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Research Article

In situ assembly of magnetic nanocrystals/graphene oxide nanosheets on tumor cells enables efficient cancer therapy

Mingyang Liu1,2Yang Lu3Qilin Yu1,2( )Shu-Hong Yu2 ( )
Key Laboratory of Molecular Microbiology and Technology, Ministry of Education, Department of Microbiology, College of Life Sciences, Nankai University, Tianjin 300071, China
Division of Nanomaterials and Chemistry, Hefei National Laboratory for Physical Sciences at the Microscale, CAS Center for Excellence in Nanoscience, Department of Chemistry, University of Science and Technology of China, Hefei 230026, China
Key Laboratory of Advanced Catalytic Materials and Reaction Engineering, School of Chemistry and Chemical Engineering, Hefei University of Technology, Hefei 230009, China
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Abstract

Owing to the stimulus-responsive and dynamic properties, magnetism-driven assembly of building blocks to form ordered structures is always a marvelous topic. While abundant magnetic assemblies have been developed in ideal physical and chemical conditions, it remains a challenge to realize magnetic assembly in complicated biological systems. Herein, we report a kind of biomacromolecule-modified magnetic nanosheets, which are mainly composed of superparamagnetic graphene oxide (γ-Fe2O3@GO), the tumor-targeting protein transferrin (TF), and the mitochondrion-targeting peptide (MitP). Such large-size nanosheets (0.5-1 μm), noted as L-Fe2O3@GO-MitP-TF, can successfully in situ assemble on the surface of tumor cells in a size-dependent and tumor cell-specific way, leading to severe inhibition of nutrient uptake for the tumor cells. More significantly, the nanostructures could efficiently confine the tumor cells, preventing both invasion and metastasis of tumor cells both in vitro and in vivo. Moreover, the 2D assemblies could remarkably disrupt the mitochondria and induce apoptosis, remarkably eradicating tumors under near-infrared (NIR) irradiation. This study sheds light on the development of new nano-systems for efficient cancer therapy and other biomedical applications.

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References

[1]
Erb, R. M.; Son, H. S.; Samanta, B.; Rotello, V. M.; Yellen, B. B. Magnetic assembly of colloidal superstructures with multipole symmetry. Nature 2009, 457, 999-1002.
[2]
Nie, Z. H.; Petukhova, A.; Kumacheva, E. Properties and emerging applications of self-assembled structures made from inorganic nanoparticles. Nat. Nanotechnol. 2010, 5, 15-25.
[3]
Ahniyaz, A.; Sakamoto, Y.; Bergström, L. Magnetic field-induced assembly of oriented superlattices from maghemite nanocubes. Proc. Natl. Acad. Sci. USA 2007, 104, 17570-17574.
[4]
Chen, G.; Gibson, K. J.; Liu, D.; Rees, H. C.; Lee, J. H.; Xia, W. W.; Lin, R. Q.; Xin, H. L.; Gang, O.; Weizmann, Y. Regioselective surface encoding of nanoparticles for programmable self-assembly. Nat. Mater. 2019, 18, 169-174.
[5]
Wang, M. S.; Yin, Y. D. Magnetically responsive nanostructures with tunable optical properties. J. Am. Chem. Soc. 2016, 138, 6315-6323.
[6]
Tasoglu, S.; Yu, C. H.; Gungordu, H. I.; Guven, S.; Vural, T.; Demirci, U. Guided and magnetic self-assembly of tunable magnetoceptive gels. Nat. Commun. 2014, 5, 4702.
[7]
Li, Z. W.; Wang, M. S.; Zhang, X. L.; Wang, D. W.; Xu, W. J.; Yin, Y. D. Magnetic assembly of nanocubes for orientation-dependent photonic responses. Nano Lett. 2019, 19, 6673-6680.
[8]
Balcells, L.; Stanković, I.;Konstantinović, Z.; Alagh, A.; Fuentes, V.; López-Mir, L.; Oró, J.; Mestres, N.; García, G.; Pomar, A. et al. Spontaneous in-flight assembly of magnetic nanoparticles into macroscopic chains. Nanoscale 2019, 11, 14194-14202.
[9]
Velez, C.; Torres-Díaz, I.; Maldonado-Camargo, L.; Rinaldi, C.; Arnold, D. P. Magnetic assembly and cross-linking of nanoparticles for releasable magnetic microstructures. ACS Nano 2015, 9, 10165-10172.
[10]
Han, Q.; Wang, X.; Yang, Z. Y.; Zhu, W. Y.; Zhou, X. M.; Jiang, H. J. Fe3O4@rGO doped molecularly imprinted polymer membrane based on magnetic field directed self-assembly for the determination of amaranth. Talanta 2014, 123, 101-108.
[11]
Lee, H.; Thirunavukkarasu, G. K.; Kim, S.; Lee, J. Y. Remote induction of in situ hydrogelation in a deep tissue, using an alternating magnetic field and superparamagnetic nanoparticles. Nano Res. 2018, 11, 5997-6009.
[12]
Diller, E.; Sitti, M. Three-dimensionalprogrammable assembly by untethered magnetic robotic micro-grippers. Adv. Func. Mater. 2014, 24, 4397-4404.
[13]
Han, K.; Shields, C. W.; Diwakar, N. M.; Bharti, B.; López, G. P.; Velev, O. D. Sequence-encoded colloidal origami and microbot assemblies from patchy magnetic cubes. Sci. Adv. 2017, 3, e1701108.
[14]
Yuan, J. Y.; Xu, Y. Y.; Müller, A. H. E. One-dimensional magnetic inorganic-organic hybrid nanomaterials. Chem. Soc. Rev. 2011, 40, 640-655.
[15]
Meyer, A.; Franz, N.; Oepen, H. P.; Perlich, J.; Carbone, G.; Metzger, T. H. In situ grazing-incidence small-angle X-ray scattering observation of block-copolymer templated formation of magnetic nanodot arrays and their magnetic properties. Nano Res. 2017, 10, 456-471.
[16]
Ramade, J.; Troc, N.; Boisron, O.; Pellarin, M.; Lebault, M. A.; Cottancin, E.; Oiko, V. T. A.;Gomes R. C.; Rodrigues, V.; Hillenkamp, M. Nano-fried-eggs: Structural, optical, and magnetic characterization of physically prepared iron-silver nanoparticles. Nano Res. 2018, 11, 6074-6085.
[17]
Wang, L.; Dong, S. L.; Hao, J. C. Recent progress of magnetic surfactants: Self-assembly, properties and functions. Curr. Opin. Colloid InterfaceSci. 2018, 35, 81-90.
[18]
Tabassum, D. P.; Polyak, K. Tumorigenesis: It takes a village. Nat. Rev. Cancer 2015, 15, 473-483.
[19]
Carmeliet, P. Angiogenesis in life, disease and medicine. Nature 2005, 438, 932-936.
[20]
Hoffman, R. M. Patient-derived orthotopic xenografts: Better mimic of metastasis than subcutaneous xenografts. Nat. Rev. Cancer 2015, 15, 451-452.
[21]
Strilic, B.;Yang, L. D.; Albarrán-Juárez, J.; Wachsmuth, L.; Han, K.; Müller, U. C.; Pasparakis, M.; Offermanns, S. Tumour-cell-induced endothelial cell necroptosis via death receptor 6 promotes metastasis. Nature 2016, 536, 215-218.
[22]
Martin, O. A.; Anderson, R. L.; Narayan, K.; MacManus, M. P. Does the mobilization of circulating tumour cells during cancer therapy cause metastasis? Nat. Rev. Clin. Oncol. 2017, 14, 32-44.
[23]
Shi, J. J.; Kantoff, P. W.; Wooster, R.; Farokhzad, O. C. Cancer nanomedicine: Progress, challenges and opportunities. Nat. Rev. Cancer 2017, 17, 20-37.
[24]
Kai, F.; Drain, A. P.; Weaver, V. M. The extracellular matrix modulates the metastatic journey. Dev. Cell 2019, 49, 332-346.
[25]
Ngwa, W.; Irabor, O. C.; Schoenfeld, J. D.; Hesser, J.; Demaria, S.; Formenti, S. C. Using immunotherapy to boost the abscopal effect. Nat. Rev. Cancer 2018, 18, 313-322.
[26]
Arvanitis, C. D.; Ferraro, G. B.; Jain, R. K. The blood-brain barrier and blood-tumour barrier in brain tumours and metastases. Nat. Rev. Cancer 2020, 20, 26-41.
[27]
D’Costa, Z.; Jones, K.; Azad, A.; Van Stiphout, R.; Lim, S. Y.; Gomes, A. L.;Kinchesh, P.; Smart, S. C.; Gillies McKenna, W.; Buffa, F. M. et al. Gemcitabine-induced TIMP1 attenuates therapy response and promotes tumor growth and liver metastasis in pancreatic cancer. Cancer Res. 2017, 77, 5952-5962.
[28]
Bushnell, G. G.; Hardas, T. P.; Hartfield, R. M.; Zhang, Y. N.; Oakes, R. S.; Ronquist, S.; Chen, H. M.; Rajapakse, I.; Wicha, M. S.; Jeruss, J. S. et al. Biomaterial scaffolds recruit an aggressive population of metastatic tumor cells in vivo. Cancer Res. 2019, 79, 2042-2053.
[29]
Chablani, P.; Nguyen, P.; Pan, X. L.; Robinson, A.; Walston, S.; Wu, C.; Frankel, W. L.; Chen, W.; Bekaii-Saab, T.;Chakravarti, A. et al. Perineural invasion predicts for distant metastasis in locally advanced rectal cancer treated with neoadjuvant chemoradiation and surgery. Am. J. Clin. Oncol. 2017, 40, 561-568.
[30]
Peela, N.; Truong, D.; Saini, H.; Chu, H.; Mashaghi, S.; Ham, S. L.; Singh, S.; Tavana, H.; Mosadegh. B.; Nikkhah, M. Advanced biomaterials and microengineering technologies to recapitulate the stepwise process of cancer metastasis.Biomaterials 2017, 133, 176-207.
[31]
Ye, H.; Wang, K. Y.; Wang, M. L.; Liu, R. Z.; Song, H.; Li, N.; Lu, Q.; Zhang, W. J.;Du, Y. Q.; Yang, W. Q. et al. Bioinspired nanoplatelets for chemo-photothermal therapy of breast cancer metastasis inhibition. Biomaterials 2019, 206, 1-12.
[32]
Yu, Q. L.; Zhang, Y. M.; Liu, Y. H.; Xu, X.; Liu, Y. Magnetism and photo dual-controlled supramolecular assembly for suppression of tumor invasion and metastasis. Sci. Adv. 2018, 4, eaat2297.
[33]
Yu, Q. L.; Zhang, Y. M.; Liu, Y. H.; Liu, Y. Magnetic supramolecular nanofibers of gold nanorods for photothermal therapy. Adv. Ther. 2019, 2, 1800137.
[34]
Choi, C. H. J.; Alabi, C. A.; Webster, P.; Davis, M. E. Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles. Proc. Natl. Acad. Sci. USA 2010, 107, 1235-1240.
[35]
Li, Y. F.; Chen, M.; Yao, B. W.; Lu, X.; Zhang, X. Q.; He, P.; Vasilatos, S. N.; Ren, X. M.; Bian, W. H.; Yao, C. Transferrin receptor-targeted redox/pH-sensitive podophyllotoxin prodrug micelles for multidrug-resistant breast cancer therapy. J. Mater. Chem. B 2019, 7, 5814-5824.
[36]
Wei, Y. H.; Gu, X. L.; Sun, Y. P.; Meng, F. H.; Storm, G.; Zhong, Z. Y. Transferrin-binding peptide functionalized polymersomes mediate targeted doxorubicin delivery to colorectal cancer in vivo. J. Control. Release 2020, 319, 407-415.
[37]
Horton, K. L.; Stewart, K. M.; Fonseca, S. B.; Guo, Q.; Kelley, S. O. Mitochondria-penetrating peptides. Chem. Biol. 2008, 15, 375-382.
[38]
Zhang, B.; Yu, Q. L.; Zhang, Y. M.; Liu, Y. Two-dimensional supramolecular assemblies based on β-cyclodextrin-grafted graphene oxide for mitochondrial dysfunction and photothermal therapy. Chem. Commun. 2019, 55, 12200-12203.
[39]
Marcano, D. C.; Kosynkin, D. V.; Berlin, J. M.; Sinitskii, A.; Sun, Z. Z.; Slesarev, A.; Alemany, L. B.; Lu, W.; Tour, J. M. Improved synthesis of graphene oxide. ACS Nano 2010, 4, 4806-4814.
[40]
Robinson, J. T.; Tabakman, S. M.; Liang, Y.Y.; Wang, H. L.; Sanchez Casalongue, H.; 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.
[41]
Daniels, T. R.; Delgado, T.; Rodriguez, J. A.; Helguera, G.; Penichet, M. L. The transferrin receptor part I: Biology and targeting with cytotoxic antibodies for the treatment of cancer. Clin. Immun. 2006, 121, 144-158.
[42]
Mu, Q. X.; Su, G. X.; Li, L. W.; Gilbertson, B. O.; Yu, L. H.; Zhang, Q.; Sun, Y. P.; Yan, B. Size-dependent cell uptake of protein-coated graphene oxide nanosheets. ACS Appl. Mater. Interfaces 2012, 4, 2259-2266.
[43]
Zhu, J. Q.; Xu, M.; Gao, M.; Zhang, Z. H.; Xu, Y.; Xia, T.; Liu, S. J. Graphene oxide induced perturbation to plasma membrane and cytoskeletal meshwork sensitize cancer cells to chemotherapeutic agents. ACS Nano 2017, 11, 2637-2651.
Nano Research
Pages 1133-1140
Cite this article:
Liu M, Lu Y, Yu Q, et al. In situ assembly of magnetic nanocrystals/graphene oxide nanosheets on tumor cells enables efficient cancer therapy. Nano Research, 2020, 13(4): 1133-1140. https://doi.org/10.1007/s12274-020-2759-z
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Received: 20 February 2020
Revised: 15 March 2020
Accepted: 16 March 2020
Published: 14 April 2020
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2020
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