Journal of Biomolecular NMR

, Volume 12, Issue 1, pp 1–23 | Cite as

Recommendations for the presentation of NMR structures of proteins and nucleic acids – IUPAC-IUBMB-IUPAB Inter-Union Task Group on the Standardization of Data Bases of Protein and Nucleic Acid Structures Determined by NMR Spectroscopy

  • John L. Markley
  • Ad Bax
  • Yoji Arata
  • C. W. Hilbers
  • Robert Kaptein
  • Brian D. Sykes
  • Peter E. Wright
  • Kurt Wüthrich


The recommendations presented here are designed to support easier communication of NMR data and NMR structures of proteins and nucleic acids through unified nomenclature and reporting standards. Much of this document pertains to the reporting of data in journal articles; however, in the interest of the future development of structural biology, it is desirable that the bulk of the reported information be stored in computer-accessible form and be freely accessible to the scientific community in standardized formats for data exchange. These recommendations stem from an IUPAC-IUBMB-IUPAB inter-union venture with the direct involvement of ICSU and CODATA. The Task Group has reviewed previous formal recommendations and has extended them in the light of more recent developments in the field of biomolecular NMR spectroscopy. Drafts of the recommendations presented here have been examined critically by more than 50 specialists in the field and have gone through two rounds of extensive modification to incorporate suggestions and criticisms.

References and notes

  1. 3.
    Berman, H.M., Olson, W.K., Beveridge, D.L., Westbrook, J., Gelbin, A., Demeny, T., Hsieh, S.-H., Srinivasan, A.R. and Schneider, B. (1992) The Nucleic Acid Database: A Comprehensive Relational Database of Three-Dimensional Structures of Nucleic Acids, Biophys. J., 63, 751–759. The Nucleic Acid Data Bank can be reached on the Internet at Scholar
  2. 4.
    Hendrickson, W.A. and Wüthrich, K. (1991) Macromolecular Structures, Current Biology, London, UK.Google Scholar
  3. 5.
    Nomenclature Committee of IUBMB (NC-IUBMB) and IUPAC-IUBMB Joint Commission on Biochemical Nomenclature (JCBN) (1992) Newsletter 1992, Biochem. Int., 26, 567–575; and references therein.Google Scholar
  4. 6.
    Commission on Molecular Structure and Spectroscopy (1972) Recommendations for Presentation of NMR Data for Publication in Chemical Journals,Pure Appl. Chem., 29, 627–628.Google Scholar
  5. 7.
    Commission on Molecular Structure and Spectroscopy (1976) Presentation of NMR Data for Publication in Chemical Journals-B. Conventions Relating to Spectra from Nuclei other than Protons (Recommendations 1975), Pure Appl. Chem., 45, 219.Google Scholar
  6. 8.
    Harris, R.K., Kowalewski, J., and Cabral de Menezes, S. (1996) Parameters and Symbols for use in Nuclear Magnetic Resonance, draft IUPAC document to be published in Pure Appl. Chem., 69, 2489–2495.Google Scholar
  7. 9.
    Liébecq, C. (Ed.) (1992) Biochemical Nomenclature and Related Documents - A Compendium, 2nd ed., Portland Press on behalf of IUBMB, London, U.K.Google Scholar
  8. 10.
    Bonnett, R. (1978) In The Porphyrins (Ed., Dolphin, D.), Vol. 1, Part A, Academic Press, New York, NY, pp. 1–27.Google Scholar
  9. 11.
    IUPAC-IUB Commission on Biochemical Nomenclature (CBN) (1975) Nomenclature of Iron-Sulfur Proteins. Recommendations 1973, Eur. J. Biochem., 35, 1–2.Google Scholar
  10. 12.
    IUPAC-IUB Commission on Biochemical Nomenclature (1975) The Nomenclature of Peptide Hormones, Recommendations 1974, Biochemistry, 14, 2559–2560; reprinted in the Compendium (ref. 9).Google Scholar
  11. 13.
    IUPAC-IUB Commission on Biochemical Nomenclature (1972) Abbreviated Nomenclature of Synthetic Polypeptides (Polymerized Amino Acids), Revised Recommendations 1971, Biochemistry, 11, 942–944; reprinted in the Compendium (ref. 9).Google Scholar
  12. 14.
    Nomenclature Committee of the International Union of Biochemistry (NC-IUB) Nomenclature for Incompletely Specified Bases in Nucleic Acids (1985), Eur. J. Biochem., 150, 1–5; reprinted in the Compendium (ref. 9).Google Scholar
  13. 16.
    Protein Identification Resource, Georgetown University, Washington, D.C., U.S.A. The Protein Identification Resource can be searched with tools located at: Scholar
  14. 17.
    SWISS-PROT Annotated Protein Sequence Database ( ml).Google Scholar
  15. 18.
    International Union of Biochemistry and Molecular Biology (1992) Enzyme Nomenclature, Recommendations 1992, Academic Press, Orlando, FL, U.S.A.Google Scholar
  16. 19.
    Chemical Abstracts Service, Columbus, OH, U.S.A. ( Scholar
  17. 20.
    IUPAC-IUB Commission on Biochemical Nomenclature (CBN) (1970) Abbreviations and Symbols for the Description of the Conformation of Polypeptide Chains, Tentative Rules 1969, Biochemistry, 9, 3471–3479; reprinted in the Compendium (ref. 9).Google Scholar
  18. 21.
    IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN) (1984) Nomenclature and Symbolism for Amino Acids and Peptides, Recommendations 1983, Eur. J. Biochem., 138, 9–37; reprinted in the Compendium (ref. 9).Google Scholar
  19. 22.
    IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN) (1983) Abbreviations and Symbols for the Description of Conformations of Polynucleotide Chains, Recommendations 1982, Eur. J. Biochem., 131, 9–15; reprinted in the Compendium (ref. 9).Google Scholar
  20. 23.
    Hanson, K.R. (1966) Applications of the Sequence Rule. I. Naming the Paired Ligands g,g at a Tetrahedral Atom X ggij. II. Naming the Two Faces of a Trigonal Atom Y ghi, J. Am. Chem. Soc., 88, 2731–2742.Google Scholar
  21. 25.
    Cahn, R.S., Ingold, C.K. and Prelog, V. (1966) Specification of Molecular Chirality, Angew. Chem. Int. Ed. Engl., 5, 385–415; 511.Google Scholar
  22. 26.
    Prelog, V. and Helmchen, G. (1982) Basic Principles of the CIP-System and Proposals for a Revision, Angew. Chem. Int. Ed. Engl., 21, 567–583.Google Scholar
  23. 27.
    Blackwood, J.E., Gladys, C.L., Loening, K.L., Petrarca, A.E. and Rush, J.E. (1968) Unambiguous Specification of Stereoisomerism about a Double Bond, J. Am. Chem. Soc., 90, 509–510.Google Scholar
  24. 28.
    Blackwood, J.E., Gladys, C.L., Petrarca, A.E., Powell, W.H. and Rush, J.E. (1968) Unique and Unambiguous Specification of Stereoisomerism about a Double Bond in Nomenclature and Other Notation Systems, J. Chem. Doc., 8, 30–32.Google Scholar
  25. 29.
    IUPAC Commission on Nomenclature of Organic Chemistry (CNOC) (1976) Nomenclature of Organic Chemistry, Sec22 tion E: Stereochemistry, Recommendations 1974, Pure Appl. Chem., 45, 11–30 (1976); reprinted in the Compendium (ref. 9).Google Scholar
  26. 30.
    Wüthrich, K., Billeter, M. and Braun, W. (1983) Pseudo-Structures for the 20 Common Amino Acids for Use in Studies of Protein Conformations by Measurements of Intramolecular Proton-Proton Distance Constraints with Nuclear Magnetic Resonance, J. Mol. Biol., 169, 949–961.Google Scholar
  27. 32.
    Koning, T.M.G., Boelens, R. and Kaptein, R. (1990) Calculation of the Nuclear Overhauser Effect and Determination of Proton-Proton Distances in the Presence of Internal Motions, J. Magn. Reson., 90, 111–123.Google Scholar
  28. 33.
    Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley Interscience, New York, NY.Google Scholar
  29. 34.
    Güntert, P., Braun, W. and Wüthrich, K. (1991) Efficient Computation of Three-Dimensional Protein Structures in Solution from Nuclear Magnetic Resonance Data Using the Program DIANA and the Supporting Programs CALIBA, HABAS and GLOMSA, J. Mol. Biol., 217, 517–530.Google Scholar
  30. 35.
    Historical changes in the definition of these angles have contributed to confusion. Their use in numerous textbooks does not conform to the current IUPAC-IUBMB nomenclature: Clauwaert, J. and Xia, J.-Z. (1993) Straightening out the Dihedral Angles, Trends Biochem. Sci., 18, 317–318; 464.Google Scholar
  31. 36.
    Wilmott, C.M. and Thornton, J.M. (1990) β-Turns and their Distortions: A Proposed New Nomenclature, Protein Eng., 3, 479–493.Google Scholar
  32. 37.
    Richardson, J.S. (1981) The Anatomy and Taxonomy of Protein Structure, Adv. Protein Chem., 34, 167–339.Google Scholar
  33. 38.
    Milner-White, E.J., Bell, L.H. and Maccallum, P.H. (1992) Pyrrolidine Ring Puckering in cis- and trans-Proline Residues in Proteins and Polypeptides. Different Puckers are Favoured in Certain Situations, J. Mol. Biol., 228, 725–734.Google Scholar
  34. 39.
    De Leeuw, H.P.M., Haasnoot, C.A.G. and Altona, C. (1980) Empirical Correlations between Conformational Parameters in β-D-Furanoside Fragments Derived from a Statistical Survey of Crystal Structures of Nucleic Acid Constituents, Isr. J. Chem., 20, 108–126.Google Scholar
  35. 40.
    Haasnoot, C.A.G., De Leeuw, F.A.A.M., de Leeuw, H.P.M. and Altona, C. (1981) The Relationship between Proton-Proton NMR Coupling Constants and Substituent Electronegativities, Org. Magn. Reson., 15, 43–52.Google Scholar
  36. 41.
    Harris, R.K., Becker, E.D., Bremser, W., Cabral de Menezes, S., Goodfellow, R. and Granger, P. (1997) IUPAC (Commission on Molecular Structure and Spectroscopy, I.5) Recommendations for NMR Nomenclature. A. Nuclear Spin Properties and Conventions for Chemical Shifts (in preparation).Google Scholar
  37. 42.
    Wishart, D.S., Bigam, C.G., Yao, J., Abildgaard, F., Dyson, H.J., Oldfield, E., Markley, J.L. and Sykes, B.D. (1995) 1H, 13C and 15N Chemical Shift Referencing in Biomolecular NMR, J. Biomol. NMR., 6, 135–140.Google Scholar
  38. 44.
    Live, D.H., Davis, D.G., Agosta, W.C. and Cowburn, D. (1984) Long Range Hydrogen Bond Mediated Effects in Peptides: 15N NMR Study of Gramicidin S in Water and Organic Solvents, J. Am. Chem. Soc., 106, 1939–1943.Google Scholar
  39. 47.
    NOE distances may be represented rigorously by notation analogous to that used for J-couplings. However, since protons are always implied, a shorthand notation is widely used: for example, d αN for d HαHN, d NN for d HNHN, d βN for d HβHN, and d αβ for d HαHβ.Google Scholar
  40. 48.
    Williamson, M.P., Havel, T.F. and Wüthrich, K. (1985) Solution Conformation of Proteinase Inhibitor IIA from Bull Seminal Plasma by 1H NMR Spectroscopy and Distance Geometry, J. Mol. Biol., 182, 295–315.Google Scholar
  41. 49.
    Gronenborn, A.M. and Clore, G.M. (1994) Identification of N-Terminal Helix Capping Boxes by Means of 13C Chemical Shifts, J. Biomol. NMR, 4, 455–458.Google Scholar
  42. 50.
    Eberstadt, M., Gemmecker, G., Mierke, D.F. and Kessler, H. (1995) Scalar Coupling Constants-Their Analysis and their Application for the Elucidation of Structures, Angew. Chem. Int. Ed. Engl., 34, 1671–1695.Google Scholar
  43. 51.
    Ottiger, M., Szyperski, T., Luginbühl, L., Ortenzi, C., Luporini, P., Bradshaw, R.A. and Wüthrich, K. (1994) The NMR Solution Structure of the Pheromone Er-2 from the Ciliated Protozoan Euplotes raikovi, Protein Sci., 3, 1515–1526.Google Scholar
  44. 52.
    Saenger, W., (1983) Principles of Nucleic Acid Structure, Springer Verlag, New York, NY, pp. 123–124.Google Scholar
  45. 53.
    Sutcliffe, M.J. (1993) Representing an Ensemble of NMRDerived Protein Structures by a Single Structure, Protein Sci., 2, 936–944.Google Scholar
  46. 54.
    Fletcher, C.M., Jones, D.N.M., Diamond, R. and Neuhaus, D. (1996) Treatment of NOE Constraints Involving Equivalent or Nonstereoassigned Protons in Calculations of Biomacromolecular Structures, J. Biomol. NMR, 8, 292–310.Google Scholar
  47. 55.
    MacArthur, M.W. and Thornton, J.M. (1993) Conformational Analysis of Protein Structures Derived from NMR Data, Proteins, 17, 232–251.Google Scholar
  48. 56.
    Hyberts, S.G., Goldberg, M.S., Havel, T.F. and Wagner, G. (1992) The Solution Structure of Eglin c Based on Measurements of Many NOEs and Coupling Constants and its Comparison with X-ray Structures, Protein Sci., 1, 736–751.Google Scholar
  49. 57.
    Colovos, C. and Yeates, T.O. (1993) Verification of Protein Structures: Patterns of Nonbonded Atomic Interactions, Protein Sci., 2, 1511–1519.Google Scholar
  50. 58.
    Sippl, M.J. (1993) Recognition of Errors in 3–Dimensional Structures of Proteins, Proteins, 17, 355–362.Google Scholar
  51. 59.
    Vriend, G. and Sander, C. (1993) Quality Control of Protein Models: Directional Atomic Contact Analysis, J. Appl. Crystallogr., 26, 47–60.Google Scholar
  52. 60.
    MacArthur, M.W., Laskowski, R.A and Thornton, J.M. (1994) Knowledge-Based Validation of Protein-Structure Coordinates Derived by X-ray Crystallography and NMR Spectroscopy, Curr. Opin. Struct. Biol., 4, 731–737.Google Scholar
  53. 61.
    Laskowski, R.A., Rullmann, J.A.C., MacArthur, M.W., Kaptein, R. and Thornton, J.M. (1996) AQUA and PROCHECK-NMR: Programs for Checking the Quality of Protein Structures Solved by NMR. J. Biomol. NMR, 8, 477–486.Google Scholar
  54. 62.
    Jardetzky, O. and Roberts, G.C.K. (1981) NMR in Molecular Biology, Academic Press, New York, NY, pp. 126–142.Google Scholar
  55. 63.
    Watenpaugh, K.D., Berman, H.M., Bourne, P.E. and Fitzgerald, P.M.D. (1993) The Macromolecular CIF Dictionary, Acta Crystallogr. Ser. A, 49(Supplement), IVI International Congress (IUCr), Abstract OCM-18.02.07.Google Scholar
  56. 64.
    Fitzgerald, P.M.D., Berman, H., Bourne, P. and Watenpaugh, K. (1993) The Macromolecular CIF Dictionary, Abstract No. D008, American Crystallographic Association Annual Meeting, Albuquerque, NM, May 23–28 (available from: Scholar
  57. 65.
    Hall, S.R. and Spadaccini, N. (1994) The STAR File: Detailed Specifications, J. Chem. Inf. Comput. Sci., 34, 505–508.Google Scholar
  58. 66.
    Hall, S.R., Allen, F.H. and Brown, I.D. [International Union of Crystallography, Commission on Crystallographic Data, Commission on Journals, Working Party on Crystallographic Information] (1991) The Crystallographic Information File (CIF): a New Standard Archive File for Crystallography, Acta Crystallogr. Ser. A, 47, 655–685.Google Scholar
  59. 67.
    International Organization for Standardization (1987) Information Processing Systems-Open Systems Interconnection-Specification of Abstract Syntax Notation One (ASN.1), Technical Report ISO8824.Google Scholar
  60. 68.
    International Organization for Standardization (1987) Information Processing Systems-Open Systems Interconnection-Specification of Basic Encoding Rules for Abstract Syntax Notation One (ASN.1), Technical Report ISO8825.Google Scholar
  61. 69.
    Ostell, J. (1990) GenInfo ASN.1 Syntax: Sequences, Technical Report 1 & 2, National Center for Biotechnology Information, National Library of Medicine.Google Scholar
  62. 70.
    Mockus, J. and Steckert, T.D. (1994) CXF Chemical eXchange Format Version 1.0, Chemical Abstracts Service: Columbus, OH, USA.Google Scholar
  63. 71.
    Ulrich, E.L. and Markley, J.L. (1994) A Data Dictionary and Information File for the Exchange and Archiving of NMR Experimental Results, 35th Experimental Nuclear Magnetic Resonance Conference, April 10–15, Asilomar, CA, Abstract WP 112, p. 264. The BioMagResBank web pages ( contain complete information about this effort including user entry protocols and software.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • John L. Markley
    • 1
  • Ad Bax
    • 2
  • Yoji Arata
    • 3
  • C. W. Hilbers
    • 4
  • Robert Kaptein
    • 5
  • Brian D. Sykes
    • 6
  • Peter E. Wright
    • 7
  • Kurt Wüthrich
    • 8
  1. 1.Department of BiochemistryUniversity of Wisconsin-MadisonMadisonU.S.A
  2. 2.Laboratory of Chemical PhysicsNIDDK, National Institutes of HealthBethesdaU.S.A
  3. 3.Water Research InstituteTsukubaJapan
  4. 4.Laboratory of Biophysical ChemistryUniversity of NijmegenED NijmegenThe Netherlands
  5. 5.Department of ChemistryUniversity of UtrechtUtrechtThe Netherlands
  6. 6.Department of BiochemistryUniversity of AlbertaEdmontonCanada
  7. 7.Department of Molecular BiologyThe Scripps Research InstituteLa JollaU.S.A
  8. 8.Institut für Molekularbiologie und Biophysik, ETH-HönggerbergZürichSwitzerland

Personalised recommendations