The landscape of RNA-binding proteins in mammalian spermatogenesis-Reference-Cited by-同舟云学术

The landscape of RNA-binding proteins in mammalian spermatogenesis

Published:2024-08-29 Issue: Volume: Page:
ISSN:0036-8075
Container-title:Science
language:en
Short-container-title:Science

Author:

Li Yang¹^ORCID,Wang Yuanyuan¹²^ORCID,Tan Yue-Qiu³⁴^ORCID,Yue Qiuling¹⁵^ORCID,Guo Yueshuai¹^ORCID,Yan Ruoyu¹⁶^ORCID,Meng Lanlan³⁴,Zhai Huicong¹^ORCID,Tong Lingxiu¹^ORCID,Yuan Zihan¹^ORCID,Li Wu¹,Wang Cuicui¹,Han Shenglin¹^ORCID,Ren Sen¹^ORCID,Yan Yitong²,Wang Weixu⁷,Gao Lei¹,Tan Chen³,Hu Tongyao³,Zhang Hao¹^ORCID,Liu Liya²,Yang Pinglan¹,Jiang Wanyin¹,Ye Yiting¹,Tan Huanhuan¹,Wang Yanfeng¹,Lu Chenyu¹,Li Xin¹,Xie Jie¹^ORCID,Yuan Gege¹,Cui Yiqiang¹^ORCID,Shen Bin¹^ORCID,Wang Cheng¹⁸^ORCID,Guan Yichun⁹,Li Wei¹⁰^ORCID,Shi Qinghua¹¹^ORCID,Lin Ge³⁴,Ni Ting¹²^ORCID,Sun Zheng¹³^ORCID,Ye Lan¹^ORCID,Vourekas Anastasios¹⁴^ORCID,Guo Xuejiang¹^ORCID,Lin Mingyan²¹⁵¹⁶^ORCID,Zheng Ke¹^ORCID

Affiliation:

1. State Key Laboratory of Reproductive Medicine and Offspring Health, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing 211166, China.

2. Department of Neurobiology, School of Basic Medical Science, Nanjing Medical University, Nanjing 211166, China.

3. Institute of Reproductive and Stem Cell Engineering, NHC Key Laboratory of Human Stem Cell and Reproductive Engineering, School of Basic Medical Science, Central South University, Changsha 410083, China.

4. Clinical Research Center for Reproduction and Genetics in Hunan Province, Reproductive and Genetic Hospital of CITIC-Xiangya, Changsha 410008, China.

5. Department of Andrology, Nanjing Drum Tower Hospital, the Affiliated Hospital of Nanjing University, Nanjing 210008, China.

6. College of Life Sciences, Northwest A&F University, Yangling 712100, China.

7. Institute of Computational Biology, Helmholtz Center Munich, Munich 85764, Germany.

8. Department of Bioinformatics, School of Biomedical Engineering and Informatics, Nanjing Medical University, Nanjing 211166, China.

9. Center for Reproductive Medicine, the Third Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, China.

10. Guangzhou Women and Children’s Medical Center, Guangzhou Medical University, Guangzhou 510623, China.

11. Division of Reproduction and Genetics, First Affiliated Hospital of USC, Hefei National Laboratory for Physical Sciences at Microscale, School of Basic Medical Sciences, Division of Life Sciences and Medicine, Biomedical Sciences and Health Laboratory of Anhui Province, University of Science and Technology of China, Hefei 230027, Anhui, China.

12. State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Human Phenome Institute, Shanghai Engineering Research Center of Industrial Microorganisms, School of Life Sciences and Huashan Hospital, Fudan University, Shanghai 200438, China.

13. Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.

14. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.

15. Changzhou Medical Center, The Affiliated Changzhou Second People’s Hospital of Nanjing Medical University, Changzhou 213000, China.

16. Division of Birth Cohort Study, Fujian Maternity and Child Health Hospital, Fuzhou 350014, China.

Abstract

Despite continuous expansion of the RNA-binding protein (RBP) world, there is a lack of systematic understanding of RBPs in mammalian testis, which harbors one of the most complex tissue transcriptomes. We adapted RNA interactome capture to mouse male germ cells, building an RBP atlas characterized by multiple layers of dynamics along spermatogenesis. Trapping of RNA-crosslinked peptides showed that the glutamic acid-arginine (ER) patch, a residue-coevolved polyampholytic element present in coiled-coils, enhances RNA binding of its host RBPs. Deletion of this element in NONO (non-POU domain-containing octamer-binding protein) led to a defective mitosis-to-meiosis transition due to compromised NONO-RNA interactions. Whole-exome sequencing of over 1000 infertile men revealed a prominent role of RBPs in the human genetic architecture of male infertility and identified risk ER patch variants.

Publisher

American Association for the Advancement of Science (AAAS)

Link

https://www.science.org/doi/pdf/10.1126/science.adj8172

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