In situ architecture of the intercellular organelle reservoir between epididymal epithelial cells by volume electron microscopy

Xia Li, Feng Qiao, Jiansheng Guo, Ting Jiang, Huifang Lou, Huixia Li, Gangcai Xie, Hangjun Wu, Weizhen Wang, Ruoyu Pei, Sha Liu, Mei Ye, Jin Li, Shiqin Huang, Mengya Zhang, Chaoye Ma, Yiwen Huang, Shushu Xu, Xiaofeng Li, Xiao Sun, Jun Yu, Kin Lam Fok, Shumin Duan () and Hao Chen ()
Additional contact information
Xia Li: Guangzhou Medical University
Feng Qiao: Guangzhou Medical University
Jiansheng Guo: Zhejiang University
Ting Jiang: Guangzhou Medical University
Huifang Lou: Zhejiang University
Huixia Li: Guangzhou Medical University
Gangcai Xie: Guangzhou Medical University
Hangjun Wu: Zhejiang University
Weizhen Wang: Guangzhou Medical University
Ruoyu Pei: Guangzhou Medical University
Sha Liu: Guangzhou Medical University
Mei Ye: Guangzhou Medical University
Jin Li: Guangzhou Medical University
Shiqin Huang: Guangzhou Medical University
Mengya Zhang: Guangzhou Medical University
Chaoye Ma: Guangzhou Medical University
Yiwen Huang: Guangzhou Medical University
Shushu Xu: Guangzhou Medical University
Xiaofeng Li: Department of Laboratory Medicine, Peking University Shenzhen Hospital
Xiao Sun: Zhejiang University School of Medicine
Jun Yu: Guangzhou Medical University
Kin Lam Fok: The Chinese University of Hong Kong
Shumin Duan: Zhejiang University
Hao Chen: Guangzhou Medical University

Nature Communications, 2025, vol. 16, issue 1, 1-15

Abstract: Abstract Mammalian epididymal epithelial cells are crucial for sperm maturation. Historically, vacuole-like ultrastructures in epididymal epithelial cells were observed via transmission electron microscopy but were undefined. Here, we utilize volume electron microscopy (vEM) to generate 3D reconstructions of epididymal epithelial cells and identify these vacuoles as intercellular organelle reservoirs (IORs) in the lateral intercellular space (LIS), which contains protein aggregates, autophagosomes, lysosome-related organelles and mitochondrial residues. Immunolabelling of organelle markers such as P62, LC3, LAMP1 and TOMM20 confirm these findings. The IOR size or number varies across four epididymal regions and decreases with age. Rab27a mutant mice exhibit reduced IORs in the caput epididymis and a subfertility phenotype, suggesting the involvement of Rab27a in the formation of IORs. Furthermore, we observe the presence of IORs between intestinal epithelial cells besides epididymis. Amino acid transporters at IOR edges suggest dynamic protein recycling. Our findings reveal that the IOR is an important structure critical for organelle turnover and recycling outside epithelial cells with limited self-degradation capabilities.

Date: 2025
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DOI: 10.1038/s41467-025-56807-9

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