Hostname: page-component-669899f699-chc8l Total loading time: 0 Render date: 2025-04-26T14:20:18.407Z Has data issue: false hasContentIssue false
  • English
  • Français

A molecular mechanism of mouse placental spongiotrophoblast differentiation regulated by prolyl oligopeptidase

Published online by Cambridge University Press:  04 February 2019

Yuki Maruyama  and
Atsushi P. Kimura Open the ORCID record for Atsushi P. Kimura [Opens in a new window]
Yuki Maruyama
Affiliation:
Graduate School of Life Science, Hokkaido University, Sapporo 060–0810, Japan
Atsushi P. Kimura*
Affiliation:
Graduate School of Life Science, Hokkaido University, Sapporo 060–0810, Japan Department of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan
*
*Address for correspondence: Atsushi P. Kimura. Department of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo 060–0810, Japan. Tel: +81 11 706 4452. E-mail: akimura@sci.hokudai.ac.jp
Get access Rights & Permissions [Opens in a new window]

Summary

In eutherian mammals, the placenta plays a critical role in embryo development by supplying nutrients and hormones and mediating interaction with the mother. To establish the fine connection between mother and embryo, the placenta needs to be formed normally, but the mechanism of placental differentiation is not fully understood. We previously revealed that mouse prolyl oligopeptidase (POP) plays a role in trophoblast stem cell (TSC) differentiation into two placental cell types, spongiotrophoblasts (SpT) and trophoblast giant cells. Here, we focused on SpT differentiation and attempted to elucidate a molecular mechanism. For Ascl2, Arnt, and Egfr genes that are indispensable for SpT formation, we found that a POP-specific inhibitor, SUAM-14746, significantly decreased Ascl2 expression, which was consistent with a significant decrease in expression of Flt1, a gene downstream of Ascl2. Although this downregulation was unlikely to be mediated by the PI3K-Akt pathway, our results indicated that POP controls TSC differentiation into SpT by regulating the Ascl2 gene.

Keywords

Ascl2Prolyl oligopeptidaseSpongiotrophoblastSUAM-14746Trophoblast stem cell
Type
Short Communication
Information
Zygote , Volume 27 , Issue 1 , February 2019 , pp. 49 - 53
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

Cite this article: Y. Maruyama and A.P. Kimura (2019) A molecular mechanism of mouse placental spongiotrophoblast differentiation regulated by prolyl oligopeptidase. Zygote page 1 of 5. doi: 10.1017/S0967199418000655

References

Adelman, DM, Gertsenstein, M, Nagy, A, Simon, MC and Maltepe, E (2000) Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 14, 3191–3203.Google Scholar
Cross, JC (2005) How to make a placenta: mechanisms of trophoblast cell differentiation in mice – a review. Placenta 26, S3–S9.Google Scholar
Cross, JC (2006) Placental function in development and disease. Reprod Fertil Dev 18, 71–76.Google Scholar
Duan, L, Ying, G, Danzer, B, Perez, RE, Shariat-Madar, Z, Levenson, VV and Maki, CG (2014) The prolyl peptidases PRCP/PREP regulate IRS-1 stability critical for rapamycin-induced feedback activation of PI3K and AKT. J Biol Chem 289, 21694–21705.Google Scholar
El-Hashash, AHK, Warburton, D and Kimber, SJ (2010) Genes and signals regulating murine trophoblast cell development. Mech Dev 127, 1–20.Google Scholar
García-Horsman, JA, Männistö, PT and Venäläinen, JI (2007) On the role of prolyl oligopeptidase in health and disease. Neuropeptides 41, 1–24.Google Scholar
Guillemot, F, Nagy, A, Auerbach, A, Rossant, J and Joyner, AL (1994) Essential role of Mash-2 in extraembryonic development. Nature 371, 333–336.Google Scholar
Guillemot, F, Caspary, T, Tilghman, SM, Copeland, NG, Gilbert, DJ, Jenkins, NA, Anderson, DJ, Joyner, AL, Rossant, J and Nagy, A (1995) Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat Genet 9, 235–242.Google Scholar
Himeno, E, Tanaka, S and Kunath, T (2008) Isolation and manipulation of mouse trophoblast stem cells. Curr Protoc Stem Cell Biol 7, 1E4.1–1E4.27.Google Scholar
Hirashima, M, Lu, Y, Byers, L and Rossant, J (2003) Trophoblast expression of fms-like tyrosine kinase 1 is not required for the establishment of the maternal-fetal interface in the mouse placenta. Proc Natl Acad Sci 100, 15637–15642.Google Scholar
Hu, D and Cross, JC (2010) Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol 54, 341–354.Google Scholar
Hu, D and Cross, JC (2011) Ablation of Tpbpa-positive trophoblast precursors leads to defects in maternal spiral artery remodeling in the mouse placenta. Dev Biol 358, 231–239.Google Scholar
Hughes, M, Dobric, N, Scott, IC, Su, L, Starovic, M, St-Pierre, B, Egan, SE, Kingdom, JCP and Cross, JC (2004) The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells. Dev Biol 271, 26–37.Google Scholar
Ishino, T, Ohtsuki, S, Homma, K and Natori, S (1998) cDNA cloning of mouse prolyl endopeptidase and its involvement in DNA synthesis by Swiss 3T3 cells. J Biochem 123, 540–545.Google Scholar
Johnson, JE, Birren, SJ, Saito, T and Anderson, DJ (1992) DNA binding and transcriptional regulatory activity of mammalian achaete-scute homologous (MASH) proteins revealed by interaction with a muscle-specific enhancer. Proc Natl Acad Sci USA 89, 3596–3600.Google Scholar
Jubb, AM, Chalasani, S, Frantz, GD, Smits, R, Grabsch, HI, Kavi, V, Maughan, NJ, Hillan, KJ, Quirke, P and Koeppen, H (2006) Achaete-scute like 2 (ascl2) is a target of Wnt signalling and is upregulated in intestinal neoplasia. Oncogene 25, 3445–3457.Google Scholar
Kozak, KR, Abbott, B and Hankinson, O (1997) ARNT-deficient mice and placental differentiation. Dev Biol 191, 297–305.Google Scholar
Latos, PA and Hemberger, M (2014) The transcriptional and signalling networks of mouse trophoblast stem cells. Placenta 35, S81–S85.Google Scholar
Maruyama, Y, Matsubara, S and Kimura, AP (2017) Mouse prolyl oligopeptidase plays a role in trophoblast stem cell differentiation into trophoblast giant cell and spongiotrophoblast. Placenta 53, 8–15.Google Scholar
Matsubara, S, Takahashi, T and Kimura, AP (2010) Epigenetic patterns at the mouse prolyl oligopeptidase gene locus suggest the CpG island in the gene body to be a novel regulator for gene expression. Gene 465, 17–29.Google Scholar
Matsubara, S, Takahashi, T and Kimura, AP (2011) Localization and subcellular distribution of prolyl oligopeptidase in the mouse placenta. J Mol Histol 42, 251–264.Google Scholar
Matsubara, S, Maruyama, Y and Kimura, AP (2013) A 914-bp promoter is sufficient to reproduce the endogenous prolyl oligopeptidase gene localization in the mouse placenta if not subject to position effect. Gene 524, 114–123.Google Scholar
Miettinen, PJ, Berger, JE, Meneses, J, Phung, Y, Pedersen, RA, Werb, Z and Derynck, R (1995) Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376, 337–341.Google Scholar
Myöhänen, TT, García-Horsman, JA, Tenorio-Laranga, J and Männistö, PT (2009) Issues about the physiological functions of prolyl oligopeptidase based on its discordant spatial association with substrates and inconsistencies among mRNA, protein levels, and enzymatic activity. J Histochem Cytochem 57, 831–848.Google Scholar
Ohtsuki, S, Homma, K, Kurata, S, Komano, H and Natori, S (1994) A prolyl endopeptidase of Sarcophaga peregrina (flesh fly): its purification and suggestion for its participation in the differentiation of the imaginal discs. J Biochem 115, 449–453.Google Scholar
Rielland, M, Hue, I, Renard, J-P and Alice, J (2008) Trophoblast stem cell derivation, cross-species comparison and use of nuclear transfer: new tools to study trophoblast growth and differentiation. Dev Biol 322, 1–10.Google Scholar
Rossant, J and Cross, JC (2001) Placental development: lessons from mouse mutants. Nat Rev Genet 2, 538–548.Google Scholar
Saito, M, Hashimoto, M, Kawaguchi, N, Shibata, H, Fukami, H, Tanaka, T and Higuchi, N (1991) Synthesis and inhibitory activity of acyl-peptidyl-pyrrolidine derivatives toward post-proline cleaving enzyme; a study of subsite specificity. J Enzyme Inhib 5, 51–75.Google Scholar
Sharma, N, Kubaczka, C, Kaiser, S, Nettersheim, D, Mughal, SS, Riesenberg, S, Hölzel, M, Winterhager, E and Schorle, H (2016) Tpbpa-Cre-mediated deletion of TFAP2C leads to deregulation of Cdkn1a, Akt1 and the ERK pathway, causing placental growth arrest. Development 143, 787–798.Google Scholar
Sibilia, M and Wagner, EF (1995) Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269, 234–238.Google Scholar
Takao, T, Asanoma, K, Tsunematsu, R, Kato, K and Wake, N (2012) The maternally expressed gene Tssc3 regulates the expression of MASH2 transcription factor in mouse trophoblast stem cells through the AKT-Sp1 signaling pathway. J Biol Chem 287, 42685–42694.Google Scholar
Tanaka, M, Gertsenstein, M, Rossant, J and Nagy, A (1997) Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev Biol 190, 55–65.Google Scholar
Tanaka, S, Kunath, T, Hadjantonakis, AK, Nagy, A and Rossant, J (1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072–2075.Google Scholar
Threadgill, D, Dlugosz, A, Hansen, L, Tennenbaum, T, Lichti, U, Yee, D, LaMantia, C, Mourton, T, Herrup, K, Harris, R, et al. (1995) Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269, 230–234.Google Scholar
Venditti, M and Minucci, S (2018) Subcellular localization of prolyl endopeptidase during the first wave of rat spermatogenesis and in rat and human sperm. J Histochem Cytochem 2215541881006. doi: 10.1369/0022155418810064 [Epub ahead of print]Google Scholar
Watson, ED and Cross, JC (2005) Development of structures and transport functions in the mouse placenta. Physiology 20, 180–193.Google Scholar
Williams, RS, Eames, M, Ryves, WJ, Viggars, J and Harwood, AJ (1999) Loss of a prolyl oligopeptidase confers resistance to lithium by elevation of inositol (1,4,5)trisphosphate. EMBO J 18, 2734–2745.Google Scholar
Zhou, Z, Rao, J, Yang, J, Wu, F, Tan, J, Xu, S, Ding, Y, Zhan, N, Hu, X, Cui, Y, Zhang, X, Dong, W, Liu, XD and Bian, XW (2015) SEMA3F prevents metastasis of colorectal cancer by PI3K-AKT-dependent down-regulation of the ASCL2-CXCR4 axis. J Pathol 236, 467–478.Google Scholar