Skip to main content
Log in

Recent deveolpment of multifunctional responsive gas-releasing nanoplatforms for tumor therapeutic application

  • Review Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

Gas therapy (GT) exhibits great potential for clinical application due to its high therapeutic efficiency, low systemic side effects, and biosafety, thereinto, a multifunctional nanoplatform is generally needed for controllable gas release and precise delivery to tumor tissue. In this review, the recent development of multifunctional nanoplatforms for efficient tumor delivery of stimuli-responsive gas-releasing molecules (GRMs), which could be triggered by either exogenous physical or endogenous tumor microenvironment (TME) is summarized. The reported therapeutic gas molecules, including oxygen (O2), hydrogen sulfide (H2S), nitric oxide (NO), hydrogen (H2), and carbon monoxide (CO), etc., could directly influence or change the pathological status. Additionally, abundant nanocarriers have been employed for gas delivery into cancer region, such as mesoporous silica nanoparticles (MSNs), metal-organic frameworks (MOFs), two-dimensional (2D) nanomaterials, and liposomes, as well as non-nanocarriers including inorganic and organic nanoparticles. In the end, the outlooks of current challenges of GT and GRMs delivery nanoplatforms as well as the prospects of future clinical applications are proposed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Chen, L. C.; Zhou, S. F.; Su, L. C.; Song, J. B. Gas-mediated cancer bioimaging and therapy. ACS Nano 2019, 13, 10887–10917.

    CAS  Google Scholar 

  2. Jia, L. F.; Zhang, W. C.; Wang, C. Y. BMI1 inhibition eliminates residual cancer stem cells after PD1 blockade and activates antitumor immunity to prevent metastasis and relapse. Cell Stem Cell 2020, 27, 238–253.

    CAS  Google Scholar 

  3. Shannon, A. M.; Bouchier-Hayes, D. J.; Condron, C. M.; Toomey, D. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat. Rev. 2003, 29, 297–307.

    CAS  Google Scholar 

  4. Xavierselvan, M.; Cook, J.; Duong, J.; Diaz, N.; Homan, K.; Mallidi, S. Photoacoustic nanodroplets for oxygen enhanced photodynamic therapy of cancer. Photoacoustics 2022, 25, 100306.

    Google Scholar 

  5. Markman, J. L.; Rekechenetskiy, A.; Holler, E.; Ljubimova, J. Y. Nanomedicine therapeutic approaches to overcome cancer drug resistance. Adv. Drug Deliver. Rev. 2013, 65, 1866–1879.

    CAS  Google Scholar 

  6. He, Q. J. Precision gas therapy using intelligent nanomedicine. Biomater. Sci. 2017, 5, 2226–2230.

    CAS  Google Scholar 

  7. Szabó, C. Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 2007, 6, 917–935.

    Google Scholar 

  8. Szabó, C. Gasotransmitters in cancer: From pathophysiology to experimental therapy. Nat. Rev. Drug Discov. 2016, 15, 185–203.

    Google Scholar 

  9. Motterlini, R.; Otterbein, L. E. The therapeutic potential of carbon monoxide. Nat. Rev. Drug Discov. 2010, 9, 728–743.

    CAS  Google Scholar 

  10. Wegiel, B.; Gallo, D.; Csizmadia, E.; Harris, C.; Belcher, J.; Vercellotti, G. M.; Penacho, N.; Seth, P.; Sukhatme, V.; Ahmed, A. et al. Carbon monoxide expedites metabolic exhaustion to inhibit tumor growth. Cancer Res. 2013, 73, 7009–7021.

    CAS  Google Scholar 

  11. Moncada, S.; Erusalimsky, J. D. Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev. Mol. Cell Biol. 2002, 3, 214–220.

    CAS  Google Scholar 

  12. Wong, C. C. L.; Gilkes, D. M.; Zhang, H. F.; Chen, J.; Wei, H.; Chaturvedi, P.; Fraley, S. I.; Wong, C. M.; Khoo, U. S.; Ng, I. O. L. et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc. Natl. Acad. Sci. USA 2011, 108, 16369–16374.

    CAS  Google Scholar 

  13. Song, G. S.; Cheng, L.; Chao, Y.; Yang, K.; Liu, Z. Emerging nanotechnology and advanced materials for cancer radiation therapy. Adv. Mater. 2017, 29, 1700996.

    Google Scholar 

  14. Wang, Y. S.; Yang, T.; He, Q. J. Strategies for engineering advanced nanomedicines for gas therapy of cancer. Natl. Sci. Rev. 2020, 7, 1485–1512.

    CAS  Google Scholar 

  15. Powell, C. R.; Dillon, K. M.; Matson, J. B. A review of hydrogen sulfide (H2S) donors: Chemistry and potential therapeutic applications. Biochem. Pharmacol. 2018, 149, 110–123.

    CAS  Google Scholar 

  16. Ji, X. Y.; Wang, B. H. Strategies toward organic carbon monoxide prodrugs. Acc. Chem. Res. 2018, 51, 1377–1385.

    CAS  Google Scholar 

  17. Brown, J. M.; Wilson, W. R. Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 2004, 4, 437–447.

    CAS  Google Scholar 

  18. Chen, Q.; Liang, C.; Sun, X. Q.; Chen, J. W.; Yang, Z. J.; Zhao, H.; Feng, L. Z.; Liu, Z. H2O2-responsive liposomal nanoprobe for photoacoustic inflammation imaging and tumor theranostics via in vivo chromogenic assay. Proc. Natl. Acad. Sci. USA. 2017, 114, 5343–5348.

    CAS  Google Scholar 

  19. Maman, S.; Witz, I. P. A history of exploring cancer in context. Nat. Rev. Cancer 2018, 18, 359–376.

    CAS  Google Scholar 

  20. Zhao, Y. J.; Ouyang, X. M.; Peng, Y. J.; Peng, S. J. Stimuli responsive nitric oxide-based nanomedicine for synergistic therapy. Pharmaceutics 2021, 13, 1917.

    CAS  Google Scholar 

  21. Yu, L. D.; Hu, P.; Chen, Y. Gas-generating nanoplatforms: Material chemistry, multifunctionality, and gas therapy. Adv. Mater. 2018, 30, 1801964.

    Google Scholar 

  22. Wu, X. Q.; Cheng, Y.; Zheng, R. X.; Xu, K. Q.; Yan, J.; Song, P. P.; Wang, Y. J.; Rauf, A.; Pan, Y.; Zhang, H. Y. Immunomodulation of tumor microenvironment by arginine-loaded iron oxide nanoparticles for gaseous immunotherapy. ACS Appl. Mater. Interfaces 2021, 13, 19825–19835.

    CAS  Google Scholar 

  23. Yang, Z. B.; Luo, Y.; Hu, Y. A.; Liang, K. C.; He, G.; Chen, Q.; Wang, Q. G.; Chen, H. R. Photothermo-promoted nanocatalysis combined with H2S-mediated respiration inhibition for efficient cancer therapy. Adv. Funct. Mater. 2021, 31, 2007991.

    CAS  Google Scholar 

  24. Kresge, C. T.; Leonowicz, M. E.; Roth, W. J.; Vartuli, J. C.; Beck, J. S. Ordered mesoporous molecular sieves synthesized by a liquid-crystal template mechanism. Nature 1992, 359, 710–712.

    CAS  Google Scholar 

  25. Manzano, M.; Vallet-Regí, M. Mesoporous silica nanoparticles for drug delivery. Adv. Funct. Mater. 2020, 30, 1902634.

    CAS  Google Scholar 

  26. Yang, B. W.; Chen, Y.; Shi, J. L. Mesoporous silica/organosilica nanoparticles: Synthesis, biological effect and biomedical application. Mater. Sci. Eng. R Rep. 2019, 137, 66–105.

    Google Scholar 

  27. Davis, M. E. Ordered porous materials for emerging applications. Nature 2002, 417, 813–821.

    CAS  Google Scholar 

  28. Wang, P. G.; Xian, M.; Tang, X. P.; Wu, X. J.; Wen, Z.; Cai, T. W.; Janczuk, A. J. Nitric oxide donors: Chemical activities and biological applications. Chem. Rev. 2002, 102, 1091–1134.

    CAS  Google Scholar 

  29. G, U. R.; Axthelm, J.; Hoffmann, P.; Taye, N.; Gläser, S.; Görls, H.; Hopkins, S. L.; Plass, W.; Neugebauer, U.; Bonnet, S. et al. Coregistered molecular logic gate with a CO-releasing molecule triggered by light and peroxide. J. Am. Chem. Soc. 2017, 139, 4991–4994.

    CAS  Google Scholar 

  30. Rimmer, R. D.; Pierri, A. E.; Ford, P. C. Photochemically activated carbon monoxide release for biological targets. Toward developing air-stable photoCORMs labilized by visible light. Coordin. Chem. Rev. 2012, 256, 1509–1519.

    CAS  Google Scholar 

  31. Hong, G. S.; Lee, J. C.; Robinson, J. T.; Raaz, U.; Xie, L. M.; Huang, N. F.; Cooke, J. P.; Dai, H. J. Multifunctional in vivo vascular imaging using near-infrared II fluorescence. Nat. Med. 2012, 18, 1841–1846.

    CAS  Google Scholar 

  32. Tsai, M. F.; Chang, S. H. G.; Cheng, F. Y.; Shanmugam, V.; Cheng, Y. S.; Su, C. H.; Yeh, C. S. Au nanorod design as lightabsorber in the first and second biological near-infrared windows for in vivo photothermal therapy. ACS Nano 2013, 7, 5330–5342.

    CAS  Google Scholar 

  33. Guo, R. R.; Tian, Y.; Wang, Y. J.; Yang, W. L. Near-infrared lasertriggered nitric oxide nanogenerators for the reversal of multidrug resistance in cancer. Adv. Funct. Mater. 2017, 27, 1606398.

    Google Scholar 

  34. 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-infrared-sensitized upconversion nanoparticles for tumor therapy. Adv. Funct. Mater. 2015, 25, 3049–3056.

    CAS  Google Scholar 

  35. Marin, A.; Muniruzzaman, M.; Rapoport, N. Mechanism of the ultrasonic activation of micellar drug delivery. J. Control. Release 2001, 75, 69–81.

    CAS  Google Scholar 

  36. Chen, J.; Luo, H. L.; Liu, Y.; Zhang, W.; Li, H. X.; Luo, T.; Zhang, K.; Zhao, Y. X.; Liu, J. J. Oxygen-self-produced nanoplatform for relieving hypoxia and breaking resistance to sonodynamic treatment of pancreatic cancer. ACS Nano 2017, 11, 12849–12862.

    CAS  Google Scholar 

  37. Jin, Z. K.; Wen, Y. Y.; Hu, Y. X.; Chen, W. W.; Zheng, X. F.; Guo, W. S.; Wang, T. F.; Qian, Z. Y.; Su, B. L.; He, Q. J. MRI-guided and ultrasound-triggered release of NO by advanced nanomedicine. Nanoscale 2017, 9, 3637–3645.

    CAS  Google Scholar 

  38. Zhang, K.; Xu, H. X.; Jia, X. Q.; Chen, Y.; Ma, M.; Sun, L. P.; Chen, H. R. Ultrasound-triggered nitric oxide release platform based on energy transformation for targeted inhibition of pancreatic tumor. ACS Nano 2016, 10, 10816–10828.

    CAS  Google Scholar 

  39. Cao, W.; Gu, Y. W.; Meineck, M.; Xu, H. P. The combination of chemotherapy and radiotherapy towards more efficient drug delivery. Chem. Asian J. 2014, 9, 48–57.

    CAS  Google Scholar 

  40. Fan, W. P.; Bu, W. B.; Zhang, Z.; Shen, B.; Zhang, H.; He, Q. J.; Ni, D. L.; Cui, Z. W.; Zhao, K. L.; Bu, J. W. et al. X-ray radiation-controlled no-release for ON-demand depth-independent hypoxic radiosensitization. Angew. Chem., Int. Ed. 2015, 54, 14026–14030.

    CAS  Google Scholar 

  41. Juzenas, P.; Chen, W.; Sun, Y. P.; Coelho, M. A. N.; Generalov, R.; Generalov, N.; Christensen, I. L. Quantum dots and nanoparticles for photodynamic and radiation therapies of cancer. Adv. Drug Deliver. Rev. 2008, 60, 1600–1614.

    CAS  Google Scholar 

  42. Ma, N.; Xu, H. P.; An, L. P.; Li, J.; Sun, Z. W.; Zhang, X. Radiation-sensitive diselenide block co-polymer micellar aggregates: Toward the combination of radiotherapy and chemotherapy. Langmuir 2011, 27, 5874–5878.

    CAS  Google Scholar 

  43. Shao, D.; Zhang, F.; Chen, F. M.; Zheng, X.; Hu, H. Z.; Yang, C.; Tu, Z. X.; Wang, Z.; Chang, Z. M.; Lu, J. N. et al. Biomimetic diselenide-bridged mesoporous organosilica nanoparticles as an X-ray-responsive biodegradable carrier for chemo-immunotherapy. Adv. Mater 2020, 32, 2004385.

    CAS  Google Scholar 

  44. Dou, Y.; Liu, Y. J.; Zhao, F. S.; Guo, Y. Y.; Li, X.; Wu, M. L.; Chang, J.; Yu, C. S. Radiation-responsive scintillating nanotheranostics for reduced hypoxic radioresistance under ROS/NO-mediated tumor microenvironment regulation. Theranostics 2018, 8, 5870–5889.

    CAS  Google Scholar 

  45. Liu, T. Z.; Zhang, N.; Wang, Z. G.; Wu, M. Y.; Chen, Y.; Ma, M.; Chen, H. R.; Shi, J. L. Endogenous catalytic generation of O2 bubbles for in situ ultrasound-guided high intensity focused ultrasound ablation. ACS Nano 2017, 11, 9093–9102.

    CAS  Google Scholar 

  46. Fan, W. P.; Lu, N.; Huang, P.; Liu, Y.; Yang, Z.; Wang, S.; Yu, G. C.; Liu, Y. J.; Hu, J. K.; He, Q. J. et al. Glucose-responsive sequential generation of hydrogen peroxide and nitric oxide for synergistic cancer starving-like/gas therapy. Angew. Chem. 2017, 129, 1249–1253.

    Google Scholar 

  47. Jin, Z. K.; Wen, Y. Y.; Xiong, L. W.; Yang, T.; Zhao, P. H.; Tan, L. W.; Wang, T. F.; Qian, Z. Y.; Su, B. L.; He, Q. J. Intratumoral H2O2-triggered release of CO from a metal carbonyl-based nanomedicine for efficient CO therapy. Chem. Commun. 2017, 53, 5557–5560.

    CAS  Google Scholar 

  48. Laurent, S.; Forge, D.; Port, M.; Roch, A.; Robic, C.; Elst, L. V.; Muller, R. N. Magnetic iron oxide nanoparticles: Synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem. Rev. 2010, 110, 2574.

    CAS  Google Scholar 

  49. Liu, J. A.; Bu, W. B.; Pan, L. M.; Shi, J. L. NIR-triggered anticancer drug delivery by upconverting nanoparticles with integrated azobenzene-modified mesoporous silica. Angew. Chem., Int. Ed. 2013, 52, 4375–4379.

    CAS  Google Scholar 

  50. Thomas, C. R.; Ferris, D. P.; Lee, J. H.; Choi, E.; Cho, M. H.; Kim, E. S.; Stoddart, J. F.; Shin, J. S.; Cheon, J.; Zink, J. I. Noninvasive remote-controlled release of drug molecules in vitro using magnetic actuation of mechanized nanoparticles. J. Am. Chem. Soc. 2010, 132, 10623–10625.

    CAS  Google Scholar 

  51. Choi, H. W.; Kim, J.; Kim, J.; Kim, Y.; Song, H. B.; Kim, J. H.; Kim, K.; Kim, W. J. Light-induced acid generation on a gatekeeper for smart nitric oxide delivery. ACS Nano 2016, 10, 4199–4208.

    CAS  Google Scholar 

  52. Zhao, B.; Zhao, P. H.; Jin, Z. K.; Fan, M. J.; Meng, J.; He, Q. J. Programmed ROS/CO-releasing nanomedicine for synergetic chemodynamic-gas therapy of cancer. J. Nanobiotechnol. 2019, 17, 75.

    Google Scholar 

  53. Yang, T.; Jin, Z. K.; Wang, Z. H.; Zhao, P. H.; Zhao, B.; Fan, M. J.; Chen, L. H.; Wang, T. F; Su, B. L.; He, Q. J. Intratumoral high-payload delivery and acid-responsive release of H2 for efficient cancer therapy using the ammonia borane-loaded mesoporous silica nanomedicine. Appl. Mater. Today 2018, 11, 136–143.

    Google Scholar 

  54. Yaghi, O. M.; Li, H. L. Hydrothermal synthesis of a metal-organic framework containing large rectangular channels. J. Am. Chem. Soc. 1995, 117, 10401–10402.

    CAS  Google Scholar 

  55. Yaghi, O. M.; Li, G. M.; Li, H. L. Selective binding and removal of guests in a microporous metal-organic framework. Nature 1995, 378, 703–706.

    CAS  Google Scholar 

  56. Jiao, L.; Wang, Y.; Jiang, H. L.; Xu, Q. Metal-organic frameworks as platforms for catalytic applications. Adv. Mater 2018, 30, 1703663.

    Google Scholar 

  57. Zhao, X.; Wang, Y. X.; Li, D. S.; Bu, X. H.; Feng, P. Y. Metal-organic frameworks for separation. Adv. Mater 2011, 33, 1705189.

    Google Scholar 

  58. Yang, J.; Yang, Y. W. Metal-organic frameworks for biomedical applications. Small 2020, 16, 1906846.

    CAS  Google Scholar 

  59. Chen, J. J.; Zhu, Y. F.; Kaskel, S. Porphyrin-based metal-organic frameworks for biomedical applications. Angew. Chem., Int. Ed. 2021, 60, 5010–5035.

    CAS  Google Scholar 

  60. Gao, P.; Chen, Y. Y.; Pan, W.; Li, N.; Liu, Z.; Tang, B. Antitumor agents based on metal-organic frameworks. Angew. Chem., Int. Ed. 2021, 60, 16763–16776.

    CAS  Google Scholar 

  61. Jin, D. N.; Zhang, J. A.; Huang, Y. Y.; Qin, X. R.; Zhuang, J. Y.; Yin, W. J.; Chen, S. J.; Wang, Y.; Hua, P.; Yao, Y. Recent advances in the development of metal-organic framework-based gas-releasing nanoplatforms for synergistic cancer therapy. Dalton Trans. 2021, 53, 1189–1196.

    Google Scholar 

  62. Pinto, R. V.; Wang, S. J.; Tavares, S. R.; Pires, J.; Antunes, F.; Vimont, A.; Clet, G.; Daturi, M.; Maurin, G.; Serre, C. et al. Tuning cellular biological functions through the controlled release of NO from a porous Ti-MOF. Angew. Chem., Int. Ed. 2020, 59, 5135–5143.

    CAS  Google Scholar 

  63. Jin, Z. K.; Zhao, P. H.; Zhang, J. H.; Yang, T.; Zhou, G. X.; Zhang, D. H.; Wang, T. F.; He, Q. J. Intelligent metal carbonyl metal-organic framework nanocomplex for fluorescent traceable H2O2-triggered CO delivery. Chem.—Eur. J. 2018, 24, 11667–11674.

    CAS  Google Scholar 

  64. Cai, W.; Wang, J. Q.; Chu, C. C.; Chen, W.; Wu, C. S.; Liu, G. Metal-organic framework-based stimuli-responsive systems for drug delivery. Adv. Sci. 2019, 6, 1801526.

    Google Scholar 

  65. Gao, S. T.; Zheng, P. L.; Li, Z. H.; Feng, X. C.; Yan, W. X.; Chen, S. Z.; Guo, W. S.; Liu, D. D.; Yang, X. J.; Wang, S. X. et al. Biomimetic O2-evolving metal-organic framework nanoplatform for highly efficient photodynamic therapy against hypoxic tumor. Biomaterials 2018, 178, 83–94.

    CAS  Google Scholar 

  66. Yao, J. Z.; Liu, Y.; Wang, J. W.; Jiang, Q.; She, D. J.; Guo, H. S.; Sun, N. R.; Pang, Z. Q.; Deng, C. H.; Yang, W. L. et al. On-demand CO release for amplification of chemotherapy by MOF functionalized magnetic carbon nanoparticles with NIR irradiation. Biomaterials 2019, 195, 51–62.

    CAS  Google Scholar 

  67. Diring, S.; Carné-Sánchez, A.; Zhang, J. C.; Ikemura, S.; Kim, C.; Inaba, H.; Kitagawa, S.; Furukawa, S. Light responsive metal-organic frameworks as controllable CO-releasing cell culture substrates. Chem. Sci. 2017, 8, 2381–2386.

    CAS  Google Scholar 

  68. An, J.; Hu, Y. G.; Li, C.; Hou, X. L.; Cheng, K.; Zhang, B.; Zhang, R. Y.; Li, D. Y.; Liu, S. J.; Liu, B. et al. A pH/ultrasound dual-response biomimetic nanoplatform for nitric oxide gas-sonodynamic combined therapy and repeated ultrasound for relieving hypoxia. Biomaterials 2020, 230, 119636.

    CAS  Google Scholar 

  69. Cheng, H.; Zhu, J. Y.; Li, S. Y.; Zeng, J. Y.; Lei, Q.; Chen, K. W.; Zhang, C.; Zhang, X. An O2 self-sufficient biomimetic nanoplatform for highly specific and efficient photodynamic therapy. Adv. Funct. Mater. 2016, 26, 7847–7860.

    CAS  Google Scholar 

  70. Feng, J.; Yu, W. Q.; Xu, Z.; Wang, F. A. An intelligent ZIF-8-gated polydopamine nanoplatform for in vivo cooperatively enhanced combination phototherapy. Chem. Sci. 2020, 11, 1649–1656.

    CAS  Google Scholar 

  71. Ren, Q.; Yu, N.; Wang, L. Y.; Wen, M.; Geng, P.; Jiang, Q.; Li, M. Q.; Chen, Z. G. Nanoarchitectonics with metal-organic frameworks and platinum nanozymes with improved oxygen evolution for enhanced sonodynamic/chemo-therapy. J. Colloid Interface Sci. 2022, 614, 147–159.

    CAS  Google Scholar 

  72. He, L. C.; Ni, Q. Q.; Mu, J.; Fan, W. P.; Liu, L.; Wang, Z. T.; Li, L.; Tang, W.; Liu, Y. J.; Cheng, Y. Y. et al. Solvent-assisted self-assembly of a metal-organic framework based biocatalyst for cascade reaction driven photodynamic therapy. J. Am. Chem. Soc. 2020, 142, 6822–6832.

    CAS  Google Scholar 

  73. Johnson, T. R.; Mann, B. E.; Clark, J. E.; Foresti, R.; Green, C. J.; Motterlini, R. Metal carbonyls: A new class of pharmaceuticals? Angew. Chem., Int. Ed. 2003, 42, 3722–3729.

    CAS  Google Scholar 

  74. Johnson, T. R.; Mann, B. E.; Clark, J. E.; Foresti, R.; Green, C. J.; Motterlini, R. Carbonylmetallkomplexe-eine neue klasse von pharmazeutika? Angew. Chem. 2003, 115, 3850–3858.

    Google Scholar 

  75. Guan, Q.; Zhou, L. L.; Li, Y. A.; Dong, Y. B. A nanoscale metal-organic framework for combined photodynamic and starvation therapy in treating breast tumors. Chem. Commun. 2019, 55, 14898–14901.

    CAS  Google Scholar 

  76. Xie, Z. X.; Liang, S.; Cai, X. H.; Ding, B. B.; Huang, S. S.; Hou, Z. Y.; Ma, P. A.; Cheng, Z. Y.; Lin, J. O2-Cu/ZIF-8@Ce6/ZIF-8@F127 composite as a tumor microenvironment-responsive nanoplatform with enhanced photo-/chemodynamic antitumor efficacy. ACS Appl. Mater. Interfaces 2019, 11, 31671–31680.

    CAS  Google Scholar 

  77. Gao, S. T.; Jin, Y.; Ge, K.; Li, Z. H.; Liu, H. F.; Dai, X. Y.; Zhang, Y. H.; Chen, S. Z.; Liang, X. J.; Zhang, J. C. Self-supply of O2 and H2O2 by a nanocatalytic medicine to enhance combined chemo/chemodynamic therapy. Adv. Sci. 2019, 6, 1902137.

    CAS  Google Scholar 

  78. Yao, X. X.; Chen, D. Y.; Zhao, B.; Yang, B. R.; Jin, Z. K.; Fan, M. J.; Tao, G. R.; Qin, S. C.; Yang, W. L.; He, Q. J. Acid-degradable hydrogen-generating metal-organic framework for overcoming cancer resistance/metastasis and off-target side effects. Adv. Sci. 2022, 9, 2101965.

    CAS  Google Scholar 

  79. Liu, Z.; Robinson, J. T.; Sun, X. M.; Dai, H. J. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J. Am. Chem. Soc. 2008, 130, 10876–10877.

    CAS  Google Scholar 

  80. Zhang, L. M.; Xia, J. G.; Zhao, Q. H.; Liu, L. W.; Zhang, Z. J. Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs. Small 2010, 6, 537–544.

    CAS  Google Scholar 

  81. Xu, J. S.; Zeng, F.; Wu, H.; Hu, C. P.; Yu, C. M.; Wu, S. Z. Preparation of a mitochondria-targeted and no-releasing nanoplatform and its enhanced pro-apoptotic effect on cancer cells. Small 2014, 13, 3750–3760.

    CAS  Google Scholar 

  82. Wei, F. M.; Kuang, S.; Rees, T. W.; Liao, X. X.; Liu, J. P.; Luo, D. Q.; Wang, J. Q.; Zhang, X. T.; Ji, L. N.; Chao, H. Ruthenium(II) complexes coordinated to graphitic carbon nitride: Oxygen self-sufficient photosensitizers which produce multiple ROS for photodynamic therapy in hypoxia. Biomaterials 2021, 276, 121064.

    CAS  Google Scholar 

  83. Jin, Z. K.; Duo, Y. H.; Li, Y.; Qiu, M.; Jiang, M. N.; Liu, Q.; Zhao, P. H.; Yang, T.; Liang, W. Y.; Zhang, H. et al. A novel NIR-responsive CO gas-releasing and hyperthermia-generating nanomedicine provides a curative approach for cancer therapy. Nano Today 2021, 38, 101197.

    CAS  Google Scholar 

  84. Chen, D. Y.; Jin, Z. K.; Zhao, B.; Wang, Y. S.; He, Q. J. MBene as a theranostic nanoplatform for photocontrolled intratumoral retention and drug release. Adv. Mater 2021, 33, 2008089.

    CAS  Google Scholar 

  85. Robinson, J. T.; Tabakman, S. M.; Liang, Y. Y.; Wang, H. L.; Casalongue, H. S.; Vinh, D.; Dai, H. J. Ultrasmall reduced graphene oxide with high near-infrared absorbance for photothermal therapy. J. Am. Chem. Soc. 2011, 133, 6825–6831.

    CAS  Google Scholar 

  86. Yang, Z. B.; Liu, J. T.; Liu, J. K.; Chen, X. L.; Yan, T. T.; Chen, Q. H. Investigation on physicochemical properties of graphene oxide/nano-hydroxyapatite composites and its biomedical applications. J. Aust. Ceram. Soc. 2021, 57, 625–633.

    CAS  Google Scholar 

  87. He, Q. J.; Kiesewetter, D. O.; Qu, Y.; Fu, X.; Fan, J.; Huang, P.; Liu, Y. J.; Zhu, G. Z.; Liu, Y.; Qian, Z. Y. et al. NIR-responsive on-demand release of CO from metal carbonyl-caged graphene oxide nanomedicine. Adv. Mater 2015, 27, 6740–6746.

    Google Scholar 

  88. Fan, J.; He, N. Y.; He, Q. J.; Liu, Y.; Ma, Y.; Fu, X.; Liu, Y. J.; Huang, P.; Chen, X. Y. A novel self-assembled sandwich nanomedicine for NIR-responsive release of NO. Nanoscale 2015, 7, 20055–20062.

    CAS  Google Scholar 

  89. Li, H. F.; Yao, Y.; Shi, H.; Lei, Y. L.; Wang, K. M.; He, X. X.; Liu, J. B. A near-infrared light-responsive nanocomposite for photothermal release of H2S and suppression of cell viability. J. Mater. Chem. B 2019, 7, 5992–5997.

    CAS  Google Scholar 

  90. Cao, L.; Wang, X.; Meziani, M. J.; Lu, F. S.; Wang, H. F.; Luo, P. G.; Lin, Y.; Harruff, B. A.; Veca, M.; Murray, D. et al. Carbon dots for multiphoton bioimaging. J. Am. Chem. Soc. 2007, 129, 11318–11319.

    CAS  Google Scholar 

  91. Yang, Z. B.; Luo, Y.; Yu, H. Z.; Liang, K. C.; Wang, M.; Wang, Q. G.; Yin, B.; Chen, H. R. Reshaping the tumor immune microenvironment based on a light-activated nanoplatform for efficient cancer therapy. Adv. Mater. 2022, 34, 2108908.

    CAS  Google Scholar 

  92. Fang, X.; Cai, S. X.; Wang, M.; Chen, Z. W.; Lu, C. H.; Yang, H. H. Photogenerated holes mediated nitric oxide production for hypoxic tumor treatment. Angew. Chem., Int. Ed. 2021, 60, 7046–7050.

    CAS  Google Scholar 

  93. Liu, X.; Liu, Y. L.; Thakor, A. S.; Kevadiya, B. D.; Cheng, J. M.; Chen, M. L.; Li, Y.; Xu, Q.; Wu, Q. H.; Wu, Y. et al. Endogenous NO-releasing carbon nanodots for tumor-specific gas therapy. Acta Biomater. 2021, 136, 485–494.

    CAS  Google Scholar 

  94. Fan, M. J.; Wen, Y. Y.; Ye, D. E.; Jin, Z. K.; Zhao, P. H.; Chen, D. Y.; Lu, X. F.; He, Q. J. Acid-responsive H2-releasing 2D MgB2 nanosheet for therapeutic synergy and side effect attenuation of gastric cancer chemotherapy. Adv. Healthcare Mater. 2019, 8, 1900157.

    Google Scholar 

  95. Bangham, A. D.; Standish, M. M.; Watkins, J. C. Diffusion of univalent ions across the lamellae of swollen phospholipids. Mol. Biol. 1965, 13, 238–252, IN26-IN27.

    CAS  Google Scholar 

  96. Long, M. M.; Lu, A. L.; Lu, M.; Weng, L. Y.; Chen, Q. P.; Zhu, L.; Chen, Z. P. Azo-inserted responsive hybrid liposomes for hypoxiaspecific drug delivery. Acta Biomater. 2020, 115, 343–357.

    CAS  Google Scholar 

  97. Opoku-Damoah, Y.; Zhang, R.; Ta, H. T.; Jose, D. A.; Sakla, R.; Xu, Z. P. Lipid-encapsulated upconversion nanoparticle for near-infrared light-mediated carbon monoxide release for cancer gas therapy. Eur. J. Pharm. Biopharm. 2021, 158, 211–221.

    CAS  Google Scholar 

  98. Wu, W. W.; Yang, Y.; Liang, Z. Y.; Song, X. L.; Huang, Y. D.; Qiu, L.; Qiu, X. Z.; Yu, S. M.; Xue, W. Near infrared II laser controlled free radical releasing nanogenerator for synergistic nitric oxide and alkyl radical therapy of breast cancer. Nanoscale 2021, 13, 11169–11187.

    CAS  Google Scholar 

  99. Zhang, Z.; Yang, J. R.; Min, Q. Q.; Ling, C. J.; Maiti, D.; Xu, J. Y.; Qin, L. Q.; Yang, K. Holo-lactoferrin modified liposome for relieving tumor hypoxia and enhancing radiochemotherapy of cancer. Small 2019, 15, 1803703.

    Google Scholar 

  100. Suchyta, D. J.; Schoenfisch, M. H. Encapsulation of N-diazeniumdiolates within liposomes for enhanced nitric oxide donor stability and delivery. Mol. Pharmaceutics 2015, 12, 3569–3574.

    CAS  Google Scholar 

  101. Chen, X. H.; Jia, F.; Li, Y. Z.; Deng, Y. Y.; Huang, Y.; Liu, W. F.; Jin, Q.; Ji, J. Nitric oxide-induced stromal depletion for improved nanoparticle penetration in pancreatic cancer treatment. Biomaterials 2020, 246, 119999.

    CAS  Google Scholar 

  102. Zhang, X. B.; Li, N.; Zhang, S. W.; Sun, B. J.; Chen, Q.; He, Z. G.; Luo, C.; Sun, J. Emerging carrier-free nanosystems based on molecular self-assembly of pure drugs for cancer therapy. Med. Res. Rev. 2020, 40, 1754–1775.

    CAS  Google Scholar 

  103. Li, Y. A.; Yang, Y. L.; An, F. F.; Liu, Z.; Zhang, X. J.; Zhang, X. H. Carrier-free, functionalized pure drug nanorods as a novel cancer-targeted drug delivery platform. Nanotechnology 2013, 24, 015103.

    Google Scholar 

  104. Zhang, X.; Du, J. F.; Guo, Z.; Yu, J.; Gao, Q.; Yin, W. Y.; Zhu, S.; Gu, Z. J.; Zhao, Y. L. Efficient near infrared light triggered nitric oxide release nanocomposites for sensitizing mild photothermal therapy. Adv. Sci. 2019, 6, 1801122.

    Google Scholar 

  105. Zhao, P. H.; Jin, Z. K.; Chen, Q.; Yang, T.; Chen, D. Y.; Meng, J.; Lu, X. F.; Gu, Z.; He, Q. J. Local generation of hydrogen for enhanced photothermal therapy. Nat. Commun. 2018, 9, 4241.

    Google Scholar 

  106. Xue, Z. L.; Jiang, M. Y.; Liu, H. R.; Zeng, S. J.; Hao, J. H. Low dose soft X-ray-controlled deep-tissue long-lasting NO release of persistent luminescence nanoplatform for gas-sensitized anticancer therapy. Biomaterials 2020, 263, 120384.

    CAS  Google Scholar 

  107. Zhang, F. M.; Liu, S. K.; Zhang, N.; Kuang, Y.; Li, W. T.; Gai, S. L.; He, F.; Gulzar, A.; Yang, P. P. X-ray-triggered NO-released Bi-SNO nanoparticles: All-in-one nano-radiosensitizer with photothermal/gas therapy for enhanced radiotherapy. Nanoscale 2020, 12, 19293–19307.

    CAS  Google Scholar 

  108. Wang, Y.; Zhang, J. Y.; Lv, X. Y.; Wang, L.; Zhong, Z. H.; Yang, D. P.; Si, W. L.; Zhang, T.; Dong, X. C. Mitoxantrone as photothermal agents for ultrasound/fluorescence imaging-guided chemo-phototherapy enhanced by intratumoral H2O2-Induced CO. Biomaterials 2020, 252, 120111.

    CAS  Google Scholar 

  109. Sasakura, K.; Hanaoka, K.; Shibuya, N.; Mikami, Y.; Kimura, Y.; Komatsu, T.; Ueno, T.; Terai, T.; Kimura, H.; Nagano, T. Development of a highly selective fluorescence probe for hydrogen sulfide. J. Am. Chem. Soc. 2011, 133, 18003–18005.

    CAS  Google Scholar 

  110. Zheng, H. L.; Ma, B. X.; Shi, Y. S.; Dai, Q. X.; Li, D. S.; Ren, E.; Zhu, J.; Liu, J. M.; Chen, H.; Yin, Z. Y. et al. Tumor microenvironment-triggered MoS2@GA-Fe nanoreactor: A self-rolling enhanced chemodynamic therapy and hydrogen sulfide treatment for hepatocellular carcinoma. Chem. Eng. J. 2021, 406, 126888.

    CAS  Google Scholar 

  111. Liu, J. J.; Li, M. H; Luo, Z.; Dai, L. L.; Guo, X. M.; Cai, K. Y. Design of nanocarriers based on complex biological barriers in vivo for tumor therapy. Nano Today 2017, 15, 56–90.

    Google Scholar 

  112. Sun, P. P.; Jia, L.; Hai, J.; Li, S. Y.; Chen, F. J.; Liang, K.; Sun, S. H.; Liu, H. W.; Fu, X.; Zhu, Y. H. et al. Tumor microenvironment- “AND” near-infrared light-activated coordination polymer nanoprodrug for on-demand CO-sensitized synergistic cancer therapy. Adv. Healthcare Mater. 2021, 10, 2001728.

    CAS  Google Scholar 

  113. Huang, X. H.; Xu, F. N.; Hou, H. B.; Hou, J. W.; Wang, Y.; Zhou, S. B. Stimuli-responsive nitric oxide generator for light-triggered synergistic cancer photothermal/gas therapy. Nano Res. 2019, 12, 1361–1370.

    CAS  Google Scholar 

  114. Xu, Y.; Liu, J. W.; Liu, Z. Y.; Chen, G. G.; Li, X. M.; Ren, H. Damaging tumor vessels with an ultrasound-triggered NO release nanosystem to enhance drug accumulation and T cells infiltration. Int. J. Nanomed. 2021, 16, 2597–2613.

    Google Scholar 

  115. Chen, H.; Shi, T.; Wang, Y.; Liu, Z. Y.; Liu, F. C.; Zhang, H. Y.; Wang, X. W.; Miao, Z. Y.; Liu, B. R.; Wan, M. M. et al. Deep penetration of nanolevel drugs and micrometer-level T cells promoted by nanomotors for cancer immunochemotherapy. J. Am. Chem. Soc. 2021, 143, 12025–12037.

    CAS  Google Scholar 

  116. Deng, Y. Y.; Jia, F.; Chen, X. H.; Jin, Q.; Ji, J. ATP suppression by pH-activated mitochondria-targeted delivery of nitric oxide nanoplatform for drug resistance reversal and metastasis inhibition. Small 2020, 16, 2001747.

    CAS  Google Scholar 

  117. Zhang, J. M.; Song, H. J.; Ji, S. L.; Wang, X. M.; Huang, P. S.; Zhang, C. N.; Wang, W. W.; Kong, D. L. NO prodrug-conjugated, self-assembled, pH-responsive and galactose receptor targeted nanoparticles for co-delivery of nitric oxide and doxorubicin. Nanoscale 2018, 10, 4179–4188.

    CAS  Google Scholar 

  118. Li, J.; Xie, L. S.; Li, B.; Yin, C.; Wang, G. H.; Sang, W.; Li, W. X.; Tian, H.; Zhang, Z.; Zhang, X. J. et al. Engineering a hydrogen-sulfide-based nanomodulator to normalize hyperactive photothermal immunogenicity for combination cancer therapy. Adv. Mater 2021, 33, 2008481.

    CAS  Google Scholar 

  119. Deng, Y. Y.; Wang, Y. P.; Jia, F.; Liu, W. F.; Zhou, D. F.; Jin, Q.; Ji, J. Tailoring supramolecular prodrug nanoassemblies for reactive nitrogen species-potentiated chemotherapy of liver cancer. ACS Nano 2021, 15, 8663–8675.

    CAS  Google Scholar 

  120. Tu, J. Y.; Tu, K.; Xu, H. R.; Wang, L.; Yuan, X. L.; Qin, X. Y.; Kong, L.; Chu, Q.; Zhang, Z. P. Improving tumor hypoxia and radiotherapy resistance via in situ nitric oxide release strategy. Eur. J. Pharm. Biopharm. 2020, 150, 96–107.

    CAS  Google Scholar 

  121. Li, S.; Liao, R. R.; Sheng, X. Y.; Luo, X. J.; Zhang, X.; Wen, X. M.; Zhou, J.; Peng, K. Hydrogen gas in cancer treatment. Front. Oncol. 2019, 9, 696.

    Google Scholar 

  122. Tamura, T.; Hayashida, K.; Sano, M.; Suzuki, M.; Shibusawa, T.; Yoshizawa, J.; Kobayashi, Y.; Suzuki, T.; Ohta, S.; Morisaki, H. et al. Feasibility and safety of hydrogen gas inhalation for post-cardiac arrest syndrome- first-in-human pilot study. Circ. J. 2016, 80, 1870–1873.

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Key R&D Program of China (No. 2021YFB3801001), the National Natural Science Foundation of China (Nos. 32030061 and 81720108023), and the Key Program for Basic Research of Shanghai (Nos. 19JC1415600 and 21JC1406000).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hangrong Chen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Z., Chen, H. Recent deveolpment of multifunctional responsive gas-releasing nanoplatforms for tumor therapeutic application. Nano Res. 16, 3924–3938 (2023). https://doi.org/10.1007/s12274-022-4473-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-022-4473-5

Keywords

Navigation