Tousled-like kinase 2 targets ASF1 histone chaperones through client mimicry

Simon, Bertrand; Lou, Hua Jane; Huet-Calderwood, Clotilde; Shi, Guangda; Boggon, Titus J.; Turk, Benjamin E.; Calderwood, David A.

doi:10.1038/s41467-022-28427-0

Title: Tousled-like kinase 2 targets ASF1 histone chaperones through client mimicry

Journal Article · 08 February 2022 · Nature Communications

DOI: https://doi.org/10.1038/s41467-022-28427-0 · OSTI ID:1847125

Simon, Bertrand ^[1]; Lou, Hua Jane ^[1]; Huet-Calderwood, Clotilde ^[1]; Shi, Guangda ^[1];

^[2];

^[1];

^[2]

Yale School of Medicine, New Haven, CT (United States)
Yale School of Medicine, New Haven, CT (United States); Yale Univ., New Haven, CT (United States)

Tousled-like kinases (TLKs) are nuclear serine-threonine kinases essential for genome maintenance and proper cell division in animals and plants. A major function of TLKs is to phosphorylate the histone chaperone proteins ASF1a and ASF1b to facilitate DNA replication-coupled nucleosome assembly, but how TLKs selectively target these critical substrates is unknown. Here, we show that TLK2 selectivity towards ASF1 substrates is achieved in two ways. First, the TLK2 catalytic domain recognizes consensus phosphorylation site motifs in the ASF1 C-terminal tail. Second, a short sequence at the TLK2 N-terminus docks onto the ASF1a globular N-terminal domain in a manner that mimics its histone H3 client. Disrupting either catalytic or non-catalytic interactions through mutagenesis hampers ASF1 phosphorylation by TLK2 and cell growth. Our results suggest that the stringent selectivity of TLKs for ASF1 is enforced by an unusual interaction mode involving mutual recognition of a short sequence motifs by both kinase and substrate.

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

Sponsoring Organization:: NIH; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1847125

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 13; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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59 BASIC BIOLOGICAL SCIENCES
Chaperones
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Nucleosomes
X-ray crystallography

Title: Tousled-like kinase 2 targets ASF1 histone chaperones through client mimicry

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