Cytocompatibility of stabilized black phosphorus nanosheets tailored by directly conjugated polymeric micelles for human breast cancer therapy.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
29 04 2021
29 04 2021
Historique:
received:
11
02
2021
accepted:
13
04
2021
entrez:
30
4
2021
pubmed:
1
5
2021
medline:
16
10
2021
Statut:
epublish
Résumé
The novel procedure of few-layer black phosphorus (FLBP) stabilization and functionalisation was here proposed. The cationic polymer PLL and non-ionic PEG have been involved into encapsulation of FLBP to allow sufficient time for further nanofabrication process and overcome environmental degradation. Two different spacer chemistry was designed to bind polymers to tumor-homing peptides. The efficiency of functionalisation was examined by RP-HPLC, microscopic (TEM and SEM) and spectroscopic (FT-IR and Raman) techniques as well supported by ab-initio modelling. The cell and dose dependent cytotoxicity of FLBP and its bioconjugates was evaluated against HB2, MCF-7 and MDA-MB-231 cell lines. Functionalisation allowed not only for improvement of environmental stability, but also enhances therapeutic effect by abolished the cytotoxicity of FLBP against HB2 cell line. Moreover, modification of FLBP with PLL caused increase of selectivity against highly aggressive breast cancer cell lines. Results indicate the future prospect application of black phosphorus nanosheets as nanocarrier, considering its unique features synergistically with conjugated polymeric micelles.
Identifiants
pubmed: 33927292
doi: 10.1038/s41598-021-88791-7
pii: 10.1038/s41598-021-88791-7
pmc: PMC8085149
doi:
Substances chimiques
Antineoplastic Agents
0
Drug Carriers
0
Micelles
0
Oligopeptides
0
Polylysine
25104-18-1
Phosphorus
27YLU75U4W
Polyethylene Glycols
3WJQ0SDW1A
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9304Références
Novoselov, K. S. et al. A.A.F. electric field effect in atomically thin carbon films. Science 306, 666–669 (2004).
pubmed: 15499015
doi: 10.1126/science.1102896
Chen, P., Li, N., Chen, X., Ong, W. J. & Zhao, X. The rising star of 2D black phosphorus beyond graphene: Synthesis, properties and electronic applications. 2D Mater. 5, 014002 (2018).
doi: 10.1088/2053-1583/aa8d37
Society, A. C., Xie, L. & Wu, J. Optical anisotropy of black phosphorus in the Visible Regime. J. Am. Chem. Soc. 138, 300–305 (2015).
Shao, L. et al. Facile preparation of NH
doi: 10.1039/C7TA10884B
Tao, Y. et al. Few-layer phosphorene: An emerging electrode material for electrochemical energy storage. Appl. Mater. Today 15, 18–33 (2019).
doi: 10.1016/j.apmt.2018.12.008
Jiang, J. W. & Park, H. S. Mechanical properties of single-layer black phosphorus. J. Phys. D Appl. Phys. 47, 385304 (2014).
doi: 10.1088/0022-3727/47/38/385304
Tang, H. et al. Progress in natural science: Materials international MXene—2D layered electrode materials for energy storage. Prog. Nat. Sci. Mater. Int. 28, 133–147 (2018).
doi: 10.1016/j.pnsc.2018.03.003
Das, S. et al. Tunable transport gap in phosphorene. Nano Lett. 14, 5733–5739 (2014).
pubmed: 25111042
doi: 10.1021/nl5025535
Torbatian, Z. & Asgari, R. Optical absorption properties of few-layer phosphorene. Phys. Rev. B 98, 205407 (2018).
doi: 10.1103/PhysRevB.98.205407
Sun, C. et al. One-pot solventless preparation of PEGylated black phosphorus nanoparticles for photoacoustic imaging and photothermal therapy of cancer. Biomaterials 91, 81–89 (2016).
pubmed: 27017578
doi: 10.1016/j.biomaterials.2016.03.022
Liang, X. et al. Photothermal cancer immunotherapy by erythrocyte membrane-coated black phosphorus formulation. J. Control. Release 296, 150–161 (2019).
pubmed: 30682441
doi: 10.1016/j.jconrel.2019.01.027
Kang, T. H., Lee, S., Kwon, J. A., Song, J. & Choi, I. Photothermally enhanced molecular delivery and cellular positioning on patterned plasmonic interfaces. ACS Appl. Mater. Interfaces 11, 36420–36427 (2019).
pubmed: 31509376
doi: 10.1021/acsami.9b13576
Hashemzadeh, H. & Raissi, H. Loading and release of anticancer drug from phosphorene as a template material with high efficient carrier: From vacuum to cell membrane. J. Mol. Liq. 291, 111346 (2019).
doi: 10.1016/j.molliq.2019.111346
Jakóbczyk, P. et al. Low-power microwave-induced fabrication of functionalised few-layer black phosphorus electrodes: A novel route towards Haemophilus Influenzae pathogen biosensing devices. Appl. Surf. Sci. 539, 148286 (2021).
doi: 10.1016/j.apsusc.2020.148286
Kim, J., Sando, S. & Cui, T. Biosensor based on layer by layer deposited phosphorene nanoparticles for liver cancer detection. ASME Int. Mech. Eng. Congr. Expo. Proc. 2, 1–6 (2017).
Murugan, C., Sharma, V., Murugan, R. K., Malaimegu, G. & Sundaramurthy, A. Two-dimensional cancer theranostic nanomaterials: Synthesis, surface functionalization and applications in photothermal therapy. J. Control. Release 299, 1–20 (2019).
pubmed: 30771414
doi: 10.1016/j.jconrel.2019.02.015
Chen, W. et al. Black phosphorus nanosheet-based drug delivery system for synergistic photodynamic/photothermal/chemotherapy of cancer. Adv. Mater. 29, 1–7 (2017).
Mu, X. et al. Black phosphorus quantum dot induced oxidative stress and toxicity in living cells and mice. ACS Appl. Mater. Interfaces 9, 20399–20409 (2017).
pubmed: 28553710
doi: 10.1021/acsami.7b02900
Hu, K. et al. Marriage of black phosphorus and Cu
doi: 10.1038/s41467-020-16513-0
Imaging, P. E. T. et al. Pegylated Arg-Gly-Asp peptide: 64Cu labeling and PET imaging of brain tumor αvβ3-integrin expression. J. Nucl. Med. 45, 1776–1783 (2004).
Zhao, Y. et al. Synthesis of a poly‑L-lysine/blackpPhosphorus hybrid for biosensors. Anal. Chem. 90, 3149–3155 (2018).
Banerjee, S. S., Aher, N., Patil, R. & Khandare, J. Poly(ethylene glycol)-prodrug conjugates: concept, design, and applications. J. Drug Deliv. 2012, 1–17 (2012).
Cui, Y. Black phosphorus-based drug nanocarrier for targeted and synergetic chemophotothermal therapy of acute lymphoblastic leukemia. ACS Appl. Mater. Interfaces 11, 5896–5902 (2019).
doi: 10.1021/acsami.8b22563
pubmed: 31889444
pmcid: 7006996
Wu, F. et al. Black phosphorus nanosheets-based nanocarriers for enhancing chemotherapy drug sensitiveness via depleting mutant p53 and resistant cancer multimodal therapy. Chem. Eng. J. 370, 387–399 (2019).
doi: 10.1016/j.cej.2019.03.228
Miller, J. S. et al. Biomaterials bioactive hydrogels made from step-growth derived PEG-peptide macromers. Biomaterials 31, 3736–3743 (2010).
pubmed: 20138664
pmcid: 2837100
doi: 10.1016/j.biomaterials.2010.01.058
Guerrini, L., Alvarez-puebla, R. A. & Pazos-perez, N. Surface modifications of nanoparticles for stability in biological fluids. Materials 11, 1154 (2018).
Shen, W.-C. & Ryser, H.J.-P. Poly(L-lysine) and poly(D-lysine) conjugates of methotrexate: Different inhibitory effect on drug resistant cells. Mol. Pharmacol. 16, 614–622 (1979).
pubmed: 514261
Ryser, H. J. P. & Shen, W. C. Conjugation of methotrexate to poly(L-lysine) increases drug transport and overcomes drug resistance in cultured cells. Proc. Natl. Acad. Sci. USA 75, 3867–3870 (1978).
pubmed: 279001
doi: 10.1073/pnas.75.8.3867
pmcid: 392889
Chiou, H. C. et al. Enhanced resistance to nuclease degradation of nucleic acids complexed to asialoglycoprotein-polylysine carriers. Nucl. Acids Res. 22, 5439–5446 (1994).
pubmed: 7816636
doi: 10.1093/nar/22.24.5439
pmcid: 332094
Northover, A. Gene transfer therapy in cancer. J. Br. Sug. 80, 566–572 (1993).
Zhu, F. et al. Smart nanoplatform for sequential drug release and enhanced chemo-thermal effect of dual drug loaded gold nanorod vesicles for cancer therapy. J. Nanobiotechnol. https://doi.org/10.1186/s12951-019-0473-3 (2019).
doi: 10.1186/s12951-019-0473-3
Wan, S., Zhang, B., Li, S., He, B. & Pu, Y. Combination of PEG-decorated black phosphorus nanosheets and immunoadjuvant for photoimmunotherapy of melanoma. J. Mater. Chem. B. 8, 2805–2813 (2020).
pubmed: 32163088
doi: 10.1039/D0TB00434K
Kim, K., Lee, J., Kim, D. & Yoon, I. Recent progress in the development of poly(lactic-co-glycolic acid) based nanostructures for cancer imaging and therapy. Pharmaceutics 11, 280 (2019).
pmcid: 6630460
doi: 10.3390/pharmaceutics11060280
Pisal, D. S., Kosloski, M. P. & Balu-iyer, S. V. Delivery of therapeutic. Proteins 99, 2557–2575 (2010).
Yavari, B., Mahjub, R., Saidijam, M., Raigani, M. & Soleimani, M. The potential use of peptides in cancer treatment. Curr Protein Pept Sci 19, 759–770 (2018).
Lieber, D. S., Elemento, O. & Tavazoie, S. Large-scale discovery and characterization of protein regulatory motifs in eukaryotes. PLoS ONE 5, e14444 (2010).
pubmed: 21206902
pmcid: 3012054
doi: 10.1371/journal.pone.0014444
Rathore, S. S. et al. Intracellular vesicle fusion requires a membrane-destabilizing peptide located at the juxtamembrane region of the v-SNARE. Cell Rep. 29, 4583-4592.e3 (2019).
pubmed: 31875562
pmcid: 6990648
doi: 10.1016/j.celrep.2019.11.107
Hoffman, J. A. et al. Progressive vascular changes in a transgenic mouse model of squamous cell carcinoma. Cancer Cell 4, 383–391 (2003).
pubmed: 14667505
doi: 10.1016/S1535-6108(03)00273-3
Yao, X. L. et al. Optimization and internalization mechanisms of PEGylated adenovirus vector with targeting peptide for cancer gene therapy. Biomacromol 13, 2402–2409 (2012).
doi: 10.1021/bm300665u
Craggs, G. & Kellie, S. A functional nuclear localization sequence in the C-terminal domain of SHP-1. J. Biol. Chem. 276, 23719–23725 (2001).
pubmed: 11323437
doi: 10.1074/jbc.M102846200
Agemy, L. et al. Targeted nanoparticle enhanced proapoptotic peptide as potential therapy for glioblastoma. Proc. Natl. Acad. Sci. USA. 111, 11906 (2014).
doi: 10.1073/pnas.1413457111
Majumder, P. Integrin-mediated delivery of drugs and nucleic acids for anti-angiogenic cancer therapy: Current landscape and remaining challenges. Bioengineering 5, 76 (2018).
pmcid: 6315429
doi: 10.3390/bioengineering5040076
Kang, B., Mackey, M. A. & El-Sayed, M. A. Nuclear targeting of gold nanoparticles in cancer cells induces DNA damage, causing cytokinesis arrest and apoptosis. J. Am. Chem. Soc. 132, 1517–1519 (2010).
pubmed: 20085324
doi: 10.1021/ja9102698
Smidstrup, S. et al. QuantumATK: An integrated platform of electronic and atomic-scale modelling tools. J. Phys. Condens. Matter 32, 015901 (2020).
pubmed: 31470430
doi: 10.1088/1361-648X/ab4007
Perdew, J. P., Burke, K. & Ernzerhof, M. Generalized gradient approximation made simple. Phys. Rev. Lett. 77, 3865–3868 (1996).
pubmed: 10062328
doi: 10.1103/PhysRevLett.77.3865
Morita, A. Semiconducting black phosphorus. Appl. Phys. A Solids Surf. 39, 227–242 (1986).
doi: 10.1007/BF00617267
Takao, Y., Asahina, H. & Morita, A. Electronic structure of black phosphorus in tight binding approach. J. Phys. Soc. Jpn. 50, 3362–3369 (1981).
doi: 10.1143/JPSJ.50.3362
Morga, M., Adamczyk, Z., Gödrich, S. & Oc, M. Monolayers of poly-L-lysine on mica—Electrokinetic characteristics. J. Colloid Interface Sci. 456, 116–124 (2015).
pubmed: 26115031
doi: 10.1016/j.jcis.2015.05.044
Sauer, B. B., Kampert, W. G., McLean, R. S. & Monteiro, R. Thermal properties and influence of orientation on crystalline morphologies in stereoblock polypropylene and related elastomers. J. Polym. Sci. Part B Polym. Phys. 49(3), 222–243. https://doi.org/10.1002/polb.22163 (2011).
doi: 10.1002/polb.22163
Tran, V., Fei, R. & Yang, L. Quasiparticle energies, excitons, and optical spectra of few-layer black phosphorus. 2D Mater. 2, 044014 (2015).
doi: 10.1088/2053-1583/2/4/044014
Liang, L. et al. Electronic bandgap and edge reconstruction in phosphorene materials. Nano Lett. 14, 6400–6406 (2014).
pubmed: 25343376
doi: 10.1021/nl502892t
Sun, H., Jiang, C., Wu, L., Bai, X. & Zhai, S. Cytotoxicity-related bioeffects induced by nanoparticles: The role of surface chemistry. Front. Bioeng. Biotechnol. 7, 1–22 (2019).
doi: 10.3389/fbioe.2019.00414
Bakshi, K., Liyanage, M. R., Volkin, D. B. & Middaugh, C. R. Fourier transform infrared spectroscopy of peptides. Therapeutic Peptides 1088, 255–269 (2014).
doi: 10.1007/978-1-62703-673-3_18
Abellán, G. et al. Fundamental insights into the degradation and stabilization of thin layer black phosphorus. J. Am. Chem. Soc. 139, 10432–10440 (2017).
pubmed: 28675300
pmcid: 5578363
doi: 10.1021/jacs.7b04971
Gómez-Pérez, J., Barna, B., Tóth, I. Y., Kónya, Z. & Kukovecz, Á. Quantitative tracking of the oxidation of black phosphorus in the few-layer regime. ACS Omega 3, 12482–12488 (2018).
pubmed: 31457979
pmcid: 6644649
doi: 10.1021/acsomega.8b01989
Wang, X., Mao, N., Luo, W., Kitadai, H. & Ling, X. Anomalous phonon modes in black phosphorus revealed by resonant raman scattering. J. Phys. Chem. Lett. 9, 2830–2837 (2018).
pubmed: 29746770
doi: 10.1021/acs.jpclett.8b01098
Carrier, D. & Pezolet, M. Raman spectroscopic study of the interaction of poly-L-lysine with dipalmitoylphosphatidylglycerol bilayers. Biophys. J. 46, 497–506. https://doi.org/10.1016/S0006-3495(84)84047-3 (1978).
doi: 10.1016/S0006-3495(84)84047-3
Qiu, M. et al. Novel concept of the smart NIR-light-controlled drug release of black phosphorus nanostructure for cancer therapy. Proc. Natl. Acad. Sci. USA. 115, 501–506 (2018).
pubmed: 29295927
doi: 10.1073/pnas.1714421115
pmcid: 5776980
Wang, M. et al. Ultrasmall black phosphorus quantum dots: Synthesis, characterization, and application in cancer treatment. Analyst 143, 5822–5833 (2018).
pubmed: 30371695
doi: 10.1039/C8AN01612G
Song, S. J. et al. Comparison of cytotoxicity of black phosphorus nanosheets in different types of fibroblasts. Biomater. Res. 23, 1–7 (2019).
doi: 10.1186/s40824-019-0174-x
Song, S. J. et al. Dose-and time-dependent cytotoxicity of layered black phosphorus in fibroblastic cells. Nanomaterials 8, 9–13 (2018).
doi: 10.3390/nano8060408
Kong, N. et al. Ros-mediated selective killing effect of black phosphorus: Mechanistic understanding and its guidance for safe biomedical applications. Nano Lett. 20, 3943–3955 (2020).
pubmed: 32243175
doi: 10.1021/acs.nanolett.0c01098
Li, Y., Feng, P., Wang, C., Miao, W. & Huang, H. Black phosphorus nanophototherapeutics with enhanced stability and safety for breast cancer treatment. Chem. Eng. J. 400, 125851 (2020).
doi: 10.1016/j.cej.2020.125851
Liu, Z., Robinson, J. T., Sun, X. & Dai, H. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J. Am. Chem. Soc. 130, 10876–10877 (2008).
pubmed: 18661992
pmcid: 2597374
doi: 10.1021/ja803688x
Liu, X. Y., Nothias, J. M., Scavone, A., Garfinkel, M. & Millis, J. M. Biocompatibility investigation of polyethylene glycol and alginate-poly-L-lysine for islet encapsulation. ASAIO J. 56, 241–245 (2010).
pubmed: 20400892
doi: 10.1097/MAT.0b013e3181d7b8e3
Jeong, H. et al. In vitro blood cell viability profiling of polymers used in molecular assembly. Sci. Rep. 7, 1–13 (2017).
doi: 10.1038/s41598-017-10169-5