Rational Design Principles for the Transport and Subcellular Distribution of Nanomaterials into Plant Protoplasts
Abstract
Abstract The ability to control the subcellular localization of nanoparticles within living plants offers unique advantages for targeted biomolecule delivery and enables important applications in plant bioengineering. However, the mechanism of nanoparticle transport past plant biological membranes is poorly understood. Here, a mechanistic study of nanoparticle cellular uptake into plant protoplasts is presented. An experimentally validated mathematical model of lipid exchange envelope penetration mechanism for protoplasts, which predicts that the subcellular distribution of nanoparticles in plant cells is dictated by the particle size and the magnitude of the zeta potential, is advanced. The mechanism is completely generic, describing nanoparticles ranging from quantum dots, gold and silica nanoparticles, nanoceria, and single‐walled carbon nanotubes (SWNTs). In addition, the use of imaging flow cytometry to investigate the influence of protoplasts' morphological characteristics on nanoparticle uptake efficiency is demonstrated. Using DNA‐wrapped SWNTs as model nanoparticles, it is found that glycerolipids, the predominant lipids in chloroplast membranes, exhibit stronger lipid–nanoparticle interaction than phospholipids, the major constituent in protoplast membrane. This work can guide the rational design of nanoparticles for targeted delivery into specific compartments within plant cells without the use of chemical or mechanical aid, potentially enabling various plant engineering applications.
- Authors:
-
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- Publication Date:
- Research Org.:
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1609981
- Alternate Identifier(s):
- OSTI ID: 1469026
- Grant/Contract Number:
- FG02-08ER46488; DE‐FG02‐08ER46488 Mod 0008
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Small
- Additional Journal Information:
- Journal Volume: 14; Journal Issue: 44; Journal ID: ISSN 1613-6810
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE; Chemistry; Science & Technology; Materials Science; Physics
Citation Formats
Lew, Tedrick Thomas Salim, Wong, Min Hao, Kwak, Seon-Yeong, Sinclair, Rosalie, Koman, Volodymyr B., and Strano, Michael S. Rational Design Principles for the Transport and Subcellular Distribution of Nanomaterials into Plant Protoplasts. United States: N. p., 2018.
Web. doi:10.1002/smll.201802086.
Lew, Tedrick Thomas Salim, Wong, Min Hao, Kwak, Seon-Yeong, Sinclair, Rosalie, Koman, Volodymyr B., & Strano, Michael S. Rational Design Principles for the Transport and Subcellular Distribution of Nanomaterials into Plant Protoplasts. United States. https://doi.org/10.1002/smll.201802086
Lew, Tedrick Thomas Salim, Wong, Min Hao, Kwak, Seon-Yeong, Sinclair, Rosalie, Koman, Volodymyr B., and Strano, Michael S. Thu .
"Rational Design Principles for the Transport and Subcellular Distribution of Nanomaterials into Plant Protoplasts". United States. https://doi.org/10.1002/smll.201802086. https://www.osti.gov/servlets/purl/1609981.
@article{osti_1609981,
title = {Rational Design Principles for the Transport and Subcellular Distribution of Nanomaterials into Plant Protoplasts},
author = {Lew, Tedrick Thomas Salim and Wong, Min Hao and Kwak, Seon-Yeong and Sinclair, Rosalie and Koman, Volodymyr B. and Strano, Michael S.},
abstractNote = {Abstract The ability to control the subcellular localization of nanoparticles within living plants offers unique advantages for targeted biomolecule delivery and enables important applications in plant bioengineering. However, the mechanism of nanoparticle transport past plant biological membranes is poorly understood. Here, a mechanistic study of nanoparticle cellular uptake into plant protoplasts is presented. An experimentally validated mathematical model of lipid exchange envelope penetration mechanism for protoplasts, which predicts that the subcellular distribution of nanoparticles in plant cells is dictated by the particle size and the magnitude of the zeta potential, is advanced. The mechanism is completely generic, describing nanoparticles ranging from quantum dots, gold and silica nanoparticles, nanoceria, and single‐walled carbon nanotubes (SWNTs). In addition, the use of imaging flow cytometry to investigate the influence of protoplasts' morphological characteristics on nanoparticle uptake efficiency is demonstrated. Using DNA‐wrapped SWNTs as model nanoparticles, it is found that glycerolipids, the predominant lipids in chloroplast membranes, exhibit stronger lipid–nanoparticle interaction than phospholipids, the major constituent in protoplast membrane. This work can guide the rational design of nanoparticles for targeted delivery into specific compartments within plant cells without the use of chemical or mechanical aid, potentially enabling various plant engineering applications.},
doi = {10.1002/smll.201802086},
journal = {Small},
number = 44,
volume = 14,
place = {United States},
year = {Thu Sep 06 00:00:00 EDT 2018},
month = {Thu Sep 06 00:00:00 EDT 2018}
}
Web of Science
Works referenced in this record:
Imaging Flow Cytometry: Coping with Heterogeneity in Biological Systems
journal, June 2012
- Barteneva, Natasha S.; Fasler-Kan, Elizaveta; Vorobjev, Ivan A.
- Journal of Histochemistry & Cytochemistry, Vol. 60, Issue 10
Ultrasmall Gold Nanoparticles as Carriers for Nucleus-Based Gene Therapy Due to Size-Dependent Nuclear Entry
journal, May 2014
- Huo, Shuaidong; Jin, Shubin; Ma, Xiaowei
- ACS Nano, Vol. 8, Issue 6
Surface-structure-regulated cell-membrane penetration by monolayer-protected nanoparticles
journal, May 2008
- Verma, Ayush; Uzun, Oktay; Hu, Yuhua
- Nature Materials, Vol. 7, Issue 7
In vitro transformation of plant protoplasts with Ti-plasmid DNA
journal, March 1982
- Krens, F. A.; Molendijk, L.; Wullems, G. J.
- Nature, Vol. 296, Issue 5852
Synthesis of Water-Soluble Blue Photoluminescent Silicon Nanocrystals with Oxide Surface Passivation
journal, January 2009
- Lin, Sheng-Wei; Chen, Dong-Hwang
- Small, Vol. 5, Issue 1
Self-Assembly of Lipids and Single-Walled Carbon Nanotubes: Effects of Lipid Structure and PEGylation
journal, April 2012
- Lee, Hwankyu; Kim, Hyungsu
- The Journal of Physical Chemistry C, Vol. 116, Issue 16
Biochemical and biophysical properties of thylakoid acyl lipids
journal, October 1991
- Webb, Murray S.; Green, Beverley R.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1060, Issue 2
Carbon Nanotubes as Molecular Transporters for Walled Plant Cells
journal, March 2009
- Liu, Qiaoling; Chen, Bo; Wang, Qinli
- Nano Letters, Vol. 9, Issue 3
Electroporation-mediated infection of tobacco leaf protoplasts with tobacco mosaic virus RNA and cucumber mosaic virus RNA
journal, February 1986
- Nishiguchi, M.; Langridge, W. H. R.; Szalay, A. A.
- Plant Cell Reports, Vol. 5, Issue 1
Calcium phosphate nanoparticle mediated genetic transformation in plants
journal, January 2012
- Naqvi, Saba; Maitra, A. N.; Abdin, M. Z.
- Journal of Materials Chemistry, Vol. 22, Issue 8
Translocation of polyarginines and conjugated nanoparticles across asymmetric membranes
journal, January 2013
- Li, Zhen-lu; Ding, Hong-ming; Ma, Yu-qiang
- Soft Matter, Vol. 9, Issue 4
Designing Nanoparticle Translocation through Membranes by Computer Simulations
journal, January 2012
- Ding, Hong-ming; Tian, Wen-de; Ma, Yu-qiang
- ACS Nano, Vol. 6, Issue 2
Optical Detection of DNA Conformational Polymorphism on Single-Walled Carbon Nanotubes
journal, January 2006
- Heller, D. A.
- Science, Vol. 311, Issue 5760
Fluid Phase Endocytic Uptake of Artificial Nano-Spheres and Fluorescent Quantum Dots by Sycamore Cultured Cells: Evidence for the Distribution of Solutes to Different Intracellular Compartments
journal, July 2006
- Etxeberria, Ed; Gonzalez, Pedro; Baroja-Fernández, Edurne
- Plant Signaling & Behavior, Vol. 1, Issue 4
Functionalized Carbon Nanotubes for Plasmid DNA Gene Delivery
journal, October 2004
- Pantarotto, Davide; Singh, Ravi; McCarthy, David
- Angewandte Chemie International Edition, Vol. 43, Issue 39
Plant nanobionic materials with a giant temperature response mediated by pectin-Ca 2+
journal, March 2015
- Di Giacomo, Raffaele; Daraio, Chiara; Maresca, Bruno
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 15
Free Volume Properties of Sphingomyelin, DMPC, DPPC, and PLPC Bilayers
journal, September 2005
- Kupiainen, M.; Falck, E.; Ollila, S.
- Journal of Computational and Theoretical Nanoscience, Vol. 2, Issue 3
Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order
journal, September 2002
- Harris, Faith M.; Best, Katrina B.; Bell, John D.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1565, Issue 1
A simple and effective method to encapsulate tobacco mesophyll protoplasts to maintain cell viability
journal, January 2015
- Lei, Rong; Qiao, Wenjie; Hu, Fan
- MethodsX, Vol. 2
Nanoparticle-induced surface reconstruction of phospholipid membranes
journal, November 2008
- Wang, B.; Zhang, L.; Bae, S. C.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 47
Mechanical Properties of the Plasma Membrane of Isolated Plant Protoplasts: Mechanism of Hyperosmotic and Extracellular Freezing Injury
journal, February 1983
- Wolfe, Joe; Steponkus, Peter L.
- Plant Physiology, Vol. 71, Issue 2
Non-endocytic penetration of core histones into petunia protoplasts and cultured cells: a novel mechanism for the introduction of macromolecules into plant cells
journal, August 2004
- Rosenbluh, Joseph; Singh, Sunil Kumar; Gafni, Yedidya
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1664, Issue 2
Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol
journal, June 2007
- Block, Maryse A.; Douce, Roland; Joyard, Jacques
- Photosynthesis Research, Vol. 92, Issue 2
Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression
journal, March 1994
- Abel, Steffen; Theologis, Athanasios
- The Plant Journal, Vol. 5, Issue 3
Coating Single-Walled Carbon Nanotubes with Phospholipids
journal, February 2006
- Wu, Yonnie; Hudson, JoAn S.; Lu, Qi
- The Journal of Physical Chemistry B, Vol. 110, Issue 6
Organically modified silica nanoparticles: A nonviral vector for in vivo gene delivery and expression in the brain
journal, July 2005
- Bharali, D. J.; Klejbor, I.; Stachowiak, E. K.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 32
A Polyethylene Glycol-Mediated Protoplast Transformation System for Production of Fertile Transgenic Rice Plants
journal, July 1990
- Hayashimoto, Akio; Li, Zhijian; Murai, Norimoto
- Plant Physiology, Vol. 93, Issue 3
Molecular biology of the plasma membrane of higher plants.
journal, October 1989
- Sussman, M. R.; Harper, J. F.
- The Plant Cell, Vol. 1, Issue 10
Homogeneous Hydrophobic–Hydrophilic Surface Patterns Enhance Permeation of Nanoparticles through Lipid Membranes
journal, May 2013
- Gkeka, Paraskevi; Sarkisov, Lev; Angelikopoulos, Panagiotis
- The Journal of Physical Chemistry Letters, Vol. 4, Issue 11
Protein-targeted corona phase molecular recognition
journal, January 2016
- Bisker, Gili; Dong, Juyao; Park, Hoyoung D.
- Nature Communications, Vol. 7, Issue 1
Surface Patterning of Carbon Nanotubes Can Enhance Their Penetration through a Phospholipid Bilayer
journal, January 2011
- Pogodin, Sergey; Slater, Nigel K. H.; Baulin, Vladimir A.
- ACS Nano, Vol. 5, Issue 2
On The Mechanical and Dynamic Properties of Plant Cell Membranes: Their Role in Growth, Direct Gene Transfer and Protoplast Fusion
journal, January 1993
- Kell, Antje; Glaser, Ralf W.
- Journal of Theoretical Biology, Vol. 160, Issue 1
Interparticle Dispersion, Membrane Curvature, and Penetration Induced by Single-Walled Carbon Nanotubes Wrapped with Lipids and PEGylated Lipids
journal, January 2013
- Lee, Hwankyu
- The Journal of Physical Chemistry B, Vol. 117, Issue 5
Bioconjugated Nanoparticles for DNA Protection from Cleavage
journal, June 2003
- He, Xiao-xiao; Wang, Kemin; Tan, Weihong
- Journal of the American Chemical Society, Vol. 125, Issue 24
Plant lipids and their role in membrane function
journal, January 1979
- Quinn, P. J.; Williams, W. P.
- Progress in Biophysics and Molecular Biology, Vol. 34
Enhanced Gene Delivery and siRNA Silencing by Gold Nanoparticles Coated with Charge-Reversal Polyelectrolyte
journal, August 2010
- Guo, Shutao; Huang, Yuanyu; Jiang, Qiao
- ACS Nano, Vol. 4, Issue 9
Spectroscopy of Single- and Double-Wall Carbon Nanotubes in Different Environments
journal, March 2005
- Hertel, Tobias; Hagen, Axel; Talalaev, Vadim
- Nano Letters, Vol. 5, Issue 3
Role of the Plasma Membrane in Freezing Injury and Cold Acclimation
journal, June 1984
- Steponkus, P. L.
- Annual Review of Plant Physiology, Vol. 35, Issue 1
Molecular Insight into the Line Tension of Bilayer Membranes Containing Hybrid Polyunsaturated Lipids
journal, February 2017
- Rosetti, Carla M.; Montich, Guillermo G.; Pastorino, Claudio
- The Journal of Physical Chemistry B, Vol. 121, Issue 7
Enhancement of biomolecule transport by electroporation: A review of theory and practical application to transformation ofCorynebacterium glutamicum
journal, January 2006
- Tryfona, Theodora; Bustard, Mark T.
- Biotechnology and Bioengineering, Vol. 93, Issue 3
Plant nanobionics approach to augment photosynthesis and biochemical sensing
journal, March 2014
- Giraldo, Juan Pablo; Landry, Markita P.; Faltermeier, Sean M.
- Nature Materials, Vol. 13, Issue 4
One Protoplast Is Not the Other!
journal, March 2011
- Faraco, Marianna; Di Sansebastiano, Gian Pietro; Spelt, Kees
- Plant Physiology, Vol. 156, Issue 2
Debundling of Single-Walled Nanotubes by Dilution: Observation of Large Populations of Individual Nanotubes in Amide Solvent Dispersions
journal, August 2006
- Giordani, Silvia; Bergin, Shane D.; Nicolosi, Valeria
- The Journal of Physical Chemistry B, Vol. 110, Issue 32
Signal Transduction in Maize and Arabidopsis Mesophyll Protoplasts
journal, December 2001
- Sheen, Jen
- Plant Physiology, Vol. 127, Issue 4
Determination of the Pore Size of Cell Walls of Living Plant Cells
journal, September 1979
- Carpita, N.; Sabularse, D.; Montezinos, D.
- Science, Vol. 205, Issue 4411
Nanoparticle-Induced Permeability of Lipid Membranes
journal, November 2012
- Pogodin, Sergey; Werner, Marco; Sommer, Jens-Uwe
- ACS Nano, Vol. 6, Issue 12
Cold Acclimation of Arabidopsis thaliana (Effect on Plasma Membrane Lipid Composition and Freeze-Induced Lesions)
journal, September 1995
- Uemura, M.; Joseph, R. A.; Steponkus, P. L.
- Plant Physiology, Vol. 109, Issue 1
Nanosensor Technology Applied to Living Plant Systems
journal, June 2017
- Kwak, Seon-Yeong; Wong, Min Hao; Lew, Tedrick Thomas Salim
- Annual Review of Analytical Chemistry, Vol. 10, Issue 1
Vehicles and ways for efficient nuclear transformation in plants
journal, November 2010
- Husaini, Amjad Masood; Abdin, Mallik Zainul; Parray, Ghulam Ahmad
- GM Crops, Vol. 1, Issue 5
A Nanobionic Light-Emitting Plant
journal, November 2017
- Kwak, Seon-Yeong; Giraldo, Juan Pablo; Wong, Min Hao
- Nano Letters, Vol. 17, Issue 12
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis
journal, June 2007
- Yoo, Sang-Dong; Cho, Young-Hee; Sheen, Jen
- Nature Protocols, Vol. 2, Issue 7
Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons
journal, February 2013
- Lu, Y.; Rijzaani, H.; Karcher, D.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 8
Physical Trauma and Tungsten Toxicity Reduce the Efficiency of Biolistic Transformation
journal, March 1992
- Russell, Julie A.; Roy, Mihir K.; Sanford, John C.
- Plant Physiology, Vol. 98, Issue 3
A simple plant gene delivery system using mesoporous silica nanoparticles as carriers
journal, January 2013
- Chang, Feng-Peng; Kuang, Lin-Yun; Huang, Chia-An
- Journal of Materials Chemistry B, Vol. 1, Issue 39
Chemical Basis of Interactions Between Engineered Nanoparticles and Biological Systems
journal, June 2014
- Mu, Qingxin; Jiang, Guibin; Chen, Lingxin
- Chemical Reviews, Vol. 114, Issue 15
Lipid Exchange Envelope Penetration (LEEP) of Nanoparticles for Plant Engineering: A Universal Localization Mechanism
journal, January 2016
- Wong, Min Hao; Misra, Rahul P.; Giraldo, Juan P.
- Nano Letters, Vol. 16, Issue 2
Root Uptake and Phytotoxicity of ZnO Nanoparticles
journal, August 2008
- Lin, Daohui; Xing, Baoshan
- Environmental Science & Technology, Vol. 42, Issue 15
Polyethylene glycol and electric field treatment of plant protoplasts: characterization of some membrane properties
journal, July 1986
- Hahn-Hagerdal, Barbel; Hosono, Kuniaki; Zaehrisson, Anders
- Physiologia Plantarum, Vol. 67, Issue 3
Functional Platform for Controlled Subcellular Distribution of Carbon Nanotubes
journal, October 2011
- Serag, Maged F.; Kaji, Noritada; Venturelli, Enrica
- ACS Nano, Vol. 5, Issue 11
SoyDB: a knowledge database of soybean transcription factors
journal, January 2010
- Wang, Zheng; Libault, Marc; Joshi, Trupti
- BMC Plant Biology, Vol. 10, Issue 1
Urea-Hydroxyapatite Nanohybrids for Slow Release of Nitrogen
journal, January 2017
- Kottegoda, Nilwala; Sandaruwan, Chanaka; Priyadarshana, Gayan
- ACS Nano, Vol. 11, Issue 2
Assessment of cell wall porosity in Arabidopsis thaliana by NMR spectroscopy
journal, March 2008
- Rondeau-Mouro, C.; Defer, D.; Leboeuf, E.
- International Journal of Biological Macromolecules, Vol. 42, Issue 2
journal, January 2002
- Wanichapichart, Pikul; Bunthawin, Sarawuth; Kaewpaiboon, Amnuoy
- ScienceAsia, Vol. 28, Issue 2
Nitroaromatic detection and infrared communication from wild-type plants using plant nanobionics
journal, October 2016
- Wong, Min Hao; Giraldo, Juan P.; Kwak, Seon-Yeong
- Nature Materials, Vol. 16, Issue 2
Cellular Image Analysis and Imaging by Flow Cytometry
journal, September 2007
- Basiji, David A.; Ortyn, William E.; Liang, Luchuan
- Clinics in Laboratory Medicine, Vol. 27, Issue 3
Cationic Au Nanoparticle Binding with Plasma Membrane-like Lipid Bilayers: Potential Mechanism for Spontaneous Permeation to Cells Revealed by Atomistic Simulations
journal, May 2014
- Heikkilä, Elena; Martinez-Seara, Hector; Gurtovenko, Andrey A.
- The Journal of Physical Chemistry C, Vol. 118, Issue 20
Enhancement of transfection by physical concentration of DNA at the cell surface
journal, August 2000
- Luo, Dan; Saltzman, W. Mark
- Nature Biotechnology, Vol. 18, Issue 8
Direct Synthesis of Nanoceria in Aqueous Polyhydroxyl Solutions
journal, October 2007
- Karakoti, A. S.; Kuchibhatla, Satyanarayana V. N. T.; Babu, K. Suresh
- The Journal of Physical Chemistry C, Vol. 111, Issue 46
High-velocity microprojectiles for delivering nucleic acids into living cells
journal, May 1987
- Klein, T. M.; Wolf, E. D.; Wu, R.
- Nature, Vol. 327, Issue 6117, p. 70-73
Cellular Uptake of Nanoparticles by Membrane Penetration: A Study Combining Confocal Microscopy with FTIR Spectroelectrochemistry
journal, January 2012
- Wang, Tiantian; Bai, Jing; Jiang, Xiue
- ACS Nano, Vol. 6, Issue 2
Dielectric spectroscopy of plant protoplasts
journal, December 1992
- Asami, Koji; Yamaguchi, Tohru
- Biophysical Journal, Vol. 63, Issue 6
Expression of genes transferred into monocot and dicot plant cells by electroporation.
journal, September 1985
- Fromm, M.; Taylor, L. P.; Walbot, V.
- Proceedings of the National Academy of Sciences, Vol. 82, Issue 17, p. 5824-5828
The thickness, composition and structure of some lipid bilayers and natural membranes
journal, September 1971
- Fettiplace, R.; Andrews, D. M.; Haydon, D. A.
- The Journal of Membrane Biology, Vol. 5, Issue 3
Highly efficient uptake of ultrafine mesoporous silica nanoparticles with excellent biocompatibility by Liriodendron hybrid suspension cells
journal, December 2012
- Xia, Bing; Dong, Chen; Zhang, WenYi
- Science China Life Sciences, Vol. 56, Issue 1
Cell Surface Area Regulation and Membrane Tension
journal, January 2001
- Morris, C. E.; Homann, U.
- The Journal of Membrane Biology, Vol. 179, Issue 2
Hybrid genes in the analysis of transformation conditions: I. Setting up a simple method for direct gene transfer in plant protoplasts
journal, January 1987
- Negrutiu, I.; Shillito, R.; Potrykus, I.
- Plant Molecular Biology, Vol. 8, Issue 5
Laurdan fluorescence spectroscopy in the thylakoid bilayer: The effect of violaxanthin to zeaxanthin conversion on the galactolipid dominated lipid environment
journal, January 2008
- Szilágyi, Anna; Selstam, Eva; Åkerlund, Hans-Erik
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 1
Application of Nanoparticle Antioxidants to Enable Hyperstable Chloroplasts for Solar Energy Harvesting
journal, March 2013
- Boghossian, Ardemis A.; Sen, Fatih; Gibbons, Brenna M.
- Advanced Energy Materials, Vol. 3, Issue 7
Transient gene expression in electroporated Solanum protoplasts
journal, November 1989
- Jones, Heddwyn; Ooms, Gert; Jones, Michael G. K.
- Plant Molecular Biology, Vol. 13, Issue 5
Mesoporous silica nanoparticles deliver DNA and chemicals into plants
journal, April 2007
- Torney, François; Trewyn, Brian G.; Lin, Victor S. -Y.
- Nature Nanotechnology, Vol. 2, Issue 5
Surface charge of protoplasts and their significance in cell-cell interaction
journal, January 1978
- Nagata, Toshiyuki; Melchers, Georg
- Planta, Vol. 142, Issue 2
Carbon Nanotubes Protect DNA Strands during Cellular Delivery
journal, October 2008
- Wu, Yanrong; Phillips, Joseph A.; Liu, Haipeng
- ACS Nano, Vol. 2, Issue 10
Urea-Hydroxyapatite Nanohybrids for Slow Release of Nitrogen
text, January 2017
- Kottegoda, N.; Sandaruwan, C.; Priyadarshana, G.
- Apollo - University of Cambridge Repository
Molecular Biology of the Plasma Membrane of Higher Plants
journal, October 1989
- Sussman, Michael R.; Harper, Jeffrey F.
- The Plant Cell, Vol. 1, Issue 10
Functionalized Carbon Nanotubes for Plasmid DNA Gene Delivery
journal, October 2004
- Pantarotto, Davide; Singh, Ravi; McCarthy, David
- Angewandte Chemie, Vol. 116, Issue 39
Chemical Basis of Interactions Between Engineered Nanoparticles and Biological Systems
text, January 2014
- Qingxin, Mu,; Bing, Yan,; Hongyu, Zhou,
- The University of North Carolina at Chapel Hill University Libraries
Surface patterning of carbon nanotubes can enhance their penetration through a phospholipid bilayer
text, January 2012
- Pogodin, Sergey; Slater, Nigel K. H.; Baulin, Vladimir A.
- arXiv
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- Lew, Tedrick Thomas Salim; Koman, Volodymyr B.; Gordiichuk, Pavlo
- Advanced Materials Technologies, Vol. 5, Issue 3
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journal, June 2019
- Mouhib, Mohammed; Antonucci, Alessandra; Reggente, Melania
- Nano Research, Vol. 12, Issue 9
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journal, February 2019
- Kwak, Seon-Yeong; Lew, Tedrick Thomas Salim; Sweeney, Connor J.
- Nature Nanotechnology, Vol. 14, Issue 5
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journal, February 2019
- Demirer, Gozde S.; Zhang, Huan; Matos, Juliana L.
- Nature Nanotechnology, Vol. 14, Issue 5