Clinical and Experimental Reproductive Medicine

  • 제47권2호
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  • Pages.114-121
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  • 2020
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  • 2233-8233(pISSN)
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  • 2233-8241(eISSN)
대한생식의학회 (The Korean Society for Reproductive Medicine)
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Endometrial profilin 1: A key player in embryo-endometrial crosstalk

  • Lee, Chang-Jin (Department of Biomedical Science, School of Life Science, CHA University) ;
  • Hong, Seon-Hwa (CHA Fertility Center Bundang, School of Medicine, CHA University) ;
  • Yoon, Min-Ji (Department of Biomedical Science, School of Life Science, CHA University) ;
  • Lee, Kyung-Ah (Department of Biomedical Science, School of Life Science, CHA University) ;
  • Ko, Jung-Jae (Department of Biomedical Science, School of Life Science, CHA University) ;
  • Koo, Hwa Seon (CHA Fertility Center Bundang, School of Medicine, CHA University) ;
  • Kim, Jee Hyun (CHA Fertility Center Bundang, School of Medicine, CHA University) ;
  • Choi, Dong Hee (CHA Fertility Center Bundang, School of Medicine, CHA University) ;
  • Kwon, Hwang (CHA Fertility Center Bundang, School of Medicine, CHA University) ;
  • Kang, Youn-Jung (Department of Biomedical Science, School of Life Science, CHA University)
  • 투고 : 2019.12.05
  • 심사 : 2019.12.14
  • 발행 : 2020.06.30
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초록

Objective: Despite extensive research on implantation failure, little is known about the molecular mechanisms underlying the crosstalk between the embryo and the maternal endometrium, which is critical for successful pregnancy. Profilin 1 (PFN1), which is expressed both in the embryo and in the endometrial epithelium, acts as a potent regulator of actin polymerization and the cytoskeletal network. In this study, we identified the specific role of endometrial PFN1 during embryo implantation. Methods: Morphological alterations depending on the status of PFN1 expression were assessed in PFN1-depleted or control cells grown on Matrigel-coated cover glass. Day-5 mouse embryos were cocultured with Ishikawa cells. Comparisons of the rates of F-actin formation and embryo attachment were performed by measuring the stability of the attached embryo onto PFN1-depleted or control cells. Results: Depletion of PFN1 in endometrial epithelial cells induced a significant reduction in cell-cell adhesion displaying less formation of colonies and a more circular cell shape. Mouse embryos co-cultured with PFN1-depleted cells failed to form actin cytoskeletal networks, whereas more F-actin formation in the direction of surrounding PFN1-intact endometrial epithelial cells was detected. Furthermore, significantly lower embryo attachment stability was observed in PFN1-depleted cells than in control cells. This may have been due to reduced endometrial receptivity caused by impaired actin cytoskeletal networks associated with PFN1 deficiency. Conclusion: These observations definitively demonstrate an important role of PFN1 in mediating cell-cell adhesion during the initial stage of embryo implantation and suggest a potential therapeutic target or novel biomarker for patients suffering from implantation failure.

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참고문헌

  1. Bashiri A, Halper KI, Orvieto R. Recurrent Implantation Failureupdate overview on etiology, diagnosis, treatment and future directions. Reprod Biol Endocrinol 2018;16:121. https://doi.org/10.1186/s12958-018-0414-2
  2. Simon A, Laufer N. Assessment and treatment of repeated implantation failure (RIF). J Assist Reprod Genet 2012;29:1227-39. https://doi.org/10.1007/s10815-012-9861-4
  3. Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, et al. Molecular cues to implantation. Endocr Rev 2004;25:341-73. https://doi.org/10.1210/er.2003-0020
  4. Psychoyos A. Hormonal control of ovoimplantation. Vitam Horm 1973;31:201-56. https://doi.org/10.1016/S0083-6729(08)60999-1
  5. Tabibzadeh S. Molecular control of the implantation window. Hum Reprod Update 1998;4:465-71. https://doi.org/10.1093/humupd/4.5.465
  6. Achache H, Revel A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update 2006;12:731-46. https://doi.org/10.1093/humupd/dml004
  7. Norwitz ER. Defective implantation and placentation: laying the blueprint for pregnancy complications. Reprod Biomed Online 2006;13:591-9. https://doi.org/10.1016/S1472-6483(10)60649-9
  8. Margalioth EJ, Ben-Chetrit A, Gal M, Eldar-Geva T. Investigation and treatment of repeated implantation failure following IVF-ET. Hum Reprod 2006;21:3036-43. https://doi.org/10.1093/humrep/del305
  9. Koot YE, Boomsma CM, Eijkemans MJ, Lentjes EG, Macklon NS. Recurrent pre-clinical pregnancy loss is unlikely to be a 'cause' of unexplained infertility. Hum Reprod 2011;26:2636-41. https://doi.org/10.1093/humrep/der217
  10. Tang DD, Gerlach BD. The roles and regulation of the actin cytoskeleton, intermediate filaments and microtubules in smooth muscle cell migration. Respir Res 2017;18:54. https://doi.org/10.1186/s12931-017-0544-7
  11. Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod 2010;16:135-52. https://doi.org/10.1093/molehr/gap095
  12. Tan K, An L, Wang SM, Wang XD, Zhang ZN, Miao K, et al. Actin disorganization plays a vital role in impaired embryonic development of in vitro-produced mouse preimplantation embryos. PLoS One 2015;10:e0130382. https://doi.org/10.1371/journal.pone.0130382
  13. Alkam D, Feldman EZ, Singh A, Kiaei M. Profilin1 biology and its mutation, actin(g) in disease. Cell Mol Life Sci 2017;74:967-81. https://doi.org/10.1007/s00018-016-2372-1
  14. Berglund L, Bjorling E, Oksvold P, Fagerberg L, Asplund A, Szigyarto CA, et al. A genecentric human protein atlas for expression profiles based on antibodies. Mol Cell Proteomics 2008;7:2019-27. https://doi.org/10.1074/mcp.R800013-MCP200
  15. Thul PJ, Akesson L, Wiking M, Mahdessian D, Geladaki A, Ait Blal H, et al. A subcellular map of the human proteome. Science 2017;356:eaal3321. https://doi.org/10.1126/science.aal3321
  16. Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, et al. Proteomics: tissue-based map of the human proteome. Science 2015;347:1260419. https://doi.org/10.1126/science.1260419
  17. Bae YH, Ding Z, Zou L, Wells A, Gertler F, Roy P. Loss of profilin-1 expression enhances breast cancer cell motility by Ena/VASP proteins. J Cell Physiol 2009;219:354-64. https://doi.org/10.1002/jcp.21677
  18. Zou L, Ding Z, Roy P. Profilin-1 overexpression inhibits proliferation of MDA-MB-231 breast cancer cells partly through p27kip1 upregulation. J Cell Physiol 2010;223:623-9. https://doi.org/10.1002/jcp.22058
  19. Kang YJ, Forbes K, Carver J, Aplin JD. The role of the osteopontinintegrin ${\alpha}v{\beta}3$ interaction at implantation: functional analysis using three different in vitro models. Hum Reprod 2014;29:739-49. https://doi.org/10.1093/humrep/det433
  20. Kang YJ, Lees M, Matthews LC, Kimber SJ, Forbes K, Aplin JD. MiR-145 suppresses embryo-epithelial juxtacrine communication at implantation by modulating maternal IGF1R. J Cell Sci 2015;128:804-14. https://doi.org/10.1242/jcs.164004
  21. Carver J, Martin K, Spyropoulou I, Barlow D, Sargent I, Mardon H. An in-vitro model for stromal invasion during implantation of the human blastocyst. Hum Reprod 2003;18:283-90. https://doi.org/10.1093/humrep/deg072
  22. Kang YJ, Balter B, Csizmadia E, Haas B, Sharma H, Bronson R, et al. Contribution of classical end-joining to PTEN inactivation in p53-mediated glioblastoma formation and drug-resistant survival. Nat Commun 2017;8:14013. https://doi.org/10.1038/ncomms14013
  23. Ding Z, Roy P. Profilin-1 versus profilin-2: two faces of the same coin? Breast Cancer Res 2013;15:311. https://doi.org/10.1186/bcr3433
  24. Cheng YJ, Zhu ZX, Zhou JS, Hu ZQ, Zhang JP, Cai QP, et al. Silencing profilin-1 inhibits gastric cancer progression via integrin ${\beta}1$/focal adhesion kinase pathway modulation. World J Gastroenterol 2015;21:2323-35. https://doi.org/10.3748/wjg.v21.i8.2323
  25. Suetsugu S, Takenawa T. Regulation of cortical actin networks in cell migration. Int Rev Cytol 2003;229:245-86. https://doi.org/10.1016/S0074-7696(03)29006-9
  26. Bachir AI, Horwitz AR, Nelson WJ, Bianchini JM. Actin-based adhesion modules mediate cell interactions with the extracellular matrix and neighboring cells. Cold Spring Harb Perspect Biol 2017;9:a023234. https://doi.org/10.1101/cshperspect.a023234
  27. Aplin JD, Ruane PT. Embryo-epithelium interactions during implantation at a glance. J Cell Sci 2017;130:15-22. https://doi.org/10.1242/jcs.175943
  28. Nimbkar-Joshi S, Rosario G, Katkam RR, Manjramkar DD, Metkari SM, Puri CP, et al. Embryo-induced alterations in the molecular phenotype of primate endometrium. J Reprod Immunol 2009;83:65-71. https://doi.org/10.1016/j.jri.2009.08.011
  29. Singh H, Aplin JD. Adhesion molecules in endometrial epithelium: tissue integrity and embryo implantation. J Anat 2009;215:3-13. https://doi.org/10.1111/j.1469-7580.2008.01034.x
  30. Kim SM, Kim JS. A review of mechanisms of implantation. Dev Reprod 2017;21:351-9. https://doi.org/10.12717/DR.2017.21.4.351
  31. Ding Z, Lambrechts A, Parepally M, Roy P. Silencing profilin-1 inhibits endothelial cell proliferation, migration and cord morphogenesis. J Cell Sci 2006;119(Pt 19):4127-37. https://doi.org/10.1242/jcs.03178
  32. Zou L, Hazan R, Roy P. Profilin-1 overexpression restores adherens junctions in MDA-MB-231 breast cancer cells in R-cadherindependent manner. Cell Motil Cytoskeleton 2009;66:1048-56. https://doi.org/10.1002/cm.20407
  33. Bitko V, Oldenburg A, Garmon NE, Barik S. Profilin is required for viral morphogenesis, syncytium formation, and cell-specific stress fiber induction by respiratory syncytial virus. BMC Microbiol 2003;3:9. https://doi.org/10.1186/1471-2180-3-9
  34. Quinlan MP. Vinculin, VASP, and profilin are coordinately regulated during actin remodeling in epithelial cells, which requires de novo protein synthesis and protein kinase signal transduction pathways. J Cell Physiol 2004;200:277-90. https://doi.org/10.1002/jcp.20009
  35. Rawe VY, Payne C, Schatten G. Profilin and actin-related proteins regulate microfilament dynamics during early mammalian embryogenesis. Hum Reprod 2006;21:1143-53. https://doi.org/10.1093/humrep/dei480
  36. Caglayan E, Romeo GR, Kappert K, Odenthal M, Sudkamp M, Body SC, et al. Profilin-1 is expressed in human atherosclerotic plaques and induces atherogenic effects on vascular smooth muscle cells. PLoS One 2010;5:e13608. https://doi.org/10.1371/journal.pone.0013608
  37. Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J, et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001;166:7309-18. https://doi.org/10.4049/jimmunol.166.12.7309
  38. Menkhorst EM, Van Sinderen ML, Rainczuk K, Cuman C, Winship A, Dimitriadis E. Invasive trophoblast promote stromal fibroblast decidualization via Profilin 1 and ALOX5. Sci Rep 2017;7:8690. https://doi.org/10.1038/s41598-017-05947-0
  39. Liang X, Jin Y, Wang H, Meng X, Tan Z, Huang T, et al. Transgelin 2 is required for embryo implantation by promoting actin polymerization. FASEB J 2019;33:5667-75. https://doi.org/10.1096/fj.201802158rrr

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  1. Sperm Proteome after Interaction with Reproductive Fluids in Porcine: From the Ejaculation to the Fertilization Site vol.21, pp.17, 2020, https://doi.org/10.3390/ijms21176060