Age-related declines in niche self-renewal factors controls testis aging and spermatogonial stem cell competition through Hairless, Imp, and Chinmo

Aging is associated with progressive tissue decline and shifts in stem cell clonality. The role of niche signals in driving these processes remains poorly understood. Using the testis, we identify a regulatory axis in which age-related decline of niche signals (BMPs) lead to upregulation of the co-r...

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Main Authors Zheng, Yu, Lee, Ya-Chien, Wang, Yu-Ting, Chiang, Pin-Kuan, Chang, Shao-Lun, Hsu, Hwei-Jan, Hsu, Li-Sung, Bach, Erika A, Tseng, Chen-Yuan
Format Journal Article Paper
LanguageEnglish
Published United States Cold Spring Harbor Laboratory 03.05.2025
Edition1.2
Subjects
Genetics
stem cell niche
Chinmo
spermatogonial stem cell
BMP
Dpp
Gbb
germline stem cell
competition
testis
aging
Hairless
Imp
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Abstract Aging is associated with progressive tissue decline and shifts in stem cell clonality. The role of niche signals in driving these processes remains poorly understood. Using the testis, we identify a regulatory axis in which age-related decline of niche signals (BMPs) lead to upregulation of the co-repressor Hairless, which downregulates the RNA-binding protein Imp in aged germline stem cells (GSCs). Reduced Imp causes loss of Chinmo, a key factor in GSC aging and competition. Reduced Chinmo causes ectopic Perlecan secretion which accumulates in the testis lumen and causes GSC loss. Aging of the testis is reversed by increasing BMPs in the niche, or by overexpressing Imp or depleting Hairless in GSCs. Furthermore, GSC clones with reduced Imp or increased Hairless are more competitive, expelling wild-type neighbors and monopolizing the niche. Thus, BMPs regulate testicular niche aging through the Hairless-Imp-Chinmo axis and "winning" GSCs usurp these aging mechanisms. Aged niche cells produce less BMPs, resulting in more Hairless (H) in aged GSCs Elevated H represses , resulting in less Chinmo and in ectopic ECM secretion Aging is prevented by higher BMP in niche cells, or by higher Imp or lower H in GSCs GSCs with low or high exploit these aging mechanisms to colonize the GSC pool.
AbstractList Aging is associated with progressive tissue decline and shifts in stem cell clonality. The role of niche signals in driving these processes remains poorly understood. Using the Drosophila testis, we identify a regulatory axis in which age-related decline of niche signals (BMPs) lead to upregulation of the co-repressor Hairless, which downregulates the RNA-binding protein Imp in aged germline stem cells (GSCs). Reduced Imp causes loss of Chinmo, a key factor in GSC aging and competition. Reduced Chinmo causes ectopic Perlecan secretion which accumulates in the testis lumen and causes GSC loss. Aging of the testis is reversed by increasing BMPs in the niche, or by overexpressing Imp or depleting Hairless in GSCs. Furthermore, GSC clones with reduced Imp or increased Hairless are more competitive, expelling wild-type neighbors and monopolizing the niche. Thus, BMPs regulate testicular niche aging through the Hairless–Imp–Chinmo axis and “winning” GSCs usurp these aging mechanisms. Aged niche cells produce less BMPs, resulting in more Hairless (H) in aged GSCs Elevated H represses Imp, resulting in less Chinmo and in ectopic ECM secretion Aging is prevented by higher BMP in niche cells, or by higher Imp or lower H in GSCs GSCs with low Imp or high H exploit these aging mechanisms to colonize the GSC pool
Aging is associated with progressive tissue decline and shifts in stem cell clonality. The role of niche signals in driving these processes remains poorly understood. Using the Drosophila testis, we identify a regulatory axis in which age-related decline of niche signals (BMPs) lead to upregulation of the co-repressor Hairless, which downregulates the RNA-binding protein Imp in aged germline stem cells (GSCs). Reduced Imp causes loss of Chinmo, a key factor in GSC aging and competition. Reduced Chinmo causes ectopic Perlecan secretion which accumulates in the testis lumen and causes GSC loss. Aging of the testis is reversed by increasing BMPs in the niche, or by overexpressing Imp or depleting Hairless in GSCs. Furthermore, GSC clones with reduced Imp or increased Hairless are more competitive, expelling wild-type neighbors and monopolizing the niche. Thus, BMPs regulate testicular niche aging through the Hairless-Imp-Chinmo axis and "winning" GSCs usurp these aging mechanisms.Aging is associated with progressive tissue decline and shifts in stem cell clonality. The role of niche signals in driving these processes remains poorly understood. Using the Drosophila testis, we identify a regulatory axis in which age-related decline of niche signals (BMPs) lead to upregulation of the co-repressor Hairless, which downregulates the RNA-binding protein Imp in aged germline stem cells (GSCs). Reduced Imp causes loss of Chinmo, a key factor in GSC aging and competition. Reduced Chinmo causes ectopic Perlecan secretion which accumulates in the testis lumen and causes GSC loss. Aging of the testis is reversed by increasing BMPs in the niche, or by overexpressing Imp or depleting Hairless in GSCs. Furthermore, GSC clones with reduced Imp or increased Hairless are more competitive, expelling wild-type neighbors and monopolizing the niche. Thus, BMPs regulate testicular niche aging through the Hairless-Imp-Chinmo axis and "winning" GSCs usurp these aging mechanisms.Aged niche cells produce less BMPs, resulting in more Hairless (H) in aged GSCs Elevated H represses Imp , resulting in less Chinmo and in ectopic ECM secretion Aging is prevented by higher BMP in niche cells, or by higher Imp or lower H in GSCs GSCs with low Imp or high H exploit these aging mechanisms to colonize the GSC pool.HighlightsAged niche cells produce less BMPs, resulting in more Hairless (H) in aged GSCs Elevated H represses Imp , resulting in less Chinmo and in ectopic ECM secretion Aging is prevented by higher BMP in niche cells, or by higher Imp or lower H in GSCs GSCs with low Imp or high H exploit these aging mechanisms to colonize the GSC pool.
Aging is associated with progressive tissue decline and shifts in stem cell clonality. The role of niche signals in driving these processes remains poorly understood. Using the Drosophila testis, we identify a regulatory axis in which age-related decline of niche signals (BMPs) lead to upregulation of the co-repressor Hairless, which downregulates the RNA-binding protein Imp in aged germline stem cells (GSCs). Reduced Imp causes loss of Chinmo, a key factor in GSC aging and competition. Reduced Chinmo causes ectopic Perlecan secretion which accumulates in the testis lumen and causes GSC loss. Aging of the testis is reversed by increasing BMPs in the niche, or by overexpressing Imp or depleting Hairless in GSCs. Furthermore, GSC clones with reduced Imp or increased Hairless are more competitive, expelling wild-type neighbors and monopolizing the niche. Thus, BMPs regulate testicular niche aging through the Hairless–Imp–Chinmo axis and “winning” GSCs usurp these aging mechanisms.
Aging is associated with progressive tissue decline and shifts in stem cell clonality. The role of niche signals in driving these processes remains poorly understood. Using the testis, we identify a regulatory axis in which age-related decline of niche signals (BMPs) lead to upregulation of the co-repressor Hairless, which downregulates the RNA-binding protein Imp in aged germline stem cells (GSCs). Reduced Imp causes loss of Chinmo, a key factor in GSC aging and competition. Reduced Chinmo causes ectopic Perlecan secretion which accumulates in the testis lumen and causes GSC loss. Aging of the testis is reversed by increasing BMPs in the niche, or by overexpressing Imp or depleting Hairless in GSCs. Furthermore, GSC clones with reduced Imp or increased Hairless are more competitive, expelling wild-type neighbors and monopolizing the niche. Thus, BMPs regulate testicular niche aging through the Hairless-Imp-Chinmo axis and "winning" GSCs usurp these aging mechanisms. Aged niche cells produce less BMPs, resulting in more Hairless (H) in aged GSCs Elevated H represses , resulting in less Chinmo and in ectopic ECM secretion Aging is prevented by higher BMP in niche cells, or by higher Imp or lower H in GSCs GSCs with low or high exploit these aging mechanisms to colonize the GSC pool.
Author Hsu, Hwei-Jan
Zheng, Yu
Tseng, Chen-Yuan
Chang, Shao-Lun
Hsu, Li-Sung
Chiang, Pin-Kuan
Lee, Ya-Chien
Wang, Yu-Ting
Bach, Erika A
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Keywords stem cell niche
Chinmo
spermatogonial stem cell
BMP
Dpp
Gbb
germline stem cell
competition
testis
aging
Hairless
Imp
Language English
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Snippet Aging is associated with progressive tissue decline and shifts in stem cell clonality. The role of niche signals in driving these processes remains poorly...
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SubjectTerms Genetics
Title Age-related declines in niche self-renewal factors controls testis aging and spermatogonial stem cell competition through Hairless, Imp, and Chinmo
URI https://www.ncbi.nlm.nih.gov/pubmed/40370955
https://www.proquest.com/docview/3204332839
https://www.biorxiv.org/content/10.1101/2025.05.01.651651
https://pubmed.ncbi.nlm.nih.gov/PMC12077873
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