Advances in mass spectrometry-enabled multiomics at single-cell resolution

Kumar, Rashmi; Zemaitis, Kevin; Fulcher, James M.; Pasa-Tolic, Ljiljana

doi:10.1016/j.copbio.2024.103096

Advances in mass spectrometry-enabled multiomics at single-cell resolution

Journal Article · Sat Mar 02 00:00:00 EST 2024 · Current Opinion in Biotechnology

DOI:https://doi.org/10.1016/j.copbio.2024.103096· OSTI ID:2322504

Kumar, Rashmi ^[1]; ^[1]; Fulcher, James M. ^[1]; Pasa-Tolic, Ljiljana ^[1]

Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

We report biological organisms are multifaceted, intricate systems where slight perturbations can result in extensive changes in gene expression, protein abundance and/or activity, and metabolic flux. These changes occur at different timescales, spatially across cells of heterogeneous origins, and within single-cells. Hence, multimodal measurements at the smallest biological scales are necessary to capture dynamic changes in heterogeneous biological systems. Of the analytical techniques used to measure biomolecules, mass spectrometry (MS) has proven to be a powerful option due to its sensitivity, robustness, and flexibility with regard to the breadth of biomolecules that can be analyzed. Recently, many studies have coupled MS to other analytical techniques with the goal of measuring multiple modalities from the same single-cell. It is with these concepts in mind that we focus this review on MS-enabled multiomic measurements at single-cell or near-single- cell resolution.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2322504

Report Number(s):: PNNL-SA--194867

Journal Information:: Current Opinion in Biotechnology, Journal Name: Current Opinion in Biotechnology Vol. 87; ISSN 0958-1669

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (48)

Mass Spectrometric Method for Analyzing Metabolites in Yeast with Single Cell Sensitivity Amantonico, Andrea; Oh, Joo Yeon; Sobek, Jens Angewandte Chemie International Edition, Vol. 47, Issue 29 https://doi.org/10.1002/anie.200705923	journal	July 2008
Exploring the Fundamental Structures of Life: Non‐Targeted, Chemical Analysis of Single Cells and Subcellular Structures Neumann, Elizabeth K.; Do, Thanh D.; Comi, Troy J. Angewandte Chemie International Edition, Vol. 58, Issue 28 https://doi.org/10.1002/anie.201811951	journal	July 2019
Lipid Heterogeneity between Astrocytes and Neurons Revealed by Single‐Cell MALDI‐MS Combined with Immunocytochemical Classification Neumann, Elizabeth K.; Comi, Troy J.; Rubakhin, Stanislav S. Angewandte Chemie International Edition, Vol. 58, Issue 18 https://doi.org/10.1002/anie.201812892	journal	April 2019
In Vivo Subcellular Mass Spectrometry Enables Proteo‐Metabolomic Single‐Cell Systems Biology in a Chordate Embryo Developing to a Normally Behaving Tadpole (X. laevis)** Lombard‐Banek, Camille; Li, Jie; Portero, Erika P. Angewandte Chemie International Edition, Vol. 60, Issue 23 https://doi.org/10.1002/anie.202100923	journal	April 2021
Multiplexed imaging mass spectrometry of the extracellular matrix using serial enzyme digests from formalin-fixed paraffin-embedded tissue sections Clift, Cassandra L.; Drake, Richard R.; Mehta, Anand Analytical and Bioanalytical Chemistry, Vol. 413, Issue 10 https://doi.org/10.1007/s00216-020-03047-z	journal	November 2020
Evaluation of antibody-based single cell type imaging techniques coupled to multiplexed imaging of N-glycans and collagen peptides by matrix-assisted laser desorption/ionization mass spectrometry imaging Dunne, Jaclyn; Griner, Jake; Romeo, Martin Analytical and Bioanalytical Chemistry, Vol. 415, Issue 28 https://doi.org/10.1007/s00216-023-04983-2	journal	October 2023
MALDI-TOF MS in microbiological diagnostics—identification of microorganisms and beyond (mini review) Wieser, Andreas; Schneider, Lukas; Jung, Jette Applied Microbiology and Biotechnology, Vol. 93, Issue 3 https://doi.org/10.1007/s00253-011-3783-4	journal	December 2011
RaMALDI: Enabling simultaneous Raman and MALDI imaging of the same tissue section Yang, Ethan; Kim, Jeong Hee; Tressler, Caitlin M. Biosensors and Bioelectronics, Vol. 239 https://doi.org/10.1016/j.bios.2023.115597	journal	November 2023
The Human Tumor Atlas Network: Charting Tumor Transitions across Space and Time at Single-Cell Resolution Rozenblatt-Rosen, Orit; Regev, Aviv; Oberdoerffer, Philipp Cell, Vol. 181, Issue 2 https://doi.org/10.1016/j.cell.2020.03.053	journal	April 2020
Integrated analysis of multimodal single-cell data Hao, Yuhan; Hao, Stephanie; Andersen-Nissen, Erica Cell, Vol. 184, Issue 13 https://doi.org/10.1016/j.cell.2021.04.048	journal	June 2021
Simultaneous deep transcriptome and proteome profiling in a single mouse oocyte Jiang, Yi-Rong; Zhu, Le; Cao, Lan-Rui Cell Reports, Vol. 42, Issue 11 https://doi.org/10.1016/j.celrep.2023.113455	journal	November 2023
Useful ion yields for Cameca IMS 3f and 6f SIMS: Limits on quantitative analysis Hervig, Richard L.; Mazdab, Frank K.; Williams, Peter Chemical Geology, Vol. 227, Issue 1-2 https://doi.org/10.1016/j.chemgeo.2005.09.008	journal	March 2006
Combined protein and nucleic acid imaging reveals virus-dependent B cell and macrophage immunosuppression of tissue microenvironments Jiang, Sizun; Chan, Chi Ngai; Rovira-Clavé, Xavier Immunity, Vol. 55, Issue 6 https://doi.org/10.1016/j.immuni.2022.03.020	journal	June 2022
Into the multiverse: advances in single-cell multiomic profiling Ogbeide, Silvia; Giannese, Francesca; Mincarelli, Laura Trends in Genetics, Vol. 38, Issue 8 https://doi.org/10.1016/j.tig.2022.03.015	journal	August 2022
Protocol for multimodal analysis of human kidney tissue by imaging mass spectrometry and CODEX multiplexed immunofluorescence Neumann, Elizabeth K.; Patterson, Nathan Heath; Allen, Jamie L. STAR Protocols, Vol. 2, Issue 3 https://doi.org/10.1016/j.xpro.2021.100747	journal	September 2021
Ultrasensitive Proteomics Using High-Efficiency On-Line Micro-SPE-NanoLC-NanoESI MS and MS/MS Shen, Yufeng; Tolić, Nikola; Masselon, Christophe Analytical Chemistry, Vol. 76, Issue 1, p. 144-154 https://doi.org/10.1021/ac030096q	journal	January 2004
An Integrated Strategy for Mass Spectrometry-Based Multiomics Analysis of Single Cells Li, Yuanyuan; Li, Hang; Xie, Yuping Analytical Chemistry, Vol. 93, Issue 42 https://doi.org/10.1021/acs.analchem.0c05209	journal	October 2021
Multiomics Imaging Using High-Energy Water Gas Cluster Ion Beam Secondary Ion Mass Spectrometry [(H₂O)_n-GCIB-SIMS] of Frozen-Hydrated Cells and Tissue Tian, Hua; Sheraz née Rabbani, Sadia; Vickerman, John C. Analytical Chemistry, Vol. 93, Issue 22 https://doi.org/10.1021/acs.analchem.0c05210	journal	May 2021
Single-Cell Lipidomics Using Analytical Flow LC-MS Characterizes the Response to Chemotherapy in Cultured Pancreatic Cancer Cells Saunders, Kyle D. G.; von Gerichten, Johanna; Lewis, Holly-May Analytical Chemistry, Vol. 95, Issue 39 https://doi.org/10.1021/acs.analchem.3c02854	journal	September 2023
Microsampling Capillary Electrophoresis Mass Spectrometry Enables Single-Cell Proteomics in Complex Tissues: Developing Cell Clones in Live Xenopus laevis and Zebrafish Embryos Lombard-Banek, Camille; Moody, Sally A.; Manzini, M. Chiara Analytical Chemistry, Vol. 91, Issue 7 https://doi.org/10.1021/acs.analchem.9b00345	journal	February 2019
Charge Distribution between Different Classes of Glycerophospolipids in MALDI-MS Imaging Boskamp, Marcel S.; Soltwisch, Jens Analytical Chemistry, Vol. 92, Issue 7 https://doi.org/10.1021/acs.analchem.9b05761	journal	March 2020
Laser Ablation–Inductively Coupled Plasma–Mass Spectrometry Imaging in Biology Doble, Philip A.; de Vega, Raquel Gonzalez; Bishop, David P. Chemical Reviews, Vol. 121, Issue 19 https://doi.org/10.1021/acs.chemrev.0c01219	journal	May 2021
Multiomics Method Enabled by Sequential Metabolomics and Proteomics for Human Pluripotent Stem-Cell-Derived Cardiomyocytes Bayne, Elizabeth F.; Simmons, Aaron D.; Roberts, David S. Journal of Proteome Research, Vol. 20, Issue 10 https://doi.org/10.1021/acs.jproteome.1c00611	journal	September 2021
Integration of Metabolomics, Lipidomics, and Proteomics Reveals the Metabolic Characterization of Nonalcoholic Steatohepatitis Zhang, Ji; Yang, Yiqin; Wang, Zipeng Journal of Proteome Research, Vol. 22, Issue 8 https://doi.org/10.1021/acs.jproteome.3c00009	journal	July 2023
MALDI-TOF Mass Spectrometry in Clinical Analysis and Research Li, Dandan; Yi, Jia; Han, Guobin ACS Measurement Science Au, Vol. 2, Issue 5 https://doi.org/10.1021/acsmeasuresciau.2c00019	journal	July 2022
Reproducibility crisis: Blame it on the antibodies Baker, Monya Nature, Vol. 521, Issue 7552 https://doi.org/10.1038/521274a	journal	May 2015
Profiling metabolites and peptides in single cells Rubakhin, Stanislav S.; Romanova, Elena V.; Nemes, Peter Nature Methods, Vol. 8, Issue S4 https://doi.org/10.1038/nmeth.1549	journal	March 2011
Assessment of a method to characterize antibody selectivity and specificity for use in immunoprecipitation Marcon, Edyta; Jain, Harshika; Bhattacharya, Anandi Nature Methods, Vol. 12, Issue 8 https://doi.org/10.1038/nmeth.3472	journal	June 2015
Highly multiplexed simultaneous detection of RNAs and proteins in single cells Frei, Andreas P.; Bava, Felice-Alessio; Zunder, Eli R. Nature Methods, Vol. 13, Issue 3 https://doi.org/10.1038/nmeth.3742	journal	January 2016
Advances and prospects for the Human BioMolecular Atlas Program (HuBMAP) Jain, Sanjay; Pei, Liming; Spraggins, Jeffrey M. Nature Cell Biology, Vol. 25, Issue 8 https://doi.org/10.1038/s41556-023-01194-w	journal	July 2023
Spatial metabolomics of in situ host–microbe interactions at the micrometre scale Geier, Benedikt; Sogin, Emilia M.; Michellod, Dolma Nature Microbiology, Vol. 5, Issue 3 https://doi.org/10.1038/s41564-019-0664-6	journal	February 2020
Integrative single-cell analysis Stuart, Tim; Satija, Rahul Nature Reviews Genetics, Vol. 20, Issue 5 https://doi.org/10.1038/s41576-019-0093-7	journal	January 2019
The technological landscape and applications of single-cell multi-omics Baysoy, Alev; Bai, Zhiliang; Satija, Rahul Nature Reviews Molecular Cell Biology, Vol. 24, Issue 10 https://doi.org/10.1038/s41580-023-00615-w	journal	June 2023
An atlas of healthy and injured cell states and niches in the human kidney Lake, Blue B.; Menon, Rajasree; Winfree, Seth Nature, Vol. 619, Issue 7970 https://doi.org/10.1038/s41586-023-05769-3	journal	July 2023
A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain Yao, Zizhen; van Velthoven, Cindy T. J.; Kunst, Michael Nature, Vol. 624, Issue 7991 https://doi.org/10.1038/s41586-023-06812-z	journal	December 2023
Spatial multimodal analysis of transcriptomes and metabolomes in tissues Vicari, Marco; Mirzazadeh, Reza; Nilsson, Anna Nature Biotechnology https://doi.org/10.1038/s41587-023-01937-y	journal	September 2023
Single-cell multimodal omics: the power of many Zhu, Chenxu; Preissl, Sebastian; Ren, Bing Nature Methods, Vol. 17, Issue 1 https://doi.org/10.1038/s41592-019-0691-5	journal	January 2020
Parallel measurement of transcriptomes and proteomes from same single cells using nanodroplet splitting Fulcher, James M.; Markillie, Lye Meng; Mitchell, Hugh D. https://doi.org/10.1101/2022.05.17.492137	preprint	May 2022
Multi-modal mass spectrometry imaging reveals single-cell metabolic states in mammalian liver Tian, Hua; Rajbhandari, Presha; Tarolli, Jay https://doi.org/10.1101/2022.09.26.508878	preprint	September 2022
MIBI-TOF: A multiplexed imaging platform relates cellular phenotypes and tissue structure Keren, Leeat; Bosse, Marc; Thompson, Steve Science Advances, Vol. 5, Issue 10 https://doi.org/10.1126/sciadv.aax5851	journal	October 2019
Single-cell RNA-seq reveals new types of human blood dendritic cells, monocytes, and progenitors Villani, Alexandra-Chloé; Satija, Rahul; Reynolds, Gary Science, Vol. 356, Issue 6335 https://doi.org/10.1126/science.aah4573	journal	April 2017
Comprehensive single-cell transcriptional profiling of a multicellular organism Cao, Junyue; Packer, Jonathan S.; Ramani, Vijay Science, Vol. 357, Issue 6352 https://doi.org/10.1126/science.aam8940	journal	August 2017
Single-cell reconstruction of developmental trajectories during zebrafish embryogenesis Farrell, Jeffrey A.; Wang, Yiqun; Riesenfeld, Samantha J. Science, Vol. 360, Issue 6392 https://doi.org/10.1126/science.aar3131	journal	April 2018
Cellular senescence: a key therapeutic target in aging and diseases Zhang, Lei; Pitcher, Louise E.; Yousefzadeh, Matthew J. Journal of Clinical Investigation, Vol. 132, Issue 15 https://doi.org/10.1172/JCI158450	journal	August 2022
Correction to: Integrative analysis of metabolomics and proteomics reveals amino acid metabolism disorder in sepsis Chen, Qi; Liang, Xi; Wu, Tianzhou Journal of Translational Medicine, Vol. 20, Issue 1 https://doi.org/10.1186/s12967-022-03548-8	journal	August 2022
SCoPE-MS: mass spectrometry of single mammalian cells quantifies proteome heterogeneity during cell differentiation Budnik, Bogdan; Levy, Ezra; Harmange, Guillaume Genome Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s13059-018-1547-5	journal	October 2018
ClusterDE: a post-clustering differential expression (DE) method robust to false-positive inflation caused by double dipping Li, Jingyi Jessica; Song, Dongyuan; Li, Kexin https://doi.org/10.21203/rs.3.rs-3211191/v1	preprint	August 2023
The Human Cell Atlas Regev, Aviv; Teichmann, Sarah A.; Lander, Eric S. eLife, Vol. 6 https://doi.org/10.7554/eLife.27041	journal	December 2017

Similar Records

The Future of a Myriad of Accelerated Biodiscoveries Lies in AI‐Powered Mass Spectrometry and Multiomics Integration

Journal Article · Fri Jul 04 20:00:00 EDT 2025 · Journal of Mass Spectrometry · OSTI ID:2574265

Enabling Ultralow Volume Analysis with a High-Resolution Ion Mobility Mass Spectrometry Platform

Technical Report · Mon Sep 30 00:00:00 EDT 2024 · OSTI ID:2462804

In-Depth Mass Spectrometry-Based Single-Cell and Nanoscale Proteomics

Book · Mon Nov 09 23:00:00 EST 2020 · OSTI ID:1721680

Related Subjects

47 OTHER INSTRUMENTATION
genomics
imaging mass spectrometry
lipidomics
metabolomics
multi-omics
proteomics
single cell
spatial analysis
transcriptomics

Advances in mass spectrometry-enabled multiomics at single-cell resolution

Citation Formats

References (48)

Similar Records

Related Subjects