The strategic combination of trastuzumab emtansine with oncolytic rhabdoviruses leads to therapeutic synergy.
Animals
Antineoplastic Combined Chemotherapy Protocols
/ pharmacology
Apoptosis
Breast Neoplasms
/ metabolism
Cell Proliferation
Combined Modality Therapy
Drug Synergism
Female
Humans
Maytansine
/ administration & dosage
Mice
Mice, Nude
Oncolytic Virotherapy
/ methods
Rhabdoviridae
/ genetics
Trastuzumab
/ administration & dosage
Tumor Cells, Cultured
Xenograft Model Antitumor Assays
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
22 05 2020
22 05 2020
Historique:
received:
05
09
2019
accepted:
29
04
2020
entrez:
24
5
2020
pubmed:
24
5
2020
medline:
16
6
2021
Statut:
epublish
Résumé
We have demonstrated that microtubule destabilizing agents (MDAs) can sensitize tumors to oncolytic vesicular stomatitis virus (VSVΔ51) in various preclinical models of cancer. The clinically approved T-DM1 (Kadcyla®) is an antibody-drug conjugate consisting of HER2-targeting trastuzumab linked to the potent MDA and maytansine derivative DM1. We reveal that combining T-DM1 with VSVΔ51 leads to increased viral spread and tumor killing in trastuzumab-binding, VSVΔ51-resistant cancer cells. In vivo, co-treatment of VSVΔ51 and T-DM1 increased overall survival in HER2-overexpressing, but trastuzumab-refractory, JIMT1 human breast cancer xenografts compared to monotherapies. Furthermore, viral spread in cultured HER2
Identifiants
pubmed: 32444806
doi: 10.1038/s42003-020-0972-7
pii: 10.1038/s42003-020-0972-7
pmc: PMC7244474
doi:
Substances chimiques
Maytansine
14083FR882
Trastuzumab
P188ANX8CK
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
254Subventions
Organisme : CIHR
ID : 390880
Pays : Canada
Organisme : CIHR
ID : INI-147824
Pays : Canada
Organisme : CIHR
ID : 705952
Pays : Canada
Références
Verri, E. et al. HER2/neu oncoprotein overexpression in epithelial ovarian cancer: evaluation of its prevalence and prognostic significance. Clin. Study Oncol. 68, 154–161 (2005).
Chung, C. H. et al. Increased epidermal growth factor receptor gene copy number is associated with poor prognosis in head and neck squamous cell carcinomas. J. Clin. Oncol. 24, 4170–4176 (2006).
pubmed: 16943533
doi: 10.1200/JCO.2006.07.2587
Palle, J. et al. Human epidermal growth factor receptor 2 (HER2) in advanced gastric cancer: current knowledge and future perspectives. Drugs 80, 401–415 (2020).
Iqbal, N. & Iqbal, N. Human epidermal growth factor receptor 2 (HER2) in cancers: overexpression and therapeutic implications. Mol. Biol. Int. 2014, 852748 (2014).
pubmed: 25276427
pmcid: 4170925
doi: 10.1155/2014/852748
Slamon, D. J. et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235, 177–182 (1987).
doi: 10.1126/science.3798106
Bang, Y. J. et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 376, 687–697 (2010).
pubmed: 20728210
doi: 10.1016/S0140-6736(10)61121-X
von Minckwitz, G. et al. Trastuzumab emtansine for residual invasive HER2-positive breast cancer. N. Engl. J. Med. 380, 617–628 (2019).
doi: 10.1056/NEJMoa1814017
Leyland-Jones, B. Trastuzumab: hopes and realities. Lancet Oncol. 3, 137–144 (2002).
pubmed: 11902499
doi: 10.1016/S1470-2045(02)00676-9
Fiszman, G. L. & Jasnis, M. A. Molecular mechanisms of trastuzumab resistance in HER2 overexpressing breast cancer. Int J. Breast Cancer 2011, 352182 (2011).
pubmed: 22295219
pmcid: 3262573
doi: 10.4061/2011/352182
Martinez, M. T. et al. Treatment of HER2 positive advanced breast cancer with T-DM1: a review of the literature. Crit. Rev. Oncol. Hematol. 97, 96–106 (2016).
pubmed: 26318092
doi: 10.1016/j.critrevonc.2015.08.011
Gujar, S., Bell, J. & Diallo, J. S. SnapShot: cancer immunotherapy with oncolytic viruses. Cell 176, 1240–1240.e1241 (2019).
pubmed: 30794777
doi: 10.1016/j.cell.2019.01.051
Arulanandam, R. et al. Microtubule disruption synergizes with oncolytic virotherapy by inhibiting interferon translation and potentiating bystander killing. Nat. Commun. 6, 6410 (2015).
pubmed: 25817275
doi: 10.1038/ncomms7410
Dornan, M. H. et al. First-in-class small molecule potentiators of cancer virotherapy. Sci. Rep. 6, 26786 (2016).
pubmed: 27226390
pmcid: 4880900
doi: 10.1038/srep26786
Selman, M. et al. Multi-modal Potentiation of oncolytic virotherapy by vanadium compounds. Mol. Ther. 26, 56–69 (2018).
pubmed: 29175158
doi: 10.1016/j.ymthe.2017.10.014
Selman, M. et al. Dimethyl fumarate potentiates oncolytic virotherapy through NF-kappaB inhibition. Sci. Transl. Med. 10, eaao1613 (2018).
Phan, M., Watson, M. F., Alain, T. & Diallo, J. S. Oncolytic viruses on drugs:achieving higher therapeutic efficacy. ACS Infect. Dis. 4, 1448–1467 (2018).
pubmed: 30152676
doi: 10.1021/acsinfecdis.8b00144
Burstein, H. J. et al. Trastuzumab plus vinorelbine or taxane chemotherapy for HER2-overexpressing metastatic breast cancer: the trastuzumab and vinorelbine or taxane study. Cancer 110, 965–972 (2007).
pubmed: 17614302
doi: 10.1002/cncr.22885
Lopus, M. Antibody-DM1 conjugates as cancer therapeutics. Cancer Lett. 307, 113–118 (2011).
pubmed: 21481526
pmcid: 3105156
doi: 10.1016/j.canlet.2011.03.017
Dumontet, C. & Jordan, M. A. Microtubule-binding agents: a dynamic field of cancer therapeutics. Nat. Rev. Drug Discov. 9, 790–803 (2010).
pubmed: 20885410
pmcid: 3194401
doi: 10.1038/nrd3253
Diamantis, N. & Banerji, U. Antibody-drug conjugates-an emerging class of cancer treatment. Br. J. Cancer 114, 362–367 (2016).
pubmed: 26742008
pmcid: 4815767
doi: 10.1038/bjc.2015.435
Schrama, D., Reisfeld, R. A. & Becker, J. C. Antibody targeted drugs as cancer therapeutics. Nat. Rev. Drug Discov. 5, 147–159 (2006).
pubmed: 16424916
doi: 10.1038/nrd1957
Cilliers, C., Menezes, B., Nessler, I., Linderman, J. & Thurber, G. M. Improved tumor penetration and single-cell targeting of antibody-drug conjugates increases anticancer efficacy and host survival. Cancer Res. 78, 758–768 (2018).
pubmed: 29217763
doi: 10.1158/0008-5472.CAN-17-1638
Bauzon, M. et al. Maytansine-bearing antibody-drug conjugates induce in vitro hallmarks of immunogenic cell death selectively in antigen-positive target cells. Oncoimmunology 8, e1565859 (2019).
pubmed: 30906660
pmcid: 6422391
doi: 10.1080/2162402X.2019.1565859
Junttila, T. T., Li, G., Parsons, K., Phillips, G. L. & Sliwkowski, M. X. Trastuzumab-DM1 (T-DM1) retains all the mechanisms of action of trastuzumab and efficiently inhibits growth of lapatinib insensitive breast cancer. Breast Cancer Res. Treat. 128, 347–356 (2011).
pubmed: 20730488
doi: 10.1007/s10549-010-1090-x
Lewis Phillips, G. D. et al. Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibody-cytotoxic drug conjugate. Cancer Res. 68, 9280–9290 (2008).
pubmed: 19010901
doi: 10.1158/0008-5472.CAN-08-1776
Baron, J. M., Boster, B. L. & Barnett, C. M. Ado-trastuzumab emtansine (T-DM1): a novel antibody-drug conjugate for the treatment of HER2-positive metastatic breast cancer. J. Oncol. Pharm. Pract. 21, 132–142 (2015).
pubmed: 24682654
doi: 10.1177/1078155214527144
Poon, K. A. et al. Preclinical safety profile of trastuzumab emtansine (T-DM1): mechanism of action of its cytotoxic component retained with improved tolerability. Toxicol. Appl. Pharm. 273, 298–313 (2013).
doi: 10.1016/j.taap.2013.09.003
Verma, S. et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N. Engl. J. Med. 367, 1783–1791 (2012).
pubmed: 23020162
pmcid: 5125250
doi: 10.1056/NEJMoa1209124
Garcia, V. et al. High-throughput titration of luciferase-expressing recombinant viruses. J. Vis. Exp. e51890, https://doi.org/10.3791/51890 (2014).
Kershaw, M. H. et al. Gene-engineered T cells as a superior adjuvant therapy for metastatic cancer. J. Immunol. 173, 2143–2150 (2004).
pubmed: 15265951
doi: 10.4049/jimmunol.173.3.2143
Schwartz, E. L. Antivascular actions of microtubule-binding drugs. Clin. Cancer Res. 15, 2594–2601 (2009).
pubmed: 19351751
pmcid: 2745203
doi: 10.1158/1078-0432.CCR-08-2710
Kanthou, C. & Tozer, G. M. Microtubule depolymerizing vascular disrupting agents: novel therapeutic agents for oncology and other pathologies. Int. J. Exp. Pathol. 90, 284–294 (2009).
pubmed: 19563611
pmcid: 2697551
doi: 10.1111/j.1365-2613.2009.00651.x
Breitbach, C. J. et al. Targeting tumor vasculature with an oncolytic virus. Mol. Ther. 19, 886–894 (2011).
pubmed: 21364541
pmcid: 3098639
doi: 10.1038/mt.2011.26
Russell, S. J., Peng, K. W. & Bell, J. C. Oncolytic virotherapy. Nat. Biotechnol. 30, 658–670 (2012).
pubmed: 22781695
pmcid: 3888062
doi: 10.1038/nbt.2287
Lyon, R. Drawing lessons from the clinical development of antibody-drug conjugates. Drug Discov. Today Technol. 30, 105–109 (2018).
pubmed: 30553514
doi: 10.1016/j.ddtec.2018.10.001
Diallo, J. S., Vaha-Koskela, M., Le Boeuf, F. & Bell, J. Propagation, purification, and in vivo testing of oncolytic vesicular stomatitis virus strains. Methods Mol. Biol. 797, 127–140 (2012).
pubmed: 21948474
doi: 10.1007/978-1-61779-340-0_10
Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001).
pubmed: 11328886
pmcid: 55695
doi: 10.1093/nar/29.9.e45