한국발생생물학회지:발생과생식 (Development and Reproduction)

  • 제22권4호
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  • Pages.331-339
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  • 2018
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  • 2465-9525(pISSN)
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  • 2465-9541(eISSN)
한국발생생물학회 (The Korean Society of Developmental Biology)
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Tissue-Specific Localization NUCB2/nesfatin-1 in the Liver and Heart of Mouse Fetus

  • Sun, Sojung (Dept. of Bioenvironmental Technology, College of Natural Sciences, Seoul Women's University) ;
  • Yang, Hyunwon (Dept. of Bioenvironmental Technology, College of Natural Sciences, Seoul Women's University)
  • 투고 : 2018.10.29
  • 심사 : 2018.12.05
  • 발행 : 2018.12.31
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초록

NUCB2/nesfatin-1 is first known to be expressed in the hypothalamus while controlling appetite and energy metabolism. However, recent studies have shown that NUCB2/nesfatin-1 was expressed in the various organs as well as the hypothalamus. Our previous reports also demonstrated that NUCB2/nesfatin-1 was expressed in the ovary, testis, pituitary gland, lung, kidney, and stomach of fetal and adult mice. However, the role of NUCB2/nesfatin-1 in mouse fetus remains unknown. Thus, the aim of this study was to investigate whether NUCB2/nestatin-1 is expressed in mouse fetus at the developmental stage in which organogenesis begins. To do this, we performed in situ hybridization (ISH) and immunohistochemistry (IHC) staining to examine the distribution of NUCB2 mRNA and nesfatin-1 protein in the mouse fetal organs during early developmental stages, especially at embryonic day (E) 10.5. As a result of ISH, NUCB2 mRNA positive signals were more frequent in the liver, but there were relatively few positive signals in heart. On the other hand, no positive signals were detected in other organs. These ISH results were validated by IHC staining and qRT-PCR analysis. Expression of nesfatin-1 protein detected by IHC staining was similar to that of NUCB2 mRNA detected by ISH in the liver and heart. In addition, the levels of NUCB2 mRNA expression analyzed by qRT-PCR were significantly increased in the liver and heart compared to other organs of the mouse fetus at E13.5, whereas its level was extensively decreased in the liver, but increased in the lung, stomach, and kidney of the mouse fetus at E17.5. These results suggest that NUCB2/nesfatin-1 may play an important role in liver and heart development and physiological functions in the developmental process of mouse fetus. Further studies are needed on the function of NUCB2/nesfatin-1, which is highly expressed in the various organs, including liver and heart during mouse development.

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참고문헌

  1. 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
  2. Baskin LS, Hayward SW, Sutherland RA, DiSandro MJ, Thomson AA, Goodman J, Cunha GR (1996) Mesenchymal-epithelial interactions in the bladder. World J Urol 14:301-309.
  3. Baumgart E, Schad A, Volkl A, Fahimi HD (1997) Detection of mRNAs encoding peroxisomal proteins by nonradioactive in situ hybridization with digoxigenin-labelled cRNAs. Histochem Cell Biol 108:371-379. https://doi.org/10.1007/s004180050178
  4. Brailoiu GC, Dun SL, Brailoiu E, Inan S, Yang J, Chang JK, Dun NJ (2007) Nesfatin-1: Distribution and interaction with a G protein-coupled receptor in the rat brain. Endocrinology 148:5088-5094. https://doi.org/10.1210/en.2007-0701
  5. Chotteau-Lelievre A, Dolle P, Gofflot F (2006) Expression analysis of murine genes using in situ hybridization with radioactive and nonradioactively labeled RNA probes. Methods Mol Biol 326:61-87.
  6. Chung Y, Jung E, Kim H, Kim J, Yang H (2013) Expression of nesfatin-1/NUCB2 in fetal, neonatal and adult mice. Dev Reprod 17:461-467. https://doi.org/10.12717/DR.2013.17.4.461
  7. Chung Y, Kim J, Im E, Kim H, Yang H (2015) Progesterone and $17{\beta}$-estradiol regulate expression of nesfatin-1/NUBC2 in mouse pituitary gland. Peptides 63:4-9. https://doi.org/10.1016/j.peptides.2014.10.011
  8. Chung Y, Kim H, Seon S, Yang H (2017) Serum cytokine levels are related to nesfatin-1/NUCB2 expression in the implantation sites of spontaneous abortion model of CBA/j$\times$DBA/2 mice. Dev Reprod 21:35-46. https://doi.org/10.12717/DR.2017.21.1.035
  9. Cunha GR, Baskin L (2016) Mesenchymal-epithelial interaction techniques. Differentiation 91:20-27. https://doi.org/10.1016/j.diff.2015.10.006
  10. Foo KS, Brismar H, Broberger C (2008) Distribution and neuropeptide coexistence of nucleobindin-2 mRNA/nesfatin like immunoreactivityin the rat CNS. Neuroscience 156:563-579. https://doi.org/10.1016/j.neuroscience.2008.07.054
  11. 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
  12. Garcia-Galiano D, Pineda R, Ilhan T, Castellano JM, Ruiz-Pino F, Sanchez-Garrido MA, Vazquez MJ, Sangiao-Alvarellos S, Romero-Ruiz A, Pinilla L, Dieguez C, Gaytan F, Tena-Sempere M (2012) Cellular distribution, regulated expression, and functional role of the anorexigenic peptide, NUCB2/ nesfatin-1, in the testis. Endocrinology 153:1959-1971. https://doi.org/10.1210/en.2011-2032
  13. Goebel M, Stengel A, Wang L, Tache Y (2009) Restraint stress activates nesfatin-1-immunoreactive brain nuclei in rats. Brain Res 1300:114-124. https://doi.org/10.1016/j.brainres.2009.08.082
  14. Goebel-Stengel M, Wang L, Stengel A, Tache Y (2011) Localization of nesfatin-1 neurons in the mouse brain and functional implication. Brain Res 1396:20-34. https://doi.org/10.1016/j.brainres.2011.04.031
  15. 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
  16. Hoggard N, Hunter L, Duncan JS, Williams LM, Trayhurn P, Mercer JG (1997) Leptin and leptin receptor mRN and protein expressio in the murine fetus and placenta. Proc Natl Acad Sci USA 94:11073-11078. https://doi.org/10.1073/pnas.94.20.11073
  17. 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
  18. 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
  19. Miura K, Titani K, Kurosawa Y, Kanai Y (1992) Molecular cloning of nucleobindin, a novel DNA-binding 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
  20. Nozawa S, Kimura T, Kurishima M, Mimura K, Saeki K, Miki Y, Oda H, Mori A, Momota Y, Azakami D, Ishioka K (2016) Analyses of a satiety factor NUCB2/nesfatin-1; gene expressions and modulation by different dietary components in dogs. J Vet Med Sci 78:411-417. https://doi.org/10.1292/jvms.15-0255
  21. 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
  22. 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
  23. Santos M, Bastos P, Gonzaga S, Roriz JM, Baptista MJ, Nogueira-Silva C, Melo-Rocha G, Henriques-Coelho T, Roncon-Albuquerque R Jr, Leite-Moreir AF, De Krijger RR, Tibboel D, Rottier R, Correia-Pinto J (2006) Ghrelin expression in human and rat fetal lungs and the effect of ghrelin administration in nitrofen-induced congenital diaphragmatic hernia. Pediatr Res 59:531-537. https://doi.org/10.1203/01.pdr.0000202748.66359.a9
  24. Schalla MA, Stengel A (2018) Current understanding of the role of nesfatin-1. J Endocr Soc 10:1188-1206.
  25. Seon S, Jeon D, Kim H, Chung Y, Choi N, Yang H (2017) Testosterone regulates NUCB2 mRNA expression in male mouse hypothalamus and pituitary gland. Dev Reprod 21:71-78.
  26. 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
  27. Stengel A, Goebel M, Wang L, Tache Y (2010) Abdominal surgery activates nesfatin-1 immunoreactive brain nuclei in rats. Peptides 31:263-270. https://doi.org/10.1016/j.peptides.2009.11.015
  28. Stengel A, Goebel-Stengel M, Wang L, Kato I, Mori M, Tache Y (2012) Nesfatin-1(30-59) but not the N- and Cterminal fragments, nesfatin-1(1-29) and nesfatin-1(60-82) 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
  29. Stylianopoulou E, Lykidis D, Ypsilantis P, Simopoulos C, Skavdis G, Grigoriou M (2012) A rapid and highly sensitive method of non radioactive colorimetric in situ hybridization for the detection of mRNA on tissue sections. PLOS ONE 7:e33898. https://doi.org/10.1371/journal.pone.0033898
  30. Tam PP, Behringer RR (1997) Mouse gastrulation: The formation of a mammalian body plan. Mech Dev 68:3-25. https://doi.org/10.1016/S0925-4773(97)00123-8
  31. Warchol M, Krauss H, Wojciechowska M, Opala T, Pieta B, Zukiewicz-Sobczak W, Kupsz J, Grochowalska A (2014) The role of ghrelin, leptin and insulin in foetal development. Ann Agric Environ Med 21:349-352. https://doi.org/10.5604/1232-1966.1108603
  32. Xu L, Bloem B, Gaszner B, Roubos EW, Kozicz T (2009) Sex-specific effects of fasting on urocortin 1, cocaineand amphetamine-regulated transcript peptide and nesfatin-1 expression in the rat Edinger-Westphal nucleus. Neuroscience 162:1141-1149. https://doi.org/10.1016/j.neuroscience.2009.05.003
  33. Zorn AM, Wells JM (2009) Vertebrate endoderm development and organ formation. Annu Rev Cell Dev Biol 25:221-251. https://doi.org/10.1146/annurev.cellbio.042308.113344