugs. 2009;20(2):115–122.19209028
  • GreenH, StålO, BachmeierK, et al. Pegylated liposomal doxorubicin as first-line monotherapy in elderly women with locally advanced or metastatic breast cancer: novel treatment predictive factors identified. Cancer Lett. 2011;313(2):145–153.22056077
  • YuK-D, ZhuR, ZhanM, et al. Identification of Prognosis-Relevant Subgroups in Patients with Chemoresistant Triple Negative Breast Cancer. Clin Cancer Res. 2013;19(10):2723–2733.23549873
  • SharmaP, López-TarruellaS, García-SaenzJA, et al. Efficacy of neoadjuvant carboplatin plus docetaxel in triple negative breast cancer: combined analysis of two cohorts. Clin Cancer Res. 2017;23(3):649–657.27301700
  • MansillaS, PriebeW, PortugalJ. Mitotic catastrophe results in cell death by caspase-dependent and caspase-independent mechanisms. Cell Cycle. 2006;5(1):53–60.16319532
  • LehmannBD, BauerJA, ChenX, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011;121(7):2750–2767.21633166
  • MagerDE, WooS, JuskoWJ. Scaling pharmacodynamics from in vitro and preclinical animal studies to humans. Drug Metab Pharmacokinet. 2009;24(1):16–24.19252333