CP-HISQC: A better version of HSQC experiment for intrinsically disordered proteins under physiological conditions

Journal of Biomolecular NMR

Volumn 58, Issue 3, 2014, Pages 175-192

  Yuwen, Tairan ^a   Skrynnikov, Nikolai R ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

Amide solvent exchange; Cross polarization; Intrinsically disordered proteins; Proton decoupled HSQC

Indexed keywords

ARGININE; CARBON 13; INTRINSICALLY DISORDERED PROTEIN;

ANALYTIC METHOD; ARTICLE; CONFORMATIONAL TRANSITION; CROSS POLARIZATION ASSISTED HETERONUCLEAR IN PHASE SINGLE QUANTUM CORRELATION; DIPOLE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MEASUREMENT; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN UNFOLDING; SOLVENT EFFECT;

AMIDES; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR CONFORMATION; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SOLVENTS; WATER;

EID: 84896317133     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-014-9815-5     Document Type: Article

References (64)

1. Abragam A (1961) The principles of nuclear magnetism. Clarendon Press, Oxford
2. Amezcua CA, Harper SM, Rutter J, Gardner KH (2002) Structure and interactions of PAS kinase N-terminal PAS domain: model for intramolecular kinase regulation. Structure 10:1349-1361 (Pubitemid 35232384)
3. Bai YW, Milne JS, Mayne L, Englander SW (1993) Primary structure effects on peptide group hydrogen exchange. Proteins Struct Funct Genet 17:75-86 (Pubitemid 23261059)
4. Ban D, Gossert AD, Giller K, Becker S, Griesinger C, Lee D (2012) Exceeding the limit of dynamics studies on biomolecules using high spin-lock field strengths with a cryogenically cooled probehead. J Magn Reson 221:1-4
5. Bax A, Ikura M, Kay LE, Torchia DA, Tschudin R (1990) Comparison of different modes of two-dimensional reverse-correlation NMR for the study of proteins. J Magn Reson 86:304-318
6. 13C-detected protonless NMR spectroscopy of proteins in solution. Prog NMR Spectrosc 48:25-45
7. Bermel W, Bertini I, Csizmok V, Felli IC, Pierattelli R, Tompa P (2009) H-start for exclusively heteronuclear NMR spectroscopy: the case of intrinsically disordered proteins. J Magn Reson 198:275-281
8. Bista M, Freund SM, Fersht AR (2012) Domain-domain interactions in full-length p53 and a specific DNA complex probed by methyl NMR spectroscopy. Proc Natl Acad Sci USA 109:15752-15756
9. Blaum BS, Deakin JA, Johansson CM, Herbert AP, Barlow PN, Lyon M, Uhrin D (2010) Lysine and arginine side chains in glycosaminoglycan-protein complexes investigated by NMR, cross-linking, and mass spectrometry: a case study of the Factor H-Heparin interaction. J Am Chem Soc 132:6374-6381
10. H/D-SOLEXSY experiment for accurate measurement of amide solvent exchange rates. Application to denatured drkN SH3. J Biomol NMR 46:227-244
11. Connelly GP, Bai YW, Jeng MF, Englander SW (1993) Isotope effects in peptide group hydrogen exchange. Proteins Struct Funct Genet 17:87-92 (Pubitemid 23261060)
12. Croke RL, Sallum CO, Watson E, Watt ED, Alexandrescu AT (2008) Hydrogen exchange of monomeric α-synuclein shows unfolded structure persists at physiological temperature and is independent of molecular crowding in Escherichia coli. Protein Sci 17:1434-1445
13. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on unix pipes. J Biomol NMR 6:277-293
14. Diehl C, Engstrom O, Delaine T, Hakansson M, Genheden S, Modig K, Leffler H, Ryde U, Nilsson UJ, Akke M (2010) Protein flexibility and conformational entropy in ligand design targeting the carbohydrate recognition domain of galectin-3. J Am Chem Soc 132:14577-14589
15. 15N NMR spectroscopy. J Am Chem Soc 133:909-919
16. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium. J Biomol NMR 4:727-734
17. Farrow NA, Zhang OW, Forman-Kay JD, Kay LE (1995) Comparison of the backbone dynamics of a folded and an unfolded SH3 domain existing in equilibrium in aqueous buffer. Biochemistry 34:868-878
18. Felli IC, Brutscher B (2009) Recent advances in solution NMR: fast methods and heteronuclear direct detection. ChemPhysChem 10:1356-1368
19. Fernandez C, Hilty C, Wider G, Guntert P, Wuthrich K (2004) NMR structure of the integral membrane protein OmpX. J Mol Biol 336:1211-1221 (Pubitemid 38229708)
20. Gil S, Hošek T, Solyom Z, Kümmerle R, Brutscher B, Pierattelli R, Felli IC (2013) NMR spectroscopic studies of intrinsically disordered proteins at near-physiological conditions. Angew Chem Int Edit 52:11808-11812
21. 13C-detected NMR. Protein Sci 21:1954-1960
22. 2O in protein NMR: application to sensitivity enhancement and NOE measurements. J Am Chem Soc 115:12593-12594
23. 57 mobilities and catalytic activities. Proc Natl Acad Sci USA 102:1006-1011
24. Hansen DF, Kay LE (2007) Improved magnetization alignment schemes for spin-lock relaxation experiments. J Biomol NMR 37:245-255 (Pubitemid 46390087)
25. Hiller S, Wider G, Etezady-Esfarjani T, Horst R, Wuthrich K (2005) Managing the solvent water polarization to obtain improved NMR spectra of large molecular structures. J Biomol NMR 32:61-70 (Pubitemid 41086468)
26. Hsu STD, Bertoncini CW, Dobson CM (2009) Use of protonless NMR spectroscopy to alleviate the loss of information resulting from exchange-broadening. J Am Chem Soc 131:7222-7223
27. Hu F, Schmidt-Rohr K, Hong M (2012) NMR detection of pH-dependent histidine-water proton exchange reveals the conduction mechanism of a transmembrane proton channel. J Am Chem Soc 134:3703-3713
28. Iwahara J, Jung YS, Clore GM (2007) Heteronuclear NMR spectroscopy for lysine NH3 groups in proteins: unique effect of water exchange on 15N transverse relaxation. J Am Chem Soc 129:2971-2980 (Pubitemid 46417975)
29. 15N relaxation rate constants. J Biomol NMR 54:389-400
30. Kay LE, Keifer P, Saarinen T (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J Am Chem Soc 114:10663-10665
31. Keifer PA (1999) 90° degrees pulse width calibrations: how to read a pulse width array. Concept Magnetic Res 11:165-180
32. Krishnan VV, Rance M (1995) Influence of chemical exchange among homonuclear spins in heteronuclear coherence-transfer experiments in liquids. J Magn Reson A 116:97-106
33. Kupce E, Freeman R (1996) Optimized adiabatic pulses for wideband spin inversion. J Magn Reson A 118:299-303 (Pubitemid 126751707)
34. Levitt MH (1991) Heteronuclear cross polarization in liquid-state nuclear magnetic resonance: mismatch compensation and relaxation behavior. J Chem Phys 94:30-38
35. Loh SN, Kay MS, Baldwin RL (1995) Structure and stability of a second molten globule intermediate in the apomyoglobin folding pathway. Proc Natl Acad Sci USA 92:5446-5450
36. Majumdar A, Zuiderweg ERP (1995) Efficiencies of double-resonance and triple-resonance J cross-polarization in multidimensional NMR. J Magn Reson A 113:19-31
37. Marion D, Ikura M, Tschudin R, Bax A (1989) Rapid recording of 2D NMR spectra without phase cycling: application to the study of hydrogen exchange in proteins. J Magn Reson 85:393-399
38. Marsh JA, Forman-Kay JD (2009) Structure and disorder in an unfolded state under nondenaturing conditions from ensemble models consistent with a large number of experimental restraints. J Mol Biol 391:359-374
39. Mori S, Abeygunawardana C, Johnson MO, van Zijl PCM (1995) Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J Magn Reson B 108:94-98
40. Mueller GA, Smith AM, Chapman MD, Rule GS, Benjamin DC (2001) Hydrogen exchange nuclear magnetic resonance spectroscopy mapping of antibody epitopes on the house dust mite allergen Der p 2*. J Biol Chem 276:9359-9365
41. Mulder FAA, Spronk CAEM, Slijper M, Kaptein R, Boelens R (1996) Improved HSQC experiments for the observation of exchange broadened signals. J Biomol NMR 8:223-228 (Pubitemid 126706792)
42. Muller L, Legault P, Pardi A (1995) Improved RNA structure determination by detection of NOE contacts to exchange-broadened amino protons. J Am Chem Soc 117:11043-11048
43. 13C-detected experiments for backbone assignment of unstructured proteins with a very low signal dispersion. J Biomol NMR 50:1-11
44. Orij R, Postmus J, Ter Beek A, Brul S, Smits GJ (2009) In vivo measurement of cytosolic and mitochondrial pH using a pH-J sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiology 155:268-278
45. Palmer AG, Cavanagh J, Wright PE, Rance M (1991) Sensitivty improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J Magn Reson 93:151-170
46. 13C detection for carbonyl relaxation studies of protein dynamics. J Magn Reson 193:226-232
47. Rucker SP, Shaka AJ (1989) Broad-band homonuclear cross-polarization in 2D NMR using DIPSI-2. Mol Phys 68:509-517
48. Schanda P, Brutscher B (2005) Very fast two-dimensional NMR spectroscopy for real-time investigation of dynamic events in proteins on the time scale of seconds. J Am Chem Soc 127:8014-8015 (Pubitemid 40799646)
49. Schanda P, Kupce E, Brutscher B (2005) SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J Biomol NMR 33:199-211 (Pubitemid 43118574)
50. Segawa T, Kateb F, Duma L, Bodenhausen G, Pelupessy P (2008) Exchange rate constants of invisible protons in proteins determined by NMR spectroscopy. ChemBioChem 9:537-542
51. Shaka AJ, Keeler J, Frenkiel T, Freeman R (1983) An improved sequence for broad-band decoupling: WALTZ-16. J Magn Reson 52:335-338
52. 15N HSQC experiments optimized to retain full sensitivity. J Magn Reson A 102:241-245
53. Skrynnikov NR, Ernst RR (1999) Detection of intermolecular chemical exchange through decorrelation of two-spin order. J Magn Reson 137:276-280 (Pubitemid 129608253)
54. Takayama Y, Castaneda CA, Chimenti M, Garcia-Moreno B, Iwahara J (2008) Direct evidence for deprotonation of a lysine side chain buried in the hydrophobic core of a protein. J Am Chem Soc 130:6714-6715 (Pubitemid 351748401)
55. Theillet FX, Binolfi A, Liokatis S, Verzini S, Selenko P (2011) Paramagnetic relaxation enhancement to improve sensitivity of fast NMR methods: application to intrinsically disordered proteins. J Biomol NMR 51:487-495
56. Trbovic N, Cho JH, Abel R, Friesner RA, Rance M, Palmer AG (2009) Protein side-chain dynamics and residual conformational entropy. J Am Chem Soc 131:615-622
57. Vidovic V, Prongidi-Fix L, Bechinger B, Werten S (2009) Production and isotope labeling of antimicrobial peptides in Escherichia coli by means of a novel fusion partner that enables high-yield insoluble expression and fast purification. J Pept Sci 15:278-284
58. Werbeck ND, Kirkpatrick J, Hansen DF (2013) Probing arginine side chains and their dynamics with carbon-detected NMR spectroscopy: application to the 42 kDa human histone deacetylase 8 at high pH. Angew Chem Int Edit 52:3145-3147
59. Wu XD, Knudsen B, Feller SM, Zheng J, Sali A, Cowburn D, Hanafusa H, Kuriyan J (1995) Structural basis for the specific interaction of lysine-containing proline-rich peptides with the N-terminal SH3 domain of c-Crk. Structure 3:215-226
60. 15N heteronuclear correlation spectra acquired with band-selective pulses. J Magn Reson 211:243-247
61. 2 relaxation in disordered proteins. J Magn Reson [ePub ahead of print]
62. Zangger K, Armitage IM (1998) Sensitivity-enhanced detection of fast exchanging protons by an exchange-edited gradient HEHAHA-HSQC experiment. J Magn Reson 135:70-75 (Pubitemid 128450687)
63. Zhang O, Forman-Kay JD (1995) Structural characterization of a folded and an unfolded state of an SH3 domain in aqueous buffer and solution structure of this domain by NMR. Biochemistry 34:6784-6794
64. 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed-field gradient NMR techniques. J Biomol NMR 4:845-858