Cadmium-induced autophagy in rat kidney: An early biomarker of subtoxic exposure

Toxicological Sciences

Volumn 121, Issue 1, 2011, Pages 31-42

  Chargui, Abderrahman ^a,b,c,d   Zekri, Sami ^a,b   Jacquillet, Gregory ^b,d   Rubera, Isabelle ^b,d   Ilie, Marius ^b,c,d,e   Belaid, Amine ^b,c,d   Duranton, Christophe ^b,d   Tauc, Michel ^b,d   Hofman, Paul ^b,c,d,e   Poujeol, Philippe ^b,c   El May, Michèle V ^a,b   Mograbi, Baharia ^b,c,d  

^a UNIVERSITY OF TUNIS EL MANAR   (Tunisia)

^b CNRS   (France)

^c INSERM   (France)

^d UNIVERSITÉ CÔTE D'AZUR   (France)

^e PASTEUR HOSPITAL   (France)

Author keywords

Apoptosis; Autophagy; Cadmium; Exposure to subtoxic doses; Kidney; Proliferation

Indexed keywords

CADMIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL LINE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM STRESS; ENVIRONMENTAL EXPOSURE; FEMALE; IMMUNOHISTOCHEMISTRY; KIDNEY CELL; KIDNEY CORTEX; KIDNEY PROXIMAL TUBULE; LYSOSOME; NEPHROTOXICITY; NONHUMAN; PROTEIN DEGRADATION; RAT; ULTRASTRUCTURE; UPREGULATION;

RATTUS;

EID: 79955422848     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr031     Document Type: Article

References (51)

1. Abouhamed, M., Wolff, N. A., Lee, W. K., Smith, C. P., and Thévenod, F. (2007). Knockdown of endosomal/lysosomal divalent metal transporter 1 by RNA interference prevents cadmium-metallothionein-1 cytotoxicity in renal proximal tubule cells. Am. J. Physiol. Renal Physiol. 293, F705-F12.
2. Aoyagi, T., Hayakawa, K., Miyaji, K., Ishikawa, H., and Hata, M. (2003). Cadmium nephrotoxicity and evacuation from the body in a rat modeled subchronic intoxication. Int. J. Urol. 10, 332-338.
3. Barbier, O., Jacquillet, G., Tauc, M., Cougnon, M., and Poujeol, P. (2005). Effect of heavy metals on, and handling by, the kidney. Nephron Physiol. 99, 105-110.
4. Brzoska, M. M., Kaminski, M., and Supernak-Bobko, D. (2003). Changes in the structure and function of the kidney of rats chronically exposed to Cd. I. Biochemical and histopathological studies. Arch. Toxicol. 77, 344-352.
5. Buchet, J. P., Lauwerys, R., Roels, H., Bernard, A., Bruaux, P., Claeys, F., Ducoffre, G., de Plaen, P., Staessen, J., Amery, A., et al. (1990). Renal effects of cadmium body burden of the general population. Lancet 336, 699-702.
6. Christensen, E. I., and Birn, H. (2001). Megalin and cubilin: Synergistic endocytic receptors in renal proximal tubule. Am. J. Physiol. Renal Physiol. 280, F562-F573.
7. Chuang, S. M., Wang, I. C., and Yang, J. L. (2000). Roles of JNK, p38 and ERK mitogen-activated protein kinases in the growth inhibition and apoptosis induced by cadmium. Carcinogenesis 21, 1423-1432.
8. Corcelle, E., Nebout, M., Bekri, S., Gauthier, N., Hofman, P., Poujeol, P., Fénichel, P., and Mograbi, B. (2006). Disruption of autophagy at the maturation step by the carcinogen lindane is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Cancer Res. 66, 6861-6870.
9. Di Gioacchino, M., Petrarca,C., Perrone, A., Farina,M., Sabbioni, E.,Hartung, T., Martino, S., Esposito, D. L., Lotti, L. V., and Mariani-Costantini, R. (2008). Autophagy as an ultrastructural marker of heavy metal toxicity in human cord blood hematopoietic stem cells. Sci. Total Environ. 392, 50-58.
10. Dong, Z., Wang, L., Xu, J., Li, Y., Zhang, Y., Zhang, S., and Miao, J. (2009). Promotion of autophagy and inhibition of apoptosis by low concentrations of cadmium in vascular endothelial cells. Toxicol. In Vitro. 23, 105-110.
11. Dudley, R. E., Gammal, L., and Klaassen, C. (1985). Cadmium-induced hepatic and renal injury in chronically exposed rats: Likely role of hepatic cadmium-metallothionein in nephrotoxicity. Toxicol. Appl. Pharmacol. 77, 414-426.
12. Fowler, B. A. (2009). Monitoring of human populations for early markers of cadmium toxicity: A review. Toxicol. Appl. Pharmacol. 238, 294-300.
13. Galluzzi, L., Maiuri, M. C., Vitale, I., Zischka, H., Castedo, M., Zitvogel, L., and Kroemer, G. (2007). Cell death modalities: Classification and pathophysiological implications. Cell Death Differ. 14, 1237-1243.
14. Golstein, P., and Kroemer, G. (2007). Cell death by necrosis: Towards a molecular definition. Trends Biochem. Sci. 32, 37-43.
15. Gulisano, M., Pacini, S., Punzi, T., Morucci, G., Quagliata, S., Delfino, G., Sarchielli, E., Marini, M., and Vannelli, G. B. (2009). Cadmium modulates proliferation and differentiation of human neuroblasts. J. Neurosci. Res. 87, 228-237.
16. Herak-Kramberger, C. M., Brown, D., and Sabolić, I. (1998). Cadmium inhibits vacuolar H(+)-ATPase and endocytosis in rat kidney cortex. Kidney Int. 53, 1713-1726.
17. Hiramatsu, N., Kasai, A., Du, S., Takeda, M., Hayakawa, K., Okamura, M., Yao, J., and Kitamura, M. (2007). Rapid, transient induction of ER stress in the liver and kidney after acute exposure to heavy metal: Evidence from transgenic sensor mice. FEBS Lett. 581, 2055-2059.
18. Hu, J., Mao, Y., and White, P. (2002). Canadian Cancer Registries Epidemiology Research Group. Renal cell carcinoma and occupational exposure in Canada. Occup. Med. 52, 157-164.
19. IARC. (1993). Beryllium, cadmium, mercury, and exposures in the glass manufacturing industry, Monographs on the Evaluation of Carcinogenic Risk to Humans, Vol. 58, pp. 119-238, International Agency For Research On Cancer, Lyon, France.
20. Jacquillet, G., Barbier, O., Cougnon, M., Tauc, M., Namorado, M., Martin, D., Reyes, J. L., and Poujeol, P. (2006). Zinc protects renal function during cadmium intoxication in the rat. Am. J. Physiol. Renal Physiol. 290, F127-F137.
21. Järup, L. (2003). Hazards of heavy metal contamination. Brit. Med. Bull. 68, 167-182.
22. Järup, L., and Åkesson, A. (2009). Current status of cadmium as an environmental health problem. Toxicol. Appl. Pharmacol. 238, 201-208.
23. Jianga, G., Duana, W., Xub, L., Songa, S., Zhua, C., and Wua, L. (2009). Biphasic effect of cadmium on cell proliferation in human embryo lung fibroblast cells and its molecular mechanism. Toxicol. In Vitro. 23, 973-978.
24. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728.
25. Kamunde, C. (2009). Early subcellular partitioning of cadmium in gill and liver of rainbow trout (Oncorhynchus mykiss) following low-to-near-lethal waterborne cadmium exposure. Aquat. Toxicol. 91, 291-301.
26. Kawata, K., Shimazaki, R., and Okabe, S. (2009). Comparison of gene expression profiles in HepG2 cells exposed to arsenic, cadmium, nickel, and three model carcinogens for investigating the mechanisms of metal carcinogenesis. Environ. Mol. Mutagen. 50, 46-59.
27. Kim, K. W., Moretti, L., Mitchell, L. R., Jung, D. K., and Lu, B. (2010). Endoplasmic reticulum stress mediates radiation-induced autophagy by perk-eIF2alpha in caspase-3/7-deficient cells. Oncogene 29, 3241-3251.
28. Klionsky, D. J., Abeliovich, H., Agostinis, P., Agrawal, D. K., Aliev, G., Askew, D. S., Baba, M., Baehrecke, E. H., Bahr, B. A., Ballabio, A., et al. (2008). Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175.
29. Koizumi, S., and Yamada, H. (2003). DNA microarray analysis of altered gene expression in cadmium-exposed human cells. J. Occup. Health. 45, 331-334.
30. Kuma, A., Matsui, M., and Mizushima, N. (2007). LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: Caution in the interpretation of LC3 localization. Autophagy 3, 323-328.
31. Lee, W. K., Torchalski, B., and Thévenod, F. (2007). Cadmium-induced ceramide formation triggers calpain-dependent apoptosis in cultured kidney proximal tubule cells. Am. J. Physiol. Cell Physiol. 293, C839-C47.
32. L'hoste, S., Chargui, A., Belfodil, R., Duranton, C., Rubera, I., Mograbi, B., Poujeol, C., Tauc, M., and Poujeol, P. (2009). CFTR mediates cadmiuminduced apoptosis through modulation of ROS level in mouse proximal tubule cells. Free Radic. Biol. Med. 46, 1017-1031.
33. Mao, W. P., Ye, J. L., Guan, Z. B., Zhao, J. M., Zhang, C., Zhang, N. N., Jiang, P., and Tian, T. (2007). Cadmium induces apoptosis in human embryonic kidney (HEK) 293 cells by caspase-dependent and -independent pathways acting on mitochondria. Toxicol. In Vitro 21, 343-354.
34. Mizushima, N., Levine, B., Cuervo, A. M., and Klionsky, D. J. (2008). Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075.
35. National Toxicology Program (NTP). (2000). Tenth Report on Carcinogens In III-42-III-44. Department of Health and Human Services, Research Triangle Park, NC.
36. Ord, M. J., Chibber, R., Bouffler, S. D., and Courtney, T. (1990). Changes in muntjac fibroblasts associated with the acquisition of cadmium resistance. A pre-resistance, transitional and post-resistance study. Arch. Toxicol. 64, 77-90.
37. Roberts, C. A., and Clark, J. M. (1986). Improved determination of cadmium in blood and plasma by flameless atomic absorption spectroscopy. Bull. Environ. Contam. Toxicol. 36, 496-499.
38. Romero, D., Gómez-Zapata, M., Luna, A., and García-Fernóndez, A. J. (2003). Morphological characterisation of BGM (Buffalo Green Monkey) cell line exposed to low doses of cadmium chloride. Toxicol. In Vitro 17, 293-299.
39. Satoh, M., Koyama, H., Kaji, T., Kito, H., and Tohyama, C. (2002). Perspectives on cadmium toxicity research. Tohoku J. Exp. Med. 196, 23-32.
40. Scarlatti, F., Granata, R., Meijer, A. J., and Codogno, P. (2009). Does autophagy have a license to kill mammalian cells? Cell Death Differ. 16, 12-20.
41. Singh, K. P., Kumari, R., Pevey, C., Jackson, D., and Dumond, J. W. (2009). Long duration exposure to cadmium leads to increased cell survival, decreased DNA repair capacity, and genomic instability in mouse testicular Leydig cells. Cancer Lett. 279, 84-92.
42. Tanimoto, A., Hamada, T., and Koide, O. (1993). Cell death and regeneration of renal proximal tubular cells in rats with subchronic cadmium intoxication. Toxicol. Pathol. 21, 341-352.
43. Thévenod, F. (2009). Cadmium and cellular signaling cascades: To be or not to be? Toxicol. Appl. Pharmacol. 238, 221-239.
44. Thévenod, F., and Friedmann, J. M. (1999). Cadmium-mediated oxidative stress in kidney proximal tubule cells induces degradation of Na+/K+-ATPase through proteasomal and endo-/lysosomal proteolytic pathways. FASEB J. 13, 1751-1761.
45. Wang, S. H., Shih, Y. L., Ko, W. C., Wei, Y. H., and Shih, C. (2008). Cadmium-induced autophagy and apoptosis are mediated by a calcium signaling pathway. Cell Mol. Life Sci. 65, 3640-3652.
46. Wang, S. H., Shih, Y. L., Kuo, T. C., Ko, W. C., and Shih, C. M. (2009). Cadmium toxicity toward autophagy through ROS-activated GSK-3beta in mesangial cells. Toxicol. Sci. 108, 124-131.
47. World Health Organization (WHO) (2004). Cadmium in Drinking-Water Background document for development of WHO Guidelines for Drinking-Water Quality. World Health Organization, Geneva, Switzerland.
48. Xie, Z., and Klionsky, D. J. (2007). Autophagosome formation: Core machinery and adaptations. Nat. Cell. Biol. 9, 1102-1109.
49. Yokouchi, M., Hiramatsu, N., Hayakawa, K., Kasai, A., Takano, Y., Yao, J., and Kitamura, M. (2007). Atypical, bidirectional regulation of cadmiuminduced apoptosis via distinct signaling of unfolded protein response. Cell Death Differ. 14, 1467-1474.
50. Yokouchi, M., Hiramatsu, N., Hayakawa, K., Okamura, M., Du, S., Kasai, A., Takano, Y., Shitamura, A., Shimada, T., Yao, J., et al. (2008). Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J. Biol. Chem. 283, 4252-4260.
51. Zalups, R. K. (2000). Evidence for basolateral uptake of cadmium in the kidneys of rats. Toxicol. Appl. Pharmacol. 164, 15-23.