Immune responses to CCAR1 and other dermatomyositis autoantigens are associated with attenuated cancer emergence.
Antigen
Autoimmune diseases
Autoimmunity
Cancer
Immunology
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
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
Références
Science. 2014 Jan 10;343(6167):152-7
pubmed: 24310608
Cancer Epidemiol Biomarkers Prev. 2017 Apr;26(4):632-641
pubmed: 27956436
Arthritis Rheum. 2013 Nov;65(11):2954-62
pubmed: 24037894
Arthritis Rheum. 2012 Feb;64(2):513-22
pubmed: 21987216
Front Immunol. 2017 Nov 28;8:1679
pubmed: 29234329
Arthritis Rheumatol. 2015 Jan;67(1):266-72
pubmed: 25186009
Rheumatology (Oxford). 2020 Mar 1;59(3):469-477
pubmed: 31883334
Curr Rheumatol Rep. 2018 Apr 10;20(5):28
pubmed: 29637414
Front Immunol. 2020 Oct 14;11:587014
pubmed: 33163002
Clin Exp Rheumatol. 2018 Nov-Dec;36(6):990-995
pubmed: 29745874
J Am Acad Dermatol. 2011 Jul;65(1):25-34
pubmed: 21531040
Annu Rev Immunol. 2016 May 20;34:395-420
pubmed: 26907212
J Biol Chem. 2020 Mar 13;295(11):3532-3552
pubmed: 32024692
Ann Intern Med. 2001 Jun 19;134(12):1087-95
pubmed: 11412048
Medicine (Baltimore). 2018 Jan;97(2):e9639
pubmed: 29480875
Arthritis Rheum. 2006 Nov;54(11):3682-9
pubmed: 17075819
Rheumatology (Oxford). 2019 Apr 1;58(4):650-655
pubmed: 30535395
Clin Rheumatol. 2020 Nov;39(11):3409-3416
pubmed: 32372292
Oncotarget. 2015 Mar 30;6(9):6499-510
pubmed: 25894788
Arthritis Rheumatol. 2019 Sep;71(9):1571-1579
pubmed: 30888702
Sci Transl Med. 2012 Oct 24;4(157):157ra142
pubmed: 23100628
Proc Natl Acad Sci U S A. 2016 Nov 22;113(47):E7526-E7534
pubmed: 27821747
Immunol Lett. 2015 Jan;163(1):56-68
pubmed: 25445494
IEEE Trans Vis Comput Graph. 2014 Dec;20(12):1983-92
pubmed: 26356912
Clin Exp Rheumatol. 2019 Nov-Dec;37(6):1048-1051
pubmed: 31376258
Arthritis Rheumatol. 2017 Dec;69(12):2271-2282
pubmed: 29106061
Dermatol Clin. 2002 Jul;20(3):387-408
pubmed: 12170874
Acta Derm Venereol. 2019 Mar 1;99(3):256-262
pubmed: 30460368
Cancer Res. 2015 Jun 1;75(11):2285-91
pubmed: 25832653
Arthritis Rheum. 2010 Sep;62(9):2787-95
pubmed: 20506513
Lancet. 2001 Jan 13;357(9250):96-100
pubmed: 11197446
Rheumatology (Oxford). 2018 Feb 1;57(2):388-396
pubmed: 29149307
N Engl J Med. 1975 Feb 13;292(7):344-7
pubmed: 1090839
Rheumatology (Oxford). 2007 Jan;46(1):25-8
pubmed: 16728436
Annu Rev Immunol. 2004;22:329-60
pubmed: 15032581
Cancer Immunol Res. 2021 Jan;9(1):103-112
pubmed: 33177107
Arthritis Rheumatol. 2015 Feb;67(2):317-26
pubmed: 25371098
N Engl J Med. 1992 Feb 6;326(6):363-7
pubmed: 1729618