Three-dimensional cryoEM reconstruction of native LDL particles to 16å resolution at physiological body temperature

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Kumar, Vibhor ^a,b   Butcher, Sarah J ^c   Öörni, Katariina ^d   Engelhardt, Peter ^a,e   Heikkonen, Jukka ^a,f   Kaski, Kimmo ^a   Ala Korpela, Mika ^g   Kovanen, Petri T ^d  

^a AALTO UNIVERSITY   (Finland)

^b GENOME INSTITUTE OF SINGAPORE   (Singapore)

^c UNIVERSITY OF HELSINKI   (Finland)

^d WIHURI RESEARCH INSTITUTE   (Finland)

^e UNIVERSITY OF HELSINKI   (Finland)

^f UNIVERSITY OF TURKU   (Finland)

^g UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B100; CHOLESTEROL ESTER; LIPOVITELLIN; LOW DENSITY LIPOPROTEIN;

ARTICLE; BINDING AFFINITY; BODY TEMPERATURE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; HUMAN; IMAGE RECONSTRUCTION; LIPID ANALYSIS; PARTICLE SIZE; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE; THREE DIMENSIONAL IMAGING; X RAY ANALYSIS; METHODOLOGY; ULTRASTRUCTURE;

BODY TEMPERATURE; CRYOELECTRON MICROSCOPY; HUMANS; LIPOPROTEINS, LDL;

EID: 79955914489     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018841     Document Type: Article

References (51)

1. Brown MS, Kovanen PT, Goldstein JL, (1981) Regulation of plasma cholesterol by lipoprotein receptors. Science 212: 628-35.
2. Hegele RA, (2009) Plasma lipoproteins: genetic influences and clinical implications. Nat Rev Genet 10: 109-121.
3. Williams KJ, Tabas I, (1998) The response-to-retention hypothesis of atherogenesis reinforced. Curr Opin Lipidol 9: 471-474.
4. Hevonoja T, Pentikäinen MO, Hyvonen MT, Kovanen PT, Ala-Korpela M, (2000) Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim Biophys Acta 1488: 189-210.
5. Pentikäinen MO, Öörni K, Ala-Korpela M, Kovanen PT, (2000) Modified LDL- trigger of atherosclerosis and inflammation in the arterial intima. J Intern Med 247: 359-370.
6. Steim JM, Edner OJ, Bargoot FG, (1968) Structure of human serum lipoproteins: nuclear magnetic resonance supports a micellar model. Science 162: 909-911.
7. Öörni K, Pentikäinen MO, Ala-Korpela M, Kovanen PT, (2000) Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J Lipid Res 41: 1703-1714.
8. Kumpula LS, Kumpula JM, Taskinen MR, Jauhiainen M, Kaski K, et al. (2008) Reconsideration of hydrophobic lipid distributions in lipoprotein particles. Chem Phys Lipids 155: 57-62.
9. Prassl R, Laggner P, (2009) Molecular structure of low density lipoprotein: current status and future challenges. Eur Biophys J 38: 145-158.
10. Segrest JP, Jones MK, De Loof H, Dashti N, (2001) Structure of apolipoprotein B-100 in low density lipoproteins. J Lipid Res 42: 1346-1367.
11. Schumaker VN, Phillips ML, Chatterton JE, (1994) Apolipoprotein B and low-density lipoprotein structure: implications for biosynthesis of triglyceride-rich lipoproteins. Adv Protein Chem 45: 205-248.
12. Thompson JR, Banaszak LJ, (2002) Lipid-protein interactions in lipovitellin. Biochemistry 41: 9398-9409.
13. Koivuniemi A, Kovanen PT, Hyvönen MT, (2008) Molecular dynamics simulations of a lipovitellin-derived amphiphilic beta-sheet homologous to apoB-100 beta-sheets at a hydrophobic decane-water interface. Biochim Biophys Acta 1784: 1668-1675.
14. Wang L, Walsh MT, Small DM, (2006) Apolipoprotein B is conformationally flexible but anchored at a triolein/water interface: a possible model for lipoprotein surfaces. Proc Natl Acad Sci U S A 103: 6871-6876.
15. Baumstark MW, Kreutz W, Berg A, Frey I, Keul J, (1990) Structure of human low-density lipoprotein subfractions, determined by X-ray small-angle scattering. Biochim Biophys Acta 1037: 48-57.
16. Coronado-Gray A, van Antwerpen R, (2005) Lipid composition influences the shape of human low density lipoprotein in vitreous ice. Lipids 40: 495-500.
17. Sherman MB, Orlova EV, Decker GL, Chiu W, Pownall HJ, (2003) Structure of triglyceride-rich human low-density lipoproteins according to cryoelectron microscopy. Biochemistry 42: 14988-14993.
18. van Antwerpen R, Chen GC, Pullinger CR, Kane JP, LaBelle M, et al. (1997) Cryo-electron microscopy of low density lipoprotein and reconstituted discoidal high density lipoprotein: imaging of the apolipoprotein moiety. J Lipid Res 38: 659-669.
19. van Antwerpen R, Gilkey JC, (1994) Cryo-electron microscopy reveals human low density lipoprotein substructure. J Lipid Res 35: 2223-2231.
20. van Antwerpen R, La Belle M, Navratilova E, Krauss RM, (1999) Structural heterogeneity of apoB-containing serum lipoproteins visualized using cryo-electron microscopy. J Lipid Res 40: 1827-1836.
21. Orlova EV, Sherman MB, Chiu W, Mowri H, Smith LC, et al. (1999) Three-dimensional structure of low density lipoproteins by electron cryomicroscopy. Proc Natl Acad Sci U S A 96: 8420-8425.
22. Poulos GW, (2001) The three-dimensional structure of low-density lipoprotein via cryoelectron microscopy. Boston Boston University University Microfilms International, Publication #AAT 993754.ISBN 0-493-01861-1.
23. Ren G, Rudenko G, Ludtke SJ, Deisenhofer J, Chiu W, et al. (2010) Model of human low-density lipoprotein and bound receptor based on cryoEM. Proc Natl Acad Sci U S A 107: 1059-1064.
24. Johs A, Hammel M, Waldner I, May RP, Laggner P, et al. (2006) Modular structure of solubilized human apolipoprotein B-100. Low resolution model revealed by small angle neutron scattering. J Biol Chem 281: 19732-19739.
25. Kumar V, Heikkonen J, Engelhardt P, Kaski K, (2004) Robust filtering and particle picking in micrograph images towards 3D reconstruction of purified proteins with cryo-electron microscopy. J Struct Biol 145: 41-51.
26. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
27. Adrian M, Dubochet J, Lepault J, McDowall AW, (1984) Cryo-electron microscopy of viruses. Nature (London) 308: 32-36.
28. Huiskonen JT, Kivelä HM, Bamford DH, Butcher SJ, (2004) The PM2 virion has a novel organization with an internal membrane and pentameric receptor binding spikes. Nat Struct Mol Biol 11: 850-856.
29. Ludtke SJ, Baldwin PR, Chiu W, (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97.
30. Frank J, (2006) Three-dimensional electron microscopy of macromolecular assemblies. New York Oxford University Press.
31. van Heel M, Frank J, (1981) Use of multivariate statistics in analysing the images of biological macromolecules. Ultramicroscopy 6: 187-194.
32. Penczek PA, Frank J, Spahn CM, (2006) A method of focused classification, based on the bootstrap 3D variance analysis, and its application to EF-G-dependent translocation. J Struct Biol 154: 184-194.
33. Penczek PA, Yang C, Frank J, Spahn CM, (2006) Estimation of variance in single-particle reconstruction using the bootstrap technique. J Struct Biol 154: 168-183.
34. Garzon JI, Kovacs J, Abagyan R, Chacon P, (2007) ADP_EM: fast exhaustive multi-resolution docking for high-throughput coverage. Bioinformatics 23: 427-433.
35. Jiang ZG, Carraway M, McKnight CJ, (2005) Limited proteolysis and biophysical characterization of the lipovitellin homology region in apolipoprotein B. Biochemistry 44: 1163-1173.
36. Segrest JP, Jones MK, Dashti N, (1999) N-terminal domain of apolipoprotein B has structural homology to lipovitellin and microsomal triglyceride transfer protein: a "lipid pocket" model for self-assembly of apob-containing lipoprotein particles. J Lipid Res 40: 1401-1416.
37. Anderson TA, Levitt DG, Banaszak LJ, (1998) The structural basis of lipid interactions in lipovitellin, a soluble lipoprotein. Structure 6: 895-909.
38. Roseman AM, (2000) Docking structures of domains into maps from cryo-electron microscopy using local correlation. Acta Crystallogr D Biol Crystallogr 56: 1332-1340.
39. Chatterton JE, Phillips ML, Curtiss LK, Milne R, Fruchart JC, et al. (1995) Immunoelectron microscopy of low density lipoproteins yields a ribbon and bow model for the conformation of apolipoprotein B on the lipoprotein surface. J Lipid Res 36: 2027-2037.
40. Richardson PE, Manchekar M, Dashti N, Jones MK, Beigneux A, et al. (2005) Assembly of lipoprotein particles containing apolipoprotein-B: structural model for the nascent lipoprotein particle. Biophys J 88: 2789-2800.
41. Ginsburg GS, Atkinson D, Small DM, (1984) Physical properties of cholesteryl esters. Prog Lipid Res 23: 135-167.
42. Segrest JP, Jones MK, Mishra VK, Anantharamaiah GM, Garber DW, (1994) apoB-100 has a pentapartite structure composed of three amphipathic alpha-helical domains alternating with two amphipathic beta-strand domains. Detection by the computer program LOCATE. Arterioscler Thromb 14: 1674-1685.
43. Ritter S, Frey I, Diederichs K, Grathwohl D, Keul J, et al. (1997) Crystallization and preliminary X-ray diffraction data of two different human low-density lipoprotein (LDL) subfractions. Proteins 28: 293-297.
44. Qiu X, Mistry A, Ammirati MJ, Chrunyk BA, Clark RW, et al. (2007) Crystal structure of cholesteryl ester transfer protein reveals a long tunnel and four bound lipid molecules. Nat Struct Mol Biol 14: 106-113.
45. Krisko A, Etchebest C, (2007) Theoretical model of human apolipoprotein B100 tertiary structure. Proteins 66: 342-358.
46. Coronado-Gray A, van Antwerpen R, (2003) The physical state of the LDL core influences the conformation of apolipoprotein B-100 on the lipoprotein surface. FEBS Lett 533: 21-24.
47. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-12.
48. Scheres SHW, Gao H, Valle M, Herman GT, Eggermont PPB, et al. (2007) Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat Methods 4: 27-29.
49. White HE, Saibil HR, Ignatiou A, Orlova EV, (2004) Recognition and Separation of Single Particles with Size Variation by Statistical Analysis of their Images. J Mol Biol 336: 453-460.
50. Elmlund D, Davis R, Elmlund H, (2010) Ab initio structure determination from electron microscopic images of single molecules coexisting in different functional states. Structure 18: 777-86.51.
51. Elad N, Clare DK, Saibil HR, Orlova EV, (2008) Detection and separation of heterogeneity in molecular complexes by statistical analysis of their two-dimensional projections. J Struct. Biol 162: 108-120.