Structural and functional analysis of the GABARAP interaction motif (GIM)

Rogov, Vladimir V.; Stolz, Alexandra; Ravichandran, Arvind C.; Rios‐Szwed, Diana O.; Suzuki, Hironori; Kniss, Andreas; Lohr, Frank; Wakatsuki, Soichi; Dotsch, Volker; Dikic, Ivan; Dobson, Renwick C. J.; McEwan, David G.

doi:10.15252/embr.201643587

Title: Structural and functional analysis of the GABARAP interaction motif (GIM)

Journal Article · Tue Jun 27 00:00:00 EDT 2017 · EMBO Reports

DOI:https://doi.org/10.15252/embr.201643587· OSTI ID:1390293

Rogov, Vladimir V. ^[1]; Stolz, Alexandra ^[2]; Ravichandran, Arvind C. ^[3]; Rios‐Szwed, Diana O. ^[4]; Suzuki, Hironori ^[5]; Kniss, Andreas ^[1]; Lohr, Frank ^[1]; Wakatsuki, Soichi ^[6]; Dotsch, Volker ^[1];

^[7];

^[8];

^[9]

Goethe Univ., Frankfurt am Main (Germany)
Goethe Univ. School of Medicine, Frankfurt (Main) (Germany)
Univ. of Canterbury, Christchurch (New Zealand)
Univ. of Dundee, Dundee (United Kingdom)
Univ. of Canterbury, Christchurch (New Zealand); High Energy Accelerator Research Organization (KEK), Tsukuba Ibaraki (Japan)
High Energy Accelerator Research Organization (KEK), Tsukuba Ibaraki (Japan); SLAC National Accelerator Lab., Menlo Park, CA (United States); Structural Biology (School of Medicine), Stanford, CA (United States)
Goethe Univ. School of Medicine, Frankfurt (Main) (Germany); Goethe Univ., Frankfurt am Main (Germany)
Univ. of Canterbury, Christchurch (New Zealand); Univ. of Melbourne, Parkville, VIC (Australia)
Goethe Univ. School of Medicine, Frankfurt (Main) (Germany); Univ. of Dundee, Dundee (United Kingdom)

Through the canonical LC3 interaction motif (LIR), [W/F/Y]–X₁–X₂[I/L/V], protein complexes are recruited to autophagosomes to perform their functions as either autophagy adaptors or receptors. How these adaptors/receptors selectively interact with either LC3 or GABARAP families remains unclear. Herein, we determine the range of selectivity of 30 known core LIR motifs towards individual LC3s and GABARAPs. From these, we define a GABARAP Interaction Motif (GIM) sequence ([W/F]–[V/I]–X₂–V) that the adaptor protein PLEKHM1 tightly conforms to. Using biophysical and structural approaches, we show that the PLEKHM1–LIR is indeed 11–fold more specific for GABARAP than LC3B. Selective mutation of the X₁ and X₂ positions either completely abolished the interaction with all LC3 and GABARAPs or increased PLEKHM1–GIM selectivity 20–fold towards LC3B. Finally, we show that conversion of p62/SQSTM1, FUNDC1 and FIP200 LIRs into our newly defined GIM, by introducing two valine residues, enhances their interaction with endogenous GABARAP over LC3B. In conclusion, the identification of a GABARAP–specific interaction motif will aid the identification and characterization of the expanding array of autophagy receptor and adaptor proteins and their in vivo functions.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-76SF00515; SFB 1177; EXC115; SPP 1580; HFSP RGP55; UOCX1208; W911NF‐11‐1‐0481; UOC1013; UOC1506; FY2012; Az. 10.14.2.208; 202061/Z/16/Z; T16/44

OSTI ID:: 1390293

Journal Information:: EMBO Reports, Vol. 18, Issue 8; ISSN 1469-221X

Publisher:: European Molecular Biology OrganizationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 106 works

Citation information provided by
Web of Science

References (50)

Selective autophagy mediated by autophagic adapter proteins Johansen, Terje; Lamark, Trond Autophagy, Vol. 7, Issue 3 https://doi.org/10.4161/auto.7.3.14487	journal	March 2011
Organellophagy: Eliminating cellular building blocks via selective autophagy Okamoto, Koji The Journal of Cell Biology, Vol. 205, Issue 4 https://doi.org/10.1083/jcb.201402054	journal	May 2014
Interactions between Autophagy Receptors and Ubiquitin-like Proteins Form the Molecular Basis for Selective Autophagy Rogov, Vladimir; Dötsch, Volker; Johansen, Terje Molecular Cell, Vol. 53, Issue 2 https://doi.org/10.1016/j.molcel.2013.12.014	journal	January 2014
Regulation of endoplasmic reticulum turnover by selective autophagy Khaminets, Aliaksandr; Heinrich, Theresa; Mari, Muriel Nature, Vol. 522, Issue 7556 https://doi.org/10.1038/nature14498	journal	June 2015
A ubiquitin-like system mediates protein lipidation Ichimura, Yoshinobu; Kirisako, Takayoshi; Takao, Toshifumi Nature, Vol. 408, Issue 6811 https://doi.org/10.1038/35044114	journal	November 2000
Atg8: an autophagy-related ubiquitin-like protein family Shpilka, Tomer; Weidberg, Hilla; Pietrokovski, Shmuel Genome Biology, Vol. 12, Issue 7 https://doi.org/10.1186/gb-2011-12-7-226	journal	January 2011
p62/SQSTM1 Binds Directly to Atg8/LC3 to Facilitate Degradation of Ubiquitinated Protein Aggregates by Autophagy Pankiv, Serhiy; Clausen, Terje Høyvarde; Lamark, Trond Journal of Biological Chemistry, Vol. 282, Issue 33 https://doi.org/10.1074/jbc.M702824200	journal	June 2007
A Role for NBR1 in Autophagosomal Degradation of Ubiquitinated Substrates Kirkin, Vladimir; Lamark, Trond; Sou, Yu-Shin Molecular Cell, Vol. 33, Issue 4 https://doi.org/10.1016/j.molcel.2009.01.020	journal	February 2009
Autophagic Clearance of PolyQ Proteins Mediated by Ubiquitin-Atg8 Adaptors of the Conserved CUET Protein Family Lu, Kefeng; Psakhye, Ivan; Jentsch, Stefan Cell, Vol. 158, Issue 3 https://doi.org/10.1016/j.cell.2014.05.048	journal	July 2014
Phosphorylation of the Autophagy Receptor Optineurin Restricts Salmonella Growth Wild, P.; Farhan, H.; McEwan, D. G. Science, Vol. 333, Issue 6039 https://doi.org/10.1126/science.1205405	journal	May 2011
LC3C, Bound Selectively by a Noncanonical LIR Motif in NDP52, Is Required for Antibacterial Autophagy von Muhlinen, Natalia; Akutsu, Masato; Ravenhill, Benjamin J. Molecular Cell, Vol. 48, Issue 3 https://doi.org/10.1016/j.molcel.2012.08.024	journal	November 2012
TBK1 Kinase Addiction in Lung Cancer Cells Is Mediated via Autophagy of Tax1bp1/Ndp52 and Non-Canonical NF-κB Signalling Newman, Alice C.; Scholefield, Caroline L.; Kemp, Alain J. PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0050672	journal	November 2012
Nix is a selective autophagy receptor for mitochondrial clearance Novak, Ivana; Kirkin, Vladimir; McEwan, David G. EMBO reports, Vol. 11, Issue 1 https://doi.org/10.1038/embor.2009.256	journal	December 2009
Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells Liu, Lei; Feng, Du; Chen, Guo Nature Cell Biology, Vol. 14, Issue 2 https://doi.org/10.1038/ncb2422	journal	January 2012
Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy Mancias, Joseph D.; Wang, Xiaoxu; Gygi, Steven P. Nature, Vol. 509, Issue 7498 https://doi.org/10.1038/nature13148	journal	March 2014
Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy: Regulation of Atg1 kinase function Kraft, Claudine; Kijanska, Monika; Kalie, Eyal The EMBO Journal, Vol. 31, Issue 18 https://doi.org/10.1038/emboj.2012.225	journal	August 2012
FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end–directed vesicle transport Pankiv, Serhiy; Alemu, Endalkachew A.; Brech, Andreas The Journal of Cell Biology, Vol. 188, Issue 2 https://doi.org/10.1083/jcb.200907015	journal	January 2010
Rab GTPase-Activating Proteins in Autophagy: Regulation of Endocytic and Autophagy Pathways by Direct Binding to Human ATG8 Modifiers Popovic, D.; Akutsu, M.; Novak, I. Molecular and Cellular Biology, Vol. 32, Issue 9 https://doi.org/10.1128/MCB.06717-11	journal	February 2012
PLEKHM1 Regulates Autophagosome-Lysosome Fusion through HOPS Complex and LC3/GABARAP Proteins McEwan, David G.; Popovic, Doris; Gubas, Andrea Molecular Cell, Vol. 57, Issue 1 https://doi.org/10.1016/j.molcel.2014.11.006	journal	January 2015
CUL3-KBTBD6/KBTBD7 Ubiquitin Ligase Cooperates with GABARAP Proteins to Spatially Restrict TIAM1-RAC1 Signaling Genau, Heide Marika; Huber, Jessica; Baschieri, Francesco Molecular Cell, Vol. 57, Issue 6 https://doi.org/10.1016/j.molcel.2014.12.040	journal	March 2015
The Autophagy Receptor TAX1BP1 and the Molecular Motor Myosin VI Are Required for Clearance of Salmonella Typhimurium by Autophagy Tumbarello, David A.; Manna, Paul T.; Allen, Mark PLOS Pathogens, Vol. 11, Issue 10 https://doi.org/10.1371/journal.ppat.1005174	journal	October 2015
Structural and Functional Analysis of a Novel Interaction Motif within UFM1-activating Enzyme 5 (UBA5) Required for Binding to Ubiquitin-like Proteins and Ufmylation Habisov, Sabrina; Huber, Jessica; Ichimura, Yoshinobu Journal of Biological Chemistry, Vol. 291, Issue 17 https://doi.org/10.1074/jbc.M116.715474	journal	February 2016
Structure and potential function of γ-aminobutyrate type A receptor-associated protein: Structure and function of GABARAP Mohrlüder, Jeannine; Schwarten, Melanie; Willbold, Dieter FEBS Journal, Vol. 276, Issue 18 https://doi.org/10.1111/j.1742-4658.2009.07207.x	journal	August 2009
Atg8-family interacting motif crucial for selective autophagy Noda, Nobuo N.; Ohsumi, Yoshinori; Inagaki, Fuyuhiko FEBS Letters, Vol. 584, Issue 7 https://doi.org/10.1016/j.febslet.2010.01.018	journal	January 2010
ATG8 Family Proteins Act as Scaffolds for Assembly of the ULK Complex: SEQUENCE REQUIREMENTS FOR LC3-INTERACTING REGION (LIR) MOTIFS Alemu, Endalkachew Ashenafi; Lamark, Trond; Torgersen, Knut Martin Journal of Biological Chemistry, Vol. 287, Issue 47 https://doi.org/10.1074/jbc.M112.378109	journal	October 2012
Structural determinants in GABARAP required for the selective binding and recruitment of ALFY to LC3B-positive structures Lystad, A. H.; Ichimura, Y.; Takagi, K. EMBO reports, Vol. 15, Issue 5 https://doi.org/10.1002/embr.201338003	journal	March 2014
FYCO1 Contains a C-terminally Extended, LC3A/B-preferring LC3-interacting Region (LIR) Motif Required for Efficient Maturation of Autophagosomes during Basal Autophagy Olsvik, Hallvard L.; Lamark, Trond; Takagi, Kenji Journal of Biological Chemistry, Vol. 290, Issue 49 https://doi.org/10.1074/jbc.M115.686915	journal	October 2015
GABARAP activates ULK1 and traffics from the centrosome dependent on Golgi partners WAC and GOLGA2/GM130 Joachim, Justin; Tooze, Sharon A. Autophagy, Vol. 12, Issue 5 https://doi.org/10.1080/15548627.2016.1159368	journal	March 2016
LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis Weidberg, Hilla; Shvets, Elena; Shpilka, Tomer The EMBO Journal, Vol. 29, Issue 11 https://doi.org/10.1038/emboj.2010.74	journal	April 2010
Characterization of the Interaction of GABARAPL-1 with the LIR Motif of NBR1 Rozenknop, Alexis; Rogov, Vladimir V.; Rogova, Natalia Yu. Journal of Molecular Biology, Vol. 410, Issue 3 https://doi.org/10.1016/j.jmb.2011.05.003	journal	July 2011
Structural basis for phosphorylation-triggered autophagic clearance of Salmonella Rogov, Vladimir V.; Suzuki, Hironori; Fiskin, Evgenij Biochemical Journal, Vol. 454, Issue 3 https://doi.org/10.1042/BJ20121907	journal	August 2013
Cargo recognition and trafficking in selective autophagy Stolz, Alexandra; Ernst, Andreas; Dikic, Ivan Nature Cell Biology, Vol. 16, Issue 6 https://doi.org/10.1038/ncb2979	journal	May 2014
Actin nucleation by WH2 domains at the autophagosome Coutts, Amanda S.; La Thangue, Nicholas B. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8888	journal	July 2015
Structural Basis of the Differential Function of the Two C. elegans Atg8 Homologs, LGG-1 and LGG-2, in Autophagy Wu, Fan; Watanabe, Yasunori; Guo, Xiang-Yang Molecular Cell, Vol. 60, Issue 6 https://doi.org/10.1016/j.molcel.2015.11.019	journal	December 2015
Atg8 family LC3/GABARAP proteins are crucial for autophagosome–lysosome fusion but not autophagosome formation during PINK1/Parkin mitophagy and starvation Nguyen, Thanh Ngoc; Padman, Benjamin Scott; Usher, Joanne The Journal of Cell Biology, Vol. 215, Issue 6 https://doi.org/10.1083/jcb.201607039	journal	November 2016
Defective recognition of LC3B by mutant SQSTM1/p62 implicates impairment of autophagy as a pathogenic mechanism in ALS-FTLD Goode, Alice; Butler, Kevin; Long, Jed Autophagy, Vol. 12, Issue 7 https://doi.org/10.1080/15548627.2016.1170257	journal	May 2016
Structural basis for the phosphorylation of FUNDC1 LIR as a molecular switch of mitophagy Kuang, Yao; Ma, Kaili; Zhou, Changqian Autophagy, Vol. 12, Issue 12 https://doi.org/10.1080/15548627.2016.1238552	journal	September 2016
Structural Basis of the Autophagy-Related LC3/Atg13 LIR Complex: Recognition and Interaction Mechanism Suzuki, Hironori; Tabata, Keisuke; Morita, Eiji Structure, Vol. 22, Issue 1 https://doi.org/10.1016/j.str.2013.09.023	journal	January 2014
A Universal Expression Tag for Structural and Functional Studies of Proteins Rogov, Vladimir V.; Rozenknop, Alexis; Rogova, Natalia Yu. ChemBioChem, Vol. 13, Issue 7 https://doi.org/10.1002/cbic.201200045	journal	March 2012
TECPR2 Cooperates with LC3C to Regulate COPII-Dependent ER Export Stadel, Daniela; Millarte, Valentina; Tillmann, Kerstin D. Molecular Cell, Vol. 60, Issue 1 https://doi.org/10.1016/j.molcel.2015.09.010	journal	October 2015
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
How good are my data and what is the resolution? Evans, Philip R.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000061	journal	June 2013
Molecular replacement with MOLREP Vagin, Alexei; Teplyakov, Alexei Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042589	journal	December 2009
Solving structures of protein complexes by molecular replacement with Phaser McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 1 https://doi.org/10.1107/S0907444906045975	journal	December 2006
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Structural basis for the phosphorylation of FUNDC1 LIR as a molecular switch of mitophagy Kuang, Yao; Ma, Kaili; Zhou, Changqian Taylor & Francis https://doi.org/10.6084/m9.figshare.4126647.v1	text	January 2016
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010

Cited By (40)

Ankyrin-G regulates forebrain connectivity and network synchronization via interaction with GABARAP Nelson, A. D.; Caballero-Florán, R. N.; Rodríguez Díaz, J. C. Molecular Psychiatry, Vol. 25, Issue 11 https://doi.org/10.1038/s41380-018-0308-x	journal	November 2018
LC3/GABARAPs drive ubiquitin-independent recruitment of Optineurin and NDP52 to amplify mitophagy Padman, Benjamin Scott; Nguyen, Thanh Ngoc; Uoselis, Louise Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08335-6	journal	January 2019
Autophagy regulates lipid metabolism through selective turnover of NCoR1 Saito, Tetsuya; Kuma, Akiko; Sugiura, Yuki Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08829-3	journal	April 2019
Molecular determinants regulating selective binding of autophagy adapters and receptors to ATG8 proteins Wirth, Martina; Zhang, Wenxin; Razi, Minoo Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10059-6	journal	May 2019
Selective autophagy maintains centrosome integrity and accurate mitosis by turnover of centriolar satellites Holdgaard, Søs Grønbæk; Cianfanelli, Valentina; Pupo, Emanuela Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12094-9	journal	September 2019
A brief history of autophagy from cell biology to physiology and disease Mizushima, Noboru Nature Cell Biology, Vol. 20, Issue 5 https://doi.org/10.1038/s41556-018-0092-5	journal	April 2018
Host–pathogen interactions and subversion of autophagy McEwan, David G. Essays in Biochemistry, Vol. 61, Issue 6 https://doi.org/10.1042/ebc20170058	journal	December 2017
A helical LC3-interacting region mediates the interaction between the retroviral restriction factor Trim5α and mammalian autophagy-related ATG8 proteins Keown, Jeremy R.; Black, Moyra M.; Ferron, Aaron Journal of Biological Chemistry, Vol. 293, Issue 47 https://doi.org/10.1074/jbc.ra118.004202	journal	October 2018
Time-resolved FRET and NMR analyses reveal selective binding of peptides containing the LC3-interacting region to ATG8 family proteins Atkinson, Jennifer M.; Ye, Yansheng; Gebru, Melat T. Journal of Biological Chemistry, Vol. 294, Issue 38 https://doi.org/10.1074/jbc.ra119.008723	journal	July 2019
iLIR@viral: A web resource for LIR motif-containing proteins in viruses Jacomin, Anne-Claire; Samavedam, Siva; Charles, Hannah Autophagy, Vol. 13, Issue 10 https://doi.org/10.1080/15548627.2017.1356978	journal	August 2017
GABARAPs and LC3s have opposite roles in regulating ULK1 for autophagy induction Grunwald, Douglas S.; Otto, Neil Michael; Park, Ji-Man Autophagy https://doi.org/10.1080/15548627.2019.1632620	journal	June 2019
Human ubiquitin-like proteins as central coordinators in autophagy Mohan, Jagan; Wollert, Thomas Interface Focus, Vol. 8, Issue 5 https://doi.org/10.1098/rsfs.2018.0025	journal	August 2018
Molecular interplay of autophagy and endocytosis in human health and diseases Mahapatra, Kewal K.; Panigrahi, Debasna P.; Praharaj, Prakash P. Biological Reviews https://doi.org/10.1111/brv.12515	journal	April 2019
ER‐phagy: shaping up and destressing the endoplasmic reticulum Wilkinson, Simon The FEBS Journal https://doi.org/10.1111/febs.14932	journal	June 2019
Autophagy and autophagy-related proteins in cancer Li, Xiaohua; He, Shikun; Ma, Binyun Molecular Cancer, Vol. 19, Issue 1 https://doi.org/10.1186/s12943-020-1138-4	journal	January 2020
ER-phagy at a glance Grumati, Paolo; Dikic, Ivan; Stolz, Alexandra Journal of Cell Science, Vol. 131, Issue 17 https://doi.org/10.1242/jcs.217364	journal	September 2018
N-terminal β-strand underpins biochemical specialization of an ATG8 isoform Zess, Erin K.; Jensen, Cassandra; Cruz-Mireles, Neftaly PLOS Biology, Vol. 17, Issue 7 https://doi.org/10.1371/journal.pbio.3000373	journal	July 2019
A selective ER ‐phagy exerts procollagen quality control via a Calnexin‐ FAM 134B complex Forrester, Alison; De Leonibus, Chiara; Grumati, Paolo The EMBO Journal, Vol. 38, Issue 2 https://doi.org/10.15252/embj.201899847	journal	November 2018
Mammalian Atg8 proteins regulate lysosome and autolysosome biogenesis through SNARE s Gu, Yuexi; Princely Abudu, Yakubu; Kumar, Suresh The EMBO Journal, Vol. 38, Issue 22 https://doi.org/10.15252/embj.2019101994	journal	October 2019
A conserved ATG2‐GABARAP family interaction is critical for phagophore formation Bozic, Mihaela; van den Bekerom, Luuk; Milne, Beth A. EMBO reports, Vol. 21, Issue 3 https://doi.org/10.15252/embr.201948412	journal	February 2020
The Multifaceted Roles of Autophagy in Flavivirus-Host Interactions Ke, Po-Yuan International Journal of Molecular Sciences, Vol. 19, Issue 12 https://doi.org/10.3390/ijms19123940	journal	December 2018
Epstein–Barr Virus BALF0 and BALF1 Modulate Autophagy Shao, Zhouwulin; Borde, Chloé; Quignon, Frédérique Viruses, Vol. 11, Issue 12 https://doi.org/10.3390/v11121099	journal	November 2019
Members of the autophagy class III phosphatidylinositol 3-kinase complex I interact with GABARAP and GABARAPL1 via LIR motifs Birgisdottir, Åsa Birna; Mouilleron, Stephane; Bhujabal, Zambarlal Taylor & Francis https://doi.org/10.6084/m9.figshare.7726157.v1	text	January 2019
Human LC3 and GABARAP subfamily members achieve functional specificity via specific structural modulations Jatana, Nidhi; Ascher, David B.; Pires, Douglas E. V. Taylor & Francis https://doi.org/10.6084/m9.figshare.7992503.v1	text	January 2019
An atypical LIR motif within UBA5 (ubiquitin like modifier activating enzyme 5) interacts with GABARAP proteins and mediates membrane localization of UBA5 Huber, Jessica; Obata, Miki; Gruber, Jens Taylor & Francis https://doi.org/10.6084/m9.figshare.7999352	text	January 2019
Emerging lysosomal pathways for quality control at the endoplasmic reticulum De Leonibus, Chiara; Cinque, Laura; Settembre, Carmine FEBS Letters, Vol. 593, Issue 17 https://doi.org/10.1002/1873-3468.13571	journal	August 2019
ER-phagy and human diseases Hübner, Christian A.; Dikic, Ivan Cell Death & Differentiation, Vol. 27, Issue 3 https://doi.org/10.1038/s41418-019-0444-0	journal	October 2019
Molecular determinants regulating selective binding of autophagy adapters and receptors to ATG8 proteins. Wirth, Martina; Zhang, Wenxin; Razi, Minoo The Francis Crick Institute https://doi.org/10.25418/crick.11538312	text	January 2020
Dynamic Regulation of the 26S Proteasome: From Synthesis to Degradation Marshall, Richard S.; Vierstra, Richard D. Frontiers in Molecular Biosciences, Vol. 6 https://doi.org/10.3389/fmolb.2019.00040	journal	June 2019
Members of the autophagy class III phosphatidylinositol 3-kinase complex I interact with GABARAP and GABARAPL1 via LIR motifs Birgisdottir, Åsa Birna; Mouilleron, Stephane; Bhujabal, Zambarlal Taylor & Francis https://doi.org/10.6084/m9.figshare.7726157	text	January 2020
GABARAPs and LC3s have opposite roles in regulating ULK1 for autophagy induction Grunwald, Douglas S.; Otto, Neil Michael; Park, Ji-Man Taylor & Francis https://doi.org/10.6084/m9.figshare.8287646	text	January 2019
Members of the autophagy class III phosphatidylinositol 3-kinase complex I interact with GABARAP and GABARAPL1 via LIR motifs Birgisdottir, Åsa Birna; Mouilleron, Stephane; Bhujabal, Zambarlal Autophagy, Vol. 15, Issue 8 https://doi.org/10.1080/15548627.2019.1581009	journal	March 2019
Human LC3 and GABARAP subfamily members achieve functional specificity via specific structural modulations Jatana, Nidhi; Ascher, David B.; Pires, Douglas E. V. Autophagy https://doi.org/10.1080/15548627.2019.1606636	journal	April 2019
An atypical LIR motif within UBA5 (ubiquitin like modifier activating enzyme 5) interacts with GABARAP proteins and mediates membrane localization of UBA5 Huber, Jessica; Obata, Miki; Gruber, Jens Taylor & Francis https://doi.org/10.6084/m9.figshare.7999352.v1	text	January 2019
An atypical LIR motif within UBA5 (ubiquitin like modifier activating enzyme 5) interacts with GABARAP proteins and mediates membrane localization of UBA5 Huber, Jessica; Obata, Miki; Gruber, Jens Autophagy https://doi.org/10.1080/15548627.2019.1606637	journal	April 2019
Members of the autophagy class III phosphatidylinositol 3-kinase complex I interact with GABARAP and GABARAPL1 via LIR motifs Birgisdottir, Åsa Birna; Mouilleron, Stephane; Bhujabal, Zambarlal The Francis Crick Institute https://doi.org/10.25418/crick.11353700	text	January 2019
GABARAPs and LC3s have opposite roles in regulating ULK1 for autophagy induction Grunwald, Douglas S.; Otto, Neil Michael; Park, Ji-Man Taylor & Francis https://doi.org/10.6084/m9.figshare.8287646.v1	text	January 2019
A selective ER-phagy exerts procollagen quality control via a Calnexin-FAM134B complex. Forrester, Alison; De Leonibus, Chiara; Grumati, Paolo EMBO Press https://doi.org/10.7892/boris.130257	text	January 2019
Human LC3 and GABARAP subfamily members achieve functional specificity via specific structural modulations Jatana, Nidhi; Ascher, David B.; Pires, Douglas E. V. Taylor & Francis https://doi.org/10.6084/m9.figshare.7992503.v2	text	January 2020
A selective ER-phagy exerts procollagen quality control via a Calnexin-FAM134B complex Alison, Forrester,; Chiara, De Leonibus,; Paolo, Grumati, ETH Zurich https://doi.org/10.3929/ethz-b-000321162	text	January 2019

Similar Records

LC3B is indispensable for selective autophagy of p62 but not basal autophagy

Journal Article · Fri Mar 28 00:00:00 EDT 2014 · Biochemical and Biophysical Research Communications · OSTI ID:1390293

Maruyama, Yoko; Sou, Yu-Shin; Kageyama, Shun; +5 more

Insights on autophagosome–lysosome tethering from structural and biochemical characterization of human autophagy factor EPG5

Journal Article · Fri Mar 05 00:00:00 EST 2021 · Communications Biology · OSTI ID:1390293

Nam, Sung-Eun; Cheung, Yiu Wing Sunny; Nguyen, Thanh Ngoc; +4 more

Neferine, is not inducer but blocker for macroautophagic flux targeting on lysosome malfunction

Journal Article · Mon Jan 15 00:00:00 EST 2018 · Biochemical and Biophysical Research Communications · OSTI ID:1390293

Xu, Tao; Singh, Deepti; Liu, Jing; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
autophagy
Atg8
GABARAP
LC3
PLEKHM1

Title: Structural and functional analysis of the GABARAP interaction motif (GIM)

Citation Formats

References (50)

Cited By (40)

Similar Records

Related Subjects