AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Article Link
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Silicon-based nanoprobes cross the blood–brain barrier for photothermal therapy of glioblastoma

Rong Sun§Mingzhu Liu§Zhaojian XuBin SongYao He ( )Houyu Wang ( )
Suzhou Key Laboratory of Nanotechnology and Biomedicine, Institute of Functional Nano and Soft Materials (FUNSOM) and Collaborative Innovation Center of Suzhou Nano Science and Technology, Soochow University, Suzhou 215123, China

§ Rong Sun and Mingzhu Liu contributed equally to this work.

Show Author Information

Graphical Abstract

We present a kind of SiNPs-based nanoprobes that can bypass the blood−brain barrier, suitable for glioblastoma photothermal therapy.

Abstract

Traditional photothermal agents of indocyanine green (ICG) have poor stability, short circulation time, and poor brain permeability due to the blood–brain barrier (BBB), greatly impairing their therapeutic efficacy in glioblastoma (GBM). Herein, we develop a novel kind of SiNPs-based nanoprobes to bypass the BBB for photothermal therapy of GBM. Typically, the SiNPs-based nanoprobes are composed of the particle itself, the BBB-targeting ligand of glucosamine (G), and the therapeutic agent of ICG. We demonstrate that the as-synthesized nanoprobes could cross the BBB through glucose transporter-1 (GLUT1)-mediated transcytosis, followed by accumulation at GBM tissues in mice. Compared with free ICG, G-ICG-SiNPs show stronger stability (for example, the fluorescence intensity of G-ICG-SiNPs loaded with the same dose of ICG decays by 34.6% after 25 days of storage, while the fluorescence intensity of ICG decays by 99.5% under the same conditions). Furthermore, the blood circulation time of G-ICG-SiNPs increases by about 17.3-fold compared with their ICG counterparts. After injection of the therapeutic agents into the GBM-bearing mice, GBM-surface temperature rises to 45.3 °C in G-ICG-SiNPs group after 5-min 808 nm irradiation but climbs only to 36.1 °C in equivalent ICG group under the identical conditions, indicating the superior photothermal effects of G-ICG-SiNPsin vivo.

Electronic Supplementary Material

Download File(s)
12274_2022_4367_MOESM1_ESM.pdf (968.5 KB)

References

1

Tang, W.; Fan, W. P.; Lau, J.; Deng, L. M.; Shen, Z. Y.; Chen, X. Y. Emerging blood–brain-barrier-crossing nanotechnology for brain cancer theranostics. Chem. Soc. Rev. 2019, 48, 2967–3014.

2

Song, E.; Mao, T. Y.; Dong, H. P.; Boisserand, L. S. B.; Antila, S.; Bosenberg, M.; Alitalo, K.; Thomas, J. L.; Iwasaki, A. VEGF-C-driven lymphatic drainage enables immunosurveillance of brain tumours. Nature 2020, 577, 689–694.

3

Wang, D. R.; Starr, R.; Chang, W. C.; Aguilar, B.; Alizadeh, D.; Wright, S. L.; Yang, X.; Brito, A.; Sarkissian, A.; Ostberg, J. R. et al. Chlorotoxin-directed CAR T cells for specific and effective targeting of glioblastoma. Sci. Transl. Med. 2020, 12, eaaw2672.

4

Yang, Z. Z.; Du, Y. T.; Sun, Q.; Peng, Y. W.; Wang, R. D.; Zhou, Y.; Wang, Y. Q.; Zhang, C. L.; Qi. X. R. Albumin-based nanotheranostic probe with hypoxia alleviating potentiates synchronous multimodal imaging and phototherapy for glioma. ACS Nano 2020, 14, 6191–6212.

5

Wang, X. X.; Yang, K. L.; Wu, Q. L.; Kim, L. J. Y.; Morton, A. R.; Gimple, R. C.; Prager, B. C.; Shi, Y.; Zhou, W. C.; Bhargava, S. et al. Targeting pyrimidine synthesis accentuates molecular therapy response in glioblastoma stem cells. Sci. Transl. Med. 2019, 11, eaau4972.

6

Kadiyala, P.; Li, D.; Nuñez, F. M.; Altshuler, D.; Doherty, R.; Kuai, R.; Yu, M. Z.; Kamran, N.; Edwards, M.; Moon, J. J. et al. High-density lipoprotein-mimicking nanodiscs for chemo-immunotherapy against glioblastoma multiforme. ACS Nano 2019, 13, 1365–1384.

7

Patil, R.; Galstyan, A.; Sun, T.; Shatalova, E. S.; Butte, P.; Mamelak, A. N.; Carico, C.; Kittle, D. S.; Grodzinski, Z. B.; Chiechi, A. et al. Polymalic acid chlorotoxin nanoconjugate for near-infrared fluorescence guided resection of glioblastoma multiforme. Biomaterials 2019, 206, 146–159.

8

Hu, S. Q.; Dong, C. Y.; Wang, J. Q.; Liu, K. X.; Zhou, Q.; Xiang, J. J.; Zhou, Z. X.; Liu. F. S.; Shen, Y. Q. Assemblies of indocyanine green and chemotherapeutic drug to cure established tumors by synergistic chemo-photo therapy. J. Control. Rel. 2020, 324, 250–259.

9

Ott, P. Hepatic elimination of indocyanine green with special reference to distribution kinetics and the influence of plasma protein binding. Pharmacol. Toxicol. 1998, 83, 7–48.

10

Hu, N.; Shi, X. L.; Zhang, Q.; Liu, W. T.; Zhu, Y. T.; Wang, Y. Q.; Hou, Y.; Ji, Y. L.; Cao, Y. P.; Zeng, Q. et al. Special interstitial route can transport nanoparticles to the brain bypassing the blood–brain barrier. Nano Res. 2019, 12, 2760–2765.

11

Singh, A.; Kim, W.; Kim, Y.; Jeong, K.; Kang, C. S.; Kim, Y. S.; Koh, J.; Mahajan, S. D.; Prasad, P. N.; Kim, S. Multifunctional photonics nanoparticles for crossing the blood–brain barrier and effecting optically trackable brain theranostics. Adv. Funct. Mater. 2016, 26, 7057–7066.

12

Gilbert, M. R.; Dignam, J. J.; Armstrong, T. S.; Wefel, J. S.; Blumenthal, D. T.; Vogelbaum, M. A.; Colman, H.; Chakravarti, A.; Pugh, S.; Won, M. et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N. Engl. J. Med. 2014, 370, 699–708.

13

Chinot, O. L.; Wick, W.; Mason, W.; Henriksson, R.; Saran, F.; Nishikawa, R.; Carpentier, A. F.; Hoang-Xuan, K.; Kavan, P.; Cernea, D. et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N. Engl. J. Med. 2014, 370, 709–722.

14

Hao, Y.; Chen, Y. W.; He, X. L.; Yang, F.; Han, R. X.; Yang, C. L.; Li, W.; Qian, Z. Y. Near-infrared responsive 5-fluorouracil and indocyanine green loaded MPEG-PCL nanoparticle integrated with dissolvable microneedle for skin cancer therapy. Bioact. Mater. 2020, 5, 542–552.

15

Wang, Y.; Luo, S. Y.; Wu, Y. S.; Tang, P.; Liu, J. J.; Liu, Z. Y.; Shen, S. H.; Ren, H. Z.; Wu, D. C. Highly penetrable and on-demand oxygen release with tumor activity composite nanosystem for photothermal/photodynamic synergetic therapy. ACS Nano 2020, 14, 17046–17062.

16

Zhu, J. Y.; Sevencan, C.; Zhang, M. K.; McCoy, R. S. A.; Ding, X. G.; Ye, J. J.; Xie, J. P.; Ariga, K.; Feng, J.; Bay, B. H. et al. Increasing the potential interacting area of nanomedicine enhances its homotypic cancer targeting efficacy. ACS Nano 2021, 14, 3259–3271.

17

Chen, Q.; Xu, L. G.; Liang, C.; Wang, C.; Peng, R.; Liu, Z. Photothermal therapy with immune-adjuvant nanoparticles together with checkpoint blockade for effective cancer immunotherapy. Nat. Commun. 2016, 7, 13193.

18

Tapeinos, C.; Battaglini, M.; Ciofani, G. Advances in the design of solid lipid nanoparticles and nanostructured lipid carriers for targeting brain diseases. J. Control. Rel. 2017, 264, 306–332.

19

Gong, N. Q.; Zhang, Y. X.; Teng, X. C.; Wang, Y. C.; Huo, S. D.; Qing, G. C.; Ni, Q. K.; Li, X. L.; Wang, J. J.; Ye, X. X. et al. Proton-driven transformable nanovaccine for cancer immunotherapy. Nat. Nanotechnol. 2020, 15, 1053–1064.

20

Lundy, D. J.; Lee, K. J.; Peng, I. C.; Hsu, C. H.; Lin, J. H.; Chen, K. H.; Tien, Y. W.; Hsieh, P. C. H. Inducing a transient increase in blood-brain barrier permeability for improved liposomal drug therapy of glioblastoma multiforme. ACS Nano 2019, 13, 97–113.

21

del Bonis-O’Donnell, J. T.; Chio, L.; Dorlhiac, G. F.; McFarlane, I. R.; Landry, M. P. Advances in nanomaterials for brain microscopy. Nano Res. 2018, 11, 5144–5172.

22

Etame, A. B.; Smith, C. A.; Chan, W. C. W.; Rutka, J. T. Design and potential application of PEGylated gold nanoparticles with size-dependent permeation through brain microvasculature. Nanomedicine 2011, 7, 992–1000.

23

Qin, Y.; Fan, W.; Chen, H. L.; Yao, N.; Tang, W. W.; Tang, J.; Yuan, W. M.; Kuai, R.; Zhang, Z. R.; Wu, Y. et al. In vitro and in vivo investigation of glucose-mediated brain-targeting liposomes. J. Drug Target. 2010, 18, 536–549.

24

Ruan, S. B.; Hu, C.; Tang, X.; Cun, X. L.; Xiao, W.; Shi, K. R.; He, Q.; Gao, H. L. Increased gold nanoparticle retention in brain tumors by in situ enzyme-induced aggregation. ACS Nano 2016, 10, 10086–10098.

25

Li, Y. R.; Zhang, X. J.; Qi, Z. F.; Guo, X. L.; Liu, X. P.; Shi, W. J.; Liu, Y.; Du, L. B. The enhanced protective effects of salvianic acid A: A functionalized nanoparticles against ischemic stroke through increasing the permeability of the blood-brain barrier. Nano Res. 2020, 13, 2791–2802.

26

Peng, C. Q.; Gao, X. F.; Xu, J.; Du, B. J.; Ning, X. H.; Tang, S. H.; Bachoo, R. M.; Yu, M. X.; Ge, W. P.; Zheng, J. Targeting orthotopic gliomas with renal-clearable luminescent gold nanoparticles. Nano Res. 2017, 10, 1366–1376.

27

Cai, X. L.; Bandla, A.; Mao, D.; Feng, G. G.; Qin, W.; Liao, L. D.; Thakor, N.; Tang, B. Z.; Liu, B. Biocompatible red fluorescent organic nanoparticles with tunable size and aggregation-induced emission for evaluation of blood-brain barrier damage. Adv. Mater. 2016, 28, 8760–8765.

28

Park, J. H.; Gu, L.; von Maltzahn, G.; Ruoslahti, E.; Bhatia S. N.; Sailor, M. J. Biodegradable luminescent porous silicon nanoparticles for in vivo applications. Nat. Mater. 2009, 8, 331–336.

29

Gu, L.; Hall, D. J.; Qin, Z. T.; Anglin, E.; Joo, J.; Mooney, D. J.; Howell, S. B.; Sailor, M. J. In vivo time-gated fluorescence imaging with biodegradable luminescent porous silicon nanoparticles. Nat. Commun. 2013, 4, 2326.

30

Zhong, Y. L.; Sun, X. T.; Wang, S. Y.; Peng, F.; Bao, F.; Su, Y. Y.; Li, Y. Y.; Lee, S. T.; He, Y. Facile, large-quantity synthesis of stable, tunable-color silicon nanoparticles and their application for long-term cellular imaging. ACS Nano 2015, 9, 5958–5967.

31

Ji, X. Y.; Peng, F.; Zhong, Y. L.; Su, Y. Y.; Jiang, X. X.; Song, C. X.; Yang, L.; Chu, B. B.; Lee, S. T.; He, Y. Highly fluorescent, photostable, and ultrasmall silicon drug nanocarriers for long-term tumor cell tracking and in-vivo cancer therapy. Adv. Mater. 2015, 27, 1029–1034.

32

Su, Y. Y.; Ji, X. Y.; He, Y. Water-dispersible fluorescent silicon nanoparticles and their optical applications. Adv. Mater. 2016, 28, 10567–10574.

33

Tang, M. M.; Ji, X. Y.; Xu, H.; Zhang, L.; Jiang, A. R.; Song, B.; Su, Y. Y.; He, Y. Photostable and biocompatible fluorescent silicon nanoparticles-based theranostic probes for simultaneous imaging and treatment of ocular neovascularization. Anal. Chem. 2018, 90, 8188–8195.

34

Ji, X. Y.; Guo, D. X.; Song, B.; Wu, S. C.; Chu, B. B.; Su, Y. Y.; He, Y. Traditional Chinese medicine molecule-assisted chemical synthesis of fluorescent anti-cancer silicon nanoparticles. Nano Res. 2018, 11, 5629–5641.

35

Guo, D. X.; Ji, X. Y.; Peng, F.; Zhong, Y. L.; Chu, B. B.; Su, Y. Y.; He, Y. Photostable and biocompatible fluorescent silicon nanoparticles for imaging-guided co-delivery of siRNA and doxorubicin to drug-resistant cancer cells. Nano-Micro Lett. 2019, 11, 27.

36

Tang, J. L.; Chu, B. B.; Wang, J. H.; Song, B.; Su, Y. Y.; Wang, H. Y.; He, Y. Multifunctional nanoagents for ultrasensitive imaging and photoactive killing of Gram-negative and Gram-positive bacteria. Nat. Commun. 2019, 10, 4057.

37

Zhang, L.; Ji, X. Y.; Su, Y. Y.; Zhai, X.; Xu, H.; Song, B.; Jiang, A. R.; Guo, D. X.; He, Y. Fluorescent silicon nanoparticles-based nanotheranostic agents for rapid diagnosis and treatment of bacteria-induced keratitis. Nano Res. 2021, 14, 52–58.

38

Liu, C. H.; Sun, Y.; Li, J.; Gong, Y.; Tian, K. T.; Evans, L. P.; Morss, P. C.; Fredrick, T. W.; Saba, N. J.; Chen, J. Endothelial microRNA-150 is an intrinsic suppressor of pathologic ocular neovascularization. Proc. Natl. Acad. Sci. USA 2015, 112, 12163–12168.

39

Setyawati, M. I.; Tay, C. Y.; Bay, B. H.; Leong, D. T. Gold nanoparticles induced endothelial leakiness depends on particle size and endothelial cell origin. ACS Nano 2017, 11, 5020–5030.

40

Arnaoutova, I.; Kleinman, H. K. In vitro angiogenesis: Endothelial cell tube formation on gelled basement Membrane Extract. Nat. Protoc. 2010, 5, 628–635.

41

Watkins, S.; Robel, S.; Kimbrough, I. F.; Robert, S. M.; Ellis-Davies, G.; Sontheimer, H. Disruption of astrocyte-vascular coupling and the blood–brain barrier by invading glioma cells. Nat. Commun. 2014, 5, 4196.

42

Tardito, S.; Oudin, A.; Ahmed, S. U.; Fack, F.; Keunen, O.; Zheng, L.; Miletic, H.; Sakariassen, P. Ø.; Weinstock, A.; Wagner, A. et al. Glutamine synthetase activity fuels nucleotide biosynthesis and supports growth of glutamine-restricted glioblastoma. Nat. Cell Biol. 2015, 17, 1556–1568.

43

Pang, J. Y.; Su, Y. Y.; Zhong, Y. L.; Peng, F.; Song, B.; He, Y. Fluorescent silicon nanoparticle-based gene carriers featuring strong photostability and feeble cytotoxicity. Nano Res. 2016, 9, 3027–3037.

44

Li, G. Z.; Wang, S. P.; Deng, D. S.; Xiao, Z. S.; Dong, Z. L.; Wang, Z. P.; Lei, Q. F.; Gao, S.; Huang, G. X.; Zhang, E. P. et al. Fluorinated chitosan to enhance transmucosal delivery of sonosensitizer-conjugated catalase for sonodynamic bladder cancer treatment post-intravesical instillation. ACS Nano 2020, 14, 1586–1599.

45

Jiang, A. R.; Song, B.; Ji, X. Y.; Peng, F.; Wang, H. Y.; Su, Y. Y.; He, Y. Doxorubicin-loaded silicon nanoparticles impregnated into red blood cells featuring bright fluorescence, strong photostability, and lengthened blood residency. Nano Res. 2018, 11, 2285–2294.

46

Ren, X. Q.; Zheng, R.; Fang, X. L.; Wang, X. F.; Zhang, X. Y.; Yang, W. L.; Sha, X. Y. Red blood cell membrane camouflaged magnetic nanoclusters for imaging-guided photothermal therapy. Biomaterials 2016, 92, 13–24.

47

Xue, J. W.; Zhao, Z. K.; Zhang, L.; Xue, L. J.; Shen, S. Y.; Wen, Y. J.; Wei, Z. Y.; Wang, L.; Kong, L. Y.; Sun, H. B. et al. Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence. Nat. Nanotechnol. 2017, 12, 692–700.

48

Zhou, T.; Yu, M. F.; Zhang, B.; Wang, L. M.; Wu, X. C.; Zhou, H. J.; Du, Y. P.; Hao, J. F.; Tu, Y. P.; Chen, C. Y. et al. Inhibition of cancer cell migration by gold nanorods: Molecular mechanisms and implications for cancer therapy. Adv. Funct. Mater. 2014, 24, 6922–6932.

49

Mindt, S.; Karampinis, I.; John, M.; Neumaier, M.; Nowak, K. Stability and degradation of indocyanine green in plasma, aqueous solution and whole blood. Photochem. Photobiol. Sci. 2018, 17, 1189–1196.

50

Ho, C. M.; Dhawan, A.; Hughes, R. D.; Lehec, S. C.; Puppi, J.; Philippeos, C.; Lee, P. H.; Mitry, R. R. Use of indocyanine green for functional assessment of human hepatocytes for transplantation. Asian J. Surg. 2012, 35, 9–15.

51

Zhou, H.; Fan, Z. Y.; Li, P. Y.; Deng, J. J.; Arhontoulis, D. C.; Li, C. Y.; Bowne, W. B.; Cheng, H. Dense and dynamic polyethylene glycol shells cloak nanoparticles from uptake by liver endothelial cells for long blood circulation. ACS Nano 2018, 12, 10130–10141.

52

Yang, L.; Kuang, H. J.; Zhang, W. Y.; Aguilar, Z. P.; Xiong, Y. H.; Lai, W. H.; Xu, H. Y.; Wei, H. Size dependent biodistribution and toxicokinetics of iron oxide magnetic nanoparticles in mice. Nanoscale 2015, 7, 625–636.

53

Wang, B.; He, X.; Zhang, Z. Y.; Zhao, Y. L.; Feng, W. Y. Metabolism of nanomaterials in vivo: Blood circulation and organ clearance. Acc. Chem. Res. 2013, 46, 761–769.

54

Lopez-Chaves, C.; Soto-Alvaredo, J.; Montes-Bayon, M.; Bettmer, J.; Llopis, J.; Sanchez-Gonzalez, C. Gold nanoparticles: Distribution, bioaccumulation and toxicity. In vitro and in vivo studies. Nanomedicine 2018, 14, 1–12.

Nano Research
Pages 7392-7401
Cite this article:
Sun R, Liu M, Xu Z, et al. Silicon-based nanoprobes cross the blood–brain barrier for photothermal therapy of glioblastoma. Nano Research, 2022, 15(8): 7392-7401. https://doi.org/10.1007/s12274-022-4367-6
Topics:

1153

Views

10

Crossref

10

Web of Science

11

Scopus

1

CSCD

Altmetrics

Received: 09 February 2022
Revised: 22 March 2022
Accepted: 28 March 2022
Published: 14 June 2022
© Tsinghua University Press 2022
Return