Structural Basis for Lipid Binding and Function by an Evolutionarily Conserved Protein, Serum Amyloid A

Journal of Molecular Biology

Volumn 432, Issue 7, 2020, Pages 1978-1995

  Frame, Nicholas M ^a   Kumanan, Meera ^b   Wales, Thomas E ^c   Bandara, Asanga ^b   Fändrich, Marcus ^d   Straub, John E ^b   Engen, John R ^c   Gursky, Olga ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Boston University   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

hydrogen deuterium exchange mass spectrometry; inflammation and immunity; lipoprotein nanoparticle; molecular dynamics simulations; hairpin misfolding intermediate

Indexed keywords

LIPOPROTEIN; SERUM AMYLOID A; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; LIGAND; PHOSPHATIDYLCHOLINE;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; GENETIC CONSERVATION; HUMAN; HYDROGEN DEUTERIUM EXCHANGE-MASS SPECTROMETRY; HYDROPHOBICITY; MOLECULAR DYNAMICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; ANIMAL; CHEMICAL PHENOMENA; CHEMISTRY; METABOLISM; MOUSE;

ANIMALS; BINDING SITES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIGANDS; MICE; MOLECULAR DYNAMICS SIMULATION; PHOSPHATIDYLCHOLINES; PROTEIN CONFORMATION; PROTEIN FOLDING; SERUM AMYLOID A PROTEIN;

EID: 85079549943     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2020.01.029     Document Type: Article

References (66)

1. Urieli-Shoval, S., Linke, R.P., Matzner, Y., Expression and function of serum amyloid A, a major acute-phase protein, in normal and disease states. Curr. Opin. Hematol. 7 (2000), 64–69.
2. Eklund, K.K., Niemi, K., Kovanen, P.T., Immune functions of serum amyloid A. Crit. Rev. Immunol. 32:4 (2012), 335–348.
3. Westermark, G.T., Fändrich, M., Westermark, P., AA amyloidosis: pathogenesis and targeted therapy. Annu. Rev. Pathol. 10 (2015), 321–344.
4. Papa, R., Lachmann, H.J., Secondary, AA, amyloidosis. Rheum. Dis. Clin. N. Am. 44:4 (2018), 585–603.
5. Shridas, P., Tannock, L.R., Role of serum amyloid A in atherosclerosis. Curr. Opin. Lipidol. 30:4 (2019), 320–325.
6. Uhlar, C.M., Burgess, C.J., Sharp, P.M., Whitehead, A.S., Evolution of the serum amyloid A (SAA) protein superfamily. Genomics 19:2 (1994), 228–235.
7. Sun, L., Ye, R.D., Serum amyloid A1: structure, function and gene polymorphism. Gene 583:1 (2016), 48–57.
8. De Buck, M., Gouwy, M., Wang, J.M., Van Snick, J., Opdenakker, G., Struyf, S., Van Damme, J., Structure and expression of different serum amyloid A (SAA) variants and their concentration-dependent functions during host insults. Curr. Med. Chem. 23 (2016), 1725–1755.
9. Ye, R.D., Sun, L., Emerging functions of serum amyloid A in inflammation. J. Leukoc. Biol. 98:6 (2015), 923–929.
10. Uhlar, C.M., Whitehead, A.S., Serum amyloid A, the major vertebrate acute-phase reactant. Eur. J. Biochem. 265 (1999), 501–523.
11. Sack, G.H. Jr., Serum amyloid A - a review. Mol. Med., 24(1), 2018, 46.
12. Benditt, E.P., Eriksen, N., Amyloid protein SAA is associated with high density lipoprotein from human serum. Proc. Natl. Acad. Sci. U.S.A. 74 (1977), 4025–4028.
13. Kisilevsky, R., Manley, P.N., Acute-phase serum amyloid A: perspectives on its physiological and pathological roles. Amyloid 19 (2012), 5–14.
14. Wilson, P.G., Thompson, J.C., Shridas, P., McNamara, P.J., de Beer, M.C., de Beer, F.C., Webb, N.R., Tannock, L.R., Serum amyloid A is an exchangeable apolipoprotein. Arterioscler. Thromb. Vasc. Biol. 38:8 (2018), 1890–1900.
15. Das, M., Gursky, O., Amyloid-forming properties of human apolipoproteins: sequence analyses and structural insights. Adv. Exp. Med. Biol. 855 (2015), 175–211.
16. Claus, S., Meinhardt, K., Aumüller, T., Puscalau-Girtu, I., Linder, J., Haupt, C., Walther, P., Syrovets, T., Simmet, T., Fändrich, M., Cellular mechanism of fibril formation from serum amyloid A1 protein. EMBO Rep. 18:8 (2017), 1352–1366.
17. Jayaraman, S., Gantz, D.L., Haupt, C., Fändrich, M., Gursky, O., Serum amyloid A sequesters diverse phospholipids and their hydrolytic products, hampering fibril formation and proteolysis in a lipid-dependent manner. Chem. Commun. 54:28 (2018), 3532–3535.
18. Liang, J.S., Schreiber, B.M., Salmona, M., Phillip, G., Gonnerman, W.A., de Beer, F.C., Sipe, J.D., Amino terminal region of acute phase, but not constitutive, serum amyloid A (apoSAA) specifically binds and transports cholesterol into aortic smooth muscle and HepG2 cells. J. Lipid Res. 37:10 (1996), 2109–2116.
19. Takase, H., Furuchi, H., Tanaka, M., Yamada, T., Matoba, K., Iwasaki, K., Kawakami, T., Mukai, T., Characterization of reconstituted high-density lipoprotein particles formed by lipid interactions with human serum amyloid A. Biochim. Biophys. Acta 1842:10 (2014), 1467–1474.
20. Jayaraman, S., Haupt, C., Gursky, O., Thermal transitions in serum amyloid A in solution and on the lipid: implications for structure and stability of acute-phase HDL. J. Lipid Res. 56:8 (2015), 1531–1542.
21. Frame, N.M., Gursky, O., Structure of serum amyloid A suggests a mechanism for selective lipoprotein binding and functions: SAA as a hub in macromolecular interaction networks. FEBS Lett. 590:6 (2016), 866–879.
22. Tanaka, M., Nishimura, A., Takeshita, H., Takase, H., Yamada, T., Mukai, T., Effect of lipid environment on amyloid fibril formation of human serum amyloid A. Chem. Phys. Lipids 202 (2017), 6–12.
23. Jayaraman, S., Gantz, D.L., Haupt, C., Gursky, O., Serum amyloid A forms stable oligomers that disrupt vesicles at lysosomal pH and contribute to the pathogenesis of reactive amyloidosis. Proc. Natl. Acad. Sci. U.S.A. 114:32 (2017), E6507–E6515.
24. Jayaraman, S., Haupt, C., Gursky, O., Paradoxical effects of SAA on lipoprotein oxidation suggest a new antioxidant function for SAA. J. Lipid Res. 57:12 (2016), 2138–2149.
25. Derebe, M.G., Zlatkov, C.M., Gattu, S., Ruhn, K.A., Vaishnava, S., Diehl, G.E., MacMillan, J.B., Williams, N.S., Hooper, L.V., Serum amyloid A is a retinol binding protein that transports retinol during bacterial infection. eLife, 3, 2014, e03206.
26. Hu, Z., Bang, Y.J., Ruhn, K.A., Hooper, L.V., Molecular basis for retinol binding by serum amyloid A during infection. Proc. Natl. Acad. Sci. U.S.A. 116:38 (2019), 19077–19082.
27. Jayaraman, S., Fändrich, M., Gursky, O., Synergy between serum amyloid A and secretory phospholipase A2 suggests a vital role for an ancient protein in lipid clearance. eLife 46630:1 (2019), 200–210.
28. Stonik, J.A., Remaley, A.T., Demosky, S.J., Neufeld, E.B., Bocharov, A., Brewer, H.B., Serum amyloid A promotes ABCA1-dependent and ABCA1-independent lipid efflux from cells. Biochem. Biophys. Res. Commun. 321:4 (2004), 936–941.
29. Frame, N.M., Jayaraman, S., Gantz, D.L., Gursky, O., Serum amyloid A self-assembles with phospholipids to form stable protein-rich nanoparticles with a distinct structure: a hypothetical function of SAA as a “molecular mop” in immune response. J. Struct. Biol. 200:3 (2017), 293–302.
30. Colón, W., Aguilera, J.J., Srinivasan, S., Intrinsic stability, oligomerization, and amyloidogenicity of HDL-free serum amyloid A. Adv. Exp. Med. Biol. 855 (2015), 117–134.
31. Lu, J., Yu, Y., Zhu, I., Cheng, Y., Sun, P.D., Structural mechanism of serum amyloid A-mediated inflammatory amyloidosis. Proc. Natl. Acad. Sci. U.S.A. 111:14 (2014), 5189–5194.
32. Patel, H., Bramall, J., Waters, H., De Beer, M.C., Woo, P., Expression of recombinant human serum amyloid A in mammalian cells and demonstration of the region necessary for high-density lipoprotein binding and amyloid fibril formation by site-directed mutagenesis. Biochem. J. 318:3 (1996), 1041–1049.
33. Wang, L., Colón, W., The interaction between apolipoprotein serum amyloid A and high-density lipoprotein. Biochem. Biophys. Res. Commun. 317:1 (2004), 157–361.
34. Liberta, F., Loerch, S., Rennegarbe, M., Schierhorn, A., Westermark, P., Westermark, G.T., Hazenberg, B.P.C., Grigorieff, N., Fändrich, M., Schmidt, M., Cryo-EM fibril structures from systemic AA amyloidosis reveal the species complementarity of pathological amyloids. Nat. Commun., 10(1), 2019, 1104.
35. Engen, J.R., Wales, T.E., Shi, X., Hydrogen exchange mass spectrometry for conformational analysis of proteins. Encyclopedia of Analytical Chemistry, 2011, John Wiley, Chichester. R. A. Meyers, 10.1002/9780470027318.a9201.
36. Patke, S., Srinivasan, S., Maheshwari, R., Srivastava, S.K., J Aguilera, J., Colón, W., Kane, R.S., Characterization of the oligomerization and aggregation of human Serum Amyloid A. PloS One, 8(6), 2013 e64974.
37. Ferraro, D.M., Lazo, N., Robertson, A.D., EX1 hydrogen exchange and protein folding. Biochemistry 43:3 (2004), 587–594.
38. Weis, D.D., Wales, T.E., Engen, J.R., Hotchko, M., Ten Eyck, L.F., Identification and characterization of EX1 kinetics in H/D exchange mass spectrometry by peak width analysis. J. Am. Soc. Mass Spectrom. 17:11 (2006), 1498–1509.
39. Stevens, F.J., Hypothetical structure of human serum amyloid A protein. Amyloid 11 (2004), 71–80.
40. Neculai, D., Schwake, M., Ravichandran, M., Zunke, F., Collins, R.F., Peters, J., Neculai, M., Plumb, J., Loppnau, P., Pizarro, J.C., Seitova, A., Trimble, W.S., Saftig, P., Grinstein, S., Dhe-Paganon, S., Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36. Nature 504:7478 (2013), 172–176.
41. Conrad, K.S., Cheng, T.W., Ysselstein, D., Heybrock, S., Hoth, L.R., Chrunyk, B.A., Am Ende, C.W., Krainc, D., Schwake, M., Saftig, P., Liu, S., Qiu, X., Ehlers, M.D., Lysosomal integral membrane protein-2 as a phospholipid receptor revealed by biophysical and cellular studies. Nat. Commun., 8(1), 2017, 1908.
42. Straub, J.E., Thirumalai, D., Principles governing oligomer formation in amyloidogenic peptides. Curr. Opin. Struct. Biol. 20:2 (2010), 187–195.
43. Straub, J.E., Thirumalai, D., Toward a molecular theory of early and late events in monomer to amyloid fibril formation. Annu. Rev. Phys. Chem. 62 (2011), 437–463.
44. Hoyer, W., Grönwall, C., Jonsson, A., Ståhl, S., Härd, T., Stabilization of a β-hairpin in monomeric Alzheimer's amyloid-β peptide inhibits amyloid formation. Proc. Natl. Acad. Sci. U.S.A. 105:13 (2008), 5099–5104.
45. Orr, A.A., Shaykhalishahi, H., Mirecka, E.A., Jonnalagadda, S.V.R., Hoyer, W., Tamamis, P., Elucidating the multi-targeted anti-amyloid activity and enhanced islet amyloid polypeptide binding of β-wrapins. Comput. Chem. Eng. 116 (2018), 322–332.
46. Sipe, J., Revised nomenclature for serum amyloid A (SAA). Nomencl Committ. Int. Soc. Amyloidosis vol. 6:1 (1999), 67–70 Part 2, Amyloid.
47. Kollmer, M., Meinhardt, K., Haupt, C., Liberta, F., Wulff, M., Linder, J., Handl, L., Heinrich, L., Loos, C., Schmidt, M., Syrovets, T., Simmet, T., Westermark, P., Westermark, G.T., Horn, U., Schmidt, V., Walther, P., Fändrich, M., Electron tomography reveals the fibril structure and lipid interactions in amyloid deposits. Proc. Natl. Acad. Sci. U.S.A. 113:20 (2016), 5604–5609.
48. Das, M., Wilson, C.J., Mei, X., Wales, T.E., Engen, J.R., Gursky, O., Structural stability and local dynamics in disease-causing mutants of human apolipoprotein A-I: what makes the protein amyloidogenic?. J. Mol. Biol. 428:2 Pt B (2016), 449–462.
49. Masson, G.R., Burke, J.E., Ahn, N.G., Anand, G.S., Borchers, C., Brier, S., Bou-Assaf, G.M., Engen, J.R., Englander, S.W., Faber, J., Garlish, R., Griffin, P.R., Gross, M.L., Guttman, M., Hamuro, Y., Heck, A.J.R., Houde, D., Iacob, R.E., Jørgensen, T.J.D., Kaltashov, I.A., Klinman, J.P., Konermann, L., Man, P., Mayne, L., Pascal, B.D., Reichmann, D., Skehel, M., Snijder, J., Strutzenberg, T.S., Underbakke, E.S., Wagner, C., Wales, T.E., Walters, B.T., Weis, D.D., Wilson, D.J., Wintrode, P.L., Zhang, Z., Zheng, J., Schriemer, D.C., Rand, K.D., Recommendations for performing, interpreting and reporting hydrogen deuterium exchange mass spectrometry (HDX-MS) experiments. Nat. Methods 16:7 (2019), 595–602.
50. Perez-Riverol, Y., Csordas, A., Bai, J., Bernal-Llinares, M., Hewapathirana, S., Kundu, D.J., Inuganti, A., Griss, J., Maye, r. G., Eisenacher, M., Pérez, E., Uszkoreit, J., Pfeuffer, J., Sachsenberg, T., Yilma, z. S., Tiwary, S., Cox, J., Audain, E., Walzer, M., Jarnuczak, A.F., Ternent, T., Brazma, A., Vizcaíno, J.A., The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47:D1 (2019), D442–D450.
51. Abraham, M.J., Murtola, T., Schulz, R., Páll, S., Smith, J.C., Hess, B., Linda h, E., Gromacs: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2 (2015), 19–25.
52. Huang, J., Rauscher, S., Nawrocki, G., Ran, T., Feig, M., de Groot, B.L., Grubmüller, H., MacKerell, A.D., CHARMM36m: an improved force field for folded and intrinsically disordered proteins. Nat. Methods 14:1 (2017), 71–73.
53. Klauda, J.B., Venable, R.M., Freites, J.A., O'Connor, J.W., Tobias, D.J., Mondragon-Ramirez, C., Vorobyov, I., MacKerell, A.D. Jr., Pastor, R.W., Update of the CHARMM all-atom additive force Field for lipids: validation on six lipid types. J. Phys. Chem. B 114:23 (2010), 7830–7843.
54. Humphrey, W., Dalke, A., Schulten, K., VMD: visual molecular dynamics. J. Mol. Graph. 14:1 (1996), 33–38.
55. Gowers, R., Linke, M., Barnoud, J., Reddy, T., Melo, M., Seyle, r. S., Domanski, J., Dotson, D.L., Buchouxk, S., Kenney, I.M., Beckstein, O., MDAnalysis: a Python package for the rapid analysis of molecular dynamics simulations, Proceedings of the 15th Python in Science Conference (Scipy). 2018, 98–105.
56. Heinig, M., Frishman, D., STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins. Nucleic Acids Res. 32 (2004), W500–W502.
57. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., Klein, M.L., Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:2 (1983), 926–935.
58. Hoover, W.G., Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A 31:3 (1985), 1695–1697.
59. Nosé, S., A unified formulation of the constant temperature molecular dynamics methods. J. Chem. Phys. 81:1 (1984), 511–519.
60. Parrinello, M., Rahman, A., Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52:12 (1981), 7182–7190.
61. Jo, S., Cheng, X., Lee, J., Kim, S., Park, S.-J., Patel, D.S., Beaven, A.H., Lee, K.I., Rui, H., Park, S., Lee, H.S., Roux, B., MacKerell, A.D. Jr., Klauda, J.B., Qi, Y., Im, W., CHARMM-GUI 10 years for biomolecular modeling and simulation. J. Comput. Chem. 38:15 (2017), 1114–1124.
62. Daura, X., Gademann, K., Jaun, B., Seebac, h. D., van Gunsteren, W.F., Mark, A.E., Peptide folding: when simulation meets experiment. Angew. Chem. Int. 38:1–2 (1999), 236–240.
63. Martínez, L., Andrade, R., Birgin, E.G., Martínez, J.M., PACKMOL: a package for building initial configurations for molecular dynamics simulations. J. Comput. Chem. 30:13 (2009), 2157–2164.
64. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., D Thompson, J., Higgins, D.G., Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7, 2011, 539.
65. Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M., Barto, n. G.J., Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:9 (2009), 1189–1191 http://www.jalview.org/.
66. Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., umienny, G.R., Heer, F.T., de Beer, T.A.P., Rempfer, C., Bordoli, L., Lepore, R., Schwede, T., SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 46:W1 (2018), W296–W303.