skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Target preference of Type III-A CRISPR-Cas complexes at the transcription bubble

Abstract

Type III-A CRISPR-Cas systems are prokaryotic RNA-guided adaptive immune systems that use a protein-RNA complex, Csm, for transcription-dependent immunity against foreign DNA. Csm can cleave RNA and single-stranded DNA (ssDNA), but whether it targets one or both nucleic acids during transcription elongation is unknown. Here, we show that binding of a Thermus thermophilus (T. thermophilus) Csm (TthCsm) to a nascent transcript in a transcription elongation complex (TEC) promotes tethering but not direct contact of TthCsm with RNA polymerase (RNAP). Biochemical experiments show that both TthCsm and Staphylococcus epidermidis (S. epidermidis) Csm (SepCsm) cleave RNA transcripts, but not ssDNA, at the transcription bubble. Taken together, these results suggest that Type III systems primarily target transcripts, instead of unwound ssDNA in TECs, for immunity against double-stranded DNA (dsDNA) phages and plasmids. This reveals similarities between Csm and eukaryotic RNA interference, which also uses RNA-guided RNA targeting to silence actively transcribed genes.

Authors:
ORCiD logo [1];  [2];  [1]; ORCiD logo [2]; ORCiD logo [2]
  1. Univ. of California, Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1559231
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Liu, Tina Y., Liu, Jun-Jie, Aditham, Abhishek J., Nogales, Eva, and Doudna, Jennifer A. Target preference of Type III-A CRISPR-Cas complexes at the transcription bubble. United States: N. p., 2019. Web. https://doi.org/10.1038/s41467-019-10780-2.
Liu, Tina Y., Liu, Jun-Jie, Aditham, Abhishek J., Nogales, Eva, & Doudna, Jennifer A. Target preference of Type III-A CRISPR-Cas complexes at the transcription bubble. United States. https://doi.org/10.1038/s41467-019-10780-2
Liu, Tina Y., Liu, Jun-Jie, Aditham, Abhishek J., Nogales, Eva, and Doudna, Jennifer A. Fri . "Target preference of Type III-A CRISPR-Cas complexes at the transcription bubble". United States. https://doi.org/10.1038/s41467-019-10780-2. https://www.osti.gov/servlets/purl/1559231.
@article{osti_1559231,
title = {Target preference of Type III-A CRISPR-Cas complexes at the transcription bubble},
author = {Liu, Tina Y. and Liu, Jun-Jie and Aditham, Abhishek J. and Nogales, Eva and Doudna, Jennifer A.},
abstractNote = {Type III-A CRISPR-Cas systems are prokaryotic RNA-guided adaptive immune systems that use a protein-RNA complex, Csm, for transcription-dependent immunity against foreign DNA. Csm can cleave RNA and single-stranded DNA (ssDNA), but whether it targets one or both nucleic acids during transcription elongation is unknown. Here, we show that binding of a Thermus thermophilus (T. thermophilus) Csm (TthCsm) to a nascent transcript in a transcription elongation complex (TEC) promotes tethering but not direct contact of TthCsm with RNA polymerase (RNAP). Biochemical experiments show that both TthCsm and Staphylococcus epidermidis (S. epidermidis) Csm (SepCsm) cleave RNA transcripts, but not ssDNA, at the transcription bubble. Taken together, these results suggest that Type III systems primarily target transcripts, instead of unwound ssDNA in TECs, for immunity against double-stranded DNA (dsDNA) phages and plasmids. This reveals similarities between Csm and eukaryotic RNA interference, which also uses RNA-guided RNA targeting to silence actively transcribed genes.},
doi = {10.1038/s41467-019-10780-2},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 15 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

An updated evolutionary classification of CRISPR–Cas systems
journal, September 2015

  • Makarova, Kira S.; Wolf, Yuri I.; Alkhnbashi, Omer S.
  • Nature Reviews Microbiology, Vol. 13, Issue 11, p. 722-736
  • DOI: 10.1038/nrmicro3569

Revealing the world of RNA interference
journal, September 2004


Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2
journal, November 2016

  • Kimanius, Dari; Forsberg, Björn O.; Scheres, Sjors HW
  • eLife, Vol. 5
  • DOI: 10.7554/eLife.18722

Type III CRISPR-Cas systems: when DNA cleavage just isn’t enough
journal, June 2017


Biology and Applications of CRISPR Systems: Harnessing Nature’s Toolbox for Genome Engineering
journal, January 2016


The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
journal, November 2005


CRISPR-Cas12a target binding unleashes indiscriminate single-stranded DNase activity
journal, February 2018


Temporal Regulation of Viral Transcription during Development of Thermus thermophilus Bacteriophage ϕYS40
journal, February 2007

  • Sevostyanova, Anastasiya; Djordjevic, Marko; Kuznedelov, Konstantin
  • Journal of Molecular Biology, Vol. 366, Issue 2
  • DOI: 10.1016/j.jmb.2006.11.050

Appion: An integrated, database-driven pipeline to facilitate EM image processing
journal, April 2009

  • Lander, Gabriel C.; Stagg, Scott M.; Voss, Neil R.
  • Journal of Structural Biology, Vol. 166, Issue 1
  • DOI: 10.1016/j.jsb.2009.01.002

CTFFIND4: Fast and accurate defocus estimation from electron micrographs
journal, November 2015


A Ruler Protein in a Complex for Antiviral Defense Determines the Length of Small Interfering CRISPR RNAs
journal, August 2013

  • Hatoum-Aslan, Asma; Samai, Poulami; Maniv, Inbal
  • Journal of Biological Chemistry, Vol. 288, Issue 39
  • DOI: 10.1074/jbc.M113.499244

Cryo-EM Structures Reveal Mechanism and Inhibition of DNA Targeting by a CRISPR-Cas Surveillance Complex
journal, October 2017


Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target
journal, August 2014


MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy
journal, February 2017

  • Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul
  • Nature Methods, Vol. 14, Issue 4
  • DOI: 10.1038/nmeth.4193

Structure Studies of the CRISPR-Csm Complex Reveal Mechanism of Co-transcriptional Interference
journal, January 2019


Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems
journal, August 2016

  • Mohanraju, Prarthana; Makarova, Kira S.; Zetsche, Bernd
  • Science, Vol. 353, Issue 6299
  • DOI: 10.1126/science.aad5147

UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004

  • Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
  • Journal of Computational Chemistry, Vol. 25, Issue 13
  • DOI: 10.1002/jcc.20084

Crystal Structure of the CRISPR-Cas RNA Silencing Cmr Complex Bound to a Target Analog
journal, May 2015


Programmed DNA destruction by miniature CRISPR-Cas14 enzymes
journal, October 2018

  • Harrington, Lucas B.; Burstein, David; Chen, Janice S.
  • Science, Vol. 362, Issue 6416
  • DOI: 10.1126/science.aav4294

Degradation of Phage Transcripts by CRISPR-Associated RNases Enables Type III CRISPR-Cas Immunity
journal, February 2016


A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems
journal, June 2017

  • Kazlauskiene, Migle; Kostiuk, Georgij; Venclovas, Česlovas
  • Science, Vol. 357, Issue 6351
  • DOI: 10.1126/science.aao0100

Bipartite recognition of target RNAs activates DNA cleavage by the Type III-B CRISPR–Cas system
journal, February 2016

  • Elmore, Joshua R.; Sheppard, Nolan F.; Ramia, Nancy
  • Genes & Development, Vol. 30, Issue 4
  • DOI: 10.1101/gad.272153.115

EMAN2: An extensible image processing suite for electron microscopy
journal, January 2007

  • Tang, Guang; Peng, Liwei; Baldwin, Philip R.
  • Journal of Structural Biology, Vol. 157, Issue 1
  • DOI: 10.1016/j.jsb.2006.05.009

Type III CRISPR-Cas Immunity: Major Differences Brushed Aside
journal, January 2017

  • Tamulaitis, Gintautas; Venclovas, Česlovas; Siksnys, Virginijus
  • Trends in Microbiology, Vol. 25, Issue 1
  • DOI: 10.1016/j.tim.2016.09.012

MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

  • Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
  • DOI: 10.1107/S0907444909042073

Crystal Structure of a Transcribing RNA Polymerase II Complex Reveals a Complete Transcription Bubble
journal, July 2015


Non-specific degradation of transcripts promotes plasmid clearance during type III-A CRISPR–Cas immunity
journal, January 2019


Genetic Characterization of Antiplasmid Immunity through a Type III-A CRISPR-Cas System
journal, November 2013

  • Hatoum-Aslan, A.; Maniv, I.; Samai, P.
  • Journal of Bacteriology, Vol. 196, Issue 2
  • DOI: 10.1128/JB.01130-13

Coot model-building tools for molecular graphics
journal, November 2004

  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

Programmable type III-A CRISPR-Cas DNA targeting modules
journal, April 2017


RNA-activated DNA cleavage by the Type III-B CRISPR–Cas effector complex
journal, February 2016

  • Estrella, Michael A.; Kuo, Fang-Ting; Bailey, Scott
  • Genes & Development, Vol. 30, Issue 4
  • DOI: 10.1101/gad.273722.115

Single Particle Electron Microscopy Reconstruction of the Exosome Complex Using the Random Conical Tilt Method
journal, January 2011

  • Liu, Xueqi; Wang, Hong-Wei
  • Journal of Visualized Experiments, Issue 49
  • DOI: 10.3791/2574

RELION: Implementation of a Bayesian approach to cryo-EM structure determination
journal, December 2012


Spatiotemporal Control of Type III-A CRISPR-Cas Immunity: Coupling DNA Degradation with the Target RNA Recognition
journal, April 2016


Type III CRISPR–Cas systems produce cyclic oligoadenylate second messengers
journal, July 2017

  • Niewoehner, Ole; Garcia-Doval, Carmela; Rostøl, Jakob T.
  • Nature, Vol. 548, Issue 7669
  • DOI: 10.1038/nature23467

The ribonuclease activity of Csm6 is required for anti-plasmid immunity by Type III-A CRISPR-Cas systems
journal, June 2018


Structure of a bacterial RNA polymerase holoenzyme open promoter complex
journal, September 2015

  • Bae, Brian; Feklistov, Andrey; Lass-Napiorkowska, Agnieszka
  • eLife, Vol. 4
  • DOI: 10.7554/eLife.08504

Co-transcriptional DNA and RNA Cleavage during Type III CRISPR-Cas Immunity
journal, May 2015


Structural basis for transcription elongation by bacterial RNA polymerase
journal, June 2007

  • Vassylyev, Dmitry G.; Vassylyeva, Marina N.; Perederina, Anna
  • Nature, Vol. 448, Issue 7150
  • DOI: 10.1038/nature05932

Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting
journal, August 2014

  • Goldberg, Gregory W.; Jiang, Wenyan; Bikard, David
  • Nature, Vol. 514, Issue 7524
  • DOI: 10.1038/nature13637

Crystal Structure of the Csm1 Subunit of the Csm Complex and Its Single-Stranded DNA-Specific Nuclease Activity
journal, April 2015


R Loops: From Transcription Byproducts to Threats to Genome Stability
journal, April 2012


Structures of the CRISPR-Cmr complex reveal mode of RNA target positioning
journal, April 2015


CELLULAR DNA REPLICASES: Components and Dynamics at the Replication Fork
journal, June 2005


RNA Targeting by the Type III-A CRISPR-Cas Csm Complex of Thermus thermophilus
journal, November 2014


Automated electron microscope tomography using robust prediction of specimen movements
journal, October 2005


Programmable RNA Shredding by the Type III-A CRISPR-Cas System of Streptococcus thermophilus
journal, November 2014


cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination
journal, February 2017

  • Punjani, Ali; Rubinstein, John L.; Fleet, David J.
  • Nature Methods, Vol. 14, Issue 3
  • DOI: 10.1038/nmeth.4169

A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus : Novel CRISPR type IIIB interference
journal, February 2013

  • Deng, Ling; Garrett, Roger A.; Shah, Shiraz A.
  • Molecular Microbiology, Vol. 87, Issue 5
  • DOI: 10.1111/mmi.12152

Crystal Structure of the Csm3–Csm4 Subcomplex in the Type III-A CRISPR–Cas Interference Complex
journal, January 2015

  • Numata, Tomoyuki; Inanaga, Hideko; Sato, Chikara
  • Journal of Molecular Biology, Vol. 427, Issue 2
  • DOI: 10.1016/j.jmb.2014.09.029

RNA and DNA Targeting by a Reconstituted Thermus thermophilus Type III-A CRISPR-Cas System
journal, January 2017


The ribonuclease activity of Csm6 is required for anti-plasmid immunity by Type III-A CRISPR-Cas systems
text, January 2018


The ribonuclease activity of Csm6 is required for anti-plasmid immunity by Type III-A CRISPR-Cas systems
text, January 2020


    Works referencing / citing this record:

    UCSF Chimera?A visualization system for exploratory research and analysis
    journal, January 2004

    • Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
    • Journal of Computational Chemistry, Vol. 25, Issue 13
    • DOI: 10.1002/jcc.20084

    Co-transcriptional DNA and RNA Cleavage during Type III CRISPR-Cas Immunity
    journal, May 2015


    Biology and Applications of CRISPR Systems: Harnessing Nature’s Toolbox for Genome Engineering
    journal, January 2016


    Degradation of Phage Transcripts by CRISPR-Associated RNases Enables Type III CRISPR-Cas Immunity
    journal, February 2016


    Cryo-EM Structures Reveal Mechanism and Inhibition of DNA Targeting by a CRISPR-Cas Surveillance Complex
    journal, October 2017


    Structure Studies of the CRISPR-Csm Complex Reveal Mechanism of Co-transcriptional Interference
    journal, January 2019


    Temporal Regulation of Viral Transcription during Development of Thermus thermophilus Bacteriophage ϕYS40
    journal, February 2007

    • Sevostyanova, Anastasiya; Djordjevic, Marko; Kuznedelov, Konstantin
    • Journal of Molecular Biology, Vol. 366, Issue 2
    • DOI: 10.1016/j.jmb.2006.11.050

    Crystal Structure of the Csm3–Csm4 Subcomplex in the Type III-A CRISPR–Cas Interference Complex
    journal, January 2015

    • Numata, Tomoyuki; Inanaga, Hideko; Sato, Chikara
    • Journal of Molecular Biology, Vol. 427, Issue 2
    • DOI: 10.1016/j.jmb.2014.09.029

    Automated electron microscope tomography using robust prediction of specimen movements
    journal, October 2005


    EMAN2: An extensible image processing suite for electron microscopy
    journal, January 2007

    • Tang, Guang; Peng, Liwei; Baldwin, Philip R.
    • Journal of Structural Biology, Vol. 157, Issue 1
    • DOI: 10.1016/j.jsb.2006.05.009

    Appion: An integrated, database-driven pipeline to facilitate EM image processing
    journal, April 2009

    • Lander, Gabriel C.; Stagg, Scott M.; Voss, Neil R.
    • Journal of Structural Biology, Vol. 166, Issue 1
    • DOI: 10.1016/j.jsb.2009.01.002

    RELION: Implementation of a Bayesian approach to cryo-EM structure determination
    journal, December 2012


    CTFFIND4: Fast and accurate defocus estimation from electron micrographs
    journal, November 2015


    Type III CRISPR-Cas systems: when DNA cleavage just isn’t enough
    journal, June 2017


    R Loops: From Transcription Byproducts to Threats to Genome Stability
    journal, April 2012


    Programmable RNA Shredding by the Type III-A CRISPR-Cas System of Streptococcus thermophilus
    journal, November 2014


    RNA Targeting by the Type III-A CRISPR-Cas Csm Complex of Thermus thermophilus
    journal, November 2014


    Crystal Structure of the CRISPR-Cas RNA Silencing Cmr Complex Bound to a Target Analog
    journal, May 2015


    Crystal Structure of a Transcribing RNA Polymerase II Complex Reveals a Complete Transcription Bubble
    journal, July 2015


    Spatiotemporal Control of Type III-A CRISPR-Cas Immunity: Coupling DNA Degradation with the Target RNA Recognition
    journal, April 2016


    Crystal Structure of the Csm1 Subunit of the Csm Complex and Its Single-Stranded DNA-Specific Nuclease Activity
    journal, April 2015


    Type III CRISPR-Cas Immunity: Major Differences Brushed Aside
    journal, January 2017

    • Tamulaitis, Gintautas; Venclovas, Česlovas; Siksnys, Virginijus
    • Trends in Microbiology, Vol. 25, Issue 1
    • DOI: 10.1016/j.tim.2016.09.012

    Revealing the world of RNA interference
    journal, September 2004


    Structural basis for transcription elongation by bacterial RNA polymerase
    journal, June 2007

    • Vassylyev, Dmitry G.; Vassylyeva, Marina N.; Perederina, Anna
    • Nature, Vol. 448, Issue 7150
    • DOI: 10.1038/nature05932

    Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting
    journal, August 2014

    • Goldberg, Gregory W.; Jiang, Wenyan; Bikard, David
    • Nature, Vol. 514, Issue 7524
    • DOI: 10.1038/nature13637

    Type III CRISPR–Cas systems produce cyclic oligoadenylate second messengers
    journal, July 2017

    • Niewoehner, Ole; Garcia-Doval, Carmela; Rostøl, Jakob T.
    • Nature, Vol. 548, Issue 7669
    • DOI: 10.1038/nature23467

    cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination
    journal, February 2017

    • Punjani, Ali; Rubinstein, John L.; Fleet, David J.
    • Nature Methods, Vol. 14, Issue 3
    • DOI: 10.1038/nmeth.4169

    MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy
    journal, February 2017

    • Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul
    • Nature Methods, Vol. 14, Issue 4
    • DOI: 10.1038/nmeth.4193

    An updated evolutionary classification of CRISPR–Cas systems
    journal, September 2015

    • Makarova, Kira S.; Wolf, Yuri I.; Alkhnbashi, Omer S.
    • Nature Reviews Microbiology, Vol. 13, Issue 11, p. 722-736
    • DOI: 10.1038/nrmicro3569

    Non-specific degradation of transcripts promotes plasmid clearance during type III-A CRISPR–Cas immunity
    journal, January 2019


    A Ruler Protein in a Complex for Antiviral Defense Determines the Length of Small Interfering CRISPR RNAs
    journal, August 2013

    • Hatoum-Aslan, Asma; Samai, Poulami; Maniv, Inbal
    • Journal of Biological Chemistry, Vol. 288, Issue 39
    • DOI: 10.1074/jbc.m113.499244

    The ribonuclease activity of Csm6 is required for anti-plasmid immunity by Type III-A CRISPR-Cas systems
    journal, June 2018


    The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
    journal, November 2005


    Bipartite recognition of target RNAs activates DNA cleavage by the Type III-B CRISPR–Cas system
    journal, February 2016

    • Elmore, Joshua R.; Sheppard, Nolan F.; Ramia, Nancy
    • Genes & Development, Vol. 30, Issue 4
    • DOI: 10.1101/gad.272153.115

    RNA-activated DNA cleavage by the Type III-B CRISPR–Cas effector complex
    journal, February 2016

    • Estrella, Michael A.; Kuo, Fang-Ting; Bailey, Scott
    • Genes & Development, Vol. 30, Issue 4
    • DOI: 10.1101/gad.273722.115

    Coot model-building tools for molecular graphics
    journal, November 2004

    • Emsley, Paul; Cowtan, Kevin
    • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
    • DOI: 10.1107/s0907444904019158

    MolProbity : all-atom structure validation for macromolecular crystallography
    journal, December 2009

    • Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
    • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
    • DOI: 10.1107/s0907444909042073

    A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus : Novel CRISPR type IIIB interference
    journal, February 2013

    • Deng, Ling; Garrett, Roger A.; Shah, Shiraz A.
    • Molecular Microbiology, Vol. 87, Issue 5
    • DOI: 10.1111/mmi.12152

    Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target
    journal, August 2014


    Structures of the CRISPR-Cmr complex reveal mode of RNA target positioning
    journal, April 2015


    Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems
    journal, August 2016

    • Mohanraju, Prarthana; Makarova, Kira S.; Zetsche, Bernd
    • Science, Vol. 353, Issue 6299
    • DOI: 10.1126/science.aad5147

    A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems
    journal, June 2017

    • Kazlauskiene, Migle; Kostiuk, Georgij; Venclovas, Česlovas
    • Science, Vol. 357, Issue 6351
    • DOI: 10.1126/science.aao0100

    CRISPR-Cas12a target binding unleashes indiscriminate single-stranded DNase activity
    journal, February 2018


    Programmed DNA destruction by miniature CRISPR-Cas14 enzymes
    journal, October 2018

    • Harrington, Lucas B.; Burstein, David; Chen, Janice S.
    • Science, Vol. 362, Issue 6416
    • DOI: 10.1126/science.aav4294

    Genetic Characterization of Antiplasmid Immunity through a Type III-A CRISPR-Cas System
    journal, November 2013

    • Hatoum-Aslan, A.; Maniv, I.; Samai, P.
    • Journal of Bacteriology, Vol. 196, Issue 2
    • DOI: 10.1128/jb.01130-13

    CELLULAR DNA REPLICASES: Components and Dynamics at the Replication Fork
    journal, June 2005


    RNA and DNA Targeting by a Reconstituted Thermus thermophilus Type III-A CRISPR-Cas System
    journal, January 2017


    Programmable type III-A CRISPR-Cas DNA targeting modules
    journal, April 2017


    Single Particle Electron Microscopy Reconstruction of the Exosome Complex Using the Random Conical Tilt Method
    journal, January 2011

    • Liu, Xueqi; Wang, Hong-Wei
    • Journal of Visualized Experiments, Issue 49
    • DOI: 10.3791/2574

    Structure of a bacterial RNA polymerase holoenzyme open promoter complex
    journal, September 2015

    • Bae, Brian; Feklistov, Andrey; Lass-Napiorkowska, Agnieszka
    • eLife, Vol. 4
    • DOI: 10.7554/elife.08504

    Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2
    journal, November 2016

    • Kimanius, Dari; Forsberg, Björn O.; Scheres, Sjors HW
    • eLife, Vol. 5
    • DOI: 10.7554/elife.18722