ABHD10 is an S-depalmitoylase affecting redox homeostasis through peroxiredoxin-5

Cao, Yang; Qiu, Tian; Kathayat, Rahul S.; Azizi, Saara-Anne; Thorne, Anneke K.; Ahn, Daniel; Fukata, Yuko; Fukata, Masaki; Rice, Phoebe A.; Dickinson, Bryan C.

doi:10.1038/s41589-019-0399-y

Title: ABHD10 is an S-depalmitoylase affecting redox homeostasis through peroxiredoxin-5

Journal Article · 18 November 2019 · Nature Chemical Biology

DOI: https://doi.org/10.1038/s41589-019-0399-y · OSTI ID:1576007

^[1]; Qiu, Tian ^[1];

^[1]; Azizi, Saara-Anne ^[1]; Thorne, Anneke K. ^[1]; Ahn, Daniel ^[1];

^[2];

^[2]; Rice, Phoebe A. ^[1];

^[1]

Univ. of Chicago, IL (United States)
National Institutes of Natural Sciences, Okazaki (Japan)

We discuss how S-Palmitoylation is a reversible lipid post-translational modification that has been observed on mitochondrial proteins, but both the regulation and functional consequences of mitochondrial S-palmitoylation are poorly understood. Here, we show that perturbing the ‘erasers’ of S-palmitoylation, acyl protein thioesterases (APTs), with either pan-active inhibitors or a mitochondrial-targeted APT inhibitor, diminishes the antioxidant buffering capacity of mitochondria. Surprisingly, this effect was not mediated by the only known mitochondrial APT, but rather by a resident mitochondrial protein with no known endogenous function, ABHD10. We show that ABHD10 is a member of the APT family of regulatory proteins and identify peroxiredoxin-5 (PRDX5), a key antioxidant protein, as a target of ABHD10 S-depalmitoylase activity. We then find that ABHD10 regulates the S-palmitoylation status of the nucleophilic active site residue of PRDX5, providing a direct mechanistic connection between ABHD10-mediated S-depalmitoylation of PRDX5 and its antioxidant capacity.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division

Contributing Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1576007

Journal Information:: Nature Chemical Biology, Journal Name: Nature Chemical Biology Journal Issue: 12 Vol. 15; ISSN 1552-4450

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (61)

Raptorx: Exploiting structure information for protein alignment by statistical inference Peng, Jian; Xu, Jinbo Proteins: Structure, Function, and Bioinformatics, Vol. 79, Issue S10 https://doi.org/10.1002/prot.23175	journal	January 2011
Use of an aqueous soluble tetrazolium/formazan assay to measure viability and proliferation of lymphokine-dependent cell lines Buttke, Thomas M.; McCubrey, James A.; Owen, Terence C. Journal of Immunological Methods, Vol. 157, Issue 1-2 https://doi.org/10.1016/0022-1759(93)90092-L	journal	January 1993
Crystal Structure of the Human Acyl Protein Thioesterase I from a Single X-Ray Data Set to 1.5 Å Devedjiev, Yancho; Dauter, Zbigniew; Kuznetsov, Sergey R. Structure, Vol. 8, Issue 11 https://doi.org/10.1016/S0969-2126(00)00529-3	journal	November 2000
Importin α Partitioning to the Plasma Membrane Regulates Intracellular Scaling Brownlee, Christopher; Heald, Rebecca Cell, Vol. 176, Issue 4 https://doi.org/10.1016/j.cell.2018.12.001	journal	February 2019
Synthetic Fluorogenic Peptides Reveal Dynamic Substrate Specificity of Depalmitoylases Amara, Neri; Foe, Ian T.; Onguka, Ouma Cell Chemical Biology, Vol. 26, Issue 1 https://doi.org/10.1016/j.chembiol.2018.10.005	journal	January 2019
Mitochondrial localization and function of a subset of 22q11 deletion syndrome candidate genes Maynard, T. M.; Meechan, D. W.; Dudevoir, M. L. Molecular and Cellular Neuroscience, Vol. 39, Issue 3 https://doi.org/10.1016/j.mcn.2008.07.027	journal	October 2008
Dynamic Protein Acylation: New Substrates, Mechanisms, and Drug Targets Lanyon-Hogg, Thomas; Faronato, Monica; Serwa, Remigiusz A. Trends in Biochemical Sciences, Vol. 42, Issue 7 https://doi.org/10.1016/j.tibs.2017.04.004	journal	July 2017
A Fluorescent Probe with Improved Water Solubility Permits the Analysis of Protein S -Depalmitoylation Activity in Live Cells Qiu, Tian; Kathayat, Rahul S.; Cao, Yang Biochemistry, Vol. 57, Issue 2 https://doi.org/10.1021/acs.biochem.7b00835	journal	October 2017
Mitochondria-Targeted Triphenylphosphonium-Based Compounds: Syntheses, Mechanisms of Action, and Therapeutic and Diagnostic Applications Zielonka, Jacek; Joseph, Joy; Sikora, Adam Chemical Reviews, Vol. 117, Issue 15 https://doi.org/10.1021/acs.chemrev.7b00042	journal	June 2017
Redox Signaling by Reactive Electrophiles and Oxidants Parvez, Saba; Long, Marcus J. C.; Poganik, Jesse R. Chemical Reviews, Vol. 118, Issue 18 https://doi.org/10.1021/acs.chemrev.7b00698	journal	August 2018
Selective Enrichment and Direct Analysis of Protein S-Palmitoylation Sites Thinon, Emmanuelle; Fernandez, Joseph P.; Molina, Henrik Journal of Proteome Research, Vol. 17, Issue 5 https://doi.org/10.1021/acs.jproteome.8b00002	journal	March 2018
Molecular Mechanism for Isoform-Selective Inhibition of Acyl Protein Thioesterases 1 and 2 (APT1 and APT2) Won, Sang Joon; Davda, Dahvid; Labby, Kristin J. ACS Chemical Biology, Vol. 11, Issue 12 https://doi.org/10.1021/acschembio.6b00720	journal	October 2016
The Metabolic Serine Hydrolases and Their Functions in Mammalian Physiology and Disease Long, Jonathan Z.; Cravatt, Benjamin F. Chemical Reviews, Vol. 111, Issue 10 https://doi.org/10.1021/cr200075y	journal	October 2011
A Palette of Fluorescent Probes with Varying Emission Colors for Imaging Hydrogen Peroxide Signaling in Living Cells Dickinson, Bryan C.; Huynh, Calvin; Chang, Christopher J. Journal of the American Chemical Society, Vol. 132, Issue 16 https://doi.org/10.1021/ja1014103	journal	April 2010
Competitive Activity-Based Protein Profiling Identifies Aza-β-Lactams as a Versatile Chemotype for Serine Hydrolase Inhibition Zuhl, Andrea M.; Mohr, Justin T.; Bachovchin, Daniel A. Journal of the American Chemical Society, Vol. 134, Issue 11 https://doi.org/10.1021/ja300799t	journal	March 2012
Confirming Target Engagement for Reversible Inhibitors in Vivo by Kinetically Tuned Activity-Based Probes Adibekian, Alexander; Martin, Brent R.; Chang, Jae Won Journal of the American Chemical Society, Vol. 134, Issue 25 https://doi.org/10.1021/ja303400u	journal	June 2012
A Targetable Fluorescent Probe for Imaging Hydrogen Peroxide in the Mitochondria of Living Cells Dickinson, Bryan C.; Chang, Christopher J. Journal of the American Chemical Society, Vol. 130, Issue 30 https://doi.org/10.1021/ja802355u	journal	July 2008
A Targetable Fluorescent Probe for Imaging Hydrogen Peroxide in the Mitochondria of Living Cells Dickinson, Bryan C.; Chang, Christopher J. Journal of the American Chemical Society, Vol. 130, Issue 34 https://doi.org/10.1021/ja805448s	journal	August 2008
S-palmitoylation represents a novel mechanism regulating the mitochondrial targeting of BAX and initiation of apoptosis Fröhlich, M.; Dejanovic, B.; Kashkar, H. Cell Death & Disease, Vol. 5, Issue 2 https://doi.org/10.1038/cddis.2014.17	journal	February 2014
Palmitoylation-dependent activation of MC1R prevents melanomagenesis Chen, Shuyang; Zhu, Bo; Yin, Chengqian Nature, Vol. 549, Issue 7672 https://doi.org/10.1038/nature23887	journal	September 2017
Autopalmitoylation of TEAD proteins regulates transcriptional output of the Hippo pathway Chan, PuiYee; Han, Xiao; Zheng, Baohui Nature Chemical Biology, Vol. 12, Issue 4 https://doi.org/10.1038/nchembio.2036	journal	February 2016
A fluorescent probe for cysteine depalmitoylation reveals dynamic APT signaling Kathayat, Rahul S.; Elvira, Pablo D.; Dickinson, Bryan C. Nature Chemical Biology, Vol. 13, Issue 2 https://doi.org/10.1038/nchembio.2262	journal	December 2016
Small-molecule inhibition of APT1 affects Ras localization and signaling Dekker, Frank J.; Rocks, Oliver; Vartak, Nachiket Nature Chemical Biology, Vol. 6, Issue 6 https://doi.org/10.1038/nchembio.362	journal	April 2010
Large-scale profiling of protein palmitoylation in mammalian cells Martin, Brent R.; Cravatt, Benjamin F. Nature Methods, Vol. 6, Issue 2, p. 135-138 https://doi.org/10.1038/nmeth.1293	journal	January 2009
Global profiling of dynamic protein palmitoylation Martin, Brent R.; Wang, Chu; Adibekian, Alexander Nature Methods, Vol. 9, Issue 1 https://doi.org/10.1038/nmeth.1769	journal	November 2011
Palmitoylated proteins: purification and identification Wan, Junmei; Roth, Amy F.; Bailey, Aaron O. Nature Protocols, Vol. 2, Issue 7 https://doi.org/10.1038/nprot.2007.225	journal	June 2007
A simple and rapid nonviral approach to efficiently transfect primary tissue–derived cells using polyethylenimine Hsu, Charlie Yu Ming; Uludağ, Hasan Nature Protocols, Vol. 7, Issue 5 https://doi.org/10.1038/nprot.2012.038	journal	April 2012
Template-based protein structure modeling using the RaptorX web server Källberg, Morten; Wang, Haipeng; Wang, Sheng Nature Protocols, Vol. 7, Issue 8 https://doi.org/10.1038/nprot.2012.085	journal	July 2012
Active and dynamic mitochondrial S-depalmitoylation revealed by targeted fluorescent probes Kathayat, Rahul S.; Cao, Yang; Elvira, Pablo D. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02655-1	journal	January 2018
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
Selective blockade of the lyso-PS lipase ABHD12 stimulates immune responses in vivo Ogasawara, Daisuke; Ichu, Taka-Aki; Vartabedian, Vincent F. Nature Chemical Biology, Vol. 14, Issue 12 https://doi.org/10.1038/s41589-018-0155-8	journal	November 2018
Structure and function of DHHC protein S-acyltransferases Gottlieb, Colin D.; Linder, Maurine E. Biochemical Society Transactions, Vol. 45, Issue 4 https://doi.org/10.1042/BST20160304	journal	June 2017
Activity-based protein profiling: The serine hydrolases Liu, Y.; Patricelli, M. P.; Cravatt, B. F. Proceedings of the National Academy of Sciences, Vol. 96, Issue 26 https://doi.org/10.1073/pnas.96.26.14694	journal	December 1999
Purification, cDNA Cloning, and Regulation of Lysophospholipase from Rat Liver Sugimoto, Hiroyuki; Hayashi, Hiroaki; Yamashita, Satoshi Journal of Biological Chemistry, Vol. 271, Issue 13 https://doi.org/10.1074/jbc.271.13.7705	journal	March 1996
A Cytoplasmic Acyl-Protein Thioesterase That Removes Palmitate from G Protein α Subunits and p21 ^RAS Duncan, Joseph A.; Gilman, Alfred G. Journal of Biological Chemistry, Vol. 273, Issue 25 https://doi.org/10.1074/jbc.273.25.15830	journal	June 1998
Regulation of Mitochondrial Carbamoyl-phosphate Synthetase 1 Activity by Active Site Fatty Acylation Corvi, Maria M.; Soltys, Carrie-Lynn M.; Berthiaume, Luc G. Journal of Biological Chemistry, Vol. 276, Issue 49 https://doi.org/10.1074/jbc.M102766200	journal	September 2001
Specific Modification of Mitochondrial Protein Thiols in Response to Oxidative Stress: A PROTEOMICS APPROACH Lin, T. -K.; Hughes, G.; Muratovska, A. Journal of Biological Chemistry, Vol. 277, Issue 19 https://doi.org/10.1074/jbc.M110797200	journal	May 2002
Human α/β Hydrolase Domain Containing 10 (ABHD10) Is Responsible Enzyme for Deglucuronidation of Mycophenolic Acid Acyl-glucuronide in Liver Iwamura, Atsushi; Fukami, Tatsuki; Higuchi, Ryota Journal of Biological Chemistry, Vol. 287, Issue 12 https://doi.org/10.1074/jbc.M111.271288	journal	January 2012
Mitochondria Are a Major Source of Paraquat-induced Reactive Oxygen Species Production in the Brain Castello, Pablo R.; Drechsel, Derek A.; Patel, Manisha Journal of Biological Chemistry, Vol. 282, Issue 19 https://doi.org/10.1074/jbc.M700827200	journal	March 2007
Peroxiredoxin 5: Structure, Mechanism, and Function of the Mammalian Atypical 2-Cys Peroxiredoxin Knoops, Bernard; Goemaere, Julie; Van der Eecken, Valérie Antioxidants & Redox Signaling, Vol. 15, Issue 3 https://doi.org/10.1089/ars.2010.3584	journal	August 2011
Palmitoylation signaling: a novel mechanism of mitochondria dynamics and diverse pathologies Tang, Mingzhu; Lu, Liqun; Huang, Zhen Acta Biochimica et Biophysica Sinica, Vol. 50, Issue 8 https://doi.org/10.1093/abbs/gmy065	journal	June 2018
Identification of palmitoylated mitochondrial proteins using a bio-orthogonal azido-palmitate analogue Kostiuk, Morris A.; Corvi, Maria M.; Keller, Bernd O. The FASEB Journal, Vol. 22, Issue 3 https://doi.org/10.1096/fj.07-9199com	journal	March 2008
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
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
An Orphan Esterase ABHD10 Modulates Probenecid Acyl Glucuronidation in Human Liver Ito, Yusuke; Fukami, Tatsuki; Yokoi, Tsuyoshi Drug Metabolism and Disposition, Vol. 42, Issue 12 https://doi.org/10.1124/dmd.114.059485	journal	September 2014
Proteomic Mapping of Mitochondria in Living Cells via Spatially Restricted Enzymatic Tagging Rhee, H. -W.; Zou, P.; Udeshi, N. D. Science, Vol. 339, Issue 6125 https://doi.org/10.1126/science.1230593	journal	January 2013
Multiple Functions and Regulation of Mammalian Peroxiredoxins Rhee, Sue Goo; Kil, In Sup Annual Review of Biochemistry, Vol. 86, Issue 1 https://doi.org/10.1146/annurev-biochem-060815-014431	journal	June 2017
Mitochondrial Reactive Oxygen Species (ROS) and ROS-Induced ROS Release Zorov, Dmitry B.; Juhaszova, Magdalena; Sollott, Steven J. Physiological Reviews, Vol. 94, Issue 3 https://doi.org/10.1152/physrev.00026.2013	journal	July 2014
SwissPalm: Protein Palmitoylation database Blanc, Mathieu; David, Fabrice; Abrami, Laurence F1000Research, Vol. 4 https://doi.org/10.12688/f1000research.6464.1	journal	January 2015
Development of an activity-based probe for acyl-protein thioesterases Garland, Megan; Schulze, Christopher J.; Foe, Ian T. PLOS ONE, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pone.0190255	journal	January 2018
Identification of PSD-95 Depalmitoylating Enzymes Yokoi, Norihiko; Fukata, Yuko; Sekiya, Atsushi The Journal of Neuroscience, Vol. 36, Issue 24 https://doi.org/10.1523/JNEUROSCI.0419-16.2016	journal	June 2016
Mitochondrial localization and function of a subset of 22q11 deletion syndrome candidate genes D. W., Meechan,; C. C., Heindel,; M. L., Dudevoir, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/gmeq-0841	text	January 2008
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
S-palmitoylation represents a novel mechanism regulating the mitochondrial targeting of BAX and initiation of apoptosis Fröhlich, Michael; Dejanovic, Borislav; Kaskhar, Hamid Universität Stuttgart https://doi.org/10.18419/opus-8169	collection	January 2014
Protein Palmitoylation and Its Role in Bacterial and Viral Infections Sobocińska, Justyna; Roszczenko-Jasińska, Paula; Ciesielska, Anna Frontiers in Immunology, Vol. 8 https://doi.org/10.3389/fimmu.2017.02003	journal	January 2018
Insights Into Protein S-Palmitoylation in Synaptic Plasticity and Neurological Disorders: Potential and Limitations of Methods for Detection and Analysis Zaręba-Kozioł, Monika; Figiel, Izabela; Bartkowiak-Kaczmarek, Anna Frontiers in Molecular Neuroscience, Vol. 11 https://doi.org/10.3389/fnmol.2018.00175	journal	May 2018
Peroxiredoxin proteins protect MCF-7 breast cancer cells from doxorubicin-induced toxicity McDONALD, C.; Muhlbauer, J.; Perlmutter, G. International Journal of Oncology, Vol. 45, Issue 1 https://doi.org/10.3892/ijo.2014.2398	journal	April 2014
ABHD17 proteins are novel protein depalmitoylases that regulate N-Ras palmitate turnover and subcellular localization Lin, David Tse Shen; Conibear, Elizabeth eLife, Vol. 4 https://doi.org/10.7554/eLife.11306	journal	December 2015
Wnt5a signaling induced phosphorylation increases APT1 activity and promotes melanoma metastatic behavior Sadeghi, Rochelle Shirin; Kulej, Katarzyna; Kathayat, Rahul Singh eLife, Vol. 7 https://doi.org/10.7554/eLife.34362	journal	April 2018

Similar Records

Molecular Mechanism for Isoform-Selective Inhibition of Acyl Protein Thioesterases 1 and 2 (APT1 and APT2)

Journal Article · 2016 · ACS Chemical Biology · OSTI ID:1339742

Won, Sang Joon; Davda, Dahvid; Labby, Kristin J.; +14 more

Contribution of liver mitochondrial membrane-bound glutathione transferase to mitochondrial permeability transition pores

Journal Article · 2009 · Toxicology and Applied Pharmacology · OSTI ID:21182734

Hossain, Quazi Sohel; Ulziikhishig, Enkhbaatar; Lee, Kang Kwang; +2 more

Palmitoylation Regulates Epidermal Homeostasis and Hair Follicle Differentiation

Journal Article · 2009 · PLoS Genetics · OSTI ID:1627280

Mill, Pleasantine; Lee, Angela W. S.; Fukata, Yuko; +7 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES

Title: ABHD10 is an S-depalmitoylase affecting redox homeostasis through peroxiredoxin-5

Citation Formats

References (61)

Similar Records

Related Subjects