HDL surface lipids mediate CETP binding as revealed by electron microscopy and molecular dynamics simulation

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Zhang, Meng ^a   Charles, River ^a   Tong, Huimin ^a   Zhang, Lei ^a   Patel, Mili ^b   Wang, Francis ^a   Rames, Matthew J ^a   Ren, Amy ^a   Rye, Kerry Anne ^b   Qiu, Xiayang ^c   Johns, Douglas G ^d   Charles, M Arthur ^e   Ren, Gang ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c PFIZER INC   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CETP PROTEIN, HUMAN; CHOLESTEROL ESTER TRANSFER PROTEIN; HIGH DENSITY LIPOPROTEIN; LIPOSOME; MEMBRANE LIPID; PROTEIN BINDING; RECOMBINANT PROTEIN;

BLOOD; CHEMICAL PHENOMENA; CHEMISTRY; CRYOELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

CHOLESTEROL ESTER TRANSFER PROTEINS; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMAGING, THREE-DIMENSIONAL; LIPOPROTEINS, HDL; LIPOSOMES; MEMBRANE LIPIDS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; RECOMBINANT PROTEINS;

EID: 84924187426     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08741     Document Type: Article

References (56)

1. Drayna, D. et al. Cloning and sequencing of human cholesteryl ester transfer protein cDNA. Nature 327, 632-4 (1987).
2. Inazu, A. et al. Increased high-density lipoprotein levels caused by a common cholesteryl-ester transfer protein gene mutation. N Engl J Med 323, 1234-8 (1990).
3. Brown, M. L. et al. Molecular basis of lipid transfer protein deficiency in a family with increased high-density lipoproteins. Nature 342, 448-51 (1989).
4. Zhong, S. et al. Increased coronary heart disease in Japanese-American men with mutation in the cholesteryl ester transfer protein gene despite increased HDL levels. J Clin Invest 97, 2917-23 (1996).
5. Barter, P. J. et al. Effects of torcetrapib in patients at high risk for coronary events. N Engl J Med 357, 2109-22 (2007).
6. Funder, J. W. The off-target effects of torcetrapib. Endocrinology 150, 2024-6 (2009).
7. Stein, E. A. et al. Safety and tolerability of dalcetrapib. Am J Cardiol 104, 82-91 (2009).
8. Derks, M., Anzures-Cabrera, J., Turnbull, L. & Phelan, M. Safety, tolerability and pharmacokinetics of dalcetrapib following single and multiple ascending doses in healthy subjects: a randomized, double-blind, placebo-controlled, phase I study. Clin Drug Investig 31, 325-35 (2011).
9. Gotto, A. M., Jr. et al. Evaluation of lipids, drug concentration, and safety parameters following cessation of treatment with the cholesteryl ester transfer protein inhibitor anacetrapib in patients with or at high risk for coronary heart disease. Am J Cardiol 113, 76-83 (2014).
10. Friedrich, S. et al. The pharmacokinetics and pharmacokinetic/pharmacodynamic relationships of evacetrapib administered as monotherapy or in combination with statins. CPT Pharmacometrics Syst Pharmacol 3, e94 (2014).
11. Qiu, X. et al. Crystal structure of cholesteryl ester transfer protein reveals a long tunnel and four bound lipid molecules. Nat Struct Mol Biol 14, 106-13 (2007).
12. Liu, S. et al. Crystal structures of cholesteryl ester transfer protein in complex with inhibitors. J Biol Chem 287, 37321-9 (2012).
13. Zhang, L. et al. Structural basis of transfer between lipoproteins by cholesteryl ester transfer protein. Nat Chem Biol 8, 342-9 (2012).
14. Lei, D. et al. Structural features of cholesteryl ester transfer protein: a molecular dynamics simulation study. Proteins 81, 415-25 (2013).
15. Cilpa-Karhu, G., Jauhiainen,M. & Riekkola, M. L. Atomistic molecular dynamics simulation reveals the mechanism by which CETP penetrates into HDL enabling lipid transfer from HDL to CETP. J Lipid Res (2014).
16. van Antwerpen, R., La Belle, M., Navratilova, E. & Krauss, R. M. Structural heterogeneity of apoB-containing serum lipoproteins visualized using cryoelectron microscopy. J Lipid Res 40, 1827-36 (1999).
17. van Antwerpen, R. et al. Cryo-electron microscopy of low density lipoprotein and reconstituted discoidal high density lipoprotein: imaging of the apolipoprotein moiety. J Lipid Res 38, 659-69 (1997).
18. Pattnaik, N. M. & Zilversmit, D. B. Interaction of cholesteryl ester exchange protein with human plasma lipoproteins and phospholipid vesicles. J Biol Chem 254, 2782-6 (1979).
19. Jeyarajah, E. J., Cromwell, W. C. & Otvos, J. D. Lipoprotein particle analysis by nuclear magnetic resonance spectroscopy. Clin Lab Med 26, 847-70 (2006).
20. Otvos, J. D., Jeyarajah, E. J. & Cromwell, W. C. Measurement issues related to lipoprotein heterogeneity. Am J Cardiol 90, 22i-29i (2002).
21. Lund-Katz, S., Liu, L., Thuahnai, S. T. & Phillips, M. C. High density lipoprotein structure. Front Biosci 8, d1044-54 (2003).
22. Orlova, E. V. et al. Three-dimensional structure of low density lipoproteins by electron cryomicroscopy. Proc Natl Acad Sci U S A 96, 8420-5 (1999).
23. Zhang, L. et al. An optimized negative-staining protocol of electron microscopy for apoE4 POPC lipoprotein. J Lipid Res 51, 1228-36 (2010).
24. Zhang, L., Tong, H., Garewal, M. & Ren, G. Optimized negative-staining electron microscopy for lipoprotein studies. Biochim Biophys Acta 1830, 2150-9 (2013).
25. Zhang, L. et al.Morphology and structure of lipoproteins revealed by an optimized negative-staining protocol of electron microscopy. J Lipid Res 52, 175-84 (2011).
26. Zhang, B. et al. Effects of reconstituted HDL on charge-based LDL subfractions as characterized by capillary isotachophoresis. J Lipid Res 48, 1175-89 (2007).
27. Zhang, L. & Ren, G. IPET and FETR: experimental approach for studying molecular structure dynamics by cryo-electron tomography of a single-molecule structure. PLoS One 7, e30249 (2012).
28. Fernandez, J. J., Li, S. & Crowther, R. A. CTF determination and correction in electron cryotomography. Ultramicroscopy 106, 587-96 (2006).
29. Jensen, M. B. et al. Membrane curvature sensing by amphipathic helices: a single liposome study using alpha-synuclein and annexin B12. J Biol Chem 286, 42603-14 (2011).
30. Barter, P. J. & Jones, M. E. Kinetic studies of the transfer of esterified cholesterol between human plasma low and high density lipoproteins. J Lipid Res 21, 238-49 (1980).
31. Ihm, J., Quinn, D. M., Busch, S. J., Chataing, B. & Harmony, J. A. Kinetics of plasma protein-catalyzed exchange of phosphatidylcholine and cholesteryl ester between plasma lipoproteins. J Lipid Res 23, 1328-41 (1982).
32. Tall, A. R. Plasma cholesteryl ester transfer protein. J Lipid Res 34, 1255-74 (1993).
33. Ren, G. et al. Model of human low-density lipoprotein and bound receptor based on cryoEM. Proc Natl Acad Sci U S A 107, 1059-64 (2010).
34. Morton, R. E. & Zilversmit, D. B. Inter-relationship of lipids transferred by the lipid-transfer protein isolated from human lipoprotein-deficient plasma. J Biol Chem 258, 11751-7 (1983).
35. Bruce, C. et al.Molecular determinants of plasma cholesteryl ester transfer protein binding to high density lipoproteins. J Biol Chem 270, 11532-42 (1995).
36. Dergunov, A. D., Shabrova, E. V. & Dobretsov, G. E. Cholesteryl ester diffusion, location and self-association constraints determine CETP activity with discoidal HDL: Excimer probe study. Arch Biochem Biophys 564, 211-8 (2014).
37. Koivuniemi, A., Vuorela, T., Kovanen, P. T., Vattulainen, I. & Hyvonen, M. T. Lipid exchange mechanism of the cholesteryl ester transfer protein clarified by atomistic and coarse-grained simulations. PLoS Comput Biol 8, e1002299 (2012).
38. Han, S. et al. Comparison of lipoprotein separation and lipid analysis methodologies for human and cynomolgus monkey plasma samples. J Cardiovasc Transl Res 5, 75-83 (2012).
39. Rye, K. A., Hime, N. J. & Barter, P. J. Evidence that cholesteryl ester transfer protein-mediated reductions in reconstituted high density lipoprotein size involve particle fusion. J Biol Chem 272, 3953-60 (1997).
40. Rye, K. A. & Barter, P. J. The influence of apolipoproteins on the structure and function of spheroidal, reconstituted high density lipoproteins. J Biol Chem 269, 10298-303 (1994).
41. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for highresolution single-particle reconstructions. J Struct Biol 128, 82-97 (1999).
42. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116, 71-6 (1996).
43. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 142, 334-47 (2003).
44. Pettersen, E. F. et al. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-12 (2004).
45. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116, 190-9 (1996).
46. Scheres, S. H. & Chen, S. Prevention of overfitting in cryo-EM structure determination. Nat Methods 9, 853-4 (2012).
47. Kucerka, N., Nieh, M. P. & Katsaras, J. Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochim Biophys Acta 1808, 2761-71 (2011).
48. Tahara, Y. & Fujiyoshi, Y. A new method to measure bilayer thickness: cryoelectron microscopy of frozen hydrated liposomes and image simulation. Micron 25, 141-9 (1994).
49. Risselada, H. J.&Marrink, S. J. Curvature effects on lipid packing and dynamics in liposomes revealed by coarse grained molecular dynamics simulations. Phys Chem Chem Phys 11, 2056-67 (2009).
50. de Vries, A. H.,Mark, A. E. &Marrink, S. J. Molecular dynamics simulation of the spontaneous formation of a small DPPC vesicle in water in atomistic detail. J Am Chem Soc 126, 4488-9 (2004).
51. Marrink, S. J. & Mark, A. E. Molecular dynamics simulation of the formation, structure, and dynamics of small phospholipid vesicles. J Am Chem Soc 125, 15233-42 (2003).
52. Marrink, S. J., de Vries, A. H. & Mark, A. E. Coarse grained model for semiquantitative lipid simulations. Journal of Physical Chemistry B 108, 750-760 (2004).
53. Marrink, S. J., Risselada, J. & Mark, A. E. Simulation of gel phase formation and melting in lipid bilayers using a coarse grained model. Chem Phys Lipids 135, 223-44 (2005).
54. Shih, A. Y., Freddolino, P. L., Arkhipov, A. & Schulten, K. Assembly of lipoprotein particles revealed by coarse-grained molecular dynamics simulations. J Struct Biol 157, 579-92 (2007).
55. Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J Comput Chem 26, 1781-802 (2005).
56. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J Mol Graph 14, 33-8, 27-8 (1996).