CELL RECEPTORS MEDIATING COMMUNICATION BETWEEN PREIMPLANTATION EMBRYO AND SURROUNDING ENVIRONMENT: CLUES FROM MOUSE AND RABBIT MODELS: A REVIEW

Authors

  • Štefan Čikoš Institute of Animal Physiology, Centre of Biosciences, SAS
  • Alexandra Spirkova Institute of Animal Physiology, Centre of Biosciences, SAS
  • Janka Kubandová Institute of Animal Physiology, Centre of Biosciences, SAS
  • Veronika Kovarikova Institute of Animal Physiology, Centre of Biosciences, SAS
  • Zuzana Sefcikova Institute of Animal Physiology, Centre of Biosciences, SAS
  • Dusan Fabian Institute of Animal Physiology, Centre of Biosciences, SAS
  • Juraj Koppel Institute of Animal Physiology, Centre of Biosciences, SAS

Keywords:

preimplantation embryo, cell receptors, embryo-maternal communication

Abstract

Preimplantation period of embryo development is one of the most sensitive phases in mammalian ontogeny, and disturbances at this developmental stage can result in poor pregnancy outcomes (in both embryos resulting from natural conception or from biotechnology procedures). Results of experimental studies have shown that maternal physiological condition and external environmental factors can significantly influence preimplantation embryo development, indicating a communication between the early embryo and its environment. The study of communication between the early embryo and surrounding environment has been mainly focused on protein signaling molecules such as growth factors and cytokines. However, small-molecule ligands, such as biogenic monoamines, have been shown to influence preimplantation embryo development as well, and results obtained in mouse and rabbit models indicate that biogenic monoamine receptors are expressed in preimplantation embryos. Several adrenergic, dopamine serotonin and histamine receptors were detected in mouse and rabbit ovulated oocytes and preimplantation embryos, and in mouse embryonic stem cells. Although the physiological role of biogenic monoamine receptors in early embryonic cells is not fully understood, experimental data indicate their involvement in the regulation of cell proliferation, differentiation and survival under physiological as well as unfavorable or pathological conditions (e.g. during maternal stress).

References

Amireault, P., & Dubé, F. (2005). Intracellular cAMP and calcium signaling by serotonin in mouse cumulus-oocyte complexes. Molecular Pharmacology, 68, 1678-1687.

Babeľová, J., Šefčíková, Z., Čikoš, Š., Špirková, A., Kovaříková, V., Koppel, J., Makarevich, A.V., Chrenek, P. & Fabian, D. (2017). Exposure to neonicotinoid insecticides induces embryotoxicity in mice and rabbits. Toxicology, 392, 71-80.

Burkuš, J., Čikoš Š., Fabian D., Kubandová J., Czikková, S. & Koppel, J. (2013). Maternal restraint stress negatively influences growth capacity of preimplantation mouse embryos. General Physiology and Biophysics, 32, 129–137.

Burkuš, J., Kačmarová, M., Kubandová, J., Kokošová, N., Fabianová, K., Fabian, D., Koppel, J. & Čikoš, Š. (2015). Stress exposure during the preimplantation period affects blastocyst lineages and offspring development. Journal of Reproduction and Development, 61, 325-31.

Chen, Q., Zhang, Y., Peng, H., Lei, L., Kuang, H., Zhang, L., Ning, L., Cao, Y. & Duan, E. (2011). Transient beta 2-adrenoceptor activation confers pregnancy loss by disrupting embryo spacing at implantation. Journal of Biological Chemistry 286, 4349–4356.

Čikoš, Š., Veselá, J., Iľková, G., Rehák, P., Czikková, S. & Koppel, J. (2005). Expression of beta adrenergic receptors in mouse oocytes and preimplantation embryos. Molecular Reproduction and Development, 71, 145-153.

Čikoš, Š., Rehák, P., Czikková, S., Veselá, J. & Koppel, J. (2007). Expression of adrenergic receptors in mouse preimplantation embryos and ovulated oocytes. Reproduction, 133, 1139-1147.

Čikoš, Š., Czikková, S., Chrenek, P., Makarevich, A.V., Burkuš, J., Janštová, Ž., Fabian, D. & Koppel, J. (2014). Expression of adrenergic receptors in bovine and rabbit oocytes and preimplantation embryos. Reproduction in Domestic Animals, 19:92-100.

Čikoš, Š., Fabian, D., Burkuš, J., Janštová, Ž. & Koppel, J. (2015). Expression of dopamine and adrenergic receptors in mouse embryonic stem cells and preimplantation embryos. Biologia, 70, 1263-1271.

Diskin, M.G. & Morfia, D.G. (2008). Embryonic and Early Foetal Losses in Cattle and Other Ruminants. Reproduction in Domestic Animals, 43 (Suppl.) 260–267.

Fabian, D., Bystriansky, J., Čikoš, S., Bukovská, A., Burkuš, J. & Koppel, J. (2010). The effect on preimplantation embryo development of non-specific inflammation localized outside the reproductive tract. Theriogenology, 74, 1652-1660.

Faherty, S., Fitzgerald, A., Keohan, M. & Quinlan, L.R. (2007). Selfrenewal and differentiation of mouse embryonic stem cells as measured by Oct4 expression: the role of the cAMP/PAK pathway. In Vitro Cellular & Developmental Biology - Animal, 43, 37–47.

Fischer, B., Chavatte-Palmer, P., Viebahn, C., Navarrete Santos, A. & Duranthon, V. (2012). Rabbit as a reproductive model for human health. Reproduction, 144, 1-10.

Fleming, T.P., Wilkins, A., Mears, A., Miller, D.J., Thomas, F., Ghassemifar, M.R., Fesenko, I., Sheth, B., Kwong, W.Y. & Eckert, J.J. (2004). Society for Reproductive Biology Founders' Lecture 2003. The making of an embryo: short-term goals and long-term implications. Reproduction and Fertility, 16, 325-337.

Hardy, K. & Spanos, S. (2002). Growth factor expression and function in the human and mouse preimplantation embryo. Journal of Endocrinology, 172, 221-36.

Henriquez, S., Tapia, A., Quezada, M., Vargas, M., Cardenas, H., Rios, M., Salvatierra, A.M., Croxatto, H., Orihuela, P., Zegers-Hochschild, F., Munroe, D.J. & Velasquez, L. (2006). Deficient expression of monoamine oxidace A in the endometrium is associated with implantation failure in women participating as recipients in oocyte donation. Molecular Human Reproduction, 12, 749–754.

Herlenius, E. & Lagercrantz, H. (2001). Neurotransmitters and neuromodulators during early human development. Early Human Development, 65, 21–37.

Humblot P. (2001). Use of pregnancy specific proteins and progesterone assays to monitor pregnancy and determine the timing, frequencies and sources of embryonic mortality in ruminants. Theriogenology, 56, 1417–1433.

Iľková, G., Rehák, P., Veselá, J., Čikoš, Š., Fabian, D., Czikková, S. & Koppel, J. (2004). Serotonin localization and its functional significance during mouse preimplantation embryo development. Zygote, 12, 205-213.

Janštová, Ž., Burkuš, J., Kubandová, J., Fabian, D., Koppel, J. & Čikoš Š. (2017). The effect of maternal stress on blastocyst quality depends on maternal physiological status. General Physiology and Biophysics, 36, 53-63.

Khatchadourian, C., Menezo, Y., Gerard, M. & Thibault, C. (1987). Catecholamines within the rabbit oviduct at fertilization time. Human Reproduction, 2, 1–5.

Khosla, S., Dean, W., Reik, W. & Feil R. (2001). Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Human Reproduction Update, 7, 419-27.

Kim, M.O., Na, S.I., Lee, M.Y., Heo, J.S. & Han H.J. (2008). Epinephrine increases DNA synthesis via ERK1/2s through cAMP, Ca2+/PKC, and PI3K/Akt signaling pathways in mouse embryonic stem cells. Journal of Cellular Biochemistry, 104, 1407–1420.

Krauss, G. (2014) Biochemistry of Signal Transduction and Regulation, 5th edn. Weinheim, Germany: Wiley-VCH Verlag GmbH.

Kubandová, J., Čikoš, S., Burkuš, J., Czikková, S., Koppel, J. & Fabian, D. (2014). Amount of maternal body fat significantly affected the quality of isolated mouse preimplantation embryos and slowed down their development. Theriogenology, 81, 187-195.

Kwong, W.Y., Wild, A.E., Roberts, P., Willis, A.C. & Fleming, T.P. (2000). Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development, 127, 4195–4202.

Layden B.T., Newman, M., Chen, F., Fisher, A. & Lowe W.L. Jr. (2010). G protein coupled receptors in embryonic stem cells: a role for Gs-α signaling. PLoS One 5: e9105.

Lee, M.Y., Heo, J.S. & Han H.J. (2006ň. Dopamine regulates cell cycle regulatory proteins via cAMP, Ca2+/PKC, MAPKs, and NF-κB in mouse embryonic stem cells. Journal of Cellular Physiology, 208, 399–406.

Markova, L.N., Sadykova, K.A. & Sakharova, N.I.U. (1990). The effect of biogenic monoamine antagonists on the development of preimplantation mouse embryos cultured in vitro. Zhurnal evoliutsionnoĭ biokhimii i fiziologii, 26,726–732.

Nepomnaschy, P.A.,Welch, K.B., McConnell, D.S., Low, B.S., Strassmann, B.I. & England, B.G. (2006). Cortisol levels and very early pregnancy loss in humans. Proceedings of

the National Academy of Sciences of the United States of America, 103, 3938–3942.

Pendleton, R.G., Rasheed, A., Roychowdhury, R. & Hillman, R., (1998). A new role for catecholamines: ontogenesis. Trends in Pharmacological Sciences, 19, 248–251.

Seeling, T., Čikoš, Š., Grybel, K.J., Janštová, Ž., Pendzialek, S.M., Schindler, M., Špirková, A. & Navarrete Santos, A. (2018). A Diabetic Pregnancy Alters the Expression of Stress-Related Receptors in Gastrulating Rabbit Blastocyst and in the Reproductive Tract. Reproductive Sciences, 25, 174-184.

Sun, F., Yang, X.J., Lv, H.Y., Tang, Y.B., An, S.M., Ding, X.P., Li, W.B., Teng, L., Shen, Y.. Chen, H.Z. & Zhu, L. (2015). β2- Adrenoreceptor-mediated proliferation inhibition of embryonic pluripotent stem cells. Journal of Cellular Physiology, 230, 2640–2646.

Tanaka, T.S., Kunath, T., Kimber, W.L., Jaradat, S.A., Stagg, C.A., Usuda, M., Yokota, T., Niwa, H., Rossant, J. & Ko, M.S. (2002). Gene expression profiling of embryo-derived stem cells reveals candidate genes associated with pluripotency and lineage specificity. Genome Research, 12, 1921–1928.

Tan, X.W., Ji, C.L., Zheng, L..L, Zhang, J., Yuan, H.J., Gong, S., Zhu, J. & Tan, J.H. (2017). Corticotrophin-releasing hormone and corticosterone impair development of preimplantation embryos by inducing oviductal cell apoptosis via activating the Fas system: an in vitro study. Human Reproduction, 32, 1583-1597.

Tang, F., Barbacioru, C., Bao, S., Lee, C., Nordman, E., Wang, X., Lao, K. & Surani, M.A. (2010). Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNASeq analysis. Cell Stem Cell, 6, 468–478.

Thouas, G.A., Dominguez, F., Green, M.P., Vilella, F., Simon, C. & Gardner, D.K. (2015). Soluble ligands and their receptors in human embryo development and implantation. Endocrine Reviews, 36, 92-130.

Ventura-Juncá, P., Irarrázaval, I., Rolle, A.J., Gutiérrez, J.I., Moreno, R.D. & Santos, M.J. (2015). In vitro fertilization (IVF) in mammals: epigenetic and developmental alterations. Scientific and bioethical implications for IVF in humans. Biological Research, 48, 68. doi: 10.1186/s40659-015-0059-y.

Veselá, J., Rehák, P., Mihalik, J., Czikková, S., Pokorný, J. &, Koppel, J. (2003). Expression of serotonin receptors in mouse oocytes and preimplantation embryos. Physiological Research, 52, 223-228.

Von Borell, E., Dobson, H. & Prunier, A. (2007). Stress, behaviour and reproductive performance in female cattle and pigs. Hormones and Behaviour, 52, 130–138.

Way, A.L., Barbato, G.F. & Killian, G.J. (2001) Identification of norepinephrine in bovine oviductal fluid by high performance liquid chromatography. Life Sciences, 70, 567–576.

Zhao, X., Ma, W., Das, S.K., Dey, S. & Paria, B.C. (2000). Blastocyst H2 receptor is the target for uterine histamine in implantation in the mouse. Development, 127, 2643-2651.

Zheng, L.L., Tan, X.W., Cui, X.Z., Yuan, H.J., Li, H., Jiao, G.Z., Ji, C.L. & Tan, J.H. (2016). Preimplantation maternal stress impairs embryo development by inducing oviductal apoptosis with activation of the Fas system. Molecular Human Reproduction, 22,778-790.

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Published

2019-03-29

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