Reciprocal regulation of chaperone-mediated autophagy and the circadian clock.
ARNTL Transcription Factors
/ genetics
Aging
/ physiology
Animals
CLOCK Proteins
/ metabolism
Chaperone-Mediated Autophagy
/ physiology
Circadian Clocks
/ physiology
Circadian Rhythm
/ physiology
Lysosomal-Associated Membrane Protein 2
/ genetics
Lysosomes
/ chemistry
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Photoperiod
Proteome
/ genetics
Proteostasis
/ physiology
Sleep Deprivation
/ physiopathology
Transcription, Genetic
/ genetics
Journal
Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
14
08
2020
accepted:
22
10
2021
pubmed:
9
12
2021
medline:
24
2
2022
entrez:
8
12
2021
Statut:
ppublish
Résumé
Circadian rhythms align physiological functions with the light-dark cycle through oscillatory changes in the abundance of proteins in the clock transcriptional programme. Timely removal of these proteins by different proteolytic systems is essential to circadian strength and adaptability. Here we show a functional interplay between the circadian clock and chaperone-mediated autophagy (CMA), whereby CMA contributes to the rhythmic removal of clock machinery proteins (selective chronophagy) and to the circadian remodelling of a subset of the cellular proteome. Disruption of this autophagic pathway in vivo leads to temporal shifts and amplitude changes of the clock-dependent transcriptional waves and fragmented circadian patterns, resembling those in sleep disorders and ageing. Conversely, loss of the circadian clock abolishes the rhythmicity of CMA, leading to pronounced changes in the CMA-dependent cellular proteome. Disruption of this circadian clock/CMA axis may be responsible for both pathways malfunctioning in ageing and for the subsequently pronounced proteostasis defect.
Identifiants
pubmed: 34876687
doi: 10.1038/s41556-021-00800-z
pii: 10.1038/s41556-021-00800-z
pmc: PMC8688252
mid: NIHMS1750705
doi:
Substances chimiques
ARNTL Transcription Factors
0
Bmal1 protein, mouse
0
Lysosomal-Associated Membrane Protein 2
0
Proteome
0
CLOCK Proteins
EC 2.3.1.48
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1255-1270Subventions
Organisme : NIA NIH HHS
ID : R01 AG021904
Pays : United States
Organisme : NICHD NIH HHS
ID : P50 HD105354
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG043517
Pays : United States
Organisme : NIA NIH HHS
ID : R37 AG021904
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007491
Pays : United States
Organisme : NIA NIH HHS
ID : RF1 AG054108
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG038072
Pays : United States
Organisme : NICHD NIH HHS
ID : U54 HD086984
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL144456
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI113919
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK020541
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK098408
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007288
Pays : United States
Organisme : NIA NIH HHS
ID : RF1 AG043517
Pays : United States
Organisme : NIA NIH HHS
ID : P01 AG031782
Pays : United States
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Dunlap, J. C. Molecular bases for circadian clocks. Cell 96, 271–290 (1999).
pubmed: 9988221
doi: 10.1016/S0092-8674(00)80566-8
Bass, J. & Takahashi, J. S. Circadian integration of metabolism and energetics. Science 330, 1349–1354 (2010).
pubmed: 21127246
pmcid: 3756146
doi: 10.1126/science.1195027
Mohawk, J. A., Green, C. B. & Takahashi, J. S. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35, 445–462 (2012).
pubmed: 22483041
pmcid: 3710582
doi: 10.1146/annurev-neuro-060909-153128
Lowrey, P. L. & Takahashi, J. S. Genetics of circadian rhythms in mammalian model organisms. Adv. Genet. 74, 175–230 (2011).
pubmed: 21924978
pmcid: 3709251
doi: 10.1016/B978-0-12-387690-4.00006-4
King, D. P. et al. Positional cloning of the mouse circadian clock gene. Cell 89, 641–653 (1997).
pubmed: 9160755
pmcid: 3815553
doi: 10.1016/S0092-8674(00)80245-7
Lee, C., Etchegaray, J. P., Cagampang, F. R., Loudon, A. S. & Reppert, S. M. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107, 855–867 (2001).
pubmed: 11779462
doi: 10.1016/S0092-8674(01)00610-9
Gekakis, N. et al. Role of the CLOCK protein in the mammalian circadian mechanism. Science 280, 1564–1569 (1998).
pubmed: 9616112
doi: 10.1126/science.280.5369.1564
Cho, H. et al. Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 485, 123–127 (2012).
pubmed: 22460952
pmcid: 3367514
doi: 10.1038/nature11048
Brown, S. A., Kowalska, E. & Dallmann, R. (Re)inventing the circadian feedback loop. Dev. Cell 22, 477–487 (2012).
pubmed: 22421040
doi: 10.1016/j.devcel.2012.02.007
Stojkovic, K., Wing, S. S. & Cermakian, N. A central role for ubiquitination within a circadian clock protein modification code. Front. Mol. Neurosci. 7, 69 (2014).
pubmed: 25147498
pmcid: 4124793
doi: 10.3389/fnmol.2014.00069
Gatfield, D. & Schibler, U. Physiology. Proteasomes keep the circadian clock ticking. Science 316, 1135–1136 (2007).
pubmed: 17495136
doi: 10.1126/science.1144165
Liu, J. et al. Distinct control of PERIOD2 degradation and circadian rhythms by the oncoprotein and ubiquitin ligase MDM2. Sci. Signal 11, 556 (2018).
Siepka, S. M. et al. Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell 129, 1011–1023 (2007).
pubmed: 17462724
pmcid: 3762874
doi: 10.1016/j.cell.2007.04.030
Toledo, M. et al. Autophagy regulates the liver clock and glucose metabolism by degrading CRY1. Cell Metab. 28, 268–281.e264 (2018).
pubmed: 29937374
pmcid: 6082686
doi: 10.1016/j.cmet.2018.05.023
Yang, M. et al. Clockophagy is a novel selective autophagy process favoring ferroptosis. Sci. Adv. 5, eaaw2238 (2019).
pubmed: 31355331
pmcid: 6656546
doi: 10.1126/sciadv.aaw2238
Kaushik, S. & Cuervo, A. M. The coming of age of chaperone-mediated autophagy. Nat. Rev. Mol. Cell Biol. 19, 365–381 (2018).
pubmed: 29626215
pmcid: 6399518
doi: 10.1038/s41580-018-0001-6
Chiang, H., Terlecky, S., Plant, C. & Dice, J. F. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246, 382–385 (1989).
pubmed: 2799391
doi: 10.1126/science.2799391
Cuervo, A. M. & Dice, J. F. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273, 501–503 (1996).
pubmed: 8662539
doi: 10.1126/science.273.5274.501
Bandyopadhyay, U., Sridhar, S., Kaushik, S., Kiffin, R. & Cuervo, A. M. Identification of regulators of chaperone-mediated autophagy. Mol. Cell 39, 535–547 (2010).
pubmed: 20797626
pmcid: 2945256
doi: 10.1016/j.molcel.2010.08.004
Agarraberes, F., Terlecky, S. & Dice, J. An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J. Cell Biol. 137, 825–834 (1997).
pubmed: 9151685
pmcid: 2139836
doi: 10.1083/jcb.137.4.825
Dice, J. F. Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem. Sci. 15, 305–309 (1990).
pubmed: 2204156
doi: 10.1016/0968-0004(90)90019-8
Bandyopadhyay, U., Kaushik, S., Varticovski, L. & Cuervo, A. M. The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol. Cell Biol. 28, 5747–5763 (2008).
pubmed: 18644871
pmcid: 2546938
doi: 10.1128/MCB.02070-07
Cuervo, A. M., Dice, J. F. & Knecht, E. A population of rat liver lysosomes responsible for the selective uptake and degradation of cytosolic proteins. J. Biol. Chem. 272, 5606–5615 (1997).
pubmed: 9038169
doi: 10.1074/jbc.272.9.5606
Gatfield, D. & Schibler, U. Proteasomes keep the circadian clock ticking. Science 316, 1135 (2007).
pubmed: 17495136
doi: 10.1126/science.1144165
Chen, S. et al. Ubiquitin-conjugating enzyme UBE2O regulates cellular clock function by promoting the degradation of the transcription factor BMAL1. J. Biol. Chem. 293, 11296–11309 (2018).
pubmed: 29871923
pmcid: 6065165
doi: 10.1074/jbc.RA117.001432
D’ Alessandro, M. et al. Stability of wake–sleep cycles requires robust degradation of the PERIOD protein. Curr. Biol. 27, 3454–3467.e3458 (2017).
doi: 10.1016/j.cub.2017.10.014
DeBruyne, J. P., Baggs, J. E., Sato, T. K. & Hogenesch, J. B. Ubiquitin ligase Siah2 regulates RevErbα degradation and the mammalian circadian clock. Proc. Natl Acad. Sci. USA 112, 12420–12425 (2015).
pubmed: 26392558
pmcid: 4603519
doi: 10.1073/pnas.1501204112
Zhao, X. et al. Circadian amplitude regulation via FBXW7-targeted REV-ERBα degradation. Cell 165, 1644–1657 (2016).
pubmed: 27238018
pmcid: 4912445
doi: 10.1016/j.cell.2016.05.012
Ma, D., Panda, S. & Lin, J. D. Temporal orchestration of circadian autophagy rhythm by C/EBPβ. EMBO J. 30, 4642–4651 (2011).
pubmed: 21897364
pmcid: 3243590
doi: 10.1038/emboj.2011.322
Schneider, J. L. et al. Loss of hepatic chaperone-mediated autophagy accelerates proteostasis failure in aging. Aging Cell 14, 249–264 (2015).
pubmed: 25620427
pmcid: 4364837
doi: 10.1111/acel.12310
Schneider, J. L., Suh, Y. & Cuervo, A. M. Deficient chaperone-mediated autophagy in liver leads to metabolic dysregulation. Cell Metab. 20, 417–432 (2014).
pubmed: 25043815
pmcid: 4156578
doi: 10.1016/j.cmet.2014.06.009
Kaushik, S. & Cuervo, A. M. Degradation of lipid droplet-associated proteins by chaperone-mediated autophagy facilitates lipolysis. Nat. Cell Biol. 17, 759–770 (2015).
pubmed: 25961502
pmcid: 4449813
doi: 10.1038/ncb3166
Pastore, N. et al. Nutrient-sensitive transcription factors TFEB and TFE3 couple autophagy and metabolism to the peripheral clock. EMBO J. 38, e101347 (2019).
pubmed: 31126958
pmcid: 6576167
doi: 10.15252/embj.2018101347
Kisselev, A. F. & Goldberg, A. L. Proteasome inhibitors: from research tools to drug candidates. Chem. Biol. 8, 739–758 (2001).
pubmed: 11514224
doi: 10.1016/S1074-5521(01)00056-4
Hornbeck, P. V. et al. PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res. 43, D512–D520 (2015).
pubmed: 25514926
doi: 10.1093/nar/gku1267
Brenna, A. & Albrecht, U. Phosphorylation and circadian molecular timing. Front. Physiol. 11, 612510 (2020).
pubmed: 33324245
pmcid: 7726318
doi: 10.3389/fphys.2020.612510
Nakahata, Y. et al. The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134, 329–340 (2008).
pubmed: 18662547
pmcid: 3526943
doi: 10.1016/j.cell.2008.07.002
Hirayama, J. et al. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 450, 1086–1090 (2007).
pubmed: 18075593
doi: 10.1038/nature06394
Park, C., Suh, Y. & Cuervo, A. M. Regulated degradation of Chk1 by chaperone-mediated autophagy in response to DNA damage. Nat. Commun. 6, 6823 (2015).
pubmed: 25880015
doi: 10.1038/ncomms7823
Lowrey, P. L. & Takahashi, J. S. Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu. Rev. Genomics Hum. Genet. 5, 407–441 (2004).
pubmed: 15485355
pmcid: 3770722
doi: 10.1146/annurev.genom.5.061903.175925
Kwon, I. et al. BMAL1 shuttling controls transactivation and degradation of the CLOCK/BMAL1 heterodimer. Mol. Cell. Biol. 26, 7318–7330 (2006).
pubmed: 16980631
pmcid: 1592876
doi: 10.1128/MCB.00337-06
Jud, C., Schmutz, I., Hampp, G., Oster, H. & Albrecht, U. A guideline for analyzing circadian wheel-running behavior in rodents under different lighting conditions. Biol. Proced. Online 7, 101–116 (2005).
pubmed: 16136228
pmcid: 1190381
doi: 10.1251/bpo109
Cuervo, A. M. & Dice, J. F. Age-related decline in chaperone-mediated autophagy. J. Biol. Chem. 275, 31505–31513 (2000).
pubmed: 10806201
doi: 10.1074/jbc.M002102200
Zhang, C. & Cuervo, A. M. Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat. Med. 14, 959–965 (2008).
pubmed: 18690243
pmcid: 2722716
doi: 10.1038/nm.1851
Bourdenx, M. et al. Chaperone-mediated autophagy prevents collapse of the neuronal metastable proteome. Cell 184, 2696–2714 e2625 (2021).
pubmed: 33891876
doi: 10.1016/j.cell.2021.03.048
Dong, S. et al. Chaperone-mediated autophagy sustains haematopoietic stem-cell function. Nature 591, 117–123 (2021).
pubmed: 33442062
pmcid: 8428053
doi: 10.1038/s41586-020-03129-z
Valdor, R. et al. Chaperone-mediated autophagy regulates T cell responses through targeted degradation of negative regulators of T cell activation. Nat. Immunol. 15, 1046–1054 (2014).
pubmed: 25263126
pmcid: 4208273
doi: 10.1038/ni.3003
Chang, H.-C. & Guarente, L. SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell 153, 1448–1460 (2013).
pubmed: 23791176
pmcid: 3748806
doi: 10.1016/j.cell.2013.05.027
Solanas, G. et al. Aged stem cells reprogram their daily rhythmic functions to adapt to stress. Cell 170, 678–692.e620 (2017).
pubmed: 28802040
doi: 10.1016/j.cell.2017.07.035
Sato, S. et al. Circadian reprogramming in the liver identifies metabolic pathways of aging. Cell 170, 664–677.e611 (2017).
pubmed: 28802039
pmcid: 7792549
doi: 10.1016/j.cell.2017.07.042
Dong, S. et al. Monitoring spatiotemporal changes in chaperone-mediated autophagy in vivo. Nat. Commun. 11, 645 (2020).
pubmed: 32005807
pmcid: 6994528
doi: 10.1038/s41467-019-14164-4
Ma, Q. et al. Age-related autophagy alterations in the brain of senescence accelerated mouse prone 8 (SAMP8) mice. Exp. Gerontol. 46, 533–541 (2011).
pubmed: 21385605
doi: 10.1016/j.exger.2011.02.006
Cuervo, A. M. & Dice, J. F. Regulation of lamp2a levels in the lysosomal membrane. Traffic 1, 570–583 (2000).
pubmed: 11208145
doi: 10.1034/j.1600-0854.2000.010707.x
Kirchner, P. et al. Proteome-wide analysis of chaperone-mediated autophagy targeting motifs. PLoS Biol. 17, e3000301 (2019).
pubmed: 31150375
pmcid: 6561683
doi: 10.1371/journal.pbio.3000301
Yang, G. et al. Timing of expression of the core clock gene Bmal1 influences its effects on aging and survival. Sci. Transl. Med. 8, 324ra316 (2016).
Koike, N. et al. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338, 349–354 (2012).
pubmed: 22936566
pmcid: 3694775
doi: 10.1126/science.1226339
Anguiano, J. et al. Chemical modulation of chaperone-mediated autophagy by retinoic acid derivatives. Nat. Chem. Biol. 9, 374–382 (2013).
pubmed: 23584676
pmcid: 3661710
doi: 10.1038/nchembio.1230
Cuervo, A. M., Knecht, E., Terlecky, S. R. & Dice, J. F. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am. J. Physiol. 269, C1200–C1208 (1995).
pubmed: 7491910
doi: 10.1152/ajpcell.1995.269.5.C1200
Kiffin, R., Bandyopadhyay, U. & Cuervo, A. Oxidative stress and autophagy. Antioxid. Redox Signal 8, 152–162 (2006).
pubmed: 16487049
doi: 10.1089/ars.2006.8.152
Pittendrigh, C. S. Circadian rhythms and the circadian organization of living systems. Cold Spring Harb. Symp. Quant. Biol. 25, 159–184 (1960).
pubmed: 13736116
doi: 10.1101/SQB.1960.025.01.015
Kaushik, S., Massey, A., Mizushima, N. & Cuervo, A. M. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol. Biol. Cell 19, 2179–2192 (2008).
pubmed: 18337468
pmcid: 2366850
doi: 10.1091/mbc.e07-11-1155
Massey, A. C., Kaushik, S., Sovak, G., Kiffin, R. & Cuervo, A. M. Consequences of the selective blockage of chaperone-mediated autophagy. Proc. Natl Acad. Sci. USA 103, 5905–5910 (2006).
doi: 10.1073/pnas.0507436103
Cuervo, A. M., Palmer, A., Rivett, A. J. & Knecht, E. Degradation of proteasomes by lysosomes in rat liver. Eur. J. Biochem. 227, 792–800 (1995).
pubmed: 7867640
doi: 10.1111/j.1432-1033.1995.tb20203.x
Zhou, B. et al. CLOCK/BMAL1 regulates circadian change of mouse hepatic insulin sensitivity by SIRT1. Hepatology 59, 2196–2206 (2014).
pubmed: 24442997
doi: 10.1002/hep.26992
Cuervo, A. M., Stefanis, L., Fredenburg, R., Lansbury, P. T. & Sulzer, D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305, 1292–1295 (2004).
pubmed: 15333840
doi: 10.1126/science.1101738
Caballero, B. et al. Interplay of pathogenic forms of human tau with different autophagic pathways. Aging Cell https://doi.org/10.1111/acel.12692 (2018).
Abbott, S. M. & Videnovic, A. Chronic sleep disturbance and neural injury: links to neurodegenerative disease. Nat. Sci. Sleep. 8, 55–61 (2016).
pubmed: 26869817
pmcid: 4734786
Kondratova, A. A. & Kondratov, R. V. The circadian clock and pathology of the ageing brain. Nat. Rev. Neurosci. 13, 325–335 (2012).
pubmed: 22395806
pmcid: 3718301
doi: 10.1038/nrn3208
Mattis, J. & Sehgal, A. Circadian rhythms, sleep, and disorders of aging. Trends Endocrinol. Metab. 27, 192–203 (2016).
pubmed: 26947521
pmcid: 4808513
doi: 10.1016/j.tem.2016.02.003
Martinez-Lopez, N. et al. System-wide benefits of intermeal fasting by autophagy. Cell Metab. 26, 856–871 e855 (2017).
pubmed: 29107505
pmcid: 5718973
doi: 10.1016/j.cmet.2017.09.020
Balsalobre, A. et al. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289, 2344–2347 (2000).
pubmed: 11009419
doi: 10.1126/science.289.5488.2344
Storrie, B. & Madden, E. Isolation of subcellular organelles. Methods Enzymol. 182, 203–225 (1990).
pubmed: 2156127
doi: 10.1016/0076-6879(90)82018-W
Lowry, O., Rosebrough, N., Farr, A. & Randall, R. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951).
pubmed: 14907713
doi: 10.1016/S0021-9258(19)52451-6
Juste, Y. R. & Cuervo, A. M. Analysis of chaperone-mediated autophagy. Methods Mol. Biol. 1880, 703–727 (2019).
pubmed: 30610733
pmcid: 7017676
doi: 10.1007/978-1-4939-8873-0_47
Ye, R., Selby, C. P., Ozturk, N., Annayev, Y. & Sancar, A. Biochemical analysis of the canonical model for the mammalian circadian clock. J. Biol. Chem. 286, 25891–25902 (2011).
pubmed: 21613214
pmcid: 3138243
doi: 10.1074/jbc.M111.254680
Bolte, S. & Cordelieres, F. P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213–232 (2006).
pubmed: 17210054
doi: 10.1111/j.1365-2818.2006.01706.x