Structural basis of G-quadruplex unfolding by the DEAH/RHA helicase DHX36

Chen, Michael C.; Tippana, Ramreddy; Demeshkina, Natalia A.; Murat, Pierre; Balasubramanian, Shankar; Myong, Sua; Ferré-D’Amaré, Adrian R.

doi:10.1038/s41586-018-0209-9

Structural basis of G-quadruplex unfolding by the DEAH/RHA helicase DHX36

Journal Article · Wed Jun 13 00:00:00 EDT 2018 · Nature (London)

DOI:https://doi.org/10.1038/s41586-018-0209-9· OSTI ID:1544820

Chen, Michael C. ^[1]; Tippana, Ramreddy ^[2]; Demeshkina, Natalia A. ^[3]; Murat, Pierre ^[4]; Balasubramanian, Shankar ^[4]; Myong, Sua ^[2]; Ferré-D’Amaré, Adrian R. ^[3]

National Institutes of Health, Bethesda, MD (United States). National Heart, Lung and Blood Inst.; Univ. of Cambridge (United Kingdom)
Johns Hopkins Univ., Baltimore, MD (United States)
National Institutes of Health, Bethesda, MD (United States). National Heart, Lung and Blood Inst.
Univ. of Cambridge (United Kingdom)

Guanine-rich nucleic acid sequences challenge the replication, transcription, and translation machinery by spontaneously folding into G-quadruplexes, the unfolding of which requires forces greater than most polymerases can exert. Eukaryotic cells contain numerous helicases that can unfold G-quadruplexes. The molecular basis of the recognition and unfolding of G-quadruplexes by helicases remains poorly understood. DHX36 (also known as RHAU and G4R1), a member of the DEAH/RHA family of helicases, binds both DNA and RNA G-quadruplexes with extremely high affinity, is consistently found bound to G-quadruplexes in cells, and is a major source of G-quadruplex unfolding activity in HeLa cell lysates. DHX36 is a multi-functional helicase that has been implicated in G-quadruplex-mediated transcriptional and post-transcriptional regulation, and is essential for heart development, haematopoiesis, and embryogenesis in mice. Here we report the co-crystal structure of bovine DHX36 bound to a DNA with a G-quadruplex and a 3' single-stranded DNA segment. Furthermore, we show that the N-terminal DHX36-specific motif folds into a DNA-binding-induced α-helix that, together with the OB-fold-like subdomain, selectively binds parallel G-quadruplexes. Comparison with unliganded and ATP-analogue-bound DHX36 structures, together with single-molecule fluorescence resonance energy transfer (FRET) analysis, suggests that G-quadruplex binding alone induces rearrangements of the helicase core; by pulling on the single-stranded DNA tail, these rearrangements drive G-quadruplex unfolding one residue at a time.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: American Chemical Society; Cancer Research UK; European Research Council (ERC); NIH-Oxford-Cambridge Scholars Program; National Heart, Lung and Blood Institute (NHLBI); National Institutes of Health (NIH); National Science Foundation (NSF) Physics Frontiers Center Program; USDOE; Wellcome Trust

OSTI ID:: 1544820

Journal Information:: Nature (London), Journal Name: Nature (London) Journal Issue: 7710 Vol. 558; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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