Near-Infrared Light-Responsive Nitric Oxide Delivery Platform for Enhanced Radioimmunotherapy
Corresponding Author: Chao Wang
Nano-Micro Letters,
Vol. 12 (2020), Article Number: 100
Abstract
Radiotherapy (RT) is a widely used way for cancer treatment. However, the efficiency of RT may come with various challenges such as low specificity, limitation by resistance, high dose and so on. Nitric oxide (NO) is known a very effective radiosensitizer of hypoxic tumor. However, NO cannot circulate in body with high concentration. Herein, an NIR light-responsive NO delivery system is developed for controlled and precisely release of NO to hypoxic tumors during radiotherapy. Tert-Butyl nitrite, which is an efficient NO source, is coupled to Ag2S quantum dots (QDs). NO could be generated and released from the Ag2S QDs effectively under the NIR irradiation due to the thermal effect. In addition, Ag is also a type of heavy metal that can benefit the RT therapy. We demonstrate that Ag2S NO delivery platforms remarkably maximize radiotherapy effects to inhibit tumor growth in CT26 tumor model. Furthermore, immunosuppressive tumor microenvironment is improved by our NO delivery system, significantly enhancing the anti-PD-L1 immune checkpoint blockade therapy. 100% survival rate is achieved by the radio-immune combined therapy strategy based on the Ag2S NO delivery platforms. Our results suggest the promise of Ag2S NO delivery platforms for multifunctional cancer radioimmunotherapy.
Highlights:
1 Ag2S NO delivery platforms maximize radiotherapy effects remarkably to inhibit the tumor growth.
2 Immunosuppressive tumor microenvironment was improved by Ag2S NO delivery system, significantly enhancing the anti-PD-L1 immune checkpoint blockade therapy.
Keywords
Download Citation
Endnote/Zotero/Mendeley (RIS)BibTeX
- R.N. Kjellberg, Radiation therapy. Science 176(4039), 1071–1071 (1972). https://doi.org/10.1126/science.176.4039.1071
- M.J. O'Connor, Targeting the DNA damage response in cancer. Mol. Cell 60(4), 547–560 (2015). https://doi.org/10.1016/j.molcel.2015.10.040
- R. Atun, D.A. Jaffray, M.B. Barton, F. Bray, M. Baumann et al., Expanding global access to radiotherapy. Lancet Oncol. 16(10), 1153–1186 (2015). https://doi.org/10.1016/s1470-2045(15)00222-3
- S. Siva, M.P. MacManus, R.F. Martin, O.A. Martin, Abscopal effects of radiation therapy: a clinical review for the radiobiologist. Cancer Lett. 356(1), 82–90 (2015). https://doi.org/10.1016/j.canlet.2013.09.018
- H.E. Barker, J.T.E. Paget, A.A. Khan, K.J. Harrington, The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat. Rev. Cancer 15(7), 409–425 (2015). https://doi.org/10.1038/nrc3958
- G.S. Song, L. Cheng, Y. Chao, K. Yang, Z. Liu, Emerging nanotechnology and advanced materials for cancer radiation therapy. Adv. Mater. 29(32), 26 (2017). https://doi.org/10.1002/adma.201700996
- P. Retif, S. Pinel, M. Toussaint, C. Frochot, R. Chouikrat, T. Bastogne, M. Barberi-Heyob, Nanoparticles for radiation therapy enhancement: the key parameters. Theranostics 5(9), 1030–1045 (2015). https://doi.org/10.7150/thno.11642
- S. Her, D.A. Jaffray, C. Allen, Gold nanoparticles for applications in cancer radiotherapy: Mechanisms and recent advancements. Adv. Drug Del. Rev. 109, 84–101 (2017). https://doi.org/10.1016/j.addr.2015.12.012
- B. Bonavida, S. Khineche, S. Huerta-Yepez, H. Garbán, Therapeutic potential of nitric oxide in cancer. Drug Resist. Updates 9(3), 157–173 (2006). https://doi.org/10.1016/j.drup.2006.05.003
- H. Yasuda, Solid tumor physiology and hypoxia-induced chemo/radio-resistance: novel strategy for cancer therapy: Nitric oxide donor as a therapeutic enhancer. Nitric Oxide 19(2), 205–216 (2008). https://doi.org/10.1016/j.niox.2008.04.026
- Y.-C. Sung, P.-R. Jin, L.-A. Chu, F.-F. Hsu, M.-R. Wang et al., Delivery of nitric oxide with a nanocarrier promotes tumour vessel normalization and potentiates anti-cancer therapies. Nat. Nanotechnol. 14, 1160–1169 (2019). https://doi.org/10.1038/s41565-019-0570-3
- Q. Song, S. Tan, X. Zhuang, Y. Guo, Y. Zhao, T. Wu, Q. Ye, L. Si, Z. Zhang, Nitric oxide releasing d-α-tocopheryl polyethylene glycol succinate for enhancing antitumor activity of doxorubicin. Mol. Pharm. 11(11), 4118–4129 (2014). https://doi.org/10.1021/mp5003009
- J. Fan, Q. He, Y. Liu, F. Zhang, X. Yang et al., Light-responsive biodegradable nanomedicine overcomes multidrug resistance via NO-enhanced chemosensitization. ACS Appl. Mater. Interfaces 8(22), 13804–13811 (2016). https://doi.org/10.1021/acsami.6b03737
- M. De Ridder, D. Verellen, V. Verovski, G. Storme, Hypoxic tumor cell radiosensitization through nitric oxide. Nitric Oxide 19(2), 164–169 (2008). https://doi.org/10.1016/j.niox.2008.04.015
- F. Frérart, P. Sonveaux, G. Rath, A. Smoos, A. Meqor et al., The acidic tumor microenvironment promotes the reconversion of nitrite into nitric oxide: towards a new and safe radiosensitizing strategy. Clin. Cancer Res. 14(9), 2768–2774 (2008). https://doi.org/10.1158/1078-0432.CCR-07-4001
- W. Fan, W. Bu, Z. Zhang, B. Shen, H. Zhang et al., X-ray radiation-controlled NO-release for on-demand depth-independent hypoxic radiosensitization. Angew. Chem. Int. Ed. 54(47), 14026–14030 (2015). https://doi.org/10.1002/anie.201504536
- P.G. Wang, M. Xian, X. Tang, X. Wu, Z. Wen, T. Cai, A.J. Janczuk, Nitric oxide donors: chemical activities and biological applications. Chem. Rev. 102(4), 1091–1134 (2002). https://doi.org/10.1021/cr000040l
- J. Xu, F. Zeng, H. Wu, C. Hu, C. Yu, S. Wu, Preparation of a mitochondria-targeted and NO-releasing nanoplatform and its enhanced pro-apoptotic effect on cancer cells. Small 10(18), 3750–3760 (2014). https://doi.org/10.1002/smll.201400437
- S.P. Hussain, G.E. Trivers, L.J. Hofseth, P. He, I. Shaikh et al., Nitric oxide, a mediator of inflammation, suppresses tumorigenesis. Cancer Res. 64(19), 6849–6853 (2004). https://doi.org/10.1158/0008-5472.CAN-04-2201
- C. Bogdan, Nitric oxide and the immune response. Nat. Immunol. 2(10), 907–916 (2001). https://doi.org/10.1038/ni1001-907
- C. Fionda, M.P. Abruzzese, A. Santoni, M. Cippitelli, Immunoregulatory and effector activities of nitric oxide and reactive nitrogen species in cancer. Curr. Med. Chem. 23(24), 2618–2636 (2016). https://doi.org/10.2174/0929867323666160727105101
- A.W. Carpenter, M.H. Schoenfisch, Nitric oxide release: Part II. Therapeutic applications. Chem. Soc. Rev. 41(10), 3742–3752 (2012). https://doi.org/10.1039/C2CS15273H
- K. Sato, K. Ozaki, I. Oh, A. Meguro, K. Hatanaka, T. Nagai, K. Muroi, K. Ozawa, Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109(1), 228–234 (2007). https://doi.org/10.1182/blood-2006-02-002246
- Z. Huang, J. Fu, Y. Zhang, Nitric oxide donor-based cancer therapy: advances and prospects. J. Med. Chem. 60(18), 7617–7635 (2017). https://doi.org/10.1021/acs.jmedchem.6b01672
- J.W. Wiley, The many faces of nitric oxide: cytotoxic, cytoprotective or both. Neurogastroenterol. Motil. 19(7), 541–544 (2007). https://doi.org/10.1111/j.1365-2982.2007.00958.x
- J.F. Quinn, M.R. Whittaker, T.P. Davis, Delivering nitric oxide with nanoparticles. J. Control. Release 205, 190–205 (2015). https://doi.org/10.1016/j.jconrel.2015.02.007
- X. Jia, Y. Zhang, Y. Zou, Y. Wang, D. Niu et al., Dual intratumoral redox/enzyme-responsive NO-releasing nanomedicine for the specific, high-efficacy, and low-toxic cancer therapy. Adv. Mater. 30(30), 1704490 (2018). https://doi.org/10.1002/adma.201704490
- R. Yahyapour, E. Motevaseli, A. Rezaeyan, H. Abdollahi, B. Farhood et al., Reduction–oxidation (redox) system in radiation-induced normal tissue injury: molecular mechanisms and implications in radiation therapeutics. Clin. Transl. Oncol. 20(8), 975–988 (2018). https://doi.org/10.1007/s12094-017-1828-6
- L. Tian, Y. Wang, L. Sun, J. Xu, Y. Chao, K. Yang, S. Wang, Z. Liu, Cerenkov luminescence-induced NO release from 32P-Labeled ZnFe(CN)5NO nanosheets to enhance radioisotope-immunotherapy. Matter 1(4), 1061–1076 (2019). https://doi.org/10.1016/j.matt.2019.07.007
- Y. Deng, F. Jia, S. Chen, Z. Shen, Q. Jin, G. Fu, J. Ji, Nitric oxide as an all-rounder for enhanced photodynamic therapy: hypoxia relief, glutathione depletion and reactive nitrogen species generation. Biomaterials 187, 55–65 (2018). https://doi.org/10.1016/j.biomaterials.2018.09.043
- M. Feelisch, The use of nitric oxide donors in pharmacological studies. Naunyn-Schmiedeberg's Arch. Pharmacol 358(1), 113–122 (1998). https://doi.org/10.1007/pl00005231
- A. Fraix, S. Sortino, Photoactivable platforms for nitric oxide delivery with fluorescence imaging. Chem. Asian J. 10(5), 1116–1125 (2015). https://doi.org/10.1002/asia.201403398
- B. Bonavida, S. Baritaki, S. Huerta-Yepez, M.I. Vega, D. Chatterjee, K. Yeung, Novel therapeutic applications of nitric oxide donors in cancer: roles in chemo- and immunosensitization to apoptosis and inhibition of metastases. Nitric Oxide 19(2), 152–157 (2008). https://doi.org/10.1016/j.niox.2008.04.018
- J. Fan, N. He, Q. He, Y. Liu, Y. Ma et al., A novel self-assembled sandwich nanomedicine for NIR-responsive release of NO. Nanoscale 7(47), 20055–20062 (2015). https://doi.org/10.1039/c5nr06630a
- C. Oliveira, S. Benfeito, C. Fernandes, F. Cagide, T. Silva, F. Borges, NO and HNO donors, nitrones, and nitroxides: past, present, and future. Med. Res. Rev. 38(4), 1159–1187 (2018). https://doi.org/10.1002/med.21461
- H.W. Choi, J. Kim, J. Kim, Y. Kim, H.B. Song, J.H. Kim, K. Kim, W.J. Kim, Light-induced acid generation on a gatekeeper for smart nitric oxide delivery. ACS Nano 10(4), 4199–4208 (2016). https://doi.org/10.1021/acsnano.5b07483
- L. Tan, R. Huang, X. Li, S. Liu, Y.M. Shen, Controllable release of nitric oxide and doxorubicin from engineered nanospheres for synergistic tumor therapy. Acta Biomater. 57, 498–510 (2017). https://doi.org/10.1016/j.actbio.2017.05.019
- J. Kim, B.C. Yung, W.J. Kim, X. Chen, Combination of nitric oxide and drug delivery systems: tools for overcoming drug resistance in chemotherapy. J. Control. Release 263, 223–230 (2017). https://doi.org/10.1016/j.jconrel.2016.12.026
- L. Chen, Q. He, M. Lei, L. Xiong, K. Shi, L. Tan, Z. Jin, T. Wang, Z. Qian, Facile coordination-precipitation route to insoluble metal roussin’s black salts for NIR-responsive release of NO for anti-metastasis. ACS Appl. Mater. Interfaces 9(42), 36473–36477 (2017). https://doi.org/10.1021/acsami.7b11325
- W. Fan, N. Lu, P. Huang, Y. Liu, Z. Yang et al., Glucose-responsive sequential generation of hydrogen peroxide and nitric oxide for synergistic cancer starving-like/gas therapy. Angew. Chem. Int. Ed. 56(5), 1229–1233 (2017). https://doi.org/10.1002/anie.201610682
- K. Zhang, H. Xu, X. Jia, Y. Chen, M. Ma, L. Sun, H. Chen, Ultrasound-triggered nitric oxide release platform based on energy transformation for targeted inhibition of pancreatic tumor. ACS Nano 10(12), 10816–10828 (2016). https://doi.org/10.1021/acsnano.6b04921
- Z. Jin, Y. Wen, Y. Hu, W. Chen, X. Zheng et al., MRI-guided and ultrasound-triggered release of NO by advanced nanomedicine. Nanoscale 9(10), 3637–3645 (2017). https://doi.org/10.1039/c7nr00231a
- T. Yang, Y. Tang, L. Liu, X. Lv, Q. Wang et al., Size-dependent Ag2S nanodots for second near-infrared fluorescence/photoacoustics imaging and simultaneous photothermal therapy. ACS Nano 11(2), 1848–1857 (2017). https://doi.org/10.1021/acsnano.6b07866
- R. Guo, Y. Tian, Y. Wang, W. Yang, Near-infrared laser-triggered nitric oxide nanogenerators for the reversal of multidrug resistance in cancer. Adv. Funct. Mater. 27(13), 1606398 (2017). https://doi.org/10.1002/adfm.201606398
- L. Tan, A. Wan, X. Zhu, H. Li, Visible light-triggered nitric oxide release from near-infrared fluorescent nanospheric vehicles. Analyst 139(13), 3398–3406 (2014). https://doi.org/10.1039/c4an00275j
- H.-J. Xiang, M. Guo, L. An, S.-P. Yang, Q.-L. Zhang, J.-G. Liu, A multifunctional nanoplatform for lysosome targeted delivery of nitric oxide and photothermal therapy under 808 nm near-infrared light. J. Mater. Chem. B 4(27), 4667–4674 (2016). https://doi.org/10.1039/c6tb00730a
- X. Zhang, G. Tian, W. Yin, L. Wang, X. Zheng et al., Controllable generation of nitric oxide by near-infrared-sensitized upconversion nanoparticles for tumor therapy. Adv. Funct. Mat. 25(20), 3049–3056 (2015). https://doi.org/10.1002/adfm.201404402
- X. Hao, C. Li, Y. Zhang, H. Wang, G. Chen, M. Wang, Q. Wang, Programmable chemotherapy and immunotherapy against breast cancer guided by multiplexed fluorescence imaging in the second near-infrared window. Adv. Mater. 30(51), 1804437 (2018). https://doi.org/10.1002/adma.201804437
- J. Gao, C. Wu, D. Deng, P. Wu, C. Cai, Direct synthesis of water-soluble aptamer-Ag2S quantum dots at ambient temperature for specific imaging and photothermal therapy of cancer. Adv. Healthc. Mater. 5(18), 2437–2449 (2016). https://doi.org/10.1002/adhm.201600545
- G.M. Neelgund, M.C. Okolie, F.K. Williams, A.J.M.C. Oki, Physics, Ag2S nanocrystallites deposited over polyamidoamine grafted carbon nanotubes: an efficient NIR active photothermal agent. Mater. Chem. Phys. 234, 32–37 (2019). https://doi.org/10.1016/j.matchemphys.2019.05.040
- D.-H. Zhao, J. Yang, R.-X. Xia, M.-H. Yao, R.-M. Jin, Y.-D. Zhao, B.J.C.C. Liu, High quantum yield Ag2S quantum dot@ polypeptide-engineered hybrid nanogels for targeted second near-infrared fluorescence/photoacoustic imaging and photothermal therapy. Chem. Commun. 54(5), 527–530 (2018). https://doi.org/10.1016/j.matchemphys.2019.05.040
- Y. Du, B. Xu, T. Fu, M. Cai, F. Li, Y. Zhang, Q. Wang, Near-infrared photoluminescent Ag2S quantum dots from a single source precursor. J. Am. Chem. Soc. 132(5), 1470–1471 (2010). https://doi.org/10.1021/ja909490r
- Y. Shen, J. Lifante, E. Ximendes, H.D. Santos, D. Ruiz et al., Perspectives for Ag2S NIR-II nanoparticles in biomedicine: from imaging to multifunctionality. Nanoscale 11(41), 19251–19264 (2019). https://doi.org/10.1039/C9NR05733A
- Y. Zhang, Y. Zhang, G. Hong, W. He, K. Zhou et al., Biodistribution, pharmacokinetics and toxicology of Ag2S near-infrared quantum dots in mice. Biomaterials 34(14), 3639–3646 (2013). https://doi.org/10.1016/j.biomaterials.2013.01.089
- G. Hong, J.T. Robinson, Y. Zhang, S. Diao, A.L. Antaris, Q. Wang, H. Dai, In vivo fluorescence imaging with Ag2S quantum dots in the second near-infrared region. Angew. Chem. Int. Ed. 51(39), 9818–9821 (2012). https://doi.org/10.1002/anie.201206059
- J. Javidi, A. Haeri, F. Nowroozi, S. Dadashzadeh, Pharmacokinetics, Tissue distribution and excretion of Ag2S quantum dots in mice and rats: the effects of injection dose, particle size and surface charge. Pharm. Res. 36(3), 46 (2019). https://doi.org/10.1007/s11095-019-2571-1
- L. Huang, Y. Li, Y. Du, Y. Zhang, X. Wang et al., Mild photothermal therapy potentiates anti-PD-L1 treatment for immunologically cold tumors via an all-in-one and all-in-control strategy. Nat. Commun. 10(1), 1–15 (2019). https://doi.org/10.1038/s41467-019-12771-9
- K. Ni, G. Lan, C. Chan, B. Quigley, K. Lu et al., Nanoscale metal-organic frameworks enhance radiotherapy to potentiate checkpoint blockade immunotherapy. Nat. Commun. 9(1), 2351 (2018). https://doi.org/10.1038/s41467-018-04703-w
References
R.N. Kjellberg, Radiation therapy. Science 176(4039), 1071–1071 (1972). https://doi.org/10.1126/science.176.4039.1071
M.J. O'Connor, Targeting the DNA damage response in cancer. Mol. Cell 60(4), 547–560 (2015). https://doi.org/10.1016/j.molcel.2015.10.040
R. Atun, D.A. Jaffray, M.B. Barton, F. Bray, M. Baumann et al., Expanding global access to radiotherapy. Lancet Oncol. 16(10), 1153–1186 (2015). https://doi.org/10.1016/s1470-2045(15)00222-3
S. Siva, M.P. MacManus, R.F. Martin, O.A. Martin, Abscopal effects of radiation therapy: a clinical review for the radiobiologist. Cancer Lett. 356(1), 82–90 (2015). https://doi.org/10.1016/j.canlet.2013.09.018
H.E. Barker, J.T.E. Paget, A.A. Khan, K.J. Harrington, The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat. Rev. Cancer 15(7), 409–425 (2015). https://doi.org/10.1038/nrc3958
G.S. Song, L. Cheng, Y. Chao, K. Yang, Z. Liu, Emerging nanotechnology and advanced materials for cancer radiation therapy. Adv. Mater. 29(32), 26 (2017). https://doi.org/10.1002/adma.201700996
P. Retif, S. Pinel, M. Toussaint, C. Frochot, R. Chouikrat, T. Bastogne, M. Barberi-Heyob, Nanoparticles for radiation therapy enhancement: the key parameters. Theranostics 5(9), 1030–1045 (2015). https://doi.org/10.7150/thno.11642
S. Her, D.A. Jaffray, C. Allen, Gold nanoparticles for applications in cancer radiotherapy: Mechanisms and recent advancements. Adv. Drug Del. Rev. 109, 84–101 (2017). https://doi.org/10.1016/j.addr.2015.12.012
B. Bonavida, S. Khineche, S. Huerta-Yepez, H. Garbán, Therapeutic potential of nitric oxide in cancer. Drug Resist. Updates 9(3), 157–173 (2006). https://doi.org/10.1016/j.drup.2006.05.003
H. Yasuda, Solid tumor physiology and hypoxia-induced chemo/radio-resistance: novel strategy for cancer therapy: Nitric oxide donor as a therapeutic enhancer. Nitric Oxide 19(2), 205–216 (2008). https://doi.org/10.1016/j.niox.2008.04.026
Y.-C. Sung, P.-R. Jin, L.-A. Chu, F.-F. Hsu, M.-R. Wang et al., Delivery of nitric oxide with a nanocarrier promotes tumour vessel normalization and potentiates anti-cancer therapies. Nat. Nanotechnol. 14, 1160–1169 (2019). https://doi.org/10.1038/s41565-019-0570-3
Q. Song, S. Tan, X. Zhuang, Y. Guo, Y. Zhao, T. Wu, Q. Ye, L. Si, Z. Zhang, Nitric oxide releasing d-α-tocopheryl polyethylene glycol succinate for enhancing antitumor activity of doxorubicin. Mol. Pharm. 11(11), 4118–4129 (2014). https://doi.org/10.1021/mp5003009
J. Fan, Q. He, Y. Liu, F. Zhang, X. Yang et al., Light-responsive biodegradable nanomedicine overcomes multidrug resistance via NO-enhanced chemosensitization. ACS Appl. Mater. Interfaces 8(22), 13804–13811 (2016). https://doi.org/10.1021/acsami.6b03737
M. De Ridder, D. Verellen, V. Verovski, G. Storme, Hypoxic tumor cell radiosensitization through nitric oxide. Nitric Oxide 19(2), 164–169 (2008). https://doi.org/10.1016/j.niox.2008.04.015
F. Frérart, P. Sonveaux, G. Rath, A. Smoos, A. Meqor et al., The acidic tumor microenvironment promotes the reconversion of nitrite into nitric oxide: towards a new and safe radiosensitizing strategy. Clin. Cancer Res. 14(9), 2768–2774 (2008). https://doi.org/10.1158/1078-0432.CCR-07-4001
W. Fan, W. Bu, Z. Zhang, B. Shen, H. Zhang et al., X-ray radiation-controlled NO-release for on-demand depth-independent hypoxic radiosensitization. Angew. Chem. Int. Ed. 54(47), 14026–14030 (2015). https://doi.org/10.1002/anie.201504536
P.G. Wang, M. Xian, X. Tang, X. Wu, Z. Wen, T. Cai, A.J. Janczuk, Nitric oxide donors: chemical activities and biological applications. Chem. Rev. 102(4), 1091–1134 (2002). https://doi.org/10.1021/cr000040l
J. Xu, F. Zeng, H. Wu, C. Hu, C. Yu, S. Wu, Preparation of a mitochondria-targeted and NO-releasing nanoplatform and its enhanced pro-apoptotic effect on cancer cells. Small 10(18), 3750–3760 (2014). https://doi.org/10.1002/smll.201400437
S.P. Hussain, G.E. Trivers, L.J. Hofseth, P. He, I. Shaikh et al., Nitric oxide, a mediator of inflammation, suppresses tumorigenesis. Cancer Res. 64(19), 6849–6853 (2004). https://doi.org/10.1158/0008-5472.CAN-04-2201
C. Bogdan, Nitric oxide and the immune response. Nat. Immunol. 2(10), 907–916 (2001). https://doi.org/10.1038/ni1001-907
C. Fionda, M.P. Abruzzese, A. Santoni, M. Cippitelli, Immunoregulatory and effector activities of nitric oxide and reactive nitrogen species in cancer. Curr. Med. Chem. 23(24), 2618–2636 (2016). https://doi.org/10.2174/0929867323666160727105101
A.W. Carpenter, M.H. Schoenfisch, Nitric oxide release: Part II. Therapeutic applications. Chem. Soc. Rev. 41(10), 3742–3752 (2012). https://doi.org/10.1039/C2CS15273H
K. Sato, K. Ozaki, I. Oh, A. Meguro, K. Hatanaka, T. Nagai, K. Muroi, K. Ozawa, Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109(1), 228–234 (2007). https://doi.org/10.1182/blood-2006-02-002246
Z. Huang, J. Fu, Y. Zhang, Nitric oxide donor-based cancer therapy: advances and prospects. J. Med. Chem. 60(18), 7617–7635 (2017). https://doi.org/10.1021/acs.jmedchem.6b01672
J.W. Wiley, The many faces of nitric oxide: cytotoxic, cytoprotective or both. Neurogastroenterol. Motil. 19(7), 541–544 (2007). https://doi.org/10.1111/j.1365-2982.2007.00958.x
J.F. Quinn, M.R. Whittaker, T.P. Davis, Delivering nitric oxide with nanoparticles. J. Control. Release 205, 190–205 (2015). https://doi.org/10.1016/j.jconrel.2015.02.007
X. Jia, Y. Zhang, Y. Zou, Y. Wang, D. Niu et al., Dual intratumoral redox/enzyme-responsive NO-releasing nanomedicine for the specific, high-efficacy, and low-toxic cancer therapy. Adv. Mater. 30(30), 1704490 (2018). https://doi.org/10.1002/adma.201704490
R. Yahyapour, E. Motevaseli, A. Rezaeyan, H. Abdollahi, B. Farhood et al., Reduction–oxidation (redox) system in radiation-induced normal tissue injury: molecular mechanisms and implications in radiation therapeutics. Clin. Transl. Oncol. 20(8), 975–988 (2018). https://doi.org/10.1007/s12094-017-1828-6
L. Tian, Y. Wang, L. Sun, J. Xu, Y. Chao, K. Yang, S. Wang, Z. Liu, Cerenkov luminescence-induced NO release from 32P-Labeled ZnFe(CN)5NO nanosheets to enhance radioisotope-immunotherapy. Matter 1(4), 1061–1076 (2019). https://doi.org/10.1016/j.matt.2019.07.007
Y. Deng, F. Jia, S. Chen, Z. Shen, Q. Jin, G. Fu, J. Ji, Nitric oxide as an all-rounder for enhanced photodynamic therapy: hypoxia relief, glutathione depletion and reactive nitrogen species generation. Biomaterials 187, 55–65 (2018). https://doi.org/10.1016/j.biomaterials.2018.09.043
M. Feelisch, The use of nitric oxide donors in pharmacological studies. Naunyn-Schmiedeberg's Arch. Pharmacol 358(1), 113–122 (1998). https://doi.org/10.1007/pl00005231
A. Fraix, S. Sortino, Photoactivable platforms for nitric oxide delivery with fluorescence imaging. Chem. Asian J. 10(5), 1116–1125 (2015). https://doi.org/10.1002/asia.201403398
B. Bonavida, S. Baritaki, S. Huerta-Yepez, M.I. Vega, D. Chatterjee, K. Yeung, Novel therapeutic applications of nitric oxide donors in cancer: roles in chemo- and immunosensitization to apoptosis and inhibition of metastases. Nitric Oxide 19(2), 152–157 (2008). https://doi.org/10.1016/j.niox.2008.04.018
J. Fan, N. He, Q. He, Y. Liu, Y. Ma et al., A novel self-assembled sandwich nanomedicine for NIR-responsive release of NO. Nanoscale 7(47), 20055–20062 (2015). https://doi.org/10.1039/c5nr06630a
C. Oliveira, S. Benfeito, C. Fernandes, F. Cagide, T. Silva, F. Borges, NO and HNO donors, nitrones, and nitroxides: past, present, and future. Med. Res. Rev. 38(4), 1159–1187 (2018). https://doi.org/10.1002/med.21461
H.W. Choi, J. Kim, J. Kim, Y. Kim, H.B. Song, J.H. Kim, K. Kim, W.J. Kim, Light-induced acid generation on a gatekeeper for smart nitric oxide delivery. ACS Nano 10(4), 4199–4208 (2016). https://doi.org/10.1021/acsnano.5b07483
L. Tan, R. Huang, X. Li, S. Liu, Y.M. Shen, Controllable release of nitric oxide and doxorubicin from engineered nanospheres for synergistic tumor therapy. Acta Biomater. 57, 498–510 (2017). https://doi.org/10.1016/j.actbio.2017.05.019
J. Kim, B.C. Yung, W.J. Kim, X. Chen, Combination of nitric oxide and drug delivery systems: tools for overcoming drug resistance in chemotherapy. J. Control. Release 263, 223–230 (2017). https://doi.org/10.1016/j.jconrel.2016.12.026
L. Chen, Q. He, M. Lei, L. Xiong, K. Shi, L. Tan, Z. Jin, T. Wang, Z. Qian, Facile coordination-precipitation route to insoluble metal roussin’s black salts for NIR-responsive release of NO for anti-metastasis. ACS Appl. Mater. Interfaces 9(42), 36473–36477 (2017). https://doi.org/10.1021/acsami.7b11325
W. Fan, N. Lu, P. Huang, Y. Liu, Z. Yang et al., Glucose-responsive sequential generation of hydrogen peroxide and nitric oxide for synergistic cancer starving-like/gas therapy. Angew. Chem. Int. Ed. 56(5), 1229–1233 (2017). https://doi.org/10.1002/anie.201610682
K. Zhang, H. Xu, X. Jia, Y. Chen, M. Ma, L. Sun, H. Chen, Ultrasound-triggered nitric oxide release platform based on energy transformation for targeted inhibition of pancreatic tumor. ACS Nano 10(12), 10816–10828 (2016). https://doi.org/10.1021/acsnano.6b04921
Z. Jin, Y. Wen, Y. Hu, W. Chen, X. Zheng et al., MRI-guided and ultrasound-triggered release of NO by advanced nanomedicine. Nanoscale 9(10), 3637–3645 (2017). https://doi.org/10.1039/c7nr00231a
T. Yang, Y. Tang, L. Liu, X. Lv, Q. Wang et al., Size-dependent Ag2S nanodots for second near-infrared fluorescence/photoacoustics imaging and simultaneous photothermal therapy. ACS Nano 11(2), 1848–1857 (2017). https://doi.org/10.1021/acsnano.6b07866
R. Guo, Y. Tian, Y. Wang, W. Yang, Near-infrared laser-triggered nitric oxide nanogenerators for the reversal of multidrug resistance in cancer. Adv. Funct. Mater. 27(13), 1606398 (2017). https://doi.org/10.1002/adfm.201606398
L. Tan, A. Wan, X. Zhu, H. Li, Visible light-triggered nitric oxide release from near-infrared fluorescent nanospheric vehicles. Analyst 139(13), 3398–3406 (2014). https://doi.org/10.1039/c4an00275j
H.-J. Xiang, M. Guo, L. An, S.-P. Yang, Q.-L. Zhang, J.-G. Liu, A multifunctional nanoplatform for lysosome targeted delivery of nitric oxide and photothermal therapy under 808 nm near-infrared light. J. Mater. Chem. B 4(27), 4667–4674 (2016). https://doi.org/10.1039/c6tb00730a
X. Zhang, G. Tian, W. Yin, L. Wang, X. Zheng et al., Controllable generation of nitric oxide by near-infrared-sensitized upconversion nanoparticles for tumor therapy. Adv. Funct. Mat. 25(20), 3049–3056 (2015). https://doi.org/10.1002/adfm.201404402
X. Hao, C. Li, Y. Zhang, H. Wang, G. Chen, M. Wang, Q. Wang, Programmable chemotherapy and immunotherapy against breast cancer guided by multiplexed fluorescence imaging in the second near-infrared window. Adv. Mater. 30(51), 1804437 (2018). https://doi.org/10.1002/adma.201804437
J. Gao, C. Wu, D. Deng, P. Wu, C. Cai, Direct synthesis of water-soluble aptamer-Ag2S quantum dots at ambient temperature for specific imaging and photothermal therapy of cancer. Adv. Healthc. Mater. 5(18), 2437–2449 (2016). https://doi.org/10.1002/adhm.201600545
G.M. Neelgund, M.C. Okolie, F.K. Williams, A.J.M.C. Oki, Physics, Ag2S nanocrystallites deposited over polyamidoamine grafted carbon nanotubes: an efficient NIR active photothermal agent. Mater. Chem. Phys. 234, 32–37 (2019). https://doi.org/10.1016/j.matchemphys.2019.05.040
D.-H. Zhao, J. Yang, R.-X. Xia, M.-H. Yao, R.-M. Jin, Y.-D. Zhao, B.J.C.C. Liu, High quantum yield Ag2S quantum dot@ polypeptide-engineered hybrid nanogels for targeted second near-infrared fluorescence/photoacoustic imaging and photothermal therapy. Chem. Commun. 54(5), 527–530 (2018). https://doi.org/10.1016/j.matchemphys.2019.05.040
Y. Du, B. Xu, T. Fu, M. Cai, F. Li, Y. Zhang, Q. Wang, Near-infrared photoluminescent Ag2S quantum dots from a single source precursor. J. Am. Chem. Soc. 132(5), 1470–1471 (2010). https://doi.org/10.1021/ja909490r
Y. Shen, J. Lifante, E. Ximendes, H.D. Santos, D. Ruiz et al., Perspectives for Ag2S NIR-II nanoparticles in biomedicine: from imaging to multifunctionality. Nanoscale 11(41), 19251–19264 (2019). https://doi.org/10.1039/C9NR05733A
Y. Zhang, Y. Zhang, G. Hong, W. He, K. Zhou et al., Biodistribution, pharmacokinetics and toxicology of Ag2S near-infrared quantum dots in mice. Biomaterials 34(14), 3639–3646 (2013). https://doi.org/10.1016/j.biomaterials.2013.01.089
G. Hong, J.T. Robinson, Y. Zhang, S. Diao, A.L. Antaris, Q. Wang, H. Dai, In vivo fluorescence imaging with Ag2S quantum dots in the second near-infrared region. Angew. Chem. Int. Ed. 51(39), 9818–9821 (2012). https://doi.org/10.1002/anie.201206059
J. Javidi, A. Haeri, F. Nowroozi, S. Dadashzadeh, Pharmacokinetics, Tissue distribution and excretion of Ag2S quantum dots in mice and rats: the effects of injection dose, particle size and surface charge. Pharm. Res. 36(3), 46 (2019). https://doi.org/10.1007/s11095-019-2571-1
L. Huang, Y. Li, Y. Du, Y. Zhang, X. Wang et al., Mild photothermal therapy potentiates anti-PD-L1 treatment for immunologically cold tumors via an all-in-one and all-in-control strategy. Nat. Commun. 10(1), 1–15 (2019). https://doi.org/10.1038/s41467-019-12771-9
K. Ni, G. Lan, C. Chan, B. Quigley, K. Lu et al., Nanoscale metal-organic frameworks enhance radiotherapy to potentiate checkpoint blockade immunotherapy. Nat. Commun. 9(1), 2351 (2018). https://doi.org/10.1038/s41467-018-04703-w