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Published in: Archives of Gynecology and Obstetrics 4/2014

01-10-2014 | Gynecologic Endocrinology and Reproductive Medicine

Interferon stimulated gene 15 expression at the human embryo−maternal interface

Authors: Andrea Schanz, Dunja M. Baston-Büst, Christian Heiss, Ines M. Beyer, Jan S. Krüssel, Alexandra P. Hess

Published in: Archives of Gynecology and Obstetrics | Issue 4/2014

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Abstract

Purpose

In early pregnancy the dialogue between maternal endometrium and embryo is a key process in establishing a receptive decidua and placental network. Decidual ISG15 induction is thought to promote pregnancy maintenance and development. ISG15 is involved in RNA splicing, cytoskeletal organization, stress response and further intracellular processes.

Methods

ISG15 expression was examined immunohistologically in paraffin-embedded human placental and decidual tissue samples of all pregnancy trimesters on adjacent sections (first trimester n = 5, second n = 5, third n = 3). Samples were processed using a protocol applying a rabbit polyclonal ISG15 antibody. A mouse monoclonal cytokeratin seven antibody was utilized to identify the different placental departments and decidual glands. Staining results and anatomical features were evaluated blindly with strict rating criteria.

Results

ISG15 expression was identified in first and second trimester tissue samples. ISG15 localized especially to the extravillous cytotrophoblasts in the maternal wall and in maternal blood vessel. Expression was detected in cytotrophoblast progenitor cells in the placental villi and the cell column with a maximum in the first trimester. The syncytial layer stained positive in first and second trimester samples. Third trimester samples showed no expression of ISG15 at all.

Conclusions

ISG15 abundance in the human placenta is an interesting finding, with implications for placental development, fetal growth and potential defense mechanism against infections. The maximal expression of ISG15 in the first and second trimester of pregnancy suggests that ISG function is needed when placental and embryo development is enormous and embryo susceptibility to external influences is high.
Literature
1.
go back to reference Hess AP, Hamilton AE, Talbi S, Dosiou C, Nyegaard M, Nayak N, Genbecev-Krtolica O, Mavrogianis P, Ferrer K, Kruessel J, Fazleabas AT, Fisher SJ, Giudice LC (2007) Decidual stromal cell response to paracrine signals from the trophoblast: amplification of immune and angiogenic modulators. Biol Reprod 76(1):102–117. doi:10.1095/biolreprod.106.054791 PubMedCrossRef Hess AP, Hamilton AE, Talbi S, Dosiou C, Nyegaard M, Nayak N, Genbecev-Krtolica O, Mavrogianis P, Ferrer K, Kruessel J, Fazleabas AT, Fisher SJ, Giudice LC (2007) Decidual stromal cell response to paracrine signals from the trophoblast: amplification of immune and angiogenic modulators. Biol Reprod 76(1):102–117. doi:10.​1095/​biolreprod.​106.​054791 PubMedCrossRef
2.
go back to reference Ashley RL, Henkes LE, Bouma GJ, Pru JK, Hansen TR (2010) Deletion of the Isg15 gene results in up-regulation of decidual cell survival genes and down-regulation of adhesion genes: implication for regulation by IL-1beta. Endocrinology 151(9):4527–4536. doi:10.1210/en.2010-0166 PubMedCrossRef Ashley RL, Henkes LE, Bouma GJ, Pru JK, Hansen TR (2010) Deletion of the Isg15 gene results in up-regulation of decidual cell survival genes and down-regulation of adhesion genes: implication for regulation by IL-1beta. Endocrinology 151(9):4527–4536. doi:10.​1210/​en.​2010-0166 PubMedCrossRef
3.
go back to reference Bebington C, Bell SC, Doherty FJ, Fazleabas AT, Fleming SD (1999) Localization of ubiquitin and ubiquitin cross-reactive protein in human and baboon endometrium and decidua during the menstrual cycle and early pregnancy. Biol Reprod 60(4):920–928PubMedCrossRef Bebington C, Bell SC, Doherty FJ, Fazleabas AT, Fleming SD (1999) Localization of ubiquitin and ubiquitin cross-reactive protein in human and baboon endometrium and decidua during the menstrual cycle and early pregnancy. Biol Reprod 60(4):920–928PubMedCrossRef
4.
go back to reference Bebington C, Doherty FJ, Fleming SD (1999) Ubiquitin cross-reactive protein gene expression is increased in decidualized endometrial stromal cells at the initiation of pregnancy. Mol Hum Reprod 5(10):966–972PubMedCrossRef Bebington C, Doherty FJ, Fleming SD (1999) Ubiquitin cross-reactive protein gene expression is increased in decidualized endometrial stromal cells at the initiation of pregnancy. Mol Hum Reprod 5(10):966–972PubMedCrossRef
5.
go back to reference Giannakopoulos NV, Luo JK, Papov V, Zou W, Lenschow DJ, Jacobs BS, Borden EC, Li J, Virgin HW, Zhang DE (2005) Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem Biophys Res Commun 336(2):496–506. doi:10.1016/j.bbrc.2005.08.132 PubMedCrossRef Giannakopoulos NV, Luo JK, Papov V, Zou W, Lenschow DJ, Jacobs BS, Borden EC, Li J, Virgin HW, Zhang DE (2005) Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem Biophys Res Commun 336(2):496–506. doi:10.​1016/​j.​bbrc.​2005.​08.​132 PubMedCrossRef
6.
go back to reference Malakhov MP, Kim KI, Malakhova OA, Jacobs BS, Borden EC, Zhang DE (2003) High-throughput immunoblotting. Ubiquitiin-like protein ISG15 modifies key regulators of signal transduction. J Biol Chem 278(19):16608–16613. doi:10.1074/jbc.M208435200 PubMedCrossRef Malakhov MP, Kim KI, Malakhova OA, Jacobs BS, Borden EC, Zhang DE (2003) High-throughput immunoblotting. Ubiquitiin-like protein ISG15 modifies key regulators of signal transduction. J Biol Chem 278(19):16608–16613. doi:10.​1074/​jbc.​M208435200 PubMedCrossRef
7.
go back to reference Rivieccio MA, John GR, Song X, Suh HS, Zhao Y, Lee SC, Brosnan CF (2005) The cytokine IL-1beta activates IFN response factor 3 in human fetal astrocytes in culture. J Immunol 174(6):3719–3726PubMedCrossRef Rivieccio MA, John GR, Song X, Suh HS, Zhao Y, Lee SC, Brosnan CF (2005) The cytokine IL-1beta activates IFN response factor 3 in human fetal astrocytes in culture. J Immunol 174(6):3719–3726PubMedCrossRef
9.
go back to reference D’Cunha J, Ramanujam S, Wagner RJ, Witt PL, Knight E Jr, Borden EC (1996) In vitro and in vivo secretion of human ISG15, an IFN-induced immunomodulatory cytokine. J Immunol 157(9):4100–4108PubMed D’Cunha J, Ramanujam S, Wagner RJ, Witt PL, Knight E Jr, Borden EC (1996) In vitro and in vivo secretion of human ISG15, an IFN-induced immunomodulatory cytokine. J Immunol 157(9):4100–4108PubMed
10.
go back to reference Desai SD, Reed RE, Burks J, Wood LM, Pullikuth AK, Haas AL, Liu LF, Breslin JW, Meiners S, Sankar S (2012) ISG15 disrupts cytoskeletal architecture and promotes motility in human breast cancer cells. Exp Biol Med 237(1):38–49. doi:10.1258/ebm.2011.011236 CrossRef Desai SD, Reed RE, Burks J, Wood LM, Pullikuth AK, Haas AL, Liu LF, Breslin JW, Meiners S, Sankar S (2012) ISG15 disrupts cytoskeletal architecture and promotes motility in human breast cancer cells. Exp Biol Med 237(1):38–49. doi:10.​1258/​ebm.​2011.​011236 CrossRef
11.
go back to reference Red-Horse K, Kapidzic M, Zhou Y, Feng KT, Singh H, Fisher SJ (2005) EPHB4 regulates chemokine-evoked trophoblast responses: a mechanism for incorporating the human placenta into the maternal circulation. Development 132(18):4097–4106. doi:10.1242/dev.01971 PubMedCrossRef Red-Horse K, Kapidzic M, Zhou Y, Feng KT, Singh H, Fisher SJ (2005) EPHB4 regulates chemokine-evoked trophoblast responses: a mechanism for incorporating the human placenta into the maternal circulation. Development 132(18):4097–4106. doi:10.​1242/​dev.​01971 PubMedCrossRef
13.
go back to reference Damsky CH, Fitzgerald ML, Fisher SJ (1992) Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 89(1):210–222. doi:10.1172/JCI115565 Damsky CH, Fitzgerald ML, Fisher SJ (1992) Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 89(1):210–222. doi:10.​1172/​JCI115565
14.
go back to reference Honig A, Rieger L, Kapp M, Dietl J, Kammerer U (2005) Immunohistochemistry in human placental tissue—pitfalls of antigen detection. J Histochem Cytochem Off J Histochem Soc 53(11):1413–1420. doi:10.1369/jhc.5A6664.2005 CrossRef Honig A, Rieger L, Kapp M, Dietl J, Kammerer U (2005) Immunohistochemistry in human placental tissue—pitfalls of antigen detection. J Histochem Cytochem Off J Histochem Soc 53(11):1413–1420. doi:10.​1369/​jhc.​5A6664.​2005 CrossRef
15.
go back to reference Bebington C, Doherty FJ, Fleming SD (2000) Ubiquitin and ubiquitin-protein conjugates are present in human cytotrophoblast throughout gestation. Early Pregnancy 4(4):240–252PubMed Bebington C, Doherty FJ, Fleming SD (2000) Ubiquitin and ubiquitin-protein conjugates are present in human cytotrophoblast throughout gestation. Early Pregnancy 4(4):240–252PubMed
19.
go back to reference Farrell PJ, Broeze RJ, Lengyel P (1979) Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature 279(5713):523–525PubMedCrossRef Farrell PJ, Broeze RJ, Lengyel P (1979) Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature 279(5713):523–525PubMedCrossRef
20.
go back to reference Durfee W, Iaizzo P, Burgstahler B, Ponkshe S (2010) Non-invasive muscle force assessment apparatus for use in the intensive care unit. Conf Proc Annu Int Conf IEEE Eng Med Biol Soc IEEE Eng Med Biol Soc Conf 2010:5835–5838. doi:10.1109/IEMBS.2010.5627502 Durfee W, Iaizzo P, Burgstahler B, Ponkshe S (2010) Non-invasive muscle force assessment apparatus for use in the intensive care unit. Conf Proc Annu Int Conf IEEE Eng Med Biol Soc IEEE Eng Med Biol Soc Conf 2010:5835–5838. doi:10.​1109/​IEMBS.​2010.​5627502
21.
go back to reference Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D, Salem S, Radovanovic I, Grant AV, Adimi P, Mansouri N, Okada S, Bryant VL, Kong X-F, Kreins A, Velez MM, Boisson B, Khalilzadeh S, Ozcelik U, Darazam IA, Schoggins JW, Rice CM, Al-Muhsen S, Behr M, Vogt G, Puel A, Bustamante J, Gros P, Huibregtse JM, Abel L, Boisson-Dupuis S, Casanova J-L (2012) Mycobacterial disease and impaired IFN-γ immunity in humans with inherited ISG15 deficiency. Science 337(6102):1684–1688. doi:10.1126/science.1224026 PubMedCentralPubMedCrossRef Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D, Salem S, Radovanovic I, Grant AV, Adimi P, Mansouri N, Okada S, Bryant VL, Kong X-F, Kreins A, Velez MM, Boisson B, Khalilzadeh S, Ozcelik U, Darazam IA, Schoggins JW, Rice CM, Al-Muhsen S, Behr M, Vogt G, Puel A, Bustamante J, Gros P, Huibregtse JM, Abel L, Boisson-Dupuis S, Casanova J-L (2012) Mycobacterial disease and impaired IFN-γ immunity in humans with inherited ISG15 deficiency. Science 337(6102):1684–1688. doi:10.​1126/​science.​1224026 PubMedCentralPubMedCrossRef
22.
go back to reference Tripathy SN (2002) Infertility and pregnancy outcome in female genital tuberculosis. Int J Gynaecol Obstet Off Organ Int Fed Gynaecol Obstet 76(2):159–163CrossRef Tripathy SN (2002) Infertility and pregnancy outcome in female genital tuberculosis. Int J Gynaecol Obstet Off Organ Int Fed Gynaecol Obstet 76(2):159–163CrossRef
Metadata
Title
Interferon stimulated gene 15 expression at the human embryo−maternal interface
Authors
Andrea Schanz
Dunja M. Baston-Büst
Christian Heiss
Ines M. Beyer
Jan S. Krüssel
Alexandra P. Hess
Publication date
01-10-2014
Publisher
Springer Berlin Heidelberg
Published in
Archives of Gynecology and Obstetrics / Issue 4/2014
Print ISSN: 0932-0067
Electronic ISSN: 1432-0711
DOI
https://doi.org/10.1007/s00404-014-3290-9

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