Post-Translational Modification Analysis of VDAC1 in ALS-SOD1 Model Cells Reveals Specific Asparagine and Glutamine Deamidation.

{"sci_version": "1.2", "schema": "https://corpus.bntrg.co.uk/sci/1.0/sci.schema.json", "id": "pmid:33276691", "kind": "science-record", "revision": 6, "content_hash": "sha256:e8642ccaac7a3dbdf8d365cf72f0408d157b5e1c50dca44b6d85a4fd59b44485", "created_at": "2026-11-01T15:41:17Z", "updated_at": "2026-11-01T21:24:13Z", "generator": {"name": "corpus-assay-engine", "run_id": "reading-sci-2026-11-01"}, "paper": {"state": "complete", "title": "Post-Translational Modification Analysis of VDAC1 in ALS-SOD1 Model Cells Reveals Specific Asparagine and Glutamine Deamidation.", "doi": "10.3390/antiox9121218", "pmid": "33276691", "authors": ["Maria Gaetana Giovanna Pittalà", "Simona Reina", "Salvatore Antonio Maria Cubisino", "Annamaria Cucina", "Beatrice Formicola", "Vincenzo Cunsolo", "Salvatore Foti", "Rosaria Saletti", "Angela Messina"], "journal": "Antioxidants (Basel, Switzerland)", "year": 2020, "abstract": "Mitochondria from affected tissues of amyotrophic lateral sclerosis (ALS) patients show morphological and biochemical abnormalities. Mitochondrial dysfunction causes oxidative damage and the accumulation of ROS, and represents one of the major triggers of selective death of motor neurons in ALS. We aimed to assess whether oxidative stress in ALS induces post-translational modifications (PTMs) in VDAC1, the main protein of the outer mitochondrial membrane and known to interact with SOD1 mutants related to ALS. In this work, specific PTMs of the VDAC1 protein purified by hydroxyapatite from mitochondria of a NSC34 cell line expressing human SOD1G93A, a suitable ALS motor neuron model, were analyzed by tryptic and chymotryptic proteolysis and UHPLC/High-Resolution ESI-MS/MS. We found selective deamidations of asparagine and glutamine of VDAC1 in ALS-related NSC34-SOD1G93A cells but not in NSC34-SOD1WT or NSC34 cells. In addition, we identified differences in the over-oxidation of methionine and cysteines between VDAC1 purified from ALS model or non-ALS NSC34 cells. The specific range of PTMs identified exclusively in VDAC1 from NSC34-SOD1G93A cells but not from NSC34 control lines, suggests the appearance of important changes to the structure of the VDAC1 channel and therefore to the bioenergetics metabolism of ALS motor neurons. Data are available via ProteomeXchange with identifier <PXD022598>.", "claims": [{"id": "claim-method", "statement": "The latter set of values was sampled with replacement (bootstrapped) 1000 times.", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:33276691", "locator": "sections[8] \"2.5.1. Identification of Deamidation Sites on VDAC1\" paragraph 3", "quote": "The latter set of values was sampled with replacement (bootstrapped) 1000 times."}], "state": "complete"}, {"id": "claim-data-access", "statement": "The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the PRIDE [60] partner repository with the dataset identifier <PXD022598>.", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:33276691", "locator": "sections[22] \"Acknowledgments\" paragraph 2", "quote": "The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the PRIDE [60] partner repository with the dataset identifier <PXD022598>."}], "state": "complete"}], "gaps": []}, "experiment": {"state": "partial", "objective": null, "steps": [{"id": "read_published_estimate", "order": 1, "name": "Read the published estimate from the source", "kind": "other", "state": "complete", "blocked_on": null, "description": "The claim, method and evidence span published with the source article.", "duration_hours": null, "parameters": {}, "inputs": ["source:pmid:33276691"], "outputs": ["the published estimate and its evidence"], "instruments": [], "reagents": []}, {"id": "obtain_source_data", "order": 2, "name": "Obtain the source data from the named repository", "kind": "data-preparation", "state": "blocked", "blocked_on": "data:accession_absent", "description": "The GEO series accession resolves and its sample accessions are listed. This lane did not download the dataset or read its licence.", "duration_hours": null, "parameters": {}, "inputs": [], "outputs": ["the source data with its repository provenance"], "instruments": [], "reagents": []}, {"id": "run_analysis", "order": 3, "name": "Run the published analysis", "kind": "analysis", "state": "complete", "blocked_on": null, "description": "Apply the paper's statistical method to the resolved series and compare the result with the published target.", "duration_hours": null, "parameters": {}, "inputs": [], "outputs": ["the replicated result and its comparison"], "instruments": [], "reagents": []}], "materials": [], "instruments": [], "reagents": [], "conditions": {}, "gaps": ["step:obtain_source_data blocked on data:accession_absent"]}, "data": {"state": "partial", "assets": [{"id": "source:pmid:33276691", "role": "manuscript", "format": "xml", "media_type": "application/xml", "uri": "https://doi.org/10.3390/antiox9121218", "sha256": "sha256:c671922293fb160d44136ef5a3c19edb84184cdcca2bbaa1c0fffe589325b1a1", "bytes": 79763, "access": "open", "state": "resolved", "reader": null, "reader_status": "reader_required", "identifier": "10.3390/antiox9121218", "version": null, "note": "Full article fetched from PMC; the checksum covers the rendered section body, not the original XML bytes.", "structure": {"pmcid": "PMC7761621", "source": "europe_pmc_fulltext", "coverage": "whole_body", "text_hash_scope": "rendered_section_body"}}, {"id": "asset:table:pmid:33276691:1", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:16f0eab708f417b5bc93730af785c31d460d8e245b6cd21e01e70388d123b885", "bytes": 1720, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[14]/table-wrap[1]#antioxidants-09-01218-t001", "version": null, "note": "Ratio of the absolute intensities of the molecular ions of the sulfur-containing tryptic peptides found in the analysis of VDAC1 from NSC34-SOD1G93A cells HTP-preparation reduced with DTT, carboxyamidomethylated and digested in-solution.", "structure": {"pmcid": "PMC7761621", "section_index": 14, "section_title": "3.3. Mass Spectrometry Analysis of VDAC1 from NSC34-SOD1G93A Cell Line", "row_count": 19, "column_count": 6}, "table": {"label": "Table 1", "caption": "Ratio of the absolute intensities of the molecular ions of the sulfur-containing tryptic peptides found in the analysis of VDAC1 from NSC34-SOD1G93A cells HTP-preparation reduced with DTT, carboxyamidomethylated and digested in-solution.", "rows": [["Technical Replicate", "Peptide", "Position in the Sequence", "Measured Monoisotopic m/z", "Absolute Intensity", "Ratio Ox/Red"], ["I", "EHINLGCDVDFDIAGPSIR", "121–139", "1059.9921 (+2)", "8.2 × 105", "29.3"], ["I", "EHINLGCDVDFDIAGPSIR", "710.0155 (+3)", "2.8 × 104"], ["II", "EHINLGCDVDFDIAGPSIR", "1059.9915 (+2)", "6.9 × 105", "19.2"], ["II", "EHINLGCDVDFDIAGPSIR", "710.0140 (+3)", "3.6 × 104"], ["III", "EHINLGCDVDFDIAGPSIR", "1059.9928 (+2)", "7.8 × 105", "23.6"], ["III", "EHINLGCDVDFDIAGPSIR", "710.0140 (+3)", "3.3 × 104"], ["I", "GALVLGYEGWLAGYQMNFETSK", "140–161", "1225.5892 (+2)", "4.5 × 106", "60.0"], ["I", "GALVLGYEGWLAGYQMNFETSK", "1217.5931 (+2)", "7.5 × 104"], ["II", "GALVLGYEGWLAGYQMNFETSK", "1225.5897 (+2)", "4.9 × 106", "71.0"], ["II", "GALVLGYEGWLAGYQMNFETSK", "1217.5913 (+2)", "6.9 × 104"], ["III", "GALVLGYEGWLAGYQMNFETSK", "817.3946 (+3)", "2.8 × 106", "51.9"], ["III", "GALVLGYEGWLAGYQMNFETSK", "812.0656 (+3)", "5.4 × 104"], ["I", "GALVLGYEGWLAGYQMNFETSK", "140–161", "822.7261 (+3)", "2.2 × 105", "2.9"], ["I", "GALVLGYEGWLAGYQMNFETSK", "1217.5931 (+2)", "7.5 × 104"], ["II", "GALVLGYEGWLAGYQMNFETSK", "822.7269 (+3)", "4.5 × 105", "6.5"], ["II", "GALVLGYEGWLAGYQMNFETSK", "1217.5913 (+2)", "6.9 × 104"], ["III", "GALVLGYEGWLAGYQMNFETSK", "822.7277 (+3)", "2.6 × 105", "4.8"], ["III", "GALVLGYEGWLAGYQMNFETSK", "812.0656 (+3)", "5.4 × 104"]], "row_count": 19, "column_count": 6, "numeric_cells": 48, "header_rows": 1, "locator": "section[14]/table-wrap[1]#antioxidants-09-01218-t001"}}, {"id": "asset:table:pmid:33276691:2", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:b93e9176f1c2bb67a3e40081547f5a8040b59e38174a1fb5de39a059d9ae80bf", "bytes": 1502, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[17]/table-wrap[1]#antioxidants-09-01218-t002", "version": null, "note": "Ratio of the absolute intensities of the molecular ions of tryptic peptides containing deamidated against not deamidated amino acids, found in the analysis of VDAC1 from NSC34-SOD1G93A cell HTP-preparation reduced with DTT, carboxyamidomethylated and digested in-solution.", "structure": {"pmcid": "PMC7761621", "section_index": 17, "section_title": "3.4.2. Identification of VDAC1 Deamidation Sites from NSC34-SOD1G93A Cell Line", "row_count": 17, "column_count": 5}, "table": {"label": "Table 2", "caption": "Ratio of the absolute intensities of the molecular ions of tryptic peptides containing deamidated against not deamidated amino acids, found in the analysis of VDAC1 from NSC34-SOD1G93A cell HTP-preparation reduced with DTT, carboxyamidomethylated and digested in-solution.", "rows": [["Peptide", "Position in the Sequence", "Measured Monoisotopic m/z", "Absolute Intensity", "Ratio Deam/Norm"], ["TKSENGLEFTSSGSANTETTK", "33–53", "730.6730 (+3)", "6.3 × 106", "0.02"], ["TKSENGLEFTSSGSANTETTK", "730.3450(+3)", "3.3 × 108"], ["SENGLEFTSSGSANTETTK", "35–53", "654.2921 (+3)", "6.3 × 105", "0.01"], ["SENGLEFTSSGSANTETTK", "980.4425(+2)", "1.4 × 108"], ["LTFDSSFSPNTGKK", "97–110", "510.5876 (+3)", "1.3 × 106", "0.01"], ["LTFDSSFSPNTGKK", "764.8857 (+2)", "9.9 × 107"], ["VTQSNFAVGYK", "164–174", "607.8062 (+2)", "1.4 × 106", "0.002"], ["VTQSNFAVGYK", "607.3142 (+2)", "6.2 × 108"], ["KLETAVNLAWTAGNSNTR", "201–218", "649.6692 (+3)", "9.6 × 106", "0.6"], ["KLETAVNLAWTAGNSNTR", "649.3412 (+3)", "1.6 × 107"], ["LETAVNLAWTAGNSNTR", "202–218", "909.9527(+2)", "6.8 × 105", "0.04"], ["LETAVNLAWTAGNSNTR", "909.4607 (+2)", "1.9 × 107"], ["YQVDPDACFSAK", "225–236", "701.3032(+2)", "1.6 × 106", "0.002"], ["YQVDPDACFSAK", "700.8112(+2)", "7.1 × 108"], ["VNNSSLIGLGYTQTLKPGIK", "237–256", "702.0598 (+3)", "2.4 × 106", "0.03"], ["VNNSSLIGLGYTQTLKPGIK", "701.7318 (+3)", "7.4 × 107"]], "row_count": 17, "column_count": 5, "numeric_cells": 48, "header_rows": 1, "locator": "section[17]/table-wrap[1]#antioxidants-09-01218-t002"}}, {"id": "asset:table:pmid:33276691:3", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:c9d062823187a2d64e6317043e1b6140a54e17b0a468ac758112687a3a39ac60", "bytes": 670, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[17]/table-wrap[2]#antioxidants-09-01218-t003", "version": null, "note": "Asparagine (N) and glutamine (Q) deamidation in the VDAC1 from NSC34 cells HTP-preparations. Mean, standard deviation, (95%) lower and upper confidence level and the number of scansions are reported.", "structure": {"pmcid": "PMC7761621", "section_index": 17, "section_title": "3.4.2. Identification of VDAC1 Deamidation Sites from NSC34-SOD1G93A Cell Line", "row_count": 7, "column_count": 7}, "table": {"label": "Table 3", "caption": "Asparagine (N) and glutamine (Q) deamidation in the VDAC1 from NSC34 cells HTP-preparations. Mean, standard deviation, (95%) lower and upper confidence level and the number of scansions are reported.", "rows": [["Cell Lines", "Residue", "Mean", "Std", "CI_Low", "CI_Up", "N. of Scansions"], ["NSC34", "N", "0", "0", "0", "0", "51"], ["Q", "0", "0", "0", "0", "30"], ["NSC34-SOD1WT", "N", "0", "0", "0", "0", "61"], ["Q", "0", "0", "0", "0", "41"], ["NSC34-SOD1G93A", "N", "0.98", "0.81", "0.04", "2.76", "87"], ["Q", "0.02", "0.02", "0.00", "0.06", "47"]], "row_count": 7, "column_count": 7, "numeric_cells": 33, "header_rows": 1, "locator": "section[17]/table-wrap[2]#antioxidants-09-01218-t003"}}, {"id": "asset:table:pmid:33276691:4", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:d5af7f43412abab38ee820030ab40c587244b841137ad84a779ead1cbe7c86bf", "bytes": 642, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[18]/table-wrap[1]#antioxidants-09-01218-t004", "version": null, "note": "Relative percentage of each VDAC isoform in the three cell lines.", "structure": {"pmcid": "PMC7761621", "section_index": 18, "section_title": "3.5. Semi-Quantitative Analysis of VDAC1 in NSC34 Cell Lines", "row_count": 5, "column_count": 10}, "table": {"label": "Table 4", "caption": "Relative percentage of each VDAC isoform in the three cell lines.", "rows": [["Protein", "NSC34", "NSC34-SOD1WT", "NSC34-SOD1G93A"], ["LFQ Intensity", "SD%", "%", "LFQ Intensity", "SD %", "%", "LFQ Intensity", "SD %", "%"], ["VDAC1", "1.10 × 109", "1", "66.71", "1.19 × 109", "27", "65.67", "1.10 × 109", "7", "64.08"], ["VDAC2", "2.40 × 108", "4", "14.55", "2.46 × 108", "20", "13.59", "3.51 × 108", "11", "20.43"], ["VDAC3", "3.09 × 108", "15", "18.74", "3.75 × 108", "16", "20.74", "2.66 × 108", "13", "15.50"]], "row_count": 5, "column_count": 10, "numeric_cells": 30, "header_rows": 2, "locator": "section[18]/table-wrap[1]#antioxidants-09-01218-t004"}}, {"id": "asset:table:pmid:33276691:5", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:458a388fe89961c9722f72d2011e7feddbc1a5e3d65dccdb7242a2d5f41f51d4", "bytes": 1064, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[19]/table-wrap[1]#antioxidants-09-01218-t005", "version": null, "note": "Distribution of secondary structures as predicted by Ramachandran Plot analysis. The table reports the percentage of allowed, favored and total secondary structure consisting of outliers, β-strand or α-helix, as obtained by RP analysis of VDAC1 WT and mutant structures.", "structure": {"pmcid": "PMC7761621", "section_index": 19, "section_title": "3.6. Bioinformatic Analysis Reveals an Increased Instability for Mutant Structures", "row_count": 10, "column_count": 8}, "table": {"label": "Table 5", "caption": "Distribution of secondary structures as predicted by Ramachandran Plot analysis. The table reports the percentage of allowed, favored and total secondary structure consisting of outliers, β-strand or α-helix, as obtained by RP analysis of VDAC1 WT and mutant structures.", "rows": [["", "Outliers", "β-Strand", "α-Helix"], ["", "Total", "Allowed", "Favored", "Total", "Allowed", "Favored", "Total"], ["VDAC1 WT", "12.4", "11.3", "67.6", "78.9", "6.3", "2.4", "8.7"], ["VDAC1 N37D", "10.6", "13.5", "63.2", "76.7", "7.8", "4.9", "12.7"], ["VDAC1 N106D", "8.8", "12.8", "65.4", "78.2", "7.0", "6.0", "13.0"], ["VDAC1 N207D", "9.1", "13.6", "64.6", "78.2", "7.4", "5.3", "12.7"], ["VDAC1N214D", "7.7", "12.3", "66.1", "78.4", "6.7", "7.1", "13.8"], ["VDAC1N239D", "8.1", "12.3", "66.4", "78.7", "7.1", "6.1", "13.2"], ["VDAC1 5 Asn/Asp", "7.3", "16.6", "60.7", "77.3", "8.4", "7.0", "15.4"], ["VDAC1 5 Asn/Asp + 2 Gln/Glu", "7.7", "14.4", "60.7", "75.1", "8.4", "8.4", "16.8"]], "row_count": 10, "column_count": 8, "numeric_cells": 63, "header_rows": 2, "locator": "section[19]/table-wrap[1]#antioxidants-09-01218-t005"}}, {"id": "asset:table:pmid:33276691:6", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:92eeae66105b26cf9fb96bffc3af0b7269018d24990e6d36c590dbf0d06b2815", "bytes": 1274, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[19]/table-wrap[2]#antioxidants-09-01218-t006", "version": null, "note": "Modified residues found in VDAC1 from NSC34, NSC34-SOD1WT and NSC34-SOD1G93A cell lines. The ratio between modified and unmodified residues is shown in brackets; where the ratio is not indicated the residue is only present in a single form. The dashes indicate residues found exclusively in non-modified form. The asterisk indicates a fully carboxyamidomethylated form.", "structure": {"pmcid": "PMC7761621", "section_index": 19, "section_title": "3.6. Bioinformatic Analysis Reveals an Increased Instability for Mutant Structures", "row_count": 14, "column_count": 4}, "table": {"label": "Table 6", "caption": "Modified residues found in VDAC1 from NSC34, NSC34-SOD1WT and NSC34-SOD1G93A cell lines. The ratio between modified and unmodified residues is shown in brackets; where the ratio is not indicated the residue is only present in a single form. The dashes indicate residues found exclusively in non-modified form. 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We found selective deamidations of aspar", "2. Materials and Methods 3.1. Mass Spectrometry Analysis of VDAC1 from NSC34 Cell Line The m", "y Analysis of VDAC1 from NSC34 Cell Line The mass spectrometry analysis was first performed on material obt", "(Supplementary Table S2, fragment 30). 3.2. Mass Spectrometry Analysis of VDAC1 from NSC34-SOD1WT Cell Lin"], "order_basis": "paper_text_order:856", "id": "assay:1"}, {"role": "data_generation", "definition_id": "transfection", "definition_version": "99e1195c7d6f", "definition_digest": null, "required_operations": [], "support_state": "partial", "source_hashes": {"assay_lexicon": "99e1195c7d6f"}, "confidence": 0.85, "evidence": ["rted for the same isoform from the NSC34 non transfected cells, discussed previously. 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