Targeting Nanodiamonds to the Nucleus in Yeast Cells
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fluorescent Nanodiamonds Starting Material
2.2. Preparation of FNDs Conjugated Antibody
2.3. Zeta Potential and Size Measurements
2.4. Fourier-Transform Infrared Spectroscopy (FTIR) Measurements
2.5. Co-Localization of FND–AB
2.6. FND Particle Uptake in Saccharomyces Cerevisiae
2.7. Immobilizing Yeast Cells
2.8. Biocompatibility Assay
2.9. Distance Measurement from the Nucleus
2.10. Statistical Analysis
3. Results
3.1. Characterization of FND–AB
3.2. Biocompatibility of FND–AB
3.3. Position of FNDs and FND–AB Inside Cells
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Vaijayanthimala, V.; Cheng, P.-Y.; Yeh, S.-H.; Liu, K.-K.; Hsiao, C.-H.; Chao, J.-I.; Chang, H.-C. Biomaterials The long-term stability and biocompatibility of fluorescent nanodiamond as an in vivo contrast agent. Biomaterials 2012, 33, 7794–7802. [Google Scholar] [CrossRef] [PubMed]
- Su, L.-J.; Wu, M.-S.; Hui, Y.Y.; Chang, B.-M.; Pan, L.; Hsu, P.-C.; Chen, Y.-T.; Ho, H.-N.; Huang, Y.-H.; Ling, T.-Y.; et al. Fluorescent nanodiamonds enable quantitative tracking of human mesenchymal stem cells in miniature pigs. Sci. Rep. 2017, 7, 1–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hui, Y.Y.; Su, L.-J.; Chen, O.Y.; Chen, Y.-T.; Liu, T.-M.; Chang, H.-C. Wide-field imaging and flow cytometric analysis of cancer cells in blood by fluorescent nanodiamond labeling and time gating. Sci. Rep. 2014, 4, 1–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haziza, S.; Mohan, N.; Loe-Mie, Y.; Lepagnol-Bestel, A.-M.; Massou, S.; Adam, M.-P.; Le, X.L.; Viard, J.; Plancon, C.; Daudin, R.; et al. Fluorescent nanodiamond tracking reveals intraneuronal transport abnormalities induced by brain-disease-related genetic risk factors. Nat. Nanotechnol. 2016, 12, 322–328. [Google Scholar] [CrossRef]
- Liu, K.-K.; Wang, C.-C.; Cheng, C.-L.; Chao, J.-I. Endocytic carboxylated nanodiamond for the labeling and tracking of cell division and differentiation in cancer and stem cells. Biomaterials 2009, 30, 4249–4259. [Google Scholar] [CrossRef] [PubMed]
- Lien, Z.-Y.; Hsu, T.-C.; Liu, K.-K.; Liao, W.-S.; Hwang, K.C.; Chao, J.-I. Cancer cell labeling and tracking using fl uorescent and magnetic nanodiamond. Biomaterials 2012, 33, 6172–6185. [Google Scholar] [CrossRef]
- Hemelaar, S.R.; De Boer, P.; Chipaux, M.; Zuidema, W.; Hamoh, T.; Martinez, F.P.; Nagl, A.; Hoogenboom, J.P.; Giepmans, B.N.G.; Schirhagl, R. Nanodiamonds as multi-purpose labels for microscopy. Sci. Rep. 2017, 7, 1–9. [Google Scholar] [CrossRef]
- Li, Y.; Tong, Y.; Cao, R.; Tian, Z.; Yang, B.; Yang, P. In vivo enhancement of anticancer therapy using bare or chemotherapeutic drug-bearing nanodiamond particles. Int. J. Nanomed. 2014, 9, 1065–1082. [Google Scholar] [CrossRef] [Green Version]
- Cui, Z.; Zhang, Y.; Zhang, J.; Kong, H.; Tang, X.; Pan, L.; Xia, K.; Aldalbahi, A.; Li, A.; Tai, R.; et al. Sodium alginate-functionalized nanodiamonds as sustained chemotherapeutic drug-release vectors. Carbon 2016, 97, 78–86. [Google Scholar] [CrossRef]
- Wang, D.-X.; Tong, Y.; Li, Y.; Tian, Z.; Cao, R.; Yang, B. PEGylated nanodiamond for chemotherapeutic drug delivery. Diam. Relat. Mater. 2013, 36, 26–34. [Google Scholar] [CrossRef]
- Zhao, L.; Xu, Y.-H.; Akasaka, T.; Abe, S.; Komatsu, N.; Watari, F.; Chen, X. Polyglycerol-coated nanodiamond as a macrophage-evading platform for selective drug delivery in cancer cells. Biomaterials 2014, 35, 5393–5406. [Google Scholar] [CrossRef] [PubMed]
- Kossovsky, N.; Gelman, A.; Hnatyszyn, H.J.; Rajguru, S.; Garrell, R.L.; Torbati, S.; Freitas, S.S.F.; Chow, G.-M. Surface-Modified Diamond Nanoparticles as Antigen Delivery Vehicles. Bioconjugate Chem. 1995, 6, 507–511. [Google Scholar] [CrossRef] [PubMed]
- Van Der Laan, K.; Hasani, M.; Zheng, T.; Schirhagl, R. Nanodiamonds for In Vivo Applications. Small. 2018, 14, 1703838. [Google Scholar] [CrossRef] [PubMed]
- Kucsko, G.; Maurer, P.C.; Yao, N.Y.; Kubo, M.; Noh, H.J.; Lo, P.K.; Park, H.; Lukin, M.D. Nanometre-scale thermometry in a living cell. Nature 2013, 500, 54–58. [Google Scholar] [CrossRef] [PubMed]
- Simpson, D.A.; Morrisroe, E.; McCoey, J.; Lombard, A.H.; Mendis, D.C.; Treussart, F.; Hall, L.T.; Petrou, S.; Hollenberg, L.C.L. Non-neurotoxic nanodiamond probes for intraneuronal temperature mapping. ACS Nano 2017, 11, 12077–12086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rendler, T.; Neburkova, J.; Zemek, O.; Kotek, J.; Zappe, A.; Chu, Z.; Cígler, P.; Wrachtrup, J. Optical imaging of localized chemical events using programmable diamond quantum nanosensors. Nat. Commun. 2017, 8, 1–9. [Google Scholar] [CrossRef]
- Steinert, S.; Ziem, F.; Hall, L.T.; Zappe, A.; Schweikert, M.; Götz, N.; Aird, A.; Balasubramanian, G.; Hollenberg, L.C.L.; Wrachtrup, J. Magnetic spin imaging under ambient conditions with sub-cellular resolution. Nat. Commun. 2013, 4, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Glenn, D.R.; Lee, K.; Park, H.; Weissleder, R.; Yacoby, A.; Lukin, M.D.; Lee, H.; Walsworth, R.L.; Connolly, C.B. Single-cell magnetic imaging using a quantum diamond microscope. Nat. Methods 2015, 12, 736–738. [Google Scholar] [CrossRef]
- Hemelaar, S.R.; Van Der Laan, K.J.; Hinterding, S.R.; Koot, M.V.; Ellermann, E.; Perona-Martinez, F.P.; Roig, D.; Hommelet, S.; Novarina, D.; Takahashi, H.; et al. Generally applicable transformation protocols for fluorescent nanodiamond internalization into cells. Sci. Rep. 2017, 7, 5862. [Google Scholar] [CrossRef]
- Chipaux, M.; Van Der Laan, K.J.; Hemelaar, S.R.; Hasani, M.; Zheng, T.; Schirhagl, R. Nanodiamonds and their applications in cells. Small 2018, 14, 1–25. [Google Scholar] [CrossRef]
- Hemelaar, S.R.; Saspaanithy, B.; L’Hommelet, S.R.M.; Martinez, F.P.P.; Van Der Laan, K.J.; Schirhagl, R. The response of HeLa cells to fluorescent nanodiamond uptake. Sensors 2018, 18, 355. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mkandawire, M.; Pohl, A.; Gubarevich, T.; Lapina, V.; Appelhans, D.; Rödel, G.; Pompe, W.; Schreiber, J.; Opitz, J.; Opitz, J. Selective targeting of green fluorescent nanodiamond conjugates to mitochondria in HeLa cells. J. Biophotonics 2009, 2, 596–606. [Google Scholar] [CrossRef] [PubMed]
- Chang, B.-M.; Lin, H.-H.; Su, L.-J.; Lin, W.-D.; Lin, R.-J.; Tzeng, Y.-K.; Lee, R.T.; Lee, Y.C.; Yu, A.L.; Chang, H.-C. Highly fluorescent nanodiamonds protein-functionalized for cell labeling and targeting. Adv. Funct. Mater. 2013, 23, 5737–5745. [Google Scholar] [CrossRef]
- Slegerova, J.; Hajek, M.; Řehoř, I.; Sedlak, F.; Stursa, J.; Hruby, M.; Cígler, P. Designing the nanobiointerface of fluorescent nanodiamonds: Highly selective targeting of glioma cancer cells. Nanoscale 2015, 7, 415–420. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, B.; Li, Y.; Fang, C.-Y.; Chang, C.-C.; Chen, C.-S.; Chen, Y.-Y.; Chang, H.-C. Receptor-mediated cellular uptake of folate-conjugated fluorescent nanodiamonds: A combined ensemble and single-particle study. Small 2009, 5, 2716–2721. [Google Scholar] [CrossRef]
- Zurbuchen, M.A.; Lake, M.P.; Kohan, S.A.; Leung, B.; Bouchard, L.-S. Nanodiamond landmarks for subcellular multimodal optical and electron imaging. Sci. Rep. 2013, 3, 1–5. [Google Scholar] [CrossRef] [Green Version]
- Torelli, M.D.; Rickard, A.G.; Backer, M.V.; Filonov, D.S.; Nunn, N.A.; Kinev, A.V.; Backer, J.M.; Palmer, G.; Shenderova, O.A. Targeting fluorescent nanodiamonds to vascular endothelial growth factor receptors in tumor. Bioconjugate Chem. 2019, 30, 604–613. [Google Scholar] [CrossRef]
- Kong, X.L.; Huang, L.C.L.; Hsu, C.-M.; Chen, W.-H.; Han, A.C.-C.; Chang, H.-C. High-affinity capture of proteins by diamond nanoparticles for mass spectrometric analysis. Anal. Chem. 2005, 77, 259–265. [Google Scholar] [CrossRef]
- Zhang, W.; Patel, K.; Schexnider, A.; Banu, S.; Radadia, A.D. Nanostructuring of biosensing electrodes with nanodiamonds for antibody immobilization. ACS Nano 2014, 8, 1419–1428. [Google Scholar] [CrossRef]
- Morita, A.; Martinez, F.P.P.; Chipaux, M.; Jamot, N.; Hemelaar, S.R.; Van Der Laan, K.J.; Schirhagl, R. Cell uptake of lipid-coated diamond. Part. Part. Syst. Charact. 2019, 36, 1–8. [Google Scholar] [CrossRef]
- Burgers, P.M.; Percival, K.J. Transformation of yeast spheroplasts without cell fusion. Anal. Biochem. 1987, 163, 391–397. [Google Scholar] [CrossRef]
- Russell, B.I.; Stewart, G.G. Spheroplast fusion of Brewer’s yeast strains. J. Inst. Brew. 1979, 85, 95–98. [Google Scholar] [CrossRef]
- Ovalle, R.; Lim, S.T.; Holder, B.; Jue, C.K.; Moore, C.W.; Lipke, P.N. A spheroplast rate assay for determination of cell wall integrity in yeast. Yeast 1998, 14, 1159–1166. [Google Scholar] [CrossRef]
- Lake, M.P.; Bouchard, L.S. Targeted nanodiamonds for identification of subcellular protein assemblies in mammalian cells. PLoS ONE 2017, 12, 1–18. [Google Scholar] [CrossRef] [PubMed]
- Spector, D.L. The dynamics of chromosome organization and gene regulation. Annu. Rev. Biochem. 2013, 72, 573–608. [Google Scholar] [CrossRef] [PubMed]
- Ong, Y.; Van Harmelen, R.J.; Norouzi, N.; Offens, F.; Venema, I.M.; Najafi, M.B.H.; Schirhagl, R. Interaction of nanodiamonds with bacteria. Nanoscale 2018, 10, 17117–17124. [Google Scholar] [CrossRef] [PubMed]
- Martinez, F.P.; Nagl, A.; Guluzade, S.; Schirhagl, R. Nanodiamond for sample preparation in proteomics. Anal. Chem. 2019, 91, 9800–9805. [Google Scholar] [CrossRef] [Green Version]
- Hemelaar, S.R.; Nagl, A.; Bigot, F.; Rodríguez-García, M.M.; De Vries, M.P.; Chipaux, M.; Schirhagl, R. The interaction of fluorescent nanodiamond probes with cellular media. Microchim. Acta 2017, 184, 1001–1009. [Google Scholar] [CrossRef] [Green Version]
- Karas, B.J.; Jablanovic, J.; Irvine, E.; Sun, L.; Ma, L.; Weyman, P.D.; Gibson, D.G.; Glass, J.I.; Venter, J.C.; Hutchison, C.A.; et al. Transferring whole genomes from bacteria to yeast spheroplasts using entire bacterial cells to reduce DNA shearing. Nat. Protoc. 2014, 9, 743–750. [Google Scholar] [CrossRef]
- Van Der Laan, K.J.; Naulleau, J.; Damle, V.G.; Sigaeva, A.; Jamot, N.; Perona-Martinez, F.P.; Chipaux, M.; Schirhagl, R. Towards using fluorescent nanodiamonds to study chronological ageing in Saccharomyces cerevisiae. Anal. Chem. 2018, 90, 13506–13513. [Google Scholar] [CrossRef]
- Smith, A.H.; Robinson, E.; Zhang, X.; Ho, D.; Lin, Y.; Osawa, E.; Xi, J.; Ho, D. Triggered release of therapeutic antibodies from nanodiamond complexes. Nanoscale 2011, 3, 2844–2848. [Google Scholar] [CrossRef]
- Tammam, S.N.; Azzazy, H.M.E.; Lamprecht, A. How successful is nuclear targeting by nanocarriers. J. Control. Release 2016, 229, 140–153. [Google Scholar] [CrossRef] [PubMed]
- Chu, Z.; Miu, K.K.; Lung, P.; Zhang, S.; Zhao, S.; Chang, H.-C.; Lin, G.; Li, Q. Rapid endosomal escape of prickly nanodiamonds: Implications for gene delivery. Sci. Rep. 2015, 5, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heitz, F.; Morris, M.C.; Divita, G. Twenty years of cell-penetrating peptides: From molecular mechanisms to therapeutics. Br. J. Pharmacol. 2009, 157, 195–206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Morita, A.; Nusantara, A.C.; Martinez, F.P.P.; Hamoh, T.; Damle, V.G.; Van Der Laan, K.J.; Sigaeva, A.; Vedelaar, T.; Chang, M.; Chipaux, M.; et al. Quantum monitoring the metabolism of individual yeast mutant strain cells when aged, stressed or treated with antioxidant. arXiv 2020, arXiv:2007.16130. Available online: https://arxiv.org/abs/2007.16130 (accessed on 25 September 2020).
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Morita, A.; Hamoh, T.; Sigaeva, A.; Norouzi, N.; Nagl, A.; van der Laan, K.J.; Evans, E.P.P.; Schirhagl, R. Targeting Nanodiamonds to the Nucleus in Yeast Cells. Nanomaterials 2020, 10, 1962. https://doi.org/10.3390/nano10101962
Morita A, Hamoh T, Sigaeva A, Norouzi N, Nagl A, van der Laan KJ, Evans EPP, Schirhagl R. Targeting Nanodiamonds to the Nucleus in Yeast Cells. Nanomaterials. 2020; 10(10):1962. https://doi.org/10.3390/nano10101962
Chicago/Turabian StyleMorita, Aryan, Thamir Hamoh, Alina Sigaeva, Neda Norouzi, Andreas Nagl, Kiran J. van der Laan, Emily P. P. Evans, and Romana Schirhagl. 2020. "Targeting Nanodiamonds to the Nucleus in Yeast Cells" Nanomaterials 10, no. 10: 1962. https://doi.org/10.3390/nano10101962