한국동물생명공학회지 (Journal of Animal Reproduction and Biotechnology)

  • 제36권1호
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  • Pages.51-58
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  • 2021
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  • 2671-4639(pISSN)
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  • 2671-4663(eISSN)
한국동물생명공학회 (The Korean Society of Animal Reproduction and Biotechnology)
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Kisspeptin regulates the development of caprine primordial follicles in vitro

  • 투고 : 2021.02.02
  • 심사 : 2021.03.18
  • 발행 : 2021.03.31
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초록

Kisspeptin, a neuropeptide and the master controller of reproductive axis upstream to GnRH neurons, and its receptor are also expressed in extra-hypothalamic tissues, such as ovaries. As systemic kisspeptin has been shown to modulate follicular dynamics in cattle, we hypothesized that kisspeptin has direct actions on the ovarian follicular development. We also hypothesized that kisspeptin regulation of primordial follicle development is via modulation of VEGF expression. In order to test these hypotheses, we cultured caprine ovarian cortical strips in vitro for 7 days with supplementation of kisspeptin at 1, 10 and 100 µM concentration and observed the development of primordial follicles into intermediate, primary and secondary follicles. We also studied the alteration in the expression profile of VEGF and VEGF transcript variant 2 mRNA during follicular development in the presence of kisspeptin. We confirmed the presence of GPR54 in goat ovaries in our preliminary studies. Supplementation of kisspeptin at 1 and 10 µM concentration facilitated the development of primordial follicles into intermediate, primary and secondary follicles with less number of degenerated follicles while the same at 100 µM resulted in degeneration of follicles. We observed a drastic increase in the expression profile of VEGF and VEGF transcript variant 2 mRNA upon culture which was independent of kisspeptin treatment. In conclusion, our studies show that kisspeptin facilitates ovarian primordial development in vitro.

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과제정보

Research infrastructure and manpower support by NIAB to SV is acknowledged.

참고문헌

  1. Arcondeguy T, Lacazette E, Millevoi S, Prats H, Touriol C. 2013. VEGF-A mRNA processing, stability and translation: a paradigm for intricate regulation of gene expression at the post-transcriptional level. Nucleic Acids Res. 41:7997-8010. https://doi.org/10.1093/nar/gkt539
  2. Caraty A and Franceschini I. 2008. Basic aspects of the control of GnRH and LH secretions by kisspeptin: potential applications for better control of fertility in females. Reprod. Domest. Anim. 43 Suppl 2:172-178. https://doi.org/10.1111/j.1439-0531.2008.01158.x
  3. Castellano JM, Gaytan M, Roa J, Vigo E, Navarro VM, Bellido C, Dieguez C, Aguilar E, Sanchez-Criado JE, Pellicer A, Pinilla L, Gaytan F, Tena-Sempere M. 2006. Expression of KiSS-1 in rat ovary: putative local regulator of ovulation? Endocrinology 147:4852-4862. https://doi.org/10.1210/en.2006-0117
  4. Cho SG, Yi Z, Pang X, Yi T, Wang Y, Luo J, Wu Z, Li D, Liu M. 2009. Kisspeptin-10, a KISS1-derived decapeptide, inhibits tumor angiogenesis by suppressing Sp1-mediated VEGF expression and FAK/Rho GTPase activation. Cancer Res. 69:7062-7070. https://doi.org/10.1158/0008-5472.CAN-09-0476
  5. Clarke H, Dhillo WS, Jayasena CN. 2015. Comprehensive review on kisspeptin and its role in reproductive disorders. Endocrinol. Metab. (Seoul) 30:124-141. https://doi.org/10.3803/EnM.2015.30.2.124
  6. Drake CJ, LaRue A, Ferrara N, Little CD. 2000. VEGF regulates cell behavior during vasculogenesis. Dev. Biol. 224:178-188. https://doi.org/10.1006/dbio.2000.9744
  7. Findlay JK, Hutt KJ, Hickey M, Anderson RA. 2015. How is the number of primordial follicles in the ovarian reserve established? Biol. Reprod. 93:111.
  8. Fraser HM. 2006. Regulation of the ovarian follicular vasculature. Reprod. Biol. Endocrinol. 4:18. https://doi.org/10.1186/1477-7827-4-18
  9. Geva E and Jaffe RB. 2000. Role of vascular endothelial growth factor in ovarian physiology and pathology. Fertil. Steril. 74:429-438. https://doi.org/10.1016/S0015-0282(00)00670-1
  10. Golzar F and Javanmard SH. 2015. The effects of kisspeptin-10 on migration and proliferation of endothelial cell. Adv. Biomed. Res. 4:41. https://doi.org/10.4103/2277-9175.151250
  11. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA. 2004. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145:4073-4077. https://doi.org/10.1210/en.2004-0431
  12. Kezele PR, Ague JM, Nilsson E, Skinner MK. 2005. Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol. Reprod. 72:241-255. https://doi.org/10.1095/biolreprod.104.032060
  13. Kim JY. 2012. Control of ovarian primordial follicle activation. Clin. Exp. Reprod. Med. 39:10-14. https://doi.org/10.5653/cerm.2012.39.1.10
  14. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. 1989. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246:1306-1309. https://doi.org/10.1126/science.2479986
  15. Magamage MPS, Zengyo M, Moniruzzaman M, Miyano T. 2010. Testosterone induces activation of porcine primordial follicles in vitro. Reprod Med Biol. 10:21-30. https://doi.org/10.1007/s12522-010-0068-z
  16. McFee RM, Artac RA, McFee RM, Clopton DT, Smith RA, Rozell TG, Cupp AS. 2009. Inhibition of vascular endothelial growth factor receptor signal transduction blocks follicle progression but does not necessarily disrupt vascular development in perinatal rat ovaries. Biol. Reprod. 81:966-977. https://doi.org/10.1095/biolreprod.109.078071
  17. Pepper MS, Ferrara N, Orci L, Montesano R. 1992. Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem. Biophys. Res. Commun. 189:824-831. https://doi.org/10.1016/0006-291X(92)92277-5
  18. Pottapenjera V, Rajanala SR, Reddy C, Gangineni A, Avula K, Bejjanki SK, Sathagopam S, Kesharwani S, Velmurugan S. 2018. Kisspeptin modulates luteinizing hormone release and ovarian follicular dynamics in pre-pubertal and adult Murrah buffaloes. Front. Vet. Sci. 5:149. https://doi.org/10.3389/fvets.2018.00149
  19. Reynolds LP, Grazul-Bilska AT, Redmer DA. 2002. Angiogenesis in the female reproductive organs: pathological implications. Int. J. Exp. Pathol. 83:151-163. https://doi.org/10.1046/j.1365-2613.2002.00277.x
  20. Roberts AE, Arbogast LK, Friedman CI, Cohn DE, Kaumaya PT, Danforth DR. 2007. Neutralization of endogenous vascular endothelial growth factor depletes primordial follicles in the mouse ovary. Biol. Reprod. 76:218-223. https://doi.org/10.1095/biolreprod.106.050880
  21. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. 1983. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219:983-985. https://doi.org/10.1126/science.6823562
  22. Senger DR, Van de Water L, Brown LF, Nagy JA, Yeo KT, Yeo TK, Berse B, Jackman RW, Dvorak AM, Dvorak HF. 1993. Vascular permeability factor (VPF, VEGF) in tumor biology. Cancer Metastasis Rev. 12:303-324. https://doi.org/10.1007/BF00665960
  23. Stouffer RL, Martinez-Chequer JC, Molskness TA, Xu F, Hazzard TM. 2001. Regulation and action of angiogenic factors in the primate ovary. Arch. Med. Res. 32:567-575. https://doi.org/10.1016/S0188-4409(01)00323-X
  24. Tischer E, Mitchell R, Hartman T, Silva M, Gospodarowicz D, Fiddes JC, Abraham JA. 1991. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem. 266:11947-11954. https://doi.org/10.1016/S0021-9258(18)99049-6
  25. Uenoyama Y, Pheng V, Tsukamura H, Maeda KI. 2016. The roles of kisspeptin revisited: inside and outside the hypothalamus. J. Reprod. Dev. 62:537-545. https://doi.org/10.1262/jrd.2016-083
  26. Zimmermann RC, Xiao E, Husami N, Sauer MV, Lobo R, Kitajewski J, Ferin M. 2001. Short-term administration of antivascular endothelial growth factor antibody in the late follicular phase delays follicular development in the rhesus monkey. J. Clin. Endocrinol. Metab. 86:768-772. https://doi.org/10.1210/jcem.86.2.7181