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Structural rearrangements allow nucleic acid discrimination by type I-D Cascade

Author

Listed:
  • Evan A. Schwartz

    (University of Texas at Austin
    University of Texas at Austin)

  • Tess M. McBride

    (University of Otago)

  • Jack P. K. Bravo

    (University of Texas at Austin)

  • Daniel Wrapp

    (University of Texas at Austin
    University of Texas at Austin)

  • Peter C. Fineran

    (University of Otago
    University of Otago
    University of Otago)

  • Robert D. Fagerlund

    (University of Otago
    University of Otago
    University of Otago)

  • David W. Taylor

    (University of Texas at Austin
    University of Texas at Austin
    University of Texas at Austin
    LIVESTRONG Cancer Institutes, Dell Medical School)

Abstract

CRISPR-Cas systems are adaptive immune systems that protect prokaryotes from foreign nucleic acids, such as bacteriophages. Two of the most prevalent CRISPR-Cas systems include type I and type III. Interestingly, the type I-D interference proteins contain characteristic features of both type I and type III systems. Here, we present the structures of type I-D Cascade bound to both a double-stranded (ds)DNA and a single-stranded (ss)RNA target at 2.9 and 3.1 Å, respectively. We show that type I-D Cascade is capable of specifically binding ssRNA and reveal how PAM recognition of dsDNA targets initiates long-range structural rearrangements that likely primes Cas10d for Cas3′ binding and subsequent non-target strand DNA cleavage. These structures allow us to model how binding of the anti-CRISPR protein AcrID1 likely blocks target dsDNA binding via competitive inhibition of the DNA substrate engagement with the Cas10d active site. This work elucidates the unique mechanisms used by type I-D Cascade for discrimination of single-stranded and double stranded targets. Thus, our data supports a model for the hybrid nature of this complex with features of type III and type I systems.

Suggested Citation

  • Evan A. Schwartz & Tess M. McBride & Jack P. K. Bravo & Daniel Wrapp & Peter C. Fineran & Robert D. Fagerlund & David W. Taylor, 2022. "Structural rearrangements allow nucleic acid discrimination by type I-D Cascade," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30402-8
    DOI: 10.1038/s41467-022-30402-8
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    References listed on IDEAS

    as
    1. M. Cemre Manav & Lan B. Van & Jinzhong Lin & Anders Fuglsang & Xu Peng & Ditlev E. Brodersen, 2020. "Structural basis for inhibition of an archaeal CRISPR–Cas type I-D large subunit by an anti-CRISPR protein," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    2. Ole Niewoehner & Carmela Garcia-Doval & Jakob T. Rostøl & Christian Berk & Frank Schwede & Laurent Bigler & Jonathan Hall & Luciano A. Marraffini & Martin Jinek, 2017. "Type III CRISPR–Cas systems produce cyclic oligoadenylate second messengers," Nature, Nature, vol. 548(7669), pages 543-548, August.
    3. Mu-Sen Liu & Shanzhong Gong & Helen-Hong Yu & Kyungseok Jung & Kenneth A. Johnson & David W. Taylor, 2020. "Engineered CRISPR/Cas9 enzymes improve discrimination by slowing DNA cleavage to allow release of off-target DNA," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    4. Jack P. K. Bravo & Mu-Sen Liu & Grace N. Hibshman & Tyler L. Dangerfield & Kyungseok Jung & Ryan S. McCool & Kenneth A. Johnson & David W. Taylor, 2022. "Structural basis for mismatch surveillance by CRISPR–Cas9," Nature, Nature, vol. 603(7900), pages 343-347, March.
    5. Hannah G. Hampton & Bridget N. J. Watson & Peter C. Fineran, 2020. "The arms race between bacteria and their phage foes," Nature, Nature, vol. 577(7790), pages 327-336, January.
    6. Robert P. Hayes & Yibei Xiao & Fran Ding & Paul B. G. van Erp & Kanagalaghatta Rajashankar & Scott Bailey & Blake Wiedenheft & Ailong Ke, 2016. "Structural basis for promiscuous PAM recognition in type I–E Cascade from E. coli," Nature, Nature, vol. 530(7591), pages 499-503, February.
    7. Gregory W. Goldberg & Wenyan Jiang & David Bikard & Luciano A. Marraffini, 2014. "Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting," Nature, Nature, vol. 514(7524), pages 633-637, October.
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    Cited by:

    1. Meiling Lu & Chenlin Yu & Yuwen Zhang & Wenjun Ju & Zhi Ye & Chenyang Hua & Jinze Mao & Chunyi Hu & Zhenhuang Yang & Yibei Xiao, 2024. "Structure and genome editing of type I-B CRISPR-Cas," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Evan A. Schwartz & Jack P. K. Bravo & Mohd Ahsan & Luis A. Macias & Caitlyn L. McCafferty & Tyler L. Dangerfield & Jada N. Walker & Jennifer S. Brodbelt & Giulia Palermo & Peter C. Fineran & Robert D., 2024. "RNA targeting and cleavage by the type III-Dv CRISPR effector complex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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