Article

You have full text access to this OnlineOpen article

Three-dimensional structure of the weakly associated protein homodimer SeR13 using RDCs and paramagnetic surface mapping

  1. Hsiau-Wei Lee1,
  2. Greg Wylie1,
  3. Sonal Bansal2,
  4. Xu Wang1,
  5. Adam W. Barb1,
  6. Megan A. Macnaughtan3,
  7. Asli Ertekin4,
  8. Gaetano T. Montelione4,
  9. James H. Prestegard1,*

Article first published online: 29 JUN 2010

DOI: 10.1002/pro.447

Issue

Protein Science

Protein Science

Volume 19, Issue 9, pages 1673–1685, September 2010

Additional Information

How to Cite

Lee, H.-W., Wylie, G., Bansal, S., Wang, X., Barb, A. W., Macnaughtan, M. A., Ertekin, A., Montelione, G. T. and Prestegard, J. H. (2010), Three-dimensional structure of the weakly associated protein homodimer SeR13 using RDCs and paramagnetic surface mapping. Protein Science, 19: 1673–1685. doi: 10.1002/pro.447

Author Information

  1. 1

    Complex Carbohydrate Research Center, Northeast Structural Genomics Consortium, The University of Georgia, Athens, Georgia 30602

  2. 2

    Department of Biochemistry, Washington University, St Louis, Missouri 63130

  3. 3

    Department of Chemistry, Louisiana State University Baton Rouge, Louisiana 70803

  4. 4

    Department of Molecular Biology and Biochemistry, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854, and Robert Wood Johnson Medical School, University of Medicine and Dentistry, Piscataway, New Jersey 08854, and Northeast Structural Genomics Consortium, Piscataway, New Jersey 08854

*Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602

Publication History

  1. Issue published online: 23 AUG 2010
  2. Article first published online: 29 JUN 2010
  3. Manuscript Accepted: 13 JUN 2010
  4. Manuscript Revised: 10 JUN 2010
  5. Manuscript Received: 16 APR 2010

Funded by

  • National Institutes of Health Protein Structure Initiative. Grant Number: U54-GM074958

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (671K)

References

  • 1
    Goodsell DS, Olson AJ ( 2000) Structural symmetry and protein function. Annu Rev Biophys Biomol Struct 29: 105–153.
  • 2
    Ali MH, Imperiali B ( 2005) Protein oligomerization: how and why. Bioorg Med Chem 13: 5013–5020.
  • 3
    Lee RT, Lee YC ( 2000) Affinity enhancement by multivalent lectin-carbohydrate interaction. Glycoconj J 17: 543–551.
  • 4
    Drickamer K ( 1999) C-type lectin-like domains. Curr Opin Struct Biol 9: 585–590.
  • 5
    Wang X, Bansal S, Jiang M, Prestegard JH ( 2008) RDC-assisted modeling of symmetric protein homo-oligomers. Protein Sci 17: 899–907.
    Direct Link:
  • 6
    Zwahlen C, Legault P, Vincent SJF, Greenblatt J, Konrat R, Kay LE ( 1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage lambda N-peptide/boxB RNA complex. J Am Chem Soc 119: 6711–6721.
  • 7
    Folkers PJ, Nilges M, Folmer RH, Konings RN, Hilbers CW ( 1994) The solution structure of the Tyr41–>His mutant of the single-stranded DNA binding protein encoded by gene V of the filamentous bacteriophage M13. J Mol Biol 236: 229–246.
  • 8
    Ikura M, Bax A ( 1992) Isotope-filtered 2D NMR of a protein peptide complex—study of a skeletal-muscle myosin light chain kinase fragment bound to calmodulin. J Am Chem Soc 114: 2433–2440.
  • 9
    Prestegard JH, Bougault CM, Kishore AI ( 2004) Residual dipolar couplings in structure determination of biomolecules. Chem Rev 104: 3519–3540.
  • 10
    Al-Hashimi HM, Bolon PJ, Prestegard JH ( 2000) Molecular symmetry as an aid to geometry determination in ligand protein complexes. J Magn Reson 142: 153–158.
  • 11
    Bewley CA, Clore GM ( 2000) Determination of the relative orientation of the two halves of the domain-swapped dimer of cyanovirin-N in solution using dipolar couplings and rigid body minimization. J Am Chem Soc 122: 6009–6016.
  • 12
    Zweckstetter M, Bax A ( 2000) Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR. J Am Chem Soc 122: 3791–3792.
  • 13
    Ortega-Roldan JL, Jensen MR, Brutscher B, Azuaga AI, Blackledge M, van Nuland NA ( 2009) Accurate characterization of weak macromolecular interactions by titration of NMR residual dipolar couplings: application to the CD2AP SH3-C:ubiquitin complex. Nucleic Acids Res 37: e70.
  • 14
    Wang J, Zuo X, Yu P, Byeon IJ, Jung J, Wang X, Dyba M, Seifert S, Schwieters CD, Qin J, Gronenborn AM, Wang YX ( 2009) Determination of multicomponent protein structures in solution using global orientation and shape restraints. J Am Chem Soc 131: 10507–10515.
  • 15
    Petros AM, Mueller L, Kopple KD ( 1990) NMR identification of protein surfaces using paramagnetic probes. Biochemistry 29: 10041–10048.
  • 16
    Bernini A, Spiga O, Ciutti A, Venditti V, Prischi F, Governatori M, Bracci L, Lelli B, Pileri S, Botta M, Barge A, Laschi F, Niccolai N ( 2006) NMR studies of BPTI aggregation by using paramagnetic relaxation reagents. Biochim Biophys Acta 1764: 856–862.
  • 17
    Pintacuda G, Otting G ( 2002) Identification of protein surfaces by NMR measurements with a pramagnetic Gd(III) chelate. J Am Chem Soc 124: 372–373.
  • 18
    Bernini A, Venditti V, Spiga O, Ciutti A, Prischi F, Consonni R, Zetta L, Arosio I, Fusi P, Guagliardi A, Niccolai N ( 2008) NMR studies on the surface accessibility of the archaeal protein Sso7d by using TEMPOL and Gd(III)(DTPA-BMA) as paramagnetic probes. Biophys Chem 137: 71–75.
  • 19
    Bernini A, Venditti V, Spiga O, Niccolai N ( 2009) Probing protein surface accessibility with solvent and paramagnetic molecules. Prog Nucl Mag Res Sep 54: 278–289.
  • 20
    Otting G ( 2010) Protein NMR using paramagnetic ions. Annu Rev Biophys 39: 387–405.
  • 21
    Schilke B, Voisine C, Beinert H, Craig E ( 1999) Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96: 10206–10211.
  • 22
    Mercier KA, Baran M, Ramanathan V, Revesz P, Xiao R, Montelione GT, Powers R ( 2006) FAST-NMR: functional annotation screening technology using NMR spectroscopy. J Am Chem Soc 128: 15292–15299.
  • 23
    Liu Y, Qi W, Cowan JA ( 2009) Iron-sulfur cluster biosynthesis: functional characterization of the N- and C-terminal domains of human NFU. Biochemistry 48: 973–980.
  • 24
    Sattler M, Schleucher J, Griesinger C ( 1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog Nucl Mag Res Sep 34: 93–158.
  • 25
    Silver MS, Joseph RI, Hoult DI ( 1984) Highly selective Pi/2 and Pi-pulse generation. J Magn Reson 59: 347–351.
  • 26
    Kay LE, Keifer P, Saarinen T ( 1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. JACS 114: 10663–10665.
  • 27
    Zhang O, Kay LE, Olivier JP, Forman-Kay JD ( 1994) Backbone 1H and 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.
  • 28
    Bendall MR ( 1995) Heteronuclear J coupling precession during spin-lock and adiabatic pulses. Use of adiabatic inversion pulses in high-resolution NMR. J Magn Reson Series A 116: 46–58.
  • 29
    Guntert P, Mumenthaler C, Wuthrich K ( 1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273: 283–298.
  • 30
    Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM ( 2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160: 65–73.
  • 31
    Cornilescu G, Bax A ( 2000) Measurement of proton, nitrogen, and carbonyl chemical shielding anisotropies in a protein dissolved in a dilute liquid crystalline phase. J Am Chem Soc 122: 10143–10154.
  • 32
    Cornilescu G, Delaglio F, Bax A ( 1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289–302.
  • 33
    Farmer BT, 2nd, Constantine KL, Goldfarb V, Friedrichs MS, Wittekind M, Yanchunas J, Jr., Robertson JG, Mueller L ( 1996) Localizing the NADP+ binding site on the MurB enzyme by NMR. Nat Struct Biol 3: 995–997.
  • 34
    Al-Hashimi HM, Valafar H, Terrell M, Zartler ER, Eidsness MK, Prestegard JH ( 2000) Variation of molecular alignment as a means of resolving orientational ambiguities in protein structures from dipolar couplings. J Magn Reson 143: 402–406.
  • 35
    Henrick K, Thornton JM ( 1998) PQS: a protein quaternary structure file server. Trends Biochem Sci 23: 358–361.
  • 36
    Humphrey W, Dalke A, Schulten K ( 1996) VMD: Visual molecular dynamics. J Mol Graphics 14: 33.
  • 37
    Jain NU, Noble S, Prestegard JH ( 2003) Structural characterization of a mannose-binding protein-trimannoside complex using residual dipolar couplings. J Mol Biol 328: 451–462.
  • 38
    Fischer MW, Losonczi JA, Weaver JL, Prestegard JH ( 1999) Domain orientation and dynamics in multidomain proteins from residual dipolar couplings. Biochemistry 38: 9013–9022.
  • 39
    Clore GM, Omichinski JG, Sakaguchi K, Zambrano N, Sakamoto H, Appella E, Gronenborn AM ( 1995) Interhelical angles in the solution structure of the oligomerization domain of p53: correction. Science 267: 1515–1516.
  • 40
    Lambert LJ, Schirf V, Demeler B, Cadene M, Werner MH ( 2004) Flipping a genetic switch by subunit exchange. EMBO J 23: 3186–3186.
  • 41
    Nabuurs SB, Spronk CAEM, Vuister GW, Vriend G ( 2006) Traditional biomolecular structure determination by NMR spectroscopy allows for major errors. PLOS Comput Biol 2: 71–79.
  • 42
    Bhattacharya A, Tejero R, Montelione GT ( 2007) Evaluating protein structures determined by structural genomics consortia. Prot Struct Funct Bioinform 66: 778–795.
    Direct Link:
  • 43
    Bardiaux B, Bernard A, Rieping W, Habeck M, Malliavin TE, Nilges M ( 2009) Influence of different assignment conditions on the determination of symmetric homodimeric structures with ARIA. Prot Struct Funct Bioinformatics 75: 569–585.
    Direct Link:
  • 44
    Acton TB, Gunsalus KC, Xiao R, Ma LC, Aramini J, Baran MC, Chiang YW, Climent T, Cooper B, Denissova NG, Douglas SM, Everett JK, Ho CK, Macapagal D, Rajan PK, Shastry R, Shih LY, Swapna GV, Wilson M, Wu M, Gerstein M, Inouye M, Hunt JF, Montelione GT ( 2005) Robotic cloning and protein production platform of the northeast structural genomics consortium. Methods Enzymol 394: 210–243.
  • 45
    Jansson M, Li YC, Jendeberg L, Anderson S, Montelione GT, Nilsson B ( 1996) High-level production of uniformly N-15- and C-13-enriched fusion proteins in Escherichia coli. J Biomol NMR 7: 131–141.
  • 46
    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.
  • 47
    Goddard TD, Keneller DG. ( 2006) Sparky 3. University of California, San Francisco.
  • 48
    Kontaxis G, Clore GM, Bax A ( 2000) Evaluation of cross-correlation effects and measurement of one-bond couplings in proteins with short transverse relaxation times. J Magn Reson 143: 184–196.
  • 49
    Bax A, Tjandra N ( 1997) High-resolution heteronuclear NMR of human ubiquitin in an aqueous liquid crystalline medium. J Biomol NMR 10: 289–292.
  • 50
    Cierpicki T, Bushweller JH ( 2004) Charged gels as orienting media for measurement of residual dipolar couplings in soluble and integral membrane proteins. J Am Chem Soc 126: 16259–16266.
  • 51
    Herrmann T, Guntert P, Wuthrich K ( 2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319: 209–227.
  • 52
    Valafar H, Prestegard JH ( 2004) REDCAT: a residual dipolar coupling analysis tool. J Magn Reson 167: 228–241.
  • 53
    Ulmer TS, Ramirez BE, Delaglio F, Bax A ( 2003) Evaluation of backbone proton positions and dynamics in a small protein by liquid crystal NMR spectroscopy. J Am Chem Soc 125: 9179–9191.
  • 54
    Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K ( 2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781–1802.
    Direct Link:
  • 55
    Moont G, Gabb HA, Sternberg MJ ( 1999) Use of pair potentials across protein interfaces in screening predicted docked complexes. Proteins 35: 364–373.
    Direct Link:
View Full Article (HTML) Get PDF (671K)