Bioenergetic failure correlates with autophagy and apoptosis in rat liver following silver nanoparticle intraperitoneal administration

Particle and Fibre Toxicology

Volumn 10, Issue 1, 2013, Pages

  Lee, Tzu Ying ^a   Liu, Maw Shung ^a   Huang, Li Ju ^a,b   Lue, Sheng I ^a   Lin, Lung Chang ^c   Kwan, Aij Lie ^a,c   Yang, Rei Cheng ^c,d,e  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b Foo Yin University   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^e CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

Author keywords

Apoptosis; ATP; Autophagy; Silver nanoparticles

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE 3; LC3 II PROTEIN; PROTEIN; SILVER NANOPARTICLE; UNCLASSIFIED DRUG; CASP3 PROTEIN, RAT; LC3 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN; NANOPARTICLE; SILVER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BIOENERGY; BLOOD LEVEL; CELL STRUCTURE; CONTROLLED STUDY; ENERGY METABOLISM; EXPOSURE; HISTOPATHOLOGY; IN VIVO STUDY; INFLAMMATION; LIVER DYSFUNCTION; LIVER LEVEL; LIVER TOXICITY; MALE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPRAGUE DAWLEY RAT; ANIMAL; BLOOD; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; INTRAPERITONEAL DRUG ADMINISTRATION; LIVER; LIVER FUNCTION TEST; METABOLISM; PATHOLOGY; TIME; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; AUTOPHAGY; CASPASE 3; DRUG-INDUCED LIVER INJURY; ENERGY METABOLISM; IN SITU NICK-END LABELING; INJECTIONS, INTRAPERITONEAL; LIVER; LIVER FUNCTION TESTS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULE-ASSOCIATED PROTEINS; NANOPARTICLES; RATS, SPRAGUE-DAWLEY; SILVER; TIME FACTORS;

EID: 84884316196     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/1743-8977-10-40     Document Type: Article

References (44)

1. Lewinski N, Colvin V, Drezek R. Cytotoxicity of nanoparticles. Small 2008, 4:26-49. 10.1002/smll.200700595, 18165959.
2. Quadros ME, Marr LC. Environmental and human health risks of aerosolized silver nanoparticles. J Air Waste Manag Assoc 2010, 60:770-781. 10.3155/1047-3289.60.7.770, 20681424.
3. Ahamed M, Alsalhi MS, Siddiqui MK. Silver nanoparticle applications and human health. Clin Chim Acta 2010, 411:1841-1848. 10.1016/j.cca.2010.08.016, 20719239.
4. Woodrow Wilson International Center for Scholars Project on emerging nanotechnologies, consumer products inventory of nanotechnology products 2012, Available from: http://www.nanotechproject.org/inventories/consumer/analysis_draft/ Accessed January 22, 2013, Woodrow Wilson International Center for Scholars.
5. Martinez-Gutierrez F, Thi EP, Silverman JM, De Oliveira CC, Svensson SL, Vanden Hoek A, Sanchez EM, Reiner NE, Gaynor EC, Pryzdial EL, Conway EM, Orrantia E, Ruiz F, Av-Gay Y, Bach H. Antibacterial activity, inflammatory response, coagulation and cytotoxicity effects of silver nanoparticles. Nanomedicine 2012, 8:328-336. 10.1016/j.nano.2011.06.014, 21718674.
6. Phalen RF, Morrow PE. Experimental inhalation of metallic silver. Health Phys 1973, 24:509-518. 10.1097/00004032-197305000-00005, 4707665.
7. Loeschner K, Hadrup N, Qvortrup K, Larsen A, Gao X, Vogel U, Mortensen A, Lam HR, Larsen EH. Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part Fibre Toxicol 2011, 8:18. 10.1186/1743-8977-8-18, 3123173, 21631937.
8. Xue Y, Zhang S, Huang Y, Zhang T, Liu X, Hu Y, Zhang Z, Tang M. Acute toxic effects and gender-related biokinetics of silver nanoparticles following an intravenous injection in mice. J Appl Toxicol 2012, 32:890-899. 10.1002/jat.2742, 22522906.
9. Tiwari DK, Jin T, Behari J. Dose-dependent in-vivo toxicity assessment of silver nanoparticle in wistar rats. Toxicol Mech Methods 2011, 21:13-24. 10.3109/15376516.2010.529184, 21080782.
10. Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, Choi BS, Lim R, Chang HK, Chung YH, Kwon IH, Jeong J, Han BS, Yu IJ. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in sprague-dawley rats. Inhal Toxicol 2008, 20:575-583. 10.1080/08958370701874663, 18444010.
11. Cha K, Hong HW, Choi YG, Lee MJ, Park JH, Chae HK, Ryu G, Myung H. Comparison of acute responses of mice livers to short-term exposure to nano-sized or micro-sized silver particles. Biotechnol Lett 2008, 30:1893-1899. 10.1007/s10529-008-9786-2, 18604478.
12. Sung JH, Ji JH, Park JD, Yoon JU, Kim DS, Jeon KS, Song MY, Jeong J, Han BS, Han JH, Chung YH, Chang HK, Lee JH, Cho MH, Kelman BJ, Yu IJ. Subchronic inhalation toxicity of silver nanoparticles. Toxicol Sci 2009, 108:452-461. 10.1093/toxsci/kfn246, 19033393.
13. Kim YS, Song MY, Park JD, Song KS, Ryu HR, Chung YH, Chang HK, Lee JH, Oh KH, Kelman BJ, Hwang IK, Yu IJ. Subchronic oral toxicity of silver nanoparticles. Part Fibre Toxicol 2010, 7:20. 10.1186/1743-8977-7-20, 2928176, 20691052.
14. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol 2010, 221:3-12. 10.1002/path.2697, 2990190, 20225336.
15. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004, 6:463-477. 10.1016/S1534-5807(04)00099-1, 15068787.
16. Mizushima N. Autophagy: process and function. Genes Dev 2007, 21:2861-2873. 10.1101/gad.1599207, 18006683.
17. Tanida I. Autophagosome formation and molecular mechanism of autophagy. Antioxid Redox Signal 2011, 14:2201-2214. 10.1089/ars.2010.3482, 20712405.
18. Shen HM, Codogno P. Autophagy is a survival force via suppression of necrotic cell death. Exp Cell Res 2012, 318:1304-1308. 10.1016/j.yexcr.2012.02.006, 22366289.
19. Chen D, Xi T, Bai J. Biological effects induced by nanosilver particles: in vivo study. Biomed Mater 2007, 2:S126-S128. 10.1088/1748-6041/2/3/S08, 18458456.
20. Rahman MF, Wang J, Patterson TA, Saini UT, Robinson BL, Newport GD, Murdock RC, Schlager JJ, Hussain SM, Ali SF. Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol Lett 2009, 187:15-21. 10.1016/j.toxlet.2009.01.020, 19429238.
21. Katsnelson BA, Privalova LI, Gurvich VB, Makeyev OH, Shur VY, Beikin YB, Sutunkova MP, Kireyeva EP, Minigalieva IA, Loginova NV, Vasilyeva MS, Korotkov AV, Shuman EA, Vlasova LA, Shishkina EV, Tyurnina AE, Kozin RV, Valamina IE, Pichugova SV, Tulakina LG. Comparative in vivo assessment of some adverse bioeffects of equidimensional gold and silver nanoparticles and the attenuation of nanosilver's effects with a complex of innocuous bioprotectors.". Int J Mol Sci 2013, 14:2449-2483. 10.3390/ijms14022449, 3587996, 23354478.
22. Katsnelson BA, Degtyareva TD, Minigalieva II, Privalova LI, Kuzmin SV, Yeremenko OS, Kireyeva EP, Sutunkova MP, Valamina II, Khodos MY, Kozitsina AN, Shur VY, Vazhenin VA, Potapov AP, Morozova MV. Subchronic systemic toxicity and bioaccumulation of Fe3O4 nano- and microparticles following repeated intraperitoneal administration to rats. Int J Toxicol 2011, 30:59-68. 10.1177/1091581810385149, 21398218.
23. Johnston HJ, Hutchison G, Christensen FM, Peters S, Hankin S, Stone V. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol 2010, 40:328-346. 10.3109/10408440903453074, 20128631.
24. Park K, Park EJ, Chun IK, Choi K, Lee SH, Yoon J, Lee BC. Bioavailability and toxicokinetics of citrate-coated silver nanoparticles in rats. Arch Pharm Res 2011, 34:153-158. 10.1007/s12272-011-0118-z, 21468927.
25. Kumar R, Roy I, Ohulchanskky TY, Vathy LA, Bergey EJ, Sajjad M, Prasad PN. In vivo biodistribution and clearance studies using multimodal organically modified silica nanoparticles. ACS Nano 2010, 4:699-708. 10.1021/nn901146y, 2827663, 20088598.
26. Souris JS, Lee CH, Cheng SH, Chen CT, Yang CS, Ho JA, Mou CY, Lo LW. Surface charge-mediated rapid hepatobiliary excretion of mesoporous silica nanoparticles. Biomaterials 2010, 31:5564-5574. 10.1016/j.biomaterials.2010.03.048, 2875342, 20417962.
27. AshaRani PV, Low Kah Mun G, Hande MP, Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 2009, 3:279-290. 10.1021/nn800596w, 19236062.
28. Bell RA, Kramer JR. Structural chemistry and geochemistry of silver-sulfur compound: critical review. Environ Toxicol Chem 1999, 18:9-22.
29. Panyam J, Labhasetwar V. Dynamics of endocytosis and exocytosis of poly(D, L-lactide-co-glycolide) nanoparticles in vascular smooth muscle cells. Pharm Res 2003, 20:212-220. 10.1023/A:1022219003551, 12636159.
30. Singh A, Bhat TK, Sharma OP. Clinical biochemistry of hepatotoxicity. J Clinic Toxicol 2011, S4:001.
31. Halamoda Kenzaoui B, Chapuis Bernasconi C, Guney-Ayra S, Juillerat-Jeanneret L. Induction of oxidative stress, lysosome activation and autophagy by nanoparticles in human brain-derived endothelial cells. Biochem J 2012, 441:813-821. 10.1042/BJ20111252, 22026563.
32. Li JJ, Hartono D, Ong CN, Bay BH, Yung LY. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials 2010, 31:5996-6003. 10.1016/j.biomaterials.2010.04.014, 20466420.
33. Andon FT, Fadeel B. Programmed 2012, Molecular Mechanisms and Implications for Safety Assessment of Nanomaterials. Acc Chem Res: Cell Death.
34. Almofti MR, Ichikawa T, Yamashita K, Terada H, Shinohara Y. Silver ion induces a cyclosporine a-insensitive permeability transition in rat liver mitochondria and release of apoptogenic cytochrome C. J Biochem 2003, 134:43-49. 10.1093/jb/mvg111, 12944369.
35. Costa CS, Ronconi JV, Daufenbach JF, Goncalves CL, Rezin GT, Streck EL, Paula MM. In vitro effects of silver nanoparticles on the mitochondrial respiratory chain. Mol Cell Biochem 2010, 342:51-56. 10.1007/s11010-010-0467-9, 20411305.
36. Rikiishi H. Novel insights into the interplay between apoptosis and autophagy. Int J Cell Biol 2012, 2012:317645. 3312193, 22496691.
37. Pratsinis A, Hervella P, Leroux JC, Pratsinis SE, Sotiriou GA. Toxicity of silver nanoparticles in macrophages. Small 2013, 9:2576-2784. 10.1002/smll.201202120, 23418027.
38. Kim S, Choi JE, Choi J, Chung KH, Park K, Yi J, Ryu DY. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol In Vitro 2009, 23:1076-1084. 10.1016/j.tiv.2009.06.001, 19508889.
39. Ghosh M, Sinha JM, Sinha JM, Mallick SK, Bandyopadhyay M, Mukherjee A. In vitro and in vivo genotoxicity of silver nanoparticles. Mutat Res 2012, 749:60-69. 10.1016/j.mrgentox.2012.08.007, 22960309.
40. Kim WY, Kim J, Park JD, Ryu HY, Yu IJ. Histological study of gender differences in accumulation of silver nanoparticles in kidneys of fischer 344 rats. J Toxicol Environ Health A 2009, 72:1279-1284. 10.1080/15287390903212287, 20077197.
41. Chien WS, Chen YH, Chiang PC, Hsiao HW, Chuang SM, Lue SI, Hsu C. Suppression of autophagy in rat liver at late stage of polymicrobial sepsis. Shock 2011, 35:506-511. 10.1097/SHK.0b013e31820b2f05, 21263383.
42. Liu CM, Zheng YL, Lu J, Zhang ZF, Fan SH, Wu DM, Ma JQ. Quercetin protects rat liver against lead-induced oxidative stress and apoptosis. Environ Toxicol Pharmacol 2010, 29:158-166. 10.1016/j.etap.2009.12.006, 21787598.
43. Bashir S, Sharma Y, Irshad M, Nag TC, Tiwari M, Kabra M, Dogra TD. Arsenic induced apoptosis in rat liver following repeated 60 days exposure. Toxicology 2006, 217:63-70. 10.1016/j.tox.2005.08.023, 16288947.
44. Drew B, Leeuwenburgh C. Method for measuring ATP production in isolated mitochondria: ATP production in brain and liver mitochondria of fischer-344 rats with age and caloric restriction. Am J Physiol Regul Integr Comp Physiol 2003, 285:R1259-R1267.