Circadian clocks, epigenetics, and cancer

Current Opinion in Oncology

Volumn 27, Issue 1, 2015, Pages 50-56

  Masri, Selma ^a   Kinouchi, Kenichiro ^a   Sassone Corsi, Paolo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer; Cell cycle; Circadian clock; Epigenome; Metabolism

Indexed keywords

ANTINEOPLASTIC AGENT; DNA; HISTONE; RNA;

CANCER CELL; CANCER CHEMOTHERAPY; CANCER GENETICS; CANCER GROWTH; CANCER THERAPY; CARCINOGENESIS; CELL CYCLE REGULATION; CELL PROLIFERATION; CHRONOTHERAPY; CIRCADIAN RHYTHM; DNA METHYLATION; EPIGENETICS; HISTONE MODIFICATION; HUMAN; METABOLISM; NEOPLASM; NONHUMAN; REVIEW; CELL CYCLE; CELL TRANSFORMATION; ENERGY METABOLISM; GENETIC EPIGENESIS; GENETICS; PATHOPHYSIOLOGY; PHYSIOLOGY;

CARCINOGENESIS; CELL CYCLE; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; ENERGY METABOLISM; EPIGENESIS, GENETIC; HUMANS; NEOPLASMS;

EID: 84916882416     PISSN: 10408746     EISSN: 1531703X     Source Type: Journal    
DOI: 10.1097/CCO.0000000000000153     Document Type: Review

References (84)

1. Feng D, Lazar MA. Clocks, metabolism, and the epigenome. Mol Cell 2012; 47: 158-167.
2. Gamble KL, Berry R, Frank SJ, et al. Circadian clock control of endocrine factors. Nat Rev Endocrinol 2014; 10: 466-475.
3. Fu L, Lee CC. The circadian clock: Pacemaker and tumour suppressor. Nat Rev Cancer 2003; 3: 350-361.
4. Sahar S, Sassone-Corsi P. Metabolism and cancer: The circadian clock connection. Nat Rev Cancer 2009; 9: 886-896.
5. Schernhammer ES, Laden F, Speizer FE, et al. Rotating night shifts and risk of breast cancer in women participating in the Nurses' Health Study. J Natl Cancer Inst 2001; 93: 1563-1568.
6. Filipski E, King VM, Li X, et al. Host circadian clock as a control point in tumor progression. J Natl Cancer Inst 2002; 94: 690-697.
7. Masri S, Sassone-Corsi P. Plasticity and specificity of the circadian epigenome. Nat Neurosci 2010; 13: 1324-1329.
8. Partch CL, Green CB, Takahashi JS.Molecular architecture of the mammalian circadian clock. Trends Cell Biol 2014; 24: 90-99.
9. Koike N, Yoo SH, Huang HC, et al. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 2012; 338: 349-354.
10. Rey G, Cesbron F, Rougemont J, et al. Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS Biol 2011; 9: E1000595.
11. Ripperger JA, Schibler U. Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat Genet 2006; 38: 369-374.
12. Wang L, Chen B, Wang Y, et al. hClock gene expression in human colorectal carcinoma. Mol Med Rep 2013; 8: 1017-1022.
13. Li A, Lin X, Tan X, et al. Circadian gene Clock contributes to cell proliferation and migration of glioma and is directly regulated by tumor-suppressive miR-124. FEBS Lett 2013; 587: 2455-2460.
14. Xiao L, Chang AK, Zang MX, et al. Induction of the CLOCK gene by E2-ERalpha signaling promotes the proliferation of breast cancer cells. PLoS One 2014; 9: E95878.
15. Li S, Wang M, Ao X, et al. CLOCK is a substrate of SUMO and sumoylation of CLOCK upregulates the transcriptional activity of estrogen receptor-Alpha. Oncogene 2013; 32: 4883-4891.
16. Lee S, Donehower LA, Herron AJ, et al. Disrupting circadian homeostasis of sympathetic signaling promotes tumor development in mice. PLoS One 2010; 5: E10995.
17. Fu L, Pelicano H, Liu J, et al. The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 2002; 111: 41-50.
18. Zhao H, Zeng ZL, Yang J, et al. Prognostic relevance of Period1 (Per1) and Period2 (Per2) expression in human gastric cancer. Int J Clin Exp Pathol 2014; 7: 619-630.
19. Pluquet O, Dejeans N, Bouchecareilh M, et al. Posttranscriptional regulation of PER1 underlies the oncogenic function of IREalpha. Cancer Res 2013; 73: 4732-4743.
20. Hwang-Verslues WW, Chang PH, Jeng YM, et al. Loss of corepressor PER2 under hypoxia up-regulates OCT1-mediated EMT gene expression and enhances tumor malignancy. Proc Natl Acad Sci USA 2013; 110: 12331-12336.
21. Dekens MP, Santoriello C, Vallone D, et al. Light regulates the cell cycle in zebrafish. Curr Biol 2003; 13: 2051-2057.
22. Grechez-Cassiau A, Rayet B, Guillaumond F, et al. The circadian clock component BMAL1 is a critical regulator of p21WAF1/CIP1 expression and hepatocyte proliferation. J Biol Chem 2008; 283: 4535-4542.
23. Laranjeiro R, Tamai TK, Peyric E, et al. Cyclin-dependent kinase inhibitor p20 controls circadian cell-cycle timing. Proc Natl Acad Sci USA 2013; 110: 6835-6840.
24. Matsuo T, Yamaguchi S, Mitsui S, et al. Control mechanism of the circadian clock for timing of cell division in vivo. Science 2003; 302: 255-259.
25. 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-E2115.
26. Feillet C, Krusche P, Tamanini F, et al. Phase locking and multiple oscillating attractors for the coupled mammalian clock and cell cycle. Proc Natl Acad Sci USA 2014; 111: 9828-9833.
27. Kelleher FC, Rao A, Maguire A. Circadian molecular clocks and cancer. Cancer Lett 2014; 342: 9-18.
28. Masri S, Cervantes M, Sassone-Corsi P. The circadian clock and cell cycle: Interconnected biological circuits. Curr Opin Cell Biol 2013; 25: 730-734.
29. Hunt T, Sassone-Corsi P. Riding tandem: Circadian clocks and the cell cycle. Cell 2007; 129: 461-464.
30. Kowalska E, Ripperger JA, Hoegger DC, et al. NONO couples the circadian clock to the cell cycle. Proc Natl Acad Sci USA 2013; 110: 1592-1599.
31. Bouchard-Cannon P, Mendoza-Viveros L, Yuen A, et al. The circadian molecular clock regulates adult hippocampal neurogenesis by controlling the timing of cell-cycle entry and exit. Cell Rep 2013; 5: 961-973.
32. Karpowicz P, Zhang Y, Hogenesch JB, et al. The circadian clock gates the intestinal stem cell regenerative state. Cell Rep 2013; 3: 996-1004.
33. Siffroi-Fernandez S, Dulong S, Li XM, et al. Functional genomics identify Birc5/survivin as a candidate gene involved in the chronotoxicity of cyclindependent kinase inhibitors. Cell Cycle 2014; 13: 984-991.
34. Agarwal ML, Agarwal A, Taylor WR, et al. p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc Natl Acad Sci USA 1995; 92: 8493-8497.
35. Miki T, Matsumoto T, Zhao Z, et al. p53 regulates Period2 expression and the circadian clock. Nat Commun 2013; 4: 2444.
36. Bouchard C, Thieke K, Maier A, et al. Direct induction of cyclin D2 by Myc contributes to cell cycle progression and sequestration of p27. EMBO J 1999; 18: 5321-5333.
37. Perez-Roger I, Kim SH, Griffiths B, et al. Cyclins D1 and D2 mediate mycinduced proliferation via sequestration of p27(Kip1) and p21(Cip1). EMBO J 1999; 18: 5310-5320.
38. Relogio A, Thomas P, Medina-Perez P, et al. Ras-mediated deregulation of the circadian clock in cancer. PLoS Genet 2014; 10: E1004338.
39. Chi P, Allis CD, Wang GG. Covalent histone modifications - miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 2010; 10: 457-469.
40. Doi M, Hirayama J, Sassone-Corsi P. Circadian regulator CLOCK is a histone acetyltransferase. Cell 2006; 125: 497-508.
41. Etchegaray JP, Lee C, Wade PA, et al. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 2003; 421: 177-182.
42. Hirayama J, Sahar S, Grimaldi B, et al. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 2007; 450: 1086-1090.
43. Asher G, Gatfield D, Stratmann M, et al. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 2008; 134: 317-328.
44. Nakahata Y, Kaluzova M, Grimaldi B, et al. The NAD-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 2008; 134: 329-340.
45. Masri S, Rigor P, Cervantes M, et al. Partitioning circadian transcription by SIRT6 leads to segregated control of cellular metabolism. Cell 2014; 158: 659-672.
46. Katada S, Sassone-Corsi P. The histone methyltransferase MLL1 permits the oscillation of circadian gene expression. Nat Struct Mol Biol 2010; 17: 1414-1421.
47. Etchegaray JP, Yang X, DeBruyne JP, et al. The polycomb group protein EZH2 is required for mammalian circadian clock function. J Biol Chem 2006; 281: 21209-21215.
48. Duong HA, Weitz CJ. Temporal orchestration of repressive chromatin modifiers by circadian clock Period complexes. Nat Struct Mol Biol 2014; 21: 126-132.
49. Roth M, Chen WY. Sorting out functions of sirtuins in cancer. Oncogene 2014; 33: 1609-1620.
50. Menssen A, Hydbring P, Kapelle K, et al. The c-MYC oncoprotein, the NAMPT enzyme, the SIRT1-inhibitor DBC1, and the SIRT1 deacetylase form a positive feedback loop. Proc Natl Acad Sci USA 2012; 109: E187-E196.
51. Lin Z, Fang D. The roles of SIRT1 in cancer. Genes Cancer 2013; 4: 97-104.
52. Li L, Osdal T, Ho Y, et al. SIRT1 activation by a c-MYC oncogenic network promotes the maintenance and drug resistance of human FLT3-ITD acute myeloid leukemia stem cells. Cell Stem Cell 2014; 15: 431-446.
53. Sebastian C, Zwaans BM, Silberman DM, et al. The histone deacetylase SIRT6 is a tumor suppressor that controls cancer metabolism. Cell 2012; 151: 1185-1199.
54. Bhaskara S, Knutson SK, Jiang G, et al. Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell 2010; 18: 436-447.
55. Alenghat T, Meyers K, Mullican SE, et al. Nuclear receptor corepressor and histone deacetylase 3 govern circadian metabolic physiology. Nature 2008; 456: 997-1000.
56. Feng D, Liu T, Sun Z, et al. A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 2011; 331: 1315-1319.
57. Valekunja UK, Edgar RS, Oklejewicz M, et al. Histone methyltransferase MLL3 contributes to genome-scale circadian transcription. Proc Natl Acad Sci USA 2013; 110: 1554-1559.
58. Krivtsov AV, Armstrong SA. MLL translocations, histone modifications and leukaemia stem-cell development. Nat Rev Cancer 2007; 7: 823-833.
59. Cao F, Townsend EC, Karatas H, et al. Targeting MLL1 H3K4 methyltransferase activity in mixed-lineage leukemia. Mol Cell 2014; 53: 247-261.
60. Chen C, Liu Y, Rappaport AR, et al. MLL3 is a haploinsufficient 7q tumor suppressor in acute myeloid leukemia. Cancer Cell 2014; 25: 652-665.
61. Kotani A, Ha D, Hsieh J, et al. miR-128b is a potent glucocorticoid sensitizer in MLL-AF4 acute lymphocytic leukemia cells and exerts cooperative effects with miR-221. Blood 2009; 114: 4169-4178.
62. Jiang X, Huang H, Li Z, et al. MiR-495 is a tumor-suppressor microRNA downregulated in MLL-rearranged leukemia. Proc Natl Acad Sci USA 2012; 109: 19397-19402.
63. Chen P, Price C, Li Z, et al. miR-9 is an essential oncogenic microRNA specifically overexpressed in mixed lineage leukemia-rearranged leukemia. Proc Natl Acad Sci USA 2013; 110: 11511-11516.
64. Luo W, Sehgal A. Regulation of circadian behavioral output via a MicroRNAJAK/STAT circuit. Cell 2012; 148: 765-779.
65. Gatfield D, Le Martelot G, Vejnar CE, et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev 2009; 23: 1313-1326.
66. Cheng HY, Papp JW, Varlamova O, et al. microRNA modulation of circadianclock period and entrainment. Neuron 2007; 54: 813-829.
67. Nam HJ, Boo K, Kim D, et al. Phosphorylation of LSD1 by PKCalpha is crucial for circadian rhythmicity and phase resetting. Mol Cell 2014; 53: 791-805.
68. Zhang X, Lu F, Wang J, et al. Pluripotent stem cell protein Sox2 confers sensitivity to LSD1 inhibition in cancer cells. Cell Rep 2013; 5: 445-457.
69. Ding J, Zhang ZM, Xia Y, et al. LSD1-mediated epigenetic modification contributes to proliferation and metastasis of colon cancer. Br J Cancer 2013; 109: 994-1003.
70. DiTacchio L, Le HD, Vollmers C, et al. Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 2011; 333: 1881-1885.
71. Chicas A, Kapoor A, Wang X, et al. H3K4 demethylation by Jarid1a and Jarid1b contributes to retinoblastoma-mediated gene silencing during cellular senescence. Proc Natl Acad Sci USA 2012; 109: 8971-8976.
72. Azzi A, Dallmann R, Casserly A, et al. Circadian behavior is lightreprogrammed by plastic DNA methylation. Nat Neurosci 2014; 17: 377-382.
73. The first demonstration of dynamic light-induced DNA methylation in the SCN. 73. Ripperger JA, Merrow M. Perfect timing: Epigenetic regulation of the circadian clock. FEBS Lett 2011; 585: 1406-1411.
74. Joska TM, Zaman R, Belden WJ. Regulated DNA methylation and the circadian clock: Implications in cancer. Biology (Basel) 2014; 3: 560-577.
75. Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis 2010; 31: 27-36.
76. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-674.
77. Cavuoto P, Fenech MF. A review of methionine dependency and the role of methionine restriction in cancer growth control and life-span extension. Cancer Treat Rev 2012; 38: 726-736.
78. Carracedo A, Cantley LC, Pandolfi PP. Cancer metabolism: Fatty acid oxidation in the limelight. Nat Rev Cancer 2013; 13: 227-232.
79. Minami Y, Kasukawa T, Kakazu Y, et al. Measurement of internal body time by blood metabolomics. Proc Natl Acad Sci USA 2009; 106: 9890-9895.
80. Eckel-Mahan KL, Patel VR, Mohney RP, et al. Coordination of the transcriptome and metabolome by the circadian clock. Proc Natl Acad Sci USA 2012; 109: 5541-5546.
81. Dallmann R, Viola AU, Tarokh L, et al. The human circadian metabolome. Proc Natl Acad Sci USA 2012; 109: 2625-2629.
82. Li XM, Mohammad-Djafari A, Dumitru M, et al. A circadian clock transcription model for the personalization of cancer chronotherapy. Cancer Res 2013; 73: 7176-7188.
83. Zeng ZL, Luo HY, Yang J, et al. Overexpression of the circadian clock gene Bmal1 increases sensitivity to oxaliplatin in colorectal cancer. Clin Cancer Res 2014; 20: 1042-1052.
84. Okazaki H, Matsunaga N, Fujioka T, et al. Circadian regulation of mTOR by the ubiquitin pathway in renal cell carcinoma. Cancer Res 2014; 74: 543-551.