380
Views
69
CrossRef citations to date
0
Altmetric
Original Article

p38 MAPK-SKN-1/Nrf signaling cascade is required for intestinal barrier against graphene oxide toxicity in Caenorhabditis elegans

, , , , &
Pages 1469-1479 | Received 22 Feb 2016, Accepted 28 Jul 2016, Published online: 27 Sep 2016

References

  • Antoshechkin I, Sternberg PW. 2007. The versatile worm: genetic and genomic resources for Caenorhabditis elegans research. Nat Rev Genet 8:518–32.
  • Bitounis D, Ali-Boucetta H, Hong BH, Min D, Kostarelos K. 2013. Prospects and challenges of graphene in biomedical applications. Adv Mater 25:2258–68.
  • Blackwell TK, Steinbaugh MJ, Hourihan JM, Ewald CY. 2015. SKN-1/Nrf, stress responses, and aging in Caenorhabditis elegans. Free Radic Biol Med 88:290–301.
  • Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94.
  • Chang Y, Yang S, Liu J, Dong E, Wang Y, Cao A, et al. 2011. In vitro toxicity evaluation of grapheme oxide on A549 cells. Toxicol Lett 200:201–10
  • Chatterjee N, Eom H, Choi J. 2014a. A Systems toxicology approach to the surface functionality control of graphene-cell interactions. Biomaterials 35:1109–27.
  • Chatterjee N, Eom H, Choi J. 2014b. Effects of silver nanoparticles on oxidative DNA damage-repair as a function of p38 MAPK status: a comparative approach using human Jurkat T cells and the nematode Caenorhabditis elegans. Environ Mol Mutagen 55:122–33.
  • Donkin S, Williams PL. 1995. Influence of developmental stage, salts and food presence on various end points using Caenorhabditis elegans for aquatic toxicity testing. Environ Toxicol Chem 14:2139–47.
  • Eom H, Kim H, Kim B, Chon T, Choi J. 2014. Integrative assessment of benzene exposure to Caenorhabditis elegans using computational behavior and toxicogenomic analyses. Environ Sci Technol 48:8143–51.
  • Geim AK. 2009. Graphene: status and prospects. Science 324:1530–4.
  • Hayakawa T, Kato K, Jayakawa R, Hisamoto N, Katsumoto K, Takeda K, et al. 2011. Regulation of anoxic death in Caenorhabditis elegans by mammalian apoptosis signal-regulating kinase (ASK) family proteins. Genetics 187:785–92
  • Ju J-J, Ruan Q-L, Li X-B, Liu R, Li Y-H, Pu Y-P, et al. 2013. Neurotoxicological evaluation of microcystin-LR exposure at environmental relevant concentrations on nematode Caenorhabditis elegans. Environ Sci Pollut Res 20:1823–30
  • Kamath RK, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J. 2001. Effectiveness of specific RNA-mediated interference through ingested double stranded RNA in C. elegans. Genome Biol 2:1–10.
  • Kim DH, Ausubel FM. 2005. Evolutionary perspectives on innate immunity from the study of Caenorhabditis elegans. Curr Opin Immunol 17:4–10.
  • Kovtyukhova NI, Olivier PJ, Martin BR, Mallouk TE, Chizhik SA, Buzaneva EV, et al. 1999. Layer-by-layer assembly of ultrathin composite films from micron-sized graphite oxide sheets and polycations. Chem Mater 11:771–8.
  • Leiers B, Kampkotter A, Grevelding CG, Link CD, Johnson TE, Henkle-Duhrsen K. 2003. A stress-responsive glutathione S-transferase confers resistance to oxidative stress in Caenorhabditis elegans. Free Radic Biol Med 34:1405–15.
  • Li Y-P, Li Y-X, Wu Q-L, Ye H-Y, Sun L-M, Ye B-P, et al. 2013. High concentration of vitamin E decreases thermosensation and thermotaxis learning and the underlying mechanisms in nematode Caenorhabditis elegans. PLoS One 8:e71180
  • Li Y-P, Wu Q-L, Zhao Y-L, Bai Y-F, Chen P-S, Xia T, et al. 2014. Response of microRNAs to in vitro treatment with graphene oxide. ACS Nano 8:2100–10
  • Liang S, Xu S, Zhang D, He J, Chu M. 2015. Reproductive toxicity of nanosclae graphene oxide in male mice. Biomaterials 9:92–105.
  • Lim D, Roh J, Eom H, Choi J, Hyun J, Choi J. 2012. Oxidative stress-related PMK-1 p38 MAPK activation as a mechanism for toxicity of silver nanoparticles to reproduction in the nematode Caenorhabditis elegans. Environ Toxicol Chem 31:585–92.
  • Liu Z-F, Zhou X-F, Wu Q-L, Zhao Y-L, Wang D-Y. 2015. Crucial role of intestinal barrier in the formation of transgenerational toxicity in quantum dots exposed nematodes Caenorhabditis elegans. RSC Adv 5:94257–66.
  • Matsukawa J, Matsuzawa A, Takeda K, Ichijo H. 2004. The ASK1-MAP kinase cascades in mammalian stress response. J Biochem 136:261–5.
  • Mello C, Fire A. 1995. DNA transformation. Methods Cell Biol 48:451–82.
  • Qu G, Zhang S, Wang L, Wang X, Sun B, Yin N, et al. 2013. Graphen oxide induces Toll-like receptor 4 (TLR4)-dependent necrosis in macrophages. ACS Nano 7:5732–45.
  • Roux PP, Blenis J. 2004. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68:320–44.
  • Rui Q, Lu Q, Wang D-Y. 2009. Administration of Bushenkangshuai Tang alleviates the UV irradiation- and oxidative stress-induced lifespan defects in nematode Caenorhabditis elegans. Front Med China 3:76–90.
  • Settivari R, VanDuyn N, LeVora J, Nass R. 2013. The Nrf2/SKN-1-dependent glutathione S-transferase π homologue GST-1 inhibits dopamine neuron degeneration in a Caenorhabditis elegans model of manganism. Neurotoxicology 38:51–60.
  • Sun L-M, Lin Z-Q, Liao K, Xi Z-G, Wang D-Y. 2015. Adverse effects of coal combustion related fine particulate matter (PM2.5) on nematode Caenorhabditis elegans. Sci Total Environ 512–513:251–60.
  • Wang D-Y, Wang Y, Shen L-L. 2010. Confirmation of the combinational effects of calcium with other metals in a paper recycling mill effluent on nematode lifespan with the toxicity identification evaluation method. J Environ Sci 22:731–7.
  • Wu Q-L, Rui Q, He K-W, Shen L-L, Wang D-Y. 2010. UNC-64 and RIC-4, the plasma membrane associated SNAREs syntaxin and SNAP-25, regulate fat storage in nematode Caenorhabditis elegans. Neurosci Bull 26:104–16.
  • Wu Q-L, Liu P-D, Li Y-X, Du M, Xing X-J, Wang D-Y. 2012. Inhibition of ROS elevation and damage on mitochondrial function prevents lead-induced neurotoxic effects on structures and functions of AFD neurons in Caenorhabditis elegans. J Environ Sci 24:733–42.
  • Wu Q-L, Yin L, Li X, Tang M, Zhang T, Wang D-Y. 2013a. Contributions of altered permeability of intestinal barrier and defecation behavior to toxicity formation from graphene oxide in nematode Caenorhabditis elegans. Nanoscale 5:9934–43.
  • Wu Q-L, Li Y-X, Li Y-P, Zhao Y-L, Ge L, Wang H-F, et al. 2013b. Crucial role of biological barrier at the primary targeted organs in controlling translocation and toxicity of multi-walled carbon nanotubes in nematode Caenorhabditis elegans. Nanoscale 5:11166–78.
  • Wu Q-L, Zhao Y-L, Fang J-P, Wang D-Y. 2014a. Immune response is required for the control of in vivo translocation and chronic toxicity of graphene oxide. Nanoscale 6:5894–906.
  • Wu Q-L, Zhao Y-L, Zhao G, Wang D-Y. 2014b. microRNAs control of in vivo toxicity from graphene oxide in Caenorhabditis elegans. Nanomedicine: Nanotechnol Biol Med 10:1401–10.
  • Wu Q-L, Zhao Y-L, Li Y-P, Wang D-Y. 2014c. Molecular signals regulating translocation and toxicity of graphene oxide in nematode Caenorhabditis elegans. Nanoscale 6:11204–12.
  • Yang K, Zhang S, Zhang G, Sun X, Lee S, Liu Z. 2010. Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett 10:3318–23.
  • Yang J-N, Zhao Y-L, Wang Y-W, Wang H-F, Wang D-Y. 2015a. Toxicity evaluation and translocation of carboxyl functionalized graphene in Caenorhabditis elegans. Toxicol Res 4:1498–510.
  • Yang R-L, Zhao Y-L, Yu X-M, Lin Z-Q, Xi Z-G, Rui Q, et al. 2015b. Insulin signaling regulates toxicity of traffic-related PM2.5 on intestinal development and function in nematode Caenorhabditis elegans. Toxicol Res 4:333–43.
  • Yang K, Li Y, Tan X, Peng R, Liu Z. 2013. Behavior and toxicity of graphene and its functionalized derivatives in biological systems. Small 9:1492–503.
  • Zhang W, Wang C, Li Z, Lu Z, Li Y, Yin J, et al. 2012. Unraveling stress-induced toxicity properties of graphene oxide and the underlying mechanism. Adv Mater 24:5391–7.
  • Zhao Y-L, Wu Q-L, Li Y-P, Wang D-Y. 2013. Translocation, transfer, and in vivo safety evaluation of engineered nanomaterials in the non-mammalian alternative toxicity assay model of nematode Caenorhabditis elegans. RSC Adv 3:5741–57.
  • Zhao Y-L, Wu Q-L, Li Y-P, Nouara A, Jia R-H, Wang D-Y. 2014. In vivo translocation and toxicity of multi-walled carbon nanotubes are regulated by microRNAs. Nanoscale 6:4275–84.
  • Zhao Y-L, Wu Q-L, Wang D-Y. 2015a. A microRNAs-mRNAs network involved in the control of graphene oxide toxicity in Caenorhabditis elegans. RSC Adv 5:92394–405.
  • Zhao Y-L, Yu X-M, Jia R-H, Yang R-L, Rui Q, Wang D-Y. 2015b. Lactic acid bacteria protects Caenorhabditis elegans from toxicity of graphene oxide by maintaining normal intestinal permeability under different genetic backgrounds. Sci Rep 5:17233
  • Zhao Y-L, Wang X, Wu Q-L, Li Y-P, Wang D-Y. 2015c. Translocation and neurotoxicity of CdTe quantum dots in RMEs motor neurons in nematode Caenorhabditis elegans. J Hazard Mater 283:480–9.
  • Zhao Y-L, Wang X, Wu Q-L, Li Y-P, Tang M, Wang D-Y. 2015d. Quantum dots exposure alters both development and function of D-type GABAergic motor neurons in nematode Caenorhabditis elegans. Toxicol Res 4:399–408.
  • Zhao Y-L, Wu Q-L, Wang D-Y. 2016a. An epigenetic signal encoded protection mechanism is activated by graphene oxide to inhibit its induced reproductive toxicity in Caenorhabditis elegans. Biomaterials 79:15–24.
  • Zhao Y-L, Yang R-L, Rui Q, Wang D-Y. 2016b. Intestinal insulin signaling encodes two different molecular mechanisms for the shortened longevity induced by graphene oxide in Caenorhabditis elegans. Sci Rep 6:24024
  • Zhi X, Fang H, Bao C, Shen G, Zhang J, Wang K, et al. 2013. The immunotoxicity of graphene oxides and the effect of PVP-coating. Biomaterials 34:5254–61.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.