The structure, dynamics, and binding of the LA45 module pair of the low-density lipoprotein receptor suggest an important role for LA4 in ligand release

Biochemistry

Volumn 50, Issue 51, 2011, Pages 11001-11008

  Guttman, Miklos ^a   Komives, Elizabeth A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACKBONE DYNAMICS; CALCIUM BINDING; CHEMICAL SHIFT PERTURBATIONS; INTER-MODULE; LIGAND AFFINITY; LIGAND BINDING; LOW DENSITY LIPOPROTEINS; NUCLEAR OVERHAUSER EFFECTS; PHYSIOLOGICAL PH; SOLUTION STRUCTURES;

BINDING ENERGY; CRYSTAL STRUCTURE; DYNAMICS; LIGANDS; PH;

NUCLEAR MAGNETIC RESONANCE;

APOENZYME; LOW DENSITY LIPOPROTEIN RECEPTOR;

ARTICLE; BINDING AFFINITY; CALCIUM BINDING; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN REFOLDING; PROTEIN STRUCTURE; TITRIMETRY;

APOLIPOPROTEINS E; BINDING SITES; CALCIUM; CALORIMETRY; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; LIGANDS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN REFOLDING; RECEPTORS, LDL; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; THERMODYNAMICS; TITRIMETRY;

EID: 84055193068     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2014486     Document Type: Article

References (55)

1. Blacklow, S. C. (2007) Versatility in ligand recognition by LDL receptor family proteins: Advances and frontiers Curr. Opin. Struct. Biol. 17, 419-426 (Pubitemid 47451775)
2. Rudenko, G., Henry, L., Henderson, K., Ichtchenko, K., Brown, M. S., Goldstein, J. L., and Deisenhofer, J. (2002) Structure of the LDL receptor extracellular domain at endosomal pH Science 298, 2353-2358 (Pubitemid 36014201)
3. Zhao, Z. and Michaely, P. (2009) The Role of Calcium in Lipoprotein Release by the Low-Density Lipoprotein Receptor Biochemistry 48, 7313-7324
4. Fass, D., Blacklow, S., Kim, P. S., and Berger, J. M. (1997) Molecular basis of familial hypercholesterolaemia from structure of LDL receptor module Nature 388, 691-693 (Pubitemid 27366442)
5. Simonovic, M., Dolmer, K., Huang, W., Strickland, D. K., Volz, K., and Gettins, P. G. W. (2001) Calcuim coordination and pH dependence of the calcium affinity of ligand-binding repeat CR7 from the LRP. Comparision with related domains from the LRP and the LDL receptor Biochemistry 40, 15127-15134 (Pubitemid 33151927)
6. Fisher, C., Beglova, N., and Blacklow, S. C. (2006) Structure of an LDLR-RAP complex reveals a general mode for ligand recognition by lipoprotein receptors Mol. Cell 22, 277-283
7. Daly, N. L., Scanlon, M. J., Djordijevic, J. T., Kroon, P. A., and Smith, R. (1995) Three-dimernsional structure of a cysteine-rich repeat from the low-density lipoprotein receptor Proc. Natl. Acad. Sci. U.S.A. 92, 6334-6338
8. Daly, N. L., Djordjevic, J. T., Kroon, P. A., and Smith, R. (1995) Three-dimensional structure of the second cysteine-rich repeat from the human low-density lipoprotein receptor Biochemistry 34, 14474-14481
9. North, C. L. and Blacklow, S. C. (2000) Solution structure of the sixth LDL-A module of the LDL receptor Biochem. J. 39, 2564-2571 (Pubitemid 30148908)
10. Guo, Y., Yu, X., Rihani, K., Wang, Q. Y., and Rong, L. (2004) The role of a conserved acidic residue in calcium-dependent protein folding for a low density lipoprotein (LDL)-A module: Implications in structure and function for the LDL receptor superfamily J. Biol. Chem. 279, 16629-16637 (Pubitemid 38509364)
11. Blacklow, S. C. and Kim, P. S. (1996) Protein folding and calcium binding defects arising from familial hypercholesterolemia mutations of the LDL receptor Nat. Struct. Biol. 3, 758-762 (Pubitemid 26303401)
12. Jeon, H. and Shipley, G. G. (2000) Vesicle-reconstituted low density lipoprotein receptor. Visualization by cryoelectron microscopy J. Biol. Chem. 275, 30458-30464
13. Bieri, S., Atkins, A. R., Lee, H. T., Winzor, D. J., Smith, R., and Kroon, P. A. (1998) Folding, Calcium Binding, and Structural Characterization of a Concatemer of the First and Second Ligand-Binding Modules of the Low-Density Lipoprotein Receptor Biochemistry 37, 10994-11002 (Pubitemid 28368924)
14. Kurniawan, N. D., Atkins, A. R., Bieri, S., Brown, C. J., Brereton, I. M., Kroon, P. A., and Smith, R. (2000) NMR structure of a concatemer of the first and second ligand-binding modules of the human low-density lipoprotein receptor Protein Sci. 9, 1282-1293 (Pubitemid 30602281)
15. North, C. L. and Blacklow, S. C. (1999) Structural independence of ligand-binding modules five and six of the LDL receptor Biochem. J. 38, 3926-3935
16. Esser, V., Limbird, L. E., Brown, M. S., Goldstein, J. L., and Russell, D. W. (1988) Mutational analysis of the ligand binding domain of the low density lipoprotein receptor J. Biol. Chem. 263, 13282-13290
17. Russell, D. W., Brown, M. S., and Goldstein, J. L. (1989) Different combinations of cysteine-rich repeats mediate binding of low density lipoprotein receptor to two different proteins J. Biol. Chem. 264, 21682-21688 (Pubitemid 20028736)
18. Fisher, C., Abdul-Aziz, D., and Blacklow, S. C. (2004) A two-module region of the low-density lipoprotein receptor sufficient for formation of complexes with apolipoprotein E ligands Biochem. J. 43, 1037-1044 (Pubitemid 38141503)
19. Yamamoto, T. and Ryan, R. O. (2009) Domain swapping reveals that low density lipoprotein (LDL) type A repeat order affects ligand binding to the LDL receptor J. Biol. Chem. 284, 13396-133400
20. Ren, G., Rudenko, G., Ludtke, S. J., Deisenhofer, J., Chiu, W., and Pownall, H. J. (2010) Model of human low-density lipoprotein and bound receptor based on cryoEM Proc. Natl. Acad. Sci. U.S.A. 107, 1059-1064
21. Guttman, M., Prieto, J. H., Croy, J. E., and Komives, E. A. (2010) Decoding of lipoprotein-receptor interactions: Properties of ligand binding modules governing interactions with ApoE Biochemistry 49, 1207-1216
22. Jez, J. M., Ferrer, J. L., Bowman, M. E., Dixon, R. A., and Noel, J. P. (2000) Dissection of Malonyl-Coenzyme A Decarboxylation from Polyketide Formation in the Reaction Mechanism of a Plant Polyketide Synthase Biochemistry 39, 890-902 (Pubitemid 30075315)
23. Grzesiek, S. and Bax, A. (1992) An Efficient Experiment for Sequential Backbone Assignment of Medium-Sized Isotopically Enriched Proteins J. Magn. Reson. 99, 201-207
24. Grzesiek, S. and Bax, A. (1992) Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR J. Am. Chem. Soc. 114, 6291-6293
25. Kay, L. E., Ikura, M., Tschudin, R., and Bax, A. (1990) Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins J. Magn. Reson. 89, 496-514
26. 15N-labelled proteins J. Biomol. NMR 3, 349-354
27. Talluri, S. and Wagner, G. (1996) An Optimized 3D NOESY-HSQC J. Magn. Reson. 112, 200-205 (Pubitemid 126758725)
28. Bax, A., Clore, G. M., and Gronenborn, A. M. (1990) Proton-proton correlation via isotropic mixing of carbon-13 magnetization, a new three-dimensional approach for assigning proton and carbon-13 spectra of carbon-13-enriched proteins J. Magn. Reson. 88, 425-431
29. 13C-labeled protein using constant-time evolution J. Biomol. NMR 1, 299-304
30. Zuiderweg, E. R. P., McIntosh, L. P., Dahlquist, F. W., and Fesik, S. W. (1990) Three-dimensional carbon-13-resolved proton NOE spectroscopy of uniformly carbon-13-labeled proteins for the NMR assignment and structure determination of larger molecules J. Magn. Reson. 86, 210-216
31. Delaglio, F., Grzesiek, S., Vuister, G., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
32. Goddard, T. D. and Kneller, D. G. (2007) SPARKY 3, University of California, San Francisco.
33. Cordier, F., Dingley, A. J., and Grzesiek, S. (1999) A doublet-separated sensitivity-enhanced HSQC for the determination of scalar and dipolar one-bond J-couplings J. Biomol. NMR 13, 175-180 (Pubitemid 29089227)
34. Rieping, W., Habeck, M., Bardiaux, B., Bernard, A., Malliavin, T. E., and Nilges, M. (2007) ARIA2: Automated NOE assignment and data integration in NMR structure calculation Bioinformatics 23, 381-382 (Pubitemid 46323164)
35. 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, 298-302
36. Warren, J. J. and Moore, P. B. (2001) A Maximum Likelihood Method for Determining DaPQ and R for Sets of Dipolar Coupling Data J. Magn. Reson. 149, 271-275
37. Brunger, A. T. (2007) Version 1.2 of the Crystallography and NMR System Nat. Protoc. 2, 2728-2733
38. Jensen, G. A., Andersen, O. M., Bonvin, A. M., Bjerrum-Bohr, I., Etzerodt, M., Thøgersen, H. C., O'Shea, C., Poulsen, F. M., and Kragelund, B. B. (2006) Binding site structure of one LRP-RAP complex: Implications for a common ligand-receptor binding motif J. Mol. Biol. 362, 700-716 (Pubitemid 44332418)
39. Maiti, R., Van Domselaar, G. H., Zhang, H., and Wishart, D. S. (2004) SuperPose: A simple server for sophisticated structural superposition Nucleic Acids Res. 32, 590-594
40. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
41. 2 J. Mol. Biol. 281, 341-361 (Pubitemid 28360598)
42. García de la Torre, J., Huertas, M. L., and Carrasco, B. (2000) HYDRONMR: Prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations J. Magn. Reson. 147, 138-146
43. Hoffman, R. M. B., Li, M. X., and Sykes, B. D. (2005) The Binding of W7, an Inhibitor of Striated Muscle Contraction, to Cardiac Troponin C Biochemistry 44, 15750-15759 (Pubitemid 41746906)
44. 2+ binding to complement-type repeat domains 5 and 6 from the low-density lipoprotein receptor-related protein BMC Biochem. 4 (7) 1-7 (Pubitemid 38783245)
45. Rudenko, G. and Deisenhofer, J. (2003) The low-density lipoprotein receptor: Ligands, debates and lore Curr. Opin. Struct. Biol. 13, 683-689 (Pubitemid 37522143)
46. Zweckstetter, M. (2008) NMR: Prediction of molecular alignment from structure using the PALES software Nat. Protoc. 3, 679-690 (Pubitemid 351522648)
47. Andersen, O. M., Schwarz, F. P., Eisenstein, E., Jacobsen, C., Moestrup, S. K., Etzerodt, M., and Thøgersen, H. C. (2001) Dominant thermodynamic role of the third independent receptor binding site in the receptor-associated protein RAP Biochem. J. 40, 15408-15417 (Pubitemid 33151957)
48. Abdul-Aziz, D., Fisher, C., Beglova, N., and Blacklow, S. C. (2005) Folding and binding integrity of variants of a prototype ligand-binding module from the LDL receptor possessing multiple alanine substitutions Biochem. J. 44, 5075-5085 (Pubitemid 40471223)
49. Marshall, W. J. (1995) in Clinical Chemistry, Mosby, London.
50. Gerasimenko, J. V., Tepikin, A. V., Petersen, O. H., and Gerasimenko, O. V. (1998) Calcium uptake via endocytosis with rapid release from acidifying endosomes Curr. Biol. 8, 1335-1338 (Pubitemid 29006710)
51. 2+ affinity of the fifth binding module of the LDL receptor J. Biol. Chem. 283, 22670-22679
52. Ruiz, J., Kouiavskaia, D., Migliorini, M., Robinson, S., Saenko, E. L., Gorlatova, N., Li, D., Lawrence, D., Hyman, B. T., Weisgraber, K. H., and Strickland, D. K. (2005) The apoE isoform binding properties of the VLDL receptor reveal marked differences from LRP and the LDL receptor J. Lipid Res. 46, 1721-1731 (Pubitemid 41099339)
53. Murphy, J. M., Hansen, F. D., Wiesner, S., Muhandiram, R. D., Borg, M., Smith, M. J., Sicheri, F., Kay, L. E., Forman-Kay, J. D., and Pawson, T. (2009) Structural Studies of FF Domains of the Transcription Factor CA150 Provide Insights into the Organization of FF Domain Tandem Arrays J. Mol. Biol. 393, 409-424
54. Spitzafden, C., Grant, R. P., Mardon, H. J., and Campbell, I. D. (1997) Module-Module Interactions in the Cell Binding Region of Fibronectin: Stability, Flexibility and Specificity J. Mol. Biol. 265, 565-579 (Pubitemid 27113041)
55. Beglova, N., North, C. L., and Blacklow, S. C. (2001) Backbone dynamics of a module pair from the ligand-binding domain of the LDL receptor Biochemistry 40, 2808-2815 (Pubitemid 32198282)