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Expression of SDF-$1{\alpha}$ and leptin, and their effect on expression of angiogenic factors in mouse ovaries

  • Park, Min-Jung (Center for Reproductive Medicine, Good Moonhwa Hospital) ;
  • Park, Sea-Hee (Center for Reproductive Medicine, Good Moonhwa Hospital) ;
  • Lee, Su-Kyung (Center for Reproductive Medicine, Good Moonhwa Hospital) ;
  • Moon, Sung-Eun (Department of Obstetrics and Gynecology, Good Moonhwa Hospital) ;
  • Moon, Hwa-Sook (Department of Obstetrics and Gynecology, Good Moonhwa Hospital) ;
  • Joo, Bo-Sun (Center for Reproductive Medicine, Good Moonhwa Hospital)
  • Received : 2011.08.08
  • Accepted : 2011.09.07
  • Published : 2011.09.30

Abstract

Objective: Ovarian angiogenesis plays an important role in folliculogenesis. However, little is known about the expression of angiogenic factors during follicular development according to female age. Stromal cell derived factor-$1{\alpha}$ (SDF-$1{\alpha}$) plays a role in granulosa cell survival and embryo quality as an angiogenic chemokine. Leptin is also involved in folliculogenesis and angiogenesis. This study examined expression of SDF-$1{\alpha}$ and leptin, and their effects on the expression of angiogenic factors in the ovary during follicular development according to female age. Methods: Ovaries were collected from C57BL mice of two age groups (6-9 weeks and 24-26 weeks) at 6, 12, 24, and 48 hours after 5 IU pregnant mare's serum gonadotropin (PMSG) injection. The expression of ovarian SDF-$1{\alpha}$ and leptin mRNA was evaluated by RT-PCR. In the organ culture experiment, the ovaries were cultured in transwell permeable supports with Waymouth's medium treated with various doses of SDF-$1{\alpha}$(50-200 ng/mL) or leptin (0.01-1 ${\mu}g$/mL) for 7 days. Then, mRNA expression of vascular endothelial growth factor (VEGF), endothelial nitric oxide synthase (eNOS), and visfatin were examined in the cultured ovaries. Results: Expression of SDF-$1{\alpha}$ and leptin in the ovary was significantly lower in the aged mouse group compared to the young mouse group ($p$ <0.05). Expression of these two factors increased with follicular development after PMSG administration. SDF-$1{\alpha}$ treatment stimulated visfatin expression in a dose-dependent manner, while leptin treatment significantly increased eNOS expression. Conclusion: These results suggest that decrease of ovarian SDF-$1{\alpha}$ and leptin expression may be associated with aging-related reduction of ovarian function. SDF-$1{\alpha}$ and leptin may play a role in follicular development by regulating the expression of angiogenic factors in mouse ovaries.

Keywords

References

  1. Geva E, Jaffe RB. Role of vascular endothelial growth factor in ovarian physiology and pathology. Fertil Steril 2000;74:429-38. https://doi.org/10.1016/S0015-0282(00)00670-1
  2. Redmer CA, Reynolds LP. Angiogenesis in the ovary. Rev Reprod 1996;1:182-92. https://doi.org/10.1530/ror.0.0010182
  3. Ravindranath N, Little-Ihrig L, Phillips HS, Ferrara N, Zeleznik AJ. Vascular endothelial growth factor messenger ribonucleic acid expression in the primate ovary. Endocrinology 1992;131:254-60. https://doi.org/10.1210/en.131.1.254
  4. Zeleznik AJ, Schuler HM, Reichert LE Jr. Gonadotropin-binding sites in the rhesus monkey ovary: role of the vasculature in the selective distribution of human chorionic gonadotropin to the preovulatory follicle. Endocrinology 1981;109:356-62. https://doi.org/10.1210/endo-109-2-356
  5. Fraser HM. Regulation of the ovarian follicular vasculature. Reprod Biol Endocrinol 2006;4:18. https://doi.org/10.1186/1477-7827-4-18
  6. Tarin JJ, Perez-Albala S, Cano A. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol Reprod 2001;65:141-50. https://doi.org/10.1095/biolreprod65.1.141
  7. te Velde ER, Peasron PL. The variability of female reproductive aging. Hum Reprod Update 2002;8:141-54. https://doi.org/10.1093/humupd/8.2.141
  8. Thouas GA, Trounson AO, Jones GM. Effect of female age on mouse oocyte developmental competence following mitochondrial injury. Biol Reprod 2005;73:366-73. https://doi.org/10.1095/biolreprod.105.040956
  9. Tatone C, Amicarelli F, Carbone MC, Monteleone P, Caserta D, Marci R, et al. Cellular and molecular aspects of ovarian follicle ageing. Hum Reprod Update 2008;14:131-42. https://doi.org/10.1093/humupd/dmm048
  10. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006;107:1761-7. https://doi.org/10.1182/blood-2005-08-3182
  11. Bachelder RE, Wendt MA, Mercurio AM. Vascular endothelial growth factor promotes breast carcinoma invasion in an autocrine manner by regulating the chemokine receptor CXCR4. Cancer Res 2002;62:7203-6.
  12. Kryczek I, Lange A, Mottram P, Alvarez X, Cheng P, Hogan M, et al. CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Res 2005;65:465-72.
  13. Kryczek I, Frydman N, Gaudin F, Krzysiek R, Fanchin R, Emilie D, et al. The chemokine SDF-1/CXCL12 contributes to T lymphocyte recruitment in human pre-ovulatory follicles and coordinates with lymphocytes to increase granulosa cell survival and embryo quality. Am J Reprod Immunol 2005;54:270-83. https://doi.org/10.1111/j.1600-0897.2005.00307.x
  14. Zhou C, Borillo J, Wu J, Torres L, Lou YH. Ovarian expression of chemokines and their receptors. J Reprod Immunol 2004;63:1-9. https://doi.org/10.1016/j.jri.2004.03.002
  15. Sierra-Honigmann MR, Nath AK, Murakami C, Garcia-Cardena G, Papapetropoulos A, Sessa WC, et al. Biological action of leptin as an angiogenic factor. Science 1998;281:1683-6. https://doi.org/10.1126/science.281.5383.1683
  16. Cao R, Brakenhielm E, Wahlestedt C, Thyberg J, Cao Y. Leptin induces vascular permeability and synergistically stimulates angiogenesis with FGF-2 and VEGF. Proc Natl Acad Sci USA 2001;98:6390-5.
  17. Park HY, Kwon HM, Lim HJ, Hong BK, Lee JY, Park BE, et al. Potential role of leptin in angiogenesis: leptin induces endothelial cell proliferation and expression of matrix metalloproteinases in vivo and in vitro. Exp Mol Med 2001;33:95-102. https://doi.org/10.1038/emm.2001.17
  18. Yamagishi S, Amano S, Inagaki Y, Okamoto T, Takeuchi M, Inoue H. Pigment epithelium-derived factor inhibits leptin-induced angiogenesis by suppressing vascular endothelial growth factor gene expression through anti-oxidative properties. Microvasc Res 2003;65:186-90. https://doi.org/10.1016/S0026-2862(03)00005-0
  19. Almog B. Leptin attenuates follicular apoptosis and accelerates the onset of puberty in immature rat. Mol Cellular Endocrinol 2001;183:179-91. https://doi.org/10.1016/S0303-7207(01)00543-3
  20. Craig J, Zhu H, Dyce PW, Petrik J, Li J. Leptin enhances oocyte nuclear and cytoplasmic maturation via the mitogen-activated protein kinase pathway. Endocrinology 2004;145:5355-63. https://doi.org/10.1210/en.2004-0783
  21. Gonzalez RR, Simon C, Caballero-Campo P, Norman R, Chardonnens D, Devoto L, et al. Leptin and reproduction. Hum Reprod Update 2000;6:290-300. https://doi.org/10.1093/humupd/6.3.290
  22. Moschos S, Chan JL, Mantzoros CS. Leptin and reproduction: a review. Fertil Steril 2002;77:433-44. https://doi.org/10.1016/S0015-0282(01)03010-2
  23. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum Reprod 1992;7:1342-6. https://doi.org/10.1093/oxfordjournals.humrep.a137570
  24. Vaskivuo TE, Anttonen M, Herva R, Billig H, Dorland M, te Velde ER, et al. Survival of human ovarian follicles from fetal to adult life: apoptosis, apoptosis-related proteins, and transcription factor GATA-4. J Clin Endocrinol Metab 2001;86:3421-9. https://doi.org/10.1210/jc.86.7.3421
  25. Skinner MK, Schmidt M, Savenkova MI, Sadler-Riggleman I, Nilsson EE. Regulation of granulosa and theca cell transcriptomes during ovarian antral follicle development. Mol Reprod Dev 2008;75:1457-72. https://doi.org/10.1002/mrd.20883
  26. Cioffi JA, Van Blerkom J, Antczak M, Shafer A, Wittner S, Snidgrass HR. The expression of leptin and its receptors in pre-ovulatory human follicles. Mol Hum Reprod 1997;3:467-72. https://doi.org/10.1093/molehr/3.6.467
  27. Loffler S, Aust G, Kohler U, Spanel-Borowski K. Evidence of leptin expression in normal and polycystic human ovaries. Mol Hum Reprod 2001;7:1143-9. https://doi.org/10.1093/molehr/7.12.1143
  28. Tajima K, Orisaka M, Yata H, Goto K, Hosokawa K, Kotsuji F. Role of granulosa and theca cell interactions in ovarian follicular maturation. Microsc Res Tech 2006;69:450-8. https://doi.org/10.1002/jemt.20304
  29. Nishigaki A, Okada H, Okamoto R, Sugiyama S, Miyazaki K, Yasuda K, et al. Concentrations of stromal cell-derived factor-1 and vascular endothelial growth factor in relation to the diameter of human follicles. Fertil Steril 2011;95:742-6. https://doi.org/10.1016/j.fertnstert.2010.10.028
  30. Shimizu H, Shimomura Y, Nakanishi Y, Futawatari T, Ohtani K, Sato N, et al. Estrogen increases in vivo leptin production in rats and human subjects. J Endocrinol 1997;154:285-89. https://doi.org/10.1677/joe.0.1540285
  31. Hong SC, Yoo SW, Cho GJ, Kim T, Hur JY, Park YK, et al. Correlation between estrogens and serum adipocytokines in premenopausal and postmenopausal women. Menopause 2007;14:835-40. https://doi.org/10.1097/gme.0b013e31802cddca
  32. Chehab FF, Lim ME, Lu R. Correction of the sterility defect in homozygous obsess female mice by treatment with the human recombinant leptin. Nat Genet 1996;12:318-20. https://doi.org/10.1038/ng0396-318
  33. Sirotkin AV, Rafay J, Kotwica J. Leptin controls rabbit ovarian function in vivo and in vitro: Possible interrelationships with ghrelin. Theriogenology 2009;72:765-72. https://doi.org/10.1016/j.theriogenology.2009.05.011
  34. Joo JK, Joo BS, Kim SC, Choi JR, Park SH, Lee KS. Role of leptin in improvement of oocyte quality by regulation of ovarian angiogenesis. Anim Reprod Sci 2010;119:329-34. https://doi.org/10.1016/j.anireprosci.2010.02.002
  35. Robinson RS, Woad KJ, Hammond AJ, Laird M, Hunter MG, Mann GE. Angiogenesis and vascular function in the ovary. Reproduction 2009;138:869-81. https://doi.org/10.1530/REP-09-0283
  36. Yamaguchi J, Kusano KF, Masuo O, Kawamoto A, Silver M, Murasawa S, et al. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 2003;107:1322-8. https://doi.org/10.1161/01.CIR.0000055313.77510.22
  37. Hug C, Lodish HF. Medicine. Visfatin: a new adipokine. Science 2005;307:366-7. https://doi.org/10.1126/science.1106933
  38. Ognjanovic S, Bryant-Greenwood GD. Pre-B-cell colony-enhancing factor, a novel cytokine of human fetal membranes. Am J Obstet Gynecol 2002;187:1051-8. https://doi.org/10.1067/mob.2002.126295
  39. Luk T, Malam Z, Marshall JC. Pre-B cell colony-enhancing factor (PBEF)/visfatin: a novel mediator of innate immunity. J Leukoc Biol 2008;83:804-16. https://doi.org/10.1189/jlb.0807581
  40. Adya R, Tan BK, Punn A, Chen J, Randeva HS. Visfatin induces human endothelial VEGF and MMP-2/9 production via MAPK and PI3K/Akt signalling pathways: novel insights into visfatin-induced angiogenesis. Cardiovasc Res 2008;78:356-65. https://doi.org/10.1093/cvr/cvm111
  41. Shen CJ, Tsai EM, Lee JN, Chen YL, Lee CH, Chan TF. The concentrations of visfatin in the follicular fluids of women undergoing controlled ovarian stimulation are correlated to the number of oocytes retrieved. Fertil Steril 2010;93:1844-50. https://doi.org/10.1016/j.fertnstert.2008.12.090
  42. Sengoku K, Takuma N, Horikawa M, Tsuchiya K, Komori H, Sharifa D, et al. Requirement of nitric oxide for murine oocyte maturation, embryo development, and trophoblast outgrowth in vitro. Mol Reprod Dev 2001;58:262-8. https://doi.org/10.1002/1098-2795(200103)58:3<262::AID-MRD3>3.0.CO;2-8
  43. Murohara T, Horowitz JR, Silver M, Tsurumi Y, Chen D, Sullivan A, et al. Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin. Circulation 1998;97:99-107. https://doi.org/10.1161/01.CIR.97.1.99

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