A micro-sized model for the in vivo study of nanoparticle toxicity: what has Caenorhabditis elegans taught us?

Jinhee Choi; Olga V. Tsyusko; Jason M. Unrine; Nivedita Chatterjee; Jeong-Min Ahn; Xinyu Yang; B. Lila Thornton; Ian T. Ryde; Daniel Starnes; Joel N. Meyer

doi:10.1071/EN13187

RESEARCH FRONT

A micro-sized model for the in vivo study of nanoparticle toxicity: what has Caenorhabditis elegans taught us?

Jinhee Choi ^A ^E , Olga V. Tsyusko ^B ^C ^E , Jason M. Unrine ^B ^C , Nivedita Chatterjee ^A , Jeong-Min Ahn ^A , Xinyu Yang ^C ^D , B. Lila Thornton ^C ^D , Ian T. Ryde ^C ^D , Daniel Starnes ^B ^C and Joel N. Meyer ^C ^D ^E

+ Author Affiliations

- Author Affiliations

^A School of Environmental Engineering and Graduate School of Energy and Environmental System Engineering, University of Seoul, Seoul 130-743, South Korea.

^B Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546, USA.

^C The Center for Environmental Implications of Nanotechnology, Duke University, Durham, NC 27708, USA.

^D Nicholas School of the Environment and Center for the Environmental Implications of Nanotechnology, Duke University, Durham, NC 27708-0328, USA.

^E Corresponding authors. Email: jinhchoi@uos.ac.kr; olga.tsyusko@uky.edu; jnm4@duke.edu

Dr Choi received her B.Sc. (1991) and Master's in Environmental Planning (1993) from Seoul National University and moved to France for study in graduate school. She earned a Ph.D. in Environmental Toxicology from University of Paris XI (Paris-Sud) in 1998 and then carried out her postdoctoral research at the College of Medicine of Seoul National University from 1999 to 2001. She serves as a professor of the School of Environmental Engineering at the University of Seoul from 2002. Her laboratory studies the mechanism of eco- and human toxicity of various environmental contaminants, including nanomaterials, using systems toxicology approaches.

Olga Tsyusko is Assistant Research Professor at the Department of Plant and Soil Sciences at the University of Kentucky. She received her B.Sc. in Biology from Uzhgorod National University in Ukraine and her Ph.D. in Toxicology at the University of Georgia in the United States. Her postdoctoral training was completed at the Savannah River Ecology Laboratory where she later worked as Molecular Biologist. The focus of her research is on environmental toxicogenomics, examining effects and toxicity mechanisms of engineered nanomaterials in soil invertebrates and plants. She is a member of the Center for Environmental Implications of NanoTechnology.

Jason M. Unrine is Assistant Professor in the Department of Plant and Soil Sciences at the University of Kentucky. Prior to this he served as a research scientist at the University of Georgia Savannah River Ecology Laboratory where he also undertook his doctoral and postdoctoral training in toxicology and environmental analytical chemistry. He earned his B.Sc. in Biology from Antioch College. His research focuses on understanding the fate, transport, bioavailability and adverse ecological effects of trace-elements and metal-based manufactured nanomaterials. He is a member of the steering committee of the Center for Environmental Implications of NanoTechnology (CEINT).

Dr Chatterjee received her B.Sc. (2001) and M.Sc. (2003) from University of Calcutta and moved to China to peruse her Ph.D. with the fellowship of India Government and Chinese scholarship council. She received her Ph.D. in Environmental Science (Environmental Toxicology) from China University of Geosciences, Wuhan, in 2009. Currently, she is a postdoctoral research fellow in Dr Choi's lab at the University of Seoul. She is engaged in the study of mechanisms of comparative (human and C. elegans) toxicity of environmental contaminants, specifically nanomaterials.

Ms J.-M. Ahn received her B.Sc. (2010) from University of Incheon and her M.Sc. (2013) from University of Seoul. For her M.Sc. she studied toxicity mechanisms of various nanomaterials in C. elegans. Since 2013, she has worked at the Risk Assessment Division in the Korean National Institute of Environmental Research.

Xinyu Yang received her Bachelors degree in Environmental Engineering from Shanghai Jiaotong University in July 2007, and then got her Master's degree in Zoology with Jim Oris from Miami University in July 2009. She received her Ph.D. in Environmental Toxicology from Duke University in 2014. Most of her Ph.D. work was focussed on the mechanistic toxicology of silver nanoparticles both in laboratory and environmental settings. She has published nine peer-reviewed journal articles in the field of environmental studies. With strong passion to apply her expertise in industrial settings, she currently joined Nalco-Ecolab as a regulatory specialist in Naperville, IL.

Lila Thornton graduated from Duke University in 2013 with Bachelor degrees in Biology and Environmental Science. She is currently an independent contractor for the US Environmental Protection Agency as part of the Chemical Safety for Sustainability National Research Program. Ms Thornton plans on pursuing a higher degree in the field of toxicology.

Ian Ryde received his Bachelor of Science in Biology from Bowling Green State University in Ohio in 2002 and then moved to the Raleigh–Durham area and started work in Dr Ted Slotkin's lab at Duke University in 2005. After 5 years in the Slotkin Lab, Ian moved on to Dr Joel Meyer's laboratory at Duke, where he has been for over 4 years now, working as a Laboratory Analyst II. He started working with the nematode C. elegans and on projects involving mitochondrial DNA damage and its effects on things such as mtDNA copy number, mRNA expression and neurodegeneration.

Daniel Starnes is a Ph.D. candidate in Integrated Plant and Soil Sciences within the Department of Plant and Soil Sciences at the University of Kentucky. He received his B.Sc. in Agriculture (2006) and M.Sc. in Biology (2009) from Western Kentucky University, where his research focussed on Environmental Phytoremediation and Phyto-Nanotechnology. His current research focuses on the environmental implications of manufactured nanoparticles on terrestrial ecosystems, specifically soil invertebrates.

Dr Meyer received his B.Sc. from Juniata College in 1992, and then moved to Guatemala where he worked in a number of fields including appropriate technology and high school teaching. He earned a Ph.D. in Environmental Toxicology from Duke University in 2003, carried out postdoctoral research with Dr Bennett Van Houten at NIEHS from 2003 to 2006, and joined the Nicholas School of the Environment at Duke University in 2007. His laboratory studies the effects of stressors on health, in particular studying the mechanisms by which environmental agents cause DNA damage and mitochondrial toxicity and the genetic differences that may alter sensitivity.

Environmental Chemistry 11(3) 227-246 https://doi.org/10.1071/EN13187
Submitted: 17 October 2013 Accepted: 16 April 2014 Published: 20 June 2014

Environmental context. The ability of the soil nematode Caenorhabditis elegans to withstand a wide range of environmental conditions makes it an idea model for studying the bioavailability and effects of engineered nanomaterials. We critically review what has been learned about the environmental fate of engineered nanoparticles, their effects and their mechanisms of toxicity using this model organism. Future systematic manipulation of nanoparticle properties and environmental variables should elucidate how their interaction influences toxicity and increase the predictive power of nanomaterial toxicity studies.

Abstract. Recent years have seen a rapid increase in studies of nanoparticle toxicity. These are intended both to reduce the chances of unexpected toxicity to humans or ecosystems, and to inform a predictive framework that would improve the ability to design nanoparticles that are less likely to cause toxicity. Nanotoxicology research has been carried out using a wide range of model systems, including microbes, cells in culture, invertebrates, vertebrates, plants and complex assemblages of species in microcosms and mesocosms. These systems offer different strengths and have also resulted in somewhat different conclusions regarding nanoparticle bioavailability and toxicity. We review the advantages offered by the model organism Caenorhabditis elegans, summarise what has been learned about uptake, distribution and effects of nanoparticles in this organism and compare and contrast these results with those obtained in other organisms, such as daphnids, earthworms, fish and mammalian models.

Additional keywords: bioavailability, gene expression, mechanism of toxicity, uptake.

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A micro-sized model for the in vivo study of nanoparticle toxicity: what has Caenorhabditis elegans taught us?

References

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