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Research Article

ATP-responsive hollow nanocapsules for DOX/GOx delivery to enable tumor inhibition with suppressed P-glycoprotein

Huimin Zhu1,§, Guodong Cao2,§, Yike Fu1,3,§, Chao Fang1, Qiang Chu1, Xiang Li1,3( ), Yulian Wu2( ), Gaorong Han
State Key Laboratory of Silicon Materials, School of Materials Science and Engineering, Zhejiang University, Hangzhou 310027, China
Department of Surgery, Second Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang University, Hangzhou 310000, China
ZJU-Hangzhou Global Scientific and Technological Innovation Center, Zhejiang University, Hangzhou 311200, China

§ Huimin Zhu, Guodong Cao, and Yike Fu contributed equally to this work.

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Graphical Abstract

Abstract

Multidrug resistance (MDR) restricts chemotherapy efficacy due to P-glycoprotein (P-gp) mediated drug efflux, whereas current approaches to suppressing P-gp expression suffer from intrinsic challenges, such as low transfection, high toxicity and poor specificity. Here, hollow ferric-tannic acid complex nanocapsules (HFe-TA), which can be effectively degraded by the reaction with adenosine triphosphate (ATP), are synthesized for the delivery of glucose oxidase (GOx) and doxorubicin (DOX) for tumor treatment. The findings indicate that the intracellular ATP is significantly decreased due to the combined effect of HFe-TA degradation and GOx-mediated glucose consumption. Along with this ATP down-regulation, P-gp expression of tumor cells is suppressed remarkably, which in turn promotes the intracellular accumulation and anticancer efficacy of DOX. In addition, the production of •OH by Fe ions released from HFe-TA is promoted by the by-products of the oxidation of glucose process by GOx. In consequence, HFe-TA nanocapsules loaded with DOX and GOx enable significant inhibition effect to tumors both in vitro and in vivo due to the synergistic effect of cascade reactions. This study has therefore provided an alternative therapeutic platform for effective tumor inhibition with the potential in overcoming intrinsic MDR.

Keywords

adenosine triphosphate (ATP)-responsiveP-glycoprotein (P-gp) suppressionnanocapsulesmulti-model tumor therapy

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References

[1]
R. K. Jain,; T. Stylianopoulos, Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 2010, 7, 653-664.
Google Scholar
[2]
M. Overchuk,; G. Zheng, Overcoming obstacles in the tumor microenvironment: Recent advancements in nanoparticle delivery for cancer theranostics. Biomaterials 2018, 156, 217-237.
Google Scholar
[3]
Y. H. Zheng,; X. R. You,; L. Chen,; J. Huang,; L. Y. Wang,; J. Wu,; S. Y. Guan, Biotherapeutic nanoparticles of poly(ferulic acid) delivering doxorubicin for cancer therapy. J. Biomed. Nanotechnol. 2019, 15, 1734-1743.
Google Scholar
[4]
X. Q. Zhang,; L. H. Li,; Q. Liu,; Y. W. Wang,; J. G. Yang,; T. Qiu,; G. Zhou, Co-delivery of rose bengal and doxorubicin nanoparticles for combination photodynamic and chemo-therapy. J. Biomed. Nanotechnol. 2019, 15, 184-195.
Google Scholar
[5]
H. M. Zhu,; G. D. Cao,; C. Qiang,; Y. K. Fu,; Y. L. Wu,; X. Li,; G. R. Han, Hollow ferric-tannic acid nanocapsules with sustained O2 and ROS induction for synergistic tumor therapy. Biomater. Sci. 2020, 8, 3844-3855.
Google Scholar
[6]
W. Song,; M. Das,; Y. Xu,; X. Si,; Y. Zhang,; Z. Tang,; X. Chen, Leveraging biomaterials for cancer immunotherapy: Targeting pattern recognition receptors. Mater. Today Nano 2019, 5, 100029.
Google Scholar
[7]
W. T. Xue,; Z. H. Di,; Y. Zhao,; A. P. Zhang,; L. L. Li, DNA-mediated coordinative assembly of upconversion hetero-nanostructures for targeted dual-modality imaging of cancer cells. Chin. Chem. Lett. 2019, 30, 899-902.
Google Scholar
[8]
J. H. Zhao,; J. W. Chen,; S. N. Ma,; Q. Q. Liu,; L. X. Huang,; X. N. Chen,; K. Y. Lou,; W. Wang, Recent developments in multimodality fluorescence imaging probes. Acta Pharm. Sin. B 2018, 8, 320-338.
Google Scholar
[9]
E. Blanco,; H. F. Shen,; M. Ferrari, Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat. Biotechnol. 2015, 33, 941-951.
Google Scholar
[10]
R. W. Robey,; K. M. Pluchino,; M. D. Hall,; A. T. Fojo,; S. E. Bates,; M. M. Gottesman, Revisiting the role of ABC transporters in multidrug-resistant cancer. Nat. Rev. Cancer 2018, 18, 452-464.
Google Scholar
[11]
G. Szakács,; J. K. Paterson,; J. A. Ludwig,; C. Booth-Genthe,; M. M. Gottesman, Targeting multidrug resistance in cancer. Nat Rev. Drug Discov. 2006, 5, 219-234.
Google Scholar
[12]
C. J. Chen,; J. E. Chin,; K. Ueda,; D. P. Clark,; I. Pastan,; M. M. Gottesman,; I. B. Roninson, Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 1986, 47, 381-389.
Google Scholar
[13]
A. R. Kirtane,; S. M. Kalscheuer,; J. Panyam, Exploiting nanotechnology to overcome tumor drug resistance: Challenges and opportunities. Adv. Drug Deliv. Rev. 2013, 65, 1731-1747.
Google Scholar
[14]
H. Yang,; X. Shen,; J. Yan,; X. X. Xie,; Z. Y. Chen,; T. T. Li,; S. Li,; X. Qin,; C. H. Wu,; Y. Y. Liu, Charge-reversal-functionalized PLGA nanobubbles as theranostic agents for ultrasonic-imaging-guided combination therapy. Biomater. Sci. 2018, 6, 2426-2439.
Google Scholar
[15]
C. L. Wang,; W. C. Guan,; J. L. Peng,; Y. T. Chen,; G. X. Xu,; H. J. Dou, Gene/paclitaxel co-delivering nanocarriers prepared by framework-induced self-assembly for the inhibition of highly drug-resistant tumors. Acta Biomater. 2020, 103, 247-258.
Google Scholar
[16]
Y. C. Zhou,; F. T. Huang,; Y. Yang,; P. L. Wang,; Z. Zhang,; Y. N. Tang,; Y. Q. Shen,; K. Wang, Paraptosis-inducing nanomedicine overcomes cancer drug resistance for a potent cancer therapy. Small 2018, 14, 1702446.
Google Scholar
[17]
T. T. Wang,; D. G. Wang,; J. P. Liu,; B. Feng,; F. Y. Zhou,; H. W. Zhang,; L. Zhou,; Q. Yin,; Z. W. Zhang,; Z. L. Cao, et al. Acidity-triggered ligand-presenting nanoparticles to overcome sequential drug delivery barriers to tumors. Nano Lett. 2017, 17, 5429-5436.
Google Scholar
[18]
C. Yao,; P. Y. Wang,; X. M. Li,; X. Y. Hu,; J. L. Hou,; L. Y. Wang,; F. Zhang, 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.
Google Scholar
[19]
A. Sosnik, Reversal of multidrug resistance by the inhibition of ATP-binding cassette pumps employing “generally recognized as safe” (GRAS) nanopharmaceuticals: A review. Adv. Drug Del. Rev. 2013, 65, 1828-1851.
Google Scholar
[20]
M. G. V. Heiden,; L. C. Cantley,; C. B. Thompson, Understanding the warburg effect: The metabolic requirements of cell proliferation. Science 2009, 324, 1029-1033.
Google Scholar
[21]
H. B. Wang,; Y. Li,; M. Z. Zhang,; D. Wu,; Y. Q. Shen,; G. P. Tang,; Y. Ping, Redox-activatable ATP-depleting micelles with dual modulation characteristics for multidrug-resistant cancer therapy. Adv. Healthc. Mater. 2017, 6, 1601293.
Google Scholar
[22]
H. Wang,; Z. Gao,; X. Y. Liu,; P. Agarwal,; S. T. Zhao,; D. W. Conroy,; G. Ji,; J. H. Yu,; C. P. Jaroniec,; Z. G. Liu, et al. Targeted production of reactive oxygen species in mitochondria to overcome cancer drug resistance. Nat. Commun. 2018, 9, 562.
Google Scholar
[23]
M. Leist,; B. Single,; A. F. Castoldi,; S. Kühnle,; P. Nicotera, Intracellular adenosine triphosphate (ATP) concentration: A switch in the decision between apoptosis and necrosis. J. Exp. Med. 1997, 185, 1481-1486.
Google Scholar
[24]
R. Mo,; T. Y. Jiang,; R. DiSanto,; W. Y. Tai,; Z. Gu, ATP-triggered anticancer drug delivery. Nat. Commun. 2014, 5, 3364.
Google Scholar
[25]
Y. Lu,; A. A. Aimetti,; R. Langer,; Z. Gu, Bioresponsive materials. Nat. Rev. Mater. 2017, 2, 16075.
Google Scholar
[26]
R. Mo,; T. Y. Jiang,; Z. Gu, Enhanced anticancer efficacy by ATP-mediated liposomal drug delivery. Angew. Chem., Int. Ed. 2014, 126, 5925-5930.
Google Scholar
[27]
L. Zhang,; S. S. Wan,; C. X. Li,; L. Xu,; H. Cheng,; X. Z. Zhang, An adenosine triphosphate-responsive autocatalytic fenton nanoparticle for tumor ablation with self-supplied H2O2 and acceleration of Fe(III)/Fe(II) conversion. Nano Lett. 2018, 18, 7609-7618.
Google Scholar
[28]
X. R. Song,; S. H. Li,; J. Y. Dai,; L. Song,; G. M. Huang,; R. H. Lin,; J. Li,; G. Liu,; H. H. Yang, Polyphenol-inspired facile construction of smart assemblies for ATP- and pH-responsive tumor MR/optical imaging and photothermal therapy. Small 2017, 13, 1603997.
Google Scholar
[29]
C. F. Xu,; Y. Liu,; S. Shen,; Y. H. Zhu,; J. Wang, Targeting glucose uptake with siRNA-based nanomedicine for cancer therapy. Biomaterials 2015, 51, 1-11.
Google Scholar
[30]
Y. Liu,; Y. Y. Cao,; W. H. Zhang,; S. Bergmeier,; Y. R. Qian,; H. Akbar,; R. Colvin,; J. Ding,; L. Y. Tong,; S. Y. Wu, et al. A small-molecule inhibitor of glucose transporter 1 downregulates glycolysis, induces cell-cycle arrest, and inhibits cancer cell growth in vitro and in vivo. Mol. Cancer Ther. 2012, 11, 1672-1682.
Google Scholar
[31]
W. H. Chen,; G. F. Luo,; Q. Lei,; S. Hong,; W. X. Qiu,; L. H. Liu,; S. X. Cheng,; X. Z. Zhang, Overcoming the heat endurance of tumor cells by interfering with the anaerobic glycolysis metabolism for improved photothermal therapy. ACS Nano 2017, 11, 1419-1431.
Google Scholar
[32]
J. Zhou,; M. H. Li,; Y. H. Hou,; Z. Luo,; Q. F. Chen,; H. X. Cao,; R. L. Huo,; C. C. Xue,; L. Sutrisno,; L. Hao, et al. Engineering of a nanosized biocatalyst for combined tumor starvation and low-temperature photothermal therapy. ACS Nano 2018, 12, 2858-2872.
Google Scholar
[33]
G. Gao,; Y. W. Jiang,; Y. X. Guo,; H. R. Jia,; X. T. Cheng,; Y. Deng,; X. W. Yu,; Y. X. Zhu,; H. Y. Guo,; W. Sun, et al. Enzyme-mediated tumor starvation and phototherapy enhance mild-temperature photothermal therapy. Adv. Funct. Mater. 2020, 30, 1909391.
Google Scholar
[34]
J. J. Hu,; M. D. Liu,; F. Gao,; Y. Chen,; S. Y. Peng,; Z. H. Li,; H. Cheng,; X. Z. Zhang, Photo-controlled liquid metal nanoparticle-enzyme for starvation/photothermal therapy of tumor by win-win cooperation. Biomaterials 2019, 217, 119303.
Google Scholar
[35]
J. Sánchez-Laínez,; B. Zornoza,; S. Friebe,; J. Caro,; S. Cao,; A. Sabetghadam,; B. Seoane,; J. Gascon,; F. Kapteijn,; C. Le Guillouzer, et al. Influence of ZIF-8 particle size in the performance of polybenzimidazole mixed matrix membranes for pre-combustion CO2 capture and its validation through interlaboratory test. J. Membrane Sci. 2016, 515, 45-53.
Google Scholar
[36]
M. Hu,; Y. Ju,; K. Liang,; T. Suma,; J. W. Cui,; F. Caruso, Void engineering in metal-organic frameworks via synergistic etching and surface functionalization. Adv. Funct. Mater. 2016, 26, 5827-5834.
Google Scholar
[37]
C. Fang,; P. J. Yan,; Z. H. Ren,; Y. F. Wang,; X. J. Cai,; X. Li,; G. R. Han, Multifunctional MoO2-ICG nanoplatform for 808 nm-mediated synergetic photodynamic/photothermal therapy. Appl. Mater. Today 2019, 15, 472-481.
Google Scholar
[38]
C. J. Yu,; S. M. Wu,; W. L. Tseng, Magnetite nanoparticle-induced fluorescence quenching of adenosine triphosphate-BODIPY conjugates: Application to adenosine triphosphate and pyrophosphate sensing. Anal. Chem. 2013, 85, 8559-8565.
Google Scholar
[39]
Z. J. Lu,; J. Y. Gao,; C. Fang,; Y. Zhou,; X. Li,; G. R. Han, Porous Pt nanospheres incorporated with GOx to enable synergistic oxygen-inductive starvation/electrodynamic tumor therapy. Adv. Sci., in press, .
Crossref Google Scholar
[40]
Y. Y. Kuang,; K. Balakrishnan,; V. Gandhi,; X. H. Peng, Hydrogen peroxide inducible DNA cross-linking agents: Targeted anticancer prodrugs. J. Am. Chem. Soc. 2011, 133, 19278-19281.
Google Scholar
[41]
J. Verrax,; N. Dejeans,; B. Sid,; C. Glorieux,; P. B. Calderon, Intracellular ATP levels determine cell death fate of cancer cells exposed to both standard and redox chemotherapeutic agents. Biochem. Pharmacol. 2011, 82, 1540-1548.
Google Scholar
[42]
Q. C. Mao,; J. D. Unadkat, Role of the breast cancer resistance protein (BCRP/ABCG2) in drug transport-an update. AAPS J. 2015, 17, 65-82.
Google Scholar
[43]
W. P. Zheng,; M. H. Li,; Y. X. Lin,; X. Zhan, Encapsulation of verapamil and doxorubicin by MPEG-PLA to reverse drug resistance in ovarian cancer. Biomed. Pharmacother. 2018, 108, 565-573.
Google Scholar
[44]
L. C. Gomes,; G. Di Benedetto,; L. Scorrano, During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 2011, 13, 589-598.
Google Scholar
[45]
S. E. Weinberg,; L. A. Sena,; N. S. Chandel, Mitochondria in the regulation of innate and adaptive immunity. Immunity 2015, 42, 406-417.
Google Scholar
Nano Research
Volume 14 Issue 1,
January 2021
Pages 222-231
DOI: 10.1007/s12274-020-3071-7
Cite this article:
Zhu H, Cao G, Fu Y, et al. ATP-responsive hollow nanocapsules for DOX/GOx delivery to enable tumor inhibition with suppressed P-glycoprotein. Nano Research, 2021, 14(1): 222-231. https://doi.org/10.1007/s12274-020-3071-7
Topics:
Chemotherapy Controlled drug deliveryGlucoseGlucose oxidaseGlucose sensors GlycoproteinsNanocapsules Targeted drug deliveryTumors

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Received: 17 July 2020
Revised: 17 August 2020
Accepted: 22 August 2020
Published: 05 January 2021
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature
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