Cadmium-induced activation of stress signaling pathways, disruption of ubiquitin-dependent protein degradation and apoptosis in primary rat sertoli cell-gonocyte cocultures

Toxicological Sciences

Volumn 104, Issue 2, 2008, Pages 385-396

  Yu, Xiaozhong ^a   Hong, Sungwoo ^a   Faustman, Elaine M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cadmium; Male reproductive toxicity; Sertoli cell gonocyte coculture; Stress signaling; Ubiquitin proteasome system

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CADMIUM; LACTACYSTIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEASOME; PROTEIN P53; STRESS ACTIVATED PROTEIN KINASE; UBIQUITIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CADMIUM POISONING; CELL CULTURE; CELL STRUCTURE; CELL VIABILITY; CELLULAR STRESS RESPONSE; COCULTURE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME PHOSPHORYLATION; IN VITRO STUDY; MALE; NONHUMAN; PROTEIN DEGRADATION; RAT; SERTOLI CELL; SIGNAL TRANSDUCTION; TESTIS DISEASE; UBIQUITINATION; UPREGULATION;

ACETYLCYSTEINE; ANIMALS; APOPTOSIS; CADMIUM COMPOUNDS; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; CYSTEINE PROTEINASE INHIBITORS; DOSE-RESPONSE RELATIONSHIP, DRUG; LEUPEPTINS; MALE; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, SPRAGUE-DAWLEY; SERTOLI CELLS; SIGNAL TRANSDUCTION; SPERMATOGONIA; UBIQUITINS;

ANIMALIA; RATTUS;

EID: 47849129524     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn087     Document Type: Article

References (62)

1. Araya, J., Maruyama, M., Inoue, A., Fujita, T., Kawahara, J., Sassa, K., Hayashi, R., Kawagishi, Y., Yamashita, N., Sugiyama, E., et al. (2002). Inhibition of proteasome activity is involved in cobalt-induced apoptosis in human alveolar macrophages. Am. J. Physiol. Lung Cell Mol. Physiol. 283, L849-L858.
2. Baarends, W. M., Hoogerbrugge, J. W., Roest, H. P., Ooms, M., Vreeburg, J., Hoeijmakers, J. H., and Grootegoed, J. A. (1999). Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev. Biol. 207, 322-333.
3. Ben-Neriah, Y. (2002). Regulatory functions of ubiquitination in the immune system. Nat. Immunol. 3, 20-26.
4. Bobba, A., Canu, N., Atlante; A., Petragallo, V., Calissano, P., and Marra, E. (2002). Proteasome inhibitors prevent cytochrome c release during apoptosis but not in excitotoxic death of cerebellar granule neurons. FEBS Lett. 515, 8-12.
5. Borenfreund, E., and Puerner, J. A. (1985). Toxicity determined in vitro by morphological alterations and neutral red absorption. Toxicol. Lett. 24, 119-124.
6. Canu, N., Barbaro, C., Ciotti, M. T., Serafino, A., Dus, L., and Calissano, P. (2000). Proteasome involvement and accumulation of ubiquitinated proteins in cerebellar granule neurons undergoing apoptosis. J. Neurosci. 20, 589-599.
7. Chen, F., Chang, D., Goh, M., Klibanov, S., and Ljungman, M. (2000). Role of p53 in cell cycle regulation and apoptosis following exposure to proteasome inhibitors. Cell Growth Differ. 11, 239-246.
8. 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.
9. Derfoul, A., Lin, F. J., Awumey, E. M., Kolodzeski, T., Hall, D. J., and Tuan, R. S. (2003). Estrogenic endocrine disruptive components interfere with calcium handling and differentiation of human trophoblast cells. J. Cell Biochem. 89, 755-770.
10. DiAntonio, A., Haghighi, A. P., Portman, S. L., Lee, J. D., Amaranto, A. M., and Goodman, C. S. (2001). Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412, 449-452.
11. Dickins, R. A., Frew, I. J., House, C. M., O'Bryan, M. K., Holloway, A. J., Haviv, I., Traficante, N., de Kretser, D. M., and Bowtell, D. D. (2002). The ubiquitin ligase component Siah1a is required for completion of meiosis I in male mice. Mol. Cell Biol. 22, 2294-2303.
12. Ding, W., and Templeton, D. (2000). Activation of parallel mitogen-activated protein kinase cascades and induction of c-fos by cadmium. Toxicol. Appl. Pharmacol. 162, 93-99.
13. Dong, W., Simeonova, P. P., Gallucci, R., Matheson, J., Flood, L., Wang, S., Hubbs, A., and Luster, M. I. (1998). Toxic metals stimulate inflammatory cytokines in hepatocytes through oxidative stress mechanisms. Toxicol. Appl. Pharmacol. 151, 359-366.
14. Figueiredo-Pereira, M. E., and Cohen, G. (1999). The ubiquitin/ proteasome pathway: Friend or foe in zinc-, cadmium-, and H2O2-induced neuronal oxidative stress. Mol. Biol. Rep. 26, 65-69.
15. Figueiredo-Pereira, M. E., Yakushin, S., and Cohen, G. (1998). Disruption of the intracellular sulfhydryl homeostasis by cadmium-induced oxidative stress leads to protein thiolation and ubiquitination in neuronal cells. J. Biol. Chem. 273, 12703-12709.
16. Foote, R. H. (1999). Cadmium affects testes and semen of rabbits exposed before and after puberty. Reprod. Toxicol. 13, 269-277.
17. Fridman, O., Corro, L., and Herkovits, J. (2004). Estradiol uptake, toxicity, metabolism, and adverse effects on cadmium-treated amphibian embryos. Environ. Health Perspect. 112, 862-866.
18. Garrington, T. P., and Johnson, G. L. (1999). Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr. Opin. Cell Biol. 11, 211-218,
19. Gennart, J. P., Buchet, J. P., Roels, H., Ghyselen, P., Ceulemans, E., and Lauwerys, R. (1992). Fertility of male workers exposed to cadmium, lead, or manganese. Am. J. Epidemiol. 135, 1208-1219.
20. Henson, M. C., and Chedrese, P. J. (2004). Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp. Biol. Med. (Maywood) 229, 383-392.
21. Hew, K. W., Ericson, W. A., and Welsh, M. (1993). A single low cadmium dose causes failure of spermiation in the rat. Toxicol. Appl. Pharmcol. 121, 15-21.
22. Iryo, Y., Matsuoka, M., Wispriyono, B., Sugiura, T., and Igisu, H. (2000). Involvement of the extracellular signal-regulated protein kinase (ERK) pathway in the induction of apoptosis by cadmium chloride in CCRF-CEM cells. Biochem. Pharmacol. 60, 1875-1882.
23. Johnson, M. D., Kenney, N., Stoica, A., Hilakivi-Clarke, L., Singh, B., Chepko, G., Clarke, R., Sholler, P. F., Lirio, A. A., Foss, C., et al. (2003). Cadmium mimics the in vivo effects of estrogen in the uterus and mammary gland. Nat. Med. 9, 1081-1084.
24. Jungmann, J., Reins, H. A., Schobert, C., and Jentsch, S. (1993). Resistance to cadmium mediated by ubiquitin-dependent proteolysis. Nature 361, 369-371.
25. Jurczuk, M., Brzoska, M. M., Moniuszko-Jakoniuk, J., Galazyn-Sidorczuk, M., and Kulikowska-Karpinska, E. (2004). Antioxidant enzymes activity and lipid peroxidation in liver and kidney of rats exposed to cadmium and ethanol. Food Chem. Toxicol. 42, 429-438.
26. Kirkpatrick, D., Dale, K., Catania, J., and Gandolfi, A. (2003). Low-level arsenite causis accumulation of ubiquitinated proteins in rabbit renal cortical slices and HERK293 cells. Toxicol. Appl. Pharmacol. 186, 101-109.
27. Kon, Y., Endoh, D., and Iwanaga, T. (1999). Expression of protein gene product 9.5, a neuronal ubiquitin C-terminal hydrolase, and its developing change in sertoli cells of mouse testis. Mol. Reprod. Dev. 54, 333-341.
28. Kwon, J., Kikuchi, T., Setsuie, R., Ishii, Y., Kyuwa, S., and Yoshikawa, Y. (2003). Characterization of the testis in congenitally ubiquitin carboxy-terminal hydrolase-1 (Uch-L1) defective (gad) mice. Exp. Anim. 52, 1-9.
29. Kwon, J., Wang, Y. L., Setsuie, R., Sekiguchi, S., Sakurai, M., Sato, Y., Lee, W. W., Ishii, Y., Kyuwa, S., Noda, M., et al. (2004). Developmental regulation of ubiquitin C-terminal hydrolase isozyme expression during spermatogenesis in mice. Biol Reprod. 71, 515-521.
30. Laskey, J. W., Rehnberg, G. L., Laws, S. C., and Hein, J. F. (1984). Reproductive effects of low acute doses of cadmium chloride in adult male rats. Toxicol. Appl. Pharmacol. 73, 250-255.
31. Laskey, J. W., Rehnberg, G. L., Laws, S. C., and Hein, J. F. (1986). Age-related dose response of selected reproductive parameters to acute cadmium chloride exposure in the male Long-Evans rat. J. Toxicol. Environ. Health 19, 393-401.
32. Li, M., Chen, D., Shiloh, A., Luo, J., Nikolaev, A. Y., Qin, J., and Gu, W. (2002). Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416, 648-653.
33. Lopez Salon, M., Morelli, L., Castano, E. M., Soto, E. F., and Pasquini, J. M. (2000). Defective ubiquitination of cerebral proteins in Alzheimer's disease. J. Neurosci. Res. 62, 302-310.
34. Maki, C. G., Huibregtse, J. M., and Howley, P. M. (1996). In vivo ubiquitination and proteasome-mediated degradation of p53(1). Cancer Res. 56, 2649-2654.
35. Marx, J. (2002). Cell biology. Ubiquitin lives up to its name. Science 297, 1792-1794.
36. Matsuoka, M., and Igisu, H. (2001). Cadmium induces phosphorylation of p53 at serine 15 in MCF-7 cells. Biochem. Biophys. Res. Commun. 282, 1120-1125.
37. Mukherjee, A., Gin, A. K., Shanna, A., and Talukder, G. (1988). Relative efficacy of short-term tests in detecting genotoxic effects of cadmium chloride in mice in vivo. Mutat. Res. 206.
38. Nebreda, A. R., and Porras, A. (2000). p38 MAP kinases: Beyond the stress response. Trends Biochem. Sci. 25, 257-260.
39. Ng, J. M., Vrieling, H., Sugasawa, K., Ooms, M. P., Grootegoed, J. A., Vreeburg, J. T., Visser, P., Beems, R. B., Gorgels, T. G., Hanaoka, F., et al. (2002). Developmental defects and male sterility in mice lacking the ubiquitin-like DNA repair gene mHR23B. Mol. Cell Biol. 22, 1233-1245.
40. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., et al. (1995). Identification and inhibition of the ICE/ CED-3 protease necessary for mammalian apoptosis. Nature 376 37-43.
41. NIP. (1995). Toxicity studies of cadmium oxide (CAS No. 1306-19-0) administered by inhalation to F344/N rats and B6C3F1 mice. Toxic. Rep. Ser. 39, 1-D3.
42. Pagano, M., Tam, S. W., Theodoras, A. M., Beer-Romero, P., Del Sal, G., Chan, V., Yew, P. R., Draetta, G. F., and Rolfe, M. (1995). Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269, 682-685.
43. Rajapurohitam, V., Bedard, N., and Wing, S. S. (2002). Control of ubiquitination of proteins in rat tissues by ubiquitin conjugating enzymes and isopeptidases. Am. J. Physiol. Endocrinol. Metab. 282, E739-E745.
44. Rawe, V. Y., Olmedo, S. B., Benmusa, A., Shiigi, S. M., Chemes, H. E., and Sutovsky, P. (2002). Sperm ubiquitination in patients with dysplasia of the fibrous sheath. Hum. Reprod. 17, 2119-2127.
45. Rodgers, K. J., and Dean, R. T. (2003). Assessment of proteasome activity in cell lysates and tissue homogenates using peptide substrates. Int. J. Biochem. Cell Biol. 35, 716-727.
46. Roest, H. P., van Klaveren, J., de Wit, J., van Gurp, C. G., Koken, M. H., Vermey, M., van Roijen, J. H., Hoogerbrugge, J. W., Vreeburg, J. T., Baarends, W. M., et al. (1996). Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 86, 799-810.
47. Satarug, S., Ujjin, P., Vanavanitkun, Y., Baker, J. R., and Moore, M. R. (2004). Influence of body iron store status and cigarette smoking on cadmium body burden of healthy Thai women and men. Toxicol. Lett. 148, 177-185.
48. Schulman, B. A., Carrano, A. C., Jeffrey, P. D., Bowen, Z., Kinnucan, E. R., Finnin, M. S., Elledge, S. J., Harper, J. W., Pagano, M., and Pavletich, N. P. (2000). Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408, 381-386.
49. Sen Gupta, R., Kim, J., Gomes, C., Oh, S., Park, J., Im, W. B., Seong, J. Y., Ahn, R. S., Kwon, H. B., and Soh, J. (2004). Effect of ascorbic acid supplementation on testicular steroidogenesis and germ cell death in cadmium-treated male rats. Mol. Cell. Endocrinol. 221, 57-66.
50. Shaikh, Z. A., Vu, T. T., and Zaman, K. (1999). Oxidative stress as a mechanism of chronic cadmium-induced hepatotoxicity and renal toxicity and protection by antioxidants. Toxicol. Appl. Pharmacol. 154 256-263.
51. Shi, Y., Melnikov, V. Y., Schrier, R. W., and Edelstein, C. L. (2000). Downregulation of the calpain inhibitor protein calpastatin by caspases during renal ischemia-reperfusion. Am. J. Physiol. Renal. Physiol. 279, F509-F517.
52. Sutovsky, P. (2003). Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: Killing three birds with one stone. Microsc. Res. Tech. 61, 88-102.
53. Sutovsky, P., McCauley, T. C., Sutovsky, M., and Day, B. N. (2003). Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biol. Reprod. 68, 1793-1800.
54. Sutovsky, P., Moreno, R., Ramalho-Santos, J., Dominko, T., Thompson, W. E., and Schatten, G. (2001a). A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J. Cell Sci. 114, 1665-1675.
55. Sutovsky, P., Motlik,. J., Neuber, E., Pavlok, A., Schatten, G., Palecek, J., Hyttel, P., Adebayo, O. T., Adwan, K., Alberio, R., et al. (2001b). Accumulation of the proteolytic marker peptide ubiquitin in the trophoblast of mammalian blastocysts. Cloning Stem Cells 3, 157-161.
56. Sutovsky, P., Terada, Y., and Schatten, G. (2001c). Ubiquitin-based sperm assay for the diagnosis of male factor infertility. Hum. Reprod. 16, 250-258.
57. Wlodarczyk, B., Biernacki, B., Minta, M., Kozaczynski, W., and Juszkiewicz, T. (1995). Male golden hamster in male reproductive toxicology testing: Assessment of protective activity of selenium in acute cadmium toxication. Bull. Environ. Contam. Toxicol. 54 907-912.
58. Yang, C. F., Shen, H. M., Shen, Y., Zhuang, Z. X., and Ong, C. N. (1997). Cadmium-induced oxidative cellular damage in human fetal lung fibroblasts (MRC-5 cells). Environ. Health Perspect. 105, 712-716.
59. Yang, Y., and Yu, X. (2003). Regulation of apoptosis: The ubiquitous way. FASEB J. 17, 790-799.
60. Yen, J. L., Su, N. Y., and Kaiser, P. (2005). The yeast ubiquitin ligase SCFMet30 regulates heavy metal response. Mol. Biol. Cell 16, 1872-1882.
61. Yu, X., Kubota, H., Wang, R., Saegusa, J., Ogawa, Y., Ichihara, G., Takeuchi, Y., and Hisanaga, N. (2001). Involvement of Bcl-2 family genes and Fas signaling system in primary and secondary male germ cell apoptosis induced by 2-bromopropane in rat. Toxicol. Appl. Pharmacol. 174, 35-48.
62. Yu, X., Sidhu, J. S., Hong, S., and Faustman, E. M. (2005). Essential role of extracellular matrix (ECM) overlay in establishing the functional integrity of primary neonatal rat Sertoli cell/gonocyte co-cultures: An improved in vitro model for assessment of male reproductive toxicity. Toxicol. Sci. 84, 378-393.