Circadian Reprogramming in the Liver Identifies Metabolic Pathways of Aging

Cell

Volumn 170, Issue 4, 2017, Pages 664-677.e11

  Sato, Shogo ^a   Solanas, Guiomar ^b   Peixoto, Francisca Oliveira ^b   Bee, Leonardo ^a   Symeonidi, Aikaterini ^b   Schmidt, Mark S ^c   Brenner, Charles ^c   Masri, Selma ^a   Benitah, Salvador Aznar ^b,d   Sassone Corsi, Paolo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^c UNIVERSITY OF IOWA   (United States)

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

Author keywords

Acetylation; Aging; Circadian Clock; Liver Metabolism; NAD; Reprogramming; SIRT1

Indexed keywords

3 HYDROXYBUTYRIC ACID; SIRTUIN 1; ACETYL COENZYME A; HISTONE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN; SIRT1 PROTEIN, MOUSE; TRANSCRIPTOME;

ADULT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CALORIC RESTRICTION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME METABOLISM; EPIDERMIS CELL; GENE EXPRESSION; GENE ONTOLOGY; LIVER; LIVER METABOLISM; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN TARGETING; SKELETAL MUSCLE CELL; STEM CELL; WESTERN BLOTTING; YOUNG ADULT; ACETYLATION; ANIMAL; CIRCADIAN RHYTHM; METABOLISM; PATHOLOGY;

ACETYL COENZYME A; ACETYLATION; AGING; ANIMALS; CALORIC RESTRICTION; CIRCADIAN RHYTHM; HISTONES; LIVER; METABOLIC NETWORKS AND PATHWAYS; MICE; NAD; PROTEINS; SIRTUIN 1; STEM CELLS; TRANSCRIPTOME;

EID: 85027489124     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.07.042     Document Type: Article

References (75)

1. Asher, G., Sassone-Corsi, P., Time for food: the intimate interplay between nutrition, metabolism, and the circadian clock. Cell 161 (2015), 84–92.
2. Asher, G., Gatfield, D., Stratmann, M., Reinke, H., Dibner, C., Kreppel, F., Mostoslavsky, R., Alt, F.W., Schibler, U., SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134 (2008), 317–328.
3. Belenky, P., Bogan, K.L., Brenner, C., NAD+ metabolism in health and disease. Trends Biochem. Sci. 32 (2007), 12–19.
4. Belenky, P., Racette, F.G., Bogan, K.L., McClure, J.M., Smith, J.S., Brenner, C., Nicotinamide riboside promotes Sir2 silencing and extends lifespan via Nrk and Urh1/Pnp1/Meu1 pathways to NAD+. Cell 129 (2007), 473–484.
5. Bogan, K.L., Brenner, C., Nicotinic acid, nicotinamide, and nicotinamide riboside: a molecular evaluation of NAD+ precursor vitamins in human nutrition. Annu. Rev. Nutr. 28 (2008), 115–130.
6. Brandhorst, S., Choi, I.Y., Wei, M., Cheng, C.W., Sedrakyan, S., Navarrete, G., Dubeau, L., Yap, L.P., Park, R., Vinciguerra, M., et al. A Periodic Diet that Mimics Fasting Promotes Multi-System Regeneration, Enhanced Cognitive Performance, and Healthspan. Cell Metab. 22 (2015), 86–99.
7. Cao, S.X., Dhahbi, J.M., Mote, P.L., Spindler, S.R., Genomic profiling of short- and long-term caloric restriction effects in the liver of aging mice. Proc. Natl. Acad. Sci. USA 98 (2001), 10630–10635.
8. Cartee, G.D., Hepple, R.T., Bamman, M.M., Zierath, J.R., Exercise Promotes Healthy Aging of Skeletal Muscle. Cell Metab. 23 (2016), 1034–1047.
9. 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.
10. Chen, D., Steele, A.D., Lindquist, S., Guarente, L., Increase in activity during calorie restriction requires Sirt1. Science, 310, 2005, 1641.
11. Chen, E.Y., Tan, C.M., Kou, Y., Duan, Q., Wang, Z., Meirelles, G.V., Clark, N.R., Ma'ayan, A., Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics, 14, 2013, 128.
12. Cohen, H.Y., Miller, C., Bitterman, K.J., Wall, N.R., Hekking, B., Kessler, B., Howitz, K.T., Gorospe, M., de Cabo, R., Sinclair, D.A., Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 305 (2004), 390–392.
13. Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., Schibler, U., Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14 (2000), 2950–2961.
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. Fontana, L., Partridge, L., Promoting health and longevity through diet: from model organisms to humans. Cell 161 (2015), 106–118.
16. 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.
17. Gill, S., Le, H.D., Melkani, G.C., Panda, S., Time-restricted feeding attenuates age-related cardiac decline in Drosophila. Science 347 (2015), 1265–1269.
18. Gomes, A.P., Price, N.L., Ling, A.J., Moslehi, J.J., Montgomery, M.K., Rajman, L., White, J.P., Teodoro, J.S., Wrann, C.D., Hubbard, B.P., et al. Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155 (2013), 1624–1638.
19. Grandison, R.C., Piper, M.D., Partridge, L., Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462 (2009), 1061–1064.
20. Hagopian, K., Ramsey, J.J., Weindruch, R., Caloric restriction increases gluconeogenic and transaminase enzyme activities in mouse liver. Exp. Gerontol. 38 (2003), 267–278.
21. Hallows, W.C., Lee, S., Denu, J.M., Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. USA 103 (2006), 10230–10235.
22. Hebert, A.S., Dittenhafer-Reed, K.E., Yu, W., Bailey, D.J., Selen, E.S., Boersma, M.D., Carson, J.J., Tonelli, M., Balloon, A.J., Higbee, A.J., et al. Calorie Restriction and SIRT3 Trigger Global Reprogramming of the Mitochondrial Protein Acetylome. Mol Cell 49 (2013), 186–199.
23. Hirayama, J., Sahar, S., Grimaldi, B., Tamaru, T., Takamatsu, K., Nakahata, Y., Sassone-Corsi, P., CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 450 (2007), 1086–1090.
24. Hirschey, M.D., Shimazu, T., Goetzman, E., Jing, E., Schwer, B., Lombard, D.B., Grueter, C.A., Harris, C., Biddinger, S., Ilkayeva, O.R., et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464 (2010), 121–125.
25. Horton, J.D., Shah, N.A., Warrington, J.A., Anderson, N.N., Park, S.W., Brown, M.S., Goldstein, J.L., Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. USA 100 (2003), 12027–12032.
26. Houtkooper, R.H., Pirinen, E., Auwerx, J., Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 13 (2012), 225–238.
27. 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.
28. Imai, S., Guarente, L., NAD+ and sirtuins in aging and disease. Trends Cell Biol. 24 (2014), 464–471.
29. 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.
30. Katewa, S.D., Akagi, K., Bose, N., Rakshit, K., Camarella, T., Zheng, X., Hall, D., Davis, S., Nelson, C.S., Brem, R.B., et al. Peripheral Circadian Clocks Mediate Dietary Restriction-Dependent Changes in Lifespan and Fat Metabolism in Drosophila. Cell Metab. 23 (2016), 143–154.
31. Kondratov, R.V., Kondratova, A.A., Gorbacheva, V.Y., Vykhovanets, O.V., Antoch, M.P., Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev. 20 (2006), 1868–1873.
32. Kondratova, A.A., Kondratov, R.V., The circadian clock and pathology of the ageing brain. Nat. Rev. Neurosci. 13 (2012), 325–335.
33. Kuleshov, M.V., Jones, M.R., Rouillard, A.D., Fernandez, N.F., Duan, Q., Wang, Z., Koplev, S., Jenkins, S.L., Jagodnik, K.M., Lachmann, A., et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res., 44(W1), 2016 W90-7.
34. Lee, C.K., Klopp, R.G., Weindruch, R., Prolla, T.A., Gene expression profile of aging and its retardation by caloric restriction. Science 285 (1999), 1390–1393.
35. Lin, S.J., Defossez, P.A., Guarente, L., Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289 (2000), 2126–2128.
36. Lin, S.J., Kaeberlein, M., Andalis, A.A., Sturtz, L.A., Defossez, P.A., Culotta, V.C., Fink, G.R., Guarente, L., Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 418 (2002), 344–348.
37. Lin, S.J., Ford, E., Haigis, M., Liszt, G., Guarente, L., Calorie restriction extends yeast life span by lowering the level of NADH. Genes Dev. 18 (2004), 12–16.
38. Longo, V.D., Panda, S., Fasting, Circadian Rhythms, and Time-Restricted Feeding in Healthy Lifespan. Cell Metab. 23 (2016), 1048–1059.
39. Masri, S., Sassone-Corsi, P., Sirtuins and the circadian clock: bridging chromatin and metabolism. Sci. Signal., 7, 2014, re6.
40. Masri, S., Patel, V.R., Eckel-Mahan, K.L., Peleg, S., Forne, I., Ladurner, A.G., Baldi, P., Imhof, A., Sassone-Corsi, P., Circadian acetylome reveals regulation of mitochondrial metabolic pathways. Proc. Natl. Acad. Sci. USA 110 (2013), 3339–3344.
41. Masri, S., Rigor, P., Cervantes, M., Ceglia, N., Sebastian, C., Xiao, C., Roqueta-Rivera, M., Deng, C., Osborne, T.F., Mostoslavsky, R., et al. Partitioning circadian transcription by SIRT6 leads to segregated control of cellular metabolism. Cell 158 (2014), 659–672.
42. 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.
43. Mouchiroud, L., Houtkooper, R.H., Moullan, N., Katsyuba, E., Ryu, D., Cantó, C., Mottis, A., Jo, Y.S., Viswanathan, M., Schoonjans, K., et al. The NAD(+)/Sirtuin Pathway Modulates Longevity through Activation of Mitochondrial UPR and FOXO Signaling. Cell 154 (2013), 430–441.
44. Nakahata, Y., Kaluzova, M., Grimaldi, B., Sahar, S., Hirayama, J., Chen, D., Guarente, L.P., Sassone-Corsi, P., The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134 (2008), 329–340.
45. Nakahata, Y., Sahar, S., Astarita, G., Kaluzova, M., Sassone-Corsi, P., Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324 (2009), 654–657.
46. 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.
47. Ocampo, A., Reddy, P., Izpisua Belmonte, J.C., Anti-Aging Strategies Based on Cellular Reprogramming. Trends Mol. Med. 22 (2016), 725–738.
48. Orozco-Solis, R., Sassone-Corsi, P., Circadian clock: linking epigenetics to aging. Curr. Opin. Genet. Dev. 26 (2014), 66–72.
49. Pagani, L., Schmitt, K., Meier, F., Izakovic, J., Roemer, K., Viola, A., Cajochen, C., Wirz-Justice, A., Brown, S.A., Eckert, A., Serum factors in older individuals change cellular clock properties. Proc. Natl. Acad. Sci. USA 108 (2011), 7218–7223.
50. Patel, V.R., Eckel-Mahan, K., Sassone-Corsi, P., Baldi, P., CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics. Nat. Methods 9 (2012), 772–773.
51. Patel, S.A., Chaudhari, A., Gupta, R., Velingkaar, N., Kondratov, R.V., Circadian clocks govern calorie restriction-mediated life span extension through BMAL1- and IGF-1-dependent mechanisms. FASEB J. 30 (2016), 1634–1642.
52. Patel, S.A., Velingkaar, N., Makwana, K., Chaudhari, A., Kondratov, R., Calorie restriction regulates circadian clock gene expression through BMAL1 dependent and independent mechanisms. Sci. Rep., 6, 2016, 25970.
53. Peek, C.B., Affinati, A.H., Ramsey, K.M., Kuo, H.Y., Yu, W., Sena, L.A., Ilkayeva, O., Marcheva, B., Kobayashi, Y., Omura, C., et al. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science, 342, 2013, 1243417.
54. Peleg, S., Feller, C., Ladurner, A.G., Imhof, A., The Metabolic Impact on Histone Acetylation and Transcription in Ageing. Trends Biochem. Sci. 41 (2016), 700–711.
55. Pietrocola, F., Galluzzi, L., Bravo-San Pedro, J.M., Madeo, F., Kroemer, G., Acetyl coenzyme A: a central metabolite and second messenger. Cell Metab. 21 (2015), 805–821.
56. Ramsey, K.M., Yoshino, J., Brace, C.S., Abrassart, D., Kobayashi, Y., Marcheva, B., Hong, H.K., Chong, J.L., Buhr, E.D., Lee, C., et al. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324 (2009), 651–654.
57. Reppert, S.M., Weaver, D.R., Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 63 (2001), 647–676.
58. Rodgers, J.T., Lerin, C., Haas, W., Gygi, S.P., Spiegelman, B.M., Puigserver, P., Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434 (2005), 113–118.
59. Sahar, S., Masubuchi, S., Eckel-Mahan, K., Vollmer, S., Galla, L., Ceglia, N., Masri, S., Barth, T.K., Grimaldi, B., Oluyemi, O., et al. Circadian Control of Fatty Acid Elongation by SIRT1-mediated Deacetylation of Acetyl-CoA Synthetase 1. J Biol Chem, 289, 2014 6091-7.
60. Sato, R., Okamoto, A., Inoue, J., Miyamoto, W., Sakai, Y., Emoto, N., Shimano, H., Maeda, M., Transcriptional regulation of the ATP citrate-lyase gene by sterol regulatory element-binding proteins. J. Biol. Chem. 275 (2000), 12497–12502.
61. Sellix, M.T., Evans, J.A., Leise, T.L., Castanon-Cervantes, O., Hill, D.D., DeLisser, P., Block, G.D., Menaker, M., Davidson, A.J., Aging differentially affects the re-entrainment response of central and peripheral circadian oscillators. J. Neurosci. 32 (2012), 16193–16202.
62. Seufert, C.D., Graf, M., Janson, G., Kuhn, A., Söling, H.D., Formation of free acetate by isolated perfused livers from normal, starved and diabetic rats. Biochem. Biophys. Res. Commun. 57 (1974), 901–909.
63. Shimazu, T., Hirschey, M.D., Hua, L., Dittenhafer-Reed, K.E., Schwer, B., Lombard, D.B., Li, Y., Bunkenborg, J., Alt, F.W., Denu, J.M., et al. SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab. 12 (2010), 654–661.
64. Solanas, G., Oliveira Peixoto, F., Perdiguero, E., Jardí, M., Ruiz-Bonilla, V., Datta, D., Symeonidi, A., Castellanos, A., Welz, P., Martín Caballero, J., et al. Adult stem cells undergo circadian reprogramming during ageing. Cell 170 (2017), 678–692 this issue.
65. Someya, S., Yu, W., Hallows, W.C., Xu, J., Vann, J.M., Leeuwenburgh, C., Tanokura, M., Denu, J.M., Prolla, T.A., Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143 (2010), 802–812.
66. Stein, L.R., Imai, S., Specific ablation of Nampt in adult neural stem cells recapitulates their functional defects during aging. EMBO J. 33 (2014), 1321–1340.
67. Stokkan, K.A., Yamazaki, S., Tei, H., Sakaki, Y., Menaker, M., Entrainment of the circadian clock in the liver by feeding. Science 291 (2001), 490–493.
68. Trammell, S.A., Brenner, C., Targeted, LCMS-based Metabolomics for Quantitative Measurement of NAD(+) Metabolites. Comput. Struct. Biotechnol. J., 4, 2013, e201301012.
69. Trammell, S.A., Schmidt, M.S., Weidemann, B.J., Redpath, P., Jaksch, F., Dellinger, R.W., Li, Z., Abel, E.D., Migaud, M.E., Brenner, C., Nicotinamide riboside is uniquely and orally bioavailable in mice and humans. Nat. Commun., 7, 2016, 12948.
70. Ulgherait, M., Chen, A., Oliva, M.K., Kim, H.X., Canman, J.C., Ja, W.W., Shirasu-Hiza, M., Dietary Restriction Extends the Lifespan of Circadian Mutants tim and per. Cell Metab. 24 (2016), 763–764.
71. + in aging, metabolism, and neurodegeneration. Science 350 (2015), 1208–1213.
72. Verdin, E., Ott, M., 50 years of protein acetylation: from gene regulation to epigenetics, metabolism and beyond. Nat. Rev. Mol. Cell Biol. 16 (2015), 258–264.
73. Welsh, D.K., Takahashi, J.S., Kay, S.A., Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 72 (2010), 551–577.
74. + repletion improves mitochondrial and stem cell function and enhances life span in mice. Science 352 (2016), 1436–1443.
75. Zwighaft, Z., Aviram, R., Shalev, M., Rousso-Noori, L., Kraut-Cohen, J., Golik, M., Brandis, A., Reinke, H., Aharoni, A., Kahana, C., Asher, G., Circadian Clock Control by Polyamine Levels through a Mechanism that Declines with Age. Cell Metab. 22 (2015), 874–885.