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Peer-reviewedCC BY 4.0Advanced Science

BOULE is Essential for the Dynamic Disassembly of Heat Shock Granules in Male Germ Cells

  • Xin Li1
  • Nana Zhang2
  • Zexin Bian3
  • Baobao Geng4
  • Liyun Cao1
  • Peipei Liu1
  • Zengming Li1
  • Yan Zhao1
  • Jun Tan1
4 affiliations
  1. 1Reproductive Medicine Center Jiangxi Maternal and Child Health Hospital Nanchang Medical College Nanchang Jiangxi Province China
  2. 2Center For Reproductive Medicine The Third Affiliated Hospital of Zhengzhou University Zhengzhou Henan Province China
  3. 3State Key Laboratory of Reproductive Medicine and Offspring Health Nanjing Medical University Nanjing Jiangsu China
  4. 4State Key Laboratory of Common Mechanism Research for Major Diseases Suzhou Institute of Systems Medicine Chinese Academy of Medical Sciences & Peking Union Medical College Suzhou Jiangsu China
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Abstract

Heat shock triggers stress granule (SG) formation, yet their dynamics in mammalian germ cells remain unclear. Through systematic analysis, we uncovered distinct heat shock granule (HSG) composition and stage‐specific assembly/disassembly in the mouse testis. Ribosome profiling revealed that germ cells selectively sustain translation of spermatogenic genes during heat shock. We identified that the germ cell‐specific RNA‐binding protein BOULE is essential for HSG clearance. BOULE deficiency under heat shock impairs HSG disassembly, with increased germ cell apoptosis and a disrupted ubiquitinome. Mechanistically, BOULE orchestrates HSG clearance through a two‐pronged mechanism. It post‐transcriptionally maintains the expression of the disassembly factors G3BP1 and FAF2. Additionally, BOULE promotes heat‐shock‐induced ubiquitination of G3BP1 by regulating the E3 ligase TRIM27, thereby recruiting the VCP/FAF2 complex. Our findings establish BOULE as a key regulator of proteostasis that coordinates HSG disassembly in germ cells, providing mechanistic insight into heat shock‐induced germ cell damage that may contribute to male infertility.

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Cite

BibTeXRIS
BibTeX
@article{li2026boule,
  title = {{BOULE is Essential for the Dynamic Disassembly of Heat Shock Granules in Male Germ Cells}},
  author = {Xin Li and Nana Zhang and Zexin Bian and Baobao Geng and Liyun Cao and Peipei Liu and Zengming Li and Yan Zhao and Jun Tan},
  journal = {Advanced Science},
  year = {2026},
  month = aug,
  doi = {10.1002/advs.77155},
  url = {https://doi.org/10.1002/advs.77155},
  note = {CC BY 4.0},
}
RIS
TY  - JOUR
TI  - BOULE is Essential for the Dynamic Disassembly of Heat Shock Granules in Male Germ Cells
AU  - Xin Li
AU  - Nana Zhang
AU  - Zexin Bian
AU  - Baobao Geng
AU  - Liyun Cao
AU  - Peipei Liu
AU  - Zengming Li
AU  - Yan Zhao
AU  - Jun Tan
PY  - 2026
DA  - 2026/08/13
JO  - Advanced Science
DO  - 10.1002/advs.77155
UR  - https://doi.org/10.1002/advs.77155
AB  - Heat shock triggers stress granule (SG) formation, yet their dynamics in mammalian germ cells remain unclear. Through systematic analysis, we uncovered distinct heat shock granule (HSG) composition and stage‐specific assembly/disassembly in the mouse testis. Ribosome profiling revealed that germ cells selectively sustain translation of spermatogenic genes during heat shock. We identified that the germ cell‐specific RNA‐binding protein BOULE is essential for HSG clearance. BOULE deficiency under heat shock impairs HSG disassembly, with increased germ cell apoptosis and a disrupted ubiquitinome. Mechanistically, BOULE orchestrates HSG clearance through a two‐pronged mechanism. It post‐transcriptionally maintains the expression of the disassembly factors G3BP1 and FAF2. Additionally, BOULE promotes heat‐shock‐induced ubiquitination of G3BP1 by regulating the E3 ligase TRIM27, thereby recruiting the VCP/FAF2 complex. Our findings establish BOULE as a key regulator of proteostasis that coordinates HSG disassembly in germ cells, providing mechanistic insight into heat shock‐induced germ cell damage that may contribute to male infertility.
SN  - 2198-3844
ER  -