- Volume 18 Issue 5
DOI QR Code
Inducible Nitric Oxide Synthase Expression and Luteal Cell DNA Fragmentation of Porcine Cyclic Corpora Lutea
- Tao, Yong (Department of Animal Physiology and Biochemistry, College of Biological Sciences, China Agricultural University) ;
- Fu, Zhuo (Department of Animal Physiology and Biochemistry, College of Biological Sciences, China Agricultural University) ;
- Xia, Guoliang (Department of Animal Physiology and Biochemistry, College of Biological Sciences, China Agricultural University) ;
- Lei, Lei (Department of Animal Physiology and Biochemistry, College of Biological Sciences, China Agricultural University) ;
- Chen, Xiufen (Department of Animal Physiology and Biochemistry, College of Biological Sciences, China Agricultural University) ;
- Yang, Jie (Department of Animal Physiology and Biochemistry, College of Biological Sciences, China Agricultural University)
- Received : 2004.05.05
- Accepted : 2004.11.19
- Published : 2005.05.01
Nitric oxide (NO) derived from inducible nitric oxide synthase (iNOS) is involved in cell apoptosis, which contributes to luteal regression and luteolysis in some species. In large domestic animals, no direct evidence for the relationship between NO and cell apoptosis in the process of corpus luteum regression is reported. The present study was conducted to investigate the localization of iNOS on porcine corpora lutea (CL) during the oestrus cycle and its relation to cell DNA fragmentation and CL regression. According to morphology, four luteal phases throughout the estrous cycle were defined as CL1, CL2, CL3 and CL4. By isoform-specific antibody against iNOS, the immunochemial staining was determined. Luteal cell DNA fragmentation was determined by flow cytometry. The results showed that no positive staining for iNOS was in CL1 and that iNOS was produced but limited to the periphery of CL2, while in the CL3, the spreading immunochemical staining was found inside the CL. No iNOS positive staining was detected in CL4. Meanwhile, DNA fragmentation increased dramatically when CL developed from CL2 to CL3 (p<0.05). In CL4, higher proportion of luteal cells still had fragmented DNA than that of luteal cells from CL1 or CL2 (p<0.05). These results indicate that iNOS expression is closely related to luteal cell apoptosis and then to luteal regression.
Nitric Oxide Synthase;Corpora Lutea;Apoptosis;Estrous Cycle
Supported by : National Outstanding Youth Foundation of China, Beijing Natural Science Foundation
- Boone, D. L. and B. K. Tsang. 1998. Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol. Reprod. 58:1533-1539.
- Goodman, S. B., K. Kugu, S. H. Chen, S. Preutthipan, K. I. Tilly, J. L. Tilly and A. M. Dharmarajan. 1998. Estradiol-mediated suppression of apoptosis in the rabbit corpus luteum is associated with a shift in expression of bcl-2 family members favoring cellular survival. Biol. Reprod. 59:820-827.
- Gregoraszczuk, E. L. 1992. Interrelations between steroid hormone secretion and morphological changes of porcine corpora lutea at various periods of luteal phase. Endocr. Regul. 26:189-194.
- Juengel, J. L., H. A. Garverick, A. L. Johnson, R. S. Youngquist and M. F. Smith. 1993. Apoptosis during luteal regression in cattle. Endocrinology 132:249-254.
Moeljono, M. P. E., R. W. Bazer and W. W. Thatcher. 1976. A study of prostaglandin F2
$\alpha$as the luteolysin in swine. I. Effect of prostaglandin F2 $\alpha$in hysterectomized gilts. Prostaglandins 11:737-743.
- Roughton, S. A., R. R. Lareu, A. H. Bittles and A. M. Dharmarajan. 1999. Fas and Fas ligand messenger ribonucleic acid and protein expression in the rat corpus luteum during apoptosismediated luteolysis. Biol. Reprod. 60:797-804.
- Rueda, B. R., I. R. Hendry, W. I. Hendry III, F. Stormshak, O. D. Slayden and J. S. Davis. 2000. Decreased progesterone levels and progesterone receptor antagonists promote apoptotic cell death in bovine luteal cells. Biol. Reprod. 62:269-276.
- Takesue, K., S. Tabata, F. Sato and M. A. Hattori. 2003. Expression of nitric oxide synthase-3 in porcine oocytes obtained at different follicular development. J. Reprod. Dev. 49:135-140.
- Takiguchi, S., N. Sugino, K. Esato, A. Karube-Harada, A. Sakata, Y. Nakamura, H. Ishikawa and H. Kato. 2004. Differential regulation of apoptosis in the corpus luteum of pregnancy and newly formed corpus luteum after parturition in rats. Biol. Reprod. 70:313-318.
- Vega, M., L. Urrutia, G. Iniguez, F. Gabler, L. Devoto and M. C. Johnson. 2000. Nitric oxide induces apoptosis in the human corpus luteum in vitro. Mol. Hum. Reprod. 6:681-687.
- Gadsby, J. E., J. A. Lovdal, S. Samaras, J. S. Barber and J. M. Hammond. 1996. Expression of the messenger ribonucleic acids for insulin-like growth factor-I and insulin-like growth factor binding proteins in porcine corpora lutea. Biol. Reprod. 54:339-346.
- Bacci, M. L., A. M. Barazzoni, M. Forni and G. L. Costerbosa. 1996. In situ detection of apoptosis in regressing corpus luteam of pregneant sow: evidence of an early presence of DNA fragmentation. Domest Anim. Endocrinol. 13:361-372.
- Shukovski, L. and A. Tsafriri. 1994. The involvement of nitric oxide in the ovulatory process in the rat. Endocrinology 135:2287-2290.
- Ziecik, A. J. 2002. Old, new and the newest concepts of inhibition ofluteolysis during early pregnancy in pig. Domest. Anim. Endocrinol. 23:265-275. https://doi.org/10.1016/S0739-7240(02)00162-5
- Gebarowska,D., A. J. Ziecik and E. L. Gregoraszczuk. 1997. Luteinizing hormone receptors on granulosa cells from preovulatory follicles and luteal cells throughout the oestrous cycle of pigs. Anim. Reprod. Sci. 49:191-205.
- Bu, S. M., G. L. Xia, Y. Tao, L. Lei and B. Zhou. 2003. Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol. Cell Endocrinol. 207:21-30.
- Gregoraszczuk, E. L. 1983. Steroid hormone release in cultures of pig corpus luteum and granulosa cells: effect of LH, hCG, PRL and Estradiol. Endocrinol. Exp. 17:59-63.
Chun, S. Y., K. M. Eisenhauer, M. Kubo and A. J. Hsueh. 1995. Interleukin-1
$\beta$supresses apoptosis is rat ovarian follicles by increasing nitric oxide production. Endocrinology 136:3120-3127.
- Kerr, J. F. R., A. H. Wyllie and A. D. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239-257.
- Boiti, C., G. Guelfi, M. Zerani, D. Zampini, G. Brecchia and A. Gobbetti. 2004. Expression patterns of cytokines, p53 and nitric oxide synthase isoenzymes in corpora lutea of pseudopregnant rabbits during spontaneous luteolysis. Reproduction 127:229-238.
- Grasselli, F., N. Ponderato, G. Basini and C. Tamanini. 2001. Nitric oxide synthesis expression and nitric oxide/cyclic GMP pathway in swine cumulus cells. Domest Anim. Endocrinol. 20:241-52. https://doi.org/10.1016/S0739-7240(01)00096-0
- Jablonka-Shariff, A. and L. M. Olson. 1997. Hormonal regulation of nitric oxide synthases and their cell-specific expression during follicular development in the rat ovary. Endocrinology 138:460-468.
- Ptak, A., M. Kajta and E. L. Gregoraszczuk. 2004. Effect of growth hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured luteal cells collected from early, mature, and regressing porcine corpora lutea. Anim. Reprod. Sci. 80:267-279.
- Yoon, S. J., K. H. Choi and K. A. Lee. 2002. Nitric oxide-mediated inhibition of follicular apoptosis is associated with HSP70 induction and Bax suppression. Mol. Reprod. Dev. 61:504-510.
- Dimmeler, S. and A. M. Zeiher. 1997. Nitric oxide and apoptosis: another paradigm for the double-edged role of nitric oxide. Nitric Oxide 1:275-281.
- Ge, Z., W. E. Nicholson, D. M. Plotner, C. E. Farin and J. E. Gadsgy. 2000. Insulin-like growth factor I receptor mRNA and protein expression in pig corpora lutea. J. Reprod. Fertil. 120:109-114.
- Ptak, A. and E. L. Gregoraszczuk. 2003. Growth hormone and insulin-like growth factor-I action on progesterone secretion by porcine corpora lutea isolated at various periods of the luteal phase, Acta Veterinaria Hungarica 51:197-208.
- Faletti, A., M. S. Perez, C. Perotti and M. A. de Gimeno. 1999. Activity of ovarian nitric oxide synthase (NOS) during ovulatory process in the Rat: Relationship with prostaglandins (PGs) Production. Nitric Oxide 3:340-347.
- Tao, Y., G. L. Xia, S. M. Bu, B. Zhou, M. J. Zhang and F. C. Wang. 2004a. Nitric oxide exerts different functions on porcine oocytes cultured in different models, which is affected by betamercaptoethanol. Asian-Aust. J. Anim. Sci. 17:317-324.
- Motta, A. B., A. Estevez, T. Tognetti, M. A. F. Gimeno and A. M. Franchi. 2001. Dual effects of nitric oxide in functional and regressing rat corpus luteum. Mol. Hum. Reprod. 7:43-47.
- Nicholson, W. C., Z. Ge, D. M. Plotner, C. E. Farin and J. E. Gadsby. 1999. Insulin-like growth factor (IGF)-I, IGF-I receptor, and IGF binding protein-3 messenger ribonucleic acids and protein in corpora lutea from prostaglandin F(2alpha)-treated gilts. Biol. Reprod. 61:1527-1534.
- Bu, S. M., G. L. Xia, H. R. Xie and Y. Guo. 2002. Nitric oxide derived from cumulus cells promotes the meiotic resumption in mouse. Chinese Science Bulletin 47:1730-1733.
- Gaytan, F., C. Bellido, C. Morales and J. E. Sanchez-Criado. 1998. Both prolactin and progesterone in proestrus are necessary for the induction of apoptosis in the regressing corpus luteum of the rat. Biol. Reprod. 59:1200-1206.
- Tao, Y., B. Zhou, G. L. Xia, F. C. Wang, Z. L. Wu and M. Y. Fu. 2004b. Exposure to L-ascorbic acid or a-tocopherol facilitates the development of porcine denuded oocytes from metaphase I to metaphase II and prevents cumulus cells from fragmentation. Reprod. Domest. Anim. 39:52-57.
- Wuttke, W., L. Pitzel, I. Knoke, K. Theiling and H. Jarry. 1997. Immune-endocrine interactions affecting luteal function in pigs. J. Reprod. Fertil. Suppl. 52:19-29.
- Dixit, V. D. and N. Parvizi. 2001. Nitric oxide and the control of reproduction. Anim. Reprod. Sci. 65:1-16.
- Matsumi, H., T. Yano, T. Koji, T. Ogura, O. Tsutsumi, Y. Taketani and H. Esumi. 1998. Expression and localization of inducible nitric oxide synthase in the rat ovary: a possible involvement of nitric oxide in the follicular development. Biochem. Biophys. Res. Commun. 243:67-72.
- van Voorhis, B. J., M. S. Dunn, G. D. Snyder and C. P. Weiner. 1994. Nitric oxide: an autocrine regulator of human granulosaluteal cell steroidogenesis. Endocrinology 135:1799-1806.
- Zackrisson, U., M. Mikuni, A. Wallin, D. Delbro, L. Hedin and M. Brannstrom. 1996. Cell-specific localization of nitric oxide synthases (NOS) in the rat ovary during follicular development, ovulation and luteal formation. Hum Reprod. 11:2667-2673.
- Boiti, C., D. Zampini, G. Guelfi, F. Paolocci, M. Zerani and A. Gobbetti. 2002. Expression patterns of endothelial and inducible nitric oxide synthase isoforms in corpora lutea of pseudopregnant rabbits at different luteal stages. J. Endocrinol. 173:285-96. https://doi.org/10.1677/joe.0.1730285
- Matsuyama, S., K. T. Chang, H. Kanuka, M. Ohnishi, A. Ikeda, M. Nishihara and M. Takahashi. 1996. Occurrence of deoxyribonucleic acid fragmentation during prolactin-induced structural luteolysis in cycling rats. Biol. Reprod 54:1245-1251.