Loss of C-Terminal Coiled-Coil Domains in SDCCAG8 Impairs Centriolar Satellites and Causes Defective Sperm Flagellum Biogenesis and Male Fertility

Sperm flagellum defects are tightly associated with male infertility. Centriolar satellites are small multiprotein complexes that recruit satellite proteins to the centrosome and play an essential role in sperm flagellum biogenesis, but the precise mechanisms underlying this role remain unclear. <...

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Main Authors: Kecheng Li, Xiaoli Zhou, Wenna Liu, Yange Wang, Zilong Zhang, Houbin Zhang, Li Jiang
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/14/15/1135
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author Kecheng Li
Xiaoli Zhou
Wenna Liu
Yange Wang
Zilong Zhang
Houbin Zhang
Li Jiang
author_facet Kecheng Li
Xiaoli Zhou
Wenna Liu
Yange Wang
Zilong Zhang
Houbin Zhang
Li Jiang
author_sort Kecheng Li
collection DOAJ
description Sperm flagellum defects are tightly associated with male infertility. Centriolar satellites are small multiprotein complexes that recruit satellite proteins to the centrosome and play an essential role in sperm flagellum biogenesis, but the precise mechanisms underlying this role remain unclear. <i>Serologically defined colon cancer autoantigen protein 8</i> (<i>SDCCAG8</i>), which encodes a protein containing eight coiled-coil (CC) domains, has been associated with syndromic ciliopathies and male infertility. However, its exact role in male infertility remains undefined. Here, we used an <i>Sdccag8</i> mutant mouse carrying a CC domains 5–8 truncated mutation (c.1351–1352insG p.E451GfsX467) that models the mutation causing Senior–Løken syndrome (c.1339–1340insG p.E447GfsX463) in humans. The homozygous <i>Sdccag8</i> mutant mice exhibit male infertility characterized by multiple morphological abnormalities of the flagella (MMAF) and dysmorphic structures in the sperm manchette. A mechanistic study revealed that the SDCCAG8 protein is localized to the manchette and centrosomal region and interacts with PCM1, the scaffold protein of centriolar satellites, through its CC domains 5–7. The absence of the CC domains 5–7 in mutant spermatids destabilizes PCM1, which fails to recruit satellite components such as Bardet–Biedl syndrome 4 (BBS4) and centrosomal protein of 131 kDa (CEP131) to satellites, resulting in defective sperm flagellum biogenesis, as BBS4 and CEP131 are essential to flagellum biogenesis. In conclusion, this study reveals the central role of SDCCAG8 in maintaining centriolar satellite integrity during sperm flagellum biogenesis.
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spelling doaj-art-6f6d4d990ec444d0a7690c0ca012f0362025-08-20T04:00:54ZengMDPI AGCells2073-44092025-07-011415113510.3390/cells14151135Loss of C-Terminal Coiled-Coil Domains in SDCCAG8 Impairs Centriolar Satellites and Causes Defective Sperm Flagellum Biogenesis and Male FertilityKecheng Li0Xiaoli Zhou1Wenna Liu2Yange Wang3Zilong Zhang4Houbin Zhang5Li Jiang6School of Medicine, University of Electronic Science and Technology of China, Chengdu 610072, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu 610072, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu 610072, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu 610072, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu 610072, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu 610072, ChinaSchool of Medicine, University of Electronic Science and Technology of China, Chengdu 610072, ChinaSperm flagellum defects are tightly associated with male infertility. Centriolar satellites are small multiprotein complexes that recruit satellite proteins to the centrosome and play an essential role in sperm flagellum biogenesis, but the precise mechanisms underlying this role remain unclear. <i>Serologically defined colon cancer autoantigen protein 8</i> (<i>SDCCAG8</i>), which encodes a protein containing eight coiled-coil (CC) domains, has been associated with syndromic ciliopathies and male infertility. However, its exact role in male infertility remains undefined. Here, we used an <i>Sdccag8</i> mutant mouse carrying a CC domains 5–8 truncated mutation (c.1351–1352insG p.E451GfsX467) that models the mutation causing Senior–Løken syndrome (c.1339–1340insG p.E447GfsX463) in humans. The homozygous <i>Sdccag8</i> mutant mice exhibit male infertility characterized by multiple morphological abnormalities of the flagella (MMAF) and dysmorphic structures in the sperm manchette. A mechanistic study revealed that the SDCCAG8 protein is localized to the manchette and centrosomal region and interacts with PCM1, the scaffold protein of centriolar satellites, through its CC domains 5–7. The absence of the CC domains 5–7 in mutant spermatids destabilizes PCM1, which fails to recruit satellite components such as Bardet–Biedl syndrome 4 (BBS4) and centrosomal protein of 131 kDa (CEP131) to satellites, resulting in defective sperm flagellum biogenesis, as BBS4 and CEP131 are essential to flagellum biogenesis. In conclusion, this study reveals the central role of SDCCAG8 in maintaining centriolar satellite integrity during sperm flagellum biogenesis.https://www.mdpi.com/2073-4409/14/15/1135SDCCAG8centriolar satellitesmale infertilitysperm flagellum biogenesisMMAFspermiogenesis
spellingShingle Kecheng Li
Xiaoli Zhou
Wenna Liu
Yange Wang
Zilong Zhang
Houbin Zhang
Li Jiang
Loss of C-Terminal Coiled-Coil Domains in SDCCAG8 Impairs Centriolar Satellites and Causes Defective Sperm Flagellum Biogenesis and Male Fertility
Cells
SDCCAG8
centriolar satellites
male infertility
sperm flagellum biogenesis
MMAF
spermiogenesis
title Loss of C-Terminal Coiled-Coil Domains in SDCCAG8 Impairs Centriolar Satellites and Causes Defective Sperm Flagellum Biogenesis and Male Fertility
title_full Loss of C-Terminal Coiled-Coil Domains in SDCCAG8 Impairs Centriolar Satellites and Causes Defective Sperm Flagellum Biogenesis and Male Fertility
title_fullStr Loss of C-Terminal Coiled-Coil Domains in SDCCAG8 Impairs Centriolar Satellites and Causes Defective Sperm Flagellum Biogenesis and Male Fertility
title_full_unstemmed Loss of C-Terminal Coiled-Coil Domains in SDCCAG8 Impairs Centriolar Satellites and Causes Defective Sperm Flagellum Biogenesis and Male Fertility
title_short Loss of C-Terminal Coiled-Coil Domains in SDCCAG8 Impairs Centriolar Satellites and Causes Defective Sperm Flagellum Biogenesis and Male Fertility
title_sort loss of c terminal coiled coil domains in sdccag8 impairs centriolar satellites and causes defective sperm flagellum biogenesis and male fertility
topic SDCCAG8
centriolar satellites
male infertility
sperm flagellum biogenesis
MMAF
spermiogenesis
url https://www.mdpi.com/2073-4409/14/15/1135
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