Combining native MS approaches to decipher archaeal box H/ACA ribonucleoprotein particle structure and activity

Proteomics

Volumn 15, Issue 16, 2015, Pages 2851-2861

  Saliou, Jean Michel ^a,b,d   Manival, Xavier ^c   Tillault, Anne Sophie ^c   Atmanene, Cédric ^a,b   Bobo, Claude ^c,e   Branlant, Christiane ^c   Van Dorsselaer, Alain ^a,b   Charpentier, Bruno ^c   Cianférani, Sarah ^a,b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^c UNIVERSITÉ DE LORRAINE   (France)

^d UNIV LILLE   (France)

^e Institut de Biochimie et Genetique Cellulaires   (France)

Author keywords

Ion mobility mass spectrometry; Native mass spectrometry; Ribonucleoprotein particle; Systems biology

Indexed keywords

5 FLUORO 6 HYDROXY PSEUDOURIDINE; ARCHAEAL BOX H ACA RIBONUCLEOPROTEIN PARTICLE; FLUOROURIDINE; GUIDE RNA; PSEUDOURIDINE; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; ENZYME DEGRADATION; IN VITRO STUDY; ISOMERIZATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; CHEMISTRY; METABOLISM; PROCEDURES; SYSTEMS BIOLOGY;

ARCHAEA;

ARCHAEAL PROTEINS; MASS SPECTROMETRY; RIBONUCLEOPROTEINS, SMALL NUCLEAR; SYSTEMS BIOLOGY;

EID: 84938750505     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400529     Document Type: Article

References (63)

1. Kiss, T., Fayet-Lebaron, E., Jady, B. E., Box H/ACA small ribonucleoproteins. Mol. Cell 2010, 37, 597-606.
2. Fayet-Lebaron, E., Atzorn, V., Henry, Y., Kiss, T., 18S rRNA processing requires base pairings of snR30 H/ACA snoRNA to eukaryote-specific 18S sequences. EMBO J. 2009, 28, 1260-1270.
3. Mitchell, J. R., Cheng, J., Collins, K., A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3' end. Mol. Cell. Biol. 1999, 19, 567-576.
4. Senger, B., Auxilien, S., Englisch, U., Cramer, F., Fasiolo, F., The modified wobble base inosine in yeast tRNAIle is a positive determinant for aminoacylation by isoleucyl-tRNA synthetase. Biochemistry 1997, 36, 8269-8275.
5. Ishida, K., Kunibayashi, T., Tomikawa, C., Ochi, A. et al., Pseudouridine at position 55 in tRNA controls the contents of other modified nucleotides for low-temperature adaptation in the extreme-thermophilic eubacterium Thermus thermophilus. Nucleic Acids Res. 2011, 39, 2304-2318.
6. Badis, G., Fromont-Racine, M., Jacquier, A., A snoRNA that guides the two most conserved pseudouridine modifications within rRNA confers a growth advantage in yeast. RNA 2003, 9, 771-779.
7. Ejby, M., Sorensen, M. A., Pedersen, S., Pseudouridylation of helix 69 of 23S rRNA is necessary for an effective translation termination. Proc. Natl. Acad. Sci. USA 2007, 104, 19410-19415.
8. King, T. H., Liu, B., McCully, R. R., Fournier, M. J., Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol. Cell 2003, 11, 425-435.
9. Newby, M. I., Greenbaum, N. L., Sculpting of the spliceosomal branch site recognition motif by a conserved pseudouridine. Nat. Struct. Biol. 2002, 9, 958-965.
10. Liu, N., Pan, T., Transl Res. 2015, Jan;165(1), 28-35.
11. Omer, A. D., Ziesche, S., Decatur, W. A., Fournier, M. J., Dennis, P. P., RNA-modifying machines in archaea. Mol. Microbiol. 2003, 48, 617-629.
12. Baker, D. L., Youssef, O. A., Chastkofsky, M. I., Dy, D. A. et al., RNA-guided RNA modification: functional organization of the archaeal H/ACA RNP. Genes Dev. 2005, 19, 1238-1248.
13. Charpentier, B., Muller, S., Branlant, C., Reconstitution of archaeal H/ACA small ribonucleoprotein complexes active in pseudouridylation. Nucleic Acids Res. 2005, 33, 3133-3144.
14. Manival, X., Charron, C., Fourmann, J. B., Godard, F. et al., Crystal structure determination and site-directed mutagenesis of the Pyrococcus abyssi aCBF5-aNOP10 complex reveal crucial roles of the C-terminal domains of both proteins in H/ACA sRNP activity. Nucleic Acids Res. 2006, 34, 826-839.
15. Rashid, R., Liang, B., Baker, D. L., Youssef, O. A. et al., Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita. Mol. Cell 2006, 21, 249-260.
16. Li, L., Ye, K., Crystal structure of an H/ACA box ribonucleoprotein particle. Nature 2006, 443, 302-307.
17. Duan, J., Li, L., Lu, J., Wang, W., Ye, K., Structural mechanism of substrate RNA recruitment in H/ACA RNA-guided pseudouridine synthase. Mol. Cell 2009, 34, 427-439.
18. Hamma, T., Ferre-D'Amare, A. R., The box H/ACA ribonucleoprotein complex: interplay of RNA and protein structures in post-transcriptional RNA modification. J. Biol. Chem. 2010, 285, 805-809.
19. Liang, B., Zhou, J., Kahen, E., Terns, R. M. et al., Structure of a functional ribonucleoprotein pseudouridine synthase bound to a substrate RNA. Nat. Struct. Mol. Biol. 2009, 16, 740-746.
20. Fourmann, J. B., Tillault, A. S., Blaud, M., Leclerc, F. et al., Comparative study of two box H/ACA ribonucleoprotein pseudouridine-synthases: relation between conformational dynamics of the guide RNA, enzyme assembly and activity. PLoS One 2013, 8, e70313.
21. Hamma, T., Ferre-D'Amare, A. R., Pseudouridine synthases. Chem. Biol. 2006, 13, 1125-1135.
22. Huang, L., Pookanjanatavip, M., Gu, X., Santi, D. V., A conserved aspartate of tRNA pseudouridine synthase is essential for activity and a probable nucleophilic catalyst. Biochemistry 1998, 37, 344-351.
23. Gu, X., Liu, Y., Santi, D. V., The mechanism of pseudouridine synthase I as deduced from its interaction with 5-fluorouracil-tRNA. Proc. Natl. Acad. Sci. USA 1999, 96, 14270-14275.
24. McDonald, M. K., Miracco, E. J., Chen, J., Xie, Y., Mueller, E. G., The handling of the mechanistic probe 5-fluorouridine by the pseudouridine synthase TruA and its consistency with the handling of the same probe by the pseudouridine synthases TruB and RluA. Biochemistry 2011, 50, 426-436.
25. Hoang, C., Ferre-D'Amare, A. R., Cocrystal structure of a tRNA Psi55 pseudouridine synthase: nucleotide flipping by an RNA-modifying enzyme. Cell 2001, 107, 929-939.
26. Hoang, C., Chen, J., Vizthum, C. A., Kandel, J. M. et al., Crystal structure of pseudouridine synthase RluA: indirect sequence readout through protein-induced RNA structure. Mol. Cell 2006, 24, 535-545.
27. Spedaliere, C. J., Mueller, E. G., Not all pseudouridine synthases are potently inhibited by RNA containing 5-fluorouridine. RNA 2004, 10, 192-199.
28. Benesch, J. L., Ruotolo, B. T., Simmons, D. A., Robinson, C. V., Protein complexes in the gas phase: technology for structural genomics and proteomics. Chem. Rev. 2007, 107, 3544-3567.
29. Heck, A. J., Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 2008, 5, 927-933.
30. Zhou, M., Robinson, C. V., When proteomics meets structural biology. Trends Biochem. Sci. 2010, 35, 522-529.
31. Akashi, S., Watanabe, M., Heddle, J. G., Unzai, S. et al., RNA and protein complexes of trp RNA-binding attenuation protein characterized by mass spectrometry. Anal. Chem. 2009, 81, 2218-2226.
32. Callaghan, A. J., Grossmann, J. G., Redko, Y. U., Ilag, L. L. et al., Quaternary structure and catalytic activity of the Escherichia coli ribonuclease E amino-terminal catalytic domain. Biochemistry 2003, 42, 13848-13855.
33. Ruotolo, B. T., Giles, K., Campuzano, I., Sandercock, A. M. et al., Evidence for macromolecular protein rings in the absence of bulk water. Science 2005, 310, 1658-1661.
34. Uetrecht, C., Rose, R. J., van Duijn, E., Lorenzen, K., Heck, A. J., Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 2010, 39, 1633-1655.
35. Lane, L. A., Fernandez-Tornero, C., Zhou, M., Morgner, N. et al., Mass spectrometry reveals stable modules in holo and apo RNA polymerases I and III. Structure 2011, 19, 90-100.
36. Pukala, T. L., Ruotolo, B. T., Zhou, M., Politis, A. et al., Subunit architecture of multiprotein assemblies determined using restraints from gas-phase measurements. Structure 2009, 17, 1235-1243.
37. van Duijn, E., Barbu, I. M., Barendregt, A., Jore, M. M. et al., Native tandem and ion mobility mass spectrometry highlight structural and modular similarities in clustered-regularly-interspaced shot-palindromic-repeats (CRISPR)-associated protein complexes from Escherichia coli and Pseudomonas aeruginosa. Mol. Cell. Proteomics 2012, 11, 1430-1441.
38. Politis, A., Park, A. Y., Hall, Z., Ruotolo, B. T., Robinson, C. V., Integrative modelling coupled with ion mobility mass spectrometry reveals structural features of the clamp loader in complex with single-stranded DNA binding protein. J. Mol. Biol. 2013, 425, 4790-4801.
39. Ma, C., Piccinin, S., Fabris, S., Rigid- and polarizable-ion potentials for modeling Ru-polyoxometalate catalysts for water oxidation. Acta Chim. Slov. 2014, 61, 302-307.
40. Charpentier, B., Fourmann, J. B., Branlant, C., Reconstitution of archaeal H/ACA sRNPs and test of their activity. Methods Enzymol. 2007, 425, 389-405.
41. Bush, M. F., Hall, Z., Giles, K., Hoyes, J. et al., Collision cross sections of proteins and their complexes: a calibration framework and database for gas-phase structural biology. Anal. Chem. 2010, 82, 9557-9565.
42. Shvartsburg, A. A., Jarrold, M. F., An exact hard-spheres scattering model for the mobilities of polyatomic ions. Chem. Phys. Lett. 1996, 261, 86-91.
43. Mesleh, M. F., Hunter, J. M., Shvartsburg, A. A., Schatz, G. C., Jarrold, M. F., Structural information from ion mobility measurements:effects of the long-range potential. J. Phys. Chem. 1996, 100, 16082-16086.
44. Li, S., Duan, J., Li, D., Yang, B. et al., Reconstitution and structural analysis of the yeast box H/ACA RNA-guided pseudouridine synthase. Genes Dev. 2011, 25, 2409-2421.
45. Yang, X., Duan, J., Li, S., Wang, P. et al., Kinetic and thermodynamic characterization of the reaction pathway of box H/ACA RNA-guided pseudouridine formation. Nucleic Acids Res. 2012, 40, 10925-10936.
46. Kaddis, C. S., Loo, J. A., Native protein MS and ion mobility large flying proteins with ESI. Anal. Chem. 2007, 79, 1778-1784.
47. Ruotolo, B. T., Benesch, J. L., Sandercock, A. M., Hyung, S. J., Robinson, C. V., Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc. 2008, 3, 1139-1152.
48. Bowers, M. T., Kemper, P. R., von Helden, G., van Koppen, P. A., Gas-phase ion chromatography: transition metal state selection and carbon cluster formation. Science 1993, 260, 1446-1451.
49. Charron, C., Manival, X., Clery, A., Senty-Segault, V. et al., The archaeal sRNA binding protein L7Ae has a 3D structure very similar to that of its eukaryal counterpart while having a broader RNA-binding specificity. J. Mol. Biol. 2004, 342, 757-773.
50. Charron, C., Manival, X., Charpentier, B., Branlant, C., Aubry, A., Purification, crystallization and preliminary X-ray diffraction data of L7Ae sRNP core protein from Pyrococcus abyssi. Acta Crystallogr. D 2004, 60, 122-124.
51. Bhuiya, M. W., Suryadi, J., Zhou, Z., Brown, B. A., 2nd, Structure of the Aeropyrum pernix L7Ae multifunctional protein and insight into its extreme thermostability. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2013, 69, 979-988.
52. Suryadi, J., Tran, E. J., Maxwell, E. S., Brown, B. A., 2nd, The crystal structure of the Methanocaldococcus jannaschii multifunctional L7Ae RNA-binding protein reveals an induced-fit interaction with the box C/D RNAs. Biochemistry 2005, 44, 9657-9672.
53. Hamma, T., Reichow, S. L., Varani, G., Ferre-D'Amare, A. R., The Cbf5-Nop10 complex is a molecular bracket that organizes box H/ACA RNPs. Nat. Struct. Mol. Biol. 2005, 12, 1101-1107.
54. Miracco, E. J., Mueller, E. G., The products of 5-fluorouridine by the action of the pseudouridine synthase TruB disfavor one mechanism and suggest another. J. Am. Chem. Soc. 2011, 133, 11826-11829.
55. Wright, J. R., Keffer-Wilkes, L. C., Dobing, S. R., Kothe, U., Pre-steady-state kinetic analysis of the three Escherichia coli pseudouridine synthases TruB, TruA, and RluA reveals uniformly slow catalysis. RNA 2011, 17, 2074-2084.
56. Benesch, J. L., Ruotolo, B. T., Mass spectrometry: come of age for structural and dynamical biology. Curr. Opin. Struct. Biol. 2011, 21, 641-649.
57. Hyung, S. J., Ruotolo, B. T., Integrating mass spectrometry of intact protein complexes into structural proteomics. Proteomics 2012, 12, 1547-1564.
58. Zhang, N., Gordiyenko, Y., Joly, N., Lawton, E. et al., Subunit dynamics and nucleotide-dependent asymmetry of an AAA(+) transcription complex. J. Mol. Biol. 2014, 426, 71-83.
59. Tian, Y., Simanshu, D. K., Ascano, M., Diaz-Avalos, R. et al., Multimeric assembly and biochemical characterization of the Trax-translin endonuclease complex. Nat. Struct. Mol. Biol. 2011, 18, 658-664.
60. Park, A. Y., Jergic, S., Politis, A., Ruotolo, B. T. et al., A single subunit directs the assembly of the Escherichia coli DNA sliding clamp loader. Structure 2010, 18, 285-292.
61. Muller, S., Charpentier, B., Branlant, C., Leclerc, F., A dedicated computational approach for the identification of archaeal H/ACA sRNAs. Methods Enzymol. 2007, 425, 355-387.
62. Muller, S., Leclerc, F., Behm-Ansmant, I., Fourmann, J. B. et al., Combined in silico and experimental identification of the Pyrococcus abyssi H/ACA sRNAs and their target sites in ribosomal RNAs. Nucleic Acids Res. 2008, 36, 2459-2475.
63. Spenkuch, F., Hinze, G., Kellner, S., Kreutz, C. et al., Dye label interference with RNA modification reveals 5-fluorouridine as non-covalent inhibitor. Nucleic Acids Res. 2014, 42, 12735-12745.