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Review

Structural insights into the inactivation of the type I-F CRISPR-Cas system by anti-CRISPR proteins

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Pages 562-573 | Received 30 Apr 2021, Accepted 21 Sep 2021, Published online: 04 Oct 2021

References

  • Bernheim A, Sorek R. The pan-immune system of bacteria: antiviral defence as a community resource. Nat Rev Microbiol. 2020;18:113–119.
  • Makarova KS, Wolf YI, Iranzo J, et al. Evolutionary classification of CRISPR-Cas systems: a burst of class 2 and derived variants. Nat Rev Microbiol. 2020;18:67–83.
  • Makarova KS, Wolf YI, Alkhnbashi OS, et al. An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol. 2015;13:722–736.
  • Brouns SJ, Jore MM, Lundgren M, et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science. 2008;321:960–964.
  • Bondy-Denomy J, Pawluk A, Maxwell KL, et al. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature. 2013;493:429–432.
  • Huang L, Yang B, Yi H, et al. AcrDB: a database of anti-CRISPR operons in prokaryotes and viruses. Nucleic Acids Res. 2021;49:D622–D9.
  • Bondy-Denomy J, Davidson AR, Doudna JA, et al. A unified resource for tracking Anti-CRISPR names. CRISPR J. 2018;1:304–305.
  • Borges AL, Davidson AR, Bondy-Denomy J. The discovery, mechanisms, and evolutionary impact of Anti-CRISPRs. Annu Rev Virol. 2017;4:37–59.
  • Pawluk A, Davidson AR, Maxwell KL. Anti-CRISPR: discovery, mechanism and function. Nature Rev Microbiol. 2018;16:12–17.
  • Stanley SY, Maxwell KL. Phage-encoded Anti-CRISPR defenses. Annu Rev Genet. 2018;52:445–464.
  • Zhu Y, Zhang F, Huang Z. Structural insights into the inactivation of CRISPR-Cas systems by diverse anti-CRISPR proteins. BMC Biol. 2018;16:32.
  • Davidson AR, Lu WT, Stanley SY, et al. Anti-CRISPRs: protein Inhibitors of CRISPR-Cas systems. Annu Rev Biochem. 2020;89:309–332.
  • Li Y, Bondy-Denomy J. Anti-CRISPRs go viral: the infection biology of CRISPR-Cas inhibitors. Cell Host Microbe. 2020;29:704–714.
  • Wiegand T, Karambelkar S, Bondy-Denomy J, et al. Structures and strategies of anti-CRISPR-mediated immune suppression. Annu Rev Microbiol. 2020;74:21–37.
  • Cong L, Ran FA, Cox D, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339:819–823.
  • Zetsche B, Heidenreich M, Mohanraju P, et al. Multiplex gene editing by CRISPR-Cpf1 using a single crRNA array. Nat Biotechnol. 2017;35:31–34.
  • Dolan AE, Hou Z, Xiao Y, et al. Introducing a spectrum of long-range genomic deletions in human embryonic stem cells using type I CRISPR-Cas. Mol Cell. 2019;74:936–50.e5.
  • Morisaka H, Yoshimi K, Okuzaki Y, et al. CRISPR-Cas3 induces broad and unidirectional genome editing in human cells. Nat Commun. 2019;10:5302.
  • Csörgő B, León LM, Chau-Ly IJ, et al. A compact Cascade–Cas3 system for targeted genome engineering. Nat Methods. 2020;17:1183–1190.
  • Xu Z, Li M, Li Y, et al. Native CRISPR-Cas-mediated genome editing enables dissecting and sensitizing clinical multidrug-resistant P. aeruginosa. Cell Rep. 2019;29:1707–17 e3.
  • Zheng Y, Han J, Wang B, et al. Characterization and repurposing of the endogenous Type I-F CRISPR-Cas system of Zymomonas mobilis for genome engineering. Nucleic Acids Res. 2019;47:11461–11475.
  • Chen Y, Liu J, Zhi S, et al. Repurposing type I-F CRISPR-Cas system as a transcriptional activation tool in human cells. Nat Commun. 2020;11:3136.
  • Vo PLH, Ronda C, Klompe SE, et al. CRISPR RNA-guided integrases for high-efficiency, multiplexed bacterial genome engineering. Nat Biotechnol. 2020;39:480–489.
  • Xu Z, Li Y, Cao H, et al. A transferrable and integrative type I-F Cascade for heterologous genome editing and transcription modulation. Nucleic Acids Res. 2021;gkab521. DOI:10.1093/nar/gkab521.
  • Szczelkun MD, Tikhomirova MS, Sinkunas T, et al. Direct observation of R-loop formation by single RNA-guided Cas9 and Cascade effector complexes. Proc Natl Acad Sci U S A. 2014;111:9798–9803.
  • Rutkauskas M, Sinkunas T, Songailiene I, et al. Directional R-Loop formation by the CRISPR-Cas surveillance complex cascade provides efficient off-target site rejection. Cell Rep. 2015;10:1534–1543.
  • Wilkinson ME, Nakatani Y, Staals RH, et al. Structural plasticity and in vivo activity of Cas1 from the type I-F CRISPR-Cas system. Biochem J. 2016;473:1063–1072.
  • Wang X, Yao D, Xu JG, et al. Structural basis of Cas3 inhibition by the bacteriophage protein AcrF3. Nat Struct Mol Biol. 2016;23:868–870.
  • Wang J, Ma J, Cheng Z, et al. A CRISPR evolutionary arms race: structural insights into viral anti-CRISPR/Cas responses. Cell Res. 2016;26:1165–1168.
  • Rollins MF, Chowdhury S, Carter J, et al. Cas1 and the Csy complex are opposing regulators of Cas2/3 nuclease activity. Proc Natl Acad Sci U S A. 2017;114:E5113–E21.
  • Chowdhury S, Carter J, Rollins MF, et al. Structure reveals mechanisms of viral suppressors that intercept a CRISPR RNA-guided surveillance complex. Cell. 2017;169:47–57.e11.
  • Guo TW, Bartesaghi A, Yang H, et al. Cryo-EM structures reveal mechanism and inhibition of DNA targeting by a CRISPR-Cas surveillance complex. Cell. 2017;171:414–26 e12.
  • Pausch P, Muller-Esparza H, Gleditzsch D, et al. Structural variation of Type I-F CRISPR RNA guided DNA surveillance. Mol Cell. 2017;67:622–32 e4.
  • Wiedenheft B, Zhou K, Jinek M, et al. Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure. 2009;17:904–912.
  • Rollins MF, Chowdhury S, Carter J, et al. Structure reveals a mechanism of CRISPR-RNA-guided nuclease recruitment and Anti-CRISPR viral mimicry. Mol Cell. 2019;74:132–42.e5.
  • Pawluk A, Staals RH, Taylor C, et al. Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat Microbiol. 2016;1:16085.
  • Marino NA-O, Zhang JA-O, Borges AA-O, et al. Discovery of widespread type I and type V CRISPR-Cas inhibitors. Science. 2018;362:240–242.
  • Pinilla-Redondo R, Shehreen S, Marino ND, et al. Discovery of multiple anti-CRISPRs highlights anti-defense gene clustering in mobile genetic elements. Nat Commun. 2020;11:5652.
  • Bondy-Denomy J, Garcia B, Strum S, et al. Multiple mechanisms for CRISPR-Cas inhibition by anti-CRISPR proteins. Nature. 2015;526:136–139.
  • Maxwell KL, Garcia B, Bondy-Denomy J, et al. The solution structure of an anti-CRISPR protein. Nat Commun. 2016;7:13134.
  • Peng R, Xu Y, Zhu T, et al. Alternate binding modes of anti-CRISPR viral suppressors AcrF1/2 to Csy surveillance complex revealed by cryo-EM structures. Cell Res. 2017;27:853–864.
  • Kim GE, Lee SY, Park HH. A high-resolution (1.2 A) crystal structure of the anti-CRISPR protein AcrIF9. FEBS Open Bio. 2020;10:2532–2540.
  • Hirschi M, Lu WT, Santiago-Frangos A, et al. AcrIF9 tethers non-sequence specific dsDNA to the CRISPR RNA-guided surveillance complex. Nat Commun. 2020;11:2730.
  • Zhang K, Wang S, Li S, et al. Inhibition mechanisms of AcrF9, AcrF8, and AcrF6 against type I-F CRISPR-Cas complex revealed by cryo-EM. Proc Natl Acad Sci U S A. 2020;117:7176–7182.
  • Lu WT, Trost CN, Muller-Esparza H, et al. Anti-CRISPR AcrIF9 functions by inducing the CRISPR-Cas complex to bind DNA non-specifically. Nucleic Acids Res. 2021;49:3381–3393.
  • Gabel C, Li Z, Zhang H, et al. Structural basis for inhibition of the type I-F CRISPR-Cas surveillance complex by AcrIF4, AcrIF7 and AcrIF14. Nucleic Acids Res. 2021;49:584–594.
  • Hong S, Ka D, Yoon SJ, et al. CRISPR RNA and anti-CRISPR protein binding to the Xanthomonas albilineans Csy1-Csy2 heterodimer in the type I-F CRISPR-Cas system. J Biol Chem. 2018;293:2744–2754.
  • Kim I, Koo J, An SY, et al. Structural and mechanistic insights into the CRISPR inhibition of AcrIF7. Nucleic Acids Res. 2020;48:9959–9968.
  • Niu Y, Yang L, Gao T, et al. A type I-F Anti-CRISPR protein inhibits the CRISPR-Cas surveillance complex by ADP-Ribosylation. Mol Cell. 2020;80:512–24 e5.
  • Mejdani M, Pawluk A, Maxwell KL, et al. Anti-CRISPR AcrIE2 binds the Type I-E CRISPR-Cas complex but does not block DNA binding. J Mol Biol. 2021;433:166759.
  • Dong L, Guan X, Li N, et al. An anti-CRISPR protein disables type V Cas12a by acetylation. Nat Struct Mol Biol. 2019;26:308–314.
  • Jumper J, Evans R, Pritzel A, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596(7873):583–589.
  • Tunyasuvunakool K, Adler J, Wu Z, et al. Highly accurate protein structure prediction for the human proteome. Nature. 2021;596(7873):590–596.
  • Peters JE, Makarova KS, Shmakov S, et al. Recruitment of CRISPR-Cas systems by Tn7-like transposons. Proc Natl Acad Sci U S A. 2017;114:E7358–E66.
  • Klompe SE, Vo PLH, Halpin-Healy TS, et al. Transposon-encoded CRISPR-Cas systems direct RNA-guided DNA integration. Nature. 2019;571:219–225.
  • Shin J, Jiang F, Liu -J-J, et al. Disabling Cas9 by an anti-CRISPR DNA mimic. Sci Adv. 2017;3:e1701620.
  • Li C, Psatha N, Gil S, et al. HDAd5/35(++) adenovirus vector expressing Anti-CRISPR peptides decreases CRISPR/Cas9 toxicity in human hematopoietic stem cells. Mol Ther Methods Clin Dev. 2018;9:390–401.
  • Lee JA-O, Mou HA-O, Ibraheim RA-O, et al. Tissue-restricted genome editing in vivo specified by microRNA-repressible anti-CRISPR proteins. RNA. 2019;25:1421–1431.

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