The impact of tomato fruits containing multi-walled carbon nanotube residues on human intestinal epithelial cell barrier function and intestinal microbiome composition
Abstract
Carbon nanomaterials (CNMs) can positively regulate seed germination and enhance plant growth. However, clarification of the impact of plant organs containing absorbed CNMs on animal and human health is a critical step of risk assessment for new nano–agro-technology. In this study, we have taken a comprehensive approach to studying the effect tomato fruits derived from plants exposed to multi-walled carbon nanotubes (CNTs) have on gastrointestinal epithelial barrier integrity and their impact on the human commensal intestinal microbiota using an in vitro cell culture and batch human fecal suspension models. The effects of CNTs on selected pure cultures of Salmonella enterica Typhimurium and Lactobacillus acidophilus were also evaluated. This study demonstrated that CNT-containing fruits or the corresponding residual level of pure CNTs (0.001 μg ml–1) was not sufficient to initiate a significant change in transepithelial resistance and on gene expression of the model T-84 human intestinal epithelial cells. However, at 10 μg ml–1 concentration CNTs were able to penetrate the cell membrane and change the gene expression profile of exposed cells. Furthermore, extracts from CNT-containing fruits had minimal to no effect on human intestinal microbiota as revealed by culture-based analysis and 16S rRNA sequencing.
- Authors:
-
- Univ. of Arkansas at Little Rock, Little Rock, AR (United States); National Center for Toxicological Research, Jefferson, AR (United States)
- National Center for Toxicological Research, Jefferson, AR (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Namik Kemal Univ., Corlu-Tekirdag (Turkey)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Arkansas at Little Rock, Little Rock, AR (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1510589
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nanoscale
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 8; Journal ID: ISSN 2040-3364
- Publisher:
- Royal Society of Chemistry
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES
Citation Formats
Lahiani, Mohamed H., Khare, Sangeeta, Cerniglia, Carl E., Boy, Ramiz, Ivanov, Ilia N., and Khodakovskaya, Mariya. The impact of tomato fruits containing multi-walled carbon nanotube residues on human intestinal epithelial cell barrier function and intestinal microbiome composition. United States: N. p., 2019.
Web. doi:10.1039/C8NR08604D.
Lahiani, Mohamed H., Khare, Sangeeta, Cerniglia, Carl E., Boy, Ramiz, Ivanov, Ilia N., & Khodakovskaya, Mariya. The impact of tomato fruits containing multi-walled carbon nanotube residues on human intestinal epithelial cell barrier function and intestinal microbiome composition. United States. https://doi.org/10.1039/C8NR08604D
Lahiani, Mohamed H., Khare, Sangeeta, Cerniglia, Carl E., Boy, Ramiz, Ivanov, Ilia N., and Khodakovskaya, Mariya. Tue .
"The impact of tomato fruits containing multi-walled carbon nanotube residues on human intestinal epithelial cell barrier function and intestinal microbiome composition". United States. https://doi.org/10.1039/C8NR08604D. https://www.osti.gov/servlets/purl/1510589.
@article{osti_1510589,
title = {The impact of tomato fruits containing multi-walled carbon nanotube residues on human intestinal epithelial cell barrier function and intestinal microbiome composition},
author = {Lahiani, Mohamed H. and Khare, Sangeeta and Cerniglia, Carl E. and Boy, Ramiz and Ivanov, Ilia N. and Khodakovskaya, Mariya},
abstractNote = {Carbon nanomaterials (CNMs) can positively regulate seed germination and enhance plant growth. However, clarification of the impact of plant organs containing absorbed CNMs on animal and human health is a critical step of risk assessment for new nano–agro-technology. In this study, we have taken a comprehensive approach to studying the effect tomato fruits derived from plants exposed to multi-walled carbon nanotubes (CNTs) have on gastrointestinal epithelial barrier integrity and their impact on the human commensal intestinal microbiota using an in vitro cell culture and batch human fecal suspension models. The effects of CNTs on selected pure cultures of Salmonella enterica Typhimurium and Lactobacillus acidophilus were also evaluated. This study demonstrated that CNT-containing fruits or the corresponding residual level of pure CNTs (0.001 μg ml–1) was not sufficient to initiate a significant change in transepithelial resistance and on gene expression of the model T-84 human intestinal epithelial cells. However, at 10 μg ml–1 concentration CNTs were able to penetrate the cell membrane and change the gene expression profile of exposed cells. Furthermore, extracts from CNT-containing fruits had minimal to no effect on human intestinal microbiota as revealed by culture-based analysis and 16S rRNA sequencing.},
doi = {10.1039/C8NR08604D},
journal = {Nanoscale},
number = 8,
volume = 11,
place = {United States},
year = {Tue Jan 22 00:00:00 EST 2019},
month = {Tue Jan 22 00:00:00 EST 2019}
}
Web of Science
Works referenced in this record:
Mapping internal structure of coal by confocal micro-Raman spectroscopy and scanning microwave microscopy
journal, June 2014
- Tselev, Alexander; Ivanov, Ilia N.; Lavrik, Nickolay V.
- Fuel, Vol. 126
Quercetin Enhances Intestinal Barrier Function through the Assembly of Zonnula Occludens-2, Occludin, and Claudin-1 and the Expression of Claudin-4 in Caco-2 Cells
journal, March 2009
- Suzuki, Takuya; Hara, Hiroshi
- The Journal of Nutrition, Vol. 139, Issue 5
Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism
journal, March 2016
- Morrison, Douglas J.; Preston, Tom
- Gut Microbes, Vol. 7, Issue 3
Differential Effects of Flavonoids on Barrier Integrity in Human Intestinal Caco-2 Cells
journal, April 2012
- Noda, Sakino; Tanabe, Soichi; Suzuki, Takuya
- Journal of Agricultural and Food Chemistry, Vol. 60, Issue 18
Comparison of Translocation Rates of Various Indigenous Bacteria from the Gastrointestinal Tract to the Mesenteric Lymph Node
journal, May 1988
- Steffen, E. K.; Berg, R. D.; Deitch, E. A.
- Journal of Infectious Diseases, Vol. 157, Issue 5
Nanoparticle uptake by the oral route: Fulfilling its potential?
journal, March 2005
- Florence, Alexander T.
- Drug Discovery Today: Technologies, Vol. 2, Issue 1
Carbon nanotubes as carriers of Panax ginseng metabolites and enhancers of ginsenosides Rb1 and Rg1 anti-cancer activity
journal, November 2016
- Lahiani, Mohamed H.; Eassa, Souzan; Parnell, Charlette
- Nanotechnology, Vol. 28, Issue 1
Inactivation of Bacterial Pathogens by Carbon Nanotubes in Suspensions
journal, March 2009
- Arias, L. Renea; Yang, Liju
- Langmuir, Vol. 25, Issue 5
Graphene and carbon nanotubes activate different cell surface receptors on macrophages before and after deactivation of endotoxins: Activation of macrophages before and after deactivation of endotoxin
journal, May 2017
- Lahiani, Mohamed H.; Gokulan, Kuppan; Williams, Katherine
- Journal of Applied Toxicology, Vol. 37, Issue 11
Nod2 is required for the regulation of commensal microbiota in the intestine
journal, September 2009
- Petnicki-Ocwieja, Tanja; Hrncir, Tomas; Liu, Yuen-Joyce
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 37
Multiwalled Carbon Nanotubes Dramatically Affect the Fruit Metabolome of Exposed Tomato Plants
journal, September 2017
- McGehee, Diamond L.; Lahiani, Mohamed H.; Irin, Fahmida
- ACS Applied Materials & Interfaces, Vol. 9, Issue 38
Biological Uptake and Depuration of Carbon Nanotubes by Daphnia magna
journal, April 2009
- Petersen, Elijah J.; Akkanen, Jarkko; Kukkonen, Jussi V. K.
- Environmental Science & Technology, Vol. 43, Issue 8
Human Health Risk of Ingested Nanoparticles That Are Added as Multifunctional Agents to Paints: an In Vitro Study
journal, December 2013
- Kaiser, Jean-Pierre; Roesslein, Matthias; Diener, Liliane
- PLoS ONE, Vol. 8, Issue 12
Methods to Examine Tight Junction Physiology in Cancer Stem Cells: TEER, Paracellular Permeability, and Dilution Potential Measurements
journal, December 2011
- Buchert, Michael; Turksen, Kursad; Hollande, Frédéric
- Stem Cell Reviews and Reports, Vol. 8, Issue 3
Non-functionalized multi-walled carbon nanotubes alter the paracellular permeability of human airway epithelial cells
journal, May 2008
- Rotoli, Bianca Maria; Bussolati, Ovidio; Bianchi, Massimiliano G.
- Toxicology Letters, Vol. 178, Issue 2
Complex genetic, photothermal, and photoacoustic analysis of nanoparticle-plant interactions
journal, December 2010
- Khodakovskaya, M. V.; de Silva, K.; Nedosekin, D. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 3
Antibacterial Effects of Carbon Nanotubes: Size Does Matter!
journal, July 2008
- Kang, Seoktae; Herzberg, Moshe; Rodrigues, Debora F.
- Langmuir, Vol. 24, Issue 13
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
Diversity of the Human Intestinal Microbial Flora
journal, June 2005
- Eckburg, P. B.
- Science, Vol. 308, Issue 5728
Interaction of Nanoparticles with Edible Plants and Their Possible Implications in the Food Chain
journal, April 2011
- Rico, Cyren M.; Majumdar, Sanghamitra; Duarte-Gardea, Maria
- Journal of Agricultural and Food Chemistry, Vol. 59, Issue 8
Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine
journal, February 2006
- Ley, Ruth E.; Peterson, Daniel A.; Gordon, Jeffrey I.
- Cell, Vol. 124, Issue 4
Nanotoxicology: An Emerging Discipline Evolving from Studies of Ultrafine Particles
journal, July 2005
- Oberdörster, Günter; Oberdörster, Eva; Oberdörster, Jan
- Environmental Health Perspectives, Vol. 113, Issue 7
Epithelial Tight Junctions in Intestinal Inflammation
journal, May 2009
- Schulzke, Joerg D.; Ploeger, Svenja; Amasheh, Maren
- Annals of the New York Academy of Sciences, Vol. 1165, Issue 1
Butyric acid-producing anaerobic bacteria as a novel probiotic treatment approach for inflammatory bowel disease
journal, November 2009
- Van Immerseel, F.; Ducatelle, R.; De Vos, M.
- Journal of Medical Microbiology, Vol. 59, Issue 2
Nanoparticles - A review
journal, July 2007
- Mohanraj, V. J.; Chen, Y.
- Tropical Journal of Pharmaceutical Research, Vol. 5, Issue 1
The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism
journal, July 2013
- den Besten, Gijs; van Eunen, Karen; Groen, Albert K.
- Journal of Lipid Research, Vol. 54, Issue 9
Sublethal toxicity of nano-titanium dioxide and carbon nanotubes in a sediment dwelling marine polychaete
journal, May 2010
- Galloway, Tamara; Lewis, Ceri; Dolciotti, Ida
- Environmental Pollution, Vol. 158, Issue 5
Investigating the effects of functionalized carbon nanotubes on reproduction and development in Drosophila melanogaster and CD-1 mice
journal, December 2011
- Philbrook, Nicola A.; Walker, Virginia K.; Afrooz, A. R. M. Nabiul
- Reproductive Toxicology, Vol. 32, Issue 4
A protocol for the culture and differentiation of highly polarized human retinal pigment epithelial cells
journal, April 2009
- Sonoda, Shozo; Spee, Christine; Barron, Ernesto
- Nature Protocols, Vol. 4, Issue 5
Antimicrobial Activity of Single-Walled Carbon Nanotubes: Length Effect
journal, October 2010
- Yang, Cheenou; Mamouni, Jaouad; Tang, Yongan
- Langmuir, Vol. 26, Issue 20
Broad-Spectrum Antibacterial Activity of Carbon Nanotubes to Human Gut Bacteria
journal, March 2013
- Chen, Hanqing; Wang, Bing; Gao, Di
- Small, Vol. 9, Issue 16
A Genomic View of the Human-Bacteroides thetaiotaomicron Symbiosis
journal, March 2003
- Xu, J.
- Science, Vol. 299, Issue 5615
Nanoparticles as carriers for oral peptide absorption: Studies on particle uptake and fate
journal, September 1995
- Florence, Alexander T.; Hillery, Anya M.; Hussain, Nasir
- Journal of Controlled Release, Vol. 36, Issue 1-2
DAVID-WS: a stateful web service to facilitate gene/protein list analysis
journal, April 2012
- Jiao, X.; Sherman, B. T.; Huang, D. W.
- Bioinformatics, Vol. 28, Issue 13
Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells
journal, February 1993
- Gottlieb, T. A.
- The Journal of Cell Biology, Vol. 120, Issue 3
Assessing the pulmonary toxicity of single-walled carbon nanohorns
journal, January 2007
- Lynch, Rachel M.; Voy, Brynn H.; Glass, Dana F.
- Nanotoxicology, Vol. 1, Issue 2
Colonization of Tomato Plants by Salmonella enterica Is Cultivar Dependent, and Type 1 Trichomes Are Preferred Colonization Sites
journal, November 2010
- Barak, Jeri D.; Kramer, Lara C.; Hao, Ling-yun
- Applied and Environmental Microbiology, Vol. 77, Issue 2
Origin and fate of dietary nanoparticles and microparticles in the gastrointestinal tract
journal, May 2010
- Powell, Jonathan J.; Faria, Nuno; Thomas-McKay, Emma
- Journal of Autoimmunity, Vol. 34, Issue 3
Sex Differences in the Gut Microbiome Drive Hormone-Dependent Regulation of Autoimmunity
journal, January 2013
- Markle, J. G. M.; Frank, D. N.; Mortin-Toth, S.
- Science, Vol. 339, Issue 6123
Impact of Carbon Nanotube Exposure to Seeds of Valuable Crops
journal, July 2013
- Lahiani, Mohamed H.; Dervishi, Enkeleda; Chen, Jihua
- ACS Applied Materials & Interfaces, Vol. 5, Issue 16
Dynamics of Tight and Adherens Junctions Under EGTA Treatment
journal, July 2002
- Rothen-Rutishauser, B.; Riesen, F. K.; Braun, A.
- Journal of Membrane Biology, Vol. 188, Issue 2
The Ussing type chamber model to study the intestinal transport and modulation of specific tight-junction genes using a colonic cell line
journal, October 2009
- Bergmann, Hannah; Rogoll, Dorothee; Scheppach, Wolfgang
- Molecular Nutrition & Food Research, Vol. 53, Issue 10
Role of the gut microbiota in defining human health
journal, April 2010
- Fujimura, Kei E.; Slusher, Nicole A.; Cabana, Michael D.
- Expert Review of Anti-infective Therapy, Vol. 8, Issue 4
Identifying contact-mediated, localized toxic effects of MWCNT aggregates on epithelial monolayers: a single-cell monitoring toxicity assay
journal, April 2014
- Rotoli, Bianca M.; Gatti, Rita; Movia, Dania
- Nanotoxicology, Vol. 9, Issue 2
Oxidatively Damaged DNA in Rats Exposed by Oral Gavage to C 60 Fullerenes and Single-Walled Carbon Nanotubes
journal, May 2009
- Folkmann, Janne K.; Risom, Lotte; Jacobsen, Nicklas R.
- Environmental Health Perspectives, Vol. 117, Issue 5
Interaction between Food Substances and the Intestinal Epithelium
journal, February 2010
- Shimizu, Makoto
- Bioscience, Biotechnology, and Biochemistry, Vol. 74, Issue 2
Kaempferol Enhances Intestinal Barrier Function through the Cytoskeletal Association and Expression of Tight Junction Proteins in Caco-2 Cells
journal, November 2010
- Suzuki, Takuya; Tanabe, Soichi; Hara, Hiroshi
- The Journal of Nutrition, Vol. 141, Issue 1
The intestine and its microflora are partners for the protection of the host: report on the Danone Symposium “The Intelligent Intestine,” held in Paris, June 14, 2002
journal, October 2003
- Bourlioux, Pierre; Koletzko, Berthold; Guarner, Francisco
- The American Journal of Clinical Nutrition, Vol. 78, Issue 4
Nanoparticles in the environment: assessment using the causal diagram approach
journal, January 2012
- Smita, Suchi; Gupta, Shailendra K.; Bartonova, Alena
- Environmental Health, Vol. 11, Issue Suppl 1
ACS Select on Nanotechnology in Food and Agriculture: A Perspective on Implications and Applications
journal, January 2014
- Chen, Hongda; Seiber, James N.; Hotze, Matt
- Journal of Agricultural and Food Chemistry, Vol. 62, Issue 6
Interaction of carbon nanohorns with plants: Uptake and biological effects
journal, January 2015
- Lahiani, Mohamed H.; Chen, Jihua; Irin, Fahmida
- Carbon, Vol. 81
Roles of intestinal epithelial cells in the maintenance of gut homeostasis
journal, May 2017
- Okumura, Ryu; Takeda, Kiyoshi
- Experimental & Molecular Medicine, Vol. 49, Issue 5
Role of SPI-1 Secreted Effectors in Acute Bovine Response to Salmonella enterica Serovar Typhimurium: A Systems Biology Analysis Approach
journal, November 2011
- Lawhon, Sara D.; Khare, Sangeeta; Rossetti, Carlos A.
- PLoS ONE, Vol. 6, Issue 11
Comparative study of plant responses to carbon-based nanomaterials with different morphologies
journal, May 2016
- Lahiani, Mohamed H.; Dervishi, Enkeleda; Ivanov, Ilia
- Nanotechnology, Vol. 27, Issue 26
Biodegradation of Carbon Nanotubes, Graphene, and Their Derivatives
journal, September 2017
- Chen, Ming; Qin, Xiaosheng; Zeng, Guangming
- Trends in Biotechnology, Vol. 35, Issue 9
Probiotic modulation of symbiotic gut microbial–host metabolic interactions in a humanized microbiome mouse model
journal, January 2008
- Martin, Francois‐Pierre J.; Wang, Yulan; Sprenger, Norbert
- Molecular Systems Biology, Vol. 4, Issue 1