ASB9 promotes ubiquitin-mediated degradation of TNP2 to facilitate histone-to-protamine transition in humans and mice

S Shikun Zhao (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University) G Gan Shen (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University) T Tiechao Ruan (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University) L Liangchai Zhuo (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University) Y Yan Wang X Xiang Wang Y Yunchuan Tian (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University) X Xinyao Tang (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University) J Jun Ma X Xiaohui Jiang Y Yingteng Zhang (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University) C Chuan Jiang (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University) A Anan Xie (College of Biological Sciences, University of California) X Xuejun Shang (Department of Urology, Jinling Hospital, Affiliated Hospital of Medical School, Nanjing University) J Jing Wang (Hunan Cancer Hospital Changsha China) Y Yihong Yang (Department of Reproduction Medical Centre, West China Second University Hospital, Sichuan University) Y Ying Shen (Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University)

Abstract

During spermiogenesis, nuclear remodeling occurs where histones are sequentially replaced by transition proteins (TNPs) and protamines, a process essential for sperm maturation. Although the degradation of histones and TNPs is thought to be essential for sperm nuclear remodeling, the underlying mechanisms, particularly those governing TNP degradation, remain poorly understood. In this study, we investigated the role of the ankyrin repeat-containing SOCS box protein 9 (ASB9) during spermiogenesis and found that its deficiency causes TNP2 retention, leading to a failure of the histone-to-protamine transition in both humans and mice. This disruption consequently causes male infertility, characterized by sperm head malformation and impairments in fertilization and early embryonic development. Mechanistically, we found that ASB9 assembles a testis-specific Cullin-RING ligase (CRL) complex—TNP2–ASB9–ELOB/C–CUL5–RBX1—that mediates the ubiquitin-dependent degradation of TNP2 to facilitate the histone-to-protamine transition during spermiogenesis. Collectively, our study uncovers the mechanism underlying TNP2 degradation and highlights the critical role of ASB9 in male fertility through the CRL complex-mediated ubiquitination pathway, thereby expanding the fundamental understanding of nuclear remodeling during spermiogenesis.

Article Details

Volume / Issue Vol. 123, Issue 14
Published April 07, 2026
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (17)

S

Shikun Zhao

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University

G

Gan Shen

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University

T

Tiechao Ruan

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University

L

Liangchai Zhuo

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University

Y

Yan Wang

X

Xiang Wang

Y

Yunchuan Tian

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University

X

Xinyao Tang

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University

J

Jun Ma

X

Xiaohui Jiang

Y

Yingteng Zhang

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University

C

Chuan Jiang

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University

A

Anan Xie

College of Biological Sciences, University of California

X

Xuejun Shang

Department of Urology, Jinling Hospital, Affiliated Hospital of Medical School, Nanjing University

J

Jing Wang

Hunan Cancer Hospital Changsha China

Y

Yihong Yang

Department of Reproduction Medical Centre, West China Second University Hospital, Sichuan University

Y

Ying Shen

Department of Obstetrics/Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children of Ministry of Education, West China Second University Hospital, Sichuan University