Download PDF
CC BY 4.0 · Pharmaceutical Fronts 2024; 06(02): e101-e118
DOI: 10.1055/s-0044-1786681
Review Article

Advances in Tumor Targeting Biomimetic Drug Delivery Systems: A Promising Approach for Antitumor Therapy

Ziyi Mo
1   Key Laboratory of Drug-Targeting and Drug Delivery System of the Education Ministry and Sichuan Province, Sichuan Engineering Laboratory for Plant-Sourced Drug and Sichuan Research Center for Drug Precision Industrial Technology, West China School of Pharmacy, Med-X Center for Materials, Sichuan University, Chengdu, People's Republic of China
,
Jiao He
1   Key Laboratory of Drug-Targeting and Drug Delivery System of the Education Ministry and Sichuan Province, Sichuan Engineering Laboratory for Plant-Sourced Drug and Sichuan Research Center for Drug Precision Industrial Technology, West China School of Pharmacy, Med-X Center for Materials, Sichuan University, Chengdu, People's Republic of China
,
Man Li
1   Key Laboratory of Drug-Targeting and Drug Delivery System of the Education Ministry and Sichuan Province, Sichuan Engineering Laboratory for Plant-Sourced Drug and Sichuan Research Center for Drug Precision Industrial Technology, West China School of Pharmacy, Med-X Center for Materials, Sichuan University, Chengdu, People's Republic of China
,
Rong Guo
2   Department of Biochemistry and Molecular Biology, West China School of Basic Medical Sciences and Forensic Medicine, Sichuan University, Chengdu, People's Republic of China
,
Qin He
1   Key Laboratory of Drug-Targeting and Drug Delivery System of the Education Ministry and Sichuan Province, Sichuan Engineering Laboratory for Plant-Sourced Drug and Sichuan Research Center for Drug Precision Industrial Technology, West China School of Pharmacy, Med-X Center for Materials, Sichuan University, Chengdu, People's Republic of China
› Author Affiliations Funding The work was supported by the National Natural Science Foundation (Grant No. 82173771) and the Key Project of Applied Basic Research in Sichuan province (Grant No. 22YYJC1231).
› Further Information
   Permissions and Reprints

Abstract

Cancer is one of the most fatal diseases that attract numerous efforts and attention from researchers. Among plentiful therapeutic agents, chemotherapy is frequently used in treating virulent tumors, and its insistent administration is useful in the ablation of cancers; however, it also produces side effects. Biomimetic drug delivery systems (BDDSs) provide an alternative route for antitumor therapy. Their endogenous substances may be extracellular vesicles, living cells, cell membranes, etc., which optimize single-agent chemotherapy. They “upgrade” traditional drug delivery platforms by combining the original drug with itself, disguised as a Trojan Horse, to trick the immune system or tumor tissues to achieve higher targeting and lower immunogenicity. Herein, we review three BDDS strategies being used recently in antitumor drug development and their advances, aiming at providing general guidelines and opportunities in this field in the future.

Keywords

biomimetic drug delivery system - antitumor - nanoparticles - endogenous substances


Publication History

Received: 29 August 2023

Accepted: 07 April 2024

Article published online:
22 May 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Sung H, Ferlay J, Siegel RL. et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71 (03) 209-249
    Google Scholar
  • 2 Pusuluri A, Wu D, Mitragotri S. Immunological consequences of chemotherapy: single drugs, combination therapies and nanoparticle-based treatments. J Control Release 2019; 305: 130-154
    CrossrefPubMedGoogle Scholar
  • 3 Ma Q, Cao J, Gao Y. et al. Microfluidic-mediated nano-drug delivery systems: from fundamentals to fabrication for advanced therapeutic applications. Nanoscale 2020; 12 (29) 15512-15527
    CrossrefPubMedGoogle Scholar
  • 4 Ho YJ, Chiang YJ, Kang ST, Fan CH, Yeh CK. Camptothecin-loaded fusogenic nanodroplets as ultrasound theranostic agent in stem cell-mediated drug-delivery system. J Control Release 2018; 278: 100-109
    CrossrefPubMedGoogle Scholar
  • 5 Wu HH, Zhou Y, Tabata Y, Gao JQ. Mesenchymal stem cell-based drug delivery strategy: from cells to biomimetic. J Control Release 2019; 294: 102-113
    CrossrefPubMedGoogle Scholar
  • 6 Chen HY, Deng J, Wang Y, Wu CQ, Li X, Dai HW. Hybrid cell membrane-coated nanoparticles: a multifunctional biomimetic platform for cancer diagnosis and therapy. Acta Biomater 2020; 112: 1-13
    CrossrefPubMedGoogle Scholar
  • 7 Chi J, Ma Q, Shen Z. et al. Targeted nanocarriers based on iodinated-cyanine dyes as immunomodulators for synergistic phototherapy. Nanoscale 2020; 12 (20) 11008-11025
    CrossrefPubMedGoogle Scholar
  • 8 Guan YH, Wang N, Deng ZW, Chen XG, Liu Y. Exploiting autophagy-regulative nanomaterials for activation of dendritic cells enables reinforced cancer immunotherapy. Biomaterials 2022; 282: 121434
    CrossrefPubMedGoogle Scholar
  • 9 Bush LM, Healy CP, Javdan SB, Emmons JC, Deans TL. Biological cells as therapeutic delivery vehicles. Trends Pharmacol Sci 2021; 42 (02) 106-118
    CrossrefPubMedGoogle Scholar
  • 10 Elsharkasy OM, Nordin JZ, Hagey DW. et al. Extracellular vesicles as drug delivery systems: why and how?. Adv Drug Deliv Rev 2020; 159: 332-343
    CrossrefPubMedGoogle Scholar
  • 11 Herrmann IK, Wood MJA, Fuhrmann G. Extracellular vesicles as a next-generation drug delivery platform. Nat Nanotechnol 2021; 16 (07) 748-759
    CrossrefPubMedGoogle Scholar
  • 12 Liu T, Gao C, Gu D, Tang H. Cell-based carrier for targeted hitchhiking delivery. Drug Deliv Transl Res 2022; 12 (11) 2634-2648
    CrossrefPubMedGoogle Scholar
  • 13 Zhang X, Li N, Zhang S. et al. Emerging carrier-free nanosystems based on molecular self-assembly of pure drugs for cancer therapy. Med Res Rev 2020; 40 (05) 1754-1775
    CrossrefPubMedGoogle Scholar
  • 14 Ayer M, Klok HA. Cell-mediated delivery of synthetic nano- and microparticles. J Control Release 2017; 259: 92-104
    CrossrefPubMedGoogle Scholar
  • 15 Fang RH, Gao W, Zhang L. Targeting drugs to tumours using cell membrane-coated nanoparticles. Nat Rev Clin Oncol 2023; 20 (01) 33-48
    CrossrefPubMedGoogle Scholar
  • 16 Sun S, Yang Y, Gao Z. et al. endogenous stimuli-responsive autonomous separation of dual-targeting DNA guided missile from nanospacecraft for intelligent targeted cancer therapy. ACS Appl Mater Interfaces 2022; 14 (40) 45201-45216
    CrossrefPubMedGoogle Scholar
  • 17 Théry C, Witwer KW, Aikawa E. et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles 2018; 7 (01) 1535750
    CrossrefPubMedGoogle Scholar
  • 18 Zhang H, Lyden D. Asymmetric-flow field-flow fractionation technology for exomere and small extracellular vesicle separation and characterization. Nat Protoc 2019; 14 (04) 1027-1053
    CrossrefPubMedGoogle Scholar
  • 19 van der Meel R, Fens MH, Vader P, van Solinge WW, Eniola-Adefeso O, Schiffelers RM. Extracellular vesicles as drug delivery systems: lessons from the liposome field. J Control Release 2014; 195: 72-85
    CrossrefPubMedGoogle Scholar
  • 20 Piffoux M, Silva AKA, Wilhelm C, Gazeau F, Tareste D. Modification of extracellular vesicles by fusion with liposomes for the design of personalized biogenic drug delivery systems. ACS Nano 2018; 12 (07) 6830-6842
    CrossrefPubMedGoogle Scholar
  • 21 Schulz-Siegmund M, Aigner A. Nucleic acid delivery with extracellular vesicles. Adv Drug Deliv Rev 2021; 173: 89-111
    CrossrefPubMedGoogle Scholar
  • 22 Ou YH, Liang J, Czarny B. et al. Extracellular vesicle (EV) biohybrid systems for cancer therapy: recent advances and future perspectives. Semin Cancer Biol 2021; 74: 45-61
    CrossrefPubMedGoogle Scholar
  • 23 Richter M, Vader P, Fuhrmann G. Approaches to surface engineering of extracellular vesicles. Adv Drug Deliv Rev 2021; 173: 416-426
    CrossrefPubMedGoogle Scholar
  • 24 Sharma S, Masud MK, Kaneti YV. et al. Extracellular vesicle nanoarchitectonics for novel drug delivery applications. Small 2021; 17 (42) e2102220
    CrossrefPubMedGoogle Scholar
  • 25 Roerig J, Schulz-Siegmund M. Standardization approaches for extracellular vesicle loading with oligonucleotides and biologics. Small 2023; 19 (40) e2301763
    CrossrefPubMedGoogle Scholar
  • 26 Liu YR, Cheng YQ, Wang SB. et al. Therapeutic effects and perspective of stem cell extracellular vesicles in aging and cancer. J Cell Physiol 2021; 236 (07) 4783-4796
    CrossrefPubMedGoogle Scholar
  • 27 Lan T, Luo M, Wei X. Mesenchymal stem/stromal cells in cancer therapy. J Hematol Oncol 2021; 14 (01) 195
    CrossrefPubMedGoogle Scholar
  • 28 Keshtkar S, Azarpira N, Ghahremani MH. Mesenchymal stem cell-derived extracellular vesicles: novel frontiers in regenerative medicine. Stem Cell Res Ther 2018; 9 (01) 63
    CrossrefPubMedGoogle Scholar
  • 29 Hass R, Kasper C, Böhm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011; 9: 12
    CrossrefPubMedGoogle Scholar
  • 30 Rani S, Ryan AE, Griffin MD, Ritter T. Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther 2015; 23 (05) 812-823
    CrossrefPubMedGoogle Scholar
  • 31 Xu F, Fei Z, Dai H. et al. Mesenchymal stem cell-derived extracellular vesicles with high PD-L1 expression for autoimmune diseases treatment. Adv Mater 2022; 34 (01) e2106265
    CrossrefPubMedGoogle Scholar
  • 32 Lai RC, Yeo RW, Lim SK. Mesenchymal stem cell exosomes. Semin Cell Dev Biol 2015; 40: 82-88
    CrossrefPubMedGoogle Scholar
  • 33 Su C, Zhang J, Yarden Y, Fu L. The key roles of cancer stem cell-derived extracellular vesicles. Signal Transduct Target Ther 2021; 6 (01) 109
    CrossrefPubMedGoogle Scholar
  • 34 Sohrabi B, Dayeri B, Zahedi E. et al. Mesenchymal stem cell (MSC)-derived exosomes as novel vehicles for delivery of miRNAs in cancer therapy. Cancer Gene Ther 2022; 29 (8–9): 1105-1116
    CrossrefPubMedGoogle Scholar
  • 35 Sun Y, Liu G, Zhang K, Cao Q, Liu T, Li J. Mesenchymal stem cells-derived exosomes for drug delivery. Stem Cell Res Ther 2021; 12 (01) 561
    CrossrefPubMedGoogle Scholar
  • 36 Crivelli B, Chlapanidas T, Perteghella S. et al; Italian Mesenchymal Stem Cell Group (GISM). Mesenchymal stem/stromal cell extracellular vesicles: from active principle to next generation drug delivery system. J Control Release 2017; 262: 104-117
    CrossrefPubMedGoogle Scholar
  • 37 Xunian Z, Kalluri R. Biology and therapeutic potential of mesenchymal stem cell-derived exosomes. Cancer Sci 2020; 111 (09) 3100-3110
    CrossrefPubMedGoogle Scholar
  • 38 Jahangiri B, Khalaj-Kondori M, Asadollahi E, Purrafee Dizaj L, Sadeghizadeh M. MSC-Derived exosomes suppress colorectal cancer cell proliferation and metastasis via miR-100/mTOR/miR-143 pathway. Int J Pharm 2022; 627: 122214
    CrossrefPubMedGoogle Scholar
  • 39 Yao X, Mao Y, Wu D. et al. Exosomal circ_0030167 derived from BM-MSCs inhibits the invasion, migration, proliferation and stemness of pancreatic cancer cells by sponging miR-338-5p and targeting the Wif1/Wnt8/β-catenin axis. Cancer Lett 2021; 512: 38-50
    CrossrefPubMedGoogle Scholar
  • 40 Pascucci L, Coccè V, Bonomi A. et al. Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: a new approach for drug delivery. J Control Release 2014; 192: 262-270
    CrossrefPubMedGoogle Scholar
  • 41 Pinto A, Marangon I, Méreaux J. et al. Immune reprogramming precision photodynamic therapy of peritoneal metastasis by scalable stem-cell-derived extracellular vesicles. ACS Nano 2021; 15 (02) 3251-3263
    CrossrefPubMedGoogle Scholar
  • 42 Luo T, Liu Q, Tan A. et al. Mesenchymal stem cell-secreted exosome promotes chemoresistance in breast cancer via enhancing miR-21-5p-mediated S100A6 expression. Mol Ther Oncolytics 2020; 19: 283-293
    CrossrefPubMedGoogle Scholar
  • 43 Zhu S, Yang N, Wu J. et al. Tumor microenvironment-related dendritic cell deficiency: a target to enhance tumor immunotherapy. Pharmacol Res 2020; 159: 104980
    CrossrefPubMedGoogle Scholar
  • 44 Clark GJ, Silveira PA, Hogarth PM, Hart DNJ. The cell surface phenotype of human dendritic cells. Semin Cell Dev Biol 2019; 86: 3-14
    CrossrefPubMedGoogle Scholar
  • 45 Bol KF, Schreibelt G, Gerritsen WR, de Vries IJ, Figdor CG. Dendritic cell-based immunotherapy: state of the art and beyond. Clin Cancer Res 2016; 22 (08) 1897-1906
    CrossrefPubMedGoogle Scholar
  • 46 Macri C, Pang ES, Patton T, O'Keeffe M. Dendritic cell subsets. Semin Cell Dev Biol 2018; 84: 11-21
    CrossrefPubMedGoogle Scholar
  • 47 Worbs T, Hammerschmidt SI, Förster R. Dendritic cell migration in health and disease. Nat Rev Immunol 2017; 17 (01) 30-48
    CrossrefPubMedGoogle Scholar
  • 48 Li J, Li J, Peng Y, Du Y, Yang Z, Qi X. Dendritic cell derived exosomes loaded neoantigens for personalized cancer immunotherapies. J Control Release 2023; 353: 423-433
    CrossrefPubMedGoogle Scholar
  • 49 Näslund TI, Gehrmann U, Qazi KR, Karlsson MC, Gabrielsson S. Dendritic cell-derived exosomes need to activate both T and B cells to induce antitumor immunity. J Immunol 2013; 190 (06) 2712-2719
    CrossrefPubMedGoogle Scholar
  • 50 Xiong X, Ke X, Wang L. et al. Neoantigen-based cancer vaccination using chimeric RNA-loaded dendritic cell-derived extracellular vesicles. J Extracell Vesicles 2022; 11 (08) e12243
    CrossrefPubMedGoogle Scholar
  • 51 Esser J, Gehrmann U, D'Alexandri FL. et al. Exosomes from human macrophages and dendritic cells contain enzymes for leukotriene biosynthesis and promote granulocyte migration. J Allergy Clin Immunol 2010; 126 (05) 1032-1040 , 1040.e1–1040.e4
    CrossrefPubMedGoogle Scholar
  • 52 Pitt JM, Charrier M, Viaud S. et al. Dendritic cell-derived exosomes as immunotherapies in the fight against cancer. J Immunol 2014; 193 (03) 1006-1011
    CrossrefPubMedGoogle Scholar
  • 53 Fan M, Liu H, Yan H. et al. A CAR T-inspiring platform based on antibody-engineered exosomes from antigen-feeding dendritic cells for precise solid tumor therapy. Biomaterials 2022; 282: 121424
    CrossrefPubMedGoogle Scholar
  • 54 Zhu H, Wang K, Wang Z. et al. An efficient and safe MUC1-dendritic cell-derived exosome conjugate vaccine elicits potent cellular and humoral immunity and tumor inhibition in vivo . Acta Biomater 2022; 138: 491-504
    CrossrefPubMedGoogle Scholar
  • 55 Lu Z, Zuo B, Jing R. et al. Dendritic cell-derived exosomes elicit tumor regression in autochthonous hepatocellular carcinoma mouse models. J Hepatol 2017; 67 (04) 739-748
    CrossrefPubMedGoogle Scholar
  • 56 Viaud S, Terme M, Flament C. et al. Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: a role for NKG2D ligands and IL-15Ralpha. PLoS One 2009; 4 (03) e4942
    CrossrefPubMedGoogle Scholar
  • 57 Zitvogel L, Regnault A, Lozier A. et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 1998; 4 (05) 594-600
    CrossrefPubMedGoogle Scholar
  • 58 Damo M, Wilson DS, Simeoni E, Hubbell JA. TLR-3 stimulation improves anti-tumor immunity elicited by dendritic cell exosome-based vaccines in a murine model of melanoma. Sci Rep 2015; 5: 17622
    CrossrefPubMedGoogle Scholar
  • 59 Tian X, Shen H, Li Z, Wang T, Wang S. Tumor-derived exosomes, myeloid-derived suppressor cells, and tumor microenvironment. J Hematol Oncol 2019; 12 (01) 84
    CrossrefPubMedGoogle Scholar
  • 60 Jiang C, Zhang N, Hu X, Wang H. Tumor-associated exosomes promote lung cancer metastasis through multiple mechanisms. Mol Cancer 2021; 20 (01) 117
    CrossrefPubMedGoogle Scholar
  • 61 Naseri M, Bozorgmehr M, Zöller M, Ranaei Pirmardan E, Madjd Z. Tumor-derived exosomes: the next generation of promising cell-free vaccines in cancer immunotherapy. OncoImmunology 2020; 9 (01) 1779991
    CrossrefPubMedGoogle Scholar
  • 62 Mashouri L, Yousefi H, Aref AR, Ahadi AM, Molaei F, Alahari SK. Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol Cancer 2019; 18 (01) 75
    CrossrefPubMedGoogle Scholar
  • 63 Gao Y, Xu H, Li N. et al. Renal cancer-derived exosomes induce tumor immune tolerance by MDSCs-mediated antigen-specific immunosuppression. Cell Commun Signal 2020; 18 (01) 106
    CrossrefPubMedGoogle Scholar
  • 64 Ma Z, Wei K, Yang F. et al. Tumor-derived exosomal miR-3157-3p promotes angiogenesis, vascular permeability and metastasis by targeting TIMP/KLF2 in non-small cell lung cancer. Cell Death Dis 2021; 12 (09) 840
    CrossrefPubMedGoogle Scholar
  • 65 Guo X, Sui R, Piao H. Tumor-derived small extracellular vesicles: potential roles and mechanism in glioma. J Nanobiotechnology 2022; 20 (01) 383
    CrossrefPubMedGoogle Scholar
  • 66 Hoshino A, Costa-Silva B, Shen TL. et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015; 527 (7578) 329-335
    CrossrefPubMedGoogle Scholar
  • 67 Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science 2020; 367 (6478) eaau6977
    CrossrefPubMedGoogle Scholar
  • 68 Thakur A, Parra DC, Motallebnejad P, Brocchi M, Chen HJ. Exosomes: small vesicles with big roles in cancer, vaccine development, and therapeutics. Bioact Mater 2021; 10: 281-294
    PubMedGoogle Scholar
  • 69 Qiao L, Hu S, Huang K. et al. Tumor cell-derived exosomes home to their cells of origin and can be used as Trojan horses to deliver cancer drugs. Theranostics 2020; 10 (08) 3474-3487
    CrossrefPubMedGoogle Scholar
  • 70 Andre F, Schartz NE, Movassagh M. et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002; 360 (9329) 295-305
    CrossrefPubMedGoogle Scholar
  • 71 Taghikhani A, Hassan ZM, Ebrahimi M, Moazzeni SM. microRNA modified tumor-derived exosomes as novel tools for maturation of dendritic cells. J Cell Physiol 2019; 234 (06) 9417-9427
    CrossrefPubMedGoogle Scholar
  • 72 Gong H, Zhang Q, Komarla A. et al. Nanomaterial biointerfacing via mitochondrial membrane coating for targeted detoxification and molecular detection. Nano Lett 2021; 21 (06) 2603-2609
    CrossrefPubMedGoogle Scholar
  • 73 Zeng Y, Li S, Zhang S, Wang L, Yuan H, Hu F. Cell membrane coated-nanoparticles for cancer immunotherapy. Acta Pharm Sin B 2022; 12 (08) 3233-3254
    CrossrefPubMedGoogle Scholar
  • 74 Zhen X, Cheng P, Pu K. Recent advances in cell membrane-camouflaged nanoparticles for cancer phototherapy. Small 2019; 15 (01) e1804105
    CrossrefPubMedGoogle Scholar
  • 75 Dash P, Piras AM, Dash M. Cell membrane coated nanocarriers - an efficient biomimetic platform for targeted therapy. J Control Release 2020; 327: 546-570
    CrossrefPubMedGoogle Scholar
  • 76 Liu L, Pan D, Chen S. et al. Systematic design of cell membrane coating to improve tumor targeting of nanoparticles. Nat Commun 2022; 13 (01) 6181
    CrossrefPubMedGoogle Scholar
  • 77 Luk BT, Zhang L. Cell membrane-camouflaged nanoparticles for drug delivery. J Control Release 2015; 220 (Pt B): 600-607
    CrossrefPubMedGoogle Scholar
  • 78 Wang Y, Chen X, He D, Zhou Y, Qin L. Surface-modified nanoerythrocyte loading DOX for targeted liver cancer chemotherapy. Mol Pharm 2018; 15 (12) 5728-5740
    CrossrefPubMedGoogle Scholar
  • 79 Fu S, Liang M, Wang Y. et al. Dual-modified novel biomimetic nanocarriers improve targeting and therapeutic efficacy in glioma. ACS Appl Mater Interfaces 2019; 11 (02) 1841-1854
    CrossrefPubMedGoogle Scholar
  • 80 Tao C, Nie X, Zhu W, Iqbal J, Xu C, Wang DA. Autologous cell membrane coatings on tissue engineering xenografts for suppression and alleviation of acute host immune responses. Biomaterials 2020; 258: 120310
    CrossrefPubMedGoogle Scholar
  • 81 Han X, Wang C, Liu Z. Red blood cells as smart delivery systems. Bioconjug Chem 2018; 29 (04) 852-860
    CrossrefPubMedGoogle Scholar
  • 82 Peng S, Ouyang B, Men Y. et al. Biodegradable zwitterionic polymer membrane coating endowing nanoparticles with ultra-long circulation and enhanced tumor photothermal therapy. Biomaterials 2020; 231: 119680
    CrossrefPubMedGoogle Scholar
  • 83 Ye S, Wang F, Fan Z. et al. Light/pH-triggered biomimetic red blood cell membranes camouflaged small molecular drug assemblies for imaging-guided combinational chemo-photothermal therapy. ACS Appl Mater Interfaces 2019; 11 (17) 15262-15275
    CrossrefPubMedGoogle Scholar
  • 84 Zhang Y, Xia Q, Wu T. et al. A novel multi-functionalized multicellular nanodelivery system for non-small cell lung cancer photochemotherapy. J Nanobiotechnology 2021; 19 (01) 245
    CrossrefPubMedGoogle Scholar
  • 85 Xie H, Li W, Liu H. et al. Erythrocyte membrane-coated invisible acoustic-sensitive nanoparticle for inducing tumor thrombotic infarction by precisely damaging tumor vascular endothelium. Small 2022; 18 (30) e2201933
    CrossrefPubMedGoogle Scholar
  • 86 Wang Y, Ji X, Ruan M. et al. Worm-like biomimetic nanoerythrocyte carrying siRNA for melanoma gene therapy. Small 2018; 14 (47) e1803002
    CrossrefPubMedGoogle Scholar
  • 87 Zhang Z, Qian H, Huang J. et al. Anti-EGFR-iRGD recombinant protein modified biomimetic nanoparticles loaded with gambogic acid to enhance targeting and antitumor ability in colorectal cancer treatment. Int J Nanomedicine 2018; 13: 4961-4975
    CrossrefPubMedGoogle Scholar
  • 88 Miao Y, Yang Y, Guo L. et al. Cell membrane-camouflaged nanocarriers with biomimetic deformability of erythrocytes for ultralong circulation and enhanced cancer therapy. ACS Nano 2022; 16 (04) 6527-6540
    CrossrefPubMedGoogle Scholar
  • 89 Guo H, Zhang W, Wang L, Shao Z, Huang X. Biomimetic cell membrane-coated glucose/oxygen-exhausting nanoreactor for remodeling tumor microenvironment in targeted hypoxic tumor therapy. Biomaterials 2022; 290: 121821
    CrossrefPubMedGoogle Scholar
  • 90 Pan WL, Tan Y, Meng W. et al. Microenvironment-driven sequential ferroptosis, photodynamic therapy, and chemotherapy for targeted breast cancer therapy by a cancer-cell-membrane-coated nanoscale metal-organic framework. Biomaterials 2022; 283: 121449
    CrossrefPubMedGoogle Scholar
  • 91 Fang Z, Zhang M, Kang R, Cui M, Song M, Liu K. A cancer cell membrane coated nanoparticles-based gene delivery system for enhancing cancer therapy. Int J Pharm 2022; 629: 122415
    CrossrefPubMedGoogle Scholar
  • 92 Gan J, Du G, He C. et al. Tumor cell membrane enveloped aluminum phosphate nanoparticles for enhanced cancer vaccination. J Control Release 2020; 326: 297-309
    CrossrefPubMedGoogle Scholar
  • 93 Jin J, Krishnamachary B, Barnett JD. et al. Human cancer cell membrane-coated biomimetic nanoparticles reduce fibroblast-mediated invasion and metastasis and induce T-cells. ACS Appl Mater Interfaces 2019; 11 (08) 7850-7861
    CrossrefPubMedGoogle Scholar
  • 94 Wang Z, Zhang M, Chi S, Zhu M, Wang C, Liu Z. Brain tumor cell membrane-coated lanthanide-doped nanoparticles for NIR-IIb luminescence imaging and surgical navigation of glioma. Adv Healthc Mater 2022; 11 (16) e2200521
    CrossrefPubMedGoogle Scholar
  • 95 Chen M, Cui Y, Hao W. et al. Ligand-modified homologous targeted cancer cell membrane biomimetic nanostructured lipid carriers for glioma therapy. Drug Deliv 2021; 28 (01) 2241-2255
    CrossrefPubMedGoogle Scholar
  • 96 Zheng B, Liu Z, Wang H. et al. R11 modified tumor cell membrane nanovesicle-camouflaged nanoparticles with enhanced targeting and mucus-penetrating efficiency for intravesical chemotherapy for bladder cancer. J Control Release 2022; 351: 834-846
    CrossrefPubMedGoogle Scholar
  • 97 Mohale S, Kunde SS, Wairkar S. Biomimetic fabrication of nanotherapeutics by leukocyte membrane cloaking for targeted therapy. Colloids Surf B Biointerfaces 2022; 219: 112803
    CrossrefPubMedGoogle Scholar
  • 98 Wang D, Wang S, Zhou Z. et al. White blood cell membrane-coated nanoparticles: recent development and medical applications. Adv Healthc Mater 2022; 11 (07) e2101349
    CrossrefPubMedGoogle Scholar
  • 99 Zhou X, Luo B, Kang K. et al. Leukocyte-repelling biomimetic immunomagnetic nanoplatform for high-performance circulating tumor cells isolation. Small 2019; 15 (17) e1900558
    CrossrefPubMedGoogle Scholar
  • 100 Xia Y, Rao L, Yao H, Wang Z, Ning P, Chen X. Engineering macrophages for cancer immunotherapy and drug delivery. Adv Mater 2020; 32 (40) e2002054
    CrossrefPubMedGoogle Scholar
  • 101 Chen C, Song M, Du Y. et al. Tumor-associated-macrophage-membrane-coated nanoparticles for improved photodynamic immunotherapy. Nano Lett 2021; 21 (13) 5522-5531
    CrossrefPubMedGoogle Scholar
  • 102 Li J, Wu Y, Wang J. et al. Macrophage membrane-coated nano-gemcitabine promotes lymphocyte infiltration and synergizes antiPD-L1 to restore the tumoricidal function. ACS Nano 2023; 17 (01) 322-336
    CrossrefPubMedGoogle Scholar
  • 103 Wang W, Wu F, Mohammadniaei M. et al. Genetically edited T-cell membrane coated AIEgen nanoparticles effectively prevents glioblastoma recurrence. Biomaterials 2023; 293: 121981
    CrossrefPubMedGoogle Scholar
  • 104 Kang M, Hong J, Jung M. et al. T-Cell-mimicking nanoparticles for cancer immunotherapy. Adv Mater 2020; 32 (39) e2003368
    CrossrefPubMedGoogle Scholar
  • 105 Hao W, Cui Y, Fan Y. et al. Hybrid membrane-coated nanosuspensions for multi-modal anti-glioma therapy via drug and antigen delivery. J Nanobiotechnology 2021; 19 (01) 378
    CrossrefPubMedGoogle Scholar
  • 106 Wu L, Li Q, Deng J. et al. Platelet-tumor cell hybrid membrane-camouflaged nanoparticles for enhancing therapy efficacy in glioma. Int J Nanomedicine 2021; 16: 8433-8446
    CrossrefPubMedGoogle Scholar
  • 107 Zhao Y, Li A, Jiang L, Gu Y, Liu J. Hybrid membrane-coated biomimetic nanoparticles (HM@BNPs): a multifunctional nanomaterial for biomedical applications. Biomacromolecules 2021; 22 (08) 3149-3167
    CrossrefPubMedGoogle Scholar
  • 108 Liao Y, Zhang Y, Blum NT, Lin J, Huang P. Biomimetic hybrid membrane-based nanoplatforms: synthesis, properties and biomedical applications. Nanoscale Horiz 2020; 5 (09) 1293-1302
    CrossrefPubMedGoogle Scholar
  • 109 Shen T, Yang S, Qu X. et al. A bionic “Trojan horse”-like gene delivery system hybridized with tumor and macrophage cell membrane for cancer therapy. J Control Release 2023; 358: 204-218
    CrossrefPubMedGoogle Scholar
  • 110 Ma W, Yang Y, Zhu J. et al. Biomimetic nanoerythrosome-coated aptamer-DNA tetrahedron/maytansine conjugates: pH-responsive and targeted cytotoxicity for HER2-positive breast cancer. Adv Mater 2022; 34 (46) e2109609
    CrossrefPubMedGoogle Scholar
  • 111 Zhang W, Gong C, Chen Z, Li M, Li Y, Gao J. Tumor microenvironment-activated cancer cell membrane-liposome hybrid nanoparticle-mediated synergistic metabolic therapy and chemotherapy for non-small cell lung cancer. J Nanobiotechnology 2021; 19 (01) 339
    CrossrefPubMedGoogle Scholar
  • 112 Chen H, Deng J, Yao X. et al. Bone-targeted erythrocyte-cancer hybrid membrane-camouflaged nanoparticles for enhancing photothermal and hypoxia-activated chemotherapy of bone invasion by OSCC. J Nanobiotechnology 2021; 19 (01) 342
    CrossrefPubMedGoogle Scholar
  • 113 Zang S, Huang K, Li J. et al. Metabolic reprogramming by dual-targeting biomimetic nanoparticles for enhanced tumor chemo-immunotherapy. Acta Biomater 2022; 148: 181-193
    CrossrefPubMedGoogle Scholar
  • 114 Nikfar M, Razizadeh M, Paul R, Muzykantov V, Liu Y. A numerical study on drug delivery via multiscale synergy of cellular hitchhiking onto red blood cells. Nanoscale 2021; 13 (41) 17359-17372
    CrossrefPubMedGoogle Scholar
  • 115 Anselmo AC, Gupta V, Zern BJ. et al. Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells. ACS Nano 2013; 7 (12) 11129-11137
    CrossrefPubMedGoogle Scholar
  • 116 Su Y, Xie Z, Kim GB, Dong C, Yang J. Design strategies and applications of circulating cell-mediated drug delivery systems. ACS Biomater Sci Eng 2015; 1 (04) 201-217
    CrossrefPubMedGoogle Scholar
  • 117 Yang L, Yang Y, Chen Y, Xu Y, Peng J. Cell-based drug delivery systems and their in vivo fate. Adv Drug Deliv Rev 2022; 187: 114394
    CrossrefPubMedGoogle Scholar
  • 118 Anselmo AC, Mitragotri S. Cell-mediated delivery of nanoparticles: taking advantage of circulatory cells to target nanoparticles. J Control Release 2014; 190: 531-541
    CrossrefPubMedGoogle Scholar
  • 119 Villa CH, Cines DB, Siegel DL, Muzykantov V. Erythrocytes as carriers for drug delivery in blood transfusion and beyond. Transfus Med Rev 2017; 31 (01) 26-35
    CrossrefPubMedGoogle Scholar
  • 120 Mukthavaram R, Shi G, Kesari S, Simberg D. Targeting and depletion of circulating leukocytes and cancer cells by lipophilic antibody-modified erythrocytes. J Control Release 2014; 183: 146-153
    CrossrefPubMedGoogle Scholar
  • 121 Li Y, Raza F, Liu Y. et al. Clinical progress and advanced research of red blood cells based drug delivery system. Biomaterials 2021; 279: 121202
    CrossrefPubMedGoogle Scholar
  • 122 Parodi A, Molinaro R, Sushnitha M. et al. Bio-inspired engineering of cell- and virus-like nanoparticles for drug delivery. Biomaterials 2017; 147: 155-168
    CrossrefPubMedGoogle Scholar
  • 123 Brenner JS, Pan DC, Myerson JW. et al. Red blood cell-hitchhiking boosts delivery of nanocarriers to chosen organs by orders of magnitude. Nat Commun 2018; 9 (01) 2684
    CrossrefPubMedGoogle Scholar
  • 124 Wang S, Ma S, Li R. et al. Probing the interaction between supercarrier RBC membrane and nanoparticles for optimal drug delivery. J Mol Biol 2023; 435 (01) 167539
    CrossrefPubMedGoogle Scholar
  • 125 Sun D, Chen J, Wang Y. et al. Advances in refunctionalization of erythrocyte-based nanomedicine for enhancing cancer-targeted drug delivery. Theranostics 2019; 9 (23) 6885-6900
    CrossrefPubMedGoogle Scholar
  • 126 Wang P, Wang X, Luo Q. et al. Fabrication of red blood cell-based multimodal theranostic probes for second near-infrared window fluorescence imaging-guided tumor surgery and photodynamic therapy. Theranostics 2019; 9 (02) 369-380
    CrossrefPubMedGoogle Scholar
  • 127 Ferguson LT, Hood ED, Shuvaeva T. et al. Dual affinity to RBCs and target cells (DART) enhances both organ- and cell type-targeting of intravascular nanocarriers. ACS Nano 2022; 16 (03) 4666-4683
    CrossrefPubMedGoogle Scholar
  • 128 Yan M, Jurasz P. The role of platelets in the tumor microenvironment: from solid tumors to leukemia. Biochim Biophys Acta 2016; 1863 (03) 392-400
    CrossrefPubMedGoogle Scholar
  • 129 Xu XR, Yousef GM, Ni H. Cancer and platelet crosstalk: opportunities and challenges for aspirin and other antiplatelet agents. Blood 2018; 131 (16) 1777-1789
    CrossrefPubMedGoogle Scholar
  • 130 Liu Y, Zhang Y, Ding Y, Zhuang R. Platelet-mediated tumor metastasis mechanism and the role of cell adhesion molecules. Crit Rev Oncol Hematol 2021; 167: 103502
    CrossrefPubMedGoogle Scholar
  • 131 Roweth HG, Battinelli EM. Lessons to learn from tumor-educated platelets. Blood 2021; 137 (23) 3174-3180
    CrossrefPubMedGoogle Scholar
  • 132 Morris K, Schnoor B, Papa AL. Platelet cancer cell interplay as a new therapeutic target. Biochim Biophys Acta Rev Cancer 2022; 1877 (05) 188770
    CrossrefPubMedGoogle Scholar
  • 133 Geranpayehvaghei M, Dabirmanesh B, Khaledi M. et al. Cancer-associated-platelet-inspired nanomedicines for cancer therapy. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2021; 13 (05) e1702
    CrossrefPubMedGoogle Scholar
  • 134 Cacic D, Hervig T, Reikvam H. Platelets for advanced drug delivery in cancer. Expert Opin Drug Deliv 2023; 20 (05) 673-688
    CrossrefPubMedGoogle Scholar
  • 135 Li S, Li L, Lin X, Chen C, Luo C, Huang Y. Targeted inhibition of tumor inflammation and tumor-platelet crosstalk by nanoparticle-mediated drug delivery mitigates cancer metastasis. ACS Nano 2022; 16 (01) 50-67
    CrossrefPubMedGoogle Scholar
  • 136 Fan X, Wang K, Lu Q. et al. Surface-anchored tumor microenvironment-responsive protein nanogel-platelet system for cytosolic delivery of therapeutic protein in the post-surgical cancer treatment. Acta Biomater 2022; 154: 412-423
    CrossrefPubMedGoogle Scholar
  • 137 Zhang Y, Zhu X, Chen X. et al. Activated platelets-targeting micelles with controlled drug release for effective treatment of primary and metastatic triple negative breast cancer. Adv Funct Mater 2019; 29 (13) 1806620
    CrossrefGoogle Scholar
  • 138 Hu Q, Sun W, Wang J. et al. Conjugation of haematopoietic stem cells and platelets decorated with anti-PD-1 antibodies augments anti-leukaemia efficacy. Nat Biomed Eng 2018; 2 (11) 831-840
    CrossrefPubMedGoogle Scholar
  • 139 Li Z, Ding Y, Liu J. et al. Depletion of tumor associated macrophages enhances local and systemic platelet-mediated anti-PD-1 delivery for post-surgery tumor recurrence treatment. Nat Commun 2022; 13 (01) 1845
    CrossrefPubMedGoogle Scholar
  • 140 Gajewski TF, Schreiber H, Fu YX. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 2013; 14 (10) 1014-1022
    CrossrefPubMedGoogle Scholar
  • 141 Mitchell MJ, King MR. Leukocytes as carriers for targeted cancer drug delivery. Expert Opin Drug Deliv 2015; 12 (03) 375-392
    CrossrefPubMedGoogle Scholar
  • 142 Dong X, Chu D, Wang Z. Leukocyte-mediated delivery of nanotherapeutics in inflammatory and tumor sites. Theranostics 2017; 7 (03) 751-763
    CrossrefPubMedGoogle Scholar
  • 143 Yang L, Zhang Y, Zhang Y. et al. Live macrophage-delivered doxorubicin-loaded liposomes effectively treat triple-negative breast cancer. ACS Nano 2022; 16 (06) 9799-9809
    CrossrefPubMedGoogle Scholar
  • 144 Ye B, Zhao B, Wang K. et al. Neutrophils mediated multistage nanoparticle delivery for prompting tumor photothermal therapy. J Nanobiotechnology 2020; 18 (01) 138
    CrossrefPubMedGoogle Scholar
  • 145 Hosseinalizadeh H, Mahmoodpour M, Razaghi Bahabadi Z, Hamblin MR, Mirzaei H. Neutrophil mediated drug delivery for targeted glioblastoma therapy: a comprehensive review. Biomed Pharmacother 2022; 156: 113841
    CrossrefPubMedGoogle Scholar
  • 146 Wu Y, Han X, Zheng R. et al. Neutrophil mediated postoperative photoimmunotherapy against melanoma skin cancer. Nanoscale 2021; 13 (35) 14825-14836
    CrossrefPubMedGoogle Scholar
  • 147 Ren K, He J, Qiu Y. et al. A neutrophil-mediated carrier regulates tumor stemness by inhibiting autophagy to prevent postoperative triple-negative breast cancer recurrence and metastasis. Acta Biomater 2022; 145: 185-199
    CrossrefPubMedGoogle Scholar
  • 148 Luo Z, Lu Y, Shi Y. et al. Neutrophil hitchhiking for drug delivery to the bone marrow. Nat Nanotechnol 2023; 18 (06) 647-656
    CrossrefPubMedGoogle Scholar
  • 149 Chu D, Dong X, Zhao Q, Gu J, Wang Z. Photosensitization priming of tumor microenvironments improves delivery of nanotherapeutics via neutrophil infiltration. Adv Mater 2017; 29 (27) 10 .1002/adma.201701021
    Google Scholar
  • 150 Jones RB, Mueller S, Kumari S. et al. Antigen recognition-triggered drug delivery mediated by nanocapsule-functionalized cytotoxic T-cells. Biomaterials 2017; 117: 44-53
    CrossrefPubMedGoogle Scholar
  • 151 Wang X, Zhang Q, Zhou J. et al. T cell-mediated targeted delivery of tadalafil regulates immunosuppression and polyamine metabolism to overcome immune checkpoint blockade resistance in hepatocellular carcinoma. J Immunother Cancer 2023; 11 (02) e006493
    CrossrefPubMedGoogle Scholar
  • 152 Niu W, Xiao Q, Wang X. et al. A biomimetic drug delivery system by integrating grapefruit extracellular vesicles and doxorubicin-loaded heparin-based nanoparticles for glioma therapy. Nano Lett 2021; 21 (03) 1484-1492
    CrossrefPubMedGoogle Scholar
  • 153 Qiao Z, Zhang K, Liu J. et al. Biomimetic electrodynamic nanoparticles comprising ginger-derived extracellular vesicles for synergistic anti-infective therapy. Nat Commun 2022; 13 (01) 7164
    CrossrefPubMedGoogle Scholar
  • 154 Han X, Bi L, Wu Y. et al. Genetically engineered exosomes for targetedly preventing premetastatic niche formation and suppressing postoperative melanoma lung metastasis. Nano Today 2022; 46: 101597
    CrossrefGoogle Scholar
  • 155 Taieb J, Chaput N, Schartz N. et al. Chemoimmunotherapy of tumors: cyclophosphamide synergizes with exosome based vaccines. J Immunol 2006; 176 (05) 2722-2729
    CrossrefPubMedGoogle Scholar
  • 156 Huang L, Rong Y, Tang X. et al. Engineered exosomes as an in situ DC-primed vaccine to boost antitumor immunity in breast cancer. Mol Cancer 2022; 21 (01) 45
    CrossrefPubMedGoogle Scholar
  • 157 Huang C, Liu Z, Chen M. et al. Tumor-derived biomimetic nanozyme with immune evasion ability for synergistically enhanced low dose radiotherapy. J Nanobiotechnology 2021; 19 (01) 457
    CrossrefPubMedGoogle Scholar
  • 158 Chen K, Wang Y, Liang H. et al. Intrinsic Biotaxi solution based on blood cell membrane cloaking enables fullerenol thrombolysis in vivo . ACS Appl Mater Interfaces 2020; 12 (13) 14958-14970
    CrossrefPubMedGoogle Scholar
  • 159 Wu X, Zhang X, Feng W. et al. A targeted erythrocyte membrane-encapsulated drug-delivery system with anti-osteosarcoma and anti-osteolytic effects. ACS Appl Mater Interfaces 2021; 13 (24) 27920-27933
    CrossrefPubMedGoogle Scholar
  • 160 Wu Y, Zhu R, Zhou M. et al. Homologous cancer cell membrane-camouflaged nanoparticles target drug delivery and enhance the chemotherapy efficacy of hepatocellular carcinoma. Cancer Lett 2023; 558: 216106
    CrossrefPubMedGoogle Scholar
  • 161 Xie X, Hu X, Li Q. et al. Unraveling cell-type-specific targeted delivery of membrane-camouflaged nanoparticles with plasmonic imaging. Nano Lett 2020; 20 (07) 5228-5235
    CrossrefPubMedGoogle Scholar
  • 162 Li Q, Su R, Bao X. et al. Glycyrrhetinic acid nanoparticles combined with ferrotherapy for improved cancer immunotherapy. Acta Biomater 2022; 144: 109-120
    CrossrefPubMedGoogle Scholar
  • 163 Jun Y, Tang Z, Luo C. et al. Leukocyte-mediated combined targeted chemo and gene therapy for esophageal cancer. ACS Appl Mater Interfaces 2020; 12 (42) 47330-47341
    CrossrefPubMedGoogle Scholar