Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Insulinotropic nucleobindin-2/nesfatin-1 is dynamically expressed in the haemochorial mouse and human placenta

Crystalyn B. Legg-St Pierre A B , Martina Mackova C , Ewa I. Miskiewicz A B , Denise G. Hemmings C , Suraj Unniappan A B and Daniel J. MacPhee A B D E
+ Author Affiliations
- Author Affiliations

A Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, SK, S7N 5B4, Canada.

B One Reproductive Health Research Group, University of Saskatchewan, Saskatoon, SK, S7N 5B4, Canada.

C Department of Obstetrics and Gynecology, Faculty of Medicine and Dentistry, 227 Heritage Medical Research Centre, University of Alberta, Edmonton, AB, T6G 2S2, Canada.

D Division of Biomedical Sciences, Faculty of Medicine, Memorial University of Newfoundland, St. John’s, NL, A1B 3V6, Canada.

E Corresponding author. Email: d.macphee@usask.ca

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16486
Submitted: 3 December 2016  Accepted: 29 July 2017   Published online: 31 August 2017

Abstract

The placenta is the physiological bridge between mother and fetus and has life-sustaining functions during pregnancy, including metabolic regulation, fetal protection and hormone secretion. Nucleobindin-2 (NUCB2) is a calcium- and DNA-binding protein and precursor of nesfatin-1, a signalling peptide with multiple functions, including regulation of energy homeostasis and glucose transport. These are also key functions of the placenta, yet NUCB2/nesfatin-1 expression has never been comprehensively studied in this organ. In the present study, mouse placental samples from Embryonic Day (E) 7.5 to E17.5 and human chorionic villi from the first and second trimester, as well as term pregnancy, were analysed for NUCB2/nesfatin-1 expression by immunohistochemistry with an antiserum that recognised both NUCB2 and nesfatin-1. From E7.5 to E9.5, NUCB2/nesfatin-1 was expressed in the ectoplacental cone, then parietal trophoblast giant cells and early spongiotrophoblast. At E10.5–12.5, NUCB2/nesfatin-1 expression became detectable in the developing labyrinth. From E12.5 and onwards, NUCB2/nesfatin-1 was expressed in the glycogen trophoblast cells, as well as highly expressed in syncytiotrophoblast, sinusoidal trophoblast giant cells and fetal capillary endothelial cells of the labyrinth. In all trimesters of human pregnancy, NUCB2/nesfatin-1 was highly expressed in syncytiotrophoblast. In addition, there was a significant increase in NUCB2 expression in human primary trophoblast cells induced to syncytialise. Thus, the haemochorial mammalian placenta is a novel source of NUCB2/nesfatin-1 and likely a site of its action, with potential roles in glucose homeostasis and/or nutrient sensing.

Additional keywords: labyrinth, syncytiotrophoblast, trophoblast giant cells.


References

Adamson, S. L., Lu, Y., Whiteley, K. J., Holmyard, D., Hemberger, M., Pfarrer, C., and Cross, J. C. (2002). Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev. Biol. 250, 358–373.
Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta.CrossRef | 1:CAS:528:DC%2BD38XnsFSnt74%3D&md5=a0f612035fa9bfcc57c833223442d52aCAS |

Aslan, M., Celik, O., Celik, N., Turkcuoglu, I., Yilmaz, E., Karaer, A., Simsek, Y., Celik, E., and Aydin, S. (2012). Cord blood nesfatin-1 and apelin-36 levels in gestational diabetes mellitus. Endocrine 41, 424–429.
Cord blood nesfatin-1 and apelin-36 levels in gestational diabetes mellitus.CrossRef | 1:CAS:528:DC%2BC3MXhs1Oqsb3F&md5=c8257a377f391241f56936ed426d0872CAS |

Aydin, S. (2013). Role of NUCB2/nesfatin-1 as a possible biomarker. Curr. Pharm. Des. 19, 6986–6992.
Role of NUCB2/nesfatin-1 as a possible biomarker.CrossRef | 1:CAS:528:DC%2BC3sXhvFeksr3F&md5=0db1a2b74d4ac3f9ae5f2e76a0fa3319CAS |

Barker, D. J. (2004). The developmental origins of well-being. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 1359–1366.
The developmental origins of well-being.CrossRef | 1:STN:280:DC%2BD2cvkt1eqtA%3D%3D&md5=f74d2e8a5831ce4e05ff6dd29bb57124CAS |

Benirschke, K., Kaufmann, P., and Baergen, R. N. (2006). ‘Pathology of the Human Placenta.’ 5th edn. (Springer: New York.)

Bischof, P., and Irminger-Finger, I. (2005). The human cytotrophoblastic cell, a mononuclear chameleon. Int. J. Biochem. Cell Biol. 37, 1–16.
The human cytotrophoblastic cell, a mononuclear chameleon.CrossRef | 1:CAS:528:DC%2BD2cXnslKgsrk%3D&md5=8c6bda8f060b73a92d5b41a476989ed0CAS |

Boutsikou, T., Briana, D. D., Boutsikou, M., Kafalidis, G., Piatopoulou, D., Baka, S., Hassiakos, D., Gourgiotis, D., and Malamitsi-Puchner, A. (2013). Cord blood nesfatin-1 in large for gestational age pregnancies. Cytokine 61, 591–594.
Cord blood nesfatin-1 in large for gestational age pregnancies.CrossRef | 1:CAS:528:DC%2BC38XhslajsLnF&md5=a462463820cac2b22934655a2a4b94c0CAS |

Burton, G. J., and Jones, C. J. P. (2009). Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta. Taiwan. J. Obstet. Gynecol. 48, 28–37.
Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta.CrossRef |

Cao, X., Liu, X. M., and Zhou, L. H. (2013). Recent progress in research on the distribution and function of NUCB2/nesfatin-1 in peripheral tissues. Endocr. J. 60, 1021–1027.
Recent progress in research on the distribution and function of NUCB2/nesfatin-1 in peripheral tissues.CrossRef | 1:CAS:528:DC%2BC2cXivVCmu70%3D&md5=9b4813dee29d6637f2da839ceaeb0f23CAS |

Carter, A. M. (2012). Evolution of placental function in mammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses. Physiol. Rev. 92, 1543–1576.
Evolution of placental function in mammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses.CrossRef | 1:CAS:528:DC%2BC38Xhsl2lsbnI&md5=82339fa2afb25d78dd9340415d84db00CAS |

Catak, Z., Aydin, S., Sahin, I., Kuloglu, T., Aksoy, A., and Dagli, A. F. (2014). Regulatory neuropeptides (ghrelin, obestatin and nesfatin-1) levels in serum and reproductive tissues of female and male rats with fructose-induced metabolic syndrome. Neuropeptides 48, 167–177.
Regulatory neuropeptides (ghrelin, obestatin and nesfatin-1) levels in serum and reproductive tissues of female and male rats with fructose-induced metabolic syndrome.CrossRef | 1:CAS:528:DC%2BC2cXntVChsLY%3D&md5=a49a9635cfd6328cb7753a3ffd6d2734CAS |

Constância, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C., and Reik, W. (2002). Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417, 945–948.
Placental-specific IGF-II is a major modulator of placental and fetal growth.CrossRef |

Copp, A. J. (1979). Interaction between inner cell mass and trophectoderm of the mouse blastocyst. II. The fate of the polar trophectoderm. J. Embryol. Exp. Morphol. 51, 109–120.
| 1:STN:280:DyaL3c%2Fgslyruw%3D%3D&md5=1b605311910c57ae093ddfc5e8159d3aCAS |

Cross, J. C. (2005). How to make a placenta: mechanisms of trophoblast cell differentiation in mice – a review. Placenta 26, S3–S9.
How to make a placenta: mechanisms of trophoblast cell differentiation in mice – a review.CrossRef |

Cross, J. C., Werb, Z., and Fisher, S. J. (1994). Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508–1518.
Implantation and the placenta: key pieces of the development puzzle.CrossRef | 1:CAS:528:DyaK2MXisVGmu78%3D&md5=f872eee7072554486edcfdbe73177cb9CAS |

Cross, J. C., Hemberger, M., Lu, Y., Nozaki, T., Whiteley, K., Masutani, M., and Adamson, S. L. (2002). Trophoblast functions, angiogenesis and remodeling of the maternal vasculature in the placenta. Mol. Cell. Endocrinol. 187, 207–212.
Trophoblast functions, angiogenesis and remodeling of the maternal vasculature in the placenta.CrossRef | 1:CAS:528:DC%2BD38Xjt1Sqt78%3D&md5=fc69fb6c64a00ebd43a792b7a384be8cCAS |

Dore, R., Levata, L., Lehnert, H., and Schulz, C. (2017). Nesfatin-1: functions and physiology of a novel regulatory peptide. J. Endocrinol. 232, R45–R65.
Nesfatin-1: functions and physiology of a novel regulatory peptide.CrossRef | 1:CAS:528:DC%2BC2sXktl2mtLY%3D&md5=b57bcc8f3be68edc87a3db822aa66590CAS |

Gaccioli, F., Lager, S., Powell, T., and Jansson, T. (2013). Placental transport in response to altered maternal nutrition. J. Dev. Orig. Health Dis. 4, 101–115.
Placental transport in response to altered maternal nutrition.CrossRef | 1:CAS:528:DC%2BC3sXjsVyrsrg%3D&md5=1967155a239be6f43cf42c870a829a10CAS |

Garcés, M. F., Poveda, N. E., Sánchez, E., Sanchez, A. Y., Bravo, S. B., Vázquez, M. J., Diéguez, C., Nogueiras, R., and Caminos, J. E. (2014). Regulation of NucB2/Nesfatin-1 throughout rat pregnancy. Physiol. Behav. 133, 216–222.
Regulation of NucB2/Nesfatin-1 throughout rat pregnancy.CrossRef |

García-Galiano, D., Navarro, V. M., Roa, J., Ruiz-Pino, F., Sánchez-Garrido, M. A., Pineda, R., Castellano, J. M., Romero, M., Aguilar, E., Gaytán, F., Diéguez, C., Pinilla, L., and Tena-Sempere, M. (2010). The anorexigenic neuropeptide, nesfatin-1, is indispensable for normal puberty onset in the female rat. J. Neurosci. 30, 7783–7792.
The anorexigenic neuropeptide, nesfatin-1, is indispensable for normal puberty onset in the female rat.CrossRef |

Georgiades, P., Ferguson-Smith, A. C., and Burton, G. J. (2002). Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23, 3–19.
Comparative developmental anatomy of the murine and human definitive placentae.CrossRef | 1:STN:280:DC%2BD387jt1Kluw%3D%3D&md5=64d475bae6e0923b78cae0d2021789fcCAS |

Gonçalves, C. R., Antonini, S., Vianna-Morgante, A. M., Machado-Santelli, G. M., and Bevilacqua, E. (2003). Developmental changes in the ploidy of mouse implanting trophoblast cells in vitro. Histochem. Cell Biol. 119, 189–198.
Developmental changes in the ploidy of mouse implanting trophoblast cells in vitro.CrossRef |

Gonzalez, R., Tiwari, A., and Unniappan, S. (2009). Pancreatic beta cells colocalize insulin and pronesfatin immunoreactivity in rodents. Biochem. Biophys. Res. Commun. 381, 643–648.
Pancreatic beta cells colocalize insulin and pronesfatin immunoreactivity in rodents.CrossRef | 1:CAS:528:DC%2BD1MXjvVOqsrc%3D&md5=e76b0fef73abb8af0cd3ed8172ef316dCAS |

Gonzalez, R., Reingold, B. K., Gao, X., Gaidhu, M. P., Tsushima, R. G., and Unniappan, S. (2011a). Nesfatin-1 exerts a direct, glucose-dependent insulinotropic action on mouse islet β- and MIN6 cells. J. Endocrinol. 208, R9–R16.
Nesfatin-1 exerts a direct, glucose-dependent insulinotropic action on mouse islet β- and MIN6 cells.CrossRef | 1:CAS:528:DC%2BC3MXjslelur4%3D&md5=8ac8dc538b7a2289382eb52bb9894691CAS |

Gonzalez, R., Perry, R. L. S., Gao, X., Gaidhu, M. P., Tsushima, R. G., Ceddia, R. B., and Unniappan, S. (2011b). Nutrient responsive nesfatin-1 regulates energy balance and induces glucose-stimulated insulin secretion in rats. Endocrinology 152, 3628–3637.
Nutrient responsive nesfatin-1 regulates energy balance and induces glucose-stimulated insulin secretion in rats.CrossRef | 1:CAS:528:DC%2BC3MXhsVanurvM&md5=72fae7c34a12c72df3d69f8425f4acedCAS |

Gonzalez, R., Mohan, H., and Unniappan, S. (2012). Nucleobindins: bioactive precursor proteins encoding putative endocrine factors? Gen. Comp. Endocrinol. 176, 341–346.
Nucleobindins: bioactive precursor proteins encoding putative endocrine factors?CrossRef | 1:CAS:528:DC%2BC38XlvFyisLk%3D&md5=19b5afdf8937188bf05f5a9c314fb198CAS |

Guibourdenche, J., Fournier, T., Malassine, A., and Evain-Brion, D. (2009). Development and hormonal functions of the human placenta. Folia Histochem. Cytobiol. 47, S35–S40.
Development and hormonal functions of the human placenta.CrossRef | 1:CAS:528:DC%2BC3MXitlemtLY%3D&md5=fde187c9e87cb325d8680b60c17857e2CAS |

Guilbert, L. J., Winkler-Lowen, B., Sherburne, R., Rote, N. S., Li, H., and Morrish, D. W. (2002). Preparation and functional characterization of villous cytotrophoblasts free of syncytial fragments. Placenta 23, 175–183.
Preparation and functional characterization of villous cytotrophoblasts free of syncytial fragments.CrossRef | 1:STN:280:DC%2BD383ht1Clug%3D%3D&md5=e87c2691bae46ab436e129fe23c37aa2CAS |

Gungor, S., Gurates, B., Aydin, S., Sahin, I., Kavak, S. B., Kumru, S., Celik, H., Aksoy, A., Yilmaz, M., Catak, Z., Citil, C., Baykus, Y., Deniz, R., Karakaya, F., and Özdemir, N. (2013). Ghrelins, obestatin, nesfatin-1 and leptin levels in pregnant women with and without hyperemesis gravidarum. Clin. Biochem. 46, 828–830.
Ghrelins, obestatin, nesfatin-1 and leptin levels in pregnant women with and without hyperemesis gravidarum.CrossRef | 1:CAS:528:DC%2BC3sXksVyrtr8%3D&md5=c21b19bf2c5f82bfee14261fdbb16ffeCAS |

Hu, D., and Cross, J. C. (2010). Development and function of trophoblast giant cells in the rodent placenta. Int. J. Dev. Biol. 54, 341–354.
Development and function of trophoblast giant cells in the rodent placenta.CrossRef | 1:CAS:528:DC%2BC3cXltVajtbg%3D&md5=9568d62557b67878cd5f181c27ccd4f4CAS |

Jackson, D., Volpert, O. V., Bouck, N., and Linzer, D. I. (1994). Stimulation and inhibition of angiogenesis by placental proliferin and proliferin-related protein. Science 266, 1581–1584.
Stimulation and inhibition of angiogenesis by placental proliferin and proliferin-related protein.CrossRef | 1:CAS:528:DyaK2MXisVGlsrc%3D&md5=772a1e6f930a95fbcd8f79016ad0811eCAS |

John, R., and Hemberger, M. (2012). A placenta for life. Reprod. Biomed. Online 25, 5–11.
A placenta for life.CrossRef | 1:CAS:528:DC%2BC38XhtVSgt77K&md5=6e958f1f7d945c5e927346fe5ef7914cCAS |

Kaufmann, P., Black, S., and Huppertz, B. (2003). Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod. 69, 1–7.
Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia.CrossRef | 1:CAS:528:DC%2BD3sXkvFCnsbY%3D&md5=42f6f71aea2b681ff8e04bfd8b9ac286CAS |

Kilani, R. T., Chang, L. J., Garcia-Lloret, M. I., Hemmings, D. G., Winkler-Lowen, B., and Guilbert, L. J. (1997). Placental trophoblasts resist infection by multiple human immunodeficiency virus (HIV) type 1 variants even with cytomegalovirus coinfection but support HIV replication after provirus transfection. J. Virol. 71, 6359–6372.
| 1:CAS:528:DyaK2sXlsVKqtLk%3D&md5=b89d3b46f391323c83d93dfcb3794dc1CAS |

Kim, J., Chung, Y., Kim, H., Im, E., Lee, H., and Yang, H. (2014). The tissue distribution of nesfatin-1/NUCB2 in mouse. Dev. Reprod. 18, 301–309.
The tissue distribution of nesfatin-1/NUCB2 in mouse.CrossRef |

Knox, K., Leuenberger, D., Penn, A. A., and Baker, J. C. (2011). Global hormone profiling of murine placenta reveals secretin expression. Placenta 32, 811–816.
Global hormone profiling of murine placenta reveals secretin expression.CrossRef | 1:CAS:528:DC%2BC3MXhsVagtL7J&md5=b2489390ed23016dc11b6fe170177a19CAS |

Larqué, E., Ruiz-Palacios, M., and Koletzko, B. (2013). Placental regulation of fetal nutrient supply. Curr. Opin. Clin. Nutr. Metab. Care 16, 292–297.
Placental regulation of fetal nutrient supply.CrossRef |

Li, Z., Xu, G., Li, Y., Zhao, J., and Mulholland, M. W. (2012). mTOR-dependent modulation of gastric nesfatin- 1/NUCB2. Cell. Physiol. Biochem. 29, 493–500.
mTOR-dependent modulation of gastric nesfatin- 1/NUCB2.CrossRef | 1:CAS:528:DC%2BC38Xls12isL4%3D&md5=cada735bcd688e34b51f4ca7ed9dfdeaCAS |

Li, R., Wu, Q., Zhao, Y., Jin, W., Yuan, X., Wu, X., Tang, Y., Zhang, J., Tan, X., Bi, F., and Lui, J. N. (2013a). The novel pro-osteogenic activity of NUCB2 (1–83). PLoS One 8, e61619.
The novel pro-osteogenic activity of NUCB2 (1–83).CrossRef | 1:CAS:528:DC%2BC3sXmslSjsL0%3D&md5=15231b5279a160f935d41e1360e837b1CAS |

Li, Z., Gao, L., Tang, H., Yin, Y., Xiang, X., Li, Y., Zhao, J., Mulholland, M., and Zhang, W. (2013b). Peripheral effects of nesfatin-1 on glucose homeostasis. PLoS One 8, e71513.
Peripheral effects of nesfatin-1 on glucose homeostasis.CrossRef | 1:CAS:528:DC%2BC3sXhtlCktrnP&md5=17b8ab61f6f2c06d919ebe415badf069CAS |

Linzer, D. I., and Fisher, S. J. (1999). The placenta and the prolactin family of hormones: regulation of the physiology of pregnancy. Mol. Endocrinol. 13, 837–840.
The placenta and the prolactin family of hormones: regulation of the physiology of pregnancy.CrossRef | 1:CAS:528:DyaK1MXjs1ynsrw%3D&md5=9129f932dd9543d8821443429ea61574CAS |

Mohan, H., Ramesh, N., Mortazavi, S., Le, A., Iwakura, H., and Unniappan, S. (2014). Nutrients differentially regulate nucleobindin-2/nesfatin-1 in vitro in cultured stomach ghrelinoma (MGN3–1) cells and in vivo in male mice. PLoS One 9, e115102.
Nutrients differentially regulate nucleobindin-2/nesfatin-1 in vitro in cultured stomach ghrelinoma (MGN3–1) cells and in vivo in male mice.CrossRef |

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., Honguchi, K., Yamada, M., and Mori, M. (2006). Identification of nesfatin-1 as a satiety molecule in the hypothalamus. Nature 443, 709–712.
Identification of nesfatin-1 as a satiety molecule in the hypothalamus.CrossRef | 1:CAS:528:DC%2BD28XhtVGkur3K&md5=f0633af53d0276feed5fd00f5efdd7a7CAS |

Prinz, P., Goebel-Stengel, M., Teuffel, P., Rose, M., Klapp, B. F., and Stengel, A. (2016). Peripheral and central localization of the nesfatin-1 receptor using autoradiography in rats. Biochem. Biophys. Res. Commun. 470, 521–527.
Peripheral and central localization of the nesfatin-1 receptor using autoradiography in rats.CrossRef | 1:CAS:528:DC%2BC28XhvFOkt7g%3D&md5=12cfde27e85e5c12433d692d3bdab0a4CAS |

Ramanjaneya, M., Chen, J., Brown, J. E., Tripathi, G., Hallschmid, M., Patel, S., Kern, W., Hillhouse, E. W., Lehnert, H., Tan, B. K., and Randeva, H. S. (2010). Identification of nesfatin-1 in human and murine adipose tissue: a novel depot-specific adipokine with increased levels in obesity. Endocrinology 151, 3169–3180.
Identification of nesfatin-1 in human and murine adipose tissue: a novel depot-specific adipokine with increased levels in obesity.CrossRef | 1:CAS:528:DC%2BC3cXpt1Cmsrw%3D&md5=2d1993d2728fc358dfd81a793367dc02CAS |

Ramesh, N., Mortazavi, S., and Unniappan, S. (2015). Nesfatin-1 stimulates glucagon-like peptide-1 and glucose-dependent insulinotropic polypeptide secretion from STC-1 cells in vitro. Biochem. Biophys. Res. Commun. 462, 124–130.
Nesfatin-1 stimulates glucagon-like peptide-1 and glucose-dependent insulinotropic polypeptide secretion from STC-1 cells in vitro.CrossRef | 1:CAS:528:DC%2BC2MXnslOjsLw%3D&md5=be5efbb34d6e818bdcb40d2ef47549c3CAS |

Red-Horse, K., Zhou, Y., Genbacev, O., Prakobphol, A., Foulk, R., McMaster, M., and Fisher, S. J. (2004). Trophoblast differentiation during embryo implantation and formation of the maternal–fetal interface. J. Clin. Invest. 114, 744–754.
Trophoblast differentiation during embryo implantation and formation of the maternal–fetal interface.CrossRef | 1:CAS:528:DC%2BD2cXnslWitbk%3D&md5=fc4366681d2f8fc401757ce93d730855CAS |

Rosario, F. J., Powell, T. L., and Jansson, T. (2016). Activation of placental insulin and mTOR signaling in a mouse model of maternal obesity associated with fetal overgrowth. Am. J. Physiol. Regul. Integr. Comp. Physiol. 310, R87–R93.
Activation of placental insulin and mTOR signaling in a mouse model of maternal obesity associated with fetal overgrowth.CrossRef |

Rossant, J., and Cross, J. C. (2001). Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2, 538–548.
Placental development: lessons from mouse mutants.CrossRef | 1:CAS:528:DC%2BD3MXltVCksLc%3D&md5=c3e0774ef689d11200cc65da1d12c6cbCAS |

Sati, L., Soygur, B., and Cilek-Ozenci, C. (2016). Expression of mammalian target of rapamycin and downstream targets in normal and gestational diabetic human term placenta. Reprod. Sci. 23, 324–332.
Expression of mammalian target of rapamycin and downstream targets in normal and gestational diabetic human term placenta.CrossRef | 1:CAS:528:DC%2BC28XpvVentL8%3D&md5=b087a3937ec9338d01a8aa2fa6fbb856CAS |

Senner, C. E., and Hemberger, M. (2010). Regulation of early trophoblast differentiation: lessons from the mouse. Placenta 31, 944–950.
Regulation of early trophoblast differentiation: lessons from the mouse.CrossRef | 1:STN:280:DC%2BC3cbhvFenuw%3D%3D&md5=c8db22338e52b0616e97feb8ec4473ebCAS |

Serin, S., Bakacak, M., Ercan, Ö., Köstü, B., Avci, F., Arıkan, D., and Kıran, G. (2016). The evaluation of nesfatin-1 levels in patients with and without intrauterine growth restriction. J. Matern. Fetal Neonatal Med. 29, 1409–1413.
The evaluation of nesfatin-1 levels in patients with and without intrauterine growth restriction.CrossRef | 1:CAS:528:DC%2BC28XivVGnurc%3D&md5=25d9826f7e07da0ba0cdb8ed3b722ad9CAS |

Simmons, D. G., and Cross, J. C. (2005). Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev. Biol. 284, 12–24.
Determinants of trophoblast lineage and cell subtype specification in the mouse placenta.CrossRef | 1:CAS:528:DC%2BD2MXntVGnsrw%3D&md5=ddbc66aac6dec82dc8699fed547c24a1CAS |

Simmons, D. G., Fortier, A. L., and Cross, J. C. (2007). Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 304, 567–578.
Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta.CrossRef | 1:CAS:528:DC%2BD2sXjvFehtLs%3D&md5=f6b46d403bb577fb53519ff1044ed322CAS |

Simmons, D. G., Rawn, S., Davies, A., Hughes, M., and Cross, J. C. (2008). Spatial and temporal expression of the 23 murine prolactin/placental lactogen-related genes is not associated with their position in the locus. BMC Genomics 9, 352.
Spatial and temporal expression of the 23 murine prolactin/placental lactogen-related genes is not associated with their position in the locus.CrossRef |

Stengel, A., Mori, M., and Tache, Y. (2013). The role of nesfatin-1 in the regulation of food intake and body weight: recent developments and future endeavors. Obes. Rev. 14, 859–870.
The role of nesfatin-1 in the regulation of food intake and body weight: recent developments and future endeavors.CrossRef | 1:CAS:528:DC%2BC3sXhs1elu77I&md5=53486a85df4ab2ee34c5048f7cd0ee27CAS |

Su, Y., Zhang, J., Tang, Y., Bi, F., and Liu, J. N. (2010). The novel function of nesfatin-1: anti-hyperglycemia. Biochem. Biophys. Res. Commun. 391, 1039–1042.
The novel function of nesfatin-1: anti-hyperglycemia.CrossRef | 1:CAS:528:DC%2BC3cXptlel&md5=839fbd69a2336db7a24a4802cec2a12cCAS |

Suzuki, S., Takagi, K., Miki, Y., Onodera, Y., Akahira, J., Ebata, A., Ishida, T., Watanabe, M., Sasano, H., and Suzuki, T. (2012). Nucleobindin 2 in human breast carcinoma as a potent prognostic factor. Cancer Sci. 103, 136–143.
Nucleobindin 2 in human breast carcinoma as a potent prognostic factor.CrossRef | 1:CAS:528:DC%2BC38Xhtlaht7k%3D&md5=5bab0ebe402248f76cc21104714cb88dCAS |

Tagaya, Y., Miura, A., Okada, S., Ohshima, K., and Mori, M. (2012). Nucleobindin-2 is a positive modulator of EGF-dependent signals leading to enhancement of cell growth and suppression of adipocyte differentiation. Endocrinology 153, 3308–3319.
Nucleobindin-2 is a positive modulator of EGF-dependent signals leading to enhancement of cell growth and suppression of adipocyte differentiation.CrossRef | 1:CAS:528:DC%2BC38XpsFWgu7o%3D&md5=b9575813c39177a89d04f9298c221d4eCAS |

Watson, E. D., and Cross, J. C. (2005). Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20, 180–193.
Development of structures and transport functions in the mouse placenta.CrossRef | 1:CAS:528:DC%2BD2MXls1GgtrY%3D&md5=dd3231c5dbbc0e8691e51fdf45982ed7CAS |

Wiemers, D. O., Shao, L. J., Ain, R., Dai, G., and Soares, M. J. (2003). The mouse prolactin gene family locus. Endocrinology 144, 313–325.
The mouse prolactin gene family locus.CrossRef | 1:CAS:528:DC%2BD3sXhtFSltA%3D%3D&md5=6172000891e57168b3d4bdd8162359e3CAS |

Wynne, F., Ball, M., McLellan, A. S., Dockery, P., Zimmermann, W., and Moore, T. (2006). Mouse pregnancy-specific glycoproteins: tissue-specific expression and evidence of association with maternal vasculature. Reproduction 131, 721–732.
Mouse pregnancy-specific glycoproteins: tissue-specific expression and evidence of association with maternal vasculature.CrossRef | 1:CAS:528:DC%2BD28XltV2jtrY%3D&md5=3602fe29a1633b5364335086440a827fCAS |

Yamawaki, H., Takahashi, M., Mukohda, M., Morita, T., Okada, M., and Hara, Y. (2012). A novel adipocytokine, nesfatin-1 modulates peripheral arterial contractility and blood pressure in rats. Biochem. Biophys. Res. Commun. 418, 676–681.
A novel adipocytokine, nesfatin-1 modulates peripheral arterial contractility and blood pressure in rats.CrossRef | 1:CAS:528:DC%2BC38XitFyisL8%3D&md5=edb071485716fa3f938f77bbfa2794ceCAS |

Yui, J., Garcia-Lloret, M., Brown, A. J., Berdan, R. C., Morrish, D. W., Wegmann, T. G., and Guilbert, L. J. (1994). Functional, long-term cultures of human term trophoblasts purified by column-elimination of CD9 expressing cells. Placenta 15, 231–246.
Functional, long-term cultures of human term trophoblasts purified by column-elimination of CD9 expressing cells.CrossRef | 1:CAS:528:DyaK2cXksFGgurk%3D&md5=7a3d0f8b9839c4c959b628f12ba6b94bCAS |

Zhang, A. Q., Li, X. L., Jiang, C. Y., Lin, L., Shi, R. H., Chen, J. D., and Oomura, Y. (2010). Expression of nesfatin-1/NUCB2 in rodent digestive system. World J. Gastroenterol. 16, 1735–1741.
Expression of nesfatin-1/NUCB2 in rodent digestive system.CrossRef | 1:CAS:528:DC%2BC3cXltVKhu7w%3D&md5=1502c1d00f038779cb2df66c48ed1d86CAS |

Zhang, H., Qi, C., Wang, A., Yao, B., Li, L., Wang, Y., and Hu, Y. (2013). Prognostication of prostate cancer based on NUCB2 protein assessment: NUCB2 in prostate cancer. J. Exp. Clin. Cancer Res. 32, 77.
Prognostication of prostate cancer based on NUCB2 protein assessment: NUCB2 in prostate cancer.CrossRef | 1:CAS:528:DC%2BC2cXhtFGktb7I&md5=137454755db811d72103230ab4f28a35CAS |

Zhang, C., Wang, Y., Wang, Y., Li, J., Liu, R., and Liu, H. (2014). Decreased levels of serum nesfatin-1 in patients with preeclampsia. Biomarkers 19, 402–406.
Decreased levels of serum nesfatin-1 in patients with preeclampsia.CrossRef | 1:CAS:528:DC%2BC2cXhtFynsbfN&md5=cd75a57c3dd8c3efabdd2519c557f191CAS |



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