Advanced multi-modal mass spectrometry imaging reveals functional differences of placental villous compartments at microscale resolution

The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms l...

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Published in:Nature communications Vol. 16; no. 1; pp. 2061 - 13
Main Authors: Veličković, Marija, Kadam, Leena, Kim, Joonhoon, Zemaitis, Kevin J., Veličković, Dušan, Gao, Yuqian, Wu, Ruonan, Fillmore, Thomas L., Orton, Daniel, Williams, Sarah M., Monroe, Matthew E., Moore, Ronald J., Piehowski, Paul D., Bramer, Lisa M., Myatt, Leslie, Burnum-Johnson, Kristin E.
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 28.02.2025
Nature Publishing Group
Nature Portfolio
Subjects:
631/136
631/45/320
631/45/475
82/58
Biological analysis
Chemical synthesis
Chorionic Villi - diagnostic imaging
Chorionic Villi - metabolism
Compartments
Female
Fetuses
Heterogeneity
Humanities and Social Sciences
Humans
Imaging
Lipid Metabolism
Lipidomics - methods
Lipids
Mass spectrometry
Mass Spectrometry - methods
Mass spectroscopy
Metabolites
Metabolome
Metabolomics
Metabolomics - methods
Microenvironments
Molecular Imaging - methods
multidisciplinary
Peptide mapping
Placenta
Placenta - diagnostic imaging
Placenta - metabolism
Pregnancy
Pregnancy complications
Protein interaction
Proteome - metabolism
Proteomes
Proteomics - methods
Science
Science (multidisciplinary)
Steroids
Trophoblasts - metabolism
Workflow
ISSN:2041-1723, 2041-1723
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Abstract The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms leading to the histological variations of the placenta during healthy pregnancy and pregnancy complications. Herein, we advance our metabolome-informed proteome imaging (MIPI) workflow to include lipidomic imaging, while also expanding the molecular coverage of metabolomic imaging by incorporating on-tissue chemical derivatization (OTCD). The improved MIPI workflow advances biomedical investigations by leveraging state-of-the-art molecular imaging technologies. Lipidome imaging identifies molecular differences between two morphologically distinct compartments of a placental villous functional unit, syncytiotrophoblast (STB) and villous core. Next, our advanced metabolome imaging maps villous functional units with enriched metabolomic activities related to steroid and lipid metabolism, outlining distinct molecular distributions across morphologically different villous compartments. Complementary proteome imaging on these villous functional units reveals a plethora of fatty acid- and steroid-related enzymes uniquely distributed in STB and villous core compartments. Integration across our advanced MIPI imaging modalities enables the reconstruction of active biological pathways of molecular synthesis and maternal-fetal signaling across morphologically distinct placental villous compartments with micrometer-scale resolution. Spatial multi-omics methodologies are essential for capturing the molecular heterogeneity of complex biological systems. In this study, the authors introduce a multi-omics imaging workflow capable of mapping metabolite-protein interactions with spatial specificity, enabling pathway-level resolution across distinct placental tissue microenvironments.
AbstractList Abstract The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms leading to the histological variations of the placenta during healthy pregnancy and pregnancy complications. Herein, we advance our metabolome-informed proteome imaging (MIPI) workflow to include lipidomic imaging, while also expanding the molecular coverage of metabolomic imaging by incorporating on-tissue chemical derivatization (OTCD). The improved MIPI workflow advances biomedical investigations by leveraging state-of-the-art molecular imaging technologies. Lipidome imaging identifies molecular differences between two morphologically distinct compartments of a placental villous functional unit, syncytiotrophoblast (STB) and villous core. Next, our advanced metabolome imaging maps villous functional units with enriched metabolomic activities related to steroid and lipid metabolism, outlining distinct molecular distributions across morphologically different villous compartments. Complementary proteome imaging on these villous functional units reveals a plethora of fatty acid- and steroid-related enzymes uniquely distributed in STB and villous core compartments. Integration across our advanced MIPI imaging modalities enables the reconstruction of active biological pathways of molecular synthesis and maternal-fetal signaling across morphologically distinct placental villous compartments with micrometer-scale resolution.
The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms leading to the histological variations of the placenta during healthy pregnancy and pregnancy complications. Herein, we advance our metabolome-informed proteome imaging (MIPI) workflow to include lipidomic imaging, while also expanding the molecular coverage of metabolomic imaging by incorporating on-tissue chemical derivatization (OTCD). The improved MIPI workflow advances biomedical investigations by leveraging state-of-the-art molecular imaging technologies. Lipidome imaging identifies molecular differences between two morphologically distinct compartments of a placental villous functional unit, syncytiotrophoblast (STB) and villous core. Next, our advanced metabolome imaging maps villous functional units with enriched metabolomic activities related to steroid and lipid metabolism, outlining distinct molecular distributions across morphologically different villous compartments. Complementary proteome imaging on these villous functional units reveals a plethora of fatty acid- and steroid-related enzymes uniquely distributed in STB and villous core compartments. Integration across our advanced MIPI imaging modalities enables the reconstruction of active biological pathways of molecular synthesis and maternal-fetal signaling across morphologically distinct placental villous compartments with micrometer-scale resolution.
The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms leading to the histological variations of the placenta during healthy pregnancy and pregnancy complications. Herein, we advance our metabolome-informed proteome imaging (MIPI) workflow to include lipidomic imaging, while also expanding the molecular coverage of metabolomic imaging by incorporating on-tissue chemical derivatization (OTCD). The improved MIPI workflow advances biomedical investigations by leveraging state-of-the-art molecular imaging technologies. Lipidome imaging identifies molecular differences between two morphologically distinct compartments of a placental villous functional unit, syncytiotrophoblast (STB) and villous core. Next, our advanced metabolome imaging maps villous functional units with enriched metabolomic activities related to steroid and lipid metabolism, outlining distinct molecular distributions across morphologically different villous compartments. Complementary proteome imaging on these villous functional units reveals a plethora of fatty acid- and steroid-related enzymes uniquely distributed in STB and villous core compartments. Integration across our advanced MIPI imaging modalities enables the reconstruction of active biological pathways of molecular synthesis and maternal-fetal signaling across morphologically distinct placental villous compartments with micrometer-scale resolution.The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms leading to the histological variations of the placenta during healthy pregnancy and pregnancy complications. Herein, we advance our metabolome-informed proteome imaging (MIPI) workflow to include lipidomic imaging, while also expanding the molecular coverage of metabolomic imaging by incorporating on-tissue chemical derivatization (OTCD). The improved MIPI workflow advances biomedical investigations by leveraging state-of-the-art molecular imaging technologies. Lipidome imaging identifies molecular differences between two morphologically distinct compartments of a placental villous functional unit, syncytiotrophoblast (STB) and villous core. Next, our advanced metabolome imaging maps villous functional units with enriched metabolomic activities related to steroid and lipid metabolism, outlining distinct molecular distributions across morphologically different villous compartments. Complementary proteome imaging on these villous functional units reveals a plethora of fatty acid- and steroid-related enzymes uniquely distributed in STB and villous core compartments. Integration across our advanced MIPI imaging modalities enables the reconstruction of active biological pathways of molecular synthesis and maternal-fetal signaling across morphologically distinct placental villous compartments with micrometer-scale resolution.
The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms leading to the histological variations of the placenta during healthy pregnancy and pregnancy complications. Herein, we advance our metabolome-informed proteome imaging (MIPI) workflow to include lipidomic imaging, while also expanding the molecular coverage of metabolomic imaging by incorporating on-tissue chemical derivatization (OTCD). The improved MIPI workflow advances biomedical investigations by leveraging state-of-the-art molecular imaging technologies. Lipidome imaging identifies molecular differences between two morphologically distinct compartments of a placental villous functional unit, syncytiotrophoblast (STB) and villous core. Next, our advanced metabolome imaging maps villous functional units with enriched metabolomic activities related to steroid and lipid metabolism, outlining distinct molecular distributions across morphologically different villous compartments. Complementary proteome imaging on these villous functional units reveals a plethora of fatty acid- and steroid-related enzymes uniquely distributed in STB and villous core compartments. Integration across our advanced MIPI imaging modalities enables the reconstruction of active biological pathways of molecular synthesis and maternal-fetal signaling across morphologically distinct placental villous compartments with micrometer-scale resolution. Spatial multi-omics methodologies are essential for capturing the molecular heterogeneity of complex biological systems. In this study, the authors introduce a multi-omics imaging workflow capable of mapping metabolite-protein interactions with spatial specificity, enabling pathway-level resolution across distinct placental tissue microenvironments.
The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms leading to the histological variations of the placenta during healthy pregnancy and pregnancy complications. Herein, we advance our metabolome-informed proteome imaging (MIPI) workflow to include lipidomic imaging, while also expanding the molecular coverage of metabolomic imaging by incorporating on-tissue chemical derivatization (OTCD). The improved MIPI workflow advances biomedical investigations by leveraging state-of-the-art molecular imaging technologies. Lipidome imaging identifies molecular differences between two morphologically distinct compartments of a placental villous functional unit, syncytiotrophoblast (STB) and villous core. Next, our advanced metabolome imaging maps villous functional units with enriched metabolomic activities related to steroid and lipid metabolism, outlining distinct molecular distributions across morphologically different villous compartments. Complementary proteome imaging on these villous functional units reveals a plethora of fatty acid- and steroid-related enzymes uniquely distributed in STB and villous core compartments. Integration across our advanced MIPI imaging modalities enables the reconstruction of active biological pathways of molecular synthesis and maternal-fetal signaling across morphologically distinct placental villous compartments with micrometer-scale resolution. Spatial multi-omics methodologies are essential for capturing the molecular heterogeneity of complex biological systems. In this study, the authors introduce a multi-omics imaging workflow capable of mapping metabolite-protein interactions with spatial specificity, enabling pathway-level resolution across distinct placental tissue microenvironments.
The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout pregnancy. Integrative spatial multi-omics approaches can provide a systems-level understanding of molecular changes underlying the mechanisms leading to the histological variations of the placenta during healthy pregnancy and pregnancy complications. Herein, we advance our metabolome-informed proteome imaging (MIPI) workflow to include lipidomic imaging, while also expanding the molecular coverage of metabolomic imaging by incorporating on-tissue chemical derivatization (OTCD). The improved MIPI workflow advances biomedical investigations by leveraging state-of-the-art molecular imaging technologies. Lipidome imaging identifies molecular differences between two morphologically distinct compartments of a placental villous functional unit, syncytiotrophoblast (STB) and villous core. Next, our advanced metabolome imaging maps villous functional units with enriched metabolomic activities related to steroid and lipid metabolism, outlining distinct molecular distributions across morphologically different villous compartments. Complementary proteome imaging on these villous functional units reveals a plethora of fatty acid- and steroid-related enzymes uniquely distributed in STB and villous core compartments. Integration across our advanced MIPI imaging modalities enables the reconstruction of active biological pathways of molecular synthesis and maternal-fetal signaling across morphologically distinct placental villous compartments with micrometer-scale resolution.Spatial multi-omics methodologies are essential for capturing the molecular heterogeneity of complex biological systems. In this study, the authors introduce a multi-omics imaging workflow capable of mapping metabolite-protein interactions with spatial specificity, enabling pathway-level resolution across distinct placental tissue microenvironments.
ArticleNumber 2061
Author Burnum-Johnson, Kristin E.
Fillmore, Thomas L.
Bramer, Lisa M.
Zemaitis, Kevin J.
Gao, Yuqian
Wu, Ruonan
Piehowski, Paul D.
Williams, Sarah M.
Kadam, Leena
Kim, Joonhoon
Veličković, Marija
Monroe, Matthew E.
Moore, Ronald J.
Myatt, Leslie
Veličković, Dušan
Orton, Daniel
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CitedBy_id crossref_primary_10_1016_j_microc_2025_115033
crossref_primary_10_3390_biomedicines13092149
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ContentType Journal Article
Copyright Battelle Memorial Institute and Leena Kadam, Leslie Myatt 2025 2025
2025. Battelle Memorial Institute and Leena Kadam, Leslie Myatt 2025.
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Battelle Memorial Institute and Leena Kadam, Leslie Myatt 2025 2025 2025
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Snippet The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus throughout...
Abstract The placenta is a complex and heterogeneous organ that links the mother and fetus, playing a crucial role in nourishing and protecting the fetus...
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SubjectTerms 631/136
631/45/320
631/45/475
82/58
Biological analysis
Chemical synthesis
Chorionic Villi - diagnostic imaging
Chorionic Villi - metabolism
Compartments
Female
Fetuses
Heterogeneity
Humanities and Social Sciences
Humans
Imaging
Lipid Metabolism
Lipidomics - methods
Lipids
Mass spectrometry
Mass Spectrometry - methods
Mass spectroscopy
Metabolites
Metabolome
Metabolomics
Metabolomics - methods
Microenvironments
Molecular Imaging - methods
multidisciplinary
Peptide mapping
Placenta
Placenta - diagnostic imaging
Placenta - metabolism
Pregnancy
Pregnancy complications
Protein interaction
Proteome - metabolism
Proteomes
Proteomics - methods
Science
Science (multidisciplinary)
Steroids
Trophoblasts - metabolism
Workflow
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Title Advanced multi-modal mass spectrometry imaging reveals functional differences of placental villous compartments at microscale resolution
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Volume 16
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