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Among post-translational modifications, N-terminal arginylation\u2500catalyzed by ATE1\u2500regulates protein stability and cellular stress responses, but its role in meningioma biology has not been explored. Here, we integrated mass-spectrometry\u2013based proteomics, immunoblotting, and transcriptomic reanalysis to investigate pathway regulation across tumor grades. Grade 1 meningiomas displayed higher ATE1 expression and increased arginylation of key chaperones, accompanied by activation of the PERK branch of the unfolded protein response (UPR), enhanced autophagy, and greater engagement of apoptotics pathways. In contrast, grade 2 tumors showed reduced ATE1 levels, diminished BIP arginylation, attenuated UPR-PERK signaling, impaired autophagy, and increased proliferative signaling. Proteins predicted to be substrates of ATE1-mediated degradation were upregulated in grade 2 tumors, suggesting that loss of arginylation may stabilize pro-oncogenic factors. Together, these findings reveal grade-specific remodeling of the N-degron\/arginylation axis and highlight protein arginylation as a previously unrecognized modulator of meningioma progression, with potential therapeutic relevance.<\/jats:p>","DOI":"10.1021\/acs.jproteome.5c01173","type":"journal-article","created":{"date-parts":[[2026,6,29]],"date-time":"2026-06-29T18:30:41Z","timestamp":1782757841000},"page":"3926-3936","source":"Crossref","is-referenced-by-count":0,"title":["Proteomic\nAnalysis Identifies ATE1-Dependent Arginylation\nDysregulation across Meningioma Grades"],"prefix":"10.1021","volume":"25","author":[{"given":"Janaina","family":"Macedo-da-Silva","sequence":"first","affiliation":[{"name":"University of Sa\u0303o Paulo , , ,","place":["Sao Paulo, Brazil, CEP: 05508-900"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benedito Jamilson Arau\u0301jo","family":"Pereira","sequence":"additional","affiliation":[{"name":"Universidade de Sa\u0303o Paulo , , ,","place":["Sa\u0303o Paulo, Brazil, CEP: 01246-903"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simon Ngao","family":"Mule","sequence":"additional","affiliation":[{"name":"University of Sa\u0303o Paulo , , ,","place":["Sao Paulo, Brazil, CEP: 05508-900"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sueli Mieko","family":"Oba-Shinjo","sequence":"additional","affiliation":[{"name":"Universidade de Sa\u0303o Paulo , , ,","place":["Sa\u0303o Paulo, Brazil, CEP: 01246-903"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1612-1950","authenticated-orcid":true,"given":"Livia","family":"Rosa-Fernandes","sequence":"additional","affiliation":[{"name":"Macquarie Medical School , , , ,","place":["Sydney, New South Wales, Australia, 2109"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4419-7928","authenticated-orcid":true,"given":"Suely K. N.","family":"Marie","sequence":"additional","affiliation":[{"name":"Universidade de Sa\u0303o Paulo , , ,","place":["Sa\u0303o Paulo, Brazil, CEP: 01246-903"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppe","family":"Palmisano","sequence":"additional","affiliation":[{"name":"University of Sa\u0303o Paulo , , ,","place":["Sao Paulo, Brazil, CEP: 05508-900"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,6,29]]},"reference":[{"issue":"12 Suppl 2","key":"2026080709082003700_cit1","doi-asserted-by":"publisher","first-page":"iv1","DOI":"10.1093\/neuonc\/noad149","article-title":"CBTRUS\nStatistical Report: Primary\nBrain and Other Central Nervous System Tumors Diagnosed in the United\nStates in 2016\u25002020","volume":"25","author":"Ostrom","year":"2023","journal-title":"Neuro Oncol."},{"issue":"8","key":"2026080709082003700_cit2","doi-asserted-by":"publisher","first-page":"1231","DOI":"10.1093\/neuonc\/noab106","article-title":"The 2021 WHO Classification\nof Tumors of the Central\nNervous System: a summary","volume":"23","author":"Louis","year":"2021","journal-title":"Neuro Oncol."},{"issue":"10","key":"2026080709082003700_cit3","doi-asserted-by":"publisher","first-page":"1742","DOI":"10.1093\/neuonc\/noae082","article-title":"Meningioma: International Consortium\non Meningiomas consensus review on scientific advances and treatment\nparadigms for clinicians, researchers, and patients","volume":"26","author":"Wang","year":"2024","journal-title":"Neuro Oncol."},{"key":"2026080709082003700_cit4","doi-asserted-by":"publisher","first-page":"1157182","DOI":"10.3389\/fonc.2023.1157182","article-title":"Epidemiology and survival of non-malignant\nand malignant meningiomas in middle-aged females, 2004\u20132018","volume":"13","author":"Cao","year":"2023","journal-title":"Front. Oncol."},{"issue":"4","key":"2026080709082003700_cit5","doi-asserted-by":"publisher","DOI":"10.3171\/2018.1.FOCUS17752","article-title":"Relationship between tumor location, size, and WHO\ngrade in meningioma","volume":"44","author":"Magill","year":"2018","journal-title":"Neurosurg. Focus"},{"issue":"1","key":"2026080709082003700_cit6","doi-asserted-by":"publisher","first-page":"704","DOI":"10.1007\/s10143-024-02881-4","article-title":"Impact\non natural history of atypical meningioma after changes in 2016 edition\nof the world health organization (WHO) classification of central nervous\nsystem tumors: a literature review","volume":"47","author":"Pereira","year":"2024","journal-title":"Neurosurg.\nRev."},{"issue":"2","key":"2026080709082003700_cit7","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1007\/s11060-022-04148-8","article-title":"Emerging systemic treatment\noptions in meningioma","volume":"161","author":"Mair","year":"2023","journal-title":"J. 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Natl. Acad. Sci. U. S. A."},{"issue":"12","key":"2026080709082003700_cit19","doi-asserted-by":"publisher","first-page":"1367","DOI":"10.1038\/nbt.1511","article-title":"MaxQuant enables high\npeptide identification rates, individualized\np.p.b.-range mass accuracies and proteome-wide protein quantification","volume":"26","author":"Cox","year":"2008","journal-title":"Nat. Biotechnol."},{"issue":"D1","key":"2026080709082003700_cit20","doi-asserted-by":"publisher","first-page":"D638","DOI":"10.1093\/nar\/gkac1000","article-title":"The STRING\ndatabase in 2023: protein-protein association networks and functional\nenrichment analyses for any sequenced genome of interest","volume":"51","author":"Szklarczyk","year":"2023","journal-title":"Nucleic Acids Res."},{"issue":"11","key":"2026080709082003700_cit21","doi-asserted-by":"publisher","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: a software environment\nfor integrated models\nof biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome\nRes."},{"issue":"1","key":"2026080709082003700_cit22","doi-asserted-by":"publisher","first-page":"3675","DOI":"10.1038\/s41467-024-48009-6","article-title":"MetaboAnalystR 4.0: a unified LC-MS workflow for global metabolomics","volume":"15","author":"Pang","year":"2024","journal-title":"Nat. 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Oncol."},{"issue":"11","key":"2026080709082003700_cit28","doi-asserted-by":"publisher","first-page":"1821","DOI":"10.1093\/neuonc\/noab150","article-title":"EANO guideline on the diagnosis and\nmanagement of meningiomas","volume":"23","author":"Goldbrunner","year":"2021","journal-title":"Neuro Oncol."},{"issue":"1","key":"2026080709082003700_cit29","doi-asserted-by":"publisher","first-page":"2232","DOI":"10.1038\/s41467-023-38004-8","article-title":"The structural basis\nof tRNA recognition by arginyl-tRNA-protein transferase","volume":"14","author":"Abeywansha","year":"2023","journal-title":"Nat. Commun."},{"issue":"10","key":"2026080709082003700_cit30","doi-asserted-by":"publisher","first-page":"690","DOI":"10.1038\/s41419-019-1934-1","article-title":"ER stress and UPR activation in glioblastoma:\nidentification of a noncanonical PERK mechanism regulating GBM stem\ncells through SOX2 modulation","volume":"10","author":"Pen\u0303aranda-Fajardo","year":"2019","journal-title":"Cell Death Dis."},{"issue":"12","key":"2026080709082003700_cit31","doi-asserted-by":"publisher","first-page":"6520","DOI":"10.3390\/ijms23126520","article-title":"The Unfolded\nProtein Response Sensor\nPERK Mediates Stiffness-Dependent Adaptation in Glioblastoma Cells","volume":"23","author":"Khoonkari","year":"2022","journal-title":"Int. J. Mol. Sci."},{"key":"2026080709082003700_cit32","doi-asserted-by":"publisher","first-page":"102735","DOI":"10.1155\/2013\/102735","article-title":"Role of the Crosstalk between Autophagy and Apoptosis\nin Cancer","volume":"2013","author":"Su","year":"2013","journal-title":"J. Oncol."},{"issue":"4","key":"2026080709082003700_cit33","doi-asserted-by":"publisher","first-page":"857","DOI":"10.3390\/ijms20040857","article-title":"Endoplasmic\nReticulum Stress and Unfolded Protein Response in Breast Cancer: The\nBalance between Apoptosis and Autophagy and Its Role in Drug Resistance","volume":"20","author":"Sisinni","year":"2019","journal-title":"Int. J. Mol. 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Cancer Res."},{"issue":"7","key":"2026080709082003700_cit38","doi-asserted-by":"publisher","first-page":"490","DOI":"10.1038\/s41419-019-1729-4","article-title":"Expression of UPR effector\nproteins ATF6 and XBP1 reduce colorectal cancer cell proliferation\nand stemness by activating PERK signaling","volume":"10","author":"Spaan","year":"2019","journal-title":"Cell\nDeath Dis."},{"issue":"2","key":"2026080709082003700_cit39","doi-asserted-by":"publisher","first-page":"261","DOI":"10.3390\/cancers13020261","article-title":"An Emerging Role for\nthe Unfolded Protein Response\nin Pancreatic Cancer","volume":"13","author":"Robinson","year":"2021","journal-title":"Cancers"},{"issue":"1","key":"2026080709082003700_cit40","doi-asserted-by":"publisher","first-page":"577","DOI":"10.3390\/ijms24010577","article-title":"Increasing\nStress to Induce Apoptosis in Pancreatic\nCancer via the Unfolded Protein Response (UPR)","volume":"24","author":"Botrus","year":"2023","journal-title":"Int. J. Mol. Sci."},{"issue":"22","key":"2026080709082003700_cit41","doi-asserted-by":"publisher","first-page":"3094","DOI":"10.1038\/onc.2016.459","article-title":"ER stress protein AGR2 precedes and\nis involved in the regulation of pancreatic cancer initiation","volume":"36","author":"Dumartin","year":"2017","journal-title":"Oncogene"},{"issue":"11","key":"2026080709082003700_cit42","doi-asserted-by":"publisher","first-page":"4074","DOI":"10.1158\/1078-0432.CCR-04-2550","article-title":"Different activation of mitogen-activated\nprotein kinase and Akt signaling is associated with aggressive phenotype\nof human meningiomas","volume":"11","author":"Mawrin","year":"2005","journal-title":"Clin. Cancer Res."},{"issue":"1","key":"2026080709082003700_cit43","doi-asserted-by":"publisher","first-page":"390","DOI":"10.1186\/s12964-025-02376-9","article-title":"ATE1 promotes breast cancer progression via arginylation-dependent\nregulation of MAPK-MYC signaling","volume":"23","author":"Nawale","year":"2025","journal-title":"Cell Commun.\nSignal"},{"issue":"31","key":"2026080709082003700_cit44","doi-asserted-by":"publisher","first-page":"4058","DOI":"10.1038\/onc.2015.473","article-title":"Arginyltransferase\nsuppresses cell tumorigenic potential and inversely correlates with\nmetastases in human cancers","volume":"35","author":"Rai","year":"2016","journal-title":"Oncogene"}],"container-title":["Journal of Proteome Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.jproteome.5c01173","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/jprobs\/article-pdf\/25\/8\/3926\/65281675\/acs.jproteome.5c01173.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/jprobs\/article-pdf\/25\/8\/3926\/65281675\/acs.jproteome.5c01173.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T13:15:27Z","timestamp":1786108527000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/jprobs\/article\/25\/8\/3926\/5170801\/Proteomic-Analysis-Identifies-ATE1-Dependent"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,29]]},"references-count":44,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2026,6,29]]},"published-print":{"date-parts":[[2026,8,7]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.jproteome.5c01173","relation":{},"ISSN":["1535-3893","1535-3907"],"issn-type":[{"value":"1535-3893","type":"print"},{"value":"1535-3907","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,29]]}}}