Dedicated macrophages organize and maintain the enteric nervous system.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
Jun 2023
Historique:
received: 23 08 2022
accepted: 11 05 2023
medline: 23 6 2023
pubmed: 15 6 2023
entrez: 14 6 2023
Statut: ppublish

Résumé

Correct development and maturation of the enteric nervous system (ENS) is critical for survival

Identifiants

pubmed: 37316669
doi: 10.1038/s41586-023-06200-7
pii: 10.1038/s41586-023-06200-7
doi:

Substances chimiques

Lymphotoxin-alpha 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

818-826

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Fung, C. & Vanden Berghe, P. Functional circuits and signal processing in the enteric nervous system. Cell. Mol. Life Sci. 77, 4505–4522 (2020).
pubmed: 32424438 pmcid: 7599184 doi: 10.1007/s00018-020-03543-6
Parathan, P., Wang, Y., Leembruggen, A. J., Bornstein, J. C. & Foong, J. P. The enteric nervous system undergoes significant chemical and synaptic maturation during adolescence in mice. Dev. Biol. 458, 75–87 (2020).
pubmed: 31629713 doi: 10.1016/j.ydbio.2019.10.011
Michel, K. et al. How big is the little brain in the gut? Neuronal numbers in the enteric nervous system of mice, Guinea pig, and human. Neurogastroenterol. Motil. 34, e14440 (2022).
pubmed: 35929768 doi: 10.1111/nmo.14440
Terra, S. A., De Arruda Lourenção, P. L., Silva, M. G., Miot, H. A. & Rodrigues, M. A. M. A critical appraisal of the morphological criteria for diagnosing intestinal neuronal dysplasia type B. Mod. Pathol. 30, 978–985 (2017).
pubmed: 28304401 doi: 10.1038/modpathol.2017.4
Rao, M. & Gershon, M. D. The bowel and beyond: the enteric nervous system in neurological disorders. Nat. Rev. Gastroenterol. Hepatol. 13, 517–528 (2016).
pubmed: 27435372 pmcid: 5005185 doi: 10.1038/nrgastro.2016.107
Vries, P., de, Soret, R., Suply, E., Heloury, Y. & Neunlist, M. Postnatal development of myenteric neurochemical phenotype and impact on neuromuscular transmission in the rat colon. Am. J. Physiol. Gastrointest. Liver Physiol. 299, 539–547 (2010).
doi: 10.1152/ajpgi.00092.2010
Bergner, A. J. et al. Birthdating of myenteric neuron subtypes in the small intestine of the mouse. J. Comp. Neurol. 522, 514–527 (2014).
pubmed: 23861145 doi: 10.1002/cne.23423
Nobs, S. P. & Kopf, M. Tissue-resident macrophages: guardians of organ homeostasis. Trends Immunol. 42, 495–507 (2021).
pubmed: 33972166 doi: 10.1016/j.it.2021.04.007
Ginhoux, F. & Guilliams, M. Tissue-resident macrophage ontogeny and homeostasis. Immunity 44, 439–449 (2016).
Guilliams, M., Thierry, G. R., Bonnardel, J. & Bajenoff, M. Establishment and maintenance of the macrophage niche. Immunity 52, 434–451 (2020).
pubmed: 32187515 doi: 10.1016/j.immuni.2020.02.015
Viola, M. F. & Boeckxstaens, G. Niche-specific functional heterogeneity of intestinal resident macrophages. Gut https://doi.org/10.1136/gutjnl-2020-323121 (2020).
De Schepper, S. et al. Self-maintaining gut macrophages are essential for intestinal homeostasis. Cell 175, 400–415 (2018).
pubmed: 30173915 doi: 10.1016/j.cell.2018.07.048
Hashimoto, D. et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38, 792–804 (2013).
pubmed: 23601688 doi: 10.1016/j.immuni.2013.04.004
Muller, P. A. et al. Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 158, 300–313 (2014).
pubmed: 25036630 pmcid: 4149228 doi: 10.1016/j.cell.2014.04.050
Gabanyi, I. et al. Neuro-immune interactions drive itssue programming in intestinal macrophages. Cell 164, 378–391 (2016).
pubmed: 26777404 pmcid: 4733406 doi: 10.1016/j.cell.2015.12.023
Morarach, K. et al. Diversification of molecularly defined myenteric neuron classes revealed by single-cell RNA sequencing. Nat. Neurosci. 24, 34–46 (2021).
pubmed: 33288908 doi: 10.1038/s41593-020-00736-x
Summers, K. M., Bush, S. J. & Hume, D. A. Network analysis of transcriptomic diversity amongst resident tissue macrophages and dendritic cells in the mouse mononuclear phagocyte system. PLoS Biol. 18, e3000859 (2020).
pubmed: 33031383 pmcid: 7575120 doi: 10.1371/journal.pbio.3000859
Wang, P. L. et al. Peripheral nerve resident macrophages share tissue-specific programming and features of activated microglia. Nat. Commun. 11, 2552 (2020).
pubmed: 32439942 pmcid: 7242366 doi: 10.1038/s41467-020-16355-w
Ydens, E. et al. Profiling peripheral nerve macrophages reveals two macrophage subsets with distinct localization, transcriptome and response to injury. Nat. Neurosci. 23, 676–689 (2020).
pubmed: 32284604 pmcid: 7611025 doi: 10.1038/s41593-020-0618-6
Chakarov, S. et al. Two distinct interstitial macrophage populations coexist across tissues in specific subtissular niches. Science 363, eaau0964 (2019).
pubmed: 30872492 doi: 10.1126/science.aau0964
Luissint, A.-C., Nusrat, A. & Parkos, C. A. JAM-related proteins in mucosal homeostasis and inflammation. Semin. Immunopathol. 36, 211–226 (2014).
pubmed: 24667924 pmcid: 4084508 doi: 10.1007/s00281-014-0421-0
La Manno, G. et al. RNA velocity of single cells. Nature 560, 494–498 (2018).
pubmed: 30089906 pmcid: 6130801 doi: 10.1038/s41586-018-0414-6
Aibar, S. et al. SCENIC: single-cell regulatory network inference and clustering. Nat. Methods 14, 1083–1086 (2017).
pubmed: 28991892 pmcid: 5937676 doi: 10.1038/nmeth.4463
Liu, Z. et al. Fate mapping via Ms4a3-expression history traces monocyte-derived cells. Cell 178, 1509–1525 (2019).
pubmed: 31491389 doi: 10.1016/j.cell.2019.08.009
Butovsky, O. et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 17, 131–143 (2014).
pubmed: 24316888 doi: 10.1038/nn.3599
Joseph, N. M. et al. Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J. Clin. Invest. 121, 3398–3411 (2011).
pubmed: 21865643 pmcid: 3163971 doi: 10.1172/JCI58186
Sakata, K., Kunieda, T., Furuta, T. & Sato, A. Selective destruction of intestinal nervous elements by local application of benzalkonium solution in the rat. Experientia 35, 1611–1613 (1979).
pubmed: 520469 doi: 10.1007/BF01953222
Sato, A. et al. Pathophysiology of aganglionic colon and anorectum: an experimental study on aganglionosis produced by a new method in the rat. J. Pediatr. Surg. 13, 399–435 (1978).
pubmed: 682089 doi: 10.1016/S0022-3468(78)80464-3
Gombash, S. E. et al. Intravenous AAV9 efficiently transduces myenteric neurons in neonate and juvenile mice. Front. Mol. Neurosci. 7, 81 (2014).
pubmed: 25360081 pmcid: 4197761 doi: 10.3389/fnmol.2014.00081
Zöller, T. et al. Silencing of TGFβ signalling in microglia results in impaired homeostasis. Nat. Commun. 9, 4011 (2018).
pubmed: 30275444 pmcid: 6167353 doi: 10.1038/s41467-018-06224-y
Wrana, J. L., Attisano, L., Wieser, R., Ventura, F. & Massagué, J. Mechanism of activation of the TGF-β receptor. Nature 370, 341–347 (1994).
pubmed: 8047140 doi: 10.1038/370341a0
Bain, C. C. et al. TGFβR signalling controls CD103
pubmed: 28931816 pmcid: 5607002 doi: 10.1038/s41467-017-00658-6
Drokhlyansky, E. et al. The human and mouse enteric nervous system at single-cell resolution. Cell 182, 1606–1622 (2020).
pubmed: 32888429 pmcid: 8358727 doi: 10.1016/j.cell.2020.08.003
Elmentaite, R. et al. Cells of the human intestinal tract mapped across space and time. Nature 597, 250–255 (2021).
pubmed: 34497389 pmcid: 8426186 doi: 10.1038/s41586-021-03852-1
Cipriani, G. et al. Muscularis propria macrophages alter the proportion of nitrergic but not cholinergic gastric myenteric neurons. Cell. Mol. Gastroenterol. Hepatol. 7, 689–691 (2019).
Ahrends, T. et al. Enteric pathogens induce tissue tolerance and prevent neuronal loss from subsequent infections. Cell 184, 5715–5727 (2021).
pubmed: 34717799 pmcid: 8595755 doi: 10.1016/j.cell.2021.10.004
Wang, P. et al. Macrophage achieves self-protection against oxidative stress-induced ageing through the Mst-Nrf2 axis. Nat. Commun. 10, 755 (2019).
pubmed: 30765703 pmcid: 6376064 doi: 10.1038/s41467-019-08680-6
Schafer, D. P. et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691–705 (2012).
pubmed: 22632727 pmcid: 3528177 doi: 10.1016/j.neuron.2012.03.026
Walton, N. M. et al. Microglia instruct subventricular zone neurogenesis. Glia 54, 815–825 (2006).
pubmed: 16977605 doi: 10.1002/glia.20419
Kierdorf, K. et al. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 16, 273–280 (2013).
pubmed: 23334579 doi: 10.1038/nn.3318
Matcovitch-Natan, O. et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science 353, aad8670 (2016).
pubmed: 27338705 doi: 10.1126/science.aad8670
Lenz, K. M. & Nelson, L. H. Microglia and beyond: innate immune cells as regulators of brain development and behavioral function. Front. Immunol. 9, 698 (2018).
pubmed: 29706957 pmcid: 5908908 doi: 10.3389/fimmu.2018.00698
Orłowski, D., Sołtys, Z. & Janeczko, K. Morphological development of microglia in the postnatal rat brain. A quantitative study. Int. J. Dev. Neurosci. 21, 445–450 (2003).
pubmed: 14659995 doi: 10.1016/j.ijdevneu.2003.09.001
Parkhurst, C. N. et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155, 1596–1609 (2013).
pubmed: 24360280 pmcid: 4033691 doi: 10.1016/j.cell.2013.11.030
Nelson, L. H. & Lenz, K. M. Microglia depletion in early life programs persistent changes in social, mood-related, and locomotor behavior in male and female rats. Behav. Brain Res. https://doi.org/10.1016/j.bbr.2016.09.006 (2017).
Athow, A. C., Filipe, M. I. & Drake, D. P. Hyperganglionosis mimicking Hirschsprung’s disease. Arch. Dis. Child. 66, 1300–1303 (1991).
pubmed: 1755642 pmcid: 1793294 doi: 10.1136/adc.66.11.1300
Wedel, T. et al. Enteric nerves and interstitial cells of Cajal are altered in patients with slow-transit constipation and megacolon. Gastroenterology 123, 1459–1467 (2002).
pubmed: 12404220 doi: 10.1053/gast.2002.36600
Bassotti, G., Villanacci, V. & Nejad, M. R. Chronic constipation: no more idiopathic, but a true neuropathological entity. Gastroenterol. Hepatol. Bed Bench 4, 109–115 (2011).
pubmed: 24834167 pmcid: 4017417
Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79–91 (2013).
pubmed: 23273845 doi: 10.1016/j.immuni.2012.12.001
Hao, M. M. et al. Early emergence of neural activity in the developing mouse enteric nervous system. J. Neurosci. 31, 15352 (2011).
pubmed: 22031881 pmcid: 6703522 doi: 10.1523/JNEUROSCI.3053-11.2011
Vanden Berghe, P., Kenyon, J. L. & Smith, T. K. Mitochondrial Ca
pubmed: 12177194 pmcid: 6757860 doi: 10.1523/JNEUROSCI.22-16-06962.2002
Schafer, D. P., Lehrman, E. K., Heller, C. T. & Stevens, B. An engulfment assay: a protocol to assess interactions between CNS phagocytes and neurons. J. Vis. Exp. https://doi.org/10.3791/51482 (2014).
Becker, L. et al. Age-dependent shift in macrophage polarisation causes inflammation-mediated degeneration of enteric nervous system. Gut https://doi.org/10.1136/gutjnl-2016-312940 (2017).
Picelli, S. et al. Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9, 171–181 (2014).
pubmed: 24385147 doi: 10.1038/nprot.2014.006
Cifone, M. G. et al. Dexamethasone-induced thymocyte apoptosis: apoptotic signal involves the sequential activation of hyposphoinositide-specific phospholipase C, acidic sphingomyelinase, and caspases. Blood 93, 2282–2296 (1999).
pubmed: 10090938 doi: 10.1182/blood.V93.7.2282
Cooper, H. S., Murthy, S. N., Shah, R. S. & Sedergran, D. J. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab. Invest. 69, 238–249 (1993).
pubmed: 8350599
Boirivant, M., Fuss, I. J., Chu, A. & Strober, W. Oxazolone colitis: a murine model of T helper cell type 2 colitis treatable with antibodies to interleukin 4. J. Exp. Med. 188, 1929–1939 (1998).
pubmed: 9815270 pmcid: 2212414 doi: 10.1084/jem.188.10.1929
Kennedy, R. J. et al. Interleukin 10-deficient colitis: new similarities to human inflammatory bowel disease. Br. J. Surg. 87, 1346–1351 (2000).
pubmed: 11044159 doi: 10.1046/j.1365-2168.2000.01615.x

Auteurs

Maria Francesca Viola (MF)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Marta Chavero-Pieres (M)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Elodie Modave (E)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Marcello Delfini (M)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Nathalie Stakenborg (N)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Maria Cuende Estévez (MC)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Naomi Fabre (N)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Iris Appeltans (I)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Tobie Martens (T)

Laboratory for Enteric NeuroScience, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Katy Vandereyken (K)

Laboratory of Reproductive Genomics, Department of Human Genetics, KU Leuven, Leuven, Belgium.
KU Leuven Institute for Single Cell Omics, KU Leuven, Leuven, Belgium.

Hannah Theobald (H)

Quantitative Systems Biology, LIMES-Institute, University of Bonn, Bonn, Germany.

Jens Van Herck (J)

Laboratory of Reproductive Genomics, Department of Human Genetics, KU Leuven, Leuven, Belgium.

Philippe Petry (P)

Institute of Neuropathology, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Faculty of Biology, University of Freiburg, Freiburg, Germany.

Simon Verheijden (S)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.
Janssen Research and Development, Janssen Pharmaceutica NV, Beerse, Belgium.

Sebastiaan De Schepper (S)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.
UK Dementia Research Institute, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences, University College London, London, UK.

Alejandro Sifrim (A)

KU Leuven Institute for Single Cell Omics, KU Leuven, Leuven, Belgium.
Laboratory of Multi-Omic Integrative Bioinformatics, Department of Genetics, KU Leuven, Leuven, Belgium.
Leuven AI Institute, KU Leuven, Leuven, Belgium.

Zhaoyuan Liu (Z)

Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

Florent Ginhoux (F)

Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
Singapore Immunology Network, Agency for Science, Technology & Research, Singapore, Singapore.
Translational Immunology Institute, SingHealth Duke-NUS Academic Medical Centre, Singapore, Singapore.

Mohamad Azhar (M)

Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, Columbia, SC, USA.

Andreas Schlitzer (A)

Quantitative Systems Biology, LIMES-Institute, University of Bonn, Bonn, Germany.

Gianluca Matteoli (G)

Laboratory for Mucosal Immunology, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Katrin Kierdorf (K)

Institute of Neuropathology, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Centre for Integrative Biological Signalling Studies, University of Freiburg, Freiburg, Germany.
Center for Basics in NeuroModulation (NeuroModulBasics), Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Marco Prinz (M)

Institute of Neuropathology, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Basics in NeuroModulation (NeuroModulBasics), Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Signalling Research Centres BIOSS and CIBSS, University of Freiburg, Freiburg, Germany.

Pieter Vanden Berghe (P)

Laboratory for Enteric NeuroScience, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium.

Thierry Voet (T)

Laboratory of Reproductive Genomics, Department of Human Genetics, KU Leuven, Leuven, Belgium.
KU Leuven Institute for Single Cell Omics, KU Leuven, Leuven, Belgium.

Guy Boeckxstaens (G)

Laboratory for Intestinal Neuro-Immune Interaction, Translational Research Center for Gastrointestinal Disorders, Department of Chronic Diseases, Metabolism and Ageing, KU Leuven, Leuven, Belgium. guy.boeckxstaens@kuleuven.be.
KU Leuven Institute for Single Cell Omics, KU Leuven, Leuven, Belgium. guy.boeckxstaens@kuleuven.be.

Articles similaires

Animals Tail Swine Behavior, Animal Animal Husbandry
alpha-Synuclein Humans Animals Mice Lewy Body Disease
Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger
Animals Natural Killer T-Cells Mice Adipose Tissue Lipid Metabolism

Classifications MeSH