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The male germline-specific protein MAPS is indispensable for pachynema progression and fertility

Authors
  • Li, Miao1, 2
  • Zheng, Jiahuan1, 2
  • Li, Gaopeng3
  • Lin, Zexiong1
  • Li, Dongliang1
  • Liu, Dongteng1, 2
  • Feng, Haiwei1, 2
  • Cao, Dandan1
  • Ng, Ernest H. Y.1, 2
  • Li, Raymond H. W.1, 2
  • Han, Chunsheng4, 4, 4
  • Yeung, William S. B.1, 2
  • Chow, Louise T.3
  • Wang, Hengbin3
  • Liu, Kui1, 2
  • 1 The University of Hong Kong–Shenzhen Hospital, China , (China)
  • 2 The University of Hong Kong, China , (China)
  • 3 University of Alabama at Birmingham, AL
  • 4 Chinese Academy of Sciences, China , (China)
Type
Published Article
Journal
Proceedings of the National Academy of Sciences
Publisher
Proceedings of the National Academy of Sciences
Publication Date
Feb 18, 2021
Volume
118
Issue
8
Identifiers
DOI: 10.1073/pnas.2025421118
PMID: 33602822
PMCID: PMC7923350
Source
PubMed Central
Keywords
Disciplines
  • Biological Sciences
  • Developmental Biology
License
Green

Abstract

Meiosis is a specialized cell division that creates haploid germ cells from diploid progenitors. Through differential RNA expression analyses, we previously identified a number of mouse genes that were dramatically elevated in spermatocytes, relative to their very low expression in spermatogonia and somatic organs. Here, we investigated in detail 1700102P08Rik, one of these genes, and independently conclude that it encodes a male germline-specific protein, in agreement with a recent report. We demonstrated that it is essential for pachynema progression in spermatocytes and named it male pachynema-specific (MAPS) protein. Mice lacking Maps ( Maps −/− ) suffered from pachytene arrest and spermatocyte death, leading to male infertility, whereas female fertility was not affected. Interestingly, pubertal Maps −/− spermatocytes were arrested at early pachytene stage, accompanied by defects in DNA double-strand break (DSB) repair, crossover formation, and XY body formation. In contrast, adult Maps −/− spermatocytes only exhibited partially defective crossover but nonetheless were delayed or failed in progression from early to mid- and late pachytene stage, resulting in cell death. Furthermore, we report a significant transcriptional dysregulation in autosomes and XY chromosomes in both pubertal and adult Maps −/− pachytene spermatocytes, including failed meiotic sex chromosome inactivation (MSCI). Further experiments revealed that MAPS overexpression in vitro dramatically decreased the ubiquitination levels of cellular proteins. Conversely, in Maps −/− pachytene cells, protein ubiquitination was dramatically increased, likely contributing to the large-scale disruption in gene expression in pachytene cells. Thus, MAPS is a protein essential for pachynema progression in male mice, possibly in mammals in general.

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