The histone H3 methyltransferase G9A epigenetically activates the serine-glycine synthesis pathway to sustain cancer cell survival and proliferation

Cell Metabolism

Volumn 18, Issue 6, 2013, Pages 896-907

  Ding, Jane ^a   Li, Tai ^a,b   Wang, Xiangwei ^c   Zhao, Erhu ^a,b   Choi, Jeong Hyeon ^a   Yang, Liqun ^b   Zha, Yunhong ^d   Dong, Zheng ^a   Huang, Shuang ^a   Asara, John M ^e   Cui, Hongjuan ^b   Ding, Han Fei ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b SOUTHWEST UNIVERSITY   (China)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

^d Three Gorges University College of Medicine   (China)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; HISTONE H3; HISTONE H3 LYSINE 9 METHYLTRANSFERASE G9A; HISTONE METHYLTRANSFERASE; SERINE; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ARTICLE; AUTOPHAGY; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CANCER MORTALITY; CANCER PATIENT; CANCER SURVIVAL; CARCINOGENICITY; CELL CYCLE PROGRESSION; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EPIGENETICS; FEMALE; GENE ACTIVATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HISTONE METHYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; RIBOSOME; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; AUTOPHAGY; AZEPINES; BONE NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; EPIGENOMICS; GLYCINE; HELA CELLS; HISTOCOMPATIBILITY ANTIGENS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; METHYLATION; MICE; MICROTUBULE-ASSOCIATED PROTEINS; QUINAZOLINES; RIBOSOMES; SERINE; TRANSCRIPTION, GENETIC;

EID: 84889684498     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.11.004     Document Type: Article

References (53)

1. C.M. Adams Role of the transcription factor ATF4 in the anabolic actions of insulin and the anti-anabolic actions of glucocorticoids J. Biol. Chem. 282 2007 16744 16753
2. J.C. Black, C. Van Rechem, and J.R. Whetstine Histone lysine methylation dynamics: establishment, regulation, and biological impact Mol. Cell 48 2012 491 507
3. R.A. Cairns, I.S. Harris, and T.W. Mak Regulation of cancer cell metabolism Nat. Rev. Cancer 11 2011 85 95
4. M.-W. Chen, K.-T. Hua, H.-J. Kao, C.-C. Chi, L.-H. Wei, G. Johansson, S.-G. Shiah, P.-S. Chen, Y.-M. Jeng, and T.-Y. Cheng H3K9 histone methyltransferase G9a promotes lung cancer invasion and metastasis by silencing the cell adhesion molecule Ep-CAM Cancer Res. 70 2010 7830 7840
5. H.S. Cho, J.D. Kelly, S. Hayami, G. Toyokawa, M. Takawa, M. Yoshimatsu, T. Tsunoda, H.I. Field, D.E. Neal, and B.A. Ponder Enhanced expression of EHMT2 is involved in the proliferation of cancer cells through negative regulation of SIAH1 Neoplasia 13 2011 676 684
6. B.E. Corkey, and O. Shirihai Metabolic master regulators: sharing information among multiple systems Trends Endocrinol. Metab. 23 2012 594 601
7. R.J. DeBerardinis, J.J. Lum, G. Hatzivassiliou, and C.B. Thompson The biology of cancer: metabolic reprogramming fuels cell growth and proliferation Cell Metab. 7 2008 11 20
8. T.J. de Koning, K. Snell, M. Duran, R. Berger, B.T. Poll-The, and R. Surtees L-serine in disease and development Biochem. J. 371 2003 653 661
9. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, and J. Gentry Bioconductor: open software development for computational biology and bioinformatics Genome Biol. 5 2004 R80
10. I. Grummt, and A.G. Ladurner A metabolic throttle regulates the epigenetic state of rDNA Cell 133 2008 577 580
11. H.P. Harding, Y. Zhang, H. Zeng, I. Novoa, P.D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, and R. Paules An integrated stress response regulates amino acid metabolism and resistance to oxidative stress Mol. Cell 11 2003 619 633
12. C. He, and D.J. Klionsky Regulation mechanisms and signaling pathways of autophagy Annu. Rev. Genet. 43 2009 67 93
13. K. Herbig, E.P. Chiang, L.R. Lee, J. Hills, B. Shane, and P.J. Stover Cytoplasmic serine hydroxymethyltransferase mediates competition between folate-dependent deoxyribonucleotide and S-adenosylmethionine biosyntheses J. Biol. Chem. 277 2002 38381 38389
14. W. Huang, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57
15. J. Huang, J. Dorsey, S. Chuikov, L. Pérez-Burgos, X. Zhang, T. Jenuwein, D. Reinberg, and S.L. Berger G9a and Glp methylate lysine 373 in the tumor suppressor p53 J. Biol. Chem. 285 2010 9636 9641
16. S.C. Kalhan, and R.W. Hanson Resurgence of serine: an often neglected but indispensable amino acid J. Biol. Chem. 287 2012 19786 19791
17. M.S. Kilberg, Y.X. Pan, H. Chen, and V. Leung-Pineda Nutritional control of gene expression: how mammalian cells respond to amino acid limitation Annu. Rev. Nutr. 25 2005 59 85
18. M.S. Kilberg, J. Shan, and N. Su ATF4-dependent transcription mediates signaling of amino acid limitation Trends Endocrinol. Metab. 20 2009 436 443
19. J. Kim, and K.L. Guan Amino acid signaling in TOR activation Annu. Rev. Biochem. 80 2011 1001 1032
20. D.J. Klionsky, H. Abeliovich, P. Agostinis, D.K. Agrawal, G. Aliev, D.S. Askew, M. Baba, E.H. Baehrecke, B.A. Bahr, and A. Ballabio Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes Autophagy 4 2008 151 175
21. Y. Kondo, L. Shen, S. Ahmed, Y. Boumber, Y. Sekido, B.R. Haddad, and J.-P.J. Issa Downregulation of histone H3 lysine 9 methyltransferase G9a induces centrosome disruption and chromosome instability in cancer cells PLoS ONE 3 2008 e2037
22. S. Kubicek, R.J. O'Sullivan, E.M. August, E.R. Hickey, Q. Zhang, M.L. Teodoro, S. Rea, K. Mechtler, J.A. Kowalski, and C.A. Homon Reversal of H3K9me2 by a small-molecule inhibitor for the G9a histone methyltransferase Mol. Cell 25 2007 473 481
23. A. Kuma, M. Hatano, M. Matsui, A. Yamamoto, H. Nakaya, T. Yoshimori, Y. Ohsumi, T. Tokuhisa, and N. Mizushima The role of autophagy during the early neonatal starvation period Nature 432 2004 1032 1036
24. T.I. Lee, S.E. Johnstone, and R.A. Young Chromatin immunoprecipitation and microarray-based analysis of protein location Nat. Protoc. 1 2006 729 748
25. J.W. Locasale Serine, glycine and one-carbon units: cancer metabolism in full circle Nat. Rev. Cancer 13 2013 572 583
26. J.W. Locasale, A.R. Grassian, T. Melman, C.A. Lyssiotis, K.R. Mattaini, A.J. Bass, G. Heffron, C.M. Metallo, T. Muranen, and H. Sharfi Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis Nat. Genet. 43 2011 869 874
27. N. Mizushima, A. Yamamoto, M. Hatano, Y. Kobayashi, Y. Kabeya, K. Suzuki, T. Tokuhisa, Y. Ohsumi, and T. Yoshimori Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells J. Cell Biol. 152 2001 657 668
28. N. Mizushima, T. Yoshimori, and B. Levine Methods in mammalian autophagy research Cell 140 2010 313 326
29. N. Mosammaparast, and Y. Shi Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases Annu. Rev. Biochem. 79 2010 155 179
30. M.R. Narkewicz, S.D. Sauls, S.S. Tjoa, C. Teng, and P.V. Fennessey Evidence for intracellular partitioning of serine and glycine metabolism in Chinese hamster ovary cells Biochem. J. 313 1996 991 996
31. A.H.F.M. Peters, S. Kubicek, K. Mechtler, R.J. O'Sullivan, A.A.H.A. Derijck, L. Perez-Burgos, A. Kohlmaier, S. Opravil, M. Tachibana, and Y. Shinkai Partitioning and plasticity of repressive histone methylation states in mammalian chromatin Mol. Cell 12 2003 1577 1589
32. W. Pfendner, and L.I. Pizer The metabolism of serine and glycine in mutant lines of Chinese hamster ovary cells Arch. Biochem. Biophys. 200 1980 503 512
33. S. Pollari, S.M. Käkönen, H. Edgren, M. Wolf, P. Kohonen, H. Sara, T. Guise, M. Nees, and O. Kallioniemi Enhanced serine production by bone metastatic breast cancer cells stimulates osteoclastogenesis Breast Cancer Res. Treat. 125 2011 421 430
34. R. Possemato, K.M. Marks, Y.D. Shaul, M.E. Pacold, D. Kim, K. Birsoy, S. Sethumadhavan, H.K. Woo, H.G. Jang, and A.K. Jha Functional genomics reveal that the serine synthesis pathway is essential in breast cancer Nature 476 2011 346 350
35. J.D. Rabinowitz, and E. White Autophagy and metabolism Science 330 2010 1344 1348
36. J.C. Rice, S.D. Briggs, B. Ueberheide, C.M. Barber, J. Shabanowitz, D.F. Hunt, Y. Shinkai, and C.D. Allis Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains Mol. Cell 12 2003 1591 1598
37. A. Roberts, H. Pimentel, C. Trapnell, and L. Pachter Identification of novel transcripts in annotated genomes using RNA-Seq Bioinformatics 27 2011 2325 2329
38. J. Seo, E.S. Fortuno III, J.M. Suh, D. Stenesen, W. Tang, E.J. Parks, C.M. Adams, T. Townes, and J.M. Graff Atf4 regulates obesity, glucose homeostasis, and energy expenditure Diabetes 58 2009 2565 2573
39. Y. Shinkai, and M. Tachibana H3K9 methyltransferase G9a and the related molecule GLP Genes Dev. 25 2011 781 788
40. P.J. Stover, L.H. Chen, J.R. Suh, D.M. Stover, K. Keyomarsi, and B. Shane Molecular cloning, characterization, and regulation of the human mitochondrial serine hydroxymethyltransferase gene J. Biol. Chem. 272 1997 1842 1848
41. M. Tachibana, K. Sugimoto, M. Nozaki, J. Ueda, T. Ohta, M. Ohki, M. Fukuda, N. Takeda, H. Niida, H. Kato, and Y. Shinkai G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis Genes Dev. 16 2002 1779 1791
42. R. Teperino, K. Schoonjans, and J. Auwerx Histone methyl transferases and demethylases; can they link metabolism and transcription? Cell Metab. 12 2010 321 327
43. A.S. Tibbetts, and D.R. Appling Compartmentalization of Mammalian folate-mediated one-carbon metabolism Annu. Rev. Nutr. 30 2010 57 81
44. N. Touroutoglou, and R. Pazdur Thymidylate synthase inhibitors Clin. Cancer Res. 2 1996 227 243
45. C. Trapnell, L. Pachter, and S.L. Salzberg TopHat: discovering splice junctions with RNA-Seq Bioinformatics 25 2009 1105 1111
46. L.J. Valentijn, J. Koster, F. Haneveld, R.A. Aissa, P. van Sluis, M.E. Broekmans, J.J. Molenaar, J. van Nes, and R. Versteeg Functional MYCN signature predicts outcome of neuroblastoma irrespective of MYCN amplification Proc. Natl. Acad. Sci. USA 109 2012 19190 19195
47. M.G. Vander Heiden, L.C. Cantley, and C.B. Thompson Understanding the Warburg effect: the metabolic requirements of cell proliferation Science 324 2009 1029 1033
48. O. Warburg On respiratory impairment in cancer cells Science 124 1956 269 270
49. J. Ye, A. Mancuso, X. Tong, P.S. Ward, J. Fan, J.D. Rabinowitz, and C.B. Thompson Pyruvate kinase M2 promotes de novo serine synthesis to sustain mTORC1 activity and cell proliferation Proc. Natl. Acad. Sci. USA 109 2012 6904 6909
50. T. Yoshida, and G. Kikuchi Major pathways of glycine and serine catabolism in rat liver Arch. Biochem. Biophys. 139 1970 380 392
51. X. Yuan, W. Feng, A. Imhof, I. Grummt, and Y. Zhou Activation of RNA polymerase I transcription by cockayne syndrome group B protein and histone methyltransferase G9a Mol. Cell 27 2007 585 595
52. M. Yuan, S.B. Breitkopf, X. Yang, and J.M. Asara A positive/negative ion-switching, targeted mass spectrometry-based metabolomics platform for bodily fluids, cells, and fresh and fixed tissue Nat. Protoc. 7 2012 872 881
53. Y. Zhang, T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu Model-based analysis of ChIP-Seq (MACS) Genome Biol. 9 2008 R137