Register      Login
Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
Shopping Cart: ( empty )
You are here: Home > Journals > CH > CH14319
RESEARCH FRONT
Contents Vol 67(12)

RNA and RNA–Protein Complex Crystallography and its Challenges

Janine K. Flores A B , James L. Walshe A B and Sandro F. Ataide A C
+ Author Affiliations
- Author Affiliations

A School of Molecular Bioscience, University of Sydney, Sydney, NSW 2006, Australia.

B These authors contributed equally to this paper.

C Corresponding author. Email: sandro.ataide@sydney.edu.au




Janine Flores received her B.Sc. in biochemistry and psychology from the University of Sydney in 2012. She completed her B.Sc. (Honours) in biochemistry in 2013 in the Ataide laboratory, where her research focused on determining the crystal structure of the protein and RNA components of the eukaryotic signal recognition particle (SRP). Currently, Janine is a Ph.D. candidate at the Ataide laboratory focusing on the structural characterisation of ribonucleoprotein complexes.


James Walshe received his B.Sc. degree from the University of Western Australia (UWA) in 2010. He completed his B.Sc. (Honours) in biochemistry in 2011, working in Alice Vrielink's laboratory (UWA) on metal binding sites found in the crystal structure of N. meningitidis Lipopolysaccharide transferase A. He is currently a Ph.D. candidate at the Ataide laboratory (University of Sydney) investigating the structural interactions of ribonucleoproteins that associate with non-coding RNAs.


Dr Sandro Ataide received his B.Sc. in chemistry in 1999 from UNICAMP (Brazil) and obtained his M.Sc. in biochemistry from the University of Sao Paulo (Brazil) in 2001. He was awarded his Ph.D. by The Ohio State University (USA) in 2006. Aiming to gain better experience in the RNA and crystallography field, he conducted research on the complex signal recognition particle (SRP) and ribosome while working as a post-doctorate researcher at Jennifer Doudna's laboratory at UC Berkeley (USA) and Dr Nenad Ban's laboratory at ETH Zurich (Switzerland). He joined the University of Sydney as a lecturer in 2012 to continue his work on structural and molecular characterisation of RNA and RNA-protein complexes.

Australian Journal of Chemistry 67(12) 1741-1750 https://doi.org/10.1071/CH14319
Submitted: 20 May 2014  Accepted: 24 June 2014   Published: 19 August 2014

Abstract

RNA biology has changed completely in the past decade with the discovery of non-coding RNAs. Unfortunately, obtaining mechanistic information about these RNAs alone or in cellular complexes with proteins has been a major problem. X-ray crystallography of RNA and RNA–protein complexes has suffered from the major problems encountered in preparing and purifying them in large quantity. Here, we review the available techniques and methods in vitro and in vivo used to prepare and purify RNA and RNA–protein complex for crystallographic studies. We also discuss the future directions necessary to explore the vast number of RNA species waiting for their atomic-resolution structure to be determined.


References

[1]  B. Dey, S. Thukral, S. Krishnan, M. Chakrobarty, S. Gupta, C. Manghani, V. Rani, Mol. Cell. Biochem. 2012, 365, 279.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtVejtrk%3D&md5=2b23453aa9edc5fcf90bd16c43f43d22CAS | 22399265PubMed |

[2]  A. Perederina, A. Krasilnikov, in Bacterial Regulatory RNA, Methods in Molecular Biology Series (Ed. K. C. Keiler) 2012, Vol. 905, pp. 123–143 (Humana Press: Totowa, NJ).

[3]  E. Obayashi, C. Oubridge, D. Pomeranz Krummel, K. Nagai, Methods Mol. Biol. 2007, 363, 259.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmslCmsA%3D%3D&md5=4a2c1e83de1f4785fa1f60b71432a69cCAS | 17272846PubMed |

[4]  S. Cusack, Curr. Opin. Struct. Biol. 1999, 9, 66.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvVSktLs%3D&md5=a29b6c773d617a0558437f290f9b40e4CAS | 10400475PubMed |

[5]  J. L. Linpinsel, G. L. Conn, Methods Mol. Biol. 2013, 941, 43.
         | Crossref | GoogleScholarGoogle Scholar |

[6]  J. F. Milligan, D. R. Groebe, G. W. Witherell, O. C. Uhlenbeck, Nucleic Acids Res. 1987, 15, 8783.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXntFKhuw%3D%3D&md5=0fad42828f67be14037c146fe171894bCAS | 3684574PubMed |

[7]  H. Schurer, K. Lang, J. Schuster, M. Morl, Nucleic Acids Res. 2002, 30, 56e.
         | Crossref | GoogleScholarGoogle Scholar |

[8]  S. C. Walker, J. M. Avis, G. L. Conn, Nucleic Acids Res. 2003, 31, 82e.
         | Crossref | GoogleScholarGoogle Scholar |

[9]  A. R. Ferre-D’Amare, J. A. Doudna, Nucleic Acids Res. 1996, 24, 977.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xhs1Cktrw%3D&md5=f8deb2de25605ffe9a1b307c1f9dc8c8CAS | 8600468PubMed |

[10]  S. R. Price, N. Ito, C. Oubridge, J. M. Avis, K. Nagai, J. Mol. Biol. 1995, 249, 398.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtlWrs7w%3D&md5=f43a8c82aae3d7892ad64d7022a42adbCAS | 7540213PubMed |

[11]  See pp. 365–370 in: J. A. Doudna, Ribozyme Protocols 1997 (Springer: Berlin).

[12]  A. Petrov, T. Wu, E. V. Puglisi, J. D. Puglisi, Methods Enzymol. 2013, 530, 315.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGgt7jK&md5=45622bd9e064c1d05c1c71a0968d59d4CAS | 24034329PubMed |

[13]  O. C. Uhlenbeck, RNA 1995, 1, 4.
         | 1:CAS:528:DyaK2MXkvFemtbc%3D&md5=94db5f324fbab60462ceada6c1294ffaCAS | 7489487PubMed |

[14]  N. J. Reiter, A. Osterman, A. Torres-Larios, K. K. Swinger, T. Pan, A. Mondragon, Nature 2010, 468, 784.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVWmurvE&md5=f4ed816cc519bd0fc23fd50a2bf1fb2fCAS | 21076397PubMed |

[15]  L. Cunningham, K. Kittikamron, Y. Lu, Nucleic Acids Res. 1996, 24, 3647.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmt1ajurk%3D&md5=c4f034cba09ebf6f306a73da11f804aeCAS | 8836197PubMed |

[16]  C. Lu, F. Ding, A. Chowdhury, V. Pradhan, J. Tomsic, W. M. Holmes, T. M. Henkin, A. Ke, J. Mol. Biol. 2010, 404, 803.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVGiur%2FO&md5=ebe030cc899a593a0ac8dd45fbe5400eCAS | 20951706PubMed |

[17]  F. Wincott, A. DiRenzo, C. Shaffer, S. Grimm, D. Tracz, C. Workman, D. Sweedler, C. Gonzalez, S. Scaringe, N. Usman, Nucleic Acids Res. 1995, 23, 2677.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXns1aksbo%3D&md5=a80706ee1053c28d489887789260adc1CAS | 7544462PubMed |

[18]  C. Wilms, P. Wollenzien, Anal. Biochem. 1994, 221, 204.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFamtLo%3D&md5=6007b1ff1b73f4e10b3b3073c7633007CAS | 7527188PubMed |

[19]  T. P. Shields, E. Mollova, L. Ste. Marie, M. R. Hansen, A. Pardi, RNA 1999, 5, 1259.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvVSmt7c%3D&md5=61bf743956ff68cfb2ad38e0704220f6CAS | 10496226PubMed |

[20]  Z. Huang, S. Jayaseelan, J. Hebert, H. Seo, L. Niu, Anal. Biochem. 2013, 435, 35.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVKhs7g%3D&md5=38474839300ea6d61d007be5dafe45d8CAS | 23274387PubMed |

[21]  J. Sheng, J. Gan, A. S. Soares, J. Salon, Z. Huang, Nucleic Acids Res. 2013, 41, 10476.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2lsbzF&md5=5225cb51bf248f8299562bb856859b64CAS | 24013566PubMed |

[22]  I. Kim, S. A. McKenna, E. Viani Puglisi, J. D. Puglisi, RNA 2006, 13, 289.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVCitA%3D%3D&md5=23a0a39c0b271717d1908f0b04ed843fCAS | 17179067PubMed |

[23]  P. J. Lukavsky, J. D. Puglisi, RNA 2004, 10, 889.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1GntLw%3D&md5=5b7df4f4183aec297dfbf2126f358afbCAS | 15100443PubMed |

[24]  J. Koubek, K. F. Lin, Y. R. Chen, R. P. Cheng, J. J. T. Huang, RNA 2013, 19, 1449.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFeksrnO&md5=06fed1793488dad0dc5ef7ca0480f7feCAS | 23929938PubMed |

[25]  L. E. Easton, Y. Shibata, P. J. Lukavsky, RNA 2010, 16, 647.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVams7Y%3D&md5=8ec93e65ac86ca707b8778f8db7973e9CAS | 20100812PubMed |

[26]  A. Y. Keel, L. E. Easton, P. J. Lukavsky, J. S. Kieft, Methods Enzymol. 2009, 469, 3.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtlSmtg%3D%3D&md5=87582153a94defb96612ffbbe3f6777cCAS | 20946782PubMed |

[27]  E. P. Booy, H. Meng, S. A. McKenna, Methods Mol. Biol. 2013, 941, 69.
         | Crossref | GoogleScholarGoogle Scholar |

[28]  R. T. Batey, Curr. Opin. Struct. Biol. 2014, 26, 1.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ylt7%2FL&md5=479825a58c941f9c6d0dc00ebea147ebCAS |

[29]  J. C. Grigg, Y. Chen, F. J. Grundy, T. M. Henkin, L. Pollack, A. Ke, Proc. Natl. Acad. Sci. USA 2013, 110, 7240.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXos1OisLk%3D&md5=43a629f97ff5e3adfd3ed6c5e98a6a65CAS | 23589841PubMed |

[30]  Y. Itoh, S. Chiba, S.-i. Sekine, S. Yokoyama, Nucleic Acids Res. 2009, 37, 6259.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlWlt7jJ&md5=47e3913d4a3653136ccf82be8b2c6a84CAS | 19692584PubMed |

[31]  A. V. Kazantsev, A. A. Krivenko, N. R. Pace, RNA 2009, 15, 266.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Oju74%3D&md5=c379a3108025a0372851e28240587658CAS | 19095619PubMed |

[32]  L. Huang, A. Serganov, D. J. Patel, Mol. Cell 2010, 40, 774.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFGhu7vK&md5=7acf2c219ac45bcda5cf511ba38655d7CAS | 21145485PubMed |

[33]  H.-K. Cheong, E. Hwang, C. Lee, B.-S. Choi, C. Cheong, Nucleic Acids Res. 2004, 32, e84.
         | Crossref | GoogleScholarGoogle Scholar | 15199176PubMed |

[34]  H.-K. Cheong, E. Hwang, C. Cheong, Methods Mol. Biol. 2013, 941, 113.
         | Crossref | GoogleScholarGoogle Scholar |

[35]  R. T. Batey, J. S. Kieft, RNA 2007, 13, 1384.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos1Ghsbk%3D&md5=5d3eeee7ea813df6db407332f59c141dCAS | 17548432PubMed |

[36]  G. Di Tomasso, P. Dagenais, A. Desjardins, A. Rompre-Brodeur, V. Delfosse, P. Legault, Methods Mol. Biol. 2013, 941, 137.
         | Crossref | GoogleScholarGoogle Scholar |

[37]  G. Di Tomasso, P. Lampron, P. Dagenais, J. G. Omichinski, P. Legault, Nucleic Acids Res. 2011, 39, e18.
         | Crossref | GoogleScholarGoogle Scholar | 21071425PubMed |

[38]  A. Salvail-Lacoste, G. Di Tomasso, B. L. Piette, P. Legault, RNA 2013, 19, 1003.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVegtLfO&md5=67ac41186a4fba95fc6a32e38a0f3632CAS | 23657939PubMed |

[39]  D. H. Turner, N. Sugimoto, S. M. Freier, Annu. Rev. Biophys. Biophys. Chem. 1988, 17, 167.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkvVyhsbw%3D&md5=f6f9cab915f19d6a33915cdb13e90ddeCAS | 2456074PubMed |

[40]  L. Ponchon, G. Beauvais, S. Nonin-Lecomte, F. Dardel, Nat. Protoc. 2009, 4, 947.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsFWqu7o%3D&md5=10dd23939d8a7a01e754b3df13832f99CAS | 19478810PubMed |

[41]  L. Ponchon, F. Dardel, Nat. Methods 2007, 4, 571.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVCitLo%3D&md5=6a12c3223a6256ea6bb416d95f23ef84CAS | 17558412PubMed |

[42]  L. Ponchon, M. Catala, B. Seijo, M. El Khouri, F. Dardel, S. Nonin-Lecomte, C. Tisne, Nucleic Acids Res. 2013, 41, e150.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGmtrnJ&md5=b9fd6b7d77939f09a1e240941f87a377CAS | 23804766PubMed |

[43]  C. Tisné, M. Rigourd, R. Marquet, C. Ehresmann, F. Dardel, RNA 2000, 6, 1403.
         | Crossref | GoogleScholarGoogle Scholar | 11073216PubMed |

[44]  F. H. Nelissen, E. H. Leunissen, L. van de Laar, M. Tessari, H. A. Heus, S. S. Wijmenga, Nucleic Acids Res. 2012, 40, e102.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFSlsL7M&md5=7d6e87c0838be9e3e127ce4f7e064caeCAS | 22457065PubMed |

[45]  L. Ponchon, F. Dardel, Methods 2011, 54, 267.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVynt7g%3D&md5=0cc5df4ff1bb370d2ed44c8c0ea195e3CAS | 21320602PubMed |

[46]  A. R. Ferré-D’Amaré, K. Zhou, J. A. Doudna, J. Mol. Biol. 1998, 279, 621.
         | Crossref | GoogleScholarGoogle Scholar | 9641982PubMed |

[47]  A. McPherson, J. Cryst. Growth 1991, 110, 1.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXitVKis78%3D&md5=1d76e698c72ca1ccceebc20052f58511CAS |

[48]  A. McPherson, Crystallization of Biological Macromolecules 1999 (Cold Spring Harbor Laboratory Press: New York, NY).

[49]  J. A. Doudna, C. Grosshans, A. Gooding, C. E. Kundrot, Proc. Natl. Acad. Sci. USA 1993, 90, 7829.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslKls7s%3D&md5=53e6a4fae20ae676dba23549642dc420CAS | 8356090PubMed |

[50]  J. Jancarik, S.-H. Kim, J. Appl. Cryst. 1991, 24, 409.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltlWgtrk%3D&md5=1ca4f1fbdd1c4a73502085c937799746CAS |

[51]  W. G. Scott, J. T. Finch, R. Grenfell, J. Fogg, T. Smith, M. J. Gait, A. Klug, J. Mol. Biol. 1995, 250, 327.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvFynsb0%3D&md5=eeda43cf4383e7f5e21c4e9476f1eb06CAS | 7608978PubMed |

[52]  C. Carter, J. Biol. Chem. 1979, 254, 12219.
         | 1:CAS:528:DyaL3cXitFyg&md5=a88f98d61715199a66260d9ac7a6f9feCAS | 500706PubMed |

[53]  M. S. Jurica, L. J. Licklider, S. R. Gygi, N. Grigorieff, M. J. Moore, RNA 2002, 8, 426.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsFarsLk%3D&md5=14d1c5eae655625091d561664564ccb2CAS | 11991638PubMed |

[54]  A. R. Ferré‐D’Amaré, J. A. Doudna, Curr. Protoc. Nucleic Acid Chem. 2001, 7, 1.

[55]  F. E. Reyes, A. D. Garst, R. T. Batey, in Methods in Enzymology (Ed. H. Daniel) 2009, Vol. 469, pp. 119–139 (Academic Press: New York, NY).

[56]  D. W. Celander, T. R. Cech, Biochemistry 1990, 29, 1355.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXpsVSruw%3D%3D&md5=5e58ab8d459a32421b4945e7f2e31a97CAS | 2110477PubMed |

[57]  C. Ehresmann, F. Baudin, M. Mougel, P. Romby, J.-P. Ebel, B. Ehresmann, Nucleic Acids Res. 1987, 15, 9109.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlt1WmsQ%3D%3D&md5=f8c1fd1a809432eb99a3285f58cb3689CAS | 2446263PubMed |

[58]  E. J. Merino, K. A. Wilkinson, J. L. Coughlan, K. M. Weeks, J. Am. Chem. Soc. 2005, 127, 4223.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVSitLc%3D&md5=e9ebd3b2df488971762ec5db711e6e07CAS | 15783204PubMed |

[59]  See pp. 53-67 in: E. E. Regulski, R. R. Breaker, Post-Transcriptional Gene Regulation 2008 (Springer: Berlin).

[60]  H. W. Pley, K. M. Flaherty, D. B. McKay, Nature 1994, 372, 111.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitVGhurk%3D&md5=1b58515bfa67ef72e95b249e0e6f8c1fCAS | 7526219PubMed |

[61]  L. A. Coonrod, J. R. Lohman, J. A. Berglund, Biochemistry 2012, 51, 8330.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVejs7%2FP&md5=3244a83b7a5cf58567210c1145d2c33dCAS | 23025897PubMed |

[62]  J. L. Childs-Disney, I. Yildirim, H. Park, J. R. Lohman, L. Guan, T. Tran, P. Sarkar, G. C. Schatz, M. D. Disney, ACS Chem. Biol. 2014, 9, 538.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2ku7zK&md5=4f1741f5f059c46336e4865abaf2d455CAS | 24341895PubMed |

[63]  A. R. Ferré-D’Amaré, K. Zhou, J. A. Doudna, Nature 1998, 395, 567.
         | Crossref | GoogleScholarGoogle Scholar | 9783582PubMed |

[64]  K. B. Hall, W. T. Stump, Nucleic Acids Res. 1992, 20, 4283.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhtF2gsLo%3D&md5=0b40e84b22cb20b2574eb5e5cd1dddf1CAS | 1508720PubMed |

[65]  C. Oubridge, N. Ito, P. R. Evans, C.-H. Teo, K. Nagai, Nature 1994, 372, 432.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisVGqsbg%3D&md5=d1ac97d13670728be79b849ee28df7cfCAS | 7984237PubMed |

[66]  A. R. Ferré-D’Amaré, Methods 2010, 52, 159.
         | Crossref | GoogleScholarGoogle Scholar | 20554048PubMed |

[67]  P. B. Rupert, A. R. Ferré-D’Amaré, Nature 2001, 410, 780.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVemurw%3D&md5=b9f58ebc1eb33a51782bf1649b545515CAS | 11298439PubMed |

[68]  J. C. Cochrane, S. V. Lipchock, S. A. Strobel, Chem. Biol. 2007, 14, 97.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVaqtr4%3D&md5=41dccf8f84703f1ed6af50e5f074175eCAS | 17196404PubMed |

[69]  H. Xiao, H. Murakami, H. Suga, A. R. Ferre-D’Amare, Nature 2008, 454, 358.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosFCqtLc%3D&md5=123163990dd0eda8b443b61e1c9b5491CAS | 18548004PubMed |

[70]  S. Uysal, V. Vásquez, V. Tereshko, K. Esaki, F. A. Fellouse, S. S. Sidhu, S. Koide, E. Perozo, A. Kossiakoff, Proc. Natl. Acad. Sci. USA 2009, 106, 6644.
         | 1:CAS:528:DC%2BD1MXlsVOrurk%3D&md5=73e7e779f4cbe1fb47c4206581b3e4fcCAS | 19346472PubMed |

[71]  Y. Koldobskaya, E. M. Duguid, D. M. Shechner, N. B. Suslov, J. Ye, S. S. Sidhu, D. P. Bartel, S. Koide, A. A. Kossiakoff, J. A. Piccirilli, Nat. Struct. Mol. Biol. 2011, 18, 100.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFGgsbfM&md5=4fe06a5e4a49e49f2b03355643d33695CAS | 21151117PubMed |

[72]  J.-D. Ye, V. Tereshko, J. K. Frederiksen, A. Koide, F. A. Fellouse, S. S. Sidhu, S. Koide, A. A. Kossiakoff, J. A. Piccirilli, Proc. Natl. Acad. Sci. USA 2008, 105, 82.
         | 1:CAS:528:DC%2BD1cXpvV2rsA%3D%3D&md5=50e436cb7c06c50a63a1f2c3631c0309CAS | 18162543PubMed |

[73]  D. M. Shechner, R. A. Grant, S. C. Bagby, Y. Koldobskaya, J. A. Piccirilli, D. P. Bartel, Science 2009, 326, 1271.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVKhtbfI&md5=fba48bada28e43cb493f504a03dea1b3CAS | 19965478PubMed |

[74]  F. Baneyx, Curr. Opin. Biotechnol. 1999, 10, 411.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmslGisL8%3D&md5=03c7feb45f90317e92e486196337411cCAS | 10508629PubMed |

[75]  J.-C. Janson, Protein Purification: Principles, High Resolution Methods and Applications 2012 (John Wiley & Sons: Hoboken, NJ).

[76]  A. Ke, J. A. Doudna, Methods 2004, 34, 408.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFCrsL0%3D&md5=1d56005f24ff1405987f1d3973f5c67bCAS | 15325657PubMed |

[77]  R. T. Batey, M. B. Sagar, J. A. Doudna, J. Mol. Biol. 2001, 307, 229.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslSnsLw%3D&md5=f30c2e3a9cf442e0d8cf11c8f75585ddCAS | 11243816PubMed |

[78]  F. Y. Siu, R. J. Spanggord, J. A. Doudna, RNA 2007, 13, 240.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVKms74%3D&md5=ff7d39341fd718ce6578006c6613a16fCAS | 17164479PubMed |

[79]  S. F. Ataide, N. Schmitz, K. Shen, A. Ke, S.-o. Shan, J. A. Doudna, N. Ban, Science 2011, 331, 881.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFSjtLg%3D&md5=d72ab63718faa039b6bf608cfc5ff793CAS | 21330537PubMed |

[80]  H. Nishimasu, F. A. Ran, P. D. Hsu, S. Konermann, S. I. Shehata, N. Dohmae, R. Ishitani, F. Zhang, O. Nureki, Cell 2014, 156, 935.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFCiu7Y%3D&md5=452f157324cea5f7831b7c232fe1d29cCAS | 24529477PubMed |

[81]  D. L. Makino, M. Baumgartner, E. Conti, Nature 2013, 495, 70.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFCht7w%3D&md5=615a46be85b19469ed999b1faa1f6d10CAS | 23376952PubMed |

[82]  J. C. Greimann, C. D. Lima, in Methods in Enzymology (Eds E. M. Lynne, K. Megerditch) 2008, Vol. 448, pp. 185–210 (Academic Press: New York, NY).

[83]  G. G. Pickett, D. S. Peabody, Nucleic Acids Res. 1993, 21, 4621.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmt1Wns7o%3D&md5=48613bea0081f80db9899330576e02e8CAS | 8233800PubMed |

[84]  F. Schluenzen, A. Tocilj, R. Zarivach, J. Harms, M. Gluehmann, D. Janell, A. Bashan, H. Bartels, I. Agmon, F. Franceschi, A. Yonath, Cell 2000, 102, 615.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsFWitLw%3D&md5=065e6fae70dfb503ed3511b831c1a275CAS | 11007480PubMed |

[85]  B. T. Wimberly, D. E. Brodersen, W. M. Clemons, R. J. Morgan-Warren, A. P. Carter, C. Vonrhein, T. Hartsch, V. Ramakrishnan, Nature 2000, 407, 327.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFyktb4%3D&md5=ead46bde1aa74786539f6400e9ca05ccCAS | 11014182PubMed |

[86]  N. Ban, P. Nissen, J. Hansen, P. B. Moore, T. A. Steitz, Science 2000, 289, 905.
         | Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvgslCgsA%3D%3D&md5=80873847f19d7662e7996797903f3d9fCAS | 10937989PubMed |

[87]  A. Ben-Shem, L. Jenner, G. Yusupova, M. Yusupov, Science 2010, 330, 1203.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVGrtr7P&md5=299ad9f89dc7c96efadeeed62502df3dCAS | 21109664PubMed |

[88]  J. Rabl, M. Leibundgut, S. F. Ataide, A. Haag, N. Ban, Science 2011, 331, 730.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yrs7k%3D&md5=24d81f607a1b5fa65ac1a1eb6fab79ccCAS | 21205638PubMed |

[89]  S. Klinge, F. Voigts-Hoffmann, M. Leibundgut, S. Arpagaus, N. Ban, Science 2011, 334, 941.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVGktL%2FI&md5=40a2dd702713dfd9fdeda1db4b539f98CAS | 22052974PubMed |

[90]  K. Kruger, P. J. Grabowski, A. J. Zaug, J. Sands, D. E. Gottschling, T. R. Cech, Cell 1982, 31, 147.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXht1eguw%3D%3D&md5=e6305e646ad168e5813dc6ec025e92f6CAS | 6297745PubMed |

[91]  E. Birney, J. A. Stamatoyannopoulos, A. Dutta, R. Guigó, T. R. Gingeras, E. H. Margulies, et al. Nature 2007, 447, 799.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXms1Wjsb0%3D&md5=9638d60ead661b00d285289f6cd1fc21CAS | 17571346PubMed |

[92]  J. Cheng, P. Kapranov, J. Drenkow, S. Dike, S. Brubaker, S. Patel, J. Long, D. Stern, H. Tammana, G. Helt, V. Sementchenko, A. Piccolboni, S. Bekiranov, D. K. Bailey, M. Ganesh, S. Ghosh, I. Bell, D. S. Gerhard, T. R. Gingeras, Science 2005, 308, 1149.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1Sltrk%3D&md5=943ae4a7592bb15df674fdffd4809917CAS | 15790807PubMed |

[93]  E. M. Landau, J. P. Rosenbusch, Proc. Natl. Acad. Sci. USA 1996, 93, 14532.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsVKrsb8%3D&md5=e314c8b84a1c6662b6535079c1a6035eCAS | 8962086PubMed |