Nuclear magnetic resonance (NMR) solution structure, dynamics, and binding properties of the kringle IV type 8 module of apolipoprotein(a)

Biochemistry

Volumn 46, Issue 7, 2007, Pages 1732-1742

  Chitayat, Seth ^a   Kanelis, Voula ^b   Koschinsky, Marlys L ^a   Smith, Steven P ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; CONFORMATIONS; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE;

BINDING PROPERTIES; KRINGLE MODULES; LYSINE ANALOGUES; PLASMINOGENS;

PROTEINS;

AMINOCAPROIC ACID; APOLIPOPROTEIN A; APOLIPOPROTEIN B100; ARGININE; CELL SURFACE RECEPTOR; FIBRIN; LYSINE; PLASMINOGEN; TYROSINE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; COVALENT BOND; HYDROPHOBICITY; KRINGLE DOMAIN; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE;

6-AMINOCAPROIC ACID; AMINO ACID MOTIFS; APOLIPOPROTEINS A; KRINGLES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN BINDING; SOLUTIONS;

EID: 33847078064     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061814g     Document Type: Article

References (61)

1. Brunner, C., Kraft, H. G., Utermann, G., and Muller, H. J. (1993) Cys4057 of apolipoprotein(a) is essential for lipoprotein(a) assembly, Proc. Natl. Acad. Sci. U.S.A. 90, 11643-11647.
2. Koschinsky, M. L., Cote, G. P., Gabel, B., and van der Hoek, Y. Y. (1993) Identification of the cysteine residue in apolipoprotein(a) that mediates extracellular coupling with apolipoprotein B-100, J. Biol. Chem. 268, 19819-19825.
3. Fless, G. M., ZumMallen, M. E., and Scanu, A. M. (1986) Physicochemical properties of apolipoprotein(a) and lipoprotein(a-) derived from the dissociation of human plasma lipoprotein (a), J. Biol. Chem. 261, 8712-8718.
4. McLean, J. W., Tomlinson, J. E., Kuang, W. J., Eaton, D. L., Chen, E. Y., Fless, G. M., Scanu, A. M., and Lawn, R. M. (1987) cDNA sequence of human apolipoprotein(a) is homologous to plasminogen, Nature 330, 132-137.
5. Lackner, C., Cohen, J. C., and Hobbs, H. H. (1993) Molecular definition of the extreme size polymorphism in apolipoprotein(a), Hum. Mol. Genet. 2, 933-940.
6. van der Hoek, Y. Y., Wittekoek, M. E., Beisiegel, U., Kastelein, J. J., and Koschinsky, M. L. (1993) The apolipoprotein(a) kringle IV repeats which differ from the major repeat kringle are present in variably-sized isoforms, Hum. Mol. Genet. 2, 361-366.
7. Marcovina, S. M., and Koschinsky, M. L. (2002) A critical evaluation of the role of Lp(a) in cardiovascular disease: Can Lp(a) be useful in risk assessment? Semin. Vasc. Med. 2, 335-344.
8. Koschinsky, M. L., and Marcovina, S. M. (2004) Structure-function relationships in apolipoprotein(a): Insights into lipoprotein(a) assembly and pathogenicity, Curr. Opin. Lipidol. 15, 167-174.
9. Boffa, M. B., Marcovina, S. M., and Koschinsky, M. L. (2004) Lipoprotein(a) as a risk factor for atherosclerosis and thrombosis: Mechanistic insights from animal models, Clin. Biochem. 37, 333-343.
10. Catena, C., Novello, M., Lapenna, R., Baroselli, S., Colussi, G., Nadalini, E., Favret, G., Cavarape, A., Soardo, G., and Sechi, L. A. (2005) New risk factors for atherosclerosis in hypertension: Focus on the prothrombotic state and lipoprotein(a), J. Hypertens. 23, 1617-1631.
11. Koschinsky, M. L. (2005) Lipoprotein(a) and atherosclerosis: New perspectives on the mechanism of action of an enigmatic lipoprotein, Curr. Atheroscler. Rep. 7, 389-395.
12. Becker, L., Cook, P. M., Wright, T. G., and Koschinsky, M. L. (2004) Quantitative evaluation of the contribution of weak lysine-binding sites present within apolipoprotein(a) kringle IV types 6-8 to lipoprotein(a) assembly, J. Biol. Chem. 279, 2679-2688.
13. Becker, L., McLeod, R. S., Marcovina, S. M., Yao, Z., and Koschinsky, M. L. (2001) Identification of a critical lysine residue in apolipoprotein B-100 that mediates noncovalent interaction with apolipoprotein(a), J. Biol. Chem. 276, 36155-36162.
14. Caterer, N. R., Graversen, J. H., Jacobsen, C., Moestrup, S. K., Sigurskjold, B. W., Etzerodt, M., and Thogersen, H. C. (2002) Specificity determinants in the interaction of apolipoprotein(a) kringles with tetranectin and LDL, Biol. Chem. 383, 1743-1750.
15. Gabel, B. R., and Koschinsky, M. L. (1998) Sequences within apolipoprotein(a) kringle IV types 6-8 bind directly to low-density lipoprotein and mediate noncovalent association of apolipoprotein(a) with apolipoprotein B-100, Biochemistry 37, 7892-7898.
16. Trieu, V. N., and McConathy, W. J. (1998) Functional characterization of T7 and T8 of human apolipoprotein (a), Biochem. Biophys. Res. Commun. 251, 356-359.
17. Guevara, J., Jr., Spurlino, J., Jan, A. Y., Yang, C. Y., Tulinsky, A., Prasad, B. V., Gaubatz, J. W., and Morrisett, J. D. (1993) Proposed mechanisms for binding of apo[a] kringle type 9 to apo B-100 in human lipoprotein[a], Biophys. J. 64, 686-700.
18. Guevara, J., Jr., Valentinova, N. V., Garcia, O., Gotto, A. M., Yang, C. Y., Legal, S., Gaubatz, J., and Sparrow, J. T. (1996) Interaction of apolipoprotein[a] with apolipoproteinB-100 Cys3734 region in lipoprotein[a] is confirmed immunochemically, J. Protein Chem. 15, 17-25.
19. Callow, M. J., and Rubin, E. M. (1995) Site-specific mutagenesis demonstrates that cysteine 4326 of apolipoprotein B is required for covalent linkage with apolipoprotein (a) in vivo, J. Biol. Chem. 270, 23914-23917.
20. McCormick, S. P., Ng, J. K., Taylor, S., Flynn, L. M., Hammer, R. E., and Young, S. G. (1995) Mutagenesis of the human apolipoprotein B gene in a yeast artificial chromosome reveals the site of attachment for apolipoprotein(a), Proc. Natl. Acad. Sci. U.S.A. 92, 10147-10151.
21. Frank, S., Durovic, S., Kostner, K., and Kostner, G. M. (1995) Inhibitors for the in vitro assembly of Lp(a), Arterioscler., Thromb., Vasc. Biol. 15, 1774-1780.
22. Gabel, B. R., May, L. F., Marcovina, S. M., and Koschinsky, M. L. (1996) Lipoprotein(a) assembly. Quantitative assessment of the role of apo(a) kringle IV types 2-10 in particle formation, Arterioscler., Thromb., Vasc. Biol. 16, 1559-1567.
23. Koschinsky, M. L., and Marcovina, S. M. (1997) Lipoprotein(a): Structural implications for pathophysiology, Int. J. Clin. Lab. Res. 27, 14-23.
24. Ernst, A., Helmhold, M., Brunner, C., Petho-Schramm, A., Armstrong, V. W., and Muller, H. J. (1995) Identification of two functionally distinct lysine-binding sites in kringle 37 and in kringles 32-36 of human apolipoprotein(a), J. Biol. Chem. 270, 6227-6234.
25. Gabel, B. R., McLeod, R. S., Yao, Z., and Koschinsky, M. L. (1998) Sequences within the amino terminus of ApoB100 mediate its noncovalent association with apo(a), Arterioscler., Thromb., Vasc. Biol. 18, 1738-1744.
26. Trieu, V. N., and McConathy, W. J. (1995) A two-step model for lipoprotein(a) formation, J. Biol. Chem. 270, 15471-15474.
27. Maderegger, B., Bermel, W., Hrzenjak, A., Kostner, G. M., and Sterk, H. (2002) Solution structure of human apolipoprotein(a) kringle IV type 6, Biochemistry 41, 660-668.
28. LoGrasso, P. V., Cornell-Kennon, S., and Boettcher, B. R. (1994) Cloning, expression, and characterization of human apolipoprotein(a) kringle IV37, J. Biol. Chem. 269, 21820-21827.
29. Mikol, V., LoGrasso, P. V., and Boettcher, B. R. (1996) Crystal structures of apolipoprotein(a) kringle IV37 free and complexed with 6-aminohexanoic acid and with p-aminomethylbenzoic acid: Existence of novel and expected binding modes, J. Mol. Biol. 256, 751-761.
30. Mochalkin, I., Cheng, B., Klezovitch, O., Scanu, A. M., and Tulinsky, A. (1999) Recombinant kringle IV-10 modules of human apolipoprotein(a): Structure, ligand binding modes, and biological relevance, Biochemistry 38, 1990-1998.
31. Rahman, M. N., Becker, L., Petrounevitch, V., Hill, B. C., Jia, Z., and Koschinsky, M. L. (2002) Comparative analyses of the lysine binding site properties of apolipoprotein(a) kringle IV types 7 and 10, Biochemistry 41, 1149-1155.
32. Ye, Q., Rahman, M. N., Koschinsky, M. L., and Jia, Z. (2001) High-resolution crystal structure of apolipoprotein(a) kringle IV type 7: Insights into ligand binding, Protein Sci. 10, 1124-1129.
33. Sotiriou, S. N., Orlova, V. V., Al-Fakhri, N., Ihanus, E., Economopoulou, M., Isermann, B., Bdeir, K., Nawroth, P. P., Preissner, K. T., Gahmberg, C. G., Koschinsky, M. L., and Chavakis, T. (2006) Lipoprotein(a) in atherosclerotic plaques recruits inflammatory cells through interaction with Mac-1 integrin, FASEB J. 20, 559-561.
34. Barre, D. E. (2006) Arginyl-glycyl-aspartyl (ROD) epitope of human apolipoprotein (a) inhibits platelet aggregation by antagonizing the lib subunit of the fibrinogen (GPIIb/IIIa) receptor, Thromb. Res., in press.
35. Kay, L., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
36. Wittekind, M., and Mueller, L. (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the α- and β-carbon resonances, J. Magn. Reson., Ser. B 101, 171-180.
37. 15N- enriched proteins, J. Biomol. NMR 3, 185-204.
38. α J couplings in calcium-free calmodulin using new 2D and 3D water-flip-back methods, J. Biomol. NMR 4, 871-878.
39. α J-couplings in staphylococcal nuclease, J. Biomol. NMR 4, 193-200.
40. Muhandiram, D. R., and Kay, L. E. (1994) Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity, J. Magn. Reson., Ser. B 103, 203-216.
41. 2O samples of proteins, J. Magn. Reson., Ser. B 101, 333-337.
42. 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.
43. 2O, J. Magn. Reson., Ser. B 103, 197-201.
44. Schleucher, J., Schwendinger, M., Sattler, M., Schmidt, P., Schedletzky, O., Glaser, S. J., Sorensen, O. W., and Griesinger, C. (1994) A general enhancement scheme in heteronuclear multidimensional NMR employing pulsed field gradients, J. Biomol. NMR 4, 301-306.
45. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
46. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules, Methods Mol. Biol. 278, 313-352.
47. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium, J. Biomol. NMR 4, 727-734.
48. Palmer, A. G., III (1997) Probing molecular motion by NMR, Curr. Opin. Struct. Biol. 7, 732-737.
49. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (part 5), 905-921.
50. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology, J. Biomol. NMR 13, 289-302.
51. δ carbons of leucine residues in staphylococcal nuclease, J. Biomol. NMR 3, 297-306.
52. Laskowski, R., MacArthur, M., Moss, D., and Thornton, J. (1993) PROCHECK: A program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
53. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 29-32, 51-55.
54. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
55. Zajicek, J., Chang, Y., and Castellino, F. J. (2000) The effects of ligand binding on the backbone dynamics of the kringle 1 domain of human plasminogen, J. Mol. Biol. 301, 333-347.
56. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease, Biochemistry 28, 8972-8979.
57. 15N relaxation studies of the amino-terminal fragment of urokinase-type plasminogen activator, Biochemistry 33, 15418-15424.
58. Marti, D. N., Schaller, J., and Llinas, M. (1999) Solution structure and dynamics of the plasminogen kringle 2-AMCHA complex: 3(1)-helix in homologous domains, Biochemistry 38, 15741-15755.
59. Nielsen, P. R., Einer-Jensen, K., Holtet, T. L., Andersen, B. D., Poulsen, F. M., and Thogersen, H. C. (1993) Protein-ligand interactions in the lysine-binding site of plasminogen kringle 4 are different in crystal and solution. Electrostatic interactions studied by site-directed mutagenesis exclude Lys35 as an important acceptor in solution, Biochemistry 32, 13019-13025.
60. Leahy, D. J., Aukhil, I., and Erickson, H. P. (1996) 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region, Cell 84, 155-164.
61. + binding site on the MurB enzyme by NMR, Nat. Struct. Biol. 3, 995-997.