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Nano Research

, Volume 11, Issue 6, pp 2932–2950 | Cite as

Nanomaterial-assisted sensitization of oncotherapy

  • Yufei Wang
  • Juan Liu
  • Xiaowei MaEmail author
  • Xing-Jie LiangEmail author
Review Article

Abstract

Globally, cancer is growing at an alarming pace, which calls for development of more efficient cancer treatments. Conventional chemotherapy and radiotherapy have become crucial first-line clinical treatments for cancer. However, along with their wide usage, limited therapeutic effects, severe adverse reactions, unaffordable costs, and complicated operations lead to failures of these treatments. Moreover, the emergence of multidrug resistance inhibits the longtime usage of chemotherapeutics. One of the major causes of treatment failure is the insufficient sensitivity of cancer cells to therapeutic drugs or treatments. With the rigorous development of nanotechnology, tailored nanoparticles can efficiently sensitize malignant cells by inducing intracellular structural and functional changes, which could affect vital intracellular processes such as metabolism, signal conduction, proliferation, cell death as well as intracellular drug delivery. Here, we review recent advances in nanomaterial-assisted sensitization of oncotherapy, and challenges and strategies in the development of nanomedical approaches.

Keywords

nanomaterial oncotherapy sensitization of oncotherapy multidrug resistance 

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Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31600808), the Beijing Natural Science Foundation (No. 7164316). This work was also supported by the Key Laboratory of Biomedical Effects of Nanomaterials and Nanosafety, CAS (No. NSKF201601). This work was supported in part by the Natural Science Foundation key projects (Nos. 31630027 and 31430031). The authors also appreciate the support of the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA09030301).

References

  1. [1]
    World Health Organization. Global health observatory data repository. 2011. Number of deaths (World) by cause [Online]. http://apps.who.int/gho/data/node.main.CODWORLD?lang=en. (accessed Oct 25, 2017).Google Scholar
  2. [2]
    Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D. M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: Sources, methods and major patterns in globocan 2012. Int. J. Cancer 2015, 136, 359–386.CrossRefGoogle Scholar
  3. [3]
    Torre, L. A.; Bray, F.; Siegel, R. L.; Ferlay, J.; Lortet-Tieulent, J.; Jemal, A. Global cancer statistics, 2012. CA Cancer J. Clin. 2015, 65, 87–108.CrossRefGoogle Scholar
  4. [4]
    Steliarova-Foucher, E.; Colombet, M.; Ries, L. A. G.; Moreno, F.; Dolya, A.; Bray, F.; Hesseling, P.; Shin, H. Y.; Stiller, C. A.; Bouzbid, S. et al. International incidence of childhood cancer, 2001-10: A population-based registry study. Lancet Oncol. 2017, 18, 719–731.CrossRefGoogle Scholar
  5. [5]
    Chen, L. M.; Sun, J. H.; Yang, X. M. Radiofrequency ablation-combined multimodel therapies for hepatocellular carcinoma: Current status. Cancer Lett. 2016, 370, 78–84.CrossRefGoogle Scholar
  6. [6]
    Ribas, A. Releasing the brakes on cancer immunotherapy. N. Engl. J. Med. 2015, 373, 1490–1492.CrossRefGoogle Scholar
  7. [7]
    Li, F. Y.; Lu, J. X.; Kong, X. Q.; Hyeon, T.; Ling, D. S. Dynamic nanoparticle assemblies for biomedical applications. Adv. Mater. 2017, 29, 1605897.CrossRefGoogle Scholar
  8. [8]
    Lu, Y.; Aimetti, A. A.; Langer, R.; Gu, Z. Bioresponsive materials. Nat. Rev. Mater. 2016, 2, 16075.CrossRefGoogle Scholar
  9. [9]
    Sun, T. M.; Zhang, Y. S.; Pang, B.; Hyun, D. C.; Yang, M. X.; Xia, Y. N. Engineered nanoparticles for drug delivery in cancer therapy. Angew. Chem, Int. Ed. 2014, 53, 12320–12364.Google Scholar
  10. [10]
    Lazarovits, J.; Chen, Y. Y.; Sykes, E. A.; Chan, W. C. W. Nanoparticle-blood interactions: The implications on solid tumour targeting. Chem. Commun. 2015, 51, 2756–2767.CrossRefGoogle Scholar
  11. [11]
    Zeng, L. L.; Gupta, P.; Chen, Y. L.; Wang, E. J.; Ji, L. N.; Chao, H.; Chen, Z. S. The development of anticancer ruthenium(II) complexes: From single molecule compounds to nanomaterials. Chem. Soc. Rev. 2017, 46, 5771–5804.CrossRefGoogle Scholar
  12. [12]
    Luqmani, Y. A. Mechanisms of drug resistance in cancer chemotherapy. Med. Prin. Pract. 2005, 14, 35–48.CrossRefGoogle Scholar
  13. [13]
    Ma, N. N.; Wu, F. G.; Zhang, X. D.; Jiang, Y. W.; Jia, H. R.; Wang, H. Y.; Li, Y. H.; Liu, P. D.; Gu, N.; Chen, Z. Shapedependent radiosensitization effect of gold nanostructures in cancer radiotherapy: Comparison of gold nanoparticles, nanospikes, and nanorods. ACS Appl. Mater. Interfaces 2017, 9, 13037–13048.CrossRefGoogle Scholar
  14. [14]
    Bedard, P. L.; Hansen, A. R.; Ratain, M. J.; Siu, L. L. Tumour heterogeneity in the clinic. Nature 2013, 501, 355–364.CrossRefGoogle Scholar
  15. [15]
    Mujokoro, B.; Adabi, M.; Sadroddiny, E.; Adabi, M.; Khosravani, M. Nano-structures mediated co-delivery of therapeutic agents for glioblastoma treatment: A review. Mat. Sci. Eng. C 2016, 69, 1092–1102.CrossRefGoogle Scholar
  16. [16]
    Ramu, A.; Glaubiger, D.; Fuks, Z. Reversal of acquired resistance to doxorubicin in p388 murine leukemia cells by tamoxifen and other triparanol analogues. Cancer Res. 1984, 44, 4392–4395.Google Scholar
  17. [17]
    Vinod, B. S.; Maliekal, T. T.; Anto, R. J. Phytochemicals as chemosensitizers: From molecular mechanism to clinical significance. Antioxid. Redox Signal. 2013, 18, 1307–1348.CrossRefGoogle Scholar
  18. [18]
    Fletcher, D. A.; Mullins, R. D. Cell mechanics and the cytoskeleton. Nature 2010, 463, 485–492.CrossRefGoogle Scholar
  19. [19]
    Pawlak, G.; Helfman, D. M. Cytoskeletal changes in cell transformation and tumorigenesis. Curr. Opin. Genet. Dev. 2001, 11, 41–47.CrossRefGoogle Scholar
  20. [20]
    Zhang, Z.; Yang, M.; Chen, R.; Su, W.; Li, P.; Chen, S.; Chen, Z.; Chen, A.; Li, S.; Hu, C. IBP regulates epithelial-tomesenchymal transition and the motility of breast cancer cells via rac1, rhoa and cdc42 signaling pathways. Oncogene 2014, 33, 3374–3382.CrossRefGoogle Scholar
  21. [21]
    Tavares, S.; Vieira, A. F.; Taubenberger, A. V.; Araujo, M.; Martins, N. P.; Bras-Pereira, C.; Polonia, A.; Herbig, M.; Barreto, C.; Otto, O. et al. Actin stress fiber organization promotes cell stiffening and proliferation of pre-invasive breast cancer cells. Nat. Commun. 2017, 8, 15237.CrossRefGoogle Scholar
  22. [22]
    Zhu, J. Q.; Xu, M.; Gao, M.; Zhang, Z. H.; Xu, Y.; Xia, T.; Liu, S. J. Graphene oxide induced perturbation to plasma membrane and cytoskeletal meshwork sensitize cancer cells to chemotherapeutic agents. ACS Nano 2017, 11, 2637–2651.CrossRefGoogle Scholar
  23. [23]
    Overgaard, J. Influence of extracellular pH on the viability and morphology of tumor cells exposed to hyperthermia. J. Natl. Cancer Inst. 1976, 56, 1243–1250.CrossRefGoogle Scholar
  24. [24]
    Hildebrandt, B.; Wust, P.; Ahlers, O.; Dieing, A.; Sreenivasa, G.; Kerner, T.; Felix, R.; Riess, H. The cellular and molecular basis of hyperthermia. Crit. Rev. Oncol. Hematol. 2002, 43, 33–56.CrossRefGoogle Scholar
  25. [25]
    Cherukuri, P.; Glazer, E. S.; Curley, S. A. Targeted hyperthermia using metal nanoparticles. Adv. Drug. Deliv. Rev. 2010, 62, 339–345.CrossRefGoogle Scholar
  26. [26]
    Huff, T. B.; Tong, L.; Zhao, Y.; Hansen, M. N.; Cheng, J. X.; Wei, A. Hyperthermic effects of gold nanorods on tumor cells. Nanomedicine 2007, 2, 125–132.CrossRefGoogle Scholar
  27. [27]
    Ali, M. R. K.; Wu, Y.; Tang, Y.; Xiao, H. P.; Chen, K. C.; Han, T. G.; Fang, N.; Wu, R. H.; El-Sayed, M. A. Targeting cancer cell integrins using gold nanorods in photothermal therapy inhibits migration through affecting cytoskeletal proteins. Proc. Natl. Acad. Sci. USA 2017, 114, e5655–E5663.CrossRefGoogle Scholar
  28. [28]
    Zhao, R. F.; Han, X. X.; Li, Y. Y.; Wang, H.; Ji, T. J.; Zhao, Y. L.; Nie, G. J. Photothermal effect enhanced cascade-targeting strategy for improved pancreatic cancer therapy by gold nanoshell@mesoporous silica nanorod. ACS Nano 2017, 11, 8103–8113.CrossRefGoogle Scholar
  29. [29]
    Sanz, B.; Calatayud, M. P.; Torres, T. E.; Fanarraga, M. L.; Ibarra, M. R.; Goya, G. F. Magnetic hyperthermia enhances cell toxicity with respect to exogenous heating. Biomaterials 2017, 114, 62–70.CrossRefGoogle Scholar
  30. [30]
    Yoshimori, T. Autophagy: A regulated bulk degradation process inside cells. Biochem. Biophys. Res. Commun. 2004, 313, 453–458.CrossRefGoogle Scholar
  31. [31]
    Klionsky, D. J. Autophagy: From phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8, 931–937.CrossRefGoogle Scholar
  32. [32]
    Kumar, D.; Shankar, S.; Srivastava, R. K. Rottlerin induces autophagy and apoptosis in prostate cancer stem cells via Pl3K/Akt/mTOR signaling pathway. Cancer Lett. 2014, 343, 179–189.CrossRefGoogle Scholar
  33. [33]
    Li, T. L.; Su, L.; Zhong, N.; Hao, X. X.; Zhong, D. S.; Singhal, S.; Liu, X. G. Salinomycin induces cell death with autophagy through activation of endoplasmic reticulum stress in human cancer cells. Autophagy 2013, 9, 1057–1068.CrossRefGoogle Scholar
  34. [34]
    Yang, A. N.; Rajeshkumar, N. V.; Wang, X. X.; Yabuuchi, S.; Alexander, B. M.; Chu, G. C.; Von Hoff, D. D.; Maitra, A.; Kimmelman, A. C. Autophagy is critical for pancreatic tumor growth and progression in tumors with p53 alterations. CancerDiscov. 2014, 4, 905–913.Google Scholar
  35. [35]
    Zhang, Q. Y.; Linqing, W. U.; Zhang, T.; Han, Y. F.; Lin, X. Autophagy-mediated hmgb1 release promotes gastric cancer cell survival via RAGE activation of extracellular signalregulated kinases 1/2. Oncol. Rep. 2015, 33, 1630–1638.CrossRefGoogle Scholar
  36. [36]
    Joshi, S.; Kumar, S.; Ponnusamy, M. P.; Batra, S. K. Hypoxia-induced oxidative stress promotes MUC4 degradation via autophagy to enhance pancreatic cancer cells survival. Oncogene 2016, 35, 5882–5892.CrossRefGoogle Scholar
  37. [37]
    Guo, S. J.; Dong, S. J. Graphene nanosheet: Synthesis, molecular engineering, thin film, hybrids, and energy and analytical applications. Chem. Soc. Rev. 2011, 40, 2644–2672.CrossRefGoogle Scholar
  38. [38]
    Jiang, H. J. Chemical preparation of graphene-based nanomaterials and their applications in chemical and biological sensors. Small 2011, 7, 2413–2427.Google Scholar
  39. [39]
    Zhang, Q.; Yang, W. J.; Man, N.; Zheng, F.; Shen, Y. Y.; Sun, K. J.; Li, Y; Wen, L.-P. Autophagy-mediated chemosensitization in cancer cells by fullerene C60 nanocrystal. Autophagy 2009, 5, 1107–1117.CrossRefGoogle Scholar
  40. [40]
    Wei, P. F.; Zhang, L.; Lu, Y.; Man, N.; Wen, L. P. C60(Nd) nanoparticles enhance chemotherapeutic susceptibility of cancer cells by modulation of autophagy. Nanotechnology 2010, 21, 495101.CrossRefGoogle Scholar
  41. [41]
    Franskevych, D. V.; Grynyuk, I. I.; Prylutska, S. V; Matyshevska, O. P. Modulation of cisplatin-induced reactive oxygen species production by fullerene C(60) in normal and transformed lymphoid cells. Ukrain. Biochem. J. 2016, 88, 44–50.CrossRefGoogle Scholar
  42. [42]
    Chen, G. Y.; Meng, C. L.; Lin, K. C.; Tuan, H. Y.; Yang, H. J.; Chen, C. L.; Li, K. C.; Chiang, C. S.; Hu, Y C. Graphene oxide as a chemosensitizer: Diverted autophagic flux, enhanced nuclear import, elevated necrosis and improved antitumor effects. Biomaterials 2015, 40, 12–22.CrossRefGoogle Scholar
  43. [43]
    Yang, K.; Lu, Y.; Xie, F.; Zou, H.; Fan, X.; Li, B.; Li, W.; Zhang, W.; Mei, L.; Feng, S. S. et al. Cationic liposomes induce cell necrosis through lysosomal dysfunction and late- 15 stage autophagic flux inhibition. Nanomedicine 2016, 11, 3117–3137.CrossRefGoogle Scholar
  44. [44]
    Iyer, A. K.; Khaled, G.; Fang, J.; Maeda, H. Exploiting the enhanced permeability and retention effect for tumor targeting. Drug Discov. Today 2006, 11, 812–818.CrossRefGoogle Scholar
  45. [45]
    Ishitsuka, A.; Fujine, E.; Mizutani, Y.; Tawada, C.; Kanoh, H.; Banno, Y.; Seishima, M. FTY720 and cisplatin synergistically induce the death of cisplatin-resistant melanoma cells through the downregulation of the PI3K pathway and the decrease in epidermal growth factor receptor expression. Int. J. Mol. Med. 2014, 34, 1169–1174.CrossRefGoogle Scholar
  46. [46]
    Wang, Q.; Alshaker, H.; Bohler, T.; Srivats, S.; Chao, Y. M.; Cooper, C.; Pchejetski, D. Core shell lipid-polymer hybrid nanoparticles with combined docetaxel and molecular targeted therapy for the treatment of metastatic prostate cancer. Sci. Rep. 2017, 7, 5901.CrossRefGoogle Scholar
  47. [47]
    Wink, D. A.; Miranda, K. M.; Espey, M. G.; Pluta, R. M.; Hewett, S. J.; Colton, C.; Vitek, M.; Feelisch, M.; Grisham, M. B. Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox. Sign. 2001, 3, 203–213.CrossRefGoogle Scholar
  48. [48]
    Zhang, X.; Tian, G.; Yin, W. Y.; Wang, L. M.; Zheng, X. P.; Yan, L.; Li, J. X.; Su, H. R.; Chen, C. Y.; Gu, Z. J. et al. Controllable generation of nitric oxide by near-infraredsensitized upconversion nanoparticles for tumor therapy. Adv. Funct. Mater. 2015, 25, 3049–3056.CrossRefGoogle Scholar
  49. [49]
    Fan, J.; He, Q. J.; Liu, Y.; Zhang, F. W.; Yang, X. Y.; Wang, Z.; Lu, N.; Fan, W. P.; Lin, L. S.; Niu, G. et al. Light-responsive biodegradable nanomedicine overcomes multidrug resistance via no-enhanced chemosensitization. ACS Appl. Mater. Interfaces 2016, 8, 13804–13811.CrossRefGoogle Scholar
  50. [50]
    Guo, S. R.; Lv, L.; Shen, Y. Y.; Hu, Z. L.; He, Q. J.; Chen, X. Y. A nanoparticulate pre-chemosensitizer for efficacious chemotherapy of multidrug resistant breast cancer. Sci. Rep. 2016, 6, 21459.CrossRefGoogle Scholar
  51. [51]
    Singh, M.; Bhatnagar, P.; Mishra, S.; Kumar, P.; Shukla, Y.; Gupta, K. C. Plga-encapsulated tea polyphenols enhance the chemotherapeutic efficacy of cisplatin against human cancer cells and mice bearing ehrlich ascites carcinoma. Int. J. Nanomedicine 2015, 10, 6789–6809.CrossRefGoogle Scholar
  52. [52]
    Katiyar, S. S.; Muntimadugu, E.; Rafeeqi, T. A.; Domb, A. J.; Khan, W. Co-delivery of rapamycin-and piperine-loaded polymeric nanoparticles for breast cancer treatment. Drug Deliv. 2016, 23, 2608–2616.Google Scholar
  53. [53]
    Johnson, B. M.; Charman W. N.; Porter, C. J. H. Application of compartmental modeling to an examination of in vitro intestinal permeability data: Assessing the impact of tissue uptake, p-glycoprotein, and CYP3A. Drug Metab. Dispos. 2003, 31, 1151–1160.CrossRefGoogle Scholar
  54. [54]
    Zaki, N. M. Augmented cytotoxicity of hydroxycamptothecinloaded nanoparticles in lung and colon cancer cells by chemosensitizing pharmaceutical excipients. Drug Deliv. 2014, 21, 265–275.CrossRefGoogle Scholar
  55. [55]
    Matsunaga, S.; Asano, T.; Tsutsuda-Asano, A.; Fukunaga, Y. Indomethacin overcomes doxorubicin resistance with inhibiting multi-drug resistance protein 1 (MRP1). Cancer Chemother. Pharmacol. 2006, 58, 348–353.CrossRefGoogle Scholar
  56. [56]
    Ji, W.; Wang, B.; Fan, Q.; Xu, C.; He, Y.; Chen, Y. Chemosensitizing indomethacin-conjugated dextran-based micelles for effective delivery of paclitaxel in resistant breast cancer therapy. PLoS One 2017, 12, e180037.Google Scholar
  57. [57]
    Drinberg, V; Bitcover, R.; Rajchenbach, W.; Peer, D. Modulating cancer multidrug resistance by sertraline in combination with a nanomedicine. Cancer Lett. 2014, 354, 290–298.CrossRefGoogle Scholar
  58. [58]
    Lee, E.; Oh, C.; Kim, I. S.; Kwon, I. C.; Kim, S. Co-delivery of chemosensitizing sirna and an anticancer agent via multiple monocomplexation-induced hydrophobic association. J. Control. Release 2015, 210, 105–114.CrossRefGoogle Scholar
  59. [59]
    Kim, S. S.; Rait, A.; Kim, E.; Pirollo, K. F.; Nishida, M.; Farkas, N.; Dagata, J. A.; Chang, E. H. A nanoparticle carrying the p53 gene targets tumors including cancer stem cells, sensitizes glioblastoma to chemotherapy and improves survival. ACS Nano 2014, 8, 5494–5514.CrossRefGoogle Scholar
  60. [60]
    Khatri, N.; Rathi, M.; Baradia, D.; Misra, A. cRGD grafted sirna nano-constructs for chemosensitization of gemcitabine hydrochloride in lung cancer treatment. Pharm. Res. 2015, 32, 806–818.CrossRefGoogle Scholar
  61. [61]
    Caster, J. M.; Sethi, M.; Kowalczyk, S.; Wang, E.; Tian, X.; Nabeel Hyder, S.; Wagner, K. T.; Zhang, Y. A.; Kapadia, C.; Man Au, K. et al. Nanoparticle delivery of chemosensitizers improve chemotherapy efficacy without incurring additional toxicity. Nanoscale 2015, 7, 2805–2811.CrossRefGoogle Scholar
  62. [62]
    Banerjee, S.; Sahoo, A. K.; Chattopadhyay, A.; Ghosh, S. S. Chemosensitization of iKBa-overexpressing glioblastoma towards anti-cancer agents. RSCAdv. 2014, 4, 39257–39267.Google Scholar
  63. [63]
    Chen, Y.; Zheng, X. L.; Fang, D. L.; Yang, Y.; Zhang, J. K.; Li, H. L.; Xu, B.; Lei, Y.; Ren, K.; Song, X. R. Dual agent loaded plga nanoparticles enhanced antitumor activity in a multidrug-resistant breast tumor eenograft model. Int. J. Mol. Sci. 2014, 15, 2761–2772.CrossRefGoogle Scholar
  64. [64]
    Liu, C. W.; Lin, W. J. Using doxorubicin and sirna-loaded heptapeptide-conjugated nanoparticles to enhance chemosensitization in epidermal growth factor receptor high-expressed breast cancer cells. J. Drug Target. 2013, 21, 776–786.CrossRefGoogle Scholar
  65. [65]
    Kouvaris, J. R.; Kouloulias, V. E.; Vlahos, L. J. Amifostine: The first selective-target and broad-spectrum radioprotector. Oncologist 2007, 12, 738–747.CrossRefGoogle Scholar
  66. [66]
    Wardman, P. Chemical radiosensitizers for use in radiotherapy. Clin. Oncol. 2007, 19, 397–417.CrossRefGoogle Scholar
  67. [67]
    Klein, S.; Dell’Arciprete, M. L.; Wegmann, M.; Distel, L. V. R.; Neuhuber, W.; Gonzalez, M. C.; Kryschi, C. Oxidized silicon nanoparticles for radiosensitization of cancer and tissue cells. Biochem. Biophys. Res. Commun. 2013, 434, 217–222.CrossRefGoogle Scholar
  68. [68]
    Yong, Y.; Zhang, C. F.; Gu, Z. J.; Du, J. F.; Guo, Z.; Dong, X. H.; Xie, J. N.; Zhang, G. J.; Liu, X. F.; Zhao, Y. L. Polyoxometalate- based radiosensitization platform for treating hypoxic tumors by attenuating radioresistance and enhancing radiation response. ACS Nano 2017, 11, 7164–7176.CrossRefGoogle Scholar
  69. [69]
    Yang, T. B.; Liang, Y.; Hou, J. Z.; Dou, Y. L.; Zhang, W. X. Metabolizable lanthanum-coordination nanoparticles as efficient radiosensitizers for solid tumor therapy. J. Mater. Chem. B 2017, 5, 5137–5144.CrossRefGoogle Scholar
  70. [70]
    Wu, H.; Lin, J.; Liu, P. D.; Huang, Z. H.; Zhao, P.; Jin, H. Z.; Ma, J.; Wen, L. P.; Gu, N. Reactive oxygen species acts as executor in radiation enhancement and autophagy inducing by AgNPs. Biomaterials 2016, 101, 1–9.CrossRefGoogle Scholar
  71. [71]
    Du, F. Y.; Li, Z. R.; Zhang, L.; Zhang, M. M.; Gong, A. H.; Tan, Y. W.; Miao, J. W.; Gong, Y. H.; Sun, M. Z.; Ju, H. X. et al. Engineered gadolinium-doped carbon dots for magnetic resonance imaging-guided radiotherapy of tumors. Biomaterials 2017, 121, 109–120.CrossRefGoogle Scholar
  72. [72]
    Fang, X.; Wang, Y. L.; Ma, X. C.; Li, Y. Y.; Zhang, Z. L.; Xiao, Z. S.; Liu, L. J.; Gao, X. Y.; Liu, J. Mitochondriatargeting Au nanoclusters enhance radiosensitivity of cancer cells. J. Mater. Chem. B 2017, 5, 4190–4197.CrossRefGoogle Scholar
  73. [73]
    Hainfeld, J. F.; Slatkin, D. N.; Smilowitz, H. M. The use of gold nanoparticles to enhance radiotherapy in mice. Phys. Med. Biol. 2004, 49, N309–N315.CrossRefGoogle Scholar
  74. [74]
    Ma, N. N.; Liu, P. D.; He, N. Y.; Gu, N.; Wu, F. G.; Chen, Z. Action of gold nanospikes-based nanoradiosensitizers: Cellular internalization, radiotherapy, and autophagy. ACS Appl. Mater. Interfaces 2017, 9, 31526–31542.CrossRefGoogle Scholar
  75. [75]
    Dou, Y.; Guo, Y. Y.; Li, X. D.; Li, X.; Wang, S.; Wang, L.; Lv, G. X.; Zhang, X. N.; Wang, H. J.; Gong, X. Q. et al. Sizetuning ionization to optimize gold nanoparticles for simultaneous enhanced CT imaging and radiotherapy. ACS Nano 2016, 10, 2536–2548.CrossRefGoogle Scholar
  76. [76]
    Zhao, N.; Yang, Z. R.; Li, B. X.; Meng, J.; Shi, Z. L.; Li, P.; Fu, S. RGD-conjugated mesoporous silica-encapsulated gold nanorods enhance the sensitization of triple-negative breast cancer to megavoltage radiation therapy. Int. J. Nanomedicine 2016, 11, 5595–5610.CrossRefGoogle Scholar
  77. [77]
    Rosa, S.; Connolly, C.; Schettino, G.; Butterworth, K. T.; Prise, K. M. Biological mechanisms of gold nanoparticle radiosensitization. CancerNanotechnol. 2017, 8, 2.Google Scholar
  78. [78]
    Hubbell, J. H.; Seltzer, S. M. Tables of X-ray mass attenuation coefficients and mass energy-absorption coefficients (version I.4) [Online]. http://www.nist.gov/pml/data/xraycoef (accessed Oct 25,2017).Google Scholar
  79. [79]
    Téoule, R. Radiation-induced DNA damage and its repair. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 1987, 51, 573–589.CrossRefGoogle Scholar
  80. [80]
    Her, S.; Cui, L.; Bristow, R. G.; Allen, C. Dual action enhancement of gold nanoparticle radiosensitization by pentamidine in triple negative breast cancer. Radiat. Res. 2016, 185, 549–562.CrossRefGoogle Scholar
  81. [81]
    Yasui, H.; Takeuchi, R.; Nagane, M.; Meike, S.; Nakamura, Y.; Yamamori, T.; Ikenaka, Y.; Kon, Y.; Murotani, H.; Oishi, M. et al. Radiosensitization of tumor cells through endoplasmic reticulum stress induced by pegylated nanogel containing gold nanoparticles. Cancer Lett. 2014, 347, 151–158.CrossRefGoogle Scholar
  82. [82]
    Pawlik, T. M.; Keyomarsi, K. Role of cell cycle in mediating sensitivity to radiotherapy. Int. J. Radiat. Oncol. 2004, 59, 928–942.CrossRefGoogle Scholar
  83. [83]
    Liang, Y; Liu, J.; Liu, T.; Yang, X. S. Anti-C-Met antibody bioconjugated with hollow gold nanospheres as a novel nanomaterial for targeted radiation ablation of human cervical cancer cell. Oncol. Lett. 2017, 14, 2254–2260.CrossRefGoogle Scholar
  84. [84]
    Saberi, A.; Shahbazi-Gahrouei, D.; Abbasian, M.; Fesharaki, M.; Baharlouei, A.; Arab-Bafrani, Z. Gold nanoparticles in combination with megavoltage radiation energy increased radiosensitization and apoptosis in colon cancer HT-29 cells. Int. J. Radiat. Biol. 2017, 93, 315–323.CrossRefGoogle Scholar
  85. [85]
    Jain, S.; Coulter, J. A.; Hounsell, A. R.; Butterworth, K. T.; McMahon, S. J.; Hyland, W. B.; Muir, M. F.; Dickson, G. R.; Prise, K. M.; Currell, F. J. et al. Cell-specific radiosensitization by gold nanoparticles at megavoltage radiation energies. Int. J. Radiat. Oncol. Biol. Phys. 2011, 79, 531–539.CrossRefGoogle Scholar
  86. [86]
    Uz, M.; Bulmus, V.; Alsoy Altinkaya, S. Effect of PEG grafting density and hydrodynamic volume on gold nanoparticle-cell interactions: An investigation on cell cycle, apoptosis, and DNA damage. Langmuir 2016, 32, 5997–6009.CrossRefGoogle Scholar
  87. [87]
    Joyce, J. A. Therapeutic targeting of the tumor microenvironment. Cancer Cell 2005, 7, 513–520.CrossRefGoogle Scholar
  88. [88]
    Quail, D. F.; Joyce, J. A. Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 2013, 19, 1423–1437.CrossRefGoogle Scholar
  89. [89]
    Vaupel, P. W.; Hockel, M. Oxygenation status of human tumors: A reappraisal using computerized pO2 histography. In: Tumor Oxygenation. Vaupel, P. W.; Kelleher, D. K.; Gunderoth, M., eds.; Fischer-Verlag: New York, 1995; pp219-232.Google Scholar
  90. [90]
    Vaupel, P.; Kallinowski, F.; Okunieff, P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: A review. Cancer Res. 1989, 49, 6449–6465.Google Scholar
  91. [91]
    Gray, L. H.; Conger, A. D.; Ebert, M.; Hornsey, S.; Scott, O. C. A. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br. J. Radiol. 1953, 26, 638–648.CrossRefGoogle Scholar
  92. [92]
    Dowdy, A. H.; Bennett, L. R.; Chastain, S. M. Protective action of anoxic anoxia against total body roentgen irradiation of mammals. Radiology 1950, 55, 879–885.CrossRefGoogle Scholar
  93. [93]
    Cheng, N. N.; Starkewolf, Z.; Davidson, R. A.; Sharmah, A.; Lee, C. J.; Lien, J.; Guo, T. Chemical enhancement by nanomaterials under X-ray irradiation. J. Am. Chem. Soc. 2012, 134, 1950–1953.CrossRefGoogle Scholar
  94. [94]
    Misawa, M.; Takahashi, J. Generation of reactive oxygen species induced by gold nanoparticles under X-ray and UV irradiations. Nanomed. Nanotechnol. 2011, 7, 604–614.CrossRefGoogle Scholar
  95. [95]
    Chang, Y. Z.; He, L. Z.; Li, Z. L.; Zeng, L. L.; Song, Z. H.; Li, P. H.; Chan, L.; You, Y. Y.; Yu, X. F.; Chu, P. K. et al. Designing core-shell gold and selenium nanocomposites for cancer radiochemotherapy. ACS Nano 2017, 11, 4848–4858.CrossRefGoogle Scholar
  96. [96]
    Yi, X.; Chen, L.; Zhong, X. Y.; Gao, R. L.; Qian, Y. T.; Wu, F.; Song, G. S.; Chai, Z.; Liu, Z.; Yang, K. Core-shell Au@MnO2 nanoparticles for enhanced radiotherapy via improving the tumor oxygenation. Nano Res. 2016, 9, 3267–3278.CrossRefGoogle Scholar
  97. [97]
    Wang, Y.; Roche, O.; Yan, M. S.; Finak, G.; Evans, A. J.; Metcalf, J. L.; Hast, B. E.; Hanna, S. C.; Wondergem, B.; Furge, K. A. et al. Regulation of endocytosis via the oxygen-sensing pathway. Nat. Med. 2009, 15, 319–324.CrossRefGoogle Scholar
  98. [98]
    Cui, L.; Tse, K.; Zahedi, P.; Harding, S. M.; Zafarana, G.; Jaffray, D. A.; Bristow, R. G.; Allen, C. Hypoxia and cellular localization influence the radiosensitizing effect of gold nanoparticles (AuNPs) in breast cancer cells. Radiat. Res. 2014, 182, 475–488.CrossRefGoogle Scholar
  99. [99]
    Wang, C. M.; Sun, A.; Qiao, Y.; Zhang, P. P.; Ma, L. Y.; Su, M. Cationic surface modification of gold nanoparticles for enhanced cellular uptake and X-ray radiation therapy. J. Mater. Chem B 2015, 3, 7372–7376.CrossRefGoogle Scholar
  100. [100]
    Guo, M. L.; Sun, Y. M.; Zhang, X.-D. Enhanced radiation therapy of gold nanoparticles in liver cancer. Appl. Sci. 2017, 7, 232.CrossRefGoogle Scholar
  101. [101]
    Lin, Y. T.; McMahon, S. J.; Paganetti, H.; Schuemann, J. Biological modeling of gold nanoparticle enhanced radiotherapy for proton therapy. Phys. Med. Biol. 2015, 60, 4149–4168.CrossRefGoogle Scholar
  102. [102]
    Shi, M.; Paquette, B.; Thippayamontri, T.; Gendron, L.; Guerin, B.; Sanche, L. Increased radiosensitivity of colorectal tumors with intra-tumoral injection of low dose of gold nanoparticles. Int. J. Nanomedicine 2016, 11, 5323–5333.CrossRefGoogle Scholar
  103. [103]
    Desoize, B.; Jardillier, J. C. Multicellular resistance: A paradigm for clinical resistance? Crit. Rev. Oncol. Hematol. 2000, 36, 193–207.CrossRefGoogle Scholar
  104. [104]
    Szakács, G.; Paterson, J. K.; Ludwig, J. A.; Booth-Genthe, C.; Gottesman, M. M. Targeting multidrug resistance in cancer. Nat. Rev. Drug Discov. 2006, 5, 219–234.CrossRefGoogle Scholar
  105. [105]
    Baguley, B. C. Multiple drug resistance mechanisms in cancer. Mol. Biotechnol. 2010, 46, 308–316.CrossRefGoogle Scholar
  106. [106]
    Gao, Z. B.; Zhang, L. N.; Sun, Y. J. Nanotechnology applied to overcome tumor drug resistance. J. Control. Release 2012, 162, 45–55.CrossRefGoogle Scholar
  107. [107]
    Singh, M. S.; Tammam, S. N.; Shetab Boushehri, M. A.; Lamprecht, A. MDR in cancer: Addressing the underlying cellular alterations with the use of nanocarriers. Pharmacol. Res. 2017, 126, 2–30.CrossRefGoogle Scholar
  108. [108]
    Li, S. Y; Li, C.; Jin, S. B.; Liu, J.; Xue, X. D.; Eltahan, A. S.; Sun, J. D.; Tan, J. J.; Dong, J. C.; Liang, X. J. Overcoming resistance to cisplatin by inhibition of glutathione S-transferases (GSTs) with ethacraplatin micelles in vitro and in vivo. Biomaterials 2017, 144, 119–129.CrossRefGoogle Scholar
  109. [109]
    Liu, J.; Wei, T.; Zhao, J.; Huang, Y. Y.; Deng, H.; Kumar, A.; Wang, C. X.; Liang, Z. C.; Ma, X. W.; Liang, X. J. Multifunctional aptamer-based nanoparticles for targeted drug delivery to circumvent cancer resistance. Biomaterials 2016, 91, 44–56.CrossRefGoogle Scholar
  110. [110]
    Mercado-Lubo, R.; Zhang, Y. W.; Zhao, L.; Rossi, K.; Wu, X.; Zou, Y. K.; Castillo, A.; Leonard, J.; Bortell, R.; Greiner, D. L. et al. A Salmonella nanoparticle mimic overcomes multidrug resistance in tumours. Nat. Commun. 2016, 7, 12225.CrossRefGoogle Scholar
  111. [111]
    Tredan, O.; Galmarini, C. M.; Patel, K.; Tannock, I. F. Drug resistance and the solid tumor microenvironment. J. Natl. Cancer Inst. 2007, 99, 1441–1454.CrossRefGoogle Scholar
  112. [112]
    Cheng, W.; Nie, J. P.; Gao, N. S.; Liu, G.; Tao, W.; Xiao, X. J.; Jiang, L. J.; Liu, Z. G.; Zeng, X. W.; Mei, L. A multifunctional nanoplatform against multidrug resistant cancer: Merging the best of targeted chemo/gene/photothermal therapy. Adv. Funct. Mater. 2017, 27, 1704135.CrossRefGoogle Scholar
  113. [113]
    He, Y. J.; Xing, L.; Cui, P. F.; Zhang, J. L.; Zhu, Y.; Qiao, J. B.; Lyu, J. Y.; Zhang, M.; Luo, C. Q.; Zhou, Y X. et al. Transferrin-inspired vehicles based on pH-responsive coordination bond to combat multidrug-resistant breast cancer. Biomaterials 2017, 113, 266–278.CrossRefGoogle Scholar
  114. [114]
    Tian, H.; Luo, Z. Y.; Liu, L. L.; Zheng, M. B.; Chen, Z.; Ma, A. Q.; Liang, R. J.; Han, Z. Q.; Lu, C. Y.; Cai, L. T. Cancer cell membrane-biomimetic oxygen nanocarrier for breaking hypoxia-induced chemoresistance. Adv. Funct. Mater. 2017, 27, 1703197.CrossRefGoogle Scholar
  115. [115]
    Wang, A. T.; Liang, D. S.; Liu, Y. J.; Qi, X. R. Roles of ligand and tpgs of micelles in regulating internalization, penetration and accumulation against sensitive or resistant tumor and therapy for multidrug resistant tumors. Biomaterials 2015, 53, 160–172.CrossRefGoogle Scholar
  116. [116]
    Yuan, X.; Ji, W. X.; Chen, S.; Bao, Y. L.; Tan, S. W.; Lu, S.; Wu, K. M.; Qian, C. A novel paclitaxel-loaded poly(d,llactide-co-glycolide)-tween 80 copolymer nanoparticle overcoming multidrug resistance for lung cancer treatment. Int. J. Nanomed. 2016, 11, 2119–2131.CrossRefGoogle Scholar
  117. [117]
    Yu, Y.; Wang, Z. H.; Zhang, L.; Yao, H. J.; Zhang, Y.; Li, R. J.; Ju, R. J.; Wang, X. X.; Zhou, J.; Li, N. et al. Mitochondrial targeting topotecan-loaded liposomes for treating drugresistant breast cancer and inhibiting invasive metastases of melanoma. Biomaterials 2012, 33, 1808–1820.CrossRefGoogle Scholar
  118. [118]
    Tang, S.; Yin, Q.; Zhang, Z. W.; Gu, W. W.; Chen, L. L.; Yu, H. J.; Huang, Y. Z.; Chen, X. Z.; Xu, M. H.; Li, Y. P. Codelivery of doxorubicin and rna using pH-sensitive poly (Pamino ester) nanoparticles for reversal of multidrug resistance of breast cancer. Biomaterials 2014, 35, 6047–6059.CrossRefGoogle Scholar
  119. [119]
    Liu, J.; Ma, X. W.; Jin, S. B.; Xue, X. D.; Zhang, C. Q.; Wei, T.; Guo, W. S.; Liang, X. J. Zinc oxide nanoparticles as adjuvant to facilitate doxorubicin intracellular accumulation and visualize pH-responsive release for overcoming drug resistance. Mol. Pharmaceutics 2016, 13, 1723–1730.CrossRefGoogle Scholar
  120. [120]
    Yao, C.; Wang, P. Y.; Li, X. M.; Hu, X. Y.; Hou, J. L.; Wang, L. Y.; Zhang, F. Near-infrared-triggered azobenzene-liposome/upconversion nanoparticle hybrid vesicles for remotely controlled drug delivery to overcome cancer multidrug resistance. Adv. Mater. 2016, 28, 9341–9348.CrossRefGoogle Scholar
  121. [121]
    Lukianova-Hleb, E. Y.; Belyanin, A.; Kashinath, S.; Wu, X. W.; Lapotko, D. O. Plasmonic nanobubble-enhanced endosomal escape processes for selective and guided intracellular delivery of chemotherapy to drug-resistant cancer cells. Biomaterials 2012, 33, 1821–1826.CrossRefGoogle Scholar
  122. [122]
    Lukianova-Hleb, E. Y.; Kim, Y. S.; Belatsarkouski, I.; Gillenwater, A. M.; O’Neill, B. E.; Lapotko, D. O. Intraoperative diagnostics and elimination of residual microtumours with plasmonic nanobubbles. Nat. Nanotechnol. 2016, 11, 525–532.CrossRefGoogle Scholar
  123. [123]
    Lukianova-Hleb, E.; Hu, Y.; Latterini, L.; Tarpani, L.; Lee, S.; Drezek, R. A.; Hafner, J. H.; Lapotko, D. O. Plasmonic nanobubbles as transient vapor nanobubbles generated around plasmonic nanoparticles. ACSNano 2010, 4, 2109–2123.Google Scholar
  124. [124]
    Li, F. Y.; Lu, J. X.; Kong, X. Q.; Hyeon, T.; Ling, D. S. Dynamic nanoparticle assemblies for biomedical applications. Adv. Mater. 2017, 29, 1605897.CrossRefGoogle Scholar
  125. [125]
    Sabharwal, S. S.; Schumacker, P. T. Mitochondrial ros in cancer: Initiators, amplifiers or an achilles’ heel? Nat. Rev. Cancer 2014, 14, 709–721.CrossRefGoogle Scholar
  126. [126]
    Fulda, S.; Galluzzi, L.; Kroemer, G. Targeting mitochondria for cancer therapy. Nat. Rev. Drug Discovery 2010, 9, 447–464.CrossRefGoogle Scholar
  127. [127]
    Mallick, A.; More, P.; Syed, M. M. K.; Basu, S. Nanoparticlemediated mitochondrial damage induces apoptosis in cancer. ACS Appl. Mater Interfaces 2016, 8, 13218–13231.CrossRefGoogle Scholar
  128. [128]
    Tuguntaev, R. G.; Chen, S. Z.; Eltahan, A. S.; Mozhi, A.; Jin, S. B.; Zhang, J. C.; Li, C.; Wang, P. C.; Liang, X. J. P-gp inhibition and mitochondrial impairment by dual-functional nanostructure based on vitamin E derivatives to overcome multidrug resistance. ACS Appl. Mater. Interfaces 2017, 9, 16900–16912.CrossRefGoogle Scholar
  129. [129]
    Wang, D. F.; Rong, W. T.; Lu, Y; Hou, J.; Qi, S. S.; Xiao, Q.; Zhang, J.; You, J.; Yu, S. Q.; Xu, Q. TPGS/PLGA nanoparticles for overcoming multidrug resistance by interfering mitochondria of human alveolar adenocarcinoma cells. ACS Appl. Mater. Interfaces 2015, 7, 3888–3901.CrossRefGoogle Scholar
  130. [130]
    Qiu, L. P.; Qiao, M. X.; Chen, Q.; Tian, C. M.; Long, M. M.; Wang, M. Y.; Li, Z.; Hu, W.; Li, G.; Cheng, L. et al. Enhanced effect of pH-sensitive mixed copolymer micelles for overcoming multidrug resistance of doxorubicin. Biomaterials 2014, 35, 9877–9887.CrossRefGoogle Scholar
  131. [131]
    Chen, W.-H.; Luo, G.-F.; Qiu, W.-X.; Lei, Q.; Liu, L.-H.; Zheng, D.-W.; Hong, S.; Cheng, S.-X.; Zhang, X.-Z. Tumortriggered drug release with tumor-targeted accumulation and elevated drug retention to overcome multidrug resistance. Chem. Mater. 2016, 28, 6742–6752.CrossRefGoogle Scholar
  132. [132]
    Zhang, R. X.; Li, L. Y.; Li, J.; Xu, Z. S.; Abbasi, A. Z.; Lin, L.; Amini, M. A.; Weng, W. Y.; Sun, Y.; Rauth, A. M. et al. Coordinating biointeraction and bioreaction of a nanocarrier material and an anticancer drug to overcome membrane rigidity and target mitochondria in multidrug-resistant cancer cells. Adv. Funct. Mater. 2017, 27, 1700804.CrossRefGoogle Scholar
  133. [133]
    Zhou, H. J.; Zhang, B.; Zheng, J. J.; Yu, M. F.; Zhou, T.; Zhao, K.; Jia, Y. X.; Gao, X. F.; Chen, C. Y.; Wei, T. T. The inhibition of migration and invasion of cancer cells by graphene via the impairment of mitochondrial respiration. Biomaterials 2014, 35, 1597–1607.CrossRefGoogle Scholar
  134. [134]
    Chen, Y.; Wang, Z.; Xu, M.; Wang, X.; Liu, R.; Liu, Q.; Zhang, Z. H.; Xia, T.; Zhao, J. C.; Jiang, G. B. et al. Nanosilver incurs an adaptive shunt of energy metabolism mode to glycolysis in tumor and nontumor cells. ACS Nano 2014, 8, 5813–5825.CrossRefGoogle Scholar
  135. [135]
    Mizutani, H.; Tada-Oikawa, S.; Hiraku, Y.; Kojima, M.; Kawanishi, S. Mechanism of apoptosis induced by doxorubicin through the generation of hydrogen peroxide. Life Sci. 2005, 76, 1439–1453.CrossRefGoogle Scholar
  136. [136]
    Eastman, A. The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes. Pharmacol. Ther. 1987, 34, 155–166.CrossRefGoogle Scholar
  137. [137]
    Fahrenkrog, B.; Aebi, U. The nuclear pore complex: Nucleocytoplasmic transport and beyond. Nat. Rev. Mol. Cell Biol. 2003, 4, 757–766.CrossRefGoogle Scholar
  138. [138]
    Pante, N.; Kann, M. Nuclear pore complex is able to transport macromolecules with diameters of ∼39 nm. Mol. Biol. Cell 2002, 13, 425–434.CrossRefGoogle Scholar
  139. [139]
    Fan, Y. B.; Li, C. Y.; Li, F. Y.; Chen, D. Y. pH-activated size reduction of large compound nanoparticles for in vivo nucleus-targeted drug delivery. Biomaterials 2016, 85, 30–39.CrossRefGoogle Scholar
  140. [140]
    Pan, L. M.; Liu, J. N.; Shi, J. L. Nuclear-targeting gold nanorods for extremely low NIR activated photothermal therapy. ACS Appl. Mater. Interfaces 2017, 9, 15952–15961.CrossRefGoogle Scholar
  141. [141]
    Maity, A. R.; Stepensky, D. Efficient subcellular targeting to the cell nucleus of quantum dots densely decorated with a nuclear localization sequence peptide. ACS Appl. Mater. Interfaces 2016, 8, 2001–2009.CrossRefGoogle Scholar
  142. [142]
    Lee, J. Y.; Lee, S. H.; Oh, M. H.; Kim, J. S.; Park, T. G.; Nam, Y. S. Prolonged gene silencing by sirna/chitosan-g-deoxycholic acid polyplexes loaded within biodegradable polymer nanoparticles. J. Control. Release 2012, 162, 407–413.CrossRefGoogle Scholar
  143. [143]
    Liu, C. X.; Zhao, G.; Liu, J.; Ma, N. C.; Chivukula, P.; Perelman, L.; Okada, K.; Chen, Z. Y.; Gough, D.; Yu, L. Novel biodegradable lipid nano complex for sirna delivery significantly improving the chemosensitivity of human colon cancer stem cells to paclitaxel. J. Control. Release 2009, 140, 277–283.CrossRefGoogle Scholar
  144. [144]
    Chen, A. M.; Zhang, M.; Wei, D. G.; Stueber, D.; Taratula, O.; Minko, T.; He, H. X. Co-delivery of doxorubicin and Bcl-2 sirna by mesoporous silica nanoparticles enhances the efficacy of chemotherapy in multidrug resistant cancer cells. Small 2009, 5, 2673–2677.CrossRefGoogle Scholar
  145. [145]
    Talekar, M.; Ouyang, Q.; Goldberg, M. S.; Amiji, M. M. Cosilencing of PKM-2 and MDR-1 sensitizes multidrug-resistant ovarian cancer cells to paclitaxel in a murine model of ovarian cancer. Mol. Cancer Ther. 2015, 14, 1521–1531.CrossRefGoogle Scholar
  146. [146]
    Zhang, T. B,; Guo, W. S.; Zhang, C. Q.; Yu, J.; Xu, J.; Li, S. Y.; Tian, J. H.; Wang, P. C.; Xing, J. F.; Liang, X. J. Transferrin-dressed virus-like ternary nanoparticles with aggregation-induced emission for targeted delivery and rapid cytosolic release of sirna. ACS Appl. Mater. Interfaces 2017, 9, 16006–16014.CrossRefGoogle Scholar
  147. [147]
    Gu, X. G.; Kwok, R. T. K.; Lam, J. W. Y; Tang, B. Z. Aiegens for biological process monitoring and disease theranostics. Biomaterials 2017, 146, 115–135.CrossRefGoogle Scholar
  148. [148]
    Wang, Y. F.; Zhang, T. B.; Liang, X. J. Aggregation-induced emission: Lighting up cells, revealing life! Small 2016, 12, 6451–6477.CrossRefGoogle Scholar
  149. [149]
    Xue, X. D.; Jin, S. B.; Zhang, C. Q.; Yang, K. N.; Huo, S. D.; Chen, F.; Zou, G. Z.; Liang, X. J. Probe-inspired nano-prodrug with dual-color fluorogenic property reveals spatiotemporal drug release in living cells. ACS Nano 2015, 9, 2729–2739.CrossRefGoogle Scholar
  150. [150]
    Peer, D.; Karp, J. M.; Hong, S.; Farokhzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2007, 2, 751–760.CrossRefGoogle Scholar
  151. [151]
    Fan, W. P.; Yung, B.; Huang, P.; Chen, X. Y. Nanotechnology for multimodal synergistic cancer therapy. Chem. Rev. 2017, 117, 13566–13638.CrossRefGoogle Scholar
  152. [152]
    Goel, S.; Ni, D. L.; Cai, W. B. Harnessing the power of nanotechnology for enhanced radiation therapy. ACS Nano 2017, 11, 5233–5237.CrossRefGoogle Scholar
  153. [153]
    He, Q. J.; Shi, J. L. MSN anti-cancer nanomedicines: Chemotherapy enhancement, overcoming of drug resistance, and metastasis inhibition. Adv. Mater. 2014, 26, 391–411.CrossRefGoogle Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, CAS Center for Excellence in NanoscienceNational Center for Nanoscience and Technology of ChinaBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Tissue Engineering LabBeijing Institute of Transfusion MedicineBeijingChina

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