Induction of Apoptosis in Chicken Oviduct Cells by C2-Ceramide

  • Kim, Sung Hak (Department of Biology, College of Science, Kyung Hee University) ;
  • Choi, Ji Young (Department of Biology, College of Science, Kyung Hee University) ;
  • Sihn, Choon-Ryoul (Department of Biology, College of Science, Kyung Hee University) ;
  • Suh, Eun Jung (Department of Biology, College of Science, Kyung Hee University) ;
  • Kim, Sun Young (School of Agricultural Biotechnology, Seoul National University) ;
  • Choi, Kang Duk (Graduate School of Bio and Information Technology, Hankyong National University) ;
  • Jeon, Iksoo (Laboratory of Transgenic Chicken, Animal Biotechnology Division, National Livestock Research Institute) ;
  • Han, Jae Yong (School of Agricultural Biotechnology, Seoul National University) ;
  • Kim, Tae-Yoon (Department of Dermato-Immunology, The Catholic University of Korea) ;
  • Kim, Sang Hoon (Department of Biology, College of Science, Kyung Hee University)
  • 투고 : 2004.09.17
  • 심사 : 2004.11.22
  • 발행 : 2005.04.30

초록

The chicken oviduct is a dynamic organ that produces secretory proteins such as ovalbumin and its cells undergo cell proliferation and differentiation. There has been no study of the cellular mechanism involved in cell death in the chicken oviduct. Therefore, this study has focused on the study of apoptosis in primary oviduct cells. Because ceramide is known to activate apoptosis in tumor cells and is produced in the oviduct, we used an exogenous ceramide analog to induce cell death. The viability of ceramide-treated chicken oviduct cells decreased in a dose-dependent manner and apoptotic cells were detected by staining with annexin V. The expression of apoptosis-related genes was assessed by RT-PCR and bcl-2 mRNA was found to decrease after exposure to ceramide while Bcl-x mRNA increased 12 h post-treatment. In addition, caspase-3 was expressed strongly in the early stages of apoptosis, while caspase-1 and -9 transcripts increased at later times. We conclude that ceramide induces apoptosis in oviduct-derived primary cells via a caspase- and bcl-2-dependent pathway.

키워드

과제정보

연구 과제 주관 기관 : Rural Development Administration

참고문헌

  1. Ahn, J. H., Ko, Y. G., Park, W. Y., Kang, Y. S., Chung, H. Y., et al. (1999) Suppression of ceramide-mediated apoptosis by HSP70. Mol. Cells 9, 200-206
  2. Cohen, G. M. (1997) Caspases: the executioners of apoptosis. Biochem. J. 326, 1-6
  3. Droin, N., Bichat, F., Rebe, C., Wotawa, A., Sordet, O., et al. (2001) Involvement of caspase-2 long isoform in Fasmediated cell death of human leukemic cells. Blood 97, 1835-1844 https://doi.org/10.1182/blood.V97.6.1835
  4. Futerman, A. H. and Hannun, Y. A. (2004) The complex life of simple sphingolipids. EMBO Rep. 5, 777-782 https://doi.org/10.1038/sj.embor.7400208
  5. Genini, D., Sheeter, D., Rought, S., Zaunders, J., Susin, S. A., et al. (2001) HIV induces lymphocyte apoptosis by a p53- initiated, mitochondrial-mediated mechanism. FASEB J. 15, 5-6
  6. Gibson, L., Holmgreen, S. P., Huang, D. C., Bernard, O., Copeland, N. G., et al. (1996) Bcl-w, a novel member of the bcl-2 family, promotes cell survival. Oncogene 13, 665-675
  7. Hannun, Y. A. and Luberto, C. (2000) Ceramide in the eukaryotic stress response. Trends Cell Biol. 10, 73-80 https://doi.org/10.1016/S0962-8924(99)01694-3
  8. Heryanto, B., Yoshimura, Y., Tamura, T., and Okamoto, T. (1997) Involvement of apoptosis and lysosomal hydrolase activity in the oviducal regression during induced molting in chickens: a cytochemical study for end labeling of fragmented DNA and acid phosphatase. Poult. Sci. 76, 67-72
  9. Janicke, R. U., Sprengart, M. L., Wati, M. R., and Porter, A. G. (1998) Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273, 9357-9360 https://doi.org/10.1074/jbc.273.16.9357
  10. Jeong, K. and Kim-Ha, J. (2003) Expression of Rbp 9 during and mid-oogenesis induces apoptosis in egg chambers. Mol. Cells 16, 392-396
  11. Jung-Testas, I., Garcia, T., and Baulieu, E. E. (1986) Steroid hormones induce cell proliferation and specific protein synthesis in primary chick oviduct cultures. J. Steroid Biochem. 24, 273-279 https://doi.org/10.1016/0022-4731(86)90064-6
  12. Kim, H. J., Kim, H. J., Lim, S. C., Kim, S. H., and Kim, T. Y. (2003) Induction of apoptosis and expression of cell cycle regulatory proteins in response to a phytosphingosine derivative in HaCaT human keratinocyte cells. Mol. Cells 16, 331- 337
  13. Kolesnick, R. N., Haimovitz-Friedman, A., and Fuks, Z. (1994) The sphingomyelin signal transduction pathway mediates apoptosis for tumor necrosis factor, Fas, and ionizing radiation. Biochem. Cell. Biol. 72, 471-474 https://doi.org/10.1139/o94-063
  14. Kolesnick, R. N., Goni, F. M., and Alonso, A. (2000) Compartmentalization of ceramide signaling: physical foundations and biological effects. J. Cell Physiol. 184, 285-300 https://doi.org/10.1002/1097-4652(200009)184:3<285::AID-JCP2>3.0.CO;2-3
  15. Kumar, S. and Colussi, P. A. (1999) Prodomains--adaptors-- oligomerization: the pursuit of caspase activation in apoptosis. Trends Biochem Sci. 24, 1-4 https://doi.org/10.1016/S0968-0004(98)01332-2
  16. Metcalfe, A. D., Gilmore, A., Klinowska, T., Oliver, J., Valentijn, A. J., et al. (1999) Developmental regulation of Bcl-2 family protein expression in the involuting mammary gland. J. Cell Sci. 112, 1771-1783
  17. Miyashita, T., Krajewski, S., Krajewska, M., Wang, H. G., Lin, H. K., et al. (1994) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncegene 9, 1799-1805
  18. Mizushima, N., Koike, R., Kohsaka, H., Kushi, Y., Handa, S., et al. (1996) Ceramide induces apoptosis via CPP32 activation. FEBS Lett. 395, 267-271 https://doi.org/10.1016/0014-5793(96)01050-2
  19. Monroe, D. G., Jin, D. F., and Sanders, M. M. (2000) Estrogen opposes the apoptotic effects of bone morphogenetic protein- 7 on tissue remodeling. Mol. Cell. Biol. 20, 4626-4634 https://doi.org/10.1128/MCB.20.13.4626-4634.2000
  20. Monroe, D. G., Berger, R. R., and Sanders, M. M. (2002) Tissue- protective effects of estrogen involve regulation of caspase gene expression. Mol. Endocrinol. 16, 1322-1331 https://doi.org/10.1210/me.16.6.1322
  21. Nicholson, D. W. and Thornberry, N. A. (1999) Caspases: killer proteases. Trends Biochem Sci. 22, 299-306 https://doi.org/10.1016/S0968-0004(97)01085-2
  22. Reed, J. C. (1999) Mechanism of apoptosis avoidance in cancer. Curr. Opin. Oncol. 11, 68-75 https://doi.org/10.1097/00001622-199901000-00014
  23. Ruvolo, P. P. (2001) Ceramide regulates cellular homeostasis via diverse stress signaling pathways. Leukemia 15, 1153-1160 https://doi.org/10.1038/sj.leu.2402197
  24. Santana, P., Lanes, L., Herndandez, I., Gonzale-Robayana, I., Tabraue, C., et al. (1996) Interleukin -1beta stimulates sphinogmyelin hydrolysis in cultured granulose cells: evidence for a regulatory role of ceramide on progesterone and prostaglandin biosynthesis. Endocrinology 127, 2480-2489
  25. Smyth, M. J., Perry, D. K., Zhang, J., Poirier, G. G., Hannun, Y. A., et al. (1996) prICE: a downstream target for ceramideinduced apoptosis and for the inhibitory action of Bcl-2. Biochem. J. 316, 25-28
  26. Thompson, E. B. (1994) Apoptosis and steroid hormones. Mol. Endocrinol. 8, 665-671 https://doi.org/10.1210/me.8.6.665
  27. Tilly, J. L., Kowalski, K. I., Johnson, A. L., and Hsueh, A. J. (1991) Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinolgy 129, 2799-2801 https://doi.org/10.1210/endo-129-5-2799
  28. Venkataraman, K. and Futerman, A. H. (2000) Ceramide as a second messenger: sticky solutions to sticky problems. Trends Cell Biol. 10, 408-412 https://doi.org/10.1016/S0962-8924(00)01830-4
  29. Verheij, M., Bose, R., Lin, X. H., Yao, B., Jarvis, W. D., et al. (1996) Requirement for ceramide-initiated SAPK/JNK signaling in stress-induced apoptosis. Nature 380, 75-79 https://doi.org/10.1038/380075a0
  30. Vilagrasa, X., Mezquita, C., and Mezquita, J. (1997) Differential expression of bcl-2 and bcl-x during chicken spermatogenesis. Mol. Reprod. Dev. 47, 26-29 https://doi.org/10.1002/(SICI)1098-2795(199705)47:1<26::AID-MRD4>3.0.CO;2-S
  31. Witty, J. P., Bridgham, J. T., and Johnson, A. L. (1996) Induction of apoptotic cell death in hen granulose cells by ceramide. Endocrinology 137, 5269-5277 https://doi.org/10.1210/en.137.12.5269
  32. Zhang, P., Liu, B., Kang, S. W., Seo, M. S., Rhee, S. G., et al. (1997) Thioredoxin peroxidase is a novel inhibitor of apoptosis with a mechanism distinct from that of Bcl-2. J. Biol. Chem. 272, 30615-30618 https://doi.org/10.1074/jbc.272.49.30615
  33. Zhang, H., Heim, J., and Meyhack, B. (1999) Novel BNIP1 variants and their interaction with BCL2 family members. Fed. Eur. Biochem. Sci. Lett. 448, 23-27 https://doi.org/10.1016/S0014-5793(99)00335-X