Mechanisms of cellular rejuvenation.


Journal

FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157

Informations de publication

Date de publication:
12 2019
Historique:
received: 03 04 2019
revised: 29 04 2019
accepted: 02 05 2019
pubmed: 15 6 2019
medline: 20 6 2020
entrez: 15 6 2019
Statut: ppublish

Résumé

Aging leads to changes on an organismal but also cellular level. However, the exact mechanisms of cellular aging in mammals remain poorly understood and the identity and functional role of aging factors, some of which have previously been defined in model organisms such as Saccharomyces cerevisiae, remain elusive. Remarkably, during cellular reprogramming most if not all aging hallmarks are erased, offering a novel entry point to study aging and rejuvenation on a cellular level. On the other hand, direct reprogramming of old cells into cells of a different fate preserves many aging signs. Therefore, investigating the process of reprogramming and comparing it to direct reprogramming may yield novel insights about the clearing of aging factors, which is the basis of rejuvenation. Here, we discuss how reprogramming might lead to rejuvenation of a cell, an organ, or even the whole organism.

Identifiants

pubmed: 31197818
doi: 10.1002/1873-3468.13483
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3381-3392

Subventions

Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : BSCGI0_157859
Pays : International
Organisme : H2020 European Research Council
Pays : International
Organisme : Zurich Neuroscience Center (ZNZ)
Pays : International

Informations de copyright

© 2019 Federation of European Biochemical Societies.

Références

López-Otín C, Blasco MA, Partridge L, Serrano M and Kroemer G (2013) The hallmarks of aging. Cell 153, 1194-1217.
Denoth Lippuner A, Julou T and Barral Y (2014) Budding yeast as a model organism to study the effects of age. FEMS Microbiol Rev 38, 300-325.
Denzel MS, Lapierre LR and Mack HID (2019) Emerging topics in C. elegans aging research: transcriptional regulation, stress response and epigenetics. Mech Ageing Dev 177, 4-21.
Sun Y, Yolitz J, Wang C, Spangler E, Zhan M and Zou S (2013) Aging studies in Drosophila melanogaster. Methods Mol Biol 1048, 77-93.
Kaeberlein M (2010) Lessons on longevity from budding yeast. Nature 464, 513-519.
Janssens G and Veenhoff L (2016) Evidence for the hallmarks of human aging in replicatively aging yeast. Microbial Cell 3, 263-274
Johnson SC, Rabinovitch PS and Kaeberlein M (2013) MTOR is a key modulator of ageing and age-related disease. Nature 493, 338-345.
Cornu M, Albert V and Hall MN (2013) mTOR in aging, metabolism, and cancer. Curr Opin Genet Dev 23, 53-62.
Takahashi K and Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
Lapasset L, Milhavet O, Prieur A, Besnard E, Babled A, Ät-Hamou N, Leschik J, Pellestor F, Ramirez JM, De Vos J et al. (2011) Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state. Genes Dev 25, 2248-2253.
Mahmoudi S, Xu L and Brunet A (2019) Turning back time with emerging rejuvenation strategies. Nat Cell Biol 21, 32-43.
Barton AA (2009) Some aspects of cell division in Saccharomyces cerevisiae. J Gen Microbiol 4, 84-86.
Sinclair DA and Guarente L (1997) Extrachromosomal rDNA circles - a cause of aging in yeast. Cell 91, 1033-1042.
Henderson KA and Gottschling DE (2008) A mother's sacrifice: what is she keeping for herself? Curr Opin Cell Biol 20, 723-728.
Shcheprova Z, Baldi S, Frei SB, Gonnet G and Barral Y (2008) A mechanism for asymmetric segregation of age during yeast budding. Nature 454, 728-734.
Denoth-Lippuner A, Krzyzanowski MK, Stober C and Barral Y (2014) Role of SAGA in the asymmetric segregation of DNA circles during yeast ageing. Elife 3, e03790.
Saarikangas J, Caudron F, Prasad R, Moreno DF, Bolognesi A, Aldea M and Barral Y (2017) Compartmentalization of ER-bound chaperone confines protein deposit formation to the aging yeast cell. Curr Biol 27, 773-783.
Erjavec N, Larsson L, Grantham J and Nyström T (2007) Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes Dev 21, 2410-2421.
Liu B, Larsson L, Caballero A, Hao X, Öling D, Grantham J and Nyström T (2010) The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140, 257-267.
Aunan JR, Watson MM, Hagland HR and Søreide K (2016) Molecular and biological hallmarks of ageing. Br J Surg 103, e29-e46.
Goodell MA and Rando TA (2015) Stem cells and healthy aging. Science 350, 1199-1204.
Cohen S, Agmon N, Sobol O and Segal D (2010) Extrachromosomal circles of satellite repeats and 5S ribosomal DNA in human cells. Mobile DNA 1, 11.
Shibata Y, Kumar P, Layer R, Willcox S, Gagan JR, Griffith JD and Dutta A (2012) Extrachromosomal microDNAs and chromosomal microdeletions in normal tissues. Science 336, 82-86.
Møller HD, Mohiyuddin M, Prada-Luengo I, Sailani MR, Halling JF, Plomgaard P, Maretty L, Hansen AJ, Snyder MP, Pilegaard H et al. (2018) Circular DNA elements of chromosomal origin are common in healthy human somatic tissue. Nat Commun 9, 1069.
Wang X, Le N, Denoth-Lippuner A, Barral Y and Kroschewski R (2016) Asymmetric partitioning of transfected DNA during mammalian cell division. Proc Natl Acad Sci 113, 7177-7182.
Walther DM, Kasturi P, Zheng M, Pinkert S, Vecchi G, Ciryam P, Morimoto RI, Dobson CM, Vendruscolo M, Mann M et al. (2015) Widespread proteome remodeling and aggregation in aging C. elegans. Cell 161, 919-932.
Caudron F and Barral Y (2013) A Super-Assembly of Whi3 encodes memory of deceptive encounters by single cells during yeast courtship. Cell 155, 1244-1257.
Majumdar A, Cesario WC, White-Grindley E, Jiang H, Ren F, Khan MR, Li L, Choi EML, Kannan K, Guo F et al. (2012) Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 148, 515-529.
Rujano MA, Bosveld F, Salomons FA, Dijk F, Van Waarde MAWH, Van Der Want JJL, De Vos RAI, Brunt ER, Sibon OCM and Kampinga HH (2006) Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLoS Biol 4, e417.
Bufalino MR, DeVeale B and van der Kooy D (2013) The asymmetric segregation of damaged proteins is stem cell-type dependent. J Cell Biol 201, 523-530.
Moore DL, Pilz GA, Araúzo-Bravo MJ, Barral Y and Jessberger S (2015) A mechanism for the segregation of age in mammalian neural stem cells. Science 349, 1334-1338.
Saarikangas J and Caudron F (2017) Spatial regulation of coalesced protein assemblies: lessons from yeast to diseases. Prion 11, 162-173.
Sun N, Youle RJ and Finkel T (2016) The mitochondrial basis of aging. Mol Cell 61, 654-666.
Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 1, 298-300.
Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, Bohlooly-Y M, Gldlöf S, Oldfors A, Wibom R et al. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429, 417-423.
Kauppila TES, Kauppila JHK and Larsson NG (2017) Mammalian mitochondria and aging: An Update. Cell Metab 25, 57-71.
Katajisto P, Dohla J, Chaffer CL, Pentinmikko N, Marjanovic N, Iqbal S, Zoncu R, Chen W, Weinberg RA and Sabatini DM (2015) Asymmetric apportioning of aged mitochondria between daughter cells is required for stemness. Science 348, 340-343.
Sen P, Shah PP, Nativio R and Berger SL (2016) Epigenetic mechanisms of longevity and aging. Cell 166, 822-839.
Han S and Brunet A (2012) Histone methylation makes its mark on longevity. Trends Cell Biol 22, 42-49.
Field AE, Robertson NA, Wang T, Havas A, Ideker T and Adams PD (2018) DNA methylation clocks in aging: categories, causes, and consequences. Mol Cell 71, 882-895.
Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda SV, Klotzle B, Bibikova M, Fan JB, Gao Y et al. (2013) Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell 49, 359-367.
Horvath S (2013) DNA methylation age of human tissues and cell types. Genome Biol 14, R115.
Marioni RE, Shah S, McRae AF, Chen BH, Colicino E, Harris SE, Gibson J, Henders AK, Redmond P, Cox SR et al. (2015) DNA methylation age of blood predicts all-cause mortality in later life. Genome Biol 16, 25.
Rando TA and Chang HY (2012) Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 148, 46-57.
Frobel J, Hemeda H, Lenz M, Abagnale G, Joussen S, Denecke B, Šarić T, Zenke M and Wagner W (2014) Epigenetic rejuvenation of mesenchymal stromal cells derived from induced pluripotent stem cells. Stem Cell Reports 3, 414-422.
Liu GH, Barkho BZ, Ruiz S, Diep D, Qu J, Yang SL, Panopoulos AD, Suzuki K, Kurian L, Walsh C et al. (2011) Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome. Nature472, 221-225.
Cheung HH, Liu X, Canterel-Thouennon L, Li L, Edmonson C and Rennert OM (2014) Telomerase protects werner syndrome lineage-specific stem cells from premature aging. Stem Cell Rep 2, 534-546.
Chung CY, Khurana V, Auluck PK, Tardiff DF, Mazzulli JR, Soldner F, Baru V, Lou Y, Freyzon Y, Cho S et al. (2013) Identification and rescue of α-synuclein toxicity in Parkinson patient-derived neurons. Science 342, 983-987.
Kondo T, Asai M, Tsukita K, Kutoku Y, Ohsawa Y, Sunada Y, Imamura K, Egawa N, Yahata N, Okita K et al. (2013) Modeling Alzheimer's disease with iPSCs reveals stress phenotypes associated with intracellular Aβ and differential drug responsiveness. Cell Stem Cell 12, 487-496.
Xu J, Du Y and Deng H (2015) Direct lineage reprogramming: Strategies, mechanisms, and applications. Cell Stem Cell 16, 119-134.
Sheng C, Jungverdorben J, Wiethoff H, Lin Q, Flitsch LJ, Eckert D, Hebisch M, Fischer J, Kesavan J, Weykopf B et al. (2018) A stably self-renewing adult blood-derived induced neural stem cell exhibiting patternability and epigenetic rejuvenation. Nat Commun 9, 4047.
Kim J, Efe JA, Zhu S, Talantova M, Yuan X, Wang S, Lipton SA, Zhang K and Ding S (2011) Direct reprogramming of mouse fibroblasts to neural progenitors. Proc Natl Acad Sci USA 108, 7838-7843.
Biddy BA, Kong W, Kamimoto K, Guo C, Waye SE, Sun T and Morris SA (2018) Single-cell mapping of lineage and identity in direct reprogramming. Nature 564, 219-224.
Wang S, Xia P, Ye B, Huang G, Liu J and Fan Z (2013) Transient activation of autophagy via Sox2-mediated suppression of mTOR is an important early step in reprogramming to pluripotency. Cell Stem Cell 13, 617-625.
Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Südhof TC and Wernig M (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035-1041.
Mertens J, Reid D, Lau S, Kim Y and Gage FH (2018) Aging in a dish: iPSC-derived and directly induced neurons for studying brain aging and age-related neurodegenerative diseases. Ann Rev Genet 52, 271-293.
Mertens J, Paquola ACM, Ku M, Hatch E, Böhnke L, Ladjevardi S, McGrath S, Campbell B, Lee H, Herdy JR et al. (2015) Directly reprogrammed human neurons retain aging-associated transcriptomic signatures and reveal age-related nucleocytoplasmic defects. Cell Stem Cell 17, 705-718.
Tang Y, Liu M-L, Zang T and Zhang C-L (2017) Direct reprogramming rather than iPSC-based reprogramming maintains aging hallmarks in human motor neurons. Front Mol Neurosci 10, 359.
Huh CJ, Zhang B, Victor MB, Dahiya S, Batista LFZ, Horvath S and Yoo AS. (2016) Maintenance of age in human neurons generated by microRNA-based neuronal conversion of fibroblasts. Elife 5, e18648.
Kim Y, Zheng X, Ansari Z, Bunnell MC, Herdy JR, Traxler L, Lee H, Paquola ACM, Blithikioti C, Ku M et al. (2018) Mitochondrial aging defects emerge in directly reprogrammed human neurons due to their metabolic profile. Cell Rep 23, 2550-2558.
Victor MB, Richner M, Olsen HE, Lee SW, Monteys AM, Ma C, Huh CJ, Zhang B, Davidson BL, Yang XW et al. (2018) Striatal neurons directly converted from Huntington's disease patient fibroblasts recapitulate age-associated disease phenotypes. Nat Neurosci 21, 341-352.
Ocampo A, Reddy P, Martinez-Redondo P, Platero-Luengo A, Hatanaka F, Hishida T, Li M, Lam D, Kurita M, Beyret E et al. (2016) In vivo amelioration of age-associated hallmarks by partial reprogramming. Cell 167, 1719-1733.e12.
Abad M, Mosteiro L, Pantoja C, Cañamero M, Rayon T, Ors I, Graña O, Megías D, Domínguez O, Martínez D et al. (2013) Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502, 340-345.
Nissan X, Blondel S, Navarro C, Maury Y, Denis C, Girard M, Martinat C, DeSandre-Giovannoli A, Levy N and Peschanski M (2012) Unique preservation of neural cells in hutchinson- gilford progeria syndrome is due to the expression of the neural-specific miR-9 microRNA. Cell Rep 2, 1-9.
Mosteiro L, Pantoja C, Alcazar N, Marión RM, Chondronasiou D, Rovira M, Fernandez-Marcos PJ, Muñoz-Martin M, Blanco-Aparicio C, Pastor J et al. (2016) Tissue damage and senescence provide critical signals for cellular reprogramming in vivo. Science 354, aaf4445.
Chiche A, Le Roux I, von Joest M, Sakai H, Aguín SB, Cazin C, Salam R, Fiette L, Alegria O, Flamant P et al. (2017) Injury-induced senescence enables in vivo reprogramming in skeletal muscle. Cell Stem Cell 20, 407-414.e4.
Moore DL and Jessberger S (2017) Creating age asymmetry: consequences of inheriting damaged goods in mammalian cells. Trends Cell Biol 27, 82-92.
Ori A, Toyama BH, Harris MS, Bock T, Iskar M, Bork P, Ingolia NT, Hetzer MW and Beck M (2015) Integrated transcriptome and proteome analyses reveal organ-specific proteome deterioration in old rats. Cell Systems 1, 224-237.
Benayoun BA, Pollina E, Singh PP, Mahmoudi S, Harel I, Casey K, Dulken B, Kundaje A and Brunet A (2018) Remodeling of epigenome and transcriptome landscapes with aging in mice reveals widespread induction of inflammatory responses. bioRxiv [Preprint].
Braun SMG and Jessberger S (2014) Adult neurogenesis: mechanisms and functional significance. Development 141, 1983-1986.
Kuhn H, Dickinson-Anson H and Gage F (2018) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16, 2027-2033.

Auteurs

Annina Denoth-Lippuner (A)

Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, Switzerland.

Sebastian Jessberger (S)

Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, Switzerland.

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