Excessive apoptosis and defective autophagy contribute to developmental testicular toxicity induced by fluoride

Environmental Pollution

Volumn 212, Issue , 2016, Pages 97-104

  Zhang, Shun ^a   Niu, Qiang ^a   Gao, Hui ^a   Ma, Rulin ^a   Lei, Rongrong ^a   Zhang, Cheng ^a   Xia, Tao ^a   Li, Pei ^a   Xu, Chunyan ^a   Wang, Chao ^a   Chen, Jingwen ^a   Dong, Lixing ^a   Zhao, Qian ^a   Wang, Aiguo ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Apoptosis; Autophagy; Fluoride; Reproductive toxicity; Testis

Indexed keywords

CELL DEATH; CELL MEMBRANES; POTABLE WATER; TOXICITY;

AUTOPHAGY; CASPASE-3 ACTIVATION; CHROMATIN CONDENSATION; ENVIRONMENTAL CONTAMINANT; FLUORIDE; REPRODUCTIVE TOXICITIES; SPRAGUE-DAWLEY RATS; TESTIS;

FLUORINE COMPOUNDS;

CASPASE 3; CYTOCHROME C; DNA; DRINKING WATER; FAS ANTIGEN; PROTEIN P62; SODIUM FLUORIDE; BECLIN 1; DAXX PROTEIN, RAT; FLUORIDE; FLUOROPHOSPHATE; LC3 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; PHOSPHATE; SEQUESTOSOME 1; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SQSTM1 PROTEIN, RAT;

APOPTOSIS; DEVELOPMENTAL BIOLOGY; DRINKING WATER; FLUORIDE; HISTOPATHOLOGY; REPRODUCTIVE BIOLOGY; TOXICITY;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA FRAGMENTATION; ENZYME ACTIVATION; FEMALE; GERM CELL; MALE; NONHUMAN; PREGNANCY; PROGENY; PROTEIN EXPRESSION; PUBERTY; RAT; REPRODUCTIVE TOXICITY; SIGNAL TRANSDUCTION; SPERMATOCYTE; TESTIS; ANIMAL; ANIMAL MODEL; CHROMATIN ASSEMBLY AND DISASSEMBLY; DRUG EFFECTS; FERTILITY; HUMAN; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; TRANSMISSION ELECTRON MICROSCOPY;

RATTUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; AUTOPHAGY; BECLIN-1; CASPASE 3; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOCHROMES C; DNA FRAGMENTATION; FEMALE; FERTILITY; FLUORIDES; HUMANS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, ANIMAL; NUCLEAR PROTEINS; PHOSPHATES; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SEQUESTOSOME-1 PROTEIN; SODIUM FLUORIDE; TESTIS;

EID: 84960936846     PISSN: 02697491     EISSN: 18736424     Source Type: Journal    
DOI: 10.1016/j.envpol.2016.01.059     Document Type: Article

References (39)

1. M. Amini, K. Mueller, K.C. Abbaspour, and et al. Statistical modeling of global geogenic fluoride contamination in groundwaters Environ. Sci. Technol. 42 2008 3662 3668
2. B. Angmar-Mansson, and G.M. Whitford Enamel fluorosis related to plasma F levels in the rat Caries Res. 18 1984 25 32
3. S. Ayoob, and A.K. Gupta Fluoride in drinking water: A review on the status and stress effects Crit. Rev. Env. Sci. Tec. 36 2006 433 487
4. O. Barbier, L. Arreola-Mendoza, and L.M. Del Razo Molecular mechanisms of fluoride toxicity Chem. Biol Interact. 188 2010 319 333
5. G. Bjorkoy, T. Lamark, A. Brech, and et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death J. Cell Biol. 171 2005 603 614
6. J. Cao, J. Chen, J. Wang, and et al. Effects of fluoride on liver apoptosis and Bcl-2, Bax protein expression in freshwater teleost, Cyprinus carpio Chemosphere 91 2013 1203 1212
7. T.F. Collins, R.L. Sprando, T.N. Black, and et al. Developmental toxicity of sodium fluoride measured during multiple generations Food Chem. Toxicol. 39 2001 867 876
8. S.C. Freni Exposure to high fluoride concentrations in drinking water is associated with decreased birth rates J. Toxicol. Environ. Health 42 1994 109 121
9. S.P. Han, D.X. Zhou, P. Lin, and et al. Formaldehyde exposure induces autophagy in testicular tissues of adult male rats Environ. Toxicol. 30 2013 323 331
10. A. Herpin, E. Englberger, M. Zehner, and et al. Defective autophagy through epg5 mutation results in failure to reduce germ plasm and mitochondria FASEB J. 29 2015 4145 4161
11. M. Ito, H. Nakagawa, T. Okada, and et al. ER-stress caused by accumulated intracistanal granules activates autophagy through a different signal pathway from unfolded protein response in exocrine pancreas cells of rats exposed to fluoride Arch. Toxicol. 83 2009 151 159
12. C. Jiang, S. Zhang, H. Liu, and et al. Low glucose utilization and neurodegenerative changes caused by sodium fluoride exposure in rat's developmental brain Neuromol. Med. 16 2014 94 105
13. Y. Kabeya, N. Mizushima, T. Ueno, and et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing EMBO J. 19 2000 5720 5728
14. A. Krasowska, T. Wlostowski, and E. Bonda Zinc protection from fluoride-induced testicular injury in the bank vole (Clethrionomys glareolus) Toxicol. Lett. 147 2004 229 235
15. J. Lee, J.H. Richburg, S.C. Younkin, and et al. The Fas system is a key regulator of germ cell apoptosis in the testis Endocrinology 138 1997 2081 2088
16. B. Levine, and G. Kroemer Autophagy in the pathogenesis of disease Cell 132 2008 27 42
17. W.R. Li, L. Chen, Z.J. Chang, and et al. Autophagic deficiency is related to steroidogenic decline in aged rat Leydig cells Asian J. Androl. 13 2011 881 888
18. Y.J. Li, T.B. Song, Y.Y. Cai, and et al. Bisphenol A exposure induces apoptosis and upregulation of Fas/FasL and caspase-3 expression in the testes of mice Toxicol. Sci. 108 2009 427 436
19. H. Long, Y. Jin, M. Lin, and et al. Fluoride toxicity in the male reproductive system Fluoride 42 2009 260 276
20. Z. Lu, S. Wang, Z. Sun, and et al. In vivo influence of sodium fluoride on sperm chemotaxis in male mice Arch. Toxicol. 88 2014 533 539
21. D.M. Lyaruu, A.L. Bronckers, F. Santos, and et al. The effect of fluoride on enamel and dentin formation in the uremic rat incisor Pediatr. Nephrol. 23 2008 1973 1979
22. K. Miao, L. Zhang, S. Yang, and et al. Intervention of selenium on apoptosis and Fas/FasL expressions in the liver of fluoride-exposed rats Environ. Toxicol. Pharmacol. 36 2013 913 920
23. N. Mizushima, T. Yoshimori, and B. Levine Methods in mammalian autophagy research Cell 140 2010 313 326
24. M.M. Monick, L.S. Powers, K. Walters, and et al. Identification of an autophagy defect in smokers' alveolar macrophages J. Immunol. 185 2010 5425 5435
25. N. Mumtaz, G. Pandey, and P.K. Labhasetwar Global fluoride occurrence, available technologies for fluoride removal and electrolytic defluoridation: A review Crit. Rev. Env. Sci. Tec. 45 2015 2357 2389
26. B. Saradha, S. Vaithinathan, and P.P. Mathur Lindane induces testicular apoptosis in adult Wistar rats through the involvement of Fas-FasL and mitochondria-dependent pathways Toxicology 255 2009 131 139
27. J.L. Schneider, and A.M. Cuervo Autophagy and human disease: Emerging themes Curr. Opin. Genet. Dev. 26 2014 16 23
28. C. Settembre, A. Fraldi, L. Jahreiss, and et al. A block of autophagy in lysosomal storage disorders Hum. Mol. Genet. 17 2008 119 129
29. C. Shaha, R. Tripathi, and D.P. Mishra Male germ cell apoptosis: Regulation and biology Philos. T R. Soc. B 365 2010 1501 1515
30. Z. Sun, R. Niu, B. Wang, and et al. Fluoride-induced apoptosis and gene expression profiling in mice sperm in vivo Arch. Toxicol. 85 2011 1441 1452
31. I. Tabas, and D. Ron Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress Nat. Cell Biol. 13 2011 184 190
32. S.W. Tait, and D.R. Green Mitochondria and cell death: Outer membrane permeabilization and beyond Nat. Rev. Mol. Cell Biol. 11 2010 621 632
33. H. Wang, H. Wan, X. Li, and et al. Atg7 is required for acrosome biogenesis during spermatogenesis in mice Cell Res. 24 2014 852 869
34. E. Wirawan, B.T. Vanden, S. Lippens, and et al. Autophagy: For better or for worse Cell Res. 22 2012 43 61
35. B. Xu, Z. Xu, T. Xia, and et al. Effects of the Fas/Fas-L pathway on fluoride-induced apoptosis in SH-SY5Y cells Environ. Toxicol. 26 2011 86 92
36. Z. Yang, and D.J. Klionsky Eaten alive: A history of macroautophagy Nat. Cell Biol. 12 2010 814 822
37. M. Zhang, M. Jiang, Y. Bi, and et al. Autophagy and apoptosis act as partners to induce germ cell death after heat stress in mice PLoS One 7 2012 e41412
38. S. Zhang, C. Jiang, H. Liu, and et al. Fluoride-elicited developmental testicular toxicity in rats: Roles of endoplasmic reticulum stress and inflammatory response Toxicol. Appl. Pharmacol. 271 2013 206 215
39. X.F. Zhao, Q. Wang, Y.L. Ji, and et al. Fenvalerate induces germ cell apoptosis in mouse testes through the Fas/FasL signaling pathway Arch. Toxicol. 85 2011 1101 1108