Issue

Vol. 12 (2020)

Recent Advances in Tumor Microenvironment Hydrogen Peroxide-Responsive Materials for Cancer Photodynamic Therapy

https://doi.org/10.1007/s40820-019-0347-0
Nan Yang
Key Laboratory of Flexible Electronics (KLOFE) and Institute of Advanced Materials (IAM), School of Physical and Mathematical Sciences, Nanjing Tech University (Nanjing Tech), Nanjing 211800, People’s Republic of China
Wanyue Xiao
Key Laboratory of Flexible Electronics (KLOFE) and Institute of Advanced Materials (IAM), School of Physical and Mathematical Sciences, Nanjing Tech University (Nanjing Tech), Nanjing 211800, People’s Republic of China
Xuejiao Song
Key Laboratory of Flexible Electronics (KLOFE) and Institute of Advanced Materials (IAM), School of Physical and Mathematical Sciences, Nanjing Tech University (Nanjing Tech), Nanjing 211800, People’s Republic of China
Wenjun Wang
School of Physical Science and Information Technology, Liaocheng University, Liaocheng 252059, People’s Republic of China
Xiaochen Dong
Key Laboratory of Flexible Electronics (KLOFE) and Institute of Advanced Materials (IAM), School of Physical and Mathematical Sciences, Nanjing Tech University (Nanjing Tech), Nanjing 211800, People’s Republic of China

Corresponding Author: Xiaochen Dong

iamxcdong@njtech.edu.cn

Nano-Micro Letters, Vol. 12 (2020), Article Number: 15

Abstract

Photodynamic therapy (PDT), as one of the noninvasive clinical cancer phototherapies, suffers from the key drawback associated with hypoxia at the tumor microenvironment (TME), which plays an important role in protecting tumor cells from damage caused by common treatments. High concentration of hydrogen peroxide (H2O2), one of the hallmarks of TME, has been recognized as a double-edged sword, posing both challenges, and opportunities for cancer therapy. The promising perspectives, strategies, and approaches for enhanced tumor therapies, including PDT, have been developed based on the fast advances in H2O2-enabled theranostic nanomedicine. In this review, we outline the latest advances in H2O2-responsive materials, including organic and inorganic materials for enhanced PDT. Finally, the challenges and opportunities for further research on H2O2-responsive anticancer agents are envisioned.


Highlights:


1 The reaction mechanism of various kinds of nanomaterials with endogenous H2O2 is outlined.
2 The design and application guideline for various H2O2-responsive nanomaterials in photodynamic therapy (PDT) are reviewed.
3 The development and prospect of various H2O2-response nanomaterials for PDT and clinical application are envisioned.

Keywords

Tumor microenvironment H2O2-responsive Cancer Nanomaterials Photodynamic therapy
Yang, Nan, Wanyue Xiao, Xuejiao Song, Wenjun Wang, and Xiaochen Dong. 2020. “Recent Advances in Tumor Microenvironment Hydrogen Peroxide-Responsive Materials for Cancer Photodynamic Therapy”. Nano-Micro Letters 12 (January):15. https://doi.org/10.1007/s40820-019-0347-0.
Download Citation
Endnote/Zotero/Mendeley (RIS)
BibTeX
References
  1. K.D. Miller, R.L. Siegel, C.C. Lin, A.B. Mariotto, J.L. Kramer et al., Cancer treatment and survivorship statistics. CA Cancer J. Clin. 66(4), 271–289 (2016). https://doi.org/10.3322/caac.21349
  2. D. Luo, K.A. Carter, D. Miranda, J.F. Lovell, Chemophototherapy: an emerging treatment option for solid tumors. Adv. Sci. 4(1), 1600106 (2017). https://doi.org/10.1002/advs.201600106
  3. I.F. Tannock, C.M. Lee, J.K. Tunggal, D.S.M. Cowan, M.J. Egorin, Limited penetration of anticancer drugs through tumor tissue: a potential cause of resistance of solid tumors to chemotherapy. Clin. Cancer Res. 8(3), 878–884 (2002)
  4. A.P. Castano, P. Mroz, M.R. Hamblin, Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 6(7), 535–545 (2006). https://doi.org/10.1038/nrc1894
  5. P.N. Manghnani, W. Wu, S. Xu, F. Hu, C. The, B. Liu, Visualizing photodynamic therapy in transgenic zebrafish using organic nanoparticles with aggregation-induced emission. Nano-Micro Lett. 10, 61 (2018). https://doi.org/10.1007/s40820-018-0214-4
  6. F. Chen, X. Zhuang, L. Lin, P. Yu, Y. Wang, Y. Shi, G. Hu, Y. Sun, New horizons in tumor microenvironment biology: challenges and opportunities. BMC Med. 13, 45 (2015). https://doi.org/10.1186/s12916-015-0278-7
  7. R. Mroue, M.J. Bissell, Three-dimensional cultures of mouse mammary epithelial cells. Methods Mol. Biol. 945, 221–250 (2013). https://doi.org/10.1007/978-1-62703-125-7_14
  8. M. Wang, J. Zhao, L. Zhang, F. Wei, Y. Lian et al., Role of tumor microenvironment in tumorigenesis. J. Cancer 8(5), 761–773 (2017). https://doi.org/10.7150/jca.17648
  9. D. Hanahan, R.A. Weinberg, Hallmarks of cancer: the next generation. Cell 144(5), 646–674 (2011). https://doi.org/10.1016/j.cell.2011.02.013
  10. C.E. Weber, P.C. Kuo, The tumor microenvironment. Surg. Oncol. 21(3), 172–177 (2012). https://doi.org/10.1016/j.suronc.2011.09.001
  11. M.V. Blagosklonny, Antiangiogenic therapy and tumor progression. Cancer Cell 5(1), 13–17 (2004). https://doi.org/10.1016/S1535-6108(03)00336-2
  12. S. Xu, X. Zhu, C. Zhang, W. Huang, Y. Zhou, D. Yan, Oxygen and Pt(II) self-generating conjugate for synergistic photo-chemo therapy of hypoxic tumor. Nat. Commun. 9(1), 2053 (2018). https://doi.org/10.1038/s41467-018-04318-1
  13. R. Weinstain, E.N. Sayariar, C.N. Felsen, R.Y. Tsien, In vivo targeting of hydrogen peroxide by activatable cell-penetrating peptides. J. Am. Chem. Soc. 136(3), 874–877 (2014). https://doi.org/10.1021/ja411547j
  14. Q. Chen, L. Feng, J. Liu, W. Zhu, Z. Dong, Y. Wu, Z. Liu, Intelligent albumin–MnO2 nanoparticles as pH-/H2O2-responsive dissociable nanocarriers to modulate tumor hypoxia for effective combination therapy. Adv. Mater. 28(33), 7129–7136 (2016). https://doi.org/10.1002/adma.201601902
  15. J. Liu, Q. Chen, W. Zhu, X. Yi, Y. Yang, Z. Dong, Z. Liu, Nanoscale-coordination-polymer-shelled manganese dioxide composite nanoparticles: a multistage redox/pH/H2O2-responsive cancer theranostic nanoplatform. Adv. Funct. Mater. 27(10), 1605926 (2017). https://doi.org/10.1002/adfm.201605926
  16. G. Csire, L. Nagy, K. Varnagy, C. Kallay, Copper(II) interaction with the human prion 103–112 fragment coordination and oxidation. J. Inorg. Biochem. 170, 195–201 (2017). https://doi.org/10.1016/j.jinorgbio.2017.02.018
  17. Q.Y. Tang, W.Y. Xiao, C.H. Huang, W.L. Si, J.J. Shao et al., pH-triggered and enhanced simultaneous photodynamic and photothermal therapy guided by photoacoustic and photothermal imaging. Chem. Mater. 29(12), 5216–5224 (2017). https://doi.org/10.1021/acs.chemmater.7b01075
  18. F. Wang, C. Li, J. Cheng, Z. Yuan, Recent advances on inorganic nanoparticle-based cancer therapeutic agents. Int. J. Environ. Res. Public Health 13(12), 1182 (2016). https://doi.org/10.3390/ijerph13121182
  19. S.S. Lucky, K.C. Soo, Y. Zhang, Nanoparticles in photodynamic therapy. Chem. Rev. 115(4), 1990–2042 (2015). https://doi.org/10.1021/cr5004198
  20. P. Prasad, C.R. Gordijo, A.Z. Abbasi, A. Maeda, A. Ip, A.M. Rauth, R.S. DaCosta, X.Y. Wu, Multifunctional albumin-MnO2 nanoparticles modulate solid tumor microenvironment by attenuating hypoxia, acidosis, vascular endothelial growth factor and enhance radiation response. ACS Nano 8(4), 3202–3212 (2014). https://doi.org/10.1021/nn405773r
  21. Q. Tang, Z. Cheng, N. Yang, Q. Li, P. Wang et al., Hydrangea-structured tumor microenvironment responsive degradable nanoplatform for hypoxic tumor multimodal imaging and therapy. Biomaterials 205, 1–10 (2019). https://doi.org/10.1016/j.biomaterials.2019.03.005
  22. H. Min, J. Wang, Y. Qi, Y. Zhang, X. Han et al., Biomimetic metal-organic framework nanoparticles for cooperative combination of antiangiogenesis and photodynamic therapy for enhanced efficacy. Adv. Mater. 31(15), e1808200 (2019). https://doi.org/10.1002/adma.201808200
  23. Z. Yuan, F. Lu, M. Peng, C.W. Wang, Y.T. Tseng et al., Selective colorimetric detection of hydrogen sulfide based on primary amine-active ester cross-linking of gold nanoparticles. Anal. Chem. 87(14), 7267–7273 (2015). https://doi.org/10.1021/acs.analchem.5b01302
  24. G. Frens, Controlled nucleation for the regulation of the particle size in monodisperse gold suspensions. Nat. Phys. Sci. 241(105), 20–22 (1973). https://doi.org/10.1038/physci241020a0
  25. J. Turkevich, P.C. Stevenson, J. Hillier, A study of the nucleation and growth processes in the synthesis of colloidal gold. Disc. Faraday Soc. 11, 55–75 (1951). https://doi.org/10.1039/df9511100055
  26. Y. Sun, B.T. Mayers, Y. Xia, Template-engaged replacement reaction: a one-step approach to the large-scale synthesis of metal nanostructures with hollow interiors. Nano Lett. 2(5), 481–485 (2002). https://doi.org/10.1021/nl025531v
  27. Y. Sun, Y. Xia, Shape-controlled synthesis of gold and silver nanoparticles. Science 298(5601), 2176–2179 (2002). https://doi.org/10.1126/science.1077229
  28. B. Nikoobakht, M.A. El-Sayed, Preparation and growth mechanism of gold nanorods (NRs) using seed-mediated growth method. Chem. Mater. 15(10), 1957–1962 (2003). https://doi.org/10.1021/cm020732l
  29. A.K. Khan, R. Rashid, G. Murtaza, A. Zahra, Gold nanoparticles: synthesis and applications in drug delivery. Trop. J. Pharm. Res. 13(7), 1169–1177 (2014). https://doi.org/10.4314/tjpr.v13i7.23
  30. D. Pissuwan, S.M. Valenzuela, C.M. Miller, M.B. Cortie, A golden bullet? Selective targeting of toxoplasma gondii tachyzoites using anti body-functionalized gold nanorods. Nano Lett. 7(12), 3808–3812 (2007). https://doi.org/10.1021/nl072377+
  31. R. Vankayala, A. Sagadevan, P. Vijayaraghavan, C.-L. Kuo, K.C. Hwang, Metal nanoparticles sensitize the formation of singlet oxygen. Angew. Chem. Int. Ed. 50(45), 10640–10644 (2011). https://doi.org/10.1002/anie.201105236
  32. C.-P. Liu, T.-H. Wu, C.-Y. Liu, K.-C. Chen, Y.-X. Chen, G.-S. Chen, S.-Y. Lin, Self-supplying O-2 through the catalase-like activity of gold nanoclusters for photodynamic therapy against hypoxic cancer cells. Small 13(26), 1700278 (2017). https://doi.org/10.1002/smll.201700278
  33. Q. Chen, J. Chen, Z. Yang, L. Zhang, Z. Dong, Z. Liu, NIR-II light activated photodynamic therapy with protein-capped gold nanoclusters. Nano Res. 11(10), 5657–5669 (2018). https://doi.org/10.1007/s12274-017-1917-4
  34. J. Wei, J. Li, D. Sun, Q. Li, J. Ma et al., A novel theranostic nanoplatform based on Pd@Pt-PEG-Ce6 for enhanced photodynamic therapy by modulating tumor hypoxia microenvironment. Adv. Funct. Mater. 28(17), 1706310 (2018). https://doi.org/10.1002/adfm.201706310
  35. X.-S. Wang, J.-Y. Zeng, M.-K. Zhang, X. Zeng, X.-Z. Zhang, A versatile Pt-based core–shell nanoplatform as a nanofactory for enhanced tumor therapy. Adv. Funct. Mater. 28(36), 1801783 (2018). https://doi.org/10.1002/adfm.201801783
  36. W.-P. Li, C.-H. Su, Y.-C. Chang, Y.-J. Lin, C.-S. Yeh, Ultrasound-induced reactive oxygen species mediated therapy and imaging using a fenton reaction activable polymersome. ACS Nano 10(2), 2017–2027 (2016). https://doi.org/10.1021/acsnano.5b06175
  37. Z. Ma, M. Zhang, X. Jia, J. Bai, Y. Ruan, C. Wang, X. Sun, X. Jiang, Fe-III-doped two-dimensional C3N4 nanofusiform: a new O2-evolving and mitochondria-targeting photodynamic agent for MRI and enhanced antitumor therapy. Small 12(39), 5477–5487 (2016). https://doi.org/10.1002/smll.201601681
  38. Y. Ruan, X. Jia, C. Wang, W. Zhen, X. Jiang, Mn–FE layered double hydroxide nanosheets: a new photothermal nanocarrier for O2-evolving phototherapy. Chem. Commun. 54(83), 11729–11732 (2018). https://doi.org/10.1039/C8CC06033A
  39. P. Ma, H. Xiao, C. Yu, J. Liu, Z. Cheng et al., Enhanced cisplatin chemotherapy by iron oxide nanocarrier-mediated generation of highly toxic reactive oxygen species. Nano Lett. 17(2), 928–937 (2017). https://doi.org/10.1021/acs.nanolett.6b04269
  40. N. Masomboon, C. Ratanatamskul, M.C. Lu, Chemical oxidation of 2,6-dimethylaniline in the fenton process. Environ. Sci. Technol. 43(22), 8629–8634 (2009). https://doi.org/10.1021/es802274h
  41. E. Brillas, M.A. Baños, S. Camps, C. Arias, P.-L. Cabot, J.A. Garrido, R.M. Rodríguez, Catalytic effect of Fe2+, Cu2+ and UVA light on the electrochemical degradation of nitrobenzene using an oxygen-diffusion cathode. New J. Chem. 28(2), 314–322 (2004). https://doi.org/10.1039/B312445B
  42. T. Soltani, B.-K. Lee, Enhanced formation of sulfate radicals by metal-doped BiFeO3 under visible light for improving photo-fenton catalytic degradation of 2-chlorophenol. Chem. Eng. J. 313, 1258–1268 (2017). https://doi.org/10.1016/j.cej.2016.11.016
  43. B. Ma, S. Wang, F. Liu, S. Zhang, J. Duan et al., Self-assembled copper–amino acid nanoparticles for in situ glutathione “and” H2O2 sequentially triggered chemodynamic therapy. J. Am. Chem. Soc. 141(2), 849–857 (2018). https://doi.org/10.1021/jacs.8b08714
  44. C. Wang, F. Cao, Y. Ruan, X. Jia, W. Zhen, X. Jiang, Specific generation of singlet oxygen through the russell mechanism in hypoxic tumors and GSH depletion by Cu-TCPP nanosheets for cancer therapy. Angew. Chem. Int. Ed. 131(29), 9951–9955 (2019). https://doi.org/10.1002/ange.201903981
  45. Y. Fan, P. Li, B. Hu, T. Liu, Z. Huang et al., A smart photosensitizer-cerium oxide nanoprobe for highly selective and efficient photodynamic therapy. Inorg. Chem. 58(11), 7295–7302 (2019). https://doi.org/10.1021/acs.inorgchem.9b00363
  46. Y. Li, L. An, J. Lin, Q. Tian, S. Yang, Smart nanomedicine agents for cancer, triggered by pH, glutathione, H2O2, or H2S. Int. J. Nanomed. 14, 5729–5749 (2019). https://doi.org/10.2147/IJN.S210116
  47. Y. Zeng, W. Zeng, Q. Zhou, X. Jia, J. Li, Z. Yang, Y. Hao, J. Liu, Hyaluronic acid mediated biomineralization of multifunctional ceria nanocomposites as ROS scavengers and tumor photodynamic therapy agents. J. Mater. Chem. B 7(20), 3210–3219 (2019). https://doi.org/10.1039/C8TB03374A
  48. T. Jia, J. Xu, S. Dong, F. He, C. Zhong et al., Mesoporous cerium oxide-coated upconversion nanoparticles for tumor-responsive chemo-photodynamic therapy and bioimaging. Chem. Sci. 10(37), 8618–8633 (2019). https://doi.org/10.1039/C9SC01615E
  49. W. Jiang, C. Zhang, A. Ahmed, Y. Zhao, Y. Deng, Y. Ding, J. Cai, Y. Hu, H2O2 -sensitive upconversion nanocluster bomb for tri-mode imaging-guided photodynamic therapy in deep tumor tissue. Adv. Healthc. Mater. 8(20), e1900972 (2019). https://doi.org/10.1002/adhm.201900972
  50. X. Lu, M. Zhao, P. Chen, Q. Fan, W. Wang, W. Huang, Enhancing hydrophilicity of photoacoustic probes for effective ratiometric imaging of hydrogen peroxide. J. Mater. Chem. B 6(27), 4531–4538 (2018). https://doi.org/10.1039/C8TB01158C
  51. X. Shang, X. Song, C. Faller, R. Lai, H. Li, R. Cerny, W. Niu, J. Guo, Fluorogenic protein labeling using a genetically encoded unstrained alkene. Chem. Sci. 8(2), 1141–1145 (2017). https://doi.org/10.1039/C6SC03635J
  52. H. Ren, Y. Wu, Y. Li, W. Cao, Z. Sun, H. Xu, X. Zhang, Visible-light-induced disruption of diselenide-containing layer-by-layer films: toward combination of chemotherapy and photodynamic therapy. Small 9(23), 3981–3986 (2013). https://doi.org/10.1002/smll.201300628
  53. R.L. Cunha, I.E. Gouvea, L. Juliano, A glimpse on biological activities of tellurium compounds. An. Acad. Bras. Cienc. 81(3), 393–407 (2009). https://doi.org/10.1590/S0001-37652009000300006
  54. C. Li, R. Pan, P. Li, Q. Guan, J. Ao et al., Hydrogen peroxide-responsive nanoprobe assists circulating tumor cell identification and colorectal cancer diagnosis. Anal. Chem. 89(11), 5966–5975 (2017). https://doi.org/10.1021/acs.analchem.7b00497
  55. Y. Kuang, K. Baakrishnan, V. Gandhi, X. Peng, Hydrogen peroxide inducible DNA cross-linking agents: targeted anticancer prodrugs. J. Am. Chem. Soc. 133(48), 19278–19281 (2011). https://doi.org/10.1021/ja2073824
  56. J. Noh, B. Kwon, E. Han, M. Park, W. Yang et al., Amplification of oxidative stress by a dual stimuli-responsive hybrid drug enhances cancer cell death. Nat. Commun. 6, 6907 (2015). https://doi.org/10.1038/ncomms7907
  57. G. Saravanakumar, J. Kim, W.J. Kim, Reactive-oxygen-species-responsive drug delivery systems: promises and challenges. Adv. Sci. 4(1), 1600124 (2017). https://doi.org/10.1002/advs.201600124
  58. D. Gonzalez-Ballester, A.R. Grossman, in Chapter 5—sulfur: From Acquisition to Assimilation, ed. by E.H. Harris, D.B. Stern, G.B. Witman (Academic Press, London, 2009), pp. 159–187 https://doi.org/10.1016/B978-0-12-370873-1.00013-7
  59. U. Tinggi, Selenium: its role as antioxidant in human health. Environ. Health Prev. Med. 13(2), 102–108 (2008). https://doi.org/10.1007/s12199-007-0019-4
  60. L. Wang, W. Wang, W. Cao, H. Xu, Multi-hierarchical responsive polymers: stepwise oxidation of a selenium- and tellurium-containing block copolymer with sensitivity to both chemical and electrochemical stimuli. Polym. Chem. 8(31), 4520–4527 (2017). https://doi.org/10.1039/C7PY00971B
  61. L. Wang, X. Qu, Y. Xie, S. Lv, Study of 8 types of glutathione peroxidase mimics based on β-cyclodextrin. Catalysts 7(10), 289 (2017). https://doi.org/10.3390/catal7100289
  62. D. Lee, S. Bae, Q. Ke, J. Lee, B. Song et al., Hydrogen peroxide-responsive copolyoxalate nanoparticles for detection and therapy of ischemia–reperfusion injury. J. Control. Release 172(3), 1102–1110 (2013). https://doi.org/10.1016/j.jconrel.2013.09.020
  63. D. Mao, W. Wu, S. Ji, C. Chen, F. Hu, D. Kong, D. Ding, B. Liu, Chemiluminescence-guided cancer therapy using a chemiexcited photosensitizer. Chem 3(6), 991–1007 (2017). https://doi.org/10.1016/j.chempr.2017.10.002
  64. B. Liu, D. Wang, Y. Liu, Q. Zhang, L. Meng et al., Hydrogen peroxide-responsive anticancer hyperbranched polymer micelles for enhanced cell apoptosis. Polym. Chem. 6(18), 3460–3471 (2015). https://doi.org/10.1039/C5PY00257E
  65. J. Wang, H. He, X. Xu, X. Wang, Y. Chen, L. Yin, Far-red light-mediated programmable anti-cancer gene delivery in cooperation with photodynamic therapy. Biomaterials 171, 72–82 (2018). https://doi.org/10.1016/j.biomaterials.2018.04.020
  66. M. Iwaoka, S. Tomoda, A model study on the effect of an amino group on the antioxidant activity of glutathione-peroxidase. J. Am. Chem. Soc. 116(6), 2557–2561 (1994). https://doi.org/10.1021/ja00085a040
  67. T. Sun, Y. Jin, R. Qi, S. Peng, B. Fan, Oxidation responsive mono-cleavable amphiphilic di-block polymer micelles labeled with a single diselenide. Polym. Chem. 4(14), 4017–4023 (2013). https://doi.org/10.1039/c3py00406f
  68. T. Sun, Y. Jin, R. Qi, S. Peng, B. Fan, Post-assembly of oxidation-responsive amphiphilic triblock polymer containing a single diselenide. Macromol. Chem. Phys. 214(24), 2875–2881 (2013). https://doi.org/10.1002/macp.201300579
  69. C. Sun, S. Ji, F. Li, H. Xu, Diselenide-containing hyperbranched polymer with light-induced cytotoxicity. ACS Appl. Mater. Interfaces. 9(15), 12924–12929 (2017). https://doi.org/10.1021/acsami.7b02367
  70. K.Y. Lu, P.Y. Lin, E.Y. Chuang, C.M. Shih, T.M. Cheng et al., H2O2-depleting and O2-generating selenium nanoparticles for fluorescence imaging and photodynamic treatment of proinflammatory-activated macrophages. ACS Appl. Mater. Interfaces. 9(6), 5158–5172 (2017). https://doi.org/10.1021/acsami.6b15515
  71. W. Cao, Y. Gu, M. Meineck, T. Li, H. Xu, Tellurium-containing polymer micelles: competitive-ligand-regulated coordination responsive systems. J. Am. Chem. Soc. 136(13), 5132–5137 (2014). https://doi.org/10.1021/ja500939m
  72. W. Cao, Y. Gu, T. Li, H. Xu, Ultra-sensitive ros-responsive tellurium-containing polymers. Chem. Commun. 51(32), 7069–7071 (2015). https://doi.org/10.1039/C5CC01779C
  73. F. Fan, L. Wang, F. Li, Y. Fu, H. Xu, Stimuli-responsive layer-by-layer tellurium-containing polymer films for the combination of chemotherapy and photodynamic therapy. ACS Appl. Mater. Interfaces. 8(26), 17004–17010 (2016). https://doi.org/10.1021/acsami.6b04998
Read More
Author biographies are not available.
Download this PDF file
PDF
Statistic
Read Counter : 6133 Download : 4660