Cadmium-induced germline apoptosis in caenorhabditis elegans: The roles of HUS1, p53, and MAPK signaling pathways

Toxicological Sciences

Volumn 102, Issue 2, 2008, Pages 345-351

  Wang, Shunchang ^a,b   Tang, Minli ^a   Pei, Bei ^a   Xiao, Xiang ^a   Wang, Jun ^a   Hang, Haiying ^c   Wu, Lijun ^a  

^a INSTITUTE OF PLASMA PHYSICS   (China)

^b HUAINAN NORMAL UNIVERSITY   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

Author keywords

Apoptosis; Cadmium; Caenorhabditis elegans; HUS1; MAPK; p53

Indexed keywords

CADMIUM; CELL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN HUS1; PROTEIN P53; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DOSE TIME EFFECT RELATION; GAMMA IRRADIATION; GENE MUTATION; GENOTOXICITY; GERM CELL; KNOCKOUT GENE; LETHAL DOSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CADMIUM CHLORIDE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; GENE SILENCING; GERM CELLS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 40949114546     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfm220     Document Type: Article

References (40)

1. Achanzar, W. E., Achanzar, K. B., Lewis, J. G., Webber, M. M., and Waalkes, M. P. (2000). Cadmium induces c-myc, p53, and c-jun expression in normal human prostate epithelial cells as a prelude to apoptosis. Toxicol. Appl. Pharmacol. 164, 291-300.
2. Anderson, G. L., Cole, R. D., and Williams, P. L. (2004). Assessing behavioral toxicity with Caenorhabditis elegans. Environ. Taxicol. Chem. 23, 1235-1240.
3. Caffrey, D. R., O'Neill, L. A., and Shields, D. C. (1999). The evolution of the MAP kinase pathways: Co-duplication of interacting proteins leads to new signaling cascades. J. Mol. Evol. 49, 567-582.
4. Chao, J. I., and Yang, J. L. (2001). Opposite roles of ERK and p38 mitogen-activated protein kinases in cadmium-induced genotoxicity and mitotic arrest. Chem. Res. Toxicol. 14, 1193-1202.
5. 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 (Oxf) 21, 1423-1432.
6. Chuang, S. M., and Yang, J. L. (2001). Comparison of roles of three mitogen-activated protein kinases induced by chromium(VI) and cadmium in nonsmall-cell lung carcinoma cells. Mol. Cell. Biochem. 222, 85-95.
7. Deng, X., Hofmann, E. R., Villanueva, A., Hobert, O., Capodieci, P., Veach, D. R., Yin, X., Campodonico, L., Glekas, A., Cordon-Cardo, C., et al. (2004). Caenorhabditis elegans ABL-1 antagonizes p53-mediated germline apoptosis after ionizing irradiation. Nat. Genet. 36, 906-912.
8. Derry, W. B., Patzke, A. P., and Rothman, J. H. (2001). Caenorhabditis elegans p53: Role in apoptosis, meiosis, and strew sesistance. Science 294, 591-595.
9. Galan, A., Garcia-Bermejo, M. L., Troyano, A., Vilaboa, N. E., de Blas, E., Kazanietz, M. G., and Aller, P. (2000). Stimulation of p38 mitogen-activated protein kinase is an early regulatory event for the cadmium-induced apoptosis in human promonocytic cells. J. Biol. Chem. 275, 11418-11424.
10. Gartner, A., Milstein, S., Ahmed, S., Hodgkin, J., and Hengartner, M. O. (2000). A conserved checkpoint pathway Mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol. Cell. 5, 435-443.
11. Gumienny, T. L., Lambie, E., Hartwieg, E., Horvitz H. R., and Hengartner, M. O. (1999). Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126, 1011-1022.
12. Habeebu, S. S., Liu, J., and Klaassen, C. D. (1998). Cadmium-induced apoptosis in mouse liver. Toxicol. Appl. Pharmacol. 149, 203-209.
13. Harada, H., Kurauchi, M., Hayashi, R., and Eki, T. (2007). Shortened lifespan of nematode Caenorhabditis elegans after prolonged exposure to heavy metals and detergents. Ecotoxicol. Environ. Saf. 66, 378-383.
14. Harstad, E. B., and Klaassen, C. D. (2002). Tumor necrosis factor-a-null mice are not resistant to cadmium chloride-induced hepatotoxicity. Toxicol. Appl. Pharmacol. 179, 155-162.
15. Hofmann, E. R., Milstein, S., Boulton, S. J., Ye, M., Hofmann, J. J., Stergiou, L., Gartner, A., Vidal, M., and Hengartner, M. O. (2002). Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoposis. Curr. Biol. 12, 1908-1918.
16. Hung, J. J., Cheng, T. J., Lai, Y. K., and Chang, M. D. (1998). Differential activation of p38 mitogen-activated protein kinase and extracellular signal-regulated protein kinases confers cadmiuminduced HSP70 expression in 9L rat brain tumor cells. J. Biol.Chem. 273 31924-31931.
17. Ihle, J. N. (2000). The challenges of translating phenotypes into gene function. Cell 102, 131-134.
18. Johnson, G. L., and Lapadat, R. (2002). Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinase. Science 298, 1911-1912.
19. Kelly, K. O., Demburg, A. F., Stanfield, G. M., and Villeneuve, A. M. (2000). Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156, 617-630.
20. Kim, D. H., Feinbaum, R., Alloing, G., Emerson, F. E., Garsin, D. A., Inoue, H., Tanaka-Hino, M., Hisamoto, N., Matsumoto, K., Tan, M. W., et al. (2002). A conserved p38 MAP kinose pathway in Caenorhabditis elegans innate immunity. Science 297, 623-626.
21. Kim, D. H., Liberati, N. T., Mizuno, T., Inoue, H., Hisamoto, N., Matsumoto, K., and Ausubel, F. M. (2004). Integration of Caenorhabditis elegans MAPK pathways mediating immunity and stress resistance by MEK-1 MAPK kinase and VHP-1 MAPK phosphatase. Proc. Natl. Acad. Sci. U.S.A. 101, 10990-10994.
22. Kim, J., and Sharma, R. P. (2004). Calcium-mediated activation of c-Jun NH2-terminal kinase (INK) and apoptosis in response to cadmium in murine macrophages. Toxicol. Sci. 81, 518-527.
23. Kim, S. D., Moon, C. K., Eun, S., Ryu, P. D., and Jo, S. A. (2005). Identification of ASK1, MKK4, JNK, c-Jun, and caspase-3 as a signaling cascade involved in cadmium-induced neuronal cell apoptosis. Biochem. Biophys. Res. Commun. 328, 326-334.
24. Koga, M., Zwaal, R., Guan, K., Avery, L., and Oshima, Y. (2000). A Caenorhabditis elegans MAP kinase kinase, MEK-1, is involved in stress responses. EMBO J. 19, 5148-5156.
25. Kondoh, M., Araragi, S., Sato, K., Higashimoto, M., Takiguchi, M., and Sato, M. (2002). Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170, 111-117.
26. Låg, M., Refsnes, M. M., Lilleaas, E. M., Holme, J. A., Becher, R., and Schwarze, P. E. (2005). Role of mitogen activated protein kinases and protein kinase C in cadmium-induced apoptosis of primary epithelial lung cells. Toxicology 211, 253-264.
27. Låg, M., Westly, S., Lerstad, T., Bjornsrud, C., Refsnes, M., and Schwarze, P. E. (2002). Cadmium-induced apoptosis of primary epithelial lung cells: Involvement of Bax and p53, but not of oxidative stress. Cell Biol. Toxicol. 18, 29-42.
28. Mizuno, T., Hisamoto, N., Terada, T., Kondo, T., Adachi, M., Nishida, E., Kim, D. H., Ausubel, F. M., and Matsumoto, K. (2004). The Caenorhabditis elegans MAPK phosphatase VHP-1 mediates a novel JNK-like-signaling pathway in stress response. EMBO J. 23, 2226-2234.
29. Nawrot, T., Plusquin, M., Hogervorst, J., Roels, H. A., Celis, H., Thijs, L., Vangronsveld, J., Van Hecke, E., and Staessen, J. A. (2006). Environmental exposure to cadmium and risk of cancer: A prospective population-based study. Lancet Oncol. 7, 119-126.
30. Ono, K., and Han, J. (2000). The p38 signal transduction pathway: Activation and function. Cell Signalling 12, 1-13.
31. Papadakis, E. S., Finegan, K. G., Wang, X., Robinson, A. C., Guo, C., Kayahara, M., and Tournier, C. (2006). The regulation of Bax by c-Jun N-terminal protein kinase (JNK) is a prerequisite to the mitochondrial- induced apoptotic pathway. FEBS Lett. 580, 1320-1326.
32. Pearson, G., Robinson, F., Gibson, T. B., Xu, B. E., Karandikar, M., Berman, K., and Cobb, M. H. (2001). Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr. Rev. 22, 153-183.
33. Pham, T. N. D., Marion, M., Denizeau, F., and Jumarie, C. (2006). Cadmium-induced apoptosis in rat hepatocytes does not necessarily involve caspase-dependent pathways. Toxicol. In Vitro 20, 1331-1342.
34. Roos, W. P., and Kaina, B. (2006). DNA damage-induced cell death by apoptosis. Trends Mol. Med. 12, 440-450.
35. Salinas, L. S., Maldonado, E., and Navarro, R. E. (2006). Stress-induced germ cell apoptosis by a p53 independent pathway in Caenorhabditis elegans. Cell Death Differ. 13, 2129-2139.
36. Stergiou, L., and Hengartner, M. O. (2004). Death and more: DNA damage response pathways in the nematode C. elegans. Cell Death Differ. 11, 21-28.
37. Sulston, J., and Hodgkin, J. (1988). Methods. In The Nematode Caenorhabditis elegans (W. B. Wood, Ed.), pp. 587-606. Cold. Spring Harbor Laboratory, New York.
38. Wang, S., Zhao, Y., Wu, L., Tang, M., Su, C., Hei, T. K., and Yu, Z. (2007). Induction of germline cell cycle arrest and apoptosis by sodium arsenite in Caenorhabditis elegans. Chem. Res. Toxicol. 20, 181-186.
39. Wang, X., Mcgowan, C. H., Zhao, M., He, L., Downey, J. S., Fearns, C., Wang, Y., Huang, S., and Han, J. (2000). Involvement of the MKK6-p38 cascade in γ-radiation-induced cell cycle arrest. Mol. Cell. Biol. 20, 4543-4552.
40. Williams, P. L., and Dusenbery, D. B. (1990). Aquatic toxicity testing using the nematode Caenorhabditis elegans. Environ. Taxicol. Chem. 9, 1285-1290.