Synthesis of micellar-like terpolymer nanoparticles with reductively-cleavable cross-links and evaluation of efficacy in 2D and 3D models of triple negative breast cancer
Center for Education and Research on Macromolecules (CERM) Complex and Entangled Systems from Atoms to Materials (CESAM) Research Unit
Disciplines :
Chemistry Materials science & engineering
Author, co-author :
Monteiro, Patricia F.; University of Nottingham, School of Pharmacy, United Kingdom
Gulfam, Muhammad; University of Nottingham, School of Pharmacy, United Kingdom
Monteiro, Cíntia J.; University of Nottingham, School of Pharmacy, United Kingdom
Travanut, Alessandra; University of Nottingham, School of Pharmacy, United Kingdom
Abelha, Thais Fedatto; University of Nottingham, School of Pharmacy, United Kingdom
Pearce, Amanda K. Pearcea,; University of Nottingham, School of Pharmacy, United Kingdom
Jérôme, Christine ; University of Liège (ULiège), Complex and Entangled Systems from Atoms to Materials (CESAM) Research Unit, Center for Education and Research on Macromolecules (CERM), Belgium
Grabowska, Anna M. Grabowskac,; University of Nottingham, Cancer Biology, Division of Cancer and Stem Cells, UK
Clarke, Philip A.; University of Nottingham, Cancer Biology, Division of Cancer and Stem Cells, UK
Collins, Hilary M.; University of Nottingham, School of Pharmacy, United Kingdom
Heery, David M.; University of Nottingham, School of Pharmacy, United Kingdom
Gershkovich, Pavel; School of Pharmacy, University of NottinghamNG7 2RD, United Kingdom
Alexander, Cameron; University of Nottingham, School of Pharmacy, United Kingdom
Synthesis of micellar-like terpolymer nanoparticles with reductively-cleavable cross-links and evaluation of efficacy in 2D and 3D models of triple negative breast cancer
Publication date :
10 July 2020
Journal title :
Journal of Controlled Release
ISSN :
0168-3659
eISSN :
1873-4995
Publisher :
Elsevier B.V.
Volume :
323
Pages :
549-564
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
EPSRC Programme Grant for Next Generation Biomaterials Discoveryand [Grants EP/H005625/1, EP/N03371X/1]; The Erasmus Mundus Joint Doctoral Program; NanoFarJointDoctoralProgram
Funders :
EPSRC - Engineering and Physical Sciences Research Council CAPES - Coordenação de Aperfeicoamento de Pessoal de Nível Superior Royal Society EC - European Commission EACEA - European Education and Culture Executive Agency
Boyle, P., Triple-negative breast cancer: epidemiological considerations and recommendations. Ann. Oncol., 23(Suppl. 6), 2012 (vi7-12).
Stockmans, G., Deraedt, K., Wildiers, H., Moerman, P., Paridaens, R., Triple-negative breast cancer. Curr. Opin. Oncol. 20:6 (2008), 614–620.
De Laurentiis, M., Cianniello, D., Caputo, R., Stanzione, B., Arpino, G., Cinieri, S., Lorusso, V., De Placido, S., Treatment of triple negative breast cancer (TNBC): current options and future perspectives. Cancer Treat. Rev. 36:Suppl. 3 (2010), S80–S86.
Perou, C.M., Sorlie, T., Eisen, M.B., van de Rijn, M., Jeffrey, S.S., Rees, C.A., Pollack, J.R., Ross, D.T., Johnsen, H., Akslen, L.A., Fluge, O., Pergamenschikov, A., Williams, C., Zhu, S.X., Lonning, P.E., Borresen-Dale, A.L., Brown, P.O., Botstein, D., Molecular portraits of human breast tumours. Nature 406:6797 (2000), 747–752.
Crown, J., O'Shaughnessy, J., Gullo, G., Emerging targeted therapies in triple-negative breast cancer. Ann. Oncol., 23(Suppl. 6), 2012 (vi56-65).
Schneider, B.P., Winer, E.P., Foulkes, W.D., Garber, J., Perou, C.M., Richardson, A., Sledge, G.W., Carey, L.A., Triple-negative breast cancer: risk factors to potential targets. Clin. Cancer Res. 14:24 (2008), 8010–8018.
Gelderblom, H., Verweij, J., Nooter, K., Sparreboom, A., Cremophor EL: the drawbacks and advantages of vehicle selection for drug formulation. Eur. J. Cancer 37:13 (2001), 1590–1598.
Andre, F., Zielinski, C.C., Optimal strategies for the treatment of metastatic triple-negative breast cancer with currently approved agents. Ann. Oncol., 23(Suppl. 6), 2012 (vi46-51).
Lu, H., Samanta, D., Xiang, L., Zhang, H., Hu, H., Chen, I., Bullen, J.W., Semenza, G.L., Chemotherapy triggers HIF-1-dependent glutathione synthesis and copper chelation that induces the breast cancer stem cell phenotype. Proc. Natl. Acad. Sci. U. S. A. 112:33 (2015), E4600–E4609.
Miran, T., Vogg, A.T.J., Drude, N., Mottaghy, F.M., Morgenroth, A., Modulation of glutathione promotes apoptosis in triple-negative breast cancer cells. FASEB J. 32:5 (2018), 2803–2813.
Beatty, A., Fink, L.S., Singh, T., Strigun, A., Peter, E., Ferrer, C.M., Nicolas, E., Cai, K.Q., Moran, T.P., Reginato, M.J., Rennefahrt, U., Peterson, J.R., Metabolite profiling reveals the glutathione biosynthetic pathway as a therapeutic target in triple-negative breast cancer. Mol. Cancer Ther. 17:1 (2018), 264–275.
Yao, H., He, G.C., Yan, S.C., Chen, C., Song, L.J., Rosol, T.J., Deng, X.Y., Triple-negative breast cancer: is there a treatment on the horizon?. Oncotarget 8:1 (2017), 1913–1924.
Peer, D., Karp, J.M., Hong, S., Farokhzad, O.C., Margalit, R., Langer, R., Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2:12 (2007), 751–760.
He, X., Cai, K., Zhang, Y., Lu, Y., Guo, Q., Zhang, Y., Liu, L., Ruan, C., Chen, Q., Chen, X., Li, C., Sun, T., Cheng, J., Jiang, C., Dimeric prodrug self-delivery nanoparticles with enhanced drug loading and bioreduction responsiveness for targeted cancer therapy. ACS Appl. Mater. Interfaces 10:46 (2018), 39455–39467.
Kutty, R.V., Chia, S.L., Setyawati, M.I., Muthu, M.S., Feng, S.S., Leong, D.T., In vivo and ex vivo proofs of concept that cetuximab conjugated vitamin E TPGS micelles increases efficacy of delivered docetaxel against triple negative breast cancer. Biomaterials 63 (2015), 58–69.
Deng, X., Cao, M., Zhang, J., Hu, K., Yin, Z., Zhou, Z., Xiao, X., Yang, Y., Sheng, W., Wu, Y., Zeng, Y., Hyaluronic acid-chitosan nanoparticles for co-delivery of MiR-34a and doxorubicin in therapy against triple negative breast cancer. Biomaterials 35:14 (2014), 4333–4344.
Devulapally, R., Sekar, N.M., Sekar, T.V., Foygel, K., Massoud, T.F., Willmann, J.K., Paulmurugan, R., Polymer nanoparticles mediated codelivery of antimiR-10b and antimiR-21 for achieving triple negative breast cancer therapy. ACS Nano 9:3 (2015), 2290–2302.
Mura, S., Nicolas, J., Couvreur, P., Stimuli-responsive nanocarriers for drug delivery. Nat. Mater. 12:11 (2013), 991–1003.
Balendiran, G.K., Dabur, R., Fraser, D., The role of glutathione in cancer. Cell Biochem. Funct. 22:6 (2004), 343–352.
Perry, R.R., Mazetta, J., Levin, M., Barranco, S.C., Glutathione levels and variability in breast-tumors and normal tissue. Cancer 72:3 (1993), 783–787.
Berger, S.J., Gosky, D., Zborowska, E., Willson, J.K.V., Berger, N.A., Sensitive enzymatic cycling assay for glutathione - measurements of glutathione content and its modulation by buthionine sulfoximine in-vivo and in-vitro in human colon-cancer. Cancer Res. 54:15 (1994), 4077–4083.
Cook, J.A., Pass, H.I., Iype, S.N., Friedman, N., Degraff, W., Russo, A., Mitchell, J.B., Cellular glutathione and thiol measurements from surgically resected human lung-tumor and normal lung-tissue. Cancer Res. 51:16 (1991), 4287–4294.
Xia, Y.C., He, H., Liu, X.Y., Hu, D., Yin, L.C., Lu, Y.B., Xua, W.J., Redox-responsive, core-crosslinked degradable micelles for controlled drug release. Polym. Chem.-U.K. 7:41 (2016), 6330–6339.
Zhao, X.B., Liu, P., Reduction-responsive core-shell-corona micelles based on triblock copolymers: novel synthetic strategy, characterization, and application as a tumor microenvironment-responsive drug delivery system. ACS Appl. Mater. Inter. 7:1 (2015), 166–174.
Conte, C., Mastrotto, F., Taresco, V., Tchoryk, A., Quaglia, F., Stolnik, S., Alexander, C., Enhanced uptake in 2D-and 3D-lung cancer cell models of redox responsive PEGylated nanoparticles with sensitivity to reducing extra- and intracellular environments. J. Control. Release 277 (2018), 126–141.
Zhang, X., Peng, X., Zhang, S.W., 7 - Synthetic biodegradable medical polymers: polymer blends. Zhang, X., (eds.) Science and Principles of Biodegradable and Bioresorbable Medical Polymers, 2017, Woodhead Publishing, 217–254.
Newman, D., Laredo, E., Bello, A., Grillo, A., Feijoo, J.L., Müller, A.J., Molecular mobilities in biodegradable poly(dl-lactide)/poly(ε-caprolactone) blends. Macromolecules 42:14 (2009), 5219–5225.
Chen, H., Kim, S., Li, L., Wang, S., Park, K., Cheng, J.X., Release of hydrophobic molecules from polymer micelles into cell membranes revealed by Forster resonance energy transfer imaging. Proc. Natl. Acad. Sci. U. S. A. 105:18 (2008), 6596–6601.
Wei, R., Cheng, L., Zheng, M., Cheng, R., Meng, F., Deng, C., Zhong, Z., Reduction-responsive disassemblable core-cross-linked micelles based on poly(ethylene glycol)-b-poly(N-2-hydroxypropyl methacrylamide)-lipoic acid conjugates for triggered intracellular anticancer drug release. Biomacromolecules 13:8 (2012), 2429–2438.
Zhang, L., Katapodi, K., Davis, T.P., Barner-Kowollik, C., Stenzel, M.H., Using the reversible addition–fragmentation chain transfer process to synthesize core-crosslinked micelles. J. Polym. Sci. A Polym. Chem. 44:7 (2006), 2177–2194.
Zhang, P., Zhang, H., He, W., Zhao, D., Song, A., Luan, Y., Disulfide-linked amphiphilic polymer-docetaxel conjugates assembled redox-sensitive micelles for efficient antitumor drug delivery. Biomacromolecules 17:5 (2016), 1621–1632.
Du, A.W., Lu, H., Stenzel, M.H., Core-cross-linking accelerates antitumor activities of paclitaxel-conjugate micelles to prostate multicellular tumor spheroids: a comparison of 2D and 3D models. Biomacromolecules 16:5 (2015), 1470–1479.
Hu, Q., Rijcken, C.J., Bansal, R., Hennink, W.E., Storm, G., Prakash, J., Complete regression of breast tumour with a single dose of docetaxel-entrapped core-cross-linked polymeric micelles. Biomaterials 53 (2015), 370–378.
Talelli, M., Barz, M., Rijcken, C.J.F., Kiessling, F., Hennink, W.E., Lammers, T., Core-crosslinked polymeric micelles: principles, preparation, biomedical applications and clinical translation. Nano Today 10:1 (2015), 93–117.
Kenry, B. Liu, Bio-orthogonal click chemistry for In Vivo bioimaging. Trends Chem. 1:8 (2019), 763–778.
Moses, J.E., Moorhouse, A.D., The growing applications of click chemistry. Chem. Soc. Rev. 36:8 (2007), 1249–1262.
Gulfam, M., Matini, T., Monteiro, P.F., Riva, R., Collins, H., Spriggs, K., Howdle, S.M., Jerome, C., Alexander, C., Bioreducible cross-linked core polymer micelles enhance in vitro activity of methotrexate in breast cancer cells. Biomater. Sci. 5:3 (2017), 532–550.
Lenoir, S., Riva, R., Lou, X., Detrembleur, C., Jérôme, R., Lecomte, P., Ring-opening polymerization of α-Chloro-ε-caprolactone and chemical modification of poly(α-chloro-ε-caprolactone) by atom transfer radical processes. Macromolecules 37:11 (2004), 4055–4061.
Cajot, S., Lautram, N., Passirani, C., Jerome, C., Design of reversibly core cross-linked micelles sensitive to reductive environment. J. Control. Release 152:1 (2011), 30–36.
Saunders, J.H., Onion, D., Collier, P., Dorrington, M.S., Argent, R.H., Clarke, P.A., Reece-Smith, A.M., Parsons, S.L., Grabowska, A.M., Individual patient oesophageal cancer 3D models for tailored treatment. Oncotarget 8:15 (2017), 24224–24236.
Su, H.Y., Liu, Y.H., Wang, D., Wu, C.Q., Xia, C.C., Gong, Q.Y., Song, B., Ai, H., Amphiphilic starlike dextran wrapped superparamagnetic iron oxide nanoparticle clsuters as effective magnetic resonance imaging probes. Biomaterials 34:4 (2013), 1193–1203.
Acharya, S., Sahoo, S.K., PLGA nanoparticles containing various anticancer agents and tumour delivery by EPR effect. Adv. Drug Deliv. Rev. 63:3 (2011), 170–183.
Perrault, S.D., Walkey, C., Jennings, T., Fischer, H.C., Chan, W.C.W., Mediating tumor targeting efficiency of nanoparticles through design. Nano Lett. 9:5 (2009), 1909–1915.
Cabral, H., Matsumoto, Y., Mizuno, K., Chen, Q., Murakami, M., Kimura, M., Terada, Y., Kano, M.R., Miyazono, K., Uesaka, M., Nishiyama, N., Kataoka, K., Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nat. Nanotechnol. 6:12 (2011), 815–823.
Huang, M.-H., Li, S., Hutmacher, D.W., Coudane, J., Vert, M., Degradation characteristics of poly(ϵ-caprolactone)-based copolymers and blends. J. Appl. Polym. Sci. 102:2 (2006), 1681–1687.
Cajot, S., Schol, D., Danhier, F., Preat, V., De Pauw, M.C.G., Jerome, C., In vitro investigations of smart drug delivery systems based on redox-sensitive cross-linked micelles. Macromol. Biosci. 13:12 (2013), 1661–1670.
Syed Alwi, S.S., Cavell, B.E., Donlevy, A., Packham, G., Differential induction of apoptosis in human breast cancer cell lines by phenethyl isothiocyanate, a glutathione depleting agent. Cell Stress Chaperones 17:5 (2012), 529–538.
Cheng, S.H., Tseng, Y.M., Wu, S.H., Tsai, S.M., Tsai, L.Y., Whey protein concentrate renders MDA-MB-231 cells sensitive to rapamycin by altering cellular redox state and activating GSK3beta/mTOR signaling. Sci. Rep., 7(1), 2017, 15976.
Lee, Eunkyung, Choi, Ahyoung, Jun, Yukyung, Kim, Namhee, Yook, Jong In, et al. Glutathione peroxidase-1 regulates adhesion and metastasis of triple-negative breast cancer cells via FAK signaling. Redox Biology, 29, 2020, 101391.
Jardim, B.V., Moschetta, M.G., Leonel, C., Gelaleti, G.B., Regiani, V.R., Ferreira, L.C., Lopes, J.R., Zuccari, D.A., Glutathione and glutathione peroxidase expression in breast cancer: an immunohistochemical and molecular study. Oncol. Rep. 30:3 (2013), 1119–1128.
Vargo-Gogola, T., Rosen, J.M., Modelling breast cancer: one size does not fit all. Nat. Rev. Cancer 7:9 (2007), 659–672.
Holliday, D.L., Speirs, V., Choosing the right cell line for breast cancer research. Breast Cancer Res., 13(4), 2011, 215.
Cheng, R., Meng, F.H., Deng, C., Klok, H.A., Zhong, Z.Y., Dual and multi-stimuli responsive polymeric nanoparticles for programmed site-specific drug delivery. Biomaterials 34:14 (2013), 3647–3657.
Rajak, A., Karan, C.K., Theato, P., Das, A., Supramolecularly cross-linked amphiphilic block copolymer assembly by the dipolar interaction of a merocyanine dye. Polym. Chem. U.K. 11:3 (2020), 607–754.
Zoetemelk, M., Rausch, M., Colin, D.J., Dormond, O., Nowak-Sliwinska, P., Short-term 3D culture systems of various complexity for treatment optimization of colorectal carcinoma. Sci. Rep., 9(1), 2019, 7103.
Li, L., Lu, Y., Optimizing a 3D culture system to study the interaction between epithelial breast cancer and its surrounding fibroblasts. J. Cancer 2 (2011), 458–466.
Mirbagheri, M., Adibnia, V., Hughes, B.R., Waldman, S.D., Banquy, X., Hwang, D.K., Advanced cell culture platforms: a growing quest for emulating natural tissues. Mater. Horiz. 6:1 (2019), 45–71.
Longati, Paola, Jia, Xiaohui, Eimer, Johannes, Wagman, Annika, Witt, Michael-Robin, 3D pancreatic carcinoma spheroids induce a matrix-rich, chemoresistant phenotype offering a better model for drug testing. BMC Cancer 13 (2013), 95–108.
