Solution structure by NMR of circulin A: A macrocyclic knotted peptide having anti-HIV activity

Journal of Molecular Biology

Volumn 285, Issue 1, 1999, Pages 333-345

  Daly, Norelle L ^a   Koltay, Anita ^b   Gustafson, Kirk R ^c   Boyd, Michael R ^c   Casas Finet, Jose R ^d   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c NATIONAL CANCER INSTITUTE   (United States)

^d SAIC FREDERICK INC   (United States)

Author keywords

Anti HIV activity; Circulin A; Cyclic peptides; Cystine knot; NMR

Indexed keywords

CYCLOPEPTIDE; MACROCYCLIC COMPOUND; SOLVENT; TRYPTOPHAN;

ANTIVIRAL ACTIVITY; ARTICLE; CHEMICAL STRUCTURE; COMPUTER PROGRAM; DISULFIDE BOND; FLUORESCENCE SPECTROSCOPY; HIGHER PLANT; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE;

CHASSALIA; CHASSALIA PARVIFOLIA; CUCURBITA MAXIMA; EMBRYOPHYTA; HUMAN IMMUNODEFICIENCY VIRUS; RUBIACEAE;

EID: 0033534366     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2276     Document Type: Article

References (51)

1. Atkinson A. H., Heath R. L., Simpson R. J., Clarke A. E., Anderson M. A. Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. Plant Cell. 5:1993;203-213.
2. Bax A., Davis D. G. MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65:1985;355-360.
3. Boyd M. R. DeVita V. T., Hellman S., Rosenberg S. A. AIDS Etiology, Diagnosis, Treatment and Prevention. 1988;305-319 Lippincott, Philadelphia.
4. Braunschweiler L., Ernst R. R. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53:1983;521-528.
5. Broekaert W. F., Terras F. R. G., Cammue B. P. A., Osborn R. W. Plant defensins: novel antimicrobial peptides as components of the host defence system. Plant Physiol. 108:1995;1353-1358.
6. Brooks B. R., Bruccoleri R. E., Olafson B. D., States D. J., Swaminathan S., Karplus M. CHARM: a program for macromolecular energy minimization and dynamics calculations. J. Comput. Chem. 4:1983;187-217.
7. Brünger A. T. X-PLOR Manual Version 3.1. 1992;Yale University Press, New Haven.
8. Clore G. M., Nilges M., Sukuraman D. K., Brünger A. T., Karplus M., Gronenborn A. M. The three-dimensional structure of α1l-purothionin in solution: combined use of nuclear magnetic resonance, distance geometry and restrained molecular dynamics. EMBO J. 5:1986a;2729-2735.
9. Clore G. M., Brünger A. T., Karplus M., Gronenborn A. M. Application of molecular dynamics with interproton distance restraints to three-dimensional protein structure determination. A model study of crambin. J. Mol. Biol. 191:1986b;523-551.
10. Derua R., Gustafson K. R., Pannell L. K. Analysis of the disulfide linkage pattern in circulin A and B, HIV-inhibitory macrocyclic peptides. Biochem. Biophys. Res. Commun. 228:1996;632-638.
11. De Wit P. J. G. M. Fungal avirulence genes and plant resistance genes: unraveling the molecular basis of gene-for-gene interactions. Advan. Bot. Res. 21:1995;147-185.
12. Favel A., Mattras H., Coletti-Previero M. A., Zwilling R., Robinson E. A., Castro B. Protease inhibitors from Ecballium elaterium seeds. Int. J. Pept. Protein Res. 33:1988;202-208.
13. Flor H. H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:1971;275-296.
14. Gran L. An oxytocic principle found in Oldenlandia affinis DC. Medd. Nor. Farm. Selsk. 12:1970;173-180.
15. Gran L. 5-Hydroxytryptamine found in Oldenlandia affinis. Medd. Nor. Farm. Selsk. 34:1972;125-135.
16. Gran L. Isolation of oxytocic peptides from Oldenlandia affinis by solvent extraction of tetraphenylborate complexes and chromatography on sephadex LH-20. Lloydia. 36:1973;174-178.
17. Greisinger C., Sorenson O. W., Ernst R. R. Practical aspects of the E. COSY technique, measurement of scalar spin-spin coupling constants in peptides. J. Magn. Reson. 75:1987;474-492.
18. Gulakowski R. L., McMahon L. B., Staley P. G., Moran R. A., Boyd M. R. A semiautomated multiparameter approach for anti-HIV drug screening. J. Virol. Methods. 33:1991;87-100.
19. Gustafson K. R., Sowder R. C. II, Henderson L. E., Parsons 1. C., Kashman Y., Cardellina J. H. II, McMahon J. B., Buckheit R. W. Jr, Pannell L. K., Boyd M. R. Circulins A and B: Novel HIV-inhibitory macrocyclic peptides from the tropical tree Chassalia parvifolia. J. Am. Chem. Soc. 116:1994;9337-9338.
20. Harrison P. M., Sternberg M. J. E. The disulfide β-cross: from. cystine geometry and clustering to classification of small disulfide-rich protein folds. J. Mol. Biol. 264:1996;603-623.
21. Holak T. A., Bode W., Huber R., Otlewski J., Wilusz T. Nuclear magnetic resonance solution and X-ray structures of squash trypsin inhibitor exhibit the same conformation of the proteinase binding loop. J. Mol. Biol. 210:1989a;649-654.
22. Holak T. A., Gondol D., Otlewski J., Wilusz T. Determination of the complete three-dimensional structure of the trypsin inhibitor from squash seeds in aqueous solution by nuclear magnetic resonance and a combination of distance geometry and dynamical simulated annealing. J. Mol. Biol. 210:1989b;635-648.
23. Hutchinson E. G., Thornton J. M. PROMOTIF - A program to identify and analyze structural motifs in proteins. Protein Sci. 5:1996;212-220.
24. Hyberts S. G., Goldberg M. S., Havel T. S., Wagner G. The solution structure of eglin c based on measurements of many NOEs and coupling constants and its comparison with X-ray structures. Protein Sci. 1:1992;736-751.
25. Isaacs N. W. Cystine knots. Curr. Opin. Struct. Biol. 5:1995;391-395.
26. Jeener J., Meier B. H., Bachmann P., Ernst R. R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71:1979;4546-4553.
27. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113:1983;967-974.
28. McDonald N. Q., Hendrickson W. A. A structural superfamily of growth factors containing a cystine knot motif. Cell. 73:1993;421-424.
29. 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J. Biomol. NMR. 5:1995;14-24.
30. 1H NMR determination of the three-dimensional structures of mirror-image forms of a Leu-5 variant of the trypsin inhibitor from Ecballium elaterium (EETI-II). Protein Sci. 3:1994a;291-302.
31. 1H NMR of a 6-kDa proteinase inhibitor isolated from the stigma of Nicotiana alata. J. Mol. Biol. 242:1994b;231-243.
32. Nielsen K. J., Heath R. L., Anderson M. A., Craik D. J. Structures of a series of 6-kDa trypsin inhibitors isolated from the stigma of Nicotiana alata. Biochemistry. 34:1995;14304-14311.
33. Nilges M., Gronenborn A. M., B r̈ A. T., Clore G. M. Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2. Protein Eng. 2:1988;27-38.
34. 1H NMR studies of the solution conformations of an analogue of the C-peptide of ribonuclease A. Biochemistry. 28:1989;7059-7064.
35. Pallaghy P. K., Nielsen K. J., Craik D. J., Norton R. S. A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides. Protein Sci. 3:1994;1833-1839.
36. Piotto M., Saudek V., Sklenar V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR. 2:1992;661-665.
37. 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117:1983;479-485.
38. Richardson J. S. The anatomy and taxonomy of protein structure. Advan. Protein Chem. 34:1981;167-339.
39. Saether O., Craik D. J., Campbell I. D., Sletten K., Juul J., Norman D. G. Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1. Biochemistry. 34:1995;4147-4158.
40. Srinivasan N., Sowdhamini R., Ramakrishnan C., Balaram P. Conformation of disulfide bridges in proteins. Int. J. Pept. Protein Res. 36:1990;147-155.
41. Thornton J. M. Disulfide bridges in globular proteins. J. Mol. Biol. 151:1981;261-287.
42. Van den Ackerveken G. F. J. M., Vossen J. P. M. J., De Wit P. J. G. M. The AVR9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases. Plant Physiol. 103:1993;91-96.
43. Van Wagenen B. C., Larse R., Cardellina J. H. II, Randazzo D., Lidert Z. C., Swithenbank C. Ulosantoin, a potent insecticide from sponge Ulosa ruetzleri. J. Org. Chem. 58:1993;335-337.
44. 1H NMR assignments, secondary structure and global fold of the protein. FEBS Letters. 404:1997;153-158.
45. 1H nuclear magnetic resonance and distance geometry. J. Mol. Biol. 182:1985;295-315.
46. Wilson J. C., Nielsen K. J., McLeish M. J., Craik D. J. A determination of the solution conformation of the nonmammalian tachykinin eledoisin by NMR and CD spectroscopy. Biochemistry. 33:1994;6802-6811.
47. 13C chemical-shift data. J. Biomol. NMR. 4:1994;171-180.
48. Wishart D. S., Sykes B. D., Richards F. M. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry. 31:1992;1647-1651.
49. Witherup K. M., Bogusky M. L., Anderson P. S., Ramjit H., Ransom R. W., Wood T., Sardana M. Cyclopsychotride A, a biologically active, 31-residue cyclic peptide isolated from Psychotria longipes. J. Nat. Prod. 57:1994;1619-1625.
50. Wüthrich K. NMR of Proteins and Nucleic Acids. 1986;Wiley-Interscience, New York.
51. Wüthrich K., Billeter M., Braun W. 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. 169:1983;949-961.