1932

Abstract

Diverse factors including metabolism, chromatin remodeling, and mitotic kinetics influence development at the cellular level. These factors are well known to interact with the circadian transcriptional-translational feedback loop (TTFL) after its emergence. What is only recently becoming clear, however, is how metabolism, mitosis, and epigenetics may become organized in a coordinated cyclical precursor signaling module in pluripotent cells prior to the onset of TTFL cycling. We propose that both the precursor module and the TTFL module constrain cellular identity when they are active during development, and that the emergence of these modules themselves is a key lineage marker. Here we review the component pathways underlying these ideas; how proliferation, specification, and differentiation decisions in both developmental and adult stem cell populations are or are not regulated by the classical TTFL; and emerging evidence that we propose implies a primordial clock that precedes the classical TTFL and influences early developmental decisions.

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2020-10-06
2024-04-15
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Literature Cited

  1. Aardal NP, Laerum OD. 1983. Circadian variations in mouse bone marrow. Exp. Hematol. 11:9792–801
    [Google Scholar]
  2. Abrahamsen JF, Smaaland R, Sothern RB, Laerum OD 1998. Variation in cell yield and proliferative activity of positive selected human CD34 bone marrow cells along the circadian time scale. Eur. J. Haematol. 60:17–15 https://doi.org/10.1111/j.1600-0609.1998.tb00990.x
    [Crossref] [Google Scholar]
  3. Aguilar-Arnal L, Hakim O, Patel VR, Baldi P, Hager GL, Sassone-Corsi P 2013. Cycles in spatial and temporal chromosomal organization driven by the circadian clock. Nat. Struct. Mol. Biol. 20:101206–13 https://doi.org/10.1038/nsmb.2667
    [Crossref] [Google Scholar]
  4. Aires R, Dias A, Mallo M 2018. Deconstructing the molecular mechanisms shaping the vertebrate body plan. Curr. Opin. Cell Biol. 55:81–86 https://doi.org/10.1016/j.ceb.2018.05.009
    [Crossref] [Google Scholar]
  5. Ait-Hmyed O, Felder-Schmittbuhl M-P, Garcia-Garrido M, Beck S, Seide C et al. 2013. Mice lacking Period 1 and Period 2 circadian clock genes exhibit blue cone photoreceptor defects. Eur. J. Neurosci. 37:71048–60 https://doi.org/10.1111/ejn.12103
    [Crossref] [Google Scholar]
  6. Akle V, Stankiewicz AJ, Kharchenko V, Yu L, Kharchenko PV, Zhdanova IV 2017. Circadian kinetics of cell cycle progression in adult neurogenic niches of a diurnal vertebrate. J. Neurosci. 37:71900–9 https://doi.org/10.1523/jneurosci.3222-16.2017
    [Crossref] [Google Scholar]
  7. Albaugh BN, Arnold KM, Denu JM 2011. KAT(ching) metabolism by the tail: insight into the links between lysine acetyltransferases and metabolism. ChemBioChem 12:2290–98 https://doi.org/10.1002/cbic.201000438
    [Crossref] [Google Scholar]
  8. Ali AAH, Schwartz-Herzke B, Mir S, Sahlender B, Victor M et al. 2019. Deficiency of the clock gene Bmal1 affects neural progenitor cell migration. Brain Struct. Funct. 224:1373–86 https://doi.org/10.1007/s00429-018-1775-1
    [Crossref] [Google Scholar]
  9. Ali AAH, Schwarz-Herzke B, Stahr A, Prozorovski T, Aktas O, von Gall C 2015. Premature aging of the hippocampal neurogenic niche in adult Bmal1‐deficient mice. Aging 7:6435–49 https://doi.org/10.18632/aging.100764
    [Crossref] [Google Scholar]
  10. Almeida S, Chaves M, Delaunay F 2020. Control of synchronization ratios in clock/cell cycle coupling by growth factors and glucocorticoids. R. Soc. Open Sci. 7:2192054 https://doi.org/10.1098/rsos.192054
    [Crossref] [Google Scholar]
  11. Altman BJ, Hsieh AL, Sengupta A, Krishnanaiah SY, Stine ZE et al. 2015. MYC disrupts the circadian clock and metabolism in cancer cells. Cell Metab 22:61009–19 https://doi.org/10.1016/j.cmet.2015.09.003
    [Crossref] [Google Scholar]
  12. Alvarez JD, Chen D, Storer E, Sehgal A 2003. Non-cyclic and developmental stage-specific expression of circadian clock proteins during murine spermatogenesis. Biol. Reprod. 69:181–91 https://doi.org/10.1095/biolreprod.102.011833
    [Crossref] [Google Scholar]
  13. Alvarez JD, Hansen A, Ord T, Bebas P, Chappell PE et al. 2008. The circadian clock protein BMAL1 is necessary for fertility and proper testosterone production in mice. J. Biol. Rhythms 23:126–36 https://doi.org/10.1177/0748730407311254
    [Crossref] [Google Scholar]
  14. Alvarez-Dominguez JR, Donaghey J, Rasouli N, Kenty JHR, Helman A et al. 2020. Circadian entrainment triggers maturation of human in vitro islets. Cell Stem Cell 26:1108–22.e10 https://doi.org/10.1016/j.stem.2019.11.011
    [Crossref] [Google Scholar]
  15. Amano T, Matsushita A, Hatanaka Y, Watanabe T, Oishi K et al. 2009. Expression and functional analyses of circadian genes in mouse oocytes and preimplantation embryos: Cry1 is involved in the meiotic process independently of circadian clock regulation. Biol. Reprod. 80:3473–83 https://doi.org/10.1095/biolreprod.108.069542
    [Crossref] [Google Scholar]
  16. Ameneiro C, Moreira T, Fuentes-Iglesias A, Coego A, Garcia-Outeiral V et al. 2020. BMAL1 coordinates energy metabolism and differentiation of pluripotent stem cells. Life Sci. Alliance 3:5e201900534 https://doi.org/10.26508/lsa.201900534
    [Crossref] [Google Scholar]
  17. Asher G, Gatfield D, Stratmann M, Reinke H, Dibner C et al. 2008. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134:2317–28 https://doi.org/10.1016/j.cell.2008.06.050
    [Crossref] [Google Scholar]
  18. Baba K, Piano I, Lyuboslavsky P, Chrenek MA, Sellers JT et al. 2018. Removal of clock gene Bmal1 from the retina affects retinal development and accelerates cone photoreceptor degeneration during aging. PNAS 115:5113099–104 https://doi.org/10.1073/pnas.1808137115
    [Crossref] [Google Scholar]
  19. Balakrishnan A, Stearns AT, Ashley SW, Tavakkolizadeh A, Rhoads DB 2010. Restricted feeding phase shifts clock gene and sodium glucose cotransporter 1 (SGLT1) expression in rats. J. Nutr. 140:5908–14 https://doi.org/10.3945/jn.109.116749
    [Crossref] [Google Scholar]
  20. Balsalobre A, Damiola F, Schibler U 1998. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:6929–37 https://doi.org/10.1016/s0092-8674(00)81199-x
    [Crossref] [Google Scholar]
  21. Bannister AJ, Kouzarides T. 2011. Regulation of chromatin by histone modifications. Cell Res 21:38195 https://doi.org/10.1038/cr.2011.22
    [Crossref] [Google Scholar]
  22. Bebas P, Goodall CP, Majewska M, Neumann A, Giebultowicz JM, Chappell PE 2009. Circadian clock and output genes are rhythmically expressed in extratesticular ducts and accessory organs of mice. FASEB J 23:2523–33 https://doi.org/10.1096/fj.08-113191
    [Crossref] [Google Scholar]
  23. Bedont JL, Blackshaw S. 2015. Constructing the suprachiasmatic nucleus: a watchmaker's perspective on the central clockworks. Front. Syst. Neurosci. 9:e74 https://doi.org/10.3389/fnsys.2015.00074
    [Crossref] [Google Scholar]
  24. Bedont JL, Newman EA, Blackshaw S 2015. Patterning, specification, and differentiation in the developing hypothalamus. Dev. Biol. 4:5445–68 https://doi.org/10.1002/wdev.187
    [Crossref] [Google Scholar]
  25. Bellet MM, Nakahata Y, Boudjelal M, Watts E, Mossakowska DE et al. 2013. Pharmacological modulation of circadian rhythms by synthetic activators of the deacetylase SIRT1. PNAS 110:93333–38 https://doi.org/10.1073/pnas.1214266110
    [Crossref] [Google Scholar]
  26. Bernardos RL, Barthel LK, Meyers JR, Raymond PA 2007. Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J. Neurosci. 27:267028–40 https://doi.org/10.1523/jneurosci.1624-07.2007
    [Crossref] [Google Scholar]
  27. Bhatwadekar AD, Beli E, Diao Y, Chen J, Luo Q et al. 2017. Conditional deletion of Bmal1 accentuates microvascular and macrovascular injury. Am. J. Pathol. 187:61426–35 https://doi.org/10.1016/j.ajpath.2017.02.014
    [Crossref] [Google Scholar]
  28. Bhatwadekar AD, Yan Y, Qi X, Thinschmidt JS, Neu MB et al. 2013. Per2 mutation recapitulates the vascular phenotype of diabetes in the retina and bone marrow. Diabetes 62:1273–82 https://doi.org/10.2337/db12-0172
    [Crossref] [Google Scholar]
  29. Bian S-S, Zheng X-L, Sun H-Q, Chen J-H, Lu Y-L et al. 2017. Clock1a affects mesoderm development and primitive hematopoiesis by regulating Nodal-Smad3 signaling in the zebrafish embryo. J. Biol. Chem. 292:3414165–75 https://doi.org/10.1074/jbc.m117.794289
    [Crossref] [Google Scholar]
  30. Bieler J, Cannavo R, Gustafson K, Gobet C, Gatfield D, Naef F 2014. Robust synchronization of coupled circadian and cell cycle oscillators in single mammalian cells. Mol. Syst. Biol. 10:7739 https://doi.org/10.15252/msb.20145218
    [Crossref] [Google Scholar]
  31. Borgs L, Beukelaers P, Vandenbosch R, Nguyen L, Moonen G et al. 2009. Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci 10:130 https://doi.org/10.1186/1471-2202-10-30
    [Crossref] [Google Scholar]
  32. Boroughs LK, Deberardinis RJ. 2015. Metabolic pathways promoting cancer cell survival and growth. Nat. Cell Biol. 17:4351–59 https://doi.org/10.1038/ncb3124
    [Crossref] [Google Scholar]
  33. Bouchard-Cannon P, Mendoza-Viveros L, Yuen A, Kaern M, Cheng H-YM 2013. The circadian molecular clock regulates adult hippocampal neurogenesis by controlling the timing of cell-cycle entry and exit. Cell Rep 5:4961–73 https://doi.org/10.1016/j.celrep.2013.10.037
    [Crossref] [Google Scholar]
  34. Boucher H, Vanneaux V, Domet T, Parouchev A, Larghero J 2016. Circadian clock genes modulate human bone marrow mesenchymal stem cell differentiation, migration and cell cycle. PLOS ONE 11:1e0146674 https://doi.org/10.1371/journal.pone.0146674
    [Crossref] [Google Scholar]
  35. Bourin P, Ledain AF, Beau J, Mille D, Lévi F 2002. In-vitro circadian rhythm of murine bone marrow progenitor production. Chronobiol. Int. 19:157–67 https://doi.org/10.1081/cbi-120002677
    [Crossref] [Google Scholar]
  36. Buhr ED, Vemaraju S, Diaz N, Lang RA, Van Gelder RN 2019. Neuropsin (OPN5) mediates local light-dependent induction of circadian clock genes and circadian photoentrainment in exposed murine skin. Curr. Biol. 29:203478–87.e4 https://doi.org/10.1016/j.cub.2019.08.063
    [Crossref] [Google Scholar]
  37. Byerly MS, Blackshaw S. 2009. Vertebrate retina and hypothalamus development. Syst. Biol. Med. 1:3380–89 https://doi.org/10.1002/wsbm.22
    [Crossref] [Google Scholar]
  38. Calvanese V, Lara E, Suárez-Álvarez B, Abu Dawud R, Vázquez-Chantada M et al. 2010. Sirtuin 1 regulation of developmental genes during differentiation of stem cells. PNAS 107:3113736–41 https://doi.org/10.1073/pnas.1001399107
    [Crossref] [Google Scholar]
  39. Cao Q, Zhao X, Bai J, Gery S, Sun H et al. 2017. Circadian clock cryptochrome proteins regulate autoimmunity. PNAS 114:4712548–53 https://doi.org/10.1073/pnas.1619119114
    [Crossref] [Google Scholar]
  40. Carey BW, Finley LWS, Cross JR, Allis CD, Thompson CB 2015. Intracellular α-ketoglutarate maintains the pluripotency of embryonic stem cells. Nature 518:7539413–16 https://doi.org/10.1038/nature13981
    [Crossref] [Google Scholar]
  41. Carmel R, Jacobsen DW. 2011. Homocysteine in Health and Disease New York: Cambridge Univ. Press
  42. Carmona-Alcocer V, Abel JH, Sun TC, Petzold LR, Doyle FJ III et al. 2018. Ontogeny of circadian rhythms and synchrony in the suprachiasmatic nucleus. J. Neurosci. 38:61326–34 https://doi.org/10.1523/jneurosci.2006-17.2017
    [Crossref] [Google Scholar]
  43. Carmona‐Alcocer V, Rohr KE, Joye DAM, Evans JA 2020. Circuit development in the master clock network of mammals. Eur. J. Neurosci. 51:182–108 https://doi.org/10.1111/ejn.14259
    [Crossref] [Google Scholar]
  44. Cartwright P, McLean C, Sheppard A, Rivett D, Jones K, Dalton S 2005. LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 132:5885–96 https://doi.org/10.1242/dev.01670
    [Crossref] [Google Scholar]
  45. Casey T, Crodian J, Suárez-Trujillo A, Erickson E, Weldon B et al. 2016. CLOCK regulates mammary epithelial cell growth and differentiation. Regul. Integr. Comp. Physiol. 311:6R1125–34 https://doi.org/10.1152/ajpregu.00032.2016
    [Crossref] [Google Scholar]
  46. Cela O, Scrima R, Pazienza V, Merla G, Benegiamo G et al. 2016. Clock genes-dependent acetylation of Complex I sets rhythmic activity of mitochondrial OxPhos. Biochim. Biophys. Acta Mol. Cell Res. 1863:4596–606 https://doi.org/10.1016/j.bbamcr.2015.12.018
    [Crossref] [Google Scholar]
  47. Cepko C. 2014. Intrinsically different retinal progenitor cells produce specific types of progeny. Nat. Rev. Neurosci. 15:9615–27 https://doi.org/10.1038/nrn3767
    [Crossref] [Google Scholar]
  48. Cha Y, Han M-J, Cha H-J, Zoldan J, Burkart A et al. 2017. Metabolic control of primed human pluripotent stem cell fate and function by the MiR-200c-SIRT2 axis. Nat. Cell Biol. 19:5445–56 https://doi.org/10.1038/ncb3517
    [Crossref] [Google Scholar]
  49. Chaker Z, George C, Petrovska M, Caron J-B, Lacube P et al. 2016. Hypothalamic neurogenesis persists in the aging brain and is controlled by energy-sensing IGF-I pathway. Neurobiol. Aging 41:64–72 https://doi.org/10.1016/j.neurobiolaging.2016.02.008
    [Crossref] [Google Scholar]
  50. Chen Y, Xu X, Tan Z, Ye C, Zhao Q, Chen Y 2012. Age-related BMAL1 change affects mouse bone marrow stromal cell proliferation and osteo-differentiation potential. Arch. Med. Sci. 8:130–38 https://doi.org/10.5114/aoms.2012.27277
    [Crossref] [Google Scholar]
  51. Chiou Y-Y, Yang Y, Rashid N, Ye R, Selby CP, Sancar A 2016. Mammalian period represses and de-represses transcription by displacing CLOCK-BMAL1 from promoters in a Cryptochrome-dependent manner. PNAS 113:41E6072–79 https://doi.org/10.1073/pnas.1612917113
    [Crossref] [Google Scholar]
  52. Clark RH, Korst DR. 1969. Circadian periodicity of bone marrow mitotic activity and reticulocyte counts in rats and mice. Science 166:3902236–37 https://doi.org/10.1126/science.166.3902.236
    [Crossref] [Google Scholar]
  53. Clevers H, Loh KM, Nusse R 2014. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346:62051248012 https://doi.org/10.1126/science.1248012
    [Crossref] [Google Scholar]
  54. Costa MJ, So AY-L, Kaasik K, Krueger KC, Pillsbury ML et al. 2011. Circadian rhythm gene Period 3 is an inhibitor of the adipocyte cell fate. J. Biol. Chem. 286:119063–70 https://doi.org/10.1074/jbc.m110.164558
    [Crossref] [Google Scholar]
  55. Curtis AM, Seo S, Westgate EJ, Rudic RD, Smyth EM et al. 2004. Histone acetyltransferase-dependent chromatin remodeling and the vascular clock. J. Biol. Chem. 279:87091–97 https://doi.org/10.1074/jbc.m311973200
    [Crossref] [Google Scholar]
  56. Das AV, Mallya KB, Zhao X, Ahmad F, Bhattacharya S et al. 2006. Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev. Biol. 299:1283–302 https://doi.org/10.1016/j.ydbio.2006.07.029
    [Crossref] [Google Scholar]
  57. Das G, Clark AM, Levine EM 2012. Cyclin D1 inactivation extends proliferation and alters histogenesis in the postnatal mouse retina. Dev. Dyn. 241:5941–52 https://doi.org/10.1002/dvdy.23782
    [Crossref] [Google Scholar]
  58. DeBruyne JP, Baggs JE, Sato TK, Hogenesch JB 2015. Ubiquitin ligase Siah2 regulates RevErbα degradation and the mammalian circadian clock. PNAS 112:4012420–25 https://doi.org/10.1073/pnas.1501204112
    [Crossref] [Google Scholar]
  59. Diano S, Horvath TL. 2012. Mitochondrial uncoupling protein 2 (UCP2) in glucose and lipid metabolism. Trends Mol. Med. 18:152–58 https://doi.org/10.1016/j.molmed.2011.08.003
    [Crossref] [Google Scholar]
  60. Ding L, Morrison SJ. 2013. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495:7440231–35 https://doi.org/10.1038/nature11885
    [Crossref] [Google Scholar]
  61. DiTacchio L, Le HD, Vollmers C, Hatori M, Witcher M et al. 2011. Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 333:60511881–85 https://doi.org/10.1126/science.1206022
    [Crossref] [Google Scholar]
  62. Dolatshad H, Cary AJ, Davis FC 2010. Differential expression of the circadian clock in maternal and embryonic tissues of mice. PLOS ONE 5:3e9855 https://doi.org/10.1371/journal.pone.0009855
    [Crossref] [Google Scholar]
  63. Draijer S, Chaves I, Hoekman MFM 2019. The circadian clock in adult neural stem cell maintenance. Prog. Neurobiol. 173:41–53 https://doi.org/10.1016/j.pneurobio.2018.05.007
    [Crossref] [Google Scholar]
  64. Duan L, Peng C-Y, Pan L, Kessler JA 2015. Human pluripotent stem cell-derived radial glia recapitulate developmental events and provide real-time access to cortical neurons and astrocytes. Transl. Med. 4:5437–47 https://doi.org/10.5966/sctm.2014-0137
    [Crossref] [Google Scholar]
  65. Duong HA, Robles MS, Knutti D, Weitz CJ 2011. A molecular mechanism for circadian clock negative feedback. Science 332:60361436–39 https://doi.org/10.1126/science.1196766
    [Crossref] [Google Scholar]
  66. El Cheikh R, Bernard S, El Khatib N 2014. Modeling circadian clock–cell cycle interaction effects on cell population growth rates. J. Theor. Biol. 363:318–31 https://doi.org/10.1016/j.jtbi.2014.08.008
    [Crossref] [Google Scholar]
  67. Encinas JM, Michurina TV, Peunova N, Park J-H, Tordo J et al. 2011. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8:5566–79 https://doi.org/10.1016/j.stem.2011.03.010
    [Crossref] [Google Scholar]
  68. Engelen E, Janssens RC, Yagita K, Smits VAJ, van der Horst GTJ, Tamanini F 2013. Mammalian TIMELESS is involved in period determination and DNA damage-dependent phase advancing of the circadian clock. PLOS ONE 8:2e56623 https://doi.org/10.1371/journal.pone.0056623
    [Crossref] [Google Scholar]
  69. Etchegaray J-P, Lee C, Wade PA, Reppert SM 2003. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421:6919177–82 https://doi.org/10.1038/nature01314
    [Crossref] [Google Scholar]
  70. Etchegaray J-P, Yang X, DeBruyne JP, Peters AHFM, Weaver DR et al. 2006. The polycomb group protein EZH2 is required for mammalian circadian clock function. J. Biol. Chem. 281:3021209–15 https://doi.org/10.1074/jbc.m603722200
    [Crossref] [Google Scholar]
  71. Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:5819154–56 https://doi.org/10.1038/292154a0
    [Crossref] [Google Scholar]
  72. Fahrenkrug J, Georg B, Hannibal J, Hindersson P, Gräs S 2006. Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology 147:83769–76 https://doi.org/10.1210/en.2006-0305
    [Crossref] [Google Scholar]
  73. Fan SM-Y, Chang Y-T, Chen C-L, Wang W-H, Pan M-K et al. 2018. External light activates hair follicle stem cells through eyes via an IpRGC–SCN–sympathetic neural pathway. PNAS 115:29E6880–89 https://doi.org/10.1073/pnas.1719548115 Corrigendum. 2018 PNAS 115:51E12121 https://doi.org/10.1073/pnas.1819671116
    [Crossref] [Google Scholar]
  74. Farshadi E, Yan J, Leclere P, Goldbeter A, Chaves I, van der Horst GTJ 2019. The positive circadian regulators CLOCK and BMAL1 control G2/M cell cycle transition through Cyclin B1. Cell Cycle 18:116–33 https://doi.org/10.1080/15384101.2018.1558638
    [Crossref] [Google Scholar]
  75. Feillet C, Krusche P, Tamanini F, Janssens RC, Downey MJ et al. 2014. Phase locking and multiple oscillating attractors for the coupled mammalian clock and cell cycle. PNAS 111:279828–33 https://doi.org/10.1073/pnas.1320474111
    [Crossref] [Google Scholar]
  76. Ferreira MS, Alves PC, Callahan CM, Giska I, Farelo L et al. 2020. Transcriptomic regulation of seasonal coat color change in hares. Ecol. Evol. 10:31180–92 https://doi.org/10.1002/ece3.5956
    [Crossref] [Google Scholar]
  77. Fischer B, Bavister BD. 1993. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. Reproduction 99:2673–79 https://doi.org/10.1530/jrf.0.0990673
    [Crossref] [Google Scholar]
  78. Fu L, Kettner NM. 2013. The circadian clock in cancer development and therapy. Progress in Molecular Biology and Translational Science, Vol. 119: Chronobiology: Biological Timing in Health and Disease, ed. MU Gillette 221–82 Oxford, UK: Acad. Press https://doi.org/10.1016/b978-0-12-396971-2.00009-9
    [Crossref] [Google Scholar]
  79. Fu L, Patel MS, Bradley A, Wagner EF, Karsenty G 2005. The molecular clock mediates leptin-regulated bone formation. Cell 122:5803–15 https://doi.org/10.1016/j.cell.2005.06.028
    [Crossref] [Google Scholar]
  80. Fu L, Pelicano H, Liu J, Huang P, Lee CC 2002. The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111:141–50 https://doi.org/10.1016/s0092-8674(02)00961-3
    [Crossref] [Google Scholar]
  81. Fustin J-M, Doi M, Yamaguchi Y, Hida H, Nishimura S et al. 2013. RNA-methylation-dependent RNA processing controls the speed of the circadian clock. Cell 155:4793–806 https://doi.org/10.1016/j.cell.2013.10.026
    [Crossref] [Google Scholar]
  82. Gallardo A, Molina A, Asenjo HG, Martorell-Marugán J, Montes R et al. 2020. The molecular clock protein Bmal1 regulates cell differentiation in mouse embryonic stem cells. Life Sci. Alliance 3:5e201900535 https://doi.org/10.26508/lsa.201900535
    [Crossref] [Google Scholar]
  83. García-García A, Korn C, García-Fernández M, Domingues O, Villadiego J et al. 2019. Dual cholinergic signals regulate daily migration of hematopoietic stem cells and leukocytes. Blood 133:3224–36 https://doi.org/10.1182/blood-2018-08-867648
    [Crossref] [Google Scholar]
  84. Garrett RW, Gasiewicz TA. 2006. The aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin alters the circadian rhythms, quiescence, and expression of clock genes in murine hematopoietic stem and progenitor cells. Mol. Pharmacol. 69:62076–83 https://doi.org/10.1124/mol.105.021006
    [Crossref] [Google Scholar]
  85. Gérard C, Goldbeter A. 2012. Entrainment of the mammalian cell cycle by the circadian clock: modeling two coupled cellular rhythms. PLOS Comput. Biol. 8:5e1002516 https://doi.org/10.1371/journal.pcbi.1002516
    [Crossref] [Google Scholar]
  86. Geyfman M, Kumar V, Lui Q, Ruiz R, Gordon W et al. 2012. Brain and muscle Arnt-like protein-1 (BMAL1) controls circadian cell proliferation and susceptibility to UVB-induced DNA damage in the epidermis. PNAS 109:2911758–63 https://doi.org/10.1073/pnas.1209592109
    [Crossref] [Google Scholar]
  87. Gilhooley MJ, Pinnock SB, Herbert J 2011. Rhythmic expression of per1 in the dentate gyrus is suppressed by corticosterone: implications for neurogenesis. Neurosci. Lett. 489:3177–81 https://doi.org/10.1016/j.neulet.2010.12.011
    [Crossref] [Google Scholar]
  88. Golan K, Kumari A, Kollet O, Khatib-Massalha E, Subramanian MD et al. 2018. Daily onset of light and darkness differentially controls hematopoietic stem cell differentiation and maintenance. Cell Stem Cell 23:4572–85.e7 https://doi.org/10.1016/j.stem.2018.08.002
    [Crossref] [Google Scholar]
  89. Gréchez-Cassiau A, Rayet B, Guillaumond F, Teboul M, Delaunay F 2008. The circadian clock component BMAL1 is a critical regulator of p21WAF1/CIP1 expression and hepatocyte proliferation. J. Biol. Chem. 283:84535–42 https://doi.org/10.1074/jbc.m705576200
    [Crossref] [Google Scholar]
  90. Grunz H, Tacke L. 1989. Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. Cell Differ. Dev. 28:3211–17 https://doi.org/10.1016/0922-3371(89)90006-3
    [Crossref] [Google Scholar]
  91. Gu W, Gaeta X, Sahakyan A, Chan AB, Hong CS et al. 2016. Glycolytic metabolism plays a functional role in regulating human pluripotent stem cell state. Cell Stem Cell 19:4476–90 https://doi.org/10.1016/j.stem.2016.08.008
    [Crossref] [Google Scholar]
  92. Guilding C, Hughes ATL, Brown TM, Namvar S, Piggins HD 2009. A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus. Mol. Brain 2:128 https://doi.org/10.1186/1756-6606-2-28
    [Crossref] [Google Scholar]
  93. Guo B, Chatterjee S, Li L, Kim JM, Lee J et al. 2012. The clock gene, brain and muscle Arnt‐like 1, regulates adipogenesis via Wnt signaling pathway. FASEB J 26:83453–63 https://doi.org/10.1096/fj.12-205781
    [Crossref] [Google Scholar]
  94. Gupta A, Hepp B, Khammash M 2016. Noise induces the population-level entrainment of incoherent, uncoupled intracellular oscillators. Cell Syst 3:6521–31.e13 https://doi.org/10.1016/j.cels.2016.10.006
    [Crossref] [Google Scholar]
  95. Haan N, Goodman T, Najdi-Samiei A, Stratford CM, Rice R et al. 2013. Fgf10-expressing tanycytes add new neurons to the appetite/energy-balance regulating centers of the postnatal and adult hypothalamus. J. Neurosci. 33:146170–80 https://doi.org/10.1523/jneurosci.2437-12.2013
    [Crossref] [Google Scholar]
  96. Hallows WC, Lee S, Denu JM 2006. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. PNAS 103:2710230–35 https://doi.org/10.1073/pnas.0604392103
    [Crossref] [Google Scholar]
  97. Han Y, Ishibashi S, Iglesias-Gonzalez J, Chen Y, Love NR, Amaya E 2018. Ca2+-induced mitochondrial ROS regulate the early embryonic cell cycle. Cell Rep 22:1218–31 https://doi.org/10.1016/j.celrep.2017.12.042
    [Crossref] [Google Scholar]
  98. Hardman JA, Tobin DJ, Haslam IS, Farjo N, Farjo B et al. 2015. The peripheral clock regulates human pigmentation. J. Investig. Dermatol. 135:41053–64 https://doi.org/10.1038/jid.2014.442
    [Crossref] [Google Scholar]
  99. Hawkins KE, Joy S, Delhove JMKM, Kotiadis VN, Fernandez E et al. 2016. NRF2 orchestrates the metabolic shift during induced pluripotent stem cell reprogramming. Cell Rep 14:81883–91 https://doi.org/10.1016/j.celrep.2016.02.003
    [Crossref] [Google Scholar]
  100. He P-J, Hirata M, Yamauchi N, Hashimoto S, Hattori M 2007. Gonadotropic regulation of circadian clockwork in rat granulosa cells. Mol. Cell. Biochem. 302:111–18 https://doi.org/10.1007/s11010-007-9432-7
    [Crossref] [Google Scholar]
  101. He Y, Chen Y, Zhao Q, Tan Z 2013. Roles of brain and muscle ARNT-like 1 and Wnt antagonist Dkk1 during osteogenesis of bone marrow stromal cells. Cell Prolif 46:6644–53 https://doi.org/10.1111/cpr.12075
    [Crossref] [Google Scholar]
  102. He Y, Lin F, Chen Y, Tan Z, Bai D, Zhao Q 2015. Overexpression of the circadian clock gene Rev-erbα; affects murine bone mesenchymal stem cell proliferation and osteogenesis. Stem Cells Dev 24:101194–204 https://doi.org/10.1089/scd.2014.0437
    [Crossref] [Google Scholar]
  103. Herzog ED, Grace MS, Harrer C, Williamson J, Shinohara K, Block GD 2000. The role of Clock in the developmental expression of neuropeptides in the suprachiasmatic nucleus. J. Comp. Neurol. 424:186–98 https://doi.org/10.1002/1096-9861(20000814)424:1<86::aid-cne7>3.0.co;2-w
    [Crossref] [Google Scholar]
  104. Hirayama J, Sahar S, Grimaldi B, Tamaru T, Takamatsu K et al. 2007. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 450:71721086–90 https://doi.org/10.1038/nature06394
    [Crossref] [Google Scholar]
  105. Houghton FD, Thompson JG, Kennedy CJ, Leese HJ 1996. Oxygen consumption and energy metabolism of the early mouse embryo. Mol. Reprod. Dev. 44:4476–85 https://doi.org/10.1002/(sici)1098-2795(199608)44:4<476::aid-mrd7>3.0.co;2-i
    [Crossref] [Google Scholar]
  106. Hsu Y-C, Li L, Fuchs E 2014. Emerging interactions between skin stem cells and their niches. Nat. Med. 20:8847–56 https://doi.org/10.1038/nm.3643
    [Crossref] [Google Scholar]
  107. Huang T‐S, Grodeland G, Sleire L, Wang MY, Kvalheim G, Laerum OD 2009. Induction of circadian rhythm in cultured human mesenchymal stem cells by serum shock and cAMP analogs in vitro. Chronobiol. Int. 26:2242–57 https://doi.org/10.1080/07420520902766025
    [Crossref] [Google Scholar]
  108. Huang Z, Wei H, Wang X, Xiao J, Li Z et al. 2020. Icariin promotes osteogenic differentiation of BMSCs by upregulating BMAL1 expression via BMP signaling. Mol. Med. Rep. 21:31590–96 https://doi.org/10.3892/mmr.2020.10954
    [Crossref] [Google Scholar]
  109. Ieyasu A, Tajima Y, Shimba S, Nakauchi H, Yamazaki S 2014. Clock gene Bmal1 is dispensable for intrinsic properties of murine hematopoietic stem cells. J. Negat. Results BioMed. 13:4 https://doi.org/10.1186/1477-5751-13-4
    [Crossref] [Google Scholar]
  110. Inada Y, Uchida H, Umemura Y, Nakamura W, Sakai T et al. 2014. Cell and tissue-autonomous development of the circadian clock in mouse embryos. FEBS Lett 588:3459–65 https://doi.org/10.1016/j.febslet.2013.12.007
    [Crossref] [Google Scholar]
  111. Isagawa T, Nagae G, Shiraki N, Fujita T, Sato N et al. 2011. DNA methylation profiling of embryonic stem cell differentiation into the three germ layers. PLOS ONE 6:10e26052 https://doi.org/10.1371/journal.pone.0026052
    [Crossref] [Google Scholar]
  112. Isern J, García-García A, Martín AM, Arranz L, Martín-Pérez D et al. 2014. The neural crest is a source of mesenchymal stem cells with specialized hematopoietic stem cell niche function. eLife 3:e03696 https://doi.org/10.7554/elife.03696
    [Crossref] [Google Scholar]
  113. Ito M, Cotsarelis G, Kizawa K, Hamada K 2004. Hair follicle stem cells in the lower bulge form the secondary germ, a biochemically distinct but functionally equivalent progenitor cell population, at the termination of catagen. Differentiation 72:9–10548–57 https://doi.org/10.1111/j.1432-0436.2004.07209008.x
    [Crossref] [Google Scholar]
  114. Ito M, Liu Y, Yang Z, Nguyen J, Liang F et al. 2005. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat. Med. 11:121351–54 https://doi.org/10.1038/nm1328
    [Crossref] [Google Scholar]
  115. Janich P, Pascual G, Merlos-Suárez A, Batlle E, Ripperger J et al. 2011. The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 480:7376209–14 https://doi.org/10.1038/nature10649
    [Crossref] [Google Scholar]
  116. Janich P, Toufighi K, Solanas G, Luis NM, Minkwitz S et al. 2013. Human epidermal stem cell function is regulated by circadian oscillations. Cell Stem Cell 13:6745–53 https://doi.org/10.1016/j.stem.2013.09.004
    [Crossref] [Google Scholar]
  117. Ji A-R, Ku S-Y, Cho MS, Kim YY, Kim YJ et al. 2010. Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage. Exp. Mol. Med. 42:317586 https://doi.org/10.3858/emm.2010.42.3.018
    [Crossref] [Google Scholar]
  118. Kaasik K, Kivimäe S, Allen JJ, Chalkley RJ, Huang Y et al. 2013. Glucose sensor O-GlcNAcylation coordinates with phosphorylation to regulate circadian clock. Cell Metab 17:2291–302 https://doi.org/10.1016/j.cmet.2012.12.017
    [Crossref] [Google Scholar]
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