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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Vydané v:	Nature communications Ročník 16; číslo 1; s. 2061 - 13
Hlavní autori:	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.
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	London Nature Publishing Group UK 28.02.2025 Nature Publishing Group Nature Portfolio
Predmet:	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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Shrnutí:	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.
Bibliografia:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 PNNL-SA-201502 AC05-76RL01830 USDOE Laboratory Directed Research and Development (LDRD) Program USDOE Office of Science (SC), Biological and Environmental Research (BER)
ISSN:	2041-1723 2041-1723
DOI:	10.1038/s41467-025-57107-y