Notum produced by Paneth cells attenuates regeneration of aged intestinal epithelium.


Journal

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

Informations de publication

Date de publication:
07 2019
Historique:
received: 12 04 2016
accepted: 10 06 2019
pubmed: 12 7 2019
medline: 8 10 2019
entrez: 12 7 2019
Statut: ppublish

Résumé

A decline in stem cell function impairs tissue regeneration during ageing, but the role of the stem-cell-supporting niche in ageing is not well understood. The small intestine is maintained by actively cycling intestinal stem cells that are regulated by the Paneth cell niche

Identifiants

pubmed: 31292548
doi: 10.1038/s41586-019-1383-0
pii: 10.1038/s41586-019-1383-0
pmc: PMC8151802
mid: NIHMS1626400
doi:

Substances chimiques

Lgr5 protein, mouse 0
PPAR alpha 0
Receptors, G-Protein-Coupled 0
Wnt Proteins 0
Mechanistic Target of Rapamycin Complex 1 EC 2.7.11.1
Esterases EC 3.1.-
Notum protein, human EC 3.1.1.-
Notum protein, mouse EC 3.1.1.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

398-402

Subventions

Organisme : NIGMS NIH HHS
ID : T32 GM007287
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA014051
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NIA NIH HHS
ID : R00 AG045144
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA034992
Pays : United States

Références

Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003–1007 (2007).
pubmed: 17934449 doi: 10.1038/nature06196
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
Sengupta, S., Peterson, T. R., Laplante, M., Oh, S. & Sabatini, D. M. mTORC1 controls fasting-induced ketogenesis and its modulation by ageing. Nature 468, 1100–1104 (2010).
pubmed: 21179166 doi: 10.1038/nature09584
Molofsky, A. V. et al. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443, 448–452 (2016).
doi: 10.1038/nature05091
Rossi, D. J. et al. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447, 725–729 (2007).
pubmed: 17554309 doi: 10.1038/nature05862
Conboy, I. M. & Rando, T. A. Heterochronic parabiosis for the study of the effects of aging on stem cells and their niches. Cell Cycle 11, 2260–2267 (2012).
pubmed: 22617385 pmcid: 3383588 doi: 10.4161/cc.20437
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
Warren, P. M., Pepperman, M. A. & Montgomery, R. D. Age changes in small-intestinal mucosa. Lancet 312, 849–850 (1978).
doi: 10.1016/S0140-6736(78)92639-9
Feibusch, J. M. & Holt, P. R. Impaired absorptive capacity for carbohydrate in the aging human. Dig. Dis. Sci. 27, 1095–1100 (1982).
pubmed: 7172959 doi: 10.1007/BF01391447
Feldman, M., Cryer, B., McArthur, K. E., Huet, B. A. & Lee, E. Effects of aging and gastritis on gastric acid and pepsin secretion in humans: a prospective study. Gastroenterology 110, 1043–1052 (1996).
pubmed: 8612992 doi: 10.1053/gast.1996.v110.pm8612992
Potten, C. S., Martin, K. & Kirkwood, T. B. Ageing of murine small intestinal stem cells. Novartis Found Symp. 235, 66–79 (2001).
pubmed: 11280034
Yilmaz, O. H. et al. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486, 490–495 (2012).
pubmed: 22722868 pmcid: 3387287 doi: 10.1038/nature11163
Nalapareddy, K. et al. Canonical Wnt signaling ameliorates aging of intestinal stem cells. Cell Rep. 18, 2608–2621 (2017).
pubmed: 28297666 pmcid: 5987258 doi: 10.1016/j.celrep.2017.02.056
Mihaylova, M. M. et al. Fasting activates fatty acid oxidation to enhance intestinal stem cell function during homeostasis and aging. Cell Stem Cell 22, 769–778 (2018).
pubmed: 29727683 pmcid: 5940005 doi: 10.1016/j.stem.2018.04.001
Giráldez, A. J., Copley, R. R. & Cohen, S. M. HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev. Cell 2, 667–676 (2002).
pubmed: 12015973 doi: 10.1016/S1534-5807(02)00180-6
Kakugawa, S. et al. Notum deacylates Wnt proteins to suppress signalling activity. Nature 519, 187–192 (2015).
pubmed: 25731175 pmcid: 4376489 doi: 10.1038/nature14259
Shoshkes-Carmel, M. et al. Subepithelial telocytes are an important source of Wnts that supports intestinal crypts. Nature 557, 242–246 (2018).
pubmed: 29720649 pmcid: 5966331 doi: 10.1038/s41586-018-0084-4
Degirmenci, B., Valenta, T., Dimitrieva, S., Hausmann, G. & Basler, K. GLI1-expressing mesenchymal cells form the essential Wnt-secreting niche for colon stem cells. Nature 558, 449–453 (2018).
pubmed: 29875413 doi: 10.1038/s41586-018-0190-3
Farin, H. F., Van Es, J. H. & Clevers, H. Redundant sources of Wnt regulate intestinal stem cells and promote formation of Paneth cells. Gastroenterology 143, 1518–1529 (2012).
pubmed: 22922422 doi: 10.1053/j.gastro.2012.08.031
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
McCay, C. M., Maynard, L. A., Sperling, G. & Barnes, L. L. Retarded growth, life span, ultimate body size and age changes in the albino rat after feeding diets restricted in calories. Nutr. Rev. 33, 241–243 (1975).
pubmed: 1095975 doi: 10.1111/j.1753-4887.1975.tb05227.x
Harrison, D. E. et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460, 392–395 (2009).
pubmed: 19587680 pmcid: 2786175 doi: 10.1038/nature08221
Lamming, D. W. et al. Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 335, 1638–1643 (2012).
pubmed: 22461615 pmcid: 3324089 doi: 10.1126/science.1215135
Naillat, F. et al. Identification of the genes regulated by Wnt-4, a critical signal for commitment of the ovary. Exp. Cell Res. 332, 163–178 (2015).
pubmed: 25645944 doi: 10.1016/j.yexcr.2015.01.010
Suciu, R. M., Cognetta, A. B., III, Potter, Z. E. & Cravatt, B. F. Selective irreversible inhibitors of the Wnt-deacylating enzyme NOTUM developed by activity-based protein profiling. ACS Med. Chem. Lett. 9, 563–568 (2018).
pubmed: 29937983 pmcid: 6004566 doi: 10.1021/acsmedchemlett.8b00191
Longley, D. B., Harkin, D. P. & Johnston, P. G. 5-fluorouracil: mechanisms of action and clinical strategies. Nat. Rev. Cancer 3, 330–338 (2003).
pubmed: 12724731 doi: 10.1038/nrc1074
Song, M. K., Park, M. Y. & Sung, M. K. 5-fluorouracil-induced changes of intestinal integrity biomarkers in BALB/c mice. J. Cancer Prev. 18, 322–329 (2013).
pubmed: 25337561 pmcid: 4189444 doi: 10.15430/JCP.2013.18.4.322
Nusse, R. & Clevers, H. Wnt/β-catenin signaling, disease, and emerging therapeutic modalities. Cell 169, 985–999 (2017).
pubmed: 28575679 doi: 10.1016/j.cell.2017.05.016
Kim, T. H., Escudero, S. & Shivdasani, R. A. Intact function of Lgr5 receptor-expressing intestinal stem cells in the absence of Paneth cells. Proc. Natl Acad. Sci. USA 109, 3932–3937 (2012).
pubmed: 22355124 doi: 10.1073/pnas.1113890109 pmcid: 3309789
Zou, W. Y. et al. Epithelial WNT ligands are essential drivers of intestinal stem cell activation. Cell Rep. 22, 1003–1015 (2018).
pubmed: 29386123 pmcid: 5798462 doi: 10.1016/j.celrep.2017.12.093
Kozar, S. et al. Continuous clonal labeling reveals small numbers of functional stem cells in intestinal crypts and adenomas. Cell Stem Cell 13, 626–633 (2013).
pubmed: 24035355 doi: 10.1016/j.stem.2013.08.001
Frey, J. L. et al. Wnt–Lrp5 signaling regulates fatty acid metabolism in the osteoblast. Mol. Cell. Biol. 35, 1979–1991 (2015).
pubmed: 25802278 pmcid: 4420919 doi: 10.1128/MCB.01343-14
Huels, D. J. et al. Wnt ligands influence tumour initiation by controlling the number of intestinal stem cells. Nat. Commun. 9, 1132 (2018).
pubmed: 29556067 pmcid: 5859272 doi: 10.1038/s41467-018-03426-2
Beyaz, S. et al. High-fat diet enhances stemness and tumorigenicity of intestinal progenitors. Nature 531, 53–58 (2016).
pubmed: 26935695 pmcid: 4846772 doi: 10.1038/nature17173
Chang, S., Goldstein, N. E. & Dharmarajan, K. V. Managing an older adult with cancer: considerations for radiation oncologists. BioMed Res. Int. 2017, 1695101 (2017).
pubmed: 29387715 pmcid: 5745659
Sato, T. et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology 141, 1762–1772 (2011).
pubmed: 21889923 doi: 10.1053/j.gastro.2011.07.050
Chen, B. et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 5, 100–107 (2009).
pubmed: 19125156 pmcid: 2628455 doi: 10.1038/nchembio.137
Shalem, O. et al. Genome-scale CRISPR–Cas9 knockout screening in human cells. Science 343, 84–87 (2014).
pubmed: 24336571 doi: 10.1126/science.1247005
Sanjana, N. E., Shalem, O. & Zhang, F. Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods 11, 783–784 (2014).
pubmed: 25075903 pmcid: 4486245 doi: 10.1038/nmeth.3047
Konermann, S. et al. Genome-scale transcriptional activation by an engineered CRISPR–Cas9 complex. Nature 517, 583–588 (2015).
pubmed: 25494202 doi: 10.1038/nature14136
Dahlman, J. E. et al. Orthogonal gene knockout and activation with a catalytically active Cas9 nuclease. Nat. Biotechnol. 33, 1159–1161 (2015).
pubmed: 26436575 pmcid: 4747789 doi: 10.1038/nbt.3390
Sánchez-Rivera, F. J. et al. Rapid modelling of cooperating genetic events in cancer through somatic genome editing. Nature 516, 428–431 (2014).
pubmed: 25337879 pmcid: 4292871 doi: 10.1038/nature13906
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 17.1.2001 (2011).
doi: 10.14806/ej.17.1.200
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886 doi: 10.1093/bioinformatics/bts635
Lawrence, M. et al. Software for computing and annotating genomic ranges. PLOS Comput. Biol. 9, e1003118 (2013).
pubmed: 23950696 pmcid: 3738458 doi: 10.1371/journal.pcbi.1003118
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281 pmcid: 4302049 doi: 10.1186/s13059-014-0550-8
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).
pubmed: 16199517 pmcid: 1239896 doi: 10.1073/pnas.0506580102
Adhikary, T. et al. Genomewide analyses define different modes of transcriptional regulation by peroxisome proliferator-activated receptor-β/δ (PPARβ/δ). PLoS ONE 6, e16344 (2011).
pubmed: 21283829 pmcid: 3023804 doi: 10.1371/journal.pone.0016344
Kwiatkowski, D. J. et al. A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells. Hum. Mol. Genet. 11, 525–534 (2002).
pubmed: 11875047 doi: 10.1093/hmg/11.5.525
el Marjou, F. et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39, 186–193 (2004).
pubmed: 15282745 doi: 10.1002/gene.20042
Roper, J. et al. Colonoscopy-based colorectal cancer modeling in mice with CRISPR-Cas9 genome editing and organoid transplantation. Nat. Protoc. 13, 217–234 (2018).
pubmed: 29300388 pmcid: 6145089 doi: 10.1038/nprot.2017.136
Roper, J. et al. In vivo genome editing and organoid transplantation models of colorectal cancer and metastasis. Nat. Biotechnol. 35, 569–576 (2017).
pubmed: 28459449 pmcid: 5462879 doi: 10.1038/nbt.3836

Auteurs

Nalle Pentinmikko (N)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland.

Sharif Iqbal (S)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland.

Miyeko Mana (M)

The David H. Koch Institute for Integrative Cancer Research at MIT, Department of Biology, MIT, Cambridge, MA, USA.

Simon Andersson (S)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland.

Armand B Cognetta (AB)

The Skaggs Institute for Chemical Biology, Department of Chemical Physiology, The Scripps Research Institute, La Jolla, CA, USA.

Radu M Suciu (RM)

The Skaggs Institute for Chemical Biology, Department of Chemical Physiology, The Scripps Research Institute, La Jolla, CA, USA.

Jatin Roper (J)

Department of Medicine, Division of Gastroenterology, Duke University, Durham, NC, USA.

Kalle Luopajärvi (K)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland.

Eino Markelin (E)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland.

Swetha Gopalakrishnan (S)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland.

Olli-Pekka Smolander (OP)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland.

Santiago Naranjo (S)

The David H. Koch Institute for Integrative Cancer Research at MIT, Department of Biology, MIT, Cambridge, MA, USA.

Tuure Saarinen (T)

Obesity Research Unit, Research Programs Unit, Diabetes and Obesity, University of Helsinki, Helsinki, Finland.
Abdominal Center, Department of Gastrointestinal Surgery, Helsinki University Hospital, Helsinki, Finland.

Anne Juuti (A)

Abdominal Center, Department of Gastrointestinal Surgery, Helsinki University Hospital, Helsinki, Finland.

Kirsi Pietiläinen (K)

Obesity Research Unit, Research Programs Unit, Diabetes and Obesity, University of Helsinki, Helsinki, Finland.

Petri Auvinen (P)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland.

Ari Ristimäki (A)

Department of Pathology, Research Programs Unit and HUSLAB, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.

Nitin Gupta (N)

Atlanta Gastroenterology Associates, Atlanta, GA, USA.

Tuomas Tammela (T)

Cancer Biology and Genetics, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Tyler Jacks (T)

The David H. Koch Institute for Integrative Cancer Research at MIT, Department of Biology, MIT, Cambridge, MA, USA.
Howard Hughes Medical Institute, MIT, Cambridge, MA, USA.

David M Sabatini (DM)

The David H. Koch Institute for Integrative Cancer Research at MIT, Department of Biology, MIT, Cambridge, MA, USA.
Howard Hughes Medical Institute, MIT, Cambridge, MA, USA.
Whitehead Institute for Biomedical Research, Howard Hughes Medical Institute, Department of Biology, MIT, Cambridge, MA, USA.

Benjamin F Cravatt (BF)

The Skaggs Institute for Chemical Biology, Department of Chemical Physiology, The Scripps Research Institute, La Jolla, CA, USA.

Ömer H Yilmaz (ÖH)

The David H. Koch Institute for Integrative Cancer Research at MIT, Department of Biology, MIT, Cambridge, MA, USA.

Pekka Katajisto (P)

Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, Finland. pekka.katajisto@helsinki.fi.
Molecular and Integrative Bioscience Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland. pekka.katajisto@helsinki.fi.
Department of Biosciences and Nutrition, Karolinska Institutet, Stockholm, Sweden. pekka.katajisto@helsinki.fi.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH