Cutting it Right: Plasticity and Strategy of CRISPR RNA Specific Nucleases
Keywords:
CRISPR RNA, CRISPR-Cas system, guide RNA, Cascade, Cas5, Cas6, Csy4, RNase, DNase, surveillance complex
Abstract
The existence of adaptive immunity in prokaryotes came to light with the discovery of the Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR) in association with CRISPR-associated (Cas) proteins. This RNA mediated defence system confers resistance against the invading mobile genetic elements such as phages and plasmids. The CRISPR-Cas system operates by forming a ribonucleoprotein complex that comprises of an invader derived small RNA and Cas proteins. Herein the small RNA acts as a guide to recognize the nucleic acid target whereas the Cas proteins facilitate target annihilation. Given the cardinal role adopted by this small RNA, its maturation from the pre-CRISPR transcript forms a pivot for successful adaptive immunity. The mandate to generate the guide CRISPR RNA (crRNA) is fulfilled by specific endonucleases, which process the pre-crRNA transcript in between the repeats to liberate the individual mature crRNA units. Intriguingly, while some endoRNases of the CRISPR system are able to process the pre-crRNA unaided, others require association of additional Cas proteins to form a multi-protein complex, which then process the pre- crRNA. Additionally, some CRISPR variants require auxiliary factors to process the pre- crRNA. The mode of crRNA maturation further diversifies as the endoRNases in CRISPR variants coevolve with repeat clusters that exhibit high diversity in sequence and folding. Therefore, the maturation of specific crRNA requires a distinct mechanistic solution for substrate discrimination by these endoRNases, the understanding of which is essential for appreciating the CRISPR biology. This review highlights the vivid modes adopted by the diverse CRISPR-Cas systems to generate the mature crRNA.
References
Abudayyeh O O, Gootenberg J S, Konermann S, Joung J, Slaymaker I M, et al. (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector Science 353:aaf5573
Agari Y, Sakamoto K, Tamakoshi M, Oshima T, Kuramitsu S, et al. (2010) Transcription profile of Thermus thermophilus CRISPR systems after phage infection J Mol Biol 395:270-281
Al-Attar S, Westra E R, van der Oost J, Brouns S J (2011) Clustered regularly interspaced short palindromic repeats (CRISPRs): the hallmark of an ingenious antiviral defense mechanism in prokaryotes Biol Chem 392:277-289
Amitai G, Sorek R (2016) CRISPR-Cas adaptation: insights into the mechanism of action Nat Rev Microbiol 14:67-76
Arslan Z, Hermanns V, Wurm R, Wagner R, Pul U (2014) Detection and characterization of spacer integration intermediates in type I-E CRISPR-Cas system Nucleic Acids Res 42:7884-7893
Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes Science 315:1709-1712
Benda C, Ebert J, Scheltema R A, Schiller H B, Baumgartner M, et al. (2014) Structural model of a CRISPR RNA-silencing complex reveals the RNA-target cleavage activity in Cmr4 Mol Cell 56:43-54
Bhaya D, Davison M, Barrangou R (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation Annu Rev Genet 45:273-297
Brouns S J, Jore M M, Lundgren M, Westra E R, Slijkhuis R J, et al. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes Science 321:960-964
Carte J, Pfister N T, Compton M M, Terns R M, Terns M P (2010) Binding and cleavage of CRISPR RNA by Cas6 RNA 16:2181-2188
Carte J, Wang R, Li H, Terns R M, Terns M P (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes Genes Dev 22:3489-3496
Datsenko K A, Pougach K, Tikhonov A, Wanner B L, Severinov K, et al. (2012) Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system Nat Commun 3:945
Deltcheva E, Chylinski K, Sharma C M, Gonzales K, Chao Y, et al. (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III Nature 471:602-607
East-Seletsky A, O'Connell M R, Knight S C, Burstein D, Cate J H, et al. (2016) Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection Nature 538:270-273
Fineran P C, Charpentier E (2012) Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information Virology 434:202-209
Fonfara I, Richter H, Bratovic M, Le Rhun A, Charpentier E (2016) The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA Nature 532:517-521
Gao P, Yang H, Rajashankar K R, Huang Z, Patel D J (2016) Type V CRISPR-Cas Cpf1 endonuclease employs a unique mechanism for crRNA-mediated target DNA recognition Cell Res 26:901-913
Garneau J E, Dupuis M E, Villion M, Romero D A, Barrangou R, et al. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA Nature 468:67-71
Garside E L, Schellenberg M J, Gesner E M, Bonanno J B, Sauder J M, et al. (2012) Cas5d processes pre-crRNA and is a member of a larger family of CRISPR RNA endonucleases RNA 18:2020-2028
Gesner E M, Schellenberg M J, Garside E L, George M M, Macmillan A M (2011) Recognition and maturation of effector RNAs in a CRISPR interference pathway Nat Struct Mol Biol 18:688-692
Grissa I, Vergnaud G, Pourcel C (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats BMC Bioinformatics 8:172
Haft D H, Selengut J, Mongodin E F, Nelson K E (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes PLoS Comput Biol 1:e60
Hale C R, Zhao P, Olson S, Duff M O, Graveley B R, et al. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex Cell 139:945-956
Haurwitz R E, Jinek M, Wiedenheft B, Zhou K, Doudna J A (2010) Sequence- and structure-specific RNA processing by a CRISPR endonuclease Science 329:1355-1358
Haurwitz R E, Sternberg S H, Doudna J A (2012) Csy4 relies on an unusual catalytic dyad to position and cleave CRISPR RNA EMBO J 31:2824-2832
Hayes R P, Ke A (2015) One More Piece Down to Solve the III-A CRISPR Puzzle J Mol Biol 427:228-230
Hayes R P, Xiao Y, Ding F, van Erp P B, Rajashankar K, et al. (2016) Structural basis for promiscuous PAM recognition in type I-E Cascade from E. coli Nature 530:499-503
Hille F, Charpentier E (2016) CRISPR-Cas: biology, mechanisms and relevance Philos Trans R Soc Lond B Biol Sci 371
Hochstrasser M L, Doudna J A (2015) Cutting it close: CRISPR-associated endoribonuclease structure and function Trends Biochem Sci 40:58-66
Hooton S P, Connerton I F (2014) Campylobacter jejuni acquire new host-derived CRISPR spacers when in association with bacteriophages harboring a CRISPR-like Cas4 protein Front Microbiol 5:744
Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea Science 327:167-170
Hyman P, Abedon S T (2010) Bacteriophage host range and bacterial resistance Adv Appl Microbiol 70:217-248
Jackson R N, Golden S M, van Erp P B, Carter J, Westra E R, et al. (2014) Structural biology. Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli Science 345:1473-1479
Jackson S A, McKenzie R E, Fagerlund R D, Kieper S N, Fineran P C, et al. (2017) CRISPR-Cas: Adapting to change Science 356:eaal5056
Jansen R, Embden J D, Gaastra W, Schouls L M (2002) Identification of genes that are associated with DNA repeats in prokaryotes Mol Microbiol 43:1565-1575
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna J A, et al. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science 337:816-821
Jore M M, Lundgren M, van Duijn E, Bultema J B, Westra E R, et al. (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade Nat Struct Mol Biol 18:529-536
Karginov F V, Hannon G J (2010) The CRISPR system: small RNA-guided defense in bacteria and archaea Mol Cell 37:7-19
Koo Y, Ka D, Kim E J, Suh N, Bae E (2013) Conservation and variability in the structure and function of the Cas5d endoribonuclease in the CRISPR-mediated microbial immune system J Mol Biol 425:3799-3810
Kunin V, Sorek R, Hugenholtz P (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats Genome Biol 8:R61
Labrie S J, Samson J E, Moineau S (2010) Bacteriophage resistance mechanisms Nat Rev Microbiol 8:317-327
Lewis K M, Ke A (2017) Building the Class 2 CRISPR-Cas Arsenal Mol Cell 65:377-379
Li H (2015) Structural Principles of CRISPR RNA Processing Structure 23:13-20
Li M, Wang R, Zhao D, Xiang H (2014) Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process Nucleic Acids Res 42:2483-2492
Lillestol R K, Shah S A, Brugger K, Redder P, Phan H, et al. (2009) CRISPR families of the crenarchaeal genus Sulfolobus: bidirectional transcription and dynamic properties Mol Microbiol 72:259-272
Lintner N G, Kerou M, Brumfield S K, Graham S, Liu H, et al. (2011) Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE) J Biol Chem 286:21643-21656
Liu L, Chen P, Wang M, Li X, Wang J, et al. (2017a) C2c1-sgRNA Complex Structure Reveals RNA-Guided DNA Cleavage Mechanism Mol Cell 65:310-322
Liu L, Li X, Wang J, Wang M, Chen P, et al. (2017b) Two Distant Catalytic Sites Are Responsible for C2c2 RNase Activities Cell 168:121-134
Makarova K S, Wolf Y I, Alkhnbashi O S, Costa F, Shah S A, et al. (2015) An updated evolutionary classification of CRISPR-Cas systems Nat Rev Microbiol 13:722-736
Makarova K S, Zhang F, Koonin E V (2017a) SnapShot: Class 1 CRISPR-Cas Systems Cell 168:946-946
Makarova K S, Zhang F, Koonin E V (2017b) SnapShot: Class 2 CRISPR-Cas Systems Cell 168:328-328
Marraffini L A (2015) CRISPR-Cas immunity in prokaryotes Nature 526:55-61
Marraffini L A, Sontheimer E J (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA Science 322:1843-1845
Marraffini L A, Sontheimer E J (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea Nat Rev Genet 11:181-190
Mohanraju P, Makarova K S, Zetsche B, Zhang F, Koonin E V, et al. (2016) Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems Science 353:aad5147
Nam K H, Haitjema C, Liu X, Ding F, Wang H, et al. (2012) Cas5d protein processes pre-crRNA and assembles into a cascade-like interference complex in subtype I-C/Dvulg CRISPR-Cas system Structure 20:1574-1584
Nishimasu H, Nureki O (2016) Structures and mechanisms of CRISPR RNA-guided effector nucleases Curr Opin Struct Biol 43:68-78
Osawa T, Inanaga H, Sato C, Numata T (2015) Crystal structure of the CRISPR-Cas RNA silencing Cmr complex bound to a target analog Mol Cell 58:418-430
Perez-Rodriguez R, Haitjema C, Huang Q, Nam K H, Bernardis S, et al. (2011) Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli Mol Microbiol 79:584-599
Pettersen E F, Goddard T D, Huang C C, Couch G S, Greenblatt D M, et al. (2004) UCSF Chimera--a visualization system for exploratory research and analysis J Comput Chem 25:1605-1612
Pougach K, Semenova E, Bogdanova E, Datsenko K A, Djordjevic M, et al. (2010) Transcription, processing and function of CRISPR cassettes in Escherichia coli Mol Microbiol 77:1367-1379
Pul U, Wurm R, Arslan Z, Geissen R, Hofmann N, et al. (2010) Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS Mol Microbiol 75:1495-1512
Punetha A, Sivathanu R, Anand B (2014) Active site plasticity enables metal-dependent tuning of Cas5d nuclease activity in CRISPR-Cas type I-C system Nucleic Acids Res 42:3846-3856
Raines R T (1998) Ribonuclease A Chem Rev 98:1045-1066
Richter C, Dy R L, McKenzie R E, Watson B N, Taylor C, et al. (2014) Priming in the Type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bi-directionally from the primed protospacer Nucleic Acids Res 42:8516-8526
Rollins M F, Schuman J T, Paulus K, Bukhari H S, Wiedenheft B (2015) Mechanism of foreign DNA recognition by a CRISPR RNA-guided surveillance complex from Pseudomonas aeruginosa Nucleic Acids Res 43:2216-2222
Rouillon C, Zhou M, Zhang J, Politis A, Beilsten-Edmands V, et al. (2013) Structure of the CRISPR interference complex CSM reveals key similarities with cascade Mol Cell 52:124-134
Rousseau C, Gonnet M, Le Romancer M, Nicolas J (2009) CRISPI: a CRISPR interactive database Bioinformatics 25:3317-3318
Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, et al. (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli Nucleic Acids Res 39:9275-9282
Sashital D G, Jinek M, Doudna J A (2011) An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3 Nat Struct Mol Biol 18:680-687
Semenova E, Jore M M, Datsenko K A, Semenova A, Westra E R, et al. (2011) Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence Proc Natl Acad Sci U S A 108:10098-10103
Semenova E, Nagornykh M, Pyatnitskiy M, Artamonova, II, Severinov K (2009) Analysis of CRISPR system function in plant pathogen Xanthomonas oryzae FEMS Microbiol Lett 296:110-116
Shao Y, Li H (2013) Recognition and cleavage of a nonstructured CRISPR RNA by its processing endoribonuclease Cas6 Structure 21:385-393
Shao Y, Richter H, Sun S, Sharma K, Urlaub H, et al. (2016) A Non-Stem-Loop CRISPR RNA Is Processed by Dual Binding Cas6 Structure 24:547-554
Shmakov S, Smargon A, Scott D, Cox D, Pyzocha N, et al. (2017) Diversity and evolution of class 2 CRISPR-Cas systems Nat Rev Microbiol 15:169-182
Smargon A A, Cox D B, Pyzocha N K, Zheng K, Slaymaker I M, et al. (2017) Cas13b Is a Type VI-B CRISPR-Associated RNA-Guided RNase Differentially Regulated by Accessory Proteins Csx27 and Csx28 Mol Cell 65:618-630.e617
Spilman M, Cocozaki A, Hale C, Shao Y, Ramia N, et al. (2013) Structure of an RNA silencing complex of the CRISPR-Cas immune system Mol Cell 52:146-152
Staals R H, Zhu Y, Taylor D W, Kornfeld J E, Sharma K, et al. (2014) RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus Mol Cell 56:518-530
Sternberg S H, Haurwitz R E, Doudna J A (2012) Mechanism of substrate selection by a highly specific CRISPR endoribonuclease RNA 18:661-672
Sternberg S H, Richter H, Charpentier E, Qimron U (2016) Adaptation in CRISPR-Cas Systems Mol Cell 61:797-808
Swarts D C, Mosterd C, van Passel M W, Brouns S J (2012) CRISPR interference directs strand specific spacer acquisition PLoS One 7:e35888
Tamulaitis G, Kazlauskiene M, Manakova E, Venclovas C, Nwokeoji A O, et al. (2014) Programmable RNA shredding by the type III-A CRISPR-Cas system of Streptococcus thermophilus Mol Cell 56:506-517
Tang T H, Bachellerie J P, Rozhdestvensky T, Bortolin M L, Huber H, et al. (2002) Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus Proc Natl Acad Sci U S A 99:7536-7541
Tang T H, Polacek N, Zywicki M, Huber H, Brugger K, et al. (2005) Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus Mol Microbiol 55:469-481
Taylor D W, Zhu Y, Staals R H, Kornfeld J E, Shinkai A, et al. (2015) Structural biology. Structures of the CRISPR-Cmr complex reveal mode of RNA target positioning Science 348:581-585
Terns M P, Terns R M (2011) CRISPR-based adaptive immune systems Curr Opin Microbiol 14:321-327
Tsui T K, Li H (2015) Structure Principles of CRISPR-Cas Surveillance and Effector Complexes Annual Review of Biophysics, Vol 44 44:229-255
van der Oost J, Brouns S J (2009) RNAi: prokaryotes get in on the act Cell 139:863-865
Viswanathan P, Murphy K, Julien B, Garza A G, Kroos L (2007) Regulation of dev, an operon that includes genes essential for Myxococcus xanthus development and CRISPR-associated genes and repeats J Bacteriol 189:3738-3750
Wang R, Preamplume G, Terns M P, Terns R M, Li H (2011) Interaction of the Cas6 Riboendonuclease with CRISPR RNAs: Recognition and Cleavage Structure 19:257-264
Wei Y, Terns R M, Terns M P (2015) Cas9 function and host genome sampling in Type II-A CRISPR-Cas adaptation Genes Dev 29:356-361
Westra E R, Pul U, Heidrich N, Jore M M, Lundgren M, et al. (2010) H-NS-mediated repression of CRISPR-based immunity in Escherichia coli K12 can be relieved by the transcription activator LeuO Mol Microbiol 77:1380-1393
Westra E R, Semenova E, Datsenko K A, Jackson R N, Wiedenheft B, et al. (2013) Type I-E CRISPR-cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition PLoS Genet 9:e1003742
Westra E R, Swarts D C, Staals R H, Jore M M, Brouns S J, et al. (2012a) The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity Annu Rev Genet 46:311-339
Westra E R, van Erp P B, Kunne T, Wong S P, Staals R H, et al. (2012b) CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3 Mol Cell 46:595-605
Wiedenheft B, Lander G C, Zhou K, Jore M M, Brouns S J, et al. (2011a) Structures of the RNA-guided surveillance complex from a bacterial immune system Nature 477:486-489
Wiedenheft B, Sternberg S H, Doudna J A (2012) RNA-guided genetic silencing systems in bacteria and archaea Nature 482:331-338
Wiedenheft B, van Duijn E, Bultema J B, Waghmare S P, Zhou K, et al. (2011b) RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions Proc Natl Acad Sci U S A 108:10092-10097
Wright A V, Nunez J K, Doudna J A (2016) Biology and Applications of CRISPR Systems: Harnessing Nature's Toolbox for Genome Engineering Cell 164:29-44
Yamano T, Nishimasu H, Zetsche B, Hirano H, Slaymaker I M, et al. (2016) Crystal Structure of Cpf1 in Complex with Guide RNA and Target DNA Cell 165:949-962
Yang H, Gao P, Rajashankar K R, Patel D J (2016) PAM-Dependent Target DNA Recognition and Cleavage by C2c1 CRISPR-Cas Endonuclease Cell 167:1814-1828
Yosef I, Goren M G, Qimron U (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli Nucleic Acids Res 40:5569-5576
Zetsche B, Gootenberg J S, Abudayyeh O O, Slaymaker I M, Makarova K S, et al. (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system Cell 163:759-771
Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, et al. (2012) Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity Mol Cell 45:303-313
Zhang Y, Heidrich N, Ampattu B J, Gunderson C W, Seifert H S, et al. (2013) Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis Mol Cell 50:488-503
Zhao H, Sheng G, Wang J, Wang M, Bunkoczi G, et al. (2014) Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli Nature 515:147-150
Agari Y, Sakamoto K, Tamakoshi M, Oshima T, Kuramitsu S, et al. (2010) Transcription profile of Thermus thermophilus CRISPR systems after phage infection J Mol Biol 395:270-281
Al-Attar S, Westra E R, van der Oost J, Brouns S J (2011) Clustered regularly interspaced short palindromic repeats (CRISPRs): the hallmark of an ingenious antiviral defense mechanism in prokaryotes Biol Chem 392:277-289
Amitai G, Sorek R (2016) CRISPR-Cas adaptation: insights into the mechanism of action Nat Rev Microbiol 14:67-76
Arslan Z, Hermanns V, Wurm R, Wagner R, Pul U (2014) Detection and characterization of spacer integration intermediates in type I-E CRISPR-Cas system Nucleic Acids Res 42:7884-7893
Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes Science 315:1709-1712
Benda C, Ebert J, Scheltema R A, Schiller H B, Baumgartner M, et al. (2014) Structural model of a CRISPR RNA-silencing complex reveals the RNA-target cleavage activity in Cmr4 Mol Cell 56:43-54
Bhaya D, Davison M, Barrangou R (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation Annu Rev Genet 45:273-297
Brouns S J, Jore M M, Lundgren M, Westra E R, Slijkhuis R J, et al. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes Science 321:960-964
Carte J, Pfister N T, Compton M M, Terns R M, Terns M P (2010) Binding and cleavage of CRISPR RNA by Cas6 RNA 16:2181-2188
Carte J, Wang R, Li H, Terns R M, Terns M P (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes Genes Dev 22:3489-3496
Datsenko K A, Pougach K, Tikhonov A, Wanner B L, Severinov K, et al. (2012) Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system Nat Commun 3:945
Deltcheva E, Chylinski K, Sharma C M, Gonzales K, Chao Y, et al. (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III Nature 471:602-607
East-Seletsky A, O'Connell M R, Knight S C, Burstein D, Cate J H, et al. (2016) Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection Nature 538:270-273
Fineran P C, Charpentier E (2012) Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information Virology 434:202-209
Fonfara I, Richter H, Bratovic M, Le Rhun A, Charpentier E (2016) The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA Nature 532:517-521
Gao P, Yang H, Rajashankar K R, Huang Z, Patel D J (2016) Type V CRISPR-Cas Cpf1 endonuclease employs a unique mechanism for crRNA-mediated target DNA recognition Cell Res 26:901-913
Garneau J E, Dupuis M E, Villion M, Romero D A, Barrangou R, et al. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA Nature 468:67-71
Garside E L, Schellenberg M J, Gesner E M, Bonanno J B, Sauder J M, et al. (2012) Cas5d processes pre-crRNA and is a member of a larger family of CRISPR RNA endonucleases RNA 18:2020-2028
Gesner E M, Schellenberg M J, Garside E L, George M M, Macmillan A M (2011) Recognition and maturation of effector RNAs in a CRISPR interference pathway Nat Struct Mol Biol 18:688-692
Grissa I, Vergnaud G, Pourcel C (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats BMC Bioinformatics 8:172
Haft D H, Selengut J, Mongodin E F, Nelson K E (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes PLoS Comput Biol 1:e60
Hale C R, Zhao P, Olson S, Duff M O, Graveley B R, et al. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex Cell 139:945-956
Haurwitz R E, Jinek M, Wiedenheft B, Zhou K, Doudna J A (2010) Sequence- and structure-specific RNA processing by a CRISPR endonuclease Science 329:1355-1358
Haurwitz R E, Sternberg S H, Doudna J A (2012) Csy4 relies on an unusual catalytic dyad to position and cleave CRISPR RNA EMBO J 31:2824-2832
Hayes R P, Ke A (2015) One More Piece Down to Solve the III-A CRISPR Puzzle J Mol Biol 427:228-230
Hayes R P, Xiao Y, Ding F, van Erp P B, Rajashankar K, et al. (2016) Structural basis for promiscuous PAM recognition in type I-E Cascade from E. coli Nature 530:499-503
Hille F, Charpentier E (2016) CRISPR-Cas: biology, mechanisms and relevance Philos Trans R Soc Lond B Biol Sci 371
Hochstrasser M L, Doudna J A (2015) Cutting it close: CRISPR-associated endoribonuclease structure and function Trends Biochem Sci 40:58-66
Hooton S P, Connerton I F (2014) Campylobacter jejuni acquire new host-derived CRISPR spacers when in association with bacteriophages harboring a CRISPR-like Cas4 protein Front Microbiol 5:744
Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea Science 327:167-170
Hyman P, Abedon S T (2010) Bacteriophage host range and bacterial resistance Adv Appl Microbiol 70:217-248
Jackson R N, Golden S M, van Erp P B, Carter J, Westra E R, et al. (2014) Structural biology. Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli Science 345:1473-1479
Jackson S A, McKenzie R E, Fagerlund R D, Kieper S N, Fineran P C, et al. (2017) CRISPR-Cas: Adapting to change Science 356:eaal5056
Jansen R, Embden J D, Gaastra W, Schouls L M (2002) Identification of genes that are associated with DNA repeats in prokaryotes Mol Microbiol 43:1565-1575
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna J A, et al. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science 337:816-821
Jore M M, Lundgren M, van Duijn E, Bultema J B, Westra E R, et al. (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade Nat Struct Mol Biol 18:529-536
Karginov F V, Hannon G J (2010) The CRISPR system: small RNA-guided defense in bacteria and archaea Mol Cell 37:7-19
Koo Y, Ka D, Kim E J, Suh N, Bae E (2013) Conservation and variability in the structure and function of the Cas5d endoribonuclease in the CRISPR-mediated microbial immune system J Mol Biol 425:3799-3810
Kunin V, Sorek R, Hugenholtz P (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats Genome Biol 8:R61
Labrie S J, Samson J E, Moineau S (2010) Bacteriophage resistance mechanisms Nat Rev Microbiol 8:317-327
Lewis K M, Ke A (2017) Building the Class 2 CRISPR-Cas Arsenal Mol Cell 65:377-379
Li H (2015) Structural Principles of CRISPR RNA Processing Structure 23:13-20
Li M, Wang R, Zhao D, Xiang H (2014) Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process Nucleic Acids Res 42:2483-2492
Lillestol R K, Shah S A, Brugger K, Redder P, Phan H, et al. (2009) CRISPR families of the crenarchaeal genus Sulfolobus: bidirectional transcription and dynamic properties Mol Microbiol 72:259-272
Lintner N G, Kerou M, Brumfield S K, Graham S, Liu H, et al. (2011) Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE) J Biol Chem 286:21643-21656
Liu L, Chen P, Wang M, Li X, Wang J, et al. (2017a) C2c1-sgRNA Complex Structure Reveals RNA-Guided DNA Cleavage Mechanism Mol Cell 65:310-322
Liu L, Li X, Wang J, Wang M, Chen P, et al. (2017b) Two Distant Catalytic Sites Are Responsible for C2c2 RNase Activities Cell 168:121-134
Makarova K S, Wolf Y I, Alkhnbashi O S, Costa F, Shah S A, et al. (2015) An updated evolutionary classification of CRISPR-Cas systems Nat Rev Microbiol 13:722-736
Makarova K S, Zhang F, Koonin E V (2017a) SnapShot: Class 1 CRISPR-Cas Systems Cell 168:946-946
Makarova K S, Zhang F, Koonin E V (2017b) SnapShot: Class 2 CRISPR-Cas Systems Cell 168:328-328
Marraffini L A (2015) CRISPR-Cas immunity in prokaryotes Nature 526:55-61
Marraffini L A, Sontheimer E J (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA Science 322:1843-1845
Marraffini L A, Sontheimer E J (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea Nat Rev Genet 11:181-190
Mohanraju P, Makarova K S, Zetsche B, Zhang F, Koonin E V, et al. (2016) Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems Science 353:aad5147
Nam K H, Haitjema C, Liu X, Ding F, Wang H, et al. (2012) Cas5d protein processes pre-crRNA and assembles into a cascade-like interference complex in subtype I-C/Dvulg CRISPR-Cas system Structure 20:1574-1584
Nishimasu H, Nureki O (2016) Structures and mechanisms of CRISPR RNA-guided effector nucleases Curr Opin Struct Biol 43:68-78
Osawa T, Inanaga H, Sato C, Numata T (2015) Crystal structure of the CRISPR-Cas RNA silencing Cmr complex bound to a target analog Mol Cell 58:418-430
Perez-Rodriguez R, Haitjema C, Huang Q, Nam K H, Bernardis S, et al. (2011) Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli Mol Microbiol 79:584-599
Pettersen E F, Goddard T D, Huang C C, Couch G S, Greenblatt D M, et al. (2004) UCSF Chimera--a visualization system for exploratory research and analysis J Comput Chem 25:1605-1612
Pougach K, Semenova E, Bogdanova E, Datsenko K A, Djordjevic M, et al. (2010) Transcription, processing and function of CRISPR cassettes in Escherichia coli Mol Microbiol 77:1367-1379
Pul U, Wurm R, Arslan Z, Geissen R, Hofmann N, et al. (2010) Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS Mol Microbiol 75:1495-1512
Punetha A, Sivathanu R, Anand B (2014) Active site plasticity enables metal-dependent tuning of Cas5d nuclease activity in CRISPR-Cas type I-C system Nucleic Acids Res 42:3846-3856
Raines R T (1998) Ribonuclease A Chem Rev 98:1045-1066
Richter C, Dy R L, McKenzie R E, Watson B N, Taylor C, et al. (2014) Priming in the Type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bi-directionally from the primed protospacer Nucleic Acids Res 42:8516-8526
Rollins M F, Schuman J T, Paulus K, Bukhari H S, Wiedenheft B (2015) Mechanism of foreign DNA recognition by a CRISPR RNA-guided surveillance complex from Pseudomonas aeruginosa Nucleic Acids Res 43:2216-2222
Rouillon C, Zhou M, Zhang J, Politis A, Beilsten-Edmands V, et al. (2013) Structure of the CRISPR interference complex CSM reveals key similarities with cascade Mol Cell 52:124-134
Rousseau C, Gonnet M, Le Romancer M, Nicolas J (2009) CRISPI: a CRISPR interactive database Bioinformatics 25:3317-3318
Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, et al. (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli Nucleic Acids Res 39:9275-9282
Sashital D G, Jinek M, Doudna J A (2011) An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3 Nat Struct Mol Biol 18:680-687
Semenova E, Jore M M, Datsenko K A, Semenova A, Westra E R, et al. (2011) Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence Proc Natl Acad Sci U S A 108:10098-10103
Semenova E, Nagornykh M, Pyatnitskiy M, Artamonova, II, Severinov K (2009) Analysis of CRISPR system function in plant pathogen Xanthomonas oryzae FEMS Microbiol Lett 296:110-116
Shao Y, Li H (2013) Recognition and cleavage of a nonstructured CRISPR RNA by its processing endoribonuclease Cas6 Structure 21:385-393
Shao Y, Richter H, Sun S, Sharma K, Urlaub H, et al. (2016) A Non-Stem-Loop CRISPR RNA Is Processed by Dual Binding Cas6 Structure 24:547-554
Shmakov S, Smargon A, Scott D, Cox D, Pyzocha N, et al. (2017) Diversity and evolution of class 2 CRISPR-Cas systems Nat Rev Microbiol 15:169-182
Smargon A A, Cox D B, Pyzocha N K, Zheng K, Slaymaker I M, et al. (2017) Cas13b Is a Type VI-B CRISPR-Associated RNA-Guided RNase Differentially Regulated by Accessory Proteins Csx27 and Csx28 Mol Cell 65:618-630.e617
Spilman M, Cocozaki A, Hale C, Shao Y, Ramia N, et al. (2013) Structure of an RNA silencing complex of the CRISPR-Cas immune system Mol Cell 52:146-152
Staals R H, Zhu Y, Taylor D W, Kornfeld J E, Sharma K, et al. (2014) RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus Mol Cell 56:518-530
Sternberg S H, Haurwitz R E, Doudna J A (2012) Mechanism of substrate selection by a highly specific CRISPR endoribonuclease RNA 18:661-672
Sternberg S H, Richter H, Charpentier E, Qimron U (2016) Adaptation in CRISPR-Cas Systems Mol Cell 61:797-808
Swarts D C, Mosterd C, van Passel M W, Brouns S J (2012) CRISPR interference directs strand specific spacer acquisition PLoS One 7:e35888
Tamulaitis G, Kazlauskiene M, Manakova E, Venclovas C, Nwokeoji A O, et al. (2014) Programmable RNA shredding by the type III-A CRISPR-Cas system of Streptococcus thermophilus Mol Cell 56:506-517
Tang T H, Bachellerie J P, Rozhdestvensky T, Bortolin M L, Huber H, et al. (2002) Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus Proc Natl Acad Sci U S A 99:7536-7541
Tang T H, Polacek N, Zywicki M, Huber H, Brugger K, et al. (2005) Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus Mol Microbiol 55:469-481
Taylor D W, Zhu Y, Staals R H, Kornfeld J E, Shinkai A, et al. (2015) Structural biology. Structures of the CRISPR-Cmr complex reveal mode of RNA target positioning Science 348:581-585
Terns M P, Terns R M (2011) CRISPR-based adaptive immune systems Curr Opin Microbiol 14:321-327
Tsui T K, Li H (2015) Structure Principles of CRISPR-Cas Surveillance and Effector Complexes Annual Review of Biophysics, Vol 44 44:229-255
van der Oost J, Brouns S J (2009) RNAi: prokaryotes get in on the act Cell 139:863-865
Viswanathan P, Murphy K, Julien B, Garza A G, Kroos L (2007) Regulation of dev, an operon that includes genes essential for Myxococcus xanthus development and CRISPR-associated genes and repeats J Bacteriol 189:3738-3750
Wang R, Preamplume G, Terns M P, Terns R M, Li H (2011) Interaction of the Cas6 Riboendonuclease with CRISPR RNAs: Recognition and Cleavage Structure 19:257-264
Wei Y, Terns R M, Terns M P (2015) Cas9 function and host genome sampling in Type II-A CRISPR-Cas adaptation Genes Dev 29:356-361
Westra E R, Pul U, Heidrich N, Jore M M, Lundgren M, et al. (2010) H-NS-mediated repression of CRISPR-based immunity in Escherichia coli K12 can be relieved by the transcription activator LeuO Mol Microbiol 77:1380-1393
Westra E R, Semenova E, Datsenko K A, Jackson R N, Wiedenheft B, et al. (2013) Type I-E CRISPR-cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition PLoS Genet 9:e1003742
Westra E R, Swarts D C, Staals R H, Jore M M, Brouns S J, et al. (2012a) The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity Annu Rev Genet 46:311-339
Westra E R, van Erp P B, Kunne T, Wong S P, Staals R H, et al. (2012b) CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3 Mol Cell 46:595-605
Wiedenheft B, Lander G C, Zhou K, Jore M M, Brouns S J, et al. (2011a) Structures of the RNA-guided surveillance complex from a bacterial immune system Nature 477:486-489
Wiedenheft B, Sternberg S H, Doudna J A (2012) RNA-guided genetic silencing systems in bacteria and archaea Nature 482:331-338
Wiedenheft B, van Duijn E, Bultema J B, Waghmare S P, Zhou K, et al. (2011b) RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions Proc Natl Acad Sci U S A 108:10092-10097
Wright A V, Nunez J K, Doudna J A (2016) Biology and Applications of CRISPR Systems: Harnessing Nature's Toolbox for Genome Engineering Cell 164:29-44
Yamano T, Nishimasu H, Zetsche B, Hirano H, Slaymaker I M, et al. (2016) Crystal Structure of Cpf1 in Complex with Guide RNA and Target DNA Cell 165:949-962
Yang H, Gao P, Rajashankar K R, Patel D J (2016) PAM-Dependent Target DNA Recognition and Cleavage by C2c1 CRISPR-Cas Endonuclease Cell 167:1814-1828
Yosef I, Goren M G, Qimron U (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli Nucleic Acids Res 40:5569-5576
Zetsche B, Gootenberg J S, Abudayyeh O O, Slaymaker I M, Makarova K S, et al. (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system Cell 163:759-771
Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, et al. (2012) Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity Mol Cell 45:303-313
Zhang Y, Heidrich N, Ampattu B J, Gunderson C W, Seifert H S, et al. (2013) Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis Mol Cell 50:488-503
Zhao H, Sheng G, Wang J, Wang M, Bunkoczi G, et al. (2014) Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli Nature 515:147-150
Published
2018-02-19
Issue
Section
Special Section on RNA Biology
Copyright (c) 2018 Proceedings of the Indian National Science Academy
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
