Cai-Jhen Wu, Chien-Tai Hong, Jiun-Lin Horng, Hung-Shao Lai, Hao-Yu Tsai, Tsorng-Harn Fong, Chen-Yuan Hsiao, Cheng-Ying Chu, Yvonne Jing Mei Liew, Tien-Chun Yang
Aging is the primary risk factor for neurodegenerative disorders, yet the extent to which pervasive environmental oxidants disrupt redox homeostasis to accelerate neuronal aging remains poorly understood. Chlorate (ClO3-) is a ubiquitous disinfection byproduct (DBP) in global drinking-water systems, with current regulatory safety limits established primarily to prevent acute systemic toxicity. Here, we report that chlorate exposure at concentrations overlapping with World Health Organization (WHO) and U.S. Environmental Protection Agency (EPA) guidelines accelerates a p21/p16-mediated senescence program in human induced pluripotent stem cell (iPSC)-derived dopaminergic neurons. Our results demonstrate that this premature aging phenotype is driven by sustained Nrf2/HO-1 signaling activation, signifying a chronic oxidative shift that triggers early-stage neurodegenerative hallmarks, including tau mislocalization and increased alpha-synuclein phosphorylation (pS129). In an in vivo aged zebrafish model, chronic low-dose chlorate exposure induced a progressive locomotor decline that preceded overt neuronal loss, revealing a state of functional senescence distinct from acute apoptosis observed at higher millimolar doses. By identifying chlorate as a previously unrecognized environmental gerontogen that targets redox-sensitive aging pathways, our findings challenge the adequacy of current drinking-water safety frameworks. These results underscore the urgent necessity of incorporating aging-focused endpoints into chemical risk assessments to mitigate the escalating global burden of neurodegenerative diseases.