AMPK regulates histone H2B O-GlcNAcylation

Nucleic Acids Research

Volumn 42, Issue 9, 2014, Pages 5594-5604

  Xu, Qiuran ^a   Yang, Caihong ^b   Du, Yu ^b,c   Chen, Yali ^c   Liu, Hailong ^c   Deng, Min ^d   Zhang, Haoxing ^c,d   Zhang, Lei ^d   Liu, Tongzheng ^d   Liu, Qingguang ^a   Wang, Liewei ^e   Lou, Zhenkun ^d   Pei, Huadong ^c  

^a THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^d MAYO CLINIC   (United States)

^e MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA N ACETYLGLUCOSAMINE TRANSFERASE; HEXOSAMINE; HISTONE H2B; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; N ACETYLGLUCOSAMINE; PROTEIN KINASE LKB1; TRANSFERASE; UNCLASSIFIED DRUG;

ACYLATION; ARTICLE; CARBOHYDRATE SYNTHESIS; CELL ENERGY; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOLYSIS; ENERGY BALANCE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FEEDBACK SYSTEM; HISTONE MODIFICATION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

ACETYLGLUCOSAMINE; AMP-ACTIVATED PROTEIN KINASES; CHROMATIN; ENERGY METABOLISM; EPIGENESIS, GENETIC; GLYCOSYLATION; HEP G2 CELLS; HISTONES; HOMEOSTASIS; HUMANS; N-ACETYLGLUCOSAMINYLTRANSFERASES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSCRIPTION, GENETIC;

EID: 84901313642     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku236     Document Type: Article

References (47)

1. Chen, Q., Chen, Y., Bian, C., Fujiki, R. and Yu, X. (2013) TET2 promotes histone O-GlcNAcylation during gene transcription. Nature, 493, 561-564.
2. Cotney, J., Leng, J., Yin, J., Reilly, S.K., Demare, L.E., Emera, D., Ayoub, A.E., Rakic, P. and Noonan, J.P. (2013) The evolution of lineage-specific regulatory activities in the human embryonic limb. Cell, 154, 185-196.
3. Fuchs, G., Shema, E., Vesterman, R., Kotler, E., Wolchinsky, Z., Wilder, S., Golomb, L., Pribluda, A., Zhang, F., Haj-Yahya, M. et al. (2012) RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol. Cell, 46, 662-673.
4. Fujiki, R., Hashiba, W., Sekine, H., Yokoyama, A., Chikanishi, T., Ito, S., Imai, Y., Kim, J., He, H.H., Igarashi, K. et al. (2011) GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature, 480, 557-560.
5. Greer, E.L. and Shi, Y. (2012) Histone methylation: A dynamic mark in health, disease and inheritance. Nat. Rev. Genet., 13, 343-357.
6. Hu, R., Wang, E., Peng, G., Dai, H. and Lin, S.Y. (2013) Zinc finger protein 668 interacts with Tip60 to promote H2AX acetylation after DNA damage. Cell Cycle, 12, 2033-2041
7. Kartikasari, A.E., Zhou, J.X., Kanji, M.S., Chan, D.N., Sinha, A., Grapin-Botton, A., Magnuson, M.A., Lowry, W.E. and Bhushan, A. (2013) The histone demethylase Jmjd3 sequentially associates with the transcription factors Tbx3 and Eomes to drive endoderm differentiation. Embo J., 32, 1393-1408.
8. Keum, Y.S., Kim, H.G., Bode, A.M., Surh, Y.J. and Dong, Z. (2013) UVB-induced COX-2 expression requires histone H3 phosphorylation at Ser10 and Ser28. Oncogene, 32, 444-452.
9. Rothbart, S.B., Dickson, B.M., Ong, M.S., Krajewski, K., Houliston, S., Kireev, D.B., Arrowsmith, C.H. and Strahl, B.D. (2013) Multivalent histone engagement by the linked tandem Tudor and PHD domains of UHRF1 is required for the epigenetic inheritance of DNA methylation. Genes Dev., 27, 1288-1298.
10. Yang, W., Xia, Y., Hawke, D., Li, X., Liang, J., Xing, D., Aldape, K., Hunter, T., Alfred Yung, W.K. and Lu, Z. (2012) PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell, 150, 685-696.
11. Zhang, F. and Yu, X. (2011) WAC, a functional partner of RNF20/40, regulates histone H2B ubiquitination and gene transcription. Mol Cell, 41, 384-397.
12. Zhang, Z., Jones, A., Joo, H.Y., Zhou, D., Cao, Y., Chen, S., Erdjument-Bromage, H., Renfrow, M., He, H., Tempst, P. et al. (2013) USP49 deubiquitinates histone H2B and regulates cotranscriptional pre-mRNA splicing. Genes Dev., 27, 1581-1595
13. Sakabe, K., Wang, Z. and Hart, G.W. (2010)-N-Acetylglucosamine (O-GlcNAc) is part of the histone code. Proc. Natl. Acad. Sci., 107, 19915-19920.
14. Vella, P., Scelfo, A., Jammula, S., Chiacchiera, F., Williams, K., Cuomo, A., Roberto, A., Christensen, J., Bonaldi, T., Helin, K. et al. (2013) Tet proteins connect the O-linked N-Acetylglucosamine transferase Ogt to chromatin in embryonic stem cells. Mol. Cell, 49, 645-656.
15. Deplus, R., Delatte, B., Schwinn, M.K., Defrance, M., Mendez, J., Murphy, N., Dawson, M.A., Volkmar, M., Putmans, P., Calonne, E. et al. (2013) TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. Embo J., 32, 645-655.
16. Pavri, R., Zhu, B., Li, G., Trojer, P., Mandal, S., Shilatifard, A. and Reinberg, D. (2006) Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell, 125, 703-717. (Pubitemid 43732350
17. Zhu, B., Zheng, Y., Pham, A.D., Mandal, S.S., Erdjument-Bromage, H., Tempst, P. and Reinberg, D. (2005) Monoubiquitination of human histone H2B: The factors involved and their roles in HOX gene regulation. Mol. Cell, 20, 601-611.
18. McFadden, S.A., Menchella, J.A., Chalmers, J.A., Centeno, M.L. and Belsham, D.D. (2013) Glucose responsiveness in a novel adult-derived GnRH cell line, mHypoA-GnRH/GFP: Involvement of AMP-Activated protein kinase. Mol. Cell Endocrinol., 377, 65-74
19. Stockebrand, M., Sauter, K., Neu, A., Isbrandt, D. and Choe, C.U. (2013) Differential regulation of AMPK activation in leptin-And creatine-deficient mice. Faseb J., 27, 4147-4156
20. Sun, Y., Connors, K.E. and Yang, D.Q. (2007) AICAR induces phosphorylation of AMPK in an ATM-dependent, LKB1-independent manner. Mol. Cell Biochem., 306, 239-245. (Pubitemid 350001836
21. Kahn, B.B., Alquier, T., Carling, D. and Hardie, D.G. (2005) AMP-Activated protein kinase: Ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab., 1, 15-25. (Pubitemid 43960587
22. Faubert, B., Boily, G., Izreig, S., Griss, T., Samborska, B., Dong, Z., Dupuy, F., Chambers, C., Fuerth, B.J. and Viollet, B. (2012) AMPK is a negative regulator of theWarburg effect and suppresses tumor growth in vivo. Cell Metab., 17, 113-124.
23. Hardie, D.G. (2013) AMPK: A target for drugs and natural products with effects on both diabetes and cancer. Diabetes, 62, 2164-2172.
24. Hurley, R.L., Anderson, K.A., Franzone, J.M., Kemp, B.E., Means, A.R. and Witters, L.A. (2005) The Ca2+/calmodulin-dependent protein kinase kinases are AMP-Activated protein kinase kinases. J. Biol. Chem., 280, 29060-29066.
25. Lizcano, J.M., Goransson, O., Toth, R., Deak, M., Morrice, N.A., Boudeau, J., Hawley, S.A., Udd, L., Makela, T.P., Hardie, D.G. et al. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. Embo J., 23, 833-843. (Pubitemid 38418750
26. Woods, A., Dickerson, K., Heath, R., Hong, S.P., Momcilovic, M., Johnstone, S.R., Carlson, M. and Carling, D. (2005) Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-Activated protein kinase in mammalian cells. Cell Metab., 2, 21-33.
27. Hawley, S.A., Pan, D.A., Mustard, K.J., Ross, L., Bain, J., Edelman, A.M., Frenguelli, B.G. and Hardie, D.G. (2005) Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-Activated protein kinase. Cell Metab., 2, 9-19. (Pubitemid 43239821
28. Shaw, R.J., Kosmatka, M., Bardeesy, N., Hurley, R.L., Witters, L.A., DePinho, R.A. and Cantley, L.C. (2004) The tumor suppressor LKB1 kinase directly activates AMP-Activated kinase and regulates apoptosis in response to energy stress. Proc. Natl. Acad. Sci. U.S.A., 101, 3329-3335.
29. Sanders, M.J., Grondin, P.O., Hegarty, B.D., Snowden, M.A. and Carling, D. (2007) Investigating the mechanism for AMP activation of the AMP-Activated protein kinase cascade. Biochem. J., 403, 139-148.
30. Nakagawa, K., Uehata, Y., Natsuizaka, M., Kohara, T., Darmanin, S., Asaka, M., Takeda, H. and Kobayashi, M. (2012) The nuclear protein Artemis promotes AMPK activation by stabilizing the LKB1-AMPK complex. Biochem. Biophys. Res. Commun., 427, 790-795.
31. Inoki, K., Zhu, T. and Guan, K.L. (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell, 115, 577-590. (Pubitemid 37506046
32. Sato, A., Sunayama, J., Okada, M., Watanabe, E., Seino, S., Shibuya, K., Suzuki, K., Narita, Y., Shibui, S., Kayama, T. et al. (2012) Glioma-initiating cell elimination by metformin activation of FOXO3 via AMPK. Stem Cells Transl. Med., 1, 811-824.
33. Gwinn, D.M., Shackelford, D.B., Egan, D.F., Mihaylova, M.M., Mery, A., Vasquez, D.S., Turk, B.E. and Shaw, R.J. (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell, 30, 214-226.
34. Choi, Y.K. and Park, K.G. (2013) Metabolic roles of AMPK and metformin in cancer cells. Mol. Cells., 36, 279-287
35. Greer, E.L., Oskoui, P.R., Banko, M.R., Maniar, J.M., Gygi, M.P., Gygi, S.P. and Brunet, A. (2007) The energy sensor AMP-Activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J. Biol. Chem., 282, 30107-30119.
36. Green, A.S., Chapuis, N., Lacombe, C., Mayeux, P., Bouscary, D. and Tamburini, J. (2011) LKB1/AMPK/mTOR signaling pathway in hematological malignancies: From metabolism to cancer cell biology. Cell Cycle, 10, 2115-2120.
37. Lin, C.C., Yeh, H.H., Huang, W.L., Yan, J.J., Lai, W.W., Su, W.P., Chen, H.H. and Su, W.C. (2013) Metformin enhances cisplatin cytotoxicity by suppressing Stat3 activity independently of the LKB1-AMPK pathway. Am. J. Respir. Cell Mol. Biol., 49, 241-250
38. Shackelford, D.B. and Shaw, R.J. (2009) The LKB1-AMPK pathway: Metabolism and growth control in tumour suppression. Nat. Rev. Cancer, 9, 563-575.
39. Bungard, D., Fuerth, B.J., Zeng, P.Y., Faubert, B., Maas, N.L., Viollet, B., Carling, D., Thompson, C.B., Jones, R.G. and Berger, S.L. (2010) Signaling kinase AMPK activates stress-promoted transcription via histone H2B phosphorylation. Science, 329, 1201-1205.
40. Schimpl, M., Zheng, X., Borodkin, V.S., Blair, D.E., Ferenbach, A.T., Schuttelkopf, A.W., Navratilova, I., Aristotelous, T., Albarbarawi, O., Robinson, D.A. et al. (2012) O-GlcNAc transferase invokes nucleotide sugar pyrophosphate participation in catalysis. Nat. Chem. Biol., 8, 969-974.
41. Wellen, K.E., Lu, C., Mancuso, A., Lemons, J.M., Ryczko, M., Dennis, J.W., Rabinowitz, J.D., Coller, H.A. and Thompson, C.B. (2010) The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism. Genes Dev., 24, 2784-2799.
42. Yang, X., Zhang, F. and Kudlow, J.E. (2002) Recruitment of O-GlcNAc transferase to promoters by corepressor mSin3A: Coupling protein O-GlcNAcylation to transcriptional repression. Cell, 110, 69-80. (Pubitemid 34874607
43. Gambetta, M.C., Oktaba, K. and Muller, J. (2009) Essential role of the glycosyltransferase sxc/Ogt in polycomb repression. Science, 325, 93-96.
44. Slawson, C., Lakshmanan, T., Knapp, S. and Hart, G.W. (2008) A mitotic GlcNAcylation/phosphorylation signaling complex alters the posttranslational state of the cytoskeletal protein vimentin. Mol. Biol. Cell, 19, 4130-4140.
45. Dias, W.B., Cheung, W.D. and Hart, G.W. (2012) O-GlcNAcylation of kinases. Biochem. Biophys. Res. Commun., 422, 224-228.
46. Hu, P., Shimoji, S. and Hart, G.W. (2010) Site-specific interplay between O-GlcNAcylation and phosphorylation in cellular regulation. FEBS Lett., 584, 2526-2538.
47. Daou, S., Mashtalir, N., Hammond-Martel, I., Pak, H., Yu, H., Sui, G., Vogel, J.L., Kristie, T.M. and Affar el, B. (2011) Crosstalk between O-GlcNAcylation and proteolytic cleavage regulates the host cell factor-1 maturation pathway. Proc. Natl. Acad. Sci. U.S.A., 108, 2747-2752.