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Autocrine embryotropins revisited : how do embryos talk to each other in vitro when cultured in groups?

Eline Wydooghe UGent, Leen Vandaele UGent, Sonia Heras Garcia, Petra De Sutter UGent, Dieter Deforce UGent, Luc Peelman UGent, Catharina De Schauwer UGent and Ann Van Soom UGent (2017) BIOLOGICAL REVIEWS. 92(1). p.505-520
abstract
In the absence of the maternal genital tract, preimplantation embryos can develop in vitro in culture medium where all communication with the oviduct or uterus is absent. In several mammalian species, it has been observed that embryos cultured in groups thrive better than those cultured singly. Here we argue that group-cultured embryos are able to promote their own development in vitro by the production of autocrine embryotropins that putatively serve as a communication tool. The concept of effective communication implies an origin, a signalling agent, and finally a recipient that is able to decode the message. We illustrate this concept by demonstrating that preimplantation embryos are able to secrete autocrine factors in several ways, including active secretion, passive outflow, or as messengers bound to a molecular vehicle or transported within extracellular vesicles. Likewise, we broaden the traditional view that inter-embryo communication is dictated mainly by growth factors, by discussing a wide range of other biochemical messengers including proteins, lipids, neurotransmitters, saccharides, and microRNAs, all of which can be exchanged among embryos cultured in a group. Finally, we describe how different classes of messenger molecules are decoded by the embryo and influence embryo development by triggering different pathways. When autocrine embryotropins such as insulin-like growth factor-I (IGF-I) or platelet activating factor (PAF) bind to their appropriate receptor, the phosphatidylinositol-4,5-bisphosphate 3-kinase (PI3K) pathway will be activated which is important for embryo survival. On the other hand, the mitogen-activated protein kinase (MAPK) pathway is activated when compounds such as hyaluronic acid and serotonin bind to their respective receptors, thereby acting as growth factors. By activating the peroxisome-proliferator-activated receptor family (PPAR) pathway, lipophilic autocrine factors such as prostaglandins or fatty acids have both survival and anti-apoptotic functions. In conclusion, considering different types of messenger molecules simultaneously will be crucial to understanding more comprehensively how embryos communicate with each other in group-culture systems. This approach will assist in the development of novel media for single-embryo culture.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
in vitro fertilization, preimplantation embryo, autocrine factors, growth factors, group culture, survival factors, paracrine factors, inter-embryo communication, exosome, COLONY-STIMULATING FACTOR, PLATELET-ACTIVATING-FACTOR, EPIDERMAL-GROWTH-FACTOR, MOUSE PREIMPLANTATION EMBRYOS, LEUKEMIA INHIBITORY FACTOR, HUMAN FALLOPIAN-TUBE, INNER CELL MASS, FACTOR GM-CSF, ENDOMETRIAL EPITHELIAL-CELLS, MESSENGER RIBONUCLEIC-ACIDS
journal title
BIOLOGICAL REVIEWS
Biol. Rev.
volume
92
issue
1
pages
505 - 520
Web of Science type
Article
Web of Science id
000391937700027
ISSN
1464-7931
DOI
10.1111/brv.12241
language
English
UGent publication?
yes
classification
A1
additional info
the last two authors contributed equally to this manuscript
copyright statement
I have transferred the copyright for this publication to the publisher
id
7258280
handle
http://hdl.handle.net/1854/LU-7258280
date created
2016-06-17 10:53:04
date last changed
2017-02-27 11:49:13
@article{7258280,
  abstract     = {In the absence of the maternal genital tract, preimplantation embryos can develop in vitro in culture medium where all communication with the oviduct or uterus is absent. In several mammalian species, it has been observed that embryos cultured in groups thrive better than those cultured singly. Here we argue that group-cultured embryos are able to promote their own development in vitro by the production of autocrine embryotropins that putatively serve as a communication tool. The concept of effective communication implies an origin, a signalling agent, and finally a recipient that is able to decode the message. We illustrate this concept by demonstrating that preimplantation embryos are able to secrete autocrine factors in several ways, including active secretion, passive outflow, or as messengers bound to a molecular vehicle or transported within extracellular vesicles. Likewise, we broaden the traditional view that inter-embryo communication is dictated mainly by growth factors, by discussing a wide range of other biochemical messengers including proteins, lipids, neurotransmitters, saccharides, and microRNAs, all of which can be exchanged among embryos cultured in a group. Finally, we describe how different classes of messenger molecules are decoded by the embryo and influence embryo development by triggering different pathways. When autocrine embryotropins such as insulin-like growth factor-I (IGF-I) or platelet activating factor (PAF) bind to their appropriate receptor, the phosphatidylinositol-4,5-bisphosphate 3-kinase (PI3K) pathway will be activated which is important for embryo survival. On the other hand, the mitogen-activated protein kinase (MAPK) pathway is activated when compounds such as hyaluronic acid and serotonin bind to their respective receptors, thereby acting as growth factors. By activating the peroxisome-proliferator-activated receptor family (PPAR) pathway, lipophilic autocrine factors such as prostaglandins or fatty acids have both survival and anti-apoptotic functions. In conclusion, considering different types of messenger molecules simultaneously will be crucial to understanding more comprehensively how embryos communicate with each other in group-culture systems. This approach will assist in the development of novel media for single-embryo culture.},
  author       = {Wydooghe, Eline and Vandaele, Leen and Heras Garcia, Sonia and De Sutter, Petra and Deforce, Dieter and Peelman, Luc and De Schauwer, Catharina and Van Soom, Ann},
  issn         = {1464-7931},
  journal      = {BIOLOGICAL REVIEWS},
  keyword      = {in vitro fertilization,preimplantation embryo,autocrine factors,growth factors,group culture,survival factors,paracrine factors,inter-embryo communication,exosome,COLONY-STIMULATING FACTOR,PLATELET-ACTIVATING-FACTOR,EPIDERMAL-GROWTH-FACTOR,MOUSE PREIMPLANTATION EMBRYOS,LEUKEMIA INHIBITORY FACTOR,HUMAN FALLOPIAN-TUBE,INNER CELL MASS,FACTOR GM-CSF,ENDOMETRIAL EPITHELIAL-CELLS,MESSENGER RIBONUCLEIC-ACIDS},
  language     = {eng},
  number       = {1},
  pages        = {505--520},
  title        = {Autocrine embryotropins revisited : how do embryos talk to each other in vitro when cultured in groups?},
  url          = {http://dx.doi.org/10.1111/brv.12241},
  volume       = {92},
  year         = {2017},
}

Chicago
Wydooghe, Eline, Leen Vandaele, Sonia Heras García, Petra De Sutter, Dieter Deforce, Luc Peelman, Catharina De Schauwer, and Ann Van Soom. 2017. “Autocrine Embryotropins Revisited : How Do Embryos Talk to Each Other in Vitro When Cultured in Groups?” Biological Reviews 92 (1): 505–520.
APA
Wydooghe, E., Vandaele, L., Heras García, S., De Sutter, P., Deforce, D., Peelman, L., De Schauwer, C., et al. (2017). Autocrine embryotropins revisited : how do embryos talk to each other in vitro when cultured in groups? BIOLOGICAL REVIEWS, 92(1), 505–520.
Vancouver
1.
Wydooghe E, Vandaele L, Heras García S, De Sutter P, Deforce D, Peelman L, et al. Autocrine embryotropins revisited : how do embryos talk to each other in vitro when cultured in groups? BIOLOGICAL REVIEWS. 2017;92(1):505–20.
MLA
Wydooghe, Eline, Leen Vandaele, Sonia Heras García, et al. “Autocrine Embryotropins Revisited : How Do Embryos Talk to Each Other in Vitro When Cultured in Groups?” BIOLOGICAL REVIEWS 92.1 (2017): 505–520. Print.