Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-08T02:58:09.210Z Has data issue: false hasContentIssue false
  • English
  • Français

The Kit ligand/c-Kit receptor system in goat ovaries: gene expression and protein localization

Published online by Cambridge University Press:  01 November 2006

J.R.V. Silva ,
R. van den Hurk ,
H.T.A. van Tol ,
B.A.J. Roelen  and
J.R. Figueiredo
J.R.V. Silva*
Affiliation:
Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands. Faculty of Veterinary Medicine, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
R. van den Hurk
Affiliation:
Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
H.T.A. van Tol
Affiliation:
Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
B.A.J. Roelen
Affiliation:
Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
J.R. Figueiredo
Affiliation:
Faculty of Veterinary Medicine, PPGCV, State University of Ceara, Fortaleza, CE, Brazil.
*
All correspondence to: J.R.V. Silva, Faculdade de Medicina Veterinária, Universidade Estadual do Ceará, Avenida Paranjana 1700, CEP: 60740-000, Fortaleza – Ceará, Brazil. Tel: +55 85 3101 9852. Fax: +55 85 3101 9860. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Relatively little information is available on the local factors that regulate folliculogenesis in goats. To examine the possibility that the Kit ligand (KL) system is expressed throughout the folliculogenesis, we studied the presence and distribution of KL and its receptor, c-Kit, in goat ovaries. Ovaries of goats were collected and either fixed in paraformaldehyde for immunohistochemical localization of KL and c-Kit proteins, or used for the isolation of follicles, luteal cells, surface epithelium and medullary samples to study mRNA expression for KL and c-Kit, using the reverse transcriptase polymerase chain reaction (RT-PCR). KL protein and mRNA were found in follicles at all stages of development, i.e. primordial, primary, secondary, small and large antral follicles, as well as in corpora lutea, surface epithelium and medullary tissue. Antral follicles expressed both KL-1 and KL-2 mRNAs, while earlier staged follicles expressed KL-1 transcript only. KL protein was demonstrated in granulosa cells from the primordial follicle onward. Its mRNA could be detected in granulosa cells isolated from antral follicles and occasionally in their theca cells. c-Kit mRNA was expressed in all antral follicular compartments and at all stages of follicular development. c-Kit protein was predominantly found in oocytes from the primordial follicle stage onwards, in theca cells of antral follicles, as well as in corpora lutea, surface epithelium and medullary tissue, particularly in the wall of blood vessels, which may indicate these cells as the main sites of action of KL. It is concluded that the KL/c-Kit system, in goat ovaries, is widespread and that it may be involved in the regulation of various local processes, including folliculogenesis and luteal activity.

Keywords

c-kitFolliclesGoatKit ligandOvary
Type
Research Article
Information
Zygote , Volume 14 , Issue 4 , November 2006 , pp. 317 - 328
Copyright
Copyright © Cambridge University Press 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allard, E.K., Blanchard, K.T. & Boekelheide, K. (1996). Exogenous stem cell factor (SCF) compensates for altered endogenous SCF expression in 2,5-hexanedione-induced testicular atrophy in rats. Biol. Reprod. 55, 185–93.CrossRefGoogle ScholarPubMed
Bedell, M.A., Brannan, C.I., Evans, E.P., Copeland, N.G., Jenkins, N.A. & Donovan, P.J. (1995). DNA rearrangements located over 100 kb 5’ of the Steel (Sl)-coding region in Steel-panda and Steel-contrasted mice deregulate Sl expression and cause female sterility by disrupting ovarian follicle development. Genes Dev. 9, 455–70.CrossRefGoogle ScholarPubMed
Brankin, V., Mitchell, M.R., Webb, B. & Hunter, M.G. (2003). Paracrine effects of oocyte secreted factors and stem cell factor on porcine granulosa and theca cells in vitro. Reprod. Biol. Endocr. 1, 55.CrossRefGoogle ScholarPubMed
Broudy, V.C. (1997). Stem cell factor and hematopoiesis. Blood 90, 1345–64.CrossRefGoogle ScholarPubMed
Clark, D.E., Tisdall, D.J., Fidler, A.E. & McNatty, K.P. (1996). Localization of mRNA encoding c-kit during the initiation of folliculogenesis in ovine fetal ovaries. J. Reprod. Fertil. 106, 329–35.CrossRefGoogle ScholarPubMed
Dolci, S., Williams, D.E., Ernst, M.K., Resnick, J.L., Brannan, C.I., Lock, L.F., Lyman, S.D., Boswell, H.S. & Donovan, P.J. (1991). Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature 352, 809–11.CrossRefGoogle ScholarPubMed
Driancourt, M.A., Reynaud, K., Cortvrindt, R. & Smitz, J. (2000). Roles of Kit and Kit ligand in ovarian function. Rev. Reprod. 5, 143–52.CrossRefGoogle ScholarPubMed
Eckery, D.C., Lawrence, S.B., Juengel, J.L., Greenwood, P., McNatty, K.P. & Fidler, A.E. (2002). Gene expression of the tyrosine kinase receptor c-kit during ovarian development in the brushtail possum (Trichosurus vulpecula). Biol. Reprod. 66, 346–53.CrossRefGoogle ScholarPubMed
Eppig, J.J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–38.CrossRefGoogle ScholarPubMed
Gentry, P.C., Smith, G.W., Anthony, R.V., Zhang, Z., Long, D.K. & Smith, M.F. (1996). Characterization of ovine stem cell factor messenger ribonucleic acid and protein in the corpus luteum throughout the luteal phase. Biol. Reprod. 54, 970–9.CrossRefGoogle ScholarPubMed
Gentry, P.C., Smith, G.W., Leighr, D.R., Bao, B. & Smith, M.F. (1998). Ontogeny of stem cell factor receptor (c-kit) messenger ribonucleic acid in the ovine corpus luteum. Biol. Reprod. 59, 983–90.CrossRefGoogle ScholarPubMed
Gougeon, A. & Busso, D. (2000). Morphologic and functional determinants of primordial and primary follicles in the monkey ovary. Mol. Cell. Endocrinol. 163, 33–41.CrossRefGoogle ScholarPubMed
Horie, K., Takakura, K., Taii, S., Narimoto, K., Noda, Y., Nishikawa, S., Nakayama, H., Fujita, J. & Mori, T. (1991). The expression of c-kit protein during oogenesis and early embryonic development. Biol. Reprod. 45, 547–52.CrossRefGoogle ScholarPubMed
Hoyer, P.E., Byskov, A.G. & Mollgard, P.E. (2005). Stem cell factor and c-kit in human primordial germ cells and fetal ovaries. Mol. Cell. Endocrinol. 234, 1–10.CrossRefGoogle ScholarPubMed
Huang, E.J., Nocka, K.H., Buck, J. & Besmer, P. (1992). Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol. Biol. Cell 3, 349–62.CrossRefGoogle ScholarPubMed
Huang, E.J., Manova, K., Packer, A.I., Sanchez, S., Bachvarova, R.F. & Besmer, P. (1993). The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev. Biol. 157, 100–9.CrossRefGoogle ScholarPubMed
Huang, C.T., Weitsman, S.R., Dykes, B.N. & Magoffin, D.A. (2001). Stem cell factor and insulin-like growth factor-I stimulate luteinizing hormone-independent differentiation of rat ovarian theca cells. Biol. Reprod. 64, 451–6.CrossRefGoogle ScholarPubMed
Ismail, R.S., Okawara, Y., Fryer, J.N. & Vanderhyden, B.C. (1996). Hormonal regulation of the ligand for c-kit in the rat ovary and its effects on spontaneous oocyte meiotic maturation. Mol. Reprod. Dev. 43, 458–69.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Ismail, R.S., Cada, M. & Vanderhyden, B.C. (1999). Trans- forming growth factor-beta regulates Kit ligand expression in rat ovarian surface epithelial cells. Oncogene 18, 4734–41.CrossRefGoogle Scholar
Juengel, J.L., Quirke, L.D., Tisdall, D.J., Smith, P., Hudson, N.L. & McNatty, K.P. (2000). Gene expression in abnormal ovarian structures of ewes homozygous for the inverdale prolificacy gene. Biol. Reprod. 62, 1467–78.CrossRefGoogle ScholarPubMed
Kang, J.S., Lee, C.J., Lee, J.M., Rha, J.Y., Song, K.W. & Park, M.H. (2003). Follicular expression of c-Kit/SCF and inhibin-α in mouse ovary during development. J. Histochem. Cytochem. 51, 1447–58.CrossRefGoogle ScholarPubMed
Kuroda, H., Terada, N., Nakayama, H., Matsumoto, K. & Kitamura, Y. (1988). Infertility due to growth arrest of ovarian follicles in Sl/Slt mice. Dev. Biol. 126, 71–9.CrossRefGoogle ScholarPubMed
Laitinen, M., Rutanen, E.M. & Ritvos, O. (1995). Expression of c-kit ligand messenger ribonucleic acids in human ovaries and regulation of their steady state levels by gonadotropins in cultured granulosa-luteal cells. Endocrinology 136, 4407–14.CrossRefGoogle ScholarPubMed
Lucci, C.M., Amorim, C.A., Bao, S.N., Figueiredo, J.R., Rodrigues, A.P.R., Silva, J.R.V. & Goncalves, P.B.D. (1999). Effect of the interval of serial sections of ovarian tissue in the tissue chopper on the number of isolated caprine preantral follicles. Anim. Reprod. Sci. 56, 39–49.CrossRefGoogle ScholarPubMed
Manova, K., Nocka, K., Besmer, P. & Bachvarova, R.F. (1990). Gonadal expression of c-kit encoded at the W locus of the mouse. Development 110, 1057–69.CrossRefGoogle Scholar
Manova, K., Huang, E.J., Angeles, M., De Leon, V., Sanchez, S., Pronovost, S.M., Besmer, P. & Bachvarova, R.F. (1993). The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia. Dev. Biol. 157, 85–99.CrossRefGoogle ScholarPubMed
McNatty, K.P., Heath, D.A., Lundy, T., Fidler, A.E., Quirke, L., O'Connell, A., Smith, P., Groome, N. & Tisdall, D.J. (1999). Control of early ovarian follicular development. J. Reprod. Fertil. Suppl. 54, 3–16.Google ScholarPubMed
Miyamoto, T., Sasaguri, Y., Sasaguri, T., Azakami, S., Yasukawa, H., Kato, S., Arima, N., Sugama, K. & Morimatsum, M. (1997). Expression of stem cell factor in human aortic endothelial and smooth muscle cells. Atherosclerosis 129, 207–13.CrossRefGoogle ScholarPubMed
Motro, B. & Bernstein, A. (1993). Dynamic changes in ovarian c-kit and Steel expression during the estrous reproductive cycle. Dev. Dyn. 197, 69–79.CrossRefGoogle ScholarPubMed
Nilsson, E.E. & Skinner, M.K. (2001). Cellular interactions that control primordial follicle development and folliculogenesis. J. Soc. Gynecol. Invest. 8, 17–20.CrossRefGoogle ScholarPubMed
Otsuka, F. & Shimasaki, S. (2002). A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc. Natl. Acad. Sci. USA 99, 8060–5.CrossRefGoogle ScholarPubMed
Parrott, J.A. & Skinner, M.K. (1997). Direct actions of kit-ligand on theca cell growth and differentiation during follicle development. Endocrinology 138, 3819–27.CrossRefGoogle ScholarPubMed
Parrott, J.A. & Skinner, M.K. (1999). Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140, 4262–71.CrossRefGoogle ScholarPubMed
Parrott, J.A. & Skinner, M.K. (2000). Kit ligand actions on ovarian stromal cells: effects on theca cell recruitment and steroid production. Mol. Reprod. Dev. 55, 55–64.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Parrott, J.A., Mosher, R., Kim, G. & Skinner, M.K. (2000). Autocrine interactions of keratinocyte growth factor, hepatocyte growth factor, and kit-ligand in the regulation of normal ovarian surface epithelial cells. Endocrinology 141, 2532–9.CrossRefGoogle ScholarPubMed
Reynaud, K., Cortvrindt, R., Smitz, J. & Driancourt, M.A. (2000). Effects of Kit ligand and anti-Kit antibody on growth of cultured mouse preantral follicles. Mol. Reprod. Dev. 56, 483–94.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Silva, J.R.V., van den Hurk, R., van Tol, H.T.A., Roelen, B.A.J. & Figueiredo, J.R. (2004). Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15) and BMP receptors in the ovaries of goats. Mol. Reprod. Dev. 70, 11–19.CrossRefGoogle Scholar
Tisdall, D.J., Quirke, L.D., Smith, P. & McNatty, K.P. (1997). Expression of the ovine stem cell factor gene during folliculogenesis in late fetal and adult ovaries. J. Mol. Endocrinol. 18, 127–35.CrossRefGoogle ScholarPubMed
Tisdall, D.J., Fidler, A.E., Smith, P., Quirke, L.D., Stent, V.C., Heath, D.A. & McNatty, K.P. (1999). Stem cell factor and c-kit gene expression and protein localization in the sheep ovary during fetal development. J. Reprod. Fertil. 116, 277–91.CrossRefGoogle ScholarPubMed
van den Hurk, R. & Zhao, J. (2005). Formation of ovarian follicles and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63,1717–51.CrossRefGoogle ScholarPubMed
van den Hurk, R., Dijkstra, G., Hulshof, S.C.J. & Vos, P.L.A.M. (1994). Micromorphology of antral follicles in cattle after prostaglandin-induced luteolysis, with particular reference to atypical granulosa cells. J. Reprod. Fertil. 100, 137–42.CrossRefGoogle ScholarPubMed
van Tol, H.T.A. & Bevers, M.M. (1998). Theca cells and theca-cell conditioned medium inhibit the progression of FSH-induced meiosis of bovine oocytes surrounded by cumulus cells connected to membrana granulosa. Mol. Reprod. Dev. 51, 315–21.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Yoshida, H., Takakura, N., Kataoka, H., Kunisada, T., Okamura, H. & Nishikawa, S.I. (1997). Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev. Biol. 184, 122–37.CrossRefGoogle ScholarPubMed