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

Marija Veličković, Leena Kadam, Joonhoon Kim, Kevin J. Zemaitis, Dušan Veličković, Yuqian Gao, Ruonan Wu, Thomas L. Fillmore, Daniel Orton, Sarah M. Williams, Matthew E. Monroe, Ronald J. Moore, Paul D. Piehowski, Lisa M. Bramer (), Leslie Myatt () and Kristin E. Burnum-Johnson ()
Additional contact information
Marija Veličković: Pacific Northwest National Laboratory
Leena Kadam: Oregon Health & Science University
Joonhoon Kim: Pacific Northwest National Laboratory
Kevin J. Zemaitis: Pacific Northwest National Laboratory
Dušan Veličković: Pacific Northwest National Laboratory
Yuqian Gao: Pacific Northwest National Laboratory
Ruonan Wu: Pacific Northwest National Laboratory
Thomas L. Fillmore: Pacific Northwest National Laboratory
Daniel Orton: Pacific Northwest National Laboratory
Sarah M. Williams: Pacific Northwest National Laboratory
Matthew E. Monroe: Pacific Northwest National Laboratory
Ronald J. Moore: Pacific Northwest National Laboratory
Paul D. Piehowski: Pacific Northwest National Laboratory
Lisa M. Bramer: Pacific Northwest National Laboratory
Leslie Myatt: Oregon Health & Science University
Kristin E. Burnum-Johnson: Pacific Northwest National Laboratory

Nature Communications, 2025, vol. 16, issue 1, 1-13

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-025-57107-y

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