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Biomimetic nanomedicine toward personalized disease theranostics

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Abstract

Despite nanoparticle-based drug delivery systems have aroused broad research interest in the biomedical fields, the rising challenges such as easy recognition by the immune system and low accumulation in diseased sites significantly hinder their further clinical translation. Nanoparticles wrapped in cell membrane have emerged as a distinctive strategy to overcome these limitations due to the superior marriage of natural cell membrane and artificial nanomaterials, which endow them with prominent advantages in disease diagnosis and treatment, such as targeted drug transport, prolonged drug half-life, and diminished immunogenicity and cytotoxicity. In this review, we mainly highlight and discuss the evolving progresses and advantages of cell membrane-based biomimetic nanosystems in the detection and treatment of various diseases over the past five years, including oncology, bacterial infections, brain diseases, and inflammatory diseases, which would benefit researchers in better and comprehensively understanding the complicated microenvironment of diseases and developing personalized biomimetic nanomedicines for different diseases. The current challenges and potential opportunities for the future clinical translation of cell membrane coating nanotechnology are also covered.

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References

  1. Pelaz, B.; Alexiou, C.; Alvarez-Puebla, R. A.; Alves, F.; Andrews, A. M.; Ashraf, S.; Balogh, L. P.; Ballerini, L.; Bestetti, A.; Brendel, C. et al. Diverse applications of nanomedicine. ACS Nano 2017, 11, 2313–2381.

    Article  CAS  Google Scholar 

  2. Zhang, L.; Gu, F. X.; Chan, J. M.; Wang, A. Z.; Langer, R. S.; Farokhzad, O. C. Nanoparticles in medicine: Therapeutic applications and developments. Clin. Pharmacol. Ther. 2008, 83, 761–769.

    Article  CAS  Google Scholar 

  3. Jones, R. L.; Berry, G. J.; Rubens, R. D.; Miles, D. W. Clinical and pathological absence of cardiotoxicity after liposomal doxorubicin. Lancet Oncol. 2004, 5, 575–577.

    Article  Google Scholar 

  4. Andreopoulou, E.; Gaiotti, D.; Kim, E.; Downey, A.; Mirchandani, D.; Hamilton, A.; Jacobs, A.; Curtin, J.; Muggia, F. Pegylated liposomal doxorubicin HCL (PLD; Caelyx/Doxil®): Experience with long-term maintenance in responding patients with recurrent epithelial ovarian cancer. Ann. Oncol. 2007, 18, 716–721.

    Article  CAS  Google Scholar 

  5. Knop, K.; Hoogenboom, R.; Fischer, D.; Schubert, U. S. Poly(ethylene glycol) in drug delivery: Pros and cons as well as potential alternatives. Angew. Chem, Int. Ed. 2010, 49, 6288–6308.

    Article  CAS  Google Scholar 

  6. Chapman, A. P. PEGylated antibodies and antibody fragments for improved therapy: A review. Adv. Drug Deliv. Rev. 2002, 54, 531–545.

    Article  CAS  Google Scholar 

  7. Lubich, C.; Allacher, P.; de la Rosa, M.; Bauer, A.; Prenninger, T.; Horling, F. M.; Siekmann, J.; Oldenburg, J.; Scheiflinger, F.; Reipert, B. M. The mystery of antibodies against polyethylene glycol (PEG)-what do we know? Pharm. Res. 2016, 33, 2239–2249.

    Article  CAS  Google Scholar 

  8. Lee, G. Y.; Kim, J. H.; Choi, K. Y.; Yoon, H. Y.; Kim, K.; Kwon, I. C.; Choi, K.; Lee, B. H.; Park, J. H.; Kim, I. S. Hyaluronic acid nanoparticles for active targeting atherosclerosis. Biomaterials 2015, 53, 341–348.

    Article  CAS  Google Scholar 

  9. Boonstra, M. C.; de Geus, S. W. L.; Prevoo, H. A. J. M.; Hawinkels, L. J. A. C.; van de Velde, C. J. H.; Kuppen, P. J. K.; Vahrmeijer, A. L.; Sier, C. F. M. Selecting targets for tumor imaging: An overview of cancer-associated membrane proteins. Biomarkers Cancer 2016, 8, 119–133.

    Article  CAS  Google Scholar 

  10. Ulbrich, K.; Holá, K.; Subr, V.; Bakandritsos, A.; Tucek, J.; Zbofil, R. Targeted drug delivery with polymers and magnetic nanoparticles: Covalent and noncovalent approaches, release control, and clinical studies. Chem. Rev. 2016, 116, 5338–5431.

    Article  CAS  Google Scholar 

  11. Mout, R.; Moyano, D. F.; Rana, S.; Rotello, V. M. Surface functionalization of nanoparticles for nanomedicine. Chem. Soc. Rev. 2012, 41, 2539–2544.

    Article  CAS  Google Scholar 

  12. Bertrand, N.; Wu, J.; Xu, X. Y.; Kamaly, N.; Farokhzad, O. C. Cancer nanotechnology: The impact of passive and active targeting in the era of modern cancer biology. Adv. Drug Deliv. Rev. 2014, 66, 2–25.

    Article  CAS  Google Scholar 

  13. Kang, J.; Joo, J.; Kwon, E. J.; Skalak, M.; Hussain, S.; She, Z. G.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Self-sealing porous silicon-calcium silicate core-shell nanoparticles for targeted siRNA delivery to the injured brain. Adv. Mater. 2016, 28, 7962–7969.

    Article  CAS  Google Scholar 

  14. Rosenblum, D.; Joshi, N.; Tao, W.; Karp, J. M.; Peer, D. Progress and challenges towards targeted delivery of cancer therapeutics. Nat. Commun. 2018, 9, 1410.

    Article  CAS  Google Scholar 

  15. Tan, S. W.; Wu, T. T.; Zhang, D.; Zhang, Z. P. Cell or cell membrane-based drug delivery systems. Theranostics 2015, 5, 863–881.

    Article  CAS  Google Scholar 

  16. Thanuja, M. Y.; Anupama, C.; Ranganath, S. H. Bioengineered cellular and cell membrane-derived vehicles for actively targeted drug delivery: So near and yet so far. Adv. Drug Deliv. Rev. 2018, 132, 57–80.

    Article  CAS  Google Scholar 

  17. Chen, Z. W.; Hu, Q. Y.; Gu, Z. Leveraging engineering of cells for drug delivery. Acc. Chem. Res. 2018, 51, 668–677.

    Article  CAS  Google Scholar 

  18. Wu, M. Y.; Zhang, H. X.; Tie, C. J.; Yan, C. H.; Deng, Z. T.; Wan, Q.; Liu, X.; Yan, F.; Zheng, H. R. MR imaging tracking of inflammation-activatable engineered neutrophils for targeted therapy of surgically treated glioma. Nat. Commun. 2018, 9, 4777.

    Article  CAS  Google Scholar 

  19. DeLoach, J. R.; Barton, C.; Culler, K. Preparation of resealed carrier erythrocytes and in vivo survival in dogs. Am. J. Vet. Res. 1981, 42, 667–669.

    CAS  Google Scholar 

  20. Nourshargh, S.; Alon, R. Leukocyte migration into inflamed tissues. Immunity 2014, 41, 694–707.

    Article  CAS  Google Scholar 

  21. Villa, C. H.; Anselmo, A. C.; Mitragotri, S.; Muzykantov, V. Red blood cells: Supercarriers for drugs, biologicals, and nanoparticles and inspiration for advanced delivery systems. Adv. Drug Deliv. Rev. 2016, 106, 88–103.

    Article  CAS  Google Scholar 

  22. Hu, C. M. J.; Zhang, L.; Aryal, S.; Cheung, C.; Fang, R. H.; Zhang, L. F. Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform. Proc. Natl. Acad. Sci. USA 2011, 108, 10980–10985.

    Article  CAS  Google Scholar 

  23. 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. et al. Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat. Nanotechnol. 2013, 8, 61–68.

    Article  CAS  Google Scholar 

  24. Tang, J. N.; Shen, D. L.; Caranasos, T. G.; Wang, Z. G.; Vandergriff, A. C.; Allen, T. A.; Hensley, M. T.; Dinh, P. U.; Cores, J.; Li, T. S. et al. Therapeutic microparticles functionalized with biomimetic cardiac stem cell membranes and secretome. Nat. Commun. 2017, 8, 13724.

    Article  CAS  Google Scholar 

  25. Kang, T.; Zhu, Q. Q.; Wei, D.; Feng, J. X.; Yao, J. H.; Jiang, T. Z.; Song, Q. X.; Wei, X. B.; Chen, H. Z.; Gao, X. L. et al. Nanoparticles coated with neutrophil membranes can effectively treat cancer metastasis. ACS Nano 2017, 11, 1397–1411.

    Article  CAS  Google Scholar 

  26. Bose, R. J. C.; Kim, B. J.; Arai, Y.; Han, I. B.; Moon, J. J.; Paulmurugan, R.; Park, H.; Lee, S. H. Bioengineered stem cell membrane functionalized nanocarriers for therapeutic targeting of severe hindlimb ischemia. Biomaterials 2018, 185, 360–370.

    Article  CAS  Google Scholar 

  27. Zhai, Y. H.; Su, J. H.; Ran, W.; Zhang, P. C.; Yin, Q.; Zhang, Z. W.; Yu, H. J.; Li, Y. P. Preparation and application of cell membrane-camouflaged nanoparticles for cancer therapy. Theranostics 2017, 7, 2575–2592.

    Article  CAS  Google Scholar 

  28. Xuan, M. J.; Shao, J. X.; Li, J. B. Cell membrane-covered nanoparticles as biomaterials. Natl. Sci. Rev. 2019, 6, 551–561.

    Article  CAS  Google Scholar 

  29. Fang, R. H.; Kroll, A. V.; Gao, W. W.; Zhang, L. F. Cell membrane coating nanotechnology. Adv. Mater. 2018, 30, 1706759.

    Article  CAS  Google Scholar 

  30. He, Z. H.; Zhang, Y. T.; Feng, N. P. Cell membrane-coated nanosized active targeted drug delivery systems homing to tumor cells: A review. Mater. Sci. Eng.: C 2020, 106, 110298.

    Article  CAS  Google Scholar 

  31. Liu, Y.; Luo, J. S.; Chen, X. J.; Liu, W.; Chen, T. K. Cell membrane coating technology: A promising strategy for biomedical applications. Nano-Micro Lett. 2019, 11, 100.

    Article  CAS  Google Scholar 

  32. Bailar III, J. C.; Gornik, H. L. Cancer undefeated. N. Engl. J. Med. 1997, 336, 1569–1574.

    Article  Google Scholar 

  33. Feng, L. Z.; Dong, Z. L.; Liang, C.; Chen, M. C.; Tao, D. L.; Cheng, L.; Yang, K.; Liu, Z. Iridium nanocrystals encapsulated liposomes as near-infrared light controllable nanozymes for enhanced cancer radiotherapy. Biomaterials 2018, 181, 81–91.

    Article  CAS  Google Scholar 

  34. Vasan, N.; Baselga, J.; Hyman, D. M. A view on drug resistance in cancer. Nature 2019, 575, 299–309.

    Article  CAS  Google Scholar 

  35. Chen, Q.; Wang, C.; Zhang, X. D.; Chen, G. J.; Hu, Q. Y.; Li, H. J.; Wang, J. Q.; Wen, D.; Zhang, Y. Q.; Lu, Y. F. et al. In situ sprayed bioresponsive immunotherapeutic gel for post-surgical cancer treatment. Nat. Nanotechnol. 2019, 14, 89–97.

    Article  CAS  Google Scholar 

  36. Chabner, B. A.; Roberts, T. G. Jr. Chemotherapy and the war on cancer. Nat. Rev. Cancer 2005, 5, 65–72.

    Article  CAS  Google Scholar 

  37. Hu, Q. Y.; Qian, C. G.; Sun, W. J.; Wang, J. Q.; Chen, Z. W.; Bomba, H. N.; Xin, H. L.; Shen, Q. D.; Gu, Z. Engineered nanoplatelets for enhanced treatment of multiple myeloma and thrombus. Adv. Mater. 2016, 28, 9573–9580.

    Article  CAS  Google Scholar 

  38. Zhang, Y.; Cai, K. M.; Li, C.; Guo, Q.; Chen, Q. J.; He, X.; Liu, L. S.; Zhang, Y. J.; Lu, Y. F.; Chen, X. L. et al. Macrophage-membrane-coated nanoparticles for tumor-targeted chemotherapy. Nano Lett. 2018, 18, 1908–1915.

    Article  CAS  Google Scholar 

  39. Zhang, W.; Yu, M. R.; Xi, Z. Y.; Nie, D.; Dai, Z.; Wang, J.; Qian, K.; Weng, H. X.; Gan, Y.; Xu, L. Cancer cell membrane-camouflaged nanorods with endoplasmic reticulum targeting for improved antitumor therapy. ACS Appl. Mater. Interfaces 2019, 11, 46614–46625.

    Article  CAS  Google Scholar 

  40. Stuckey, D. W.; Shah, K. Stem cell-based therapies for cancer treatment: Separating hope from hype. Nat. Rev. Cancer 2014, 14, 683–691.

    Article  CAS  Google Scholar 

  41. Blau, H. M.; Daley, G. Q. Stem cells in the treatment of disease. N. Engl. J. Med. 2019, 380, 1748–1760.

    Article  CAS  Google Scholar 

  42. Gao, C. Y.; Lin, Z. H.; Jurado-Sánchez, B.; Lin, X. K.; Wu, Z. G.; He, Q. Stem cell membrane-coated nanogels for highly efficient in vivo tumor targeted drug delivery. Small 2016, 12, 4056–4062.

    Article  CAS  Google Scholar 

  43. Mu, X. P.; Li, J.; Yan, S. H.; Zhang, H. M.; Zhang, W. J.; Zhang, F. Q.; Jiang, J. L. siRNA delivery with stem cell membrane-coated magnetic nanoparticles for imaging-guided photothermal therapy and gene therapy. ACS Biomater. Sci. Eng. 2018, 4, 3895–3905.

    Article  CAS  Google Scholar 

  44. Wu, H. H.; Zhou, Y.; Tabata, Y.; Gao, J. Q. Mesenchymal stem cell-based drug delivery strategy: From cells to biomimetic. J. Control. Release 2019, 294, 102–113.

    Article  CAS  Google Scholar 

  45. Wang, H. J.; Liu, Y.; He, R. Q.; Xu, D. L.; Zang, J.; Weeranoppanant, N.; Dong, H. Q.; Li, Y. Y. Cell membrane biomimetic nanoparticles for inflammation and cancer targeting in drug delivery. Biomater. Sci. 2020, 8, 552–568.

    Article  CAS  Google Scholar 

  46. Yang, N.; Ding, Y. P.; Zhang, Y. L.; Wang, B.; Zhao, X.; Cheng, K. M.; Huang, Y. X.; Taleb, M.; Zhao, J.; Dong, W. F. et al. Surface functionalization of polymeric nanoparticles with umbilical cord-derived mesenchymal stem cell membrane for tumor-targeted therapy. ACS Appl. Mater. Interfaces 2018, 10, 22963–22973.

    Article  CAS  Google Scholar 

  47. Fang, R. H.; Hu, C. M. J.; Luk, B. T.; Gao, W. W.; Copp, J. A.; Tai, Y. Y.; O’Connor, D. E.; Zhang, L. F. Cancer cell membrane-coated nanoparticles for anticancer vaccination and drug delivery. Nano Lett. 2014, 14, 2181–2188.

    Article  CAS  Google Scholar 

  48. Nie, D.; Dai, Z.; Li, J. L.; Yang, Y. W.; Xi, Z. Y.; Wang, J.; Zhang, W.; Qian, K.; Guo, S. Y.; Zhu, C. L. et al. Cancer-cell-membrane-coated nanoparticles with a yolk-shell structure augment cancer chemotherapy. Nano Lett. 2020, 20, 936–946.

    Article  CAS  Google Scholar 

  49. Sun, H. P.; Su, J. H.; Meng, Q. S.; Yin, Q.; Chen, L. L.; Gu, W. W.; Zhang, P. C.; Zhang, Z. W.; Yu, H. J.; Wang, S. L. et al. Cancer-cell-biomimetic nanoparticles for targeted therapy of homotypic tumors. Adv. Mater. 2016, 28, 9581–9588.

    Article  CAS  Google Scholar 

  50. Feng, L. Z.; Tao, D. L.; Dong, Z. L.; Chen, Q.; Chao, Y.; Liu, Z.; Chen, M. W. Near-infrared light activation of quenched liposomal Ce6 for synergistic cancer phototherapy with effective skin protection. Biomaterials 2017, 127, 13–24.

    Article  CAS  Google Scholar 

  51. Li, J. C.; Rao, J. H.; Pu, K. Y. Recent progress on semiconducting polymer nanoparticles for molecular imaging and cancer phototherapy. Biomaterials 2018, 155, 217–235.

    Article  CAS  Google Scholar 

  52. Ding, S. S.; He, L.; Bian, X. W.; Tian, G Metal-organic frameworks-based nanozymes for combined cancer therapy. Nano Today 2020, 35, 100920.

    Article  CAS  Google Scholar 

  53. Cui, X. Z.; Zhou, Z. G.; Yang, Y.; Wei, J.; Wang, J.; Wang, M. W.; Yang, H.; Zhang, Y. J.; Yang, S. P. PEGylated WS2 nanosheets for X-ray computed tomography imaging and photothermal therapy. Chin. Chem. Lett. 2015, 26, 749–754.

    Article  CAS  Google Scholar 

  54. Lan, G. X.; Ni, K. Y.; Lin, W. B. Nanoscale metal-organic frameworks for phototherapy of cancer. Coord. Chem. Rev. 2019, 379, 65–81.

    Article  CAS  Google Scholar 

  55. Liu, Y. J.; Yang, Z.; Huang, X. L.; Yu, G. C.; Wang, S.; Zhou, Z. J.; Shen, Z. Y.; Fan, W. P.; Liu, Y.; Davisson, M. et al. Glutathione-responsive self-assembled magnetic gold nanowreath for enhanced tumor imaging and imaging-guided photothermal therapy. ACS Nano 2018, 12, 8129–8137.

    Article  CAS  Google Scholar 

  56. Gilson, R. C.; Black, K. C. L.; Lane, D. D.; Achilefu, S. Hybrid TiO2-ruthenium Nano-photosensitizer synergistically produces reactive oxygen species in both hypoxic and normoxic conditions. Angew. Chem., Int. Ed. 2017, 56, 10717–10720.

    Article  CAS  Google Scholar 

  57. Zhen, X.; Cheng, P. H.; Pu, K. Y. Recent advances in cell membrane-camouflaged nanoparticles for cancer phototherapy. Small 2019, 15, 1804105.

    Article  CAS  Google Scholar 

  58. Zhang, D.; Ye, Z. J.; Wei, L.; Luo, H. B.; Xiao, L. H. Cell membrane-coated porphyrin metal-organic frameworks for cancer cell targeting and O2-evolving photodynamic therapy. ACS Appl. Mater. Interfaces 2019, 11, 39594–39602.

    Article  CAS  Google Scholar 

  59. Liu, Y. J.; Bhattarai, P.; Dai, Z. F.; Chen, X. Y. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 2019, 48, 2053–2108.

    Article  CAS  Google Scholar 

  60. Bu, L. L.; Rao, L.; Yu, G. T.; Chen, L.; Deng, W. W.; Liu, J. F.; Wu, H.; Meng, Q. F.; Guo, S. S.; Zhao, X. Z. et al. Cancer stem cell-platelet hybrid membrane-coated magnetic nanoparticles for enhanced photothermal therapy of head and neck squamous cell carcinoma. Adv. Funct. Mater. 2019, 29, 1807733.

    Article  CAS  Google Scholar 

  61. Su, J. H.; Sun, H. P.; Meng, Q. S.; Yin, Q.; Zhang, P. C.; Zhang, Z. W.; Yu, H. J.; Li, Y. P. Bioinspired nanoparticles with NIR-controlled drug release for synergetic chemophotothermal therapy of metastatic breast cancer. Adv. Funct. Mater. 2016, 26, 7495–7506.

    Article  CAS  Google Scholar 

  62. Chen, Q.; Chen, J. W.; Liang, C.; Feng, L. Z.; Dong, Z. L.; Song, X. J.; Song, G. S.; Liu, Z. Drug-induced co-assembly of albumin/catalase as smart nano-theranostics for deep intra-tumoral penetration, hypoxia relieve, and synergistic combination therapy. J. Control. Release 2017, 263, 79–89.

    Article  CAS  Google Scholar 

  63. Zhai, Y. H.; Ran, W.; Su, J. H.; Lang, T. Q.; Meng, J.; Wang, G. R.; Zhang, P. C.; Li, Y. P. Traceable bioinspired nanoparticle for the treatment of metastatic breast cancer via NIR-trigged intracellular delivery of methylene blue and cisplatin. Adv. Mater. 2018, 30, 1802378.

    Article  CAS  Google Scholar 

  64. Xuan, M. J.; Shao, J. X.; Gao, C. Y.; Wang, W.; Dai, L. R.; He, Q. Self-propelled nanomotors for thermomechanically percolating cell membranes. Angew. Chem., Int. Ed. 2018, 57, 12463–12467.

    Article  CAS  Google Scholar 

  65. Han, Y. T.; Pan, H.; Li, W. J.; Chen, Z.; Ma, A. Q.; Yin, T.; Liang, R. J.; Chen, F. M.; Ma, Y. F.; Jin, Y. et al. T cell membrane mimicking nanoparticles with bioorthogonal targeting and immune recognition for enhanced photothermal therapy. Adv. Sci. 2019, 6, 1900251.

    Article  CAS  Google Scholar 

  66. Wan, S. S.; Cheng, Q.; Zeng, X.; Zhang, X. Z. A Mn(III)-sealed metal-organic framework nanosystem for redox-unlocked tumor theranostics. ACS Nano 2019, 13, 6561–6571.

    Article  CAS  Google Scholar 

  67. Sun, H. P.; Su, J. H.; Meng, Q. S.; Yin, Q.; Chen, L. L.; Gu, W. W.; Zhang, Z. W.; Yu, H. J.; Zhang, P. C.; Wang, S. L. et al. Cancer cell membrane-coated gold nanocages with hyperthermia-triggered drug release and homotypic target inhibit growth and metastasis of breast cancer. Adv. Funct. Mater. 2017, 27, 1604300.

    Article  CAS  Google Scholar 

  68. Sang, W.; Zhang, Z.; Dai, Y. L.; Chen, X. Y. Recent advances in nanomaterial-based synergistic combination cancer immunotherapy. Chem. Soc. Rev. 2019, 48, 3771–3810.

    Article  Google Scholar 

  69. Ott, P. A.; Hu, Z. T.; Keskin, D. B.; Shukla, S. A.; Sun, J.; Bozym, D. J.; Zhang, W. D.; Luoma, A.; Giobbie-Hurder, A.; Peter, L. et al. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature 2017, 547, 217–221.

    Article  CAS  Google Scholar 

  70. June, C. H.; O’Connor, R. S.; Kawalekar, O. U.; Ghassemi, S.; Milone, M. C. CAR T cell immunotherapy for human cancer. Science 2018, 359, 1361–1365.

    Article  CAS  Google Scholar 

  71. Banchereau, J.; Palucka, K. Immunotherapy: Cancer vaccines on the move. Nat. Rev. Clin. Oncol. 2018, 15, 9–10.

    Article  Google Scholar 

  72. Palucka, K.; Banchereau, J. Cancer immunotherapy via dendritic cells. Nat. Rev. Cancer 2012, 72, 265–277.

    Article  CAS  Google Scholar 

  73. Yang, Y. P. Cancer immunotherapy: Harnessing the immune system to battle cancer. J. Clin. Invest. 2015, 125, 3335–3337.

    Article  Google Scholar 

  74. Ye, X. Y.; Liang, X.; Chen, Q.; Miao, Q. W.; Chen, X. L.; Zhang, X. D.; Mei, L. Surgical tumor-derived personalized photothermal vaccine formulation for cancer immunotherapy. ACS Nano 2019, 13, 2956–2968.

    Article  CAS  Google Scholar 

  75. Han, X.; Shen, S. F.; Fan, Q.; Chen, G. J.; Archibong, E.; Dotti, G.; Liu, Z.; Gu, Z.; Wang, C. Red blood cell-derived nanoerythrosome for antigen delivery with enhanced cancer immunotherapy. Sci. Adv. 2019, 5, eaaw6870.

    Article  CAS  Google Scholar 

  76. Ochyl, L. J.; Moon, J. J. Dendritic cell membrane vesicles for activation and maintenance of antigen-specific T cells. Adv. Healthc. Mater. 2019, 8, 1801091.

    Article  CAS  Google Scholar 

  77. 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. et al. Expandable immunotherapeutic nanoplatforms engineered from cytomembranes of hybrid cells derived from cancer and dendritic cells. Adv. Mater. 2019, 37, 1900499.

    Article  CAS  Google Scholar 

  78. Li, S. Y.; Wang, Q.; Shen, Y. Q.; Hassan, M.; Shen, J. Z.; Jiang, W.; Su, Y. T.; Chen, J.; Bai, L.; Zhou, W. C. et al. Pseudoneutrophil cytokine sponges disrupt myeloid expansion and tumor trafficking to improve cancer immunotherapy. Nano Lett. 2020, 20, 242–251.

    Article  CAS  Google Scholar 

  79. Cheng, S. S.; Xu, C.; Jin, Y.; Li, Y.; Zhong, C.; Ma, J.; Yang, J. N.; Zhang, N.; Li, Y.; Wang, C. et al. Artificial mini dendritic cells boost T cell-based immunotherapy for ovarian cancer. Adv. Sci. 2020, 7, 1903301.

    Article  CAS  Google Scholar 

  80. Zou, M. Z.; Liu, W. L.; Gao, F.; Bai, X. F.; Chen, H. S.; Zeng, X.; Zhang, X. Z. Artificial natural killer cells for specific tumor inhibition and renegade macrophage re-education. Adv. Mater. 2019, 31, 1904495.

    Article  CAS  Google Scholar 

  81. Deng, G. J.; Sun, Z. H.; Li, S. P.; Peng, X. H.; Li, W. J.; Zhou, L. H.; Ma, Y. F.; Gong, P.; Cai, L. T. 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.

    Article  CAS  Google Scholar 

  82. Cheng, Y. H.; Cheng, H.; Jiang, C. X.; Qiu, X. F.; Wang, K. K.; Huan, W.; Yuan, A. H.; Wu, J. H.; Hu, Y. Q. Perfluorocarbon nanoparticles enhance reactive oxygen levels and tumour growth inhibition in photodynamic therapy. Nat. Commun. 2015, 6, 8785.

    Article  CAS  Google Scholar 

  83. Haney, C. R.; Buehler, P. W.; Gulati, A. Purification and chemical modifications of hemoglobin in developing hemoglobin based oxygen carriers. Adv. Drug Deliv. Rev. 2000, 40, 153–169.

    Article  CAS  Google Scholar 

  84. Zhu, W. W.; Dong, Z. L.; Fu, T. T.; Liu, J. J.; Chen, Q.; Li, Y. G.; Zhu, R.; Xu, L. G.; Liu, Z. Modulation of hypoxia in solid tumor microenvironment with MnO2 nanoparticles to enhance photodynamic therapy. Adv. Funct. Mater. 2016, 26, 5490–5498.

    Article  CAS  Google Scholar 

  85. Phua, S. Z. F.; Yang, G. B.; Lim, W. Q.; Verma, A.; Chen, H. Z.; Thanabalu, T.; Zhao, Y. L. Catalase-integrated hyaluronic acid as nanocarriers for enhanced photodynamic therapy in solid tumor. ACS Nano 2019, 13, 4742–4751.

    Article  CAS  Google Scholar 

  86. Li, C.; Yang, X. Q.; An, J.; Cheng, K.; Hou, X. L.; Zhang, X. S.; Hu, Y. G.; Liu, B.; Zhao, Y. D. Red blood cell membrane-enveloped O2 self-supplementing biomimetic nanoparticles for tumor imaging-guided enhanced sonodynamic therapy. Theranostics 2020, 10, 867–879.

    Article  CAS  Google Scholar 

  87. Russell, S. J.; Peng, K. W.; Bell, J. C. Oncolytic virotherapy. Nat. Biotechnol. 2012, 30, 658–670.

    Article  CAS  Google Scholar 

  88. Lv, P.; Liu, X.; Chen, X. M.; Liu, C.; Zhang, Y.; Chu, C. C.; Wang, J. Q.; Wang, X. Y.; Chen, X. Y.; Liu, G. Genetically engineered cell membrane nanovesicles for oncolytic adenovirus delivery: A versatile platform for cancer virotherapy. Nano Lett. 2019, 79, 2993–3001.

    Article  CAS  Google Scholar 

  89. Kobayashi, H.; Choyke, P. L. Target-cancer-cell-specific activatable fluorescence imaging probes: Rational design and in vivo applications. Acc. Chem. Res. 2011, 44, 83–90.

    Article  CAS  Google Scholar 

  90. Rao, L.; Meng, Q. F.; Bu, L. L.; Cai, B.; Huang, Q. Q.; Sun, Z. J.; Zhang, W. F.; Li, A.; Guo, S. S.; Liu, W. et al. Erythrocyte membrane-coated upconversion nanoparticles with minimal protein adsorption for enhanced tumor imaging. ACS Appl. Mater. Interfaces 2017, 9, 2159–2168.

    Article  CAS  Google Scholar 

  91. 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. et al. Cancer cell membrane-coated upconversion nanoprobes for highly specific tumor imaging. Adv. Mater. 2016, 28, 3460–3466.

    Article  CAS  Google Scholar 

  92. Lv, Y. L.; Liu, M.; Zhang, Y.; Wang, X. F.; Zhang, F.; Li, F.; Bao, W. E.; Wang, J.; Zhang, Y. L.; Wei, W. et al. Cancer cell membrane-biomimetic nanoprobes with two-photon excitation and near-infrared emission for intravital tumor fluorescence imaging. ACS Nano 2018, 12, 1350–1358.

    Article  CAS  Google Scholar 

  93. Zhang, J. J.; Lin, Y.; Zhou, H.; He, H.; Ma, J. J.; Luo, M. Y.; Zhang, Z. L.; Pang, D. W. Cell membrane-camouflaged NIR II fluorescent Ag2Te quantum dots-based nanobioprobes for enhanced in vivo homotypic tumor imaging. Adv. Healthc. Mater. 2019, 8, 1900341.

    Article  CAS  Google Scholar 

  94. Antaris, A. L.; Chen, H.; Cheng, K.; Sun, Y.; Hong, G. S.; Qu, C. R.; Diao, S.; Deng, Z. X.; Hu, X. M.; Zhang, B. et al. A small-molecule dye for NIR-II imaging. Nat. Mater. 2015, 15, 235–242.

    Article  CAS  Google Scholar 

  95. Zhu, S. J.; Tian, R.; Antaris, A. L.; Chen, X. Y.; Dai, H. J. Near-infrared-II molecular dyes for cancer imaging and surgery. Adv. Mater. 2019, 31, 1900321.

    Article  CAS  Google Scholar 

  96. Zhang, X.; He, S. Q.; Ding, B. B.; Qu, C. R.; Zhang, Q.; Chen, H.; Sun, Y.; Fang, H. Y.; Long, Y.; Zhang, R. P. et al. Cancer cell membrane-coated rare earth doped nanoparticles for tumor surgery navigation in NIR-II imaging window. Chem. Eng. J. 2020, 385, 123959.

    Article  CAS  Google Scholar 

  97. Jalandhara, N.; Arora, R.; Batuman, V. Nephrogenic systemic fibrosis and gadolinium-containing radiological contrast agents: An update. Clin. Pharmacol. Ther. 2011, 89, 920–923.

    Article  CAS  Google Scholar 

  98. Nguyen, T. D. T.; Marasini, R.; Rayamajhi, S.; Aparicio, C.; Biller, D.; Aryal, S. Erythrocyte membrane concealed paramagnetic polymeric nanoparticle for contrast-enhanced magnetic resonance imaging. Nanoscale 2020, 12, 4137–4149.

    Article  CAS  Google Scholar 

  99. Pitchaimani, A.; Nguyen, T. D. T.; Marasini, R.; Eliyapura, A.; Azizi, T.; Jaberi-Douraki, M.; Aryal, S. Biomimetic natural killer membrane camouflaged polymeric nanoparticle for targeted bioimaging. Adv. Funct. Mater. 2019, 29, 1806817.

    Article  CAS  Google Scholar 

  100. Pantel, K.; Alix-Panabières, C. The clinical significance of circulating tumor cells. Nat. Rev. Clin. Oncol. 2007, 4, 62–63.

    Article  Google Scholar 

  101. Plaks, V.; Koopman, C. D.; Werb, Z. Circulating tumor cells. Science 2013, 341, 1186–1188.

    Article  CAS  Google Scholar 

  102. Wang, L. X.; Asghar, W.; Demirci, U.; Wan, Y. Nanostructured substrates for isolation of circulating tumor cells. Nano Today 2013, 8, 347–387.

    Google Scholar 

  103. Shen, Z. Y.; Wu, A. G.; Chen, X. Y. Current detection technologies for circulating tumor cells. Chem. Soc. Rev. 2017, 46, 2038–2056.

    Article  CAS  Google Scholar 

  104. Xiong, K.; Wei, W.; Jin, Y. J.; Wang, S. M.; Zhao, D. X.; Wang, S.; Gao, X. Y.; Qiao, C. M.; Yue, H.; Ma, G. H. et al. Biomimetic immuno-magnetosomes for high-performance enrichment of circulating tumor cells. Adv. Mater. 2016, 28, 7929–7935.

    Article  CAS  Google Scholar 

  105. Zhou, X. X.; Luo, B.; Kang, K.; Zhang, Y. J.; Jiang, P. P.; Lan, F.; Yi, Q. Y.; Wu, Y. Leukocyte-repelling biomimetic immunomagnetic nanoplatform for high-performance circulating tumor cells isolation. Small 2019, 15, 1900558.

    Article  CAS  Google Scholar 

  106. Rao, L.; Meng, Q. F.; Huang, Q. Q.; Wang, Z. X.; Yu, G. T.; Li, A.; Ma, W. J.; Zhang, N. G.; Guo, S. S.; Zhao, X. Z. et al. Platelet-leukocyte hybrid membrane-coated immunomagnetic beads for highly efficient and highly specific isolation of circulating tumor cells. Adv. Funct. Mater. 2018, 28, 1803531.

    Article  CAS  Google Scholar 

  107. Ding, C. P.; Zhang, C. L.; Cheng, S. S.; Xian, Y. Z. Multivalent aptamer functionalized Ag2S nanodots/hybrid cell membrane-coated magnetic nanobioprobe for the ultrasensitive isolation and detection of circulating tumor cells. Adv. Funct. Mater. 2020, 30, 1909781.

    Article  CAS  Google Scholar 

  108. Chen, H. M.; Zhang, W. Z.; Zhu, G Z.; Xie, J.; Chen, X. Y. Rethinking cancer nanotheranostics. Nat. Rev. Mater 2017, 2, 17024.

    Article  CAS  Google Scholar 

  109. Ye, S. F.; Wang, F. F.; Fan, Z. X.; Zhu, Q. X.; Tian, H. N.; Zhang, Y. B.; Jiang, B. L.; Hou, Z. Q.; Li, Y.; Su, G. H. Light/pH-triggered biomimetic red blood cell membranes camouflaged small molecular drug assemblies for imaging-guided combinational chemophotothermal therapy. ACS Appl. Mater. Interfaces 2019, 11, 15262–15275.

    Article  CAS  Google Scholar 

  110. Rao, L.; Cai, B.; Bu, L. L.; Liao, Q. Q.; Guo, S. S.; Zhao, X. Z.; Dong, W. F.; Liu, W. Microfluidic electroporation-facilitated synthesis of erythrocyte membrane-coated magnetic nanoparticles for enhanced imaging-guided cancer therapy. ACS Nano 2017, 11, 3496–3505.

    Article  CAS  Google Scholar 

  111. Xiao, F.; Fan, J. L.; Tong, C. Y.; Xiao, C.; Wang, Z.; Liu, B.; Daniyal, M.; Wang, W. An erythrocyte membrane coated mimetic nano-platform for chemo-phototherapy and multimodal imaging. RSC Adv. 2019, 9, 27911–27926.

    Article  CAS  Google Scholar 

  112. Wu, M. L.; Mei, T. X.; Lin, C. Y.; Wang, Y. C.; Chen, J. Y.; Le, W. J.; Sun, M. Y.; Xu, J. G.; Dai, H. Y.; Zhang, Y. F. et al. Melanoma cell membrane biomimetic versatile CuS nanoprobes for homologous targeting photoacoustic imaging and photothermal chemotherapy. ACS Appl. Mater. Interfaces 2020, 12, 16031–16039.

    Article  CAS  Google Scholar 

  113. Li, J.; Wang, X. D.; Zheng, D. Y.; Lin, X. Y.; Wei, Z. W.; Zhang, D.; Li, Z. F.; Zhang, Y.; Wu, M.; Liu, X. L. Cancer cell membrane-coated magnetic nanoparticles for MR/NIR fluorescence dual-modal imaging and photodynamic therapy. Biomater. Sci. 2018, 6, 1834–1845.

    Article  CAS  Google Scholar 

  114. Chen, Z.; Zhao, P. F.; Luo, Z. Y.; Zheng, M. B.; Tian, H.; Gong, P.; Gao, G. H.; Pan, H.; Liu, L. L.; Ma, A. Q. et al. Cancer cell membrane-biomimetic nanoparticles for homologous-targeting dual-modal imaging and photothermal therapy. ACS Nano 2016, 10, 10049–10057.

    Article  CAS  Google Scholar 

  115. Taubes, G. The bacteria fight back. Science 2008, 321, 356–361.

    Article  CAS  Google Scholar 

  116. Angsantikul, P.; Thamphiwatana, S.; Zhang, Q. Z.; Spiekermann, K.; Zhuang, J.; Fang, R. H.; Gao, W. W.; Obonyo, M.; Zhang, L. F. Coating nanoparticles with gastric epithelial cell membrane for targeted antibiotic delivery against Helicobacter pylori infection. Adv. Ther. 2018, 1, 1800016.

    Article  CAS  Google Scholar 

  117. Kaplan-Türköz, B.; Jiménez-Soto, L. F.; Dian, C.; Ertl, C.; Remaut, H.; Louche, A.; Tosi, T.; Haas, R.; Terradot, L. Structural insights into Helicobacter pylori oncoprotein CagA interaction with β1 integrin. Proc. Natl. Acad. Sci. USA 2012, 109, 14640–14645.

    Article  Google Scholar 

  118. Parreira, P.; Shi, Q.; Magalhaes, A.; Reis, C. A.; Bugaytsova, J.; Borén, T.; Leckband, D.; Martins, M. C. L. Atomic force microscopy measurements reveal multiple bonds between Helicobacter pylori blood group antigen binding adhesin and Lewis b ligand. J. Roy. Soc. Interface 2014, 11, 20141040.

    Article  CAS  Google Scholar 

  119. Wang, C.; Wang, Y. L.; Zhang, L. L.; Miron, R. J.; Liang, J. F.; Shi, M. S.; Mo, W. T.; Zheng, S. H.; Zhao, Y. B.; Zhang, Y. F. Pretreated macrophage-membrane-coated gold nanocages for precise drug delivery for treatment of bacterial infections. Adv. Mater. 2018, 30, 1804023.

    Article  CAS  Google Scholar 

  120. Gilbert, R. J. C. Pore-forming toxins. Cell. Mol. Life Sci. 2002, 59, 832–844.

    Article  CAS  Google Scholar 

  121. Los, F. C. O.; Randis, T. M.; Aroian, R. V.; Ratner, A. J. Role of pore-forming toxins in bacterial infectious diseases. Microbiol. Mol. Biol. Rev. 2013, 77, 173–207.

    Article  CAS  Google Scholar 

  122. Edelson, B. T.; Unanue, E. R. Intracellular antibody neutralizes Listeria growth. Immunity 2001, 14, 503–512.

    Article  CAS  Google Scholar 

  123. Wang, F.; Gao, W. W.; Thamphiwatana, S.; Luk, B. T.; Angsantikul, P.; Zhang, Q. Z.; Hu, C. M. J.; Fang, R. H.; Copp, J. A.; Pornpattananangkul, D. et al. Hydrogel retaining toxin-absorbing nanosponges for local treatment of methicillin- resistant Staphylococcus aureus infection. Adv. Mater. 2015, 27, 3437–3443.

    Article  CAS  Google Scholar 

  124. Hu, C. M. J.; Fang, R. H.; Copp, J.; Luk, B. T.; Zhang, L. F. A biomimetic nanosponge that absorbs pore-forming toxins. Nat. Nanotechnol. 2013, 8, 336–340.

    Article  CAS  Google Scholar 

  125. Chen, Y. J.; Zhang, Y.; Chen, M. C.; Zhuang, J.; Fang, R. H.; Gao, W. W.; Zhang, L. F. Biomimetic nanosponges suppress in vivo lethality induced by the whole secreted proteins of pathogenic bacteria. Small 2019, 15, 1804994.

    Article  CAS  Google Scholar 

  126. Wu, Z. G.; Li, T. L.; Gao, W.; Xu, T. L.; Jurado-Sánchez, B.; Li, J. X.; Gao, W. W.; He, Q.; Zhang, L. F.; Wang, J. Cell-membrane-coated synthetic nanomotors for effective biodetoxification. Adv. Funct. Mater. 2015, 25, 3881–3887.

    Article  CAS  Google Scholar 

  127. De Ávila, B. E. F.; Angsantikul, P.; Ramírez-Herrera, D. E.; Soto, F.; Teymourian, H.; Dehaini, D.; Chen, Y. J.; Zhang, L. F.; Wang, J. Hybrid biomembrane-functionalized nanorobots for concurrent removal of pathogenic bacteria and toxins. Sci. Robot. 2018, 3, eaat0485.

    Article  Google Scholar 

  128. Atkins, K. E.; Lipsitch, M. Can antibiotic resistance be reduced by vaccinating against respiratory disease? Lancet Respir. Med. 2018, 6, 820–821.

    Article  Google Scholar 

  129. Andre, F. E.; Booy, R.; Bock, H. L.; Clemens, J.; Datta, S. K.; John, T. J.; Lee, B. W.; Lolekha, S.; Peltola, H.; Ruff, T. A. et al. Vaccination greatly reduces disease, disability, death and inequity worldwide. Bull. World Health Organ. 2008, 86, 140–146.

    Article  CAS  Google Scholar 

  130. Pollard, A. J.; Perrett, K. P.; Beverley, P. C. Maintaining protection against invasive bacteria with protein-polysaccharide conjugate vaccines. Nat. Rev. Immunol. 2009, 9, 213–220.

    Article  CAS  Google Scholar 

  131. Cordeiro, A. S.; Alonso, M. J.; de la Fuente, M. Nanoengineering of vaccines using natural polysaccharides. Biotechnol. Adv. 2015, 33, 1279–1293.

    Article  CAS  Google Scholar 

  132. Bundle, D. Antibacterials: A sweet vaccine. Nat. Chem. 2016, 8, 201–202.

    Article  CAS  Google Scholar 

  133. Micoli, F.; Costantino, P.; Adamo, R. Potential targets for next generation antimicrobial glycoconjugate vaccines. FEMS Microbiol. Rev. 2018, 42, 388–423.

    Article  CAS  Google Scholar 

  134. Gao, W. W.; Fang, R. H.; Thamphiwatana, S.; Luk, B. T.; Li, J. M.; Angsantikul, P.; Zhang, Q. Z.; Hu, C. M. J.; Zhang, L. F. Modulating antibacterial immunity via bacterial membrane-coated nanoparticles. Nano Lett. 2015, 15, 1403–1409.

    Article  CAS  Google Scholar 

  135. Wang, S. H.; Gao, J.; Li, M.; Wang, L. G.; Wang, Z. J. A facile approach for development of a vaccine made of bacterial double-layered membrane vesicles (DMVs). Biomaterials 2018, 187, 28–38.

    Article  CAS  Google Scholar 

  136. Angsantikul, P.; Thamphiwatana, S.; Gao, W. W.; Zhang, L. F. Cell membrane-coated nanoparticles as an emerging antibacterial vaccine platform. Vaccines 2015, 3, 814–828.

    Article  CAS  Google Scholar 

  137. Hu, C. M. J.; Zhang, L. F. Nanotoxoid vaccines. Nano Today 2014, 9, 401–404.

    Article  CAS  Google Scholar 

  138. Wei, X. L.; Beltrán-Gastélum, M.; Karshalev, E.; de Ávila, B. E. F.; Zhou, J. R.; Ran, D. N.; Angsantikul, P.; Fang, R. H.; Wang, J.; Zhang, L. F. Biomimetic micromotor enables active delivery of antigens for oral vaccination. Nano Lett. 2019, 19, 1914–1921.

    Article  CAS  Google Scholar 

  139. Pang, X.; Liu, X.; Cheng, Y.; Zhang, C.; Ren, E.; Liu, C.; Zhang, Y.; Zhu, J.; Chen, X. Y.; Liu, G. Sono-immunotherapeutic nanocapturer to combat multidrug-resistant bacterial infections. Adv. Mater. 2019, 37, 1902530.

    Article  CAS  Google Scholar 

  140. Hajipour, M. J.; Fromm, K. M.; Ashkarran, A. A.; de Aberasturi, D. J.; de Larramendi, I. R.; Rojo, T.; Serpooshan, V.; Parak, W. J.; Mahmoudi, M. Antibacterial properties of nanoparticles. Trends Biotechnol. 2012, 30, 499–511.

    Article  CAS  Google Scholar 

  141. Miller, K. P.; Wang, L.; Benicewicz, B. C.; Decho, A. W. Inorganic nanoparticles engineered to attack bacteria. Chem. Soc. Rev. 2015, 44, 7787–7807.

    Article  CAS  Google Scholar 

  142. Wang, G. M.; Jin, W. H.; Qasim, A. M.; Gao, A.; Peng, X.; Li, W.; Feng, H. Q.; Chu, P. K. Antibacterial effects of titanium embedded with silver nanoparticles based on electron-transfer-induced reactive oxygen species. Biomaterials 2017, 124, 25–34.

    Article  CAS  Google Scholar 

  143. Chernousova, S.; Epple, M. Silver as antibacterial agent: Ion, nanoparticle, and metal. Angew. Chem., Int. Ed. 2013, 52, 1636–1653.

    Article  CAS  Google Scholar 

  144. Huang, X. Q.; Chen, X.; Chen, Q. C.; Yu, Q. Q.; Sun, D. D.; Liu, J. Investigation of functional selenium nanoparticles as potent antimicrobial agents against superbugs. Acta Biomater. 2016, 30, 397–407.

    Article  CAS  Google Scholar 

  145. Lin, A. G.; Liu, Y. N.; Zhu, X. F.; Chen, X.; Liu, J. W.; Zhou, Y. H.; Qin, X. Y.; Liu, J. Bacteria-responsive biomimetic selenium nanosystem for multidrug-resistant bacterial infection detection and inhibition. ACS Nano 2019, 13, 13965–13984.

    Article  CAS  Google Scholar 

  146. Abbott, N. J.; Rönnbäck, L.; Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7, 41–53.

    Article  CAS  Google Scholar 

  147. Abbott, N. J.; Patabendige, A. A. K.; Dolman, D. E. M.; Yusof, S. R.; Begley, D. J. Structure and function of the blood-brain barrier. Neurobiol. Dis. 2010, 37, 13–25.

    Article  CAS  Google Scholar 

  148. Serlin, Y.; Shelef, I.; Knyazer, B.; Friedman, A. Anatomy and physiology of the blood-brain barrier. Semin. Cell Dev. Biol. 2015, 38, 2–6.

    Article  Google Scholar 

  149. Chen, Y.; Liu, L. H. Modern methods for delivery of drugs across the blood-brain barrier. Adv. Drug Deliv. Rev. 2012, 64, 640–665.

    Article  CAS  Google Scholar 

  150. Tsou, Y. H.; Zhang, X. Q.; Zhu, H.; Syed, S.; Xu, X. Y. Drug delivery to the brain across the blood-brain barrier using nanomaterials. Small 2017, 13, 1701921.

    Article  CAS  Google Scholar 

  151. Wu, M. Y.; Chen, W. T.; Chen, Y.; Zhang, H. X.; Liu, C. B.; Deng, Z. T.; Sheng, Z. H.; Chen, J. Q.; Liu, X.; Yan, F. et al. Focused ultrasound-augmented delivery of biodegradable multifunctional nanoplatforms for imaging-guided brain tumor treatment. Adv. Sci. 2018, 5, 1700474.

    Article  CAS  Google Scholar 

  152. Tang, W.; Fan, W. P.; Lau, J.; Deng, L. M.; Shen, Z. Y.; Chen, X. Y. Emerging blood-brain-barrier-crossing nanotechnology for brain cancer theranostics. Chem. Soc. Rev. 2019, 48, 2967–3014.

    Article  CAS  Google Scholar 

  153. Omuro, A.; DeAngelis, L. M. Glioblastoma and other malignant gliomas: A clinical review. JAMA 2013, 310, 1842–1850.

    Article  CAS  Google Scholar 

  154. Rich, J. N.; Bigner, D. D. Development of novel targeted therapies in the treatment of malignant glioma. Nat. Rev. Drug Discov. 2004, 3, 430–446.

    Article  CAS  Google Scholar 

  155. van Meir, E. G.; Hadjipanayis, C. G.; Norden, A. D.; Shu, H. K.; Wen, P. Y.; Olson, J. J. Exciting new advances in neuro-oncology: The avenue to a cure for malignant glioma. CA Cancer J. Clin. 2010, 60, 166–193.

    Article  Google Scholar 

  156. Zou, Y.; Liu, Y. J.; Yang, Z. P.; Zhang, D. Y.; Lu, Y. Q.; Zheng, M.; Xue, X.; Geng, J.; Chung, R.; Shi, B. Y. Effective and targeted human orthotopic glioblastoma xenograft therapy via a multifunctional biomimetic nanomedicine. Adv. Mater. 2018, 30, 1803717.

    Article  CAS  Google Scholar 

  157. Chai, Z. L.; Ran, D. N.; Lu, L. W.; Zhan, C. Y.; Ruan, H. T.; Hu, X. F.; Xie, C.; Jiang, K.; Li, J. Y.; Zhou, J. F. et al. Ligand-modified cell membrane enables the targeted delivery of drug nanocrystals to glioma. ACS Nano 2019, 13, 5591–5601.

    Article  CAS  Google Scholar 

  158. Fu, S. Y.; Liang, M.; Wang, Y. L.; Cui, L.; Gao, C. H.; Chu, X. Y.; Liu, Q. Q.; Feng, Y.; Gong, W.; Yang, M. Y. et al. Dual-modified novel biomimetic nanocarriers improve targeting and therapeutic efficacy in glioma. ACSAppl. Mater. Interfaces 2019, 11, 1841–1854.

    Article  CAS  Google Scholar 

  159. Liu, Y. J.; Zou, Y.; Feng, C.; Lee, A.; Yin, J. L.; Chung, R.; Park, J. B.; Rizos, H.; Tao, W.; Zheng, M. et al. Charge conversional biomimetic nanocomplexes as a multifunctional platform for boosting orthotopic glioblastoma RNAi therapy. Nano Lett. 2020, 20, 1637–1646.

    Article  CAS  Google Scholar 

  160. Bose, R. J.; Paulmurugan, R.; Moon, J.; Lee, S. H.; Park, H. Cell membrane-coated nanocarriers: The emerging targeted delivery system for cancer theranostics. Drug Discov. Today 2018, 23, 891–899.

    Article  CAS  Google Scholar 

  161. Jia, Y. L.; Wang, X. B.; Hu, D. H.; Wang, P.; Liu, Q. H.; Zhang, X. J.; Jiang, J. Y.; Liu, X.; Sheng, Z. H.; Liu, B. et al. Phototheranostics: Active targeting of orthotopic glioma using biomimetic proteolipid nanoparticles. ACS Nano 2019, 13, 386–398.

    Article  CAS  Google Scholar 

  162. Tapeinos, C.; Tomatis, F.; Battaglini, M.; Larrañaga, A.; Marino, A.; Telleria, I. A.; Angelakeris, M.; Debellis, D.; Drago, F.; Brero, F. et al. Cell membrane-coated magnetic nanocubes with a homotypic targeting ability increase intracellular temperature due to ROS scavenging and act as a versatile theranostic system for glioblastoma multiforme. Adv. Healthc. Mater. 2019, 8, 1900612.

    Article  CAS  Google Scholar 

  163. Wang, C. X.; Wu, B.; Wu, Y. T.; Song, X. Y.; Zhang, S. S.; Liu, Z. H. Camouflaging nanoparticles with brain metastatic tumor cell membranes: A new strategy to traverse blood-brain barrier for imaging and therapy of brain tumors. Adv. Funct. Mater. 2020, 30, 1909369.

    Article  CAS  Google Scholar 

  164. Hacke, W.; Kaste, M.; Bluhmki, E.; Brozman, M.; Dávalos, A.; Guidetti, D.; Larrue, V.; Lees, K. R.; Medeghri, Z.; Machnig, T. et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N. Engl. J. Med. 2008, 359, 1317–1329.

    Article  CAS  Google Scholar 

  165. Rothwell, P. M. Is intravenous recombinant plasminogen activator effective up to 4.5 h after onset of ischemic stroke? Nat. Rev. Cardiol. 2009, 6, 164–165.

    Article  CAS  Google Scholar 

  166. Georgiadis, D.; Engelter, S.; Tettenborn, B.; Hungerbühler, H.; Luethy, R.; Müller, F.; Arnold, M.; Giambarba, C.; Baumann, C. R.; von Büdingen, H. C. et al. Early recurrent ischemic stroke in stroke patients undergoing intravenous thrombolysis. Circulation 2006, 114, 237–241.

    Article  Google Scholar 

  167. Slomski, A. Rapid blood pressure reduction safe for ischemic stroke. JAMA 2019, 321, 1558.

    Google Scholar 

  168. Zhou, Z. H.; Lu, J. F.; Liu, W. W.; Manaenko, A.; Hou, X. H.; Mei, Q. Y.; Huang, J. L.; Tang, J. P.; Zhang, J. H.; Yao, H. H. et al. Advances in stroke pharmacology. Pharmacol. Ther. 2018, 191, 23–42.

    Article  CAS  Google Scholar 

  169. Nesbitt, W. S.; Westein, E.; Tovar-Lopez, F. J.; Tolouei, E.; Mitchell, A.; Fu, J.; Carberry, J.; Fouras, A.; Jackson, S. P. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat. Med. 2009, 15, 665–673.

    Article  CAS  Google Scholar 

  170. Xu, J. C.; Zhang, Y. L.; Xu, J. Q.; Liu, G. N.; Di, C. Z.; Zhao, X.; Li, X.; Li, Y.; Pang, N. B.; Yang, C. Z. et al. Engineered nanoplatelets for targeted delivery of plasminogen activators to reverse thrombus in multiple mouse thrombosis models. Adv. Mater. 2020, 32, 1905145.

    Article  CAS  Google Scholar 

  171. Li, M. X.; Li, J.; Chen, J. P.; Liu, Y.; Cheng, X.; Yang, F.; Gu, N. Platelet membrane biomimetic magnetic nanocarriers for targeted delivery and in situ generation of nitric oxide in early ischemic stroke. ACS Nano 2020, 14, 2024–2035.

    Article  CAS  Google Scholar 

  172. Xu, J. P.; Wang, X. Q.; Yin, H. Y.; Cao, X.; Hu, Q. Y.; Lv, W.; Xu, Q. W.; Gu, Z.; Xin, H. L. Sequentially site-specific delivery of thrombolytics and neuroprotectant for enhanced treatment of ischemic stroke. ACS Nano 2019, 13, 8577–8588.

    Article  CAS  Google Scholar 

  173. Dong, X. Y.; Gao, J.; Zhang, C. Y.; Hayworth, C.; Frank, M.; Wang, Z. J. Neutrophil membrane-derived nanovesicles alleviate inflammation to protect mouse brain injury from ischemic stroke. ACS Nano 2019, 13, 1272–1283.

    CAS  Google Scholar 

  174. Lv, W.; Xu, J. P.; Wang, X. Q.; Li, X. R.; Xu, Q. W.; Xin, H. L. Bioengineered boronic ester modified dextran polymer nanoparticles as reactive oxygen species responsive nanocarrier for ischemic stroke treatment. ACS Nano 2018, 12, 5417–5426.

    Article  CAS  Google Scholar 

  175. Lusis, A. J. Atherosclerosis. Nature 2000, 407, 233–241.

    Article  CAS  Google Scholar 

  176. Stehbens, W. E. The role of lipid in the pathogenesis of atherosclerosis. Lancet 1975, 305, 724–727.

    Article  Google Scholar 

  177. Falk, E. Pathogenesis of atherosclerosis. J. Am. Coll. Cardiol. 2006, 47, C7–C12.

    Article  CAS  Google Scholar 

  178. Wei, X. L.; Ying, M.; Dehaini, D.; Su, Y. Y.; Kroll, A. V.; Zhou, J. R.; Gao, W. W.; Fang, R. H.; Chien, S.; Zhang, L. F. Nanoparticle functionalization with platelet membrane enables multifactored biological targeting and detection of atherosclerosis. ACS Nano 2018, 12, 109–116.

    Article  CAS  Google Scholar 

  179. Wang, Y.; Zhang, K.; Qin, X.; Li, T. H.; Qiu, J. H.; Yin, T. Y.; Huang, J. L.; McGinty, S.; Pontrelli, G.; Ren, J. et al. Biomimetic nanotherapies: Red blood cell based core-shell structured nano-complexes for atherosclerosis management. Adv. Sci. 2019, 6, 1900172.

    Article  CAS  Google Scholar 

  180. Firestein, G. S. Evolving concepts of rheumatoid arthritis. Nature 2003, 423, 356–361.

    Article  CAS  Google Scholar 

  181. Scott, D. L.; Wolfe, F.; Huizinga, T. W. J. Rheumatoid arthritis. Lancet 2010, 376, 1094–1108.

    Article  Google Scholar 

  182. Smolen, S. J.; Aletaha, D.; Barton, A.; Burmester, R. G.; Emery, P.; Firestein, S. G.; Kavanaugh, A.; McInnes, I. B.; Solomon, D. H.; Strand, V. et al. Rheumatoid arthritis. Nat. Rev. Dis. Primers 2018, 4, 18001.

    Article  Google Scholar 

  183. Fontana, F.; Albertini, S.; Correia, A.; Kemell, M.; Lindgren, R.; Mäkilä, E.; Salonen, J.; Hirvonen, J. T.; Ferrari, F.; Santos, H. A. Bioengineered porous silicon Nanoparticles@Macrophages cell membrane as composite platforms for rheumatoid arthritis. Adv. Funct. Mater. 2018, 28, 1801355.

    Article  CAS  Google Scholar 

  184. Jin, K.; Luo, Z. M.; Zhang, B.; Pang, Z. Q. Biomimetic nanoparticles for inflammation targeting. Acta Pharm. Sin. B 2018, 8, 23–33.

    Article  Google Scholar 

  185. Zhang, Q. Z.; Dehaini, D.; Zhang, Y.; Zhou, J. L.; Chen, X. Y.; Zhang, L. F.; Fang, R. H.; Gao, W. W.; Zhang, L. F. Neutrophil membrane-coated nanoparticles inhibit synovial inflammation and alleviate joint damage in inflammatory arthritis. Nat. Nanotechnol. 2018, 13, 1182–1190.

    Article  CAS  Google Scholar 

  186. Shi, Y. S.; Xie, F. F.; Rao, P. S.; Qian, H. Y.; Chen, R. J.; Chen, H.; Li, D. F.; Mu, D.; Zhang, L. L.; Lv, P. et al. TRAIL-expressing cell membrane nanovesicles as an anti-inflammatory platform for rheumatoid arthritis therapy. J. Control. Release 2020, 320, 304–313.

    Article  CAS  Google Scholar 

  187. Boilard, E.; Nigrovic, P. A.; Larabee, K.; Watts, G. F. M.; Coblyn, J. S.; Weinblatt, M. E.; Massarotti, E. M.; Remold-O’Donnell, E.; Farndale, R. W.; Ware, J. et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010, 327, 580–583.

    Article  CAS  Google Scholar 

  188. He, Y. W.; Li, R. X.; Liang, J. M.; Zhu, Y.; Zhang, S. Y.; Zheng, Z. C.; Qin, J.; Pang, Z. Q.; Wang, J. X. Drug targeting through platelet membrane-coated nanoparticles for the treatment of rheumatoid arthritis. Nano Res. 2018, 11, 6086–6101.

    Article  CAS  Google Scholar 

  189. Xie, W.; Du, L. Diabetes is an inflammatory disease: Evidence from traditional Chinese medicines. Diabetes Obes. Metab. 2011, 13, 289–301.

    Article  CAS  Google Scholar 

  190. Wheeler, T. J.; Hinkle, P. C. The glucose transporter of mammalian cells. Annu. Rev. Physiol. 1985, 47, 503–517.

    Article  CAS  Google Scholar 

  191. Zhang, J. Z.; Ismail-Beigi, F. Activation of Glut1 glucose transporter in human erythrocytes. Arch. Biochem. Biophys. 1998, 356, 86–92.

    Article  CAS  Google Scholar 

  192. Kim, I.; Kwon, D.; Lee, D.; Lee, T. H.; Lee, J. H.; Lee, G.; Yoon, D. S. A highly permselective electrochemical glucose sensor using red blood cell membrane. Biosens. Bioelectron. 2018, 102, 617–623.

    Article  CAS  Google Scholar 

  193. Kim, I.; Kim, C.; Lee, D.; Lee, S. W.; Lee, G.; Yoon, D. S. A bio-inspired highly selective enzymatic glucose sensor using a red blood cell membrane. Analyst 2020, 145, 2125–2132.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by National Natural Science Foundation of China (Nos. 81801843 and 81971737), Guangdong Basic and Applied Basic Research Foundation (No. 2020B1515020017), Technology & Innovation Commission of Shenzhen Municipality (No. JCYJ20190807152601651), Guangdong Special Support Program (No. 2019TQ05Y224), and the Fundamental Research Funds for the Central Universities (No. 19ykpy138).

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  1. School of Pharmaceutical Sciences (Shenzhen), Sun Yat-sen University, Shenzhen, 518107, China

    Huisong Hao & Meiying Wu

  2. School of Life Sciences, Shanghai University, Shanghai, 200444, China

    Yu Chen

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  1. Huisong Hao
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  2. Yu Chen
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  3. Meiying Wu
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Correspondence to Yu Chen or Meiying Wu.

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Hao, H., Chen, Y. & Wu, M. Biomimetic nanomedicine toward personalized disease theranostics. Nano Res. 14, 2491–2511 (2021). https://doi.org/10.1007/s12274-020-3265-z

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  • DOI: https://doi.org/10.1007/s12274-020-3265-z

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