Cell fate coordinates mechano-osmotic forces in intestinal crypt formation.
Animals
Cell Differentiation
Cell Lineage
Cell Movement
Cells, Cultured
Computer Simulation
Female
Intestinal Mucosa
/ cytology
Male
Mechanotransduction, Cellular
Mice, Inbred C57BL
Mice, Transgenic
Microscopy, Confocal
Microscopy, Video
Models, Biological
Morphogenesis
Myosin Type II
/ genetics
Organoids
Osmoregulation
Osmotic Pressure
Paneth Cells
/ metabolism
Sodium-Glucose Transport Proteins
/ genetics
Stem Cells
/ metabolism
Stress, Mechanical
Time Factors
Journal
Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
13
08
2020
accepted:
14
05
2021
pubmed:
23
6
2021
medline:
21
9
2021
entrez:
22
6
2021
Statut:
ppublish
Résumé
Intestinal organoids derived from single cells undergo complex crypt-villus patterning and morphogenesis. However, the nature and coordination of the underlying forces remains poorly characterized. Here, using light-sheet microscopy and large-scale imaging quantification, we demonstrate that crypt formation coincides with a stark reduction in lumen volume. We develop a 3D biophysical model to computationally screen different mechanical scenarios of crypt morphogenesis. Combining this with live-imaging data and multiple mechanical perturbations, we show that actomyosin-driven crypt apical contraction and villus basal tension work synergistically with lumen volume reduction to drive crypt morphogenesis, and demonstrate the existence of a critical point in differential tensions above which crypt morphology becomes robust to volume changes. Finally, we identified a sodium/glucose cotransporter that is specific to differentiated enterocytes that modulates lumen volume reduction through cell swelling in the villus region. Together, our study uncovers the cellular basis of how cell fate modulates osmotic and actomyosin forces to coordinate robust morphogenesis.
Identifiants
pubmed: 34155381
doi: 10.1038/s41556-021-00700-2
pii: 10.1038/s41556-021-00700-2
pmc: PMC7611267
mid: EMS124566
doi:
Substances chimiques
Sodium-Glucose Transport Proteins
0
Myosin Type II
EC 3.6.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Video-Audio Media
Langues
eng
Sous-ensembles de citation
IM
Pagination
733-744Subventions
Organisme : Swiss National Science Foundation
ID : 157531
Pays : Switzerland
Organisme : European Research Council
ID : 758617
Pays : International
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Spit, M., Koo, B.-K. & Maurice, M. M. Tales from the crypt: intestinal niche signals in tissue renewal, plasticity and cancer. Open Biol. 8, 180120 (2018).
pubmed: 30209039
pmcid: 6170508
doi: 10.1098/rsob.180120
Wells, J. M. & Spence, J. R. How to make an intestine. Development 141, 752–760 (2014).
pubmed: 24496613
pmcid: 3912826
doi: 10.1242/dev.097386
Wang, S., Walton, K. D. & Gumucio, D. L. Signals and forces shaping organogenesis of the small intestine. Curr. Top. Dev. Biol. 132, 31–65 (2019).
pubmed: 30797512
doi: 10.1016/bs.ctdb.2018.12.001
Walton, K. D., Mishkind, D., Riddle, M. R., Tabin, C. J. & Gumucio, D. L. Blueprint for an intestinal villus: species-specific assembly required. Wiley Interdiscip. Rev. Dev. Biol. 7, e317 (2018).
pubmed: 29513926
pmcid: 6002883
doi: 10.1002/wdev.317
Hughes, A. J. et al. Engineered tissue folding by mechanical compaction of the mesenchyme. Dev. Cell. 44, 165–178 (2018).
pubmed: 29290586
doi: 10.1016/j.devcel.2017.12.004
Shyer, A. E., Huycke, T. R., Lee, C., Mahadevan, L. & Tabin, C. J. Bending gradients: how the intestinal stem cell gets its home. Cell 161, 569–580 (2015).
pubmed: 25865482
pmcid: 4409931
doi: 10.1016/j.cell.2015.03.041
Farin, H. F. et al. Visualization of a short-range Wnt gradient in the intestinal stem-cell niche. Nature 530, 340–343 (2016).
pubmed: 26863187
doi: 10.1038/nature16937
Nerurkar, N. L., Mahadevan, L. & Tabin, C. J. BMP signaling controls buckling forces to modulate looping morphogenesis of the gut. Proc. Natl Acad. Sci. USA 114, 2277–2282 (2017).
pubmed: 28193855
pmcid: 5338480
doi: 10.1073/pnas.1700307114
Walton, K. D. et al. Villification in the mouse: Bmp signals control intestinal villus patterning. Development 143, 427–436 (2016).
pubmed: 26721501
pmcid: 4760312
doi: 10.1242/dev.135400
Hartl, L., Huelsz-Prince, G., van Zon, J. & Tans, S. J. Apical constriction is necessary for crypt formation in small intestinal organoids. Dev. Biol. 450, 76–81 (2019).
pubmed: 30914321
doi: 10.1016/j.ydbio.2019.03.009
Sumigray, K. D., Terwilliger, M. & Lechler, T. Morphogenesis and compartmentalization of the intestinal crypt. Dev. Cell 45, 183–197 (2018).
pubmed: 29689194
pmcid: 5987226
doi: 10.1016/j.devcel.2018.03.024
Dahl-Jensen, S. & Grapin-Botton, A. The physics of organoids: a biophysical approach to understanding organogenesis. Development 144, 946–951 (2017).
pubmed: 28292839
doi: 10.1242/dev.143693
Kretzschmar, K. & Clevers, H. Everything has its time: Id2 clocks embryonic specification of Lgr5
pubmed: 28298434
pmcid: 5376976
doi: 10.15252/embj.201796482
Sato, T. & Clevers, H. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 340, 1190–1194 (2013).
pubmed: 23744940
doi: 10.1126/science.1234852
Serra, D. et al. Self-organization and symmetry breaking in intestinal organoid development. Nature 569, 66–72 (2019).
pubmed: 31019299
pmcid: 6544541
doi: 10.1038/s41586-019-1146-y
Sato, T. et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415–418 (2011).
pubmed: 21113151
doi: 10.1038/nature09637
Sato, T. et al. Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche. Nature 459, 262–265 (2009).
pubmed: 19329995
doi: 10.1038/nature07935
Riedl, J. et al. Lifeact mice for studying F-actin dynamics. Nat. Methods 7, 168–169 (2010).
pubmed: 20195247
doi: 10.1038/nmeth0310-168
Okuda, S., Inoue, Y. & Adachi, T. Three-dimensional vertex model for simulating multicellular morphogenesis. Biophys. Physicobiol. 12, 13–20 (2015).
Messal, H. A. et al. Tissue curvature and apicobasal mechanical tension imbalance instruct cancer morphogenesis. Nature 566, 126–130 (2019).
pubmed: 30700911
pmcid: 7025886
doi: 10.1038/s41586-019-0891-2
Hannezo, E., Prost, J. & Joanny, J.-F. Theory of epithelial sheet morphology in three dimensions. Proc. Natl Acad. Sci. USA 111, 27–32 (2014).
pubmed: 24367079
doi: 10.1073/pnas.1312076111
Rozman, J., Krajnc, M. & Ziherl, P. Collective cell mechanics of small-organoid morphologies. Nat. Commun. 11, 3805 (2020).
pubmed: 32732886
pmcid: 7393134
doi: 10.1038/s41467-020-17535-4
Li, J. et al. The strength of mechanical forces determines the differentiation of alveolar epithelial cells. Dev. Cell 44, 297–312 (2018).
pubmed: 29408236
doi: 10.1016/j.devcel.2018.01.008
Fernandez-Gonzalez, R. et al. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 17, 736–743 (2009).
pubmed: 19879198
pmcid: 2854079
doi: 10.1016/j.devcel.2009.09.003
Maître, J.-L. et al. Asymmetric division of contractile domains couples cell positioning and fate specification. Nature 536, 344–348 (2016).
pubmed: 27487217
pmcid: 4998956
doi: 10.1038/nature18958
Munjal, A. & Lecuit, T. Actomyosin networks and tissue morphogenesis. Development 141, 1789–1793 (2014).
pubmed: 24757001
doi: 10.1242/dev.091645
Fath, K. R., Mamajiwalla, S. N. & Burgess, D. R. The cytoskeleton in development of epithelial cell polarity. J. Cell Sci. Suppl. 17, 65–73 (1993).
pubmed: 7511618
doi: 10.1242/jcs.1993.Supplement_17.10
Zhang, Y. et al. Mouse models of MYH9-related disease: mutations in nonmuscle myosin II-A. Blood 119, 238–250 (2012).
pubmed: 21908426
pmcid: 3251230
doi: 10.1182/blood-2011-06-358853
Chabaud, M. et al. Cell migration and antigen capture are antagonistic processes coupled by myosin II in dendritic cells. Nat. Commun. 6, 7526 (2015).
pubmed: 26109323
doi: 10.1038/ncomms8526
Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global double-fluorescent Cre reporter mouse. Genesis 45, 593–605 (2007).
pubmed: 17868096
doi: 10.1002/dvg.20335
Zhao, B. et al. The non-muscle-myosin-II heavy chain Myh9 mediates colitis-induced epithelium injury by restricting Lgr5
pubmed: 25968904
doi: 10.1038/ncomms8166
Jacobelli, J. et al. Confinement-optimized three-dimensional T cell amoeboid motility is modulated via myosin IIA-regulated adhesions. Nat. Immunol. 11, 953–961 (2010).
pubmed: 20835229
pmcid: 2943564
doi: 10.1038/ni.1936
Odenwald, M. A. et al. The scaffolding protein ZO-1 coordinates actomyosin and epithelial apical specializations in vitro and in vivo. J. Biol. Chem. 293, 17317–17335 (2018).
pubmed: 30242130
pmcid: 6231134
doi: 10.1074/jbc.RA118.003908
Jülicher, F. & Lipowsky, R. Shape transformations of vesicles with intramembrane domains. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 53, 2670–2683 (1996).
pubmed: 9964554
Miyoshi, H. et al. Prostaglandin E2 promotes intestinal repair through an adaptive cellular response of the epithelium. EMBO J. 36, 5–24 (2017).
pubmed: 27797821
doi: 10.15252/embj.201694660
Ricciotti, E. & FitzGerald, G. A. Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31, 986–1000 (2011).
pubmed: 21508345
pmcid: 3081099
doi: 10.1161/ATVBAHA.110.207449
Bagriantsev, S. N., Gracheva, E. O. & Gallagher, P. G. Piezo proteins: regulators of mechanosensation and other cellular processes. J. Biol. Chem. 289, 31673–31681 (2014).
pubmed: 25305018
pmcid: 4231648
doi: 10.1074/jbc.R114.612697
He, L., Si, G., Huang, J., Samuel, A. D. T. & Perrimon, N. Mechanical regulation of stem-cell differentiation by the stretch-activated Piezo channel. Nature 555, 103–106 (2018).
pubmed: 29414942
pmcid: 6101000
doi: 10.1038/nature25744
Syeda, R. et al. Chemical activation of the mechanotransduction channel Piezo1. eLife 4, 1884 (2015).
doi: 10.7554/eLife.07369
Grant, C. N. et al. Human and mouse tissue-engineered small intestine both demonstrate digestive and absorptive function. Am. J. Physiol. Gastrointest. Liver Physiol. 308, G664–G677 (2015).
pubmed: 25573173
pmcid: 4398842
doi: 10.1152/ajpgi.00111.2014
Pouille, P.-A., Ahmadi, P., Brunet, A.-C. & Farge, E. Mechanical signals trigger Myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci. Signal. 2, ra16 (2009).
pubmed: 19366994
doi: 10.1126/scisignal.2000098
Nishimura, T. & Takeichi, M. Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 135, 1493–1502 (2008).
pubmed: 18339671
doi: 10.1242/dev.019646
Behrndt, M. et al. Forces driving epithelial spreading in zebrafish gastrulation. Science 338, 257–260 (2012).
pubmed: 23066079
doi: 10.1126/science.1224143
Dawes-Hoang, R. E. et al. folded gastrulation, cell shape change and the control of myosin localization. Development 132, 4165–4178 (2005).
pubmed: 16123312
doi: 10.1242/dev.01938
Chauhan, B. K., Lou, M., Zheng, Y. & Lang, R. A. Balanced Rac1 and RhoA activities regulate cell shape and drive invagination morphogenesis in epithelia. Proc. Natl Acad. Sci. USA 108, 18289–18294 (2011).
pubmed: 22021442
pmcid: 3215052
doi: 10.1073/pnas.1108993108
Sui, L. et al. Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms. Nat. Commun. 9, 4620 (2018).
pubmed: 30397306
pmcid: 6218478
doi: 10.1038/s41467-018-06497-3
Rout, W. R., Formal, S. B., Dammin, G. J. & Giannella, R. A. Pathophysiology of Salmonella diarrhea in the rhesus monkey: intestinal transport, morphological and bacteriological studies. Gastroenterology 67, 59–70 (1974).
pubmed: 4210000
doi: 10.1016/S0016-5085(19)32926-9
Boshuizen, J. A. et al. Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J. Virol. 77, 13005–13016 (2003).
pubmed: 14645557
pmcid: 296055
doi: 10.1128/JVI.77.24.13005-13016.2003
Fouchard, J. et al. Curling of epithelial monolayers reveals coupling between active bending and tissue tension. Proc. Natl Acad. Sci. USA 117, 9377–9383 (2020).
pubmed: 32284424
pmcid: 7196817
doi: 10.1073/pnas.1917838117
Krndija, D. et al. Active cell migration is critical for steady-state epithelial turnover in the gut. Science 365, 705–710 (2019).
pubmed: 31416964
doi: 10.1126/science.aau3429
Perez-Gonzalez et al. Mechanical compartmentalization of the intestinal organoid enables crypt folding and collective cell migration. Nat. Cell Biol. https://doi.org/10.1038/s41556-021-00699-6 (2021).
Chan, C. J. et al. Hydraulic control of mammalian embryo size and cell fate. Nature 571, 112–116 (2019).
pubmed: 31189957
doi: 10.1038/s41586-019-1309-x
Chan, C. J. & Hiiragi, T. Integration of luminal pressure and signalling in tissue self-organization. Development 147, dev181297 (2020).
pubmed: 32122910
doi: 10.1242/dev.181297
Dumortier, J. G. et al. Hydraulic fracturing and active coarsening position the lumen of the mouse blastocyst. Science 365, 465–468 (2019).
pubmed: 31371608
doi: 10.1126/science.aaw7709
Szegedy, C. et al. Going deeper with convolutions. Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition, 1–9 (2015); https://doi.org/10.1109/CVPR.2015.7298594
Barbier de Reuille, P. et al. MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4, 05864 (2015).
pubmed: 25946108
doi: 10.7554/eLife.05864
de Reuille, P. B., Robinson, S. & Smith, R. S. Quantifying cell shape and gene expression in the shoot apical meristem using MorphoGraphX. Methods Mol. Biol. 1080, 121–134 (2014).
pubmed: 24132424
doi: 10.1007/978-1-62703-643-6_10
Yang, Q., Roiz, D., Mereu, L., Daube, M. & Hajnal, A. The invading anchor cell induces lateral membrane constriction during vulval lumen morphogenesis in C. elegans. Dev. Cell 42, 271–285 (2017).
pubmed: 28787593
doi: 10.1016/j.devcel.2017.07.008