Reciprocal control of the circadian clock and cellular redox state - A critical appraisal

Molecules and Cells

Volumn 39, Issue 1, 2016, Pages 6-19

  Putker, Marrit ^a   O’Neill, John Stuart ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Biological clock; Circadian timekeeping; Cysteine oxidation; Redox signaling

Indexed keywords

CYSTEINE; REACTIVE OXYGEN METABOLITE;

CIRCADIAN RHYTHM; DECOMPOSITION; EUKARYOTE; FEEDBACK SYSTEM; GENE EXPRESSION; HOMEOSTASIS; HUMAN; OXIDATION REDUCTION STATE; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; GENE EXPRESSION REGULATION; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CYSTEINE; GENE EXPRESSION REGULATION; HUMANS; OXIDATION-REDUCTION;

EID: 84975266395     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2016.2323     Document Type: Review

References (158)

1. Abate, C., Patel, L., Rauscher, F.J., and Curran, T. (1990). Redox regulation of fos and jun DNA-binding activity in vitro. Science 249, 1157-1161.
2. Anea, C.B., Zhang, M., Chen, F., Ali, M.I., Hart, C.M.M., Stepp, D.W., Kovalenkov, Y.O., Merloiu, A.-M., Pati, P., Fulton, D., et al. (2013). Circadian clock control of Nox4 and reactive oxygen species in the vasculature. PLoS One 8, e78626.
3. Aon, M. a., Cortassa, S., Marbán, E., and O’Rourke, B. (2003). Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 278, 44735-44744.
4. Asher, G., and Schibler, U. (2011). Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab. 13, 125-137.
5. Asher, G., Gatfield, D., Stratmann, M., Reinke, H., Dibner, C., Kreppel, F., Mostoslavsky, R., Alt, F.W., and Schibler, U. (2008). SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134, 317-328.
6. Atger, F., Gobet, C., Marquis, J., Martin, E., Wang, J., Weger, B., Lefebvre, G., Descombes, P., Naef, F., and Gachon, F. (2015). Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver. Proc. Natl. Acad. Sci. USA 112, E6579-E6588.
7. Bass, J. (2012). Circadian topology of metabolism. Nature 491, 348-356.
8. Bass, J., and Takahashi, J.S. (2010). Circadian integration of metabolism and energetics. Science 330, 1349-1354.
9. Bieler, J., Cannavo, R., Gustafson, K., Gobet, C., Gatfield, D., and Naef, F. (2014). Robust synchronization of coupled circadian and cell cycle oscillators in single mammalian cells. Mol. Syst. Biol. 10, 739.
10. Bindoli, A., and Rigobello, M.P. (2012). Principles in redox signaling: from chemistry to functional significance. Antioxid. Redox Signal. 18, 1-97.
11. Brody, S., and Harris, S. (1973). Circadian rhythms in neurospora: spatial differences in pyridine nucleotide levels. Science 180, 498-500.
12. Brunet, A., Sweeney, L.B., Sturgill, J.F., Chua, K.F., Greer, P.L., Lin, Y., Tran, H., Ross, S.E., Mostoslavsky, R., Cohen, H.Y., et al. (2004). Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 2011-2015.
13. Bulleid, N.J., and Ellgaard, L. (2011). Multiple ways to make disulfides. Trends Biochem. Sci. 36, 485-492.
14. Bunger, M.K., Wilsbacher, L.D., Moran, S.M., Clendenin, C., Radcliffe, L. a., Hogenesch, J.B., Simon, M.C., Takahashi, J.S., and Bradfield, C. a. (2000). Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103, 1009-1017.
15. Burgoyne, J.R., Madhani, M., Cuello, F., Charles, R.L., Brennan, J.P., Schröder, E., Browning, D.D., and Eaton, P. (2007). Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science 317, 1393-1397.
16. Burgoyne, J.R., Rudyk, O., Cho, H., Prysyazhna, O., Hathaway, N., Weeks, A., Evans, R., Ng, T., Schröder, K., Brandes, R.P., et al. (2015). Deficient angiogenesis in redox-dead Cys17Ser PKARIαknock-in mice. Nat. Commun. 6, 7920.
17. Cardone, L., Hirayama, J., Giordano, F., Tamaru, T., Palvimo, J., and Sassone-Corsi, P. (2005). Circadian clock control by SUMOylation of BMAL1. Science 309, 1390-1394.
18. Causton, H.C., Feeney, K.A., Ziegler, C.A., and O’Neill, J.S. (2015). Metabolic cycles in yeast share features conserved among circadian rhythms. Curr. Biol. 25, 1056-1062.
19. Chang, T.-S., Jeong, W., Woo, H.A., Lee, S.M., Park, S., and Rhee, S.G. (2004). Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J. Biol. Chem. 279, 50994-51001.
20. Chaudhury, D., Wang, L.M., and Colwell, C.S. (2005). Circadian regulation of hippocampal long-term potentiation. J. Biol. Rhythms 20, 225-236.
21. Chen, R., Schirmer, A., Lee, Y., Lee, H., Kumar, V., Yoo, S.-H., Takahashi, J.S., and Lee, C. (2009). Rhythmic PER abundance defines a critical nodal point for negative feedback within the circadian clock mechanism. Mol. Cell 36, 417-430.
22. Cho, C.S., Yoon, H.J., Kim, J.Y., Woo, H.A., and Rhee, S.G. (2014). Circadian rhythm of hyperoxidized peroxiredoxin II is determined by hemoglobin autoxidation and the 20S proteasome in red blood cells. Proc. Natl. Acad. Sci. USA 111, 12043-12048.
23. Cotto-Rios, X.M., Békés, M., Chapman, J., Ueberheide, B., and Huang, T.T. (2012). Deubiquitinases as a signaling target of oxidative stress. Cell Rep. 2, 1-10.
24. Cremers, C.M., and Jakob, U. (2013). Oxidant sensing by reversible disulfide bond formation. J. Biol. Chem. 288, 26489-26496.
25. Czech, M.P., Lawrence, J.C., and Lynn, W.S. (1974). Evidence for the involvement of sulfhydryl oxidation in the regulation of fat cell hexose transport by insulin. Proc. Natl. Acad. Sci. USA 71, 4173-4177.
26. Dansen, T.B., Smits, L.M.M., van Triest, M.H., de Keizer, P.L.J., van Leenen, D., Koerkamp, M.G., Szypowska, A., Meppelink, A., Brenkman, A.B., Yodoi, J., et al. (2009). Redox-sensitive cysteines bridge p300/CBP-mediated acetylation and FoxO4 activity. Nat. Chem. Biol. 5, 664-672.
27. DeBruyne, J.P., Noton, E., Lambert, C.M., Maywood, E.S., Weaver, D.R., and Reppert, S.M. (2006). A clock shock: mouse CLOCK is not required for circadian oscillator function. Neuron 50, 465-477.
28. 2 receptor and redoxtransducer in gene activation. Cell 111, 471-481.
29. Dickinson, B.C. (2015). Plugging the leak Synergistic MRSA combinations. Nat. Publ. Gr. 11, 831-832.
30. Dunlap, J.C. (1999). Molecular bases for circadian clocks. Cell 96, 271-290.
31. Edgar, R.S., Green, E.W., Zhao, Y., van Ooijen, G., Olmedo, M., Qin, X., Xu, Y., Pan, M., Valekunja, U.K., Feeney, K.A., et al. (2012). Peroxiredoxins are conserved markers of circadian rhythms. Nature 485, 459-464.
32. Eide, E.J., Woolf, M.F., Kang, H., Woolf, P., Hurst, W., Camacho, F., Vielhaber, E.L., Giovanni, A., and Virshup, D.M. (2005). Control of mammalian circadian rhythm by CKIepsilon-regulated proteasome-mediated PER2 degradation. Mol. Cell. Biol. 25, 2795-2807.
33. Ezeriņa, D., Morgan, B., and Dick, T.P. (2014). Imaging dynamic redox processes with genetically encoded probes. J. Mol. Cell. Cardiol. 73, 43-49.
34. Fan, Y., Hida, A., Anderson, D. a., Izumo, M., and Johnson, C.H. (2007). Cycling of CRYPTOCHROME proteins is not necessary for circadian-clock function in mammalian fibroblasts. Curr. Biol. 17, 1091-1100.
35. Feillet, C., Krusche, P., Tamanini, F., Janssens, R.C., Downey, M.J., Martin, P., Teboul, M., Saito, S., Levi, F. a., Bretschneider, T., et al. (2014). Phase locking and multiple oscillating attractors for the coupled mammalian clock and cell cycle. Proc. Natl. Acad. Sci. USA 111, 9828-9833.
36. Fogg, P.C.M., O’Neill, J.S., Dobrzycki, T., Calvert, S., Lord, E.C., McIntosh, R.L.L., Elliott, C.J.H., Sweeney, S.T., Hastings, M.H., and Chawla, S. (2014). Class IIa histone deacetylases are conserved regulators of circadian function. J. Biol. Chem. 289, 34341-34348.
37. 2 scavenging and signaling. Antioxid. Redox Signal. 10, 1565-1576.
38. Fujimoto, Y., Yagita, K., and Okamura, H. (2006). Does mPER2 protein oscillate without its coding mRNA cycling?: posttranscriptional regulation by cell clock. Genes Cells 11, 525-530.
39. Gibbs, J., Ince, L., Matthews, L., Mei, J., Bell, T., Yang, N., Saer, B., Begley, N., Poolman, T., Pariollaud, M., et al. (2014). An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nat. Med. 20, 919-926.
40. Godinho, S.I.H., Maywood, E.S., Shaw, L., Tucci, V., Barnard, A.R., Busino, L., Pagano, M., Kendall, R., Quwailid, M.M., Romero, M.R., et al. (2007). The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period. Science 316, 897-900.
41. Goldman, R., Stoyanovsky, D. a, Day, B.W., and Kagan, V.E. (1995). Reduction of phenoxyl radicals by thioredoxin results in selective oxidation of its SH-groups to disulfides. An antioxidant function of thioredoxin. Biochemistry 34, 4765-4772.
42. Gorrini, C., Harris, I.S., and Mak, T.W. (2013). Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discov. 12, 931-947.
43. Grek, C.L., Zhang, J., Manevich, Y., Townsend, D.M., and Tew, K.D. (2013). Causes and consequences of cysteine Sglutathionylation. J. Biol. Chem. 288, 26497-26504.
44. Gyöngyösi, N., Nagy, D., Makara, K., Ella, K., and Káldi, K. (2013). Reactive oxygen species can modulate circadian phase and period in Neurospora crassa. Free Radic. Biol. Med. 58, 134-143.
45. Hanschmann, E.-M., Godoy, J.R., Berndt, C., Hudemann, C., and Lillig, C.H. (2013). Thioredoxins, glutaredoxins, and peroxiredoxins--molecular mechanisms and health significance: from cofactors to antioxidants to redox signaling. Antioxid. Redox Signal. 19, 1539-1605.
46. Hardin, P.E., Hall, J.C., and Rosbash, M. (1990). Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343, 536-540.
47. Hastings, M.H., Maywood, E.S., and O’Neill, J.S. (2008). Cellular circadian pacemaking and the role of cytosolic rhythms. Curr. Biol. 18, R805-R815.
48. Hayes, J.D., and Dinkova-Kostova, A.T. (2014). The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem. Sci. 39, 199-218.
49. Homma, T., Okano, S., Lee, J., Ito, J., Otsuki, N., Kurahashi, T., Kang, E.S., Nakajima, O., and Fujii, J. (2015). SOD1 deficiency induces the systemic hyperoxidation of peroxiredoxin in the mouse. Biochem. Biophys. Res. Commun. 463, 1040-1046.
50. Horst, G.T.J. Van Der, and Muijtjens, M. (1999). Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. 3495, 627-630.
51. Van der Horst, A., Tertoolen, L.G.J., de Vries-Smits, L.M.M., Frye, R. a, Medema, R.H., and Burgering, B.M.T. (2004). FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J. Biol. Chem. 279, 28873-28879.
52. Hoyle, N.P., and O’Neill, J.S. (2014). Oxidation-reduction cycles of peroxiredoxin proteins and nontranscriptional aspects of timekeeping. Biochemistry 54, 184-193.
53. Jacobi, D., Liu, S., Burkewitz, K., Kory, N., Knudsen, N.H., Alexander, R.K., Unluturk, U., Li, X., Kong, X., Hyde, A.L., et al. (2015). Hepatic Bmal1 regulates rhythmic mitochondrial dynamics and promotes metabolic fitness. Cell Metab. 22, 709-720.
54. Jang, C., Lahens, N.F., Hogenesch, J.B., and Sehgal, A. (2015). Ribosome profiling reveals an important role for translational control in circadian gene expression. Genome Res. 25, 1836-1847.
55. Jarvis, R.M., Hughes, S.M., and Ledgerwood, E.C. (2012). Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic. Biol. Med. 53, 1522-1530.
56. Kaasik, K., Kivimäe, S., Allen, J.J.J., Chalkley, R.J.J., Huang, Y., Baer, K., Kissel, H., Burlingame, A.L.L., Shokat, K.M.M., Ptáček, L.J.J., et al. (2013). Glucose sensor O-GlcNAcylation coordinates with phosphorylation to regulate circadian clock. Cell Metab. 17, 291-302.
57. De Keizer, P.L.J., Burgering, B.M.T., and Dansen, T.B. (2011). Forkhead box o as a sensor, mediator, and regulator of redox signaling. Antioxid. Redox Signal. 14, 1093-1106.
58. 2-Dependent, Reversible Inactivation of Peroxiredoxin III in Mitochondria. Mol. Cell 46, 584-594.
59. Kil, I.S., Ryu, K.W., Lee, S.K., Kim, J.Y., Chu, S.Y., Kim, J.H., Park, S., and Rhee, S.G. (2015). Circadian Oscillation of Sulfiredoxin in the Mitochondria. Mol. Cell 59, 651-663.
60. Ko, C.H., Yamada, Y.R., Welsh, D.K., Buhr, E.D., Liu, A.C., Zhang, E.E., Ralph, M.R., Kay, S. a, Forger, D.B., and Takahashi, J.S. (2010). Emergence of noise-induced oscillations in the central circadian pacemaker. PLoS Biol. 8, e1000513.
61. Kondratov, R. V., Kondratova, A. a., Gorbacheva, V.Y., Vykhovanets, O. V., and Antoch, M.P. (2006). Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 20, 1868-1873.
62. Kondratov, R. V., Vykhovanets, O., Kondratova, A. a., and Antoch, M.P. (2009). Antioxidant N-acetyl-L-cysteine ameliorates symptoms of premature aging associated with the deficiency of the circadian protein BMAL1. Aging 1, 979-987.
63. Kruiswijk, F., Labuschagne, C.F., and Vousden, K.H. (2015). p53 in survival, death and metabolic health: a lifeguard with a licence to kill. Nat. Rev. Mol. Cell Biol. 16, 393-405.
64. Kulathu, Y., Garcia, F.J., Mevissen, T.E.T., Busch, M., Arnaudo, N., Carroll, K.S., Barford, D., and Komander, D. (2013). Regulation of A20 and other OTU deubiquitinases by reversible oxidation. Nat. Commun. 4, 1569.
65. Lamia, K. a, Sachdeva, U.M., DiTacchio, L., Williams, E.C., Alvarez, J.G., Egan, D.F., Vasquez, D.S., Juguilon, H., Panda, S., Shaw, R.J., et al. (2009). AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326, 437-440.
66. Langner, R., and Rensing, L. (1972). Circadian rhythm of oxygen consumption in rat liver suspension culture: changes of pattern. Z. Naturforsch. B. 27, 1117-1118.
67. Lee, S.-R., Kwon, K.S., Kim, S.R., and Rhee, S.G. (1998). Reversible Inactivation of Protein-tyrosine Phosphatase 1B in A431 Cells Stimulated with Epidermal Growth Factor. J. Biol. Chem. 273, 15366-15372.
68. Lee, C., Etchegaray, J.P., Cagampang, F.R., Loudon, a.S., and Reppert, S.M. (2001). Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107, 855-867.
69. Lee, J., Moulik, M., Fang, Z., Saha, P., Zou, F., Xu, Y., Nelson, D.L., Ma, K., Moore, D.D., and Yechoor, V.K. (2013a). Bmal1 and ß-cell clock are required for adaptation to circadian disruption, and their loss of function leads to oxidative stress-induced ß-cell failure in mice. Mol. Cell. Biol. 33, 2327-2338.
70. Lee, J.-G., Baek, K., Soetandyo, N., and Ye, Y. (2013b). Reversible inactivation of deubiquitinases by reactive oxygen species in vitro and in cells. Nat. Commun. 4, 1568.
71. Leise, T.L., Wang, C.W., Gitis, P.J., and Welsh, D.K. (2012). Persistent cell-autonomous circadian oscillations in fibroblasts revealed by six-week single-cell imaging of PER2::LUC bioluminescence. PLoS One 7, e33334.
72. Lipton, J.O., Yuan, E.D., Boyle, L.M., Ebrahimi-Fakhari, D., Kwiatkowski, E., Nathan, A., Güttler, T., Davis, F., Asara, J.M., and Sahin, M. (2015). The circadian protein BMAL1 regulates translation in response to S6K1-mediated phosphorylation. Cell 161, 1138-1151.
73. Lowrey, P.L., Shimomura, K., Antoch, M.P., Yamazaki, S., Zemenides, P.D., Ralph, M.R., Menaker, M., and Takahashi, J.S. (2000). Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 288, 483-492.
74. Maier, B., Wendt, S., Vanselow, J.T., Wallach, T., Reischl, S., Oehmke, S., Schlosser, A., and Kramer, A. (2009). A large-scale functional RNAi screen reveals a role for CK2 in the mammalian circadian clock. Genes Dev. 23, 708-718.
75. Maiorino, M., Roveri, A., Benazzi, L., Bosello, V., Mauri, P., Toppo, S., Tosatto, S.C.E., and Ursini, F. (2005). Functional interaction of phospholipid hydroperoxide glutathione peroxidase with sperm mitochondrion-associated cysteine-rich protein discloses the adjacent cysteine motif as a new substrate of the selenoperoxidase. J. Biol. Chem. 280, 38395-38402.
76. Masri, S., Rigor, P., Cervantes, M., Ceglia, N., Sebastian, C., Xiao, C., Roqueta-Rivera, M., Deng, C., Osborne, T.F., Mostoslavsky, R., et al. (2014). Partitioning circadian transcription by SIRT6 leads to segregated control of cellular metabolism. Cell 158, 659-672.
77. Matsuo, T., Yamaguchi, S., Mitsui, S., Emi, A., Shimoda, F., and Okamura, H. (2003). Control mechanism of the circadian clock for timing of cell division in vivo. Science 302, 255-259.
78. Mauvoisin, D., Wang, J., Jouffe, C., Martin, E., Atger, F., Waridel, P., Quadroni, M., Gachon, F., and Naef, F. (2014). Circadian clockdependent and-independent rhythmic proteomes implement distinct diurnal functions in mouse liver. Proc. Natl. Acad. Sci. USA 111, 167-172.
79. Maywood, E.S., Chesham, J.E., Brien, J.A.O., and Hastings, M.H. (2011). A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits. Proc. Natl. Acad. Sci. USA 108, 14306-14311.
80. McCord, J.M., and Fridovich, I. (1969). Superoxide dismutase: and enzymatic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244, 6049-6055.
81. Meng, Q.-J., Logunova, L., Maywood, E.S., Gallego, M., Lebiecki, J., Brown, T.M., Sládek, M., Semikhodskii, A.S., Glossop, N.R.J., Piggins, H.D., et al. (2008). Setting clock speed in mammals: the CK1 epsilon tau mutation in mice accelerates circadian pacemakers by selectively destabilizing PERIOD proteins. Neuron 58, 78-88.
82. Mitsuishi, Y., Taguchi, K., Kawatani, Y., Shibata, T., Nukiwa, T., Aburatani, H., Yamamoto, M., and Motohashi, H. (2012). Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 22, 66-79.
83. Mohawk, J. a., Green, C.B., and Takahashi, J.S. (2012). Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35, 445-462.
84. Monteiro, H.P., and Stern, A. (1996). Redox modulation of tyrosine phosphorylation-dependent signal transduction pathways. Free Radic. Biol. Med. 21, 323-333.
85. Musiek, E.S. (2015). Circadian clock disruption in neurodegenerative diseases: cause and effect? Front. Pharmacol. 6, 29.
86. Musiek, E.S., Lim, M.M., Yang, G., Bauer, A.Q., Qi, L., Lee, Y., Roh, J.H., Ortiz-gonzalez, X., Dearborn, J.T., Culver, J.P., et al. (2013). Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration. J. Clin. Invest. 123, 5389-5400.
87. Nadeau, P.J., Charette, S.J., Toledano, M.B., and Landry, J. (2007). Disulfide Bond-mediated multimerization of Ask1 and its reduction by thioredoxin-1 regulate H(2)O(2)-induced c-Jun NH(2)-terminal kinase activation and apoptosis. Mol. Biol. Cell 18, 3903-3913.
88. Nagy, P., Karton, A., Betz, A., Peskin, A.V, Pace, P., O’Reilly, R.J., Hampton, M.B., Radom, L., and Winterbourn, C.C. (2011). Model for the exceptional reactivity of peroxiredoxins 2 and 3 with hydrogen peroxide: a kinetic and computational study. J. Biol. Chem. 286, 18048-18055.
89. + salvage pathway by CLOCK-SIRT1. Science 324, 654-657.
90. Nakajima, M., Imai, K., Ito, H., Nishiwaki, T., Murayama, Y., Iwasaki, H., Oyama, T., and Kondo, T. (2005). Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308, 414-415.
91. Nangle, S.N., Rosensweig, C., Koike, N., Tei, H., Takahashi, J.S., Green, C.B., and Zheng, N. (2014). Molecular assembly of the period-cryptochrome circadian transcriptional repressor complex. Elife 15, e30674.
92. O’Neill, J.S., and Reddy, A.B. (2011). Circadian clocks in human red blood cells. Nature 469, 498-503.
93. 2+ signalling in mammalian circadian timekeeping. Biochem. Soc. Trans. 40, 44-50.
94. O’Neill, J.S., Maywood, E.S., Chesham, J.E., Takahashi, J.S., and Hastings, M.H. (2008). cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320, 949-953.
95. O’Neill, J.S., Ooijen, G. Van, Dixon, L.E., Troein, C., Corellou, F., Bouget, F.-Y., Reddy, A.B., Millar, A.J., and van Ooijen, G. (2011). Circadian rhythms persist without transcription in a eukaryote. Nature 469, 554-558.
96. O’Neill, J.S., Maywood, E.S., and Hastings, M.H. (2013). Cellular mechanisms of circadian pacemaking: beyond transcriptional loops. Handb. Exp. Pharmacol. 2013, 67-103.
97. Okano, S., Akashi, M., Hayasaka, K., and Nakajima, O. (2009). Unusual circadian locomotor activity and pathophysiology in mutant CRY1 transgenic mice. Neurosci. Lett. 451, 246-251.
98. Ono, D., Honma, S., and Honma, K. (2013). Cryptochromes are critical for the development of coherent circadian rhythms in the mouse suprachiasmatic nucleus. Nat. Commun. 4, 1666.
99. Papp, S.J., Huber, A.-L., Jordan, S.D., Kriebs, A., Nguyen, M., Moresco, J.J., Yates, J.R., and Lamia, K.A. (2015). DNA damage shifts circadian clock time via Hausp-dependent Cry1 stabilization. Elife 4, doi: 10.7554/eLife.04883.
100. Paulose, J.K., Rucker, E.B., and Cassone, V.M. (2012). Toward the beginning of time: circadian rhythms in metabolism precede rhythms in clock gene expression in mouse embryonic stem cells. PLoS One 7, e49555.
101. 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. (2013). Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 342, 1243417.
102. Pekovic-Vaughan, V., Gibbs, J., Yoshitane, H., Yang, N., Pathiranage, D., Guo, B., Sagami, A., Taguchi, K., Bechtold, D., Loudon, A., et al. (2014). The circadian clock regulates rhythmic activation of the NRF2/glutathione-mediated antioxidant defense pathway to modulate pulmonary fibrosis. Genes Dev. 28, 548-560.
103. Peralta, D., Bronowska, A.K., Morgan, B., Dóka, É., Van Laer, K., Nagy, P., Gräter, F., and Dick, T.P. (2015). A proton relay enhances H2O2 sensitivity of GAPDH to facilitate metabolic adaptation. Nat. Chem. Biol. 11, 156-163.
104. Peskin, A.V., Low, F.M., Paton, L.N., Maghzal, G.J., Hampton, M.B., and Winterbourn, C.C. (2007). The high reactivity of peroxiredoxin 2 with H(2)O(2) is not reflected in its reaction with other oxidants and thiol reagents. J. Biol. Chem. 282, 11885-11892.
105. Pittendrigh, C.S. (1960). Circadian rhythms and the circadian organization of living systems. Cold Spring Harb. Symp. Quant. Biol. 25, 159-184.
106. Pizarro, A., Hayer, K., Lahens, N.F., and Hogenesch, J.B. (2013). CircaDB: A database of mammalian circadian gene expression profiles. Nucleic Acids Res. 41, D1009-D1013.
107. Prysyazhna, O., Rudyk, O., and Eaton, P. (2012). Single atom substitution in mouse protein kinase G eliminates oxidant sensing to cause hypertension. Nat. Med. 18, 286-290.
108. Putker, M., Madl, T., Vos, H.R.R., de Ruiter, H., Visscher, M., van den Berg, M.C.W., Kaplan, M., Korswagen, H.C.C., Boelens, R., Vermeulen, M., et al. (2013). Redox-dependent control of FOXO/DAF-16 by transportin-1. Mol. Cell 49, 730-742.
109. Putker, M., Vos, H.R., and Dansen, T.B. (2014a). Intermolecular disulfide-dependent redox signalling. Biochem. Soc. Trans. 42, 971-978.
110. Putker, M., Vos, H., van Dorenmalen, K., de Ruiter, H., Duran, A.G., Snel, B., Burgering, B.M., Vermeulen, M., and Dansen, T.B. (2014b). Evolutionary acquisition of cysteines determines FOXO paralog-specific redox signaling. Antioxid. Redox Signal. 22, 15-28.
111. Radha, B.E., Hill, T.D., Rao, G.H.R., and White, J.G. (1985). GSH levels in human platelets display a circadian rythm in vitro. Trombos. Res. 40, 823-831.
112. Raghuram, S., Stayrook, K.R., Huang, P., Rogers, P.M., Nosie, A.K., McClure, D.B., Burris, L.L., Khorasanizadeh, S., Burris, T.P., and Rastinejad, F. (2007). Identification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbeta. Nat. Struct. Mol. Biol. 14, 1207-1213.
113. Rainwater, R., Parks, D., Anderson, M.E., Tegtmeyer, P., and Mann, K. (1995). Role of cysteine residues in regulation of p53 function. Mol. Cell. Biol. 15, 3892-3903.
114. + biosynthesis. Science 324, 651-654.
115. Rehder, D.S., and Borges, C.R. (2010). Cysteine sulfenic acid as an intermediate in disulfide bond formation and nonenzymatic protein folding. Biochemistry 49, 7748-7755.
116. Reischl, S., Vanselow, K., Westermark, P.O., Thierfelder, N., Maier, B., Herzel, H., and Kramer, A. (2007). Beta-TrCP1-mediated degradation of PERIOD2 is essential for circadian dynamics. J. Biol. Rhythms 22, 375-386.
117. Reppert, S.M., and Weaver, D.R. (2002). Coordination of circadian timing in mammals. Nature 418, 935-941.
118. Ripperger, J.A., and Schibler, U. (2006). Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat. Genet. 38, 369-374.
119. Robles, M.S., Cox, J., and Mann, M. (2014). In-vivo quantitative proteomics reveals a key contribution of post-transcriptional mechanisms to the circadian regulation of liver metabolism. PLoS Genet. 10, e1004047.
120. Roenneberg, T., and Merrow, M. (2002). Life before the clock: modeling circadian evolution. J. Biol. Rhythms 17, 495-505.
121. Rosbash, M. (2009). The implications of multiple circadian clock origins. PLoS Biol. 7, 0421-0425.
122. Rutter, J., Reick, M., Wu, L.C., and McKnight, S.L. (2001). Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293, 510-514.
123. + oscillation. Aging 3, 794-802.
124. Saini, C., Liani, A., Curie, T., Gos, P., Kreppel, F., Emmenegger, Y., Bonacina, L., Wolf, J.-P., Franken, P., and Schibler, U. (2013). Real-time recording of circadian liver gene expression in freely moving mice reveals the phase-setting behavior of hepatocyte clocks. Genes Dev. 27, 1526-1536.
125. Saini, C., Brown, S.A., and Dibner, C. (2015). Human peripheral clocks: applications for studying circadian phenotypes in physiology and pathophysiology. Front. Neurol. 6, 95.
126. Sato, T.K., Yamada, R.G., Ukai, H., Baggs, J.E., Miraglia, L.J., Kobayashi, T.J., Welsh, D.K., Kay, S.A, Ueda, H.R., and Hogenesch, J.B. (2006). Feedback repression is required for mammalian circadian clock function. Nat. Genet. 38, 312-319.
127. Schieber, M., and Chandel, N.S. (2014). ROS function in redox signaling and oxidative stress. Curr. Biol. 24, R453-R462.
128. Schmalen, I., Reischl, S., Wallach, T., Klemz, R., Grudziecki, A., Prabu, J.R., Benda, C., Kramer, A., and Wolf, E. (2014). Interaction of circadian clock proteins CRY1 and PER2 is modulated by zinc binding and disulfide bond formation. Cell 157, 1203-1215.
129. Shao, D., Oka, S., Liu, T., Zhai, P., Ago, T., Sciarretta, S., Li, H., and Sadoshima, J. (2014). A redox-dependent mechanism for regulation of AMPK activation by thioredoxin1 during energy starvation. Cell Metab. 19, 232-245.
130. 2 signaling. Nat. Chem. Biol. 11, 64-70.
131. Storz, G., Tartaglia, L. a, and Ames, B.N. (1990). Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248, 189-194.
132. Stringari, C., Wang, H., Geyfman, M., Crosignani, V., Kumar, V., Takahashi, J.S., Andersen, B., and Gratton, E. (2014). In vivo single-cell detection of metabolic oscillations in stem cells. Cell Rep. 10, 1-7.
133. Sundaresan, M., Yu, Z.X., Ferrans, V.J., Irani, K., and Finkel, T. (1995). Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270, 296-299.
134. Sweeney, B., and Haxo, F. (1961). Persistence of a photosynthetic rhythm in enucleated acetabularia. Science 134, 1361-1363.
135. Tamaru, T., Hattori, M., Ninomiya, Y., Kawamura, G., Varès, G., Honda, K., Mishra, D.P., Wang, B., Benjamin, I., Sassone-Corsi, P., et al. (2013). ROS stress resets circadian clocks to coordinate pro-survival signals. PLoS One 8, e82006.
136. Tomita, J., Nakajima, M., Kondo, T., and Iwasaki, H. (2005). No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307, 251-254.
137. Ueda, H.R. (2007). Systems biology of mammalian circadian clocks. Cold Spring Harb. Symp. Quant. Biol. 72, 365-380.
138. Vassilopoulos, A., Fritz, K.S., Petersen, D.R., and Gius, D. (2011). The human sirtuin family: evolutionary divergences and functions. Hum. Genomics 5, 485-496.
139. Vaziri, H., Dessain, S.K., Ng Eaton, E., Imai, S.I., Frye, R. a, Pandita, T.K., Guarente, L., and Weinberg, R.A. (2001). hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107, 149-159.
140. Wang, T.A., and Gillette, M.U. (2012). Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons. Science 337, 839-842.
141. Webster, K.A., Prentice, H., and Bishopric, N.H. (2001). Oxidation of zinc finger transcription factors: physiological consequences. Antioxid. Redox Signal. 3, 535-548.
142. Welsh, D.K., Yoo, S.-H., Liu, A.C., Takahashi, J.S., and Kay, S.A. (2004). Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr. Biol. 14, 2289-2295.
143. Welsh, D.K., Takahashi, J.S., and Kay, S.A. (2010). Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 72, 551-577.
144. Winterbourn, C.C., and Metodiewa, D. (1999). Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic. Biol. Med. 27, 322-328.
145. Winterbourn, C.C., and Hampton, M.B. (2008). Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45, 549-561.
146. Woo, H.A., Chae, H.Z., Hwang, S.C., Yang, K.-S., Kang, S.W., Kim, K., and Rhee, S.G. (2003). Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300, 653-656.
147. Woo, H.A., Yim, S.H., Shin, D.H., Kang, D., Yu, D.-Y., and Rhee, S.G. (2010). Inactivation of peroxiredoxin I by phosphorylation allows localized H(2)O(2) accumulation for cell signaling. Cell 140, 517-528.
148. Wood, Z.A, Poole, L.B., and Karplus, P.A. (2003). Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300, 650-653.
149. Wu, X., Bishopric, N.H., Discher, D.J., Murphy, B.J., Webster, K.A., Wu, X., Bishopric, N.H., Discher, D.J., Murphy, B.J., and Webster, K.A. (1996). Physical and functional sensitivity of zinc finger transcription factors to redox change. Mol. Cell. Biol. 16, 1035-1046.
150. Xu, Y.-Q., Zhang, D., Jin, T., Cai, D.-J., Wu, Q., Lu, Y., Liu, J., and Klaassen, C.D. (2012). Diurnal variation of hepatic antioxidant gene expression in mice. PLoS One 7, e44237.
151. Yang, G., Wright, C.J., Hinson, M.D., Fernando, A.P., Sengupta, S., Biswas, C., La, P., and Dennery, P.A. (2014). Oxidative stress and inflammation modulate Rev-erbαsignaling in the neonatal lung and affect circadian rhythmicity. Antioxid. Redox Signal. 21, 17-32.
152. Yoo, S.-H., Yamazaki, S., Lowrey, P.L., Shimomura, K., Ko, C.H., Buhr, E.D., Siepka, S.M., Hong, H.-K., Oh, W.J., Yoo, O.J., et al. (2004). PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. USA 101, 5339-5346.
153. Yoshida, Y., Iigusa, H., Wang, N., and Hasunuma, K. (2011). Crosstalk between the cellular redox state and the circadian system in Neurospora. PLoS One 6, e28227.
154. Yoshii, K., Tajima, F., Ishijima, S., and Sagami, I. (2015). Changes in pH and NADPH regulate the DNA binding activity of neuronal PAS domain protein 2, a mammalian circadian transcription factor. Biochemistry 54, 250-259.
155. Zhang, Q., Piston, D.W., and Goodman, R.H. (2002). Regulation of corepressor function by nuclear {NADH}. Science 295, 1895-1897.
156. Zhang, E.E., Liu, Y., Dentin, R., Pongsawakul, P.Y., Liu, A.C., Hirota, T., Nusinow, D.A., Sun, X., Landais, S., Kodama, Y., et al. (2010). Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nat. Med. 16, 1152-1156.
157. Zhang, R., Lahens, N.F., Ballance, H.I., Hughes, M.E., and Hogenesch, J.B. (2014). A circadian gene expression atlas in mammals: Implications for biology and medicine. Proc. Natl. Acad. Sci. USA 111, 16219-16224.
158. Zhou, M., Wang, W., Karapetyan, S., Mwimba, M., Marqués, J., Buchler, N.E., and Dong, X. (2015). Redox rhythm reinforces the circadian clock to gate immune response. Nature 523, 472-476.