Development and Reproduction (한국발생생물학회지:발생과생식)

The Korean Society of Developmental Biology (한국발생생물학회)
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17Beta-Estradiol Regulates NUCB2/Nesfatin-1 Expression in Mouse Oviduct

  • Sun, Sojung (Dept. of Bioenvironmental Technology, Seoul Women's University) ;
  • Shin, Jungwoo (Dept. of Bioenvironmental Technology, Seoul Women's University) ;
  • Jang, Jiwon (Dept. of Bioenvironmental Technology, Seoul Women's University) ;
  • Hwang, Seungyeon (Dept. of Bioenvironmental Technology, Seoul Women's University) ;
  • Kim, Jeongwoo (Dept. of Bioenvironmental Technology, Seoul Women's University) ;
  • Kong, Jinseong (Dept. of Bioenvironmental Technology, Seoul Women's University) ;
  • Yang, Hyunwon (Dept. of Bioenvironmental Technology, Seoul Women's University)
  • Received : 2020.01.13
  • Accepted : 2020.01.22
  • Published : 2020.03.31
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Abstract

NUCB2/nesfatin-1 known to regulate appetite and energy homeostasis is expressed not only in the hypothalamus, but also in various organs and tissues. Our previous reports also demonstrated that NUCB2/nesfatin-1 was expressed in the reproductive organs, including the ovaries, uterus, and testes of mice. However, it is yet known whether NUCB2/nesfatin-1 is expressed in the oviduct and how its expression is regulated. Therefore, we investigated the expression of NUCB2/nesfatin-1 in the oviduct and its expression is regulated by gonadotropin. Immunohistochemical staining results showed that nesfatin-1 protein was localized in epithelial cells of the oviduct. As a result of quantitative real-time PCR (qRT-PCR) and Western blot, NUCB2/nesfatin-1 was detected strongly in the oviducts. During the estrus cycle, NUCB2/nesfatin-1 expression in the oviducts was markedly higher in the proestrus stage than in other estrus stages. In order to elucidate whether the expression of NUCB2 mRNA is controlled by the gonadotropins, we injected PMSG and hCG and measured NUCB2 mRNA level in the oviduct after injection. Its level was increased in the oviduct after PMSG injection, but no significant change after hCG injection. In addition, NUCB2 mRNA levels were markedly reduced after ovariectomy, while recovered after 17β-estradiol (E2) injection, but not by progesterone (P4). This study demonstrated that NUCB2/nesfatin-1 is highly expressed in the oviduct of mouse and its expression is regulated by E2 secreted by the ovaries. These results suggest that NUCB2/nesfatin-1 expressed by the oviduct may affect the function of the oviduct regulated by the ovaries.

Keywords

References

  1. Archanco M, Gomez-Ambrosi J, Tena-Sempere M, Fruhbeck G, Burrell MA (2007) Expression of leptin and adiponectin in the rat oviduct. J Histochem Cytochem 55:1027-1037. https://doi.org/10.1369/jhc.6A7128.2007
  2. Barnikol-Watanabe S, Gross NA, Gotz H, Henkel T, Karabinos A, Kratzin H, Barnikol HU, Hilschmann N (1994) Human protein NEFA, a novel DNA binding/EF-hand/leucine zipper protein. Molecular cloning and sequence analysis of the cDNA, isolation and characterization of the protein. Biol Chem Hoppe Seyler 375:497-512. https://doi.org/10.1515/bchm3.1994.375.8.497
  3. Boatman DE (1997) Responses of gametes to the oviductal environment. Hum Reprod 12:133-149.
  4. Catak Z, Yavuzkir S, Kocdemir E, Ugur K, Yardim M, Sahin I, Agirbas EP, Aydin S (2019) NUCB2/nesfatin-1 in the blood and follicular fluid in patients with polycystic ovary syndrome and poor ovarian response. J Reprod Infertil 20:225-230.
  5. Chiu PC, Chung MK, Koistinen R, Koistinen H, Seppala M, Ho PC, Ng EH, Lee KF, Yeung WS (2007) Cumulus oophorus-associated glycodelin-C displaces sperm-bound glycodelin-A and-F and stimulates spermatozoa-zona pellucida binding. J Biol Chem 282:5378-5388. https://doi.org/10.1074/jbc.M607482200
  6. Choudhary S, Janjanam J, Kumar S, Kaushik JK, Mohanty AK (2019) Structural and functional characterization of buffalo oviduct-specific glycoprotein (OVGP1) expressed during estrous cycle. Biosci Rep 39:BSR20191501. https://doi.org/10.1042/BSR20191501
  7. Chung Y, Kim J, Im E, Kim H, Yang H (2015) Progesterone and $17{\beta}$-estradiol regulate expression of nesfatin-1/NUCB2 in mouse pituitary gland. Peptides 63:4-9. https://doi.org/10.1016/j.peptides.2014.10.011
  8. Craig JA, Zhu H, Dyce PW, Wen L, Li J (2005) Leptin enhances porcine preimplantation embryo development in vitro. Mol Cell Endocrinol 229:141-147. https://doi.org/10.1016/j.mce.2004.08.008
  9. Deaver SE, Hoyer PB, Dial SM, Field ME, Collier RJ, Rhoads ML (2013) Localization of ghrelin and its receptor in the reproductive tract of holstein heifers. J Dairy Sci 96:150-157. https://doi.org/10.3168/jds.2012-5506
  10. Garcia-Galiano D, Navarro VM, Gaytan F, Tena-Sempere M (2010) Expanding roles of NUCB2/nesfatin-1 in neuroendocrine regulation. J Mol Endocrinol 45:281-290. https://doi.org/10.1677/JME-10-0059
  11. Gonzalez R, Kerbel B, Chun A, Unniappan S (2010) Molecular, cellular and physiological evidences for the anorexigenic actions of nesfatin-1 in goldfish. PLoS One 5:e15201. https://doi.org/10.1371/journal.pone.0015201
  12. Gonzalez R, Tiwari A, Unniappan S (2009) Pancreatic beta cells colocalize insulin and pronesfatin immunoreactivity in rodents. Biochem Biophys Res Commun 381:643-648. https://doi.org/10.1016/j.bbrc.2009.02.104
  13. Jiang S, Zhou W, Zhang X, Wang D, Zhu H, Hong M, Gong Y, Ye J, Fang F (2016) Developmental expression and distribution of nesfatin-1/NUCB2 in the canine digestive system. Acta Histochem 118:90-96. https://doi.org/10.1016/j.acthis.2015.11.010
  14. Kawamura K, Sato N, Fukuda J, Kodama H, Kumagai J, Tanikawa H, Murata M, Tanaka T (2003) The role of leptin during the development of mouse preimplantation embryos. Mol Cell Endocrinol 202:185-189. https://doi.org/10.1016/S0303-7207(03)00081-9
  15. Kawamura K, Sato N, Fukuda J, Kodama H, Kumagai J, Tanikawa H, Nakamura A, Tanaka T (2002) Leptin promotes the development of mouse preimplantation embryos in vitro. Endocrinology 143:1922-1931. https://doi.org/10.1210/en.143.5.1922
  16. Kim J, Chung Y, Kim H, Im E, Lee H, Yang H (2014) The tissue distribution of nesfatin-1/NUCB2 in mouse. Dev Reprod 18:301-309. https://doi.org/10.12717/DR.2014.18.4.301
  17. Kim J, Sun S, Lee D, Youk H, Yang H (2019) Gonadotropin regulates NUCB2/nesfatin-1 expression in the mouse ovary and uterus. Biochem Biophys Res Commun 513:602-607. https://doi.org/10.1016/j.bbrc.2019.04.008
  18. Lamy J, Liere P, Pianos A, Aprahamian F, Mermillod P, Saint-Dizier M (2016) Steroid hormones in bovine oviductal fluid during the estrous cycle. Theriogenology 86:1409-1420. https://doi.org/10.1016/j.theriogenology.2016.04.086
  19. Li S, Winuthayanon W (2017) Oviduct: roles in fertilization and early embryo development. J Endocrinol 232:R1-R26. https://doi.org/10.1530/JOE-16-0104
  20. Liu Q, Xie QZ, Zhou Y, Yang J (2015) Osteopontin is expressed in the oviduct and promotes fertilization and preimplantation embryo development of mouse. Zygote 23:622-630. https://doi.org/10.1017/S0967199414000483
  21. Luque EM, Torres PJ, de Loredo N, Vincenti LM, Stutz G, Santillan ME, Ruiz RD, de Cuneo MF, Martini AC (2014) Role of ghrelin in fertilization, early embryo development, and implantation periods. Reproduction 148:159-167. https://doi.org/10.1530/REP-14-0129
  22. Miura K, Titani K, Kurosawa Y, Kanai Y (1992) Molecular cloning of nucleobindin, a novel DNAbinding protein that contains both a signal peptide and a leucine zipper structure. Biochem Biophys Res Commun 187:375-380. https://doi.org/10.1016/S0006-291X(05)81503-7
  23. Nishie T, Kobayashi Y, Kimura K, Okuda K (2018) Acute stimulation of a smooth muscle constrictor by oestradiol-$17{\beta}$ via GPER1 in bovine oviducts. Reprod Domest Anim 53:326-332. https://doi.org/10.1111/rda.13108
  24. O'Day-Bowman MB, Mavrogianis PA, Reuter LM, Johnson DE, Fazleabas AT, Verhage HG (1996) Association of oviduct-specific glycoproteins with human and baboon (Papio anubis) ovarian oocytes and enhancement of human sperm binding to human hemizonae following in vitro incubation. Biol Reprod 54:60-69. https://doi.org/10.1095/biolreprod54.1.60
  25. Oh-I S, Shimizu H, Satoh T, Okada S, Adachi S, Inoue K, Eguchi H, Yamamoto M, Imaki T, Hashimoto K, Tsuchiya T, Monden T, Horiguchi K, Yamada M, Mori M (2006) Identification of nesfatin-1 as a satiety molecule in the hypothalamus. Nature 443:709-712. https://doi.org/10.1038/nature05162
  26. Prinz P, Goebel-Stengel M, Teuffel P, Rose M, Klapp BF, Stengel A (2016) Peripheral and central localization of the nesfatin-1 receptor using autoradiography in rats. Biochem Biophys Res Commun 470:521-527. https://doi.org/10.1016/j.bbrc.2016.01.113
  27. Rapisarda JJ, Mavrogianis PA, O'Day-Bowman MB, Fazleabas AT, Verhage HG (1993) Immunological characterization and immunocytochemical localization of an oviduct-specific glycoprotein in the human. J Clin Endocrinol Metab 76:1483-1488. https://doi.org/10.1210/jc.76.6.1483
  28. Shimizu H, Tanaka M, Osaki A (2016) Transgenic mice overexpressing nesfatin/nucleobindin-2 are susceptible to high-fat diet-induced obesity. Nutr Diabetes 6:e201. https://doi.org/10.1038/nutd.2015.42
  29. Stengel A, Goebel M, Wang L, Kato I, Mori M, Tache Y (2012) Nesfatin-130-59 but not the N- and C terminal fragments, nesfatin-11-29 and nesfatin-160-82 injected intracerebroventricularly decreases dark phase food intake by increasing inter-meal intervals in mice. Peptides 35:143-148. https://doi.org/10.1016/j.peptides.2012.03.015
  30. Xi L, Liu Y, Tang Z, Sheng X, Zhang H, Weng Q, Xu M (2017) Expression of leptin receptor in the oviduct of Chinese brown frog (Rana dybowskii). Am J Physiol Regul Integr Comp Physiol 312:R912-R918.
  31. Yeung WS, Lee KF, Koistinen R, Koistinen H, Seppala M, Chiu PC (2009) Effects of glycodelins on functional competence of spermatozoa. J Reprod Immunol 83:26-30. https://doi.org/10.1016/j.jri.2009.04.012
  32. Zhang AQ, Li XL, Jiang CY, Lin L, Shi RH, Chen JD, Oomura Y (2010) Expression of nesfatin-1/NUCB2 in rodent digestive system. World J Gastroenterol 16:1735-1741. https://doi.org/10.3748/wjg.v16.i14.1735