Eribulin in non-small cell lung cancer: challenges and potential strategies

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30.
   PubMed Web of Science ®Google Scholar
• Molina JR, Yang P, Cassivi SD, et al. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc. 2008;83:584–594.
   PubMed Web of Science ®Google Scholar
• American Cancer Society. Non-small cell lung cancer survival rates, by stage. Available from: http://www.cancer.org/cancer/lungcancer-non-smallcell/detailedguide/non-small-cell-lung-cancer-survival-rates Retrieved July 5,2016
   Google Scholar
• PDQ® Adult Treatment Editorial Board. PDQ Non-Small Cell Lung Cancer Treatment. Bethesda, MD: National Cancer Institute. Updated Jan 01, 2017. [cited 2017 Feb 14]. Available from: http://www.cancer.gov/types/lung/hp/non-small-cell-lung-treatment-pdq. [PMID: 26389304]
   Google Scholar
• National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology. Non-small cell lung cancer. 2016; https://www.nccn.org/professionals/physician_gls/pdf/nscl.pdf Retrieved July 21 2016.
   Google Scholar
• Swami U, Shah U, Goel S. Eribulin in cancer treatment. Marine Drugs. 2015;13:5016–5058.
   PubMed Web of Science ®Google Scholar
• Swami U, Chaudhary I, Ghalib MH, et al. Eribulin – a review of preclinical and clinical studies. Crit Rev Oncol Hematol. 2012;81:163–184.
   PubMed Web of Science ®Google Scholar
• Hirata Y, Uemura D. Halichondrins – antitumor polyether macrolides from a marine sponge. Pure and Applied Chemistry. 1986;58:701–710.
   Web of Science ®Google Scholar
• Bai RL, Paull KD, Herald CL, et al. Halichondrin B and homohalichondrin B, marine natural products binding in the vinca domain of tubulin. Discovery of tubulin-based mechanism of action by analysis of differential cytotoxicity data. J Biol Chem. 1991;266:15882–15889.
   PubMed Web of Science ®Google Scholar
• Towle MJ, Salvato KA, Budrow J, et al. In vitro and in vivo anticancer activities of synthetic macrocyclic ketone analogues of halichondrin B. Cancer Res. 2001;61:1013–1021.
   PubMed Web of Science ®Google Scholar
• Aicher TD, Buszek KR, Fang FG, et al. Total synthesis of halichondrin B and norhalichondrin B. J Am Chem Soc. 1992;114:3162–3164.
   Web of Science ®Google Scholar
• Yu MJ, Zheng W, Seletsky BM. From micrograms to grams: scale-up synthesis of eribulin mesylate. Nat Prod Rep. 2013;30:1158–1164.
   PubMed Web of Science ®Google Scholar
• United States National Institutes of Health. Search of: eribulin – list results. Clinicaltrials Gov. Available from: https://clinicaltrials.gov/ct2/results?term=eribulinSearch=Search Retrieved July 21 2016.
   Google Scholar
• Swami U, Shah U, Goel S. Marine sponge derived eribulin in preclinical and clinical studies for cancer. In: Kim S-K, editor. Handbook of anticancer drugs from marine origin. Cham, Switzerland:Springer International Publishing. 2015. p. 59–100.
   Google Scholar
• Hirsch FR, Suda K, Wiens J, et al. New and emerging targeted treatments in advanced non-small-cell lung cancer. Lancet (London, England). 2016;388:1012–1024.
   PubMed Web of Science ®Google Scholar
• Antonia S, Goldberg SB, Balmanoukian A, et al. Safety and antitumour activity of durvalumab plus tremelimumab in non-small cell lung cancer: a multicentre, phase 1b study. Lancet Oncol. 2016;17:299–308.
   PubMed Web of Science ®Google Scholar
• Gadgeel SM, Stevenson J, Langer CJ, et al. Pembrolizumab (pembro) plus chemotherapy as front-line therapy for advanced NSCLC: KEYNOTE-021 cohorts A-C. ASCO Meet Abstr. 2016;34:9016.
   Google Scholar
• Langer CJ, Gadgeel SM, Borghaei H, et al. Carboplatin and pemetrexed with or without pembrolizumab for advanced, non-squamous non-small-cell lung cancer: a randomised, phase 2 cohort of the open-label KEYNOTE-021 study. Lancet Oncol. 2016;17:1497–1508.
   PubMed Web of Science ®Google Scholar
• United States National Institutes of Health. Study of platinum+pemetrexed chemotherapy with or without pembrolizumab (MK-3475) in participants with first line metastatic non-squamous non-small cell lung cancer (MK-3475-189/KEYNOTE-189) – full text view – clinicaltrials.gov 2016. Available from: https://clinicaltrials.gov/ct2/show/NCT02578680 Retrieved Sep 3, 2016
   Google Scholar
• United States National Institutes of Health. A study of carboplatin-paclitaxel/nab-paclitaxel chemotherapy with or without pembrolizumab (MK-3475) in adults with first line metastatic squamous non-small cell lung cancer (MK-3475-407/KEYNOTE-407) – full text view – clinicaltrials.gov 2016. Available from: https://clinicaltrials.gov/ct2/show/NCT02775435 Retrieved Sep 3, 2016
   Google Scholar
• United States National Institutes of Health. A trial of nivolumab, or nivolumab plus ipilimumab, or nivolumab plus platinum-doublet chemotherapy, compared to platinum doublet chemotherapy in patients with stage IV non-small cell lung cancer (NSCLC) – full text view – clinicaltrials.gov 2016. Available from: https://clinicaltrials.gov/ct2/show/NCT02477826 Retrieved Sep 3, 2016
   Google Scholar
• Reck M, Rodriguez-Abreu D, Robinson AG, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375:1823–1833.
   PubMed Web of Science ®Google Scholar
• National Cancer Institute Division of Cancer Treatment and Diagnosis; Featured Agents CTEP Rapid Communication Solicitation for Letters of Intent Clinical Trials Preclinical Experiments E7389 Halichondrin B analog (NSC 707389). Available from: http://dctd.cancer.gov/featuredagents/pdfs/e7389solicitationmarch2005.Pdf Retrieved July 21, 2016
   Google Scholar
• Kuznetsov G, Towle MJ, Cheng H, et al. Induction of morphological and biochemical apoptosis following prolonged mitotic blockage by halichondrin B macrocyclic ketone analog E7389. Cancer Res. 2004;64:5760–5766.
   PubMed Web of Science ®Google Scholar
• Towle MJ, Salvato KA, Wels BF, et al. Eribulin induces irreversible mitotic blockade: implications of cell-based pharmacodynamics for in vivo efficacy under intermittent dosing conditions. Cancer Res. 2011;71:496–505.
   PubMed Web of Science ®Google Scholar
• Jordan MA, Kamath K, Manna T, et al. The primary antimitotic mechanism of action of the synthetic halichondrin E7389 is suppression of microtubule growth. Mol Cancer Ther. 2005;4:1086–9527.
   PubMed Web of Science ®Google Scholar
• Smith JA, Wilson L, Azarenko O, et al. Eribulin binds at microtubule ends to a single site on tubulin to suppress dynamic instability. Biochemistry. 2010;49:1331–1337.
   PubMed Web of Science ®Google Scholar
• Morgan RJ, Synold TW, Longmate JA, et al. Pharmacodynamics (PD) and pharmacokinetics (PK) of E7389 (eribulin, halichondrin B analog) during a phase I trial in patients with advanced solid tumors: a California Cancer Consortium trial. Cancer Chemother Pharmacol. 2015;76:897–907. Epub 2015/09/13
   PubMed Web of Science ®Google Scholar
• Wilson L, Lopus M, Miller HP, et al. Effects of eribulin on microtubule binding and dynamic instability are strengthened in the absence of the betaIII tubulin isotype. Biochemistry. 2015;54:6482–6489.
   PubMed Web of Science ®Google Scholar
• Agoulnik S, Kuznetsov G, Tendyke K, et al. Sensitivity to halichondrin analog E7389 and hemiasterlin analog E7974 correlates with {beta}III tubulin isotype expression in human breast cancer cell lines. ASCO Meet Abstr. 2005;23:2012.
   Google Scholar
• Doodhi H, Prota AE, Rodriguez-Garcia R, et al. Termination of protofilament elongation by eribulin induces lattice defects that promote microtubule catastrophes. Curr Biol. 2016;26:1713–1721.
   PubMed Web of Science ®Google Scholar
• Chanez B, Goncalves A, Badache A, et al. Eribulin targets a ch-TOG-dependent directed migration of cancer cells. Oncotarget. 2015;6:41667–41678.
   PubMed Web of Science ®Google Scholar
• Kurebayashi J, Kanomata N, Yamashita T, et al. Antitumor and anticancer stem cell activities of eribulin mesylate and antiestrogens in breast cancer cells. Breast Cancer. 2016;23:425–436.
   PubMed Web of Science ®Google Scholar
• Yamaguchi S, Maida Y, Yasukawa M, et al. Eribulin mesylate targets human telomerase reverse transcriptase in ovarian cancer cells. Plos One. 2014;9:e112438. Epub 2014/11/07
   PubMed Web of Science ®Google Scholar
• Yoshida T, Ozawa Y, Kimura T, et al. Eribulin mesilate suppresses experimental metastasis of breast cancer cells by reversing phenotype from epithelial-mesenchymal transition (EMT) to mesenchymal-epithelial transition (MET) states. Br J Cancer. 2014;110:1497–1505.
   PubMed Web of Science ®Google Scholar
• Funahashi Y, Okamoto K, Adachi Y, et al. Eribulin mesylate reduces tumor microenvironment abnormality by vascular remodeling in preclinical human breast cancer models. Cancer Science. 2014;105:1334–1342.
   PubMed Web of Science ®Google Scholar
• Kawano S, Asano M, Adachi Y, et al. Antimitotic and non-mitotic effects of eribulin mesilate in soft tissue sarcoma. Anticancer Res. 2016;36:1553–1561.
   PubMed Web of Science ®Google Scholar
• Agoulnik SI, Kawano S, Taylor N, et al. Eribulin mesylate exerts specific gene expression changes in pericytes and shortens pericyte-driven capillary network in vitro. Vascular Cell. 2014;6:3.
   PubMedGoogle Scholar
• Ueda S, Saeki T, Takeuchi H, et al. In vivo imaging of eribulin-induced reoxygenation in advanced breast cancer patients: a comparison to bevacizumab. Br J Cancer. 2016;114:1212–1218.
   PubMed Web of Science ®Google Scholar
• Suzuki H, Hirata Y, Suzuki N, et al. Characterization of a new small bowel adenocarcinoma cell line and screening of anti-cancer drug against small bowel adenocarcinoma. Am J Pathol. 2015;185:550–562.
   PubMed Web of Science ®Google Scholar
• Zheng W, Seletsky BM, Palme MH. Structure-activity relationships of synthetic halichondrin B analog E7389: in vitro susceptibility to PgP-mediated drug efflux. Annu Meeting Am Assoc Cancer Res. 2003;7:abstract 2751.
   Google Scholar
• Zhang ZY, King BM, Pelletier RD, et al. Delineation of the interactions between the chemotherapeutic agent eribulin mesylate (E7389) and human CYP3A4. Cancer Chemother Pharmacol. 2008;62:707–716.
   PubMed Web of Science ®Google Scholar
• Goel S, Mita AC, Mita M, et al. A phase I study of eribulin mesylate (E7389), a mechanistically novel inhibitor of microtubule dynamics, in patients with advanced solid malignancies. Clin Cancer Res. 2009;15:4207–4212.
   PubMed Web of Science ®Google Scholar
• Dubbelman AC, Rosing H, Jansen RS, et al. Mass balance study of [(1, 4)C]eribulin in patients with advanced solid tumors. Drug Metab Dispos. 2012;40:313–321.
   PubMed Web of Science ®Google Scholar
• Devriese LA, Witteveen PO, Marchetti S, et al. Pharmacokinetics of eribulin mesylate in patients with solid tumors and hepatic impairment. Cancer Chemother Pharmacol. 2012;70:823–832.
   PubMed Web of Science ®Google Scholar
• United States Food and Drug Administration. Halaven Prescribing Information 2016. Available from: http://www.accessdata.fda.gov/drugsatfda_docs/label/2016/201532s015lbl.pdf Retrieved July 21, 2016
   Google Scholar
• Tan AR, Sarantopoulos J, Lee L, et al. Pharmacokinetics of eribulin mesylate in cancer patients with normal and impaired renal function. Cancer Chemother Pharmacol. 2015;76:1051–1061.
   PubMed Web of Science ®Google Scholar
• Devriese LA, Witteveen PE, Wanders J, et al. Pharmacokinetics of eribulin mesylate in patients with solid tumours receiving repeated oral rifampicin. Br J Clin Pharmacol. 2013;75:507–515.
   PubMed Web of Science ®Google Scholar
• Devriese LA, Mergui-Roelvink M, Wanders J, et al. Eribulin mesylate pharmacokinetics in patients with solid tumors receiving repeated oral ketoconazole. Invest New Drugs. 2013;31:381–389.
   PubMed Web of Science ®Google Scholar
• Koczywas M, Frankel PH, Synold TW, et al. Phase I study of the halichondrin B analogue eribulin mesylate in combination with cisplatin in advanced solid tumors. Br J Cancer. 2014;111:2268–2274.
   PubMed Web of Science ®Google Scholar
• Mukai H, Saeki T, Shimada K, et al. Phase 1 combination study of eribulin mesylate with trastuzumab for advanced or recurrent human epidermal growth factor receptor 2 positive breast cancer. Invest New Drugs. 2015;33:119–127.
   PubMed Web of Science ®Google Scholar
• Swami U, Petrylak DP, Raftopoulos H, et al. Phase IB study of eribulin mesylate in combination with carboplatin in patients with advanced solid tumors. J Clin Oncol (Meeting Abstracts). 2010;28:2589.
   Web of Science ®Google Scholar
• Nasim MY, Plummer R, Evans TRJ, et al. A phase Ib dose-escalation study of eribulin mesylate in combination with capecitabine in patients with advanced/metastatic cancer. ASCO Meet Abstr. 2012;30:2552.
   Google Scholar
• Sakiyama T, Tsurutani J, Iwasa T, et al. A phase I dose-escalation study of eribulin and S-1 for metastatic breast cancer. Br J Cancer. 2015;112:819–824.
   PubMed Web of Science ®Google Scholar
• Lesimple T, Edeline J, Carrothers TJ, et al. A phase I, open-label, single-arm study for QT assessment of eribulin mesylate in patients with advanced solid tumors. Invest New Drugs. 2013;31:900–909.
   PubMed Web of Science ®Google Scholar
• Tan AR, Rubin EH, Walton DC, et al. Phase I study of eribulin mesylate administered once every 21 days in patients with advanced solid tumors. Clin Cancer Res. 2009;15:4213–4219.
   PubMed Web of Science ®Google Scholar
• Mukohara T, Nagai S, Mukai H, et al. Eribulin mesylate in patients with refractory cancers: a phase I study. Invest New Drugs. 2012;30:1926–1933.
   PubMed Web of Science ®Google Scholar
• Lheureux S, Oza AM, Laurie SA, et al. A phase I combination dose-escalation study of eribulin mesylate and gemcitabine in patients with advanced solid tumours: a study of the Princess Margaret Consortium. Br J Cancer. 2015;113:1534–1540.
   PubMed Web of Science ®Google Scholar
• Waller CF, Vynnychenko I, Bondarenko I, et al. An open-label, multicenter, randomized phase Ib/II study of eribulin mesylate administered in combination with pemetrexed versus pemetrexed alone as second-line therapy in patients with advanced nonsquamous non-small-cell lung cancer. Clinical Lung Cancer. 2015;16:92–99.
   PubMed Web of Science ®Google Scholar
• Dubbelman AC, Rosing H, Jansen RS, et al. Mass balance study of [(1, 4)C]eribulin in patients with advanced solid tumors. Drug Metab Dispos. 2012;40:313–321.
   PubMed Web of Science ®Google Scholar
• Spira AI, Iannotti NO, Savin MA, et al. A phase II study of eribulin mesylate (E7389) in patients with advanced, previously treated non-small-cell lung cancer. Clinical Lung Cancer. 2012;13:31–38.
   PubMed Web of Science ®Google Scholar
• Vahdat LT, Pruitt B, Fabian CJ, et al. Phase II study of eribulin mesylate, a halichondrin B analog, in patients with metastatic breast cancer previously treated with an anthracycline and a taxane. J Clinical Oncology: Official Journal Am Soc Clin Oncol. 2009;27:2954–6163.
   PubMed Web of Science ®Google Scholar
• Gitlitz BJ, Tsao-Wei DD, Groshen S, et al. A phase II study of halichondrin B analog eribulin mesylate (E7389) in patients with advanced non-small cell lung cancer previously treated with a taxane: a California Cancer Consortium trial. J Thorac Oncol. 2012;7:574–578.
   PubMed Web of Science ®Google Scholar
• Mok TS, Geater SL, Iannotti N, et al. Randomized phase II study of two intercalated combinations of eribulin mesylate and erlotinib in patients with previously treated advanced non-small-cell lung cancer. Ann Oncol. 2014;25:1578–1584.
   PubMed Web of Science ®Google Scholar
• Raftopoulos H, Aisner J, Kumar K, et al. Phase Ib extension study of eribulin mesylate in combination with carboplatin in patients with chemotherapy-naive advanced non-small cell lung cancer (NSCLC). ASCO Meet Abstr. 2013;31:e19145.
   Google Scholar
• Spigel DR, Barlesi F, Felip E, et al. Efficacy and safety of eribulin compared with treatment of physician’s choice (TPC) in patients with advanced non-small-cell lung cancer (NSCLC): results from a phase 3 study. Int J Radiat Oncol • Biol • Phys. 2014;90:1266.
   Web of Science ®Google Scholar
• Schoffski P, Chawla S, Maki RG, et al. Eribulin versus dacarbazine in previously treated patients with advanced liposarcoma or leiomyosarcoma: a randomised, open-label, multicentre, phase 3 trial. Lancet (London, England). 2016;387:1629–1637.
   PubMed Web of Science ®Google Scholar
• Cortes J, O’Shaughnessy J, Loesch D, et al. Eribulin monotherapy versus treatment of physician’s choice in patients with metastatic breast cancer (EMBRACE): a phase 3 open-label randomised study. Lancet (London, England). 2011;377:914–923.
   PubMed Web of Science ®Google Scholar
• Kaufman PA, Awada A, Twelves C, et al. Phase III open-label randomized study of eribulin mesylate versus capecitabine in patients with locally advanced or metastatic breast cancer previously treated with an anthracycline and a taxane. J Clinical Oncology: Official Journal Am Soc Clin Oncol. 2015;33:594–601.
   PubMed Web of Science ®Google Scholar
• Cortes J, Hudgens S, Twelves C, et al. Health-related quality of life in patients with locally advanced or metastatic breast cancer treated with eribulin mesylate or capecitabine in an open-label randomized phase 3 trial. Breast Cancer Res Treat. 2015;154:509–520.
   PubMed Web of Science ®Google Scholar
• Twelves C, Cortes J, Vahdat L, et al. Efficacy of eribulin in women with metastatic breast cancer: a pooled analysis of two phase 3 studies. Breast Cancer Res Treat. 2014;148:553–561.
   PubMed Web of Science ®Google Scholar
• Cohen MH, Cortazar P, Justice R, et al. Approval summary: pemetrexed maintenance therapy of advanced/metastatic nonsquamous, non-small cell lung cancer (NSCLC). The Oncologist. 2010;15:1352–1358.
   PubMed Web of Science ®Google Scholar
• Kazandjian D, Suzman DL, Blumenthal G, et al. FDA approval summary: nivolumab for the treatment of metastatic non-small cell lung cancer with progression on or after platinum-based chemotherapy. The Oncologist. 2016;21:634–642.
   PubMed Web of Science ®Google Scholar
• ASCO post. Nivolumab did not meet primary endpoint of progression-free survival in NSCLC in checkmate-026 trial – the ASCO post 2016. Available from: http://www.ascopost.com/News/43820 Retrieved Sep 3, 2016
   Google Scholar
• Fehrenbacher L, Spira A, Ballinger M, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. Lancet (London, England). 2016;387:1837–1846.
   PubMed Web of Science ®Google Scholar
• Zubairi IH, Dean EJ, Molife LR, et al. Phase 1 multicenter, open-label study to establish the maximum tolerated dose (MTD) of two administration schedules of E7389 (eribulin) liposomal formulation in patients (pts) with solid tumors. ASCO Meet Abstr. 2016;34:2524.
   Google Scholar
• Yu MJ, Zheng W, Tendyke K. Atom-based enumeration: new eribulin analogues with low susceptibility to P-glycoprotein-mediated drug efflux. Bioorg Med Chem Lett. 2012;22:7363–7366.
   PubMed Web of Science ®Google Scholar
• Narayan S, Carlson EM, Cheng H, et al. Novel second generation analogs of eribulin. Part I: compounds containing a lipophilic C32 side chain overcome P-glycoprotein susceptibility. Bioorg Med Chem Lett. 2011;21:1630–1633.
   PubMed Web of Science ®Google Scholar
• Laughney AM, Kim E, Sprachman MM, et al. Single-cell pharmacokinetic imaging reveals a therapeutic strategy to overcome drug resistance to the microtubule inhibitor eribulin. Sci Transl Med. 2014;6:261ra152.
   PubMed Web of Science ®Google Scholar
• Kashiwagi S, Asano Y, Kurata K, et al. 173ptle3 is a useful marker for predicting the therapeutic effect of eribulin chemotherapy for triple-negative breast cancer. Ann Oncol. 2014;25:iv60.
   Google Scholar
• Dezso Z, Oestreicher J, Weaver A, et al. Gene expression profiling reveals epithelial mesenchymal transition (EMT) genes can selectively differentiate eribulin sensitive breast cancer cells. Plos One. 2014;9:e106131.
   PubMed Web of Science ®Google Scholar
• Berrak E, Atkan G, Song J, et al. Abstract OT1-03-19: design of a phase 1b/2 study to evaluate the efficacy and safety of eribulin mesylate in combination with pembrolizumab in patients with metastatic triple-negative breast cancer. Cancer Res. 2016;76:OT1-03-19-OT1-03-19.
   Web of Science ®Google Scholar
• Winer EP, Dang T, Karantza V, et al. KEYNOTE-119: a randomized phase III study of single-agent pembrolizumab (MK-3475) vs single-agent chemotherapy per physician’s choice for metastatic triple-negative breast cancer (mTNBC). ASCO Meet Abstr. 2016;34:TPS1102.
   Google Scholar