Histone methyl-transferases and demethylases in the autophagy regulatory network: the emerging role of KDM1A/LSD1 demethylase

References

• Lawrence M, Daujat S, Schneider R. Lateral thinking: how histone modifications regulate gene expression. Trends Genet. 2016;32:42–56.
   PubMed Web of Science ®Google Scholar
• Ktistakis NT, Tooze SA. Digesting the expanding mechanisms of autophagy. Trends Cell Biol. 2016;26:624–635.
   PubMed Web of Science ®Google Scholar
• Yu L, Chen Y, Tooze SA. Autophagy pathway: cellular and molecular mechanisms. Autophagy. 2018;14:207–215.
   PubMed Web of Science ®Google Scholar
• Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132–141.
   PubMed Web of Science ®Google Scholar
• Martina JA, Chen Y, Gucek M, et al. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy. 2012;8:903–914.
   PubMed Web of Science ®Google Scholar
• Füllgrabe J, Ghislat G, Cho D-H, et al. Transcriptional regulation of mammalian autophagy at a glance. J Cell Sci. 2016;129:3059–3066.
   PubMed Web of Science ®Google Scholar
• Webb AE, Brunet A. FOXO transcription factors: key regulators of cellular quality control. Trends Biochem Sci. 2014;39:159–169.
   PubMed Web of Science ®Google Scholar
• White E. Autophagy and p53. Cold Spring Harb Perspect Med. 2016;6:a026120.
   PubMed Web of Science ®Google Scholar
• Zhang H, Bosch-Marce M, Shimoda LA, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 2008;283:10892–10903.
   PubMed Web of Science ®Google Scholar
• Yang Z, Zhao T, Zou Y, et al. Hypoxia induces autophagic cell death through hypoxia-inducible factor 1α in microglia. PLoS One. 2014;9:e96509.
   PubMed Web of Science ®Google Scholar
• Polager S, Ofir M, Ginsberg D. E2F1 regulates autophagy and the transcription of autophagy genes. Oncogene. 2008;27:4860–4864.
   PubMed Web of Science ®Google Scholar
• Cho -Y-Y, Kim DJ, Lee HS, et al. Autophagy and cellular senescence mediated by Sox2 suppress malignancy of cancer cells. PLoS One. 2013;8:e57172.
   PubMed Web of Science ®Google Scholar
• Füllgrabe J, Klionsky DJ, Joseph B. The return of the nucleus: transcriptional and epigenetic control of autophagy. Nat Rev Mol Biol. 2014;15:65–74.
   PubMed Web of Science ®Google Scholar
• Füllgrabe J, Heldring N, Hermanson O, et al. Cracking the survival code: autophagy-related histone modifications. Autophagy. 2014;10:556–561.
   PubMed Web of Science ®Google Scholar
• Füllgrabe J, Lynch-Day MA, Heldring N, et al. The histone H4 lysine 16 acetyltransferase hMOF regulates the outcome of autophagy. Nature. 2013;500:468–471.
   PubMed Web of Science ®Google Scholar
• Katoh H, Qin ZS, Liu R, et al. FOXP3 Orchestrates H4K16 acetylation and H3K4 trimethylation for activation of multiple genes by recruiting MOF and causing displacement of PLU-1. Mol Cell. 2011;44:770–784.
   PubMed Web of Science ®Google Scholar
• Shin H-JR, Kim H, Oh S, et al. AMPK–SKP2–CARM1 signalling cascade in transcriptional regulation of autophagy. Nature. 2016;534:553–557.
   PubMed Web of Science ®Google Scholar
• Chen S, Jing Y, Kang X, et al. Histone H2B monoubiquitination is a critical epigenetic switch for the regulation of autophagy. Nucleic Acids Res. 2017;45:1144–1158.
   PubMed Web of Science ®Google Scholar
• Chen H, Fan M, Pfeffer LM, et al. The histone H3 lysine 56 acetylation pathway is regulated by target of rapamycin (TOR) signaling and functions directly in ribosomal RNA biogenesis. Nucleic Acids Res. 2012;40:6534–6546.
   PubMed Web of Science ®Google Scholar
• Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705.
   PubMed Web of Science ®Google Scholar
• Black JC, Van Rechem C, Whetstine JR. Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol Cell. 2012;48:491–507.
   PubMed Web of Science ®Google Scholar
• Wei F-Z, Cao Z, Wang X, et al. Epigenetic regulation of autophagy by the methyltransferase EZH2 through an MTOR-dependent pathway. Autophagy. 2015;11:2309–2322.
   PubMed Web of Science ®Google Scholar
• Artal-Martinez de Narvajas A, Gomez TS, Zhang J-S, et al. Epigenetic regulation of autophagy by the methyltransferase G9a. Mol Cell Biol. 2013;33::3983–3993.
   PubMed Web of Science ®Google Scholar
• Sakamaki J, Wilkinson S, Hahn M, et al. Bromodomain protein BRD4 is a transcriptional repressor of autophagy and lysosomal function. Mol Cell. 2017;66:517–532.e9.
   PubMed Web of Science ®Google Scholar
• Walport LJ, Hopkinson RJ, Schofield CJ. Mechanisms of human histone and nucleic acid demethylases. Curr Opin Chem Biol. 2012;16:525–534.
   PubMed Web of Science ®Google Scholar
• Labbé RM, Holowatyj A, Yang Z-Q. Histone lysine demethylase (KDM) subfamily 4: structures, functions and therapeutic potential. Am J Transl Res. 2013;6:1–15.
   PubMed Web of Science ®Google Scholar
• Hong S, Cho Y-W, Yu L-R, et al. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci. 2007;104:18439–18444.
   PubMed Web of Science ®Google Scholar
• Lee MG, Villa R, Trojer P, et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science. 2007;318:447–450.
   PubMed Web of Science ®Google Scholar
• Denton D, Aung-Htut MT, Lorensuhewa N, et al. UTX coordinates steroid hormone-mediated autophagy and cell death. Nat Commun. 2013;4:2916.
   PubMed Web of Science ®Google Scholar
• Bernard A, Jin M, González-Rodríguez P, et al. Rph1/KDM4 mediates nutrient-limitation signaling that leads to the transcriptional induction of autophagy. Curr Biol. 2015;25:546–555.
   PubMed Web of Science ®Google Scholar
• Wang B, Fan X, Ma C, et al. Downregulation of KDM4A suppresses the survival of glioma cells by promoting autophagy. J Mol Neurosci. 2016;60:137–144.
   PubMed Web of Science ®Google Scholar
• Ambrosio S, Saccà CD, Amente S, et al. Lysine-specific demethylase LSD1 regulates autophagy in neuroblastoma through SESN2-dependent pathway. Oncogene. 2017;36:6701–6711.
   PubMed Web of Science ®Google Scholar
• Periz G, Lu J, Zhang T, et al. Regulation of protein quality control by UBE4B and LSD1 through p53-mediated transcription. PLoS Biol. 2015;13:e1002114.
   PubMed Web of Science ®Google Scholar
• Byun S, Kim Y, Zhang Y, et al. A postprandial FGF19-SHP-LSD1 regulatory axis-mediates epigenetic repression of hepatic-autophagy. Embo J. 2017;36:1755–1769.
   PubMed Web of Science ®Google Scholar
• Forneris F, Binda C, Battaglioli E, et al. LSD1: oxidative chemistry for multifaceted functions in chromatin regulation. Trends Biochem Sci. 2008;33:181–189.
   PubMed Web of Science ®Google Scholar
• Forneris F, Binda C, Vanoni MA, et al. Histone demethylation catalysed by LSD1 is a flavin-dependent oxidative process. FEBS Lett. 2005;579:2203–2207.
   PubMed Web of Science ®Google Scholar
• Shi Y, Lan F, Matson C, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 2004;119:941–953.
   PubMed Web of Science ®Google Scholar
• Shi Y-J, Matson C, Lan F, et al. Regulation of LSD1 histone demethylase activity by its associated factors. Mol Cell. 2005;19:857–864.
   PubMed Web of Science ®Google Scholar
• Maiques-Diaz A, Somervaille TC. LSD1: biologic roles and therapeutic targeting. Epigenomics. 2016;8:1103–1116.
   PubMed Web of Science ®Google Scholar
• Lee MG, Wynder C, Cooch N, et al. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature. 2005;437:432–435.
   PubMed Web of Science ®Google Scholar
• Shi Y, Sawada J, Sui G, et al. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature. 2003;422:735–738.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang H, Chen Y, et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell. 2009;138:660–672.
   PubMed Web of Science ®Google Scholar
• Perillo B, Ombra MN, Bertoni A, et al. DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science. 2008;319:202–206.
   PubMed Web of Science ®Google Scholar
• Metzger E, Wissmann M, Yin N, et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature. 2005;437:436–439.
   PubMed Web of Science ®Google Scholar
• Foster CT, Dovey OM, Lezina L, et al. Lysine-specific demethylase 1 regulates the embryonic transcriptome and CoREST stability. Mol Cell Biol. 2010;30:4851–4863.
   PubMed Web of Science ®Google Scholar
• Scoumanne A, Chen X. The lysine-specific demethylase 1 is required for cell proliferation in both p53-dependent and -independent manners. J Biol Chem. 2007;282:15471–15475.
   PubMed Web of Science ®Google Scholar
• Lv S, Bu W, Jiao H, et al. LSD1 is required for chromosome segregation during mitosis. Eur J Cell Biol. 2010;89:557–563.
   PubMed Web of Science ®Google Scholar
• Ambrosio S, Saccà CD, Majello B. Epigenetic regulation of epithelial to mesenchymal transition by the Lysine-specific demethylase LSD1/KDM1A. Biochim Biophys Acta. 2017;1860:905–910.
   PubMed Web of Science ®Google Scholar
• Godmann M, Auger V, Ferraroni-Aguiar V, et al. Dynamic regulation of histone H3 methylation at lysine 4 in mammalian spermatogenesis1. Biol Reprod. 2007;77:754–764.
   PubMed Web of Science ®Google Scholar
• Musri MM, Carmona MC, Hanzu FA, et al. Histone demethylase LSD1 regulates adipogenesis. J Biol Chem. 2010;285:30034–30041.
   PubMed Web of Science ®Google Scholar
• Amente S, Lania L, Majello B. The histone LSD1 demethylase in stemness and cancer transcription programs. Biochim Biophys Acta. 2013;1829:981–986.
   PubMed Web of Science ®Google Scholar
• Adamo A, Sesé B, Boue S, et al. LSD1 regulates the balance between self-renewal and differentiation in human embryonic stem cells. Nat Cell Biol. 2011;13:652–659.
   PubMed Web of Science ®Google Scholar
• Feng S, Jin Y, Cui M, et al. Lysine-specific demethylase 1 (LSD1) inhibitor S2101 induces autophagy via the AKT/mTOR pathway in SKOV3 ovarian cancer cells. Med Sci Monitor. 2016;22:4742–4748.
   PubMed Web of Science ®Google Scholar
• Liu S, Lu W, Li S, et al. Identification of JL1037 as a novel, specific, reversible lysine-specific demethylase 1 inhibitor that induce apoptosis and autophagy of AML cells. Oncotarget. 2017;8:31901–31914.
   PubMedGoogle Scholar
• Etani T, Suzuki T, Naiki T, et al. NCL1, a highly selective lysine-specific demethylase 1 inhibitor, suppresses prostate cancer without adverse effect. Oncotarget. 2015;6:2865–2878.
   PubMedGoogle Scholar
• Wang Z, Long Q-Y, Chen L, et al. Inhibition of H3K4 demethylation induces autophagy in cancer cell lines. Biochim Biophys Acta. 2017;1864:2428–2437.
   PubMed Web of Science ®Google Scholar
• Chao A, Lin C-Y, Chao A-N, et al. Lysine-specific demethylase 1 (LSD1) destabilizes p62 and inhibits autophagy in gynecologic malignancies. Oncotarget. 2017;8:74434–74450.
   PubMedGoogle Scholar
• Saxton RA, Sabatini DM. mTOR Signaling in Growth, Metabolism, and Disease. Cell. 2017;168:960–976.
   PubMed Web of Science ®Google Scholar
• Pasha M, Eid AH, Eid AA, et al. Sestrin2 as a novel biomarker and therapeutic target for various diseases. Oxid Med Cell Longev. 2017;2017:3296294.
   PubMed Web of Science ®Google Scholar
• Wolfson RL, Chantranupong L, Saxton RA, et al. Sestrin2 is a leucine sensor for the mTORC1 pathway. Science. 2016;351:43–48.
   PubMed Web of Science ®Google Scholar
• Parmigiani A, Nourbakhsh A, Ding B, et al. Sestrins inhibit mTORC1 kinase activation through the GATOR complex. Cell Rep. 2014;9:1281–1291.
   PubMed Web of Science ®Google Scholar
• Maiuri MC, Malik SA, Morselli E, et al. Stimulation of autophagy by the p53 target gene Sestrin2. Cell Cycle. 2009;8:1571–1576.
   PubMed Web of Science ®Google Scholar
• Goldschneider D, Horvilleur E, Plassa L-F, et al. Expression of C-terminal deleted p53 isoforms in neuroblastoma. Nucleic Acids Res. 2006;34:5603–5612.
   PubMed Web of Science ®Google Scholar
• Amente S, Milazzo G, Sorrentino MC, et al. Lysine-specific demethylase (LSD1/KDM1A) and MYCN cooperatively repress tumor suppressor genes in neuroblastoma. Oncotarget. 2015;6:14572–14583.
   PubMedGoogle Scholar
• Wyatt AR, Yerbury JJ, Berghofer P, et al. Clusterin facilitates in vivo clearance of extracellular misfolded proteins. Cell Mol Life Sci. 2011;68:3919–3931.
   PubMed Web of Science ®Google Scholar
• Zhang F, Kumano M, Beraldi E, et al. Clusterin facilitates stress-induced lipidation of LC3 and autophagosome biogenesis to enhance cancer cell survival. Nat Commun. 2014;5:5775.
   PubMed Web of Science ®Google Scholar
• Seok S, Fu T, Choi S-E, et al. Transcriptional regulation of autophagy by an FXR–CREB axis. Nature. 2014;516:108–111.
   PubMed Web of Science ®Google Scholar
• Sardiello M, Palmieri M, Di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325:473–477.
   PubMed Web of Science ®Google Scholar
• Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332:1429–1433.
   PubMed Web of Science ®Google Scholar
• Palmieri M, Impey S, Kang H, et al. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet. 2011;20:3852–3866.
   PubMed Web of Science ®Google Scholar
• Huang J, Sengupta R, Espejo AB, et al. p53 is regulated by the lysine demethylase LSD1. Nature. 2007;449:105–108.
   PubMed Web of Science ®Google Scholar
• Yang S-J, Park YS, Cho JH, et al. Regulation of hypoxia responses by flavin adenine dinucleotide-dependent modulation of HIF-1α protein stability. Embo J. 2017;36:1011–1028.
   PubMed Web of Science ®Google Scholar
• Wang J, Hevi S, Kurash JK, et al. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet. 2009;41:125–129.
   PubMed Web of Science ®Google Scholar
• Kontaki H, Talianidis I. Lysine methylation regulates E2F1-induced cell death. Mol Cell. 2010;39:152–160.
   PubMed Web of Science ®Google Scholar
• Cho H-S, Suzuki T, Dohmae N, et al. Demethylation of RB regulator MYPT1 by histone demethylase LSD1 promotes cell cycle progression in cancer cells. Cancer Res. 2011;71:655–660.
   PubMed Web of Science ®Google Scholar
• Wu H, Pomeroy SL, Ferreira M, et al. UBE4B promotes Hdm2-mediated degradation of the tumor suppressor p53. Nat Med. 2011;17:347–355.
   PubMed Web of Science ®Google Scholar
• Du C, Wu H, Leng RP. UBE4B targets phosphorylated p53 at serines 15 and 392 for degradation. Oncotarget. 2016;7:2823–2836.
   PubMedGoogle Scholar
• Morselli E, Shen S, Ruckenstuhl C, et al. p53 inhibits autophagy by interacting with the human ortholog of yeast Atg17, RB1CC1/FIP200. Cell Cycle. 2011;10:2763–2769.
   PubMed Web of Science ®Google Scholar
• Kenzelmann Broz D, Spano Mello S, Bieging KT, et al. Global genomic profiling reveals an extensive p53-regulated autophagy program contributing to key p53 responses. Genes Dev. 2013;27:1016–1031.
   PubMed Web of Science ®Google Scholar
• Eby KG, Rosenbluth JM, Mays DJ, et al. ISG20L1 is a p53 family target gene that modulates genotoxic stress-induced autophagy. Mol Cancer. 2010;9:95.
   PubMed Web of Science ®Google Scholar
• Crighton D, Wilkinson S, O’Prey J, et al. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell. 2006;126:121–134.
   PubMed Web of Science ®Google Scholar
• Shvets E, Fass E, Scherz-Shouval R, et al. The N-terminus and Phe52 residue of LC3 recruit p62/SQSTM1 into autophagosomes. J Cell Sci. 2008;121:2685–2695.
   PubMed Web of Science ®Google Scholar
• Zheng Q, Su H, Ranek MJ, et al. Autophagy and p62 in cardiac proteinopathy. Circ Res. 2011;109:296–308.
   PubMed Web of Science ®Google Scholar
• Hino S, Sakamoto A, Nagaoka K, et al. FAD-dependent lysine-specific demethylase-1 regulates cellular energy expenditure. Nat Commun. 2012;3:758.
   PubMed Web of Science ®Google Scholar
• Soliman GA, Steenson SM, Etekpo AH. Effects of metformin and a mammalian target of rapamycin (mTOR) ATPCompetitive inhibitor on targeted metabolomics in pancreatic cancer cell line. J Postgenomics Drug Biomarker Dev. 2016;6:183.
   Google Scholar
• Han X, Gui B, Xiong C, et al. Destabilizing LSD1 by Jade-2 promotes neurogenesis: an antibraking system in neural development. Mol Cell. 2014;55:482–494.
   PubMed Web of Science ®Google Scholar
• Peng B, Shi R, Jiang W, et al. Phosphorylation of LSD1 by PLK1 promotes its chromatin release during mitosis. Cell Biosci. 2017;7:15.
   PubMed Web of Science ®Google Scholar
• Luo H, Shenoy AK, Li X, et al. MOF acetylates the histone demethylase LSD1 to suppress epithelial-to-mesenchymal transition. Cell Reports. 2016;15:2665–2678.
   PubMed Web of Science ®Google Scholar
• Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature. 2011;469:323–335.
   PubMed Web of Science ®Google Scholar
• White E. The role for autophagy in cancer. J Clin Investig. 2015;125:42–46.
   PubMed Web of Science ®Google Scholar
• Menzies FM, Fleming A, Caricasole A, et al. Autophagy and neurodegeneration: pathogenic mechanisms and therapeutic opportunities. Neuron. 2017;93:1015–1034.
   PubMed Web of Science ®Google Scholar
• Hidvegi T, Ewing M, Hale P, et al. An autophagy-enhancing drug promotes degradation of mutant 1-Antitrypsin Z and reduces hepatic fibrosis. Science. 2010;329:229–232.
   PubMed Web of Science ®Google Scholar
• Liao W-C, Huang M-Z, Wang ML, et al. Statin decreases helicobacter pylori burden in macrophages by promoting autophagy. Front Cell Infect Microbiol. 2016;6:203.
   PubMed Web of Science ®Google Scholar
• Parihar SP, Guler R, Khutlang R, et al. Statin therapy reduces the mycobacterium tuberculosis burden in human macrophages and in mice by enhancing autophagy and phagosome maturation. J Infect Dis. 2014;209:754–763.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Perlstein EO, Imarisio S, et al. Small molecules enhance autophagy and reduce toxicity in Huntington’s disease models. Nat Chem Biol. 2007;3:331–338.
   PubMed Web of Science ®Google Scholar
• Moosavi A, Motevalizadeh Ardekani A. Role of epigenetics in biology and human diseases. Iran Biomed J. 2016;20:246–258.
   PubMedGoogle Scholar
• Liu T-P, Lo H-L, Wei L-S, et al. S-Adenosyl-L-methionine-competitive inhibitors of the histone methyltransferase EZH2 induce autophagy and enhance drug sensitivity in cancer cells. Anticancer Drugs. 2015;26:139–147.
   PubMed Web of Science ®Google Scholar
• Zhang J, Ng S, Wang J, et al. Histone deacetylase inhibitors induce autophagy through FOXO1-dependent pathways. Autophagy. 2015;11:629–642.
   PubMed Web of Science ®Google Scholar
• Gilardini Montani MS, Granato M, Santoni C, et al. Histone deacetylase inhibitors VPA and TSA induce apoptosis and autophagy in pancreatic cancer cells. Cell Oncol (Dordr). 2017;40:167–180.
   PubMed Web of Science ®Google Scholar
• Ji -M-M, Wang L, Zhan Q, et al. Induction of autophagy by valproic acid enhanced lymphoma cell chemosensitivity through HDAC-independent and IP3-mediated PRKAA activation. Autophagy. 2015;11:2160–2171.
   PubMed Web of Science ®Google Scholar
• Gammoh N, Lam D, Puente C, et al. Role of autophagy in histone deacetylase inhibitor-induced apoptotic and nonapoptotic cell death. Proc Natl Acad Sci. 2012;109:6561–6565.
   PubMed Web of Science ®Google Scholar
• Wang J, Kim TH, Ahn MY, et al. Sirtinol, a class III HDAC inhibitor, induces apoptotic and autophagic cell death in MCF-7 human breast cancer cells. Int J Oncol. 2012;41:1101–1109.
   PubMed Web of Science ®Google Scholar
• Fan J-D, Lei P-J, Zheng J-Y, et al. The selective activation of p53 target genes regulated by SMYD2 in BIX-01294 induced autophagy-related cell death. PLoS One. 2015;10:e0116782.
   PubMed Web of Science ®Google Scholar
• Kim Y, Kim Y-S, Kim DE, et al. BIX-01294 induces autophagy-associated cell death via EHMT2/G9a dysfunction and intracellular reactive oxygen species production. Autophagy. 2013;9:2126–2139.
   PubMed Web of Science ®Google Scholar
• Ambrosio S, Majello B. Targeting histone demethylase LSD1/KDM1a in neurodegenerative diseases. J Exp Neurosci. 2018;12:117906951876574.
   Web of Science ®Google Scholar
• Christopher MA, Kyle SM, Katz DJ. Neuroepigenetic mechanisms in disease. Epigenetics Chromatin. 2017;10:47.
   PubMed Web of Science ®Google Scholar
• Christopher MA, Myrick DA, Barwick BG, et al. LSD1 protects against hippocampal and cortical neurodegeneration. Nat Commun. 2017;8:805.
   PubMed Web of Science ®Google Scholar
• Fiszbein A, Kornblihtt AR. Histone methylation, alternative splicing and neuronal differentiation. Neurogenesis. 2016;3:e1204844.
   PubMedGoogle Scholar