Helical domains that mediate lipid solubilization and ABCA1-specific cholesterol efflux in apolipoproteins C-I and A-II

Journal of Lipid Research

Volumn 54, Issue 7, 2013, Pages 1939-1948

  Smith, Loren E ^a   Segrest, Jere P ^b   Davidson, W Sean ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Amphipathic helix; Apolipoprotein mediated cholesterol efflux; Tertiary structure

Indexed keywords

ABC TRANSPORTER A1; APOLIPOPROTEIN A2; APOLIPOPROTEIN C1; CHOLESTEROL; LIPID; PHOSPHOLIPID; POLYPEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; HUMAN; LIPID SOLUBILIZATION; MOLECULAR MECHANICS; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; SOLUBILIZATION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

AMPHIPATHIC HELIX; APOLIPOPROTEIN-MEDIATED CHOLESTEROL EFFLUX; TERTIARY STRUCTURE;

APOLIPOPROTEIN A-II; APOLIPOPROTEIN C-I; ATP BINDING CASSETTE TRANSPORTER 1; CHOLESTEROL; HUMANS; LIPID BILAYERS; PHOSPHOLIPIDS; POINT MUTATION; SOLUBILITY;

EID: 84878976594     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M037903     Document Type: Article

References (53)

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. (Pubitemid 8110784)
2. Assmann, G., H. Schulte, A. vonEckardstein, and Y. D. Huang. 1996. High-density lipoprotein cholesterol as a predictor of coronary heart disease risk. The PROCAM experience and pathophysiological implications for reverse cholesterol transport. Atherosclerosis. 124: S11-S20.
3. Barter, P. J., M. Caulfield, M. Eriksson, S. M. Grundy, J. J. Kastelein, M. Komajda, J. Lopez-Sendon, L. Mosca, J. C. Tardif, D. D. Waters, et al. 2007. Effects of torcetrapib in patients at high risk for coronary events. N. Engl. J. Med. 357: 2109-2122. (Pubitemid 350146106)
4. Schwartz, G. G., A. G. Olsson, M. Abt, C. M. Ballantyne, P. J. Barter, J. Brumm, B. R. Chaitman, I. M. Holme, D. Kallend, L. A. Leiter, et al. 2012. Effects of dalcetrapib in patients with a recent acute coronary syndrome. N. Engl. J. Med. 367: 2089-2099.
5. Yvan-Charvet, L., N. Wang, and A. R. Tall. 2010. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 30: 139-143.
6. Rust, S., M. Rosier, H. Funke, J. Real, Z. Amoura, J. C. Piette, J. F. Deleuze, H. B. Brewer, N. Duverger, P. Denefle, et al. 1999. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat. Genet. 22: 352-355. (Pubitemid 29369525)
7. Bodzioch, M., E. Orso, J. Klucken, T. Langmann, A. Bottcher, W. Diederich, W. Drobnik, S. Barlage, C. Buchler, M. Porsch-Ozcurumez, et al. 1999. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 22: 347-351. (Pubitemid 29369524)
8. Brooks-Wilson, A., M. Marcil, S. M. Clee, L. H. Zhang, K. Roomp, M. van Dam, L. Yu, C. Brewer, J. A. Collins, H. O. Molhuizen, et al. 1999. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 22: 336-345. (Pubitemid 29369523)
9. Lawn, R. M., D. P. Wade, M. R. Garvin, X. Wang, K. Schwartz, J. G. Porter, J. J. Seilhamer, A. M. Vaughan, and J. F. Oram. 1999. The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J. Clin. Invest. 104: R25-R31. (Pubitemid 29536327)
10. Aiello, R. J., D. Brees, P. A. Bourassa, L. Royer, S. Lindsey, T. Coskran, M. Haghpassand, and O. L. Francone. 2002. Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler. Thromb. Vasc. Biol. 22: 630-637. (Pubitemid 34408745)
11. Remaley, A. T., J. A. Stonik, S. J. Demosky, E. B. Neufeld, A. V. Bocharov, T. G. Vishnyakova, T. L. Eggerman, A. P. Patterson, N. J. Duverger, S. Santamarina-Fojo, et al. 2001. Apolipoprotein specificity for lipid efflux by the human ABCAI transporter. Biochem. Biophys. Res. Commun. 280: 818-823. (Pubitemid 32924503)
12. Remaley, A. T., F. Thomas, J. A. Stonik, S. J. Demosky, S. E. Bark, E. B. Neufeld, A. V. Bocharov, T. G. Vishnyakova, A. P. Patterson, T. L. Eggerman, et al. 2003. Synthetic amphipathic helical peptides promote lipid efflux from cells by an ABCA1-dependent and an ABCA1-independent pathway. J. Lipid Res. 44: 828-836. (Pubitemid 37279685)
13. Wool, G. D., C. A. Reardon, and G. S. Getz. 2008. Apolipoprotein A-I mimetic peptide helix number and helix linker influence potentially anti-atherogenic properties. J. Lipid Res. 49: 1268-1283.
14. D'Souza, W., J. A. Stonik, A. Murphy, S. J. Demosky, A. A. Sethi, X. L. Moore, J. Chin-Dusting, A. T. Remaley, and D. Sviridov. 2010. Structure/function relationships of apolipoprotein a-I mimetic peptides: implications for antiatherogenic activities of high-density lipoprotein. Circ. Res. 107: 217-227.
15. Natarajan, P., T. M. Forte, B. Chu, M. C. Phillips, J. F. Oram, and J. K. Bielicki. 2004. Identification of an apolipoprotein A-I structural element that mediates cellular cholesterol efflux and stabilizes ATP binding cassette transporter A1. J. Biol. Chem. 279: 24044-24052. (Pubitemid 38725263)
16. Watson, C. E., N. Weissbach, L. Kjems, S. Ayalasomayajula, Y. Zhang, I. Chang, M. Navab, S. Hama, G. Hough, S. T. Reddy, et al. 2011. Treatment of patients with cardiovascular disease with L-4F, an apo-A1 mimetic, did not improve select biomarkers of HDL function. J. Lipid Res. 52: 361-373.
17. Bloedon, L. T., R. Dunbar, D. Duffy, P. Pinell-Salles, R. Norris, B. J. DeGroot, R. Movva, M. Navab, A. M. Fogelman, and D. J. Rader. 2008. Safety, pharmacokinetics, and pharmacodynamics of oral apoA-I mimetic peptide D-4F in high-risk cardiovascular patients. J. Lipid Res. 49: 1344-1352.
18. Tubb, M. R., L. E. Smith, and W. S. Davidson. 2009. Purification of recombinant apolipoproteins A-I and A-IV and efficient affinity tag cleavage by tobacco etch virus protease. J. Lipid Res. 50: 1497-1504.
19. Atcliffe, B. W., C. A. MacRaild, P. R. Gooley, and G. J. Howlett. 2001. The interaction of human apolipoprotein C-I with sub-micellar phospholipid. Eur. J. Biochem. 268: 2838-2846. (Pubitemid 32862966)
20. Durbin, D. M., and A. Jonas. 1997. The effect of apolipoprotein A-II on the structure and function of apolipoprotein A-I in a homogeneous reconstituted high density lipoprotein particle. J. Biol. Chem. 272: 31333-31339. (Pubitemid 28013267)
21. Oram, J. F., R. M. Lawn, M. R. Garvin, and D. P. Wade. 2000. ABCA1 is the cAMP-inducible apolipoprotein receptor that mediates cholesterol secretion from macrophages. J. Biol. Chem. 275: 34508-34511.
22. Vedhachalam, C., L. Liu, M. Nickel, P. Dhanasekaran, G. M. Anantharamaiah, S. Lund-Katz, G. H. Rothblat, and M. C. Phillips. 2004. Influence of ApoA-I structure on the ABCA1-mediated efflux of cellular lipids. J. Biol. Chem. 279: 49931-49939. (Pubitemid 39577801)
23. Gillotte, K. L., M. Zaiou, S. Lund-Katz, G. M. Anantharamaiah, P. Holvoet, A. Dhoest, M. N. Palgunachari, J. P. Segrest, K. H. Weisgraber, G. H. Rothblat, et al. 1999. Apolipoprotein-mediated plasma membrane microsolubilization. Role of lipid affinity and membrane penetration in the efflux of cellular cholesterol and phospholipid. J. Biol. Chem. 274: 2021-2028.
24. Panagotopulos, S. E., S. R. Witting, E. M. Horace, D. Y. Hui, J. N. Maiorano, and W. S. Davidson. 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. (Pubitemid 35190924)
25. Gursky, O. 2001. Solution conformation of human apolipoprotein C-1 inferred from proline mutagenesis: far- and near-UV CD study. Biochemistry. 40: 12178-12185. (Pubitemid 32946559)
26. Rozek, A., J. T. Sparrow, K. H. Weisgraber, and R. J. Cushley. 1999. Conformation of human apolipoprotein C-I in a lipid-mimetic environment determined by CD and NMR spectroscopy. Biochemistry. 38: 14475-14484.
27. Segrest, J. P., M. K. Jones, H. De Loof, C. G. Brouillette, Y. V. Venkatachalapathi, and G. M. Anantharamaiah. 1992. The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function. J. Lipid Res. 33: 141-166.
28. Segrest, J. P., H. De Loof, J. G. Dohlman, C. G. Brouillette, and G. M. Anantharamaiah. 1990. Amphipathic helix motif: classes and properties. Proteins. 8: 103-117. (Pubitemid 20262536)
29. Rost, B., G. Yachdav, and J. Liu. 2004. The PredictProtein server. Nucleic Acids Res. 32(Web Server issue): W321-W326.
30. Venkatachalapathi, Y. V., M. C. Phillips, R. M. Epand, R. F. Epand, E. M. Tytler, J. P. Segrest, and G. M. Anantharamaiah. 1993. Effect of end group blockage on the properties of a class A amphipathic helical peptide. Proteins. 15: 349-359. (Pubitemid 23107033)
31. Sethi, A. A., J. A. Stonik, F. Thomas, S. J. Demosky, M. Amar, E. Neufeld, H. B. Brewer, W. S. Davidson, W. D'Souza, D. Sviridov, et al. 2008. Asymmetry in the lipid affinity of bihelical amphipathic peptides. A structural determinant for the specificity of ABCA1-dependent cholesterol efflux by peptides. J. Biol. Chem. 283: 32273-32282.
32. Vedhachalam, C., A. B. Ghering, W. S. Davidson, S. Lund-Katz, G. H. Rothblat, and M. C. Phillips. 2007. ABCA1-induced cell surface binding sites for ApoA-I. Arterioscler. Thromb. Vasc. Biol. 27: 1603-1609. (Pubitemid 46986116)
33. Chroni, A., T. Liu, M. L. Fitzgerald, M. W. Freeman, and V. I. Zannis. 2004. Cross-linking and lipid efflux properties of ApoA-I mutants suggest direct association between ApoA-I helices and ABCA1. Biochemistry. 43: 2126-2139. (Pubitemid 38233274)
34. Martinez, L. O., B. Agerholm-Larsen, N. Wang, W. Chen, and A. R. Tall. 2003. Phosphorylation of a PEST sequence in ABCA1 promotes calpain degradation and is reversed by ApoA-I. J. Biol. Chem. 278: 37368-37374. (Pubitemid 37175255)
35. Wang, N., W. Chen, P. Linsel-Nitschke, L. O. Martinez, B. Agerholm-Larsen, D. L. Silver, and A. R. Tall. 2003. A PEST sequence in ABCA1 regulates degradation by calpain protease and stabilization of ABCA1 by apoA-I. J. Clin. Invest. 111: 99-107. (Pubitemid 36134853)
36. Segrest, J. P., D. W. Garber, C. G. Brouillette, S. C. Harvey, and G. M. Anantharamaiah. 1994. The amphipathic alpha helix: a multifunctional structural motif in plasma apolipoproteins. Adv. Protein Chem. 45: 303-369. (Pubitemid 24139891)
37. Mishra, V. K., M. N. Palgunachari, G. Datta, M. C. Phillips, S. Lund-Katz, S. O. Adeyeye, J. P. Segrest, and M. Ananthanarayanan. 1998. Studies of synthetic peptides of human apolipoprotein A-I containing tandem amphipathic alpha-helixes. Biochemistry. 37: 10313-10324. (Pubitemid 28366389)
38. Palgunachari, M. N., V. K. Mishra, S. Lund-Katz, M. C. Phillips, S. O. Adeyeye, S. Alluri, G. M. Anantharamaiah, and J. P. Segrest. 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. (Pubitemid 26056254)
39. Kono, M., T. Tanaka, M. Tanaka, C. Vedhachalam, P. S. Chetty, D. Nguyen, P. Dhanasekaran, S. Lund-Katz, M. C. Phillips, and H. Saito. 2010. Disruption of the C-terminal helix by single amino acid deletion is directly responsible for impaired cholesterol efflux ability of apolipoprotein A-I Nichinan. J. Lipid Res. 51: 809-818.
40. Saito, H., P. Dhanasekaran, D. Nguyen, E. Deridder, P. Holvoet, S. Lund-Katz, and M. C. Phillips. 2004. Alpha-helix formation is required for high affinity binding of human apolipoprotein A-I to lipids. J. Biol. Chem. 279: 20974-20981. (Pubitemid 38656497)
41. Vedhachalam, C., V. Narayanaswami, N. Neto, T. M. Forte, M. C. Phillips, S. Lund-Katz, and J. K. Bielicki. 2007. The C-terminal lipid-binding domain of apolipoprotein E is a highly efficient mediator of ABCA1-dependent cholesterol efflux that promotes the assembly of high-density lipoproteins. Biochemistry. 46: 2583-2593. (Pubitemid 46417902)
42. Choy, N., V. Raussens, and V. Narayanaswami. 2003. Inter-molecular coiled-coil formation in human apolipoprotein E C-terminal domain. J. Mol. Biol. 334: 527-539. (Pubitemid 37386352)
43. Fan, D., Q. Li, L. Korando, W. G. Jerome, and J. Wang. 2004. A monomeric human apolipoprotein E carboxyl-terminal domain. Biochemistry. 43: 5055-5064. (Pubitemid 38544459)
44. Tanaka, M., M. Koyama, P. Dhanasekaran, D. Nguyen, M. Nickel, S. Lund-Katz, H. Saito, and M. C. Phillips. 2008. Influence of tertiary structure domain properties on the functionality of apolipoprotein A-I. Biochemistry. 47: 2172-2180. (Pubitemid 351287143)
45. Tanaka, M., P. Dhanasekaran, D. Nguyen, S. Ohta, S. Lund-Katz, M. C. Phillips, and H. Saito. 2006. Contributions of the N- and C-terminal helical segments to the lipid-free structure and lipid interaction of apolipoprotein A-I. Biochemistry. 45: 10351-10358. (Pubitemid 44384811)
46. Davidson, W. S., T. Hazlett, W. W. Mantulin, and A. Jonas. 1996. The role of apolipoprotein AI domains in lipid binding. Proc. Natl. Acad. Sci. USA. 93: 13605-13610. (Pubitemid 26424166)
47. Westerlund, J. A., and K. H. Weisgraber. 1993. Discrete carboxyl-terminal segments of apolipoprotein E mediate lipoprotein association and protein oligomerization. J. Biol. Chem. 268: 15745-15750. (Pubitemid 23222075)
48. Weinberg, R. B. 1994. Identification of functional domains in the plasma apolipoproteins by analysis of inter-species sequence variability. J. Lipid Res. 35: 2212-2222.
49. Deng, X., J. Morris, J. Dressmen, M. R. Tubb, P. Tso, W. G. Jerome, W. S. Davidson, and T. B. Thompson. 2012. The structure of dimeric apolipoprotein A-IV and its mechanism of self-association. Structure. 20: 767-779.
50. Mei, X., and D. Atkinson. 2011. Crystal structure of C-terminal truncated apolipoprotein A-I reveals the assembly of high density lipoprotein (HDL) by dimerization. J. Biol. Chem. 286: 38570-38582.
51. Karathanasis, S. K., P. Oettgen, I. A. Haddad, and S. E. Antonarakis. 1986. Structure, evolution, and polymorphisms of the human apolipoprotein A4 gene (APOA4). Proc. Natl. Acad. Sci. USA. 83: 8457-8461. (Pubitemid 17194892)
52. Sviridov, D. O., A. M. Andrianov, I. V. Anishchenko, J. A. Stonik, M. J. Amar, S. Turner, and A. T. Remaley. 2013. Hydrophobic amino acids in the hinge region of the 5A apolipoprotein mimetic peptide are essential for promoting cholesterol efflux by the ABCA1 transporter. J. Pharmacol. Exp. Ther. 344: 50-58.
53. Segrest, J. P., M. K. Jones, V. K. Mishra, and G. M. Ananatharamaiah. 2002. Experimental and computational studies of the interactions of amphipathic peptides with lipid surfaces. In Peptide-Lipid Interac tions. Vol. 52. S. A. Simon and T. J. McIntosh, editors. 391-429.