Superparamagnetic iron oxide nanoparticles exacerbate the risks of reactive oxygen species-mediated external stresses

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• 作者：Cheng Luo (1)
  Yan Li (2)
  Liang Yang (1)
  Xun Wang (1)
  Jiangang Long (1)
  Jiankang Liu (1)
  
  1. The Key Laboratory of Biomedical Information Engineering of Ministry of Education ; Frontier Institute of Science and Technology ; Center for Mitochondrial Biology and Medicine ; School of Life Science and Technology ; Xi鈥檃n Jiaotong University ; Xi鈥檃n ; 710049 ; China
  2. The Key Laboratory of Biomedical Information Engineering of Ministry of Education ; Center for Bioinformatics ; School of Life Science and Technology ; Xi鈥檃n Jiaotong University ; Xi鈥檃n ; 710049 ; China
  
• 关键词：IONPs ; Mitochondria ; Acrolein ; Lysosome ; Reactive oxygen species
• 刊名：Archives of Toxicology
• 出版年：2015
• 出版时间：March 2015
• 年：2015
• 卷：89
• 期：3
• 页码：357-369
• 全文大小：3,749 KB
• 参考文献：1. Anderson EJ, Katunga LA, Willis MS (2012) Mitochondria as a source and target of lipid peroxidation products in healthy and diseased heart. Clin Exp Pharmacol Physiol 39(2):179鈥?93 CrossRef
  2. Andreas K, Georgieva R, Ladwig M, Mueller S, Notter M, Sittinger M, Ringe J (2012) Highly efficient magnetic stem cell labeling with citrate-coated superparamagnetic iron oxide nanoparticles for MRI tracking. Biomaterials 33(18):4515鈥?525 CrossRef
  3. Ansari MA, Keller JN, Scheff SW (2008) Protective effect of pycnogenol in human neuroblastoma SH-SY5Y cells following acrolein-induced cytotoxicity. Free Radic Biol Med 45(11):1510鈥?519 CrossRef
  4. Au KW, Liao SY, Lee YK, Lai WH, Ng KM, Chan YC, Yip MC, Ho CY, Wu EX, Li RA, Siu CW, Tse HF (2009) Effects of iron oxide nanoparticles on cardiac differentiation of embryonic stem cells. Biochem Biophys Res Commun 379(4):898鈥?03 CrossRef
  5. Bajaj A, Samanta B, Yan H, Jerry DJ, Rotello VM (2009) Stability, toxicity and differential cellular uptake of protein passivated-Fe3O4 nanoparticles. J Mater Chem 19(35):6328鈥?331 CrossRef
  6. Bein K, Leikauf GD (2011) Acrolein鈥攁 pulmonary hazard. Mol Nutr Food Res 55(9):1342鈥?360 CrossRef
  7. Boya P, Kroemer G (2008) Lysosomal membrane permeabilization in cell death. Oncogene 27(50):6434鈥?451 CrossRef
  8. Chen YC, Hsiao JK, Liu HM, Lai IY, Yao M, Hsu SC, Ko BS, Yang CS, Huang DM (2010) The inhibitory effect of superparamagnetic iron oxide nanoparticle (Ferucarbotran) on osteogenic differentiation and its signaling mechanism in human mesenchymal stem cells. Toxicol Appl Pharmacol 245(2):272鈥?79 CrossRef
  9. Chen Z, Yin JJ, Zhou YT, Zhang Y, Song L, Song M, Hu S, Gu N (2012) Dual enzyme-like activities of iron oxide nanoparticles and their implication for diminishing cytotoxicity. ACS Nano 6(5):4001鈥?012 CrossRef
  10. Colombo M, Carregal-Romero S, Casula MF, Gutierrez L, Morales MP, Bohm IB, Heverhagen JT, Prosperi D, Parak WJ (2012) Biological applications of magnetic nanoparticles. Chem Soc Rev 41(11):4306鈥?334 CrossRef
  11. Comfort KK, Maurer EI, Braydich-Stolle LK, Hussain SM (2011) Interference of silver, gold, and iron oxide nanoparticles on epidermal growth factor signal transduction in epithelial cells. ACS Nano 5(12):10000鈥?0008 CrossRef
  12. Feng Z, Hu W, Hu Y, Tang MS (2006) Acrolein is a major cigarette-related lung cancer agent: preferential binding at p53 mutational hotspots and inhibition of DNA repair. Proc Natl Acad Sci U S A 103(42):15404鈥?5409 CrossRef
  13. Huang G, Chen H, Dong Y, Luo X, Yu H, Moore Z, Bey EA, Boothman DA, Gao J (2013) Superparamagnetic iron oxide nanoparticles: amplifying ROS stress to improve anticancer drug efficacy. Theranostics 3(2):116鈥?26 CrossRef
  14. Kehrer JP (2000) The Haber鈥揥eiss reaction and mechanisms of toxicity. Toxicology 149(1):43鈥?0 CrossRef
  15. Khan MI, Mohammad A, Patil G, Naqvi SA, Chauhan LK, Ahmad I (2012) Induction of ROS, mitochondrial damage and autophagy in lung epithelial cancer cells by iron oxide nanoparticles. Biomaterials 33(5):1477鈥?488 CrossRef
  16. Kung G, Konstantinidis K, Kitsis RN (2011) Programmed necrosis, not apoptosis, in the heart. Circ Res 108(8):1017鈥?036 CrossRef
  17. Kurz T, Gustafsson B, Brunk UT (2006) Intralysosomal iron chelation protects against oxidative stress-induced cellular damage. FEBS J 273(13):3106鈥?117 CrossRef
  18. Lee CH, Hung HW, Hung PH, Shieh YS (2010) Epidermal growth factor receptor regulates beta-catenin location, stability, and transcriptional activity in oral cancer. Mol Cancer 9:64 CrossRef
  19. Levy M, Lagarde F, Maraloiu VA, Blanchin MG, Gendron F, Wilhelm C, Gazeau F (2010) Degradability of superparamagnetic nanoparticles in a model of intracellular environment: follow-up of magnetic, structural and chemical properties. Nanotechnology 21(39):395103 CrossRef
  20. Li Q, Tang G, Xue S, He X, Miao P, Li Y, Wang J, Xiong L, Wang Y, Zhang C, Yang G-Y (2013) Silica-coated superparamagnetic iron oxide nanoparticles targeting of聽EPCs in ischemic brain injury. Biomaterials 34(21):4982鈥?992 CrossRef
  21. Liu G, Gao J, Ai H, Chen X (2013) Applications and potential toxicity of magnetic iron oxide nanoparticles. Small 9(9鈥?0):1533鈥?545 CrossRef
  22. Lunov O, Syrovets T, Buchele B, Jiang X, Rocker C, Tron K, Nienhaus GU, Walther P, Mailander V, Landfester K, Simmet T (2010) The effect of carboxydextran-coated superparamagnetic iron oxide nanoparticles on c-Jun N-terminal kinase-mediated apoptosis in human macrophages. Biomaterials 31(19):5063鈥?071 CrossRef
  23. Luo C, Li Y, Wang H, Cui Y, Feng Z, Li H, Li Y, Wang Y, Wurtz K, Weber P, Long J, Liu J (2013a) Hydroxytyrosol promotes superoxide production and defects in autophagy leading to anti-proliferation and apoptosis on human prostate cancer cells. Curr Cancer Drug Targets 13(6):625鈥?39 CrossRef
  24. Luo C, Li Y, Wang H, Feng Z, Long J, Liu J (2013b) Mitochondrial accumulation under oxidative stress is due to defects in autophagy. J Cell Biochem 114(1):212鈥?19 CrossRef
  25. Luo C, Wang H, Chen X, Cui Y, Li H, Long J, Mo X, Liu J (2013c) Protection of H9c2 rat cardiomyoblasts against oxidative insults by total paeony glucosides from radix paeoniae rubrae. Phytomedicine 21(1):20鈥?4 CrossRef
  26. Maghzal GJ, Krause KH, Stocker R, Jaquet V (2012) Detection of reactive oxygen species derived from the family of NOX NADPH oxidases. Free Radic Biol Med 53(10):1903鈥?918 CrossRef
  27. Mahmoudi M, Laurent S, Shokrgozar MA, Hosseinkhani M (2011) Toxicity evaluations of superparamagnetic iron oxide nanoparticles: cell 鈥渧ision鈥?versus physicochemical properties of nanoparticles. ACS Nano 5(9):7263鈥?276 CrossRef
  28. Mahmoudi M, Hofmann H, Rothen-Rutishauser B, Petri-Fink A (2012) Assessing the in vitro and in vivo toxicity of superparamagnetic iron oxide nanoparticles. Chem Rev 112(4):2323鈥?338 CrossRef
  29. Mohammad MK, Avila D, Zhang J, Barve S, Arteel G, McClain C, Joshi-Barve S (2012) Acrolein cytotoxicity in hepatocytes involves endoplasmic reticulum stress, mitochondrial dysfunction and oxidative stress. Toxicol Appl Pharmacol 265(1):73鈥?2 CrossRef
  30. Park EJ, Kim H, Kim Y, Yi J, Choi K, Park K (2010) Inflammatory responses may be induced by a single intratracheal instillation of iron nanoparticles in mice. Toxicology 275(1鈥?):65鈥?1 CrossRef
  31. Ramesh V, Ravichandran P, Copeland CL, Gopikrishnan R, Biradar S, Goornavar V, Ramesh GT, Hall JC (2012) Magnetite induces oxidative stress and apoptosis in lung epithelial cells. Mol Cell Biochem 363(1鈥?):225鈥?34 CrossRef
  32. Rauch J, Kolch W, Laurent S, Mahmoudi M (2013) Big signals from small particles: regulation of cell signaling pathways by nanoparticles. Chem Rev 113(5):3391鈥?406 CrossRef
  33. Saito S, Tsugeno M, Koto D, Mori Y, Yoshioka Y, Nohara S, Murase K (2012) Impact of surface coating and particle size on the uptake of small and ultrasmall superparamagnetic iron oxide nanoparticles by macrophages. Int J Nanomedicine 7:5415鈥?421
  34. Shi R, Rickett T, Sun W (2011) Acrolein-mediated injury in nervous system trauma and diseases. Mol Nutr Food Res 55(9):1320鈥?331 CrossRef
  35. Singh N, Jenkins GJ, Asadi R, Doak SH (2010) Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev 1. doi:10.3402/nano.v1i0.5358 , http://www.nano-reviews.net/index.php/nano/article/view/5358/6032
  36. Singh N, Jenkins GJ, Nelson BC, Marquis BJ, Maffeis TG, Brown AP, Williams PM, Wright CJ, Doak SH (2012) The role of iron redox state in the genotoxicity of ultrafine superparamagnetic iron oxide nanoparticles. Biomaterials 33(1):163鈥?70 CrossRef
  37. Soenen SJ, Himmelreich U, Nuytten N, Pisanic TR 2nd, Ferrari A, De Cuyper M (2010) Intracellular nanoparticle coating stability determines nanoparticle diagnostics efficacy and cell functionality. Small 6(19):2136鈥?145 CrossRef
  38. Soenen SJ, Himmelreich U, Nuytten N, De Cuyper M (2011) Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials 32(1):195鈥?05 CrossRef
  39. Stevens JF, Maier CS (2008) Acrolein: sources, metabolism, and biomolecular interactions relevant to human health and disease. Mol Nutr Food Res 52(1):7鈥?5 CrossRef
  40. Stroh A, Zimmer C, Gutzeit C, Jakstadt M, Marschinke F, Jung T, Pilgrimm H, Grune T (2004) Iron oxide particles for molecular magnetic resonance imaging cause transient oxidative stress in rat macrophages. Free Radic Biol Med 36(8):976鈥?84 CrossRef
  41. Subramaniam S, Unsicker K (2006) Extracellular signal-regulated kinase as an inducer of non-apoptotic neuronal death. Neuroscience 138(4):1055鈥?065 science.2005.12.013" target="_blank" title="It opens in new window">CrossRef
  42. Sun Z, Yathindranath V, Worden M, Thliveris JA, Chu S, Parkinson FE, Hegmann T, Miller DW (2013) Characterization of cellular uptake and toxicity of aminosilane-coated iron oxide nanoparticles with different charges in central nervous system-relevant cell culture models. Int J Nanomedicine 8:961鈥?70 CrossRef
  43. Yu MK, Jeong YY, Park J, Park S, Kim JW, Min JJ, Kim K, Jon S (2008) Drug-loaded superparamagnetic iron oxide nanoparticles for combined cancer imaging and therapy in vivo. Angew Chem Int Ed 47(29):5362鈥?365 CrossRef
  
• 刊物主题：Pharmacology/Toxicology; Occupational Medicine/Industrial Medicine; Environmental Health; Biomedicine general;
• 出版者：Springer Berlin Heidelberg
• ISSN：1432-0738

文摘

Superparamagnetic iron oxide nanoparticles (IONPs) have been widely applied in numerous biomedical fields. The evaluation of the toxicity of IONPs to the environment and human beings is indispensable to guide their applications. IONPs are usually considered to have good biocompatibility; however, some literatures have reported the toxicity of IONPs in vitro and in vivo. The controversy surrounding the biocompatibility of IONPs prompted us to carefully consider the biological effects of IONPs, especially under stress conditions. However, the potential risks of IONPs under stress conditions have not yet been evaluated in depth. Acrolein is widespread in the environment and modulates stress-induced gene activation and cell death in many organs and tissues. In this study, we assessed the sensitivity of H9c2 cardiomyocyte cells embedded with IONPs to acrolein and investigated the possible molecular mechanisms involved in this sensitivity. IONPs, which alone exhibited no toxicity, sensitized the H9c2 cardiomyocytes to acrolein-induced dysfunction. The IONP/acrolein treatment induced a loss of viability, membrane disruption, reactive oxygen species (ROS) generation, Erk activation, mitochondrial and lysosomal dysfunction, and necrosis in H9c2 cells. Treatment with an ROS generation inhibitor (diphenyleneiodonium) or an iron chelator (deferoxamine) prevented the IONP/acrolein-induced loss of viability, suggesting that ROS and IONP degradation facilitated the toxicity of the IONP/acrolein treatment in H9c2 cells. Our data suggest that cells embedded in IONPs are more vulnerable to oxidative stress, which confirms the hypothesis that nanoparticles can sensitize cells to the adverse effects of external stimulation. The present work provides a new perspective from which to evaluate the interactions between nanoparticles and cells.