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Basic Research Paper

Epigenetic regulation of autophagy by the methyltransferase EZH2 through an MTOR-dependent pathway

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Pages 2309-2322 | Received 29 Apr 2015, Accepted 02 Nov 2015, Published online: 06 Jan 2016

References

  • Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8:931-7; PMID:17712358; http://dx.doi.org/10.1038/nrm2245
  • Mizushima N. Autophagy in Protein and Organelle Turnover. Cold Spring Harb Symp Quant Biol 2011; 76:397-402; PMID:21813637; http://dx.doi.org/10.1101/sqb.2011.76.011023
  • Feng Y, Yao Z, Klionsky DJ. How to control self-digestion: transcriptional, post-transcriptional, and post-translational regulation of autophagy. Trends Cell Biol 2015; 25:354-63; PMID:25759175; http://dx.doi.org/10.1016/j.tcb.2015.02.002
  • Kim YC, Guan KL. mTOR: a pharmacologic target for autophagy regulation. J Clin Invest 2015; 125:25-32; PMID:25654547; http://dx.doi.org/10.1172/JCI73939
  • Noda T, Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 1998; 273:3963-6; PMID:9461583; http://dx.doi.org/10.1074/jbc.273.7.3963
  • Baehrecke EH. Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol 2005; 6:505-10; PMID:15928714; http://dx.doi.org/10.1038/nrm1666
  • Rubinsztein DC, Codogno P, Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 2012; 11:709-30; PMID:22935804; http://dx.doi.org/10.1038/nrd3802
  • Copetti T, Bertoli C, Dalla E, Demarchi F, Schneider C. p65/RelA modulates BECN1 transcription and autophagy. Mol Cell Biol 2009; 29:2594-608; PMID:19289499; http://dx.doi.org/10.1128/MCB.01396-08
  • Ling J, Kang Y, Zhao R, Xia Q, Lee DF, Chang Z, Li J, Peng B, Fleming JB, Wang H, et al. KrasG12D-induced IKK2/beta/NF-kappaB activation by IL-1alpha and p62 feedforward loops is required for development of pancreatic ductal adenocarcinoma. Cancer Cell 2012; 21:105-20; PMID:22264792; http://dx.doi.org/10.1016/j.ccr.2011.12.006
  • Polager S, Ofir M, Ginsberg D. E2F1 regulates autophagy and the transcription of autophagy genes. Oncogene 2008; 27:4860-4; PMID:18408756
  • Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 2007; 6:458-71; PMID:18054315; http://dx.doi.org/10.1016/j.cmet.2007.11.001
  • Zhou J, Liao W, Yang J, Ma K, Li X, Wang Y, Wang D, Wang L, Zhang Y, Yin Y, et al. FOXO3 induces FOXO1-dependent autophagy by activating the AKT1 signaling pathway. Autophagy 2012; 8:1712-23; PMID:22931788; http://dx.doi.org/10.4161/auto.21830
  • Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6:472-83; PMID:18054316; http://dx.doi.org/10.1016/j.cmet.2007.11.004
  • Fullgrabe J, Klionsky DJ, Joseph B. The return of the nucleus: transcriptional and epigenetic control of autophagy. Nat Rev Mol Cell Biol 2014; 15:65-74; PMID:24326622; http://dx.doi.org/10.1038/nrm3716
  • Kourmouli N, Jeppesen P, Mahadevhaiah S, Burgoyne P, Wu R, Gilbert DM, Bongiorni S, Prantera G, Fanti L, Pimpinelli S, et al. Heterochromatin and tri-methylated lysine 20 of histone H4 in animals. J Cell Sci 2004; 117:2491-501; PMID:15128874; http://dx.doi.org/10.1242/jcs.01238
  • Artal-Martinez de Narvajas A, Gomez TS, Zhang JS, Mann AO, Taoda Y, Gorman JA, Herreros-Villanueva M, Gress TM, Ellenrieder V, Bujanda L, et al. Epigenetic regulation of autophagy by the methyltransferase G9a. Mol Cell Biol 2013; 33:3983-93; PMID:23918802; http://dx.doi.org/10.1128/MCB.00813-13
  • Fullgrabe J, Lynch-Day MA, Heldring N, Li W, Struijk RB, Ma Q, Hermanson O, Rosenfeld MG, Klionsky DJ, Joseph B. The histone H4 lysine 16 acetyltransferase hMOF regulates the outcome of autophagy. Nature 2013; 500:468-71; PMID:23863932; http://dx.doi.org/10.1038/nature12313
  • Badeaux AI, Shi Y. Emerging roles for chromatin as a signal integration and storage platform. Nat Rev Mol Cell Biol 2013; 14:211-24; PMID:AMBIGUOUS; http://dx.doi.org/10.1038/nrm3545
  • Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res 2011; 21:381-95; PMID:21321607; http://dx.doi.org/10.1038/cr.2011.22
  • Jenuwein T, Allis CD. Translating the Histone Code. Science 2001; 293:1074-80; PMID:11498575; http://dx.doi.org/10.1126/science.1063127
  • Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell 2007; 128:707-19; PMID:17320508; http://dx.doi.org/10.1016/j.cell.2007.01.015
  • Berger SL. The complex language of chromatin regulation during transcription. Nature 2007; 447:407-12; PMID:17522673; http://dx.doi.org/10.1038/nature05915
  • Ruthenburg AJ, Allis CD, Wysocka J. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol Cell 2007; 25:15-30; PMID:17218268; http://dx.doi.org/10.1016/j.molcel.2006.12.014
  • Denslow SA, Wade PA. The human Mi-2/NuRD complex and gene regulation. Oncogene 2007; 26:5433-8; PMID:17694084; http://dx.doi.org/10.1038/sj.onc.1210611
  • Schuettengruber B, Cavalli G. Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development (Cambridge, England) 2009; 136:3531-42; PMID:19820181; http://dx.doi.org/10.1242/dev.033902
  • Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011; 469:343-9; PMID:21248841; http://dx.doi.org/10.1038/nature09784
  • Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125:315-26; PMID:16630819; http://dx.doi.org/10.1016/j.cell.2006.02.041
  • Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006; 441:349-53; PMID:16625203; http://dx.doi.org/10.1038/nature04733
  • Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science (New York, NY) 2002; 298:1039-43; http://dx.doi.org/10.1126/science.1076997
  • Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 1998; 395:917-21; PMID:9804427; http://dx.doi.org/10.1038/27699
  • Xue Y, Wong J, Moreno GT, Young MK, Côté J, Wang W. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 1998; 2:851-61; PMID:9885572; http://dx.doi.org/10.1016/S1097-2765(00)80299-3
  • Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D. The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 1998; 95:279-89; PMID:9790534; http://dx.doi.org/10.1016/S0092-8674(00)81758-4
  • Kaji K, Caballero IM, MacLeod R, Nichols J, Wilson VA, Hendrich B. The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 2006; 8:285-92; PMID:16462733; http://dx.doi.org/10.1038/ncb1372
  • Larsen DH, Poinsignon C, Gudjonsson T, Dinant C, Payne MR, Hari FJ, Rendtlew Danielsen JM, Menard P, Sand JC, Stucki M, et al. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol 2010; 190:731-40; PMID:20805324; http://dx.doi.org/10.1083/jcb.200912135
  • Polo SE, Kaidi A, Baskcomb L, Galanty Y, Jackson SP. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J 2010; 29:3130-9; PMID:20693977; http://dx.doi.org/10.1038/emboj.2010.188
  • Smeenk G, Wiegant WW, Vrolijk H, Solari AP, Pastink A, van Attikum H. The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J Cell Biol 2010; 190:741-9; PMID:20805320; http://dx.doi.org/10.1083/jcb.201001048
  • Feng Q, Zhang Y. The NuRD complex: linking histone modification to nucleosome remodeling. Curr Top Microbiol Immunol 2003; 274:269-90; PMID:12596911
  • Yap DB, Chu J, Berg T, Schapira M, Cheng SW, Moradian A, Morin RD, Mungall AJ, Meissner B, Boyle M, et al. Somatic mutations at EZH2 Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood 2011; 117:2451-9; PMID:21190999; http://dx.doi.org/10.1182/blood-2010-11-321208
  • Reynolds N, Salmon-Divon M, Dvinge H, Hynes-Allen A, Balasooriya G, Leaford D, Behrens A, Bertone P, Hendrich B. NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression. EMBO J 2012; 31:593-605; PMID:22139358; http://dx.doi.org/10.1038/emboj.2011.431
  • Jung HY, Jun S, Lee M, Kim HC, Wang X, Ji H, McCrea PD, Park JI. PAF and EZH2 induce Wnt/β-catenin signaling hyperactivation. Mol Cell 2013; 52:193-205; PMID:24055345; http://dx.doi.org/10.1016/j.molcel.2013.08.028
  • Zhao Y, Li X, Cai MY, Ma K, Yang J, Zhou J, Fu W, Wei FZ, Wang L, Xie D, et al. XBP-1u suppresses autophagy by promoting the degradation of FoxO1 in cancer cells. Cell Res 2013; 23:491-507; PMID:23277279; http://dx.doi.org/10.1038/cr.2013.2
  • Costa BM, Smith JS, Chen Y, Chen J, Phillips HS, Aldape KD, Zardo G, Nigro J, James CD, Fridlyand J, et al. Reversing HOXA9 Oncogene Activation by PI3K Inhibition: Epigenetic Mechanism and Prognostic Significance in Human Glioblastoma. Cancer Res 2010; 70:453-62; PMID:20068170; http://dx.doi.org/10.1158/0008-5472.CAN-09-2189
  • Du W, Wang S, Zhou Q, Li X, Chu J, Chang Z, Tao Q, Ng EK, Fang J, Sung JJ, et al. ADAMTS9 is a functional tumor suppressor through inhibiting AKT/mTOR pathway and associated with poor survival in gastric cancer. Oncogene 2013; 32:3319-28; PMID:22907434; http://dx.doi.org/10.1038/onc.2012.359
  • Zhao Y, Yang J, Liao W, Liu X, Zhang H, Wang S, Wang D, Feng J, Yu L, Zhu WG. Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat Cell Biol 2010; 12:665-75; PMID:20543840; http://dx.doi.org/10.1038/ncb2069
  • Wilkinson FH, Park K, Atchison ML. Polycomb recruitment to DNA in vivo by the YY1 REPO domain. Proc Natl Acad Sci U S A 2006; 103:19296-301; PMID:17158804; http://dx.doi.org/10.1073/pnas.0603564103
  • Woo CJ, Kharchenko PV, Daheron L, Park PJ, Kingston RE. A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 2010; 140:99-110; PMID:20085705; http://dx.doi.org/10.1016/j.cell.2009.12.022
  • Xi H, Yu Y, Fu Y, Foley J, Halees A, Weng Z. Analysis of overrepresented motifs in human core promoters reveals dual regulatory roles of YY1. Genome Res 2007; 17:798-806; PMID:17567998; http://dx.doi.org/10.1101/gr.5754707
  • Li G, Margueron R, Ku M, Chambon P, Bernstein BE, Reinberg D. Jarid2 and PRC2, partners in regulating gene expression. Gen Dev 2010; 24:368-80; PMID:20123894; http://dx.doi.org/10.1101/gad.1886410
  • Pasini D, Cloos PA, Walfridsson J, Olsson L, Bukowski JP, Johansen JV, Bak M, Tommerup N, Rappsilber J, Helin K. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 2010; 464:306-10; PMID:20075857; http://dx.doi.org/10.1038/nature08788
  • Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ, Voigt P, Martin SR, Taylor WR, De Marco V, et al. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 2009; 461:762-7; PMID:19767730; http://dx.doi.org/10.1038/nature08398
  • Lai AY, Wade PA. Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat Rev Cancer 2011; 11:588-96; PMID:21734722; http://dx.doi.org/10.1038/nrc3091
  • Nicolson G, Nawa A, Toh Y, Taniguchi S, Nishimori K, Moustafa A. Tumor metastasis-associated human MTA1 gene and its MTA1 protein product: Role in epithelial cancer cell invasion, proliferation and nuclear regulation. Clin Exp Metastasis 2003; 20:19-24; PMID:12650603; http://dx.doi.org/10.1023/A:1022534217769
  • Bagheri-Yarmand R, Talukder AH, Wang RA, Vadlamudi RK, Kumar R. Metastasis-associated protein 1 deregulation causes inappropriate mammary gland development and tumorigenesis. Development (Cambridge, England) 2004; 131:3469-79; PMID:15226262; http://dx.doi.org/10.1242/dev.01213
  • Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, Wade PA. MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 2003; 113:207-19; PMID:12705869; http://dx.doi.org/10.1016/S0092-8674(03)00234-4
  • Zhang H, Singh RR, Talukder AH, Kumar R. Metastatic tumor antigen 3 is a direct corepressor of the Wnt4 pathway. Gen Dev 2006; 20:2943-8; PMID:17050676; http://dx.doi.org/10.1101/gad.1461706
  • Manavathi B, Kumar R. Metastasis Tumor Antigens, an Emerging Family of Multifaceted Master Coregulators. J Biol Chem 2007; 282:1529-33; PMID:17142453; http://dx.doi.org/10.1074/jbc.R600029200
  • Wu LP, Wang X, Li L, Zhao Y, Lu S, Yu Y, Zhou W, Liu X, Yang J, Zheng Z, et al. Histone deacetylase inhibitor depsipeptide activates silenced genes through decreasing both CpG and H3K9 methylation on the promoter. Mol Cell Biol 2008; 28:3219-35; PMID:18332107; http://dx.doi.org/10.1128/MCB.01516-07
  • Wang D, Zhou J, Liu X, Lu D, Shen C, Du Y, Wei F-Z, Song B, Lu X, Yu Y, et al. Methylation of SUV39H1 by SET7/9 results in heterochromatin relaxation and genome instability. Proc Natl Acad Sci 2013; 110:5516-21; http://dx.doi.org/10.1073/pnas.1216596110
  • Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, Roeder RG, Brivanlou AH, Allis CD. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 2005; 121:859-72; PMID:15960974; http://dx.doi.org/10.1016/j.cell.2005.03.036
  • Xie D, Ma N-F, Pan Z-Z, Wu H-X, Liu Y-D, Wu G-Q, Kung H-F, Guan X-Y. Overexpression of EIF-5A2 is associated with metastasis of human colorectal carcinoma. Hum Pathol 2008; 39:80-6; PMID:17949776; http://dx.doi.org/10.1016/j.humpath.2007.05.011

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