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Research

Integrative Proteomic and Phosphoproteomic Profiling of Testis from Wip1 Phosphatase-Knockout Mice: Insights into Mechanisms of Reduced Fertility*

Yinghui Wei, Qian Gao, Pengxia Niu, Kui Xu, Yiqing Qiu, Yanqing Hu, Shasha Liu, Xue Zhang, Miaoying Yu, Zhiguo Liu, Bingyuan Wang, View ORCID ProfileYulian Mu  Correspondence email and Kui Li  Correspondence email
Molecular & Cellular Proteomics February 1, 2019, First published on October 25, 2018, 18 (2) 216-230; https://doi.org/10.1074/mcp.RA117.000479
Yinghui Wei
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Qian Gao
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Pengxia Niu
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Kui Xu
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Yiqing Qiu
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Yanqing Hu
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Shasha Liu
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Xue Zhang
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Miaoying Yu
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Zhiguo Liu
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Bingyuan Wang
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Yulian Mu
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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  • ORCID record for Yulian Mu
  • For correspondence: mouyulian@caas.cn
Kui Li
From the ‡State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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  • For correspondence: likui@caas.cn
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Graphical Abstract

Figure1
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Highlights

  • Mice lacking Wip1 display spermatogenesis defects at the late-stage germ cell types.

  • Proteome and phosphoproteome profiling reveals impaired dynamics of testis junction.

  • Elevated levels of cytokines may lead to abnormal BTB structure and spermatogenesis.

Abstract

Mice lacking wild-type p53-induced phosphatase 1 (Wip1) display male reproductive defects including smaller testes, subfertility and spermatogenesis defects at the round- and elongating-spermatid stages. However, the molecular mechanisms underlying these abnormalities remain unclear. Here we examined the proteome and phosphoproteome of testes from Wip1-knockout mice using a quantitative proteomic approach. From a total of 6872 proteins and 4280 phosphorylation sites identified, 58 proteins and 159 phosphorylation sites were found to be differentially regulated compared with wild type mice. Pathway enrichment analyses revealed that these regulated proteins and phosphosites were mainly involved in adherens/tight junctions, apoptosis, inflammatory response, spermatogenesis, sperm motility, and cytoskeletal assembly and depolymerization. Wip1-knockout mice showed decreased expression of junction-associated proteins (occludin, ZO-1, and N-cadherin) and impaired integrity of the blood-testis barrier. In addition, Wip1 deficiency was associated with elevated levels of cytokines and germ cell apoptosis in the testis. These results suggest that proinflammatory cytokines may impair the blood-testis barrier dynamics by decreasing the expression of junction-associated proteins, which could lead to subfertility and spermatogenesis defects. Collectively, these findings help to explain the low reproductive function caused by Wip1 deletion and provide novel insights into our understanding of causes of male infertility.

  • Phosphoproteome
  • iTRAQ
  • Molecular Biology
  • Knockouts
  • Quantification

Footnotes

  • Author contributions: Y.W., Q.G., Y.M., and K.L. designed research; Y.W., Q.G., P.N., K.X., Y.Q., Y.H., and X.Z. performed research; Y.W., S.L., M.Y., Z.L., and B.W. analyzed data; Y.W. and Q.G. wrote the paper.

  • ↵* This research was supported by the National Natural Science Foundation of China (31330074, 31572378), the Major National Scientific Research Projects (2015CB943101), the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (ASTIP-IAS05), and the Special Fund of Chinese Central Government for Basic Scientific Research Operations in Commonweal Research Institutes (2016ywf-yb-4).

  • ↵Embedded Image This article contains supplemental material.

  • Received November 23, 2017.
  • Revision received October 22, 2018.
  • © 2019 Wei et al.

Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc.

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Integrative Proteomic and Phosphoproteomic Profiling of Testis from Wip1 Phosphatase-Knockout Mice: Insights into Mechanisms of Reduced Fertility*
Yinghui Wei, Qian Gao, Pengxia Niu, Kui Xu, Yiqing Qiu, Yanqing Hu, Shasha Liu, Xue Zhang, Miaoying Yu, Zhiguo Liu, Bingyuan Wang, Yulian Mu, Kui Li
Molecular & Cellular Proteomics February 1, 2019, First published on October 25, 2018, 18 (2) 216-230; DOI: 10.1074/mcp.RA117.000479

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Integrative Proteomic and Phosphoproteomic Profiling of Testis from Wip1 Phosphatase-Knockout Mice: Insights into Mechanisms of Reduced Fertility*
Yinghui Wei, Qian Gao, Pengxia Niu, Kui Xu, Yiqing Qiu, Yanqing Hu, Shasha Liu, Xue Zhang, Miaoying Yu, Zhiguo Liu, Bingyuan Wang, Yulian Mu, Kui Li
Molecular & Cellular Proteomics February 1, 2019, First published on October 25, 2018, 18 (2) 216-230; DOI: 10.1074/mcp.RA117.000479
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Molecular & Cellular Proteomics: 18 (2)
Molecular & Cellular Proteomics
Vol. 18, Issue 2
1 Feb 2019
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