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Functional significance of gap junctional coupling in preimplantation development

Functional significance of gap junctional coupling in preimplantation development
Functional significance of gap junctional coupling in preimplantation development
Gap junctional intercellular coupling allows cells to share low molecular weight metabolites and second messengers, thus facilitating homeostatic and developmental processes. Gap junctions make their appearance very early in rodent development, during compaction in the eight-cell stage. Surprisingly, preimplantation mouse embryos lacking the gap junction protein connexin 43 develop normally and establish full-term pregnancies despite severely reduced gap junctional coupling. It was suggested that this might be explained by the presence of at least five additional connexins known to be expressed in blastocysts. In the present study, we set out to clarify the number of connexins present in preimplantation rodent embryos and the role of gap junctional coupling, if any, in blastocyst development. We provide evidence from reverse transcription-polymerase chain reaction analysis that the genes encoding 3 additional connexins (connexin 30 or ß6, connexin 36 or 9, and connexin 57 or 10) are also transcribed in preimplantation mouse embryos. Furthermore, we show that multiple connexins are expressed in rat preimplantation embryos, indicating that multiplicity of connexin expression may be a common feature of early mammalian embryogenesis. We could detect no up-regulation of any of 3 coexpressed connexins examined in mouse embryos lacking connexin 43. Impaired intercellular coupling caused either by the loss of connexin 43 or by treatment of cultured embryos with the gap junctional coupling blocker 18-glycyrrhetinic acid (AGA) had no discernable effect on either apoptosis or glucose utilization, parameters known to be affected by gap junctional coupling in other contexts. These results, taken together with the reported inability of AGA to perturb blastocyst formation, imply that gap junctional coupling is not essential during this developmental period. We propose that connexin expression and the assembly of multiple types of gap junction channels in preimplantation embryos facilitates the diversification of communication pathways that will appear during postimplantation development. New evidence of this diversification is presented using rat blastocyst outgrowths.
biosynthesis, london, molecular weight, mice, utilization, signal transduction, blastocyst, in situ nick-end labeling, embryo, non-us government, physiology, up-regulation, gene expression regulation, female, glucose, connexins, metabolism, rats, acid, protein, analysis, communication, weight, direct, research support, pyruvic acid, apoptosis, drug effects, animals, gap junctions, developmental, pregnancy, role, fluorescent antibody technique, cytology, genes, genetics, reverse transcriptase polymerase chain reaction, immunohistochemistry
1403-1412
Houghton, F.D.
53946041-127e-45a8-9edb-bf4b3c23005f
Barr, K.J.
77ff83cc-83a3-4894-945f-56f342c2779c
Walter, G.
206b9c54-4d81-4703-9f18-df2c1ec78dc4
Gabriel, H.D.
8f754279-fb95-45ad-b83e-03622b36fc22
Grummer, R.
5f3e7377-51f3-493a-9133-00484011fed8
Traub, O.
a4b5977b-f280-4846-8b71-b5af02cab874
Leese, H J.
b44f6043-7a14-4c02-80e6-429ea8db6348
Winterhager, E.
f492ab4b-8c6b-49c9-898b-8ee2d5a4cd24
Kidder, G.M.
d6babdf4-43cc-4806-b0d0-d0c02088c4d9
Houghton, F.D.
53946041-127e-45a8-9edb-bf4b3c23005f
Barr, K.J.
77ff83cc-83a3-4894-945f-56f342c2779c
Walter, G.
206b9c54-4d81-4703-9f18-df2c1ec78dc4
Gabriel, H.D.
8f754279-fb95-45ad-b83e-03622b36fc22
Grummer, R.
5f3e7377-51f3-493a-9133-00484011fed8
Traub, O.
a4b5977b-f280-4846-8b71-b5af02cab874
Leese, H J.
b44f6043-7a14-4c02-80e6-429ea8db6348
Winterhager, E.
f492ab4b-8c6b-49c9-898b-8ee2d5a4cd24
Kidder, G.M.
d6babdf4-43cc-4806-b0d0-d0c02088c4d9

Houghton, F.D., Barr, K.J., Walter, G., Gabriel, H.D., Grummer, R., Traub, O., Leese, H J., Winterhager, E. and Kidder, G.M. (2002) Functional significance of gap junctional coupling in preimplantation development. Biology of Reproduction, 66 (5), 1403-1412.

Record type: Article

Abstract

Gap junctional intercellular coupling allows cells to share low molecular weight metabolites and second messengers, thus facilitating homeostatic and developmental processes. Gap junctions make their appearance very early in rodent development, during compaction in the eight-cell stage. Surprisingly, preimplantation mouse embryos lacking the gap junction protein connexin 43 develop normally and establish full-term pregnancies despite severely reduced gap junctional coupling. It was suggested that this might be explained by the presence of at least five additional connexins known to be expressed in blastocysts. In the present study, we set out to clarify the number of connexins present in preimplantation rodent embryos and the role of gap junctional coupling, if any, in blastocyst development. We provide evidence from reverse transcription-polymerase chain reaction analysis that the genes encoding 3 additional connexins (connexin 30 or ß6, connexin 36 or 9, and connexin 57 or 10) are also transcribed in preimplantation mouse embryos. Furthermore, we show that multiple connexins are expressed in rat preimplantation embryos, indicating that multiplicity of connexin expression may be a common feature of early mammalian embryogenesis. We could detect no up-regulation of any of 3 coexpressed connexins examined in mouse embryos lacking connexin 43. Impaired intercellular coupling caused either by the loss of connexin 43 or by treatment of cultured embryos with the gap junctional coupling blocker 18-glycyrrhetinic acid (AGA) had no discernable effect on either apoptosis or glucose utilization, parameters known to be affected by gap junctional coupling in other contexts. These results, taken together with the reported inability of AGA to perturb blastocyst formation, imply that gap junctional coupling is not essential during this developmental period. We propose that connexin expression and the assembly of multiple types of gap junction channels in preimplantation embryos facilitates the diversification of communication pathways that will appear during postimplantation development. New evidence of this diversification is presented using rat blastocyst outgrowths.

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More information

Published date: May 2002
Keywords: biosynthesis, london, molecular weight, mice, utilization, signal transduction, blastocyst, in situ nick-end labeling, embryo, non-us government, physiology, up-regulation, gene expression regulation, female, glucose, connexins, metabolism, rats, acid, protein, analysis, communication, weight, direct, research support, pyruvic acid, apoptosis, drug effects, animals, gap junctions, developmental, pregnancy, role, fluorescent antibody technique, cytology, genes, genetics, reverse transcriptase polymerase chain reaction, immunohistochemistry

Identifiers

Local EPrints ID: 24763
URI: http://eprints.soton.ac.uk/id/eprint/24763
PURE UUID: 3f353fdf-f6dd-4aa1-9a49-39188ad406de
ORCID for F.D. Houghton: ORCID iD orcid.org/0000-0002-5167-1694

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Date deposited: 06 Apr 2006
Last modified: 27 Apr 2022 01:49

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Contributors

Author: F.D. Houghton ORCID iD
Author: K.J. Barr
Author: G. Walter
Author: H.D. Gabriel
Author: R. Grummer
Author: O. Traub
Author: H J. Leese
Author: E. Winterhager
Author: G.M. Kidder

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