Estrogen and EGFR Pathways Regulate Notch Signaling in Opposing Directions for Multi-Ciliogenesis in the Fallopian Tube
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cell Culture Medium
2.2. Isolating Primary FTECs
2.3. Induction of the Differentiation of FTECs in the Air–Liquid Interface (ALI) Culture
2.4. Immunofluorescence Staining
2.5. Scanning Electron Microscopy (SEM)
2.6. Motility Analysis of the Ciliated Cells
2.7. Western Blot Analysis
2.8. Polymerase Chain Reaction (PCR)
2.9. Statistical Analysis
3. Results
3.1. Estrogen Regulates Ciliogenesis Through ERβ
3.2. Inhibition of the EGFR-MEK-ERK Pathway Promotes Ciliogenesis
3.3. Estrogen and EGFR Pathways Regulate Notch Signaling in Ciliogenesis
4. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Lyons, R.A.; Saridogan, E.; Djahanbakhch, O. The reproductive significance of human Fallopian tube cilia. Hum. Reprod. Update 2006, 12, 363–372. [Google Scholar] [CrossRef] [PubMed]
- Amso, N.N.; Crow, J.; Shaw, R.W. Comparative immunohistochemical study of oestrogen and progesterone receptors in the fallopian tube and uterus at different stages of the menstrual cycle and the menopause. Hum. Reprod. 1994, 9, 1027–1037. [Google Scholar] [CrossRef] [PubMed]
- Verhage, H.G.; Mavrogianis, P.A.; Boice, M.L.; Li, W.; Fazleabas, A.T. Oviductal epithelium of the baboon: hormonal control and the immuno-gold localization of oviduct-specific glycoproteins. Am. J. Anat. 1990, 187, 81–90. [Google Scholar] [CrossRef] [PubMed]
- Comer, M.T.; Leese, H.J.; Southgate, J. Induction of a differentiated ciliated cell phenotype in primary cultures of Fallopian tube epithelium. Hum. Reprod. 1998, 13, 3114–3120. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Donnez, J.; Casanas-Roux, F.; Ferin, J.; Thomas, K. Changes in ciliation and cell height in human tubal epithelium in the fertile and post-fertile years. Maturitas 1983, 5, 39–45. [Google Scholar] [CrossRef]
- Guseh, J.S.; Bores, S.A.; Stanger, B.Z.; Zhou, Q.; Anderson, W.J.; Melton, D.A.; Rajagopal, J. Notch signaling promotes airway mucous metaplasia and inhibits alveolar development. Development 2009, 136, 1751–1759. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsao, P.N.; Vasconcelos, M.; Izvolsky, K.I.; Qian, J.; Lu, J.; Cardoso, W.V. Notch signaling controls the balance of ciliated and secretory cell fates in developing airways. Development 2009, 136, 2297–2307. [Google Scholar] [CrossRef] [Green Version]
- Kang, J.H.; Lee, E.H.; Park, S.W.; Chung, I.Y. MUC5AC expression through bidirectional communication of Notch and epidermal growth factor receptor pathways. J. Immunol. 2011, 187, 222–229. [Google Scholar] [CrossRef]
- Valencia-Gattas, M.; Conner, G.E.; Fregien, N.L. Gefitinib, an EGFR tyrosine kinase inhibitor, prevents smoke-mediated ciliated airway epithelial cell loss and promotes their recovery. PLoS ONE 2016, 11, e0160216. [Google Scholar] [CrossRef]
- Perets, R.; Wyant, G.A.; Muto, K.W.; Bijron, J.G.; Poole, B.B.; Chin, K.T.; Chen, J.Y.; Ohman, A.W.; Stepule, C.D.; Kwak, S.; et al. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models. Cancer Cell 2013, 24, 751–765. [Google Scholar] [CrossRef]
- Przybycin, C.G.; Kurman, R.J.; Ronnett, B.M.; Shih Ie, M.; Vang, R. Are all pelvic (nonuterine) serous carcinomas of tubal origin? Am. J. Surg. Pathol. 2010, 34, 1407–1416. [Google Scholar] [CrossRef]
- Vang, R.; Shih Ie, M.; Kurman, R.J. Fallopian tube precursors of ovarian low- and high-grade serous neoplasms. Histopathology 2013, 62, 44–58. [Google Scholar] [CrossRef]
- Kessler, M.; Hoffmann, K.; Brinkmann, V.; Thieck, O.; Jackisch, S.; Toelle, B.; Berger, H.; Mollenkopf, H.J.; Mangler, M.; Sehouli, J.; et al. The Notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids. Nat. Commun. 2015, 6, 8989. [Google Scholar] [CrossRef]
- Inoue, T. TI Workbench, an integrated software package for electrophysiology and imaging. Microsc. 2018, 67, 129–143. [Google Scholar] [CrossRef] [PubMed]
- Deroo, B.J.; Korach, K.S. Estrogen receptors and human disease. J. Clin. Investig. 2006, 116, 561–570. [Google Scholar] [CrossRef] [Green Version]
- Maggiolini, M.; Picard, D. The unfolding stories of GPR30, a new membrane-bound estrogen receptor. J. Endocrinol. 2010, 204, 105–114. [Google Scholar] [CrossRef]
- Burgel, P.R.; Nadel, J.A. Roles of epidermal growth factor receptor activation in epithelial cell repair and mucin production in airway epithelium. Thorax 2004, 59, 992–996. [Google Scholar] [CrossRef] [Green Version]
- Marcet, B.; Chevalier, B.; Luxardi, G.; Coraux, C.; Zaragosi, L.E.; Cibois, M.; Robbe-Sermesant, K.; Jolly, T.; Cardinaud, B.; Moreilhon, C.; et al. Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat. Cell Biol. 2011, 13, 693–699. [Google Scholar] [CrossRef]
- Rock, J.R.; Gao, X.; Xue, Y.; Randell, S.H.; Kong, Y.Y.; Hogan, B.L. Notch-dependent differentiation of adult airway basal stem cells. Cell Stem Cell 2011, 8, 639–648. [Google Scholar] [CrossRef]
- Okada, A.; Ohta, Y.; Brody, S.L.; Watanabe, H.; Krust, A.; Chambon, P.; Iguchi, T. Role of foxj1 and estrogen receptor alpha in ciliated epithelial cell differentiation of the neonatal oviduct. J. Mol. Endocrinol. 2004, 32, 615–625. [Google Scholar] [CrossRef] [Green Version]
- Takeyama, K.; Dabbagh, K.; Lee, H.M.; Agusti, C.; Lausier, J.A.; Ueki, I.F.; Grattan, K.M.; Nadel, J.A. Epidermal growth factor system regulates mucin production in airways. Proc. Natl. Acad. Sci. USA 1999, 96, 3081–3086. [Google Scholar] [CrossRef] [Green Version]
- Perrais, M.; Pigny, P.; Copin, M.C.; Aubert, J.P.; Van Seuningen, I. Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signal-regulated kinase cascade and Sp1. J. Biol. Chem. 2002, 277, 32258–32267. [Google Scholar] [CrossRef]
- Artavanis-Tsakonas, S.; Rand, M.D.; Lake, R.J. Notch signaling: cell fate control and signal integration in development. Science 1999, 284, 770–776. [Google Scholar] [CrossRef]
- Shaykhiev, R.; Zuo, W.L.; Chao, I.; Fukui, T.; Witover, B.; Brekman, A.; Crystal, R.G. EGF shifts human airway basal cell fate toward a smoking-associated airway epithelial phenotype. Proc. Natl. Acad. Sci. USA 2013, 110, 12102–12107. [Google Scholar] [CrossRef] [Green Version]
- Hitoshi, S.; Alexson, T.; Tropepe, V.; Donoviel, D.; Elia, A.J.; Nye, J.S.; Conlon, R.A.; Mak, T.W.; Bernstein, A.; van der Kooy, D. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev. 2002, 16, 846–858. [Google Scholar] [CrossRef] [Green Version]
- Liu, M.M.; Albanese, C.; Anderson, C.M.; Hilty, K.; Webb, P.; Uht, R.M.; Price, R.H., Jr.; Pestell, R.G.; Kushner, P.J. Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J. Biol. Chem. 2002, 277, 24353–24360. [Google Scholar] [CrossRef]
- Gori, I.; Pellegrini, C.; Staedler, D.; Russell, R.; Jan, C.; Canny, G.O. Tumor necrosis factor-alpha activates estrogen signaling pathways in endometrial epithelial cells via estrogen receptor alpha. Mol. Cell. Endocrinol. 2011, 345, 27–37. [Google Scholar] [CrossRef]
- Wang, Y.X.; Li, M.; Zhang, H.Q.; Tang, M.X.; Guo, C.F.; Deng, A.; Chen, Y.; Xiao, L.G. Opposite function of ERalpha and ERbeta in controlling 17beta-estradiol-mediated osteogenesis in osteoblasts. Arch. Med. Res. 2016, 47, 255–261. [Google Scholar] [CrossRef]
- Haim, K.; Weitzenfeld, P.; Meshel, T.; Ben-Baruch, A. Epidermal growth factor and estrogen act by independent pathways to additively promote the release of the angiogenic chemokine CXCL8 by breast tumor cells. Neoplasia 2011, 13, 230–243. [Google Scholar] [CrossRef]
- Chen, S.; Bangaru, M.L.; Sneade, L.; Dunckley, J.A.; Ben-Jonathan, N.; Kansra, S. Epidermal growth factor receptor cross-talks with ligand-occupied estrogen receptor-alpha to modulate both lactotroph proliferation and prolactin gene expression. Am. J. Physiol. Endocrinol. Metab. 2009, 297, E331–E339. [Google Scholar] [CrossRef]
- Kato, S.; Endoh, H.; Masuhiro, Y.; Kitamoto, T.; Uchiyama, S.; Sasaki, H.; Masushige, S.; Gotoh, Y.; Nishida, E.; Kawashima, H.; et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 1995, 270, 1491–1494. [Google Scholar] [CrossRef]
- Yaish, P.; Gazit, A.; Gilon, C.; Levitzki, A. Blocking of EGF-dependent cell proliferation by EGF receptor kinase inhibitors. Science 1988, 242, 933–935. [Google Scholar] [CrossRef]
- Purow, B.W.; Haque, R.M.; Noel, M.W.; Su, Q.; Burdick, M.J.; Lee, J.; Sundaresan, T.; Pastorino, S.; Park, J.K.; Mikolaenko, I.; et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res. 2005, 65, 2353–2363. [Google Scholar] [CrossRef]
- Sun, Y.; Wang, C.; Yang, H.; Ma, X. The effect of estrogen on the proliferation of endometrial cancer cells is mediated by ERRgamma through AKT and ERK1/2. Eur. J. Cancer Prev. 2014, 23, 418–424. [Google Scholar] [CrossRef]
- Lafkas, D.; Shelton, A.; Chiu, C.; de Leon Boenig, G.; Chen, Y.; Stawicki, S.S.; Siltanen, C.; Reichelt, M.; Zhou, M.; Wu, X.; et al. Therapeutic antibodies reveal Notch control of transdifferentiation in the adult lung. Nature 2015, 528, 127–131. [Google Scholar] [CrossRef]
- Pardo-Saganta, A.; Tata, P.R.; Law, B.M.; Saez, B.; Chow, R.D.; Prabhu, M.; Gridley, T.; Rajagopal, J. Parent stem cells can serve as niches for their daughter cells. Nature 2015, 523, 597–601. [Google Scholar] [CrossRef]
- Sun, M.; Paciga, J.E.; Feldman, R.I.; Yuan, Z.; Coppola, D.; Lu, Y.Y.; Shelley, S.A.; Nicosia, S.V.; Cheng, J.Q. Phosphatidylinositol-3-OH Kinase (PI3K)/AKT2, activated in breast cancer, regulates and is induced by estrogen receptor alpha (ERalpha) via interaction between ERalpha and PI3K. Cancer Res. 2001, 61, 5985–5991. [Google Scholar]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhu, M.; Iwano, T.; Takeda, S. Estrogen and EGFR Pathways Regulate Notch Signaling in Opposing Directions for Multi-Ciliogenesis in the Fallopian Tube. Cells 2019, 8, 933. https://doi.org/10.3390/cells8080933
Zhu M, Iwano T, Takeda S. Estrogen and EGFR Pathways Regulate Notch Signaling in Opposing Directions for Multi-Ciliogenesis in the Fallopian Tube. Cells. 2019; 8(8):933. https://doi.org/10.3390/cells8080933
Chicago/Turabian StyleZhu, Maobi, Tomohiko Iwano, and Sen Takeda. 2019. "Estrogen and EGFR Pathways Regulate Notch Signaling in Opposing Directions for Multi-Ciliogenesis in the Fallopian Tube" Cells 8, no. 8: 933. https://doi.org/10.3390/cells8080933