Efficient segmental isotope labeling of multi-domain proteins using Sortase A

Journal of Biomolecular NMR

Volumn 63, Issue 1, 2015, Pages 1-8

  Freiburger, Lee ^a,b   Sonntag, Miriam ^a,b   Hennig, Janosch ^a,b   Li, Jian ^c   Zou, Peijian ^a,b,c   Sattler, Michael ^a,b,c  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c Chinese Academy of Sciences   (China)

Author keywords

Multi domain proteins; Protein expression; Protein ligation; Segmental isotope labeling; Sortase A

Indexed keywords

PEPTIDE FRAGMENT; SORTASE; SORTASE A; UNCLASSIFIED DRUG; AMINOACYLTRANSFERASE; BACTERIAL PROTEIN; CYSTEINE PROTEINASE;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME PURIFICATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; ISOTOPE LABELING; MOLECULAR INTERACTION; MOLECULAR WEIGHT; NEUTRON SCATTERING; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTON NUCLEAR MAGNETIC RESONANCE; STAPHYLOCOCCUS AUREUS; TRANS SPLICING; ENZYMOLOGY; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES; PROTEIN TERTIARY STRUCTURE;

AMINOACYLTRANSFERASES; BACTERIAL PROTEINS; CYSTEINE ENDOPEPTIDASES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ISOTOPE LABELING; PROTEIN STRUCTURE, TERTIARY; PROTON MAGNETIC RESONANCE SPECTROSCOPY; STAPHYLOCOCCUS AUREUS;

EID: 84942366316     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-015-9981-0     Document Type: Article

References (31)

1. Chen I, Dorr BM, Liu DR (2011) A general strategy for the evolution of bond-forming enzymes using yeast display. Proc Natl Acad Sci USA 108:11399-11404. doi: 10.1073/pnas.1101046108
2. Clow F, Fraser J, Proft T (2008) Immobilization of proteins to biacore sensor chips using Staphylococcus aureus sortase A. Biotechnol Lett 30:1603-1607. doi: 10.1007/s10529-008-9718-1
3. Cowburn D, Shekhtman A, Xu R, Ottesen JJ, Muir TW (2004) Segmental isotopic labeling for structural biological applications of NMR. Methods Mol Biol 278:47-56. doi: 10.1385/1-59259-809-9:047
4. 15N multidimensional NMR to study the structure and dynamics of proteins. Annu Rev Biophys Biomol Struct 27:357-406. doi: 10.1146/annurev.biophys.27.1.357
5. Gobl C, Madl T, Simon B, Sattler M (2014) NMR approaches for structural analysis of multidomain proteins and complexes in solution. Prog Nucl Magn Reson Spectrosc 80:26-63. doi: 10.1016/j.pnmrs.2014.05.003
6. Guimaraes CP, Witte MD, Theile CS, Bozkurt G, Kundrat L, Blom AEM, Ploegh HL (2013) Site-specific C-terminal and internal loop labeling of proteins using sortase-mediated reactions. Nat Protoc 8:1787-1799. doi: 10.1038/nprot.2013.101
7. Hennig J, Wang I, Sonntag M, Gabel F, Sattler M (2013) Combining NMR and small angle X-ray and neutron scattering in the structural analysis of a ternary protein-RNA complex. J Biomol NMR 56:17-30. doi: 10.1007/s10858-013-9719-9
8. Hennig J et al (2014) Structural basis for the assembly of the Sxl-Unr translation regulatory complex. Nature 515:287-290. doi: 10.1038/nature13693
9. Kobashigawa Y, Kumeta H, Ogura K, Inagaki F (2009) Attachment of an NMR-invisible solubility enhancement tag using a sortase-mediated protein ligation method. J Biomol NMR 43:145-150. doi: 10.1007/s10858-008-9296-5
10. Lapinaite A, Simon B, Skjaerven L, Rakwalska-Bange M, Gabel F, Carlomagno T (2013) The structure of the box C/D enzyme reveals regulation of RNA methylation. Nature 502:519-523. doi: 10.1038/nature12581
11. Levary DA, Parthasarathy R, Boder ET, Ackerman ME (2011) Protein-protein fusion catalyzed by sortase A. PLoS One 6:e18342. doi: 10.1371/journal.pone.0018342
12. Lorenz OR et al (2014) Modulation of the Hsp90 chaperone cycle by a stringent client protein. Mol Cell 53:941-953. doi: 10.1016/j.molcel.2014.02.003
13. Madl T, Gabel F, Sattler M (2011) NMR and small-angle scattering-based structural analysis of protein complexes in solution. J Struct Biol 173:472-482. doi: 10.1016/j.jsb.2010.11.004
14. Mao H, Hart SA, Schink A, Pollok BA (2004) Sortase-mediated protein ligation: a new method for protein engineering. J Am Chem Soc 126:2670-2671. doi: 10.1021/ja039915e
15. Mazmanian SK, Liu G, Hung TT, Schneewind O (1999) Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285:760-763. doi: 10.1126/science.285.5428.760
16. Muona M, Aranko AS, Raulinaitis V, Iwai H (2010) Segmental isotopic labeling of multi-domain and fusion proteins by protein trans-splicing in vivo and in vitro. Nat Protoc 5:574-587. doi: 10.1038/nprot.2009.240
17. Pervushin K, Riek R, Wider G, Wuthrich K (1997) Attenuated T-2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci USA 94:12366-12371. doi: 10.1073/pnas.94.23.12366
18. Ramakrishnan V (1986) Distribution of protein and RNA in the 30S ribosomal subunit. Science 231:1562-1564. doi: 10.1126/science.3513310
19. Refaei M et al (2011) Observing selected domains in multi-domain proteins via sortase-mediated ligation and NMR spectroscopy. J Biomol NMR 49:3-7. doi: 10.1007/s10858-010-9464-2
20. Riek R, Pervushin K, Wuthrich K (2000) TROSY and CRINEPT: NMR with large molecular and supramolecular structures in solution. Trends Biochem Sci 25:462-468. doi: 10.1016/S0968-0004(00)01665-0
21. Riek R, Fiaux J, Bertelsen EB, Horwich AL, Wuthrich K (2002) Solution NMR techniques for large molecular and supramolecular structures. J Am Chem Soc 124:12144-12153. doi: 10.1021/ja026763z
22. Sattler M, Fesik SW (1996) Use of deuterium labeling in NMR: overcoming a sizeable problem. Structure 4:1245-1249. doi: 10.1016/S0969-2126(96)00133-5
23. Skrisovska L, Schubert M, Allain FHT (2010) Recent advances in segmental isotope labeling of proteins: NMR applications to large proteins and glycoproteins. J Biomol NMR 46:51-65. doi: 10.1007/s10858-009-9362-7
24. Sprangers R, Velyvis A, Kay LE (2007) Solution NMR of supramolecular complexes: providing new insights into function. Nat Methods 4:697-703. doi: 10.1038/nmeth1080
25. Ton-That H, Mazmanian SK, Faull KF, Schneewind O (2000) Anchoring of surface proteins to the cell wall of Staphylococcus aureus. Sortase catalyzed in vitro transpeptidation reaction using LPXTG peptide and NH(2)-Gly(3) substrates. J Biol Chem 275:9876-9881. doi: 10.1074/jbc.275.13.9876
26. Tugarinov V, Hwang PM, Kay LE (2004) Nuclear magnetic resonance spectroscopy of high-molecular-weight proteins. Annu Rev Biochem 73:107-146. doi: 10.1146/annurev.biochem.73.011303.074004
27. Tugarinov V, Kanelis V, Kay LE (2006) Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat Protoc 1:749-754. doi: 10.1038/nprot.2006.101
28. Wang I, Hennig J, Jagtap PK, Sonntag M, Valcarcel J, Sattler M (2014) Structure, dynamics and RNA binding of the multi-domain splicing factor TIA-1. Nucleic Acids Res 42:5949-5966. doi: 10.1093/nar/gku193
29. Williamson DJ, Webb ME, Turnbull WB (2014) Depsipeptide substrates for sortase-mediated N-terminal protein ligation. Nat Protoc 9:253-262. doi: 10.1038/nprot.2014.003
30. Xu R, Ayers B, Cowburn D, Muir TW (1999) Chemical ligation of folded recombinant proteins: segmental isotopic labeling of domains for NMR studies. Proc Natl Acad Sci USA 96:388-393. doi: 10.1073/pnas.96.2.388
31. Zuger S, Iwai H (2005) Intein-based biosynthetic incorporation of unlabeled protein tags into isotopically labeled proteins for NMR studies. Nat Biotechnol 23:736-740. doi: 10.1038/nbt1097