Collection 24 May 2021

Metabolism at the single-cell resolution

Single-cell technologies have revolutionized our ability to probe some of the most important questions in metabolism research. Here, we highlight innovative use of single-cell technology in studies published in Nature Metabolism.

Content

Spatial single-cell isotope tracing reveals heterogeneity of de novo fatty acid synthesis in cancer

Buglakova et al. present ¹³C-SpaceM, a method that combines stable isotope tracing with imaging mass spectrometry thus enabling spatial analysis of lipid dynamics with near-single-cell resolution in tissues.
- Elena Buglakova
- Måns Ekelöf
- Theodore Alexandrov
ArticleOpen Access9 Sep 2024 Nature Metabolism
Delineating mouse β-cell identity during lifetime and in diabetes with a single cell atlas

This study reports the mouse islet atlas, a curated resource integrating scRNA-seq data of over 300,000 cells from nine datasets, covering pancreas development, homeostasis and disease states.
- Karin Hrovatin
- Aimée Bastidas-Ponce
- Fabian J. Theis
ArticleOpen Access11 Sep 2023 Nature Metabolism
Spatial metabolomics: from a niche field towards a driver of innovation

Spatial metabolomics has matured and is driving innovation in mass spectrometry, metabolomics and spatial omics. With exciting discoveries, complementary capabilities and increasing accessibility, it has secured its place in the spatial biology toolbox, showing promise in biology, medicine and pharmacology.
- Theodore Alexandrov
Comment7 Sep 2023 Nature Metabolism
Subcellular quantitative imaging of metabolites at the organelle level

Subcellular quantitative analysis has been a long-standing goal of mass spectrometry imaging, but was originally thought to be unattainable. However, recent advances have made organelle-level absolute quantification through mass spectrometry imaging a reality, thanks to the development of nano secondary ion mass spectrometry.
- Gary Siuzdak
Comment7 Sep 2023 Nature Metabolism
Spatially resolved metabolomics and isotope tracing reveal dynamic metabolic responses of dentate granule neurons with acute stimulation

Miller et al. use fast thermal preservation and mass spectrometry imaging to reveal rapid neuron-layer metabolic responses to stimulation within a brain slice. Stimulation increases glucose use and converts spent ATP into metabolic fuel, via inosine.
- Anne Miller
- Elisa M. York
- Gary Yellen
Article5 Oct 2023 Nature Metabolism
Adipogenic and SWAT cells separate from a common progenitor in human brown and white adipose depots

Single-cell transcriptomic analysis of progenitor cells from human adipose depots reveals an adipogenic and a structural branch of cells, the latter named SWAT cells and shown to display a multipotent phenotype.
- Nagendra P. Palani
- Carla Horvath
- Camilla Scheele
ArticleOpen Access19 Jun 2023 Nature Metabolism
Wnt signaling preserves progenitor cell multipotency during adipose tissue development

Single-cell transcriptomic analysis of human multipotent progenitor cells reveals that upon adipogenic stimulation, Wnt signaling regulates the generation of functional multipotent mesenchymal progenitors, named structural Wnt-regulated adipose tissue resident cells, which maintain the progenitor pool.
- Zinger Yang Loureiro
- Shannon Joyce
- Silvia Corvera
ArticleOpen Access19 Jun 2023 Nature Metabolism
HypoMap—a unified single-cell gene expression atlas of the murine hypothalamus

Steuernagel and Lam et al. present HypoMap, an integrated reference atlas of the murine hypothalamus based on 384,925 hypothalamic cells from publicly available single-cell sequencing datasets.
- Lukas Steuernagel
- Brian Y. H. Lam
- Jens C. Brüning
ArticleOpen Access20 Oct 2022 Nature Metabolism
Analyzing cell-type-specific dynamics of metabolism in kidney repair

Understanding dynamic metabolic changes in complex biological samples often overlooks heterogeneity in cell composition. Wang et al. combine mass spectrometry imaging, isotope tracing, and multiplexed immunofluorescence microscopy to study metabolic dynamics in the kidney upon ischemia–reperfusion.
- Gangqi Wang
- Bram Heijs
- Ton J. Rabelink
LetterOpen Access25 Aug 2022 Nature Metabolism
Single-cell multi-omics analysis of human pancreatic islets reveals novel cellular states in type 1 diabetes

Fasolino et al. provide insights into ductal cell roles and type 1 diabetes pathogenesis using a pancreatic islet single-cell atlas generated by the Human Pancreas Analysis Program.
- Maria Fasolino
- Gregory W. Schwartz
- Golnaz Vahedi
Article28 Feb 2022 Nature Metabolism
Diet-induced alteration of intestinal stem cell function underlies obesity and prediabetes in mice

A combination of single-cell approaches, lineage tracing and metabolomics is used to characterize the changes to intestinal stem cell function in the small intestine that underlie intestinal maladaptation in mice fed an obesogenic diet.
- Alexandra Aliluev
- Sophie Tritschler
- Anika Böttcher
ArticleOpen Access22 Sep 2021 Nature Metabolism
Single-cell metabolic imaging reveals a SLC2A3-dependent glycolytic burst in motile endothelial cells

Wu, Harrison and colleagues visualize lactate production at subcellular resolution in migrating endothelial cells and identify hotspots of glycolytic activity, mediated by RhoA and the glucose transporter SLC2A3, that couple cellular energy metabolism with cytoskeleton remodelling and cell motility.
- David Wu
- Devin L. Harrison
- Yun Fang
Article24 May 2021 Nature Metabolism
The cellular-resolution revolution

Few technologies have changed the language and approach of biological research as dramatically and pervasively as single-cell technology, which has joined lipidomics, GFP, ChIP–seq and CRISPR–Cas in the pantheon of biotechnology. Here, we reflect on the influence of single-cell technology on metabolism research, some of which can be found in our new Collection on Single-cell technology in metabolism, featuring articles published in Nature Metabolism.

Editorial24 May 2021 Nature Metabolism
Defining the lineage of thermogenic perivascular adipose tissue

Angueira et al. identify distinct populations of thermogenic perivascular adipocyte progenitors from thoracic adipose tissue in mice and humans.
- Anthony R. Angueira
- Alexander P. Sakers
- Patrick Seale
Article12 Apr 2021 Nature Metabolism
Vascular smooth muscle-derived Trpv1⁺ progenitors are a source of cold-induced thermogenic adipocytes

Shamsi et al. identify vascular smooth muscle cells marked by expression of Trpv1 as a part of the cellular lineage of brown and beige fat. Cold stimulates the expansion and differentiation of Trpv1-expressing progenitors to highly thermogenic adipocytes.
- Farnaz Shamsi
- Mary Piper
- Yu-Hua Tseng
Article12 Apr 2021 Nature Metabolism
A genetic map of the mouse dorsal vagal complex and its role in obesity

Ludwig et al. map transcription and chromatin accessibility in single cells across the brainstem dorsal vagal complex, thereby identifying neuronal populations, including some that control feeding.
- Mette Q. Ludwig
- Wenwen Cheng
- Tune H. Pers
Article25 Mar 2021 Nature Metabolism
A unique subset of glycolytic tumour-propagating cells drives squamous cell carcinoma

Choi et al. highlight the centrality of glycolysis in squamous cell carcinoma, revealing the glycolysis-dampening tumour suppressor role of Sirt6, and identifying a subset of highly glycolytic tumour-propagating cells with elevated antioxidant capacity.
- Jee-Eun Choi
- Carlos Sebastian
- Raul Mostoslavsky
Article22 Feb 2021 Nature Metabolism
Multiple cell types contribute to the atherosclerotic lesion fibrous cap by PDGFRβ and bioenergetic mechanisms

Newman et al. explore the origins of myofibroblasts in atherosclerotic fibrous caps, finding that while composed of cells from multiple origins, smooth muscle cells predominate and are required for long-term plaque stability.
- Alexandra A. C. Newman
- Vlad Serbulea
- Gary K. Owens
Article22 Feb 2021 Nature Metabolism
Space-time logic of liver gene expression at sub-lobular scale

Previously, liver zonation was analysed statically, and liver chronobiology was analysed at the tissue level. Using single-cell RNA-seq and single-molecule FISH, Droin et al. study the interplay between liver gene regulation in space and time at the sub-lobular scale.
- Colas Droin
- Jakob El Kholtei
- Felix Naef
Article11 Jan 2021 Nature Metabolism
Stepwise cell fate decision pathways during osteoclastogenesis at single-cell resolution

Osteoclasts are the body’s exclusive bone-resorbing cells; however, their differentiation trajectory remains unclear. Using single-cell RNA sequencing, Tsukasaki et al. provide a comprehensive road map of osteoclastogenesis, unveiling stepwise molecular events underlying osteoclast cell fate transitions.
- Masayuki Tsukasaki
- Nam Cong-Nhat Huynh
- Hiroshi Takayanagi
Letter7 Dec 2020 Nature Metabolism
Single-cell lineage analysis reveals extensive multimodal transcriptional control during directed beta-cell differentiation

By using single-cell transcriptomics, Weng et al. reveal complex temporal gene control during pancreatic beta-cell differentiation from human embryonic stem cells, allowing for the construction of a unique lineage tree and optimization of differentiation protocols.
- Chen Weng
- Jiajia Xi
- Yan Li
Article30 Nov 2020 Nature Metabolism
Age-related loss of gene-to-gene transcriptional coordination among single cells

Levy et al. report a method to measure transcriptional coordination between cells in single-cell RNA sequencing data and demonstrate that transcriptional dysregulation between cells is a general phenomenon in ageing and is associated with genetic damage.
- Orr Levy
- Guy Amit
- Amir Bashan
Article2 Nov 2020 Nature Metabolism
RIPK1 gene variants associate with obesity in humans and can be therapeutically silenced to reduce obesity in mice

Using holistic and reductionist approaches, Karunakaran et al. identify a causal association between higher expression of RIPK1 (a central regulator of inflammatory cell function) and the risk of obesity. RIPK1 induces activation of proinflammatory signalling in adipose tissue, promoting the accumulation of macrophages that drive metabolic inflammation and obesity simultaneously.
- Denuja Karunakaran
- Adam W. Turner
- Katey J. Rayner
Article28 Sep 2020 Nature Metabolism
Single-cell analysis of human adipose tissue identifies depot- and disease-specific cell types

Adipose tissue varies depending on localization. Vijay et al. perform single-cell RNA sequencing in multiple adipose tissue depots from obese individuals and identify distinct subpopulations of endothelial cells, immune cells and pre-adipocytes.
- Jinchu Vijay
- Marie-Frédérique Gauthier
- Elin Grundberg
Article23 Dec 2019 Nature Metabolism
Spatial sorting enables comprehensive characterization of liver zonation

The liver is a heterogeneous organ organized in lobules that are radially polarized. The use of single-cell spatial transcriptomics has revealed that half of hepatic genes are differentially expressed across the lobule. Ben-Moshe et al. show how a multi-omics approach, which consists of transcriptomics, micro RNA profiling and proteomics, allows for characterization of liver heterogeneity with higher resolution.
- Shani Ben-Moshe
- Yonatan Shapira
- Shalev Itzkovitz
Article16 Sep 2019 Nature Metabolism

Metabolism at the single-cell resolution

Content

Spatial single-cell isotope tracing reveals heterogeneity of de novo fatty acid synthesis in cancer

Delineating mouse β-cell identity during lifetime and in diabetes with a single cell atlas

Spatial metabolomics: from a niche field towards a driver of innovation

Subcellular quantitative imaging of metabolites at the organelle level

Spatially resolved metabolomics and isotope tracing reveal dynamic metabolic responses of dentate granule neurons with acute stimulation

Adipogenic and SWAT cells separate from a common progenitor in human brown and white adipose depots

Wnt signaling preserves progenitor cell multipotency during adipose tissue development

HypoMap—a unified single-cell gene expression atlas of the murine hypothalamus

Analyzing cell-type-specific dynamics of metabolism in kidney repair

Single-cell multi-omics analysis of human pancreatic islets reveals novel cellular states in type 1 diabetes

Diet-induced alteration of intestinal stem cell function underlies obesity and prediabetes in mice

Single-cell metabolic imaging reveals a SLC2A3-dependent glycolytic burst in motile endothelial cells

The cellular-resolution revolution

Defining the lineage of thermogenic perivascular adipose tissue

Vascular smooth muscle-derived Trpv1⁺ progenitors are a source of cold-induced thermogenic adipocytes

A genetic map of the mouse dorsal vagal complex and its role in obesity

A unique subset of glycolytic tumour-propagating cells drives squamous cell carcinoma

Multiple cell types contribute to the atherosclerotic lesion fibrous cap by PDGFRβ and bioenergetic mechanisms

Space-time logic of liver gene expression at sub-lobular scale

Stepwise cell fate decision pathways during osteoclastogenesis at single-cell resolution

Single-cell lineage analysis reveals extensive multimodal transcriptional control during directed beta-cell differentiation

Age-related loss of gene-to-gene transcriptional coordination among single cells

RIPK1 gene variants associate with obesity in humans and can be therapeutically silenced to reduce obesity in mice

Single-cell analysis of human adipose tissue identifies depot- and disease-specific cell types

Spatial sorting enables comprehensive characterization of liver zonation

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