GSDMD-mediated mitochondrial dysfunction in marginal cells: A potential driver of inflammation and stria vascularis damage in CIHL

Y Yu Xiao X Xiaohan Zhang (Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences) S Siwei Guo (Hunan Provincial Key Laboratory of Anti-Resistance Microbial Drugs) Z Ziyi Liu (New Energy Research Institute, School of Environment and Energy) X Xiaoxu Zhao F Fengyue Dong (Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Science, Shandong University) X Xiuli Bi (Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences) G Guodong Hong (Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences) M Miao Chang (Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences) R Ruifeng Qiao (Department of Otolaryngology-Head and Neck Surgery, Shandong Provincial Ear, Nose and Throat Hospital, Cheeloo College of Medicine, Shandong University) S Shengda Cao (Department of Otorhinolaryngology, Qilu Hospital of Shandong University, National Health Commission Key Laboratory of Otorhinolaryngology, Shandong University) Y Ying Liu M Ming Xia (Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences) W Wei Yuan J Jing Zhang W Wen Li L Liya Zhu (State Key Laboratory of Digital Medical Engineering, Department of Otolaryngology Head and Neck Surgery, Zhongda Hospital, School of Life Sciences and Technology, School of Medicine, Advanced Institute for Life and Health, Jiangsu Province High-Tech Key Laboratory for Bio-Medical Research, Southeast University) R Renjie Chai J Jiangang Gao X Xiaolong Fu

Abstract

Inflammation is among the known causes of cisplatin-induced hearing loss (CIHL), but its exact pathophysiological mechanisms remain unclear. Herein, we demonstrated that pyroptosis—a recently identified inflammatory type of regulated cell death dependent on gasdermin D (GSDMD)—was activated in the cochleae of cisplatin-treated mice, causing CIHL. Meanwhile, treatment with the GSDMD inhibitor necrosulfonamide alleviated CIHL in these mice. To further examine the role of GSDMD-mediated pyroptosis in CIHL, we conducted experiments in Gsdmd- deficient mice . Gsdmd −/− mice demonstrated significantly lower cisplatin-induced cochlear damage than control mice and appeared to be invulnerable to CIHL. Furthermore, GSDMD-mediated pyroptosis in the stria vascularis (SV), but not in the hair cells (HCs), played a dominant role in CIHL. In marginal cells (MCs) of SV, cisplatin induced caspase-dependent GSDMD cleavage, and the pore-forming N-terminal of GSDMD rapidly localized to the mitochondria, leading to abnormal mitochondrial aggregation and oxidative stress. The consequent mitochondrial dysfunction in MCs might result in the severe progression of inflammation, SV damage, and HC loss. Notably, the pharmacological inhibition of pyroptosis using the FDA-approved drug disulfiram effectively alleviated the symptoms of CIHL. Collectively, these findings offer a broad avenue for inhibiting pyroptosis-induced cisplatin ototoxicity and provide valuable theoretical insights for the clinical management of CIHL.

Article Details

Volume / Issue Vol. 122, Issue 11
Published March 18, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (20)

Y

Yu Xiao

X

Xiaohan Zhang

Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences

S

Siwei Guo

Hunan Provincial Key Laboratory of Anti-Resistance Microbial Drugs

Z

Ziyi Liu

New Energy Research Institute, School of Environment and Energy

X

Xiaoxu Zhao

F

Fengyue Dong

Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Science, Shandong University

X

Xiuli Bi

Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences

G

Guodong Hong

Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences

M

Miao Chang

Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences

R

Ruifeng Qiao

Department of Otolaryngology-Head and Neck Surgery, Shandong Provincial Ear, Nose and Throat Hospital, Cheeloo College of Medicine, Shandong University

S

Shengda Cao

Department of Otorhinolaryngology, Qilu Hospital of Shandong University, National Health Commission Key Laboratory of Otorhinolaryngology, Shandong University

Y

Ying Liu

M

Ming Xia

Department of Otolaryngology, Shandong Provincial Hospital, Medical Science and Technology Innovation Center, School of Clinical and Basic Medical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences

W

Wei Yuan

J

Jing Zhang

W

Wen Li

L

Liya Zhu

State Key Laboratory of Digital Medical Engineering, Department of Otolaryngology Head and Neck Surgery, Zhongda Hospital, School of Life Sciences and Technology, School of Medicine, Advanced Institute for Life and Health, Jiangsu Province High-Tech Key Laboratory for Bio-Medical Research, Southeast University

R

Renjie Chai

J

Jiangang Gao

X

Xiaolong Fu