Epigenetic regulation of autophagy by the methyltransferase G9a

Molecular and Cellular Biology

Volumn 33, Issue 20, 2013, Pages 3983-3993

  De Narvajas, Amaia Artal Martinez ^a   Gomez, Timothy S ^a   Zhang, Jin San ^a   Mann, Alexander O ^a   Taoda, Yoshiyuki ^b   Gorman, Jacquelyn A ^a   Herreros Villanueva, Marta ^a   Gress, Thomas M ^c   Ellenrieder, Volker ^c   Bujand, Luis ^d   Kim, Do Hyung ^e   Kozikowski, Alan P ^b   Koenig, Alexander ^a,c   Billadeau, Daniel D ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d HOSPITAL DONOSTIA   (Spain)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; METHYLTRANSFERASE; METHYLTRANSFERASE G9A; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CHROMATIN; EHMT2 PROTEIN, HUMAN; GLUCOSE; HISTOCOMPATIBILITY ANTIGEN; HISTONE LYSINE METHYLTRANSFERASE; MAP1LC3B PROTEIN, HUMAN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; SMALL INTERFERING RNA; WIPI-1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CHROMATIN; CONTROLLED STUDY; ENZYME ACTIVITY; EPIGENETICS; GENE EXPRESSION; HUMAN; HUMAN CELL; MACROAUTOPHAGY; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; RNA SYNTHESIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOLOGY; DEFICIENCY; FIBROBLAST; GENETIC EPIGENESIS; GENETICS; HELA CELL LINE; METABOLISM; MOUSE; PHAGOSOME; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; CARRIER PROTEINS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; FIBROBLASTS; GLUCOSE; HELA CELLS; HISTOCOMPATIBILITY ANTIGENS; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; PHAGOSOMES; PRIMARY CELL CULTURE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSCRIPTIONAL ACTIVATION;

EID: 84886920194     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00813-13     Document Type: Article

References (44)

1. Klionsky DJ. 2007. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8:931-937.
2. Mehrpour M, Esclatine A, Beau I, Codogno P. 2010. Overview of macroautophagy regulation in mammalian cells. Cell Res. 20:748-762.
3. Johansen T, Lamark T. 2011. Selective autophagy mediated by autophagic adapter proteins. Autophagy 7:279-296.
4. Fimia GM, Kroemer G, Piacentini M. 2013. Molecular mechanisms of selective autophagy. Cell Death Differ. 20:1-2.
5. Choi AMK, Ryter SW, Levine B. 2013. Autophagy in human health and disease. N. Engl. J. Med. 368:651-662.
6. Tsukada M, Ohsumi Y. 1993. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333: 169-174.
7. Mauthe M, Jacob A, Freiberger S, Hentschel K, Stierhof Y-D, Codogno P, Proikas-Cezanne T. 2011. Resveratrol-mediated autophagy requires WIPI-1-regulated LC3 lipidation in the absence of induced phagophore formation. Autophagy 7:1448-1461.
8. Mauthe M, Yu W, Krut O, Krönke M, Götz F, Robenek H, Proikas-Cezanne T. 2012. WIPI-1 positive autophagosome-like vesicles entrap pathogenic Staphylococcus aureus for lysosomal degradation. Int. J. Cell Biol. 2012:179207.
9. Mauvezin C, Orpinell M, Francis VA, Mansilla F, Duran J, Ribas V, Palacín M, Boya P, Teleman AA, Zorzano A. 2010. The nuclear cofactor DOR regulates autophagy in mammalian and Drosophila cells. EMBO Rep. 11:37-44.
10. Sancho A, Duran J, García-España A, Mauvezin C, Alemu EA, Lamark T, Macias MJ, DeSalle R, Royo M, Sala D, Chicote JU, Palacín M, Johansen T, Zorzano A. 2012. DOR/Tp53inp2 and Tp53inp1 constitute a metazoan gene family encoding dual regulators of autophagy and transcription. PLoS One 7:e34034. doi:10.1371/journal.pone.0034034.
11. Codogno P, Mehrpour M, Proikas-Cezanne T. 2012. Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat. Rev. Mol. Cell Biol. 13:7-12.
12. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A. 2011. TFEB links autophagy to lysosomal biogenesis. Science 332:1429-1433.
13. Polager S, Ofir M, Ginsberg D. 2008. E2F1 regulates autophagy and the transcription of autophagy genes. Oncogene 27:4860-4864.
14. Juhász G, Puskás LG, Komonyi O, Erdi B, Maróy P, Neufeld TP, Sass M. 2007. Gene expression profiling identifies FKBP39 as an inhibitor of autophagy in larval Drosophila fat body. Cell Death Differ. 14:1181-1190.
15. Esteller M. 2008. Epigenetics in cancer. N. Engl. J. Med. 358:1148-1159.
16. Chen MW, Hua KT, Kao HJ, Chi CC, Wei LH, Johansson G, Shiah SG, Chen PS, Jeng YM, Cheng TY, Lai TC, Chang JS, Jan YH, Chien MH, Yang CJ, Huang MS, Hsiao M, Kuo ML. 2010. H3K9 histone methyltransferase G9a promotes lung cancer invasion and metastasis by silencing the cell adhesion molecule Ep-CAM. Cancer Res. 70:7830-7840.
17. Huang J, Dorsey J, Chuikov S, Pérez-Burgos L, Zhang X, Jenuwein T, Reinberg D, Berger SL. 2010. G9a and Glp methylate lysine 373 in the tumor suppressor p53. J. Biol. Chem. 285:9636-9641.
18. Kondo Y, Shen L, Ahmed S, Boumber Y, Sekido Y, Haddad BR, Issa J-PJ. 2008. Downregulation of histone H3 lysine 9 methyltransferase G9a induces centrosome disruption and chromosome instability in cancer cells. PLoS One 3:e2037. doi:10.1371/journal.pone.0002037.
19. Kondo Y, Shen L, Suzuki S, Kurokawa T, Masuko K, Tanaka Y, Kato H, Mizuno Y, Yokoe M, Sugauchi F, Hirashima N, Orito E, Osada H, Ueda R, Guo Y, Chen X, Issa J-PJ, Sekido Y. 2007. Alterations of DNA methylation and histone modifications contribute to gene silencing in hepatocellular carcinomas. Hepatol. Res. 37:974-983.
20. Duan Z, Zarebski A, Montoya-Durango D, Grimes HL, Horwitz M. 2005. Gfi1 coordinates epigenetic repression of p21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1. Mol. Cell. Biol. 25:10338-10351.
21. Nishio H, Walsh MJ. 2004. CCAAT displacement protein/cut homolog recruits G9a histone lysine methyltransferase to repress transcription. Proc. Natl. Acad. Sci. U. S. A. 101:11257-11262.
22. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y. 2002. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16:1779-1791.
23. Smallwood A, Estève P-O, Pradhan S, Carey M. 2007. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev. 21:1169-1178.
24. Estève P-O, Chin HG, Smallwood A, Feehery GR, Gangisetty O, Karpf AR, Carey MF, Pradhan S. 2006. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 20:3089-3103.
25. Zhang J, Gao Q, Li P, Liu X, Jia Y, Wu W, Li J, Dong S, Koseki H, Wong J. 2011. S phase-dependent interaction with DNMT1 dictates the role of UHRF1 but not UHRF2 in DNA methylation maintenance. Cell Res. 21: 1723-1739.
26. Gomez TS, Billadeau DD. 2009. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17:699-711.
27. Vedadi M, Barsyte-Lovejoy D, Liu F, Rival-Gervier S, Allali-Hassani A, Labrie V, Wigle TJ, DiMaggio PA, Wasney GA, Siarheyeva A, Dong A, Tempel W, Wang S-C, Chen X, Chau I, Mangano TJ, Huang X-P, Simpson CD, Pattenden SG, Norris JL, Kireev DB, Tripathy A, Edwards A, Roth BL, Janzen WP, Garcia BA, Petronis A, Ellis J, Brown PJ, Frye SV, Arrowsmith CH, Jin J. 2011. A chemical probe selectively inhibits G9a and GLP methyltransferase activity in cells. Nat. Chem. Biol. 7:566-574.
28. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ. 2011. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331:456-461.
29. Kim J, Kundu M, Viollet B, Guan K-L. 2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13: 132-141.
30. Shang L, Chen S, Du F, Li S, Zhao L, Wang X. 2011. Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK. Proc. Natl. Acad. Sci. U. S. A. 108:4788-4793.
31. Habib SL, Kasinath BS, Arya RR, Vexler S, Velagapudi C. 2010. Novel mechanism of reducing tumourigenesis: upregulation of the DNA repair enzyme OGG1 by rapamycin-mediated AMPK activation and mTOR inhibition. Eur. J. Cancer 46:2806-2820.
32. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. 2001. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152:657-668.
33. Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y. 2007. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 282:37298-37302.
34. Bjørkøy G, Lamark T, Pankiv S, _vervatn A, Brech A, Johansen T. 2009. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol. 452:181-197.
35. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun J-A, Outzen H, _vervatn A, Bjørkøy G, Johansen T. 2007. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282:24131-24145.
36. Itakura E, Mizushima N. 2011. p62 Targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J. Cell Biol. 192:17-27.
37. Proikas-Cezanne T, Robenek H. 2011. Freeze-fracture replica immunolabelling reveals human WIPI-1 and WIPI-2 as membrane proteins of autophagosomes. J. Cell. Mol. Med. 15:2007-2010.
38. Kramer JM, Kochinke K, Oortveld MAW, Marks H, Kramer D, de Jong EK, Asztalos Z, Westwood JT, Stunnenberg HG, Sokolowski MB, Keleman K, Zhou H, van Bokhoven H, Schenck A. 2011. Epigenetic regulation of learning and memory by Drosophila EHMT/G9a. PLoS Biol. 9:e1000569. doi:10.1371/journal.pbio.1000569.
39. Yokochi T, Poduch K, Ryba T, Lu J, Hiratani I, Tachibana M, Shinkai Y, Gilbert DM. 2009. G9a selectively represses a class of late-replicating genes at the nuclear periphery. Proc. Natl. Acad. Sci. U. S. A. 106:19363-19368.
40. Walsh CM, Bell BD. 2010. T cell intrinsic roles of autophagy in promoting adaptive immunity. Curr. Opin. Immunol. 22:321-325.
41. Yogev O, Goldberg R, Anzi S, Yogev O, Shaulian E. 2010. Jun proteins are starvation-regulated inhibitors of autophagy. Cancer Res. 70:2318-2327.
42. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Erdin S, Huynh T, Ferron M, Karsenty G, Vellard MC, Facchinetti V, Sabatini DM, Ballabio A. 2012. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 31:1095-1108.
43. Shaulian E. 2010. AP-1-the Jun proteins: oncogenes or tumor suppressors in disguise? Cell. Signal. 22:894-899.
44. Qiang M, Denny A, Lieu M, Carreon S, Li J. 2011. Histone H3K9 modifications are a local chromatin event involved in ethanol-induced neuroadaptation of the NR2B gene. Epigenetics 6:1095-1104.