Immune responses to CCAR1 and other dermatomyositis autoantigens are associated with attenuated cancer emergence.


Journal

The Journal of clinical investigation
ISSN: 1558-8238
Titre abrégé: J Clin Invest
Pays: United States
ID NLM: 7802877

Informations de publication

Date de publication:
18 01 2022
Historique:
received: 05 04 2021
accepted: 12 11 2021
entrez: 18 1 2022
pubmed: 19 1 2022
medline: 19 2 2022
Statut: ppublish

Résumé

BACKGROUNDThe temporal clustering of a cancer diagnosis with dermatomyositis (DM) onset is strikingly associated with autoantibodies against transcriptional intermediary factor 1-γ (TIF1-γ). Nevertheless, many patients with anti-TIF1-γ antibodies never develop cancer. We investigated whether additional autoantibodies are found in anti-TIF1-γ-positive patients without cancer.METHODSUsing a proteomic approach, we defined 10 previously undescribed autoantibody specificities in 5 index anti-TIF1-γ-positive DM patients without cancer. These were subsequently examined in discovery (n = 110) and validation (n = 142) cohorts of DM patients with anti-TIF1-γ autoantibodies.RESULTSWe identified 10 potentially novel autoantibodies in anti-TIF1-γ-positive DM patients, 6 with frequencies ranging from 3% to 32% in 2 independent DM cohorts. Autoantibodies recognizing cell division cycle and apoptosis regulator protein 1 (CCAR1) were the most frequent, and were significantly negatively associated with contemporaneous cancer (discovery cohort OR 0.27 [95% CI 0.7-1.00], P = 0.050; validation cohort OR 0.13 [95% CI 0.03-0.59], P = 0.008). When cancer did emerge, it occurred significantly later in anti-CCAR1-positive compared with anti-CCAR1-negative patients (median time from DM onset 4.3 vs. 0.85 years, respectively; P = 0.006). Cancers that emerged were more likely to be localized (89% of anti-CCAR1-positive cancers presenting at stage 0 or 1 compared with 42% of patients without anti-CCAR1 antibodies, P = 0.02). As the number of additional autoantibody specificities increased in anti-TIF1-γ-positive DM patients, the frequency of cancer decreased (P < 0.001).CONCLUSIONAs the diversity of immune responses in anti-TIF1-γ DM patients increases, the likelihood of cancer emerging decreases. Our findings have important relevance for cancer risk stratification in DM patients and for understanding natural immune regulation of cancer in humans.TRIAL REGISTRATIONNot applicable.FUNDING SOURCESThe NIH, the Donald B. and Dorothy L. Stabler Foundation, and the Huayi and Siuling Zhang Discovery Fund.

Identifiants

pubmed: 35040440
pii: 150201
doi: 10.1172/JCI150201
pmc: PMC8759791
doi:
pii:

Substances chimiques

Apoptosis Regulatory Proteins 0
Autoantibodies 0
CCAR1 protein, human 0
Cell Cycle Proteins 0
Neoplasm Proteins 0
TRIM33 protein, human 0
Transcription Factors 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIAMS NIH HHS
ID : K23 AR075898
Pays : United States
Organisme : NIAMS NIH HHS
ID : P30 AR053503
Pays : United States
Organisme : NIAMS NIH HHS
ID : P30 AR070254
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR073208
Pays : United States

Commentaires et corrections

Type : CommentIn

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Auteurs

David F Fiorentino (DF)

Department of Dermatology, Stanford University School of Medicine, Redwood City, California, USA.

Christopher A Mecoli (CA)

Division of Rheumatology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

Matthew C Rosen (MC)

Department of Neurobiology, The University of Chicago, Chicago, Illinois, USA.

Lorinda S Chung (LS)

Division of Immunology and Rheumatology, Stanford University School of Medicine, Palo Alto, California, USA.

Lisa Christopher-Stine (L)

Division of Rheumatology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

Antony Rosen (A)

Division of Rheumatology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

Livia Casciola-Rosen (L)

Division of Rheumatology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

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Classifications MeSH