Cys-Ph-TAHA: A lanthanide binding tag for RDC and PCS enhanced protein NMR

Journal of Biomolecular NMR

Volumn 51, Issue 3, 2011, Pages 329-337

  Peters, Fabian ^a   Maestre Martinez, Mitcheell ^a   Leonov, Andrei ^a   Kovačič, Lidija ^b,c   Becker, Stefan ^a   Boelens, Rolf ^b   Griesinger, Christian ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

^c JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

Lanthanides; Paramagnetic NMR; Pseudocontact shifts; Residual dipolar couplings

Indexed keywords

CYSTEINE DERIVATIVE; CYSTEINYL PHENYL TRIAMINOHEXAACETATE; DNA; LANTHANIDE; PHENYL GROUP; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BIOCHEMISTRY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; METAL BINDING; MOLECULAR INTERACTION; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; PSEUDOCONTACT SHIFT; RESIDUAL DIPOLAR COUPLING; STEREOCHEMISTRY; SYNTHESIS; THERMOSTABILITY;

ACETIC ACIDS; BINDING SITES; CYSTEINE; LANTHANOID SERIES ELEMENTS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS; UBIQUITIN;

EID: 80755175871     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-011-9560-y     Document Type: Article

References (52)

1. M Allegrozzi I Bertini MBL Janik G Lee YM Liu C Luchinat 2000 Lanthanide- induced pseudocontact shifts for solution structure refinements of macromolecules in shells up to 40 Å from the metal ion J Am Chem Soc 122 4154 4161 10.1021/ja993691b (Pubitemid 30304849)
2. MC Alpoim AM Urbano CFGC Geraldes JA Peters 1992 Determination of the number of inner-sphere water molecules in lanthanide(III) polyaminocarboxylate complexes J Chem Soc Dalton Trans 1992 463 467 10.1039/dt9920000463
3. E Arslantas PM Smith-Jones G Ritter RR Schmidt 2004 TAME-Hex A - a novel bifunctional chelating agent for radioimmunoimaging Eur J Org Chem 19 3979 3984 10.1002/ejoc.200400224
4. K Barthelmes A Reynolds E Peizach HRA Jonker N Denunzio K Allen B Imperiali H Schwalbe 2011 Engineering encodable lanthanide-binding tags (LBTs) into loop regions of proteins J Am Chem Soc 133 808 819
5. I Bertini C Luchinat 1999 New applications of paramagnetic NMR in chemical biology Curr Opin Chem Biol 3 145 151 10.1016/S1367-5931(99)80026-X (Pubitemid 29145780)
6. I Bertini MBL Janik YM Lee C Luchinat A Rosato 2001 Magnetic susceptibility tensor anisotropies for a lanthanide ion series in a fixed protein matrix J Am Chem Soc 123 4181 4188 10.1021/ja0028626 (Pubitemid 32899436)
7. I Bertini C Luchinat G Parigi 2002 Magnetic susceptibility in paramagnetic NMR Prog Nucl Magn Res Spec 40 249 273 10.1016/S0079-6565(02)00002- X (Pubitemid 34544213)
8. I Bertini I Gelis N Katsaros C Luchinat A Provenzani 2003 Tuning the affinity for lanthanides of calcium binding proteins Biochemistry 42 8011 8021 10.1021/bi034494z (Pubitemid 36807718)
9. G Cornilescu JL Marquardt M Ottiger A Bax 1998 Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase J Am Chem Soc 120 6836 6837 10.1021/ja9812610 (Pubitemid 28347351)
10. RN De Jong MA Daniels R Kaptein GE Folkers 2006 Enzyme free cloning for high throughput gene cloning and expression J Struct Funct Genom 7 109 118 10.1007/s10969-006-9014-z (Pubitemid 47050873)
11. F Delaglio S Grzesiek GW Vuister G Zhu J Pfeifer A Bax 1995 NMR-Pipe: a multidimensional spectral processing system based on UNIX pipes J Biomol NMR 6 277 293 10.1007/BF00197809
12. Fenwick RB, Esteban-Martin S, Richter B, Lee D, Walter KFA, Milovanovic D, Becker S, Lakomek NA, Griesinger C, Salvatella X (2011) Weak long-range correlated motions in a surface patch of ubiquitin involved in molecular recognition. J Am Chem Soc 133:10336-10339
13. V Gaponenko AS Altieri J Li A Byrd 2002 Breaking symmetry in the structure determination of (large) symmetric protein dimers J Biomol NMR 24 143 148 10.1023/A:1020948529076 (Pubitemid 35414677)
14. Goddard TD, Kneller DG (2008) Sparky 3. University of California, San Francisco
15. P Haberz F Rodriguez-Castañeda J Junker S Becker A Leonov C Griesinger 2006 Two new chiral EDTA-based metal chelates for weak alignment of proteins in solution Org Lett 8 1275 1278 10.1021/ol053049o (Pubitemid 43587419)
16. D Häussinger JR Huang S Grzesiek 2009 DOTA-M8: An extremely rigid, high- affinity lanthanide chelating tag for PCS NMR spectroscopy J Am Chem Soc 131 14761 14767 10.1021/ja903233w
17. JC Hus D Marion M Blackledge 2000 De novo determination of protein structure by NMR using orientational and long-range order restraints J Mol Biol 298 927 936 10.1006/jmbi.2000.3714
18. T Ikegami L Verdier P Sakhaii S Grimme B Pescatore K Saxena KM Fiebig C Griesinger 2004 Novel techniques for weak alignment of proteins in solution using chemical tags coordinating lanthanide ions J Biomol NMR 29 339 349 10.1023/B:JNMR.0000032611.72827.de (Pubitemid 38864832)
19. PHJ Keizers JF Desreux M Overhand M Ubbink 2007 Increased paramagnetic effect of a lanthanide protein probe by two-point attachment J Am Chem Soc 129 9292 9293 10.1021/ja0725201 (Pubitemid 47218791)
20. PHJ Keizers A Saragliadis Y Hiruma M Overhand M Ubbink 2008 Design, synthesis, and evaluation of a lanthanide chelating protein probe: CLaNP-5 yields predictable paramagnetic effects independent of environment J Am Chem Soc 130 14802 14812 10.1021/ja8054832
21. Keller RLJ (2004) Optimizing the process of nuclear magnetic resonance spectrum analysis and computer aided resonance assignment. Dissertation, Swiss Federal Institute of Technology, Zürich
22. F Kramer MV Deshmukh H Kessler SJ Glaser 2004 Residual dipolar coupling constants: an elementary derivation of key equations Concepts Magn Res Part A 21 10 21 10.1002/cmr.a.20003 (Pubitemid 40646231)
23. NA Lakomek T Carlomagno S Becker C Griesinger J Meiler 2006 A thorough dynamic interpretation of residual dipolar couplings in ubiquitin J Biomol NMR 34 101 115 10.1007/s10858-005-5686-0
24. NA Lakomek OF Lange KFA Walter C Farès D Egger P Lunkenheimer J Meiler H Grubmüller S Becker BL de Groot C Griesinger 2008 Residual dipolar couplings as a tool to study molecular recognition of ubiquitin Biochem Soc Trans 36 1433 1437 10.1042/BST0361433
25. OF Lange NA Lakomek C Farès GF Schröder KFA Walter S Becker J Meiler H Grubmüller C Griesinger BL de Groot 2008 Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution Science 320 1471 1475 2008Sci...320.1471L 10.1126/science.1157092 (Pubitemid 351929422)
26. GA Lazar JR Desjarlais TM Handel 1997 De novo design of the hydrophobic core of ubiquitin Protein Sci 6 1167 1178 10.1002/pro.5560060605 (Pubitemid 27260151)
27. A Leonov B Voigt F Rodriguez-Castañeda P Sakhaii C Griesinger 2005 Convenient synthesis of multifunctional EDTA-based chiral metal chelates substituted with an S-mesylcysteine Chemistry 11 3342 3348 10.1002/chem. 200400907 (Pubitemid 40750992)
28. B Man XC Su H Liang S Simonsen T Huber BA Messerle G Otting 2010 3- Mercapto-2, 6-pyridinedicarboxylic acid: a small lanthanide-binding tag for protein studies by NMR spectroscopy Chem Eur J 16 3827 3832 10.1002/chem. 200902904
29. LJ Martin MJ Hähnke M Nitz J Wöhnert NR Silvaggi KN Allen H Schwalbe B Imperiali 2007 Double-lanthanide-binding tags: design, photophysical properties, and NMR applications J Am Chem Soc 129 7106 7113 10.1021/ja070480v (Pubitemid 46903275)
30. BR McGarvey 1979 Temperature dependence of the pseudocontact shift in lanthanide shift reagents J Magn Res 33 445 455
31. M Nitz M Sherawat KJ Franz E Peisach KN Allen B Imperiali 2004 Structural origin of the high affinity of a chemically evolved lanthanide-binding peptide Angew Chem Int Ed 43 3682 3685 10.1002/anie.200460028 (Pubitemid 39257518)
32. M Ottiger F Delaglio A Bax 1998 Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra J Magn Reson 131 373 378 1998JMagR.131..373O 10.1006/jmre.1998.1361 (Pubitemid 128450579)
33. G Otting 2008 Prospects for lanthanides in structural biology by NMR J Biomol NMR 42 1 9 10.1007/s10858-008-9256-0
34. G Pintacuda A Moshref A Leonchiks A Sharipo G Otting 2004 Site-specific labelling with a metal chelator for protein-structure refinement J Biomol NMR 29 351 361 10.1023/B:JNMR.0000032610.17058.fe (Pubitemid 38864833)
35. M Prudêncio J Rohovec JA Peters E Tocheva MJ Boulanger MEP Murphy HJ Hupkes W Kosters A Impagliazzo M Ubbink 2004 A caged lanthanide complex as a paramagnetic shift agent for protein NMR Chem Eur J 10 3252 3260 10.1002/chem.200306019
36. F Rodriguez-Castañeda P Haberz A Leonov C Griesinger 2006 Paramagnetic tagging of diamagnetic proteins for solution NMR Magn Reson Chem 44 10 16 10.1002/mrc.1811 (Pubitemid 44090386)
37. J Romanuka H van den Bulke R Kaptein R Boelens GE Folkers 2009 Novel strategies to overcome expression problems encountered with toxic proteins: application to the production of Lac repressor proteins for NMR studies Protein Expr Purif 67 104 112 10.1016/j.pep.2009.05.008
38. P Schanda BH Meier M Ernst 2010 Quantitative analysis of protein backbone dynamics in microcrystalline ubiquitin by solid-state NMR spectroscopy J Am Chem Soc 132 15957 15967 10.1021/ja100726a
39. CAEM Spronk GE Folkers AGW Noordman R Wechselberger N van den Brink R Boelens R Kaptein 1999 Hinge-helix formation and DNA bending in various lac repressor-operator complexes The EMBO J 22 6472 6480 10.1093/emboj/18.22.6472 (Pubitemid 29533251)
40. FW Studier 2005 Protein production by auto-induction in high-density shaking cultures Protein Expr Purif 41 207 234 10.1016/j.pep.2005.01.016
41. XC Su G Otting 2010 Paramagnetic labelling of proteins and oligonucleotides for NMR J Biomol NMR 46 101 112 10.1007/s10858-009-9331-1
42. XC Su K McAndrew T Huber G Otting 2008 Lanthanide-binding peptides for NMR measurements of residual dipolar couplings and paramagnetic effects from multiple angles J Am Chem Soc 130 1681 1687 10.1021/ja076564l (Pubitemid 351214087)
43. XC Su B Man S Beeren H Liang S Simonsen C Schmitz T Huber BA Messerle G Otting 2008 A dipicolinic acid tag for rigid lanthanide tagging of proteins and paramagnetic NMR spectroscopy J Am Chem Soc 130 10486 10487 10.1021/ja803741f
44. JD Swarbrick P Ung S Chhabra B Graham 2011 An iminodiacetic acid based lanthanide binding tag for paramagnetic exchange NMR spectroscopy Angew Chem Int Ed 50 4403 4406 10.1002/anie.201007221
45. JD Swarbrick P Ung XC Su A Maleckis S Chhabra T Huber G Otting B Graham 2011 Engineering of a bis-chelator motif into a protein α-helix for rigid lanthanide binding and paramagnetic NMR spectroscopy Chem Commun 47 7368 7370 10.1039/c1cc11893e
46. JR Tolman JM Flanagan MA Kennedy JH Prestegard 1995 Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution Proc Natl Acad Sci USA 92 9279 9283 1995PNAS...92.9279T 10.1073/pnas.92.20.9279
47. R Viguier G Serratrice A Dupraz C Dupuy 2001 New polypodal polycarboxylic ligands - complexation of rare-earth ions in aqueous solution Eur J Inorg Chem 7 1789 1795 10.1002/1099-0682(200107)2001:7<1789::AID-EJIC1789>3.0.CO;2-C (Pubitemid 32613353)
48. MD Vlasie C Comuzzi AMCH van den Nieuwendijk M Prudêncio M Overhand M Ubbink 2007 Long-range-distance NMR effects in a protein labeled with a lanthanide-DOTA chelate Chem Eur J 13 1715 1723 10.1002/chem.200600916 (Pubitemid 46941926)
49. J Wöhnert KJ Franz M Nitz B Imperiali H Schwalbe 2003 Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings J Am Chem Soc 125 13338 13339 10.1021/ja036022d (Pubitemid 37352103)
50. J Xu KS Matthews 2009 Flexibility in the inducer binding region is crucial for allostery in Escherichia coli lactose repressor Biochemistry 48 4988 4998 10.1021/bi9002343
51. X Xu PHJ Keizers W Reinle F Hannemann R Bernhardt M Ubbink 2009 Intermolecular dynamics studied by paramagnetic tagging J Biomol NMR 43 247 254 10.1007/s10858-009-9308-0
52. J You RE Cohen CM Pickart 1999 Construct for high-level expression and low misincorporation of lysine for arginine during expression of pET-encoded eukaryotic proteins in Escherichia coli Biotechniques 27 950 954 (Pubitemid 29529618)