Analysis of changes in gene expression and metabolic profiles induced by silica-coated magnetic nanoparticles

ACS Nano

Volumn 6, Issue 9, 2012, Pages 7665-7680

  Shim, Wooyoung ^a   Paik, Man Jeong ^b   Nguyen, Duc Toan ^a   Lee, Jin Kyu ^c   Lee, Yuwon ^c   Kim, Jae Ho ^a   Shin, Eun Hee ^c,d   Kang, Jin Seok ^e   Jung, Hak Sung ^c   Choi, Sangdun ^a   Park, Sungsu ^f,g   Shim, Jeom Soon ^a   Lee, Gwang ^a,h  

^a Ajou University   (South Korea)

^b Sunchon National University   (South Korea)

^c Seoul National University   (South Korea)

^d Seoul National University Bundang Hospital   (South Korea)

^e Namseoul University   (South Korea)

^f Ewha Womans University   (South Korea)

^g NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^h Ajou University School of Medicine   (South Korea)

Author keywords

cytotoxicity; magnetic nanoparticles; metabolism; microarray; mitochondria

Indexed keywords

293 CELLS; ATP SYNTHESIS; BIOMEDICAL RESEARCH; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GLUTAMIC ACID; HUMAN EMBRYO; ISOTHIOCYANATES; KREBS CYCLE; MAGNETIC NANOPARTICLES; METABOLIC CHANGES; METABOLIC PATHWAYS; METABOLIC PROFILES; MITOCHONDRIAL DAMAGE; MITOCHONDRIAL FUNCTION; REACTIVE OXYGEN SPECIES; RHODAMINE B; TOXICOLOGICAL EVALUATION;

AMINO ACIDS; CYTOTOXICITY; GAS CHROMATOGRAPHY; GENE EXPRESSION; MICROARRAYS; MITOCHONDRIA; NANOPARTICLES; SILICA;

METABOLISM;

BIOMATERIAL; MAGNETITE NANOPARTICLE; PROTEOME; SILICON DIOXIDE;

ARTICLE; CELL STRAIN HEK293; DOSE RESPONSE; DRUG EFFECT; GENE EXPRESSION REGULATION; HUMAN; MATERIALS TESTING; METABOLISM; METABOLOME; PHYSIOLOGY;

COATED MATERIALS, BIOCOMPATIBLE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MAGNETITE NANOPARTICLES; MATERIALS TESTING; METABOLOME; PROTEOME; SILICON DIOXIDE;

EID: 84866682731     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn301113f     Document Type: Article

References (71)

1. Tholouli, E.; Sweeney, E.; Barrow, E.; Clay, V.; Hoyland, J. A.; Byers, R. J. Quantum Dots Light up Pathology J. Pathol. 2008, 216, 275-285
2. Stark, W. J. Nanoparticles in Biological Systems Angew. Chem., Int. Ed. 2011, 50, 1242-1258
3. Hussain, S. M.; Javorina, A. K.; Schrand, A. M.; Duhart, H. M.; Ali, S. F.; Schlager, J. J. The Interaction of Manganese Nanoparticles with PC-12 Cells Induces Dopamine Depletion Toxicol. Sci. 2006, 92, 456-463
4. Jun, Y. W.; Seo, J. W.; Cheon, J. Nanoscaling Laws of Magnetic Nanoparticles and Their Applicabilities in Biomedical Sciences Acc. Chem. Res. 2008, 41, 179-189
5. Amemiya, Y.; Tanaka, T.; Yoza, B.; Matsunaga, T. Novel Detection System for Biomolecules Using Nano-Sized Bacterial Magnetic Particles and Magnetic Force Microscopy J. Biotechnol. 2005, 120, 308-314
6. Horak, D.; Babic, M.; Mackova, H.; Benes, M. J. Preparation and Properties of Magnetic Nano- and Microsized Particles for Biological and Environmental Separations J. Sep. Sci. 2007, 30, 1751-1772
7. McCarthy, J. R.; Kelly, K. A.; Sun, E. Y.; Weissleder, R. Targeted Delivery of Multifunctional Magnetic Nanoparticles Nanomedicine 2007, 2, 153-167
8. Scarberry, K. E.; Dickerson, E. B.; McDonald, J. F.; Zhang, Z. J. Magnetic Nanoparticle-Peptide Conjugates for In Vitro and In Vivo Targeting and Extraction of Cancer Cells J. Am. Chem. Soc. 2008, 130, 10258-10262
9. Kim, J. S.; Yoon, T. J.; Yu, K. N.; Kim, B. G.; Park, S. J.; Kim, H. W.; Lee, K. H.; Park, S. B.; Lee, J. K.; Cho, M. H. Toxicity and Tissue Distribution of Magnetic Nanoparticles in Mice Toxicol. Sci. 2006, 89, 338-347
10. Gupta, A. K.; Gupta, M. Cytotoxicity Suppression and Cellular Uptake Enhancement of Surface Modified Magnetic Nanoparticles Biomaterials 2005, 26, 1565-1573
11. Morgan, K. Development of a Preliminary Framework for Informing the Risk Analysis and Risk Management of Nanoparticles Risk Anal. 2005, 25, 1621-1635
12. Park, K. S.; Tae, J.; Choi, B.; Kim, Y. S.; Moon, C.; Kim, S. H.; Lee, H. S.; Kim, J.; Park, J.; Lee, J. H. et al. Characterization, In Vitro Cytotoxicity Assessment, and In Vivo Visualization of Multimodal, RITC-Labeled, Silica-Coated Magnetic Nanoparticles for Labeling Human Cord Blood-Derived Mesenchymal Stem Cells Nanomedicine: Nanotechnol., Biol., Med. 2010, 6, 263-276
13. Cavallero, A.; Marte, A.; Fedele, E. l -Aspartate as an Amino Acid Neurotransmitter: Mechanisms of the Depolarization-Induced Release from Cerebrocortical Synaptosomes J. Neurochem. 2009, 110, 924-934
14. Mathers, D. A.; McCarthy, S. M.; Cooke, J. E.; Ghavanini, A. A.; Puil, E. Effects of the β-Amino Acid Antagonist TAG on Thalamocortical Inhibition Neuropharmacology 2009, 56, 1097-1105
15. Bechet, E.; Guiral, S.; Torres, S.; Mijakovic, I.; Cozzone, A. J.; Grangeasse, C. Tyrosine-Kinases in Bacteria: From a Matter of Controversy to the Status of Key Regulatory Enzymes Amino Acids 2009, 37, 499-507
16. Chuang, D. T.; Chuang, J. L.; Wynn, R. M. Lessons from Genetic Disorders of Branched-Chain Amino Acid Metabolism J. Nutr. 2006, 136, 243S-249S
17. Kimball, S. R.; Jefferson, L. S. Signaling Pathways and Molecular Mechanisms through which Branched-Chain Amino Acids Mediate Translational Control of Protein Synthesis J. Nutr. 2006, 136, 227S-231S
18. Wang, M.; Bai, J.; Chen, W. N.; Ching, C. B. Metabolomic Profiling of Cellular Responses to Carvedilol Enantiomers in Vascular Smooth Muscle Cells PLoS One 2010, 5, e15441-e15448
19. Wang, L.; Xu, D. X.; Lv, Y. G.; Zhang, H. Purification and Biochemical Characterisation of a Novel Glutamate Decarboxylase from Rice Bran J. Sci. Food. Agric. 2010, 90, 1027-1033
20. Spink, D. C.; Wu, S. J.; Martin, D. L. Multiple Forms of Glutamate Decarboxylase in Porcine Brain J. Neurochem. 1983, 40, 1113-1119
21. Zhang, B.; Yuan, Y.; Jia, Y.; Yu, X.; Xu, Q.; Shen, Y. An Association Study between Polymorphisms in Five Genes in Glutamate and GABA Pathway and Paranoid Schizophrenia Eur. Psychiatry 2005, 20, 45-49
22. 13C Magnetic Resonance Spectroscopy FASEB J. 2009, 23, 2529-2538
23. Sharma, N.; Okere, I. C.; Brunengraber, D. Z.; McElfresh, T. A.; King, K. L.; Sterk, J. P.; Huang, H.; Chandler, M. P.; Stanley, W. C. Regulation of Pyruvate Dehydrogenase Activity and Citric Acid Cycle Intermediates during High Cardiac Power Generation J. Physiol. 2005, 562, 593-603
24. Kobayashi, K.; Neely, J. R. Mechanism of Pyruvate Dehydrogenase Activation by Increased Cardiac Work J. Mol. Cell. Cardiol. 1983, 15, 369-382
25. Yoon, T. J.; Kim, J. S.; Kim, B. G.; Yu, K. N.; Cho, M. H.; Lee, J. K. Multifunctional Nanoparticles Possessing a "Magnetic Motor Effect" for Drug or Gene Delivery Angew. Chem., Int. Ed. 2005, 44, 1068-1071
26. Limbach, L. K.; Li, Y.; Grass, R. N.; Brunner, T. J.; Hintermann, M. A.; Muller, M.; Gunther, D.; Stark, W. J. Oxide Nanoparticle Uptake in Human Lung Fibroblasts: Effects of Particle Size, Agglomeration, and Diffusion at Low Concentrations Environ. Sci. Technol. 2005, 39, 9370-9376
27. Prabha, S.; Zhou, W. Z.; Panyam, J.; Labhasetwar, V. Size-Dependency of Nanoparticle-Mediated Gene Transfection: Studies with Fractionated Nanoparticles Int. J. Pharm. 2002, 244, 105-115
28. Paik, M. J.; Moon, S. M.; Kim, K. R.; Choi, S.; Ahn, Y. H.; Lee, G. Target Metabolic Profiling Analysis of Free Amino Acids in Plasma as EOC/TBDMS Derivatives by GC-SIM-MS Biomed. Chromatogr. 2008, 22, 339-342
29. Self, J. T.; Spencer, T. E.; Johnson, G. A.; Hu, J.; Bazer, F. W.; Wu, G. Glutamine Synthesis in the Developing Porcine Placenta Biol. Reprod. 2004, 70, 1444-1451
30. Burrin, D. G.; Stoll, B. Metabolic Fate and Function of Dietary Glutamate in the Gut Am. J. Clin. Nutr. 2009, 90, 850S-856S
31. Wu, G. Amino Acids: Metabolism, Functions, and Nutrition Amino Acids 2009, 37, 1-17
32. Lin, W.; Huang, Y. W.; Zhou, X. D.; Ma, Y. In Vitro Toxicity of Silica Nanoparticles in Human Lung Cancer Cells Toxicol. Appl. Pharmacol. 2006, 217, 252-259
33. Park, E. J.; Choi, J.; Park, Y. K.; Park, K. Oxidative Stress Induced by Cerium Oxide Nanoparticles in Cultured BEAS-2B Cells Toxicology 2008, 245, 90-100
34. Park, E. J.; Park, K. Oxidative Stress and Pro-Inflammatory Responses Induced by Silica Nanoparticles in Vivo and in Vitro Toxicol. Lett. 2009, 184, 18-25
35. Park, E. J.; Bae, E.; Yi, J.; Kim, Y.; Choi, K.; Lee, S. H.; Yoon, J.; Lee, B. C.; Park, K. Repeated-Dose Toxicity and Inflammatory Responses in Mice by Oral Administration of Silver Nanoparticles Environ. Toxicol. Pharmacol. 2010, 30, 162-168
36. Bauer, A. T.; Strozyk, E. A.; Gorzelanny, C.; Westerhausen, C.; Desch, A.; Schneider, M. F.; Schneider, S. W. Cytotoxicity of Silica Nanoparticles through Exocytosis of Von Willebrand Factor and Necrotic Cell Death in Primary Human Endothelial Cells Biomaterials 2011, 32, 8385-8393
37. Liu, X.; Sun, J. Endothelial Cells Dysfunction Induced by Silica Nanoparticles through Oxidative stress via JNK/P53 and NF-κB Pathways Biomaterials 2010, 31, 8198-8209
38. Geys, J.; De Vos, R.; Nemery, B.; Hoet, P. H. In Vitro Translocation of Quantum Dots and Influence of Oxidative Stress Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297, L903-L911
39. Clichici, S.; Mocan, T.; Filip, A.; Biris, A.; Simon, S.; Daicoviciu, D.; Decea, N.; Parvu, A.; Moldovan, R.; Muresan, A. Blood Oxidative Stress Generation after Intraperitoneal Administration of Functionalized Single-Walled Carbon Nanotubes in Rats Acta Physiol. Hung. 2011, 98, 231-241
40. Shukla, R. K.; Sharma, V.; Pandey, A. K.; Singh, S.; Sultana, S.; Dhawan, A. ROS-Mediated Genotoxicity Induced by Titanium Dioxide Nanoparticles in Human Epidermal Cells Toxicol. in Vitro 2011, 25, 231-241
41. Jeong, Y. S.; Oh, W. K.; Kim, S.; Jang, J. Cellular Uptake, Cytotoxicity, and ROS Generation with Silica/Conducting Polymer Core/Shell Nanospheres Biomaterials 2011, 32, 7217-7225
42. 2 Induces Apoptosis via Activation of p53 and Bax Mediated by Oxidative Stress in Human Hepatic Cell Line Toxicol. in Vitro 2010, 24, 751-758
43. Choi, J.; Zheng, Q.; Katz, H. E.; Guilarte, T. R. Silica-Based Nanoparticle Uptake and Cellular Response by Primary Microglia Environ. Health Perspect. 2010, 118, 589-595
44. Nel, A.; Xia, T.; Madler, L.; Li, N. Toxic Potential of Materials at the Nanolevel Science 2006, 311, 622-627
45. Beck, G. R., Jr.; Ha, S. W.; Camalier, C. E.; Yamaguchi, M.; Li, Y.; Lee, J. K.; Weitzmann, M. N. Bioactive Silica-Based Nanoparticles Stimulate Bone-Forming Osteoblasts, Suppress Bone-Resorbing Osteoclasts, and Enhance Bone Mineral Density in Vivo Nanomedicine 2011, 10.1016/j.nano.2011.11.003
46. Baber, O.; Jang, M.; Barber, D.; Powers, K. Amorphous Silica Coatings on Magnetic Nanoparticles Enhance Stability and Reduce Toxicity to In Vitro BEAS-2B Cells Inhal. Toxicol. 2011, 23, 532-543
47. Udintsev, N. A.; Ivanov, V. V. Antioxidant Action of Glutamic Acid Patol. Fiziol. Eksp. Ter. 1984, 4, 60-62
48. Zhang, D. W.; Shao, J.; Lin, J.; Zhang, N.; Lu, B. J.; Lin, S. C.; Dong, M. Q.; Han, J. RIP3, an Energy Metabolism Regulator that Switches TNF-Induced Cell Death from Apoptosis to Necrosis Science 2009, 325, 332-336
49. Matthews, G. D.; Gur, N.; Koopman, W. J.; Pines, O.; Vardimon, L. Weak Mitochondrial Targeting Sequence Determines Tissue-Specific Subcellular Localization of Glutamine Synthetase in Liver and Brain Cells J. Cell. Sci. 2010, 123, 351-359
50. Smith, D. D., Jr.; Campbell, J. W. Subcellular Location of Chicken Brain Glutamine Synthetase and Comparison with Chicken Liver Mitochondrial Glutamine Synthetase J. Biol. Chem. 1983, 258, 12265-12268
51. Buddhala, C.; Hsu, C. C.; Wu, J. Y. A Novel Mechanism for GABA Synthesis and Packaging into Synaptic Vesicles Neurochem. Int. 2009, 55, 9-12
52. Rubi, B.; Ishihara, H.; Hegardt, F. G.; Wollheim, C. B.; Maechler, P. GAD65-Mediated Glutamate Decarboxylation Reduces Glucose-Stimulated Insulin Secretion in Pancreatic β Cells J. Biol. Chem. 2001, 276, 36391-36396
53. Yoshida, A.; Rzhetsky, A.; Hsu, L. C.; Chang, C. Human Aldehyde Dehydrogenase Gene Family Eur. J. Biochem. 1998, 251, 549-557
54. Hu, C. A.; Lin, W. W.; Valle, D. Cloning, Characterization, and Expression of cDNAs Encoding Human δ1-Pyrroline-5-Carboxylate Dehydrogenase J. Biol. Chem. 1996, 271, 9795-9800
55. Piao, M. J.; Kang, K. A.; Lee, I. K.; Kim, H. S.; Kim, S.; Choi, J. Y.; Choi, J.; Hyun, J. W. Silver Nanoparticles Induce Oxidative Cell Damage in Human Liver Cells through Inhibition of Reduced Glutathione and Induction of Mitochondria-Involved Apoptosis Toxicol. Lett. 2011, 201, 92-100
56. Schaeublin, N. M.; Braydich-Stolle, L. K.; Schrand, A. M.; Miller, J. M.; Hutchison, J.; Schlager, J. J.; Hussain, S. M. Surface Charge of Gold Nanoparticles Mediates Mechanism of Toxicity Nanoscale 2011, 3, 410-420
57. Di Lisa, F.; Blank, P. S.; Colonna, R.; Gambassi, G.; Silverman, H. S.; Stern, M. D.; Hansford, R. G. Mitochondrial Membrane Potential in Single Living Adult Rat Cardiac Myocytes Exposed to Anoxia or Metabolic Inhibition J. Physiol. 1995, 486, 1-13
58. Hsin, Y. H.; Chen, C. F.; Huang, S.; Shih, T. S.; Lai, P. S.; Chueh, P. J. The Apoptotic Effect of Nanosilver Is Mediated by a ROS- and JNK-Dependent Mechanism Involving the Mitochondrial Pathway in NIH3T3 Cells Toxicol. Lett. 2008, 179, 130-139
59. Pan, Y.; Leifert, A.; Ruau, D.; Neuss, S.; Bornemann, J.; Schmid, G.; Brandau, W.; Simon, U.; Jahnen-Dechent, W. Gold Nanoparticles of Diameter 1.4 nm Trigger Necrosis by Oxidative Stress and Mitochondrial Damage Small 2009, 5, 2067-2076
60. Cory, A. H.; Owen, T. C.; Barltrop, J. A.; Cory, J. G. Use of an Aqueous Soluble Tetrazolium/Formazan Assay for Cell Growth Assays in Culture Cancer Commun. 1991, 3, 207-212
61. Paik, M. J.; Cho, E. Y.; Kim, H.; Kim, K. R.; Choi, S.; Ahn, Y. H.; Lee, G. Simultaneous Clinical Monitoring of Lactic Acid, Pyruvic Acid and Ketone Bodies in Plasma as Methoxime/ tert -butyldimethylsilyl Derivatives by Gas Chromatography-Mass Spectrometry in Selected Ion Monitoring Mode Biomed. Chromatogr. 2008, 22, 450-453
62. Lu, X.; Tian, Y.; Zhao, Q.; Jin, T.; Xiao, S.; Fan, X. Integrated Metabonomics Analysis of the Size-Response Relationship of Silica Nanoparticles-Induced Toxicity in Mice Nanotechnology 2011, 22, 055101-055116
63. Prijic, S.; Scancar, J.; Romih, R.; Cemazar, M.; Bregar, V. B.; Znidarsic, A.; Sersa, G. Increased Cellular Uptake of Biocompatible Superparamagnetic Iron Oxide Nanoparticles into Malignant Cells by an External Magnetic Field J. Membr. Biol. 2010, 236, 167-179
64. Sohaebuddin, S. K.; Thevenot, P. T.; Baker, D.; Eaton, J. W.; Tang, L. Nanomaterial Cytotoxicity Is Composition, Size, and Cell Type Dependent Part. Fibre. Toxicol. 2010, 7, 1-17
65. Hanley, C.; Thurber, A.; Hanna, C.; Punnoose, A.; Zhang, J.; Wingett, D. G. The Influences of Cell Type and ZnO Nanoparticle Size on Immune Cell Cytotoxicity and Cytokine Induction Nanoscale Res. Lett. 2009, 4, 1409-1420
66. Wang, F.; Gao, F.; Lan, M.; Yuan, H.; Huang, Y.; Liu, J. Oxidative Stress Contributes to Silica Nanoparticle-Induced Cytotoxicity in Human Embryonic Kidney Cells Toxicol. in Vitro 2009, 23, 808-815
67. 3) Induced Calcium Signals and Cytotoxicity in Two Human Cell Lines: SY-5Y Neuroblastoma and 293 Embryonic Kidney (HEK) Toxicol. Appl. Pharmacol. 2007, 220, 292-301
68. Yalcin, A. Quantification of Thioredoxin mRNA Expression in the Rat Hippocampus by Real-Time PCR Following Oxidative Stress Acta. Biochim. Pol. 2004, 51, 1059-1065
69. Paik, M. J.; Kim, K. R. Sequential Ethoxycarbonylation, Methoximation and tert -Butyldimethylsilylation for Simultaneous Determination of Amino Acids and Carboxylic Acids by Dual-Column Gas Chromatography J. Chromatogr., A 2004, 1034, 13-23
70. Paik, M. J.; Ahn, Y. H.; Lee, P. H.; Kang, H.; Park, C. B.; Choi, S.; Lee, G. Polyamine Patterns in the Cerebrospinal Fluid of Patients with Parkinson's Disease and Multiple System Atrophy Clin. Chim. Acta 2010, 411, 1532-1535
71. Shimizu, N.; Ishii, S. Electron Microscopic Histochemistry of Acetylcholinesterase of Rat Brain by Karnovsky's Method Histochemie 1966, 6, 24-33