A distinct class of plant and animal viral proteins that disrupt mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1

Huaibing Jin; Zhiqiang Du; Yanjing Zhang; Judit Antal; Zongliang Xia; Yan Wang; Yang Gao; Xiaoge Zhao; Xinyun Han; Yanjun Cheng; Qianhua Shen; Kunpu Zhang; Robert E. Elder; Zsigmond Benko; Csaba Fenyvuesvolgyi; Ge Li; Dionne Rebello; Jing Li; Shilai Bao; Richard Y. Zhao; Daowen Wang

doi:10.1126/sciadv.aba3418

A distinct class of plant and animal viral proteins that disrupt mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1

Huaibing Jin, Zhiqiang Du, Yanjing Zhang, Judit Antal, Zongliang Xia, Yan Wang, Yang Gao, Xiaoge Zhao, Xinyun Han, Yanjun Cheng, Qianhua Shen, Kunpu Zhang, Robert E. Elder, Zsigmond Benko, Csaba Fenyvuesvolgyi, Ge Li, Dionne Rebello, Jing Li, Shilai Bao, Richard Y. Zhao^*Daowen Wang

^*Corresponding author for this work

Biochemistry and Molecular Genetics

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

12 Scopus citations

Abstract

Many animal viral proteins, e.g., Vpr of HIV-1, disrupt host mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1. However, it is unknown whether plant viruses may use this mechanism in their pathogenesis. Here, we report that the 17K protein, encoded by barley yellow dwarf viruses and related poleroviruses, delays G₂/M transition and disrupts mitosis in both host (barley) and nonhost (fission yeast, Arabidopsis thaliana, and tobacco) cells through interrupting the function of Wee1-Cdc25-CDKA/Cdc2 via direct protein-protein interactions and alteration of CDKA/Cdc2 phosphorylation. When ectopically expressed, 17K disrupts the mitosis of cultured human cells, and HIV-1 Vpr inhibits plant cell growth. Furthermore, 17K and Vpr share similar secondary structural feature and common amino acid residues required for interacting with plant CDKA. Thus, our work reveals a distinct class of mitosis regulators that are conserved between plant and animal viruses and play active roles in viral pathogenesis.

Original language	English (US)
Article number	eaba3418
Journal	Science Advances
Volume	6
Issue number	20
DOIs	https://doi.org/10.1126/sciadv.aba3418
State	Published - May 2020

Funding

This work was supported by the Ministry of Science and Technology of China (2017YFD0101000 and 2017YFD0100600 to D.W.) and an intramural start-up fund from Chicago Children’s Memorial Institute of Education and Research, Northwestern University Feinberg School of Medicine and the University of Maryland Medical Center (to R.Y.Z.).

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This output contributes to the following UN Sustainable Development Goals (SDGs)

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Jin, H., Du, Z., Zhang, Y., Antal, J., Xia, Z., Wang, Y., Gao, Y., Zhao, X., Han, X., Cheng, Y., Shen, Q., Zhang, K., Elder, R. E., Benko, Z., Fenyvuesvolgyi, C., Li, G., Rebello, D., Li, J., Bao, S., ... Wang, D. (2020). A distinct class of plant and animal viral proteins that disrupt mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1. Science Advances, 6(20), Article eaba3418. https://doi.org/10.1126/sciadv.aba3418

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title = "A distinct class of plant and animal viral proteins that disrupt mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1",

abstract = "Many animal viral proteins, e.g., Vpr of HIV-1, disrupt host mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1. However, it is unknown whether plant viruses may use this mechanism in their pathogenesis. Here, we report that the 17K protein, encoded by barley yellow dwarf viruses and related poleroviruses, delays G2/M transition and disrupts mitosis in both host (barley) and nonhost (fission yeast, Arabidopsis thaliana, and tobacco) cells through interrupting the function of Wee1-Cdc25-CDKA/Cdc2 via direct protein-protein interactions and alteration of CDKA/Cdc2 phosphorylation. When ectopically expressed, 17K disrupts the mitosis of cultured human cells, and HIV-1 Vpr inhibits plant cell growth. Furthermore, 17K and Vpr share similar secondary structural feature and common amino acid residues required for interacting with plant CDKA. Thus, our work reveals a distinct class of mitosis regulators that are conserved between plant and animal viruses and play active roles in viral pathogenesis.",

author = "Huaibing Jin and Zhiqiang Du and Yanjing Zhang and Judit Antal and Zongliang Xia and Yan Wang and Yang Gao and Xiaoge Zhao and Xinyun Han and Yanjun Cheng and Qianhua Shen and Kunpu Zhang and Elder, {Robert E.} and Zsigmond Benko and Csaba Fenyvuesvolgyi and Ge Li and Dionne Rebello and Jing Li and Shilai Bao and Zhao, {Richard Y.} and Daowen Wang",

note = "Publisher Copyright: Copyright {\textcopyright} 2020 The Authors.",

year = "2020",

month = may,

doi = "10.1126/sciadv.aba3418",

language = "English (US)",

volume = "6",

journal = "Science Advances",

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Jin, H, Du, Z, Zhang, Y, Antal, J, Xia, Z, Wang, Y, Gao, Y, Zhao, X, Han, X, Cheng, Y, Shen, Q, Zhang, K, Elder, RE, Benko, Z, Fenyvuesvolgyi, C, Li, G, Rebello, D, Li, J, Bao, S, Zhao, RY & Wang, D 2020, 'A distinct class of plant and animal viral proteins that disrupt mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1', Science Advances, vol. 6, no. 20, eaba3418. https://doi.org/10.1126/sciadv.aba3418

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T1 - A distinct class of plant and animal viral proteins that disrupt mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1

AU - Jin, Huaibing

AU - Du, Zhiqiang

AU - Zhang, Yanjing

AU - Antal, Judit

AU - Xia, Zongliang

AU - Wang, Yan

AU - Gao, Yang

AU - Zhao, Xiaoge

AU - Han, Xinyun

AU - Cheng, Yanjun

AU - Shen, Qianhua

AU - Zhang, Kunpu

AU - Elder, Robert E.

AU - Benko, Zsigmond

AU - Fenyvuesvolgyi, Csaba

AU - Li, Ge

AU - Rebello, Dionne

AU - Li, Jing

AU - Bao, Shilai

AU - Zhao, Richard Y.

AU - Wang, Daowen

PY - 2020/5

Y1 - 2020/5

N2 - Many animal viral proteins, e.g., Vpr of HIV-1, disrupt host mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1. However, it is unknown whether plant viruses may use this mechanism in their pathogenesis. Here, we report that the 17K protein, encoded by barley yellow dwarf viruses and related poleroviruses, delays G2/M transition and disrupts mitosis in both host (barley) and nonhost (fission yeast, Arabidopsis thaliana, and tobacco) cells through interrupting the function of Wee1-Cdc25-CDKA/Cdc2 via direct protein-protein interactions and alteration of CDKA/Cdc2 phosphorylation. When ectopically expressed, 17K disrupts the mitosis of cultured human cells, and HIV-1 Vpr inhibits plant cell growth. Furthermore, 17K and Vpr share similar secondary structural feature and common amino acid residues required for interacting with plant CDKA. Thus, our work reveals a distinct class of mitosis regulators that are conserved between plant and animal viruses and play active roles in viral pathogenesis.

AB - Many animal viral proteins, e.g., Vpr of HIV-1, disrupt host mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1. However, it is unknown whether plant viruses may use this mechanism in their pathogenesis. Here, we report that the 17K protein, encoded by barley yellow dwarf viruses and related poleroviruses, delays G2/M transition and disrupts mitosis in both host (barley) and nonhost (fission yeast, Arabidopsis thaliana, and tobacco) cells through interrupting the function of Wee1-Cdc25-CDKA/Cdc2 via direct protein-protein interactions and alteration of CDKA/Cdc2 phosphorylation. When ectopically expressed, 17K disrupts the mitosis of cultured human cells, and HIV-1 Vpr inhibits plant cell growth. Furthermore, 17K and Vpr share similar secondary structural feature and common amino acid residues required for interacting with plant CDKA. Thus, our work reveals a distinct class of mitosis regulators that are conserved between plant and animal viruses and play active roles in viral pathogenesis.

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A distinct class of plant and animal viral proteins that disrupt mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1

Abstract

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UN SDGs

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