Structural analysis of nanoscale self-assembled discoidal lipid bilayers by solid-state NMR spectroscopy

Biophysical Journal

Volumn 91, Issue 10, 2006, Pages 3819-3828

  Li, Ying ^a   Kijac, Aleksandra Z ^a   Sligar, Stephen G ^a   Rienstra, Chad M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A1; CARBON 13; HIGH DENSITY LIPOPROTEIN; MACROGOL; MEMBRANE SCAFFOLD PROTEIN 1; PROLINE DERIVATIVE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; LIPID BILAYER; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SOLID STATE;

EID: 33751237696     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.087072     Document Type: Article

References (70)

1. Gordon, T., W. P. Castelli, M. C. Hjortland, W. B. Kannel, and T. R. Dawber. 1977. High density lipoprotein as a protective factor against coronary heart disease. The Framingham Study. Am. J. Med. 62:707-714.
2. Asztalos, B. F., L. A. Cupples, S. Demissie, K. V. Horvath, C. E. Cox, M. C. Batista, and E. J. Schaefer. 2004. High-density lipoprotein sub-population profile and coronary heart disease prevalence in male participants of the Framingham Offspring Study. Arterioscler. Thromb. Vasc. Biol. 24:2181-2187.
3. Glomset, J. A. 1968. The plasma lecithins:cholesterol acyltransferase reaction. J. Lipid Res. 9:155-167.
4. Fielding, C. J., and P. E. Fielding. 1995. Molecular physiology of reverse cholesterol transport. J. Lipid Res. 36:211-228.
5. Barter, P. J., and K. A. Rye. 1996. Molecular mechanisms of reverse cholesterol transport. Curr. Opin. Lipidol. 7:82-87.
6. Colvin, P. L., and J. S. Parks. 1999. Metabolism of high density lipoprotein subfractions. Curr. Opin. Lipidol. 10:309-314.
7. Jonas, A. 2000. Lecithin cholesterol acyltransferase. Biochim. Biophys. Acta. 1529:245-256.
8. Krieger, M. 1999. Charting the fate of the "good cholesterol": identification and characterization of the high-density lipoprotein receptor SR-BI. Annu. Rev. Biochem. 68:523-558.
9. Segrest, J. P., S. C. Harvey, and V. Zannis. 2000. Detailed molecular model of apolipoprotein A-I on the surface of high-density lipoproteins and its functional implications. Trends Cardiovasc. Med. 10:246-252.
10. Bayburt, T. H., Y. V. Grinkova, and S. G. Sligar. 2002. Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett. 2:853-856.
11. Denisov, I. G., Y. V. Grinkova, A. A. Lazarides, and S. G. Sligar. 2004. Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J. Am. Chem. Soc. 126:3477-3487.
12. Baas, B. J., I. G. Denisov, and S. G. Sligar. 2004. Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch. Biochem. Biophys. 430:218-228.
13. Bayburt, T. H., and S. G. Sligar. 2002. Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks. Proc. Natl. Acad. Sci. USA. 99:6725-6730.
14. Civjan, N. R., T. H. Bayburt, M. A. Schuler, and S. G. Sligar. 2003. Direct solubilization of heterologously expressed membrane proteins by incorporation into nanoscale lipid bilayers. Biotechniques. 35:556-560, 562-553.
15. Duan, H., N. R. Civjan, S. G. Sligar, and M. A. Schuler. 2004. Co-incorporation of heterologously expressed Arabidopsis cytochrome P450 and P450 reductase into soluble nanoscale lipid bilayers. Arch. Biochem. Biophys. 424:141-153.
16. Bayburt, T. H., Y. V. Grinkova, and S. G. Sligar. 2006. Assembly of single bacteriorhodopsin trimers in bilayer Nanodiscs. Arch. Biochem. Biophys. 450:215-222.
17. Bayburt, T. H., and S. G. Sligar. 2003. Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers. Protein Sci. 12:2476-2481.
18. Leitz, A. J., T. H. Bayburt, A. N. Barnakov, B. A. Springer, and S. G. Sligar. 2006. Functional reconstitution of beta2-adrenergic receptors utilizing self-assembling Nanodisc technology. Biotechniques. 40:601-612.
19. Frank, P. G., and Y. L. Marcel. 2000. Apolipoprotein A-I: structure-function relationships. J. Lipid Res. 41:853-872.
20. Ajees, A. A., G. M. Anantharamaiah, V. K. Mishra, M. M. Hussain, and H. M. Murthy. 2006. Crystal structure of human apolipoprotein A-I: insights into its protective effect against cardiovascular diseases. Proc. Natl. Acad. Sci. USA. 103:2126-2131.
21. Borhani, D. W., D. P. Rogers, J. A. Engler, and C. G. Brouillette. 1997. Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation. Proc. Natl. Acad. Sci. USA. 94:12291-12296.
22. Koppaka, V. 2001. Structural studies of discoidal lipoprotein A-I. Cell. Mol. Life Sci. 58:885-893.
23. Brouillette, C. G., G. M. Anantharamaiah, J. A. Engler, and D. W. Borhani. 2001. Structural models of human apolipoprotein A-I: a critical analysis and review. Biochim. Biophys. Acta. 1531:4-46.
24. Nissen, S. E., T. Tsunoda, E. M. Tuzcu, P. Schoenhagen, C. J. Cooper, M. Yasin, G. M. Eaton, M. A. Lauer, W. S. Sheldon, C. L. Grines, S. Halpern, T. Crowe, J. C. Blankenship, and R. Kerensky. 2003. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. JAMA. 290:2292-2300.
25. Phillips, J. C., W. Wriggers, Z. Li, A. Jonas, and K. Schulten. 1997. Predicting the structure of apolipoprotein A-I in reconstituted high-density lipoprotein disks. Biophys. J. 73:2337-2346.
26. Segrest, J. P., M. K. Jones, A. E. Klon, C. J. Sheldahl, M. Hellinger, H. De Loof, and S. C. Harvey. 1999. A detailed molecular belt model for apolipoprotein A-I in discoidal high density lipoprotein. J. Biol. Chem. 274:31755-31758.
27. Shih, A. Y., I. G. Denisov, J. C. Phillips, S. G. Sligar, and K. Schulten. 2005. Molecular dynamics simulations of discoidal bilayers assembled from truncated human lipoproteins. Biophys. J. 88:548-556.
28. Rogers, D. P., L. M. Roberts, J. Lebowitz, G. Datta, G. M. Anantharamaiah, J. A. Engler, and C. G. Brouillette. 1998. The lipid-free structure of apolipoprotein A-I: effects of amino-terminal deletions. Biochemistry. 37:11714-11725.
29. Maiorano, J. N., R. J. Jandacek, E. M. Horace, and W. S. Davidson. 2004. Identification and structural ramifications of a hinge domain in apolipoprotein A-I discoidal high-density lipoproteins of different size. Biochemistry. 43:11717-11726.
30. Koppaka, V., L. Silvestro, J. A. Engler, C. G. Brouillette, and P. H. Axelsen. 1999. The structure of human lipoprotein A-I - evidence for the "belt" model. J. Biol. Chem. 274:14541-14544.
31. Panagotopulos, S. E., E. M. Horace, J. N. Maiorano, and W. S. Davidson. 2001. Apolipoprotein A-I adopts a belt-like orientation in reconstituted high density lipoproteins. J. Biol. Chem. 276:42965-42970.
32. Silva, R. A., G. M. Hilliard, L. Li, J. P. Segrest, and W. S. Davidson. 2005. A mass spectrometric determination of the conformation of dimeric apolipoprotein A-I in discoidal high density lipoproteins. Biochemistry. 44:8600-8607.
33. Lins, L., S. Piron, K. Conrath, B. Vanloo, R. Brasseur, M. Rosseneu, J. Baert, and J. M. Ruysschaert. 1993. Enzymatic hydrolysis of reconstituted dimyristoylphosphatidylcholine-apo A-I complexes. Biochim. Biophys. Acta. 1151:137-142.
34. Culot, C., F. Durant, S. Lazarescu, P. A. Thiry, B. Vanloo, M. Y. Rosseneu, L. Lins, and R. Brasseur. 2004. Structural investigation of reconstituted high density lipoproteins by scanning tunnelling microscopy. Appl. Surf. Sci. 230:151-157.
35. Mishra, V. K., G. M. Anantharamaiah, J. P. Segrest, M. N. Palgunachari, M. Chaddha, S. W. Sham, and N. R. Krishna. 2006. Association of a model class A (apolipoprotein) amphipathic alpha helical peptide with lipid: high resolution NMR studies of peptide.lipid discoidal complexes. J. Biol. Chem. 281:6511-6519.
36. Opella, S. J., and F. M. Marassi. 2004. Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev. 104:3587-3606.
37. Griffin, R. G. 1998. Dipolar recoupling in MAS spectra of biological solids. Nat. Struct. Biol. 5:508-512.
38. 15N resonance assignments of the alpha-spectrin SH3 domain by magic angle spinning solid state NMR at 17.6 Tesla. Chembiochem. 2:272-281.
39. Igumenova, T. I., A. E. McDermott, K. W. Zilm, R. W. Martin, E. K. Paulson, and A. J. Wand. 2004. Assignments of carbon NMR resonances for microcrystalline ubiquitin. J. Am. Chem. Soc. 126:6720-6727.
40. Igumenova, T. I., A. J. Wand, and A. E. McDermott. 2004. Assignment of the backbone resonances for microcrystalline ubiquitin. J. Am. Chem. Soc. 126:5323-5331.
41. Franks, W. T., D. H. Zhou, B. J. Wylie, B. G. Money, D. T. Graesser, H. L. Frericks, G. Sahota, and C. M. Rienstra. 2005. Magic-angle spinning solid-state NMR spectroscopy of the beta1 immunoglobulin binding domain of protein G (GB1): 15N and 13C chemical shift assignments and conformational analysis. J. Am. Chem. Soc. 127:12291-12305.
42. Bockmann, A., A. Lange, A. Galinier, S. Luca, N. Giraud, M. Juy, H. Heise, R. Montserret, F. Penin, and M. Baldus. 2003. Solid state NMR sequential resonance assignments and conformational analysis of the 2 x 10.4 kDa dimeric form of the Bacillus subtilis protein Crh. J. Biomol. NMR. 27:323-339.
43. Egorova-Zachernyuk, T. A., J. Hollander, N. Fraser, P. Gast, A. J. Hoff, R. Cogdell, H. J. M. de Groot, and M. Baldus. 2001. Heteronuclear 2D-correlations in a uniformly [C-13, N-15] labeled membrane-protein complex at ultra-high magnetic fields. J. Biomol. NMR. 19:243-253.
44. Gammeren, A. J., F. B. Hulsbergen, J. G. Hollander, and H. J. Groot. 2005. Residual backbone and side-chain 13C and 15N resonance assignments of the intrinsic transmembrane light-harvesting 2 protein complex by solid-state magic angle spinning NMR spectroscopy. J. Biomol. NMR. 31:279-293.
45. Holdeman, T. C., and K. H. Gardner. 2001. Letter to the Editor: H-1, C-13 and N-15 chemical shift assignments of the N-terminal PAS domain of mNPAS2. J. Biomol. NMR. 21:383-384.
46. Stringer, J. A., C. E. Bronnimann, C. G. Mullen, D. H. Zhou, S. A. Stellfox, Y. Li, E. H. Williams, and C. M. Rienstra. 2005. Reduction of RF-induced sample heating with a scroll coil resonator structure for solid-state NMR probes. J. Magn. Reson. 173:40-48.
47. Hediger, S., B. H. Meier, N. D. Kurur, G. Bodenhausen, and R. R. Ernst. 1994. NMR cross-polarization by adiabatic passage through the Hartmann-Hahn condition (APHH). Chem. Phys. Lett. 223:283-288.
48. Bennett, A. E., C. M. Rienstra, M. Auger, K. V. Lakshmi, and R. G. Griffin. 1995. Heteronuclear decoupling in rotating solids. J. Chem. Phys. 103:6951-6958.
49. Delaglio, F., S. Grzesiek, G. W. Vuister, G. Zhu, J. Pfeifer, and A. Bax. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6:277-293.
50. Morcombe, C. R., and K. W. Zilm. 2003. Chemical shift referencing in MAS solid state NMR. J. Magn. Reson. 162:479-486.
51. Martin, R. W., and K. W. Zilm. 2003. Preparation of protein nanocrystals and their characterization by solid state NMR. J. Magn. Reson. 165:162-174.
52. Baldus, M., A. T. Petkova, J. Herzfeld, and R. G. Griffin. 1998. Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol. Phys. 95:1197-1207.
53. BioMagResBank. http://www.bmrb.wisc.edu.
54. Takegoshi, K., S. Nakamura, and T. Terao. 2001. C-13-H-1 dipolar-assisted rotational resonance in magic-angle spinning NMR. Chem. Phys. Lett. 344:631-637.
55. Wishart, D. S., and B. D. Sykes. 1994. The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR. 4:171-180.
56. Cornilescu, G., F. Delaglio, and A. Bax. 1999. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR. 13:289-302.
57. Luca, S., D. V. Filippov, J. H. van Boom, H. Oschkinat, H. J. de Groot, and M. Baldus. 2001. Secondary chemical shifts in immobilized peptides and proteins: a qualitative basis for structure refinement under magic angle spinning. J. Biomol. NMR. 20:325-331.
58. Iwadate, M., T. Asakura, and M. P. Williamson. 1999. C alpha and C beta carbon-13 chemical shifts in proteins from an empirical database. J. Biomol. NMR. 13:199-211.
59. Li, L., J. Chen, V. K. Mishra, J. A. Kurtz, D. Cao, A. E. Klon, S. C. Harvey, G. M. Anantharamaiah, and J. P. Segrest. 2004. Double belt structure of discoidal high density lipoproteins: molecular basis for size heterogeneity. J. Mol. Biol. 343:1293-1311.
60. Lorch, M., S. Fahem, C. Kaiser, I. Weber, A. J. Mason, J. U. Bowie, and C. Glaubitz. 2005. How to prepare membrane proteins for solid-state NMR: a case study on the alpha-helical integral membrane protein diacylglycerol kinase from E. coli. ChemBioChem. 6:1693-1700.
61. Rogers, D. P., L. M. Roberts, J. Lebowitz, J. A. Engler, and C. G. Brouillette. 1998. Structural analysis of apolipoprotein A-I: effects of amino- and carboxy-terminal deletions on the lipid-free structure. Biochemistry. 37:945-955.
62. Brouillette, C. G., and G. M. Anantharamaiah. 1995. Structural models of human apolipoprotein A-I. Biochim. Biophys. Acta. 1256: 103-129.
63. Klon, A. E., J. P. Segrest, and S. C. Harvey. 2002. Comparative models for human apolipoprotein A-I bound to lipid in discoidal high-density lipoprotein particles. Biochemistry. 41:10895-10905.
64. Lovell, S. C., I. W. Davis, W. B. Arendall 3rd, P. I. de Bakker, J. M. Word, M. G. Prisant, J. S. Richardson, and D. C. Richardson. 2003. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins. 50:437-450.
65. Spera, S., and A. Bax. 1991. Empirical correlation between protein backbone conformation and C-alpha and C-beta C-13 nuclear-magnetic-resonance chemical-shifts. J. Am. Chem. Soc. 113:5490-5492.
66. Kuszewski, J., J. Qin, A. M. Gronenborn, and G. M. Clore. 1995. The impact of direct refinement against 13C alpha and 13C beta chemical shifts on protein structure determination by NMR. J. Magn. Reson. B. 106:92-96.
67. Beger, R. D., and P. H. Bolton. 1997. Protein phi and psi dihedral restraints determined from multidimensional hypersurface correlations of backbone chemical shifts and their use in the determination of protein tertiary structures. J. Biomol. NMR. 10:129-142.
68. Neal, S., A. M. Nip, H. Zhang, and D. S. Wishart. 2003. Rapid and accurate calculation of protein 1H, 13C and 15N chemical shifts. J. Biomol. NMR. 26:215-240.
69. Heise, H., S. Luca, B. L. de Groot, H. Grubmuller, and M. Baldus. 2005. Probing conformational disorder in neurotensin by two-dimensional solid-state NMR and comparison to molecular dynamics simulations. Biophys. J. 89:2113-2120.
70. Hohwy, M., C. M. Rienstra, C. P. Jaroniec, and R. G. Griffin. 1999. Fivefold symmetric homonuclear dipolar recoupling in rotating solids: application to double quantum spectroscopy. J. Chem. Phys. 110:7983-7992.