Hostname: page-component-77c89778f8-swr86 Total loading time: 0 Render date: 2024-07-24T16:01:17.009Z Has data issue: false hasContentIssue false

Sorafenib delivered by cancer cell membrane remodels tumor microenvironment to enhances the immunotherapy of mitoxantrone in breast cancer

Published online by Cambridge University Press:  18 November 2020

Jing Chen
Affiliation:
Department of Breast Surgery, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang Province310009, PR China Department of Radiation Oncology, Cancer Hospital of the University of Chinese Academy of Sciences (Zhejiang Cancer Hospital), Hangzhou, Zhejiang Province310022, PR China
Jian Huang*
Affiliation:
Department of Breast Surgery, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang Province310009, PR China Key Laboratory of Tumor Microenvironment and Immune Therapy of Zhejiang Province, Hangzhou, Zhejiang Province310009, PR China
*
a)Address all correspondence to this author. e-mail: jianhuang00@163.com
Get access

Abstract

The negative regulation effect of tumor microenvironment (TME) greatly compromised the efficacy of various cancer treatments, especially cancer immunotherapy. As a result, it is generally recognized that remodeling of TME along with the treatment is a promising way to realize satisfactory cancer therapy. Here, in our study, a drug delivery system (DDS) composed cancer cell membrane (CCM) vehicle loaded mitoxantrone (Mit) and sorafenib (Sfn) was proposed with the aim to combine TME regulation and chemotherapy-induced immunotherapy in one platform. Our results confirmed that after treating with this DDS, the Mit induced immunogenic cell death (ICD) could be augmented by Sfn-based TME regulation to realize effective cancer immunotherapy. The Sfn was shown to downregulate of the regulatory T cells (Treg) level while activating the effector T cells of TME. The synergetic TME regulation along with cancer immunotherapy might be a promising way for advanced cancer treatment.

Type
Article
Copyright
Copyright © The Author(s), 2020, published on behalf of Materials Research Society by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Couzin-Frankel, J.: Cancer Immunotherapy (American Association for the Advancement of Science, 2013), Vol. 342, Issue 6165, pp. 14321433.Google ScholarPubMed
Ribas, A. and Wolchok, J.D.: Cancer immunotherapy using checkpoint blockade. Science 359, 1350 (2018).CrossRefGoogle ScholarPubMed
Till, S.J., Francis, J.N., Nouri-Aria, K., and Durham, S.R.: Mechanisms of immunotherapy. J. Allergy Clin. Immunol. 113, 1025 (2004).CrossRefGoogle ScholarPubMed
Durham, S.R., Walker, S.M., Varga, E-M., Jacobson, M.R., O'Brien, F., Noble, W., Till, S.J., Hamid, Q.A., and Nouri-Aria, K.T.: Long-term clinical efficacy of grass-pollen immunotherapy. N. Engl. J. Med. 341, 468 (1999).CrossRefGoogle ScholarPubMed
Phuengkham, H., Ren, L., Shin, I.W., and Lim, Y.T.: Nanoengineered immune niches for reprogramming the immunosuppressive tumor microenvironment and enhancing cancer immunotherapy. Adv. Mater. 31, 1803322 (2019).CrossRefGoogle ScholarPubMed
Nakamura, K. and Smyth, M.J.: Targeting cancer-related inflammation in the era of immunotherapy. Immunol. Cell Biol. 95, 325 (2017).CrossRefGoogle ScholarPubMed
Li, Y., Liu, X., Pan, W., Li, N., and Tang, B.: Photothermal therapy-induced immunogenic cell death based on natural melanin nanoparticles against breast cancer. Chem. Commun. 56, 1389 (2020).CrossRefGoogle ScholarPubMed
Lim, S., Park, J., Shim, M.K., Um, W., Yoon, H.Y., Ryu, J.H., Lim, D-K., and Kim, K.: Recent advances and challenges of repurposing nanoparticle-based drug delivery systems to enhance cancer immunotherapy. Theranostics 9, 7906 (2019).CrossRefGoogle ScholarPubMed
Li, X., Wang, X., Qian, G., and Ito, A.: Synergistical chemotherapy and cancer immunotherapy using dual drug-delivering and immunopotentiating mesoporous silica. Appl. Mater. Today 16, 102 (2019).CrossRefGoogle Scholar
Golchin, S., Alimohammadi, R., Rostami Nejad, M., and Jalali, S.A.: Synergistic antitumor effect of anti-PD-L1 combined with oxaliplatin on a mouse tumor model. J. Cell. Physiol. 234, 19866 (2019).CrossRefGoogle ScholarPubMed
Huang, W-T., Chang, M-C., Chu, C-Y., Chang, C-C., Li, M-C., and Liu, D-M.: Self-assembled amphiphilic chitosan: A time-dependent nanostructural evolution and associated drug encapsulation/elution mechanism. Carbohydr. Polym. 215, 246 (2019).CrossRefGoogle ScholarPubMed
Saeed, M., Gao, J., Shi, Y., Lammers, T., and Yu, H.: Engineering nanoparticles to reprogram the tumor immune microenvironment for improved cancer immunotherapy. Theranostics 9, 7981 (2019).CrossRefGoogle ScholarPubMed
Dong, N., Shi, X., Wang, S., Gao, Y., Kuang, Z., Xie, Q., Li, Y., Deng, H., Wu, Y., and Li, M.: M2 macrophages mediate sorafenib resistance by secreting HGF in a feed-forward manner in hepatocellular carcinoma. Br. J. Cancer 121, 22 (2019).CrossRefGoogle Scholar
Hashemi Goradel, N., Najafi, M., Salehi, E., Farhood, B., and Mortezaee, K.: Cyclooxygenase-2 in cancer: A review. J. Cell. Physiol. 234, 5683 (2019).CrossRefGoogle ScholarPubMed
Wu, X., Luo, H., Shi, B., Di, S., Sun, R., Su, J., Liu, Y., Li, H., Jiang, H., and Li, Z.: Combined antitumor effects of sorafenib and GPC3-CAR T cells in mouse models of hepatocellular carcinoma. Mol. Ther. 27, 1483 (2019).CrossRefGoogle ScholarPubMed
Kermanizadeh, A., Powell, L.G., Stone, V., and Møller, P.: Nanodelivery systems and stabilized solid-drug nanoparticles for orally administered medicine: Current landscape. Int. J. Nanomed. 13, 7575 (2018).CrossRefGoogle ScholarPubMed
Li, X., Jia, X., and Niu, H.: Nanostructured lipid carriers co-delivering lapachone and doxorubicin for overcoming multidrug resistance in breast cancer therapy. Int. J. Nanomed. 13, 4107 (2018).CrossRefGoogle ScholarPubMed
Graham, K. and Unger, E.: Overcoming tumor hypoxia as a barrier to radiotherapy, chemotherapy and immunotherapy in cancer treatment. Int. J. Nanomed. 13, 6049 (2018).CrossRefGoogle ScholarPubMed
Zhou, B., Song, J., Wang, M., Wang, X., Wang, J., Howard, E.W., Zhou, F., Qu, J., and Chen, W.R.: BSA-bioinspired gold nanorods loaded with immunoadjuvant for the treatment of melanoma by combined photothermal therapy and immunotherapy. Nanoscale 10, 21640 (2018).CrossRefGoogle ScholarPubMed
Raik, S.V., Poshina, D.N., Lyalina, T.A., Polyakov, D.S., Vasilyev, V.B., Kritchenkov, A.S., and Skorik, Y.A.: N-[4-(N,N,N-trimethylammonium) benzyl] chitosan chloride: Synthesis, interaction with DNA and evaluation of transfection efficiency. Carbohydr. Polym. 181, 693 (2018).CrossRefGoogle ScholarPubMed
Wang, S., Liu, F., and Li, X.L.: Monitoring of “on-demand” drug release using dual tumor marker mediated DNA-capped versatile mesoporous silica nanoparticles. Chem. Commun. 53, 8755 (2017).CrossRefGoogle ScholarPubMed
Quarta, A., Amorín, M., Aldegunde, M.J., Blasi, L., Ragusa, A., Nitti, S., Pugliese, G., Gigli, G., Granja, J.R., and Pellegrino, T.: Novel synthesis of platinum complexes and their intracellular delivery to tumor cells by means of magnetic nanoparticles. Nanoscale 11, 23482 (2019).CrossRefGoogle ScholarPubMed
Jin, G., He, R., Liu, Q., Lin, M., Dong, Y., Li, K., Tang, B.Z., Liu, B., and Xu, F.: Near-infrared light-regulated cancer theranostic nanoplatform based on aggregation-induced emission luminogen encapsulated upconversion nanoparticles. Theranostics 9, 246 (2019).CrossRefGoogle ScholarPubMed
Yang, L., Gao, P., Huang, Y., Lu, X., Chang, Q., Pan, W., Li, N., and Tang, B.: Boosting the photodynamic therapy efficiency with a mitochondria-targeted nanophotosensitizer. Chin. Chem. Lett. 30, 1293 (2019).CrossRefGoogle Scholar
Cirri, M., Maestrini, L., Maestrelli, F., Mennini, N., Mura, P., Ghelardini, C., and Di Cesare Mannelli, L.: Design, characterization and in vivo evaluation of nanostructured lipid carriers (NLC) as a new drug delivery system for hydrochlorothiazide oral administration in pediatric therapy. Drug Delivery 25, 1910 (2018).CrossRefGoogle ScholarPubMed
He, H., Zhu, R., Sun, W., Cai, K., Chen, Y., and Yin, L.: Selective cancer treatment via photodynamic sensitization of hypoxia-responsive drug delivery. Nanoscale 10, 2856 (2018).CrossRefGoogle ScholarPubMed
Tang, Y., Li, Y., Li, S., Hu, H., Wu, Y., Xiao, C., Chu, Z., Li, Z., and Yang, X.: Transformable nanotherapeutics enabled by ICG: Towards enhanced tumor penetration under NIR light irradiation. Nanoscale 11, 6217 (2019).CrossRefGoogle ScholarPubMed
Liu, X., Sun, Y., Xu, S., Gao, X., Kong, F., Xu, K., and Tang, B.: Homotypic cell membrane-cloaked biomimetic nanocarrier for the targeted chemotherapy of hepatocellular carcinoma. Theranostics 9, 5828 (2019).CrossRefGoogle ScholarPubMed
Kawakami, Y., Eliyahu, S., Delgado, C.H., Robbins, P.F., Sakaguchi, K., Appella, E., Yannelli, J.R., Adema, G.J., Miki, T., and Rosenberg, S.A.: Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl. Acad. Sci. 91, 6458 (1994).CrossRefGoogle ScholarPubMed
Li, L., Yang, S., Song, L., Zeng, Y., He, T., Wang, N., Yu, C., Yin, T., Liu, L., and Wei, X.: An endogenous vaccine based on fluorophores and multivalent immunoadjuvants regulates tumor micro-environment for synergistic photothermal and immunotherapy. Theranostics 8, 860 (2018).CrossRefGoogle ScholarPubMed
Fang, J., Zhang, S., Xue, X., Zhu, X., Song, S., Wang, B., Jiang, L., Qin, M., Liang, H., and Gao, L.: Quercetin and doxorubicin co-delivery using mesoporous silica nanoparticles enhance the efficacy of gastric carcinoma chemotherapy. Int. J. Nanomedicine 13, 5113 (2018).CrossRefGoogle ScholarPubMed
Kang, S., Kang, K., Chae, A., Kim, Y-K., Jang, H., and Min, D-H.: Fucoidan-coated coral-like Pt nanoparticles for computed tomography-guided highly enhanced synergistic anticancer effect against drug-resistant breast cancer cells. Nanoscale 11, 15173 (2019).CrossRefGoogle ScholarPubMed
Li, Y., Du, Y., Liang, X., Sun, T., Xue, H., Tian, J., and Jin, Z.: EGFR-targeted liposomal nanohybrid cerasomes: Theranostic function and immune checkpoint inhibition in a mouse model of colorectal cancer. Nanoscale 10, 16738 (2018).CrossRefGoogle Scholar
Wang, X.Y., Zhang, L., Wang, J.Q., Liu, X., Lv, P., Zeng, J., and Liu, G.: Size-controlled biocompatible silver nanoplates for contrast-enhanced intravital photoacoustic mapping of tumor vasculature. J. Biomed. Nanotechnol. 14, 1448 (2018).CrossRefGoogle ScholarPubMed
Wang, Z., Liu, W., Shi, J., Chen, N., and Fan, C.: Nanoscale delivery systems for cancer immunotherapy. Mater. Horiz. 5, 344 (2018).CrossRefGoogle Scholar
Cao, L., Zhang, H., Zhou, Z., Xu, C., Shan, Y., Lin, Y., and Huang, Q.: Fluorophore-free luminescent double-shelled hollow mesoporous silica nanoparticles as pesticide delivery vehicles. Nanoscale 10, 20354 (2018).CrossRefGoogle ScholarPubMed
Chen, M., Song, F., Liu, Y., Tian, J., Liu, C., Li, R., and Zhang, Q.: A dual pH-sensitive liposomal system with charge-reversal and NO generation for overcoming multidrug resistance in cancer. Nanoscale 11, 3814 (2019).CrossRefGoogle ScholarPubMed
Nejabat, M., Mohammadi, M., Abnous, K., Taghdisi, S.M., Ramezani, M., and Alibolandi, M.: Fabrication of acetylated carboxymethylcellulose coated hollow mesoporous silica hybrid nanoparticles for nucleolin targeted delivery to colon adenocarcinoma. Carbohydr. Polym. 197, 157 (2018).CrossRefGoogle ScholarPubMed
Chen, Q., Chen, Y., Sun, Y., He, W., Han, X., Lu, E., and Sha, X.: Leukocyte–mimicking Pluronic–lipid nanovesicle hybrids inhibit the growth and metastasis of breast cancer. Nanoscale 11, 5377 (2019).CrossRefGoogle ScholarPubMed
Zhao, X., Liu, Y., Yu, Y., Huang, Q., Ji, W., Li, J., and Zhao, Y.: Hierarchically porous composite microparticles from microfluidics for controllable drug delivery. Nanoscale 10, 12595 (2018).CrossRefGoogle ScholarPubMed
Liang, B., Liu, X., Liu, Y., Kong, D., Liu, X., Zhong, R., and Ma, S.: Inhibition of autophagy sensitizes MDR-phenotype ovarian cancer SKVCR cells to chemotherapy. Biomed. Pharmacother. 82, 98 (2016).CrossRefGoogle ScholarPubMed
Abdolmohammadi Vahid, S., Ghaebi, M., Ahmadi, M., Nouri, M., Danaei, S., Aghebati-Maleki, L., Mousavi Ardehaie, R., Yousefi, B., Hakimi, P., and Hojjat-Farsangi, M.: Altered T-cell subpopulations in recurrent pregnancy loss patients with cellular immune abnormalities. J. Cell. Physiol. 234, 4924 (2019).CrossRefGoogle ScholarPubMed
Farhood, B., Najafi, M., and Mortezaee, K.: CD8+ cytotoxic T lymphocytes in cancer immunotherapy: A review. J. Cell. Physiol. 234, 8509 (2019).CrossRefGoogle ScholarPubMed
Wen, L., Liang, C., Chen, E., Chen, W., Liang, F., Zhi, X., Wei, T., Xue, F., Li, G., and Yang, Q.: Regulation of multi-drug resistance in hepatocellular carcinoma cells is TRPC6/calcium dependent. Sci. Rep. 6, 23269 (2016).CrossRefGoogle ScholarPubMed
Ni, J., Sun, Y., Song, J., Zhao, Y., Gao, Q., and Li, X.: Artificial cell-mediated photodynamic therapy enhanced anticancer efficacy through combination of tumor disruption and immune response stimulation. ACS Omega 4, 12727 (2019).CrossRefGoogle ScholarPubMed
Zhao, Z., Ji, M., Wang, Q., He, N., and Li, Y.: Ca2+ signaling modulation using cancer cell membrane coated chitosan nanoparticles to combat multidrug resistance of cancer. Carbohydr. Polym. 238, 116073 (2020).CrossRefGoogle ScholarPubMed
Zhang, J., Miao, Y., Ni, W., Xiao, H., and Zhang, J.: Cancer cell membrane coated silica nanoparticles loaded with ICG for tumour specific photothermal therapy of osteosarcoma. Artif. Cells Nanomed. Biotechnol. 47, 2298 (2019).CrossRefGoogle ScholarPubMed
Meng, L.X., Ren, Q., Meng, Q., Zheng, Y.X., He, M.L., Sun, S.Y., Ding, Z.J., Li, B.C., and Wang, H.Y.: Trastuzumab modified silica nanoparticles loaded with doxorubicin for targeted and synergic therapy of breast cancer. Artif. Cells Nanomed. Biotechnol. 46, S556 (2018).CrossRefGoogle ScholarPubMed
Lee, E-H., Lim, S-J., and Lee, M-K.: Chitosan-coated liposomes to stabilize and enhance transdermal delivery of indocyanine green for photodynamic therapy of melanoma. Carbohydr. Polym. 224, 115143 (2019).CrossRefGoogle ScholarPubMed
Chen, M.L., Yan, B.S., Lu, W.C., Chen, M.H., Yu, S.L., Yang, P.C., and Cheng, A.L.: Sorafenib relieves cell-intrinsic and cell-extrinsic inhibitions of effector T cells in tumor microenvironment to augment antitumor immunity. Int. J. Cancer 134, 319 (2014).CrossRefGoogle ScholarPubMed