Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor

Jemma Evans, Rob D. Catalano, Pamela Brown, Rob Sherwin, Hilary O.D. Critchley, Asgerally T. Fazleabas, Henry N. Jabbour

Research output: Contribution to journalArticleResearchpeer-review

79 Citations (Scopus)

Abstract

Implantation requires communication between a receptive endometrium and a healthy blastocyst. This maternal-embryonic crosstalk involves local mediators within the uterine microenvironment. We demonstrate that a secreted protein, prokineticin 1 (PROK1), is expressed in the receptive endometrium and during early pregnancy. PROK1 induces expression of leukemia inhibitory factor (LIF) in endometrial epithelial cells and first trimester decidua via a Gq-Ca 2+-cSrc-mitogen-activated protein kinase kinase-mediated pathway. We show that human embryonic chorionic gonadotropin (hCG) induces sequential mRNA expression of PROK1 and LIF in an in vivo baboon model, in human endometrial epithelial cells, and in first-trimester decidua. We have used micro RNA constructs targeted to PROK1 to demonstrate that hCG-mediated LIF expression in the endometrium is dependent on prior induction of PROK1. Dual immunohistochemical analysis colocalized expression of the luteinizing hormone/chorionic gonadotropin receptor, PROK1, PROKR1, and LIF to the glandular epithelial cells of the first trimester decidual tissue. PROK1 enhances adhesion of trophoblast cells to fibronectin and laminin matrices, which are mediated predominantly via LIF induction. These data describe a novel signaling pathway mediating maternal-embryonic crosstalk, in which embryonic hCG via endometrial PROK1 may play a pivotal role in enhancing receptivity and maintaining early pregnancy.

Original languageEnglish
Pages (from-to)2165-2175
Number of pages11
JournalFASEB Journal
Volume23
Issue number7
DOIs
Publication statusPublished - 1 Jul 2009

Keywords

  • Adhesion
  • Decidua
  • Fibronectin
  • Human chorionic gonadotropin
  • Implantation
  • Laminin

Cite this

Evans, J., Catalano, R. D., Brown, P., Sherwin, R., Critchley, H. O. D., Fazleabas, A. T., & Jabbour, H. N. (2009). Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. FASEB Journal, 23(7), 2165-2175. https://doi.org/10.1096/fj.08-124495
Evans, Jemma ; Catalano, Rob D. ; Brown, Pamela ; Sherwin, Rob ; Critchley, Hilary O.D. ; Fazleabas, Asgerally T. ; Jabbour, Henry N. / Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. In: FASEB Journal. 2009 ; Vol. 23, No. 7. pp. 2165-2175.
@article{e8b26e8032cb4e3b9845d02ff3456316,
title = "Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor",
abstract = "Implantation requires communication between a receptive endometrium and a healthy blastocyst. This maternal-embryonic crosstalk involves local mediators within the uterine microenvironment. We demonstrate that a secreted protein, prokineticin 1 (PROK1), is expressed in the receptive endometrium and during early pregnancy. PROK1 induces expression of leukemia inhibitory factor (LIF) in endometrial epithelial cells and first trimester decidua via a Gq-Ca 2+-cSrc-mitogen-activated protein kinase kinase-mediated pathway. We show that human embryonic chorionic gonadotropin (hCG) induces sequential mRNA expression of PROK1 and LIF in an in vivo baboon model, in human endometrial epithelial cells, and in first-trimester decidua. We have used micro RNA constructs targeted to PROK1 to demonstrate that hCG-mediated LIF expression in the endometrium is dependent on prior induction of PROK1. Dual immunohistochemical analysis colocalized expression of the luteinizing hormone/chorionic gonadotropin receptor, PROK1, PROKR1, and LIF to the glandular epithelial cells of the first trimester decidual tissue. PROK1 enhances adhesion of trophoblast cells to fibronectin and laminin matrices, which are mediated predominantly via LIF induction. These data describe a novel signaling pathway mediating maternal-embryonic crosstalk, in which embryonic hCG via endometrial PROK1 may play a pivotal role in enhancing receptivity and maintaining early pregnancy.",
keywords = "Adhesion, Decidua, Fibronectin, Human chorionic gonadotropin, Implantation, Laminin",
author = "Jemma Evans and Catalano, {Rob D.} and Pamela Brown and Rob Sherwin and Critchley, {Hilary O.D.} and Fazleabas, {Asgerally T.} and Jabbour, {Henry N.}",
year = "2009",
month = "7",
day = "1",
doi = "10.1096/fj.08-124495",
language = "English",
volume = "23",
pages = "2165--2175",
journal = "FASEB Journal",
issn = "0892-6638",
publisher = "Federation of American Societies for Experimental Biology",
number = "7",

}

Evans, J, Catalano, RD, Brown, P, Sherwin, R, Critchley, HOD, Fazleabas, AT & Jabbour, HN 2009, 'Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor', FASEB Journal, vol. 23, no. 7, pp. 2165-2175. https://doi.org/10.1096/fj.08-124495

Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. / Evans, Jemma; Catalano, Rob D.; Brown, Pamela; Sherwin, Rob; Critchley, Hilary O.D.; Fazleabas, Asgerally T.; Jabbour, Henry N.

In: FASEB Journal, Vol. 23, No. 7, 01.07.2009, p. 2165-2175.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor

AU - Evans, Jemma

AU - Catalano, Rob D.

AU - Brown, Pamela

AU - Sherwin, Rob

AU - Critchley, Hilary O.D.

AU - Fazleabas, Asgerally T.

AU - Jabbour, Henry N.

PY - 2009/7/1

Y1 - 2009/7/1

N2 - Implantation requires communication between a receptive endometrium and a healthy blastocyst. This maternal-embryonic crosstalk involves local mediators within the uterine microenvironment. We demonstrate that a secreted protein, prokineticin 1 (PROK1), is expressed in the receptive endometrium and during early pregnancy. PROK1 induces expression of leukemia inhibitory factor (LIF) in endometrial epithelial cells and first trimester decidua via a Gq-Ca 2+-cSrc-mitogen-activated protein kinase kinase-mediated pathway. We show that human embryonic chorionic gonadotropin (hCG) induces sequential mRNA expression of PROK1 and LIF in an in vivo baboon model, in human endometrial epithelial cells, and in first-trimester decidua. We have used micro RNA constructs targeted to PROK1 to demonstrate that hCG-mediated LIF expression in the endometrium is dependent on prior induction of PROK1. Dual immunohistochemical analysis colocalized expression of the luteinizing hormone/chorionic gonadotropin receptor, PROK1, PROKR1, and LIF to the glandular epithelial cells of the first trimester decidual tissue. PROK1 enhances adhesion of trophoblast cells to fibronectin and laminin matrices, which are mediated predominantly via LIF induction. These data describe a novel signaling pathway mediating maternal-embryonic crosstalk, in which embryonic hCG via endometrial PROK1 may play a pivotal role in enhancing receptivity and maintaining early pregnancy.

AB - Implantation requires communication between a receptive endometrium and a healthy blastocyst. This maternal-embryonic crosstalk involves local mediators within the uterine microenvironment. We demonstrate that a secreted protein, prokineticin 1 (PROK1), is expressed in the receptive endometrium and during early pregnancy. PROK1 induces expression of leukemia inhibitory factor (LIF) in endometrial epithelial cells and first trimester decidua via a Gq-Ca 2+-cSrc-mitogen-activated protein kinase kinase-mediated pathway. We show that human embryonic chorionic gonadotropin (hCG) induces sequential mRNA expression of PROK1 and LIF in an in vivo baboon model, in human endometrial epithelial cells, and in first-trimester decidua. We have used micro RNA constructs targeted to PROK1 to demonstrate that hCG-mediated LIF expression in the endometrium is dependent on prior induction of PROK1. Dual immunohistochemical analysis colocalized expression of the luteinizing hormone/chorionic gonadotropin receptor, PROK1, PROKR1, and LIF to the glandular epithelial cells of the first trimester decidual tissue. PROK1 enhances adhesion of trophoblast cells to fibronectin and laminin matrices, which are mediated predominantly via LIF induction. These data describe a novel signaling pathway mediating maternal-embryonic crosstalk, in which embryonic hCG via endometrial PROK1 may play a pivotal role in enhancing receptivity and maintaining early pregnancy.

KW - Adhesion

KW - Decidua

KW - Fibronectin

KW - Human chorionic gonadotropin

KW - Implantation

KW - Laminin

UR - http://www.scopus.com/inward/record.url?scp=68549096321&partnerID=8YFLogxK

U2 - 10.1096/fj.08-124495

DO - 10.1096/fj.08-124495

M3 - Article

VL - 23

SP - 2165

EP - 2175

JO - FASEB Journal

JF - FASEB Journal

SN - 0892-6638

IS - 7

ER -

Evans J, Catalano RD, Brown P, Sherwin R, Critchley HOD, Fazleabas AT et al. Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. FASEB Journal. 2009 Jul 1;23(7):2165-2175. https://doi.org/10.1096/fj.08-124495