Weak self-association of cytochrome c peroxidase molecules observed by paramagnetic NMR

Journal of Biomolecular NMR

Volumn 65, Issue 1, 2016, Pages 29-40

  Schilder, Jesika ^a   Ubbink, Marcellus ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Cytochrome c; Electron transfer; Ensemble docking; Paramagnetic relaxation enhancement; Ultra weak interactions

Indexed keywords

CYTOCHROME C PEROXIDASE; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBON NUCLEAR MAGNETIC RESONANCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTON NUCLEAR MAGNETIC RESONANCE; SIGNAL NOISE RATIO; SPIN LABELING; STEREOSPECIFICITY; SURFACE PROPERTY; CHEMISTRY; ELECTRON SPIN RESONANCE; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE; PROCEDURES;

CYTOCHROME-C PEROXIDASE; ELECTRON SPIN RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84970981569     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-016-0035-z     Document Type: Article

References (60)

1. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98:10037–10041. doi:10.1073/pnas.181342398
2. Bashir Q, Volkov AN, Ullmann GM, Ubbink M (2010) Visualization of the encounter ensemble of the transient electron transfer complex of cytochrome c and cytochrome c peroxidase. J Am Chem Soc 132:241–247. doi:10.1021/ja9064574
3. Battiste JL, Wagner G (2000) Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry 39:5355–5365. doi:10.1021/bi000060h
4. 15N NMR relaxation data of globular proteins using hydrodynamic calculations with HYDRONMR. J Biomol NMR 23:139–150. doi:10.1023/A:1016359412284
5. Bertini I, Luchinat C, Aime S (1996) NMR of paramagnetic substances. Coordin Chem Rev 150:29–110. doi:10.1016/0010-8545(96)01242-8
6. Bertoncini CW, Jung YS, Fernandez CO, Hoyer W, Griesinger C, Jovin TM, Zweckstetter M (2005) Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein. Proc Natl Acad Sci USA 102:1430–1435. doi:10.1073/pnas.0407146102
7. Bonagura CA et al (2003) High-resolution crystal structures and spectroscopy of native and compound I cytochrome c peroxidase. Biochemistry 42:5600–5608. doi:10.1021/bi034058c
8. Clore GM (2011) Exploring sparsely populated states of macromolecules by diamagnetic and paramagnetic NMR relaxation. Protein Sci 20:229–246. doi:10.1002/pro.576
9. Crowley PB, Matias PM, Mi H, Firbank SJ, Banfield MJ, Dennison C (2008) Regulation of protein function: crystal packing interfaces and conformational dimerization. Biochemistry 47:6583–6589. doi:10.1021/bi800125h
10. Dedmon MM, Lindorff-Larsen K, Christodoulou J, Vendruscolo M, Dobson CM (2005) Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J Am Chem Soc 127:476–477. doi:10.1021/ja044834j
11. Fawzi NL, Okabe Y, Yap EH, Head-Gordon T (2007) Determining the critical nucleus and mechanism of fibril elongation of the Alzheimer’s A beta(1-40) peptide. J Mol Biol 365:535–550. doi:10.1016/j.jmb.2006.10.011
12. Fawzi NL, Doucleff M, Suh JY, Clore GM (2010) Mechanistic details of a protein-protein association pathway revealed by paramagnetic relaxation enhancement titration measurements. Proc Natl Acad Sci USA 107:1379–1384. doi:10.1073/pnas.0909370107
13. Garcia-Ruiz JM (2003) Nucleation of protein crystals. J Struct Biol 142:22–31. doi:10.1016/S1047-8477(03)00035-2
14. Gillespie JR, Shortle D (1997a) Characterization of long-range structure in the denatured state of staphylococcal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels. J Mol Biol 268:158–169. doi:10.1006/jmbi.1997.0954
15. Gillespie JR, Shortle D (1997b) Characterization of long-range structure in the denatured state of staphylococcal nuclease. II. Distance restraints from paramagnetic relaxation and calculation of an ensemble of structures. J Mol Biol 268:170–184. doi:10.1006/jmbi.1997.0953
16. Henzler-Wildman KA et al (2007) Intrinsic motions along an enzymatic reaction trajectory. Nature 450:838–844. doi:10.1038/nature06410
17. Hiruma Y et al (2013) The structure of the cytochrome p450cam-putidaredoxin complex determined by paramagnetic NMR spectroscopy and crystallography. J Mol Biol 425:4353–4365. doi:10.1016/j.jmb.2013.07.006
18. Iwahara J, Clore GM (2006) Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature 440:1227–1230. doi:10.1038/nature04673
19. 1H paramagnetic relaxation enhancement. J Am Chem Soc 126:12800–12808. doi:10.1021/ja046246b
20. Iwahara J, Zweckstetter M, Clore GM (2006) NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA. Proc Natl Acad Sci U S A 103:15062–15067. doi:10.1073/pnas.0605868103
21. Johansson H et al (2014) Specific and nonspecific interactions in ultraweak protein-protein associations revealed by solvent paramagnetic relaxation enhancements. J Am Chem Soc 136:10277–10286. doi:10.1021/ja503546j
22. Keizers PH, Ubbink M (2011) Paramagnetic tools in protein NMR. Protein NMR spectroscopy: Practical techniques and applications. Wiley, Chichester, pp 193–219. doi:10.1002/9781119972006.ch6
23. Kleckner IR, Foster MP (2011) An introduction to NMR-based approaches for measuring protein dynamics. Biochim Biophys Acta 1814:942–968. doi:10.1016/j.bbapap.2010.10.012
24. Lescop E, Schanda P, Brutscher B (2007) A set of BEST triple-resonance experiments for time-optimized protein resonance assignment. J Magn Reson 187:163–169. doi:10.1016/j.jmr.2007.04.002
25. Liu Z, Zhang WP, Xing Q, Ren XF, Liu ML, Tang C (2012) Noncovalent dimerization of ubiquitin. Angew Chem Int Ed Engl 51:469–472. doi:10.1002/anie.201106190
26. Longinetti M, Luchinat C, Parigi G, Sgheri L (2006) Efficient determination of the most favoured orientations of protein domains from paramagnetic NMR data. Inverse Probl 22:1485–1502. doi:10.1088/0266-5611/22/4/019
27. 15N-labeled eukaryotic cytochrome c in Escherichia coli. J Biol Inorg Chem 4:220–222. doi:10.1007/s007750050307
28. Northrup SH, Boles JO, Reynolds JC (1988) Brownian dynamics of cytochrome c and cytochrome c peroxidase association. Science 241:67–70. doi:10.1126/science.2838904
29. Pelletier H, Kraut J (1992) Crystal-structure of a complex between electron-transfer partners, cytochrome c peroxidase and cytochrome c. Science 258:1748–1755. doi:10.1126/science.1334573
30. Pervushin K, Riek R, Wider G, Wüthrich K (1997) Attenuated T2 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 94:12366–12371
31. Pollock WB, Rosell FI, Twitchett MB, Dumont ME, Mauk AG (1998) Bacterial expression of a mitochondrial cytochrome c. Trimethylation of lys72 in yeast iso-1-cytochrome c and the alkaline conformational transition. Biochemistry 37:6124–6131. doi:10.1021/bi972188d
32. Scanu S, Forster J, Finiguerra MG, Shabestari MH, Huber M, Ubbink M (2012) The complex of cytochrome f and plastocyanin from Nostoc sp PCC 7119 is highly dynamic. ChemBioChem 13:1312–1318. doi:10.1002/cbic.201200073
33. Schilder J, Ubbink M (2013) Formation of transient protein complexes. Curr Opin Struct Biol 23:911–918. doi:10.1016/j.sbi.2013.07.009
34. Schilder J, Lohr F, Schwalbe H, Ubbink M (2014) The cytochrome c peroxidase and cytochrome c encounter complex: the other side of the story. FEBS Lett 588:1873–1878. doi:10.1016/j.febslet.2014.03.055
35. Schilder J, Liu WD, Kumar P, Overhand M, Huber M, Ubbink M (2015) Protein docking using an ensemble of spin labels optimized by intra-molecular paramagnetic relaxation enhancement. Phys Chem Chem Phys 18:5729–5742. doi:10.1039/c5cp03781f
36. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160:65–73. doi:10.1016/S1090-7807(02)00014-9
37. Schwieters CD, Kuszewski JJ, Clore GM (2006) Using Xplor-NIH for NMR molecular structure determination. Prog Nucl Mag Res Spectrosc 48:47–62. doi:10.1016/j.pnmrs.2005.10.001
38. Shortle D, Ackerman MS (2001) Persistence of native-like topology in a denatured protein in 8 M urea. Science 293:487–489. doi:10.1126/science.1060438
39. Suh JY, Tang C, Clore GM (2007) Role of electrostatic interactions in transient encounter complexes in protein-protein association investigated by paramagnetic relaxation enhancement. J Am Chem Soc 129:12954–12955. doi:10.1021/ja0760978
40. Tang C, Iwahara J, Clore GM (2006) Visualization of transient encounter complexes in protein-protein association. Nature 444:383–386. doi:10.1038/nature05201
41. Tang C, Schwieters CD, Clore GM (2007) Open-to-closed transition in apo maltose-binding protein observed by paramagnetic NMR. Nature 449:1078–1082. doi:10.1038/nature06232
42. Tang C, Ghirlando R, Clore GM (2008a) Visualization of transient ultra-weak protein self-association in solution using paramagnetic relaxation enhancement. J Am Chem Soc 130:4048–4056. doi:10.1021/ja710493m
43. Tang C, Louis JM, Aniana A, Suh JY, Clore GM (2008b) Visualizing transient events in amino-terminal autoprocessing of HIV-1 protease. Nature 455:693–696. doi:10.1038/nature07342
44. Ubbink M (2009) The courtship of proteins: understanding the encounter complex. FEBS Lett 583:1060–1066. doi:10.1016/j.febslet.2009.02.046
45. Ulucan O, Helms V (2015) How hydrophilic proteins form non-specific complexes. J Phys Chem B 119:10524–10530. doi:10.1021/acs.jpcb.5b05831
46. Van de Water K, Van Nuland NAJ, Volkov AN (2014) Transient protein encounters characterized by paramagnetic NMR. Chem Sci 5:4227–4236. doi:10.1039/C4sc01232a
47. Vaynberg J, Qin J (2006) Weak protein-protein interactions as probed by NMR spectroscopy. Trends Biotechnol 24:22–27. doi:10.1016/j.tibtech.2005.09.006
48. Villareal VA, Spirig T, Robson SA, Liu MY, Lei BF, Clubb RT (2011) Transient weak protein-protein complexes transfer heme across the cell wall of Staphylococcus aureus. J Am Chem Soc 133:14176–14179. doi:10.1021/ja203805b
49. Volkov AN, Worrall JA, Holtzmann E, Ubbink M (2006) Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proc Natl Acad Sci USA 103:18945–18950. doi:10.1073/pnas.0603551103
50. Volkov AN, Bashir Q, Worrall JAR, Ubbink M (2009) Binding hot spot in the weak protein complex of physiological redox partners yeast cytochrome c and cytochrome c peroxidase. J Mol Biol 385:1003–1013. doi:10.1016/j.jmb.2008.10.091
51. Volkov AN, Bashir Q, Worrall JA, Ullmann GM, Ubbink M (2010a) Shifting the equilibrium between the encounter state and the specific form of a protein complex by interfacial point mutations. J Am Chem Soc 132:11487–11495. doi:10.1021/ja100867c
52. Volkov AN, Ubbink M, van Nuland NA (2010b) Mapping the encounter state of a transient protein complex by PRE NMR spectroscopy. J Biomol NMR 48:225–236. doi:10.1007/s10858-010-9452-6
53. Volkov AN, Nicholls P, Worrall JAR (2011) The complex of cytochrome c and cytochrome c peroxidase: the end of the road? BBA-Bioenerg 1807:1482–1503. doi:10.1016/j.bbabio.2011.07.010
54. Vranken WF et al (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59:687–696. doi:10.1002/prot.20449
55. 1H] heteronuclear NMR spectroscopy. Biochemistry 40:7069–7076. doi:10.1021/bi0025823
56. Xing Q et al (2014) Visualizing an ultra-weak protein-protein interaction in phosphorylation signaling. Angew Chem Int Ed Engl 53:11501–11505. doi:10.1002/anie.201405976
57. Xu X, Reinle W, Hannemann F, Konarev PV, Svergun DI, Bernhardt R, Ubbink M (2008) Dynamics in a pure encounter complex of two proteins studied by solution scattering and paramagnetic NMR spectroscopy. J Am Chem Soc 130:6395–6403. doi:10.1021/ja7101357
58. Xu X, Keizers PH, Reinle W, Hannemann F, Bernhardt R, Ubbink M (2009) Intermolecular dynamics studied by paramagnetic tagging. J Biomol NMR 43:247–254. doi:10.1007/s10858-009-9308-0
59. 2, and ferrocytochrome c and enzymic determination of extinction coefficients of cytochrome c. J Biol Chem 240:4509–4514
60. Zlotnick A (2005) Theoretical aspects of virus capsid assembly. J Mol Recognit 18:479–490. doi:10.1002/jmr.754