Placental 13C-DHA metabolism and relationship with maternal BMI, glycemia and birthweight
Placental 13C-DHA metabolism and relationship with maternal BMI, glycemia and birthweight
Background: Fetal docosahexaenoic acid (DHA) supply relies on preferential transplacental transfer, which is regulated by placental DHA lipid metabolism. Maternal hyperglycemia and obesity associate with higher birthweight and fetal DHA insufficiency but the role of placental DHA metabolism is unclear. Methods: Explants from 17 term placenta were incubated with
13C-labeled DHA for 48 h, at 5 or 10 mmol/L glucose treatment, and the production of 17 individual newly synthesized
13C-DHA labeled lipids quantified by liquid chromatography mass spectrometry. Results: Maternal BMI positively associated with
13C-DHA-labeled diacylglycerols, triacylglycerols, lysophospholipids, phosphatidylcholine and phosphatidylethanolamine plasmalogens, while maternal fasting glycemia positively associated with five
13C-DHA triacylglycerols. In turn,
13C-DHA-labeled phospholipids and triacylglycerols positively associated with birthweight centile. In-vitro glucose treatment increased most
13C-DHA-lipids, but decreased
13C-DHA phosphatidylethanolamine plasmalogens. However, with increasing maternal BMI, the magnitude of the glucose treatment induced increase in
13C-DHA phosphatidylcholine and
13C-DHA lysophospholipids was curtailed, with further decline in
13C-DHA phosphatidylethanolamine plasmalogens. Conversely, with increasing birthweight centile glucose treatment induced increases in
13C-DHA triacylglycerols were exaggerated, while glucose treatment induced decreases in
13C-DHA phosphatidylethanolamine plasmalogens were diminished. Conclusions: Maternal BMI and glycemia increased the production of different placental DHA lipids implying impact on different metabolic pathways. Glucose-induced elevation in placental DHA metabolism is moderated with higher maternal BMI. In turn, findings of associations between many DHA lipids with birthweight suggest that BMI and glycemia promote fetal growth partly through changes in placental DHA metabolism.
Gestational diabetes, LCMS, Lipid, Placenta, Pregnancy, Stable-isotope
Watkins, Oliver C.
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Selvam, Preben
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Pillai, Reshma Appukuttan
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Cracknell, Victoria, Kathryn Bonnell
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Yong, Hannah E.J.
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Sharma, Neha
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Cazenave-Gassiot, Amaury
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Bendt, Anne K.
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Godfrey, Keith
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Lewis, Rohan
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Wenk, Markus R.
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Chan, Shiao-Yng
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6 August 2021
Watkins, Oliver C.
985df9b8-72d6-4f32-9ee3-54553c990fdc
Selvam, Preben
989ffd8a-e214-43b5-a3ce-a814fc491ee7
Pillai, Reshma Appukuttan
c6a8a2d9-eaa1-4963-8c2c-5aed5d7e0503
Cracknell, Victoria, Kathryn Bonnell
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Yong, Hannah E.J.
9d6a310c-8309-4d94-9dd2-7766cb0420ac
Sharma, Neha
c5c663b2-86e4-4e3c-8f56-c28351419587
Cazenave-Gassiot, Amaury
f53d5438-9fad-4fd6-98f9-3e289205dcd7
Bendt, Anne K.
3a269eb1-2755-4020-a6a1-12100ae89bd4
Godfrey, Keith
0931701e-fe2c-44b5-8f0d-ec5c7477a6fd
Lewis, Rohan
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502
Wenk, Markus R.
d1ba356f-b0ed-4318-886a-c8f929679060
Chan, Shiao-Yng
3c9d8970-2cc4-430a-86a7-96f6029a5293
Watkins, Oliver C., Selvam, Preben, Pillai, Reshma Appukuttan, Cracknell, Victoria, Kathryn Bonnell, Yong, Hannah E.J., Sharma, Neha, Cazenave-Gassiot, Amaury, Bendt, Anne K., Godfrey, Keith, Lewis, Rohan, Wenk, Markus R. and Chan, Shiao-Yng
(2021)
Placental 13C-DHA metabolism and relationship with maternal BMI, glycemia and birthweight.
Molecular Medicine, 27 (1), [84].
(doi:10.1186/s10020-021-00344-w).
Abstract
Background: Fetal docosahexaenoic acid (DHA) supply relies on preferential transplacental transfer, which is regulated by placental DHA lipid metabolism. Maternal hyperglycemia and obesity associate with higher birthweight and fetal DHA insufficiency but the role of placental DHA metabolism is unclear. Methods: Explants from 17 term placenta were incubated with
13C-labeled DHA for 48 h, at 5 or 10 mmol/L glucose treatment, and the production of 17 individual newly synthesized
13C-DHA labeled lipids quantified by liquid chromatography mass spectrometry. Results: Maternal BMI positively associated with
13C-DHA-labeled diacylglycerols, triacylglycerols, lysophospholipids, phosphatidylcholine and phosphatidylethanolamine plasmalogens, while maternal fasting glycemia positively associated with five
13C-DHA triacylglycerols. In turn,
13C-DHA-labeled phospholipids and triacylglycerols positively associated with birthweight centile. In-vitro glucose treatment increased most
13C-DHA-lipids, but decreased
13C-DHA phosphatidylethanolamine plasmalogens. However, with increasing maternal BMI, the magnitude of the glucose treatment induced increase in
13C-DHA phosphatidylcholine and
13C-DHA lysophospholipids was curtailed, with further decline in
13C-DHA phosphatidylethanolamine plasmalogens. Conversely, with increasing birthweight centile glucose treatment induced increases in
13C-DHA triacylglycerols were exaggerated, while glucose treatment induced decreases in
13C-DHA phosphatidylethanolamine plasmalogens were diminished. Conclusions: Maternal BMI and glycemia increased the production of different placental DHA lipids implying impact on different metabolic pathways. Glucose-induced elevation in placental DHA metabolism is moderated with higher maternal BMI. In turn, findings of associations between many DHA lipids with birthweight suggest that BMI and glycemia promote fetal growth partly through changes in placental DHA metabolism.
Text
Placental 13C DHA metabolism resubmitted_12_7_21
- Accepted Manuscript
More information
Accepted/In Press date: 26 July 2021
Published date: 6 August 2021
Additional Information:
Funding Information:
Project was conceptualized by SYC and OCW. SYC and MW were responsible for the acquisition of the financial support for the project leading to this publication. Experiments and analysis were performed by OCW, PS, VC, RP, HY and NS with supervision provided by SYC and AC-G. Manuscript was written by OCW and SYC with the assistance of AC-G, AB, KG, RL and MW. All authors have given consent for publication. All authors read and approved the final manuscript.
Publisher Copyright:
© 2021, The Author(s).
Keywords:
Gestational diabetes, LCMS, Lipid, Placenta, Pregnancy, Stable-isotope
Identifiers
Local EPrints ID: 450550
URI: http://eprints.soton.ac.uk/id/eprint/450550
ISSN: 1076-1551
PURE UUID: 1cf6a911-27b7-4f83-ab70-a492b153ae9a
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Date deposited: 03 Aug 2021 16:31
Last modified: 17 Mar 2024 06:44
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Contributors
Author:
Oliver C. Watkins
Author:
Preben Selvam
Author:
Reshma Appukuttan Pillai
Author:
Victoria, Kathryn Bonnell Cracknell
Author:
Hannah E.J. Yong
Author:
Neha Sharma
Author:
Amaury Cazenave-Gassiot
Author:
Anne K. Bendt
Author:
Markus R. Wenk
Author:
Shiao-Yng Chan
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