The tight junction protein TJP1 regulates the feeding-modulated hepatic circadian clock.
Animals
Cell Nucleus
/ metabolism
Cells, Cultured
Circadian Clocks
/ physiology
Dogs
Feeding Behavior
HEK293 Cells
Hepatocytes
/ metabolism
Humans
Insulin Resistance
Liver
/ physiology
Madin Darby Canine Kidney Cells
Mice, Inbred C57BL
Mice, Knockout
Models, Biological
Mutation
/ genetics
Period Circadian Proteins
/ metabolism
Phosphorylation
Protein Binding
Protein Transport
RNA, Messenger
/ genetics
TOR Serine-Threonine Kinases
/ metabolism
Zonula Occludens-1 Protein
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
30 01 2020
30 01 2020
Historique:
received:
24
08
2018
accepted:
10
01
2020
entrez:
1
2
2020
pubmed:
1
2
2020
medline:
14
4
2020
Statut:
epublish
Résumé
Circadian clocks in the suprachiasmatic nucleus and peripheral tissues orchestrate behavioral and physiological activities of mammals in response to environmental cues. In the liver, the circadian clock is also modulated by feeding. However, the molecular mechanisms involved are unclear. Here, we show that TJP1 (tight junction protein 1) functions as a mediator of mTOR (mechanistic target of rapamycin) to modulate the hepatic circadian clock. TJP1 interacts with PER1 (period circadian regulator 1) and prevents its nuclear translocation. During feeding, mTOR phosphorylates TJP1 and attenuates its association with PER1, thereby enhancing nuclear shuttling of PER1 to dampen circadian oscillation. Therefore, our results provide a previously uncharacterized mechanistic insight into how feeding modulates the hepatic circadian clock.
Identifiants
pubmed: 32001717
doi: 10.1038/s41467-020-14470-2
pii: 10.1038/s41467-020-14470-2
pmc: PMC6992704
doi:
Substances chimiques
Per1 protein, mouse
0
Period Circadian Proteins
0
RNA, Messenger
0
Tjp1 protein, mouse
0
Zonula Occludens-1 Protein
0
TOR Serine-Threonine Kinases
EC 2.7.11.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
589Références
Bass, J. & Lazar, M. A. Circadian time signatures of fitness and disease. Science 354, 994–999 (2016).
pubmed: 27885004
doi: 10.1126/science.aah4965
pmcid: 27885004
Bass, J. & Takahashi, J. S. Circadian integration of metabolism and energetics. Science 330, 1349–1354 (2010).
pubmed: 21127246
pmcid: 21127246
doi: 10.1126/science.1195027
Takahashi, J. S. Transcriptional architecture of the mammalian circadian clock. Nat. Rev. Genet. 18, 164–179 (2017).
pubmed: 27990019
doi: 10.1038/nrg.2016.150
pmcid: 27990019
Panda, S. Circadian physiology of metabolism. Science 354, 1008–1015 (2016).
pubmed: 27885007
doi: 10.1126/science.aah4967
pmcid: 27885007
Stokkan, K. A., Yamazaki, S., Tei, H., Sakaki, Y. & Menaker, M. Entrainment of the circadian clock in the liver by feeding. Science 291, 490–493 (2001).
pubmed: 11161204
doi: 10.1126/science.291.5503.490
pmcid: 11161204
Atger, F. et al. Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver. Proc. Natl Acad. Sci. USA 112, E6579–E6588 (2015).
pubmed: 26554015
doi: 10.1073/pnas.1515308112
pmcid: 26554015
Damiola, F. et al. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14, 2950–2961 (2000).
pubmed: 11114885
pmcid: 317100
doi: 10.1101/gad.183500
Vollmers, C. et al. Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression. Proc. Natl Acad. Sci. USA 106, 21453–21458 (2009).
pubmed: 19940241
doi: 10.1073/pnas.0909591106
pmcid: 19940241
Kawamoto, T. et al. Effects of fasting and re-feeding on the expression of Dec1, Per1, and other clock-related genes. J. Biochem 140, 401–408 (2006).
pubmed: 16873396
doi: 10.1093/jb/mvj165
Tahara, Y., Otsuka, M., Fuse, Y., Hirao, A. & Shibata, S. Refeeding after fasting elicits insulin-dependent regulation of Per2 and Rev-erbalpha with shifts in the liver clock. J. Biol. Rhythms 26, 230–240 (2011).
pubmed: 21628550
doi: 10.1177/0748730411405958
Oike, H., Nagai, K., Fukushima, T., Ishida, N. & Kobori, M. Feeding cues and injected nutrients induce acute expression of multiple clock genes in the mouse liver. PLoS ONE 6, e23709 (2011).
pubmed: 21901130
pmcid: 3162004
doi: 10.1371/journal.pone.0023709
Dang, F. et al. Insulin post-transcriptionally modulates Bmal1 protein to affect the hepatic circadian clock. Nat. Commun. 7, 12696 (2016).
pubmed: 27576939
pmcid: 5013695
doi: 10.1038/ncomms12696
Eckel-Mahan, K. L. et al. Reprogramming of the circadian clock by nutritional challenge. Cell 155, 1464–1478 (2013).
pubmed: 24360271
pmcid: 4573395
doi: 10.1016/j.cell.2013.11.034
Kohsaka, A. et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 6, 414–421 (2007).
pubmed: 17983587
doi: 10.1016/j.cmet.2007.09.006
Kojima, T. et al. Tight junction proteins and signal transduction pathways in hepatocytes. Histol. Histopathol. 24, 1463–1472 (2009).
pubmed: 19760595
pmcid: 19760595
Musch, A. The unique polarity phenotype of hepatocytes. Exp. Cell Res. 328, 276–283 (2014).
pubmed: 24956563
pmcid: 4254207
doi: 10.1016/j.yexcr.2014.06.006
Dunn, J. C., Tompkins, R. G. & Yarmush, M. L. Long-term in vitro function of adult hepatocytes in a collagen sandwich configuration. Biotechnol. Prog. 7, 237–245 (1991).
pubmed: 1367596
doi: 10.1021/bp00009a007
pmcid: 1367596
Tuschl, G., Hrach, J., Walter, Y., Hewitt, P. G. & Mueller, S. O. Serum-free collagen sandwich cultures of adult rat hepatocytes maintain liver-like properties long term: a valuable model for in vitro toxicity and drug–drug interaction studies. Chem. Biol. Interact. 181, 124–137 (2009).
pubmed: 19482013
doi: 10.1016/j.cbi.2009.05.015
pmcid: 19482013
Srinivasan, B. et al. TEER measurement techniques for in vitro barrier model systems. J. Lab Autom. 20, 107–126 (2015).
pubmed: 25586998
pmcid: 4652793
doi: 10.1177/2211068214561025
Umeda, K. et al. ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 126, 741–754 (2006).
pubmed: 16923393
doi: 10.1016/j.cell.2006.06.043
pmcid: 16923393
Umeda, K. et al. Establishment and characterization of cultured epithelial cells lacking expression of ZO-1. J. Biol. Chem. 279, 44785–44794 (2004).
pubmed: 15292177
doi: 10.1074/jbc.M406563200
pmcid: 15292177
Cao, R., Li, A., Cho, H. Y., Lee, B. & Obrietan, K. Mammalian target of rapamycin signaling modulates photic entrainment of the suprachiasmatic circadian clock. J. Neurosci. 30, 6302–6314 (2010).
pubmed: 20445056
pmcid: 2896874
doi: 10.1523/JNEUROSCI.5482-09.2010
Cao, R. et al. Translational control of entrainment and synchrony of the suprachiasmatic circadian clock by mTOR/4E-BP1 signaling. Neuron 79, 712–724 (2013).
pubmed: 23972597
doi: 10.1016/j.neuron.2013.06.026
pmcid: 23972597
Cornu, M. et al. Hepatic mTORC1 controls locomotor activity, body temperature, and lipid metabolism through FGF21. Proc. Natl Acad. Sci. USA 111, 11592–11599 (2014).
pubmed: 25082895
doi: 10.1073/pnas.1412047111
pmcid: 25082895
Liu, D. et al. mTOR signaling in VIP neurons regulates circadian clock synchrony and olfaction. Proc. Natl Acad. Sci. USA 115, E3296–E3304 (2018).
pubmed: 29555746
doi: 10.1073/pnas.1721578115
Ramanathan, C. et al. mTOR signaling regulates central and peripheral circadian clock function. PLoS Genet. 14, e1007369 (2018).
pubmed: 29750810
pmcid: 5965903
doi: 10.1371/journal.pgen.1007369
Zheng, X. & Sehgal, A. AKT and TOR signaling set the pace of the circadian pacemaker. Curr. Biol. 20, 1203–1208 (2010).
pubmed: 20619819
pmcid: 3165196
doi: 10.1016/j.cub.2010.05.027
Walton, Z. E. et al. Acid suspends the circadian clock in hypoxia through inhibition of mTOR. Cell 174, 72–87 e32 (2018).
pubmed: 29861175
pmcid: 6398937
doi: 10.1016/j.cell.2018.05.009
Hsu, P. P. et al. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 332, 1317–1322 (2011).
pubmed: 21659604
pmcid: 3177140
doi: 10.1126/science.1199498
Saxton, R. A. & Sabatini, D. M. mTOR signaling in growth, metabolism, and disease. Cell 169, 361–371 (2017).
pubmed: 28388417
pmcid: 28388417
doi: 10.1016/j.cell.2017.03.035
Han, J. et al. The CREB coactivator CRTC2 controls hepatic lipid metabolism by regulating SREBP1. Nature 524, 243–246 (2015).
pubmed: 26147081
doi: 10.1038/nature14557
pmcid: 26147081
Sengupta, S., Peterson, T. R., Laplante, M., Oh, S. & Sabatini, D. M. mTORC1 controls fasting-induced ketogenesis and its modulation by ageing. Nature 468, 1100–1104 (2010).
pubmed: 21179166
pmcid: 21179166
doi: 10.1038/nature09584
Samuel, V. T. & Shulman, G. I. Mechanisms for insulin resistance: common threads and missing links. Cell 148, 852–871 (2012).
pubmed: 22385956
pmcid: 3294420
doi: 10.1016/j.cell.2012.02.017
Hatori, M. et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 15, 848–860 (2012).
pubmed: 22608008
pmcid: 3491655
doi: 10.1016/j.cmet.2012.04.019
Zhao, X. et al. Circadian amplitude regulation via FBXW7-targeted REV-ERBalpha degradation. Cell 165, 1644–1657 (2016).
pubmed: 27238018
pmcid: 4912445
doi: 10.1016/j.cell.2016.05.012
He, B. et al. The small molecule nobiletin targets the molecular oscillator to enhance circadian rhythms and protect against metabolic syndrome. Cell Metab. 23, 610–621 (2016).
pubmed: 27076076
pmcid: 4832569
doi: 10.1016/j.cmet.2016.03.007
Chaix, A., Zarrinpar, A., Miu, P. & Panda, S. Time-restricted feeding is a preventative and therapeutic intervention against diverse nutritional challenges. Cell Metab. 20, 991–1005 (2014).
pubmed: 25470547
pmcid: 4255155
doi: 10.1016/j.cmet.2014.11.001
Odenwald, M. A. et al. ZO-1 interactions with F-actin and occludin direct epithelial polarization and single lumen specification in 3D culture. J. Cell Sci. 130, 243–259 (2017).
pubmed: 27802160
pmcid: 5394778
doi: 10.1242/jcs.188185
Spadaro, D. et al. Tension-dependent stretching activates ZO-1 to control the junctional localization of its interactors. Curr. Biol. 27, 3783–3795 e3788 (2017).
pubmed: 29199076
doi: 10.1016/j.cub.2017.11.014
Efeyan, A., Comb, W. C. & Sabatini, D. M. Nutrient-sensing mechanisms and pathways. Nature 517, 302–310 (2015).
pubmed: 25592535
pmcid: 4313349
doi: 10.1038/nature14190
Settembre, C., Fraldi, A., Medina, D. L. & Ballabio, A. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14, 283–296 (2013).
pubmed: 23609508
pmcid: 4387238
doi: 10.1038/nrm3565
Xu, H. & Ren, D. Lysosomal physiology. Annu. Rev. Physiol. 77, 57–80 (2015).
pubmed: 25668017
pmcid: 4524569
doi: 10.1146/annurev-physiol-021014-071649
Zhang, S., An, Q., Wang, T., Gao, S. & Zhou, G. Autophagy- and MMP-2/9-mediated reduction and redistribution of ZO-1 contribute to hyperglycemia-increased blood–brain barrier permeability during early reperfusion in stroke. Neuroscience 377, 126–137 (2018).
pubmed: 29524637
doi: 10.1016/j.neuroscience.2018.02.035
pmcid: 29524637
Toledo, M. et al. Autophagy regulates the liver clock and glucose metabolism by degrading CRY1. Cell Metab. 28, 268–281.e4 (2018).
pubmed: 29937374
pmcid: 6082686
doi: 10.1016/j.cmet.2018.05.023
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
Takano, A. et al. Cloning and characterization of rat casein kinase 1epsilon. FEBS Lett. 477, 106–112 (2000).
pubmed: 10899319
doi: 10.1016/S0014-5793(00)01755-5
Vielhaber, E., Eide, E., Rivers, A., Gao, Z. H. & Virshup, D. M. Nuclear entry of the circadian regulator mPER1 is controlled by mammalian casein kinase I epsilon. Mol. Cell Biol. 20, 4888–4899 (2000).
pubmed: 10848614
pmcid: 85940
doi: 10.1128/MCB.20.13.4888-4899.2000
Eide, E. J., Vielhaber, E. L., Hinz, W. A. & Virshup, D. M. The circadian regulatory proteins BMAL1 and cryptochromes are substrates of casein kinase Iepsilon. J. Biol. Chem. 277, 17248–17254 (2002).
pubmed: 11875063
pmcid: 1513548
doi: 10.1074/jbc.M111466200
Zhang, Y., Xu, L., Liu, X. & Wang, Y. Evaluation of insulin sensitivity by hyperinsulinemic-euglycemic clamps using stable isotope-labeled glucose. Cell Discov. 4, 17 (2018).
pubmed: 29675266
pmcid: 5902507
doi: 10.1038/s41421-018-0016-3
Li, E. et al. OLFR734 mediates glucose metabolism as a receptor of asprosin. Cell Metab. 30, 319–328 e318 (2019).
pubmed: 31230984
doi: 10.1016/j.cmet.2019.05.022
Wang, Y. et al. Tyrosine phosphorylated Par3 regulates epithelial tight junction assembly promoted by EGFR signaling. EMBO J. 25, 5058–5070 (2006).
pubmed: 17053785
pmcid: 1630420
doi: 10.1038/sj.emboj.7601384
Chen, L. et al. Fasting-induced hormonal regulation of lysosomal function. Cell Res. 27, 748–763 (2017).
pubmed: 28374748
pmcid: 5518872
doi: 10.1038/cr.2017.45
Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450 (2019).
pubmed: 30395289
doi: 10.1093/nar/gky1106
pmcid: 30395289