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Three-dimensional imaging of lipids and metabolites in tissues by nanospray desorption electrospray ionization mass spectrometry

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Abstract

Three-dimensional (3D) imaging of tissue sections is a new frontier in mass spectrometry imaging (MSI). Here, we report on fast 3D imaging of lipids and metabolites associated with mouse uterine decidual cells and embryo at the implantation site on day 6 of pregnancy. 2D imaging of 16–20 serial tissue sections deposited on the same glass slide was performed using nanospray desorption electrospray ionization (nano-DESI)—an ambient ionization technique that enables sensitive localized analysis of analytes on surfaces without special sample pretreatment. In this proof-of-principle study, nano-DESI was coupled to a high-resolution Q-Exactive instrument operated at high repetition rate of >5 Hz with moderate mass resolution of 35,000 (m/Δm at m/z 200), which enabled acquisition of the entire 3D image with a spatial resolution of ∼150 μm in less than 4.5 h. The results demonstrate localization of acetylcholine in the primary decidual zone (PDZ) of the implantation site throughout the depth of the tissue examined, indicating an important role of this signaling molecule in decidualization. Choline and phosphocholine—metabolites associated with cell growth—are enhanced in the PDZ and abundant in other cellular regions of the implantation site. Very different 3D distributions were obtained for fatty acids (FA), oleic acid and linoleic acid (FA 18:1 and FA 18:2), differing only by one double bond. Localization of FA 18:2 in the PDZ indicates its important role in decidualization while FA 18:1 is distributed more evenly throughout the tissue. In contrast, several lysophosphatidylcholines (LPC) observed in this study show donut-like distributions with localization around the PDZ. Complementary distributions with minimal overlap were observed for LPC 18:0 and FA 18:2 while the 3D image of the potential precursor phosphatidylcholine 36:2 (PC 36:2) showed a significant overlap with both LPC 18:0 and FA 18:2.

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Acknowledgments

The research described in this paper is part of the Chemical Imaging Initiative, at Pacific Northwest National Laboratory (PNNL). It was conducted under the Laboratory Directed Research and Development Program at PNNL a multiprogram national laboratory operated by Battelle for the US Department of Energy (DOE) under Contract DE-AC05-76RL01830. The research was performed at EMSL, a national scientific user facility sponsored by the DOE’s Office of Biological and Environmental Research and located at PNNL. This work was partially supported by NIH grants (HD068524 and DA06668) and the March of Dimes to SKD. JC is supported by a Ruth L. Kirschstein Predoctoral NRSA Fellowship (F30AG040858).

ᅟ

A single-pixel MS spectrum, MS/MS spectra of selected compounds discussed in the paper, selected 2D images, and the 3D image reconstruction can be found in the Electronic Supplementary Material.

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Authors and Affiliations

  1. Physical Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99354, USA

    Ingela Lanekoff & Julia Laskin

  2. Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99354, USA

    Kristin Burnum-Johnson

  3. Computational Sciences and Mathematics Division, Pacific Northwest National Laboratory, Richland, WA, 99354, USA

    Mathew Thomas

  4. Division of Reproductive Sciences, The Perinatal Institute, Cincinnati Children’s Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, OH, 45229, USA

    Jeeyeon Cha & Sudhansu K. Dey

  5. Thermo Fisher Scientific, San Jose, CA, 95134, USA

    Pengxiang Yang & Maria C. Prieto Conaway

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Published in the topical collection Mass Spectrometry Imaging with guest editors Andreas Römpp and Uwe Karst.

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A single-pixel MS spectrum, MS/MS spectra of selected compounds discussed in the paper, selected 2D images, and the 3D image reconstruction can be found in the Electronic Supplementary Material.

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Lanekoff, I., Burnum-Johnson, K., Thomas, M. et al. Three-dimensional imaging of lipids and metabolites in tissues by nanospray desorption electrospray ionization mass spectrometry. Anal Bioanal Chem 407, 2063–2071 (2015). https://doi.org/10.1007/s00216-014-8174-0

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