Short-term post-fast refeeding enhances intestinal stemness via polyamines.

Journal

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

Informations de publication

Date de publication:
21 Aug 2024
Historique:
received: 15 03 2024
accepted: 17 07 2024
medline: 22 8 2024
pubmed: 22 8 2024
entrez: 21 8 2024
Statut: aheadofprint

Résumé

For over a century, fasting regimens have improved health, lifespan and tissue regeneration in diverse organisms, including humans

Identifiants

DOI: 10.1038/s41586-024-07840-z PMID: 39169180
pubmed: 39169180
doi: 10.1038/s41586-024-07840-z
pii: 10.1038/s41586-024-07840-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Cheng, C. W. & Yilmaz Ö, H. 100 Years of exploiting diet and nutrition for tissue regeneration. Cell Stem Cell 28, 370–373 (2021).
pubmed: 33667357 pmcid: 8811776 doi: 10.1016/j.stem.2021.02.014
Nencioni, A., Caffa, I., Cortellino, S. & Longo, V. D. Fasting and cancer: molecular mechanisms and clinical application. Nat. Rev. Cancer 18, 707–719 (2018).
pubmed: 30327499 pmcid: 6938162 doi: 10.1038/s41568-018-0061-0
Cheng, C. W. et al. Prolonged fasting reduces IGF-1/PKA to promote hematopoietic-stem-cell-based regeneration and reverse immunosuppression. Cell Stem Cell 14, 810–823 (2014).
pubmed: 24905167 pmcid: 4102383 doi: 10.1016/j.stem.2014.04.014
Longo, V. D. & Mattson, M. P. Fasting: molecular mechanisms and clinical applications. Cell Metab. 19, 181–192 (2014).
pubmed: 24440038 pmcid: 3946160 doi: 10.1016/j.cmet.2013.12.008
Weindruch, R., Walford, R. L., Fligiel, S. & Guthrie, D. The retardation of aging in mice by dietary restriction: longevity, cancer, immunity and lifetime energy intake. J. Nutr. 116, 641–654 (1986).
pubmed: 3958810 doi: 10.1093/jn/116.4.641
Mattison, J. A. et al. Caloric restriction improves health and survival of rhesus monkeys. Nat. Commun. 8, 14063 (2017).
pubmed: 28094793 pmcid: 5247583 doi: 10.1038/ncomms14063
Calibasi-Kocal, G. et al. Nutritional control of intestinal stem cells in homeostasis and tumorigenesis. Trends Endocrinol. Metab. 32, 20–35 (2021).
pubmed: 33277157 doi: 10.1016/j.tem.2020.11.003
Cerletti, M., Jang, Y. C., Finley, L. W., Haigis, M. C. & Wagers, A. J. Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell 10, 515–519 (2012).
pubmed: 22560075 pmcid: 3561899 doi: 10.1016/j.stem.2012.04.002
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.e4 (2018).
pubmed: 29727683 pmcid: 5940005 doi: 10.1016/j.stem.2018.04.001
Yilmaz Ö, 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
Vernieri, C. et al. Fasting-mimicking diet is safe and reshapes metabolism and antitumor immunity in cancer patients. Cancer Discov. https://doi.org/10.1158/2159-8290.Cd-21-0030 (2021).
Salvadori, G. et al. Fasting-mimicking diet blocks triple-negative breast cancer and cancer stem cell escape. Cell Metab. 33, 2247–2259.e6 (2021).
pubmed: 34731655 pmcid: 8769166 doi: 10.1016/j.cmet.2021.10.008
Alonso, S. & Yilmaz Ö, H. Nutritional regulation of intestinal stem cells. Annu. Rev. Nutr. 38, 273–301 (2018).
pubmed: 29799767 doi: 10.1146/annurev-nutr-082117-051644
Beumer, J. & Clevers, H. Cell fate specification and differentiation in the adult mammalian intestine. Nat. Rev. Mol. Cell Biol. 22, 39–53 (2021).
pubmed: 32958874 doi: 10.1038/s41580-020-0278-0
Goto, N. et al. Lymphatics and fibroblasts support intestinal stem cells in homeostasis and injury. Cell Stem Cell 29, 1246–1261.e6 (2022).
pubmed: 35931033 pmcid: 9720889 doi: 10.1016/j.stem.2022.06.013
Niec, R. E. et al. Lymphatics act as a signaling hub to regulate intestinal stem cell activity. Cell Stem Cell 29, 1067–1082.e18 (2022).
pubmed: 35728595 pmcid: 9271639 doi: 10.1016/j.stem.2022.05.007
Palikuqi, B. et al. Lymphangiocrine signals are required for proper intestinal repair after cytotoxic injury. Cell Stem Cell 29, 1262–1272.e5 (2022).
pubmed: 35931034 pmcid: 9387209 doi: 10.1016/j.stem.2022.07.007
Gehart, H. & Clevers, H. Tales from the crypt: new insights into intestinal stem cells. Nat. Rev. Gastroenterol. Hepatol. 16, 19–34 (2019).
pubmed: 30429586 doi: 10.1038/s41575-018-0081-y
Cheng, C. W. et al. Ketone body signaling mediates intestinal stem cell homeostasis and adaptation to diet. Cell 178, 1115–1131.e15 (2019).
pubmed: 31442404 pmcid: 6732196 doi: 10.1016/j.cell.2019.07.048
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
Igarashi, M. & Guarente, L. mTORC1 and SIRT1 cooperate to foster expansion of gut adult stem cells during calorie restriction. Cell 166, 436–450 (2016).
pubmed: 27345368 doi: 10.1016/j.cell.2016.05.044
Zismanov, V. et al. Phosphorylation of eIF2α is a translational control mechanism regulating muscle stem cell quiescence and self-renewal. Cell Stem Cell 18, 79–90 (2016).
pubmed: 26549106 doi: 10.1016/j.stem.2015.09.020
Llorens-Bobadilla, E. et al. Single-cell transcriptomics reveals a population of dormant neural stem cells that become activated upon brain injury. Cell Stem Cell 17, 329–340 (2015).
pubmed: 26235341 doi: 10.1016/j.stem.2015.07.002
Signer, R. A., Magee, J. A., Salic, A. & Morrison, S. J. Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature 509, 49–54 (2014).
pubmed: 24670665 pmcid: 4015626 doi: 10.1038/nature13035
Morral, C. et al. Zonation of ribosomal DNA transcription defines a stem cell hierarchy in colorectal cancer. Cell Stem Cell 26, 845–861.e12 (2020).
pubmed: 32396863 pmcid: 9006079 doi: 10.1016/j.stem.2020.04.012
Benitah, S. A. & Welz, P. S. Circadian regulation of adult stem cell homeostasis and aging. Cell Stem Cell 26, 817–831 (2020).
pubmed: 32502402 doi: 10.1016/j.stem.2020.05.002
Huch, M. et al. In vitro expansion of single Lgr5
pubmed: 23354049 pmcid: 3634804 doi: 10.1038/nature11826
Liu, G. Y. & Sabatini, D. M. mTOR at the nexus of nutrition, growth, ageing and disease. Nat. Rev. Mol. Cell Biol. 21, 183–203 (2020).
pubmed: 31937935 pmcid: 7102936 doi: 10.1038/s41580-019-0199-y
Manning, B. D. & Toker, A. AKT/PKB signaling: navigating the network. Cell 169, 381–405 (2017).
pubmed: 28431241 pmcid: 5546324 doi: 10.1016/j.cell.2017.04.001
Mulvihill, M. J. et al. Discovery of OSI-906: a selective and orally efficacious dual inhibitor of the IGF-1 receptor and insulin receptor. Future Med. Chem. 1, 1153–1171 (2009).
pubmed: 21425998 doi: 10.4155/fmc.09.89
Burger, M. T. et al. Identification of NVP-BKM120 as a potent, selective, orally bioavailable class I PI3 kinase inhibitor for treating cancer. ACS Med. Chem. Lett. 2, 774–779 (2011).
pubmed: 24900266 pmcid: 4017971 doi: 10.1021/ml200156t
Haber, A. L. et al. A single-cell survey of the small intestinal epithelium. Nature 551, 333–339 (2017).
pubmed: 29144463 pmcid: 6022292 doi: 10.1038/nature24489
Biton, M. et al. T helper cell cytokines modulate intestinal stem cell renewal and differentiation. Cell 175, 1307–1320.e22 (2018).
pubmed: 30392957 pmcid: 6239889 doi: 10.1016/j.cell.2018.10.008
Ginguay, A., Cynober, L., Curis, E. & Nicolis, I. Ornithine aminotransferase, an important glutamate-metabolizing enzyme at the crossroads of multiple metabolic pathways. Biology 6, 18 (2017).
pubmed: 28272331 pmcid: 5372011 doi: 10.3390/biology6010018
Daune, G., Gerhart, F. & Seiler, N. 5-Fluoromethylornithine, an irreversible and specific inhibitor of L-ornithine:2-oxo-acid aminotransferase. Biochem. J. 253, 481–488 (1988).
pubmed: 3178724 pmcid: 1149323 doi: 10.1042/bj2530481
Poulin, R., Lu, L., Ackermann, B., Bey, P. & Pegg, A. E. Mechanism of the irreversible inactivation of mouse ornithine decarboxylase by α-difluoromethylornithine. Characterization of sequences at the inhibitor and coenzyme binding sites. J. Biol. Chem. 267, 150–158 (1992).
pubmed: 1730582 doi: 10.1016/S0021-9258(18)48472-4
Puleston, D. J. et al. Polyamine metabolism is a central determinant of helper T cell lineage fidelity. Cell 184, 4186–4202.e20 (2021).
pubmed: 34216540 pmcid: 8358979 doi: 10.1016/j.cell.2021.06.007
Park, M. H. & Wolff, E. C. Hypusine, a polyamine-derived amino acid critical for eukaryotic translation. J. Biol. Chem. 293, 18710–18718 (2018).
pubmed: 30257869 pmcid: 6290153 doi: 10.1074/jbc.TM118.003341
Puleston, D. J. et al. Polyamines and eIF5A hypusination modulate mitochondrial respiration and macrophage activation. Cell Metab. 30, 352–363.e8 (2019).
pubmed: 31130465 pmcid: 6688828 doi: 10.1016/j.cmet.2019.05.003
Zabala-Letona, A. et al. mTORC1-dependent AMD1 regulation sustains polyamine metabolism in prostate cancer. Nature 547, 109–113 (2017).
pubmed: 28658205 pmcid: 5505479 doi: 10.1038/nature22964
Mandal, S., Mandal, A., Johansson, H. E., Orjalo, A. V. & Park, M. H. Depletion of cellular polyamines, spermidine and spermine, causes a total arrest in translation and growth in mammalian cells. Proc. Natl Acad. Sci. USA 110, 2169–2174 (2013).
pubmed: 23345430 pmcid: 3568356 doi: 10.1073/pnas.1219002110
Abbruzzese, A., Park, M. H. & Folk, J. E. Deoxyhypusine hydroxylase from rat testis. Partial purification and characterization. J. Biol. Chem. 261, 3085–3089 (1986).
pubmed: 3949761 doi: 10.1016/S0021-9258(17)35750-2
Gobert, A. P. et al. Hypusination orchestrates the antimicrobial response of macrophages. Cell Rep. 33, 108510 (2020).
pubmed: 33326776 pmcid: 7812972 doi: 10.1016/j.celrep.2020.108510
Bruens, L. et al. Calorie restriction increases the number of competing stem cells and decreases mutation retention in the intestine. Cell Rep. 32, 107937 (2020).
pubmed: 32698002 pmcid: 7383228 doi: 10.1016/j.celrep.2020.107937
Fontana, L., Partridge, L. & Longo, V. D. Extending healthy life span — from yeast to humans. Science 328, 321–326 (2010).
pubmed: 20395504 pmcid: 3607354 doi: 10.1126/science.1172539
Mai, V. et al. Calorie restriction and diet composition modulate spontaneous intestinal tumorigenesis in Apc(Min) mice through different mechanisms. Cancer Res. 63, 1752–1755 (2003).
pubmed: 12702556
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
Faller, W. J. et al. mTORC1-mediated translational elongation limits intestinal tumour initiation and growth. Nature 517, 497–500 (2015).
pubmed: 25383520 doi: 10.1038/nature13896
Erdman, S. H. et al. APC-dependent changes in expression of genes influencing polyamine metabolism, and consequences for gastrointestinal carcinogenesis, in the Min mouse. Carcinogenesis 20, 1709–1713 (1999).
pubmed: 10469614 doi: 10.1093/carcin/20.9.1709
Oliver, E. R., Saunders, T. L., Tarlé, S. A. & Glaser, T. Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 131, 3907–3920 (2004).
pubmed: 15289434 doi: 10.1242/dev.01268
Knight, J. R. et al. Rpl24(Bst) mutation suppresses colorectal cancer by promoting eEF2 phosphorylation via eEF2K. eLife 10, e69729 (2021).
pubmed: 34895463 pmcid: 8668188 doi: 10.7554/eLife.69729
Nagai, M. et al. Fasting–refeeding impacts immune cell dynamics and mucosal immune responses. Cell 178, 1072–1087.e14 (2019).
pubmed: 31442401 doi: 10.1016/j.cell.2019.07.047
Napolitano, G. et al. mTOR-dependent phosphorylation controls TFEB nuclear export. Nat. Commun. 9, 3312 (2018).
pubmed: 30120233 pmcid: 6098152 doi: 10.1038/s41467-018-05862-6
Tinkum, K. L. et al. Fasting protects mice from lethal DNA damage by promoting small intestinal epithelial stem cell survival. Proc. Natl Acad. Sci. USA 112, E7148–E7154 (2015).
pubmed: 26644583 pmcid: 4697381 doi: 10.1073/pnas.1509249112
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 pmcid: 3309789 doi: 10.1073/pnas.1113890109
Zoumas-Morse, C. et al. Development of a polyamine database for assessing dietary intake. J. Am. Diet Assoc. 107, 1024–1027 (2007).
pubmed: 17524725 pmcid: 2848593 doi: 10.1016/j.jada.2007.03.012
Pegg, A. E. Functions of polyamines in mammals. J. Biol. Chem. 291, 14904–14912 (2016).
pubmed: 27268251 pmcid: 4946908 doi: 10.1074/jbc.R116.731661
Allmeroth, K. et al. N1-acetylspermidine is a determinant of hair follicle stem cell fate. J. Cell Sci. 134, jcs252767 (2021).
pubmed: 33973637 pmcid: 8182411 doi: 10.1242/jcs.252767
Fritsch, S. D. et al. Metabolic support by macrophages sustains colonic epithelial homeostasis. Cell Metab. 35, 1931–1943.e8 (2023).
pubmed: 37804836 doi: 10.1016/j.cmet.2023.09.010
Brandhorst, S. et al. A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metab. 22, 86–99 (2015).
pubmed: 26094889 pmcid: 4509734 doi: 10.1016/j.cmet.2015.05.012
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
Colnot, S. et al. Colorectal cancers in a new mouse model of familial adenomatous polyposis: influence of genetic and environmental modifiers. Lab Invest. 84, 1619–1630 (2004).
pubmed: 15502862 doi: 10.1038/labinvest.3700180
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
Ootani, A. et al. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat. Med. 15, 701–706 (2009).
pubmed: 19398967 pmcid: 2919216 doi: 10.1038/nm.1951
Fuhrer, T., Heer, D., Begemann, B. & Zamboni, N. High-throughput, accurate mass metabolome profiling of cellular extracts by flow injection-time-of-flight mass spectrometry. Anal. Chem. 83, 7074–7080 (2011).
pubmed: 21830798 doi: 10.1021/ac201267k
Sellick, C. A., Hansen, R., Stephens, G. M., Goodacre, R. & Dickson, A. J. Metabolite extraction from suspension-cultured mammalian cells for global metabolite profiling. Nat. Protoc. 6, 1241–1249 (2011).
pubmed: 21799492 doi: 10.1038/nprot.2011.366
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

Auteurs

Shinya Imada (S)

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

Saleh Khawaled (S)

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

Heaji Shin (H)

Department of Biology, The David H. Koch Institute for Integrative Cancer Research at MIT, MIT, Cambridge, MA, USA.
ORCID: 0000-0001-5208-5999

Sven W Meckelmann (SW)

Applied Analytical Chemistry, University of Duisburg-Essen, Essen, Germany.

Charles A Whittaker (CA)

Barbara K. Ostrom (1978) Bioinformatics and Computing Core Facility, Swanson Biotechnology Center, Koch Institute at the MIT, Cambridge, MA, USA.
ORCID: 0000-0002-2400-0094

Renan Oliveira Corrêa (RO)

Department of Biology, The David H. Koch Institute for Integrative Cancer Research at MIT, MIT, Cambridge, MA, USA.
Laboratory of Immunoinflammation, Department of Genetics, Evolution, Microbiology and Immunology, Institute of Biology, University of Campinas, São Paulo, Brazil.
Obesity and Comorbidities Research Center (OCRC), University of Campinas, São Paulo, Brazil.
ORCID: 0000-0002-3333-0482

Chiara Alquati (C)

Department of Biology, The David H. Koch Institute for Integrative Cancer Research at MIT, MIT, Cambridge, MA, USA.
Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy.
ORCID: 0000-0002-2003-3622

Yixin Lu (Y)

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

Guodong Tie (G)

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.
Department of Medicine, Harvard Medical School, Boston, MA, USA.

Dikshant Pradhan (D)

Barbara K. Ostrom (1978) Bioinformatics and Computing Core Facility, Swanson Biotechnology Center, Koch Institute at the MIT, Cambridge, MA, USA.

Gizem Calibasi-Kocal (G)

Department of Biology, The David H. Koch Institute for Integrative Cancer Research at MIT, MIT, Cambridge, MA, USA.
Department of Translational Oncology, Institute of Oncology, Dokuz Eylul University, Izmir-Turkey, Turkey.
ORCID: 0000-0002-3201-4752

Luiza Martins Nascentes Melo (LM)

Department of Dermatology, University Hospital Essen and German Cancer Consortium, Essen, Germany.
ORCID: 0000-0002-5980-5220

Gabriele Allies (G)

Department of Dermatology, University Hospital Essen and German Cancer Consortium, Essen, Germany.

Jonas Rösler (J)

Department of Dermatology, University Hospital Essen and German Cancer Consortium, Essen, Germany.

Pia Wittenhofer (P)

Applied Analytical Chemistry, University of Duisburg-Essen, Essen, Germany.

Jonathan Krystkiewicz (J)

Department of Dermatology, University Hospital Essen and German Cancer Consortium, Essen, Germany.

Oliver J Schmitz (OJ)

Applied Analytical Chemistry, University of Duisburg-Essen, Essen, Germany.
ORCID: 0000-0003-2184-1207

Jatin Roper (J)

Division of Gastroenterology, Department of Medicine, Duke University, Durham, NC, USA.
Department of Pharmacology and Cancer Biology, Duke University, Durham, NC, USA.
ORCID: 0000-0002-8851-1352

Marco Aurelio Ramirez Vinolo (MAR)

Laboratory of Immunoinflammation, Department of Genetics, Evolution, Microbiology and Immunology, Institute of Biology, University of Campinas, São Paulo, Brazil.
Obesity and Comorbidities Research Center (OCRC), University of Campinas, São Paulo, Brazil.

Luigi Ricciardiello (L)

Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy.
Department of Gastroenterology, Hepatology and Nutrition, MD Anderson Cancer Center, Houston, TX, USA.

Evan C Lien (EC)

Department of Metabolism and Nutritional Programming, Van Andel Institute, Grand Rapids, MI, USA.
ORCID: 0000-0001-7866-4761

Matthew G Vander Heiden (MG)

Department of Biology, The David H. Koch Institute for Integrative Cancer Research at MIT, MIT, Cambridge, MA, USA.
ORCID: 0000-0002-6702-4192

Ramesh A Shivdasani (RA)

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.
Department of Medicine, Harvard Medical School, Boston, MA, USA.
ORCID: 0000-0002-2828-1727

Chia-Wei Cheng (CW)

Department of Biology, The David H. Koch Institute for Integrative Cancer Research at MIT, MIT, Cambridge, MA, USA.
Columbia Stem Cell Initiative, Department of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USA.

Alpaslan Tasdogan (A)

Department of Dermatology, University Hospital Essen and German Cancer Consortium, Essen, Germany. alpaslan.tasdogan@uk-essen.de.
ORCID: 0000-0003-2543-852X

Ömer H Yilmaz (ÖH)

Department of Biology, The David H. Koch Institute for Integrative Cancer Research at MIT, MIT, Cambridge, MA, USA. ohyilmaz@mit.edu.
Broad Institute of Harvard and MIT, Cambridge, MA, USA. ohyilmaz@mit.edu.
Department of Pathology, Beth Israel Deaconess Medical Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA. ohyilmaz@mit.edu.
ORCID: 0000-0002-7577-4612

Classifications MeSH