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Whether oxidative stress\u2010mediated telomere erosion induces mitochondrial injury, or vice versa, in human T cells\u2014the major effectors of host adaptive immunity against infection and malignancy\u2014is poorly understood due to the pleiotropic effects of ROS. Here we employed a novel chemoptogenetic tool that selectively produces a single oxygen (<jats:sup>1<\/jats:sup>O<jats:sub>2<\/jats:sub>) only at telomeres or mitochondria in Jurkat T cells. We found that targeted <jats:sup>1<\/jats:sup>O<jats:sub>2<\/jats:sub> production at telomeres triggered not only telomeric DNA damage but also mitochondrial dysfunction, resulting in T cell apoptotic death. Conversely, targeted <jats:sup>1<\/jats:sup>O<jats:sub>2<\/jats:sub> formation at mitochondria induced not only mitochondrial injury but also telomeric DNA damage, leading to cellular crisis and apoptosis. Targeted oxidative stress at either telomeres or mitochondria increased ROS production, whereas blocking ROS formation during oxidative stress reversed the telomeric injury, mitochondrial dysfunction, and cellular apoptosis. Notably, the X\u2010ray repair cross\u2010complementing protein 1 (XRCC1) in the base excision repair (BER) pathway and multiple mitochondrial proteins in other cellular pathways were dysregulated by the targeted oxidative stress. By confining singlet <jats:sup>1<\/jats:sup>O<jats:sub>2<\/jats:sub> formation to a single organelle, this study suggests that oxidative stress induces dual injury in T cells via crosstalk between telomeres and mitochondria. Further identification of these oxidation pathways may offer a novel approach to preserve mitochondrial functions, protect telomere integrity, and maintain T cell survival, which can be exploited to combat various immune aging\u2010associated diseases.<\/jats:p>","DOI":"10.1111\/acel.13513","type":"journal-article","created":{"date-parts":[[2021,11,9]],"date-time":"2021-11-09T18:16:14Z","timestamp":1636481774000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":93,"title":["Selective oxidative stress induces dual damage to telomeres and mitochondria in human T cells"],"prefix":"10.1111","volume":"20","author":[{"given":"Ling","family":"Wang","sequence":"first","affiliation":[{"name":"Center of Excellence in Inflammation, Infectious Disease and Immunity Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious, Inflammatory and Immunologic Diseases Department of 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