Carrier-Free Cellular Transport of CRISPR/Cas9 Ribonucleoprotein for Genome Editing by Cold Atmospheric Plasma
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
3. Results and Discussion
3.1. CAP Devices and Cas9sg Characterization
3.2. CAP-Mediated Cellular Transport of Cas9sg
3.3. RONS-Mediated Endocytosis-Dependent and -Independent Uptake of Cas9sg
3.4. Intracellular Trafficking of Cas9sg
3.5. The Molecule Mechanism of Facilitating Endocytosis and Cytosolic Release of Cas9sg
3.6. Genome Editing of Cas9sg after the CAP Treatment
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Marraffini, L.A. CRISPR-Cas immunity in prokaryotes. Nature 2015, 526, 55–61. [Google Scholar] [CrossRef]
- Gilbert, L.A.; Larson, M.H.; Morsut, L.; Liu, Z.; Brar, G.A.; Torres, S.E.; Stern-Ginossar, N.; Brandman, O.; Whitehead, E.H.; Doudna, J.A.; et al. CRISPR-Mediated Modular RNA-Guided Regulation of Transcription in Eukaryotes. Cell 2013, 154, 442–451. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Konermann, S.; Brigham, M.D.; Trevino, A.E.; Joung, J.; Abudayyeh, O.O.; Barcena, C.; Hsu, P.D.; Habib, N.; Gootenberg, J.S.; Nishimasu, H.; et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 2015, 517, 583–588. [Google Scholar] [CrossRef] [Green Version]
- Tsai, S.Q.; Wyvekens, N.; Khayter, C.; Foden, J.A.; Thapar, V.; Reyon, D.; Goodwin, M.J.; Aryee, M.J.; Joung, J.K. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 2014, 32, 569–576. [Google Scholar] [CrossRef] [Green Version]
- Cox, D.B.T.; Platt, R.J.; Zhang, F. Therapeutic genome editing: Prospects and challenges. Nat. Med. 2015, 21, 121–131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, B.; Gilbert, L.A.; Cimini, B.A.; Schnitzbauer, J.; Zhang, W.; Li, G.W.; Park, J.; Blackburn, E.H.; Weissman, J.S.; Qi, L.S.; et al. Dynamic Imaging of Genomic Loci in Living Human Cells by an Optimized CRISPR/Cas System. Cell 2013, 155, 1479–1491. [Google Scholar] [CrossRef] [Green Version]
- Deng, W.; Shi, X.; Tjian, R.; Lionnet, T.; Singer, R.H. CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells. Proc. Natl. Acad. Sci. USA 2015, 112, 11870–11875. [Google Scholar] [CrossRef] [Green Version]
- Wu, Y.; Zhou, H.; Fan, X.; Zhang, Y.; Zhang, M.; Wang, Y.; Xie, Z.; Bai, M.; Yin, Q.; Liang, D.; et al. Correction of a genetic disease by CRISPR-Cas9-mediated gene editing in mouse spermatogonial stem cells. Cell Res. 2014, 25, 67–79. [Google Scholar] [CrossRef] [Green Version]
- Jacobi, A.M.; Rettig, G.R.; Turk, R.; Collingwood, M.A.; Zeiner, A.; Quadros, R.M.; Harms, D.W.; Bonthuis, P.J.; Ohtsuka, M.; Gurumurthy, C.B.; et al. Simplified CRISPR tools for efficient genome editing and streamlined protocols for their delivery into mammalian cells and mouse zygotes. Methods 2017, 121–122, 16–28. [Google Scholar] [CrossRef] [PubMed]
- Liang, X.; Potter, J.; Kumar, S.; Zou, Y.; Quintanilla, R.; Sridharan, M.; Carte, J.; Chen, W.; Roark, N.; Ranganathan, S.; et al. Rapid and highly efficient mammalian cell engineering via Cas9 protein transfection. J. Biotechnol. 2015, 208, 44–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, X.; Liang, X.; Xie, H.; Kumar, S.; Ravinder, N.; Potter, J.; de Mollerat du Jeu, X.; Chesnut, J.D. Improved delivery of Cas9 protein/gRNA complexes using lipofectamine CRISPRMAX. Biotechnol. Lett. 2016, 38, 919–929. [Google Scholar] [CrossRef] [Green Version]
- Chakraborty, S.; Ji, H.; Kabadi, A.; Gersbach, C.A.; Christoforou, N.; Leong, K. A CRISPR/Cas9-Based System for Reprogramming Cell Lineage Specification. Stem Cell Rep. 2014, 3, 940–947. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ran, F.A.; Cong, L.; Yan, W.X.; Scott, D.A.; Jonathan, A.J.K.; Gootenberg, S.; Zetsche, B.; Shalem, O.; Wu, X.; Makarova, K.S.; et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature 2015, 520, 186–191. [Google Scholar] [CrossRef] [PubMed]
- Yin, H.; Kanasty, R.L.; Eltoukhy, A.A.; Vegas, A.J.; Dorkin, J.R.; Anderson, D.G. Non-viral vectors for gene-based therapy. Nat. Rev. Genet. 2014, 15, 541–555. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.-X.; Li, M.; Lee, C.M.; Chakraborty, S.; Kim, H.W.; Bao, G.; Leong, K.W. CRISPR/Cas9-Based Genome Editing for Disease Modeling and Therapy: Challenges and Opportunities for Nonviral Delivery. Chem. Rev. 2017, 117, 9874–9906. [Google Scholar] [CrossRef] [PubMed]
- Thach, T.T.; Bae, D.H.; Kim, N.H.; Kang, E.S.; Lee, B.S. Lipopeptide-Based Nanosome-Mediated Delivery of Hyperaccurate CRISPR/Cas9 Ribonucleoprotein for Gene Editing. Small 2019, 15, 1903172. [Google Scholar] [CrossRef] [PubMed]
- Sun, W.; Ji, W.; Hall, J.M.; Hu, Q.; Wang, C.; Beisel, C.L.; Gu, Z. Self-Assembled DNA Nanoclews for the Efficient Delivery of CRISPR–Cas9 for Genome Editing. Angew. Chem. Int. Ed. 2015, 54, 12029–12033. [Google Scholar] [CrossRef]
- Mout, R.; Ray, M.; Tonga, G.Y.; Lee, Y.W.; Tay, T.; Sasaki, K.; Rotello, V.M. Direct Cytosolic Delivery of CRISPR/Cas9-Ribonucleoprotein for Efficient Gene Editing. ACS Nano 2017, 11, 2452–2458. [Google Scholar] [CrossRef] [Green Version]
- Li, L.; Song, L.; Liu, X.; Yang, X.; Li, X.; He, T.; Wang, N.; Yang, S.; Yu, C.; Yin, T.; et al. Artificial Virus Delivers CRISPR-Cas9 System for Genome Editing of Cells in Mice. ACS Nano 2017, 11, 95–111. [Google Scholar] [CrossRef] [PubMed]
- Zhou, W.; Cui, H.; Ying, L.; Yu, X.-F. Enhanced Cytosolic Delivery and Release of CRISPR/Cas9 by Black Phosphorus Nanosheets for Genome Editing. Angew. Chem. Int. Ed. 2018, 57, 10268–10272. [Google Scholar] [CrossRef]
- Alsaiari, S.K.; Patil, S.; Alyami, M.; Alamoudi, K.O.; Aleisa, F.A.; Merzaban, J.S.; Li, M.; Khashab, N.M. Endosomal Escape and Delivery of CRISPR/Cas9 Genome Editing Machinery Enabled by Nanoscale Zeolitic Imidazolate Framework. J. Am. Chem. Soc. 2018, 140, 143–146. [Google Scholar] [CrossRef] [Green Version]
- Kuhn, J.; Lin, Y.; Levacic, A.K.; Al Danaf, N.; Peng, L.; Ho, M.; Lamb, D.C.; Wagner, E.; La, U. Delivery of Cas9/sgRNA Ribonucleoprotein Complexes via Hydroxystearyl Oligoamino Amides. Bioconjug. Chem. 2020, 31, 729–742. [Google Scholar] [CrossRef] [PubMed]
- Kaushik, N.K.; Kaushik, N.; Wahab, R.; Bhartiya, P.; Linh, N.N.; Khan, F.; Al-Khedhairy, A.A.; Choi, E.H. Cold Atmospheric Plasma and Gold Quantum Dots Exert Dual Cytotoxicity Mediated by the Cell Receptor-Activated Apoptotic Pathway in Glioblastoma Cells. Cancers 2020, 12, 457. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tavares-da-Silva, E.; Pereira, E.; Pires, A.S.; Neves, A.R.; Braz-Guilherme, C.; Marques, I.A.; Abrantes, A.M.; Gonçalves, A.C.; Caramelo, F.; Silva-Teixeira, R.; et al. Cold Atmospheric Plasma, a Novel Approach against Bladder Cancer, with Higher Sensitivity for the High-Grade Cell Line. Biology 2021, 10, 41. [Google Scholar] [CrossRef] [PubMed]
- Keidar, M. Plasma for cancer treatment. Plasma Sources Sci. Technol. 2015, 24, 033001. Available online: http://iopscience.iop.org/0963-0252/24/3/033001 (accessed on 27 August 2021). [CrossRef]
- Haralambiev, L.; Nitsch, A.; Jacoby, J.M.; Strakeljahn, S.; Bekeschus, S.; Mustea, A.; Ekkernkamp, A.; Stope, M.B. Cold Atmospheric Plasma Treatment of Chondrosarcoma Cells Affects Proliferation and Cell Membrane Permeability. Int. J. Mol. Sci. 2020, 21, 2291. [Google Scholar] [CrossRef] [Green Version]
- Xu, D.; Luo, X.; Xu, Y.; Cui, Q.; Yang, Y.; Liu, D. The effects of cold atmospheric plasma on cell adhesion, differentiation, migration, apoptosis and drug sensitivity of multiple myeloma. Biochem. Biophys. Res. Commun. 2016, 473, 1125–1132. [Google Scholar] [CrossRef]
- Hirst, A.M.; Simms, M.S.; Mann, V.M.; Maitland, N.J.; O’connell, D.; Frame, F.M. Low-temperature plasma treatment induces DNA damage leading to necrotic cell death in primary prostate epithelial cells. Br. J. Cancer 2015, 112, 1536–1545. [Google Scholar] [CrossRef] [Green Version]
- Gjika, E.; Pal-Ghosh, S.; Tang, A.; Kirschner, M.; Tadvalkar, G.; Canady, J.; Stepp, M.A.; Keidar, M. Adaptation of Operational Parameters of Cold Atmospheric Plasma for in Vitro Treatment of Cancer Cells. ACS Appl. Mater. Interfaces 2018, 10, 9269–9279. [Google Scholar] [CrossRef]
- Edelblute, C.M.; Heller, L.C.; Malik, M.A.; Heller, R. Activated air produced by shielded sliding discharge plasma mediates plasmid DNA delivery to mammalian cells. Biotechnol. Bioeng. 2015, 112, 2583–2590. [Google Scholar] [CrossRef]
- Xu, D.; Wang, B.; Xu, Y.; Chen, Z.; Cui, Q.; Yang, Y.; Chen, H.; Kong, M.G. Intracellular ROS mediates gas plasma-facilitated cellular transfection in 2D and 3D cultures. Sci. Rep. 2016, 6, 27872. [Google Scholar] [CrossRef] [Green Version]
- Dolezalova, E.; Malik, M.A.; Heller, L.; Heller, R. Delivery and expression of plasmid DNA into cells by a novel non-thermal plasma source. Bioelectrochemistry 2021, 140, 107816. [Google Scholar] [CrossRef] [PubMed]
- Zhu, W.; Lee, S.-J.; Castro, N.J.; Yan, D.; Keidar, M.; Zhang, L.G. Synergistic Effect of Cold Atmospheric Plasma and Drug Loaded Core-shell Nanoparticles on Inhibiting Breast Cancer Cell Growth. Sci. Rep. 2016, 6, 21974. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, Z.; Liu, K.; Manaloto, E.; Casey, A.; Cribaro, G.P.; Byrne, H.J.; Tian, F.; Barcia, C.; Conway, G.E.; Cullen, P.J.; et al. Cold Atmospheric Plasma Induces ATP-Dependent Endocytosis of Nanoparticles and Synergistic U373MG Cancer Cell Death. Sci. Rep. 2018, 8, 5298. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ding, L.; Zhu, X.; Wang, Y.; Shi, B.; Ling, X.; Chen, H.; Nan, W.; Barrett, A.; Guo, Z.; Tao, W.; et al. Intracellular Fate of Nanoparticles with Polydopamine Surface Engineering and a Novel Strategy for Exocytosis-Inhibiting, Lysosome Impairment-Based Cancer Therapy. Nano Lett. 2017, 17, 6790–6801. [Google Scholar] [CrossRef]
- Yusupov, M.; Van der Paal, J.; Neyts, E.C.; Bogaerts, A. Synergistic effect of electric field and lipid oxidation on the permeability of cell membranes. Biochim. Biophys. Acta-Gen. Subj. 2017, 1861, 839–847. [Google Scholar] [CrossRef]
- Bauer, G.; Graves, D.B. Mechanisms of Selective Antitumor Action of Cold Atmospheric Plasma-Derived Reactive Oxygen and Nitrogen Species. Plasma Process. Polym. 2016, 13, 1157–1178. [Google Scholar] [CrossRef]
- Connolly, R.J.; Lopez, G.A.; Hoff, A.M.; Jaroszeski, M.J. Characterization of plasma mediated molecular delivery to cells in vitro. Int. J. Pharm. 2010, 389, 53–57. [Google Scholar] [CrossRef]
- Dong, X.; Liu, T.; Xiong, Y. A novel approach to regulate cell membrane permeability for ATP and NADH formation in Saccharomyces cerevisiae induced by air cold plasma. Plasma Sci. Technol. 2017, 19, 024001. Available online: http://pst.hfcas.ac.cn/EN/10.1088/2058-6272/19/2/024001 (accessed on 27 August 2021). [CrossRef] [Green Version]
- Liu, M.; Du, P.; Heinrich, G.; Cox, G.M.; Gelli, A. Cch1 Mediates Calcium Entry in Cryptococcus neoformans and Is Essential in Low-Calcium Environments. Eukaryot. Cell 2006, 5, 1788–1796. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Huang, W.; Wang, X.; Tang, T.; Hua, Z.; Yan, G. Improvement of alcoholic fermentation by calcium ions under enological conditions involves the increment of plasma membrane H+-ATPase activity. World J. Microbiol. Biotechnol. 2010, 26, 1181–1186. [Google Scholar] [CrossRef] [PubMed]
- Omata, D.; Negishi, Y.; Yamamura, S.; Hagiwara, S.; Endo-Takahashi, Y.; Suzuki, R.; Maruyama, K.; Nomizu, M.; Aramaki, Y. Involvement of Ca2+ and ATP in Enhanced Gene Delivery by Bubble Liposomes and Ultrasound Exposure. Mol. Pharm. 2012, 9, 1017–1023. [Google Scholar] [CrossRef]
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Cui, H.; Jiang, M.; Zhou, W.; Gao, M.; He, R.; Huang, Y.; Chu, P.K.; Yu, X.-F. Carrier-Free Cellular Transport of CRISPR/Cas9 Ribonucleoprotein for Genome Editing by Cold Atmospheric Plasma. Biology 2021, 10, 1038. https://doi.org/10.3390/biology10101038
Cui H, Jiang M, Zhou W, Gao M, He R, Huang Y, Chu PK, Yu X-F. Carrier-Free Cellular Transport of CRISPR/Cas9 Ribonucleoprotein for Genome Editing by Cold Atmospheric Plasma. Biology. 2021; 10(10):1038. https://doi.org/10.3390/biology10101038
Chicago/Turabian StyleCui, Haodong, Min Jiang, Wenhua Zhou, Ming Gao, Rui He, Yifan Huang, Paul K. Chu, and Xue-Feng Yu. 2021. "Carrier-Free Cellular Transport of CRISPR/Cas9 Ribonucleoprotein for Genome Editing by Cold Atmospheric Plasma" Biology 10, no. 10: 1038. https://doi.org/10.3390/biology10101038