{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T12:07:50Z","timestamp":1790856470478,"version":"4.1.0"},"reference-count":46,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T00:00:00Z","timestamp":1790812800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T00:00:00Z","timestamp":1790812800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["American J Hematol"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Nodal T\u2010follicular helper cell lymphoma (nTFHL), most commonly of angioimmunoblastic type, exhibits heterogeneous clinical outcomes that are not fully explained by current clinical and biological variables. While genetic alterations have been extensively investigated, its proteomic landscape remains largely unexplored. Here, in a discovery cohort, the classical and alternative proteome of 63 nTFHL patients at diagnosis was profiled by mass spectrometry and analyzed using unsupervised k\u2010means clustering. Two nTFHL signatures with distinct pathway enrichment and significantly different overall survival (\n                    <jats:italic>p<\/jats:italic>\n                    \u2009=\u20090.02) were identified: the nTFHL\u2010stromal profile, characterized by a complex microenvironment, and the nTFHL\u2010translational profile, enriched in protein biosynthesis and cell proliferation pathways. Profile discrimination was confirmed across multiple supervised learning algorithms, enabling selection of a 10\u2010protein biomarker panel validated by immunofluorescence. In an independent validation cohort including 31 nTFHL patients, the 10\u2010protein panel accurately predicted the proteomic profiles, reproducing the observed difference in overall survival. In multivariable Cox regression, the nTFHL\u2010translational profile remained associated with poorer OS (HR\u2009=\u20091.92,\n                    <jats:italic>p<\/jats:italic>\n                    \u2009=\u20090.01), independently of the International Prognostic Index (IPI). Integration of the proteomic profile with the IPI generated the IPI\u2010P score, which refined risk stratification and identified three groups with significantly different overall survival (\n                    <jats:italic>p<\/jats:italic>\n                    \u2009&lt;\u20090.001). Overall, these findings reveal distinct proteomic programs underlying nTFHL heterogeneity and provide a clinically applicable framework for proteome\u2010based prognostic stratification.\n                  <\/jats:p>","DOI":"10.1002\/ajh.70502","type":"journal-article","created":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T11:31:58Z","timestamp":1790854318000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Proteomic Profiling of Nodal T\u2010Follicular Helper Cell Lymphoma Reveals Distinct Biological Signatures and Improves Prognostic Stratification Beyond the\n                    <scp>IPI<\/scp>"],"prefix":"10.1002","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1866-828X","authenticated-orcid":false,"given":"David","family":"Beauvais","sequence":"first","affiliation":[{"name":"University of Lille Inserm, CHU Lille, U1192 \u2010 Prot\u00e9omique R\u00e9ponse Inflammatoire Spectrom\u00e9trie de Masse \u2010 PRISM  Lille France"},{"name":"Hematology Department Lille University Hospital  Lille France"},{"name":"Equipe labelis\u00e9e Ligue Contre le Cancer  Paris France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanis","family":"Zirem","sequence":"additional","affiliation":[{"name":"University of Lille Inserm, CHU Lille, U1192 \u2010 Prot\u00e9omique R\u00e9ponse Inflammatoire Spectrom\u00e9trie de Masse \u2010 PRISM  Lille France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tristan","family":"Cardon","sequence":"additional","affiliation":[{"name":"University of Lille Inserm, CHU Lille, U1192 \u2010 Prot\u00e9omique R\u00e9ponse Inflammatoire Spectrom\u00e9trie de Masse \u2010 PRISM  Lille France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Soulaimane","family":"Aboulouard","sequence":"additional","affiliation":[{"name":"University of Lille Inserm, CHU Lille, U1192 \u2010 Prot\u00e9omique R\u00e9ponse Inflammatoire Spectrom\u00e9trie de Masse \u2010 PRISM  Lille France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Romain","family":"Dubois","sequence":"additional","affiliation":[{"name":"University of Lille CHU Lille, Institut de Pathologie  Lille France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1096-5044","authenticated-orcid":false,"given":"Isabelle","family":"Fournier","sequence":"additional","affiliation":[{"name":"University of Lille Inserm, CHU Lille, U1192 \u2010 Prot\u00e9omique R\u00e9ponse Inflammatoire Spectrom\u00e9trie de Masse \u2010 PRISM  Lille France"},{"name":"Equipe labelis\u00e9e Ligue Contre le Cancer  Paris France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3714-9824","authenticated-orcid":false,"given":"Franck","family":"Morschhauser","sequence":"additional","affiliation":[{"name":"Hematology Department Lille University Hospital  Lille France"},{"name":"University of Lille CHU Lille, ULR 7365\u2010GRITA \u2010 Groupe de Recherche Sur Les Formes Injectables et les Technologies Associ\u00e9es \u2010 GRITA  Lille France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4318-0817","authenticated-orcid":false,"given":"Michel","family":"Salzet","sequence":"additional","affiliation":[{"name":"University of Lille Inserm, CHU Lille, U1192 \u2010 Prot\u00e9omique R\u00e9ponse Inflammatoire Spectrom\u00e9trie de Masse \u2010 PRISM  Lille France"},{"name":"Equipe labelis\u00e9e Ligue Contre le Cancer  Paris France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ibrahim","family":"Yakoub\u2010Agha","sequence":"additional","affiliation":[{"name":"Hematology Department Lille University Hospital  Lille France"},{"name":"University of Lille Inserm, CHU Lille, U1286 \u2010 INFINITE  Lille France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie","family":"Duhamel","sequence":"additional","affiliation":[{"name":"University of Lille Inserm, CHU Lille, U1192 \u2010 Prot\u00e9omique R\u00e9ponse Inflammatoire Spectrom\u00e9trie de Masse \u2010 PRISM  Lille France"},{"name":"Equipe labelis\u00e9e Ligue Contre le Cancer  Paris France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,10,1]]},"reference":[{"key":"e_1_2_12_2_1","doi-asserted-by":"crossref","first-page":"2604","DOI":"10.1182\/blood.2023020912","article-title":"Peripheral T\u2010Cell Lymphoma: Are All Patients High Risk?","volume":"144","author":"Shea L.","year":"2024","journal-title":"Blood"},{"key":"e_1_2_12_3_1","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1038\/s41591-018-0016-8","article-title":"Molecular Subtypes of Diffuse Large B Cell Lymphoma Are Associated With Distinct Pathogenic Mechanisms and Outcomes","volume":"24","author":"Chapuy B.","year":"2018","journal-title":"Nature Medicine"},{"key":"e_1_2_12_4_1","first-page":"2307","article-title":"Five\u2010Year Follow\u2010Up of ZUMA\u20101 Supports the Curative Potential of Axicabtagene Ciloleucel in Refractory Large B\u2010Cell Lymphoma","volume":"141","author":"Neelapu S. S.","year":"2023","journal-title":"Blood"},{"key":"e_1_2_12_5_1","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.1038\/s41375-022-01620-2","article-title":"The 5th Edition of the World Health Organization Classification of Haematolymphoid Tumours: Lymphoid Neoplasms","volume":"36","author":"Alaggio R.","year":"2022","journal-title":"Leukemia"},{"key":"e_1_2_12_6_1","doi-asserted-by":"crossref","first-page":"1293","DOI":"10.1182\/blood-2013-10-531509","article-title":"A Targeted Mutational Landscape of Angioimmunoblastic T\u2010Cell Lymphoma","volume":"123","author":"Odejide O.","year":"2014","journal-title":"Blood"},{"key":"e_1_2_12_7_1","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1182\/bloodadvances.2020003081","article-title":"Integrative Analysis of a Phase 2 Trial Combining Lenalidomide With CHOP in Angioimmunoblastic T\u2010Cell Lymphoma","volume":"5","author":"Lemonnier F.","year":"2021","journal-title":"Blood Advances"},{"key":"e_1_2_12_8_1","first-page":"2194","article-title":"Multicenter Phase 2 Study of Oral Azacitidine (CC\u2010486) Plus CHOP as Initial Treatment for PTCL","volume":"141","author":"Ruan J.","year":"2023","journal-title":"Blood"},{"key":"e_1_2_12_9_1","doi-asserted-by":"crossref","first-page":"e406","DOI":"10.1016\/S2352-3026(24)00102-9","article-title":"Oral Azacitidine Compared With Standard Therapy in Patients With Relapsed or Refractory Follicular Helper T\u2010Cell Lymphoma (ORACLE): An Open\u2010Label Randomised, Phase 3 Study","volume":"11","author":"Dupuis J.","year":"2024","journal-title":"Lancet Haematology"},{"key":"e_1_2_12_10_1","doi-asserted-by":"crossref","first-page":"1486","DOI":"10.1002\/ajh.27736","article-title":"Integrative Genomic and Transcriptomic Analysis Reveals Targetable Vulnerabilities in Angioimmunoblastic T\u2010Cell Lymphoma","volume":"100","author":"Bouska A.","year":"2025","journal-title":"American Journal of Hematology"},{"key":"e_1_2_12_11_1","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1182\/blood.2020010387","article-title":"Outcomes and Prognostic Factors in Angioimmunoblastic T\u2010Cell Lymphoma: Final Report From the International T\u2010Cell Project","volume":"138","author":"Advani R. 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Cancer Journal"},{"key":"e_1_2_12_18_1","doi-asserted-by":"crossref","first-page":"2533","DOI":"10.1182\/bloodadvances.2018019893","article-title":"Proteomic Profiling Identifies Outcome\u2010Predictive Markers in Patients With Peripheral T\u2010Cell Lymphoma, Not Otherwise Specified","volume":"2","author":"Ludvigsen M.","year":"2018","journal-title":"Blood Advances"},{"key":"e_1_2_12_19_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.mcpro.2023.100625","article-title":"Proteomics Identifies Circulating TIMP\u20101 as a Prognostic Biomarker for Diffuse Large B\u2010Cell Lymphoma","volume":"22","author":"Lou N.","year":"2023","journal-title":"Molecular & cellular proteomics: MCP"},{"key":"e_1_2_12_20_1","doi-asserted-by":"crossref","first-page":"2284","DOI":"10.1074\/mcp.TIR118.000853","article-title":"A Novel LC System Embeds Analytes in Pre\u2010Formed Gradients for Rapid, Ultra\u2010Robust Proteomics *","volume":"17","author":"Bache N.","year":"2018","journal-title":"Molecular & 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Research"},{"key":"e_1_2_12_24_1","first-page":"1208","article-title":"Reactome Diagram Viewer: Data Structures and Strategies to Boost Performance","volume":"34","author":"Fabregat A.","year":"2018","journal-title":"Bioinformatics (Oxford, England)"},{"key":"e_1_2_12_25_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btaf644"},{"key":"e_1_2_12_26_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.xcrm.2024.101482","article-title":"Real\u2010Time Glioblastoma Tumor Microenvironment Assessment by SpiderMass for Improved Patient Management","volume":"5","author":"Zirem Y.","year":"2024","journal-title":"Cell Reports Medicine"},{"key":"e_1_2_12_27_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.xpro.2024.103285","article-title":"Protocol to Analyze 1D and 2D Mass Spectrometry Data From Glioblastoma Tissues for Cancer Diagnosis and Immune Cell Identification","volume":"5","author":"Zirem Y.","year":"2024","journal-title":"STAR 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E.","year":"2015"},{"key":"e_1_2_12_30_1","volume-title":"Advances in Neural Information Processing Systems","author":"Ke G.","year":"2017"},{"key":"e_1_2_12_31_1","doi-asserted-by":"crossref","first-page":"1184","DOI":"10.1038\/s41375-025-02563-0","article-title":"Discrete Genetic Subtypes and Tumor Microenvironment Signatures Correlate With Peripheral T\u2010Cell Lymphoma Outcomes","volume":"39","author":"Suehara Y.","year":"2025","journal-title":"Leukemia"},{"key":"e_1_2_12_32_1","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1083\/jcb.201102147","article-title":"The Extracellular Matrix: A Dynamic Niche in Cancer Progression","volume":"196","author":"Lu P.","year":"2012","journal-title":"Journal of Cell Biology"},{"key":"e_1_2_12_33_1","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/s10555-017-9673-1","article-title":"Platelets and Cancer Angiogenesis Nexus","volume":"36","author":"Wojtukiewicz M. Z.","year":"2017","journal-title":"Cancer Metastasis Reviews"},{"key":"e_1_2_12_34_1","doi-asserted-by":"crossref","first-page":"1546","DOI":"10.1126\/science.1235122","article-title":"Cancer genome landscapes","volume":"339","author":"Vogelstein B.","year":"2013","journal-title":"Science"},{"key":"e_1_2_12_35_1","doi-asserted-by":"crossref","first-page":"1723","DOI":"10.1038\/s41375-025-02631-5","article-title":"TP53 and CDKN2A Alterations Define a Poor Prognostic Subgroup in Patients With Nodal T Follicular Helper Cell Lymphoma","volume":"39","author":"Ito Y.","year":"2025","journal-title":"Leukemia"},{"key":"e_1_2_12_36_1","doi-asserted-by":"crossref","first-page":"1664","DOI":"10.1182\/blood-2018-09-872549","article-title":"Genetic Drivers of Oncogenic Pathways in Molecular Subgroups of Peripheral T\u2010Cell Lymphoma","volume":"133","author":"Heavican T. B.","year":"2019","journal-title":"Blood"},{"key":"e_1_2_12_37_1","doi-asserted-by":"crossref","first-page":"1828","DOI":"10.1111\/bjh.20071","article-title":"Prognostic Impacts of RHOA G17V Mutation in Cell\u2010Free DNA Assessed by Droplet Digital Polymerase Chain Reaction in Patients With Angioimmunoblastic T\u2010Cell Lymphoma","volume":"206","author":"Miao Y.","year":"2025","journal-title":"British Journal of Haematology"},{"key":"e_1_2_12_38_1","doi-asserted-by":"crossref","first-page":"e148","DOI":"10.3324\/haematol.2016.158428","article-title":"Integrative Clinicopathological and Molecular Analyses of Angioimmunoblastic T\u2010Cell Lymphoma and Other Nodal Lymphomas of Follicular Helper T\u2010Cell Origin","volume":"102","author":"Dobay M. P.","year":"2017","journal-title":"Haematologica"},{"key":"e_1_2_12_39_1","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/ng.2872","article-title":"Somatic RHOA Mutation in Angioimmunoblastic T Cell Lymphoma","volume":"46","author":"Sakata\u2010Yanagimoto M.","year":"2014","journal-title":"Nature Genetics"},{"key":"e_1_2_12_40_1","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.ccell.2018.01.001","article-title":"RHOA G17V Induces T Follicular Helper Cell Specification and Promotes Lymphomagenesis","volume":"33","author":"Cortes J. R.","year":"2018","journal-title":"Cancer Cell"},{"key":"e_1_2_12_41_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2022.110418","article-title":"Nucleoporin\u201093 Reveals a Common Feature of Aggressive Breast Cancers: Robust Nucleocytoplasmic Transport of Transcription Factors","volume":"38","author":"Nataraj N. B.","year":"2022","journal-title":"Cell Reports"},{"key":"e_1_2_12_42_1","doi-asserted-by":"crossref","first-page":"5006","DOI":"10.1038\/s41467-025-60144-2","article-title":"Cleavage of CAD by Caspase\u20103 Determines the Cancer Cell Fate During Chemotherapy","volume":"16","author":"Ma J.","year":"2025","journal-title":"Nature Communications"},{"key":"e_1_2_12_43_1","doi-asserted-by":"crossref","first-page":"2915","DOI":"10.1182\/blood-2013-11-536359","article-title":"Gene Expression Signatures Delineate Biological and Prognostic Subgroups in Peripheral T\u2010Cell Lymphoma","volume":"123","author":"Iqbal J.","year":"2014","journal-title":"Blood"},{"key":"e_1_2_12_44_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.mcpro.2025.101076","article-title":"Chasing the Ghost Proteome in the Dark Matter","volume":"24","author":"Cardon T.","year":"2025","journal-title":"Molecular & Cellular Proteomics"},{"key":"e_1_2_12_45_1","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1016\/j.cell.2011.02.013","article-title":"Hallmarks of Cancer: The Next Generation","volume":"144","author":"Hanahan D.","year":"2011","journal-title":"Cell"},{"key":"e_1_2_12_46_1","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1200\/JCO.2011.37.3647","article-title":"Clinicopathologic Characteristics of Angioimmunoblastic T\u2010Cell Lymphoma: Analysis of the International Peripheral T\u2010Cell Lymphoma Project","volume":"31","author":"Federico M.","year":"2013","journal-title":"Journal of Clinical Oncology"},{"key":"e_1_2_12_47_1","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/S0140-6736(18)32984-2","article-title":"Brentuximab Vedotin With Chemotherapy for CD30\u2010Positive Peripheral T\u2010Cell Lymphoma (ECHELON\u20102): A Global, Double\u2010Blind, Randomised, Phase 3 Trial","volume":"393","author":"Horwitz S.","year":"2019","journal-title":"Lancet"}],"container-title":["American Journal of Hematology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ajh.70502","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/ajh.70502","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ajh.70502","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T11:32:04Z","timestamp":1790854324000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/ajh.70502"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,10,1]]},"references-count":46,"alternative-id":["10.1002\/ajh.70502"],"URL":"https:\/\/doi.org\/10.1002\/ajh.70502","archive":["Portico"],"relation":{},"ISSN":["0361-8609","1096-8652"],"issn-type":[{"value":"0361-8609","type":"print"},{"value":"1096-8652","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,10,1]]},"assertion":[{"value":"2026-08-19","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-07","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-10-01","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"ajh.70502"}}