Circular RNAs from BOULE play conserved roles in protection against stress-induced fertility decline

Liuze Gao; Shuhui Chang; Wenjuan Xia; Xiaolin Wang; Chenwang Zhang; Liping Cheng; Xu Liu; Liang Chen; Qinghua Shi; Juan Huang; Eugene Yujun Xu; Ge Shan

doi:10.1126/sciadv.abb7426

Circular RNAs from BOULE play conserved roles in protection against stress-induced fertility decline

Liuze Gao, Shuhui Chang, Wenjuan Xia, Xiaolin Wang, Chenwang Zhang, Liping Cheng, Xu Liu, Liang Chen, Qinghua Shi, Juan Huang, Eugene Yujun Xu^*, Ge Shan

^*Corresponding author for this work

Neurology

Research output: Contribution to journal › Article › peer-review

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Abstract

Circular RNAs (circRNAs) are a large family of newly identified transcripts, and their physiological roles and evolutionary significance require further characterization. Here, we identify circRNAs generated from a conserved reproductive gene, Boule, in species from Drosophila to humans. Flies missing circular Boule (circBoule) RNAs display decreased male fertility, and sperm of circBoule knockout mice exhibit decreased fertilization capacity, when under heat stress conditions. During spermatogenesis, fly circBoule RNAs interact with heat shock proteins (HSPs) Hsc4 and Hsp60C, and mouse circBoule RNAs in sperm interact with HSPA2. circBoule RNAs regulate levels of HSPs by promoting their ubiquitination. The interaction between HSPA2 and circBoule RNAs is conserved in human sperm, and lower levels of the human circBoule RNAs circEx3-6 and circEx2-7 are found in asthenozoospermic sperm. Our findings reveal conserved physiological functions of circBoule RNAs in metazoans and suggest that specific circRNAs may be critical modulators of male reproductive function against stresses in animals.

Original language	English (US)
Article number	eabb7426
Journal	Science Advances
Volume	6
Issue number	46
DOIs	https://doi.org/10.1126/sciadv.abb7426
State	Published - Nov 11 2020

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title = "Circular RNAs from BOULE play conserved roles in protection against stress-induced fertility decline",

abstract = "Circular RNAs (circRNAs) are a large family of newly identified transcripts, and their physiological roles and evolutionary significance require further characterization. Here, we identify circRNAs generated from a conserved reproductive gene, Boule, in species from Drosophila to humans. Flies missing circular Boule (circBoule) RNAs display decreased male fertility, and sperm of circBoule knockout mice exhibit decreased fertilization capacity, when under heat stress conditions. During spermatogenesis, fly circBoule RNAs interact with heat shock proteins (HSPs) Hsc4 and Hsp60C, and mouse circBoule RNAs in sperm interact with HSPA2. circBoule RNAs regulate levels of HSPs by promoting their ubiquitination. The interaction between HSPA2 and circBoule RNAs is conserved in human sperm, and lower levels of the human circBoule RNAs circEx3-6 and circEx2-7 are found in asthenozoospermic sperm. Our findings reveal conserved physiological functions of circBoule RNAs in metazoans and suggest that specific circRNAs may be critical modulators of male reproductive function against stresses in animals.",

author = "Liuze Gao and Shuhui Chang and Wenjuan Xia and Xiaolin Wang and Chenwang Zhang and Liping Cheng and Xu Liu and Liang Chen and Qinghua Shi and Juan Huang and Xu, {Eugene Yujun} and Ge Shan",

note = "Funding Information: This work was supported by funding from the National Key R&D Program of China (2019YFA0802600 and 2018YFC1004500), the National Natural Science Foundation of China (31930019, 31725016, 91940303, 31771652, and 31970792), and the Strategic Priority Research Program {"}Biological basis of aging and therapeutic strategies{"} of the Chinese Academy of Sciences (XDB39010400). Publisher Copyright: Copyright {\textcopyright} 2020 The Authors, some rights reserved.",

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doi = "10.1126/sciadv.abb7426",

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AU - Gao, Liuze

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AU - Xia, Wenjuan

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AU - Cheng, Liping

AU - Liu, Xu

AU - Chen, Liang

AU - Shi, Qinghua

AU - Huang, Juan

AU - Xu, Eugene Yujun

AU - Shan, Ge

N1 - Funding Information: This work was supported by funding from the National Key R&D Program of China (2019YFA0802600 and 2018YFC1004500), the National Natural Science Foundation of China (31930019, 31725016, 91940303, 31771652, and 31970792), and the Strategic Priority Research Program "Biological basis of aging and therapeutic strategies" of the Chinese Academy of Sciences (XDB39010400). Publisher Copyright: Copyright © 2020 The Authors, some rights reserved.

PY - 2020/11/11

Y1 - 2020/11/11

N2 - Circular RNAs (circRNAs) are a large family of newly identified transcripts, and their physiological roles and evolutionary significance require further characterization. Here, we identify circRNAs generated from a conserved reproductive gene, Boule, in species from Drosophila to humans. Flies missing circular Boule (circBoule) RNAs display decreased male fertility, and sperm of circBoule knockout mice exhibit decreased fertilization capacity, when under heat stress conditions. During spermatogenesis, fly circBoule RNAs interact with heat shock proteins (HSPs) Hsc4 and Hsp60C, and mouse circBoule RNAs in sperm interact with HSPA2. circBoule RNAs regulate levels of HSPs by promoting their ubiquitination. The interaction between HSPA2 and circBoule RNAs is conserved in human sperm, and lower levels of the human circBoule RNAs circEx3-6 and circEx2-7 are found in asthenozoospermic sperm. Our findings reveal conserved physiological functions of circBoule RNAs in metazoans and suggest that specific circRNAs may be critical modulators of male reproductive function against stresses in animals.

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Circular RNAs from BOULE play conserved roles in protection against stress-induced fertility decline

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