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Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition

Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition
Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition
Mammalian extra-embryonic lineages perform the crucial role of nutrient provision during gestation to support embryonic and fetal growth. These lineages derive from outer trophectoderm (TE) and internal primitive endoderm (PE) in the blastocyst and subsequently give rise to chorio-allantoic and visceral yolk sac placentae, respectively. We have shown maternal low protein diet exclusively during mouse preimplantation development (Emb-LPD) is sufficient to cause a compensatory increase in fetal and perinatal growth that correlates positively with increased adult-onset cardiovascular, metabolic and behavioural disease. Here, to investigate early mechanisms of compensatory nutrient provision, we assessed the influence of maternal Emb-LPD on endocytosis within extra-embryonic lineages using quantitative imaging and expression of markers and proteins involved. Blastocysts collected from Emb-LPD mothers within standard culture medium displayed enhanced TE endocytosis compared with embryos from control mothers with respect to the number and collective volume per cell of vesicles with endocytosed ligand and fluid and lysosomes, plus protein expression of megalin (Lrp2) LDL-family receptor. Endocytosis was also stimulated using similar criteria in the outer PE-like lineage of embryoid bodies formed from embryonic stem cell lines generated from Emb-LPD blastocysts. Using an in vitro model replicating the depleted amino acid (AA) composition found within the Emb-LPD uterine luminal fluid, we show TE endocytosis response is activated through reduced branched-chain AAs (leucine, isoleucine, valine). Moreover, activation appears mediated through RhoA GTPase signalling. Our data indicate early embryos regulate and stabilise endocytosis as a mechanism to compensate for poor maternal nutrient provision.
mouse embryo, trophectoderm, primitive endoderm, embryoid body, endocytosis, maternal diet, RhoA
1477-9129
1140-1150
Sun, C.
19650d2f-f387-444d-9874-1621763fcfd9
Velazquez, M.A.
706e7de5-8cdb-4f2b-b47d-128166bdbea4
Marfy-Smith, S.
acc55ea7-1323-4c38-8701-fefeee332230
Sheth, B.
2ca6ed58-a992-47b7-b3a5-3c5df82aada7
Cox, A.
93ffb38c-ff07-4e67-9403-264a6f72265e
Johnston, D.A.
b41163c9-b9d2-425c-af99-2a357204014e
Smyth, N.
0eba2a40-3b43-4d40-bb64-621bd7e9d505
Fleming, T.P.
2abf761a-e5a1-4fa7-a2c8-12e32d5d4c03
Sun, C.
19650d2f-f387-444d-9874-1621763fcfd9
Velazquez, M.A.
706e7de5-8cdb-4f2b-b47d-128166bdbea4
Marfy-Smith, S.
acc55ea7-1323-4c38-8701-fefeee332230
Sheth, B.
2ca6ed58-a992-47b7-b3a5-3c5df82aada7
Cox, A.
93ffb38c-ff07-4e67-9403-264a6f72265e
Johnston, D.A.
b41163c9-b9d2-425c-af99-2a357204014e
Smyth, N.
0eba2a40-3b43-4d40-bb64-621bd7e9d505
Fleming, T.P.
2abf761a-e5a1-4fa7-a2c8-12e32d5d4c03

Sun, C., Velazquez, M.A., Marfy-Smith, S., Sheth, B., Cox, A., Johnston, D.A., Smyth, N. and Fleming, T.P. (2014) Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition. Development, 141 (5), 1140-1150. (doi:10.1242/dev.103952). (PMID:24504338)

Record type: Article

Abstract

Mammalian extra-embryonic lineages perform the crucial role of nutrient provision during gestation to support embryonic and fetal growth. These lineages derive from outer trophectoderm (TE) and internal primitive endoderm (PE) in the blastocyst and subsequently give rise to chorio-allantoic and visceral yolk sac placentae, respectively. We have shown maternal low protein diet exclusively during mouse preimplantation development (Emb-LPD) is sufficient to cause a compensatory increase in fetal and perinatal growth that correlates positively with increased adult-onset cardiovascular, metabolic and behavioural disease. Here, to investigate early mechanisms of compensatory nutrient provision, we assessed the influence of maternal Emb-LPD on endocytosis within extra-embryonic lineages using quantitative imaging and expression of markers and proteins involved. Blastocysts collected from Emb-LPD mothers within standard culture medium displayed enhanced TE endocytosis compared with embryos from control mothers with respect to the number and collective volume per cell of vesicles with endocytosed ligand and fluid and lysosomes, plus protein expression of megalin (Lrp2) LDL-family receptor. Endocytosis was also stimulated using similar criteria in the outer PE-like lineage of embryoid bodies formed from embryonic stem cell lines generated from Emb-LPD blastocysts. Using an in vitro model replicating the depleted amino acid (AA) composition found within the Emb-LPD uterine luminal fluid, we show TE endocytosis response is activated through reduced branched-chain AAs (leucine, isoleucine, valine). Moreover, activation appears mediated through RhoA GTPase signalling. Our data indicate early embryos regulate and stabilise endocytosis as a mechanism to compensate for poor maternal nutrient provision.

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e-pub ahead of print date: 6 February 2014
Published date: March 2014
Keywords: mouse embryo, trophectoderm, primitive endoderm, embryoid body, endocytosis, maternal diet, RhoA
Organisations: Faculty of Medicine, Centre for Biological Sciences

Identifiers

Local EPrints ID: 363110
URI: http://eprints.soton.ac.uk/id/eprint/363110
ISSN: 1477-9129
PURE UUID: 2fd07ad7-116e-4f2d-9174-ce354b1d694d
ORCID for D.A. Johnston: ORCID iD orcid.org/0000-0001-6703-6014

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Date deposited: 13 Mar 2014 14:30
Last modified: 15 Mar 2024 03:29

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Contributors

Author: C. Sun
Author: M.A. Velazquez
Author: S. Marfy-Smith
Author: B. Sheth
Author: A. Cox
Author: D.A. Johnston ORCID iD
Author: N. Smyth
Author: T.P. Fleming

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