Polycomb group targeting through different binding partners of RING1B C-terminal domain

Renjing Wang; Alexander B. Taylor; Belinda Z. Leal; Linda V. Chadwell; Udayar Ilangovan; Angela K. Robinson; Virgil Schirf; P. John Hart; Eileen M. Lafer; Borries Demeler; Andrew P. Hinck; Donald G. McEwen; Chongwoo A. Kim

doi:10.1016/j.str.2010.04.013

Polycomb group targeting through different binding partners of RING1B C-terminal domain

Renjing Wang
, Alexander B. Taylor
, Belinda Z. Leal
, Linda V. Chadwell
, Udayar Ilangovan
, Angela K. Robinson
, Virgil Schirf
, P. John Hart
, Eileen M. Lafer
, Borries Demeler
, Andrew P. Hinck
, Donald G. McEwen
, Chongwoo A. Kim

Chemistry and Biochemistry

University of Texas Health Science Center at San Antonio

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

83 Scopus citations

Abstract

RING1B, a Polycomb Group (PcG) protein, binds methylated chromatin through its association with another PcG protein called Polycomb (Pc). However, RING1B can associate with nonmethylated chromatin suggesting an alternate mechanism for RING1B interaction with chromatin. Here, we demonstrate that two proteins with little sequence identity between them, the Pc cbox domain and RYBP, bind the same surface on the C-terminal domain of RING1B (C-RING1B). Pc cbox and RYBP each fold into a nearly identical, intermolecular beta sheet with C-RING1B and a loop structure which are completely different in the two proteins. Both the beta sheet and loop are required for stable binding and transcription repression. Further, a mutation engineered to disrupt binding on the Drosophila dRING1 protein prevents chromatin association and PcG function in vivo. These results suggest that PcG targeting to different chromatin locations relies, in part, on binding partners of C-RING1B that are diverse in sequence and structure.

Original language	English
Pages (from-to)	966-975
Number of pages	10
Journal	Structure
Volume	18
Issue number	8
DOIs	https://doi.org/10.1016/j.str.2010.04.013
State	Published - Aug 2010

Funding

We thank Paul F. Fitzpatrick and Susan T. Weintraub for their comments on the manuscript; we also thank Weintraub and her staff at the UTHSCSA Institutional Mass Spectrometry Laboratory for mass spectrometry analysis of the Se-Met proteins and Jay Nix for the data collection at the Advanced Light Source (ALS). This work was supported by the American Heart Association (0830111N), the American Cancer Society (RSG-08-285-01-GMC) and the Department of Defense Breast Cancer Research Program (BC075278) (CAK). Support for the X-ray Crystallography Laboratory, NMR facility, the Center for Macromolecular Interactions (CAUMA and SPR) and the Mass Spectrometry Laboratory was provided by UTHSCSA and NIH-NCI P30 CA54174 (CTRC at UTHSCSA). The development of the UltraScan software is supported by the National Institutes of Health (RR022200 to BD), supercomputer allocations were provided through National Science Foundation (TG-MCB070038 to BD). Structure figures were produced using the UCSF Chimera package from the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco (NIH P41 RR-01081).

Funders	Funder number
TG-MCB070038
RR022200
American Cancer Society	RSG-08-285-01-GMC
P30CA054174
American Heart Association	0830111N
BC075278

Keywords

DNA

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10.1016/j.str.2010.04.013

Cite this

@article{09e4e8b551d24657ae110b6f3c340af5,

title = "Polycomb group targeting through different binding partners of RING1B C-terminal domain",

abstract = "RING1B, a Polycomb Group (PcG) protein, binds methylated chromatin through its association with another PcG protein called Polycomb (Pc). However, RING1B can associate with nonmethylated chromatin suggesting an alternate mechanism for RING1B interaction with chromatin. Here, we demonstrate that two proteins with little sequence identity between them, the Pc cbox domain and RYBP, bind the same surface on the C-terminal domain of RING1B (C-RING1B). Pc cbox and RYBP each fold into a nearly identical, intermolecular beta sheet with C-RING1B and a loop structure which are completely different in the two proteins. Both the beta sheet and loop are required for stable binding and transcription repression. Further, a mutation engineered to disrupt binding on the Drosophila dRING1 protein prevents chromatin association and PcG function in vivo. These results suggest that PcG targeting to different chromatin locations relies, in part, on binding partners of C-RING1B that are diverse in sequence and structure.",

keywords = "DNA",

author = "Renjing Wang and Taylor, \{Alexander B.\} and Leal, \{Belinda Z.\} and Chadwell, \{Linda V.\} and Udayar Ilangovan and Robinson, \{Angela K.\} and Virgil Schirf and Hart, \{P. John\} and Lafer, \{Eileen M.\} and Borries Demeler and Hinck, \{Andrew P.\} and McEwen, \{Donald G.\} and Kim, \{Chongwoo A.\}",

note = "Funding Information: We thank Paul F. Fitzpatrick and Susan T. Weintraub for their comments on the manuscript; we also thank Weintraub and her staff at the UTHSCSA Institutional Mass Spectrometry Laboratory for mass spectrometry analysis of the Se-Met proteins and Jay Nix for the data collection at the Advanced Light Source (ALS). This work was supported by the American Heart Association (0830111N), the American Cancer Society (RSG-08-285-01-GMC) and the Department of Defense Breast Cancer Research Program (BC075278) (CAK). Support for the X-ray Crystallography Laboratory, NMR facility, the Center for Macromolecular Interactions (CAUMA and SPR) and the Mass Spectrometry Laboratory was provided by UTHSCSA and NIH-NCI P30 CA54174 (CTRC at UTHSCSA). The development of the UltraScan software is supported by the National Institutes of Health (RR022200 to BD), supercomputer allocations were provided through National Science Foundation (TG-MCB070038 to BD). Structure figures were produced using the UCSF Chimera package from the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco (NIH P41 RR-01081). ",

year = "2010",

month = aug,

doi = "10.1016/j.str.2010.04.013",

language = "English",

volume = "18",

pages = "966--975",

journal = "Structure",

issn = "0969-2126",

publisher = "Cell Press",

number = "8",

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T1 - Polycomb group targeting through different binding partners of RING1B C-terminal domain

AU - Wang, Renjing

AU - Taylor, Alexander B.

AU - Leal, Belinda Z.

AU - Chadwell, Linda V.

AU - Ilangovan, Udayar

AU - Robinson, Angela K.

AU - Schirf, Virgil

AU - Hart, P. John

AU - Lafer, Eileen M.

AU - Demeler, Borries

AU - Hinck, Andrew P.

AU - McEwen, Donald G.

AU - Kim, Chongwoo A.

N1 - Funding Information: We thank Paul F. Fitzpatrick and Susan T. Weintraub for their comments on the manuscript; we also thank Weintraub and her staff at the UTHSCSA Institutional Mass Spectrometry Laboratory for mass spectrometry analysis of the Se-Met proteins and Jay Nix for the data collection at the Advanced Light Source (ALS). This work was supported by the American Heart Association (0830111N), the American Cancer Society (RSG-08-285-01-GMC) and the Department of Defense Breast Cancer Research Program (BC075278) (CAK). Support for the X-ray Crystallography Laboratory, NMR facility, the Center for Macromolecular Interactions (CAUMA and SPR) and the Mass Spectrometry Laboratory was provided by UTHSCSA and NIH-NCI P30 CA54174 (CTRC at UTHSCSA). The development of the UltraScan software is supported by the National Institutes of Health (RR022200 to BD), supercomputer allocations were provided through National Science Foundation (TG-MCB070038 to BD). Structure figures were produced using the UCSF Chimera package from the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco (NIH P41 RR-01081).

PY - 2010/8

Y1 - 2010/8

N2 - RING1B, a Polycomb Group (PcG) protein, binds methylated chromatin through its association with another PcG protein called Polycomb (Pc). However, RING1B can associate with nonmethylated chromatin suggesting an alternate mechanism for RING1B interaction with chromatin. Here, we demonstrate that two proteins with little sequence identity between them, the Pc cbox domain and RYBP, bind the same surface on the C-terminal domain of RING1B (C-RING1B). Pc cbox and RYBP each fold into a nearly identical, intermolecular beta sheet with C-RING1B and a loop structure which are completely different in the two proteins. Both the beta sheet and loop are required for stable binding and transcription repression. Further, a mutation engineered to disrupt binding on the Drosophila dRING1 protein prevents chromatin association and PcG function in vivo. These results suggest that PcG targeting to different chromatin locations relies, in part, on binding partners of C-RING1B that are diverse in sequence and structure.

AB - RING1B, a Polycomb Group (PcG) protein, binds methylated chromatin through its association with another PcG protein called Polycomb (Pc). However, RING1B can associate with nonmethylated chromatin suggesting an alternate mechanism for RING1B interaction with chromatin. Here, we demonstrate that two proteins with little sequence identity between them, the Pc cbox domain and RYBP, bind the same surface on the C-terminal domain of RING1B (C-RING1B). Pc cbox and RYBP each fold into a nearly identical, intermolecular beta sheet with C-RING1B and a loop structure which are completely different in the two proteins. Both the beta sheet and loop are required for stable binding and transcription repression. Further, a mutation engineered to disrupt binding on the Drosophila dRING1 protein prevents chromatin association and PcG function in vivo. These results suggest that PcG targeting to different chromatin locations relies, in part, on binding partners of C-RING1B that are diverse in sequence and structure.

KW - DNA

UR - https://www.scopus.com/pages/publications/77955479981

U2 - 10.1016/j.str.2010.04.013

DO - 10.1016/j.str.2010.04.013

M3 - Article

C2 - 20696397

AN - SCOPUS:77955479981

SN - 0969-2126

VL - 18

SP - 966

EP - 975

JO - Structure

JF - Structure

IS - 8

ER -

Polycomb group targeting through different binding partners of RING1B C-terminal domain

Abstract

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Keywords

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