Contributions of the N- and C-terminal helical segments to the lipid-free structure and lipid interaction of apolipoprotein A-I

Biochemistry

Volumn 45, Issue 34, 2006, Pages 10351-10358

  Tanaka, Masafumi ^a   Dhanasekaran, Padmaja ^b   Nguyen, David ^b   Ohta, Shinya ^a   Lund Katz, Sissel ^b   Phillips, Michael C ^b,c   Saito, Hiroyuki ^a  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CONFORMATIONS; HYDROPHOBIC CHROMATOGRAPHY; LIPIDS; MOLECULAR STRUCTURE;

APOLIPOPROTEIN; CIRCULAR DICHROISM; PROLINE INSERTIONS; STRUCTURAL DOMAINS;

PROTEINS;

8 ANILINO 1 NAPHTHALENESULFONIC ACID; APOLIPOPROTEIN A1; CARBON 14; CHOLESTEROL; FORMALDEHYDE; GUANIDINE; PHOSPHATIDYLCHOLINE; PROLINE; TRITIUM; TRYPTOPHAN;

ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CHOLESTEROL TRANSPORT; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; FLUORESCENCE; ISOTHERMAL TITRATION CALORIMETRY; LIPID VESICLE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; SPECTROSCOPY;

AMINO ACID SUBSTITUTION; APOLIPOPROTEIN A-I; HUMANS; LIPID METABOLISM; LIPIDS; POINT MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 33748645937     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060726t     Document Type: Article

References (59)

1. Fielding, C. J., and Fielding, P. E. (2001) Cellular cholesterol efflux, Biochim. Biophys. Acta 1533, 175-189.
2. Yancey, P. G., Bortnick, A. E., Kellner-Weibel, G., de la Llera-Moya, M., Phillips, M. C., and Rothblat, G. H. (2003) Importance of different pathways of cellular cholesterol efflux, Arterioscler., Thromb., Vasc. Biol. 23, 712-719.
3. Lewis, G. F., and Rader, D. J. (2005) New insights into the regulation of HDL metabolism and reverse cholesterol transport, Circ. Res. 96, 1221-1232.
4. Oram, J. F. (2003) HDL apolipoproteins and ABCA1: Partners in the removal of excess cellular cholesterol, Arterioscler., Thromb., Vasc. Biol. 23, 720-727.
5. Lee, J. Y., and Parks, J. S. (2005) ATP-binding cassette transporter AI and its role in HDL formation, Curr. Opin. Lipidol. 16, 19-25.
6. Yokoyama, S. (2006) Assembly of high-density lipoprotein, Arterioscler., Thromb., Vasc. Biol. 26, 20-27.
7. Oram, J. F. (2000) Tangier disease and ABCA1, Biochim. Biophys. Acta 1529, 321-330.
8. Singaraja, R. R., Brunham, L. R., Visscher, H., Kastelein, J. J., and Hayden, M. R. (2003) Efflux and atherosclerosis: The clinical and biochemical impact of variations in the ABCA1 gene, Arterioscler., Thromb., Vasc. Biol. 23, 1322-1332.
9. Li, W. H., Tanimura, M., Luo, C. C., Datta, S., and Chan, L. (1988) The apolipoprotein multigene family: Biosynthesis, structure, structure-function relationships, and evolution, J. Lipid Res. 29, 245-271.
10. Segrest, J. P., Jones, M. K., De Loof, H., Brouillette, C. G., Venkatachalapathi, Y. V., and Anantharamaiah, G. M. (1992) The amphipathic helix in the exchangeable apolipoproteins: A review of secondary structure and function, J. Lipid Res. 33, 141-166
11. Palgunachari, M. N., Mishra, V. K., Lund-Katz, S., Phillips, M. C., Adeyeye, S. O., Alluri, S., Anantharamaiah, G. M., and Segrest, J. P. (1996) Only the two end helixes of eight tandem amphipathic helical domains of human apo A-I have significant lipid affinity. Implications for HDL assembly, Arterioscler., Thromb., Vasc. Biol. 16, 328-338.
12. Saito, H., Lund-Katz, S., and Phillips, M. C. (2004) Contributions of domain structure and lipid interaction to the functionality of exchangeable human apolipoproteins, Prog. Lipid Res. 43, 350-380.
13. Holvoet, P., Zhao, Z., Vanloo, B., Vos, R., Deridder, E., Dhoest, A., Taveirne, J., Brouwers, E., Demarsin, E., Engelborghs, Y., Rosseneu, M., Collen, D., and Brasseur, R. (1995) Phospholipid binding and lecithin-cholesterol acyltransferase activation properties of apolipoprotein A-I mutants, Biochemistry 34, 13334-13342.
14. Davidson, W. S., Hazlett, T., Mantulin, W. W., and Jonas, A. (1996) The role of apolipoprotein AI domains in lipid binding, Proc. Natl. Acad. Sci. U.S.A. 93, 13605-13610.
15. Saito, H., Dhanasekaran, P., Nguyen, D., Deridder, E., Holvoet, P., Lund-Katz, S., and Phillips, M. C. (2004) α-Helix formation is required for high affinity binding of human apolipoprotein A-I to lipids, J. Biol. Chem. 279, 20974-20981.
16. Fang, Y., Gursky, O., and Atkinson, D. (2003) Lipid-binding studies of human apolipoprotein A-I and its terminally truncated mutants, Biochemistry 42, 13260-13268.
17. Laccotripe, M., Makrides, S. C., Jonas, A., Zannis, V. I. (1997) The carboxyl-terminal hydrophobic residues of apolipoprotein A-I affect its rate of phospholipid binding and its association with high-density lipoprotein, J. Biol. Chem. 272, 17511-17522.
18. Mishra, V. K., Palgunachari, M. N., Datta, G., Phillips, M. C., Lund-Katz, S., Adeyeye, S. O., Segrest, J. P., and Anantnaramaiah, G. M. (1998) Studies of synthetic peptides of human apolipoprotein A-I containing tandem amphipathic α-helixes, Biochemistry 37, 10313-10324.
19. Zhu, H. L., and Atkinson, D. (2004) Conformation and lipid binding of the N-terminal (1-44) domain of human apolipoprotein A-I, Biochemistry 43, 13156-13164.
20. Narayanaswami, V., and Ryan, R. O. (2000) Molecular basis of exchangeable apolipoprotein function, Biochim. Biophys. Acta 1483, 15-36.
21. Brouillette, C. G., Anantharamaiah, G. M., Engler, J. A., and Borhani, D. W. (2001) Structural models of human apolipoprotein A-I: A critical analysis and review, Biochim. Biophys. Acta 1531, 4-46.
22. Lund-Katz, S., Liu, L., Thuahnai, S. T., and Phillips, M. C. (2003) High-density lipoprotein structure, Front. Biosci. 8, d1044-d1054.
23. Marcel, Y. L., and Kiss, R. S. (2003) Structure-function relationships of apolipoprotein A-I: A flexible protein with dynamic lipid associations, Curr. Opin. Lipidol. 14, 151-157.
24. Gursky, O. (2005) Apolipoprotein structure and dynamics, Curr. Opin. Lipidol. 16, 287-294.
25. Saito, H., Dhanasekaran, P., Nguyen, D., Holvoet, P., Lund-Katz, S., and Phillips, M. C. (2003) Domain structure and lipid interaction in human apolipoproteins A-I and E, a general model, J. Biol. Chem. 278, 23227-23232.
26. Silva, R. A., Hilliard, G. M., Fang, J., Macha, S., and Davidson, W. S. (2005) A three-dimensional molecular model of lipid-free apolipoprotein A-I determined by cross-linking/mass spectrometry and sequence threading, Biochemistry 44, 2759-2769.
27. Ajees, A. A., Anantharamaiah, G. M., Mishra, V. K., Hussain, M. M., and Murthy, H. M. (2006) Crystal structure of human apolipoprotein A-I: Insights into its protective effect against cardiovascular diseases, Proc. Natl. Acad. Sci. U.S.A. 103, 2126-2131.
28. Gillotte, K. L., Zaiou, M., Lund-Katz, S., Anantharamaiah, G. M., Holvoet, P., Dhoest, A., Palgunachari, M. N., Segrest, J. P., Weisgraber, K. H., Rothblat, G. H., and Phillips, M. C. (1999) Apolipoprotein-mediated plasma membrane microsolubilization. Role of lipid affinity and membrane penetration in the efflux of cellular cholesterol and phospholipids, J. Biol. Chem. 274, 2021-2028.
29. Panagotopulos, S. E., Witting, S. R., Horace, E. M., Hui, D. Y., Maiorano, J. N., and Davidson, W. S. (2002) The role of apolipoprotein A-I helix 10 in apolipoprotein-mediated cholesterol efflux via the ATP-binding cassette transporter ABCA1, J. Biol. Chem. 277, 39477-39484.
30. Favari, E., Bernini, F., Tarugi, P., Franceschini, G., and Calabresi, L. (2002) The C-terminal domain of apolipoprotein A-I is involved in ABCA1-driven phospholipid and cholesterol efflux, Biochem. Biophys. Res. Commun. 299, 801-805.
31. Chroni, A., Liu, T., Gorshkova, I., Kan, H. Y., Uehara, Y., von Eckardstein, A., and Zannis, V. I. (2003) The central helices of ApoA-I can promote ATP-binding cassette transporter A1 (ABCA1)-mediated lipid efflux. Amino acid residues 220-231 of the wild-type ApoA-I are required for lipid efflux in vitro and high-density lipoprotein formation in vivo, J. Biol. Chem. 278, 6719-6730.
32. Vedhachalam, C., Liu, L., Nickel, M., Dhanasekaran, P., Anantharamaiah, G. M., Lund-Katz, S., Rothblat, G. H., and Phillips, M. C. (2004) Influence of ApoA-I structure on the ABCA1-mediated efflux of cellular lipids, J. Biol. Chem. 279, 49931-49939.
33. Beckstead, J. A., Block, B. L., Bielicki, J. K., Kay, C. M., Oda, M. N., and Ryan, R. O. (2005) Combined N- and C-terminal truncation of human apolipoprotein A-I yields a folded, functional central domain, Biochemistry 44, 4591-4599.
34. Chou, P. Y., and Fasman, G. D. (1974) Prediction of protein conformation, Biochemistry 13, 222-245.
35. Schulman, B. A., and Kim, P. S. (1996) Proline scanning mutagenesis of a molten globule reveals non-cooperative formation of a protein's overall topology, Nat. Struct. Biol. 3, 682-687.
36. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent, J. Biol. Chem. 193, 265-275.
37. Markwell, M. A., Haas, S. M., Bieber, L. L., and Tolbert, N. E. (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples, Anal. Biochem. 87, 206-210.
38. Morrow, J. A., Segall, M. L., Lund-Katz, S., Phillips, M. C., Knapp, M., Rupp, B., and Weisgraber, K. H. (2000) Differences in stability among the human apolipoprotein E isoforms determined by the amino-terminal domain, Biochemistry 39, 11657-11666.
39. Tanaka, M., Vedhachalam, C., Sakamoto, T., Dhanasekaran, P., Phillips, M. C., Lund-Katz, S., and Saito H. (2006) Effect of carboxyl-terminal truncation on structure and lipid interaction of human apolipoprotein E4, Biochemistry 45, 4240-4247.
40. Li, S.-C., Goto, N. K., Williams, K. A., and Deber, C. M. (1996) α-Helical, but not β-sheet, propensity of proline is determined by peptide environment, Proc. Natl. Acad. Sci. U.S.A. 93, 6676-6681.
41. Rogers, D. P., Brouillette, C. G., Engler, J. A., Tendian, S. W., Roberts, L., Mishra, V. K., Anantharamaiah, G. M., Lund-Katz, S., Phillips, M. C., and Ray, M. J. (1997) Truncation of the amino terminus of human apolipoprotein A-I substantially alters only the lipid-free conformation, Biochemistry 36, 288-300.
42. Tanaka, M., Saito, H., Dhanasekaran, P., Wehrli, S., Handa, T., Lund-Katz, S., and Phillips, M. C. (2005) Effects of the core lipid on the energetics of binding of ApoA-I to model lipoprotein particles of different sizes, Biochemistry 44, 10689-10695.
43. Arnulphi, C., Jin, L., Tricerri, M. A., and Jonas, A. (2004) Enthalpy-driven apolipoprotein A-I and lipid bilayer interaction indicating protein penetration upon lipid binding, Biochemistry 43, 12258-12264.
44. Frank, P. G., and Marcel, Y. L. (2000) Apolipoprotein A-I: Structure-function relationships, J. Lipid Res. 41, 853-872.
45. Fang, Y., Gursky, O., and Atkinson, D. (2003) Structural studies of N- and C-terminally truncated human apolipoprotein A-I, Biochemistry 42, 6881-6890.
46. Tricerri, M. A., Agree, A. K. B., Sanchez, S. A., and Jonas, A. (2000) Characterization of apolipoprotein A-I structure using a cysteine-specific fluorescence probe, Biochemistry 39, 14682-14691.
47. Gross, E., Peng, D. Q., Hazen, S. L., and Smith, J. D. (2006) A novel folding intermediate state for apolipoprotein A-I: Role of the amino and carboxy termini, Biophys. J. 90, 1362-1370.
48. Krishna, M. M., and Englander, S. W. (2005) The N-terminal to C-terminal motif in protein folding and function, Proc. Natl. Acad. Sci. U.S.A. 102, 1053-1058.
49. Agree, A. K. B., Tricerri, M. A., McGuire, K. A., Tian, S.-M., and Jonas, A. (2002) Folding and stability of the C-terminal half of apolipoprotein A-I examined with a Cys-specific fluorescence probe, Biochim. Biphys. Acta 1594, 286-296.
50. Lazar, K. L., Miller-Auer, H., Getz, G. S., Orgel, J. P., and Meredith, S. C. (2005) Helix-turn-helix peptides that form α-helical fibrils: Turn sequences drive fibril structure, Biochemistry 44, 12681-12689.
51. Sorci-Thomas, M. G., and Thomas, M. J. (2002) The effects of altered apolipoprotein A-I structure on plasma HDL concentration, Trends Cardiovasc. Med. 12, 121-128.
52. Genschel, J., Haas, R., Propsting, M. J., and Schmidt, H. H. (1998) Apolipoprotein A-I induced amyloidosis, FEBS Lett. 430, 145-149.
53. Hatters, D. M., and Howlett, G. J. (2002) The structural basis for amyloid formation by plasma apolipoproteins: A review, Eur. Biophys. J. 31, 2-8.
54. Hatters D. M., MacPhee, C. E., Lawrence, L. J., Sawyer, W. H., and Howlett, G. J. (2000) Human apolipoprotein C-II forms twisted amyloid ribbons and closed loops, Biochemistry 39, 8276-8283.
55. Oda, M. N., Forte, T. M., Ryan, R. O., and Voss, J. C. (2003) The C-terminal domain of apolipoprotein A-I contains a lipid-sensitive conformational trigger, Nat. Struct. Biol. 10, 455-460.
56. Gorshkova, I. N., Liu, T., Zannis, V. I., and Atkinson, D. (2002) Lipid-free structure and stability of apolipoprotein A-I: Probing the central region by mutation, Biochemistry 41, 10529-10539.
57. Gorshkova I. N., Liu, T., Kan, H. Y., Chroni, A., Zannis, V. I., and Atkinson, D. (2006) Structure and stability of apolipoprotein A-I in solution and in discoidal high-density lipoprotein probed by double charge ablation and deletion mutation, Biochemistry 45, 1242-1254.
58. Pearson, K., Saito, H., Woods, S. C., Lund-Katz, S., Tso, P., Phillips, M. C., and Davidson W. S. (2004) Structure of human apolipoprotein A-IV: A distinct domain architecture among exchangeable apolipoproteins with potential functional implications, Biochemistry 43, 10719-10729.
59. Pearson, K., Tubb, M. R., Tanaka, M., Zhang, X. Q., Tso, P., Weinberg, R. B., and Davidson, W. S. (2005) Specific sequences in the N and C termini of apolipoprotein A-IV modulate its conformation and lipid association, J. Biol. Chem. 280, 38576-38582.