693
Views
20
CrossRef citations to date
0
Altmetric
Articles

Small variations in nanoparticle structure dictate differential cellular stress responses and mode of cell death

, , ORCID Icon, , ORCID Icon, , , , , & ORCID Icon show all
Pages 761-782 | Received 18 Sep 2018, Accepted 25 Jan 2019, Published online: 14 Feb 2019

References

  • Abdal Dayem, A., M. K. Hossain, S. B. Lee, K. Kim, S. K. Saha, G. M. Yang, H. Y. Choi, and S. G. Cho. 2017. “The Role of Reactive Oxygen Species (ROS) in the Biological Activities of Metallic Nanoparticles.” International Journal of Molecular Sciences 18 (1): 120. doi:10.3390/ijms18010120.
  • Afonyushkin, T., O. V. Oskolkova, M. Philippova, T. J. Resink, P. Erne, B. R. Binder, and V. N. Bochkov. 2010. “Oxidized Phospholipids Regulate Expression of ATF4 and VEGF in Endothelial Cells via NRF2-dependent Mechanism: Novel Point of Convergence between Electrophilic and Unfolded Protein Stress Pathways.” Arteriosclerosis, Thrombosis, and Vascular Biology 30 (5): 1007–1013. doi:10.1161/ATVBAHA.110.204354.
  • Aulas, A., M. M. Fay, S. M. Lyons, C. A. Achorn, N. Kedersha, P. Anderson, and P. Ivanov. 2017. “Stress-Specific Differences in Assembly and Composition of Stress Granules and Related Foci.” Journal of Cell Science 130 (5): 927–937. doi:10.1242/jcs.199240.
  • Barbero, F., Russo, L. M. Vitali, J. Piella, I. Salvo, M. L. Borrajo, M. Busquets-Fite, R., et al. 2017. “Formation of the Protein Corona: The Interface between Nanoparticles and the Immune System.” Seminars in Immunology 34: 52–60. doi:10.1016/j.smim.2017.10.001.
  • Bellezza, I., I. Giambanco, A. Minelli, and R. Donato. 2018. “Nrf2-Keap1 Signaling in Oxidative and Reductive Stress.” Biochimica et Biophysica Acta 1865 (5): 721–733. doi:10.1016/j.bbamcr.2018.02.010.
  • Cao, Y., J. Long, L. Liu, T. He, L. Jiang, C. Zhao, and Z. Li. 2017. “A Review of Endoplasmic Reticulum (ER) Stress and Nanoparticle (NP) Exposure.” Life Sciences 186: 33–42. doi:10.1016/j.lfs.2017.08.003.
  • Conrad, M., J. P. Angeli, P. Vandenabeele, and B. R. Stockwell. 2016. “Regulated Necrosis: Disease Relevance and Therapeutic Opportunities.” Nature Reviews Drug Discovery 15 (5): 348–366. doi:10.1038/nrd.2015.6.
  • Garic-Stankovic, A., M. Hernandez, G. R. Flentke, and S. M. Smith. 2006. “Structural Constraints for Alcohol-stimulated Ca2+ release in Neural Crest, and Dual Agonist/antagonist Properties of n-Octanol.” Alcoholism: Clinical and Experimental Research 30 (3): 552–559. doi:10.1111/j.1530-0277.2005.00061.x.
  • Gentric, G., V. Mieulet, and F. Mechta-Grigoriou. 2017. “Heterogeneity in Cancer Metabolism: New Concepts in an Old Field.” Antioxidants and Redox Signaling 26 (9): 462–485. doi:10.1089/ars.2016.6750.
  • Hangauer, M. J., Viswanathan, V. S. M. J. Ryan, D. Bole, J. K. Eaton, A. Matov, J. Galeas, H. D., et al. 2017. “Drug-Tolerant Persister Cancer Cells Are Vulnerable to GPX4 Inhibition.” Nature 551 (7679): 247–250. doi:10.1038/nature24297.
  • Hessvik, N. P., A. Overbye, A. Brech, M. L. Torgersen, I. S. Jakobsen, K. Sandvig, and A. Llorente. 2016. “PIKfyve Inhibition Increases Exosome Release and Induces Secretory Autophagy.” Cellular and Molecular Life Sciences 73 (24): 4717–4737. doi:10.1007/s00018-016-2309-8.
  • Hetz, C. 2012. “The Unfolded Protein Response: Controlling Cell Fate Decisions under ER Stress and beyond.” Nature Reviews Molecular Cell Biology 13 (2): 89–102. doi:10.1038/nrm3270.
  • Higashisaka, K., K. Nagano, Y. Yoshioka, and Y. Tsutsumi. 2017. “Nano-safety Research: Examining the Associations among the Biological Effects of Nanoparticles and Their Physicochemical Properties and Kinetics. Biological and Pharmaceutical Bulletin 40 (3): 243–248. doi:10.1248/bpb.b16-00854.
  • Itoh, K., Chiba, T. S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N., et al. 1997. “An Nrf2/small Maf Heterodimer Mediates the Induction of Phase II Detoxifying Enzyme Genes through Antioxidant Response Elements.” Biochemical and Biophysical Research Communications 236 (2): 313–322. doi:10.1006/bbrc.1997.6943.
  • Iurlaro, R., and C. Munoz-Pinedo. 2016. “Cell Death Induced by Endoplasmic Reticulum Stress.” The FEBS Journal 283 (14): 2640–2652. doi:10.1111/febs.13598.
  • Kreuter, J. 2014. “Drug Delivery to the Central Nervous System by Polymeric Nanoparticles: What Do we Know?” Advanced Drug Delivery Reviews 71: 2–14. doi:10.1016/j.addr.2013.08.008.
  • Lo, M., Y. Z. Wang, and P. W. Gout. 2008. “The x(c)- Cystine/Glutamate Antiporter: A Potential Target for Therapy of Cancer and Other Diseases.” Journal of Cellular Physiology 215 (3): 593–602. doi:10.1002/jcp.21366.
  • Lu, B., X. B. Chen, M. D. Ying, Q. J. He, J. Cao, and B. Yang. 2017. “The Role of Ferroptosis in Cancer Development and Treatment Response.” Frontiers in Pharmacology 8: 992. doi:10.3389/fphar.2017.00992
  • Lu, L., A. P. Han, and J. J. Chen. 2001. “Translation Initiation Control by Heme-Regulated Eukaryotic Initiation Factor 2alpha Kinase in Erythroid Cells under Cytoplasmic Stresses.” Molecular and Cellular Biology 21 (23): 7971–7980. doi:10.1128/MCB.21.23.7971-7980.2001.
  • Miyamoto, N., H. Izumi, R. Miyamoto, H. Bin, H. Kondo, A. Tawara, Y. Sasaguri, and K. Kohno. 2011. “Transcriptional Regulation of Activating Transcription Factor 4 under Oxidative Stress in Retinal Pigment Epithelial ARPE-19/HPV-16 Cells.” Investigative Opthalmology & Visual Science 52 (3): 1226–1234. doi:10.1167/iovs.10-5775.
  • Morata-Tarifa, C., G. Jimenez, M. A. Garcia, J. M. Entrena, C. Grinan-Lison, M. Aguilera, M. Picon-Ruiz, and J. A. Marchal. 2016. “Low Adherent Cancer Cell Subpopulations Are Enriched in Tumorigenic and Metastatic Epithelial-to-Mesenchymal Transition-induced Cancer Stem-like Cells.” Scientific Reports 6: 18772. doi:10.1038/srep18772.
  • Morch, Y., Hansen, R. S. Berg, A. K. Aslund, W. R. Glomm, S. Eggen, R. Schmid, H., et al. 2015. “Nanoparticle-Stabilized Microbubbles for Multimodal Imaging and Drug Delivery.” Contrast Media & Molecular Imaging 10 (5): 356–366. doi:10.1002/cmmi.1639.
  • Mouritsen, O. G. 2011. “Lipids, curvature, and Nano-Medicine.” European Journal of Lipid Science and Technology 113 (10): 1174–1187. doi:10.1002/ejlt.201100050.
  • Narang, V. S., G. M. Pauletti, P. W. Gout, D. J. Buckley, and A. R. Buckley. 2007. “Sulfasalazine-induced Reduction of Glutathione Levels in Breast Cancer Cells: Enhancement of Growth-inhibitory Activity of Doxorubicin.” Chemotherapy 53 (3): 210–217. doi:10.1159/000100812.
  • Nel, A. E., L. Madler, D. Velegol, T. Xia, E. M. Hoek, P. Somasundaran, F. Klaessig, V. Castranova, and M. Thompson. 2009. “Understanding Biophysicochemical Interactions at the Nano-bio Interface.” Nature Materials 8 (7): 543–557. doi:10.1038/nmat2442.
  • Pakos-Zebrucka, K., I. Koryga, K. Mnich, M. Ljujic, A. Samali, and A. M. Gorman. 2016. “The Integrated Stress Response.” EMBO Reports 17 (10): 1374–1395. doi:10.15252/embr.201642195.
  • Peynshaert, K., B. B. Manshian, F. Joris, K. Braeckmans, S. C. De Smedt, J. Demeester, and S. J. Soenen. 2014. “Exploiting Intrinsic Nanoparticle Toxicity: The Pros and Cons of Nanoparticle-induced Autophagy in Biomedical Research.” Chemical Reviews 114 (15): 7581–609. doi:10.1021/cr400372p.
  • Sarhan, M., A. von Massenhausen, C. Hugo, R. Oberbauer, and A. Linkermann. 2018. “Immunological Consequences of Kidney Cell death.” Cell Death & Disease 9 (2): 114. doi:10.1038/s41419-017-0057-9
  • Sato, M., R. Kusumi, S. Hamashima, S. Kobayashi, S. Sasaki, Y. Komiyama, T. Izumikawa, M. Conrad, S. Bannai, and H. Sato. 2018. “The Ferroptosis Inducer Erastin Irreversibly Inhibits System xc- and Synergizes with Cisplatin to Increase Cisplatin's Cytotoxicity in Cancer Cells.” Scientific Reports 8 (1): 968. doi:10.1038/s41598-018-19213-4.
  • Senft, A. P., T. P. Dalton, and H. G. Shertzer. 2000. “Determining Glutathione and Glutathione Disulfide Using the Fluorescence Probe o-Phthalaldehyde.” Analytical Biochemistry 280 (1): 80–86. doi:10.1006/abio.2000.4498.
  • Sidrauski, C., Acosta-Alvear, D. A. Khoutorsky, P. Vedantham, B. R. Hearn, H. Li, K. Gamache, C. M., et al. 2013. “Pharmacological Brake-release of mRNA Translation Enhances Cognitive Memory.” Elife 2: e00498. doi:10.7554/eLife.00498.
  • Sies, H., C. Berndt, and D. P. Jones. 2017. “Oxidative Stress.” Annual Review of Biochemistry 86 (1): 715–748. doi:10.1146/annurev-biochem-061516-045037.
  • Simon, J., T. Wolf, K. Klein, K. Landfester, V. Mailander, and F. R. Wurm. 2018. “Hydrophilicity Regulates the Stealth Properties of Polyphosphoester-coated Nanocarriers.” Angewandte Chemie. International Ed 4;57 (19): 5548–5553. In English. doi:10.1002/anie.201800272.
  • Snipstad, S., Berg, S. Y. Morch, A. Bjorkoy, E. Sulheim, R. Hansen, I. Grimstad, A., et al. 2017. “Ultrasound Improves the Delivery and Therapeutic Effect of Nanoparticle-Stabilized Microbubbles in Breast Cancer Xenografts.” Ultrasound in Medicine and Biology 43 (11): 2651–2669. doi:10.1016/j.ultrasmedbio.2017.06.029.
  • Starheim, K. K., Holien, T. K. Misund, I. Johansson, K. A. Baranowska, A. M. Sponaas, H. Hella, G., et al. 2016. “Intracellular Glutathione Determines Bortezomib Cytotoxicity in Multiple Myeloma Cells.” Blood Cancer Journal 6 (7): e446. doi:10.1038/bcj.2016.56.
  • Stockwell, B. R., Friedmann Angeli, J. P. H. Bayir, A. I. Bush, M. Conrad, S. J. Dixon, S. Fulda, S., et al. 2017. “Ferroptosis: A Regulated Cell Death Nexus Linking Metabolism, Redox Biology, and Disease.” Cell 171 (2): 273–285. doi:10.1016/j.cell.2017.09.021.
  • Sukhanova, A., S. Bozrova, P. Sokolov, M. Berestovoy, A. Karaulov, and I. Nabiev. 2018. “Dependence of Nanoparticle Toxicity on Their Physical and Chemical Properties.” Nanoscale Research Letters 13 (1): 44. doi:10.1186/s11671-018-2457-x.
  • Sulheim, E., H. Baghirov, E. von Haartman, A. Boe, A. K. Aslund, Y. Morch, and L. Davies Cde. 2016. “Cellular Uptake and Intracellular Degradation of Poly(alkyl Cyanoacrylate) Nanoparticles.” Journal of Nanobiotechnology 14: 1. doi:10.1186/s12951-015-0156-7.
  • Sulheim, E., Iversen, T. G. V. To Nakstad, G. Klinkenberg, H. Sletta, R. Schmid, A. R. Hatletveit, A. M., et al. 2017. “Cytotoxicity of Poly(Alkyl Cyanoacrylate) Nanoparticles.” International Journal of Molecular Sciences 18 (11): 2454. doi:10.3390/ijms18112454.
  • Thastrup, O., P. J. Cullen, B. K. Drobak, M. R. Hanley, and A. P. Dawson. 1990. “Thapsigargin, a Tumor Promoter, Discharges Intracellular Ca2+ stores by Specific Inhibition of the Endoplasmic Reticulum Ca2(+)-ATPase.” Proceedings of the National Academy of Sciences of the United States of America 87 (7): 2466–2470. doi:10.1073/pnas.87.7.2466.
  • Timmerman, L. A., Holton, T. M. Yuneva, R. J. Louie, M. Padro, A. Daemen, M. Hu, D. A., et al. 2013. “Glutamine Sensitivity Analysis Identifies the xCT Antiporter as a Common Triple-negative Breast Tumor Therapeutic Target.” Cancer Cell 24 (4): 450–465. doi:10.1016/j.ccr.2013.08.020.
  • van Zandwijk, N. 1995. “N-acetylcysteine (NAC) and Glutathione (GSH): Antioxidant and Chemopreventive Properties, with Special Reference to Lung cancer.” Journal of Cellular Biochemistry. Supplement22: 24–32. PMID: 8538205.
  • Vauthier, C., C. Dubernet, E. Fattal, H. Pinto-Alphandary, and P. Couvreur. 2003. “Poly(alkylcyanoacrylates) as Biodegradable Materials for Biomedical Applications.” Advanced Drug Delivery Reviews 55 (4): 519–548. doi:10.1016/S0169-409X(03)00041-3.
  • Vezin, W. R., and A. T. Florence. 1980. “In Vitro Heterogeneous Degradation of Poly(n-alkyl Alpha-cyanoacrylates).” Journal of Biomedical Materials Research 14 (2): 93–106. doi:10.1002/jbm.820140202.
  • Viswanathan, V. S., Ryan, M. J. H. D. Dhruv, S. Gill, O. M. Eichhoff, B. Seashore-Ludlow, S. D. Kaffenberger, J. K., et al. 2017. “Dependency of a Therapy-resistant State of Cancer Cells on a Lipid Peroxidase Pathway.” Nature 547 (7664): 453–457. doi:10.1038/nature23007.
  • White, M. C., R. D. Schroeder, K. Zhu, K. Xiong, and D. J. McConkey. 2018. “HRI-mediated Translational Repression Reduces Proteotoxicity and Sensitivity to Bortezomib in Human Pancreatic Cancer Cells.” Oncogene 37 (32):4413–4427. doi:10.1038/s41388-018-0227-y.
  • Yu, H., P. Guo, X. Xie, Y. Wang, and G. Chen. 2017. “Ferroptosis, a New Form of Cell Death, and Its Relationships with Tumourous Diseases.” Journal of Cellular and Molecular Medicine 21 (4): 648–657. doi:10.1111/jcmm.13008.
  • Yu, X., and Y. C. Long. 2016. “Crosstalk between Cystine and Glutathione Is Critical for the Regulation of Amino Acid Signaling Pathways and Ferroptosis.” Scientific Reports 6: 30033. doi:10.1038/srep30033.
  • Zilka, O., R. Shah, B. Li, J. P. Friedmann Angeli, M. Griesser, M. Conrad, and D. A. Pratt. 2017. “On the Mechanism of Cytoprotection by Ferrostatin-1 and Liproxstatin-1 and the Role of Lipid Peroxidation in Ferroptotic Cell Death.” ACS Central Science 3 (3): 232–243. doi:10.1021/acscentsci.7b00028.

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.