Cardiac oxidative damage in mice following exposure to nanoparticulate titanium dioxide

Journal of Biomedical Materials Research - Part A

Volumn 101, Issue 11, 2013, Pages 3238-3246

  Sheng, Lei ^a   Wang, Xiaochun ^a   Sang, Xuezi ^a   Ze, Yuguan ^a   Zhao, Xiaoyang ^a   Liu, Dong ^a   Gui, Suxin ^a   Sun, Qingqing ^a   Cheng, Jie ^a   Cheng, Zhe ^a   Hu, Renping ^a   Wang, Ling ^a   Hong, Fashui ^a  

^a SOOCHOW UNIVERSITY   (China)

Author keywords

antioxidative defense system; heart; nanoparticulate titanium dioxide; oxidative stress; pathological changes

Indexed keywords

ANTI-OXIDATIVE ENZYMES; ANTIOXIDATIVE DEFENSE SYSTEMS; GLUTATHIONE-S-TRANSFERASE; INFLAMMATORY RESPONSE; NANO PARTICULATES; PATHOLOGICAL CHANGES; PHOTOCATALYTIC PROPERTY; REACTIVE OXYGEN SPECIES;

ANTIOXIDANTS; CELL DEATH; DEGRADATION; HEART; MAMMALS; OXIDATIVE STRESS; OXIDES; OXYGEN; PEPTIDES;

TITANIUM DIOXIDE;

ASCORBATE PEROXIDASE; ASCORBIC ACID; CARBONYL DERIVATIVE; GLUTATHIONE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HYDROGEN PEROXIDE; MALONALDEHYDE; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE; THIOL; TITANIUM DIOXIDE; TITANIUM DIOXIDE NANOPARTICLE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CARDIOTOXICITY; CONTROLLED STUDY; DNA METABOLISM; ENZYME ACTIVITY; FEMALE; HEART MUSCLE CELL; HEART MUSCLE NECROSIS; INFLAMMATION; LIPID DEGRADATION; LONG TERM EXPOSURE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PEROXIDATION; PROTEIN DEGRADATION;

ANTIOXIDATIVE DEFENSE SYSTEM; HEART; NANOPARTICULATE TITANIUM DIOXIDE; OXIDATIVE STRESS; PATHOLOGICAL CHANGES;

ANIMALS; ANTIOXIDANTS; DISULFIDES; DNA; ENVIRONMENTAL EXPOSURE; FEMALE; GLUTATHIONE DISULFIDE; HEART FUNCTION TESTS; HUMANS; LIPIDS; METAL NANOPARTICLES; MICE; MYOCARDIUM; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXIDES; SPECTROPHOTOMETRY, ATOMIC; TITANIUM;

EID: 84884909062     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.34634     Document Type: Article

References (79)

1. Ordman H, Berlin M,. Titanium. In:, Friberg L, Nordberg GF, Vouk VB, editors. Handbook on the Toxicology of Metals, vol. II. Amsterdam: Elsevier; 1986. p 595-609.
2. Lomer MCE, Thompson RPH, Powell JJ,. Fine and ultrafine particles of the diet: Influence on the mucosal immune response and association with Crohn's disease. Proc Nutr Soc 2002; 61: 123-130.
3. Gelis C, Girard S, Mavon A, Delverdier M, Paillous N, Vicendo P,. Assessment of the skin photoprotective capacities of an organo-mineral broad-spectrum sunblock on two ex vivo skin models. Photodermatol Photoimmunol Photomed 2003; 19: 242-253.
4. 2 photocatalytic disinfection. Water Res 2004; 38: 1069-1077.
5. 3 composite membranes for environmental applications. Appl Catal B Environ 2006; 63: 60-67.
6. 2. AIChE J 2005; 51: 2298-2310.
7. 2 particles: Differential responses related to surface properties. Toxicol 2007; 230: 90-104.
8. 2 particles in cultured human lymphoblastoid cells. Mutat Res 2007; 628: 99-106.
9. Wang JX, Zhou GQ, Chen CY, Yu HW, Wang TC, Ma M,. Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration. Toxicol Lett 2007; 168: 176-185.
10. 2 primary particles in mice. Environ Toxic Pharmacol 2007; 24: 239-244.
11. 2 to the nematode Caenorhabditis elegans. Environ Pollut 2009; 157: 1171-1177.
12. 2, ZnO and their bulk counterparts on zebrafish: Acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 2011; 409: 1444-1452.
13. Chen HW, Su SF, Chien CT, Lin WH, Yu SL, Chou CC, Chen Jeremy JW, Yang PC,. Titanium dioxide nanoparticles induce emphysema-like lung injury in mice. FASEB J 2006; 20: 1732-1741.
14. Sun QQ, Tan DL, Zhou QP, Liu XR, Cheng Z, Liu G, Zhu M, Sang XZ, Gui SX, Cheng J, Hu RP, Tang M, Hong FS,. Oxidative damage of lung and its protective mechanism in mice caused by long-term exposure to titanium dioxide nanoparticles. J Biomed Mater Res A 2012; 100: 2554-2562.
15. Sun QQ, Tan DL, Ze YG, Sang XZ, Liu XR, Gui SX, Cheng Z, Cheng J, Hu RP, Gao GD, Liu G, Zhu M, Zhao XY, Sheng L, Wang L, Tang M, Fashui Hong FS,. Pulmotoxicological effects caused by long-term titanium dioxide nanoparticles exposure in mice. J Hazard Mater 2012; 235-236: 47-53.
16. 2 particles. Biol Trace Elem Res 2009; 129: 170-180.
17. 2. Nanosacle Res Lett 2009; 4: 1275-1278.
18. Duan YM, Liu J, Ma LL, Li N, Liu HT, Wang J, Zheng L, Liu C, Wang XF, Zhang XG, Yan JY, Wang H, Hong FS,. Toxicological characteristics of nanoparticulate anatase titanium dioxide in mice. Biomaterials 2010; 31: 894-899.
19. 2 and liver DNA from mice in vivo. Nanoscale Res Lett 2010; 5: 108-115.
20. Cui YL, Gong XL, Duan YM, Li N, Hu RP, Liu HT, Hong MM, Zhou M, Wang L, Wang H, Hong FS,. Hepatocyte apoptosis and its molecular mechanisms in mice caused by titanium dioxide nanoparticles. J Hazard Mater 2010; 183: 874-880.
21. 2 to mice: Liver injury, oxidative stress. Toxicol Environ Chem 2010; 92: 175-186.
22. 2 nanoparticles. J Biomed Mater Res A 2011; 96: 221-229.
23. Cui YL, Liu HT, Ze YG, Zhang ZL, Hu YY, Cheng Z, Hu RP, Gao GD, Cheng J, Gui SX, Sang XZ, Sun QQ, Wang L, Tang M, Hong FS,. Gene expression in liver injury caused by long-term exposure to titanium dioxide nanoparticles in mice. Toxicol Sci 2012; 128: 171-185.
24. 2. J Exp Nanosci 2010; 5: 447-462.
25. Gui SX, Zhang ZL, Zheng L, Cui YL, Liu XR, Li N, Sang XZ, Su QQ, Gao GD, Cheng Z, Cheng J, Wang L, Tang M, Hong FS,. Molecular mechanism of kidney injury of mice caused by exposure to titanium dioxide nanoparticles. J Hazard Mater 2011; 195: 365-370.
26. Li N, Duan YM, Hong MM, Zheng L, Fei M, Zhao XY, Wang Y, Cui YL, Liu HT, Cai J, Gong SJ, Wang H, Hong FS,. Spleen injury and apoptotic pathway in mice caused by titanium dioxide nanoparticles. Toxicol Lett 2010; 195: 161-168.
27. 2. Biol Trace Elem Res 2011; 140: 186-197.
28. Sang XZ, Zheng L, Sun QQ, Li N, Cui YL, Hu RP, Gao GD, Cheng Z, Cheng J, Gui SX, Liu HT, Tang M, Hong FS,. The chronic spleen injury of mice following long-term exposure to titanium dioxide nanoparticles. J Biomed Mater Res A 2012; 100: 894-902.
29. 2 nanoparticles in hairless mice and porcine skin after subchronic dermal exposure. Toxicol Lett 2009; 191: 1-8.
30. Shin JA, Lee EJ, Seo SM, Kim HS, Kang JL, Park EM,. Nanosized titanium dioxide enhanced inflammatory responses in the septic brain of mouse. Neuroscience 2010; 165: 445-454.
31. 2 delivered to the abdominal cavity. Biomaterials 2010; 31: 99-105.
32. 2 nanoparticles. Biomaterials 2010; 31: 8043-8050.
33. Hu RP, Zheng L, Zhang T, Cui YL, Gao GD, Cheng Z, Cheng J, Tang M, Hong FS,. Molecular mechanism of hippocampal apoptosis of mice following exposure to titanium dioxide nanoparticles. J Hazard Mater 2011; 191: 32-40.
34. Brook RD, Rajagopalan S, Pope CA, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC, Whitsel L, Kaufman JD,. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation 2010; 121: 2331-2378.
35. Sun Q, Hong X, Wold LE,. Cardiovascular effects of ambient particulate air pollution exposure. Circulation 2010; 121: 2755-2765.
36. Peters A, Dockery DW, Muller JE, Mittleman MA,. Increased particulate air pollution and the triggering of myocardial infarction. Circulation 2001; 103: 2810-2815.
37. Sullivan J, Sheppard L, Schreuder A, Ishikawa N, Siscovick D, Kaufman J,. Relation between short-term fine-particulate matter exposure and onset of myocardial infarction. Epidemiology 2005; 16: 41-48.
38. Ibad-Mulli A, Stieber J, Wichmann H, Koenig W, Peters A,. Effect of air pollution on blood pressure: A population-based approach. Am J Public Health 2001; 91: 571-577.
39. Choi JH, Xu QS, Park SY, Kim JH, Hwang SS, Lee KH, Lee HJ, Hong YC,. Seasonal variation of effect of air pollution on blood pressure. J Epidemiol Commun Health 2007; 61: 314-318.
40. Allen RW, Criqui MH, Diez Roux AV, Allison M, Shea S, Detrano R, Sheppard L, Wong ND, Stukovsky KH, Kaufman JD,. Fine particulate matter air pollution, proximity to traffic, and aortic atherosclerosis. Epidemiology 2009; 20: 254-264.
41. Araujo JA, Nel AE,. Particulate matter and atherosclerosis: role of particle size, composition and oxidative stress. Part Fibre Toxicol 2009; 6: 24.
42. Cavallari J, Fang S, Eisen E, Schwartz J, Hauser R, Herrick R,. Time course of heart rate variability decline following particulate matter exposures in an occupational cohort. Inhal Toxicol 2008; 20: 415-422.
43. Whitsel EA, Quibrera PM, Christ SL, Liao D, Prineas RJ, Anderson GL, Heiss G,. Heart rate variability, ambient particulate matter air pollution, and glucose homeostasis: The environmental epidemiology of arrhythmogenesis in the women's health initiative. Am J Epidemiol 2009; 169: 693-703.
44. Baccarelli A, Martinelli I, Zanobetti A, Grillo P, Hou L, Bertazzi PA, Mannucci PM, Schwartz J,. Exposure to particulate air pollution and risk of deep vein thrombosis. Arch Intern Med 2008; 168: 920-927.
45. Emmerechts J, Alfaro-Moreno E, Vanaudenaerde BM, Nemery B, Hoylaerts MF,. Short-term exposure to particulate matter induces arterial but not venous thrombosis in healthy mice. J Thromb Haemost 2010; 8: 2651-2661.
46. Puett RC, Hart JE, Yanosky JD, Paciorek C, Schwartz J, Suh H, Speizer FE, Laden F,. Chronic fine and coarse particulate exposure, mortality, and coronary heart disease in the nurses' health study. Environ Health Perspect 2009; 117: 1702-1706.
47. Simkhovich BZ, Kleinman MT, Kloner RA,. Particulate air pollution and coronary heart disease. Curr Opin Cardiol 2009; 24: 604-609.
48. 3+ ions for photocatalysis. Mater Lett 2002; 57: 794-801.
49. National Institutes of Health (NIH). Guide for the Care and Use of Laboratory Animals. Washington, DC: National Academy Press; 1996.
50. Oliveira CP, Lopasso FP, Laurindo FR, Leitao RM, Laudanna AA,. Protection against liver ischemia-reperfusion injury in rats by silymarin or verapamil. Transplant Proc 2001; 33: 3010-3014.
51. Nourooz-Zadeh J, Tajaddini-Sarmadi J, Wolff SP,. Measurement of plasma hydroperoxide concentrations by the ferrous oxidation-xylenol orange assay in conjunction with triphenylphosphine. Anal Biochem 1994; 220: 403-409.
52. Buege JA, Aust SD,. Microsomal lipid peroxidation. Method Enzymol 1978; 52: 302-310.
53. Fagan JM, Bogdan GS, Sohar I,. Quantitation of oxidative damage to tissue proteins. Int J Biochem Cell Biol 1999; 31: 751-757.
54. Beauchamp C, Fridovich I,. Superoxide dismutase: Improved assays and assay applicable to acrylamide gels. Anal Biochem 1971; 44: 276-286.
55. Claiborne A,. Catalase activity. In:, Greenwaid RA, editor. Handbook of Methods for Oxygen Free Radical Research. Boca Raton, FL: CRC Press; 1985.
56. Lundquist I, Josefsson JO,. Sensitive method for determination of peroxidase activity in tissue by means of coupled oxidation reaction. Anal Biochem 1971; 41: 567-577.
57. Habig WH, Jakoby WB,. Assay for differentiation of glutathione-S- transferases. Method Enzymol 1981; 77: 398-405.
58. Moron MS, Depierre JW, Mannervik B,. Levels of glutathione, glutathione and reductase, glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 1979; 582: 67-76.
59. Hissin PJ, Hilf RA,. Fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976; 74: 214-226.
60. Jacques-Silva MC, Nogueira CW, Broch LC, Flores EM, Rocha JBT,. Diphenyl diselenide and ascorbic changes deposition of selenium and ascorbic in liver and brain of mice. Pharmacol Toxicol 2001; 88: 119-125.
61. Yee AT,. Assay of thiols and disulfides in intestinal lymph. Method Enzymol 1975; 251: 221-228.
62. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ,. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 193: 265-275.
63. Stadtman ER, Levine RL,. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 2003; 25: 207-218.
64. Chevion M, Berenshtein E, Stadtman ER,. Human studies related to protein oxidation: Protein carbonyl content as a marker of damage. Free Radic Res 2000; 33: S99-S108.
65. Kasai H, Nishimura S,. Hydroxylation of guanine in nucleosides and DNA at the C-8 position by heated glucose and oxygen radical-forming agents. Environ Health Perspect 1986; 67: 111-116.
66. Evans MD, Dizdaroglu M, Cooke MS,. Oxidative DNA damage and disease: Induction, repair and significance. Mutat Res 2004; 567: 1-6.
67. Grollman AP, Moriya M,. Mutagenesis by 8-oxoguanine: An enemy within. Trends Genet 1993; 9: 246-249.
68. Pilger A, Rüdiger HW,. 8-Hydroxy-2'-deoxyguanosine as a marker of oxidative DNA damage related to occupational and environmental exposures. Int Arch Occup Environ Health 2006; 80: 1-15.
69. Fortunato JJ, Feier G, Vitali AM, Petronilho FC, Dal-Pizzol F, Quevedo J,. Malathion-induced oxidative stress in rat brain regions. Neurochem Res 2006; 31: 671-678.
70. Lukaszewicz-Hussain A,. Activities of brain antioxidant enzymes, lipid and protein peroxidation. Cent Eur J Med 2011; 6: 588-594.
71. Scandalias G,. Response of plant antioxidant defence genes to environmental stress. Adv Genet 1990; 28: 1-41.
72. Asada K,. The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 1999; 50: 601-639.
73. Crawford NM, Kahn ML, Leustek T, Long SR,. Nitrogen and sulfur. In:, Buchanan BB, Gruissem W, Jones RL, editors. Biochemistry and Molecular Biology of Plants. Rockville: ASPP, 2000; p 786-849.
74. Sivori JL, Casabe N, Zerba EN, Wood EJ,. Induction of glutathione S-transferase activity in Tria-tomainfestans. Mem Inst Oswaldo Cruz 1997; 92: 797-802.
75. Armstrong JS, Steinauer KK, Hornung B, Irish JM, Lecane P, Birrell GW, Peehl DM, Knox SJ,. Role of glutathione depletion and reactive oxygen species generation in apoptotic signaling in a human B lymphoma cell line. Cell Death Differ 2002; 9: 252-263.
76. Smirnoff N,. Antioxidants and Reactive Oxygen Species in Plants. Oxford: Blackwell Publishing; 2005.
77. Jovanovic-Galovic A, Blagojevic DP, Grubor-Lajsic G, Worland R, Spasic MB,. Role of antioxidant defense during different stages of preadult life cycle in European corn borer (Ostrinia nubilalis, Hubn.): Diapause and metamorphosis. Arch Insect Biochem Physiol 2004; 55: 79-89.
78. Morrison JP, Coleman MC, Aunan ES, Walsh SA, Spitz DR, Kregel KC,. Thiol supplementation in aged animals alters antioxidant enzyme activity after heat stress. J Appl Physiol 2005; 99: 2271-2277.
79. Gilbert HF,. Thiol/disulfide exchange equilibria and disulfide bond stability. Method Enzymol 1995; 251: 8-28.