Surface Patterning of Carbon Nanotubes Can Enhance Their Penetration through a Phospholipid Bilayer
Abstract

Nanotube patterning may occur naturally upon the spontaneous self-assembly of biomolecules onto the surface of single-walled carbon nanotubes (SWNTs). It results in periodically alternating bands of surface properties, ranging from relatively hydrophilic to hydrophobic, along the axis of the nanotube. Single-chain mean field (SCMF) theory has been used to estimate the free energy of systems in which a surface patterned nanotube penetrates a phospholipid bilayer. In contrast to unpatterned nanotubes with uniform surface properties, certain patterned nanotubes have been identified that display a relatively low and approximately constant system free energy (<±10 kT) as the nanotube traverses through the bilayer. These observations support the hypothesis that the spontaneous self-assembly of biomolecules on the surface of SWNTs may facilitate nanotube transduction through cell membranes.
Cited By
This article is cited by 48 publications.
- Xiaokai Xu, Rongxin Shen, Luoqi Mo, Xianfeng Yang, Xing Chen, Haozhe Wang, Yadong Li, Chaofan Hu, Bingfu Lei, Xuejie Zhang, Qiuqiang Zhan, Xingcai Zhang, Yingliang Liu, Jianle Zhuang. Improving Plant Photosynthesis through Light-Harvesting Upconversion Nanoparticles. ACS Nano 2022, 16 (11) , 18027-18037. https://doi.org/10.1021/acsnano.2c02162
- Astrid Avellan, Jie Yun, Bruno P. Morais, Emma T. Clement, Sonia M. Rodrigues, Gregory V. Lowry. Critical Review: Role of Inorganic Nanoparticle Properties on Their Foliar Uptake and in Planta Translocation. Environmental Science & Technology 2021, 55 (20) , 13417-13431. https://doi.org/10.1021/acs.est.1c00178
- Astrid Avellan, Jie Yun, Yilin Zhang, Eleanor Spielman-Sun, Jason M. Unrine, Juergen Thieme, Jieran Li, Enzo Lombi, Garret Bland, Gregory V. Lowry. Nanoparticle Size and Coating Chemistry Control Foliar Uptake Pathways, Translocation, and Leaf-to-Rhizosphere Transport in Wheat. ACS Nano 2019, 13 (5) , 5291-5305. https://doi.org/10.1021/acsnano.8b09781
- Shinji Kihara, Nadine J. van der Heijden, Chris K. Seal, Jitendra P. Mata, Andrew E. Whitten, Ingo Köper, Duncan J. McGillivray. Soft and Hard Interactions between Polystyrene Nanoplastics and Human Serum Albumin Protein Corona. Bioconjugate Chemistry 2019, 30 (4) , 1067-1076. https://doi.org/10.1021/acs.bioconjchem.9b00015
- Yachong Guo, Marco Werner, Ralf Seemann, Vladimir A. Baulin, Jean-Baptiste Fleury. Tension-Induced Translocation of an Ultrashort Carbon Nanotube through a Phospholipid Bilayer. ACS Nano 2018, 12 (12) , 12042-12049. https://doi.org/10.1021/acsnano.8b04657
- Anil Kumar Sahoo, Subbarao Kanchi, Taraknath Mandal, Chandan Dasgupta, and Prabal K. Maiti . Translocation of Bioactive Molecules through Carbon Nanotubes Embedded in the Lipid Membrane. ACS Applied Materials & Interfaces 2018, 10 (7) , 6168-6179. https://doi.org/10.1021/acsami.7b18498
- Christopher J. Serpell, Kostas Kostarelos, and Benjamin G. Davis . Can Carbon Nanotubes Deliver on Their Promise in Biology? Harnessing Unique Properties for Unparalleled Applications. ACS Central Science 2016, 2 (4) , 190-200. https://doi.org/10.1021/acscentsci.6b00005
- Reid C. Van Lehn and Alfredo Alexander-Katz . Membrane-Embedded Nanoparticles Induce Lipid Rearrangements Similar to Those Exhibited by Biological Membrane Proteins. The Journal of Physical Chemistry B 2014, 118 (44) , 12586-12598. https://doi.org/10.1021/jp506239p
- Paraskevi Gkeka, Lev Sarkisov, and Panagiotis Angelikopoulos . Homogeneous Hydrophobic–Hydrophilic Surface Patterns Enhance Permeation of Nanoparticles through Lipid Membranes. The Journal of Physical Chemistry Letters 2013, 4 (11) , 1907-1912. https://doi.org/10.1021/jz400679z
- Xiangang Hu and Qixing Zhou . Health and Ecosystem Risks of Graphene. Chemical Reviews 2013, 113 (5) , 3815-3835. https://doi.org/10.1021/cr300045n
- Elena Heister, Eric W. Brunner, Gregg R. Dieckmann, Izabela Jurewicz, and Alan B. Dalton . Are Carbon Nanotubes a Natural Solution? Applications in Biology and Medicine. ACS Applied Materials & Interfaces 2013, 5 (6) , 1870-1891. https://doi.org/10.1021/am302902d
- Sergey Pogodin, Marco Werner, Jens-Uwe Sommer, and Vladimir A. Baulin . Nanoparticle-Induced Permeability of Lipid Membranes. ACS Nano 2012, 6 (12) , 10555-10561. https://doi.org/10.1021/nn3028858
- R. Parthasarathi, N. R. Tummala, and A. Striolo . Embedded Single-Walled Carbon Nanotubes Locally Perturb DOPC Phospholipid Bilayers. The Journal of Physical Chemistry B 2012, 116 (42) , 12769-12782. https://doi.org/10.1021/jp306299x
- Sergey Pogodin, Nigel K. H. Slater, and Vladimir A. Baulin . Biomolecule Surface Patterning May Enhance Membrane Association. ACS Nano 2012, 6 (2) , 1308-1313. https://doi.org/10.1021/nn204736b
- Silvia H. De Paoli Lacerda, Jana Semberova, Karel Holada, Olga Simakova, Steven D. Hudson, and Jan Simak . Carbon Nanotubes Activate Store-Operated Calcium Entry in Human Blood Platelets. ACS Nano 2011, 5 (7) , 5808-5813. https://doi.org/10.1021/nn2015369
- Konstantin Pikula, Seyed Ali Johari, Ralph Santos-Oliveira, Kirill Golokhvast. The Comparative Toxic Impact Assessment of Carbon Nanotubes, Fullerene, Graphene, and Graphene Oxide on Marine Microalgae Porphyridium purpureum. Toxics 2023, 11 (6) , 491. https://doi.org/10.3390/toxics11060491
- Lok R. Pokhrel, Zachary L. Jacobs, Dmitriy Dikin, Shaw M. Akula. Five nanometer size highly positive silver nanoparticles are bactericidal targeting cell wall and adherent fimbriae expression. Scientific Reports 2022, 12 (1) https://doi.org/10.1038/s41598-022-10778-9
- Boyang Hu, Ruijie Liu, Qingyue Liu, Zi'an Lin, Yiwei Shi, Jun Li, Lijun Wang, Longjie Li, Xianjin Xiao, Yuzhou Wu. Engineering surface patterns on nanoparticles: new insights into nano-bio interactions. Journal of Materials Chemistry B 2022, 10 (14) , 2357-2383. https://doi.org/10.1039/D1TB02549J
- Yun Hao Feng, Bo Zhi Chen, Wen Min Fei, Yong Cui, Can Yang Zhang, Xin Dong Guo. Mechanism studies on the cellular internalization of nanoparticles using computer simulations: A review. AIChE Journal 2022, 68 (2) https://doi.org/10.1002/aic.17507
- Shinji Kihara, Ingo Köper, Jitendra P. Mata, Duncan J. McGillivray. Reviewing nanoplastic toxicology: It's an interface problem. Advances in Colloid and Interface Science 2021, 288 , 102337. https://doi.org/10.1016/j.cis.2020.102337
- Denver P. Linklater, Vladimir A. Baulin, Saulius Juodkazis, Russell J. Crawford, Paul Stoodley, Elena P. Ivanova. Mechano-bactericidal actions of nanostructured surfaces. Nature Reviews Microbiology 2021, 19 (1) , 8-22. https://doi.org/10.1038/s41579-020-0414-z
- Alexey A. Tsukanov, Olga Vasiljeva. Nanomaterials Interaction with Cell Membranes: Computer Simulation Studies. 2021, 189-210. https://doi.org/10.1007/978-3-030-60124-9_9
- Cui Song, Feng Li, Shuang Wang, Jianghua Wang, Wei Wei, Guanghui Ma. Recent Advances in Particulate Adjuvants for Cancer Vaccination. Advanced Therapeutics 2020, 3 (5) https://doi.org/10.1002/adtp.201900115
- Rakesh Gupta, Yogesh Badhe, Samir Mitragotri, Beena Rai. Permeation of nanoparticles across the intestinal lipid membrane: dependence on shape and surface chemistry studied through molecular simulations. Nanoscale 2020, 12 (11) , 6318-6333. https://doi.org/10.1039/C9NR09947F
- Suman Saurabh, Ponnurengam Malliappan Sivakumar, Venkatesan Perumal, Arezoo Khosravi, Abimanyu Sugumaran, Veluchamy Prabhawathi. Molecular Dynamics Simulations in Drug Discovery and Drug Delivery. 2020, 275-301. https://doi.org/10.1007/978-3-030-36260-7_10
- Norazlina Mohamad Yatim, Azizah Shaaban, Mohd Fairuz Dimin, Noraiham Mohamad, Faridah Yusof. Urea functionalized multiwalled carbon nanotubes as efficient nitrogen delivery system for rice. Advances in Natural Sciences: Nanoscience and Nanotechnology 2019, 10 (1) , 015011. https://doi.org/10.1088/2043-6254/ab0881
- Xinghua Shi, Falin Tian. Multiscale Modeling and Simulation of Nano‐Carriers Delivery through Biological Barriers—A Review. Advanced Theory and Simulations 2019, 2 (1) https://doi.org/10.1002/adts.201800105
- Tedrick Thomas Salim Lew, Min Hao Wong, Seon‐Yeong Kwak, Rosalie Sinclair, Volodymyr B. Koman, Michael S. Strano. Rational Design Principles for the Transport and Subcellular Distribution of Nanomaterials into Plant Protoplasts. Small 2018, 14 (44) https://doi.org/10.1002/smll.201802086
- François Sicard, Alberto Striolo. Computational simulations for particles at interfaces. 2018, 167-200. https://doi.org/10.1016/B978-0-12-804069-0.00006-X
- W Wang, R Yang, F Zhang, B Yuan, K Yang, Y Ma. Partner-facilitating transmembrane penetration of nanoparticles: a biological test in silico. Nanoscale 2018, 10 (24) , 11670-11678. https://doi.org/10.1039/C8NR01204K
- Zuoheng Zhang, Xubo Lin, Ning Gu. Effects of temperature and PEG grafting density on the translocation of PEGylated nanoparticles across asymmetric lipid membrane. Colloids and Surfaces B: Biointerfaces 2017, 160 , 92-100. https://doi.org/10.1016/j.colsurfb.2017.09.013
- Tongtao Yue, Yan Xu, Shixin Li, Zhen Luo, Xianren Zhang, Fang Huang. Surface patterning of single-walled carbon nanotubes enhances their perturbation on a pulmonary surfactant monolayer: frustrated translocation and bilayer vesiculation. RSC Advances 2017, 7 (34) , 20851-20864. https://doi.org/10.1039/C7RA01392B
- Yachong Guo, Emmanuel Terazzi, Ralf Seemann, Jean Baptiste Fleury, Vladimir A. Baulin. Direct proof of spontaneous translocation of lipid-covered hydrophobic nanoparticles through a phospholipid bilayer. Science Advances 2016, 2 (11) https://doi.org/10.1126/sciadv.1600261
- Xiangang Hu, Anqi Sun, Li Mu, Qixing Zhou. Separation and analysis of carbon nanomaterials in complex matrix. TrAC Trends in Analytical Chemistry 2016, 80 , 416-428. https://doi.org/10.1016/j.trac.2016.03.024
- Z. Ge, Y. Wang. Computer Simulation and Modeling Techniques in the Study of Nanoparticle-Membrane Interactions. 2016, 159-200. https://doi.org/10.1016/bs.arcc.2016.05.001
- Cristina M. Sabliov, Dorel Moldovan, Brian Novak, Toni Borel, Meocha Whaley. Cellular fate of delivery systems and entrapped bioactives. 2015, 35-51. https://doi.org/10.1002/9781118462157.ch3
- Hong-ming Ding, Yu-qiang Ma. Theoretical and Computational Investigations of Nanoparticle-Biomembrane Interactions in Cellular Delivery. Small 2015, 11 (9-10) , 1055-1071. https://doi.org/10.1002/smll.201401943
- FaLin Tian, TongTao Yue, Ye Li, XianRen Zhang. Computer simulation studies on the interactions between nanoparticles and cell membrane. Science China Chemistry 2014, 57 (12) , 1662-1671. https://doi.org/10.1007/s11426-014-5231-7
- Falin Tian, Xianren Zhang, Wei Dong. How hydrophobic nanoparticles aggregate in the interior of membranes: A computer simulation. Physical Review E 2014, 90 (5) https://doi.org/10.1103/PhysRevE.90.052701
- Juan Pablo Giraldo, Markita P. Landry, Sean M. Faltermeier, Thomas P. McNicholas, Nicole M. Iverson, Ardemis A. Boghossian, Nigel F. Reuel, Andrew J. Hilmer, Fatih Sen, Jacqueline A. Brew, Michael S. Strano. Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nature Materials 2014, 13 (4) , 400-408. https://doi.org/10.1038/nmat3890
- A. Djordjevic, R. Injac, D. Jovic, J. Mrdjanovic, M. Seke. Bioimpact of Carbon Nanomaterials. 2014, 193-271. https://doi.org/10.1002/9781118895399.ch6
- Lili Li, Rui Lin, Hua He, Meiling Sun, Li Jiang, Mengmeng Gao. Interaction of amidated single-walled carbon nanotubes with protein by multiple spectroscopic methods. Journal of Luminescence 2014, 145 , 125-131. https://doi.org/10.1016/j.jlumin.2013.07.008
- Thilini Silva, Lok R. Pokhrel, Brajesh Dubey, Thabet M. Tolaymat, Kurt J. Maier, Xuefeng Liu. Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: Comparison between general linear model-predicted and observed toxicity. Science of The Total Environment 2014, 468-469 , 968-976. https://doi.org/10.1016/j.scitotenv.2013.09.006
- Chiara Fabbro, Tatiana Da Ros, Maurizio Prato. Carbon nanotube derivatives as anticancer drug delivery systems. 2013, 469-486. https://doi.org/10.1002/9781118354377.ch21
- Zhen-lu Li, Hong-ming Ding, Yu-qiang Ma. Translocation of polyarginines and conjugated nanoparticles across asymmetric membranes. Soft Matter 2013, 9 (4) , 1281-1286. https://doi.org/10.1039/C2SM26519B
- Qing Liang. Penetration of polymer-grafted nanoparticles through a lipid bilayer. Soft Matter 2013, 9 (23) , 5594. https://doi.org/10.1039/c3sm27254k
- Hong-ming Ding, Yu-qiang Ma. Interactions between Janus particles and membranes. Nanoscale 2012, 4 (4) , 1116-1122. https://doi.org/10.1039/C1NR11425E
- Kai Yang, Yu-qiang Ma. Wrapping and Internalization of Nanoparticles by Lipid Bilayers: a Computer Simulation Study. Australian Journal of Chemistry 2011, 64 (7) , 894. https://doi.org/10.1071/CH11053