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Revealing the hidden reality of the mammalian 12-h ultradian rhythms

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Abstract

Biological oscillations often cycle at different harmonics of the 24-h circadian rhythms, a phenomenon we coined “Musica Universalis” in 2017. Like the circadian rhythm, the 12-h oscillation is also evolutionarily conserved, robust, and has recently gained new traction in the field of chronobiology. Originally thought to be regulated by the circadian clock and/or environmental cues, recent new evidences support the notion that the majority of 12-h rhythms are regulated by a distinct and cell-autonomous pacemaker that includes the unfolded protein response (UPR) transcription factor spliced form of XBP1 (XBP1s). 12-h cycle of XBP1s level in turn transcriptionally generates robust 12-h rhythms of gene expression enriched in the central dogma information flow (CEDIF) pathway. Given the regulatory and functional separation of the 12-h and circadian clocks, in this review, we will focus our attention on the mammalian 12-h pacemaker, and discuss our current understanding of its prevalence, evolutionary origin, regulation, and functional roles in both physiological and pathological processes.

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References

  1. Rijo-Ferreira F, Takahashi JS (2019) Genomics of circadian rhythms in health and disease. Genome Med 11(1):82. https://doi.org/10.1186/s13073-019-0704-0

    Article  PubMed  PubMed Central  Google Scholar 

  2. Zhu B, Dacso CC, O’Malley BW (2018) Unveiling “Musica Universalis” of the cell: a brief history of biological 12-hour rhythms. J Endocr Soc 2(7):727–752. https://doi.org/10.1210/js.2018-00113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, Baggs JE, Panda S, Hogenesch JB (2009) Harmonics of circadian gene transcription in mammals. PLoS Genet 5(4):e1000442. https://doi.org/10.1371/journal.pgen.1000442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zhu B, Zhang Q, Pan Y, Mace EM, York B, Antoulas AC, Dacso CC, O'Malley BW (2017) A cell-autonomous mammalian 12 h clock coordinates metabolic and stress rhythms. Cell Metab 25(6):1305–1319 e1309. https://doi.org/10.1016/j.cmet.2017.05.004

  5. Antoulas AC, Zhu B, Zhang Q, York B, O’Malley BW, Dacso CC (2018) A novel mathematical method for disclosing oscillations in gene transcription: a comparative study. PLoS ONE 13(9):e0198503. https://doi.org/10.1371/journal.pone.0198503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Pan Y, Ballance H, Meng H, Gonzalez N, Kim S-M, Abdurehman L, York B, Chen X, Schnytzer Y, Levy O, Dacso CC, McClung CA, O’Malley BW, Liu S, Zhu B (2020) 12-h clock regulation of genetic information flow by XBP1s. PLoS Biol 18(1):e3000580. https://doi.org/10.1371/journal.pbio.3000580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Hughes ME, Hogenesch JB, Kornacker K (2010) JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms 25(5):372–380. https://doi.org/10.1177/0748730410379711

    Article  PubMed  PubMed Central  Google Scholar 

  8. Yang R, Su Z (2010) Analyzing circadian expression data by harmonic regression based on autoregressive spectral estimation. Bioinformatics 26(12):i168-174. https://doi.org/10.1093/bioinformatics/btq189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Thaben PF, Westermark PO (2014) Detecting rhythms in time series with RAIN. J Biol Rhythms 29(6):391–400. https://doi.org/10.1177/0748730414553029

    Article  PubMed  PubMed Central  Google Scholar 

  10. Pan Y, Ballance H, Schnytzer Y, Chen X, Levy O, Coarfa C, Zhu B (2019) 12h-clock control of central dogma information flow by XBP1s. bioRxiv:559039. https://doi.org/10.1101/559039

  11. Ananthasubramaniam B, Diernfellner A, Brunner M, Herzel H (2018) Ultradian Rhythms in the Transcriptome of Neurospora crassa. iScience 9:475–486. doi:https://doi.org/10.1016/j.isci.2018.11.012

  12. Koike N, Yoo SH, Huang HC, Kumar V, Lee C, Kim TK, Takahashi JS (2012) Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338(6105):349–354. https://doi.org/10.1126/science.1226339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB (2014) A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci USA 111(45):16219–16224. https://doi.org/10.1073/pnas.1408886111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhu B (2020) Decoding the function and regulation of the mammalian 12h-clock. J Mol Cell Biol. https://doi.org/10.1093/jmcb/mjaa021

    Article  PubMed  PubMed Central  Google Scholar 

  15. El-Athman R, Knezevic D, Fuhr L, Relogio A (2019) A computational analysis of alternative splicing across mammalian tissues reveals circadian and ultradian rhythms in splicing events. Int J Mol Sci. https://doi.org/10.3390/ijms20163977

  16. Jiao X, Wu M, Lu D, Gu J, Li Z (2019) Transcriptional profiling of daily patterns of mRNA expression in the C57BL/6J mouse cornea. Curr Eye Res 44(10):1054–1066. https://doi.org/10.1080/02713683.2019.1625408

    Article  CAS  PubMed  Google Scholar 

  17. Mure LS, Le HD, Benegiamo G, Chang MW, Rios L, Jillani N, Ngotho M, Kariuki T, Dkhissi-Benyahya O, Cooper HM, Panda S (2018) Diurnal transcriptome atlas of a primate across major neural and peripheral tissues. Science 359(6381):1232. https://doi.org/10.1126/science.aao0318

    Article  CAS  Google Scholar 

  18. Hoon Kim Y, Lazar MA (2020) Transcriptional control of circadian rhythms and metabolism: a matter of time and space. Endocr Rev. https://doi.org/10.1210/endrev/bnaa014

    Article  Google Scholar 

  19. Koyanagi I, Akers KG, Vergara P, Srinivasan S, Sakurai T, Sakaguchi M (2019) Memory consolidation during sleep and adult hippocampal neurogenesis. Neural Regen Res 14(1):20–23. https://doi.org/10.4103/1673-5374.243695

    Article  PubMed  PubMed Central  Google Scholar 

  20. Nadel L, Hupbach A, Gomez R, Newman-Smith K (2012) Memory formation, consolidation and transformation. Neurosci Biobehav Rev 36(7):1640–1645. https://doi.org/10.1016/j.neubiorev.2012.03.001

    Article  CAS  PubMed  Google Scholar 

  21. McMaster CR (2001) Lipid metabolism and vesicle trafficking: more than just greasing the transport machinery. Biochem Cell Biol 79(6):681–692. https://doi.org/10.1139/o01-139

    Article  CAS  PubMed  Google Scholar 

  22. Genov N, Castellana S, Scholkmann F, Capocefalo D, Truglio M, Rosati J, Turco EM, Biagini T, Carbone A, Mazza T, Relogio A, Mazzoccoli G (2019) A multi-layered study on harmonic oscillations in mammalian genomics and proteomics. Int J Mol Sci. https://doi.org/10.3390/ijms20184585

  23. Hughes ME, Hong HK, Chong JL, Indacochea AA, Lee SS, Han M, Takahashi JS, Hogenesch JB (2012) Brain-specific rescue of clock reveals system-driven transcriptional rhythms in peripheral tissue. PLoS Genet 8(7):e1002835. https://doi.org/10.1371/journal.pgen.1002835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cretenet G, Le Clech M, Gachon F (2010) Circadian clock-coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver. Cell Metab 11(1):47–57. https://doi.org/10.1016/j.cmet.2009.11.002

    Article  CAS  PubMed  Google Scholar 

  25. Zhang K, Wang S, Malhotra J, Hassler JR, Back SH, Wang G, Chang L, Xu W, Miao H, Leonardi R, Chen YE, Jackowski S, Kaufman RJ (2011) The unfolded protein response transducer IRE1alpha prevents ER stress-induced hepatic steatosis. EMBO J 30(7):1357–1375. https://doi.org/10.1038/emboj.2011.52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Westermark PO, Herzel H (2013) Mechanism for 12 hr rhythm generation by the circadian clock. Cell Rep 3(4):1228–1238. https://doi.org/10.1016/j.celrep.2013.03.013

    Article  CAS  PubMed  Google Scholar 

  27. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103(7):1009–1017. https://doi.org/10.1016/s0092-8674(00)00205-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Yang G, Chen L, Grant GR, Paschos G, Song WL, Musiek ES, Lee V, McLoughlin SC, Grosser T, Cotsarelis G, FitzGerald GA (2016) Timing of expression of the core clock gene Bmal1 influences its effects on aging and survival. Sci Transl Med 8(324):324ra316. https://doi.org/10.1126/scitranslmed.aad3305

  29. Miller BH, McDearmon EL, Panda S, Hayes KR, Zhang J, Andrews JL, Antoch MP, Walker JR, Esser KA, Hogenesch JB, Takahashi JS (2007) Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci USA 104(9):3342–3347. https://doi.org/10.1073/pnas.0611724104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ray S, Valekunja UK, Stangherlin A, Howell SA, Snijders AP, Damodaran G, Reddy AB (2020) Circadian rhythms in the absence of the clock gene Bmal1. Science 367(6479):800–806. https://doi.org/10.1126/science.aaw7365

    Article  CAS  PubMed  Google Scholar 

  31. Atwood A, DeConde R, Wang SS, Mockler TC, Sabir JS, Ideker T, Kay SA (2011) Cell-autonomous circadian clock of hepatocytes drives rhythms in transcription and polyamine synthesis. Proc Natl Acad Sci USA 108(45):18560–18565. https://doi.org/10.1073/pnas.1115753108

    Article  PubMed  PubMed Central  Google Scholar 

  32. Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334(6059):1081–1086. https://doi.org/10.1126/science.1209038

    Article  CAS  PubMed  Google Scholar 

  33. Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13(2):89–102. https://doi.org/10.1038/nrm3270

    Article  CAS  PubMed  Google Scholar 

  34. Mori K (2009) Signalling pathways in the unfolded protein response: development from yeast to mammals. J Biochem 146(6):743–750. https://doi.org/10.1093/jb/mvp166

    Article  CAS  PubMed  Google Scholar 

  35. Sidrauski C, Walter P (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90(6):1031–1039. https://doi.org/10.1016/s0092-8674(00)80369-4

    Article  CAS  PubMed  Google Scholar 

  36. Majumder M, Huang C, Snider MD, Komar AA, Tanaka J, Kaufman RJ, Krokowski D, Hatzoglou M (2012) A novel feedback loop regulates the response to endoplasmic reticulum stress via the cooperation of cytoplasmic splicing and mRNA translation. Mol Cell Biol 32(5):992–1003. https://doi.org/10.1128/MCB.06665-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107(7):881–891. https://doi.org/10.1016/s0092-8674(01)00611-0

    Article  CAS  PubMed  Google Scholar 

  38. Acosta-Alvear D, Zhou Y, Blais A, Tsikitis M, Lents NH, Arias C, Lennon CJ, Kluger Y, Dynlacht BD (2007) XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol Cell 27(1):53–66. https://doi.org/10.1016/j.molcel.2007.06.011

    Article  CAS  PubMed  Google Scholar 

  39. Pramanik J, Chen X, Kar G, Henriksson J, Gomes T, Park JE, Natarajan K, Meyer KB, Miao Z, McKenzie ANJ, Mahata B, Teichmann SA (2018) Genome-wide analyses reveal the IRE1a-XBP1 pathway promotes T helper cell differentiation by resolving secretory stress and accelerating proliferation. Genome Med 10(1):76. https://doi.org/10.1186/s13073-018-0589-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yoshida H, Oku M, Suzuki M, Mori K (2006) pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J Cell Biol 172(4):565–575. https://doi.org/10.1083/jcb.200508145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Castellana S, Mazza T, Capocefalo D, Genov N, Biagini T, Fusilli C, Scholkmann F, Relogio A, Hogenesch JB, Mazzoccoli G (2018) Systematic analysis of mouse genome reveals distinct evolutionary and functional properties among circadian and ultradian genes. Front Physiol 9:1178. https://doi.org/10.3389/fphys.2018.01178

    Article  PubMed  PubMed Central  Google Scholar 

  42. Cooper CD, Newman JA, Gileadi O (2014) Recent advances in the structural molecular biology of Ets transcription factors: interactions, interfaces and inhibition. Biochem Soc Trans 42(1):130–138. https://doi.org/10.1042/BST20130227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wang Y, Song L, Liu M, Ge R, Zhou Q, Liu W, Li R, Qie J, Zhen B, Wang Y, He F, Qin J, Ding C (2018) A proteomics landscape of circadian clock in mouse liver. Nat Commun 9(1):1553. https://doi.org/10.1038/s41467-018-03898-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wilcockson D, Zhang L (2008) Circatidal clocks. Curr Biol 18(17):R753–R755. https://doi.org/10.1016/j.cub.2008.06.041

    Article  CAS  PubMed  Google Scholar 

  45. Andreatta G, Tessmar-Raible K (2020) The still dark side of the moon: molecular mechanisms of lunar-controlled rhythms and clocks. J Mol Biol 432(12):3525–3546. https://doi.org/10.1016/j.jmb.2020.03.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. NAYLOR E (1958) Tidal and Diurnal Rhythms of Locomotory Activity in Carcinus maenas (L.). J Exp Biol 35 (3):602–610

  47. Naylor E (1996) Crab clockwork: the case for interactive circatidal and circadian oscillators controlling rhythmic locomotor activity of Carcinus maenas. Chronobiol Int 13(3):153–161

    Article  CAS  PubMed  Google Scholar 

  48. Zhang L, Hastings MH, Green EW, Tauber E, Sladek M, Webster SG, Kyriacou CP, Wilcockson DC (2013) Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra. Curr Biol 23(19):1863–1873. https://doi.org/10.1016/j.cub.2013.08.038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. O’Neill JS, Lee KD, Zhang L, Feeney K, Webster SG, Blades MJ, Kyriacou CP, Hastings MH, Wilcockson DC (2015) Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra. Curr Biol 25(8):R326-327. https://doi.org/10.1016/j.cub.2015.02.052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Akiyama T (2004) Entrainment of the circatidal swimming activity rhythm in the cumacean Dimorphostylis asiatica (Crustacea) to 12.5-hour hydrostatic pressure cycles. Zool Sci 21 (1):29–38. https://doi.org/10.2108/0289-0003(2004)21[29:EOTCSA]2.0.CO;2

  51. Takekata H, Matsuura Y, Goto SG, Satoh A, Numata H (2012) RNAi of the circadian clock gene period disrupts the circadian rhythm but not the circatidal rhythm in the mangrove cricket. Biol Lett 8(4):488–491. https://doi.org/10.1098/rsbl.2012.0079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Takekata H, Numata H, Shiga S, Goto SG (2014) Silencing the circadian clock gene Clock using RNAi reveals dissociation of the circatidal clock from the circadian clock in the mangrove cricket. J Insect Physiol 68:16–22. https://doi.org/10.1016/j.jinsphys.2014.06.012

    Article  CAS  PubMed  Google Scholar 

  53. Takekata H, Numata H, Shiga S (2014) The circatidal rhythm persists without the optic lobe in the mangrove cricket Apteronemobius asahinai. J Biol Rhythms 29(1):28–37. https://doi.org/10.1177/0748730413516309

    Article  PubMed  Google Scholar 

  54. Fang B, Everett LJ, Jager J, Briggs E, Armour SM, Feng D, Roy A, Gerhart-Hines Z, Sun Z, Lazar MA (2014) Circadian enhancers coordinate multiple phases of rhythmic gene transcription in vivo. Cell 159(5):1140–1152. https://doi.org/10.1016/j.cell.2014.10.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Menet JS, Rodriguez J, Abruzzi KC, Rosbash M (2012) Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. Elife 1:e00011. https://doi.org/10.7554/eLife.00011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Eckel-Mahan KL, Patel VR, de Mateo S, Orozco-Solis R, Ceglia NJ, Sahar S, Dilag-Penilla SA, Dyar KA, Baldi P, Sassone-Corsi P (2013) Reprogramming of the circadian clock by nutritional challenge. Cell 155(7):1464–1478. https://doi.org/10.1016/j.cell.2013.11.034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Robles MS, Cox J, 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(1):e1004047. https://doi.org/10.1371/journal.pgen.1004047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sorek M, Schnytzer Y, Ben-Asher HW, Caspi VC, Chen CS, Miller DJ, Levy O (2018) Setting the pace: host rhythmic behaviour and gene expression patterns in the facultatively symbiotic cnidarian Aiptasia are determined largely by Symbiodinium. Microbiome 6(1):83. https://doi.org/10.1186/s40168-018-0465-9

    Article  PubMed  PubMed Central  Google Scholar 

  59. Schnytzer Y, Simon-Blecher N, Li J, Ben-Asher HW, Salmon-Divon M, Achituv Y, Hughes ME, Levy O (2018) Tidal and diel orchestration of behaviour and gene expression in an intertidal mollusc. Sci Rep 8(1):4917. https://doi.org/10.1038/s41598-018-23167-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Satoh A, Terai Y (2019) Circatidal gene expression in the mangrove cricket Apteronemobius asahinai. Sci Rep 9(1):3719. https://doi.org/10.1038/s41598-019-40197-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. van der Linden AM, Beverly M, Kadener S, Rodriguez J, Wasserman S, Rosbash M, Sengupta P (2010) Genome-wide analysis of light- and temperature-entrained circadian transcripts in Caenorhabditis elegans. PLoS Biol 8(10):e1000503. https://doi.org/10.1371/journal.pbio.1000503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Li Y, Li G, Wang H, Du J, Yan J (2013) Analysis of a gene regulatory cascade mediating circadian rhythm in zebrafish. PLoS Comput Biol 9(2):e1002940. https://doi.org/10.1371/journal.pcbi.1002940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Mure LS, Le HD, Benegiamo G, Chang MW, Rios L, Jillani N, Ngotho M, Kariuki T, Dkhissi-Benyahya O, Cooper HM, Panda S (2018) Diurnal transcriptome atlas of a primate across major neural and peripheral tissues. Science. https://doi.org/10.1126/science.aao0318

    Article  PubMed  PubMed Central  Google Scholar 

  64. Casali C, Malvicini R, Erjavec L, Parra L, Artuch A, Fernández Tome MC (2020) X-box binding protein 1 (XBP1): a key protein for renal osmotic adaptation. Its role in lipogenic program regulation. Biochim Biophys Acta Mol Cell Biol Lipids 1865(4):158616. https://doi.org/10.1016/j.bbalip.2020.158616

  65. Colquhoun WP, Blake MJ, Edwards RS (1968) Experimental studies of shift-work I: a comparison of “rotating” and “stabilized” 4-hour shift systems. Ergonomics 11(5):437–453. https://doi.org/10.1080/00140136808930993

    Article  CAS  PubMed  Google Scholar 

  66. Colquhoun WP, Paine MW, Fort A (1978) Circadian rhythm of body temperature during prolonged undersea voyages. Aviat Space Environ Med 49(5):671–678

    CAS  PubMed  Google Scholar 

  67. Colquhoun WP, Paine MW, Fort A (1979) Changes in the temperature rhythm of submariners following a rapidly rotating watchkeeping system for a prolonged period. Int Arch Occup Environ Health 42(3–4):185–190

    Article  CAS  PubMed  Google Scholar 

  68. Moore-Ede MC, Czeisler CA (1984) Mathematical models of the circadian sleep-wake cycle. Raven Press, New York

    Book  Google Scholar 

  69. Kronauer RE, Jewett ME (1992) The relationship between circadian and hemicircadian components of human endogenous temperature rhythms. J Sleep Res 1(2):88–92

    Article  CAS  PubMed  Google Scholar 

  70. Monk TH, Buysse DJ, Reynolds CF 3rd, Kupfer DJ (1996) Circadian determinants of the postlunch dip in performance. Chronobiol Int 13(2):123–133

    Article  CAS  PubMed  Google Scholar 

  71. Wan C, Wang Z, Cornelissen G, Halberg F (1992) Age, gender and circadian or circasemidian blood pressure and heart rate variation of children. Chronobiologia 19(3–4):121–129

    CAS  PubMed  Google Scholar 

  72. Otsuka K, Murakami S, Kubo Y, Yamanaka T, Mitsutake G, Ohkawa S, Matsubayashi K, Yano S, Cornelissen G, Halberg F (2003) Chronomics for chronoastrobiology with immediate spin-offs for life quality and longevity. Biomed Pharmacother 57(Suppl 1):1s–18s

    Article  PubMed  Google Scholar 

  73. Lee JS, Lee MS, Lee JY, Cornelissen G, Otsuka K, Halberg F (2003) Effects of diaphragmatic breathing on ambulatory blood pressure and heart rate. Biomed Pharmacother 57(Suppl 1):87s–91s

    Article  PubMed  Google Scholar 

  74. Otsuka K, Oinuma S, Cornelissen G, Weydahl A, Ichimaru Y, Kobayashi M, Yano S, Holmeslet B, Hansen TL, Mitsutake G, Engebretson MJ, Schwartzkopff O, Halberg F (2001) Alternating light-darkness-influenced human electrocardiographic magnetoreception in association with geomagnetic pulsations. Biomed Pharmacother 55(Suppl 1):63s–75s

    PubMed  Google Scholar 

  75. Otsuka K, Cornelissen G, Furukawa S, Kubo Y, Hayashi M, Shibata K, Mizuno K, Aiba T, Ohshima H, Mukai C (2016) Long-term exposure to space’s microgravity alters the time structure of heart rate variability of astronauts. Heliyon 2(12):e00211. https://doi.org/10.1016/j.heliyon.2016.e00211

    Article  PubMed  PubMed Central  Google Scholar 

  76. Otsuka K, Cornelissen G, Halberg F (1997) Circadian rhythmic fractal scaling of heart rate variability in health and coronary artery disease. Clin Cardiol 20(7):631–638

    Article  CAS  PubMed  Google Scholar 

  77. Bjerner B, Holm A, Swensson A (1955) Diurnal variation in mental performance; a study of three-shift workers. Br J Ind Med 12(2):103–110

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Mitler MM, Carskadon MA, Czeisler CA, Dement WC, Dinges DF, Graeber RC (1988) Catastrophes, sleep, and public policy: consensus report. Sleep 11(1):100–109

    Article  CAS  PubMed  Google Scholar 

  79. Dinges DF, Broughton RJ (1989) Sleep and alertness: chronobiological, behavioral, and medical aspects of napping. Raven Press, New York

    Google Scholar 

  80. Broughton RJ (1998) SCN controlled circadian arousal and the afternoon “nap zone.” Sleep Res Online 1(4):166–178

    CAS  PubMed  Google Scholar 

  81. Reinberg A, Bicakova-Rocher A, Nouguier J, Gorceix A, Mechkouri M, Touitou Y, Ashkenazi I (1997) Circadian rhythm period in reaction time to light signals: difference between right- and left-hand side. Brain Res Cogn Brain Res 6(2):135–140

    Article  CAS  PubMed  Google Scholar 

  82. Shub Y, Lewy H, Ashkenazi IE (2001) Circadian pattern of simulated flight performance of pilots is derived from ultradian components. Chronobiol Int 18(6):987–1003

    Article  CAS  PubMed  Google Scholar 

  83. Iskra-Golec I (2006) Ultradian and asymmetric rhythms of hemispheric processing speed. Chronobiol Int 23(6):1229–1239. https://doi.org/10.1080/07420520601077922

    Article  PubMed  Google Scholar 

  84. Harrington MG, Salomon RM, Pogoda JM, Oborina E, Okey N, Johnson B, Schmidt D, Fonteh AN, Dalleska NF (2010) Cerebrospinal fluid sodium rhythms. Cerebrospinal Fluid Res 7:3. https://doi.org/10.1186/1743-8454-7-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Ayala DE, Hermida RC, Garcia L, Iglesias T, Lodeiro C (1990) Multiple component analysis of plasma growth hormone in children with standard and short stature. Chronobiol Int 7(3):217–220

    Article  CAS  PubMed  Google Scholar 

  86. Francis SJ, Walker RF, Riad-Fahmy D, Hughes D, Murphy JF, Gray OP (1987) Assessment of adrenocortical activity in term newborn infants using salivary cortisol determinations. J Pediatr 111(1):129–133

    Article  CAS  PubMed  Google Scholar 

  87. Kanabrocki EL, Sothern RB, Ryan MD, Kahn S, Augustine G, Johnson C, Foley S, Gathing A, Eastman G, Friedman N, Nemchausky BA, Kaplan E (2008) Circadian characteristics of serum calcium, magnesium and eight trace elements and of their metallo-moieties in urine of healthy middle-aged men. Clin Ter 159(5):329–346

    CAS  PubMed  Google Scholar 

  88. Broughton RJ (1979) Biorhythmic variations in consciousness and psychological functions. Can Psychol Rev 16(4):217–239

    Article  Google Scholar 

  89. Broughton R, Mullington J (1992) Circasemidian sleep propensity and the phase-amplitude maintenance model of human sleep/wake regulation. J Sleep Res 1(2):93–98

    Article  CAS  PubMed  Google Scholar 

  90. Hayashi M, Morikawa T, Hori T (2002) Circasemidian 12 h cycle of slow wave sleep under constant darkness. Clin Neurophysiol 113(9):1505–1516

    Article  PubMed  Google Scholar 

  91. Billiard M, Carlander B, Besset A (1996) Circadian rhythm in normal and pathological sleep. Pathol Biol (Paris) 44(6):509–517

    CAS  Google Scholar 

  92. Nobili L, Besset A, Ferrillo F, Rosadini G, Schiavi G, Billiard M (1995) Dynamics of slow wave activity in narcoleptic patients under bed rest conditions. Electroencephalogr Clin Neurophysiol 95(6):414–425

    Article  CAS  PubMed  Google Scholar 

  93. Broughton R, Mullington J (1994) Chronobiological aspects of narcolepsy. Sleep 17(8 Suppl):S35-44

    Article  CAS  PubMed  Google Scholar 

  94. Broughton R, Dunham W, Newman J, Lutley K, Duschesne P, Rivers M (1988) Ambulatory 24 hour sleep-wake monitoring in narcolepsy-cataplexy compared to matched controls. Electroencephalogr Clin Neurophysiol 70(6):473–481

    Article  CAS  PubMed  Google Scholar 

  95. De Koninck GC, Hebert M, Carrier J, Lamarche C, Dufour S (1996) Body temperature and the return of slow wave activity in extended sleep. Electroencephalogr Clin Neurophysiol 98(1):42–50

    Article  PubMed  Google Scholar 

  96. Deng Y, Wang ZV, Tao C, Gao N, Holland WL, Ferdous A, Repa JJ, Liang G, Ye J, Lehrman MA, Hill JA, Horton JD, Scherer PE (2013) The Xbp1s/GalE axis links ER stress to postprandial hepatic metabolism. J Clin Invest 123(1):455–468. https://doi.org/10.1172/JCI62819

    Article  CAS  PubMed  Google Scholar 

  97. Shao M, Shan B, Liu Y, Deng Y, Yan C, Wu Y, Mao T, Qiu Y, Zhou Y, Jiang S, Jia W, Li J, Li J, Rui L, Yang L, Liu Y (2014) Hepatic IRE1alpha regulates fasting-induced metabolic adaptive programs through the XBP1s-PPARalpha axis signalling. Nat Commun 5:3528. https://doi.org/10.1038/ncomms4528

    Article  CAS  PubMed  Google Scholar 

  98. Fu S, Watkins SM, Hotamisligil GS (2012) The role of endoplasmic reticulum in hepatic lipid homeostasis and stress signaling. Cell Metab 15(5):623–634. https://doi.org/10.1016/j.cmet.2012.03.007

    Article  CAS  PubMed  Google Scholar 

  99. Uemura A, Oku M, Mori K, Yoshida H (2009) Unconventional splicing of XBP1 mRNA occurs in the cytoplasm during the mammalian unfolded protein response. J Cell Sci 122(Pt 16):2877–2886. https://doi.org/10.1242/jcs.040584

    Article  CAS  PubMed  Google Scholar 

  100. Yamamoto K, Takahara K, Oyadomari S, Okada T, Sato T, Harada A, Mori K (2010) Induction of liver steatosis and lipid droplet formation in ATF6alpha-knockout mice burdened with pharmacological endoplasmic reticulum stress. Mol Biol Cell 21(17):2975–2986. https://doi.org/10.1091/mbc.E09-02-0133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Rutkowski DT, Wu J, Back SH, Callaghan MU, Ferris SP, Iqbal J, Clark R, Miao H, Hassler JR, Fornek J, Katze MG, Hussain MM, Song B, Swathirajan J, Wang J, Yau GD, Kaufman RJ (2008) UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell 15(6):829–840. https://doi.org/10.1016/j.devcel.2008.10.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Herrema H, Zhou Y, Zhang D, Lee J, Salazar Hernandez MA, Shulman GI, Ozcan U (2016) XBP1s is an anti-lipogenic protein. J Biol Chem 291(33):17394–17404. https://doi.org/10.1074/jbc.M116.728949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Rong X, Albert CJ, Hong C, Duerr MA, Chamberlain BT, Tarling EJ, Ito A, Gao J, Wang B, Edwards PA, Jung ME, Ford DA, Tontonoz P (2013) LXRs regulate ER stress and inflammation through dynamic modulation of membrane phospholipid composition. Cell Metab 18(5):685–697. https://doi.org/10.1016/j.cmet.2013.10.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Meng H, Gonzales NM, Lonard DM, Putluri N, Zhu B, Dacso CC, York B, O’Malley BW (2020) XBP1 links the 12-hour clock to NAFLD and regulation of membrane fluidity and lipid homeostasis. Nat Commun 11(1):6215. https://doi.org/10.1038/s41467-020-20028-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Ahrens M, Ammerpohl O, von Schonfels W, Kolarova J, Bens S, Itzel T, Teufel A, Herrmann A, Brosch M, Hinrichsen H, Erhart W, Egberts J, Sipos B, Schreiber S, Hasler R, Stickel F, Becker T, Krawczak M, Rocken C, Siebert R, Schafmayer C, Hampe J (2013) DNA methylation analysis in nonalcoholic fatty liver disease suggests distinct disease-specific and remodeling signatures after bariatric surgery. Cell Metab 18(2):296–302. https://doi.org/10.1016/j.cmet.2013.07.004

    Article  CAS  PubMed  Google Scholar 

  106. Golan K, Kumari A, Kollet O, Khatib-Massalha E, Subramaniam MD, Ferreira ZS, Avemaria F, Rzeszotek S, Garcia-Garcia A, Xie S, Flores-Figueroa E, Gur-Cohen S, Itkin T, Ludin-Tal A, Massalha H, Bernshtein B, Ciechanowicz AK, Brandis A, Mehlman T, Bhattacharya S, Bertagna M, Cheng H, Petrovich-Kopitman E, Janus T, Kaushansky N, Cheng T, Sagi I, Ratajczak MZ, Mendez-Ferrer S, Dick JE, Markus RP, Lapidot T (2018) Daily onset of light and darkness differentially controls hematopoietic stem cell differentiation and maintenance. Cell Stem Cell 23(4):572–585 e577. https://doi.org/10.1016/j.stem.2018.08.002

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Acknowledgement

We want to thank Dr. Akhilesh Reddy for kindly sharing with us the raw RNA-seq data to analyze ultradian rhythm in BMAL1-less ex vivo liver slices. We also would like to thank Dr. Baby Anjum for assistance with initial literature search. We apologize for any potential omission of relevant works and citations due to space constraints. We thank the American Diabetes Association junior faculty development award 1-18-JDF-025 to B.Z. B.Z. was further supported by the National Institute Of General Medical Sciences of the National Institutes of Health under Award Number DP2GM140924. Research reported in this publication was further supported by the National Institute of Diabetes And Digestive And Kidney Diseases of the National Institutes of Health under award number P30DK120531 to Pittsburgh Liver Research Center, in which B.Z. is a member. H.B. is further supported by a T32 training grant T32AG021885 from National Institute of Health. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies.

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  1. Aging Institute of UPMC, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA

    Heather Ballance & Bokai Zhu

  2. Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, USA

    Bokai Zhu

  3. Division of Endocrinology and Metabolism, Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA

    Bokai Zhu

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  1. Heather Ballance
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18_2020_3730_MOESM1_ESM.tif

Figure S1. The XBP1s-dependent 12-hour pacemaker is separate from the BMAL1-dependent circadian clock in mouse. Representative gene expression of 12-hour and/or circadian genes in wild-type, XBP1 liver specific knockout [6], and BMAL1-knockout ex vivo liver slices [30]. Temporal cistrome of XBP1s as well as key core circadian clock TFs are further shown. (tif 11670 kb)

18_2020_3730_MOESM2_ESM.xlsx

Table S1. Rhythms uncovered for ETS TFs in mouse liver. For everyone EST TF, whether a 12-hour or circadian rhythm exist is shown, as well as the dominant rhythm identified (xlsx 12 kb)

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Ballance, H., Zhu, B. Revealing the hidden reality of the mammalian 12-h ultradian rhythms. Cell. Mol. Life Sci. 78, 3127–3140 (2021). https://doi.org/10.1007/s00018-020-03730-5

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