Absolute Scaling of Single-Cell Transcriptomes Reveals Pervasive Hypertranscription in Adult Stem and Progenitor Cells
Posted on: 29 March 2022
Preprint posted on 13 December 2021
Quantifying the absolute RNA content of single cells is possible for existing data sets and biologically relevant.
Selected by Vanessa Luzak
Categories: biochemistry, bioinformatics, cell biology, developmental biology, molecular biology
Introduction
Single cell RNA-seq (scRNA-seq) is a powerful tool to measure gene expression in individual cells. While relative gene expression differences are currently analyzed with great interest in single cell data, differences in total transcript levels were mainly considered technical artefacts and removed during normalization, assuming that single cells contain similar amounts of total RNA.
In this preprint, Kim et al. aimed to investigate whether current scRNA-seq protocols can be used to measure total transcript levels of single cells. By using a well characterized biological example of cells that increase their total transcript amounts during development (referred to as “hypertranscription”), the authors were able to verify that differences in total transcript levels between cells are not mainly due to technical artefacts. Instead, such differences can be quantified in existing scRNA-seq data sets using UMIs and/ or ERCC spike ins and have a biological meaning. When the authors applied their tool to scRNAseq data from adult mouse organs, they were able to show that hypertranscription is not a rare program restricted to specific cell types and periods during development. Instead, they found that it is a rather general biological process, which occurs in cells with a high demand for biomass.
Definition of the term “hypertranscription”:
Hypertranscription has been characterized previously by various groups for specific cell types during development. Transcription rates and transcript levels are globally increased in hypertranscribing cells, which is accompanied by a global opening of chromatin, high activity of chromatin remodellers and general transcription amplifiers, such as members of the Myc protein family. As a hallmark, genes summarized by the GO terms “chromatin remodelling”, “DNA repair”, “ribosome biogenesis” and “translation” show especially high transcript levels during hypertranscription.
Summary of findings
For the study, no new scRNAseq data was generated. Instead, previously published scRNAseq datasets were used.
For this summary, selected key experiments are described. More supporting data can be found in the preprint.
Step 1: Absolute scaling of RNA levels is possible using ERCC spike in or UMIs (in vitro setup)
Question: Are defined differences of RNA levels in a dilution series detected using UMIs or ERCC spike in?
UMIs: First, the authors analysed data from the previously published “scRNAseq mixology” experiment. In this experiment, extracted mRNA was prepared as a dilution series with a known amount of mRNA in each sample. Absolute scaling to UMI counts did correctly detect those defined differences in total mRNAbetween the samples of the dilution series.
ERCC spike in: The dilution series of mRNA in the “scRNAseq mixology” experiment was also successfully detected by absolute scaling to an ERCC spike in, which was used in the experiment in addition to UMIs.
In general, scaling to ERCC spike ins was even more precise than scaling to UMI counts. This was true for the in vitro control experiment, as well in experiments described below using scRNAseq data from biological samples. Nevertheless, both approaches worked well.
Answer: Yes, defined differences in RNA levels can be detected by absolute scaling to UMIs or ERCC spike in.
Step 2: Absolute scaling identifies a previously characterized case of hypertranscription in biological samples
Question: Can differences in total RNA levels be detected in biological scRNAseq samples?
Experiment 1: Embryonic mouse stem cells (mESCs) were grown in two different conditions before cells were mixed and analyzed by 10x Genomics. Condition one (Serum/LIF) induces hypertranscription, whereas condition two (dual GSK/MEK inhibition) induces hypotranscription. Using UMI counts, absolute scaling could successfully detect higher total transcript levels in Serum/LIF grown cells that undergo hypertranscription.
Experiment 2: 10x Genomics data from mouse gonads during development (from E11.5 to P5) was analyzed. Primordial germ cells (PGCs) were previously described to undergo hypertranscription during the period of mitotic expansion around E12.5 and E14.5. Indeed, absolute scaling to UMI counts could specifically detect hypertranscription in PGC cells (but not other cell types) in the indicated time period.
Answer: Yes, biological differences in total RNA levels can be detected by absolute scaling.
Step 3: Absolute scaling identifies hypertranscription as a general biological process in adult Organisms
Question: Is hypertranscription restricted to certain cell types and periods during development?
Experiment 1: The Tabula Muris atlas contains scRNAseq data of 20 different mouse organs. Most organs have been analyzed by two different scRNAseq approaches, namely 10x Genomics including UMIs and SmartSeq2 including ERCC Spike ins. Using the absolute scaling approach to analyze the Tabula Muris data sets, the authors could show that
- Low transcript levels were mainly detected in differentiated cell types.
- High transcript levels were detected in proliferative stem and progenitor cells, in polyploid cells and in secretory cells.
- Along differentiation trajectories, hypertranscription was progressively lost.
- Specific hallmarks of hypertranscription (see definition in Introduction) were detected in cells with a high demand for biomass, such as stem and progenitor cells and secretory cells.
Experiment 2: Using two scRNAseq data sets that were recorded during organ regeneration after injury, the authors could show that hypertranscription plays a role in this dynamic process. In the first data set, hypertranscription was activated in satellite stem cells shortly after cardiotoxin- induced skeletal muscle damage, which play a key role in skeletal muscle regeneration. In the second data set, hypertranscription was activated in Clu+ revival stem cells after irradiation-induced damage of the intestine. Taken together, both data sets suggest that hypertranscription plays an important role during organ regeneration.
Answer: No, hypertranscription is not restricted to development. It occurs during development as well as in adult organisms as a general biological process in cells with a high demand for biomass.
Key learnings
Technical: Quantification of total transcript levels in single cells is possible.
Absolute scaling of scRNAseq data is possible in data sets using UMIs and/ or ERCC spike ins.
Biological: Quantification of total transcript levels in single cells is biologically relevant.
Measuring absolute transcript levels of single cells reveals an overlooked, but fundamental transcriptional program in adult organs: hypertranscription is identified in cells with a high demand for biomass, such as multipotent proliferative cells during organ maintenance and regeneration, as well as differentiated secretory cells.
Personal opinion – why this work is important
The study by Kim et al. provides a potential biological meaning to an overlooked, but common aspect of scRNAseq data sets: that for individual cells quite different amounts of total transcripts can be detected. For the first time, it was shown that such differences in total RNA levels are not purely technical artefacts. In my opinion, their absolute scaling approach should routinely be used for future analysis of scRNAseq data sets. Very conveniently, the existing experimental setup does not require any changes to do so and even existing data can easily be reanalyzed.
I was amazed how much new knowledge was generated in this study by looking more closely and a bit differently at existing data sets. Hypertranscription was identified as a general cellular program in adult organs and can potentially be used as a marker during differentiation processes. Further, as a researcher studying single-celled eukaryotes, I am very curious to see if hypertrancription occurs and is relevant in single cell organisms as well?
doi: https://doi.org/10.1242/prelights.31707
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BSCB-Biochemical Society 2024 Cell Migration meeting
This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.
| List by | Reinier Prosee |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
| List by | Sergio Menchero et al. |
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
| List by | Nadja Hümpfer et al. |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |