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Intracellular Ca2+ Signaling and Preimplantation Development

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Book cover Cell Signaling During Mammalian Early Embryo Development

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 843))

Abstract

The key, versatile role of intracellular Ca2+ signaling during egg activation after fertilization has been appreciated for several decades. More recently, evidence has accumulated supporting the concept that cytoplasmic Ca2+ is also a major signaling nexus during subsequent development of the fertilized ovum. This chapter will review the molecular reactions that regulate intracellular Ca2+ levels and cell function, the role of Ca2+ signaling during egg activation and specific examples of repetitive Ca2+ signaling found throughout pre- and peri-implantation development. Many of the upstream and downstream pathways utilized during egg activation are also critical for specific processes that take place during embryonic development. Much remains to be done to elucidate the full complexity of Ca2+ signaling mechanisms in preimplantation embryos to the level of detail accomplished for egg activation. However, an emerging concept is that because this second messenger can be modulated downstream of numerous receptors and is able to bind and activate multiple cytoplasmic signaling proteins, it can help the coordination of development through up- and downstream pathways that change with each embryonic stage.

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References

  • Armant DR. Blastocysts don’t go it alone. Extrinsic signals fine-tune the intrinsic developmental program of trophoblast cells. Dev Biol. 2005;280(2):260–80.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Armant DR. Blastocyst culture. In: Soares MJ, Hunt JS, editors. Placenta and trophoblast methods and protocols, vol 1. Methods in molecular medicine. Totowa: Humana Press; 2006. pp. 35–56.

    Google Scholar 

  • Armant DR. Life and death responses to trophinin-mediated adhesion during blastocyst implantation. Cell Cycle. 2011;10(4):574–5.

    CAS  PubMed  Google Scholar 

  • Armant DR, Saunders DE. Exposure of embryonic cells to alcohol: contrasting effects during preimplantation and postimplantation development. Semin Perinatol. 1996;20:127–39.

    CAS  PubMed  Google Scholar 

  • Armant DR, Wang J, Liu Z. Intracellular signaling in the developing blastocyst as a consequence of the maternal-embryonic dialogue. Semin Reprod Med. 2000;18(3):273–87.

    CAS  PubMed  Google Scholar 

  • Ashby MC, Tepikin AV. Polarized calcium and calmodulin signaling in secretory epithelia. Physiol Rev. 2002;82(3):701–34. doi:10.1152/physrev.00006.2002.

    CAS  PubMed  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nature Rev Mol Cell Biol. 4(7):517–29. doi:10.1038/nrm1155.

    CAS  Google Scholar 

  • Blankenship TN, Given RL. Penetration of the uterine epithelial basement membrane during blastocyst implantation in the mouse. Anat Rec. 1992;233:196–204.

    CAS  PubMed  Google Scholar 

  • Brison DR, Schultz RM. Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biol Reprod. 1997;56(5):1088–96.

    CAS  PubMed  Google Scholar 

  • Brison DR, Schultz RM. Increased incidence of apoptosis in transforming growth factor alpha-deficient mouse blastocysts. Biol Reprod. 1998;59(1):136–44.

    CAS  PubMed  Google Scholar 

  • Campbell K, Swann K. Ca2+ oscillations stimulate an ATP increase during fertilization of mouse eggs. Dev Biol. 2006;298(1):225–33. doi:10.1016/j.ydbio.2006.06.032.

    CAS  PubMed  Google Scholar 

  • Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, Yoshinaga K. Embryo Implantation. Dev Biol. 2000;223(2):217–37.

    CAS  PubMed  Google Scholar 

  • Chamberlain LH, Roth D, Morgan A, Burgoyne RD. Distinct effects of alpha-SNAP, 14-3-3 proteins, and calmodulin on priming and triggering of regulated exocytosis. J Cell Biol. 1995;130(5):1063–70.

    CAS  PubMed  Google Scholar 

  • Chason RJ, Csokmay J, Segars JH, Decherney AH, Armant DR. Environmental and epigenetic effects upon preimplantation embryo metabolism and development. Trends Endocrinol Metab. 2011;22(10):412–20. doi:10.1016/j.tem.2011.05.005.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chen YA, Duvvuri V, Schulman H, Scheller RH. Calmodulin and protein kinase C increase Ca(2+)-stimulated secretion by modulating membrane-attached exocytic machinery. J Biol Chem. 1999;274(37):26469–76.

    CAS  PubMed  Google Scholar 

  • Cockburn K, Rossant J. Making the blastocyst: lessons from the mouse. J Clin Invest. 2010;120(4):995–1003. doi:10.1172/JCI41229.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cuthbertson KS, Whittingham DG, Cobbold PH. Free calcium increases in exponential phases during mouse oocyte activation. Nature (London). 1981;294:754–7.

    CAS  Google Scholar 

  • Damsky CH, Librach C, Lim KH, Fitzgerald ML, McMaster MT, Janatpour M, Zhou Y, Logan SK, Fisher SJ. Integrin switching regulates normal trophoblast invasion. Development. 1994;120:3657–66.

    CAS  PubMed  Google Scholar 

  • Das SK, Wang XN, Paria BC, Damm D, Abraham JA, Klagsbrun M, Andrews GK, Dey SK. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development. 1994;120:1071–83.

    CAS  PubMed  Google Scholar 

  • DeChiara TM, Efstratiadis A, Robertson EJ. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature (London). 1990;345:78–80.

    CAS  Google Scholar 

  • Deguchi R, Shirakawa H, Oda S, Mohri T, Miyazaki S. Spatiotemporal analysis of Ca(2+) waves in relation to the sperm entry site and animal-vegetal axis during Ca(2+) oscillations in fertilized mouse eggs. Dev Biol. 2000;218(2):299–313.

    CAS  PubMed  Google Scholar 

  • Ding YQ, Zhu LJ, Bagchi MK, Bagchi IC. Progesterone stimulates calcitonin gene expression in the uterus during implantation. Endocrinology. 1994;135:2265–74.

    CAS  PubMed  Google Scholar 

  • Ducibella T. The cortical reaction and development of activation competence in mammalian oocytes. Hum Reprod Update. 1996;2(1):29–42.

    CAS  PubMed  Google Scholar 

  • Ducibella T, Anderson E. Cell shape and membrane changes in the eight-cell mouse embryo: prerequisites for morphogenesis of the blastocyst. Dev Biol. 1975;47(1):45–58.

    CAS  PubMed  Google Scholar 

  • Ducibella T, Fissore R. The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol. 2008;315(2):257–79. doi:10.1016/j.ydbio.2007.12.012.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ducibella T, Huneau D, Angelichio E, Xu Z, Schultz RM, Kopf GS, Fissore R, Madoux S, Ozil JP. Egg-to-embryo transition is driven by differential responses to Ca(2+) oscillation number. Dev Biol. 2002;250(2):280–91.

    CAS  PubMed  Google Scholar 

  • Dumollard R, Carroll J, Dupont G, Sardet C. Calcium wave pacemakers in eggs. J Cell Sci. 2002;115(18):3557–64.

    CAS  PubMed  Google Scholar 

  • Dumollard R, Marangos P, Fitzharris G, Swann K, Duchen M, Carroll J. Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development. 2004;131(13):3057–67. doi:10.1242/dev.01181.

    CAS  PubMed  Google Scholar 

  • Emerson M, Travis AR, Bathgate R, Stojanov T, Cook DI, Harding E, Lu DP, O’Neill C. Characterization and functional significance of calcium transients in the 2-cell mouse embryo induced by an autocrine growth factor. J Biol Chem. 2000;275(29):21905–13.

    CAS  PubMed  Google Scholar 

  • Gardner DK, Lane M, Spitzer A, Batt PA. Enhanced rates of cleavage and development for sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins, and culturing embryos in groups stimulate development. Biol Reprod. 1994;50:390–400.

    CAS  PubMed  Google Scholar 

  • Giancotti FG, Ruoslahti E. Integrin signaling. Science (WashDC). 1999;285(5430):1028–32.

    CAS  Google Scholar 

  • Halet G, Tunwell R, Parkinson SJ, Carroll J. Conventional PKCs regulate the temporal pattern of Ca2+ oscillations at fertilization in mouse eggs. J Cell Biol. 2004;164(7):1033–44. doi:10.1083/jcb.200311023.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hamatani T, Daikoku T, Wang H, Matsumoto H, Carter MG, Ko MS, Dey SK. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc Natl Acad Sci U S A. 2004;101(28):10326–31.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hannigan JH, Armant DR. Alcohol in pregnancy and neonatal outcome. Semin Neonatol. 2000;5(3):243–54.

    CAS  PubMed  Google Scholar 

  • Hirano S, Nose A, Hatta K, Kawakami A, Takeichi M. Calcium-dependent cell-cell adhesion molecules (cadherins): subclass specificities and possible involvement of actin bundles. J Cell Biol. 1987;105(6 Pt 1):2501–10.

    CAS  PubMed  Google Scholar 

  • Holbro T, Hynes NE. ErbB receptors: directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol. 2004;44:195–217.

    CAS  PubMed  Google Scholar 

  • Honda Z, Ishii S, Shimizu T. Platelet-activating factor receptor. J Biochem. 2002;131(6):773–9.

    CAS  PubMed  Google Scholar 

  • Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992;69:11–25.

    CAS  PubMed  Google Scholar 

  • Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002;110(6):673–87.

    CAS  PubMed  Google Scholar 

  • Jin XL, O’Neill C. The presence and activation of two essential transcription factors (cAMP response element-binding protein and cAMP-dependent transcription factor ATF1) in the two-cell mouse embryo. Biol Reprod. 2010;82(2):459–68. doi:10.1095/biolreprod.109.078758.

    CAS  PubMed  Google Scholar 

  • Jones NP, Peak J, Brader S, Eccles SA, Katan M. PLCgamma1 is essential for early events in integrin signalling required for cell motility. J Cell Sci. 2005;118(12):2695–706.

    CAS  PubMed  Google Scholar 

  • Kashir J, Heindryckx B, Jones C, De Sutter P, Parrington J, Coward K. Oocyte activation, phospholipase C zeta and human infertility. Hum Reprod Update. 2010;16(6):690–703. doi:10.1093/humupd/dmq018.

    CAS  PubMed  Google Scholar 

  • Kline JT, Kline D. Regulation of intracellular calcium in the mouse egg: evidence for inositol trisphosphate-induced calcium release, but not calcium-induced calcium release. Biol Reprod. 1994;50:193–203.

    CAS  PubMed  Google Scholar 

  • Leach RE, Stachecki JJ, Armant DR. Development of in vitro fertilized mouse embryos exposed to ethanol during the preimplantation period: accelerated embryogenesis at subtoxic levels. Teratology. 1993;47:57–64.

    CAS  PubMed  Google Scholar 

  • Leach RE, Rout UK, Schultz JF, Saunders DE, Armant DR. Ethanol elevates c-Myc levels in cultured mouse preimplantation embryos. Alcohol Clin Exp Res. 1999;23:778–84.

    CAS  PubMed  Google Scholar 

  • Liu Z, Armant DR. Lysophosphatidic acid regulates murine blastocyst development by transactivation of receptors for heparin-binding EGF-like growth factor. Exp Cell Res. 2004;296(2):317–26.

    CAS  PubMed  Google Scholar 

  • Liu L, Hammar K, Smith PJ, Inoue S, Keefe DL. Mitochondrial modulation of calcium signaling at the initiation of development. Cell Calcium. 2001;30(6):423–33. doi:10.1054/ceca.2001.0251.

    CAS  PubMed  Google Scholar 

  • Lorca T, Abrieu A, Means A, Doree M. Calcium is involved through type II calmodulin-dependent protein kinase in cyclin degradation and exit from metaphase. Biochim Biophys Acta. 1994;1223:325–32.

    CAS  PubMed  Google Scholar 

  • Lu KP, Means AR. Regulation of the cell cycle by calcium and calmodulin. Endocr Rev. 1993;14:40–58.

    CAS  PubMed  Google Scholar 

  • Lu DP, Li Y, Bathgate R, Day M, O'Neill C. Ligand-activated signal transduction in the 2-cell embryo. Biol Reprod. 2003;69(1):106–16.

    CAS  PubMed  Google Scholar 

  • Lu DP, Chandrakanthan V, Cahana A, Ishii S, O’Neill C. Trophic signals acting via phosphatidylinositol-3 kinase are required for normal pre-implantation mouse embryo development. J Cell Sci. 2004;117(8):1567–76.

    CAS  PubMed  Google Scholar 

  • Madgwick S, Levasseur M, Jones KT (2005) Calmodulin-dependent protein kinase II, and not protein kinase C, is sufficient for triggering cell-cycle resumption in mammalian eggs. J Cell Sci. 118(Pt 17):3849–59. doi:10.1242/jcs.02506

    CAS  PubMed  Google Scholar 

  • Margolis B, Rhee SG, Felder S, Mervic M, Lyall R, Levitzki A, Ullrich A, Zilberstein A, Schlessinger J. EGF induces tyrosine phosphorylation of phospholipase C-II: a potential mechanism for EGF receptor signaling. Cell. 1989;57(7):1101–7.

    CAS  PubMed  Google Scholar 

  • Martin TJ, Findlay DM, Houssami S, Ikegame M, Rakopoulos M, Moseley JM, Sexton PM (1995) Heterogeneity of the calcitonin receptor: functional aspects in osteoclasts and other sites. J Nutr. 125(7 Suppl):2009S–14S

    Google Scholar 

  • Meisenhelder J, Suh PG, Rhee SG, Hunter T. Phospholipase C-gamma is a substrate for the PDGF and EGF receptor protein-tyrosine kinases in vivo and in vitro. Cell. 1989;57(7):1109–22.

    CAS  PubMed  Google Scholar 

  • Miao YL, Williams CJ. Calcium signaling in mammalian egg activation and embryo development: the influence of subcellular localization. Mol Reprod Dev. 2012;79(11):742–56. doi:10.1002/mrd.22078.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miyazaki S, Shirakawa H, Nakada K, Honda Y. Essential role of the inositol 1,4,5-trisphosphate receptor/calcium release channel in calcium waves and calcium oscillations at fertilization of mammalian eggs. Dev Biol. 1993;158:62–78.

    CAS  PubMed  Google Scholar 

  • Muik M, Schindl R, Fahrner M, Romanin C. Ca2+ release-activated Ca2+ (CRAC) current, structure, and function. Cell Mol Life Sci. 2012;69(24):4163–76. doi:10.1007/s00018-012-1072-8.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nixon VL, Levasseur M, McDougall A, Jones KT. Ca2+ oscillations promote APC/C-dependent cyclin B1 degradation during metaphase arrest and completion of meiosis in fertilizing mouse eggs. Curr Biol. 2002;12(9):746–50.

    CAS  PubMed  Google Scholar 

  • O’Neill C. Evidence for the requirement of autocrine growth factors for development of mouse preimplantation embryos in vitro. Biol Reprod. 1997;56(1):229–37.

    PubMed  Google Scholar 

  • O’Neill C. Autocrine mediators are required to act on the embryo by the 2-cell stage to promote normal development and survival of mouse preimplantation embryos in vitro. Biol Reprod. 1998;58(5):1303–9.

    PubMed  Google Scholar 

  • O’Neill C, Li Y, Jin XL. Survival signaling in the preimplantation embryo. Theriogenology. 2012;77(4):773–84. doi:10.1016/j.theriogenology.2011.12.016.

    PubMed  Google Scholar 

  • Ohsugi M, Ohsawa T, Yamamura H. Involvement of protein kinase C in nuclear migration during compaction and the mechanism of the migration: analyses in two- cell mouse embryos. Dev Biol. 1993;156:146–54.

    CAS  PubMed  Google Scholar 

  • Ohsugi M, Yamamura H, Semba R, Hidaka H. Immunocytochemical detection of Ca(2+)-dependent subspecies of protein kinase C in mouse embryos before and during compaction. Histochem J. 1994;26:641–3.

    CAS  PubMed  Google Scholar 

  • Ohsugi M, Larue L, Schwarz H, Kemler R. Cell-junctional and cytoskeletal organization in mouse blastocysts lacking E-cadherin. Dev Biol. 1997;185(2):261–71.

    CAS  PubMed  Google Scholar 

  • Palmieri SL, Payne J, Stiles CD, Biggers JD, Mercola M. Expression of mouse PDGF-A and PDGF alpha-receptor genes during pre- and post-implantation development: evidence for a developmental shift from an autocrine to a paracrine mode of action. Mech Dev. 1992;39(3):181–91.

    CAS  PubMed  Google Scholar 

  • Parekh AB, Putney JW Jr. Store-operated calcium channels. Physiol Rev. 2005;85(2):757–810. doi:10.1152/physrev.00057.2003.

    CAS  PubMed  Google Scholar 

  • Paria BC, Dey SK. Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc Natl Acad Sci U S A. 1990;87:4756–60.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Paria BC, Dey SK, Andrews GK. Antisense c-myc effects on preimplantation mouse embryo development. Proc Natl Acad Sci U S A. 1992;89:10051–5.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK, Hogan BL. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci U S A. 2001;98(3):1047–52.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Parr EL, Tung HN, Parr MB. Apoptosis as the mode of uterine epithelial cell death during embryo implantation in mice and rats. Biol Reprod. 1987;36(1):211–25.

    CAS  PubMed  Google Scholar 

  • Peters C, Mayer A. Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature (London). 1998;396(6711):575–80.

    CAS  Google Scholar 

  • Pey R, Vial C, Schatten G, Hafner M. Increase of intracellular Ca2+ and relocation of E-cadherin during experimental decompaction of mouse embryos. Proc Natl Acad Sci U S A. 1998;95(22):12977–82.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Quetglas S, Leveque C, Miquelis R, Sato K, Seagar M. Ca2+-dependent regulation of synaptic SNARE complex assembly via a calmodulin- and phospholipid-binding domain of synaptobrevin. Proc Natl Acad Sci U S A. 2000;97(17):9695–700.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Raab G, Kover K, Paria BC, Dey SK, Ezzell RM, Klagsbrun M. Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor. Development. 1996;122(2):637–45.

    CAS  PubMed  Google Scholar 

  • Rappolee DA, Brenner CA, Schultz R, Mark D, Werb Z. Developmental expression of PDGF, TGF-alpha, and TGF-beta genes in preimplantation mouse embryos. Science (WashDC). 1988;241:1823–5.

    CAS  Google Scholar 

  • Rebecchi MJ, Pentyala SN. Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev. 2000;80(4):1291–335.

    CAS  PubMed  Google Scholar 

  • Rout UK, Krawetz SA, Armant DR. Ethanol-induced intracellular calcium mobilization rapidly alters gene expression in the mouse blastocyst. Cell Calcium. 1997;22:463–74.

    CAS  PubMed  Google Scholar 

  • Rout UK, Wang J, Paria BC, Armant DR. alpha5beta1, alphaVbeta3 and the platelet-associated integrin alphaIIbbeta3 coordinately regulate adhesion and migration of differentiating mouse trophoblast cells. Dev Biol. 2004;268(1):135–51.

    CAS  PubMed  Google Scholar 

  • Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA. PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development. 2002;129(15):3533–44.

    CAS  PubMed  Google Scholar 

  • Schultz JF, Armant DR. Beta1- and beta3-class integrins mediate fibronectin binding activity at the surface of developing mouse peri-implantation blastocysts. Regulation by ligand-induced mobilization of stored receptor. J Biol Chem. 1995;270:11522–31.

    CAS  PubMed  Google Scholar 

  • Schultz GA, Heyner S. Gene expression in pre-implantation mammalian embryos. Mutat Res. 1992;296:17–31.

    CAS  PubMed  Google Scholar 

  • Schultz RM, Kopf GS. Molecular basis of mammalian egg activation. Curr Top Dev Biol. 1995;30:21–62.

    CAS  PubMed  Google Scholar 

  • Stachecki JJ, Armant DR. Regulation of blastocoele formation by intracellular calcium release is mediated through a phospholipase C-dependent pathway. Biol Reprod. 1996a;55:1292–8.

    CAS  PubMed  Google Scholar 

  • Stachecki JJ, Armant DR. Transient release of calcium from inositol 1,4,5-trisphosphate- specific stores regulates mouse preimplantation development. Development. 1996b;122:2485–96.

    CAS  PubMed  Google Scholar 

  • Stachecki JJ, Yelian FD, Leach RE, Armant DR. Mouse blastocyst outgrowth and implantation rates following exposure to ethanol or A23187 during culture in vitro. J Reprod Fertil. 1994a;101:611–7.

    CAS  PubMed  Google Scholar 

  • Stachecki JJ, Yelian FD, Schultz JF, Leach RE, Armant DR. Blastocyst cavitation is accelerated by ethanol- or ionophore- induced elevation of intracellular calcium. Biol Reprod. 1994b;50:1–9.

    CAS  PubMed  Google Scholar 

  • Sugihara K, Sugiyama D, Byrne J, Wolf DP, Lowitz KP, Kobayashi Y, Kabir-Salmani M, Nadano D, Aoki D, Nozawa S, Nakayama J, Mustelin T, Ruoslahti E, Yamaguchi N, Fukuda MN. Trophoblast cell activation by trophinin ligation is implicated in human embryo implantation. Proc Natl Acad Sci U S A. 2007;104(10):3799–804. doi:0611516104 [pii]10.1073/pnas.0611516104.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Swann K, Lai FA. PLCzeta and the initiation of Ca2+ oscillations in fertilizing mammalian eggs. Cell Calcium. 2013;53(1):55–62. doi:10.1016/j.ceca.2012.11.001.

    CAS  PubMed  Google Scholar 

  • Tamura N, Sugihara K, Akama TO, Fukuda MN. Trophinin-mediated cell adhesion induces apoptosis of human endometrial epithelial cells through PKC-delta. Cell Cycle. 2011;10(1):135–43. doi:14448 [pii].

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tokumura A, Yamano S, Aono T, Fukuzawa K. Lysophosphatidic acids produced by lysophospholipase D in mammalian serum and body fluid. Ann NY Acad Sci. 2000;905:347–50.

    CAS  PubMed  Google Scholar 

  • Tsien RY. Fluorescence measurement and photochemical manipulation of cytosolic free calcium. Trends Neurosci. 1988;11(10):419–24.

    CAS  PubMed  Google Scholar 

  • Tsien RW, Tsien RY. Calcium channels, stores, and oscillations. Annu Rev Cell Biol. 1990;6:715–60.

    CAS  PubMed  Google Scholar 

  • Tvorogov D, Wang XJ, Zent R, Carpenter G. Integrin-dependent PLC-gamma1 phosphorylation mediates fibronectin-dependent adhesion. J Cell Sci. 2005;118(3):601–10.

    CAS  PubMed  Google Scholar 

  • Umata T, Hirata M, Takahashi T, Ryu F, Shida S, Takahashi Y, Tsuneoka M, Miura Y, Masuda M, Horiguchi Y, Mekada E. A dual signaling cascade that regulates the ectodomain shedding of heparin-binding epidermal growth factor-like growth factor. J Biol Chem. 2001;276(32): 30475–82.

    CAS  PubMed  Google Scholar 

  • Wakai T, Fissore RA. Ca2+ homeostasis and regulation of ER Ca2+ in mammalian oocytes/eggs. Cell Calcium. 2013;53(1):63–7. doi:10.1016/j.ceca.2012.11.010.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wakai T, Zhang N, Vangheluwe P, Fissore RA. Regulation of endoplasmic reticulum Ca2+ oscillations in mammalian eggs. J Cell Sci. 2013. doi:10.1242/jcs.136549.

    Google Scholar 

  • Wang J, Armant DR. Integrin-mediated adhesion and signaling during blastocyst implantation. Cells Tissues Organs. 2002;172(3):190–201.

    CAS  PubMed  Google Scholar 

  • Wang J, Rout UK, Bagchi IC, Armant DR. Expression of calcitonin receptors in mouse preimplantation embryos and their function in the regulation of blastocyst differentiation by calcitonin. Development. 1998;125(21):4293–302.

    CAS  PubMed  Google Scholar 

  • Wang J, Mayernik L, Schultz JF, Armant DR. Acceleration of trophoblast differentiation by heparin-binding EGF-like growth factor is dependent on the stage-specific activation of calcium influx by ErbB receptors in developing mouse blastocysts. Development. 2000;127(1):33–44.

    CAS  PubMed  Google Scholar 

  • Wang J, Mayernik L, Armant DR. Integrin signaling regulates blastocyst adhesion to fibronectin at implantation: intracellular calcium transients and vesicle trafficking in primary trophoblast cells. Dev Biol. 2002;245(2):270–9.

    CAS  PubMed  Google Scholar 

  • Wang H, Matsumoto H, Guo Y, Paria BC, Roberts RL, Dey SK. Differential G protein-coupled cannabinoid receptor signaling by anandamide directs blastocyst activation for implantation. Proc Natl Acad Sci U S A. 2003;100(25):14914–9.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wang J, Mayernik L, Armant DR. Trophoblast adhesion of the peri-implantation mouse blastocyst is regulated by integrin signaling that targets phospholipase C. Dev Biol. 2007;302(1):143–53. doi:S0012-1606(06)01214-0 [pii]10.1016/j.ydbio.2006.09.015.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Watson SP, Auger JM, McCarty OJ, Pearce AC. GPVI and integrin alphaIIb beta3 signaling in platelets. J Thromb Haemost. 2005;3(8):1752–62.

    CAS  PubMed  Google Scholar 

  • Welsh AO, Enders AC. Chorioallantoic placenta formation in the rat: I. Luminal epithelial cell death and extracellular matrix modifications in the mesometrial region of implantation chambers. Am J Anat. 1991;192:215–31.

    CAS  PubMed  Google Scholar 

  • Wiley LM. Trophectoderm: the first epithelium to develop in the mammalian embryo. Scanning Microsc. 1988;2:417–26.

    CAS  PubMed  Google Scholar 

  • Wiley LM, Adamson ED, Tsark EC. Epidermal growth factor receptor function in early mammalian development. Bioessays. 1995;17(10):839–46.

    CAS  PubMed  Google Scholar 

  • Winkel GK, Ferguson JE, Takeichi M, Nuccitelli R. Activation of protein kinase C triggers premature compaction in the four-cell stage mouse embryo. Dev Biol. 1990;138:1–15.

    CAS  PubMed  Google Scholar 

  • Yoon SY, Jellerette T, Salicioni AM, Lee HC, Yoo MS, Coward K, Parrington J, Grow D, Cibelli JB, Visconti PE, Mager J, Fissore RA. Human sperm devoid of PLC, zeta 1 fail to induce Ca(2+) release and are unable to initiate the first step of embryo development. J Clin Invest. 2008;118(11):3671–81. doi:10.1172/JCI36942.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhou Y, Fisher SJ, Janatpour M, Genbacev O, Dejana E, Wheelock M, Damsky CH. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest. 1997;99:2139–51.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu LJ, Bagchi MK, Bagchi IC. Attenuation of calcitonin gene expression in pregnant rat uterus leads to a block in embryonic implantation. Endocrinology. 1998a;139:330–9.

    CAS  PubMed  Google Scholar 

  • Zhu LJ, Cullinan-Bove K, Polihronis M, Bagchi MK, Bagchi IC. Calcitonin is a progesterone-regulated marker that forecasts the receptive state of endometrium during implantation. Endocrinology. 1998b;139(9):3923–34.

    CAS  PubMed  Google Scholar 

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Acknowledgements

Supported in part by the Intramural Research Program of the National Institute for Child Health and Human Development, National Institutes of Health and grants from the NIH (HD067629) and the W.K. Kellogg Foundation.

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Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Wayne State University C.S. Mott Center for Human Growth and Development, 275 E. Hancock Street, 48201-1405, Detroit, MI, USA

    D. Randall Armant PhD

  2. Anatomy and Cell Biology, Wayne State University, Detroit, MI, USA

    D. Randall Armant PhD

  3. Program in Reproductive and Adult Endocrinology, NICHD, NIH, DHHS, 10 Center Drive, 20892-1103, Bethesda, MD, USA

    D. Randall Armant PhD

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  1. D. Randall Armant PhD
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Correspondence to D. Randall Armant PhD .

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Editors and Affiliations

  1. Hertford Building, Hull York Medical School University of Hull, Hull, United Kingdom

    Henry J. Leese

  2. St. Mary's Hospital Department of Reproductive Medicine, Central Manchester University Hospitals NHS Foundation Trust, Manchester, United Kingdom

    Daniel R. Brison

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Armant, D. (2015). Intracellular Ca2+ Signaling and Preimplantation Development. In: Leese, H., Brison, D. (eds) Cell Signaling During Mammalian Early Embryo Development. Advances in Experimental Medicine and Biology, vol 843. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2480-6_6

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