Investigating genotype-phenotype correlation of limb-girdle muscular dystrophy R8: association of clinical severity, protein biological function and protein oligomerization

Abstract Limb-girdle muscular dystrophy R8 (LGMD R8) is a hereditary muscle disease caused by biallelic defects in E3 ubiquitinated ligase gene (TRIM32). LGMD R8 is featured by high genetic heterogeneity and phenotypic diversity, most pathogenic variants are missense variants located in the NHL doma...

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Main Authors: Xiongda Liang, Jiameng Si, Hongting Xie, Yuqing Guan, Wanying Lin, Zezhang Lin, Ganwei Zheng, Xiaofeng Wei, Xingbang Xiong, Zhengfei Zhuang, Xuan Shang
Format: Article
Language:English
Published: BMC 2025-03-01
Series:Acta Neuropathologica Communications
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Online Access:https://doi.org/10.1186/s40478-025-01971-8
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author Xiongda Liang
Jiameng Si
Hongting Xie
Yuqing Guan
Wanying Lin
Zezhang Lin
Ganwei Zheng
Xiaofeng Wei
Xingbang Xiong
Zhengfei Zhuang
Xuan Shang
author_facet Xiongda Liang
Jiameng Si
Hongting Xie
Yuqing Guan
Wanying Lin
Zezhang Lin
Ganwei Zheng
Xiaofeng Wei
Xingbang Xiong
Zhengfei Zhuang
Xuan Shang
author_sort Xiongda Liang
collection DOAJ
description Abstract Limb-girdle muscular dystrophy R8 (LGMD R8) is a hereditary muscle disease caused by biallelic defects in E3 ubiquitinated ligase gene (TRIM32). LGMD R8 is featured by high genetic heterogeneity and phenotypic diversity, most pathogenic variants are missense variants located in the NHL domain, but the genotype-phenotype correlation remains unclear. We hypothesized that various missense variants in NHL domain might have different degrees of impact on the structure and function of the protein, thus resulting in disease variability. Firstly, by analyzing present patients’ clinical data, we screen out 4 variants: R394H, D487N, V591M and P619S. Patients homozygous for the aforementioned variants exhibited significant phenotypic variability, including variations in age of onset and age of any walking aid (AWA). Then, bioinformatics analysis, cellular functional experiment and biophysical assay were used to measure the effect of above variants in TRIM32 protein oligomerization and ubiquitination to target substrates. And they revealed distinct differences in the intrinsic E3 ligase activity among various mutant TRIM32 proteins, which corresponded to differences in their oligomerization status. In conclusion, our results showed a correlation between clinical severity, protein function and oligomerization state in patients homozygous for missense variants in NHL domain. It is the first time to reveal a connection between TRIM32 variant with LGMD R8 phenotype and this finding provided valuable reference in predicting disease severity and more precise guidance to affected family on genetic counseling.
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publishDate 2025-03-01
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series Acta Neuropathologica Communications
spelling doaj-art-28def78c102d4c34b3d4e3c59b7b46b52025-08-20T03:53:16ZengBMCActa Neuropathologica Communications2051-59602025-03-0113111310.1186/s40478-025-01971-8Investigating genotype-phenotype correlation of limb-girdle muscular dystrophy R8: association of clinical severity, protein biological function and protein oligomerizationXiongda Liang0Jiameng Si1Hongting Xie2Yuqing Guan3Wanying Lin4Zezhang Lin5Ganwei Zheng6Xiaofeng Wei7Xingbang Xiong8Zhengfei Zhuang9Xuan Shang10Department of Medical Genetics, School of Basic Medical Science, Southern Medical UniversityDepartment of Medical Genetics, School of Basic Medical Science, Southern Medical UniversityDepartment of Medical Genetics, School of Basic Medical Science, Southern Medical UniversityDepartment of Neurology, Nanfang Hospital, Southern Medical UniversityDepartment of Laboratory Medicine, Nanfang Hospital, Southern Medical UniversityDepartment of Medical Genetics, School of Basic Medical Science, Southern Medical UniversityDepartment of Medical Genetics, School of Basic Medical Science, Southern Medical UniversityDepartment of Medical Genetics, School of Basic Medical Science, Southern Medical UniversityCollege of Biophotonics, South China Normal UniversityCollege of Biophotonics, South China Normal UniversityDepartment of Medical Genetics, School of Basic Medical Science, Southern Medical UniversityAbstract Limb-girdle muscular dystrophy R8 (LGMD R8) is a hereditary muscle disease caused by biallelic defects in E3 ubiquitinated ligase gene (TRIM32). LGMD R8 is featured by high genetic heterogeneity and phenotypic diversity, most pathogenic variants are missense variants located in the NHL domain, but the genotype-phenotype correlation remains unclear. We hypothesized that various missense variants in NHL domain might have different degrees of impact on the structure and function of the protein, thus resulting in disease variability. Firstly, by analyzing present patients’ clinical data, we screen out 4 variants: R394H, D487N, V591M and P619S. Patients homozygous for the aforementioned variants exhibited significant phenotypic variability, including variations in age of onset and age of any walking aid (AWA). Then, bioinformatics analysis, cellular functional experiment and biophysical assay were used to measure the effect of above variants in TRIM32 protein oligomerization and ubiquitination to target substrates. And they revealed distinct differences in the intrinsic E3 ligase activity among various mutant TRIM32 proteins, which corresponded to differences in their oligomerization status. In conclusion, our results showed a correlation between clinical severity, protein function and oligomerization state in patients homozygous for missense variants in NHL domain. It is the first time to reveal a connection between TRIM32 variant with LGMD R8 phenotype and this finding provided valuable reference in predicting disease severity and more precise guidance to affected family on genetic counseling.https://doi.org/10.1186/s40478-025-01971-8Genotype-phenotype correlationLGMD R8NHL domainOligomerizationTRIM32
spellingShingle Xiongda Liang
Jiameng Si
Hongting Xie
Yuqing Guan
Wanying Lin
Zezhang Lin
Ganwei Zheng
Xiaofeng Wei
Xingbang Xiong
Zhengfei Zhuang
Xuan Shang
Investigating genotype-phenotype correlation of limb-girdle muscular dystrophy R8: association of clinical severity, protein biological function and protein oligomerization
Acta Neuropathologica Communications
Genotype-phenotype correlation
LGMD R8
NHL domain
Oligomerization
TRIM32
title Investigating genotype-phenotype correlation of limb-girdle muscular dystrophy R8: association of clinical severity, protein biological function and protein oligomerization
title_full Investigating genotype-phenotype correlation of limb-girdle muscular dystrophy R8: association of clinical severity, protein biological function and protein oligomerization
title_fullStr Investigating genotype-phenotype correlation of limb-girdle muscular dystrophy R8: association of clinical severity, protein biological function and protein oligomerization
title_full_unstemmed Investigating genotype-phenotype correlation of limb-girdle muscular dystrophy R8: association of clinical severity, protein biological function and protein oligomerization
title_short Investigating genotype-phenotype correlation of limb-girdle muscular dystrophy R8: association of clinical severity, protein biological function and protein oligomerization
title_sort investigating genotype phenotype correlation of limb girdle muscular dystrophy r8 association of clinical severity protein biological function and protein oligomerization
topic Genotype-phenotype correlation
LGMD R8
NHL domain
Oligomerization
TRIM32
url https://doi.org/10.1186/s40478-025-01971-8
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