Browse > Article

Involvement of Ski Protein Expression in Luteinization in Rat Granulosa Cells  

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)
Nighihara, 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)
Publication Information
Reproductive and Developmental Biology / v.35, no.3, 2011 , pp. 355-361 More about this Journal
Abstract
Ski protein is implicated in proliferation/differentiation in a variety of cells. We had previously reported that Ski protein is present in granulosa cells of atretic follicles, but not in preovulatory follicles, suggesting that Ski has a role in apoptosis of granulosa cells. The alternative fate of granulosa cells other than apoptosis is to differentiate to luteal cells, however, it is unknown whether Ski is expressed and has a role in granulosa cells undergoing luteinization. Thus, the aim of the present study was to locate Ski protein in the rat ovary during luteinization to predict the possible role of Ski. In order to examine the expression pattern of Ski protein along with the progress of luteinization, follicular growth was induced by administration of equine chorionic gonadotropin to immature female rat, and luteinization was induced by human chorionic gonadotropin treatment to mimic luteinizing hormone (LH) surge. While no Ski-positive granulosa cells were present in preovulatory follicle, Ski protein expression was induced in response to LH surge, and was maintained after the formation of corpus luteum (CL). Though Ski protein is absent in granulosa cells of preovulatory follicle, its mRNA (c-ski) was expressed and the level was unchanged even after LH surge. Taken together, these results demonstrated that Ski protein expression is induced in granulosa cells upon luteinization, and suggested that its expression is regulated post-transcriptionally.
Keywords
Arkadia; Granulosa cells; Luteinization; Ski;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Erickson GF, Shimasaki S (2003): The spatiotemporal expression pattern of the bone morphogenetic family in rat ovary cell types during the estrous cycle. Reprod Biol Endocrinol 1:9.   DOI
2 Grimes HL, Ambrose MR, Goodenow MM (1993): c-Ski transcripts with and without exon 2 are expressed in skeletal muscle and throughout chick embryogenesis. Oncogene 8:2863-2868.
3 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.   DOI   ScienceOn
4 Nagano Y, Mavrakis KJ, Lee KL, Fujii T, Koinuma D, Sase H, Yuki K, Isogaya K, Saitoh M, Imamura T, Episkopou V, Miyazono K, Miyazawa K (2007): Arkadia induces degradation of SnoN and c-Ski to enhance transforming growth factor-beta signaling. J Biol Chem 282:20492-501.   DOI
5 Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, Thomsen GH, Wrana JL (2000): Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol Cell 6: 1365-1375.   DOI   ScienceOn
6 Ebisawa T, Fukuchi M, Murakami G, Chiba T, Tanaka K, Imamura T, Miyazono K (2001): Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation. J Biol Chem 276:12477-12480.   DOI
7 Yamanouchi K, Kim H, Nishihara M (2006): Expression of ski in the granulosa cells of atretic follicles in the rat ovary. J Reprod Dev 52:715-721.   DOI   ScienceOn
8 Ueki N, Zhang L, Hayman MJ (2008): Ski can negatively regulates macrophage differentiation through its interaction with PU.1. Oncogene 27:300-307.   DOI   ScienceOn
9 Hanyu A, Ishidou Y, Ebisawa T, Shimanuki T, Imamura T, Miyazono K (2001): The N domain of Smad7 is essential for specific inhibition of transforming growth factor-beta signaling. J Cell Biol 155: 1017-1027.   DOI   ScienceOn
10 Episkopou V, Arkell R, Timmons PM, Walsh JJ, Andrew RL, Swan D (2001): Induction of the mammalian node requires Arkadia function in the extraembryonic lineages. Nature 410:825-830.   DOI   ScienceOn
11 O'Shea JD, Rodgers RJ, D'Occhio MJ (1989): Cellular composition of the corpus luteum of the cow. J Reprod Fertil 85:483-487.   DOI
12 Enders AC (1962): Observations on the fine structure of lutein cells. J Cell Biol 12:101-113.   DOI   ScienceOn
13 Meyer GT, Bruce NW (1980): Quantitative cell changes and vascularisation in the early corpus luteum of the pregnant rat. Anatomical Record 197:369- 374.   DOI   ScienceOn
14 Rodgers RJ, O'Shea JD, Bruce NW (1984): Morphometric analysis of the cellular composition of the ovine corpus luteum. J Anat 138:757-770.
15 Nelson SE, McLean MP, Jayatilak PG, Gibori G (1992): Isolation, characterization, and culture of cell subpopulations forming the pregnant rat corpus luteum. Endocrinology 130:954-966.   DOI   ScienceOn
16 Brannstrom M, Giesecke L, Moore IC, van den Heuvel CJ, Robertson SA (1994): Leukocyte subpopulations in the rat corpus luteum during pregnancy and pseudopregnancy. Biol Reprod 50:1161-1167.   DOI   ScienceOn
17 Matsuyama S, Takahashi M (1995): Immunoreactive (ir)-transforming growth factor (TGF)-beta in rat corpus luteum: ir-TGF beta is expressed by luteal macrophages. Endocr J 42:203-217.   DOI   ScienceOn
18 Matsuyama S, Shiota K, Tachi C, Nishihara M, Takahashi M (1992): Splenic macrophages enhance prolactin and luteinizing hormone action in rat luteal cell cultures. Endocrinol Jpn 39:51-57.   DOI   ScienceOn
19 Yamanouchi K, Matsuyama S, Nishihara M, Shiota K, Tachi C, Takahashi M (1992): Splenic macrophages enhance prolactin-induced progestin secretion from mature rat granulosa cells in vitro. Biol Reprod 46:1109-1113.   DOI   ScienceOn
20 Drummond AE, Le MT, Ethier JF, Dyson M, Findlay JK (2002): Expression and localization of localization of activin receptors, Smads, and beta glycan to the postnatal rat ovary. Endocrinology 143:1423- 1433.   DOI   ScienceOn
21 Xu J, Oakley J, McGee EA (2002): Stage-specific expression of Smad2 and Smad3 during folliculogenesis. Biol Reprod 66:1571-1578.   DOI   ScienceOn
22 Li Y, Turck CM, Teumer JK, Stavnezer E (1986): Unique sequence, Ski, in Sloan-Kettering avian retroviruses with properties of a new cell-derived oncogene. J Virol 57:1065-1072.
23 Stavnezer E, Barkas AE, Brennan LA, Brodeur D, Li Y (1986): Transforming Sloan-Kettering viruses generated from the cloned v-ski oncogene by in vitro and in vivo recombinations. J Virol 57:1073-1083.
24 Nomura N, Sasamoto S, Ishii S, Date T, Matsui M, Ishizaki R (1989): Isolation of human cDNA clones of Ski and the Ski-related gene, Sno. Nucleic Acids Res 17:5489-5500.   DOI   ScienceOn
25 Stavnezer E, Brodeur D, Brennan L (1989): The v- Ski oncogene encodes a truncated set of c-Ski coding exons with limited sequence and structural relatedness to v-myc. Mol Cell Biol 9:4038-4045.
26 Luo K (2004): Ski, SnoN: Negative regulators of TGFbeta signaling. Curr Opin Genet Dev 14:65-70.   DOI   ScienceOn
27 Sutrave P, Hughes SH (1989): Isolation and characterization of three distinct cDNAs for the chicken c-Ski gene. Mol Cell Biol 9:4046-4051.
28 Liu X, Sun Y, Weinberg RA, Lodish HF (2001): Ski/ Sno and TGF-beta signaling. Cytokine Growth Factor Rev 12:1-8.   DOI   ScienceOn
29 Luo K (2003): Negative regulation of BMP signaling by the ski oncoprotein. J Bone Joint Surg Am 3:39- 43.
30 Bell ET, Lunn SF (1968): The induction of ovulation in immature rats treated with pregnant mares' serum gonadotrophin and human chorionic gonadotrophin. J Exp Physiol Cogn Med Sci 53:129-135.
31 Nothnick WB, Curry TE Jr (1996): Divergent effects of interleukin-1 beta on steroidogenesis and matrix metalloproteinase inhibitor expression and activity in cultured rat granulosa cells. Endocrinology 137: 3784-3790.   DOI   ScienceOn
32 Nagano Y, Koinuma D, Miyazawa K, Miyazono K (2010): Context-dependent regulation of the expression of c-Ski protein by Arkadia in human cancer cells. J Biochem 147:545-554.   DOI   ScienceOn
33 Zhao J, Taverne MA, van der Weijden GC, Bevers MM, van den Hurk R (2001): Effect of activin A on in vitro development of rat preantral follicles and localization of activin A and activin receptor II. Biol Reprod 65:967-977.   DOI   ScienceOn
34 Xiao S, Farnworth PG, Findlay JK (1992): Interation between activin and follicle-stimulating hormone-suppressing protein/follistatin in the regulation of basal inhibin production by cultured rat granulosa cells. Endocrinology 131:2365-2370.   DOI   ScienceOn
35 Xiao S, Robertson DM, Findlay JK (1992): Effects of activin and follicle-stimulating hormone (FSH)-suppressing protein/follistatin on FSH receptors and differentitation of cultured rat granulosa cells. Endocrinology 131:1009-1016.   DOI   ScienceOn
36 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.   DOI   ScienceOn
37 Richards JS, Hernandez-Gonzalez I, Gonzalez-Robayna I, Teuling E, Lo Y, Boerboom D, Falender AE, Doyle KH, LeBaron RG, Thompson V, Sandy JD (2005): Regulated expression of ADAMTS family members in follicles and cumulus oocyte complexes: evidence for specific and redundant patterns during ovulation. Biol Reprod 72:1241-1255.   DOI   ScienceOn
38 Roy SK, Hughes J (1994): Ontogeny of granulosa cells in the ovary: lineage-specific expression of transforming growth factor beta 2 and transforming growth factor beta Biol Reprod 51:821-830.   DOI   ScienceOn
39 Smith MF, McIntush EW, Smith GW (1994): Mechanisms associated with corpus luteum development. J Anim Sci 72:1857-1872.
40 Espey LL, Richards JS (2002): Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotropin in the rat. Biol Reprod 67:1662-1670.   DOI   ScienceOn
41 Nilsson EE, Skinner MK (2002): Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol Reprod 67:1018-1024.   DOI   ScienceOn
42 Nilsson EE, Skinner MK (2003): Bone morpfogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod 69:1265-1272.   DOI   ScienceOn
43 Pehlivan T, Mansour A, Spaczynski RZ, Duleba AJ (2001): Effects of transforming growth factor-alpha and-beta on proliferation and apoptosis of rat theca- interstitial cells. J Endocrinol 170:639-645.   DOI
44 Knight PG, Glister C (2006): TGF-beta superfamily members and ovarian development. Reproduction 132:191-206.   DOI   ScienceOn
45 Juengel JL, McNatty KP (2005): The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum Reprod 11:143-160.
46 Knight PG, Glister C (2006): TGF-beta superfamily members and ovarian development. Reproduction 132: 191-206.   DOI   ScienceOn