Essential Structural and Functional Roles of the Cmr4 Subunit in RNA Cleavage by the Cmr CRISPR-Cas Complex

Cell Reports

Volumn 9, Issue 5, 2014, Pages 1610-1617

  Ramia, Nancy F ^a   Spilman, Michael ^a   Tang, Li ^a   Shao, Yaming ^a   Elmore, Joshua ^b   Hale, Caryn ^b   Cocozaki, Alexis ^a   Bhattacharya, Nilakshee ^a   Terns, Rebecca M ^b   Terns, Michael P ^b   Li, Hong ^a   Stagg, Scott M ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; PROTEIN CMR4; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; CARRIER PROTEIN; PROTEIN BINDING; PROTEIN SUBUNIT;

ARTICLE; CMR GENE; CONTROLLED STUDY; CRISPR CAS SYSTEM; GENE; GENE REARRANGEMENT; NONHUMAN; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; PROTEIN SUBUNIT; PYROCOCCUS FURIOSUS; RNA CLEAVAGE; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SUBSTITUTION; ARCHAEAL PROTEINS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-ASSOCIATED PROTEINS; CRYSTALLOGRAPHY, X-RAY; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PYROCOCCUS FURIOSUS; RNA CLEAVAGE;

EID: 84915825854     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.11.007     Document Type: Article

References (35)

1. Barrangou R., Marraffini L.A. CRISPR-Cas systems: Prokaryotes upgrade to adaptive immunity. Mol. Cell 2014, 54:234-244.
2. Benda C., Ebert J., Scheltema R.A., Schiller H.B., Baumgärtner M., Bonneau F., Mann M., Conti E. Structural Model of a CRISPR RNA-Silencing Complex Reveals the RNA-Target Cleavage Activity in Cmr4. Mol. Cell 2014, 56:43-54.
3. Brouns S.J., Jore M.M., Lundgren M., Westra E.R., Slijkhuis R.J., Snijders A.P., Dickman M.J., Makarova K.S., Koonin E.V., van der Oost J. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 2008, 321:960-964.
4. Egelman E.H. Reconstruction of helical filaments and tubes. Methods Enzymol. 2010, 482:167-183.
5. Ferré-D'Amaré A.R., Scott W.G. Small self-cleaving ribozymes. Cold Spring Harb. Perspect. Biol. 2010, 2:a003574.
6. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J.Struct. Biol. 1996, 116:190-199.
7. Gasiunas G., Barrangou R., Horvath P., Siksnys V. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. USA 2012, 109:E2579-E2586.
8. Hale C.R., Zhao P., Olson S., Duff M.O., Graveley B.R., Wells L., Terns R.M., Terns M.P. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 2009, 139:945-956.
9. Hale C.R., Majumdar S., Elmore J., Pfister N., Compton M., Olson S., Resch A.M., Glover C.V., Graveley B.R., Terns R.M., Terns M.P. Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol. Cell 2012, 45:292-302.
10. Hale C.R., Cocozaki A., Li H., Terns R.M., Terns M.P. Target RNA capture and cleavage by the Cmr type III-B CRISPR-Cas effector complex. Genes Dev. 2014, 28:2432-2443.
11. Hatoum-Aslan A., Maniv I., Samai P., Marraffini L.A. Genetic characterization of antiplasmid immunity through a type III-A CRISPR-Cas system. J.Bacteriol. 2014, 196:310-317.
12. Hrle A., Su A.A., Ebert J., Benda C., Randau L., Conti E. Structure and RNA-binding properties of the type III-A CRISPR-associated protein Csm3. RNA Biol. 2013, 10:1670-1678.
13. Jackson R.N., Golden S.M., van Erp P.B., Carter J., Westra E.R., Brouns S.J., van der Oost J., Terwilliger T.C., Read R.J., Wiedenheft B. Structural biology. Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli. Science 2014, 345:1473-1479.
14. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337:816-821.
15. Lilley D.M. Catalysis by the nucleolytic ribozymes. Biochem. Soc. Trans. 2011, 39:641-646.
16. Lintner N.G., Kerou M., Brumfield S.K., Graham S., Liu H., Naismith J.H., Sdano M., Peng N., She Q., Copié V., et al. Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE). J.Biol. Chem. 2011, 286:21643-21656.
17. Ludtke S.J., Baldwin P.R., Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J.Struct. Biol. 1999, 128:82-97.
18. Makarova K.S., Haft D.H., Barrangou R., Brouns S.J., Charpentier E., Horvath P., Moineau S., Mojica F.J., Wolf Y.I., Yakunin A.F., et al. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 2011, 9:467-477.
19. Makarova K.S., Aravind L., Wolf Y.I., Koonin E.V. Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol. Direct 2011, 6:38.
20. Makarova K.S., Wolf Y.I., Koonin E.V. The basic building blocks and evolution of CRISPR-CAS systems. Biochem. Soc. Trans. 2013, 41:1392-1400.
21. Mulepati S., Héroux A., Bailey S. Structural biology. Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science 2014, 345:1479-1484.
22. Park J.H., Sun J., Park S.Y., Hwang H.J., Park M.Y., Shin M., Kim J.S. Crystal structure of Cmr5 from Pyrococcus furiosus and its functional implications. FEBS Lett. 2013, 587:562-568.
23. Rouillon C., Zhou M., Zhang J., Politis A., Beilsten-Edmands V., Cannone G., Graham S., Robinson C.V., Spagnolo L., White M.F. Structure of the CRISPR interference complex CSM reveals key similarities with cascade. Mol. Cell 2013, 52:124-134.
24. Scheres S.H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J.Struct. Biol. 2012, 180:519-530.
25. Sinkunas T., Gasiunas G., Waghmare S.P., Dickman M.J., Barrangou R., Horvath P., Siksnys V. Invitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J. 2013, 32:385-394.
26. Sousa D., Grigorieff N. Ab initio resolution measurement for single particle structures. J.Struct. Biol. 2007, 157:201-210.
27. Spilman M., Cocozaki A., Hale C., Shao Y., Ramia N., Terns R., Terns M., Li H., Stagg S. Structure of an RNA silencing complex of the CRISPR-Cas immune system. Mol. Cell 2013, 52:146-152.
28. Staals R.H., Agari Y., Maki-Yonekura S., Zhu Y., Taylor D.W., van Duijn E., Barendregt A., Vlot M., Koehorst J.J., Sakamoto K., et al. Structure and activity of the RNA-targeting Type III-B CRISPR-Cas complex of Thermus thermophilus. Mol. Cell 2013, 52:135-145.
29. Suloway C., Pulokas J., Fellmann D., Cheng A., Guerra F., Quispe J., Stagg S., Potter C.S., Carragher B. Automated molecular microscopy: the new Leginon system. J.Struct. Biol. 2005, 151:41-60.
30. Terns M.P., Terns R.M. CRISPR-based adaptive immune systems. Curr. Opin. Microbiol. 2011, 14:321-327.
31. van der Oost J., Westra E.R., Jackson R.N., Wiedenheft B. Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat. Rev. Microbiol. 2014, 12:479-492.
32. Wiedenheft B., Lander G.C., Zhou K., Jore M.M., Brouns S.J., van der Oost J., Doudna J.A., Nogales E. Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 2011, 477:486-489.
33. Wiedenheft B., van Duijn E., Bultema J.B., Waghmare S.P., Zhou K., Barendregt A., Westphal W., Heck A.J.R., Boekema E.J., Dickman M.J., Doudna J.A. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl. Acad. Sci. USA 2011, 108:10092-10097.
34. Zhang J., Rouillon C., Kerou M., Reeks J., Brugger K., Graham S., Reimann J., Cannone G., Liu H., Albers S.V., et al. Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol. Cell 2012, 45:303-313.
35. Zhao H., Sheng G., Wang J., Wang M., Bunkoczi G., Gong W., Wei Z., Wang Y. Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli. Nature 2014, 515:147-150.