Reproductive and Developmental Biology

  • 제35권3호
  • /
  • Pages.341-348
  • /
  • 2011
  • /
  • 1738-2432(pISSN)
  • /
  • 2288-0151(eISSN)
한국동물번식학회 (The Korean Society of Animal Reproduction)
권호 표지

Relationship between Sloan-Kettering Virus Expression and Granulosa Cells of Atretic Follicles in the Rat Ovary

  • Kim, Hyun (Department of Veterinary Physiology, Graduate School of Agricultural and Life Sciences, The University of Tokyo) ;
  • Matsuwaki, Takashi (Department of Veterinary Physiology, Graduate School of Agricultural and Life Sciences, The University of Tokyo) ;
  • Yamanouchi, Keitaro (Department of Veterinary Physiology, Graduate School of Agricultural and Life Sciences, The University of Tokyo) ;
  • Nishihara, Masugi (Department of Veterinary Physiology, Graduate School of Agricultural and Life Sciences, The University of Tokyo) ;
  • Kim, Sung-Woo (Animal Genetic Resources Station, National Institute of Animal Science, RDA) ;
  • Ko, Yeoung-Gyu (Animal Genetic Resources Station, National Institute of Animal Science, RDA) ;
  • Yang, Boh-Suk (Animal Genetic Resources Station, National Institute of Animal Science, RDA)
  • 투고 : 2011.09.05
  • 심사 : 2011.09.15
  • 발행 : 2011.09.30
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Sloan-Kettering virus gene product of a cellular protooncogene c-Ski is an unique nuclear pro-oncoprotein and belongs to the Ski/Sno proto-oncogene family. Ski plays multiple roles in a variety of cell types, it can induce both oncogenic transformation and terminal muscle differentiation when expressed at high levels. The aim of the present study was to locate Ski protein in rat ovaries in order to predict the possible involvement of Ski in follicular development and atresia. First, expression of c-Ski mRNA in the ovaries of adult female rats was confirmed by RT-PCR. Then, ovaries obtained on the day of estrus were subjected to immunohistochemical analysis for Ski and proliferating cell nuclear antigen (PCNA) in combination with terminal deoxynucleotidyl transferase-mediated dUTP nick end-labeling (TUNEL). Ski was expressed in granulosa cells that were positive for TUNEL, but negative for PCNA, regardless of the shape and size of follicles. Expression of Ski in TUNEL-positive granulosa cells, but not in PCNA-positive granulosa cells, was also verified in immature hypophysectomized rats having a single generation of developing and atretic follicles by treatment with equine chorionic gonadotropin (eCG). These results indicate that Ski is profoundly expressed in the granulosa cells of atretic follicles, but not in growing follicles, and suggest that Ski plays a role in apoptosis of granulosa cells during follicular atresia.

키워드

참고문헌

  1. Akiyoshi S, Inoue H, Hanai J, Kusanagi K, Nemoto N, Miyazono K, Kawabata M (1999): c-Ski acts as a transcriptional co-repressor in transforming growth factor-b signaling through interaction with smads. J Biol Chem 274:35269-35277. https://doi.org/10.1074/jbc.274.49.35269
  2. Ambrose MR, Bottazzi ME, Goodenow MM (1995): Expression of the c-Ski proto-oncogene during cell cycle arrest and myogenic differentiation. DNA Cell Biol 14:701-707. https://doi.org/10.1089/dna.1995.14.701
  3. Asai S, Ohta R, Shirota M, Sato M, Watanabe G, Taya K (2002): Reproductive endocrinology in Hatano high- and low-avoidance rats during the estrous cycle. Endocrine 18:161-166. https://doi.org/10.1385/ENDO:18:2:161
  4. Baker JC, Harland RM (1997): From receptor to nucleus: The Smad pathway. Curr Opin Genet Dev 7: 467-473. https://doi.org/10.1016/S0959-437X(97)80072-X
  5. Barak Y, Juven T, Haffner R, Oren M (1993): Mdm2 expression is induced by wild type p53 activity. EMBO J 12:461-468.
  6. Berk M, Desai SY, Heyman HC, Colmenares C (1997): Mice lacking the Ski proto-oncogene have defects in neurulation, craniofacial, patterning, and skeletal muscle development. Genes and Development 11: 2029-2039. https://doi.org/10.1101/gad.11.16.2029
  7. Boone DL, Carnegie JA, Rippstein PU, Tsang BK (1997): Induction of apoptosis in eCG-primed rat ovaries by anti-eCG antibody. Biol Reprod 57:420- 427. https://doi.org/10.1095/biolreprod57.2.420
  8. Buckbinder L, Talbott R, Valesco-Miguel S, Takenaka I, Faha B, Seizinger BR, Kley N (1995): Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature 377: 646-649. https://doi.org/10.1038/377646a0
  9. Byskov AG (1978): Follicular atresia. In: Jones RE (ed) The Vertebrate Ovary. Plenum Press, NewYork 533-562.
  10. Byskov AG (1979): Atresia. In: Midgley FR, Sadler WA(eds). Ovarian Follicular Development and Function. Plenum Press, New York 41-58.
  11. Colmenares C, Stavnezer E (1989): The Ski oncogene induces muscle differentiation in quail embryo cells. Cell 59: 293-303. https://doi.org/10.1016/0092-8674(89)90291-2
  12. Dhanasekaran N, Moudgal NR (1989): Biochemical and histological validation of a model to study follicular atresia in rats. Endocrinol Exp 23:155-166.
  13. Donath J, Nishino Y, Schulz T, Michna H (2000): The antiovulatory potential of progesterone antagonists correlates with a down-regulation of progesterone receptors in the hypothalamus, pituitary and ovaries. Ann Anat 182:143-150. https://doi.org/10.1016/S0940-9602(00)80073-4
  14. El-Diery WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B (1993): WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825. https://doi.org/10.1016/0092-8674(93)90500-P
  15. Greenwald GS, Terranova PF (1988): Follicular selection and its control. In: Knobil E, Neill J (eds.) The Physiology of Reproduction. Raven Press, New York 387-435.
  16. Heldin CH, Miyazono K, ten Dijke P (1997): TGF-b signaling from cell membrane to nucleus through SMAD proteins. Nature 390:465-471. https://doi.org/10.1038/37284
  17. Hirshfield AN, Flickinger GL, Ben-Rafael Z (1988): Flow cytofluorometric analysis of granulosa cell proliferation in rats. J Reprod Fertil 84:231-238. https://doi.org/10.1530/jrf.0.0840231
  18. Hirshfield AN (1991): Development of follicles in the mammalian ovary. Int Rev Cytol 124:43-101.
  19. Hori T, Ide M, Miyake T (1969): Pituitary regulation of preovulatory estrogen secretion in the rat. Endocrinol Jpn 16:351-360. https://doi.org/10.1507/endocrj1954.16.351
  20. Hsueh AJ, Billig H, Tsafriri A (1994): Ovarian follicle atresia: A hormonally controlled apoptotic process. Endocr Rev 15: 707-724.
  21. Kastan MB, Zhan Q, El-Deiry WS, Carrier F, Jacks T, Walsh WV, Plunkett BS, Vogelstein B, Fornace Jr AJ (1992): A mammalian cell cycle checkpoit pathway utilizing p53 and GADD45 is defective in ataxia- telangiectasia. Cell 71: 587-597. https://doi.org/10.1016/0092-8674(92)90593-2
  22. Kawabata M, Imamura T, Inoue H, Hanai J, Nishihara A, Hanyu A, Takase M, Ishidou Y, Udagawa Y, Oeda E, Goto D, Yagi K, Kato M, Miyazono K (1999): Intracellular signaling of the TGF-b superfamily by Smad proteins. Ann NYA Cad Sci 886: 73-82. https://doi.org/10.1111/j.1749-6632.1999.tb09402.x
  23. Knight PG, Glister C (2006): TGF-b superfamily members and ovarian development. Reproduction 132: 191-206. https://doi.org/10.1530/rep.1.01074
  24. Liu X, Sun Y, Weinberg RA, Lodish HF (2001): Ski/ Sno and TGF-b signaling. Cytokine Growth Factor Rev 12:1-8. https://doi.org/10.1016/S1359-6101(00)00031-9
  25. Luo K, Stroschein SL, Wang W, Chen D, Martens E, Zhou S, Zhou Q (1999): The Ski oncoprotein interacts with the Smad proteins to repress TGF-b signaling. Genes Dev 13: 2196-2206. https://doi.org/10.1101/gad.13.17.2196
  26. Luo K (2003): Negative regulation of BMP signaling by the ski oncoprotein. J Bone Joint Surg Am 3:39- 43.
  27. Lyons GE, Micales BK, Herr MJ, Horrigan SK, Namciu S, Shardy D, Stavnezer E (1994): Protooncogene c-Ski is expressed in both proliferating and post mitotic neuronal populations. Developmental Dynamics 201:354-365. https://doi.org/10.1002/aja.1002010407
  28. Mahesh VB (1985): The dynamic interaction between steroids and gonadotropins in the mammalian ovulatory cycle. Neuro Sci Bio Behav Rev 2:245-260.
  29. McNatty KP, Juengel JL, Reader KL, Lun S, Myllymaa S, Lawrence SB, Western A, Meerasahib MF, Mottershead DG, Groome NP, Ritvos O, Laitinen MP (2005): Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction 129:481-487. https://doi.org/10.1530/rep.1.00517
  30. McNatty KP, Smith P, Moore LG, Reader K, Lun S, Hanrahan JP, Groome NP, Laitinen M, Ritvos O, Juengel JL (2005): Oocyte-expressed genes affecting ovulation rate. Mol Cell Endocrinol 234:57-66. https://doi.org/10.1016/j.mce.2004.08.013
  31. Medrano EE (2003): Repression of TGF-b signaling by the oncogenic protein Ski in human melanomas: consequences for proliferation, survival, and metastasis. Oncogene 22: 3123-3129. https://doi.org/10.1038/sj.onc.1206452
  32. Miyashita T, Reed JC (1995): Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299. https://doi.org/10.1016/0092-8674(95)90412-3
  33. Muller M, Strand S, Hug H, Heinemann EM, Walczak H, Hofmann WJ, Stremmel W, Krammer PH, Galle PR (1997): Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ ligand system and involves activation of wild- type p53. J Clin Invest 99:403-413. https://doi.org/10.1172/JCI119174
  34. Mutai H, Toyoshima Y, Sun W, Hattori N, Tanaka S, Shiota K (2000): PAL31, a novel nuclear protein, expressed in the developing brain. Bio Chem Biophys Res Commun 274:427-433. https://doi.org/10.1006/bbrc.2000.3133
  35. Nagase T, Mizuguchi G, Nomura N, Ishizaki R, Ueno Y, Ishii S (1990): Requirement of protein co-factor for the DNA-binding function of the human Ski proto-oncogene product. Nucleic Acids Res 18:337- 343. https://doi.org/10.1093/nar/18.2.337
  36. Okamoto K, Beach D (1994): Cyclin G is a transcriptional target of the p53 tumor suppressor protein. EMBO J 13:4816-4822.
  37. Shinagawa T, Nomura T, Colmenares C, Ohira M, Nakagawara A, Ishii S (2001): Increased susceptibility to tumorigenesis of Ski-deficient heterozygous mice. Oncogene 20:8100-8108. https://doi.org/10.1038/sj.onc.1204987
  38. Shi Y, Massague J (2003): Mechanisms of TGF-b signaling from cell membrane to the nucleus. Cell 113: 685-700. https://doi.org/10.1016/S0092-8674(03)00432-X
  39. Soeta C, Suzuki M, Suzuki S, Naito K, Tachi C, Tojo H (2001): Possible role for the c-Ski gene in the proliferation of myogenic cells in regenerating skeleta lmuscles of rats. Development Growth & Differentiation 43:155-164. https://doi.org/10.1046/j.1440-169X.2001.00565.x
  40. Sun W, Hattori N, Mutai H, Toyoshima Y, Kimura H, Tanaka S, Shiota K (2001): PAL31, a nuclear protein required for progression to the S phase. Biochem Biophys Res Commun 280:1048-1054. https://doi.org/10.1006/bbrc.2000.4244
  41. Sun Y, Liu X, Eaton EN, Lane WS, Lodish HF, Weinberg RA (1999): Interaction of the Ski oncoprotein with Smad3 regulates TGF-b signaling. Mol Cell 4:499-509. https://doi.org/10.1016/S1097-2765(00)80201-4
  42. Sun Y, Liu X, Eaton EN, Lodish HF, Weinberg RA (1999): SnoN and Ski protooncoproteins are rapidly degraded in response to transforming growth factor- b signaling. Proc Natl Acad Sci USA 96:12442- 12447. https://doi.org/10.1073/pnas.96.22.12442
  43. Sun W, Kimura H, Hattori N, Tanaka S, Matsuyama S, Shiota K (2006): Proliferation related acidic leucine-rich protein PAL31 functions as a caspase-3 inhibitor. Biochem Biophys Res Commun. 342:817- 823. https://doi.org/10.1016/j.bbrc.2006.02.026
  44. Sutrave P, Copeland TD, Showalter SD, Hughes SH (1990): Characterization of chicken c-Ski oncogene products expressed by retrovirus vectors. Mol Cell Biol 10:3137-3144.
  45. Sutrave P, Kelly AM, Hughes SH (1990): Ski can cause selective growth of skeletal muscle in transgenic mice. Genes Dev 4:1462-1472. https://doi.org/10.1101/gad.4.9.1462
  46. Tebar M, Ruiz A, Gaytan F, Sanchez-Criado JE (1995): Follicular and luteal progesterone play different roles synchronizing pituitary and ovarian events in the 4-day cyclic rat. Biol Reprod 53: 1183-1189. https://doi.org/10.1095/biolreprod53.5.1183
  47. Wu J, Chen Y, Li T (2002): Expression of Fas, and AFP in development of human fetal germ cells invitro. Zygote 10: 333-340.
  48. Wu JW, Krawitz AR, Chai J, Li W, Zhang F, Luo K, Shi Y (2002): Structural mechanism of Smad4 recognition by the nuclear oncoprotein Ski: Insights on Ski-mediated repression of TGF-$\beta$ signaling. Cell 111:357-367. https://doi.org/10.1016/S0092-8674(02)01006-1
  49. Yamanouchi K, Kano K, Soeta C, Hasegawa T, Ishida N, Mukoyama H, Tojo H, Tachi C (1997): Studies on expression of the c-Ski gene in equine(Thoroughbred) tissues. J Equine Sci 8:13-19. https://doi.org/10.1294/jes.8.13
  50. Yamanouchi K, Soeta C, Harada R, Naito K, Tojo H (1999): Endometrial expression of cellular protooncogene c-Ski and its regulation by estradiol-$17\beta$. FEBS Lett 449:273-276. https://doi.org/10.1016/S0014-5793(99)00424-X
  51. Yamanouchi K, Soeta C, Naito K, Tojo H (2000): Progesterone pretreatment inhibits the expression of c-Ski mRNA and epithelial cell proliferation induced by estrogen in the rat uterus. J Reprod Dev 46: 257-263. https://doi.org/10.1262/jrd.46.257