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

Expression of neuropeptide Y is increased in murine endometrial epithelium during the peri-implantation period under regulation by sex steroids

Hitoshi Yonaha A , Hiroyuki Minoura A C , Toshimichi Yoshida B , Shigeto Takeuchi A , Naomi Noda A , Keisuke Tanaka A , Rika Nishiura A , Hiroaki Kawato A and Nagayasu Toyoda A
+ Author Affiliations
- Author Affiliations

A Department of Obstetrics and Gynecology, Mie University School of Medicine, 2-174 Edobashi, Tsu-shi Mie, 514-0001, Japan.

B Department of Pathology, Mie University School of Medicine, 2-174 Edobashi, Tsu-shi Mie, 514-0001, Japan.

C To whom correspondence should be addressed. email: mitaki2f@cty-net.ne.jp

Reproduction, Fertility and Development 16(3) 355-361 https://doi.org/10.1071/RD02088
Submitted: 15 October 2002  Accepted: 23 March 2004   Published: 25 May 2004

Abstract

Oligopeptide hormones are involved in cell–cell interaction during embryonal implantation and neuropeptide Y (NPY) is expressed in the human placenta and decidual cells in the third trimester of pregnancy. However, there is no report regarding the intrauterine localisation and the functions of NPY during the peri-implantation period. In the present study, the spatiotemporal changes in NPY expression in the murine uterus during the peri-implantation period were investigated using reverse transcription–polymerase chain reaction (RT-PCR), quantitative RT-PCR and immunohistochemical techniques, as were the effects of sex steroids on NPY mRNA expression in primary cultured murine uterine epithelial cells. Neuropeptide Y mRNA was increased in the pregnant murine uterus, as well as in the pseudopregnant murine uterus, during the peri-implantation period. Immunohistochemical analysis revealed increases in NPY expression in luminal and glandular epithelial cells and decidualised stromal cells. Neuropeptide Y mRNA expression was strongly induced in cultured epithelial cells in response to sex steroids. The data suggest that NPY is involved in cell–cell interactions during embryonic implantation.


References

Bell, C. (1974). Control of uterine blood flow in pregnancy. Med. Biol. 52, 219–228.
PubMed |

Chomczynski, P. , and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal. Biochem. 162, 156–159.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Dotsch, J. , Nusken, K. D. , Knerr, I. , Kirschbaum, M. , Repp, R. , and Rascher, W. (1999). Leptin and neuropeptideY gene expression in human placenta: ontogeny and evidence for similalities to hypothalamic regulation. J. Clin. Endocrinol. Metab. 84, 2755–2758.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Edvinsson, L. , Emson, P. , Mc Culloch, J. , and Tatemoto, R. (1983). Neuropeptide Y cerebrovascular innervation and vasomotor effect in the cat. Neurosci. Lett. 43, 79–84.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Fallgren, B. , Edvinsson, L. , Ekblad, E. , and Ekman, R. A. (1989). Involvement of perivascular neuropeptide Y nerve fibers in uterine arterial vasoconstriction in conjunction with pregnancy. Regul. Pept. 24, 119–130.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Fried, G. , and Thoresen, M. (1990). Effects of neuropeptide Y and noradrenaline on uterine artery blood pressure and blood flow velocity in the pregnant guinea pig. Regul. Pept. 28, 1–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Garris, D. R. , and Whitehead, D. S. (1981). Uterine blood flow and timing of blastocyst implantation in the guinea pig. Am. J. Physiol. 24, 142–145.


Garris, D. R. , Fair, J. H. , Whitehead, D. S. , and Muse, P. D. (1983). Relationship between deciduoma formation and uterine blood flow in the pseudopregnant rat. Gynecol. Obstet. Invest. 15, 84–92.
PubMed |

Goumain, M. , Voisin, T. , Lorinet, A. M. , and Laburthe, M. (1998). Identification and distribution of mRNA encoding the Y1, Y2, Y4, and Y5 receptors for peptides of the PP-fold family in the rat intestine and colon. Biochem. Biophys. Res. Commun. 247, 52–56.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gray, C. A. , Bartol, F. F. , Tarleton, B. J. , Wiley, A. A. , Johnson, G. A. , Bazer, F. W. , and Spencer, T. E. (2001a). Developmental biology of uterine glands. Biol. Reprod. 65, 1311–1323.
PubMed |

Gray, C. A. , Taylor, K. M. , Ramsey, W. S. , Hill, J. R. , Bazer, F. W. , Bartol, F. F. , and Spencer, T. E. (2001b). Endometrial glands are required for preimplantation conceptus elongation and survival. Biol. Reprod. 64, 1608–1613.
PubMed |

Hart, M. V. , Hosenpud, J. D. , Hohimer, A. R. , and Morton, M. J. (1985). Hemodynamics during pregnancy and sex steroid administration in guinea pigs. Am. J. Physiol. 249, 179–185.


Inui, A. (1999). Feeding and body-weight regulation by hypothalamic neuropeptides mediation of the actions of leptin. Trends Neurosci. 22, 62–67.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Jacobs, A. L. , and Carson, D. D. (1991). Proteoglycan synthesis and metabolism by mouse uterine stroma cultured in vitro. J. Biol. Chem. 15, 15 464–15 473.


Jacobs, A. L. , Decker, G. L. , Glasser, S. R. , Julian, J. , and Carson, D. D. (1990). Vectorial secretion of prostaglandins by polarized rodent uterine epithelial cells. Endocrinology 126, 2125–2136.
PubMed |

Jovanovic, S. , Grbovic, L. , and Jovanovic, A. (2000). Pregnancy is associated with altered response to neuropeptide Y in uterine artery. Mol. Hum. Reprod. 6, 352–360.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kozak, R. , Mercer, J. G. , Burlet, C. , and Beck, B. (1998). Hypothalamic neuropeptide Y content and mRNA expression in weaning rats subjected to dietary manipulations during fetal and neonatal life. Regul. Pept. 75–76, 397–402.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Li, C. , Chen, P. , and Smith, M. S. (1998). Neuropeptide Y neurons in the arcuate nucleus (ARH) and dorsomedial nucleus (DMH), areas activated during lactation, project to the paraventricular nucleus of the hypothalamus (PVH). Regul. Pept. 75–76, 93–100.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lundberg, J. M. , Terenius, L. , Hokfelt, L. , Martling, C. R. , Tatemoto, K. , Mutt, V. , Polak, J. M. , Bloom, S. R. , and Goldstein, M. (1982). Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol. Scand. 116, 477–480.
PubMed |

Lundberg, J. M. , Rudehill, A. , Sollevi, A. , Fried, G. , and Wallin, G. (1989). Co-release of neuropeptide Y and noradrenaline from pig spleen in vivo: importance of subcellular storage, nerve impulse frequency and pattern, feedback regulation and resupply by axonal transport. Neuroscience 28, 475–486.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Mione, M. C. , Cavallotti, C. , Burnstock, G. , and Amenta, F. (1988). The peptidergic innervation of the ginea pig uterine artery in pregnancy. Basic Appl. Histochem. 32, 153–159.
PubMed |

Mione, M. C. , Cavanagh, J. F. R. , Lincoln, J. , Milner, P. , and Burnstock, G. (1990). Pregnancy reduces noradrenaline but not neuropeptide Y levels in the uterine artery of the guinea pig. Cell Tissue Res. 259, 503–509.
PubMed |

Mitchell, J. A. , and Goldman, H. (1996). Effects of alcohol on blastocyst implantation site blood flow in the rat. Alcohol Alcohol. 31, 81–87.
PubMed |

Morris, J. L. , Gibbins, I. J. , Furness, J. B. , Costa, M. , and Murphy, R. (1985). Co-localization of neuropeptide Y, vasoactive intestinal peptide and dynorphin in noradrenergic axons of the guinea pig uterine artery. Neurosci. Lett. 62, 31–37.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Morris, J. L. , Murphy, R. , and Autonom, J. (1988). Evidence that neuropeptide Y released from noradrenergic axons causes prolonged contraction of guinea pig uterine artery. J. Auton. Nerv. Syst. 24, 241–249.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Noda, N. , Minoura, H. , Nishiura, R. , Toyoda, N. , Yoshida, K. , Sakakura, T. , and Yoshida, T. (2000). Expression of tenascin-C in stromal cells of the murine uterus during early pregnancy induction by interleukin-1 alpha, prostaglandin E2, and prostaglandin F2 alpha. Biol. Reprod. 63, 1713–1720.
PubMed |

Norstrom, A. , Bryman, I. , and Dahlstrom, A. (1992). Neuropeptide Y, its localization in the human cervix and possible effect on the contractile activity of cervix smooth muscle. Gynecol. Obstet. Invest. 34, 175–179.
PubMed |

Papka, R. E. , Cotton, J. P. , and Trauring, H. H. (1985). Comparative distribution of neuropeptide tyrosine-, vasoactive intestinal peptide-, substance P-immunoreactive, acetylcholinesterase-positive and noradrenergic nerves in the reproductive tract of the female rat. Cell Tissue Res. 242, 475–490.
PubMed |

Petraglia, F. , Calza, L. , Giardino, L. , Sutton, S. , Marrama, P. , Rivier, J. , Genazzani, A. R. , and Vale, W. (1989a). Identification of immunoreactive neuropeptide-gamma in human placenta: localization, secretion, and binding sites. Endocrinology 124, 2016–2022.
PubMed |

Petraglia, F. , Coukos, G. , Battaglia, C. , Bartolotti, A. , Volpe, A. , Nappi, C. , Segre, A. , and Genazzani, A. R. (1989b). Plasma and amniotic fluid immunoreactive neuropeptide Y level changes during pregnancy, labor, and at parturition. J. Clin. Endocrinol. Metab. 69, 324–328.
PubMed |

Petraglia, F. , Calza, L. , Giardino, L. , Zanni, M. , Florio, P. , Ferrari, A. R. , Nappi, C. , and Genazzani, A. R. (1993). Maternal decidua and fetal membranes contain immunoreactive neuropeptide Y. J. Endocrinol. Invest. 16, 201–205.
PubMed |

Robidoux, J. , Simoneau, L. , St.Pierre, S. , Ech-Chadli, H. , and Lafond, J. (1998). Human syncytiotrophoblast NPY receptors are located on BBM and activate PLC-to-PKC axis. Am. J. Physiol. 274, 502–509.


Shemesh, M. (2001). Actions of gonadotrophins on the uterus. Reproduction 121, 835–842.
PubMed |

Stjernquist, M. , and Owman, C. (1987). Interaction of noradrenaline, NPY and VIP with the neurogenic cholinergic response of the rat uterine cervix in vitro. Acta Physiol. Scand. 131, 553–562.
PubMed |

Tan, J. , Paria, B. C. , Dey, S. K. , and Das, S. K. (1999). Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 140, 5310–5321.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tenmoku, S. , Ottesen, B. , and Ohare, M. M. (1988). Interaction of NPY and VIP in reguration of myometrial blood flow and mechanical activity. Peptides 9, 269–275.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tenmoku, S. , Ottesen, B. , Mairead, M. , and Ohare, T. (1994). Neuropeptide-Y gene expression in the goldfish brain: distribution and regulation by ovarian steroids. Endocrinology 134, 1095–1103.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wharton, J. , Gordon, L. , Byrne, J. , Herzog, H. , Selbie, L. A. , Moore, K. , Sullivan, M. H. , Elder, M. G. , Moscoso, G. , and Taylor, K. M. (1993). Expression of the human neuropeptide tyrosine Y1 receptor. Proc. Natl Acad. Sci. USA 90, 687–691.
PubMed |