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21 July 2022 Testis-specific serine protease PRSS54 regulates acrosomal granule localization and sperm head morphogenesis in mice
Chunling Shen, Wenfeng Xiong, Chaojie Li, Haoyang Ge, Yan Shen, Lingyun Tang, Hongxin Zhang, Shunyuan Lu, Jian Fei, Zhugang Wang
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Abstract

Serine proteases (PRSS) constitute nearly one-third of all proteases, and many of them have been identified to be testis-specific and play significant roles during sperm development and male reproduction. PRSS54 is one of the testis-specific PRSS in mouse and human but its physiological function remains largely unclear. In the present study, we demonstrate in detail that PRSS54 exists not only in testis but also in mature sperm, exhibiting a change in protein size from 50 kDa in testis to 42 kDa in sperm. Loss of PRSS54 in mice results in male subfertility, acrosome deformation, defective sperm–zona penetration, and phenotypes of male subfertility and acrosome deformation can be rescued by Prss54 transgene. Ultrastructure analyses by transmission electronic microscopy further reveal various morphological abnormalities of Prss54–/– spermatids during spermiogenesis, including unfused vacuoles in acrosome, detachment and eccentrical localization of the acrosomal granules, and asymmetrical elongation of the nucleus. Subcellular localization of PRSS54 display that it appears in the acrosomal granule at the early phase of acrosome biogenesis, then extends along the inner acrosomal membrane, and ultimately presents in the acrosome region of the mature sperm. PRSS54 interacts with acrosomal proteins ZPBP1, ZPBP2, ACRBP, and ZP3R, and loss of PRSS54 affects the distribution of these proteins in testis and sperm, although their protein levels are largely unaffected. Moreover, Prss54–/– sperm are more sensitive to acrosome reaction inducers.

Summary Sentence

These data indicate that PRSS54 is an acrosomal protein and plays an important role in regulating acrosome biogenesis, sperm function, and male fertility.

Graphical Abstract

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© The Author(s) 2022. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
Chunling Shen, Wenfeng Xiong, Chaojie Li, Haoyang Ge, Yan Shen, Lingyun Tang, Hongxin Zhang, Shunyuan Lu, Jian Fei, and Zhugang Wang "Testis-specific serine protease PRSS54 regulates acrosomal granule localization and sperm head morphogenesis in mice," Biology of Reproduction 107(4), 1139-1154, (21 July 2022). https://doi.org/10.1093/biolre/ioac146
Received: 5 February 2022; Accepted: 11 July 2022; Published: 21 July 2022
KEYWORDS
acrosomal granule
acrosome biogenesis
male subfertility
PRSS54
sperm–zona penetration
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