Molecular profiling of enteric nervous system cell lineages

Yuuki Obata, Álvaro Castaño, Todd L. Fallesen, Ana Carina Bon-Frauches, Stefan Boeing, Almaz Huseynova, Sarah McCallum, Reena Lasrado, Tiffany A. Heanue, Vassilis Pachnis

Published: 2022-06-07 DOI: 10.1038/s41596-022-00697-4

Enteric Nervous System

Transcriptomic Analysis

Nuclei Isolation

RNA Sequencing

Neuronal Glial Cells

AI 解读

Supplementary information

Supplementary Information

Supplementary Figs. 1–3.

Author Correction: Full-length sequencing of circular DNA viruses and extrachromosomal circular DNA using CIDER-Seq

Generation of heart-forming organoids from human pluripotent stem cells

Design and fabrication of wearable electronic textiles using twisted fiber-based threads

Activation of mechanoluminescent nanotransducers by focused ultrasound enables light delivery to deep-seated tissue in vivo

Chromatin accessibility profiling by ATAC-seq

Deoxyfluorination of phenols for chemoselective18F-labeling of peptides

Author Correction: cfSNV: a software tool for the sensitive detection of somatic mutations from cell-free DNA

Human primordial germ cell-like cells specified from resetting precursors develop in human hindgut organoids

An inexpensive semi-automated sample processing pipeline for cell-free RNA extraction

Application of CHyMErA Cas9-Cas12a combinatorial genome-editing platform for genetic interaction mapping and gene fragment deletion screening

查看全部

Sections

Figures

References

Supplementary information

Rao, M. & Gershon, M. D. The bowel and beyond: the enteric nervous system in neurological disorders. Nat. Rev. Gastroenterol. Hepatol. 13, 517–528 (2016).
Furness, J. B. The enteric nervous system and neurogastroenterology. Nat. Rev. Gastroenterol. Hepatol. 9, 286–294 (2012).
Yoo, B. B. & Mazmanian, S. K. The enteric network: interactions between the immune and nervous systems of the gut. Immunity 46, 910–926 (2017).
Spencer, N. J. & Hu, H. Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility. Nat. Rev. Gastroenterol. Hepatol. 17, 338–351 (2020).
Rao, M. & Gershon, M. D. Enteric nervous system development: what could possibly go wrong? Nat. Rev. Neurosci. 19, 552–565 (2018).
Obata, Y. et al. Neuronal programming by microbiota regulates intestinal physiology. Nature 578, 284–289 (2020).
McCallum, S. et al. Enteric glia as a source of neural progenitors in adult zebrafish. eLife 9, e56086 (2020).
Wright, C. M. et al. scRNA-seq reveals new enteric nervous system roles for GDNF, NRTN, and TBX3. Cell Mol. Gastroenterol. Hepatol. 11, 1548–1592.e1 (2021).
Drokhlyansky, E. et al. The human and mouse enteric nervous system at single-cell resolution. Cell 182, 1606–1622 e1623 (2020).
May-Zhang, A. A. et al. Combinatorial transcriptional profiling of mouse and human enteric neurons identifies shared and disparate subtypes in situ. Gastroenterology 160, 755–770 e726 (2021).
Gombash, S. E. et al. Intravenous AAV9 efficiently transduces myenteric neurons in neonate and juvenile mice. Front. Mol. Neurosci. 7, 81 (2014).
Wilhelmsen, K., Ketema, M., Truong, H. & Sonnenberg, A. KASH-domain proteins in nuclear migration, anchorage and other processes. J. Cell Sci. 119, 5021–5029 (2006).
van den Pol, A. N. et al. Viral strategies for studying the brain, including a replication-restricted self-amplifying delta-G vesicular stomatis virus that rapidly expresses transgenes in brain and can generate a multicolor golgi-like expression. J. Comp. Neurol. 516, 456–481 (2009).
Lasrado, R. et al. Lineage-dependent spatial and functional organization of the mammalian enteric nervous system. Science 356, 722–726 (2017).
Roy-Carson, S. et al. Defining the transcriptomic landscape of the developing enteric nervous system and its cellular environment. BMC Genomics 18, 290 (2017).
Zeisel, A. et al. Molecular architecture of the mouse nervous system. Cell 174, 999–1014 e1022 (2018).
Memic, F. et al. Transcription and signaling regulators in developing neuronal subtypes of mouse and human enteric nervous system. Gastroenterology 154, 624–636 (2018).
Lau, S. T. et al. Activation of Hedgehog signaling promotes development of mouse and human enteric neural crest cells, based on single-cell transcriptome analyses. Gastroenterology 157, 1556–1571 e1555 (2019).
Morarach, K. et al. Diversification of molecularly defined myenteric neuron classes revealed by single-cell RNA sequencing. Nat. Neurosci. 24, 34–46 (2021).
Howard, A. G. T. et al. An atlas of neural crest lineages along the posterior developing zebrafish at single-cell resolution. eLife 10, e60005 (2021).
van den Brink, S. C. et al. Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations. Nat. Methods 14, 935–936 (2017).
Piwnicka, M., Darzynkiewicz, Z. & Melamed, M. R. RNA and DNA content of isolated cell nuclei measured by multiparameter flow cytometry. Cytometry 3, 269–275 (1983).
Slyper, M. et al. A single-cell and single-nucleus RNA-seq toolbox for fresh and frozen human tumors. Nat. Med. 26, 792–802 (2020).
Taylor, C. R., Montagne, W. A., Eisen, J. S. & Ganz, J. Molecular fingerprinting delineates progenitor populations in the developing zebrafish enteric nervous system. Dev. Dyn. 245, 1081–1096 (2016).
Carney, T. J. et al. A direct role for Sox10 in specification of neural crest-derived sensory neurons. Development 133, 4619–4630 (2006).
El-Nachef, W. N. & Bronner, M. E. De novo enteric neurogenesis in post-embryonic zebrafish from Schwann cell precursors rather than resident cell types. Development 147, dev186619 (2020).
Rodrigues, F. S., Doughton, G., Yang, B. & Kelsh, R. N. A novel transgenic line using the Cre-lox system to allow permanent lineage-labeling of the zebrafish neural crest. Genesis 50, 750–757 (2012).
Wang, Y., Rovira, M., Yusuff, S. & Parsons, M. J. Genetic inducible fate mapping in larval zebrafish reveals origins of adult insulin-producing beta-cells. Development 138, 609–617 (2011).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
McQuin, C. et al. CellProfiler 3.0: next-generation image processing for biology. PLoS Biol. 16, e2005970 (2018).
Shah, S. et al. Single-molecule RNA detection at depth by hybridization chain reaction and tissue hydrogel embedding and clearing. Development 143, 2862–2867 (2016).
Long, X., Colonell, J., Wong, A. M., Singer, R. H. & Lionnet, T. Quantitative mRNA imaging throughout the entire Drosophila brain. Nat. Methods 14, 703–706 (2017).
Maynard, K. R. et al. dotdotdot: an automated approach to quantify multiplex single molecule fluorescent in situ hybridization (smFISH) images in complex tissues. Nucleic Acids Res. 48, e66 (2020).
Pharris, M. C. et al. An automated workflow for quantifying RNA transcripts in individual cells in large data-sets. MethodsX 4, 279–288 (2017).
Foust, K. D. et al. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotechnol. 27, 59–65 (2009).
Chan, K. Y. et al. Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems. Nat. Neurosci. 20, 1172–1179 (2017).
B. B. Yoo et al. Neuronal activation of the gastrointestinal tract shapes the gut environment in mice. Preprint at bioRxiv https://doi.org/10.1101/2021.04.12.439539 (2021).
Gabanyi, I. et al. Neuro-immune interactions drive tissue programming in intestinal macrophages. Cell 164, 378–391 (2016).
Yan, Y. et al. Interleukin-6 produced by enteric neurons regulates the number and phenotype of microbe-responsive regulatory T cells in the gut. Immunity 54, 499–513 e495 (2021).
Jarret, A. et al. Enteric nervous system-derived IL-18 orchestrates mucosal barrier immunity. Cell 180, 50–63 e12 (2020).
Muller, P. A. et al. Microbiota-modulated CART+ enteric neurons autonomously regulate blood glucose. Science 370, 314–321 (2020).
Laranjeira, C. et al. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J. Clin. Invest. 121, 3412–3424 (2011).
Grindberg, R. V. et al. RNA-sequencing from single nuclei. Proc. Natl Acad. Sci. USA 110, 19802–19807 (2013).
Lacar, B. et al. Nuclear RNA-seq of single neurons reveals molecular signatures of activation. Nat. Commun. 7, 11022 (2016).
Stark, R., Grzelak, M. & Hadfield, J. RNA sequencing: the teenage years. Nat. Rev. Genet. 20, 631–656 (2019).
Kamentsky, L. et al. Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software. Bioinformatics 27, 1179–1180 (2011).
Krishnaswami, S. R. et al. Using single nuclei for RNA-seq to capture the transcriptome of postmortem neurons. Nat. Protoc. 11, 499–524 (2016).
Heanue, T. A. & Pachnis, V. Enteric nervous system development and Hirschsprung’s disease: advances in genetic and stem cell studies. Nat. Rev. Neurosci. 8, 466–479 (2007).
Avetisyan, M. et al. Hepatocyte growth factor and MET support mouse enteric nervous system development, the peristaltic response, and intestinal epithelial proliferation in response to injury. J. Neurosci. 35, 11543–11558 (2015).
Barrenschee, M. et al. Site-specific gene expression and localization of growth factor ligand receptors RET, GFRα1 and GFRα2 in human adult colon. Cell Tissue Res. 354, 371–380 (2013).
Hoogerwerf, W. A. et al. Clock gene expression in the murine gastrointestinal tract: endogenous rhythmicity and effects of a feeding regimen. Gastroenterology 133, 1250–1260 (2007).
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
Obata, Y. et al. Molecular profiling of enteric nervous system cell lineages. Zenodo https://doi.org/10.5281/zenodo.5817674 (2021).

Molecular profiling of enteric nervous system cell lineages

Supplementary information

推荐阅读