Quantitative proteomics suggest a potential link between early embryonic death and trisomy 16
Ting Yao A B * , Haiyan Hou C D * , Guozhong Liu E , Jun Wu F , Zhe Qin B D , Yang Sun D , Xiaohan Jin D G , Jun Chen D , Yaqiong Chen D H and Zhongwei Xu D G HA Department of Obstetrics and Gynaecology, Tianjin Nankai Hospital, No. 6 Changjiang Road, Nankai District, Tianjin 300100, China.
B Central Laboratory, Logistics University of Chinese People’s Armed Police Force, Tianjin 300309, China.
C Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100730, China.
D Department of Obstetrics and Gynaecology, Affiliated Hospital of the Chinese People’s Armed Police Force Logistics College, Tianjin 300162, China.
E Department of Obstetrics and Gynaecology, CongraMarie Women and Children’s Hospital, Tianjin 300100, China.
F Program in Public Health, Anteater Instruction & Research Bldg (AIRB) # 2034, University of California, Irvine CA 92697-3957, USA.
G Tianjin Key Laboratory of Cardiovascular Remodelling and Target Organ Injury, Pingjin Hospital Heart Centre, Tianjin 300162, China.
H Corresponding authors. Emails: xlw113@hotmail.com; chenyq82@hotmail.com
Reproduction, Fertility and Development 31(6) 1116-1126 https://doi.org/10.1071/RD17319
Submitted: 1 June 2017 Accepted: 26 January 2019 Published: 29 March 2019
Abstract
Activation of extracellular signal-regulated kinase (ERK) signalling, alteration of the uterine microenvironment and a reduction in human chorionic gonadotrophin production have been linked with fetal trisomy 16-induced early embryonic death (EED). However, the detailed biological mechanism of EED remains unclear. Using quantitative proteomics we successfully screened differentially expressed proteins in the villous tissues from patients with EED and fetal trisomy 16 (EEDT16), patients with EED but normal fetal chromosomes (EEDNC) and patients undergoing elective abortion with normal fetal chromosomes (EANC) as the reference group. Compared with the reference group, we identified 337 and 220 differentially expressed proteins in EEDT16 patients and EEDNC patients respectively; these were involved in critical biological processes including immune response, superoxide metabolism, inflammatory responses and so on. We found that differential expression of immunological function-related molecules, such as human leukocyte antigen-g (HLA-G), HLA-C, Fc Fragment Of IgG Receptor III (FcγR III), also named CD16, interleukin 18 (IL-18) and transforming growth factor β1 (TGF-β1), might induce EED in both EEDT16 and EEDNC patients. More severe immunological dysfunction was observed in EEDT16 patients than that in EEDNC patients. Furthermore, differential expression of implantation and invasion-related molecules, such as cytochrome b-245 light chain (CYBA), neutrophil cytosol factor 2 (NCF2), Mitogen-activated protein kinase kinase kinase 4 (MAP3K4), matrix metalloproteinase 2 (MMP2), MMP9 and tumour necrosis factor α (TNF-α) might induce EED in both EEDT16 and EEDNC patients, although more severe dysfunction in the implantation and invasion ability of villous tissues was observed in EEDT16 patients.
Additional keywords: apoptosis, immunological dysfunction, implantation, invasion, NADPH oxidase.
References
Ain, R., Trinh, M. L., and Soares, M. J. (2004). Interleukin-11 signaling is required for the differentiation of natural killer cells at the maternal–fetal interface. Dev. Dyn. 231, 700–708.| Interleukin-11 signaling is required for the differentiation of natural killer cells at the maternal–fetal interface.Crossref | GoogleScholarGoogle Scholar | 15499555PubMed |
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25–29.
| Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.Crossref | GoogleScholarGoogle Scholar | 10802651PubMed |
Bauer, S., Pollheimer, J., Hartmann, J., Husslein, P., Aplin, J. D., and Knofler, M. (2004). Tumor necrosis factor-alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. J. Clin. Endocrinol. Metab. 89, 812–822.
| Tumor necrosis factor-alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures.Crossref | GoogleScholarGoogle Scholar | 14764800PubMed |
Bedard, K., and Krause, K. H. (2007). The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245–313.
| The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology.Crossref | GoogleScholarGoogle Scholar | 17237347PubMed |
Canning, M. T., Postovit, L. M., Clarke, S. H., and Graham, C. H. (2001). Oxygen-mediated regulation of gelatinase and tissue inhibitor of metalloproteinases-1 expression by invasive cells. Exp. Cell Res. 267, 88–94.
| Oxygen-mediated regulation of gelatinase and tissue inhibitor of metalloproteinases-1 expression by invasive cells.Crossref | GoogleScholarGoogle Scholar | 11412041PubMed |
Carlino, C., Stabile, H., Morrone, S., Bulla, R., Soriani, A., Agostinis, C., Bossi, F., Mocci, C., Sarazani, F., Tedesco, F., Santoni, A., and Gismondi, A. (2008). Recruitment of circulating NK cells through decidual tissues: a possible mechanism controlling NK cell accumulation in the uterus during early pregnancy. Blood 111, 3108–3115.
| Recruitment of circulating NK cells through decidual tissues: a possible mechanism controlling NK cell accumulation in the uterus during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 18187664PubMed |
Chan-Hui, P. Y., and Weaver, R. (1998). Human mitogen-activated protein kinase kinase kinase mediates the stress induce activation of mitogen-activated protein kinase cascades. Biochem. J. 336, 599–609.
| Human mitogen-activated protein kinase kinase kinase mediates the stress induce activation of mitogen-activated protein kinase cascades.Crossref | GoogleScholarGoogle Scholar | 9841871PubMed |
Chen, H., Pang, Z. J., Chen, S. L., and Xing, F. Q. (2004). Effects of exogenous tumor necrosis factor alpha on the invasiveness of human tropholasts. Di Yi Jun Yi Da Xue Xue Bao. 24, 397–399, 407.
| 15090307PubMed |
Cheng, L. H., and Cao, Y. X. (2005). Study on the correlation of transforming growth factor beta1 and its receptors with spontaneous abortion after in vitro fertilization and embryo transfer. Zhonghua Fu Chan Ke Za Zhi 40, 299–301.
| 15938776PubMed |
Cheng, G., Cao, Z., Xu, X., van-Meir, E. G., and Lambeth, J. D. (2001). Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269, 131–140.
| Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5.Crossref | GoogleScholarGoogle Scholar | 11376945PubMed |
Ciancimino, L., Laganà, A. S., Chiofalo, B., Granese, R., Grasso, R., and Triolo, O. (2014). Would it be too late? A retrospective case-control analysis to evaluate maternal–fetal outcomes in advanced maternal age. Arch. Gynecol. Obstet. 290, 1109–1114.
| Would it be too late? A retrospective case-control analysis to evaluate maternal–fetal outcomes in advanced maternal age.Crossref | GoogleScholarGoogle Scholar | 25027820PubMed |
Co, E. C., Gormley, M., Kapidzic, M., Rosen, D. B., Scott, M. A., Stolp, H. A., McMaster, M., Lanier, L. L., Barcena, A., and Fisher, S. J. (2013). Maternal decidual macrophages inhibit NK cell killing of invasive cytotrophoblasts during human pregnancy. Biol. Reprod. 88, 155.
| Maternal decidual macrophages inhibit NK cell killing of invasive cytotrophoblasts during human pregnancy.Crossref | GoogleScholarGoogle Scholar | 23553431PubMed |
Cohen, M., Meisser, A., Haenggeli, L., and Bischof, P. (2006). Involvement of MAPK pathway in TNF-alpha-induced MMP-9 expression in human trophoblastic cells. Mol. Hum. Reprod. 12, 225–232.
| Involvement of MAPK pathway in TNF-alpha-induced MMP-9 expression in human trophoblastic cells.Crossref | GoogleScholarGoogle Scholar | 16520344PubMed |
Cooper, M. A., Fehniger, T. A., Turner, S. C., Chen, K. S., Ghaheri, B. A., Ghayur, T., Carson, W. E., and Caligiuri, M. A. (2001a). Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 97, 3146–3151.
| Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset.Crossref | GoogleScholarGoogle Scholar | 11342442PubMed |
Cooper, M. A., Fehniger, T. A., and Caligiuri, M. A. (2001b). The biology of human natural killer-cell subsets. Trends Immunol. 22, 633–640.
| The biology of human natural killer-cell subsets.Crossref | GoogleScholarGoogle Scholar | 11698225PubMed |
Cox, J., and Mann, M. (2008). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372.
| MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification.Crossref | GoogleScholarGoogle Scholar | 19029910PubMed |
Dhillon, R. K., Hillman, S. C., Morris, R. K., McMullan, D., Williams, D., Coomarasamy, A., and Kilby, M. D. (2014). Additional information from chromosomal microarray analysis (CMA) over conventional karyotyping when diagnosing chromosomal abnormalities in miscarriage: a systematic review and meta-analysis. BJOG 121, 11–21.
| Additional information from chromosomal microarray analysis (CMA) over conventional karyotyping when diagnosing chromosomal abnormalities in miscarriage: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 23859082PubMed |
Emmer, P. M., Steegers, E. A., Kerstens, H. M., Bulten, J., Nelen, W. L., Boer, K., and Joosten, I. (2002). Altered phenotype of HLA-G expressing trophoblast and decidual natural killer cells in pathological pregnancies. Hum. Reprod. 17, 1072–1080.
| Altered phenotype of HLA-G expressing trophoblast and decidual natural killer cells in pathological pregnancies.Crossref | GoogleScholarGoogle Scholar | 11925408PubMed |
Faridi, R. M., and Agrawal, S. (2011). Killer immunoglobulin-like receptors (KIRs) and HLA-C allorecognition patterns implicative of dominant activation of natural killer cells contribute to recurrent miscarriages. Hum. Reprod. 26, 491–497.
| Killer immunoglobulin-like receptors (KIRs) and HLA-C allorecognition patterns implicative of dominant activation of natural killer cells contribute to recurrent miscarriages.Crossref | GoogleScholarGoogle Scholar | 21159685PubMed |
Gabbai, D., Harlev, A., Friger, M., Steiner, N., Sergienko, R., Kreinin, A., and Bashiri, A. (2018). Pregnancy outcomes among patients with recurrent pregnancy loss and uterine anatomic abnormalities. J. Perinat. Med. 46, 728–734.
| Pregnancy outcomes among patients with recurrent pregnancy loss and uterine anatomic abnormalities.Crossref | GoogleScholarGoogle Scholar | 28742523PubMed |
Giakoumelou, S., Wheelhouse, N., Cuschieri, K., Entrican, G., Howie, S. E., and Horne, A. W. (2016). The role of infection in miscarriage. Hum. Reprod. Update 22, 116–133.
| The role of infection in miscarriage.Crossref | GoogleScholarGoogle Scholar | 26386469PubMed |
Gil-Villa, A. M., Cardona-Maya, W., Agarwal, A., Sharma, R., and Cadavid, A. (2010). Assessment of sperm factors possibly involved in early recurrent pregnancy loss. Fertil. Steril. 94, 1465–1472.
| Assessment of sperm factors possibly involved in early recurrent pregnancy loss.Crossref | GoogleScholarGoogle Scholar | 19540481PubMed |
Goddijn, M., and Leschot, N. J. (2000). Genetic aspects of miscarriage. Best Pract. Res. Clin. Obstet. Gynaecol. 14, 855–865.
| Genetic aspects of miscarriage.Crossref | GoogleScholarGoogle Scholar |
Gomes, S. Z., Lorenzon, A. R., Vieira, J. S., Rocha, C. R., Bandeira, C., Hoshida, M. S., Lopes, L. R., and Bevilacqua, E. (2012). Expression of NADPH oxidase by trophoblast cells: potential implications for the postimplanting mouse embryo. Biol. Reprod. 86, 56.
| Expression of NADPH oxidase by trophoblast cells: potential implications for the postimplanting mouse embryo.Crossref | GoogleScholarGoogle Scholar | 22075471PubMed |
Goodier, M. R., and Londei, M. (2000). Lipopolysaccharide stimulates the proliferation of human CD56+CD32-NK cells: a regulatory role of monocytes and IL-10. J. Immunol. 165, 139–147.
| Lipopolysaccharide stimulates the proliferation of human CD56+CD32-NK cells: a regulatory role of monocytes and IL-10.Crossref | GoogleScholarGoogle Scholar | 10861046PubMed |
Gücer, F., Balkanli-Kaplan, P., Yüksel, M., Yüce, M. A., Türe, M., and Yardim, T. (2001). Maternal serum tumor necrosis factor-alpha in patients with preterm labor. J. Reprod. Med. 46, 232–236.
| 11304864PubMed |
Ha, H., and Lee, H. B. (2005). Reactive oxygen species amplify glucose signalling in renal cells cultured under high glucose and in diabetic kidney. Nephrology (Carlton) 10, S7–S10.
| Reactive oxygen species amplify glucose signalling in renal cells cultured under high glucose and in diabetic kidney.Crossref | GoogleScholarGoogle Scholar | 16174288PubMed |
Halasz, M., Polgar, B., Berta, G., Czimbalek, L., and Szekeres-Bartho, J. (2013). Progesterone-induced blocking factor differentially regulates trophoblast and tumor invasion by altering matrix metalloproteinase activity. Cell. Mol. Life Sci. 70, 4617–4630.
| Progesterone-induced blocking factor differentially regulates trophoblast and tumor invasion by altering matrix metalloproteinase activity.Crossref | GoogleScholarGoogle Scholar | 23807209PubMed |
Hamza, A., Meyberg-Solomayer, G., Juhasz-Boss, I., Joukhadar, R., Takacs, Z., Solomayer, E. F., Baum, S., Radosa, J., Mavrova, L., and Herr, D. (2016). Diagnostic methods of ectopic pregnancy and early pregnancy loss: a review of the literature. Geburtshilfe Frauenheilkd. 76, 377–382.
| Diagnostic methods of ectopic pregnancy and early pregnancy loss: a review of the literature.Crossref | GoogleScholarGoogle Scholar | 27134292PubMed |
Huchon, C., Deffieux, X., Beucher, G., Capmas, P., Carcopino, X., Costedoat-Chalumeau, N., Delabaere, A., Gallot, V., Iraola, E., Lavoue, V., Legendre, G., Lejeune-Saada, V., Leveque, J., Nedellec, S., Nizard, J., Quibel, T., Subtil, D., Vialard, F., Lemery, D., Collège National des Gynécologues Obstétriciens Français (2016). Pregnancy loss: French clinical practice guidelines. Eur. J. Obstet. Gynecol. Reprod. Biol. 201, 18–26.
| Pregnancy loss: French clinical practice guidelines.Crossref | GoogleScholarGoogle Scholar | 27039249PubMed |
Irani, K. (2000). Oxidant signaling in vascular cell growth, death, survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptosis signaling. Circ. Res. 87, 179–183.
| Oxidant signaling in vascular cell growth, death, survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptosis signaling.Crossref | GoogleScholarGoogle Scholar | 10926866PubMed |
Ispasoiu, C. A., Chicea, R., Stamatian, F. V., and Ispasoiu, F. (2013). High fasting insulin levels and insulin resistance may be linked to idiopathic recurrent pregnancy loss: a case-control study. Int. J. Endocrinol. 2013, 576926.
| High fasting insulin levels and insulin resistance may be linked to idiopathic recurrent pregnancy loss: a case-control study.Crossref | GoogleScholarGoogle Scholar | 24371440PubMed |
Kacprzak, M., Chrzanowska, M., Skoczylas, B., Moczulska, H., Borowiec, M., and Sieroszewski, P. (2016). Genetic causes of recurrent miscarriages. Ginekol. Pol. 87, 722–726.
| Genetic causes of recurrent miscarriages.Crossref | GoogleScholarGoogle Scholar | 27958626PubMed |
Keskin, D. B., Allan, D. S., Rybalov, B., Andzelm, M. M., Sten, J. N., Kopcow, H. D., Koopman, L. A., and Strominger, J. L. (2007). TGF-β promotes conversion of CD16+ peripheral blood NK cells into CD16-NK cells with similarities to decidual NK cells. Proc. Natl. Acad. Sci. USA 104, 3378–3383.
| TGF-β promotes conversion of CD16+ peripheral blood NK cells into CD16-NK cells with similarities to decidual NK cells.Crossref | GoogleScholarGoogle Scholar | 17360654PubMed |
Khan, A. H. (2001). Trisomy 16, cause of first trimester abortion. J. Pak. Med. Assoc. 51, 378–379.
| 11768943PubMed |
Kwak-Kim, J., Bao, S., Lee, S. K., Kim, J. W., and Gilman-Sachs, A. (2014). Immunological modes of pregnancy loss: inflammation, immune effectors, and stress. Am. J. Reprod. Immunol. 72, 129–140.
| Immunological modes of pregnancy loss: inflammation, immune effectors, and stress.Crossref | GoogleScholarGoogle Scholar | 24661472PubMed |
Le Bouteiller, P. (2015). HLA-G in human early pregnancy: control of uterine immune cell activation and likely vascular remodeling. Biomed. J. 38, 32–38.
| HLA-G in human early pregnancy: control of uterine immune cell activation and likely vascular remodeling.Crossref | GoogleScholarGoogle Scholar | 25163504PubMed |
Lee, J. Y., Hong, J. S., Kim, E. N., Ahn, S., Choe, J., Hwang, D., Kim, K. C., Kim, S. H., and Kim, C. J. (2014). Placental C4d as a common feature of chromosomally normal and abnormal miscarriages. Virchows Arch. 464, 613–620.
| Placental C4d as a common feature of chromosomally normal and abnormal miscarriages.Crossref | GoogleScholarGoogle Scholar | 24671647PubMed |
Li, S., Wang, L., Xing, Z., Huang, Y., and Miao, Z. (2017). Expression level of TNF-α in decidual tissue and peripheral blood of patients with recurrent spontaneous abortion. Cent. Eur. J. Immunol. 42, 156–160.
| Expression level of TNF-α in decidual tissue and peripheral blood of patients with recurrent spontaneous abortion.Crossref | GoogleScholarGoogle Scholar | 28860933PubMed |
Liu, A. X., Jin, F., Zhang, W. W., Zhou, T. H., Zhou, C. Y., Yao, W. M., Qian, Y. L., and Huang, H. F. (2006). Proteomic analysis on the alteration of protein expression in the placental villous tissue of early pregnancy loss. Biol. Reprod. 75, 414–420.
| Proteomic analysis on the alteration of protein expression in the placental villous tissue of early pregnancy loss.Crossref | GoogleScholarGoogle Scholar | 16738225PubMed |
Martyn, K. D., Frederic, L. M., von-Loehneysen, K., Dinauer, M. C., and Knaus, U. G. (2006). Functional analysis of NOX4 reveals unique characteristics compared to other NADPH oxidases. Cell. Signal. 18, 69–82.
| Functional analysis of NOX4 reveals unique characteristics compared to other NADPH oxidases.Crossref | GoogleScholarGoogle Scholar | 15927447PubMed |
Meuleman, T., van-Beelen, E., Kaaja, R. J., van-Lith, J. M., Class, F. H., and Bloemenkamp, K. W. (2016). HLA-C antibodies in women with recurrent miscarriage suggests that antibody mediated rejection is one of the mechanisms leading to recurrent miscarriage. J. Reprod. Immunol. 116, 28–34.
| HLA-C antibodies in women with recurrent miscarriage suggests that antibody mediated rejection is one of the mechanisms leading to recurrent miscarriage.Crossref | GoogleScholarGoogle Scholar | 27172837PubMed |
Murphy, S. P., Fast, L. D., Hanna, N. N., and Sharma, S. (2005). Uterine NK cells mediate inflammation- induced fetal demise in IL-10-null mice. J. Immunol. 175, 4084–4090.
| Uterine NK cells mediate inflammation- induced fetal demise in IL-10-null mice.Crossref | GoogleScholarGoogle Scholar | 16148158PubMed |
Nakashima, A., Shima, T., Inada, K., Ito, M., and Saito, S. (2012). The balance of the immune system between T cells and NK cells in miscarriage. Am. J. Reprod. Immunol. 67, 304–310.
| The balance of the immune system between T cells and NK cells in miscarriage.Crossref | GoogleScholarGoogle Scholar | 22364212PubMed |
Ni, X., Li, X., Guo, Y., Zhou, T., Guo, X., Zhao, C., Lin, M., Zhou, Z., Shen, R., Guo, X., Ling, X., and Huo, R. (2014). Quantitative proteomics analysis of altered protein expression in the placental villous tissue of early pregnancy loss using isobaric tandem mass tags. BioMed Res. Int. 2014, 647143.
| Quantitative proteomics analysis of altered protein expression in the placental villous tissue of early pregnancy loss using isobaric tandem mass tags.Crossref | GoogleScholarGoogle Scholar | 25028661PubMed |
Nielsen, C. M., Wolf, A. S., Goodier, M. R., and Riley, E. M. (2016). Synergy between common γ chain family cytokines and IL-18 potentiates innate and adaptive pathways of NK cell activation. Front. Immunol. 7, 101.
| Synergy between common γ chain family cytokines and IL-18 potentiates innate and adaptive pathways of NK cell activation.Crossref | GoogleScholarGoogle Scholar | 27047490PubMed |
Nissi, R., Talvensaari-Mattila, A., Kotila, V., Niinimaki, M., Jarvela, I., and Turpeenniemi-Hujanen, T. (2013). Circulating matrix metalloproteinase MMP-9 and MMP-2/TIMP-2 complex are associated with spontaneous early pregnancy failure. Reprod. Biol. Endocrinol. 11, 2.
| Circulating matrix metalloproteinase MMP-9 and MMP-2/TIMP-2 complex are associated with spontaneous early pregnancy failure.Crossref | GoogleScholarGoogle Scholar | 23320481PubMed |
Nizard, J., Guettrot-lmbert, G., Plu-Bureau, G., Ciangura, C., Jacqueminet, S., Leenhardt, L., Nedellec, S., Gallot, V., Vialard, F., Quibel, T., Huchon, C., and Costedoat-Chalumeau, N. (2014). Chronic maternal disease and pregnancy losses. French guidelines. J. Gynecol. Obstet. Biol. Reprod. (Paris) 43, 865–882.
| Chronic maternal disease and pregnancy losses. French guidelines.Crossref | GoogleScholarGoogle Scholar |
Patel, R. N., Quack, K. C., Hill, J. A., and Schust, D. J. (2003). Expression of membrane-bound HLA-G at the maternal–fetal interface is not associated with pregnancy maintenance among patients with idiopathic recurrent pregnancy loss. Mol. Hum. Reprod. 9, 551–557.
| Expression of membrane-bound HLA-G at the maternal–fetal interface is not associated with pregnancy maintenance among patients with idiopathic recurrent pregnancy loss.Crossref | GoogleScholarGoogle Scholar | 12900514PubMed |
Pustovrh, C., Jawerbaum, A., Sinner, D., Pesaresi, M., Micone, P., Gimeno, M., and Gonzalez, E. T. (2000). Membrane-type matrix metalloproteinase-9 activity in placental tissue from patients with pre-existing and gestational diabetes mellitus. Reprod. Fertil. Dev. 12, 269–275.
| Membrane-type matrix metalloproteinase-9 activity in placental tissue from patients with pre-existing and gestational diabetes mellitus.Crossref | GoogleScholarGoogle Scholar | 11451017PubMed |
Pustovrh, C., Jawerbaum, A., Sinner, D., White, V., Capobianco, E., and Gonzalez, E. (2002). Metalloproteinase 2 activity and modulation in uterus from neonatal streptozotocin-induced diabetic rats during embryo implantation. Reprod. Fertil. Dev. 14, 479–485.
| Metalloproteinase 2 activity and modulation in uterus from neonatal streptozotocin-induced diabetic rats during embryo implantation.Crossref | GoogleScholarGoogle Scholar | 12617792PubMed |
Rahat, B., Sharma, R., Bagga, R., Hamid, A., and Kaur, J. (2016). Imbalance between matrix metalloproteinases and their tissue inhibitors in preeclampsia and gestational trophoblastic disease. Reproduction 152, 11–22.
| Imbalance between matrix metalloproteinases and their tissue inhibitors in preeclampsia and gestational trophoblastic disease.Crossref | GoogleScholarGoogle Scholar | 27256632PubMed |
Ruixue, W., Hongli, Z., Zhihong, Z., Rulin, D., Dongfeng, G., and Ruizhi, L. (2013). The impact of semen quality, occupational exposure to environmental factors and lifestyle on recurrent pregnancy loss. J. Assist. Reprod. Genet. 30, 1513–1518.
| The impact of semen quality, occupational exposure to environmental factors and lifestyle on recurrent pregnancy loss.Crossref | GoogleScholarGoogle Scholar | 24046023PubMed |
Sharkey, A. M., Gardner, L., Hiby, S., Farrell, L., Apps, R., Masters, L., Goodridge, J., Lathbury, L., Stevart, C. A., Verma, S., and Moffett, A. (2008). Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age. J. Immunol. 181, 39–46.
| Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age.Crossref | GoogleScholarGoogle Scholar | 18566368PubMed |
Sharma, S. (2014). Natural killer cells and regulatory T cells in early pregnancy loss. Int. J. Dev. Biol. 58, 219–229.
| Natural killer cells and regulatory T cells in early pregnancy loss.Crossref | GoogleScholarGoogle Scholar | 25023688PubMed |
Shaw, J., Tang, Z., Schneider, H., Salje, K., Hansson, S. R., and Guller, S. (2016). Inflammatory processes are specifically enhanced in endothelial cells by placental-derived TNF-α: implications in preeclampsia (PE). Placenta 43, 1–8.
| Inflammatory processes are specifically enhanced in endothelial cells by placental-derived TNF-α: implications in preeclampsia (PE).Crossref | GoogleScholarGoogle Scholar | 27324092PubMed |
Sips, M., Liu, Q., Draghi, M., Ghebremichael, M., Berger, C. T., Suscovich, T. J., Sun, Y., Walker, B. D., Carrington, M., Altfeld, M., Brouckaert, P., De Jager, P. L., and Alter, G. (2016). HLA-C levels impact natural killer cell subset distribution and function. Hum. Immunol. 77, 1147–1153.
| HLA-C levels impact natural killer cell subset distribution and function.Crossref | GoogleScholarGoogle Scholar | 27521484PubMed |
Sturrock, A., Cahill, B., Norman, K., Huecksteadt, T. P., Hill, K., Sanders, K., Karwande, S. V., Stringham, J. C., Bull, D. A., Gleich, M., Kennedy, T. P., and Hoidal, J. R. (2006). Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 290, L661–L673.
| Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells.Crossref | GoogleScholarGoogle Scholar | 16227320PubMed |
Suman, P., Shembekar, N., and Gupta, S. K. (2013). Leukemia inhibitory factor increases the invasiveness of trophoblastic cells through integrated increase in the expression of adhesion molecules and pappalysin 1 with a concomitant decrease in the expression of tissue inhibitor of matrix metalloproteinases. Fertil. Steril. 99, 533–542.e2.
| Leukemia inhibitory factor increases the invasiveness of trophoblastic cells through integrated increase in the expression of adhesion molecules and pappalysin 1 with a concomitant decrease in the expression of tissue inhibitor of matrix metalloproteinases.Crossref | GoogleScholarGoogle Scholar | 23122949PubMed |
Thaxton, J. E., Nevers, T., Lippe, E. O., Blois, S. M., Saito, S., and Sharma, S. (2013). NKG2D blockade inhibits poly(I:C)-triggered fetal loss in wild type but not IL-10−/− mice. J. Immunol. 190, 3639–3647.
| NKG2D blockade inhibits poly(I:C)-triggered fetal loss in wild type but not IL-10−/− mice.Crossref | GoogleScholarGoogle Scholar | 23455498PubMed |
Vacca, P., Moretta, L., Moretta, A., and Mingari, M. C. (2011). Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol. 32, 517–523.
| Origin, phenotype and function of human natural killer cells in pregnancy.Crossref | GoogleScholarGoogle Scholar | 21889405PubMed |
Vaillancourt, C., Lanoix, D., Le-Bellego, F., Daoud, G., and Lafond, J. (2009). Involvement of MAPK signalling in human villous trophoblast differentiation. Mini Rev. Med. Chem. 9, 962–973.
| Involvement of MAPK signalling in human villous trophoblast differentiation.Crossref | GoogleScholarGoogle Scholar | 19601892PubMed |
Verma, S., Hiby, S. E., Loke, Y. W., and King, A. (2000). Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol. Reprod. 62, 959–968.
| Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15.Crossref | GoogleScholarGoogle Scholar | 10727265PubMed |
Walter, W., Sánchez-Cabo, F., and Ricote, M. (2015). GOplot: an R package for visually combining expression data with functional analysis. Bioinformatics 31, 2912–2914.
| GOplot: an R package for visually combining expression data with functional analysis.Crossref | GoogleScholarGoogle Scholar | 25964631PubMed |
Xavier, S. C., de-Andrade, H. M., Monte, S. J., Chiarelli, I. M., Lima, W. G., Michalick, M. S., Tafuri, W. L., and Tafuri, W. L. (2006). Comparison of paraffin-embedded skin biopsies from different anatomical regions as sampling methods for detection of Leishmania infection in dogs using histological, immunohistochemical and PCR methods. BMC Vet. Res. 2, 17.
| Comparison of paraffin-embedded skin biopsies from different anatomical regions as sampling methods for detection of Leishmania infection in dogs using histological, immunohistochemical and PCR methods.Crossref | GoogleScholarGoogle Scholar | 16762067PubMed |
Yong, P. J., McFadden, D. E., and Robinson, W. P. (2012). Protein kinase profiling in miscarriage: implications for the pathogenesis of trisomic pregnancy. J. Obstet. Gynaecol. Can. 34, 1141–1148.
| Protein kinase profiling in miscarriage: implications for the pathogenesis of trisomic pregnancy.Crossref | GoogleScholarGoogle Scholar | 23231796PubMed |