Metaboloepigenetics: The emerging network in stem cell homeostasis regulation

Current Stem Cell Research and Therapy

Volumn 11, Issue 4, 2016, Pages 352-369

  Avitabile, Daniele ^a   Magenta, Alessandra ^b   Lauri, Andrea ^a   Gambini, Elisa ^a   Spaltro, Gabriella ^a   Vinci, Maria Cristina ^a  

^a CENTRO CARDIOLOGICO MONZINO   (Italy)

^b LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Circadian rhythms; Epigenetics; Metabolism; MicroRNAs; Nutrition; Stem cells

Indexed keywords

SMALL NUCLEOLAR RNA; CHROMATIN;

ADULT STEM CELL; ARTICLE; CELL DIFFERENTIATION; CELL METABOLISM; CIRCADIAN RHYTHM; DEACETYLATION; DISEASE COURSE; DNA MODIFICATION; ENERGY METABOLISM; EPIGENETICS; GENE EXPRESSION; GENETIC REGULATION; HISTONE ACETYLATION; HISTONE DEMETHYLATION; HISTONE METHYLATION; HOMEOSTASIS; HUMAN; METABOLOEPIGENETICS; METABOLOMICS; MITOCHONDRION; MOLECULAR MECHANICS; MULTIPOTENT STEM CELL; NONHUMAN; NUTRITION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL; STEM CELL SELF-RENEWAL; TRANSCRIPTION REGULATION; CHROMATIN; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM;

CELL DIFFERENTIATION; CHROMATIN; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; METABOLOMICS; STEM CELLS;

EID: 84964058436     PISSN: 1574888X     EISSN: None     Source Type: Journal    
DOI: 10.2174/1574888X11666151203223839     Document Type: Article

References (266)

1. Weissman IL, Anderson DJ, Gage F. Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu Rev Cell Dev Biol 2001; 17: 387-403.
2. He S, Nakada D, Morrison SJ. Mechanisms of stem cell selfrenewal. Annu Rev Cell Dev Biol 2009; 25: 377-406.
3. Ito K, Suda T. Metabolic requirements for the maintenance of selfrenewing stem cells. Nat Rev Mol Cell Biol 2014; 15: 243-56.
4. Shyh-Chang N, Daley GQ, Cantley LC. Stem cell metabolism in tissue development and aging. Development 2013; 140: 2535-47.
5. Feinberg AP. Phenotypic plasticity and the epigenetics of human disease. Nature 2007; 447: 433-40.
6. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403: 41-5.
7. Wolffe AP, Guschin D. Review: chromatin structural features and targets that regulate transcription. J Struct Biol 2000; 129: 102-22.
8. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007; 447: 407-12.
9. Vinci MC, Polvani G, Pesce M. Epigenetic programming and risk: the birthplace of cardiovascular disease? Stem Cell Rev 2013; 9: 241-53.
10. Ladurner AG. Rheostat control of gene expression by metabolites. Mol Cell 2006; 24: 1-11.
11. Shi Y. Metabolic enzymes and coenzymes in transcription--a direct link between metabolism and transcription? Trends Genet 2004; 20: 445-52.
12. Lu C, Thompson CB. Metabolic regulation of epigenetics. Cell Metab 2012; 16: 9-17.
13. Racey LA, Byvoet P. Histone acetyltransferase in chromatin. Evidence for in vitro enzymatic transfer of acetate from acetylcoenzyme A to histones. Exp Cell Res 1971; 64: 366-70.
14. Cai L, Sutter BM, Li B, Tu BP. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol Cell 2011; 42: 426-37.
15. Rardin MJ, Newman JC, Held JM, et al. Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of SIRT3 in metabolic pathways. Proc Natl Acad Sci USA 2013; 110: 6601-6.
16. Hebert AS, Dittenhafer-Reed KE, Yu W, et al. Calorie restriction and SIRT3 trigger global reprogramming of the mitochondrial protein acetylome. Mol Cell 2013; 49: 186-99.
17. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui T V, Cross JR, Thompson CB. ATP-citrate lyase links cellular metabolism to histone acetylation. Science (80-) 2009; 324: 1076-80.
18. Bracha AL, Ramanathan A, Huang S, Ingber DE, Schreiber SL. Carbon metabolism-mediated myogenic differentiation. Nat Chem Biol 2010; 6: 202-4.
19. Imai S, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 2000; 403: 795-800.
20. Kawahara TL, Michishita E, Adler AS, et al. SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 2009; 136: 62-74.
21. Sassone-Corsi P. Minireview: NAD+, a circadian metabolite with an epigenetic twist. Endocrinology 2012; 153: 1-5.
22. Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P. Circadian control of the NAD+ salvage pathway by CLOCKSIRT1. Science 2009; 324: 654-7.
23. Murayama A, Ohmori K, Fujimura A, et al. Epigenetic control of rDNA loci in response to intracellular energy status. Cell 2008; 133: 627-39.
24. Mostoslavsky R, Chua KF, Lombard DB, et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 2006; 124: 315-29.
25. Naiman S, Kanfi Y, Cohen HY. Sirtuins as regulators of mammalian aging. Aging (Albany NY) 2012; 4: 521-2.
26. Jiang T, Zhou X, Taghizadeh K, Dong M, Dedon PC. Nformylation of lysine in histone proteins as a secondary modification arising from oxidative DNA damage. Proc Natl Acad Sci USA 2007; 104: 60-5.
27. Wisniewski JR, Zougman A, Mann M. Nepsilon-formylation of lysine is a widespread post-translational modification of nuclear proteins occurring at residues involved in regulation of chromatin function. Nucleic Acids Res 2008; 36: 570-7.
28. Tan M, Luo H, Lee S, et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 2011; 146: 1016-28.
29. Peng C, Lu Z, Xie Z, et al. The first identification of lysine malonylation substrates and its regulatory enzyme. Mol Cell Proteomics 2011; 10: M111.012658.
30. Zhang Z, Tan M, Xie Z, Dai L, Chen Y, Zhao Y. Identification of lysine succinylation as a new post-translational modification. Nat Chem Biol 2011; 7: 58-63.
31. Chen Y, Sprung R, Tang Y, et al. Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol Cell Proteomics 2007; 6: 812-9.
32. Dai L, Peng C, Montellier E, et al. Lysine 2- hydroxyisobutyrylation is a widely distributed active histone mark. Nat Chem Biol 2014; 10: 365-70.
33. Montellier E, Rousseaux S, Zhao Y, Khochbin S. Histone crotonylation specifically marks the haploid male germ cell gene expression program: post-meiotic male-specific gene expression. Bioessays 2012; 34: 187-93.
34. Berndsen CE, Denu JM. Catalysis and substrate selection by histone/protein lysine acetyltransferases. Curr Opin Struct Biol 2008; 18: 682-9.
35. Poirier LA, Wise CK, Delongchamp RR, Sinha R. Blood determinations of S-adenosylmethionine, S-adenosylhomocysteine, and homocysteine: correlations with diet. Cancer Epidemiol Biomarkers Prev 2001; 10: 649-55.
36. Anderson OS, Sant KE, Dolinoy DC. Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem 2012; 23: 853-9.
37. Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 2011; 13: 97-109.
38. Kim YI. Nutritional epigenetics: impact of folate deficiency on DNA methylation and colon cancer susceptibility. J Nutr 2005; 135: 2703-9.
39. Shi Y, Lan F, Matson C, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004; 119: 941-53.
40. He YF, Li BZ, Li Z, et al. Tet-mediated formation of 5- carboxylcytosine and its excision by TDG in mammalian DNA. Science (80-) 2011; 333: 1303-7.
41. Xiao M, Yang H, Xu W, et al. Inhibition of alpha-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors. Genes Dev 2012; 26: 1326-38.
42. Carey BW, Finley LW, Cross JR, Allis CD, Thompson CB. Intracellular alpha-ketoglutarate maintains the pluripotency of embryonic stem cells. Nature 2015; 518: 413-6.
43. Moran-Crusio K, Reavie L, Shih A, et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 2011; 20: 11-24.
44. Quivoron C, Couronne L, Della Valle V, et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 2011; 20: 25-38.
45. Kirchner H, Osler ME, Krook A, Zierath JR. Epigenetic flexibility in metabolic regulation: disease cause and prevention? Trends Cell Biol 2013; 23: 203-9.
46. Villeneuve LM, Reddy MA, Lanting LL, Wang M, Meng L, Natarajan R. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci USA 2008; 105: 9047-52.
47. Lumey LH, Stein AD, Kahn HS, et al. Cohort profile: the Dutch Hunger Winter families study. Int J Epidemiol 2007; 36: 1196-204.
48. Patti ME. Intergenerational programming of metabolic disease: evidence from human populations and experimental animal models. Cell Mol Life Sci 2013; 70: 1597-608.
49. Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 1998; 12: 949-57.
50. Sinclair KD, Allegrucci C, Singh R, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA 2007; 104: 19351-6.
51. Sinclair KD, Lea RG, Rees WD, Young LE. The developmental origins of health and disease: current theories and epigenetic mechanisms. Soc Reprod Fertil Suppl 2007; 64: 425-43.
52. Kaati G, Bygren LO, Pembrey M, Sjostrom M. Transgenerational response to nutrition, early life circumstances and longevity. Eur J Hum Genet 2007; 15: 784-90.
53. Lomba A, Martinez JA, Garcia-Diaz DF, et al. Weight gain induced by an isocaloric pair-fed high fat diet: A nutriepigenetic study on FASN and NDUFB6 gene promoters. Mol Genet Metab 2010; 101: 273-8.
54. Ceccarelli V, Racanicchi S, Martelli MP, et al. Eicosapentaenoic acid demethylates a single CpG that mediates expression of tumor suppressor CCAAT/enhancer-binding protein delta in U937 leukemia cells. J Biol Chem 2011; 286: 27092-102.
55. Kiec-Wilk B, Sliwa A, Mikolajczyk M, Malecki MT, Mathers JC. The CpG island methylation regulated expression of endothelial proangiogenic genes in response to beta-carotene and arachidonic acid. Nutr Cancer 2011; 63: 1053-63.
56. Ku CS, Rasmussen HE, Park Y, Jesch ED, Lee J. Unsaturated fatty acids repress the expression of ATP-binding cassette transporter A1 in HepG2 and FHs 74 Int cells. Nutr Res 2011; 31: 278-85.
57. Cordero P, Gomez-Uriz AM, Campion J, Milagro FI, Martinez JA. Dietary supplementation with methyl donors reduces fatty liver and modifies the fatty acid synthase DNA methylation profile in rats fed an obesogenic diet. Genes Nutr 2013; 8: 105-13.
58. Wang J, Wu Z, Li D, et al. Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal 2012; 17: 282-301.
59. Adams SH. Emerging perspectives on essential amino acid metabolism in obesity and the insulin-resistant state. Adv Nutr 2011; 2: 445-56.
60. Pirola L, Balcerczyk A, Okabe J, El-Osta A. Epigenetic phenomena linked to diabetic complications. Nat Rev Endocrinol 2010; 6: 665-75.
61. El-Osta A, Brasacchio D, Yao D, et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008; 205: 2409-17.
62. Brasacchio D, Okabe J, Tikellis C, et al. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes 2009; 58: 1229-36.
63. Pettitt DJ, Baird HR, Aleck KA, Bennett PH, Knowler WC. Excessive obesity in offspring of Pima Indian women with diabetes during pregnancy. N Engl J Med 1983; 308: 242-5.
64. Dabelea D, Hanson RL, Lindsay RS, et al. Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes 2000; 49: 2208-11.
65. Stein AD, Kahn HS, Rundle A, Zybert PA, van der Pal-de Bruin K, Lumey LH. Anthropometric measures in middle age after exposure to famine during gestation: evidence from the Dutch famine. Am J Clin Nutr 2007; 85: 869-76.
66. Vinci MC. Sensing the Environment: Epigenetic Regulation of Gene Expression. J Physic Chem Biophys 2012; S3: 001.
67. Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 2008; 105: 17046-9.
68. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010; 467: 963-6.
69. Zhang S, Rattanatray L, MacLaughlin SM, et al. Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring. FASEB J 2010; 24: 2772-82.
70. Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr 2008; 100: 278-82.
71. Zhou D, Pan YX. Gestational low protein diet selectively induces the amino acid response pathway target genes in the liver of offspring rats through transcription factor binding and histone modifications. Biochim Biophys Acta 2011; 1809: 549-56.
72. Howie GJ, Sloboda DM, Kamal T, Vickers MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol 2009; 587: 905-15.
73. Page KC, Malik RE, Ripple JA, Anday EK. Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to a high-fat diet in male offspring. Am J Physiol Regul Integr Comp Physiol 2009; 297: R1049-57.
74. Plagemann A, Harder T, Brunn M, et al. Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome. J Physiol 2009; 587: 4963-76.
75. Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 2010; 151: 4756-64.
76. White CL, Purpera MN, Morrison CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol 2009; 296: R1464-72.
77. Rooney K, Ozanne SE. Maternal over-nutrition and offspring obesity predisposition: targets for preventative interventions. Int J Obes 2011; 35: 883-90.
78. Harris H. A long view of fashions in cancer research. Bioessays 2005; 27: 833-8.
79. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 2011; 27: 441-64.
80. Balaban RS. Regulation of oxidative phosphorylation in the mammalian cell. Am J Physiol 1990; 258: C377-89.
81. Guppy M, Greiner E, Brand K. The role of the Crabtree effect and an endogenous fuel in the energy metabolism of resting and proliferating thymocytes. Eur J Biochem 1993; 212: 95-9.
82. Kim JW, Dang C V. Cancer’s molecular sweet tooth and the Warburg effect. Cancer Res 2006; 66: 8927-30.
83. Barbehenn EK, Wales RG, Lowry OH. Measurement of metabolites in single preimplantation embryos; a new means to study metabolic control in early embryos. J Embryol Exp Morphol 1978; 43: 29-46.
84. Pantaleon M, Kaye PL. Glucose transporters in preimplantation development. Rev Reprod 1998; 3: 77-81.
85. Varum S, Rodrigues AS, Moura MB, et al. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 2011; 6: e20914.
86. Zhang J, Khvorostov I, Hong JS, et al. UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J 2011; 30: 4860-73.
87. West JD, Flockhart JH, Peters J, Ball ST. Death of mouse embryos that lack a functional gene for glucose phosphate isomerase. Genet Res 1990; 56: 223-36.
88. Shyh-Chang N, Zheng Y, Locasale JW, Cantley LC. Human pluripotent stem cells decouple respiration from energy production. EMBO J 2011; 30: 4851-2.
89. Facucho-Oliveira JM, St John JC. The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev 2009; 5: 140-58.
90. Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A, Terzic A. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pr Cardiovasc Med 2007; 4 Suppl 1: S60-7.
91. Cho YM, Kwon S, Pak YK, et al. Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun 2006; 348: 1472-8.
92. Facucho-Oliveira JM, Alderson J, Spikings EC, Egginton S, St John JC. Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J Cell Sci 2007; 120: 4025-34.
93. Panopoulos AD, Yanes O, Ruiz S, et al. The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming. Cell Res 2012; 22: 168-77.
94. Prigione A, Fauler B, Lurz R, Lehrach H, Adjaye J. The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells 2010; 28: 721-33.
95. Folmes CD, Nelson TJ, Martinez-Fernandez A, et al. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 2011; 14: 264-71.
96. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science (80-) 2009; 324: 1029-33.
97. Manganelli G, Fico A, Masullo U, Pizzolongo F, Cimmino A, Filosa S. Modulation of the pentose phosphate pathway induces endodermal differentiation in embryonic stem cells. PLoS One 2012; 7: e29321.
98. Ozbudak EM, Tassy O, Pourquie O. Spatiotemporal compartmentalization of key physiological processes during muscle precursor differentiation. Proc Natl Acad Sci USA 2010; 107: 4224-9.
99. Yoshida Y, Takahashi K, Okita K, Ichisaka T, Yamanaka S. Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell 2009; 5: 237-41.
100. Zhu S, Li W, Zhou H, et al. Reprogramming of human primary somatic cells by OCT4 and chemical compounds. Cell Stem Cell 2010; 7: 651-5.
101. Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell 2012; 48: 612-26.
102. Yang W, Zheng Y, Xia Y, et al. ERK1/2-dependent phosphorylation and nuclear translocation of PKM2 promotes the Warburg effect. Nat Cell Biol 2012; 14: 1295-304.
103. Wang J, Alexander P, Wu L, Hammer R, Cleaver O, McKnight SL. Dependence of mouse embryonic stem cells on threonine catabolism. Science (80-) 2009; 325: 435-9.
104. Shyh-Chang N, Locasale JW, Lyssiotis CA, et al. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science (80-) 2013; 339: 222-6.
105. Alexander PB, Wang J, McKnight SL. Targeted killing of a mammalian cell based upon its specialized metabolic state. Proc Natl Acad Sci USA 2011; 108: 15828-33.
106. Yanes O, Clark J, Wong DM, et al. Metabolic oxidation regulates embryonic stem cell differentiation. Nat Chem Biol 2010; 6: 411-7.
107. Ito K, Carracedo A, Weiss D, et al. A PML-PPAR-delta pathway for fatty acid oxidation regulates hematopoietic stem cell maintenance. Nat Med 2012; 18: 1350-8.
108. Spencer JA, Ferraro F, Roussakis E, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 2014; 508: 269-73.
109. Nombela-Arrieta C, Pivarnik G, Winkel B, et al. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol 2013; 15: 533-43.
110. Lee KE, Simon MC. From stem cells to cancer stem cells: HIF takes the stage. Curr Opin Cell Biol 2012; 24: 232-5.
111. Eliasson P, Rehn M, Hammar P, et al. Hypoxia mediates low cellcycle activity and increases the proportion of long-termreconstituting hematopoietic stem cells during in vitro culture. Exp Hematol 2010; 38: 301-10 e2.
112. Covello KL, Kehler J, Yu H, et al. HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 2006; 20: 557-70.
113. Lum JJ, Bui T, Gruber M, et al. The transcription factor HIF-1alpha plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis. Genes Dev 2007; 21: 1037-49.
114. Firth JD, Ebert BL, Ratcliffe PJ. Hypoxic regulation of lactate dehydrogenase A. Interaction between hypoxia-inducible factor 1 and cAMP response elements. J Biol Chem 1995; 270: 21021-7.
115. Kim JW, Tchernyshyov I, Semenza GL, Dang C V. HIF-1- mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006; 3: 177-85.
116. Takubo K, Nagamatsu G, Kobayashi CI, et al. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 2013; 12: 49-61.
117. Tothova Z, Kollipara R, Huntly BJ, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007; 128: 325-39.
118. Ito K, Hirao A, Arai F, et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 2006; 12: 446-51.
119. Li TS, Marban E. Physiological levels of reactive oxygen species are required to maintain genomic stability in stem cells. Stem Cells 2010; 28: 1178-85.
120. Chaudhari P, Ye Z, Jang YY. Roles of reactive oxygen species in the fate of stem cells. Antioxid Redox Signal 2014; 20: 1881-90.
121. Ho PJ, Yen ML, Tang BC, Chen CT, Yen BL. H2O2 accumulation mediates differentiation capacity alteration, but not proliferative decline, in senescent human fetal mesenchymal stem cells. Antioxid Redox Signal 2013; 18: 1895-905.
122. Simsek T, Kocabas F, Zheng J, et al. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 2010; 7: 380-90.
123. Inoue S, Noda S, Kashima K, Nakada K, Hayashi J, Miyoshi H. Mitochondrial respiration defects modulate differentiation but not proliferation of hematopoietic stem and progenitor cells. FEBS Lett 2010; 584: 3402-9.
124. Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 2008; 26: 960-8.
125. Pattappa G, Heywood HK, de Bruijn JD, Lee DA. The metabolism of human mesenchymal stem cells during proliferation and differentiation. J Cell Physiol 2011; 226: 2562-70.
126. Pattappa G, Thorpe SD, Jegard NC, Heywood HK, de Bruijn JD, Lee DA. Continuous and uninterrupted oxygen tension influences the colony formation and oxidative metabolism of human mesenchymal stem cells. Tissue Eng Part C Methods 2013; 19: 68-79.
127. Kondoh H, Lleonart ME, Nakashima Y, et al. A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 2007; 9: 293-9.
128. Kelly RD, Rodda AE, Dickinson A, et al. Mitochondrial DNA haplotypes define gene expression patterns in pluripotent and differentiating embryonic stem cells. Stem Cells 2013; 31: 703-16.
129. St John JC, Ramalho-Santos J, Gray HL, et al. The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 2005; 7: 141-53.
130. Romero-Moya D, Bueno C, Montes R, et al. Cord blood-derived CD34+ hematopoietic cells with low mitochondrial mass are enriched in hematopoietic repopulating stem cell function. Haematologica 2013; 98: 1022-9.
131. Todd LR, Damin MN, Gomathinayagam R, Horn SR, Means AR, Sankar U. Growth factor erv1-like modulates Drp1 to preserve mitochondrial dynamics and function in mouse embryonic stem cells. Mol Biol Cell 2010; 21: 1225-36.
132. Lyu BN, Ismailov SB, Ismailov B, Lyu MB. Mitochondrial concept of leukemogenesis: key role of oxygen-peroxide effects. Theor Biol Med Model 2008; 5: 23.
133. Geiger H, de Haan G, Florian MC. The ageing haematopoietic stem cell compartment. Nat Rev Immunol 2013; 13: 376-89.
134. Morrison SJ, Wandycz AM, Akashi K, Globerson A, Weissman IL. The aging of hematopoietic stem cells. Nat Med 1996; 2: 1011-6.
135. Trifunovic A, Wredenberg A, Falkenberg M, et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 2004; 429: 417-23.
136. Norddahl GL, Pronk CJ, Wahlestedt M, et al. Accumulating mitochondrial DNA mutations drive premature hematopoietic aging phenotypes distinct from physiological stem cell aging. Cell Stem Cell 2011; 8: 499-510.
137. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010; 107: 1058-70.
138. Achilli A, Olivieri A, Pala M, et al. Mitochondrial DNA backgrounds might modulate diabetes complications rather than T2DM as a whole. PLoS One 2011; 6: e21029.
139. Hashizume O, Shimizu A, Yokota M, et al. Specific mitochondrial DNA mutation in mice regulates diabetes and lymphoma development. Proc Natl Acad Sci USA 2012; 109: 10528-33.
140. Shock LS, Thakkar P V, Peterson EJ, Moran RG, Taylor SM. DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proc Natl Acad Sci USA 2011; 108: 3630-5.
141. Bellizzi D, D’Aquila P, Scafone T, et al. The control region of mitochondrial DNA shows an unusual CpG and non-CpG methylation pattern. DNA Res 2013; 20: 537-47.
142. Pirola CJ, Gianotti TF, Burgueno AL, et al. Epigenetic modification of liver mitochondrial DNA is associated with histological severity of nonalcoholic fatty liver disease. Gut 2013; 62: 1356-63.
143. Byun HM, Panni T, Motta V, et al. Effects of airborne pollutants on mitochondrial DNA methylation. Part Fibre Toxicol 2013; 10: 18.
144. Sun Z, Terragni J, Borgaro JG, et al. High-resolution enzymatic mapping of genomic 5-hydroxymethylcytosine in mouse embryonic stem cells. Cell Rep 2013; 3: 567-76.
145. Liu Z, Chu G. Chronobiology in mammalian health. Mol Biol Rep 2013; 40: 2491-501.
146. Golombek DA, Casiraghi LP, Agostino PV, et al. The times they’re a-changing: effects of circadian desynchronization on physiology and disease. J Physiol Paris 2013; 107: 310-22.
147. Geyfman M, Andersen B. How the skin can tell time. J Invest Dermatol 2009; 129: 1063-6.
148. Ndiaye MA, Nihal M, Wood GS, Ahmad N. Skin, Reactive Oxygen Species, and Circadian Clocks. Antioxid Redox Signal 2013; 00.
149. Green CB, Mohawk JA, Takahashi JS. Central and Peripheral Circadian Clocks in Mammals. Annu Rev Neurosci 2012; 35: 445-62.
150. Bass J. Circadian topology of metabolism. Nature 2012; 491: 348-56.
151. Robinson I, Reddy AB. Molecular mechanisms of the circadian clockwork in mammals. FEBS Lett 2014; 588: 2477-83.
152. Bass J, Takahashi JS. Circadian integration of metabolism and energetics. Science 2010; 330: 1349-54.
153. Guillaumond F, Dardente H, Giguère V, Cermakian N. Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J Biol Rhythms 2005; 20: 391-403.
154. Lee J, Lee Y, Lee MJ, et al. Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Mol Cell Biol 2008; 28: 6056-65.
155. Asher G, Gatfield D, Stratmann M, et al. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 2008; 134: 317-28.
156. Belden WJ, Dunlap JC. SIRT1 is a circadian deacetylase for core clock components. Cell 2008; 134: 212-4.
157. Vanselow K, Vanselow JT, Westermark PO, et al. Differential effects of PER2 phosphorylation: molecular basis for the human familial advanced sleep phase syndrome (FASPS). Genes Dev 2006; 20: 2660-72.
158. Lamia K a, Sachdeva UM, DiTacchio L, et al. AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 2009; 326: 437-40.
159. Virshup DM, Eide EJ, Forger DB, Gallego M, Harnish EV. Reversible protein phosphorylation regulates circadian rhythms. Cold Spring Harb Symp Quant Biol 2007; 72: 413-20.
160. Avitabile D, Genovese L, Ponti D, et al. Nucleolar localization and circadian regulation of Per2S, a novel splicing variant of the Period 2 gene. Cell Mol Life Sci 2013; 1.
161. Malatesta M, Baldelli B, Battistelli S, Fattoretti P, Bertoni-Freddari C. Aging affects the distribution of the circadian CLOCK protein in rat hepatocytes. Microsc Res Tech 2005; 68: 45-50.
162. O’Neill JS, Reddy AB. Circadian clocks in human red blood cells. Nature 2011; 469: 498-503.
163. Avitabile D, Ranieri D, Nicolussi A, et al. Peroxiredoxin 2 nuclear levels are regulated by circadian clock synchronization in human keratinocytes. Int J Biochem Cell Biol 2014; 53: 24-34.
164. Feng D, Lazar MA. Clocks, metabolism, and the epigenome. Mol Cell 2012; 47: 158-67.
165. Panda S, Antoch MP, Miller BH, et al. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 2002; 109: 307-20.
166. Reddy AB, Karp NA, Maywood ES, et al. Circadian orchestration of the hepatic proteome. Curr Biol 2006; 16: 1107-15.
167. Barclay JL, Husse J, Bode B, et al. Circadian desynchrony promotes metabolic disruption in a mouse model of shiftwork. PLoS One 2012; 7: e37150.
168. Shi S, Ansari TS, McGuinness OP, Wasserman DH, Johnson CH. Circadian disruption leads to insulin resistance and obesity. Curr Biol 2013; 23: 372-81.
169. Lee J, Moulik M, Fang Z, et al. Bmal1 and β-cell clock are required for adaptation to circadian disruption, and their loss of function leads to oxidative stress-induced β-cell failure in mice. Mol Cell Biol 2013; 33: 2327-38.
170. Marcheva B, Ramsey KM, Buhr ED, et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 2010; 466: 627-31.
171. Turek FW, Joshu C, Kohsaka A, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 2005; 308: 1043-5.
172. Weibel L, Maccari S, Van Reeth O. Circadian clock functioning is linked to acute stress reactivity in rats. J Biol Rhythms 2002; 17: 438-46.
173. Tamaru T, Hattori M, Ninomiya Y, et al. ROS Stress Resets Circadian Clocks to Coordinate Pro-Survival Signals. PLoS One 2013; 8: e82006.
174. Tamaru T, Hattori M, Honda K, Benjamin I, Ozawa T, Takamatsu K. Synchronization of Circadian Per2 Rhythms and HSF1-BMAL1: CLOCK Interaction in Mouse Fibroblasts after Short-Term Heat Shock Pulse. PLoS One 2011; 6: e24521.
175. Borchers CH, Buttrick PM, Eckle T, et al. Adora2b-elicited Per2 stabilization promotes a HIF-dependent metabolic switch crucial for myocardial adaptation to ischemia. Nat Med 2012; 18: 774-82.
176. Yang X, Downes M, Yu RT, et al. Nuclear receptor expression links the circadian clock to metabolism. Cell 2006; 126: 801-10.
177. Oishi K, Shirai H, Ishida N. CLOCK is involved in the circadian transactivation of peroxisome-proliferator-activated receptor alpha (PPARalpha) in mice. Biochem J 2005; 386: 575-81.
178. Canaple L, Rambaud J, Dkhissi-Benyahya O, et al. Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferator-activated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock. Mol Endocrinol 2006; 20: 1715-27.
179. Schmutz I, Ripperger JA, Baeriswyl-Aebischer S, Albrecht U. The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. Genes Dev 2010; 24: 345-57.
180. Wang Y-X. PPARs: diverse regulators in energy metabolism and metabolic diseases. Cell Res 2010; 20: 124-37.
181. Chen L, Yang G. PPARs Integrate the Mammalian Clock and Energy Metabolism. PPAR Res 2014; 2014: 653017.
182. Yang Q, Li Y. Roles of PPARs on regulating myocardial energy and lipid homeostasis. J Mol Med (Berl) 2007; 85: 697-706.
183. Lecarpentier Y, Claes V, Duthoit G, Hébert J-L. Circadian rhythms, Wnt/beta-catenin pathway and PPAR alpha/gamma profiles in diseases with primary or secondary cardiac dysfunction. Front Physiol 2014; 5.
184. Vollmers C, Schmitz RJ, Nathanson J, Yeo G, Ecker JR, Panda S. Circadian oscillations of protein-coding and regulatory RNAs in a highly dynamic mammalian liver epigenome. Cell Metab 2012; 16: 833-45.
185. Doi M, Hirayama J, Sassone-Corsi P. Circadian regulator CLOCK is a histone acetyltransferase. Cell 2006; 125: 497-508.
186. Hirayama J, Sahar S, Grimaldi B, et al. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 2007; 450: 1086-90.
187. Cardone L, Hirayama J, Giordano F, Tamaru T, Palvimo JJ, Sassone-Corsi P. Circadian clock control by SUMOylation of BMAL1. Science 2005; 309: 1390-4.
188. Nakahata Y, Kaluzova M, Grimaldi B, et al. The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 2008; 134: 329-40.
189. Li X. SIRT1 and energy metabolism. Acta Biochim Biophys Sin (Shanghai) 2013; 45: 51-60.
190. Chang H-C, Guarente L. SIRT1 and other sirtuins in metabolism. Trends Endocrinol Metab 2014; 25: 138-45.
191. Aguilar-Arnal L, Katada S, Orozco-Solis R, Sassone-Corsi P. NAD(+)-SIRT1 control of H3K4 trimethylation through circadian deacetylation of MLL1. Nat Struct Mol Biol 2015; 22: 312-8.
192. Musiek ES, Lim MM, Yang G, et al. Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration. J Clin Invest 2013; 123: 5389-400.
193. O’Neill JS, Feeney K. Circadian Redox and Metabolic Oscillations in Mammalian Systems. Antioxid Redox Signal 2013; 00.
194. Stangherlin A, Reddy AB. Regulation of circadian clocks by redox homeostasis. J Biol Chem 2013; 288: 26505-11.
195. Wilking M, Ndiaye M, Mukhtar H, Ahmad N. Circadian rhythm connections to oxidative stress: implications for human health. Antioxid Redox Signal 2013; 19: 192-208.
196. Patel SA, Velingkaar N, Kondratov RV. Transcriptional control of antioxidant defense by the circadian clock. Antioxid Redox Signal 2013: 1-25.
197. Hardeland R, Coto-Montes A, Poeggeler B. Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiol Int 2003; 20: 921-62.
198. O’Neill JS, Feeney KA. Circadian redox and metabolic oscillations in mammalian systems. Antioxid Redox Signal 2013; 1: 1-61.
199. Liu H, Colavitti R, Rovira II, Finkel T. Redox-dependent transcriptional regulation. Circ Res 2005; 97: 967-74.
200. Rutter J, Reick M, Wu LC, McKnight SL. Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 2001; 293: 510-4.
201. Avitabile D, Ranieri D, Nicolussi A, et al. Peroxiredoxin 2 nuclear levels are regulated by circadian clock synchronization in human keratinocytes. Int J Biochem Cell Biol 2014.
202. Shiota M, Yokomizo A, Kashiwagi E, et al. Peroxiredoxin 2 in the nucleus and cytoplasm distinctly regulates androgen receptor activity in prostate cancer cells. Free Radic Biol Med 2011; 51: 78-87.
203. Ranieri D, Avitabile D, Shiota M, et al. Nuclear redox imbalance affects circadian oscillation in HaCaT keratinocytes. Int J Biochem Cell Biol 2015; 65: 113-24.
204. Kojima S, Gatfield D, Esau CC, Green CB. MicroRNA-122 modulates the rhythmic expression profile of the circadian deadenylase Nocturnin in mouse liver. PLoS One 2010; 5.
205. Alvarez-Saavedra M, Antoun G, Yanagiya A, et al. miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clock. Hum Mol Genet 2011; 20: 731-51.
206. Cheng HYM, Obrietan K. Revealing a role of microRNAs in the regulation of the biological clock. Cell Cycle 2007; 6: 3034-8.
207. Balakrishnan A, Stearns AT, Park PJ, et al. MicroRNA mir-16 is anti-proliferative in enterocytes and exhibits diurnal rhythmicity in intestinal crypts. Exp Cell Res 2010; 316: 3512-21.
208. Vasudevan S. Posttranscriptional Upregulation by MicroRNAs. Wiley Interdiscip Rev RNA 2012; 3: 311-30.
209. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-33.
210. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011; 12: 99-110.
211. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11: 228-34.
212. Hansen KF, Sakamoto K, Obrietan K. MicroRNAs: a potential interface between the circadian clock and human health. Genome Med 2011; 3: 10.
213. Kadener S, Menet JS, Sugino K, et al. A role for microRNAs in the Drosophila circadian clock. Genes Dev 2009; 23: 2179-91.
214. Cheng H-YM, Papp JW, Varlamova O, et al. microRNA modulation of circadian-clock period and entrainment. Neuron 2007; 54: 813-29.
215. Gatfield D, Le Martelot G, Vejnar CE, et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev 2009; 23: 1313-26.
216. Esau C, Davis S, Murray SF, et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 2006; 3: 87-98.
217. Elmén J, Lindow M, Silahtaroglu A, et al. Antagonism of microRNA-122 in mice by systemically administered LNAantimiR leads to up-regulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res 2008; 36: 1153-62.
218. Janich P, Pascual G, Merlos-Suárez A, et al. The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 2011; 480: 209-14.
219. Rogler CE, LeVoci L, Ader T, et al. MicroRNA-23b cluster microRNAs regulate transforming growth factor-beta/bone morphogenetic protein signaling and liver stem cell differentiation by targeting Smads. Hepatology 2009; 50: 575-84.
220. Cui M, Zheng M, Sun B, Wang Y, Ye L, Zhang X. A long noncoding RNA perturbs the circadian rhythm of hepatoma cells to facilitate hepatocarcinogenesis. Neoplasia 2015; 17: 79-88.
221. Dieci G, Preti M, Montanini B. Eukaryotic snoRNAs: a paradigm for gene expression flexibility. Genomics 2009; 94: 83-8.
222. Hazen SP, Naef F, Quisel T, et al. Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biol 2009; 10: R17.
223. Hughes ME, Grant GR, Paquin C, Qian J, Nitabach MN. Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res 2012; 22: 1266-81.
224. Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB. A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci USA 2014; 111: 16219-24.
225. Ko MS, Kitchen JR, Wang X, et al. Large-scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development. Development 2000; 127: 1737-49.
226. Yagita K, Tamanini F, van Der Horst GT, Okamura H. Molecular mechanisms of the biological clock in cultured fibroblasts. Science 2001; 292: 278-81.
227. O’Reilly LP, Watkins SC, Smithgall TE. An unexpected role for the clock protein timeless in developmental apoptosis. PLoS One 2011; 6: e17157.
228. Yagita K, Horie K, Koinuma S, et al. Development of the circadian oscillator during differentiation of mouse embryonic stem cells in vitro. Proc Natl Acad Sci USA 2010; 107: 3846-51.
229. Malik A, Jamasbi RJ, Kondratov RV, Geusz ME. Development of circadian oscillators in neurosphere cultures during adult neurogenesis. PLoS One 2015; 10: e0122937.
230. Umemura Y, Koike N, Matsumoto T, et al. Transcriptional program of Kpna2/Importin-α2 regulates cellular differentiationcoupled circadian clock development in mammalian cells. Proc Natl Acad Sci USA 2014; 111: E5039-48.
231. Kowalska E, Moriggi E, Bauer C, Dibner C, Brown SA. The circadian clock starts ticking at a developmentally early stage. J Biol Rhythms 2010; 25: 442-9.
232. Janich P, Meng Q-J, Benitah SA. Circadian control of tissue homeostasis and adult stem cells. Curr Opin Cell Biol 2014; 31C: 8-15.
233. Plikus MV, Vollmers C, de la Cruz D, et al. Local circadian clock gates cell cycle progression of transient amplifying cells during regenerative hair cycling. Proc Natl Acad Sci USA 2013; 110: E2106-15.
234. Janich P, Toufighi K, Solanas G, et al. Human epidermal stem cell function is regulated by circadian oscillations. Cell Stem Cell 2013; 13: 745-53.
235. Spörl F, Korge S, Jürchott K, et al. Krüppel-like factor 9 is a circadian transcription factor in human epidermis that controls proliferation of keratinocytes. Proc Natl Acad Sci USA 2012; 109: 10903-8.
236. Bjarnason GA, Jordan RC, Wood PA, et al. Circadian expression of clock genes in human oral mucosa and skin: association with specific cell-cycle phases. Am J Pathol 2001; 158: 1793-801.
237. Andersen B, Kumar V, Liu Q, et al. Brain and muscle Arnt-like protein-1 (BMAL1) controls circadian cell proliferation and susceptibility to UVB-induced DNA damage in the epidermis. Proc Natl Acad Sci 2012; 109: 11758-63.
238. Gaddameedhi S, Reardon JT, Ye R, Ozturk N, Sancar A. Effect of circadian clock mutations on DNA damage response in mammalian cells. Cell Cycle 2012; 11: 3481-91.
239. Gaddameedhi S, Selby CP, Kaufmann WK, Smart RC, Sancar A. Control of skin cancer by the circadian rhythm. Proc Natl Acad Sci USA 2011; 108: 18790-5.
240. Gaddameedhi S, Selby CP, Kemp MG, Ye R, Sancar A. The Circadian Clock Controls Sunburn Apoptosis and Erythema in Mouse Skin. J Invest Dermatol 2014.
241. Janich P, Pascual G, Merlos-Suarez A, et al. The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 2011; 480: 209-14.
242. Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H. Control mechanism of the circadian clock for timing of cell division in vivo. Science 2003; 302: 255-9.
243. Karpowicz P, Zhang Y, Hogenesch JB, Emery P, Perrimon N. The circadian clock gates the intestinal stem cell regenerative state. Cell Rep 2013; 3: 996-1004.
244. Bouchard-Cannon P, Mendoza-Viveros L, Yuen A, Kærn M, Cheng H-YM. The circadian molecular clock regulates adult hippocampal neurogenesis by controlling the timing of cell-cycle entry and exit. Cell Rep 2013; 5: 961-73.
245. Sato F, Sato H, Jin D, et al. Smad3 and Snail show circadian expression in human gingival fibroblasts, human mesenchymal stem cell, and in mouse liver. Biochem Biophys Res Commun 2012; 419: 441-6.
246. Mesenchymal H, Cells S. Circadian Expression of DEC1, SMAD3 and SNAIL in Human Mesenchymal Stem Cells 2014; 1: 1-3.
247. Andrews JL, Zhang X, McCarthy JJ, et al. CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function. Proc Natl Acad Sci USA 2010; 107: 19090-5.
248. Chatterjee S, Nam D, Guo B, et al. Brain and muscle Arnt-like 1 is a key regulator of myogenesis. J Cell Sci 2013; 126: 2213-24.
249. Méndez-Ferrer S, Lucas D, Battista M, Frenette PS. Haematopoietic stem cell release is regulated by circadian oscillations. Nature 2008; 452: 442-7.
250. Lucas D, Battista M, Shi PA, Isola L, Frenette PS. Mobilized Hematopoietic Stem Cell Yield Depends on Species-Specific Circadian Timing. Cell Stem Cell 2008; 3: 364-6.
251. Lapid K, Itkin T, D’Uva G, et al. GSK3α regulates physiological migration of stem/progenitor cells via cytoskeletal rearrangement. J Clin Invest 2013; 123: 1705-17.
252. Servais S, Baudoux E, Brichard B, et al. Circadian and circannual variations in cord blood hematopoietic cell composition. Haematologica 2014.
253. Yu X, Rollins D, Ruhn KA, et al. TH17 Cell Differentiation Is Regulated by the Circadian Clock. Science (80-) 2013; 342: 727-30.
254. Scheiermann C, Kunisaki Y, Frenette PS. Circadian control of the immune system. NatRevImmunol 2013; 13: 190-8.
255. Silver AC, Arjona A, Walker WE, Fikrig E. The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity 2012; 36: 251-61.
256. Castanon-Cervantes O, Wu M, Ehlen JC, et al. Dysregulation of inflammatory responses by chronic circadian disruption. J Immunol 2010; 185: 5796-805.
257. Gibbs J, Ince L, Matthews L, et al. An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nat Med 2014; 20: 919-26.
258. Baumann A, Feilhauer K, Bischoff SC, Froy O, Lorentz A. IgEdependent activation of human mast cells and fMLP-mediated activation of human eosinophils is controlled by the circadian clock. Mol Immunol 2014.
259. Sato S, Sakurai T, Ogasawara J, et al. A circadian clock gene, Reverb α, modulates the inflammatory function of macrophages through the negative regulation of Ccl2 expression. J Immunol 2014; 192: 407-17.
260. Pan X, Jiang XC, Hussain MM. Impaired cholesterol metabolism and enhanced atherosclerosis in clock Mutant Mice. Circulation 2013; 128: 1758-69.
261. Balsalobre A, Brown SA, Marcacci L, et al. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 2000; 289: 2344-7.
262. Balsalobre A, Marcacci L, Schibler U. Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Curr Biol 2000; 10: 1291-4.
263. Li J, Lu W-Q, Beesley S, Loudon ASI, Meng Q-J. Lithium impacts on the amplitude and period of the molecular circadian clockwork. PLoS One 2012; 7: e33292.
264. Hirota T, Lee JW, St John PC, et al. Identification of small molecule activators of cryptochrome. Science 2012; 337: 1094-7.
265. Rensing L, Ruoff P. Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular bases. Chronobiol Int 2002; 19: 807-64.
266. Kushibiki T, Awazu K. Controlling osteogenesis and adipogenesis of mesenchymal stromal cells by regulating a circadian clock protein with laser irradiation. Int J Med Sci 2008; 5: 319-26.