The circadian rhythm in intervertebral disc degeneration: an autophagy connection.
Journal
Experimental & molecular medicine
ISSN: 2092-6413
Titre abrégé: Exp Mol Med
Pays: United States
ID NLM: 9607880
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
16
07
2019
accepted:
17
09
2019
revised:
01
09
2019
pubmed:
28
1
2020
medline:
1
7
2021
entrez:
28
1
2020
Statut:
ppublish
Résumé
There is one circadian clock in the central nervous system and another in the peripheral organs, and the latter is driven by an autoregulatory molecular clock composed of several core clock genes. The height, water content, osmotic pressure and mechanical characteristics of intervertebral discs (IVDs) have been demonstrated to exhibit a circadian rhythm (CR). Recently, a molecular clock has been shown to exist in IVDs, abolition of which can lead to stress in nucleus pulposus cells (NPCs), contributing to intervertebral disc degeneration (IDD). Autophagy is a fundamental cellular process in eukaryotes and is essential for individual cells or organs to respond and adapt to changing environments; it has also been demonstrated to occur in human NPCs. Increasing evidence supports the hypothesis that autophagy is associated with CR. Thus, we review the connection between CR and autophagy and the roles of these mechanisms in IDD.
Identifiants
pubmed: 31983731
doi: 10.1038/s12276-019-0372-6
pii: 10.1038/s12276-019-0372-6
pmc: PMC7000407
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
31-40Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 81772855
Pays : International
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 81572629
Pays : International
Références
Deyo, R. A. & Weinstein, J. N. Low back pain. N. Engl. J. Med 344, 363–370 (2001).
pubmed: 11172169
doi: 10.1056/NEJM200102013440508
Pattappa, G. et al. Diversity of intervertebral disc cells: phenotype and function. J. Anat. 221, 480–496 (2012).
pubmed: 22686699
pmcid: 3512276
doi: 10.1111/j.1469-7580.2012.01521.x
Urban, J. P., Smith, S. & Fairbank, J. C. Nutrition of the intervertebral disc. Spine (Philos. Pa 1976) 29, 2700–2709 (2004).
doi: 10.1097/01.brs.0000146499.97948.52
Yuan, W. et al. Establishment of intervertebral disc degeneration model induced by ischemic sub-endplate in rat tail. Spine J. 15, 1050–1059 (2015).
pubmed: 25637466
doi: 10.1016/j.spinee.2015.01.026
Massey, C. J., van Donkelaar, C. C., Vresilovic, E., Zavaliangos, A. & Marcolongo, M. Effects of aging and degeneration on the human intervertebral disc during the diurnal cycle: a finite element study. J. Orthop. Res 30, 122–128 (2012).
pubmed: 21710607
doi: 10.1002/jor.21475
Sivan, S., Neidlinger-Wilke, C., Wurtz, K., Maroudas, A. & Urban, J. P. Diurnal fluid expression and activity of intervertebral disc cells. Biorheology 43, 283–291 (2006).
pubmed: 16912401
Numaguchi, S. et al. Passive cigarette smoking changes the circadian rhythm of clock genes in rat intervertebral discs. J. Orthop. Res 34, 39–47 (2016).
pubmed: 25939642
doi: 10.1002/jor.22941
Dudek, M. et al. The intervertebral disc contains intrinsic circadian clocks that are regulated by age and cytokines and linked to degeneration. Ann. Rheum. Dis. 76, 576–584 (2017).
pubmed: 27489225
doi: 10.1136/annrheumdis-2016-209428
Akagi, R. et al. Dysregulated circadian rhythm pathway in human osteoarthritis: NR1D1 and BMAL1 suppression alters TGF-beta signaling in chondrocytes. Osteoarthr. Cartil. 25, 943–951 (2017).
doi: 10.1016/j.joca.2016.11.007
Green, C. B., Takahashi, J. S. & Bass, J. The meter of metabolism. Cell 134, 728–742 (2008).
pubmed: 18775307
pmcid: 3760165
doi: 10.1016/j.cell.2008.08.022
Rubinsztein, D. C., Marino, G. & Kroemer, G. Autophagy and aging. Cell 146, 682–695 (2011).
pubmed: 21884931
doi: 10.1016/j.cell.2011.07.030
Ito, M. et al. Selective interference of mTORC1/RAPTOR protects against human disc cellular apoptosis, senescence, and extracellular matrix catabolism with Akt and autophagy induction. Osteoarthr. Cartil. 25, 2134–2146 (2017).
doi: 10.1016/j.joca.2017.08.019
Ma, D., Panda, S. & Lin, J. D. Temporal orchestration of circadian autophagy rhythm by C/EBPbeta. EMBO J. 30, 4642–4651 (2011).
pubmed: 21897364
pmcid: 3243590
doi: 10.1038/emboj.2011.322
Dibner, C., Schibler, U. & Albrecht, U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev. Physiol. 72, 517–549 (2010).
pubmed: 20148687
doi: 10.1146/annurev-physiol-021909-135821
Partch, C. L., Green, C. B. & Takahashi, J. S. Molecular architecture of the mammalian circadian clock. Trends Cell Biol. 24, 90–99 (2014).
pubmed: 23916625
doi: 10.1016/j.tcb.2013.07.002
Reddy, A. B. & Rey, G. Metabolic and nontranscriptional circadian clocks: eukaryotes. Annu Rev. Biochem 83, 165–189 (2014).
pubmed: 24606143
pmcid: 4768355
doi: 10.1146/annurev-biochem-060713-035623
Rey, G. & Reddy, A. B. Connecting cellular metabolism to circadian clocks. Trends Cell Biol. 23, 234–241 (2013).
pubmed: 23391694
doi: 10.1016/j.tcb.2013.01.003
Janich, P., Meng, Q. J. & Benitah, S. A. Circadian control of tissue homeostasis and adult stem cells. Curr. Opin. Cell Biol. 31, 8–15 (2014).
pubmed: 25016176
doi: 10.1016/j.ceb.2014.06.010
Reilly, T., Tyrrell, A. & Troup, J. D. Circadian variation in human stature. Chronobiol. Int 1, 121–126 (1984).
pubmed: 6600017
doi: 10.3109/07420528409059129
Kramer, J. & Gritz, A. [Changes in body length by pressure dependent fluid shifts in the intervertebral discs (author’s transl)]. Z. Orthop. Ihre Grenzgeb. 118, 161–164 (1980).
pubmed: 7191602
doi: 10.1055/s-2008-1053491
Adams, M. A., Dolan, P. & Hutton, W. C. Diurnal variations in the stresses on the lumbar spine. Spine (Philos. Pa 1976) 12, 130–137 (1987).
doi: 10.1097/00007632-198703000-00008
Gantenbein, B. et al. An in vitro organ culturing system for intervertebral disc explants with vertebral endplates: a feasibility study with ovine caudal discs. Spine (Philos. Pa 1976) 31, 2665–2673 (2006).
doi: 10.1097/01.brs.0000244620.15386.df
Suyama, K. et al. Circadian factors BMAL1 and RORalpha control HIF-1alpha transcriptional activity in nucleus pulposus cells: implications in maintenance of intervertebral disc health. Oncotarget 7, 23056–23071 (2016).
pubmed: 27049729
pmcid: 5029610
doi: 10.18632/oncotarget.8521
Wu, D., Potluri, N., Lu, J., Kim, Y. & Rastinejad, F. Structural integration in hypoxia-inducible factors. Nature 524, 303–308 (2015).
pubmed: 26245371
doi: 10.1038/nature14883
Codogno, P., Mehrpour, M. & Proikas-Cezanne, T. Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat. Rev. Mol. Cell Biol. 13, 7–12 (2011).
pubmed: 22166994
doi: 10.1038/nrm3249
Kim, J., Kundu, M., Viollet, B. & Guan, K. L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13, 132–141 (2011).
pubmed: 21258367
pmcid: 3987946
doi: 10.1038/ncb2152
Hosokawa, N. et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 20, 1981–1991 (2009).
pubmed: 19211835
pmcid: 2663915
doi: 10.1091/mbc.e08-12-1248
Lee, J. W., Park, S., Takahashi, Y. & Wang, H. G. The association of AMPK with ULK1 regulates autophagy. PLoS ONE 5, e15394 (2010).
pubmed: 21072212
pmcid: 2972217
doi: 10.1371/journal.pone.0015394
Grimmel, M., Backhaus, C. & Proikas-Cezanne, T. WIPI-Mediated Autophagy and Longevity. Cells 4, 202–217 (2015).
pubmed: 26010754
pmcid: 4493456
doi: 10.3390/cells4020202
Di Bartolomeo, S. et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J. Cell Biol. 191, 155–168 (2010).
pubmed: 20921139
pmcid: 2953445
doi: 10.1083/jcb.201002100
Itakura, E. & Mizushima, N. Atg14 and UVRAG: mutually exclusive subunits of mammalian Beclin 1-PI3K complexes. Autophagy 5, 534–536 (2009).
pubmed: 19223761
doi: 10.4161/auto.5.4.8062
Mizushima, N. & Komatsu, M. Autophagy: renovation of cells and tissues. Cell 147, 728–741 (2011).
pubmed: 22078875
doi: 10.1016/j.cell.2011.10.026
Yang, Z. & Klionsky, D. J. Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22, 124–131 (2010).
pubmed: 20034776
doi: 10.1016/j.ceb.2009.11.014
Levine, B. & Kroemer, G. Autophagy in the pathogenesis of disease. Cell 132, 27–42 (2008).
pubmed: 18191218
pmcid: 2696814
doi: 10.1016/j.cell.2007.12.018
Xu, H., Xiong, S., Wang, H., Zhang, M. & Yu, Y. The evidence and the possible significance of autophagy in degeneration model of human cervical end-plate cartilage. Exp. Ther. Med 7, 537–542 (2014).
pubmed: 24520242
doi: 10.3892/etm.2013.1465
Yu, Y. F. et al. [Change of autophagy in endplate chondrocytes of rats during aging process]. Zhonghua Yi Xue Za Zhi 93, 3632–3635 (2013).
pubmed: 24534320
Ye, W. et al. Age-related increases of macroautophagy and chaperone-mediated autophagy in rat nucleus pulposus. Connect Tissue Res 52, 472–478 (2011).
pubmed: 21591930
doi: 10.3109/03008207.2011.564336
Gruber, H. E., Hoelscher, G. L., Ingram, J. A., Bethea, S. & Hanley, E. N. Jr. Autophagy in the degenerating human intervertebral disc: in vivo molecular and morphological evidence, and induction of autophagy in cultured annulus cells exposed to proinflammatory cytokines-implications for disc degeneration. Spine (Philos. Pa 1976) 40, 773–782 (2015).
doi: 10.1097/BRS.0000000000000865
Shen, J. et al. IL-1beta induces apoptosis and autophagy via mitochondria pathway in human degenerative nucleus pulposus cells. Sci. Rep. 7, 41067 (2017).
pubmed: 28120948
pmcid: 5264394
doi: 10.1038/srep41067
Chen, L. et al. Protein kinase RNA-like ER kinase/eukaryotic translation initiation factor 2alpha pathway attenuates tumor necrosis factor alpha-induced apoptosis in nucleus pulposus cells by activating autophagy. J. Cell Physiol. 234, 11631–11645 (2019).
pubmed: 30515797
doi: 10.1002/jcp.27820
Xu, K. et al. Autophagy attenuates the catabolic effect during inflammatory conditions in nucleus pulposus cells, as sustained by NF-kappaB and JNK inhibition. Int J. Mol. Med 36, 661–668 (2015).
pubmed: 26165348
pmcid: 4533778
doi: 10.3892/ijmm.2015.2280
Shen, C., Yan, J., Jiang, L. S. & Dai, L. Y. Autophagy in rat annulus fibrosus cells: evidence and possible implications. Arthritis Res Ther. 13, R132 (2011).
pubmed: 21846367
pmcid: 3239374
doi: 10.1186/ar3443
Jiang, L. B. et al. Activation of autophagy via Ca(2+)-dependent AMPK/mTOR pathway in rat notochordal cells is a cellular adaptation under hyperosmotic stress. Cell Cycle 14, 867–879 (2015).
pubmed: 25590373
pmcid: 4615023
doi: 10.1080/15384101.2015.1004946
Liu, C. et al. Lack of evidence for involvement of TonEBP and hyperosmotic stimulus in induction of autophagy in the nucleus pulposus. Sci. Rep. 7, 4543 (2017).
pubmed: 28674405
pmcid: 5495809
doi: 10.1038/s41598-017-04876-2
Xu, H. G. et al. Autophagy protects end plate chondrocytes from intermittent cyclic mechanical tension induced calcification. Bone 66, 232–239 (2014).
pubmed: 24970040
doi: 10.1016/j.bone.2014.06.018
Kakiuchi, Y. et al. Pharmacological inhibition of mTORC1 but not mTORC2 protects against human disc cellular apoptosis, senescence, and extracellular matrix catabolism through Akt and autophagy induction. Osteoarthr. Cartil. 27, 965–976 (2019).
doi: 10.1016/j.joca.2019.01.009
Pfeifer, U. Cellular autophagy and cell atrophy in the rat liver during long-term starvation. A quantitative morphological study with regard to diurnal variations. Virchows Arch. B Cell Pathol. 12, 195–211 (1973).
pubmed: 4350479
Pfeifer, U. & Strauss, P. Autophagic vacuoles in heart muscle and liver. A comparative morphometric study including circadian variations in meal-fed rats. J. Mol. Cell Cardiol. 13, 37–49 (1981).
pubmed: 7253029
doi: 10.1016/0022-2828(81)90227-3
Yao, J. et al. Circadian and noncircadian modulation of autophagy in photoreceptors and retinal pigment epithelium. Invest Ophthalmol. Vis. Sci. 55, 3237–3246 (2014).
pubmed: 24781939
pmcid: 4037936
doi: 10.1167/iovs.13-13336
Huang, G., Zhang, F., Ye, Q. & Wang, H. The circadian clock regulates autophagy directly through the nuclear hormone receptor Nr1d1/Rev-erbalpha and indirectly via Cebpb/(C/ebpbeta) in zebrafish. Autophagy 12, 1292–1309 (2016).
pubmed: 27171500
pmcid: 4968235
doi: 10.1080/15548627.2016.1183843
He, Y. et al. Circadian rhythm of autophagy proteins in hippocampus is blunted by sleep fragmentation. Chronobiol. Int 33, 553–560 (2016).
pubmed: 27078501
doi: 10.3109/07420528.2015.1137581
Reme, C. & Wirz-Justice, A. [Circadian rhythm, the retina and light]. Klin. Monbl Augenheilkd. 186, 175–179 (1985).
pubmed: 3889477
doi: 10.1055/s-2008-1050899
Rabinovich-Nikitin, I., Lieberman, B., Martino, T. A. & Kirshenbaum, L. A. Circadian-regulated cell death in cardiovascular diseases. Circulation 139, 965–980 (2019).
pubmed: 30742538
doi: 10.1161/CIRCULATIONAHA.118.036550
Reme, C., Wirzjustice, A., Rhyner, A. & Hofmann, S. Circadian-rhythm in the light response of rat retinal disk-shedding and autophagy. Brain Res. 369, 356–360 (1986).
pubmed: 3697752
doi: 10.1016/0006-8993(86)90550-0
Frost, L. S. et al. The contribution of melanoregulin to microtubule-associated protein 1 light chain 3 (LC3) associated phagocytosis in retinal pigment epithelium. Mol. Neurobiol. 52, 1135–1151 (2015).
pubmed: 25301234
doi: 10.1007/s12035-014-8920-5
Ryzhikov, M. et al. Diurnal rhythms spatially and temporally organize autophagy. Cell Rep. 26, 1880–1892 e1886 (2019).
pubmed: 30759397
pmcid: 6442472
doi: 10.1016/j.celrep.2019.01.072
Chen, X., Kondo, K., Motoki, K., Homma, H. & Okazawa, H. Fasting activates macroautophagy in neurons of Alzheimer’s disease mouse model but is insufficient to degrade amyloid-beta. Sci. Rep. 5, 12115 (2015).
pubmed: 26169250
pmcid: 4648430
doi: 10.1038/srep12115
Pfeifer, U. & Scheller, H. A morphometric study of cellular autophagy including diurnal variations in kidney tubules of normal rats. J. Cell Biol. 64, 608–621 (1975).
pubmed: 1171105
doi: 10.1083/jcb.64.3.608
Kijak, E. & Pyza, E. TOR signaling pathway and autophagy are involved in the regulation of circadian rhythms in behavior and plasticity of L2 interneurons in the brain of Drosophila melanogaster. PLoS ONE 12, e0171848 (2017).
pubmed: 28196106
pmcid: 5308838
doi: 10.1371/journal.pone.0171848
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
Stockman, M. C., Thomas, D., Burke, J. & Apovian, C. M. Intermittent fasting: is the wait worth the weight? Curr. Obes. Rep. 7, 172–185 (2018).
pubmed: 29700718
pmcid: 5959807
doi: 10.1007/s13679-018-0308-9
Reme, C., Wirz-Justice, A., Rhyner, A. & Hofmann, S. Circadian rhythm in the light response of rat retinal disk-shedding and autophagy. Brain Res 369, 356–360 (1986).
pubmed: 3697752
doi: 10.1016/0006-8993(86)90550-0
Mohlin, C., Taylor, L., Ghosh, F. & Johansson, K. Autophagy and ER-stress contribute to photoreceptor degeneration in cultured adult porcine retina. Brain Res 1585, 167–183 (2014).
pubmed: 25173074
doi: 10.1016/j.brainres.2014.08.055
Wu, R. et al. The circadian protein period2 suppresses mTORC1 activity via recruiting Tsc1 to mTORC1 complex. Cell Metab. 29, 653–667 e656 (2019).
pubmed: 30527742
doi: 10.1016/j.cmet.2018.11.006
Kalfalah, F. et al. Crosstalk of clock gene expression and autophagy in aging. Aging (Albany NY) 8, 1876–1895 (2016).
doi: 10.18632/aging.101018
Wang, Z., Li, L. & Wang, Y. Effects of Per2 overexpression on growth inhibition and metastasis, and on MTA1, nm23-H1 and the autophagy-associated PI3K/PKB signaling pathway in nude mice xenograft models of ovarian cancer. Mol. Med Rep. 13, 4561–4568 (2016).
pubmed: 27082164
pmcid: 4878548
doi: 10.3892/mmr.2016.5116
Qiao, L. et al. The clock gene, brain and muscle Arnt-like 1, regulates autophagy in high glucose-induced cardiomyocyte injury. Oncotarget 8, 80612–80624 (2017).
pubmed: 29113329
pmcid: 5655224
Scotton, C. et al. Deep RNA profiling identified CLOCK and molecular clock genes as pathophysiological signatures in collagen VI myopathy. J. Cell Sci. 129, 1671–1684 (2016).
pubmed: 26945058
pmcid: 4852766
doi: 10.1242/jcs.175927
McGinnis, G. R. et al. Genetic disruption of the cardiomyocyte circadian clock differentially influences insulin-mediated processes in the heart. J. Mol. Cell Cardiol. 110, 80–95 (2017).
pubmed: 28736261
pmcid: 5586500
doi: 10.1016/j.yjmcc.2017.07.005
Sulli, G. et al. Pharmacological activation of REV-ERBs is lethal in cancer and oncogene-induced senescence. Nature 553, 351–355 (2018).
pubmed: 29320480
pmcid: 5924733
doi: 10.1038/nature25170
De Mei, C. et al. Dual inhibition of REV-ERBbeta and autophagy as a novel pharmacological approach to induce cytotoxicity in cancer cells. Oncogene 34, 2597–2608 (2015).
pubmed: 25023698
doi: 10.1038/onc.2014.203
Lamia, K. A. et al. AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326, 437–440 (2009).
pubmed: 19833968
pmcid: 2819106
doi: 10.1126/science.1172156
Sun, Y., Jin, L., Sui, Y. X., Han, L. L. & Liu, J. H. Circadian gene CLOCK Affects drug-resistant gene expression and cell proliferation in ovarian cancer SKOV3/DDP Cell lines through autophagy. Cancer Biother Radiopharm. 32, 139–146 (2017).
pubmed: 28514207
doi: 10.1089/cbr.2016.2153
Xiong, X., Tao, R., DePinho, R. A. & Dong, X. C. The autophagy-related gene 14 (Atg14) is regulated by forkhead box O transcription factors and circadian rhythms and plays a critical role in hepatic autophagy and lipid metabolism. J. Biol. Chem. 287, 39107–39114 (2012).
pubmed: 22992773
pmcid: 3493951
doi: 10.1074/jbc.M112.412569
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
Jeong, K. et al. Dual attenuation of proteasomal and autophagic BMAL1 degradation in Clock Delta19/+ mice contributes to improved glucose homeostasis. Sci. Rep. 5, 12801 (2015).
pubmed: 26228022
pmcid: 4521189
doi: 10.1038/srep12801
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
Belden, W. J. & Dunlap, J. C. SIRT1 is a circadian deacetylase for core clock components. Cell 134, 212–214 (2008).
pubmed: 18662537
pmcid: 3671948
doi: 10.1016/j.cell.2008.07.010
Asher, G. et al. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134, 317–328 (2008).
pubmed: 18662546
doi: 10.1016/j.cell.2008.06.050
Ghosh, H. S., McBurney, M. & Robbins, P. D. SIRT1 negatively regulates the mammalian target of rapamycin. PLoS ONE 5, e9199 (2010).
pubmed: 20169165
pmcid: 2821410
doi: 10.1371/journal.pone.0009199
Lan, F., Cacicedo, J. M., Ruderman, N. & Ido, Y. SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J. Biol. Chem. 283, 27628–27635 (2008).
pubmed: 18687677
pmcid: 2562073
doi: 10.1074/jbc.M805711200
Lee, I. H. et al. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl Acad. Sci. USA 105, 3374–3379 (2008).
pubmed: 18296641
doi: 10.1073/pnas.0712145105
pmcid: 2265142
Chung, S. et al. Regulation of SIRT1 in cellular functions: role of polyphenols. Arch. Biochem Biophys. 501, 79–90 (2010).
pubmed: 20450879
pmcid: 2930135
doi: 10.1016/j.abb.2010.05.003
Roohbakhsh, A., Shamsizadeh, A., Hayes, A. W., Reiter, R. J. & Karimi, G. Melatonin as an endogenous regulator of diseases: the role of autophagy. Pharmacol. Res. 133, 265–276 (2018).
pubmed: 29408249
doi: 10.1016/j.phrs.2018.01.022
Motilva, V., Garcia-Maurino, S., Talero, E. & Illanes, M. New paradigms in chronic intestinal inflammation and colon cancer: role of melatonin. J. Pineal Res 51, 44–60 (2011).
pubmed: 21752096
doi: 10.1111/j.1600-079X.2011.00915.x
Kongsuphol, P., Mukda, S., Nopparat, C., Villarroel, A. & Govitrapong, P. Melatonin attenuates methamphetamine-induced deactivation of the mammalian target of rapamycin signaling to induce autophagy in SK-N-SH cells. J. Pineal Res 46, 199–206 (2009).
pubmed: 19054297
doi: 10.1111/j.1600-079X.2008.00648.x
Nopparat, C., Porter, J. E., Ebadi, M. & Govitrapong, P. The mechanism for the neuroprotective effect of melatonin against methamphetamine-induced autophagy. J. Pineal Res 49, 382–389 (2010).
pubmed: 20738755
doi: 10.1111/j.1600-079X.2010.00805.x
Yoo, Y. M. & Jeung, E. B. Melatonin suppresses cyclosporine A-induced autophagy in rat pituitary GH3 cells. J. Pineal Res 48, 204–211 (2010).
pubmed: 20136702
doi: 10.1111/j.1600-079X.2010.00744.x
Jenwitheesuk, A., Nopparat, C., Mukda, S., Wongchitrat, P. & Govitrapong, P. Melatonin regulates aging and neurodegeneration through energy metabolism, epigenetics, autophagy and circadian rhythm pathways. Int J. Mol. Sci. 15, 16848–16884 (2014).
pubmed: 25247581
pmcid: 4200827
doi: 10.3390/ijms150916848
Zhao, Y. et al. Novel protective role of the circadian nuclear receptor retinoic acid-related orphan receptor-alpha in diabetic cardiomyopathy. J Pineal Res 62, https://doi.org/10.1111/jpi.12378 (2017).
He, B. et al. The nuclear melatonin receptor RORalpha is a novel endogenous defender against myocardial ischemia/reperfusion injury. J. Pineal Res 60, 313–326 (2016).
pubmed: 26797926
doi: 10.1111/jpi.12312
Zhang, L. F. et al. Coffee and caffeine potentiate the antiamyloidogenic activity of melatonin via inhibition of Abeta oligomerization and modulation of the Tau-mediated pathway in N2a/APP cells. Drug Des. Devel Ther. 9, 241–272 (2015).
pubmed: 25565776
Coronas-Samano, G., Baker, K. L., Tan, W. J., Ivanova, A. V. & Verhagen, J. V. Fus1 KO mouse as a model of oxidative stress-mediated sporadic Alzheimer’s disease: circadian disruption and long-term spatial and olfactory memory impairments. Front Aging Neurosci. 8, 268 (2016).
pubmed: 27895577
pmcid: 5108791
doi: 10.3389/fnagi.2016.00268
Damulewicz, M. et al. Daily regulation of phototransduction, circadian clock, DNA repair, and immune gene expression by heme oxygenase in the retina of Drosophila. Genes (Basel) 10, 6 (2018).
doi: 10.3390/genes10010006
Jiang, S., Zhang, M., Sun, J. & Yang, X. Casein kinase 1alpha: biological mechanisms and theranostic potential. Cell Commun. Signal 16, 23 (2018).
pubmed: 29793495
pmcid: 5968562
doi: 10.1186/s12964-018-0236-z
Pivovarova, O. et al. Regulation of the clock gene expression in human adipose tissue by weight loss. Int J. Obes. (Lond.) 40, 899–906 (2016).
doi: 10.1038/ijo.2016.34
Sun, Q. et al. Folate deprivation modulates the expression of autophagy- and circadian-related genes in HT-22 hippocampal neuron cells through GR-mediated pathway. Steroids 112, 12–19 (2016).
pubmed: 27133904
doi: 10.1016/j.steroids.2016.04.010
Tan, X. et al. Acrylamide aggravates cognitive deficits at night period via the gut-brain axis by reprogramming the brain circadian clock. Arch. Toxicol. 93, 467–486 (2019).
pubmed: 30374679
doi: 10.1007/s00204-018-2340-7
Bretin, A. et al. Activation of the EIF2AK4-EIF2A/eIF2alpha-ATF4 pathway triggers autophagy response to Crohn disease-associated adherent-invasive Escherichia coli infection. Autophagy 12, 770–783 (2016).
pubmed: 26986695
pmcid: 4854551
doi: 10.1080/15548627.2016.1156823
Chang, H. et al. Early-stage autophagy protects nucleus pulposus cells from glucose deprivation-induced degeneration via the p-eIF2alpha/ATF4 pathway. Biomed. Pharmacother. 89, 529–535 (2017).
pubmed: 28254665
doi: 10.1016/j.biopha.2017.02.074
Chen, J. W. et al. Hypoxia facilitates the survival of nucleus pulposus cells in serum deprivation by down-regulating excessive autophagy through restricting ROS generation. Int J. Biochem Cell Biol. 59, 1–10 (2015).
pubmed: 25456445
doi: 10.1016/j.biocel.2014.11.009
Elfering, A. et al. Risk factors for lumbar disc degeneration: a 5-year prospective MRI study in asymptomatic individuals. Spine (Philos. Pa 1976) 27, 125–134 (2002).
doi: 10.1097/00007632-200201150-00002
Yang, W. et al. Interleukin-1beta in intervertebral disk degeneration. Clin. Chim. Acta 450, 262–272 (2015).
pubmed: 26341894
doi: 10.1016/j.cca.2015.08.029