Aging-related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1,255 human blood samples

This study aimed to identify age-related genes and alternative splicing (AS) events by comprehensive transcriptome analysis of 1,255 healthy blood samples from individuals aged 8–87 years. We identified 1,029 up-regulated and 1,186 down-regulated genes in older individuals, including 17 genes overla...

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Main Authors: Shuhan Li, Haohao Lv, Renxin Zhang, Jinjun Li, Zhiyuan Chen, Naixue Yang, Shaoxing Dai
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Aging
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Online Access:https://www.frontiersin.org/articles/10.3389/fragi.2025.1575862/full
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author Shuhan Li
Shuhan Li
Haohao Lv
Haohao Lv
Renxin Zhang
Renxin Zhang
Jinjun Li
Jinjun Li
Zhiyuan Chen
Zhiyuan Chen
Naixue Yang
Naixue Yang
Shaoxing Dai
Shaoxing Dai
author_facet Shuhan Li
Shuhan Li
Haohao Lv
Haohao Lv
Renxin Zhang
Renxin Zhang
Jinjun Li
Jinjun Li
Zhiyuan Chen
Zhiyuan Chen
Naixue Yang
Naixue Yang
Shaoxing Dai
Shaoxing Dai
author_sort Shuhan Li
collection DOAJ
description This study aimed to identify age-related genes and alternative splicing (AS) events by comprehensive transcriptome analysis of 1,255 healthy blood samples from individuals aged 8–87 years. We identified 1,029 up-regulated and 1,186 down-regulated genes in older individuals, including 17 genes overlapped with known aging-associated genes, such as TFAP2A and Klotho. Gene set enrichment analysis revealed significant alterations in immunoregulatory and metabolic pathways during aging. However, many senescence-associated secretory phenotypes (SASP) involved genes did not exhibit changes in gene expression, suggesting that AS events may reveal additional age-related mechanisms. Aging also altered 6,320 AS events in 4,566 genes, impacting immune-related protein domains. The RNA-binding protein RBMS3 emerged as a key regulator of aging-specific AS events. In addition, neoantigen prediction analyses further identified potential neoantigens generated by aging-related AS events, with the HLA-C14:02 allele presenting the most neoantigenic peptides. Notably, 60 neoantigenic peptides were confirmed using proteomic data from elderly individuals, suggesting their potential as novel targets for anti-aging immunotherapy. Our study provides new insights into the role of alternative splicing in aging, highlights promising avenues for anti-aging immunotherapy.
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issn 2673-6217
language English
publishDate 2025-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Aging
spelling doaj-art-cfa545ccb9da4fb89d2c58ca0555d50a2025-08-20T03:53:06ZengFrontiers Media S.A.Frontiers in Aging2673-62172025-05-01610.3389/fragi.2025.15758621575862Aging-related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1,255 human blood samplesShuhan Li0Shuhan Li1Haohao Lv2Haohao Lv3Renxin Zhang4Renxin Zhang5Jinjun Li6Jinjun Li7Zhiyuan Chen8Zhiyuan Chen9Naixue Yang10Naixue Yang11Shaoxing Dai12Shaoxing Dai13State Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, ChinaYunnan Key Laboratory of Primate Biomedical Research, Kunming, Yunnan, ChinaState Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, ChinaYunnan Key Laboratory of Primate Biomedical Research, Kunming, Yunnan, ChinaState Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, ChinaYunnan Key Laboratory of Primate Biomedical Research, Kunming, Yunnan, ChinaState Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, ChinaYunnan Key Laboratory of Primate Biomedical Research, Kunming, Yunnan, ChinaState Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, ChinaYunnan Key Laboratory of Primate Biomedical Research, Kunming, Yunnan, ChinaState Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, ChinaYunnan Key Laboratory of Primate Biomedical Research, Kunming, Yunnan, ChinaState Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, ChinaYunnan Key Laboratory of Primate Biomedical Research, Kunming, Yunnan, ChinaThis study aimed to identify age-related genes and alternative splicing (AS) events by comprehensive transcriptome analysis of 1,255 healthy blood samples from individuals aged 8–87 years. We identified 1,029 up-regulated and 1,186 down-regulated genes in older individuals, including 17 genes overlapped with known aging-associated genes, such as TFAP2A and Klotho. Gene set enrichment analysis revealed significant alterations in immunoregulatory and metabolic pathways during aging. However, many senescence-associated secretory phenotypes (SASP) involved genes did not exhibit changes in gene expression, suggesting that AS events may reveal additional age-related mechanisms. Aging also altered 6,320 AS events in 4,566 genes, impacting immune-related protein domains. The RNA-binding protein RBMS3 emerged as a key regulator of aging-specific AS events. In addition, neoantigen prediction analyses further identified potential neoantigens generated by aging-related AS events, with the HLA-C14:02 allele presenting the most neoantigenic peptides. Notably, 60 neoantigenic peptides were confirmed using proteomic data from elderly individuals, suggesting their potential as novel targets for anti-aging immunotherapy. Our study provides new insights into the role of alternative splicing in aging, highlights promising avenues for anti-aging immunotherapy.https://www.frontiersin.org/articles/10.3389/fragi.2025.1575862/fullagingtranscriptome analysisalternative splicingimmunosenescenceneoantigensanti-aging immunotherapy
spellingShingle Shuhan Li
Shuhan Li
Haohao Lv
Haohao Lv
Renxin Zhang
Renxin Zhang
Jinjun Li
Jinjun Li
Zhiyuan Chen
Zhiyuan Chen
Naixue Yang
Naixue Yang
Shaoxing Dai
Shaoxing Dai
Aging-related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1,255 human blood samples
Frontiers in Aging
aging
transcriptome analysis
alternative splicing
immunosenescence
neoantigens
anti-aging immunotherapy
title Aging-related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1,255 human blood samples
title_full Aging-related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1,255 human blood samples
title_fullStr Aging-related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1,255 human blood samples
title_full_unstemmed Aging-related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1,255 human blood samples
title_short Aging-related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1,255 human blood samples
title_sort aging related alternative splicing drive neoantigen emergence revealed by transcriptome analysis of 1 255 human blood samples
topic aging
transcriptome analysis
alternative splicing
immunosenescence
neoantigens
anti-aging immunotherapy
url https://www.frontiersin.org/articles/10.3389/fragi.2025.1575862/full
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