Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Biological Chemistry

Editor-in-Chief: Brüne, Bernhard

Editorial Board: Buchner, Johannes / Lei, Ming / Ludwig, Stephan / Sies, Helmut / Thomas, Douglas D. / Turk, Boris / Wittinghofer, Alfred

12 Issues per year

IMPACT FACTOR 2016: 3.273

CiteScore 2016: 3.01

SCImago Journal Rank (SJR) 2016: 1.679
Source Normalized Impact per Paper (SNIP) 2016: 0.800

See all formats and pricing
More options …
Volume 392, Issue 4


Clustered regularly interspaced short palindromic repeats (CRISPRs): the hallmark of an ingenious antiviral defense mechanism in prokaryotes

Sinan Al-Attar
  • Laboratory of Microbiology, Wageningen University, Dreijenplein 10, NL-6703 HB Wageningen, The Netherlands
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Edze R. Westra
  • Laboratory of Microbiology, Wageningen University, Dreijenplein 10, NL-6703 HB Wageningen, The Netherlands
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ John van der Oost
  • Laboratory of Microbiology, Wageningen University, Dreijenplein 10, NL-6703 HB Wageningen, The Netherlands
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Stan J.J. Brouns
Published Online: 2011-07-25 | DOI: https://doi.org/10.1515/bc.2011.042


Many prokaryotes contain the recently discovered defense system against mobile genetic elements. This defense system contains a unique type of repetitive DNA stretches, termed Clustered Regularly Interspaced Short Palindromic Repeats (CRISPRs). CRISPRs consist of identical repeated DNA sequences (repeats), interspaced by highly variable sequences referred to as spacers. The spacers originate from either phages or plasmids and comprise the prokaryotes' ‘immunological memory’. CRISPR-associated (cas) genes encode conserved proteins that together with CRISPRs make-up the CRISPR/Cas system, responsible for defending the prokaryotic cell against invaders. CRISPR-mediated resistance has been proposed to involve three stages: (i) CRISPR-Adaptation, the invader DNA is encountered by the CRISPR/Cas machinery and an invader-derived short DNA fragment is incorporated in the CRISPR array. (ii) CRISPR-Expression, the CRISPR array is transcribed and the transcript is processed by Cas proteins. (iii) CRISPR-Interference, the invaders' nucleic acid is recognized by complementarity to the crRNA and neutralized. An application of the CRISPR/Cas system is the immunization of industry-relevant prokaryotes (or eukaryotes) against mobile-genetic invasion. In addition, the high variability of the CRISPR spacer content can be exploited for phylogenetic and evolutionary studies. Despite impressive progress during the last couple of years, the elucidation of several fundamental details will be a major challenge in future research.

Keywords: anti-phage; Cas proteins; small RNAs; spacers

About the article

Corresponding author

Received: 2010-10-27

Accepted: 2010-12-27

Published Online: 2011-07-25

Published in Print: 2011-04-01

Citation Information: Biological Chemistry, Volume 392, Issue 4, Pages 277–289, ISSN (Online) 1437-4315, ISSN (Print) 1431-6730, DOI: https://doi.org/10.1515/bc.2011.042.

Export Citation

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Tejal Aslesh, Rika Maruyama, and Toshifumi Yokota
Biomedicines, 2018, Volume 6, Number 1, Page 1
Andjela Rodic, Bojana Blagojevic, Magdalena Djordjevic, Konstantin Severinov, and Marko Djordjevic
Frontiers in Microbiology, 2017, Volume 8
Cristina Andrés-Barrao, Feras F. Lafi, Intikhab Alam, Axel de Zélicourt, Abdul A. Eida, Ameerah Bokhari, Hanin Alzubaidy, Vladimir B. Bajic, Heribert Hirt, and Maged M. Saad
Frontiers in Microbiology, 2017, Volume 8
Hikmate Abriouel, Beatriz Pérez Montoro, María del Carmen Casado Muñoz, Charles W. Knapp, Antonio Gálvez, Nabil Benomar, and Baochuan Lin
PLOS ONE, 2017, Volume 12, Number 6, Page e0176801
Stefan Kopfmann and Wolfgang R. Hess
Journal of Biological Chemistry, 2013, Volume 288, Number 10, Page 7399
Jutta Brendel, Britta Stoll, Sita J. Lange, Kundan Sharma, Christof Lenz, Aris-Edda Stachler, Lisa-Katharina Maier, Hagen Richter, Lisa Nickel, Ruth A. Schmitz, Lennart Randau, Thorsten Allers, Henning Urlaub, Rolf Backofen, and Anita Marchfelder
Journal of Biological Chemistry, 2014, Volume 289, Number 10, Page 7164
Susan Fischer, Lisa-Katharina Maier, Britta Stoll, Jutta Brendel, Eike Fischer, Friedhelm Pfeiffer, Mike Dyall-Smith, and Anita Marchfelder
Journal of Biological Chemistry, 2012, Volume 287, Number 40, Page 33351
Vijai Singh, Nisarg Gohil, Robert Ramírez García, Darren Braddick, and Christian Kuete Fofié
Journal of Cellular Biochemistry, 2017
P. Gholizadeh, M. Aghazadeh, M. Asgharzadeh, and H. S. Kafil
European Journal of Clinical Microbiology & Infectious Diseases, 2017
Xuan Zou, Lianrong Wang, Zhiqiang Li, Jie Luo, Yunfu Wang, Zixin Deng, Shiming Du, and Shi Chen
Medicinal Research Reviews, 2017
Lauren M. Childs, Whitney E. England, Mark J. Young, Joshua S. Weitz, Rachel J. Whitaker, and Welkin E. Johnson
PLoS ONE, 2014, Volume 9, Number 7, Page e101710
Robert L. Robson, Robert Jones, R. Moyra Robson, Ariel Schwartz, Toby H. Richardson, and Jean-François Pombert
PLOS ONE, 2015, Volume 10, Number 6, Page e0127997
Luca Fagnocchi, Silvia Bottini, Giacomo Golfieri, Laura Fantappiè, Francesca Ferlicca, Ana Antunes, Serafina Guadagnuolo, Elena Del Tordello, Emilio Siena, Davide Serruto, Vincenzo Scarlato, Alessandro Muzzi, Isabel Delany, and Thomas Rudel
PLOS ONE, 2015, Volume 10, Number 5, Page e0126325
José Claudio Provenzano, José F. Siqueira, Isabela N. Rôças, Romênia R. Domingues, Adriana F. Paes Leme, Márcia R. S. Silva, and Jamunarani Vadivelu
PLoS ONE, 2013, Volume 8, Number 10, Page e76108
Ingeborg Scholz, Sita J. Lange, Stephanie Hein, Wolfgang R. Hess, Rolf Backofen, and Valerie de Crécy-Lagard
PLoS ONE, 2013, Volume 8, Number 2, Page e56470
Samuel Fischer, Sophie Kittler, Günter Klein, Gerhard Glünder, and Markus M. Heimesaat
PLoS ONE, 2013, Volume 8, Number 1, Page e53899
Andjela Rodic, Bojana Blagojevic, Evgeny Zdobnov, Magdalena Djordjevic, and Marko Djordjevic
BMC Systems Biology, 2017, Volume 11, Number S1, Page 1
Alfonso H. Magadán, Marie-Ève Dupuis, Manuela Villion, Sylvain Moineau, and Anthony R. Poteete
PLoS ONE, 2012, Volume 7, Number 7, Page e40913
Maria Paloma S. Barros, Camila T. França, Rosanny Holanda F. B. Lins, Milena Danda V. Santos, Ednaldo J. Silva, Maria Betânia M. Oliveira, Vladimir M. Silveira-Filho, Antônio M. Rezende, Valdir Q. Balbino, Tereza Cristina Leal-Balbino, and Mikael Skurnik
PLoS ONE, 2014, Volume 9, Number 9, Page e108353
Daan C. Swarts, Cas Mosterd, Mark W. J. van Passel, Stan J. J. Brouns, and Igor Mokrousov
PLoS ONE, 2012, Volume 7, Number 4, Page e35888
Milos Nikolic, Tamara Stankovic, and Marko Djordjevic
Journal of Bioinformatics and Computational Biology, 2017, Volume 15, Number 02, Page 1650038
Lucía Calleros, Laura Betancor, Gregorio Iraola, Alejandra Méndez, Claudia Morsella, Fernando Paolicchi, Silvia Silveyra, Alejandra Velilla, and Ruben Pérez
Journal of Microbiological Methods, 2017, Volume 132, Page 86
Vijai Singh, Darren Braddick, and Pawan Kumar Dhar
Gene, 2017, Volume 599, Page 1
Pierre Béguin, Nicole Charpin, Eugene V. Koonin, Patrick Forterre, and Mart Krupovic
Nucleic Acids Research, 2016, Page gkw821
I-Son Ng, Ying-Hsin Hung, Pei-Hsun Kao, Yunli Zhou, and Xia Zhang
Journal of the Taiwan Institute of Chemical Engineers, 2016, Volume 68, Page 31
Enzo Messina, Dimitry Y. Sorokin, Ilya V. Kublanov, Stepan Toshchakov, Anna Lopatina, Erika Arcadi, Francesco Smedile, Gina La Spada, Violetta La Cono, and Michail M. Yakimov
Standards in Genomic Sciences, 2016, Volume 11, Number 1
Alison Luk, Timothy Williams, Susanne Erdmann, R. Papke, and Ricardo Cavicchioli
Life, 2014, Volume 4, Number 4, Page 681
Xinyi He, Victoria Hull, Julie A. Thomas, Xiaoqing Fu, Sonal Gidwani, Yogesh K. Gupta, Lindsay W. Black, and Shuang-yong Xu
Scientific Reports, 2015, Volume 5, Number 1
Li-Fang Chou, Ting-Wen Chen, Yi-Ching Ko, Ming-Jeng Pan, Ya-Chung Tian, Cheng-Hsun Chiu, Petrus Tang, Cheng-Chieh Hung, and Chih-Wei Yang
Emerging Microbes & Infections, 2014, Volume 3, Number 11, Page e82
Stephen T. Abedon
Bacteriophage, 2011, Volume 1, Number 3, Page 179
Ajla Hrle, Lisa-Katharina Maier, Kundan Sharma, Judith Ebert, Claire Basquin, Henning Urlaub, Anita Marchfelder, and Elena Conti
RNA Biology, 2014, Volume 11, Number 8, Page 1072
Zihni Arslan, Veronica Hermanns, Reinhild Wurm, Rolf Wagner, and Ümit Pul
Nucleic Acids Research, 2014, Volume 42, Number 12, Page 7884
M. Jinek, F. Jiang, D. W. Taylor, S. H. Sternberg, E. Kaya, E. Ma, C. Anders, M. Hauer, K. Zhou, S. Lin, M. Kaplan, A. T. Iavarone, E. Charpentier, E. Nogales, and J. A. Doudna
Science, 2014, Volume 343, Number 6176, Page 1247997
O. Niewoehner, M. Jinek, and J. A. Doudna
Nucleic Acids Research, 2014, Volume 42, Number 2, Page 1341
Elisabeth Sonnleitner, Alessandra Romeo, and Udo Bläsi
RNA Biology, 2012, Volume 9, Number 4, Page 364
Edze R. Westra, Benedikt Nilges, Paul B. G. van Erp, John van der Oost, Remus T. Dame, and Stan J. J. Brouns
RNA Biology, 2012, Volume 9, Number 9, Page 1134
Stephen T. Abedon
Bacteriophage, 2012, Volume 2, Number 1, Page 50
Inbal Maniv, Asma Hatoum-Aslan, and Luciano A. Marraffini
RNA Biology, 2013, Volume 10, Number 5, Page 694
Stephanie Hein, Ingeborg Scholz, Björn Voß, and Wolfgang R. Hess
RNA Biology, 2013, Volume 10, Number 5, Page 852
Lisa-Katharina Maier, Susan M Fischer, Britta Stoll, Jutta Brendel, Friedhelm Pfeiffer, Mike Dyall-Smith, and Anita Marchfelder
Mobile Genetic Elements, 2012, Volume 2, Number 5, Page 228
Lisa Nickel, Katrin Weidenbach, Dominik Jäger, Rolf Backofen, Sita J. Lange, Nadja Heidrich, and Ruth A. Schmitz
RNA Biology, 2013, Volume 10, Number 5, Page 779
Sita J. Lange, Omer S. Alkhnbashi, Dominic Rose, Sebastian Will, and Rolf Backofen
Nucleic Acids Research, 2013, Volume 41, Number 17, Page 8034
Anita Marchfelder, Lisa-Katharina Maier, Nadja Heidrich, and Ümit Pul
Biologie in unserer Zeit, 2013, Volume 43, Number 3, Page 158
Z. Arslan, R. Wurm, O. Brener, P. Ellinger, L. Nagel-Steger, F. Oesterhelt, L. Schmitt, D. Willbold, R. Wagner, H. Gohlke, S. H. J. Smits, and U. Pul
Nucleic Acids Research, 2013, Volume 41, Number 12, Page 6347
Rodolphe Barrangou
Wiley Interdisciplinary Reviews: RNA, 2013, Volume 4, Number 3, Page 267
David Paez-Espino, Wesley Morovic, Christine L. Sun, Brian C. Thomas, Ken-ichi Ueda, Buffy Stahl, Rodolphe Barrangou, and Jillian F. Banfield
Nature Communications, 2013, Volume 4, Page 1430
Tomas Sinkunas, Giedrius Gasiunas, Sakharam P Waghmare, Mark J Dickman, Rodolphe Barrangou, Philippe Horvath, and Virginijus Siksnys
The EMBO Journal, 2013, Volume 32, Number 3, Page 385
Edze R. Westra, Daan C. Swarts, Raymond H.J. Staals, Matthijs M. Jore, Stan J.J. Brouns, and John van der Oost
Annual Review of Genetics, 2012, Volume 46, Number 1, Page 311
D. Trautmann, B. Voss, A. Wilde, S. Al-Babili, and W. R. Hess
DNA Research, 2012, Volume 19, Number 6, Page 435
Anja Spang, Anja Poehlein, Pierre Offre, Sabine Zumbrägel, Susanne Haider, Nicolas Rychlik, Boris Nowka, Christel Schmeisser, Elena V. Lebedeva, Thomas Rattei, Christoph Böhm, Markus Schmid, Alexander Galushko, Roland Hatzenpichler, Thomas Weinmaier, Rolf Daniel, Christa Schleper, Eva Spieck, Wolfgang Streit, and Michael Wagner
Environmental Microbiology, 2012, Volume 14, Number 12, Page 3122
Lei Qi, Rachel E Haurwitz, Wenjun Shao, Jennifer A Doudna, and Adam P Arkin
Nature Biotechnology, 2012, Volume 30, Number 10, Page 1002
Marko Djordjevic and Magdalena Djordjevic
Physical Biology, 2012, Volume 9, Number 5, Page 056004
Rebekah A. Frampton, Andrew R. Pitman, and Peter C. Fineran
International Journal of Microbiology, 2012, Volume 2012, Page 1
Rodolphe Barrangou and Philippe Horvath
Annual Review of Food Science and Technology, 2012, Volume 3, Number 1, Page 143
Rachel E Haurwitz, Samuel H Sternberg, and Jennifer A Doudna
The EMBO Journal, 2012, Volume 31, Number 12, Page 2824
K. S. Pougach, A. V. Lopatina, and K. V. Severinov
Molecular Biology, 2012, Volume 46, Number 2, Page 175
Philipp Ellinger, Zihni Arslan, Reinhild Wurm, Britta Tschapek, Colin MacKenzie, Klaus Pfeffer, Santosh Panjikar, Rolf Wagner, Lutz Schmitt, Holger Gohlke, Ümit Pul, and Sander H.J. Smits
Journal of Structural Biology, 2012, Volume 178, Number 3, Page 350
Blake Wiedenheft, Samuel H. Sternberg, and Jennifer A. Doudna
Nature, 2012, Volume 482, Number 7385, Page 331
N. Delihas
Genome Biology and Evolution, 2011, Volume 3, Number 0, Page 959
Devaki Bhaya, Michelle Davison, and Rodolphe Barrangou
Annual Review of Genetics, 2011, Volume 45, Number 1, Page 273
Gregory R. Richards and Carin K. Vanderpool
Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 2011, Volume 1809, Number 10, Page 525
Dagmar Klostermeier
Biological Chemistry, 2011, Volume 392, Number 4
Kira S. Makarova, Daniel H. Haft, Rodolphe Barrangou, Stan J. J. Brouns, Emmanuelle Charpentier, Philippe Horvath, Sylvain Moineau, Francisco J. M. Mojica, Yuri I. Wolf, Alexander F. Yakunin, John van der Oost, and Eugene V. Koonin
Nature Reviews Microbiology, 2011, Volume 9, Number 6, Page 467

Comments (0)

Please log in or register to comment.
Log in