B56$δ$ long-disordered arms form a dynamic PP2A regulation interface coupled with global allostery and Jordan’s syndrome mutations

Wu, Cheng-Guo; Balakrishnan, Vijaya K.; Merrill, Ronald A.; Parihar, Pankaj S.; Konovolov, Kirill; Chen, Yu-Chia; Xu, Zhen; Wei, Hui; Sundaresan, Ramya; Cui, Qiang; Wadzinski, Brian E.; Swingle, Mark R.; Musiyenko, Alla; Chung, Wendy K.; Honkanen, Richard E.; Suzuki, Aussie; Huang, Xuhui; Strack, Stefan; Xing, Yongna

doi:10.1073/pnas.2310727120

Title: B56$$δ$$ long-disordered arms form a dynamic PP2A regulation interface coupled with global allostery and Jordan’s syndrome mutations

Journal Article · 27 December 2023 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.2310727120 · OSTI ID:2470213

^[1]; Balakrishnan, Vijaya K. ^[1]; Merrill, Ronald A. ^[2];

^[1]; Konovolov, Kirill ^[1]; Chen, Yu-Chia ^[1];

^[2];

^[3]; Sundaresan, Ramya ^[1];

^[4];

^[5]; Swingle, Mark R. ^[6];

^[6];

^[7];

^[6];

^[1];

^[2]; Xing, Yongna ^[1]

Univ. of Wisconsin, Madison, WI (United States)
Univ. of Iowa, Iowa City, IA (United States)
New York Structural Biology Center, NY (United States). The Simons Electron Microscopy Center
Boston Univ., MA (United States)
Vanderbilt Univ., Nashville, TN (United States)
Univ. of South Alabama, Mobile, AL (United States)
Harvard Medical School, Boston, MA (United States). Boston Children’s Hospital

Intrinsically disordered regions (IDR) and short linear motifs (SLiMs) play pivotal roles in the intricate signaling networks governed by phosphatases and kinases. B56δ (encoded by PPP2R5D) is a regulatory subunit of protein phosphatase 2A (PP2A) with long IDRs that harbor a substrate-mimicking SLiM and multiple phosphorylation sites. De novo missense mutations in PPP2R5D cause intellectual disabilities (ID), macrocephaly, Parkinsonism, and a broad range of neurological symptoms. Our single-particle cryo-EM structures of the PP2A-B56δ holoenzyme reveal that the long, disordered arms at the B56δ termini fold against each other and the holoenzyme core. This architecture suppresses both the phosphatase active site and the substrate-binding protein groove, thereby stabilizing the enzyme in a closed latent form with dual autoinhibition. The resulting interface spans over 190 Å and harbors unfavorable contacts, activation phosphorylation sites, and nearly all residues with ID-associated mutations. Our studies suggest that this dynamic interface is coupled to an allosteric network responsive to phosphorylation and altered globally by mutations. Furthermore, we found that ID mutations increase the holoenzyme activity and perturb the phosphorylation rates, and the severe variants significantly increase the mitotic duration and error rates compared to the normal variant.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Jordan’s Guardian Angels Foundation; National Institutes of Health (NIH); Simons Foundation; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2470213

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 1 Vol. 121; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Jordan’s syndrome
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phosphatase

Title: B56$$δ$$ long-disordered arms form a dynamic PP2A regulation interface coupled with global allostery and Jordan’s syndrome mutations

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