Structural plasticity of cholesteryl ester transfer protein assists the lipid transfer activity

Journal of Biological Chemistry

Volumn 291, Issue 37, 2016, Pages 19462-19473

  Chirasani, Venkat R ^a   Revanasiddappa, Prasanna D ^a   Senapati, Sanjib ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLOGY; DISEASES; ESTERS; LIPIDS; LIPOPROTEINS; MEDICAL IMAGING; MOLECULAR DYNAMICS; PROTEINS;

CARDIO-VASCULAR DISEASE; CHOLESTERYL ESTER TRANSFER PROTEINS; CONFORMATIONAL FLEXIBILITY; CONFORMATIONAL SWITCHING; LARGE-SCALE DYNAMICS; LINEAR CONFORMATION; MOLECULAR DYNAMICS SIMULATIONS; NORMAL MODE ANALYSIS;

CRYSTAL STRUCTURE;

CHOLESTEROL ESTER; CHOLESTEROL ESTER TRANSFER PROTEIN; LIPOPROTEIN; CETP PROTEIN, HUMAN; TRIACYLGLYCEROL;

ARTICLE; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; HYDROPHOBICITY; LIPID TRANSPORT; MOLECULAR DYNAMICS; PLASTICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; SIMULATION; CHEMISTRY; HUMAN; METABOLISM; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

CHOLESTEROL ESTER TRANSFER PROTEINS; CHOLESTEROL ESTERS; CRYSTALLOGRAPHY, X-RAY; HUMANS; PROTEIN DOMAINS; STRUCTURE-ACTIVITY RELATIONSHIP; TRIGLYCERIDES;

EID: 84986917815     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.744623     Document Type: Article

References (48)

1. Sharrett, A. R., Ballantyne, C. M., Coady, S. A., Heiss, G., Sorlie, P. D., Catellier, D., Patsch, W., and Atherosclerosis Risk in Communities Study Group (2001) Coronary heart disease prediction from lipoprotein cholesterol levels, triglycerides, lipoprotein(a), apolipoproteins A-I and B, and HDL density subfractions: the atherosclerosis risk in communities (ARIC) study. Circulation 104, 1108-1113
2. Luc, G., Bard, J.-M., Ferrières, J., Evans, A., Amouyel, P., Arveiler, D., Fruchart, J. C., and Ducimetière, P. (2002) Value of HDL cholesterol, apolipoprotein A-I, lipoprotein A-I, and lipoprotein A-I/A-II in prediction of coronary heart disease: The PRIME study. Arterioscler. Thromb. Vasc. Biol. 22, 1155-1161
3. Zhang, Y., Zanotti, I., Reilly, M. P., Glick, J. M., Rothblat, G. H., and Rader, D. J. (2003) Overexpression of apolipoprotein A-I promotes reverse transport of cholesterol from macrophages to feces in vivo. Circulation 108, 661-663
4. Tall, A. R., Yvan-Charvet, L., Terasaka, N., Pagler, T., and Wang, N. (2008) HDL, ABC transporters, and cholesterol efflux: implications for the treatment of atherosclerosis. Cell Metab. 7, 365-375
5. Cannon, C. P., Braunwald, E., McCabe, C. H., Rader, D. J., Rouleau, J. L., Belder, R., Joyal, S. V., Hill, K. A., Pfeffer, M. A., Skene, A. M., and Pravastatin or Atorvastatin Evaluation and Infection Therapy-Thrombolysis in Myocardial Infarction 22 Investigators (2004) Intensive versus moderate lipid lowering with statins after acute coronary syndromes. N. Engl. J. Med. 350, 1495-1504
6. Robins, S. J., Collins, D., Wittes, J. T., Papademetriou, V., Deedwania, P. C., Schaefer, E. J., McNamara, J. R., Kashyap, M. L., Hershman, J. M., Wexler, L. F., Rubins, H. B., and VA-HIT Study Group. Veterans Affairs High-Density Lipoprotein Intervention Trial (2001) Relation of gemfibrozil treatment and lipid levels with major coronary events: VA-HIT: a randomized controlled trial. JAMA 285, 1585-1591
7. Goldberg, A., Alagona, P., Jr., Capuzzi, D. M., Guyton, J., Morgan, J. M., Rodgers, J., Sachson, R., and Samuel, P. (2000) Multiple-dose efficacy and safety of an extended-release form of niacin in the management of hyperlipidemia. Am. J. Cardiol. 85, 1100-1105
8. Tall, A. R. (1993) Plasma cholesteryl ester transfer protein. J. Lipid Res. 34, 1255-1274
9. Barter, P. J., Brewer, H. B., Jr., Chapman, M. J., Hennekens, C. H., Rader, D. J., and Tall, A. R. (2003) Cholesteryl ester transfer protein: A novel target for raising HDL and inhibiting atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 23, 160-167
10. Zhong, S., Sharp, D. S., Grove, J. S., Bruce, C., Yano, K., Curb, J. D., and Tall, A. R. (1996) 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, 2917-2923
11. Koizumi, J., Mabuchi, H., Yoshimura, A., Michishita, I., Takeda, M., Itoh, H., Sakai, Y., Sakai, T., Ueda, K., and Takeda, R. (1985) Deficiency of serum cholesteryl-ester transfer activity in patients with familial hyperalphalipoproteinaemia. Atherosclerosis 58, 175-186
12. Brown, M. L., Inazu, A., Hesler, C. B., Agellon, L. B., Mann, C., Whitlock, M. E., Marcel, Y. L., Milne, R. W., Koizumi, J., and Mabuchi, H. (1989) Molecular basis of lipid transfer protein deficiency in a family with increased high-density lipoproteins. Nature 342, 448-451
13. Inazu, A., Brown, M. L., Hesler, C. B., Agellon, L. B., Koizumi, J., Takata, K., Maruhama, Y., Mabuchi, H., and Tall, A. R. (1990) Increased high-density lipoprotein levels caused by a common cholesteryl-ester transfer protein gene mutation. N. Engl. J. Med. 323, 1234-1238
14. Marotti, K. R., Castle, C. K., Boyle, T. P., Lin, A. H., Murray, R. W., and Melchior, G. W. (1993) Severe atherosclerosis in transgenic mice expressing simian cholesteryl ester transfer protein. Nature 364, 73-75
15. Plump, A. S., Masucci-Magoulas, L., Bruce, C., Bisgaier, C. L., Breslow, J. L., and Tall, A. R. (1999) Increased atherosclerosis in ApoE and LDL receptor gene knock-out mice as a result of human cholesteryl ester transfer protein transgene expression. Arterioscler. Thromb. Vasc. Biol. 19, 1105-1110
16. Sugano, M., Makino, N., Sawada, S., Otsuka, S., Watanabe, M., Okamoto, H., Kamada, M., and Mizushima, A. (1998) Effect of antisense oligonucleotides against cholesteryl ester transfer protein on the development of atherosclerosis in cholesterol-fed rabbits. J. Biol. Chem. 273, 5033-5036
17. Mantlo, N. B., and Escribano, A. (2014) Update on the discovery and development of cholesteryl ester transfer protein inhibitors for reducing residual cardiovascular risk. J. Med. Chem. 57, 1-17
18. Sikorski, J. A. (2006) Oral cholesteryl ester transfer protein (CETP) inhibitors: a potential new approach for treating coronary artery disease. J. Med. Chem. 49, 1-22
19. Gotto, A. M., Jr., and Moon, J. E. (2012) Safety of inhibition of cholesteryl ester transfer protein with anacetrapib: the DEFINE study. Expert Rev. Cardiovasc. Ther. 10, 955-963
20. Nicholls, S. J., Brewer, H. B., Kastelein, J. J. P., Krueger, K. A., Wang, M. D., Shao, M., Hu, B., McErlean, E., and Nissen, S. E. (2011) Effects of the CETP inhibitor evacetrapib administered as monotherapy or in combination with statins on HDL and LDL cholesterol: a randomized controlled trial. JAMA 306, 2099-2109
21. Zhang, L., Yan, F., Zhang, S., Lei, D., Charles, M. A., Cavigiolio, G., Oda, M., Krauss, R. M., Weisgraber, K. H., Rye K.-A., Pownall, H. J., Qiu, X., and Ren, G. (2012) Structural basis of transfer between lipoproteins by cholesteryl ester transfer protein. Nat. Chem. Biol. 8, 342-349
22. Lauer, M. E., Graff-Meyer, A., Rufer, A. C., Maugeais, C., von der Mark, E., Matile, H., D'Arcy, B., Magg, C., Ringler, P., Müller, S. A., Scherer, S., Dernick, G., Thoma, R., Hennig, M., Niesor, E. J., and Stahlberg, H. (2016) Cholesteryl ester transfer between lipoproteins does not require a ternary tunnel complex with CETP. J. Struct. Biol. 194, 191-198
23. Qiu, X., Mistry, A., Ammirati, M. J., Chrunyk, B. A., Clark, R. W., Cong, Y., Culp, J. S., Danley, D. E., Freeman, T. B., Geoghegan, K. F., Griffor, M. C., Hawrylik, S. J., Hayward, C. M., Hensley, P., Hoth, L. R., 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
24. Liu, S., Mistry, A., Reynolds, J. M., Lloyd, D. B., Griffor, M. C., Perry, D. A., Ruggeri, R. B., Clark, R. W., and Qiu, X. (2012) Crystal structures of cholesteryl ester transfer protein in complex with inhibitors. J. Biol. Chem. 287, 37321-37329
25. Lei, D., Rames, M., Zhang, X., Zhang, L., Zhang, S., and Ren, G. (2016) Insights into the tunnel mechanism of cholesteryl ester transfer protein using all-atom molecular dynamics simulations. J. Biol. Chem. 291, 14034-14044
26. Chirasani, V. R., Sankar, R., and Senapati, S. (2016) Mechanism of inhibition of cholesteryl ester transfer protein by small molecule inhibitors. J. Phys. Chem. B. 10.1021/acs.jpcb.6b01928
27. Koivuniemi, A., Vuorela, T., Kovanen, P. T., Vattulainen, I., and Hyvönen, M. T. (2012) Lipid exchange mechanism of the cholesteryl ester transfer protein clarified by atomistic and coarse-grained simulations. PLoS Comput. Biol. 8, e1002299
28. Äijänen, T., Koivuniemi A., Javanainen, M., Rissanen, S., Rog, T., and Vattulainen, I. (2014) How anacetrapib inhibits the activity of the cholesteryl ester transfer protein? Perspective through atomistic simulations. PLoS Comput. Biol. 10, e1003987
29. Senapati, S., and Berkowitz, M. L. (2003) Molecular dynamics simulation studies of polyether and perfluoropolyether surfactant based reverse micelles in supercritical carbon dioxide. J. Phys. Chem. B 107, 12906-12916
30. Alexandrov, V., Lehnert, U., Echols, N., Milburn, D., Engelman, D., and Gerstein, M. (2005) Normal modes for predicting protein motions: a comprehensive database assessment and associated Web tool. Protein Sci. 14, 633-643
31. Layten, M., Hornak, V., and Simmerling, C. (2006) The open structure of a multi-drug-resistant HIV-1 protease is stabilized by crystal packing contacts. J. Am. Chem. Soc. 128, 13360-13361
32. Wang, S., Kussie, P., Deng, L., and Tall, A. (1995) Defective binding of neutral lipids by a carboxyl-terminal deletion mutant of cholesteryl ester transfer protein: evidence for a carboxyl-terminal cholesteryl ester binding site essential for neutral lipid transfer activity. J. Biol. Chem. 270, 612-618
33. Webb, B., and Sali, A. (2014) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics 47, 5.6.1-5.6.37
34. Schuler, L. D., Daura, X., and van Gunsteren, W. F. (2001) An improved GROMOS96 force field for aliphatic hydrocarbons in the condensed phase. J. Comput. Chem. 22, 1205-1218
35. Berger, O., Edholm, O., and Jähnig, F. (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72, 2002-2013
36. Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8, 52-56, 29.
37. Bussi, G., Donadio, D., and Parrinello, M. (2007) Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101
38. Parrinello, M., and Rahman, A. (1981) Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52, 7182-7190
39. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577-8593
40. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463-1472
41. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435- 447
42. Eyal, E., Yang, L. W., and Bahar, I. (2006) Anisotropic network model : systematic evaluation and a new web interface. Bioinformatics 22, 2619-2627
43. Doruker, P., Atilgan, A. R., and Bahar, I. (2000) Dynamics of proteins predicted by molecular dynamics simulations and analytical approaches: application to α-amylase inhibitor. Proteins 40, 512-524
44. Chovancova, E., Pavelka, A., Benes, P., Strnad, O., Brezovsky, J., Kozlikova, B., Gora, A., Sustr, V., Klvana, M., Medek, P., Biedermannova, L., Sochor, J., and Damborsky, J. (2012) CAVER 3.0: a tool for the analysis of transport pathways in dynamic protein structures. PLoS Comput. Biol. 8, e1002708
45. Delano, W. L. (2011) The PyMOL Molecular Graphics System, version 1.5.0.4, Schrödinger, LLC, New York
46. Laskowski, R. A., and Swindells, M. B. (2011) LigPlotô: multiple ligandprotein interaction diagrams for drug discovery. J. Chem. Inf. Model. 51, 2778-2786
47. Kumari, R., Kumar, R., Open Source Drug Discovery Consortium, and Lynn, A. (2014) g-mmpbsa: a GROMACS tool for high-throughput MM-PBSA calculations. J. Chem. Inf. Model. 54, 1951-1962
48. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041