1,805
Views
25
CrossRef citations to date
0
Altmetric
Toolbox

AU4S: A novel synthetic peptide to measure the activity of ATG4 in living cells

, , , , , , , , , & show all
Pages 403-415 | Received 11 Nov 2013, Accepted 18 Nov 2014, Published online: 01 Apr 2015

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: process and function. Genes Dev 2007; 21:2861-73; PMID:18006683; http://dx.doi.org/10.1101/gad.1599207
  • Levine B. Autophagy in development, tumor suppression, and innate immunity. Harvey Lect 2003; 99:47-76; PMID:15984551
  • Levine B, Deretic V. Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 2007; 7:767-77; PMID:17767194; http://dx.doi.org/10.1038/nri2161
  • Deretic V. Autophagy in innate and adaptive immunity. Trends Immunol 2005; 26:523-8; PMID:16099218; http://dx.doi.org/10.1016/j.it.2005.08.003
  • Rubinsztein DC, Marino G, Kroemer G. Autophagy and aging. Cell 2011; 146:682-95; PMID:21884931; http://dx.doi.org/10.1016/j.cell.2011.07.030
  • Fulda S. Autophagy and cell death. Autophagy 2012; 8:1250-1; PMID:22575893; http://dx.doi.org/10.4161/auto.20669
  • Zhang Y, Morgan MJ, Chen K, Choksi S, Liu ZG. Induction of autophagy is essential for monocyte-macrophage differentiation. Blood 2012; 119:2895-905; PMID:22223827; http://dx.doi.org/10.1182/blood-2011-08-372383
  • Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441:880-4; PMID:16625205; http://dx.doi.org/10.1038/nature04723
  • Levine B. Cell biology: autophagy and cancer. Nature 2007; 446:745-7; PMID:17429391; http://dx.doi.org/10.1038/446745a
  • Mijaljica D, Prescott M, Devenish RJ. Autophagy in disease. Methods Mol Biol 2010; 648:79-92; PMID:20700706; http://dx.doi.org/10.1007/978-1-60761-756-3_5
  • Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 2013; 13:722-37; PMID:24064518; http://dx.doi.org/10.1038/nri3532
  • Lavandero S, Troncoso R, Rothermel BA, Martinet W, Sadoshima J, Hill JA. Cardiovascular autophagy: concepts, controversies, and perspectives. Autophagy 2013; 9:1455-66; PMID:23959233; http://dx.doi.org/10.4161/auto.25969
  • Song Y, Zhao Y, Wang F, Tao L, Xiao J, Yang C. Autophagy in hepatic fibrosis. Biomed Res Int 2014; 2014:436242; PMID:24779010
  • Nakatogawa H, Ichimura Y, Ohsumi Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 2007; 130:165-78; PMID:17632063; http://dx.doi.org/10.1016/j.cell.2007.05.021
  • Yu ZQ, Ni T, Hong B, Wang HY, Jiang FJ, Zou S, Chen Y, Zheng XL, Klionsky DJ, Liang Y, et al. Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy 2012; 8:883-92; PMID:22652539; http://dx.doi.org/10.4161/auto.19652
  • Nair U, Yen WL, Mari M, Cao Y, Xie Z, Baba M, Reggiori F, Klionsky DJ. A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy 2012; 8:780-93; PMID:22622160; http://dx.doi.org/10.4161/auto.19385
  • Nakatogawa H, Ishii J, Asai E, Ohsumi Y. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy 2012; 8:177-86; PMID:22240591; http://dx.doi.org/10.4161/auto.8.2.18373
  • Marino G, Uria JA, Puente XS, Quesada V, Bordallo J, Lopez-Otin C. Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem 2003; 278:3671-8; PMID:12446702; http://dx.doi.org/10.1074/jbc.M208247200
  • Cabrera S, Fernandez AF, Marino G, Aguirre A, Suarez MF, Espanol Y, Vega JA, Laurà R, Fueyo A, Fernández-García MS, et al. ATG4B/autophagin-1 regulates intestinal homeostasis and protects mice from experimental colitis. Autophagy 2013; 9:1188-200; PMID:23782979; http://dx.doi.org/10.4161/auto.24797
  • Kuang E, Okumura CY, Sheffy-Levin S, Varsano T, Shu VC, Qi J, Niesman IR, Yang HJ, López-Otín C, Yang WY, et al. Regulation of ATG4B stability by RNF5 limits basal levels of autophagy and influences susceptibility to bacterial infection. PLoS Genet 2012; 8:e1003007; PMID:23093945; http://dx.doi.org/10.1371/journal.pgen.1003007
  • Proenca CC, Stoehr N, Bernhard M, Seger S, Genoud C, Roscic A, Paganetti P, Liu S, Murphy LO, Kuhn R, et al. Atg4b-dependent autophagic flux alleviates Huntington's disease progression. PLoS One 2013; 8:e68357; PMID:23861892; http://dx.doi.org/10.1371/journal.pone.0068357
  • Tran E, Chow A, Goda T, Wong A, Blakely K, Rocha M, Taeb S, Hoang VC, Liu SK, Emmenegger U. Context-dependent role of ATG4B as target for autophagy inhibition in prostate cancer therapy. Biochem Biophys Res Commun 2013; 441:726-31; PMID:24184480; http://dx.doi.org/10.1016/j.bbrc.2013.10.117
  • Betin VM, Singleton BK, Parsons SF, Anstee DJ, Lane JD. Autophagy facilitates organelle clearance during differentiation of human erythroblasts: evidence for a role for ATG4 paralogs during autophagosome maturation. Autophagy 2013; 9:881-93; PMID:23508006; http://dx.doi.org/10.4161/auto.24172
  • Li Y, Luo Q, Yuan L, Miao C, Mu X, Xiao W, Li J, Sun T, Ma E. JNK-dependent Atg4 upregulation mediates asperphenamate derivative BBP-induced autophagy in MCF-7 cells. Toxicol Appl Pharmacol 2012; 263:21-31; PMID:22668848; http://dx.doi.org/10.1016/j.taap.2012.05.018
  • Farfariello V, Amantini C, Santoni G. Transient receptor potential vanilloid 1 activation induces autophagy in thymocytes through ROS-regulated AMPK and Atg4C pathways. J Leukoc Biol 2012; 92:421-31; PMID:22753949; http://dx.doi.org/10.1189/jlb.0312123
  • Korkmaz G, le Sage C, Tekirdag KA, Agami R, Gozuacik D. miR-376b controls starvation and mTOR inhibition-related autophagy by targeting ATG4C and BECN1. Autophagy 2012; 8:165-76; PMID:22248718; http://dx.doi.org/10.4161/auto.8.2.18351
  • Marino G, Salvador-Montoliu N, Fueyo A, Knecht E, Mizushima N, Lopez-Otin C. Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J Biol Chem 2007; 282:18573-83; PMID:17442669; http://dx.doi.org/10.1074/jbc.M701194200
  • Tanida I, Sou YS, Ezaki J, Minematsu-Ikeguchi N, Ueno T, Kominami E. HsAtg4B/HsApg4B/autophagin-1 cleaves the carboxyl termini of three human Atg8 homologues and delipidates microtubule-associated protein light chain 3- and GABAA receptor-associated protein-phospholipid conjugates. J Biol Chem 2004; 279:36268-76; PMID:15187094; http://dx.doi.org/10.1074/jbc.M401461200
  • Satoo K, Noda NN, Kumeta H, Fujioka Y, Mizushima N, Ohsumi Y, Inagaki F. The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. EMBO J 2009; 28:1341-50; PMID:19322194; http://dx.doi.org/10.1038/emboj.2009.80
  • Li M, Hou Y, Wang J, Chen X, Shao ZM, Yin XM. Kinetics comparisons of mammalian Atg4 homologues indicate selective preferences toward diverse Atg8 substrates. J Biol Chem 2011; 286:7327-38; PMID:21177865; http://dx.doi.org/10.1074/jbc.M110.199059
  • Shu CW, Drag M, Bekes M, Zhai D, Salvesen GS, Reed JC. Synthetic substrates for measuring activity of autophagy proteases: autophagins (Atg4). Autophagy 2010; 6:936-47; PMID:20818167; http://dx.doi.org/10.4161/auto.6.7.13075
  • 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; PMID:15169837; http://dx.doi.org/10.1242/jcs.01131
  • 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; PMID:14530254; http://dx.doi.org/10.1074/jbc.M308762200
  • Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
  • Li M, Chen X, Ye QZ, Vogt A, Yin XM. A high-throughput FRET-based assay for determination of Atg4 activity. Autophagy 2012; 8:401-12; PMID:22302004; http://dx.doi.org/10.4161/auto.18777
  • Choi KM, Nam HY, Na JH, Kim SW, Kim SY, Kim K, Kwon IC, Ahn HJ. A monitoring method for Atg4 activation in living cells using peptide-conjugated polymeric nanoparticles. Autophagy 2011; 7:1052-62; PMID:21610316; http://dx.doi.org/10.4161/auto.7.9.16451
  • Mayoral A, Barron H, Estrada-Salas R, Vazquez-Duran A, Jose-Yacaman M. Nanoparticle stability from the nano to the meso interval. Nanoscale 2010; 2:335-42; PMID:20644815; http://dx.doi.org/10.1039/b9nr00287a
  • Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988; 55:1189-93; PMID:2849510; http://dx.doi.org/10.1016/0092-8674(88)90263-2
  • Fawell S, Seery J, Daikh Y, Moore C, Chen LL, Pepinsky B, Barsoum J. Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci U S A 1994; 91:664-8; PMID:8290579; http://dx.doi.org/10.1073/pnas.91.2.664
  • Vives E, Brodin P, Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 1997; 272:16010-7; PMID:9188504; http://dx.doi.org/10.1074/jbc.272.25.16010
  • Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007; 26:1749-60; PMID:17347651; http://dx.doi.org/10.1038/sj.emboj.7601623
  • Wu YT, Tan HL, Shui G, Bauvy C, Huang Q, Wenk MR, Ong CN, Codogno P, Shen HM. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem 2010; 285:10850-61; PMID:20123989; http://dx.doi.org/10.1074/jbc.M109.080796
  • Zois CE, Giatromanolaki A, Sivridis E, Papaiakovou M, Kainulainen H, Koukourakis MI. “Autophagic flux" in normal mouse tissues: focus on endogenous LC3A processing. Autophagy 2011; 7:1371-8; PMID:21997374; http://dx.doi.org/10.4161/auto.7.11.16664
  • Wadia JS, Dowdy SF. Modulation of cellular function by TAT mediated transduction of full length proteins. Curr Protein Pept Sci 2003; 4:97-104; PMID:12678849; http://dx.doi.org/10.2174/1389203033487289
  • Burton PS, Conradi RA, Ho NF, Hilgers AR, Borchardt RT. How structural features influence the biomembrane permeability of peptides. J Pharm Sci 1996; 85:1336-40; PMID:8961149; http://dx.doi.org/10.1021/js960067d
  • Zorko M, Langel U. Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv Drug Deliv Rev 2005; 57:529-45; PMID:15722162; http://dx.doi.org/10.1016/j.addr.2004.10.010
  • Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J Biol Chem 2003; 278:585-90; PMID:12411431; http://dx.doi.org/10.1074/jbc.M209548200
  • Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 2004; 10:310-5; PMID:14770178; http://dx.doi.org/10.1038/nm996
  • Eguchi A, Akuta T, Okuyama H, Senda T, Yokoi H, Inokuchi H, Fujita S, Hayakawa T, Takeda K, Hasegawa M, et al. Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J Biol Chem 2001; 276:26204-10; PMID:11346640; http://dx.doi.org/10.1074/jbc.M010625200
  • Li GH, Li W, Mumper RJ, Nath A. Molecular mechanisms in the dramatic enhancement of HIV-1 Tat transduction by cationic liposomes. FASEB J 2012; 26:2824-34; PMID:22447980; http://dx.doi.org/10.1096/fj.11-203315
  • Miyazaki M, Yoshida S, Sakai K, Zhang QZ, Takeshita M. Quantification of concanavalin A binding to rat brain microsomal membranes detected by fluorescence polarization technique. Biochim Biophys Acta 1998; 1370:235-42; PMID:9545569; http://dx.doi.org/10.1016/S0005-2736(97)00268-X
  • Yamaguchi Y, Matsubara Y, Ochi T, Wakamiya T, Yoshida Z. How the pi conjugation length affects the fluorescence emission efficiency. J Am Chem Soc 2008; 130:13867-9; PMID:18816053; http://dx.doi.org/10.1021/ja8040493
  • Niu SL, Massif C, Ulrich G, Ziessel R, Renard PY, Romieu A. Water-solubilisation and bio-conjugation of a red-emitting BODIPY marker. Org Biomol Chem 2011; 9:66-9; PMID:21088764; http://dx.doi.org/10.1039/c0ob00693a
  • Li CH, Tu SC. Active site hydrophobicity is critical to the bioluminescence activity of Vibrio harveyi luciferase. Biochemistry 2005; 44:12970-7; PMID:16185065; http://dx.doi.org/10.1021/bi050935y
  • Wang R, Deng L, Zhang T, Li J. Substituent effect on the photophysical properties, electrochemical properties and electroluminescence performance of orange-emitting iridium complexes. Dalton Trans 2012; 41:6833-41; PMID:22517492; http://dx.doi.org/10.1039/c2dt12206e
  • Dobek K. The influence of temperature on Coumarin 153 fluorescence kinetics. J Fluoresc 2011; 21:1547-57; PMID:21246263; http://dx.doi.org/10.1007/s10895-011-0843-1
  • Suresh D, Lopes PS, Ferreira B, Figueira CA, Gomes CS, Gomes PT, Di Paolo RE, Maçanita AL, Duarte MT, Charas A, et al. Tunable fluorophores based on 2-(N-arylimino)pyrrolyl chelates of diphenylboron: synthesis, structure, photophysical characterization, and application in OLEDs. Chemistry 2014; 20:4126-40; PMID:24634317; http://dx.doi.org/10.1002/chem.201303607
  • Mocz G, Ross JA. Fluorescence techniques in analysis of protein-ligand interactions. Methods Mol Biol 2013; 1008:169-210; PMID:23729253; http://dx.doi.org/10.1007/978-1-62703-398-5_7
  • Venkatraman P, Nguyen TT, Sainlos M, Bilsel O, Chitta S, Imperiali B, Stern LJ. Fluorogenic probes for monitoring peptide binding to class II MHC proteins in living cells. Nat Chem Biol 2007; 3:222-8; PMID:17351628; http://dx.doi.org/10.1038/nchembio868
  • Montano SJ, Lu J, Gustafsson TN, Holmgren A. Activity assays of mammalian thioredoxin and thioredoxin reductase: fluorescent disulfide substrates, mechanisms, and use with tissue samples. Anal Biochem 2014; 449:139-46; PMID:24374250; http://dx.doi.org/10.1016/j.ab.2013.12.025
  • Ren X, Yang L, Tang F, Yan C, Ren J. Enzyme biosensor based on NAD-sensitive quantum dots. Biosens Bioelectron 2010; 26:271-4; PMID:20627509; http://dx.doi.org/10.1016/j.bios.2010.05.014
  • Alander J, Johansson K, Heuser VD, Farebo H, Jarvliden J, Abe H, Shibata A, Ito M, Ito Y, Morgenstern R. Characterization of a new fluorogenic substrate for microsomal glutathione transferase 1. Anal Biochem 2009; 390:52-6; PMID:19348782; http://dx.doi.org/10.1016/j.ab.2009.03.046
  • Lin JH, Tseng WL. A method for fluorescence sensing of adenosine and alkaline phosphatase based on the inhibition of S-adenosylhomocysteine hydrolase activity. Biosens Bioelectron 2013; 41:379-85; PMID:23040372; http://dx.doi.org/10.1016/j.bios.2012.08.059
  • Sartor G, Pagani R, Ferrari E, Sorbi RT, Cavaggioni A, Cavatorta P, Spisni A. Determining the binding capability of the mouse major urinary proteins using 2-naphthol as a fluorescent probe. Anal Biochem 2001; 292:69-75; PMID:11319819; http://dx.doi.org/10.1006/abio.2001.5065
  • Wang W, Chen Z, Billiar TR, Stang MT, Gao W. The carboxyl-terminal amino acids render pro-human LC3B migration similar to lipidated LC3B in SDS-PAGE. PLoS One 2013; 8:e74222; PMID:24040206; http://dx.doi.org/10.1371/journal.pone.0074222
  • Rothe K, Lin H, Lin KB, Leung A, Wang HM, Malekesmaeili M, Brinkman RR, Forrest DL, Gorski SM, Jiang X. The core autophagy protein ATG4B is a potential biomarker and therapeutic target in CML stem/progenitor cells. Blood 2014; 123:3622-34; PMID:24755409; http://dx.doi.org/10.1182/blood-2013-07-516807
  • De Vries N, De Flora S. N-acetyl-l-cysteine. J Cell Biochem Suppl 1993; 17F:270-7; PMID:8412205; http://dx.doi.org/10.1002/jcb.240531040
  • Sen CK. Redox signaling and the emerging therapeutic potential of thiol antioxidants. Biochem Pharmacol 1998; 55:1747-58; PMID:9714292; http://dx.doi.org/10.1016/S0006-2952(97)00672-2
  • Sun Y, Oberley LW. The inhibition of catalase by glutathione. Free Radic Biol Med 1989; 7:595-602; PMID:2559882; http://dx.doi.org/10.1016/0891-5849(89)90140-8
  • Chen M, Hein S, Le DQ, Feng W, Foss M, Kjems J, Besenbacher F, Zou X, Bünger C. Free radicals generated by tantalum implants antagonize the cytotoxic effect of doxorubicin. Int J Pharm 2013; 448:214-20; PMID:23538094; http://dx.doi.org/10.1016/j.ijpharm.2013.03.041
  • Kaminskyy VO, Zhivotovsky B. Free radicals in cross talk between autophagy and apoptosis. Antioxid Redox Signal 2014; 21:86-102; PMID:24359220; http://dx.doi.org/10.1089/ars.2013.5746
  • Li ZY, Yang Y, Ming M, Liu B. Mitochondrial ROS generation for regulation of autophagic pathways in cancer. Biochem Biophys Res Commun 2011; 414:5-8; PMID:21951851; http://dx.doi.org/10.1016/j.bbrc.2011.09.046
  • Filomeni G, Desideri E, Cardaci S, Rotilio G, Ciriolo MR. Under the ROS…thiol network is the principal suspect for autophagy commitment. Autophagy 2010; 6:999-1005; PMID:20639698; http://dx.doi.org/10.4161/auto.6.7.12754
  • Rafeiro E, Barr SG, Harrison JJ, Racz WJ. Effects of N-acetylcysteine and dithiothreitol on glutathione and protein thiol replenishment during acetaminophen-induced toxicity in isolated mouse hepatocytes. Toxicology 1994; 93:209-24; PMID:7974515; http://dx.doi.org/10.1016/0300-483X(94)90079-5
  • Parasassi T, Brunelli R, Costa G, De Spirito M, Krasnowska E, Lundeberg T, Pittaluga E, Ursini F. Thiol redox transitions in cell signaling: a lesson from N-acetylcysteine. ScientificWorldJournal 2010; 10:1192-202; PMID:20602078; http://dx.doi.org/10.1100/tsw.2010.104
  • Lopes de Almeida JP, Saldanha C. Dithiothreitol revisited in red cells: a new head for an old hat. Clin Hemorheol Microcirc 2010; 46:51-6; PMID:20852362
  • Chaubey S, Grover M, Tatu U. Endoplasmic reticulum stress triggers gametocytogenesis in the malaria parasite. J Biol Chem 2014; 289:16662-74; PMID:24755215; http://dx.doi.org/10.1074/jbc.M114.551549
  • Li B, Yi P, Zhang B, Xu C, Liu Q, Pi Z, Xu X, Chevet E, Liu J. Differences in endoplasmic reticulum stress signalling kinetics determine cell survival outcome through activation of MKP-1. Cell Signal 2011; 23:35-45; PMID:20727407; http://dx.doi.org/10.1016/j.cellsig.2010.07.019
  • Lai CW, Aronson DE, Snapp EL. BiP availability distinguishes states of homeostasis and stress in the endoplasmic reticulum of living cells. Mol Biol Cell 2010; 21:1909-21; PMID:20410136; http://dx.doi.org/10.1091/mbc.E09-12-1066
  • Ni Z, Wang B, Dai X, Ding W, Yang T, Li X, Lewin S, Xu L, Lian J, He F. HCC cells with high levels of Bcl-2 are resistant to ABT-737 via activation of the ROS-JNK-autophagy pathway. Free Radic Biol Med 2014; 70:194-203; PMID:24576507; http://dx.doi.org/10.1016/j.freeradbiomed.2014.02.012

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.