Membrane-coated nanoparticles as a biomimetic targeted delivery system for tumour therapy
Drug therapy towards tumours often causes adverse effects because of their non-specific nature. Membrane-coated technology and membrane-coated nanoparticles provide an advanced and promising platform of targeted and safe delivery. By camouflaging the nanoparticles with natural derived or artificially modified cell membranes, the nano-payloads are bestowed with properties from cell membranes such as longer circulation, tumour or inflammation-targeting, immune stimulation, augmenting the performance of traditional therapeutics. In this review, we review the development of membrane coating technology, and summarise the technical details, physicochemical properties, and research status of membrane-coated nanoparticles from different sources in tumour treatment. Finally, we also look forward to the prospects and challenges of transforming membrane coating technology from experiment into clinical use. Taken together, membrane-coated nanoparticles are bound to become one of the most potential anti-tumour strategies in the future.
Below is the content of the Citations in the paper which has been de-formatted, however, the content stays consistent with the original.
1. Sugahara, K. N.; Teesalu, T.; Karmali, P. P.; Kotamraju, V. R.; Agemy, L.; Greenwald, D. R.; Ruoslahti, E. Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science. 2010, 328, 1031-1035.
2. Wei, G.; Wang, Y.; Yang, G.; Wang, Y.; Ju, R. Recent progress in nanomedicine for enhanced cancer chemotherapy. Theranostics. 2021, 11, 6370-6392.
3. Ward, R. A.; Fawell, S.; Floc’h, N.; Flemington, V.; McKerrecher, D.; Smith, P. D. Challenges and opportunities in cancer drug resistance. Chem Rev. 2021, 121, 3297-3351.
4. Wang, M.; Thanou, M. Targeting nanoparticles to cancer. Pharmacol Res. 2010, 62, 90-99.
5. Seyyednia, E.; Oroojalian, F.; Baradaran, B.; Mojarrad, J. S.; Mokhtarzadeh, A.; Valizadeh, H. Nanoparticles modified with vasculature-homing peptides for targeted cancer therapy and angiogenesis imaging. J Control Release. 2021, 338, 367-393.
6. Tian, H.; Zhang, T.; Qin, S.; Huang, Z.; Zhou, L.; Shi, J.; Nice, E. C.; Xie, N.; Huang, C.; Shen, Z. Enhancing the therapeutic efficacy of nanoparticles for cancer treatment using versatile targeted strategies. J Hematol Oncol. 2022, 15, 132.
7. Fang, R. H.; Kroll, A. V.; Gao, W.; Zhang, L. Cell membrane coating nanotechnology. Adv Mater. 2018, 30, e1706759.
8. Liu, Y.; Luo, J.; Chen, X.; Liu, W.; Chen, T. Cell membrane coating technology: a promising strategy for biomedical applications. Nanomicro Lett. 2019, 11, 100.
9. Liu, L.; Pan, D.; Chen, S.; Martikainen, M. V.; Kårlund, A.; Ke, J.; Pulkkinen, H.; Ruhanen, H.; Roponen, M.; Käkelä, R.; Xu, W.; Wang, J.; Lehto, V. P. Systematic design of cell membrane coating to improve tumor targeting of nanoparticles. Nat Commun. 2022, 13, 6181.
10. Suk, J. S.; Xu, Q.; Kim, N.; Hanes, J.; Ensign, L. M. PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Adv Drug Deliv Rev. 2016, 99, 28-51.
11. Estapé Senti, M.; de Jongh, C. A.; Dijkxhoorn, K.; Verhoef, J. J. F.; Szebeni, J.; Storm, G.; Hack, C. E.; Schiffelers, R. M.; Fens, M. H.; Boross, P. Anti-PEG antibodies compromise the integrity of PEGylated lipid-based nanoparticles via complement. J Control Release. 2022, 341, 475-486.
12. Gautam, M.; Jozic, A.; Su, G. L.; Herrera-Barrera, M.; Curtis, A.; Arrizabalaga, S.; Tschetter, W.; Ryals, R. C.; Sahay, G. Lipid nanoparticles with PEG-variant surface modifications mediate genome editing in the mouse retina. Nat Commun. 2023, 14, 6468.
13. Hu, C. M.; Zhang, L.; Aryal, S.; Cheung, C.; Fang, R. H.; Zhang, L. Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform. Proc Natl Acad Sci U S A. 2011, 108, 10980-10985.
14. Xia, Q.; Zhang, Y.; Li, Z.; Hou, X.; Feng, N. Red blood cell membrane-camouflaged nanoparticles: a novel drug delivery system for antitumor application. Acta Pharm Sin B. 2019, 9, 675-689.
15. Hu, C. M.; Fang, R. H.; Zhang, L. Erythrocyte-inspired delivery systems. Adv Healthc Mater. 2012, 1, 537-547.
16. Fang, R. H.; Gao, W.; Zhang, L. Targeting drugs to tumours using cell membrane-coated nanoparticles. Nat Rev Clin Oncol. 2023, 20, 33-48.
17. Fang, R. H.; Jiang, Y.; Fang, J. C.; Zhang, L. Cell membrane-derived nanomaterials for biomedical applications. Biomaterials. 2017, 128, 69-83.
18. Wu, M.; Zhang, H.; Tie, C.; Yan, C.; Deng, Z.; Wan, Q.; Liu, X.; Yan, F.; Zheng, H. MR imaging tracking of inflammation-activatable engineered neutrophils for targeted therapy of surgically treated glioma. Nat Commun. 2018, 9, 4777.
19. Guo, H.; Wang, L.; Wu, W.; Guo, M.; Yang, L.; Zhang, Z.; Cao, L.; Pu, F.; Huang, X.; Shao, Z. Engineered biomimetic nanoreactor for synergistic photodynamic-chemotherapy against hypoxic tumor. J Control Release. 2022, 351, 151-163.
20. 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.
21. Parodi, A.; Quattrocchi, N.; van de Ven, A. L.; Chiappini, C.; Evangelopoulos, M.; Martinez, J. O.; Brown, B. S.; Khaled, S. Z.; Yazdi, I. K.; Enzo, M. V.; Isenhart, L.; Ferrari, M.; Tasciotti, E. Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat Nanotechnol. 2013, 8, 61-68.
22. Yu, J.; Wei, Z.; Li, Q.; Wan, F.; Chao, Z.; Zhang, X.; Lin, L.; Meng, H.; Tian, L. Advanced cancer starvation therapy by simultaneous deprivation of lactate and glucose using a MOF nanoplatform. Adv Sci (Weinh). 2021, 8, e2101467.
23. Yang, J.; Yang, Y. W. Metal-organic frameworks for biomedical applications. Small. 2020, 16, e1906846.
24. Liu, W.; Yan, Q.; Xia, C.; Wang, X.; Kumar, A.; Wang, Y.; Liu, Y.; Pan, Y.; Liu, J. Recent advances in cell membrane coated metal-organic frameworks (MOFs) for tumor therapy. J Mater Chem B. 2021, 9, 4459-4474.
25. Pan, W. L.; Tan, Y.; Meng, W.; Huang, N. H.; Zhao, Y. B.; Yu, Z. Q.; Huang, Z.; Zhang, W. H.; Sun, B.; Chen, J. X. 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.
26. Zhen, X.; Cheng, P.; Pu, K. Recent advances in cell membrane-camouflaged nanoparticles for cancer phototherapy. Small. 2019, 15, e1804105.
27. Cui, X.; Ruan, Q.; Zhuo, X.; Xia, X.; Hu, J.; Fu, R.; Li, Y.; Wang, J.; Xu, H. Photothermal nanomaterials: a powerful light-to-heat converter. Chem Rev. 2023, 123, 6891-6952.
28. Wu, F.; Liu, Y.; Cheng, H.; Meng, Y.; Shi, J.; Chen, Y.; Wu, Y. Enhanced cancer starvation therapy based on glucose oxidase/3-methyladenine-loaded dendritic mesoporous organosilicon nanoparticles. Biomolecules. 2021, 11, 1363.
29. Ducrot, C.; Loiseau, S.; Wong, C.; Madec, E.; Volatron, J.; Piffoux, M. Hybrid extracellular vesicles for drug delivery. Cancer Lett. 2023, 558, 216107.
30. Liu, C.; Zhang, W.; Li, Y.; Chang, J.; Tian, F.; Zhao, F.; Ma, Y.; Sun, J. Microfluidic sonication to assemble exosome membrane-coated nanoparticles for immune evasion-mediated targeting. Nano Lett. 2019, 19, 7836-7844.
31. Xia, Y.; Rao, L.; Yao, H.; Wang, Z.; Ning, P.; Chen, X. Engineering macrophages for cancer immunotherapy and drug delivery. Adv Mater. 2020, 32, e2002054.
32. Huang, X.; Guo, H.; Wang, L.; Zhang, Z.; Zhang, W. Biomimetic cell membrane-coated nanocarriers for targeted siRNA delivery in cancer therapy. Drug Discov Today. 2023, 28, 103514.
33. Jarak, I.; Isabel Santos, A.; Helena Pinto, A.; Domingues, C.; Silva, I.; Melo, R.; Veiga, F.; Figueiras, A. Colorectal cancer cell exosome and cytoplasmic membrane for homotypic delivery of therapeutic molecules. Int J Pharm. 2023, 646, 123456.
34. Albanese, A.; Tang, P. S.; Chan, W. C. The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu Rev Biomed Eng. 2012, 14, 1-16.
35. Salatin, S.; Maleki Dizaj, S.; Yari Khosroushahi, A. Effect of the surface modification, size, and shape on cellular uptake of nanoparticles. Cell Biol Int. 2015, 39, 881-890.
36. Agarwal, R.; Jurney, P.; Raythatha, M.; Singh, V.; Sreenivasan, S. V.; Shi, L.; Roy, K. Effect of shape, size, and aspect ratio on nanoparticle penetration and distribution inside solid tissues using 3D spheroid models. Adv Healthc Mater. 2015, 4, 2269-2280.
37. Lagarrigue, P.; Moncalvo, F.; Cellesi, F. Non-spherical polymeric nanocarriers for therapeutics: the effect of shape on biological systems and drug delivery properties. Pharmaceutics. 2022, 15, 32.
38. Jindal, A. B. The effect of particle shape on cellular interaction and drug delivery applications of micro- and nanoparticles. Int J Pharm. 2017, 532, 450-465.
39. Li, X.; Montague, E. C.; Pollinzi, A.; Lofts, A.; Hoare, T. Design of smart size-, surface-, and shape-switching nanoparticles to improve therapeutic efficacy. Small. 2022, 18, e2104632.
40. Bilardo, R.; Traldi, F.; Vdovchenko, A.; Resmini, M. Influence of surface chemistry and morphology of nanoparticles on protein corona formation. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2022, 14, e1788.
41. He, F.; Zhu, L.; Zhou, X.; Zhang, P.; Cheng, J.; Qiao, Y.; Feng, Y.; Yue, S.; Xu, M.; Guan, J.; Li, X.; Ao, Z.; Qin, M.; Hou, Y.; Han, D. Red blood cell membrane-coated ultrasmall NaGdF(4) nanoprobes for high-resolution 3D magnetic resonance angiography. ACS Appl Mater Interfaces. 2022. doi: 10.1021/acsami.2c03530.
42. Narain, A.; Asawa, S.; Chhabria, V.; Patil-Sen, Y. Cell membrane coated nanoparticles: next-generation therapeutics. Nanomedicine (Lond). 2017, 12, 2677-2692.
43. Oldenborg, P. A.; Zheleznyak, A.; Fang, Y. F.; Lagenaur, C. F.; Gresham, H. D.; Lindberg, F. P. Role of CD47 as a marker of self on red blood cells. Science. 2000, 288, 2051-2054.
44. Huang, S.; Song, C.; Miao, J.; Zhu, X.; Jia, Y.; Liu, Y.; Fu, D.; Li, B.; Miao, M.; Duan, S.; Zhang, Z.; Hu, Y. Red blood cell membrane-coated functionalized Au nanocage as a biomimetic platform for improved microRNA delivery in hepatocellular carcinoma. Int J Pharm. 2023, 642, 123044.
45. Telen, M. J.; Rosse, W. F. Phosphatidylinositol-glycan linked proteins of the erythrocyte membrane. Baillieres Clin Haematol. 1991, 4, 849-868.
46. Tomlinson, S.; Whitlow, M. B.; Nussenzweig, V. A synthetic peptide from complement protein C9 binds to CD59 and enhances lysis of human erythrocytes by C5b-9. J Immunol. 1994, 152, 1927-1934.
47. Zheng, B. D.; Xiao, M. T. Red blood cell membrane nanoparticles for tumor phototherapy. Colloids Surf B Biointerfaces. 2022, 220, 112895.
48. Zhang, S. Q.; Fu, Q.; Zhang, Y. J.; Pan, J. X.; Zhang, L.; Zhang, Z. R.; Liu, Z. M. Surface loading of nanoparticles on engineered or natural erythrocytes for prolonged circulation time: strategies and applications. Acta Pharmacol Sin. 2021, 42, 1040-1054.
49. Ren, X.; Zheng, R.; Fang, X.; Wang, X.; Zhang, X.; Yang, W.; Sha, X. Red blood cell membrane camouflaged magnetic nanoclusters for imaging-guided photothermal therapy. Biomaterials. 2016, 92, 13-24.
50. Rao, L.; Bu, L. L.; Xu, J. H.; Cai, B.; Yu, G. T.; Yu, X.; He, Z.; Huang, Q.; Li, A.; Guo, S. S.; Zhang, W. F.; Liu, W.; Sun, Z. J.; Wang, H.; Wang, T. H.; Zhao, X. Z. Red blood cell membrane as a biomimetic nanocoating for prolonged circulation time and reduced accelerated blood clearance. Small. 2015, 11, 6225-6236.
51. Cox, D.; Kerrigan, S. W.; Watson, S. P. Platelets and the innate immune system: mechanisms of bacterial-induced platelet activation. J Thromb Haemost. 2011, 9, 1097-1107.
52. Schlesinger, M. Role of platelets and platelet receptors in cancer metastasis. J Hematol Oncol. 2018, 11, 125.
53. Franco, A. T.; Corken, A.; Ware, J. Platelets at the interface of thrombosis, inflammation, and cancer. Blood. 2015, 126, 582-588.
54. Sabrkhany, S.; Kuijpers, M. J. E.; Griffioen, A. W.; Oude Egbrink, M. G. A. Platelets: the holy grail in cancer blood biomarker research? Angiogenesis. 2019, 22, 1-2.
55. Nash, G. F.; Turner, L. F.; Scully, M. F.; Kakkar, A. K. Platelets and cancer. Lancet Oncol. 2002, 3, 425-430.
56. Geranpayehvaghei, M.; Dabirmanesh, B.; Khaledi, M.; Atabakhshi-Kashi, M.; Gao, C.; Taleb, M.; Zhang, Y.; Khajeh, K.; Nie, G. Cancer-associated-platelet-inspired nanomedicines for cancer therapy. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2021, 13, e1702.
57. Hu, C. M.; Fang, R. H.; Wang, K. C.; Luk, B. T.; Thamphiwatana, S.; Dehaini, D.; Nguyen, P.; Angsantikul, P.; Wen, C. H.; Kroll, A. V.; Carpenter, C.; Ramesh, M.; Qu, V.; Patel, S. H.; Zhu, J.; Shi, W.; Hofman, F. M.; Chen, T. C.; Gao, W.; Zhang, K.; Chien, S.; Zhang, L. Nanoparticle biointerfacing by platelet membrane cloaking. Nature. 2015, 526, 118-121.
58. Zhuang, J.; Gong, H.; Zhou, J.; Zhang, Q.; Gao, W.; Fang, R. H.; Zhang, L. Targeted gene silencing in vivo by platelet membrane-coated metal-organic framework nanoparticles. Sci Adv. 2020, 6, eaaz6108.
59. Bahmani, B.; Gong, H.; Luk, B. T.; Haushalter, K. J.; DeTeresa, E.; Previti, M.; Zhou, J.; Gao, W.; Bui, J. D.; Zhang, L.; Fang, R. H.; Zhang, J. Intratumoral immunotherapy using platelet-cloaked nanoparticles enhances antitumor immunity in solid tumors. Nat Commun. 2021, 12, 1999.
60. Wang, D.; Wang, S.; Zhou, Z.; Bai, D.; Zhang, Q.; Ai, X.; Gao, W.; Zhang, L. White blood cell membrane-coated nanoparticles: recent development and medical applications. Adv Healthc Mater. 2022, 11, e2101349.
61. Rao, L.; Zhao, S. K.; Wen, C.; Tian, R.; Lin, L.; Cai, B.; Sun, Y.; Kang, F.; Yang, Z.; He, L.; Mu, J.; Meng, Q. F.; Yao, G.; Xie, N.; Chen, X. Activating macrophage-mediated cancer immunotherapy by genetically edited nanoparticles. Adv Mater. 2020, 32, e2004853.
62. Franklin, R. A.; Liao, W.; Sarkar, A.; Kim, M. V.; Bivona, M. R.; Liu, K.; Pamer, E. G.; Li, M. O. The cellular and molecular origin of tumor-associated macrophages. Science. 2014, 344, 921-925.
63. Oroojalian, F.; Beygi, M.; Baradaran, B.; Mokhtarzadeh, A.; Shahbazi, M. A. Immune cell membrane-coated biomimetic nanoparticles for targeted cancer therapy. Small. 2021, 17, e2006484.
64. Jain, N.; Shahrukh, S.; Famta, P.; Shah, S.; Vambhurkar, G.; Khatri, D. K.; Singh, S. B.; Srivastava, S. Immune cell-camouflaged surface-engineered nanotherapeutics for cancer management. Acta Biomater. 2023, 155, 57-79.
65. Lopes, J.; Lopes, D.; Pereira-Silva, M.; Peixoto, D.; Veiga, F.; Hamblin, M. R.; Conde, J.; Corbo, C.; Zare, E. N.; Ashrafizadeh, M.; Tay, F. R.; Chen, C.; Donnelly, R. F.; Wang, X.; Makvandi, P.; Paiva-Santos, A. C. Macrophage cell membrane-cloaked nanoplatforms for biomedical applications. Small Methods. 2022, 6, e2200289.
66. Zhang, Q.; Dehaini, D.; Zhang, Y.; Zhou, J.; Chen, X.; Zhang, L.; Fang, R. H.; Gao, W.; Zhang, L. Neutrophil membrane-coated nanoparticles inhibit synovial inflammation and alleviate joint damage in inflammatory arthritis. Nat Nanotechnol. 2018, 13, 1182-1190.
67. Bhattacharyya, S.; Ghosh, S. S. Transmembrane TNFα-expressed macrophage membrane-coated chitosan nanoparticles as cancer therapeutics. ACS Omega. 2020, 5, 1572-1580.
68. Meng, Q. F.; Rao, L.; Zan, M.; Chen, M.; Yu, G. T.; Wei, X.; Wu, Z.; Sun, Y.; Guo, S. S.; Zhao, X. Z.; Wang, F. B.; Liu, W. Macrophage membrane-coated iron oxide nanoparticles for enhanced photothermal tumor therapy. Nanotechnology. 2018, 29, 134004.
69. Johnson, D. T.; Zhou, J.; Kroll, A. V.; Fang, R. H.; Yan, M.; Xiao, C.; Chen, X.; Kline, J.; Zhang, L.; Zhang, D. E. Acute myeloid leukemia cell membrane-coated nanoparticles for cancer vaccination immunotherapy. Leukemia. 2022, 36, 994-1005.
70. Kang, T.; Zhu, Q.; Wei, D.; Feng, J.; Yao, J.; Jiang, T.; Song, Q.; Wei, X.; Chen, H.; Gao, X.; Chen, J. Nanoparticles coated with neutrophil membranes can effectively treat cancer metastasis. ACS Nano. 2017, 11, 1397-1411.
71. Cao, X.; Hu, Y.; Luo, S.; Wang, Y.; Gong, T.; Sun, X.; Fu, Y.; Zhang, Z. Neutrophil-mimicking therapeutic nanoparticles for targeted chemotherapy of pancreatic carcinoma. Acta Pharm Sin B. 2019, 9, 575-589.
72. Deng, G.; Sun, Z.; Li, S.; Peng, X.; Li, W.; Zhou, L.; Ma, Y.; Gong, P.; Cai, L. Cell-membrane immunotherapy based on natural killer cell membrane coated nanoparticles for the effective inhibition of primary and abscopal tumor growth. ACS Nano. 2018, 12, 12096-12108.
73. Wu, L.; Zhang, F.; Wei, Z.; Li, X.; Zhao, H.; Lv, H.; Ge, R.; Ma, H.; Zhang, H.; Yang, B.; Li, J.; Jiang, J. Magnetic delivery of Fe(3)O(4)@polydopamine nanoparticle-loaded natural killer cells suggest a promising anticancer treatment. Biomater Sci. 2018, 6, 2714-2725.
74. Gardner, A.; Ruffell, B. Dendritic cells and cancer immunity. Trends Immunol. 2016, 37, 855-865.
75. Wculek, S. K.; Cueto, F. J.; Mujal, A. M.; Melero, I.; Krummel, M. F.; Sancho, D. Dendritic cells in cancer immunology and immunotherapy. Nat Rev Immunol. 2020, 20, 7-24.
76. Cheng, S.; Xu, C.; Jin, Y.; Li, Y.; Zhong, C.; Ma, J.; Yang, J.; Zhang, N.; Li, Y.; Wang, C.; Yang, Z.; Wang, Y. Artificial mini dendritic cells boost T cell-based immunotherapy for ovarian cancer. Adv Sci (Weinh). 2020, 7, 1903301.
77. Ferreira-Faria, I.; Yousefiasl, S.; Macário-Soares, A.; Pereira-Silva, M.; Peixoto, D.; Zafar, H.; Raza, F.; Faneca, H.; Veiga, F.; Hamblin, M. R.; Tay, F. R.; Gao, J.; Sharifi, E.; Makvandi, P.; Paiva-Santos, A. C. Stem cell membrane-coated abiotic nanomaterials for biomedical applications. J Control Release. 2022, 351, 174-197.
78. Chen, Z.; Zhao, P.; Luo, Z.; Zheng, M.; Tian, H.; Gong, P.; Gao, G.; Pan, H.; Liu, L.; Ma, A.; Cui, H.; Ma, Y.; Cai, L. Cancer cell membrane-biomimetic nanoparticles for homologous-targeting dual-modal imaging and photothermal therapy. ACS Nano. 2016, 10, 10049-10057.
79. Su, N.; Villi表：cana, C.; Barati, D.; Freeman, P.; Luo, Y.; Yang, F. Stem cell membrane-coated microribbon scaffolds induce regenerative innate and adaptive immune responses in a critical-size cranial bone defect model. Adv Mater. 2023, 35, e2208781.
80. Fang, R. H.; Hu, C. M.; Luk, B. T.; Gao, W.; Copp, J. A.; Tai, Y.; O’Connor, D. E.; Zhang, L. Cancer cell membrane-coated nanoparticles for anticancer vaccination and drug delivery. Nano Lett. 2014, 14, 2181-2188.
81. Chen, Q.; Zhang, L.; Li, L.; Tan, M.; Liu, W.; Liu, S.; Xie, Z.; Zhang, W.; Wang, Z.; Cao, Y.; Shang, T.; Ran, H. Cancer cell membrane-coated nanoparticles for bimodal imaging-guided photothermal therapy and docetaxel-enhanced immunotherapy against cancer. J Nanobiotechnology. 2021, 19, 449.
82. Jiang, Y.; Krishnan, N.; Zhou, J.; Chekuri, S.; Wei, X.; Kroll, A. V.; Yu, C. L.; Duan, Y.; Gao, W.; Fang, R. H.; Zhang, L. Engineered cell-membrane-coated nanoparticles directly present tumor antigens to promote anticancer immunity. Adv Mater. 2020, 32, e2001808.
83. He, Z.; Zhang, Y.; Feng, N. Cell membrane-coated nanosized active targeted drug delivery systems homing to tumor cells: a review. Mater Sci Eng C Mater Biol Appl. 2020, 106, 110298.
84. 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, 3233-3254.
85. Rao, L.; Bu, L. L.; Cai, B.; Xu, J. H.; Li, A.; Zhang, W. F.; Sun, Z. J.; Guo, S. S.; Liu, W.; Wang, T. H.; Zhao, X. Z. Cancer cell membrane-coated upconversion nanoprobes for highly specific tumor imaging. Adv Mater. 2016, 28, 3460-3466.
86. Yang, R.; Xu, J.; Xu, L.; Sun, X.; Chen, Q.; Zhao, Y.; Peng, R.; Liu, Z. Cancer cell membrane-coated adjuvant nanoparticles with mannose modification for effective anticancer vaccination. ACS Nano. 2018, 12, 5121-5129.
87. Wang, D.; Liu, C.; You, S.; Zhang, K.; Li, M.; Cao, Y.; Wang, C.; Dong, H.; Zhang, X. Bacterial vesicle-cancer cell hybrid membrane-coated nanoparticles for tumor specific immune activation and photothermal therapy. ACS Appl Mater Interfaces. 2020, 12, 41138-41147.
88. Fang, R. H.; Hu, C. M.; Chen, K. N.; Luk, B. T.; Carpenter, C. W.; Gao, W.; Li, S.; Zhang, D. E.; Lu, W.; Zhang, L. Lipid-insertion enables targeting functionalization of erythrocyte membrane-cloaked nanoparticles. Nanoscale. 2013, 5, 8884-8888.
89. Ruoslahti, E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol. 1996, 12, 697-715.
90. Cossu, J.; Thoreau, F.; Boturyn, D. Multimeric RGD-based strategies for selective drug delivery to tumor tissues. Pharmaceutics. 2023, 15, 525.
91. Sun, J.; Jiang, L.; Lin, Y.; Gerhard, E. M.; Jiang, X.; Li, L.; Yang, J.; Gu, Z. Enhanced anticancer efficacy of paclitaxel through multistage tumor-targeting liposomes modified with RGD and KLA peptides. Int J Nanomedicine. 2017, 12, 1517-1537.
92. Wu, W.; Guo, H.; Jing, D.; Zhang, Z.; Zhang, Z.; Pu, F.; Yang, W.; Jin, X.; Huang, X.; Shao, Z. Targeted delivery of PD-L1-derived phosphorylation-mimicking peptides by engineered biomimetic nanovesicles to enhance osteosarcoma treatment. Adv Healthc Mater. 2022, 11, e2200955.
93. Han, Y.; Pan, H.; Li, W.; Chen, Z.; Ma, A.; Yin, T.; Liang, R.; Chen, F.; Ma, Y.; Jin, Y.; Zheng, M.; Li, B.; Cai, L. T cell membrane mimicking nanoparticles with bioorthogonal targeting and immune recognition for enhanced photothermal therapy. Adv Sci (Weinh). 2019, 6, 1900251.
94. Park, J. H.; Jiang, Y.; Zhou, J.; Gong, H.; Mohapatra, A.; Heo, J.; Gao, W.; Fang, R. H.; Zhang, L. Genetically engineered cell membrane-coated nanoparticles for targeted delivery of dexamethasone to inflamed lungs. Sci Adv. 2021, 7, eabf7820.
95. Ma, J.; Jiang, L.; Liu, G. Cell membrane-coated nanoparticles for the treatment of bacterial infection. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2022, 14, e1825.
96. Zhu, C.; Ma, J.; Ji, Z.; Shen, J.; Wang, Q. Recent advances of cell membrane coated nanoparticles in treating cardiovascular disorders. Molecules. 2021, 26, 3428.
97. Xiong, J.; Wu, M.; Chen, J.; Liu, Y.; Chen, Y.; Fan, G.; Liu, Y.; Cheng, J.; Wang, Z.; Wang, S.; Liu, Y.; Zhang, W. Cancer-erythrocyte hybrid membrane-camouflaged magnetic nanoparticles with enhanced photothermal-immunotherapy for ovarian cancer. ACS Nano. 2021, 15, 19756-19770.
98. Chen, H. Y.; Deng, J.; Wang, Y.; Wu, C. Q.; Li, X.; Dai, H. W. Hybrid cell membrane-coated nanoparticles: A multifunctional biomimetic platform for cancer diagnosis and therapy. Acta Biomater. 2020, 112, 1-13.
99. Dehaini, D.; Wei, X.; Fang, R. H.; Masson, S.; Angsantikul, P.; Luk, B. T.; Zhang, Y.; Ying, M.; Jiang, Y.; Kroll, A. V.; Gao, W.; Zhang, L. Erythrocyte-platelet hybrid membrane coating for enhanced nanoparticle functionalization. Adv Mater. 2017, 29, 1606209.
100. Jiang, Q.; Liu, Y.; Guo, R.; Yao, X.; Sung, S.; Pang, Z.; Yang, W. Erythrocyte-cancer hybrid membrane-camouflaged melanin nanoparticles for enhancing photothermal therapy efficacy in tumors. Biomaterials. 2019, 192, 292-308.
101. Zhang, Y.; Cai, K.; Li, C.; Guo, Q.; Chen, Q.; He, X.; Liu, L.; Zhang, Y.; Lu, Y.; Chen, X.; Sun, T.; Huang, Y.; Cheng, J.; Jiang, C. Macrophage-membrane-coated nanoparticles for tumor-targeted chemotherapy. Nano Lett. 2018, 18, 1908-1915.
102. Sun, M.; Duan, Y.; Ma, Y.; Zhang, Q. Cancer cell-erythrocyte hybrid membrane coated gold nanocages for near infrared light-activated photothermal/radio/chemotherapy of breast cancer. Int J Nanomedicine. 2020, 15, 6749-6760.
103. Li, M.; Zhou, H.; Jiang, W.; Yang, C.; Miao, H.; Wang, Y. Nanovaccines integrating endogenous antigens and pathogenic adjuvants elicit potent antitumor immunity. Nano Today. 2020, 35, 101007.
104. Ma, J.; Liu, F.; Sheu, W. C.; Meng, Z.; Xie, Y.; Xu, H.; Li, M.; Chen, A. T.; Liu, J.; Bao, Y.; Zhang, X.; Zhang, S.; Zhang, L.; Zou, Z.; Wu, H.; Wang, H.; Zhu, Y.; Zhou, J. Copresentation of tumor antigens and costimulatory molecules via biomimetic nanoparticles for effective cancer immunotherapy. Nano Lett. 2020, 20, 4084-4094.
105. Liu, W. L.; Zou, M. Z.; Liu, T.; Zeng, J. Y.; Li, X.; Yu, W. Y.; Li, C. X.; Ye, J. J.; Song, W.; Feng, J.; Zhang, X. Z. Cytomembrane nanovaccines show therapeutic effects by mimicking tumor cells and antigen presenting cells. Nat Commun. 2019, 10, 3199.
106. Chen, R.; Yang, J.; Wu, M.; Zhao, D.; Yuan, Z.; Zeng, L.; Hu, J.; Zhang, X.; Wang, T.; Xu, J.; Zhang, J. M2 macrophage hybrid membrane-camouflaged targeted biomimetic nanosomes to reprogram inflammatory microenvironment for enhanced enzyme-thermo-immunotherapy. Adv Mater. 2023, 35, e2304123.
