Aged Stem Cells Reprogram Their Daily Rhythmic Functions to Adapt to Stress

Cell

Volumn 170, Issue 4, 2017, Pages 678-692.e20

  Solanas, Guiomar ^a   Peixoto, Francisca Oliveira ^a   Perdiguero, Eusebio ^c   Jardí, Mercè ^c   Ruiz Bonilla, Vanessa ^c   Datta, Debayan ^a   Symeonidi, Aikaterini ^a   Castellanos, Andrés ^a   Welz, Patrick Simon ^a   Caballero, Juan Martín ^e   Sassone Corsi, Paolo ^f   Muñoz Cánoves, Pura ^b,c,d   Benitah, Salvador Aznar ^a,b  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^e Barcelona Biomedical Research Park   (Spain)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

aging; caloric restriction; circadian reprogramming; Circadian rhythms; diet; epidermal stem cells; hallmarks of aging; high fat diet; muscle stem cells (satellite cells); stem cells

Indexed keywords

ALPHA6 INTEGRIN; ALPHA7 INTEGRIN; CD34 ANTIGEN; HISTONE H2AX; HISTONE H2AX GAMMA; INTERLEUKIN 6; SINGLE STRANDED DNA; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ADAPTATION; ADULT; AGED; AMPLITUDE MODULATION; ANIMAL CELL; ARTICLE; AUTOPHAGY; CALORIC RESTRICTION; CELL AGING; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL METABOLISM; CELL PROLIFERATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; GENE EXPRESSION; HOMEOSTASIS; KERATINOCYTE; LIGHT DARK CYCLE; MITOSIS; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; OSCILLATION; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; STEM CELL; TRANSCRIPTION REGULATION; YOUNG ADULT; ADULT STEM CELL; ANIMAL; EPIDERMIS; LIPID DIET; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SKELETAL MUSCLE;

ADULT STEM CELLS; ANIMALS; AUTOPHAGY; CALORIC RESTRICTION; CELL AGING; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; DIET, HIGH-FAT; DNA DAMAGE; EPIDERMIS; HOMEOSTASIS; MICE; MUSCLE, SKELETAL; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 85027496313     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.07.035     Document Type: Article

References (60)

1. Amaral, N., Vendrell, A., Funaya, C., Idrissi, F.-Z., Maier, M., Kumar, A., Neurohr, G., Colomina, N., Torres-Rosell, J., Geli, M.-I., Mendoza, M., The Aurora-B-dependent NoCut checkpoint prevents damage of anaphase bridges after DNA replication stress. Nat. Cell Biol. 18 (2016), 516–526.
2. Bentzinger, C.F., Wang, Y.X., von Maltzahn, J., Soleimani, V.D., Yin, H., Rudnicki, M.A., Fibronectin regulates Wnt7a signaling and satellite cell expansion. Cell Stem Cell 12 (2013), 75–87.
3. Bernet, J.D., Doles, J.D., Hall, J.K., Kelly Tanaka, K., Carter, T.A., Olwin, B.B., p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat. Med. 20 (2014), 265–271.
4. Boada-Romero, E., Letek, M., Fleischer, A., Pallauf, K., Ramón-Barros, C., Pimentel-Muiños, F.X., TMEM59 defines a novel ATG16L1-binding motif that promotes local activation of LC3. EMBO J. 32 (2013), 566–582.
5. Bonaconsa, M., Malpeli, G., Montaruli, A., Carandente, F., Grassi-Zucconi, G., Bentivoglio, M., Differential modulation of clock gene expression in the suprachiasmatic nucleus, liver and heart of aged mice. Exp. Gerontol. 55 (2014), 70–79.
6. Búa, S., Sotiropoulou, P., Sgarlata, C., Borlado, L.R., Eguren, M., Domínguez, O., Ortega, S., Malumbres, M., Blanpain, C., Méndez, J., Deregulated expression of Cdc6 in the skin facilitates papilloma formation and affects the hair growth cycle. Cell Cycle 14 (2015), 3897–3907.
7. Cerletti, M., Jang, Y.C., Finley, L.W.S., Haigis, M.C., Wagers, A.J., Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell 10 (2012), 515–519.
8. Chakkalakal, J., Brack, A., Extrinsic Regulation of Satellite Cell Function and Muscle Regeneration Capacity during Aging. J Stem Cell Res Ther(Suppl 11), 2012, 001.
9. Chakkalakal, J.V., Jones, K.M., Basson, M.A., Brack, A.S., The aged niche disrupts muscle stem cell quiescence. Nature 490 (2012), 355–360.
10. Chang, H.-C., Guarente, L., SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell 153 (2013), 1448–1460.
11. Clayton, E., Doupé, D.P., Klein, A.M., Winton, D.J., Simons, B.D., Jones, P.H., A single type of progenitor cell maintains normal epidermis. Nature 446 (2007), 185–189.
12. Gentleman, R., Carey, V.J., Huber, W., Irizarry, R.A., Dudoit, S., Bioinformatics and Computational Biology Solutions Using R and Bioconductor. 2005, Springer New York, New York, NY.
13. Durcan, T.M., Fon, E.A., The three ‘P's of mitophagy: PARKIN, PINK1, and post-translational modifications. Genes Dev. 29 (2015), 989–999.
14. Eckel-Mahan, K.L., Patel, V.R., de Mateo, S., Orozco-Solis, R., Ceglia, N.J., Sahar, S., Dilag-Penilla, S.A., Dyar, K.A., Baldi, P., Sassone-Corsi, P., Reprogramming of the circadian clock by nutritional challenge. Cell 155 (2013), 1464–1478.
15. Eklund, A.C., Szallasi, Z., Correction of technical bias in clinical microarray data improves concordance with known biological information. Genome Biol., 9, 2008, R26.
16. Farajnia, S., Michel, S., Deboer, T., vanderLeest, H.T., Houben, T., Rohling, J.H., Ramkisoensing, A., Yasenkov, R., Meijer, J.H., Evidence for neuronal desynchrony in the aged suprachiasmatic nucleus clock. J. Neurosci. 32 (2012), 5891–5899.
17. Froy, O., Miskin, R., Effect of feeding regimens on circadian rhythms: implications for aging and longevity. Aging (Albany NY) 2 (2010), 7–27.
18. Gaddameedhi, S., Selby, C.P., Kaufmann, W.K., Smart, R.C., Sancar, A., Control of skin cancer by the circadian rhythm. Proc. Natl. Acad. Sci. USA 108 (2011), 18790–18795.
19. García-Prat, L., Martínez-Vicente, M., Perdiguero, E., Ortet, L., Rodríguez-Ubreva, J., Rebollo, E., Ruiz-Bonilla, V., Gutarra, S., Ballestar, E., Serrano, A.L., et al. Autophagy maintains stemness by preventing senescence. Nature 529 (2016), 37–42.
20. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol., 5, 2004, R80.
21. Geyfman, M., Kumar, V., Liu, Q., Ruiz, R., Gordon, W., Espitia, F., Cam, E., Millar, S.E., Smyth, P., Ihler, A., et al. Brain and muscle Arnt-like protein-1 (BMAL1) controls circadian cell proliferation and susceptibility to UVB-induced DNA damage in the epidermis. Proc. Natl. Acad. Sci. USA 109 (2012), 11758–11763.
22. Goetsch, K.P., Snyman, C., Myburgh, K.H., Niesler, C.U., ROCK-2 is associated with focal adhesion maturation during myoblast migration. J. Cell. Biochem. 115 (2014), 1299–1307.
23. Goodell, M.A., Rando, T.A., Stem cells and healthy aging. Science 350 (2015), 1199–1204.
24. Hughes, M.E., Hogenesch, J.B., Kornacker, K., JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J. Biol. Rhythms 25 (2010), 372–380.
25. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., Speed, T.P., Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 (2003), 249–264.
26. Ishii, A., Lo, S.H., A role of tensin in skeletal-muscle regeneration. Biochem. J. 356 (2001), 737–745.
27. Janich, P., Pascual, G., Merlos-Suárez, A., Batlle, E., Ripperger, J., Albrecht, U., Cheng, H.-Y.M., Obrietan, K., Di Croce, L., Benitah, S.A., The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 480 (2011), 209–214.
28. Janich, P., Toufighi, K., Solanas, G., Luis, N.M., Minkwitz, S., Serrano, L., Lehner, B., Benitah, S.A., Human epidermal stem cell function is regulated by circadian oscillations. Cell Stem Cell 13 (2013), 745–753.
29. Janich, P., Meng, Q.-J., Benitah, S.A., Circadian control of tissue homeostasis and adult stem cells. Curr. Opin. Cell Biol. 31 (2014), 8–15.
30. Koike, N., Yoo, S.-H., Huang, H.-C., Kumar, V., Lee, C., Kim, T.-K., Takahashi, J.S., Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338 (2012), 349–354.
31. Koren, I., Reem, E., Kimchi, A., DAP1, a novel substrate of mTOR, negatively regulates autophagy. Curr. Biol. 20 (2010), 1093–1098.
32. Lipp, H.-P., Litvin, O., Galsworthy, M., Vyssotski, A.L., Zinn, P., Rau, A.E., Neuhausser-Wespy, F., Wurbel, H., Nitsch, R., Wolfer, D.P., Automated behavioral analysis of mice using INTELLICAGE: inter-laboratory comparisons and validation with exploratory behavior and spatial learning. Noldus, L.P.J.J., Grieco, F., Loijens, L.W.S., Zimmermann, P.H., (eds.) Proceedings of Measuring Behavior 2005, 2005, 66–69.
33. López-Otín, C., Blasco, M.A., Partridge, L., Serrano, M., Kroemer, G., The hallmarks of aging. Cell 153 (2013), 1194–1217.
34. Lukjanenko, L., Jung, M.J., Hegde, N., Perruisseau-Carrier, C., Migliavacca, E., Rozo, M., Karaz, S., Jacot, G., Schmidt, M., Li, L., et al. Loss of fibronectin from the aged stem cell niche affects the regenerative capacity of skeletal muscle in mice. Nat. Med. 22 (2016), 897–905.
35. Mascré, G., Dekoninck, S., Drogat, B., Youssef, K.K., Broheé, S., Sotiropoulou, P.A., Simons, B.D., Blanpain, C., Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489 (2012), 257–262.
36. Masri, S., Papagiannakopoulos, T., Kinouchi, K., Liu, Y., Cervantes, M., Baldi, P., Jacks, T., Sassone-Corsi, P., Lung Adenocarcinoma Distally Rewires Hepatic Circadian Homeostasis. Cell 165 (2016), 896–909.
37. McCroskery, S., Thomas, M., Maxwell, L., Sharma, M., Kambadur, R., Myostatin negatively regulates satellite cell activation and self-renewal. J. Cell Biol. 162 (2003), 1135–1147.
38. Mihaylova, M.M., Sabatini, D.M., Yilmaz, Ö.H., Dietary and metabolic control of stem cell function in physiology and cancer. Cell Stem Cell 14 (2014), 292–305.
39. Montarras, D., L'honoré, A., Buckingham, M., Lying low but ready for action: the quiescent muscle satellite cell. FEBS J. 280 (2013), 4036–4050.
40. Nakamura, T.J., Nakamura, W., Yamazaki, S., Kudo, T., Cutler, T., Colwell, C.S., Block, G.D., Age-related decline in circadian output. J. Neurosci. 31 (2011), 10201–10205.
41. Plikus, M.V., Vollmers, C., de la Cruz, D., Chaix, A., Ramos, R., Panda, S., Chuong, C.M., Local circadian clock gates cell cycle progression of transient amplifying cells during regenerative hair cycling. Proc. Natl. Acad. Sci. USA 110 (2013), E2106–E2115.
42. R Development Core Team. R: A language and environment for statistical computing. 2008, R Foundation for Statistical Computing.
43. Roenneberg, T., Kuehnle, T., Juda, M., Kantermann, T., Allebrandt, K., Gordijn, M., Merrow, M., Epidemiology of the human circadian clock. Sleep Med. Rev. 11 (2007), 429–438.
44. Rozo, M., Li, L., Fan, C.-M., Targeting β1-integrin signaling enhances regeneration in aged and dystrophic muscle in mice. Nat. Med. 22 (2016), 889–896.
45. Sada, A., Jacob, F., Leung, E., Wang, S., White, B.S., Shalloway, D., Tumbar, T., Defining the cellular lineage hierarchy in the interfollicular epidermis of adult skin. Nat. Cell Biol. 18 (2016), 619–631.
46. Sato, S., Solanas, G., Peixoto, F., Bee, L., Symeonidi, A., Schmidt, M.S., Brenner, C., Masri, S., Benitah, S.A., Sassone-Corsi, P., Circadian reprogramming identifies metabolic pathways of aging. Cell 170 (2017), 664–677 this issue.
47. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
48. Segawa, M., Fukada, S., Yamamoto, Y., Yahagi, H., Kanematsu, M., Sato, M., Ito, T., Uezumi, A., Hayashi, S., Miyagoe-Suzuki, Y., et al. Suppression of macrophage functions impairs skeletal muscle regeneration with severe fibrosis. Exp. Cell Res. 314 (2008), 3232–3244.
49. Shibukawa, Y., Yamazaki, N., Daimon, E., Wada, Y., Rock-dependent calponin 3 phosphorylation regulates myoblast fusion. Exp. Cell Res. 319 (2013), 633–648.
50. Solanas, G., Benitah, S.A., Regenerating the skin: a task for the heterogeneous stem cell pool and surrounding niche. Nat. Rev. Mol. Cell Biol. 14 (2013), 737–748.
51. Sousa-Victor, P., Gutarra, S., García-Prat, L., Rodriguez-Ubreva, J., Ortet, L., Ruiz-Bonilla, V., Jardí, M., Ballestar, E., González, S., Serrano, A.L., et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506 (2014), 316–321.
52. Sousa-Victor, P., García-Prat, L., Serrano, A.L., Perdiguero, E., Muñoz-Cánoves, P., Muscle stem cell aging: regulation and rejuvenation. Trends Endocrinol. Metab. 26 (2015), 287–296.
53. Stringari, C., Wang, H., Geyfman, M., Crosignani, V., Kumar, V., Takahashi, J.S., Andersen, B., Gratton, E., In vivo single-cell detection of metabolic oscillations in stem cells. Cell Rep. 10 (2015), 1–7.
54. Suzuki, T., Franchi, L., Toma, C., Ashida, H., Ogawa, M., Yoshikawa, Y., Mimuro, H., Inohara, N., Sasakawa, C., Nuñez, G., Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog., 3, 2007, e111.
55. Tetteh, P.W., Farin, H.F., Clevers, H., Plasticity within stem cell hierarchies in mammalian epithelia. Trends Cell Biol. 25 (2015), 100–108.
56. Tierney, M.T., Gromova, A., Sesillo, F.B., Sala, D., Spenlé, C., Orend, G., Sacco, A., Autonomous Extracellular Matrix Remodeling Controls a Progressive Adaptation in Muscle Stem Cell Regenerative Capacity during Development. Cell Rep. 14 (2016), 1940–1952.
57. Vahidi Ferdousi, L., Rocheteau, P., Chayot, R., Montagne, B., Chaker, Z., Flamant, P., Tajbakhsh, S., Ricchetti, M., More efficient repair of DNA double-strand breaks in skeletal muscle stem cells compared to their committed progeny. Stem Cell Res. (Amst.) 13:3 Pt A (2014), 492–507.
58. Vermeij, W.P., Dollé, M.E.T., Reiling, E., Jaarsma, D., Payan-Gomez, C., Bombardieri, C.R., Wu, H., Roks, A.J.M., Botter, S.M., van der Eerden, B.C., et al. Restricted diet delays accelerated ageing and genomic stress in DNA-repair-deficient mice. Nature 537 (2016), 427–431.
59. Young, A.R.J., Narita, M., Ferreira, M., Kirschner, K., Sadaie, M., Darot, J.F.J., Tavaré, S., Arakawa, S., Shimizu, S., Watt, F.M., Narita, M., Autophagy mediates the mitotic senescence transition. Genes Dev. 23 (2009), 798–803.
60. Zheng, B., Albrecht, U., Kaasik, K., Sage, M., Lu, W., Vaishnav, S., Li, Q., Sun, Z.S., Eichele, G., Bradley, A., et al. Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell 105 (2001), 683–694.