Interaction of the EGFR signaling pathway with porcine cumulus oocyte complexes and oviduct cells in a coculture system

It has become increasingly recognized that coculture has a beneficial effect on the in vitro maturation (IVM) of oocytes and embryo development in many species. However, these effects of coculture on IVM have been documented only for their positive conditioning roles without any evidence on the precise mechanisms underlying the action of coculture systems on the development of cumulus oocyte complexes (COCs). It has been suggested that the epidermal growth factor receptor (EGFR) signaling pathway is important for development of COCs, mediated by several epidermal growth factor (EGF)‐like proteins with downstream mitogen‐activated protein kinase 1/3 signaling. Therefore, we hypothesized that canine oviduct cells (OCs) in a coculture system, which shows improvement of oocyte quality in several species, are associated with EGFR signaling by exposure to progesterone (P4; imitating its production before ovulation and its continuous increase while oocytes reside in the oviduct to complete maturation in dogs). We designed three experimental groups: control, OCs coculture exposed to P4, and OCs coculture without exposure to P4. The result showed that the OCs coculture exposed to P4 strongly expressed EGF‐like proteins and significantly improved COCs and subsequent embryo development. Furthermore, the expression of EGFR‐related genes in cumulus cells and GDF9 and BMP15 in oocytes was upregulated in the P4‐treated group. This study provides the first evidence that OCs exposed to P4 can induce strong expression of EGF‐like proteins, and OCs effectively mediate improved porcine COCs development and subsequent embryo development by altering EGFR signaling related mRNA expression.

[1]  M. Nowicki,et al.  “Biological Adhesion” is a Significantly Regulated Molecular Process during Long-Term Primary In Vitro Culture of Oviductal Epithelial Cells (Oecs): A Transcriptomic and Proteomic Study , 2019, International journal of molecular sciences.

[2]  Byeong-chun Lee,et al.  Effect of co-culture canine cumulus and oviduct cells with porcine oocytes during maturation and subsequent embryo development of parthenotes in vitro. , 2018, Theriogenology.

[3]  Byeong-chun Lee,et al.  Oocyte maturation-related gene expression in the canine oviduct, cumulus cells, and oocytes and effect of co-culture with oviduct cells on in vitro maturation of oocytes , 2017, Journal of Assisted Reproduction and Genetics.

[4]  A. Yousefi,et al.  The effect of conspecific ampulla oviductal epithelial cells during in vitro maturation on oocyte developmental competence and maturation-promoting factor (MPF) activity in sheep. , 2017, Theriogenology.

[5]  M. Saadat,et al.  Differential influence of ampullary and isthmic derived epithelial cells on zona pellucida hardening and in vitro fertilization in ovine. , 2016, Reproductive biology.

[6]  G. T. Sharma,et al.  Stem Cell Conditioned Media Contains Important Growth Factors and Improves In Vitro Buffalo Embryo Production , 2016, Animal biotechnology.

[7]  V. Labas,et al.  Progesterone Plays a Critical Role in Canine Oocyte Maturation and Fertilization1 , 2015, Biology of reproduction.

[8]  H. Clarke,et al.  Follicle-stimulating hormone regulates expression and activity of epidermal growth factor receptor in the murine ovarian follicle , 2014, Proceedings of the National Academy of Sciences.

[9]  R. Gilchrist,et al.  Amphiregulin co-operates with bone morphogenetic protein 15 to increase bovine oocyte developmental competence: effects on gap junction-mediated metabolite supply. , 2014, Molecular human reproduction.

[10]  M. Saint-Dizier,et al.  Folliculogenesis, ovulation and endocrine control of oocytes and embryos in the dog. , 2012, Reproduction in domestic animals = Zuchthygiene.

[11]  M. Blaha,et al.  Signaling pathways regulating FSH- and amphiregulin-induced meiotic resumption and cumulus cell expansion in the pig. , 2012, Reproduction.

[12]  D. Shi,et al.  Co-culture embedded in cumulus clumps promotes maturation of denuded oocytes and reconstructs gap junctions between oocytes and cumulus cells , 2012, Zygote.

[13]  M. Conti,et al.  Genetic Dissection of Epidermal Growth Factor Receptor Signaling during Luteinizing Hormone-Induced Oocyte Maturation , 2011, PloS one.

[14]  Byeong-chun Lee,et al.  The 9-Cis Retinoic Acid Signaling Pathway and Its Regulation of Prostaglandin-Endoperoxide Synthase 2 During In Vitro Maturation of Pig Cumulus Cell-Oocyte Complexes and Effects on Parthenogenetic Embryo Production1 , 2011, Biology of reproduction.

[15]  M. Saint-Dizier,et al.  The canine oocyte: uncommon features of in vivo and in vitro maturation. , 2011, Reproduction, fertility, and development.

[16]  A. Lange-Consiglio,et al.  Equine bone marrow mesenchymal or amniotic epithelial stem cells as feeder in a model for the in vitro culture of bovine embryos , 2010, Zygote.

[17]  J. T. Kim,et al.  Antioxidative effects of astaxanthin against nitric oxide-induced oxidative stress on cell viability and gene expression in bovine oviduct epithelial cell and the developmental competence of bovine IVM/IVF embryos. , 2010, Reproduction in domestic animals = Zuchthygiene.

[18]  D. Russell,et al.  Growth differentiation factor 9 signaling requires ERK1/2 activity in mouse granulosa and cumulus cells , 2010, Journal of Cell Science.

[19]  H. Fan,et al.  Beta-catenin (CTNNB1) promotes preovulatory follicular development but represses LH-mediated ovulation and luteinization. , 2010, Molecular endocrinology.

[20]  L. Spate,et al.  Porcine oocytes denuded before maturation can develop to the blastocyst stage if provided a cumulous cell-derived coculture system. , 2010, Journal of animal science.

[21]  M. Shimada,et al.  Progesterone is essential for maintenance of Tace/Adam17 mRNA expression, but not EGF-like factor, in cumulus cells, which enhances the EGF receptor signaling pathway during in vitro maturation of porcine COCs. , 2010, The Journal of reproduction and development.

[22]  Yitzhak Reizel,et al.  Sustained activity of the EGF receptor is an absolute requisite for LH-induced oocyte maturation and cumulus expansion. , 2010, Molecular endocrinology.

[23]  Stephen M. Hedrick,et al.  MAPK3/1 (ERK1/2) in Ovarian Granulosa Cells Are Essential for Female Fertility , 2009, Science.

[24]  K. Seow,et al.  Effects of growth factors and granulosa cell co-culture on in-vitro maturation of oocytes. , 2009, Reproductive biomedicine online.

[25]  M. Fu,et al.  Luteinizing hormone signaling in preovulatory follicles involves early activation of the epidermal growth factor receptor pathway. , 2008, Molecular endocrinology.

[26]  Hurng-Wern Huang,et al.  Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos. , 2008, Animal reproduction science.

[27]  J. Richards,et al.  Hormone-induced expression of tumor necrosis factor alpha-converting enzyme/A disintegrin and metalloprotease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor. , 2007, Endocrinology.

[28]  P. Mermillod,et al.  Effect of coculture with oviduct epithelial cells on viability after transfer of vitrified in vitro produced goat embryos. , 2007, Theriogenology.

[29]  A. Kaya,et al.  Developmental potential of bovine oocytes cultured in different maturation and culture conditions. , 2007, Animal reproduction science.

[30]  J. Opiela,et al.  Effects of oocyte quality, semen donor and embryo co-culture system on the efficiency of blastocyst production in goats. , 2007, Theriogenology.

[31]  R. Gilchrist,et al.  Oocyte-Secreted Factor Activation of SMAD 2/3 Signaling Enables Initiation of Mouse Cumulus Cell Expansion1 , 2007, Biology of reproduction.

[32]  Nicolas M Orsi,et al.  Mammalian embryo co-culture: trials and tribulations of a misunderstood method. , 2007, Theriogenology.

[33]  D. Threadgill,et al.  Luteinizing Hormone-Dependent Activation of the Epidermal Growth Factor Network Is Essential for Ovulation , 2006, Molecular and Cellular Biology.

[34]  J. Richards,et al.  Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. , 2006, Molecular endocrinology.

[35]  M. Conti,et al.  Role of the Epidermal Growth Factor Network in Ovarian Follicles the Physiology of Follicle Maturation and Ovulation , 2022 .

[36]  M. Nasr-Esfahani,et al.  Can Vero cell co-culture improve in-vitro maturation of bovine oocytes? , 2006, Reproductive biomedicine online.

[37]  S. Hammes,et al.  Epidermal growth factor receptor signaling is required for normal ovarian steroidogenesis and oocyte maturation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Goo Jang,et al.  Dogs cloned from adult somatic cells , 2005, Nature.

[39]  J. Sha,et al.  Effects of type and state of co-culture cells on in-vitro development of porcine oocytes matured and fertilized in vitro , 2005, Journal of Assisted Reproduction and Genetics.

[40]  E. Chorev,et al.  Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocyte maturation in rat ovarian follicles. , 2005, Endocrinology.

[41]  M. Conti,et al.  Epidermal growth factor family members: endogenous mediators of the ovulatory response. , 2005, Endocrinology.

[42]  G. Luvoni,et al.  Factors involved in vivo and in vitro maturation of canine oocytes. , 2005, Theriogenology.

[43]  L. Němcová,et al.  Expression of Growth Differentiation Factor 9 Messenger RNA in Porcine Growing and Preovulatory Ovarian Follicles1 , 2004, Biology of reproduction.

[44]  K. Miyamoto,et al.  Expression of epiregulin and amphiregulin in the rat ovary. , 2004, Journal of molecular endocrinology.

[45]  K. Mackie,et al.  Effect of ammonium chloride on the growth and metabolism of bovine ovarian granulosa cells and the development of ovine oocytes matured in the presence of bovine granulosa cells previously exposed to ammonium chloride. , 2004, Animal reproduction science.

[46]  G. Weskamp,et al.  Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands , 2004, The Journal of cell biology.

[47]  S. Jin,et al.  EGF-Like Growth Factors As Mediators of LH Action in the Ovulatory Follicle , 2004, Science.

[48]  B. Colenbrander,et al.  The effect of oviductal epithelial cell co-culture during in vitro maturation on sow oocyte morphology, fertilization and embryo development. , 2003, Theriogenology.

[49]  R. Procházka,et al.  Epidermal Growth Factor-Receptor Tyrosine Kinase Activity Regulates Expansion of Porcine Oocyte-Cumulus Cell Complexes In Vitro1 , 2003, Biology of reproduction.

[50]  J. Richards,et al.  Temporal and Spatial Patterns of Ovarian Gene Transcription Following an Ovulatory Dose of Gonadotropin in the Rat1 , 2002, Biology of reproduction.

[51]  K. Wigglesworth,et al.  Printed in U.S.A. Copyright © 2002 by The Endocrine Society Mitogen-Activated Protein Kinase Activity in Cumulus Cells Is Essential for Gonadotropin-Induced Oocyte Meiotic Resumption and Cumulus Expansion in the Mouse , 2022 .

[52]  J. Juengel,et al.  Bmp15 mutations and ovarian function , 2002, Molecular and Cellular Endocrinology.

[53]  J. Eppig,et al.  Oocyte control of ovarian follicular development and function in mammals. , 2001, Reproduction.

[54]  J. Fléchon,et al.  Developmental regulation of effect of epidermal growth factor on porcine oocyte–cumulus cell complexes: Nuclear maturation, expansion, and F‐actin remodeling , 2000, Molecular reproduction and development.

[55]  G. England,et al.  Synthetic oviductal fluid and oviductal cell coculture for canine oocyte maturation in vitro. , 1999, Animal reproduction science.

[56]  J. Cohen,et al.  The application of co-culture in assisted reproduction: 10 years of experience with human embryos. , 1998, Human reproduction.

[57]  E. Sarıdoğan,et al.  Human Fallopian tube epithelial cell co-culture increases fertilization rates in male factor infertility but not in tubal or unexplained infertility. , 1997, Human reproduction.

[58]  David F. Albertini,et al.  Growth differentiation factor-9 is required during early ovarian folliculogenesis , 1996, Nature.

[59]  M. Freeman,et al.  Granulosa cell co-culture enhances human embryo development and pregnancy rate following in-vitro fertilization. , 1995 .

[60]  S. Ratnam,et al.  The search for improved in-vitro systems should not be ignored: embryo co-culture may be one of them. , 1993, Human reproduction.

[61]  B. Vanderhyden,et al.  Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. , 1990, Developmental biology.