The incorporation of MALDI mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetuses

IntroductionIn 2015, the FDA released a Drug Safety Communication regarding a possible link between opioid exposure during early pregnancy and an increased risk of fetal neural tube defects (NTDs). At the time, the indications for opioid use during pregnancy were not changed due to incomplete matern...

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Main Authors: Dustyn Barnette, Amy L. Inselman, Pravin Kaldhone, Grace S. Lee, Kelly Davis, Sumit Sarkar, Pritpal Malhi, J. Edward Fisher, Joseph P. Hanig, Richard D. Beger, E. Ellen Jones
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Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Toxicology
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Online Access:https://www.frontiersin.org/articles/10.3389/ftox.2024.1452974/full
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author Dustyn Barnette
Amy L. Inselman
Pravin Kaldhone
Grace S. Lee
Kelly Davis
Sumit Sarkar
Pritpal Malhi
J. Edward Fisher
Joseph P. Hanig
Richard D. Beger
E. Ellen Jones
author_facet Dustyn Barnette
Amy L. Inselman
Pravin Kaldhone
Grace S. Lee
Kelly Davis
Sumit Sarkar
Pritpal Malhi
J. Edward Fisher
Joseph P. Hanig
Richard D. Beger
E. Ellen Jones
author_sort Dustyn Barnette
collection DOAJ
description IntroductionIn 2015, the FDA released a Drug Safety Communication regarding a possible link between opioid exposure during early pregnancy and an increased risk of fetal neural tube defects (NTDs). At the time, the indications for opioid use during pregnancy were not changed due to incomplete maternal toxicity data and limitations in human and animal studies. To assess these knowledge gaps, largescale animal studies are ongoing; however, state-of-the-art technologies have emerged as promising tools to assess otherwise non-standard endpoints. Matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI MSI) is a dynamic approach capable of generating 2D ion images to visualize the distribution of an analyte of interest across a tissue section.MethodsGiven the importance of lipid metabolism and neurotransmitters in the developing central nervous system, this study incorporates MALDI MSI to assess lipid distributions across mouse gestational day (GD) 18 fetuses, with and without observable NTDs following maternal exposure on GD 8 to morphine (400 mg/kg BW) or the NTD positive control valproic acid (VPA) (500 mg/kg BW).ResultsAnalysis of whole-body mouse fetuses revealed differential lipid distributions localized mainly in the brain and spinal cord, which included several phosphatidylcholine (PC) species such as PCs 34:1, 34:0, and 36:2 localized to the cortex or hippocampus and lyso PC 16:0 across all brain regions. Overall, differential lipids increased in with maternal morphine and VPA exposure. Neurotransmitter distributions across the brain using FMP-10 derivatizing agent were also assessed, revealing morphine-specific changes.DiscussionThe observed differential glycerophospholipid distributions in relation to treatment and NTD development in mouse fetuses provide potential targets for further investigation of molecular mechanisms of opioid-related developmental effects. Overall, these findings support the feasibility of incorporating MALDI MSI to assess non-standard endpoints of opioid exposure during gestation.
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spelling doaj-art-1d6257886cea4bb1bfcef9e77c5c5e192025-08-20T02:38:29ZengFrontiers Media S.A.Frontiers in Toxicology2673-30802024-12-01610.3389/ftox.2024.14529741452974The incorporation of MALDI mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetusesDustyn Barnette0Amy L. Inselman1Pravin Kaldhone2Grace S. Lee3Kelly Davis4Sumit Sarkar5Pritpal Malhi6J. Edward Fisher7Joseph P. Hanig8Richard D. Beger9E. Ellen Jones10National Center for Toxicological Research (FDA), Division of Systems Biology, Jefferson, AR, United StatesNational Center for Toxicological Research (FDA), Division of Systems Biology, Jefferson, AR, United StatesNational Center for Toxicological Research (FDA), Division of Systems Biology, Jefferson, AR, United StatesCenter for Drug Evaluation and Research (CDER), Office of Testing and Research, Silver Spring, MD, United StatesNational Center for Toxicological Research (FDA), Toxicologic Pathology Associates, Jefferson, AR, United StatesNational Center for Toxicological Research (FDA), Division of Neurotoxicology, Jefferson, AR, United StatesNational Center for Toxicological Research (FDA), Toxicologic Pathology Associates, Jefferson, AR, United StatesCenter for Drug Evaluation and Research (CDER), Office of Testing and Research, Silver Spring, MD, United StatesCenter for Drug Evaluation and Research (CDER), Division of Pharmacology Toxicology for Neuroscience, Silver Spring, MD, United StatesNational Center for Toxicological Research (FDA), Division of Systems Biology, Jefferson, AR, United StatesNational Center for Toxicological Research (FDA), Division of Systems Biology, Jefferson, AR, United StatesIntroductionIn 2015, the FDA released a Drug Safety Communication regarding a possible link between opioid exposure during early pregnancy and an increased risk of fetal neural tube defects (NTDs). At the time, the indications for opioid use during pregnancy were not changed due to incomplete maternal toxicity data and limitations in human and animal studies. To assess these knowledge gaps, largescale animal studies are ongoing; however, state-of-the-art technologies have emerged as promising tools to assess otherwise non-standard endpoints. Matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI MSI) is a dynamic approach capable of generating 2D ion images to visualize the distribution of an analyte of interest across a tissue section.MethodsGiven the importance of lipid metabolism and neurotransmitters in the developing central nervous system, this study incorporates MALDI MSI to assess lipid distributions across mouse gestational day (GD) 18 fetuses, with and without observable NTDs following maternal exposure on GD 8 to morphine (400 mg/kg BW) or the NTD positive control valproic acid (VPA) (500 mg/kg BW).ResultsAnalysis of whole-body mouse fetuses revealed differential lipid distributions localized mainly in the brain and spinal cord, which included several phosphatidylcholine (PC) species such as PCs 34:1, 34:0, and 36:2 localized to the cortex or hippocampus and lyso PC 16:0 across all brain regions. Overall, differential lipids increased in with maternal morphine and VPA exposure. Neurotransmitter distributions across the brain using FMP-10 derivatizing agent were also assessed, revealing morphine-specific changes.DiscussionThe observed differential glycerophospholipid distributions in relation to treatment and NTD development in mouse fetuses provide potential targets for further investigation of molecular mechanisms of opioid-related developmental effects. Overall, these findings support the feasibility of incorporating MALDI MSI to assess non-standard endpoints of opioid exposure during gestation.https://www.frontiersin.org/articles/10.3389/ftox.2024.1452974/fullmorphineexencephalyopioidMALDI MSIlipidshypoxia
spellingShingle Dustyn Barnette
Amy L. Inselman
Pravin Kaldhone
Grace S. Lee
Kelly Davis
Sumit Sarkar
Pritpal Malhi
J. Edward Fisher
Joseph P. Hanig
Richard D. Beger
E. Ellen Jones
The incorporation of MALDI mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetuses
Frontiers in Toxicology
morphine
exencephaly
opioid
MALDI MSI
lipids
hypoxia
title The incorporation of MALDI mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetuses
title_full The incorporation of MALDI mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetuses
title_fullStr The incorporation of MALDI mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetuses
title_full_unstemmed The incorporation of MALDI mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetuses
title_short The incorporation of MALDI mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetuses
title_sort incorporation of maldi mass spectrometry imaging in studies to identify markers of toxicity following in utero opioid exposures in mouse fetuses
topic morphine
exencephaly
opioid
MALDI MSI
lipids
hypoxia
url https://www.frontiersin.org/articles/10.3389/ftox.2024.1452974/full
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