Multiple roles for PARP1 in ALC1-dependent nucleosome remodeling

Soon Keat Ooi; Shigeo Sato; Chieri Tomomori-Sato; Ying Zhang; Zhihui Wen; Charles A.S. Banks; Michael P. Washburn; Jay R. Unruh; Laurence Florens; Ronald C. Conaway; Joan W. Conaway

doi:10.1073/pnas.2107277118

Multiple roles for PARP1 in ALC1-dependent nucleosome remodeling

Soon Keat Ooi, Shigeo Sato, Chieri Tomomori-Sato, Ying Zhang, Zhihui Wen, Charles A.S. Banks, Michael P. Washburn, Jay R. Unruh, Laurence Florens, Ronald C. Conaway, Joan W. Conaway

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

5 Scopus citations

Abstract

The SNF2 family ATPase Amplified in Liver Cancer 1 (ALC1) is the only chromatin remodeling enzyme with a poly(ADP-ribose) (PAR) binding macrodomain. ALC1 functions together with poly(ADPribose) polymerase PARP1 to remodel nucleosomes. Activation of ALC1 cryptic ATPase activity and the subsequent nucleosome remodeling requires binding of its macrodomain to PAR chains synthesized by PARP1 and NAD+. A key question is whether PARP1 has a role(s) in ALC1-dependent nucleosome remodeling beyond simply synthesizing the PAR chains needed to activate the ALC1 ATPase. Here, we identify PARP1 separation-of-function mutants that activate ALC1 ATPase but do not support nucleosome remodeling by ALC1. Investigation of these mutants has revealed multiple functions for PARP1 in ALC1-dependent nucleosome remodeling and provides insights into its multifaceted role in chromatin remodeling.

Original language	English (US)
Article number	e2107277118
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	118
Issue number	36
DOIs	https://doi.org/10.1073/pnas.2107277118
State	Published - Sep 7 2021
Externally published	Yes

Keywords

CHD1L
Nucleosome binding
Nucleosome remodeling
Poly(ADP-ribose) synthesis
SNF2 family ATPase

ASJC Scopus subject areas

General

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10.1073/pnas.2107277118

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Ooi, S. K., Sato, S., Tomomori-Sato, C., Zhang, Y., Wen, Z., Banks, C. A. S., Washburn, M. P., Unruh, J. R., Florens, L., Conaway, R. C., & Conaway, J. W. (2021). Multiple roles for PARP1 in ALC1-dependent nucleosome remodeling. Proceedings of the National Academy of Sciences of the United States of America, 118(36), Article e2107277118. https://doi.org/10.1073/pnas.2107277118

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title = "Multiple roles for PARP1 in ALC1-dependent nucleosome remodeling",

abstract = "The SNF2 family ATPase Amplified in Liver Cancer 1 (ALC1) is the only chromatin remodeling enzyme with a poly(ADP-ribose) (PAR) binding macrodomain. ALC1 functions together with poly(ADPribose) polymerase PARP1 to remodel nucleosomes. Activation of ALC1 cryptic ATPase activity and the subsequent nucleosome remodeling requires binding of its macrodomain to PAR chains synthesized by PARP1 and NAD+. A key question is whether PARP1 has a role(s) in ALC1-dependent nucleosome remodeling beyond simply synthesizing the PAR chains needed to activate the ALC1 ATPase. Here, we identify PARP1 separation-of-function mutants that activate ALC1 ATPase but do not support nucleosome remodeling by ALC1. Investigation of these mutants has revealed multiple functions for PARP1 in ALC1-dependent nucleosome remodeling and provides insights into its multifaceted role in chromatin remodeling.",

keywords = "CHD1L, Nucleosome binding, Nucleosome remodeling, Poly(ADP-ribose) synthesis, SNF2 family ATPase",

author = "Ooi, {Soon Keat} and Shigeo Sato and Chieri Tomomori-Sato and Ying Zhang and Zhihui Wen and Banks, {Charles A.S.} and Washburn, {Michael P.} and Unruh, {Jay R.} and Laurence Florens and Conaway, {Ronald C.} and Conaway, {Joan W.}",

year = "2021",

month = sep,

day = "7",

doi = "10.1073/pnas.2107277118",

language = "English (US)",

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journal = "Proceedings of the National Academy of Sciences of the United States of America",

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T1 - Multiple roles for PARP1 in ALC1-dependent nucleosome remodeling

AU - Ooi, Soon Keat

AU - Sato, Shigeo

AU - Tomomori-Sato, Chieri

AU - Zhang, Ying

AU - Wen, Zhihui

AU - Banks, Charles A.S.

AU - Washburn, Michael P.

AU - Unruh, Jay R.

AU - Florens, Laurence

AU - Conaway, Ronald C.

AU - Conaway, Joan W.

PY - 2021/9/7

Y1 - 2021/9/7

N2 - The SNF2 family ATPase Amplified in Liver Cancer 1 (ALC1) is the only chromatin remodeling enzyme with a poly(ADP-ribose) (PAR) binding macrodomain. ALC1 functions together with poly(ADPribose) polymerase PARP1 to remodel nucleosomes. Activation of ALC1 cryptic ATPase activity and the subsequent nucleosome remodeling requires binding of its macrodomain to PAR chains synthesized by PARP1 and NAD+. A key question is whether PARP1 has a role(s) in ALC1-dependent nucleosome remodeling beyond simply synthesizing the PAR chains needed to activate the ALC1 ATPase. Here, we identify PARP1 separation-of-function mutants that activate ALC1 ATPase but do not support nucleosome remodeling by ALC1. Investigation of these mutants has revealed multiple functions for PARP1 in ALC1-dependent nucleosome remodeling and provides insights into its multifaceted role in chromatin remodeling.

AB - The SNF2 family ATPase Amplified in Liver Cancer 1 (ALC1) is the only chromatin remodeling enzyme with a poly(ADP-ribose) (PAR) binding macrodomain. ALC1 functions together with poly(ADPribose) polymerase PARP1 to remodel nucleosomes. Activation of ALC1 cryptic ATPase activity and the subsequent nucleosome remodeling requires binding of its macrodomain to PAR chains synthesized by PARP1 and NAD+. A key question is whether PARP1 has a role(s) in ALC1-dependent nucleosome remodeling beyond simply synthesizing the PAR chains needed to activate the ALC1 ATPase. Here, we identify PARP1 separation-of-function mutants that activate ALC1 ATPase but do not support nucleosome remodeling by ALC1. Investigation of these mutants has revealed multiple functions for PARP1 in ALC1-dependent nucleosome remodeling and provides insights into its multifaceted role in chromatin remodeling.

KW - CHD1L

KW - Nucleosome binding

KW - Nucleosome remodeling

KW - Poly(ADP-ribose) synthesis

KW - SNF2 family ATPase

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DO - 10.1073/pnas.2107277118

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SN - 0027-8424

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JO - Proceedings of the National Academy of Sciences of the United States of America

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ER -

Multiple roles for PARP1 in ALC1-dependent nucleosome remodeling

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