Allosteric regulation of lysosomal enzyme recognition by the cation-independent mannose 6-phosphate receptor

Olson, Linda J.; Misra, Sandeep K.; Ishihara, Mayumi; Battaile, Kevin P.; Grant, Oliver C.; Sood, Amika; Woods, Robert J.; Kim, Jung-Ja P.; Tiemeyer, Michael; Ren, Gang; Sharp, Joshua S.; Dahms, Nancy M.

doi:10.1038/s42003-020-01211-w

Allosteric regulation of lysosomal enzyme recognition by the cation-independent mannose 6-phosphate receptor

Journal Article · Wed Sep 09 00:00:00 EDT 2020 · Communications Biology

DOI:https://doi.org/10.1038/s42003-020-01211-w· OSTI ID:1706661

^[1]; ^[2]; Ishihara, Mayumi ^[3]; ^[4]; ^[3]; Sood, Amika ^[3]; Woods, Robert J. ^[3]; ^[1]; Tiemeyer, Michael ^[3]; ^[5]; Sharp, Joshua S. ^[2]; Dahms, Nancy M. ^[1]

Medical College of Wisconsin, Milwaukee, WI (United States)
Univ. of Mississippi, Oxford, MS (United States)
Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
IMCA-CAT, Hauptman-Woodward Medical Research Inst., Argonne, IL (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Foundry

The cation-independent mannose 6-phosphate receptor (CI-MPR, IGF2 receptor or CD222), is a multifunctional glycoprotein required for normal development. Through the receptor’s ability to bind unrelated extracellular and intracellular ligands, it participates in numerous functions including protein trafficking, lysosomal biogenesis, and regulation of cell growth. Clinically, endogenous CI-MPR delivers infused recombinant enzymes to lysosomes in the treatment of lysosomal storage diseases. Although four of the 15 domains comprising CI-MPR’s extracellular region bind phosphorylated glycans on lysosomal enzymes, knowledge of how CI-MPR interacts with ~60 different lysosomal enzymes is limited. Here, we show by electron microscopy and hydroxyl radical protein footprinting that the N-terminal region of CI-MPR undergoes dynamic conformational changes as a consequence of ligand binding and different pH conditions. These data, coupled with X-ray crystallography, surface plasmon resonance and molecular modeling, allow us to propose a model explaining how high-affinity carbohydrate binding is achieved through allosteric domain cooperativity.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: American Cancer Society (ACS); National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1706661

Alternate ID(s):: OSTI ID: 1669123

Journal Information:: Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 3; ISSN 2399-3642

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (74)

Proliferin secreted by cultured cells binds to mannose 6-phosphate receptors. Lee, S. J.; Nathans, D. Journal of Biological Chemistry, Vol. 263, Issue 7 https://doi.org/10.1016/s0021-9258(18)69101-x	journal	March 1988
Accurate determination of local defocus and specimen tilt in electron microscopy Mindell, Joseph A.; Grigorieff, Nikolaus Journal of Structural Biology, Vol. 142, Issue 3 https://doi.org/10.1016/s1047-8477(03)00069-8	journal	June 2003
Demonstration of tumor suppression by mannose 6-phosphate/insulin-like growth factor 2 receptor Li, Jin; Sahagian, G. Gary Oncogene, Vol. 23, Issue 58 https://doi.org/10.1038/sj.onc.1208039	journal	November 2004
Localization of the Carbohydrate Recognition Sites of the Insulin-like Growth Factor II/Mannose 6-Phosphate Receptor to Domains 3 and 9 of the Extracytoplasmic Region Hancock, Michael K.; Yammani, Rama D.; Dahms, Nancy M. Journal of Biological Chemistry, Vol. 277, Issue 49 https://doi.org/10.1074/jbc.m208534200	journal	October 2002
FoXS, FoXSDock and MultiFoXS: Single-state and multi-state structural modeling of proteins and their complexes based on SAXS profiles Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw389	journal	May 2016
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/s0907444910045749	journal	March 2011
Data processing and analysis with the autoPROC toolbox Vonrhein, Clemens; Flensburg, Claus; Keller, Peter Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/s0907444911007773	journal	March 2011
The Biogenesis of Lysosomes Kornfeld, Stuart; Mellman, Ira Annual Review of Cell Biology, Vol. 5, Issue 1 https://doi.org/10.1146/annurev.cb.05.110189.002411	journal	November 1989
Targeting Autophagy in Cancer: Recent Advances and Future Directions Amaravadi, Ravi K.; Kimmelman, Alec C.; Debnath, Jayanta Cancer Discovery, Vol. 9, Issue 9 https://doi.org/10.1158/2159-8290.cd-19-0292	journal	August 2019
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, D.; Svergun, D. I. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/phppubdb-11993	text	January 2009
M6P/IGFII-receptor complexes urokinase receptor and plasminogen for activation of transforming growth factor-β1 Godár, Samuel; Hořejší, Václav; Weidle, Ulrich H. European Journal of Immunology, Vol. 29, Issue 3 https://doi.org/10.1002/(SICI)1521-4141(199903)29:03<1004::AID-IMMU1004>3.0.CO;2-Q	journal	March 1999
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
GLYCAM06: A generalizable biomolecular force field. Carbohydrates: GLYCAM06 Kirschner, Karl N.; Yongye, Austin B.; Tschampel, Sarah M. Journal of Computational Chemistry, Vol. 29, Issue 4 https://doi.org/10.1002/jcc.20820	journal	September 2007
Importance of ligand conformational energies in carbohydrate docking: Sorting the wheat from the chaff Nivedha, Anita K.; Makeneni, Spandana; Foley, Bethany Lachele Journal of Computational Chemistry, Vol. 35, Issue 7 https://doi.org/10.1002/jcc.23517	journal	December 2013
Determination of protein oligomeric structure from small-angle X-ray scattering: Determination of Protein Oligomeric Structure from SAXS Korasick, David A.; Tanner, John J. Protein Science, Vol. 27, Issue 4 https://doi.org/10.1002/pro.3376	journal	February 2018
SPIDER and WEB: Processing and Visualization of Images in 3D Electron Microscopy and Related Fields Frank, Joachim; Radermacher, Michael; Penczek, Pawel Journal of Structural Biology, Vol. 116, Issue 1 https://doi.org/10.1006/jsbi.1996.0030	journal	January 1996
EMAN: Semiautomated Software for High-Resolution Single-Particle Reconstructions Ludtke, Steven J.; Baldwin, Philip R.; Chiu, Wah Journal of Structural Biology, Vol. 128, Issue 1 https://doi.org/10.1006/jsbi.1999.4174	journal	December 1999
Variation in FPOP Measurements Is Primarily Caused by Poor Peptide Signal Intensity Abolhasani Khaje, Niloofar; Mobley, Charles K.; Misra, Sandeep K. Journal of The American Society for Mass Spectrometry, Vol. 29, Issue 9 https://doi.org/10.1007/s13361-018-1994-y	journal	June 2018
Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes Ryckaert, Jean-Paul; Ciccotti, Giovanni; Berendsen, Herman J. C. Journal of Computational Physics, Vol. 23, Issue 3 https://doi.org/10.1016/0021-9991(77)90098-5	journal	March 1977
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
The MRH domain suggests a shared ancestry for the mannose 6-phosphate receptors and other N-glycan-recognising proteins Munro, Sean Current Biology, Vol. 11, Issue 13 https://doi.org/10.1016/S0960-9822(01)00302-5	journal	July 2001
Accurate determination of local defocus and specimen tilt in electron microscopy Mindell, Joseph A.; Grigorieff, Nikolaus Journal of Structural Biology, Vol. 142, Issue 3 https://doi.org/10.1016/S1047-8477(03)00069-8	journal	June 2003
Molecules in focus Insulin-like growth factor II (IGF-II) O'Dell, Sandra D.; Day, Ian N. M. The International Journal of Biochemistry & Cell Biology, Vol. 30, Issue 7 https://doi.org/10.1016/S1357-2725(98)00048-X	journal	July 1998
Pathogenesis and therapies for infantile neuronal ceroid lipofuscinosis (infantile CLN1 disease) Hawkins-Salsbury, Jacqueline A.; Cooper, Jonathan D.; Sands, Mark S. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1832, Issue 11 https://doi.org/10.1016/j.bbadis.2013.05.026	journal	November 2013
Structural investigation of multivalent carbohydrate–protein interactions using synthetic biomolecules Wittmann, Valentin Current Opinion in Chemical Biology, Vol. 17, Issue 6 https://doi.org/10.1016/j.cbpa.2013.10.010	journal	December 2013
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Gctf: Real-time CTF determination and correction Zhang, Kai Journal of Structural Biology, Vol. 193, Issue 1 https://doi.org/10.1016/j.jsb.2015.11.003	journal	January 2016
Carbohydrate recognition by the mannose-6-phosphate receptors Kim, Jung-Ja P.; Olson, Linda J.; Dahms, Nancy M. Current Opinion in Structural Biology, Vol. 19, Issue 5 https://doi.org/10.1016/j.sbi.2009.09.002	journal	October 2009
Evolving SAXS versatility: solution X-ray scattering for macromolecular architecture, functional landscapes, and integrative structural biology Brosey, Chris A.; Tainer, John A. Current Opinion in Structural Biology, Vol. 58 https://doi.org/10.1016/j.sbi.2019.04.004	journal	October 2019
Keeping IGF-II under control: Lessons from the IGF-II–IGF2R crystal structure Brown, James; Jones, E. Yvonne; Forbes, Briony E. Trends in Biochemical Sciences, Vol. 34, Issue 12 https://doi.org/10.1016/j.tibs.2009.07.003	journal	December 2009
Human recombinant palmitoyl-protein thioesterase-1 (PPT1) for preclinical evaluation of enzyme replacement therapy for infantile neuronal ceroid lipofuscinosis Lu, Jui-Yun; Hu, Jie; Hofmann, Sandra L. Molecular Genetics and Metabolism, Vol. 99, Issue 4 https://doi.org/10.1016/j.ymgme.2009.12.002	journal	April 2010
Hydroxyl Radical Dosimetry for High Flux Hydroxyl Radical Protein Footprinting Applications Using a Simple Optical Detection Method Xie, Boer; Sharp, Joshua S. Analytical Chemistry, Vol. 87, Issue 21 https://doi.org/10.1021/acs.analchem.5b02865	journal	July 2015
A Dynamic Model of pH-Induced Protein G ′e Higher Order Structure Changes derived from Mass Spectrometric Analyses Yefremova, Yelena; Al-Majdoub, Mahmoud; Opuni, Kwabena F. M. Analytical Chemistry, Vol. 88, Issue 1 https://doi.org/10.1021/acs.analchem.5b03536	journal	December 2015
ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB Maier, James A.; Martinez, Carmenza; Kasavajhala, Koushik Journal of Chemical Theory and Computation, Vol. 11, Issue 8 https://doi.org/10.1021/acs.jctc.5b00255	journal	July 2015
Domain 5 of the Cation-Independent Mannose 6-Phosphate Receptor Preferentially Binds Phosphodiesters (Mannose 6-Phosphate N -Acetylglucosamine Ester) ^† Chavez, Carrie A.; Bohnsack, Richard N.; Kudo, Mariko Biochemistry, Vol. 46, Issue 44 https://doi.org/10.1021/bi7011806	journal	November 2007
Recognition of Dictyostelium discoideum Lysosomal Enzymes Is Conferred by the Amino-Terminal Carbohydrate Binding Site of the Insulin-like Growth Factor II/Mannose 6-Phosphate Receptor ^† Marron-Terada, Patricia G.; Hancock, Michael K.; Haskins, Darin J. Biochemistry, Vol. 39, Issue 9 https://doi.org/10.1021/bi992226o	journal	March 2000
Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald Salomon-Ferrer, Romelia; Götz, Andreas W.; Poole, Duncan Journal of Chemical Theory and Computation, Vol. 9, Issue 9 https://doi.org/10.1021/ct400314y	journal	August 2013
Chemoenzymatic Synthesis and Receptor Binding of Mannose-6-Phosphate (M6P)-Containing Glycoprotein Ligands Reveal Unusual Structural Requirements for M6P Receptor Recognition Yamaguchi, Takahiro; Amin, Mohammed N.; Toonstra, Christian Journal of the American Chemical Society, Vol. 138, Issue 38 https://doi.org/10.1021/jacs.6b05762	journal	August 2016
Insulin-like growth factor II receptor as a multifunctional binding protein Morgan, David O.; Edman, Jeffrey C.; Standring, David N. Nature, Vol. 329, Issue 6137 https://doi.org/10.1038/329301a0	journal	September 1987
Regulation of embryonic growth and lysosomal targeting by the imprintedIgf2/Mpr gene Wang, Zhao-Qi; Fung, Marion R.; Barlow, Denise P. Nature, Vol. 372, Issue 6505 https://doi.org/10.1038/372464a0	journal	December 1994
The FTMap family of web servers for determining and characterizing ligand-binding hot spots of proteins Kozakov, Dima; Grove, Laurie E.; Hall, David R. Nature Protocols, Vol. 10, Issue 5 https://doi.org/10.1038/nprot.2015.043	journal	April 2015
Emptying the stores: lysosomal diseases and therapeutic strategies Platt, Frances M. Nature Reviews Drug Discovery, Vol. 17, Issue 2 https://doi.org/10.1038/nrd.2017.214	journal	November 2017
Mannose 6-phosphate receptors: new twists in the tale Ghosh, Pradipta; Dahms, Nancy M.; Kornfeld, Stuart Nature Reviews Molecular Cell Biology, Vol. 4, Issue 3 https://doi.org/10.1038/nrm1050	journal	March 2003
Quantitative Protein Topography Measurements by High Resolution Hydroxyl Radical Protein Footprinting Enable Accurate Molecular Model Selection Xie, Boer; Sood, Amika; Woods, Robert J. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-04689-3	journal	July 2017
Structure of uPAR, plasminogen, and sugar-binding sites of the 300 kDa mannose 6-phosphate receptor Olson, Linda J.; Yammani, Rama D.; Dahms, Nancy M. The EMBO Journal, Vol. 23, Issue 10 https://doi.org/10.1038/sj.emboj.7600215	journal	April 2004
Structure and functional analysis of the IGF-II/IGF2R interaction Brown, James; Delaine, Carlie; Zaccheo, Oliver J. The EMBO Journal, Vol. 27, Issue 1 https://doi.org/10.1038/sj.emboj.7601938	journal	November 2007
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
The crystal structure of palmitoyl protein thioesterase 1 and the molecular basis of infantile neuronal ceroid lipofuscinosis Bellizzi, J. J.; Widom, J.; Kemp, C. Proceedings of the National Academy of Sciences, Vol. 97, Issue 9 https://doi.org/10.1073/pnas.080508097	journal	April 2000
Structural basis for recognition of phosphodiester-containing lysosomal enzymes by the cation-independent mannose 6-phosphate receptor Olson, Linda J.; Peterson, Francis C.; Castonguay, Alicia Proceedings of the National Academy of Sciences, Vol. 107, Issue 28 https://doi.org/10.1073/pnas.1004232107	journal	June 2010
The Mannose 6-Phosphate/Insulin-like Growth Factor II Receptor Is a Nanomolar Affinity Receptor for Glycosylated Human Leukemia Inhibitory Factor Blanchard, Frédéric; Raher, Sylvie; Duplomb, Laurence Journal of Biological Chemistry, Vol. 273, Issue 33 https://doi.org/10.1074/jbc.273.33.20886	journal	August 1998
Real Time Kinetics of Insulin-like Growth Factor II (IGF-II) Interaction with the IGF-II/Mannose 6-Phosphate Receptor: THE EFFECTS OF DOMAIN 13 AND pH Linnell, Jane; Groeger, Gillian; Hassan, A. Bassim Journal of Biological Chemistry, Vol. 276, Issue 26 https://doi.org/10.1074/jbc.M100700200	journal	April 2001
Glycan Microarray Analysis of P-type Lectins Reveals Distinct Phosphomannose Glycan Recognition Song, Xuezheng; Lasanajak, Yi; Olson, Linda J. Journal of Biological Chemistry, Vol. 284, Issue 50 https://doi.org/10.1074/jbc.M109.056119	journal	September 2009
Cation-independent Mannose 6-Phosphate Receptor: A COMPOSITE OF DISTINCT PHOSPHOMANNOSYL BINDING SITES Bohnsack, Richard N.; Song, Xuezheng; Olson, Linda J. Journal of Biological Chemistry, Vol. 284, Issue 50 https://doi.org/10.1074/jbc.M109.056184	journal	October 2009
Identification of Residues Essential for Carbohydrate Recognition by the Insulin-like Growth Factor II/Mannose 6-Phosphate Receptor Hancock, Michael K.; Haskins, Darin J.; Sun, Guangjie Journal of Biological Chemistry, Vol. 277, Issue 13 https://doi.org/10.1074/jbc.M109855200	journal	January 2002
Twists and Turns of the Cation-dependent Mannose 6-Phosphate Receptor: LIGAND-BOUND VERSUS LIGAND-FREE RECEPTOR Olson, Linda J.; Zhang, Jian; Dahms, Nancy M. Journal of Biological Chemistry, Vol. 277, Issue 12 https://doi.org/10.1074/jbc.M112230200	journal	January 2002
Localization of the Carbohydrate Recognition Sites of the Insulin-like Growth Factor II/Mannose 6-Phosphate Receptor to Domains 3 and 9 of the Extracytoplasmic Region Hancock, Michael K.; Yammani, Rama D.; Dahms, Nancy M. Journal of Biological Chemistry, Vol. 277, Issue 49 https://doi.org/10.1074/jbc.M208534200	journal	October 2002
The N-terminal Carbohydrate Recognition Site of the Cation-independent Mannose 6-Phosphate Receptor Olson, Linda J.; Dahms, Nancy M.; Kim, Jung-Ja P. Journal of Biological Chemistry, Vol. 279, Issue 32 https://doi.org/10.1074/jbc.M404588200	journal	May 2004
Fast photochemical oxidation of proteins (FPOP): A powerful mass spectrometry–based structural proteomics tool Johnson, Danté T.; Di Stefano, Luciano H.; Jones, Lisa M. Journal of Biological Chemistry, Vol. 294, Issue 32 https://doi.org/10.1074/jbc.REV119.006218	journal	July 2019
Identification of a fourth mannose 6-phosphate binding site in the cation-independent mannose 6-phosphate receptor Olson, Linda J.; Castonguay, Alicia C.; Lasanajak, Yi Glycobiology, Vol. 25, Issue 6 https://doi.org/10.1093/glycob/cwv001	journal	January 2015
Gly-Spec: a webtool for predicting glycan specificity by integrating glycan array screening data and 3D structure Grant, Oliver C.; Xue, Xingran; Ra, Delaram Glycobiology, Vol. 26, Issue 10 https://doi.org/10.1093/glycob/cww094	journal	October 2016
ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids Ashkenazy, H.; Erez, E.; Martz, E. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq399	journal	May 2010
SWISS-MODEL: homology modelling of protein structures and complexes Waterhouse, Andrew; Bertoni, Martino; Bienert, Stefan Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky427	journal	May 2018
Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Lau, M. M.; Stewart, C. E.; Liu, Z. Genes & Development, Vol. 8, Issue 24 https://doi.org/10.1101/gad.8.24.2953	journal	December 1994
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, Daniel; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346 https://doi.org/10.1107/S0021889809000338	journal	January 2009
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
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Data processing and analysis with the autoPROC toolbox Vonrhein, Clemens; Flensburg, Claus; Keller, Peter Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911007773	journal	March 2011
Structural analysis of glycoproteins: building N-linked glycans with Coot Emsley, Paul; Crispin, Max Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 4 https://doi.org/10.1107/S2059798318005119	journal	April 2018
Marked structural rearrangement of mannose 6-phosphate/IGF2 receptor at different pH environments Wang, Rong; Qi, Xiaofeng; Schmiege, Philip Science Advances, Vol. 6, Issue 7 https://doi.org/10.1126/sciadv.aaz1466	journal	February 2020
Enzyme Replacement for Lysosomal Diseases Brady, Roscoe O. Annual Review of Medicine, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.med.57.110104.115650	journal	February 2006
Targeting Autophagy in Cancer: Recent Advances and Future Directions Amaravadi, Ravi K.; Kimmelman, Alec C.; Debnath, Jayanta Cancer Discovery, Vol. 9, Issue 9 https://doi.org/10.1158/2159-8290.CD-19-0292	journal	August 2019
Glycosylation, transport, and complex formation of palmitoyl protein thioesterase 1 (PPT1) – distinct characteristics in neurons Lyly, Annina; von Schantz, Carina; Salonen, Tarja BMC Cell Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2121-8-22	journal	January 2007
Fast Photochemical Oxidation of Proteins Coupled with Mass Spectrometry Shi, Liuqing; Gross, Michael L. Protein & Peptide Letters, Vol. 26, Issue 1 https://doi.org/10.2174/0929866526666181128124554	journal	February 2019

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