The crystal structure of the C-terminal truncated apolipoprotein A-I sheds new light on amyloid formation by the N-terminal fragment

Biochemistry

Volumn 51, Issue 1, 2012, Pages 10-18

  Gursky, Olga ^a   Mei, Xiaohu ^a   Atkinson, David ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPATHIC; AMYLOID FORMATION; APOLIPOPROTEIN A-I; APOLIPOPROTEIN A-I (APOA-I); BUNDLE STRUCTURES; HIGH-DENSITY LIPOPROTEINS; HUMAN PROTEINS; LIPID BINDING; N-TERMINALS; PROTEIN STRUCTURES; STRUCTURAL BASIS; X RAY CRYSTAL STRUCTURES;

CHOLESTEROL; ENZYME INHIBITION; PROTEINS;

DISEASES;

AMYLOID; APOLIPOPROTEIN A1;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; AMYLOIDOSIS; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; HUMAN; HYDROPHILICITY; HYDROPHOBICITY; LIPID ANALYSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SUBSTITUTION; AMYLOID; AMYLOIDOSIS, FAMILIAL; ANIMALS; APOLIPOPROTEIN A-I; CRYSTALLOGRAPHY, X-RAY; HUMANS; PEPTIDE FRAGMENTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE DELETION;

EID: 84856857216     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2017014     Document Type: Article

References (45)

1. 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 (2), 141-166.
2. Nolte, R. T., and Atkinson, D. (1992) Conformational analysis of apolipoprotein A-I and E-3 based on primary sequence and circular dichroism. Biophys. J. 63 (5), 1221-1239. (Pubitemid 23004470)
3. Bashtovyy, D., Jones, M. K., Anantharamaiah, G. M., and Segrest, J. P. (2011) Sequence conservation of apolipoprotein A-I affords novel insights into HDL structure-function. J. Lipid Res. 52 (3), 435-450.
4. Lund-Katz, S., and Phillips, M. C. (2010) High density lipoprotein structure-function and role in reverse cholesterol transport. Subcell. Biochem. 51, 183-227.
5. Huang, R., Silva, R. A., Jerome, W. G., Kontush, A., Chapman, M. J., Curtiss, L. K., Hodges, T. J., and Davidson, W. S. (2011) Apolipoprotein A-I structural organization in high-density lipoproteins isolated from human plasma. Nat. Struct. Mol. Biol. 18 (4), 416-422.
6. Yvan-Charvet, L., Wang, N., and Tall, A. R. (2010) Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 30, 139-143.
7. Fielding, C. J., and Fielding, P. E. (1995) Molecular physiology of reverse cholesterol transport. J. Lipid Res. 36, 211-228.
8. Rye, K. A., Clay, M. A., and Barter, P. J. (1999) Remodelling of high density lipoproteins by plasma factors. Atherosclerosis 145, 227-238. (Pubitemid 29359129)
9. Cavigiolio, G., Geier, E. G., Shao, B., Heinecke, J. W., and Oda, M. N. (2010) Exchange of apolipoprotein A-I between lipid-associated and lipid-free states: A potential target for oxidative generation of dysfunctional high density lipoproteins. J. Biol. Chem. 285 (24), 18847-18857.
10. Oram, J. F., and Heinecke, J. W. (2005) ATP-binding cassette transporter A1: A cell cholesterol exporter that protects against cardiovascular disease. Physiol. Rev. 85 (4), 1343-1372. (Pubitemid 41362273)
11. Mehta, R., Gantz, D. L., and Gursky, O. (2003) Human plasma high-density lipoproteins are stabilized by kinetic factors. J. Mol. Biol. 328 (1), 183-192. (Pubitemid 36390290)
12. Gursky, O., and Atkinson, D. (1996) Thermal unfolding of human high-density apolipoprotein A-1: Implications for a lipid-free molten globular state. Proc. Natl. Acad. Sci. U.S.A. 93 (7), 2991-2995. (Pubitemid 26114351)
13. Guha, M., Gao, X., Jayaraman, S., and Gursky, O. (2008) Structural stability and functional remodeling of high-density lipoproteins: The importance of being disordered. Biochemistry 47 (44), 11393-11397.
14. Lee, J. Y., Lanningham-Foster, L., Boudyguina, E. Y., Smith, T. L., Young, E. R., Colvin, P. L., Thomas, M. J., and Parks, J. S. (2004) Prebeta high density lipoprotein has two metabolic fates in human apolipoprotein A-I transgenic mice. J. Lipid Res. 45 (4), 716-728. (Pubitemid 38405678)
15. Ramella, N. A., Rimoldi, O. J., Prieto, E. D., Schinella, G. R., Sanchez, S. A., Jaureguiberry, M. S., Vela, M. E., Ferreira, S. T., and Tricerri, M. A. (2011) Human apolipoprotein A-I-derived amyloid: Its association with atherosclerosis. PLoS One 6 (7), e22532.
16. Teoh, C. L., Griffin, M. D., and Howlett, G. J. (2011) Apolipoproteins and amyloid fibril formation in atherosclerosis. Protein Cell 2 (2), 116-127.
17. 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 (3), 121-128. (Pubitemid 34462182)
18. Obici, L., Franceschini, G., Calabresi, L., Giorgetti, S., Stoppini, M., Merlini, G., and Bellotti, V. (2006) Structure, function and amyloidogenic propensity of apolipoprotein A-I. Amyloid 13 (4), 191-205. (Pubitemid 44764459)
19. Gomaraschi, M., Obici, L., Simonelli, S., Gregorini, G., Negrinelli, A., Merlini, G., Franceschini, G., and Calabresi, L. (2011) Effect of the amyloidogenic L75P apolipoprotein A-I variant on HDL subpopulations. Clin. Chim. Acta 412 (13-14), 1262-1265.
20. Rowczenio, D., Dogan, A., Theis, J. D., Vrana, J. A., Lachmann, H. J., Wechalekar, A. D., Gilbertson, J. A., Hunt, T., Gibbs, S. D., Sattianayagam, P. T., Pinney, J. H., Hawkins, P. N., and Gillmore, J. D. (2011) Amyloidogenicity and clinical phenotype associated with five novel mutations in apolipoprotein A-I. Am. J. Pathol. 179 (4), 1978-1987.
21. Monti, D. M., Guglielmi, F., Monti, M., Cozzolino, F., Torrassa, S., Relini, A., Pucci, P., Arciello, A., and Piccoli, R. (2010) Effects of a lipid environment on the fibrillogenic pathway of the N-terminal polypeptide of human apolipoprotein A-I, responsible for in vivo amyloid fibril formation. Eur. Biophys. J. 39 (9), 1289-1299.
22. Gorbenko, G. P., and Kinnunen, P. K. (2006) The role of lipidprotein interactions in amyloid-type protein fibril formation. Chem. Phys. Lipids 141 (1-2), 72-82. (Pubitemid 43728804)
23. Rader, D. J., Gregg, R. E., Meng, M. S., Schaefer, J. R., Zech, L. A., Benson, M. D., and Brewer, H. B. Jr. (1992) In vivo metabolism of a mutant apolipoprotein, apoA-I Iowa, associated with hypoalphalipoproteinemia and hereditary systemic amyloidosis. J. Lipid Res. 33 (5), 755-763.
24. Marchesi, M., Parolini, C., Valetti, C., Mangione, P., Obici, L., Giorgetti, S., Raimondi, S., Donadei, S., Gregorini, G., Merlini, G., Stoppini, M., Chiesa, G., and Bellotti, V. (2011) The intracellular quality control system down-regulates the secretion of amyloidogenic apolipoprotein A-I variants: A possible impact on the natural history of the disease. Biochim. Biophys. Acta 1812 (1), 87-93.
25. de Sousa, M. M., Vital, C., Ostler, D., Fernandes, R., Pouget-Abadie, J., Carles, D., and Saraiva, M. J. (2000) Apolipoprotein AI and transthyretin as components of amyloid fibrils in a kindred with apoAI Leu178His amyloidosis. Am. J. Pathol. 156 (6), 1911-1917. (Pubitemid 30641760)
26. Obici, L., Bellotti, V., Mangione, P., Stoppini, M., Arbustini, E., Verga, L., Zorzoli, I., Anesi, E., Zanotti, G., Campana, C., Viganò, M., and Merlini, G. (1999) The new apolipoprotein A-I variant Leu(174) to Ser causes hereditary cardiac amyloidosis, and the amyloid fibrils are constituted by the 93-residue N-terminal polypeptide. Am. J. Pathol. 155 (3), 695-702. (Pubitemid 29426814)
27. Raimondi, S., Guglielmi, F., Giorgetti, S., Di Gaetano, S., Arciello, A., Monti, D. M., Relini, A., Nichino, D., Doglia, S. M., Natalello, A., Pucci, P., Mangione, P., Obici, L., Merlini, G., Stoppini, M., Robustelli, P., Tartaglia, G. G., Vendruscolo, M., Dobson, C. M., Piccoli, R., and Bellotti, V. (2011) Effects of the known pathogenic mutations on the aggregation pathway of the amyloidogenic peptide of apolipoprotein A-I. J. Mol. Biol. 407 (3), 465-476.
28. Zhu, H. L., and Atkinson, D. (2007) Conformation and lipid binding of a C-terminal (198-243) peptide of human apolipoprotein A-I. Biochemistry 46 (6), 1624-1634.
29. Andreola, A., Bellotti, V., Giorgetti, S., Mangione, P., Obici, L., Stoppini, M., Torres, J., Monzani, E., Merlini, G., and Sunde, M. (2003) Conformational switching and fibrillogenesis in the amyloidogenic fragment of apolipoprotein A-I. J. Biol. Chem. 278 (4), 2444-24451.
30. McManus, D. C., Scott, B. R., Franklin, V., Sparks, D. L., and Marcel, Y. L. (2001) Proteolytic degradation and impaired secretion of an apolipoprotein A-I mutant associated with dominantly inherited hypoalphalipoproteinemia. J. Biol. Chem. 276 (24), 21292-21302.
31. Mei, X., and Atkinson, D. (2011) Crystal structure of C-terminal truncated apolipoprotein A-I reveals the assembly of HDL by dimerization. J. Biol. Chem. 286 (44), 38570-38582.
32. Borhani D. W., Rogers, D. P., Engler, J. A., and Brouillette, C. G. (1997) Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation. Proc. Natl. Acad. Sci. U.S.A. 94 (23), 12291-12296. (Pubitemid 27492521)
33. Chetty, P. S., Mayne, L., Lund-Katz, S., Stranz, D., Englander, S. W., and Phillips, M. C. (2009) Helical structure and stability in human apolipoprotein A-I by hydrogen exchange and mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 106, 19005-19010.
34. Gomaraschi, M., Obici, L., Simonelli, S., Gregorini, G., Negrinelli, A., Merlini, G., Franceschini, G., and Calabresi, L. (2011) Effect of the amyloidogenic L75P apolipoprotein A-I variant on HDL subpopulations. Clin. Chim. Acta 412 (13-14), 1262-1265.
35. Jones, M. K., Gu, F., Catte, A., Li, L., and Segrest, J. P. (2011) "Sticky" and "promiscuous", the Yin and Yang of apolipoprotein A-I termini in discoidal high-density lipoproteins: A combined computational-experimental approach. Biochemistry 50 (12), 2249-2263.
36. Lagerstedt, J. O., Cavigiolio, G., Roberts, L. M., Hong, H. S., Jin, L. W., Fitzgerald, P. G., Oda, M. N., and Voss, J. C. (2007) Mapping the structural transition in an amyloidogenic apolipoprotein A-I. Biochemistry 46 (34), 9693-9699. (Pubitemid 47328575)
37. Jayaraman S., Cavigiolio, G., and Gursky, O. (2012) Folded functional lipid-poor apolipoprotein A-I obtained by heating of highdensity lipoproteins: Relevance to HDL biogenesis. Biochem. J., DOI: doi: 10.1042/BJ20111831.
38. Lagerstedt, J. O., Cavigiolio, G., Budamagunta, M. S., Pagani, I., Voss, J. C., and Oda, M. N. (2011) Structure of apolipoprotein A-I N terminus on nascent high density lipoproteins. J. Biol. Chem. 286 (4), 2966-2975.
39. Anantharamaiah, G. M., Hughes, T. A., Iqbal, M., Gawish, A., Neame, P. J., Medley, M. F., and Segrest, J. P. (1988) Effect of oxidation on the properties of apolipoproteins A-I and A-II. J. Lipid Res. 29 (3), 309-318.
40. Jonas, A., von Eckardstein, A., Churgay, L., Mantulin, W. W., and Assmann, G. (1993) Structural and functional properties of natural and chemical variants of apolipoprotein A-I. Biochim. Biophys. Acta 1166 (2-3), 202-210. (Pubitemid 23060895)
41. Sigalov, A. B., and Stern, L. J. (2001) Oxidation of methionine residues affects the structure and stability of apolipoprotein A-I in reconstituted high density lipoprotein particles. Chem. Phys. Lipids 113 (1-2), 133-146. (Pubitemid 33001482)
42. Hatters, D. M., and Howlett, G. J. (2002) The structural basis for amyloid formation by plasma apolipoproteins: A review. Eur. Biophys. J. 31 (1), 2-8.
43. Wong, Y. Q., Binger, K. J., Howlett, G. J., and Griffin, M. D. (2010) Methionine oxidation induces amyloid fibril formation by fulllength apolipoprotein A-I. Proc. Natl. Acad. Sci. U.S.A. 107 (5), 1977-1982.
44. Jayaraman, S., Gantz, D. L., and Gursky, O. (2011) Effects of phospholipase A2 and its products on structural stability of human LDL: Relevance to formation of LDL-derived lipid droplets. J. Lipid Res. 52 (3), 549-557.
45. Sparks D. L., Davidson, W. S., Lund-Katz, S., and Phillips, M. C. (1995) Effects of the neutral lipid content of high density lipoprotein on apolipoprotein A-I structure and particle stability. J. Biol. Chem. 270 (45), 26910-26917.