Regulation of Blastocyst Migration, Apposition, and Initial Adhesion by a Chemokine, Interferon γ-inducible Protein 10 kDa (IP-10), during Early Gestation

Nagaoka, Kentaro; Nojima, Hisashi; Watanabe, Fumiko; Chang, Kyu‐Tae; Christenson, R. K.; Sakai, Senkiti; Imakawa, Kazuhiko

doi:10.1074/jbc.m300470200

Cited by 86 publications

(69 citation statements)

References 45 publications

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“…Multiple factors such as insulin-like growth factor II, insulin-like growth factor-binding protein-1, endothelin-1, and heparin-binding epidermal growth factor have been shown to promote migration of trophoblast cells into the endometrium (47). In an ovine study, CXCL10 expressed in the endometrium was suggested to stimulate the migration and attachment of trophoblast cells (19). The present study demonstrated that CXCR3 ligands, CXCL9, CXCL10, and CXCL11, which derived from EEC stimulated by IFN-␥, increased migration of trophoblast cells as well as T cells.…”

Section: Discussionmentioning

confidence: 54%

“…In cultured endometrial stromal cells, IFN-␥, IL-1␤, TNF-␣, and LPS stimulated CXCL10 production (16) and progesterone induced secretions of CXCL9 and CXCL10 (17). Notably, a recent study showed that CXCL10 stimulates the migration and attachment of ovine trophoblast cells (19). In contrast, CXCL11 in the endometrium has been poorly studied despite its highest binding affinity to CXCR3 among the three chemokines (12).…”

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confidence: 98%

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The Expression and Possible Roles of Chemokine CXCL11 and Its Receptor CXCR3 in the Human Endometrium

Hirota

Osuga

Koga

et al. 2006

The Journal of Immunology

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IFN-γ secreted by a human embryo and trophoblast cells during implantation is suggested to play an important role in implantation and pregnancy. In the present study, we explored expression and possible functions of CXCL11, a CXC chemokine strongly induced by IFN-γ, and its receptor CXCR3 in the human endometrium. Secreted CXCL11 protein was not detected in cultured endometrial stromal cells (ESC) but was detected in cultured endometrial epithelial cells (EEC). IFN-γ stimulated the protein levels of CXCL11 in a dose-dependent manner in EEC and ESC. CXCL11 secreted from EEC with 100 ng/ml IFN-γ was 220-fold of the control, and 100-fold as compared with that secreted from ESC with the same dose of IFN-γ. CXCR3 was expressed in EEC, ESC, and trophoblast cells. Addition of IFN-γ to EEC increased the chemotactic activity of its culture medium to trophoblast cells and T cells, and the effect was suppressed by immunoneutralization with Abs of three CXCR3 ligands, including anti-CXCL11 Ab. CXCL11 significantly increased BrdU incorporation of ESC, which was inhibited by a p42/44 MAPK pathway inhibitor PD98059. In contrast, CXCL11 significantly decreased BrdU incorporation and increased the release of lactate dehydrogenase and the positive staining of annexin V in EEC. These findings suggest that IFN-γ promotes implantation by stimulating EEC to produce CXCL11, which induces migration of trophoblast cells and T cells, proliferation of ESC, and apoptosis of EEC.

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Section: Discussionmentioning

confidence: 54%

mentioning

confidence: 98%

The Expression and Possible Roles of Chemokine CXCL11 and Its Receptor CXCR3 in the Human Endometrium

Hirota

Osuga

Koga

et al. 2006

The Journal of Immunology

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“…A classical ISG with reported biological effects on trophectoderm growth and adhesion in ruminants is CXCL10 (chemokine (C-X-C motif) ligand 10; alias IP-10; Nagaoka et al 2003aNagaoka et al , 2003b. CXCL10 is a member of the C-X-C chemokine family that regulates multiple aspects of inflammatory and immune responses primarily through chemotactic activity toward subsets of leukocytes.…”

Section: Cxcl10mentioning

confidence: 99%

Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches

Spencer¹,

Sandra²,

Wolf³

2008

Reproduction

270

253

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This review summarizes new knowledge on expression of genes and provides insights into approaches for study of conceptus-endometrial interactions in ruminants with emphasis on the peri-implantation stage of pregnancy. Conceptus-endometrial interactions in ruminants are complex and involve carefully orchestrated temporal and spatial alterations in gene expression regulated by hormones from the ovary and conceptus. Progesterone is the hormone of pregnancy and acts on the uterus to stimulate blastocyst survival, growth, and development. Inadequate progesterone levels or a delayed rise in progesterone is associated with pregnancy loss. The mononuclear trophectoderm cells of the elongating blastocyst synthesize and secrete interferon-t (IFNT), the pregnancy recognition signal. Trophoblast giant binucleate cells begin to differentiate and produce hormones including chorionic somatomammotropin 1 (CSH1 or placental lactogen). A number of genes, induced or stimulated by progesterone, IFNT, and/or CSH1 in a cell-specific manner, are implicated in trophectoderm adhesion to the endometrial luminal epithelium and regulation of conceptus growth and differentiation. Transcriptional profiling experiments are beginning to unravel the complex dynamics of conceptus-endometrial interactions in cattle and sheep. Future experiments should incorporate physiological models of pregnancy loss and be complemented by metabolomic studies of uterine lumen contents to more completely define factors required for blastocyst survival, growth, and implantation. Both reduction and holistic approaches will be important to understand the multifactorial phenomenon of recurrent pregnancy loss and provide a basis for new strategies to improve pregnancy outcome and reproductive efficiency in cattle and other domestic animals.

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“…Furthermore, decidual epithelial cells promote villous cytotrophoblast survival and EVT migration via production of CXCL8, CXCL10 and CXCL11 that bind to CXCR1 and CXCR3 on trophoblast cells. [96][97][98] CCL5 secreted by decidual tissue is a chemoattractant for human invading trophoblasts and blastocysts. However, some chemokines, such as CXCL14 and CXCL6, inhibit trophoblast invasive growth through downregulation of MMP-2 and MMP-9 activity.…”

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confidence: 99%

The integrative roles of chemokines at the maternal–fetal interface in early pregnancy

2014

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Embryos express paternal antigens that are foreign to the mother, but the mother provides a special immune milieu at the fetal-maternal interface to permit rather than reject the embryo growth in the uterus until parturition by establishing precise crosstalk between the mother and the fetus. There are unanswered questions in the maintenance of pregnancy, including the poorly understood phenomenon of maternal tolerance to the allogeneic conceptus, and the remarkable biological roles of placental trophoblasts that invade the uterine wall. Chemokines are multifunctional molecules initially described as having a role in leukocyte trafficking and later found to participate in developmental processes such as differentiation and directed migration. It is increasingly evident that the gestational uterine microenvironment is characterized, at least in part, by the differential expression and secretion of chemokines that induce selective trafficking of leukocyte subsets to the maternal-fetal interface and regulate multiple events that are closely associated with normal pregnancy. Here, we review the expression and function of chemokines and their receptors at the maternal-fetal interface, with a special focus on chemokine as a key component in trophoblast invasiveness and placental angiogenesis, recruitment and instruction of immune cells so as to form a fetus-supporting milieu during pregnancy. The chemokine network is also involved in pregnancy complications.

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Regulation of Blastocyst Migration, Apposition, and Initial Adhesion by a Chemokine, Interferon γ-inducible Protein 10 kDa (IP-10), during Early Gestation

Cited by 86 publications

References 45 publications

The Expression and Possible Roles of Chemokine CXCL11 and Its Receptor CXCR3 in the Human Endometrium

The Expression and Possible Roles of Chemokine CXCL11 and Its Receptor CXCR3 in the Human Endometrium

Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches

The integrative roles of chemokines at the maternal–fetal interface in early pregnancy

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