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Basic Research Paper

MAPK15/ERK8 stimulates autophagy by interacting with LC3 and GABARAP proteins

, , , , , , , & show all
Pages 1724-1740 | Received 21 Feb 2012, Accepted 16 Aug 2012, Published online: 04 Sep 2012

References

  • Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717 - 21; http://dx.doi.org/10.1126/science.290.5497.1717; PMID: 11099404
  • Tooze SA, Yoshimori T. The origin of the autophagosomal membrane. Nat Cell Biol 2010; 12:831 - 5; http://dx.doi.org/10.1038/ncb0910-831; PMID: 20811355
  • Seglen PO, Bohley P. Autophagy and other vacuolar protein degradation mechanisms. Experientia 1992; 48:158 - 72; http://dx.doi.org/10.1007/BF01923509; PMID: 1740188
  • Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2001; 2:211 - 6; http://dx.doi.org/10.1038/35056522; PMID: 11265251
  • Klionsky D, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445 - 544; http://dx.doi.org/10.4161/auto.19496; PMID: 18188003
  • Chakrama FZ, Seguin-Py S, Le Grand JN, Fraichard A, Delage-Mourroux R, Despouy G, et al. GABARAPL1 (GEC1) associates with autophagic vesicles. Autophagy 2010; 6:495 - 505; http://dx.doi.org/10.4161/auto.6.4.11819; PMID: 20404487
  • Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 2004; 117:2805 - 12; http://dx.doi.org/10.1242/jcs.01131; PMID: 15169837
  • Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 2010; 29:1792 - 802; http://dx.doi.org/10.1038/emboj.2010.74; PMID: 20418806
  • Klionsky DJ. The molecular machinery of autophagy: unanswered questions. J Cell Sci 2005; 118:7 - 18; http://dx.doi.org/10.1242/jcs.01620; PMID: 15615779
  • Behrends C, Sowa ME, Gygi SP, Harper JW. Network organization of the human autophagy system. Nature 2010; 466:68 - 76; http://dx.doi.org/10.1038/nature09204; PMID: 20562859
  • Noda NN, Ohsumi Y, Inagaki F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett 2010; 584:1379 - 85; http://dx.doi.org/10.1016/j.febslet.2010.01.018; PMID: 20083108
  • Cheung ZH, Ip NY. Autophagy deregulation in neurodegenerative diseases - recent advances and future perspectives. J Neurochem 2011; 118:317 - 25; http://dx.doi.org/10.1111/j.1471-4159.2011.07314.x; PMID: 21599666
  • Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469:323 - 35; http://dx.doi.org/10.1038/nature09782; PMID: 21248839
  • Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, Degenhardt K, et al. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev 2007; 21:1367 - 81; http://dx.doi.org/10.1101/gad.1545107; PMID: 17510285
  • Gehart H, Kumpf S, Ittner A, Ricci R. MAPK signalling in cellular metabolism: stress or wellness?. EMBO Rep 2010; 11:834 - 40; http://dx.doi.org/10.1038/embor.2010.160; PMID: 20930846
  • Corcelle E, Djerbi N, Mari M, Nebout M, Fiorini C, Fénichel P, et al. Control of the autophagy maturation step by the MAPK ERK and p38: lessons from environmental carcinogens. Autophagy 2007; 3:57 - 9; PMID: 17102581
  • Lorin S, Pierron G, Ryan KM, Codogno P, Djavaheri-Mergny M. Evidence for the interplay between JNK and p53-DRAM signalling pathways in the regulation of autophagy. Autophagy 2010; 6:153 - 4; http://dx.doi.org/10.4161/auto.6.1.10537; PMID: 19949306
  • Abe MK, Saelzler MP, Espinosa R 3rd, Kahle KT, Hershenson MB, Le Beau MM, et al. ERK8, a new member of the mitogen-activated protein kinase family. J Biol Chem 2002; 277:16733 - 43; http://dx.doi.org/10.1074/jbc.M112483200; PMID: 11875070
  • Klevernic IV, Stafford MJ, Morrice N, Peggie M, Morton S, Cohen P. Characterization of the reversible phosphorylation and activation of ERK8. Biochem J 2006; 394:365 - 73; http://dx.doi.org/10.1042/BJ20051288; PMID: 16336213
  • Iavarone C, Acunzo M, Carlomagno F, Catania A, Melillo RM, Carlomagno SM, et al. Activation of the Erk8 mitogen-activated protein (MAP) kinase by RET/PTC3, a constitutively active form of the RET proto-oncogene. J Biol Chem 2006; 281:10567 - 76; http://dx.doi.org/10.1074/jbc.M513397200; PMID: 16484222
  • Klevernic IV, Martin NM, Cohen P. Regulation of the activity and expression of ERK8 by DNA damage. FEBS Lett 2009; 583:680 - 4; http://dx.doi.org/10.1016/j.febslet.2009.01.011; PMID: 19166846
  • Hazzalin CA, Mahadevan LC. MAPK-regulated transcription: a continuously variable gene switch?. Nat Rev Mol Cell Biol 2002; 3:30 - 40; http://dx.doi.org/10.1038/nrm715; PMID: 11823796
  • Xu YM, Zhu F, Cho YY, Carper A, Peng C, Zheng D, et al. Extracellular signal-regulated kinase 8-mediated c-Jun phosphorylation increases tumorigenesis of human colon cancer. Cancer Res 2010; 70:3218 - 27; http://dx.doi.org/10.1158/0008-5472.CAN-09-4306; PMID: 20395206
  • Henrich LM, Smith JA, Kitt D, Errington TM, Nguyen B, Traish AM, et al. Extracellular signal-regulated kinase 7, a regulator of hormone-dependent estrogen receptor destruction. Mol Cell Biol 2003; 23:5979 - 88; http://dx.doi.org/10.1128/MCB.23.17.5979-5988.2003; PMID: 12917323
  • Rossi M, Colecchia D, Iavarone C, Strambi A, Piccioni F, Verrotti di Pianella A, et al. Extracellular signal-regulated kinase 8 (ERK8) controls estrogen-related receptor α (ERRα) cellular localization and inhibits its transcriptional activity. J Biol Chem 2011; 286:8507 - 22; http://dx.doi.org/10.1074/jbc.M110.179523; PMID: 21190936
  • Saelzler MP, Spackman CC, Liu Y, Martinez LC, Harris JP, Abe MK. ERK8 down-regulates transactivation of the glucocorticoid receptor through Hic-5. J Biol Chem 2006; 281:16821 - 32; http://dx.doi.org/10.1074/jbc.M512418200; PMID: 16624805
  • Groehler AL, Lannigan DA. A chromatin-bound kinase, ERK8, protects genomic integrity by inhibiting HDM2-mediated degradation of the DNA clamp PCNA. J Cell Biol 2010; 190:575 - 86; http://dx.doi.org/10.1083/jcb.201002124; PMID: 20733054
  • Cerone MA, Burgess DJ, Naceur-Lombardelli C, Lord CJ, Ashworth A. High-throughput RNAi screening reveals novel regulators of telomerase. Cancer Res 2011; 71:3328 - 40; http://dx.doi.org/10.1158/0008-5472.CAN-10-2734; PMID: 21531765
  • Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720 - 8; http://dx.doi.org/10.1093/emboj/19.21.5720; PMID: 11060023
  • Wang H, Bedford FK, Brandon NJ, Moss SJ, Olsen RW. GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 1999; 397:69 - 72; http://dx.doi.org/10.1038/16264; PMID: 9892355
  • Hemelaar J, Lelyveld VS, Kessler BM, Ploegh HL. A single protease, Apg4B, is specific for the autophagy-related ubiquitin-like proteins GATE-16, MAP1-LC3, GABARAP, and Apg8L. J Biol Chem 2003; 278:51841 - 50; http://dx.doi.org/10.1074/jbc.M308762200; PMID: 14530254
  • Lorenz H, Hailey DW, Lippincott-Schwartz J. Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat Methods 2006; 3:205 - 10; http://dx.doi.org/10.1038/nmeth857; PMID: 16489338
  • Eskelinen EL. Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol Aspects Med 2006; 27:495 - 502; http://dx.doi.org/10.1016/j.mam.2006.08.005; PMID: 16973206
  • Tanida I, Ueno T, Kominami E. LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 2004; 36:2503 - 18; http://dx.doi.org/10.1016/j.biocel.2004.05.009; PMID: 15325588
  • Molnar-Kimber KL. Mechanism of action of rapamycin (Sirolimus, Rapamune). Transplant Proc 1996; 28:964 - 9; PMID: 8623482
  • Haspel J, Shaik RS, Ifedigbo E, Nakahira K, Dolinay T, Englert JA, et al. Characterization of macroautophagic flux in vivo using a leupeptin-based assay. Autophagy 2011; 7:629 - 42; http://dx.doi.org/10.4161/auto.7.6.15100; PMID: 21460622
  • Noda T, Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 1998; 273:3963 - 6; http://dx.doi.org/10.1074/jbc.273.7.3963; PMID: 9461583
  • Tanida I, Tanida-Miyake E, Ueno T, Kominami E. The human homolog of Saccharomyces cerevisiae Apg7p is a Protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J Biol Chem 2001; 276:1701 - 6; PMID: 11096062
  • Coulombe P, Meloche S. Atypical mitogen-activated protein kinases: structure, regulation and functions. Biochim Biophys Acta 2007; 1773:1376-87.
  • Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007; 3:542 - 5; PMID: 17611390
  • Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151 - 75; PMID: 18188003
  • Shacka JJ, Klocke BJ, Shibata M, Uchiyama Y, Datta G, Schmidt RE, et al. Bafilomycin A1 inhibits chloroquine-induced death of cerebellar granule neurons. Mol Pharmacol 2006; 69:1125 - 36; http://dx.doi.org/10.1124/mol.105.018408; PMID: 16391239
  • Kuo WL, Duke CJ, Abe MK, Kaplan EL, Gomes S, Rosner MR. ERK7 expression and kinase activity is regulated by the ubiquitin-proteosome pathway. J Biol Chem 2004; 279:23073 - 81; http://dx.doi.org/10.1074/jbc.M313696200; PMID: 15033983
  • Zacharogianni M, Kondylis V, Tang Y, Farhan H, Xanthakis D, Fuchs F, et al. ERK7 is a negative regulator of protein secretion in response to amino-acid starvation by modulating Sec16 membrane association. EMBO J 2011; 30:3684 - 700; http://dx.doi.org/10.1038/emboj.2011.253; PMID: 21847093
  • Geng J, Klionsky DJ. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. ‘Protein modifications: beyond the usual suspects’ review series. EMBO Rep 2008; 9:859 - 64; http://dx.doi.org/10.1038/embor.2008.163; PMID: 18704115
  • Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005; 171:603 - 14; http://dx.doi.org/10.1083/jcb.200507002; PMID: 16286508
  • Rusten TE, Stenmark H. p62, an autophagy hero or culprit?. Nat Cell Biol 2010; 12:207 - 9; http://dx.doi.org/10.1038/ncb0310-207; PMID: 20190829
  • Cherra SJ 3rd, Kulich SM, Uechi G, Balasubramani M, Mountzouris J, Day BW, et al. Regulation of the autophagy protein LC3 by phosphorylation. J Cell Biol 2010; 190:533 - 9; http://dx.doi.org/10.1083/jcb.201002108; PMID: 20713600
  • Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011; 7:279 - 96; http://dx.doi.org/10.4161/auto.7.3.14487; PMID: 21189453
  • Noda NN, Kumeta H, Nakatogawa H, Satoo K, Adachi W, Ishii J, et al. Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells 2008; 13:1211 - 8; http://dx.doi.org/10.1111/j.1365-2443.2008.01238.x; PMID: 19021777
  • Liu L, Feng D, Chen G, Chen M, Zheng Q, Song P, et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol 2012; 14:177 - 85; http://dx.doi.org/10.1038/ncb2422; PMID: 22267086
  • Popovic D, Akutsu M, Novak I, Harper JW, Behrends C, Dikic I. Rab GTPase-activating proteins in autophagy: regulation of endocytic and autophagy pathways by direct binding to human ATG8 modifiers. Mol Cell Biol 2012; 32:1733 - 44; http://dx.doi.org/10.1128/MCB.06717-11; PMID: 22354992
  • Sancho A, Duran J, García-España A, Mauvezin C, Alemu EA, Lamark T, et al. DOR/Tp53inp2 and Tp53inp1 constitute a metazoan gene family encoding dual regulators of autophagy and transcription. PLoS One 2012; 7:e34034; http://dx.doi.org/10.1371/journal.pone.0034034; PMID: 22470510
  • Davis PD, Hill CH, Lawton G, Nixon JS, Wilkinson SE, Hurst SA, et al. Inhibitors of protein kinase C. 1. 2,3-Bisarylmaleimides. J Med Chem 1992; 35:177 - 84; http://dx.doi.org/10.1021/jm00079a024; PMID: 1732526
  • Coward J, Ambrosini G, Musi E, Truman JP, Haimovitz-Friedman A, Allegood JC, et al. Safingol (L-threo-sphinganine) induces autophagy in solid tumor cells through inhibition of PKC and the PI3-kinase pathway. Autophagy 2009; 5:184 - 93; http://dx.doi.org/10.4161/auto.5.2.7361; PMID: 19098447
  • Jiang H, Cheng D, Liu W, Peng J, Feng J. Protein kinase C inhibits autophagy and phosphorylates LC3. Biochem Biophys Res Commun 2010; 395:471 - 6; http://dx.doi.org/10.1016/j.bbrc.2010.04.030; PMID: 20398630
  • Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007; 7:961 - 7; http://dx.doi.org/10.1038/nrc2254; PMID: 17972889
  • McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol 2006; 16:R551 - 60; http://dx.doi.org/10.1016/j.cub.2006.06.054; PMID: 16860735
  • Orrenius S. Reactive oxygen species in mitochondria-mediated cell death. Drug Metab Rev 2007; 39:443 - 55; http://dx.doi.org/10.1080/03602530701468516; PMID: 17786631
  • Jin S. Autophagy, mitochondrial quality control, and oncogenesis. Autophagy 2006; 2:80 - 4; PMID: 16874075
  • Villena J, Henriquez M, Torres V, Moraga F, Díaz-Elizondo J, Arredondo C, et al. Ceramide-induced formation of ROS and ATP depletion trigger necrosis in lymphoid cells. Free Radic Biol Med 2008; 44:1146 - 60; http://dx.doi.org/10.1016/j.freeradbiomed.2007.12.017; PMID: 18191646
  • Mathew R, White E. Autophagy, stress, and cancer metabolism: what doesn’t kill you makes you stronger. Cold Spring Harb Symp Quant Biol 2011; 76:389 - 96; http://dx.doi.org/10.1101/sqb.2012.76.011015; PMID: 22442109
  • Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, et al. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 2008; 10:776 - 87; http://dx.doi.org/10.1038/ncb1740; PMID: 18552835
  • Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402:672 - 6; http://dx.doi.org/10.1038/45257; PMID: 10604474
  • Mariño G, Salvador-Montoliu N, Fueyo A, Knecht E, Mizushima N, López-Otín C. Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J Biol Chem 2007; 282:18573 - 83; http://dx.doi.org/10.1074/jbc.M701194200; PMID: 17442669
  • Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006; 10:51 - 64; http://dx.doi.org/10.1016/j.ccr.2006.06.001; PMID: 16843265
  • Morselli E, Galluzzi L, Kepp O, Vicencio JM, Criollo A, Maiuri MC, et al. Anti- and pro-tumor functions of autophagy. Biochim Biophys Acta 2009; 1793:1524-32.
  • Altman BJ, Jacobs SR, Mason EF, Michalek RD, MacIntyre AN, Coloff JL, et al. Autophagy is essential to suppress cell stress and to allow BCR-Abl-mediated leukemogenesis. Oncogene 2011; 30:1855 - 67; http://dx.doi.org/10.1038/onc.2010.561; PMID: 21151168
  • Guo JY, Chen HY, Mathew R, Fan J, Strohecker AM, Karsli-Uzunbas G, et al. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev 2011; 25:460 - 70; http://dx.doi.org/10.1101/gad.2016311; PMID: 21317241
  • Sandilands E, Serrels B, McEwan DG, Morton JP, Macagno JP, McLeod K, et al. Autophagic targeting of Src promotes cancer cell survival following reduced FAK signalling. Nat Cell Biol 2012; 14:51 - 60; http://dx.doi.org/10.1038/ncb2386; PMID: 22138575
  • Sandilands E, Serrels B, Wilkinson S, Frame MC. Src-dependent autophagic degradation of Ret in FAK-signalling-defective cancer cells. EMBO Rep 2012; 13:733 - 40; http://dx.doi.org/10.1038/embor.2012.92; PMID: 22732841
  • Dalby KN, Tekedereli I, Lopez-Berestein G, Ozpolat B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy 2010; 6:322 - 9; http://dx.doi.org/10.4161/auto.6.3.11625; PMID: 20224296
  • Tanida I, Waguri S. Measurement of autophagy in cells and tissues. Methods Mol Biol 2010; 648:193 - 214; http://dx.doi.org/10.1007/978-1-60761-756-3_13; PMID: 20700714
  • Lamark T, Perander M, Outzen H, Kristiansen K, Øvervatn A, Michaelsen E, et al. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J Biol Chem 2003; 278:34568 - 81; http://dx.doi.org/10.1074/jbc.M303221200; PMID: 12813044
  • Marinissen MJ, Chiariello M, Pallante M, Gutkind JS. A network of mitogen-activated protein kinases links G protein-coupled receptors to the c-jun promoter: a role for c-Jun NH2-terminal kinase, p38s, and extracellular signal-regulated kinase 5. Mol Cell Biol 1999; 19:4289 - 301; PMID: 10330170