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Induction of forkhead box M1 (FoxM1) by EGF through ERK signaling pathway promotes trophoblast cell invasion

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Abstract

Successful placentation depends on the proper invasion of extravillous trophoblast (EVT) cells into maternal tissues. Previous reports have demonstrated that FoxM1 is oncogenic and plays important roles in angiogenesis, invasion, and metastasis. However, little is known about the roles of FoxM1 in the invasion of EVT cells. EGF, as a growth factor (epidermal growth factor), has been studied extensively in reproduction. JAR cells are a reliable model for studying early invasive trophoblast regulation. We have observed the relationship between EGF and FoxM1 in JAR cells by using specific inhibitors for the intervention in and study of potential signal pathways. We have also tested the ability of JAR cells to be influenced by the expression of FoxM1. Our data indicate that EGF promotes FoxM1 expression through the ERK signal pathway. Over-FoxM1 expression upregulates the ability of JAR cells to migrate and invade and vice versa. Our investigation of FoxM1 should provide new insights into the molecular mechanisms of EVT invasion.

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References

  • Anteby EY, Greenfield C, Natanson-Yaron S, Goldman-Wohl D, Hamani Y, Khudyak V, Ariel I, Yagel S (2004) Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and −10 stimulate trophoblast plasminogen activator system and metalloproteinase-9. Mol Hum Reprod 10:229–235

    Article  CAS  PubMed  Google Scholar 

  • Aplin JD (2010) Developmental cell biology of human villous trophoblast: current research problems. Int J Dev Biol 54:323–329

    Article  PubMed  Google Scholar 

  • Bass KE, Morrish D, Roth I, Bhardwaj D, Taylor R, Zhou Y, Fisher SJ (1994) Human cytotrophoblast invasion is up-regulated by epidermal growth factor: evidence that paracrine factors modify this process. Dev Biol 164:550–561

    Article  CAS  PubMed  Google Scholar 

  • Bischof P, Campana A (2000) Molecular mediators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 14:801–814

    Article  CAS  PubMed  Google Scholar 

  • Bischof P, Martelli M, Campana A, Itoh Y, Ogata Y, Nagase H (1995) Importance of matrix metalloproteinases in human trophoblast invasion. Early Pregnancy 1:263–269

    CAS  PubMed  Google Scholar 

  • Brar AK, Frank GR, Kessler CA, Cedars MI, Handwerger S (1997) Progesterone-dependent decidualization of the human endometrium is mediated by cAMP. Endocrine 6:301–307

    Article  CAS  PubMed  Google Scholar 

  • Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, Yoshinaga K (2000) Embryo implantation. Dev Biol 223:217–237

    Article  CAS  PubMed  Google Scholar 

  • Cohen M, Meisser A, Bischof P (2006) Metalloproteinases and human placental invasiveness. Placenta 27:783–793

    Article  CAS  PubMed  Google Scholar 

  • Di Simone N, Di Nicuolo F, Sanguinetti M, Ferrazzani S, D’Alessio MC, Castellani R, Bompiani A, Caruso A (2007) Low-molecular weight heparin induces in vitro trophoblast invasiveness: role of matrix metalloproteinases and tissue inhibitors. Placenta 28:298–304

    Article  PubMed  Google Scholar 

  • Drake PM, Red-Horse K, Fisher SJ (2004) Reciprocal chemokine receptor and ligand expression in the human placenta: implications for cytotrophoblast differentiation. Dev Dyn 229:877–885

    Article  CAS  PubMed  Google Scholar 

  • Fisher SJ, Cui TY, Zhang L, Hartman L, Grahl K, Zhang GY, Tarpey J, Damsky CH (1989) Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 109:891–902

    Article  CAS  PubMed  Google Scholar 

  • Han J, Xie Y, Lan F, Yu Y, Liu W, Chen J, Zheng F, Ouyang X, Lin X, Lin Y, Huang Q, Wang L, Tan J (2014) Additive effects of EGF and IL-1beta regulate tumor cell migration and invasion in gastric adenocarcinoma via activation of ERK1/2. Int J Oncol 45:291–301

    Article  PubMed  Google Scholar 

  • Hannan NJ, Salamonsen LA (2007) Role of chemokines in the endometrium and in embryo implantation. Curr Opin Obstet Gynecol 19:266–272

    Article  PubMed  Google Scholar 

  • Kalinichenko VV, Gusarova GA, Tan Y, Wang IC, Major ML, Wang X, Yoder HM, Costa RH (2003) Ubiquitous expression of the forkhead box M1B transgene accelerates proliferation of distinct pulmonary cell types following lung injury. J Biol Chem 278:37888–37894

    Article  CAS  PubMed  Google Scholar 

  • Karadedou CT (2006) Regulation of the FOXM1 transcription factor by the estrogen receptor alpha at the protein level, in breast cancer. Hippokratia 10:128–132

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kilani RT, Mackova M, Davidge ST, Winkler-Lowen B, Demianczuk N, Guilbert LJ (2007) Endogenous tumor necrosis factor alpha mediates enhanced apoptosis of cultured villous trophoblasts from intrauterine growth-restricted placentae. Reproduction 133:257–264

    Article  CAS  PubMed  Google Scholar 

  • Knofler M (2010) Critical growth factors and signalling pathways controlling human trophoblast invasion. Int J Dev Biol 54:269–280

    Article  PubMed  PubMed Central  Google Scholar 

  • Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, Grobelny D, Galardy R, Damsky CH, Fisher SJ (1991) 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol 113:437–449

    Article  CAS  PubMed  Google Scholar 

  • Littlepage LE, Sternlicht MD, Rougier N, Phillips J, Gallo E, Yu Y, Williams K, Brenot A, Gordon JI, Werb Z (2010) Matrix metalloproteinases contribute distinct roles in neuroendocrine prostate carcinogenesis, metastasis, and angiogenesis progression. Cancer Res 70:2224–2234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pijnenborg R, Bland JM, Robertson WB, Brosens I (1983) Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 4:397–413

    Article  CAS  PubMed  Google Scholar 

  • Puistola U, Ronnberg L, Martikainen H, Turpeenniemi-Hujanen T (1989) The human embryo produces basement membrane collagen (type IV collagen)-degrading protease activity. Hum Reprod 4:309–311

    Article  CAS  PubMed  Google Scholar 

  • Qiu Q, Yang M, Tsang BK, Gruslin A (2004) EGF-induced trophoblast secretion of MMP-9 and TIMP-1 involves activation of both PI3K and MAPK signalling pathways. Reproduction 128:355–363

    Article  CAS  PubMed  Google Scholar 

  • Red-Horse K, Drake PM, Gunn MD, Fisher SJ (2001) Chemokine ligand and receptor expression in the pregnant uterus: reciprocal patterns in complementary cell subsets suggest functional roles. Am J Pathol 159:2199–2213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, Fisher SJ (2004) Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest 114:744–754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salamonsen LA, Hannan NJ, Dimitriadis E (2007) Cytokines and chemokines during human embryo implantation: roles in implantation and early placentation. Semin Reprod Med 25:437–444

    Article  CAS  PubMed  Google Scholar 

  • Salamonsen LA, Nie G, Hannan NJ, Dimitriadis E (2009) Society for Reproductive Biology, Founders’ lecture 2009. Preparing fertile soil: the importance of endometrial receptivity. Reprod Fertil Dev 21:923–934

    Article  CAS  PubMed  Google Scholar 

  • Sanders DA, Ross-Innes CS, Beraldi D, Carroll JS, Balasubramanian S (2013) Genome-wide mapping of FOXM1 binding reveals co-binding with estrogen receptor alpha in breast cancer cells. Genome Biol 14:R6

    Article  PubMed  PubMed Central  Google Scholar 

  • Shimonovitz S, Hurwitz A, Dushnik M, Anteby E, Geva-Eldar T, Yagel S (1994) Developmental regulation of the expression of 72 and 92 kD type IV collagenases in human trophoblasts: a possible mechanism for control of trophoblast invasion. Am J Obstet Gynecol 171:832–838

    Article  CAS  PubMed  Google Scholar 

  • Staun-Ram E, Shalev E (2005) Human trophoblast function during the implantation process. Reprod Biol Endocrinol 3:56

    Article  PubMed  PubMed Central  Google Scholar 

  • Staun-Ram E, Goldman S, Gabarin D, Shalev E (2004) Expression and importance of matrix metalloproteinase 2 and 9 (MMP-2 and −9) in human trophoblast invasion. Reprod Biol Endocrinol 2:59

    Article  PubMed  PubMed Central  Google Scholar 

  • Sugiura T, Berditchevski F (1999) Function of alpha3beta1-tetraspanin protein complexes in tumor cell invasion. Evidence for the role of the complexes in production of matrix metalloproteinase 2 (MMP-2). J Cell Biol 146:1375–1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turpeenniemi-Hujanen T, Ronnberg L, Kauppila A, Puistola U (1992) Laminin in the human embryo implantation: analogy to the invasion by malignant cells. Fertil Steril 58:105–113

    Article  CAS  PubMed  Google Scholar 

  • Vicovac L, Aplin JD (1996) Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel) 156:202–216

    Article  CAS  PubMed  Google Scholar 

  • Wang IC, Chen YJ, Hughes DE, Ackerson T, Major ML, Kalinichenko VV, Costa RH, Raychaudhuri P, Tyner AL, Lau LF (2008) FoxM1 regulates transcription of JNK1 to promote the G1/S transition and tumor cell invasiveness. J Biol Chem 283:20770–20778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wierstra I, Alves J (2007) FOXM1, a typical proliferation-associated transcription factor. Biol Chem 388:1257–1274

    Article  CAS  PubMed  Google Scholar 

  • Xie Y, Cui D, Kong Y (2014) FoxM1 influences embryo implantation and is regulated by 17 beta-estradiol and progesterone in mouse uteri and endometrium cells. Int J Clin Exp Pathol 7:6585–6595

    PubMed  PubMed Central  Google Scholar 

  • Xu P, Wang YL, Zhu SJ, Luo SY, Piao YS, Zhuang LZ (2000) Expression of matrix metalloproteinase-2, −9, and −14, tissue inhibitors of metalloproteinase-1, and matrix proteins in human placenta during the first trimester. Biol Reprod 62:988–994

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Zhao W, Xu QW, Wang XS, Zhang Y, Zhang J (2014) IQGAP3 promotes EGFR-ERK signaling and the growth and metastasis of lung cancer cells. PLoS ONE 9:e97578

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Ying Kong.

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This work was supported by National Natural 467 Scientific Grants (no. 30970646), China and the Liaoning Province Natural Science Foundation of China (2014023055).

The original online version of this article was revised: The authors regret that the original version of this paper unfortunately contained an incorrect image in Figure 2C. Those are due to improperly image selection. The correct and incorrect Figure 2C are provided in the erratum article.

The original article has been corrected.

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Xie, Y., Cui, D., Sui, L. et al. Induction of forkhead box M1 (FoxM1) by EGF through ERK signaling pathway promotes trophoblast cell invasion. Cell Tissue Res 362, 421–430 (2015). https://doi.org/10.1007/s00441-015-2211-y

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  • DOI: https://doi.org/10.1007/s00441-015-2211-y

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