Computational studies of the cholesterol transport between NPC2 and the N-terminal domain of NPC1 (NPC1(NTD))

Biochemistry

Volumn 52, Issue 39, 2013, Pages 6879-6891

  Estiu, Guillermina ^a   Khatri, Nazir ^a,b   Wiest, Olaf ^a,c  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b Faculty of Social and Political Sciences   (United States)

^c PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMISTIC MODELING; CHOLESTEROL HOMEOSTASIS; CHOLESTEROL TRANSPORT; COMPUTATIONAL STUDIES; MUTAGENESIS EXPERIMENT; N-TERMINAL DOMAINS; NUDGED ELASTIC BAND; TRANSFER MECHANISMS;

BINDING ENERGY; COMPUTER SIMULATION; PROTEINS;

CHOLESTEROL;

ALANINE; CHOLESTEROL; MEMBRANE PROTEIN; PROTEIN NPC1; PROTEIN NPC2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CHOLESTEROL TRANSPORT; COMPUTER MODEL; CRYSTAL STRUCTURE; HYDROGEN BOND; MOLECULAR DYNAMICS; MUTAGENESIS; PRIORITY JOURNAL; SIMULATION;

BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CHOLESTEROL; COMPUTATIONAL BIOLOGY; GLYCOPROTEINS; HUMANS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION;

EID: 84885002064     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4005478     Document Type: Article

References (52)

1. Brown, M. S. and Goldstein, J. L. (1986) A receptor-mediated pathway for cholesterol homeostasis Science 232, 34-47
2. Brown, M. S. and Goldstein, J. L. (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor Cell 89, 331-340
3. King, G. and Sharom, F. J. (2012) Proteins that bind and move lipids: MsbA and NPC1 Crit. Rev. Biochem. Mol. Biol. 47, 75-95
4. Subramanian, K. and Balch, W. E. (2008) NPC1/NPC2 function as a tag team duo to mobilize cholesterol Proc. Natl. Acad. Sci. U.S.A. 105, 15223-15224
5. Rosenbaum, A. I. and Maxfield, F. R. (2011) Niemann-Pick type C disease:molecular mechanisms and potential therapeutic approaches J. Neurochem. 116, 789-795
6. Mesmin, B. and Maxfield, F. R. (2009) Intracellular sterol dynamics Biochim. Biophys. Acta 1791, 636-645
7. Xu, S., Gu, L., Benoff, B., and Stock, A. M. (2007) Structural basis of sterol binding by NPC2, a lysosomal protein deficient in Niemann-Pick type C2 disease J. Biol. Chem. 282, 23525-23531
8. Friedland, N. L., H., L., Lobel, P., and Stock, A. M. (2003) Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease Proc. Natl. Acad. Sci. U.S.A. 100, 2512-2517
9. Davies, J. P. and Ioannou, Y. A. (2000) Topological analysis of Niemann-Pick C1 protein reveals that the membrane orientation of the putative sterolsensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein J. Biol. Chem. 275, 24367-24374
10. Kwon, H. J., Abi-Mosleh, L., Wang, M. L., Deisenhofer, J., Goldstein, J. L., Brown, M. S., and Infante, R. E. (2009) Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol Cell 137, 1213-1224
11. Kwon, H. J., Palnitkar, M., and Deisenhofer, J. (2011) The structure of the NPC1L1 N-terminal domain in a closed conformation PLoS One 6, e18722
12. Infante, R. E., Wang, M. L., Radhakrishnan, A., Kwon, H. J., Brown, M. S., and Goldstein, J. L. (2008) NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes Proc. Natl. Acad. Sci. U.S.A. 105, 15287-15292
13. Xie, X., Brown, M. S., Shelton, J. M., Richardson, J. A., Goldstein, J. L., and Lianga, G. (2011) Amino acid substitution in NPC1 that abolishes cholesterol binding reproduces phenotype of complete NPC1 deficiency in mice Proc. Natl. Acad. Sci. U.S.A 108, 15333-15335
14. Wang, M. L., Motamed, M., Infante, R. E., Abi-Mosleh, L., Kwon, H. J., Brown, M. S., and Goldstein, J. L. (2010) Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes Cell Metab. 12, 166-173
15. Deffieu, M. S. and Pfeffer, S. R. (2011) Niemann-Pick type C 1 function requires lumenal domain residues that mediate cholesterol-dependent NPC2 binding Proc. Natl. Acad. Sci. U.S.A. 108, 18932-18936
16. Vance, J. E. and Peake, K. B. (2011) Function of the Niemann-Pick type C proteins and their bypass by cyclodextrin Curr. Opin. Lipidol. 22, 204-209
17. Kruth, H. S., Comly, M., Butler, J. D., Vanier, M. T., Fink, J. K., Wenger, D. A., Patel, S., and Pentchev, P. G. (1986) Type C Niemann-Pick disease. Abnormal metabolism of low density lipoprotein in homozygous and heterozygous fibroblasts J. Biol. Chem. 261, 9290-9298
18. Pentchev, P. G., Kruth, H. S., Comly, M., Butler, J. D., Vanier, M. T., Wenger, D. A., and Patel, S. (1986) Type C Niemann-Pick disease. A parallel loss of regulatory responses in both the uptake and esterification of low density lipoprotein-derived cholesterol in cultured fibroblasts J. Biol. Chem. 261, 16775-16780
19. Vanier, M. (2010) Niemann-Pick disease type C Orphanet J. Rare Dis. 5, 16
20. Munkacsi, A. B., Chen, F. W., Brinkman, M. A., Higaki, K., Gutiérrez, G. D., Chaudhari, J., Layer, J. V., Tong, A., Bard, M., Boone, C., Ioannou, Y. A., and Sturley, S. L. (2011) An "exacerbate-reverse" strategy in yeast identifies histone deacetylase inhibition as a correction for cholesterol and sphingolipid transport defects in human Niemann-Pick type C disease J. Biol. Chem. 286, 23842-23851
21. Helquist, P. and Wiest, O. (2009) Current status of drug therapy development for Niemann Pick type C disease Drugs Future 34, 315-331
22. Peake, K. B. and Vance, J. E. (2012) Normalization of cholesterol homeostasis by 2-hydroxypropyl-β-cyclodextrin in neurons and glia from Niemann-Pick C1 (NPC1)-deficient mice J. Biol. Chem. 287, 9290-9298
23. Pipalia, N. H., Cosner, K. C., Huang, A., Chatterjee, A., Bourbon, P., Farley, N., Helquist, P., Wiest, O., and Maxfield, F. R. (2011) Histone deacetylase inhibitor treatment dramatically reduces cholesterol accumulation in Niemann-Pick type C1 mutant human fibroblasts Proc. Natl. Acad. Sci. U.S.A. 108, 5620-5625
24. te Vruchte, D., Lloyd-Evans, E., Veldman, R. J., Neville, D. C. A., Dwek, R. A., Platt, F., van Blitterswijk, W. J., and Sillence, D. J. (2004) Accumulation of glycosphingolipids in Niemann-Pick C disease disrupts endosomal transport J. Biol. Chem. 279, 26167-26175
25. Chang, T.-Y., Reid, P. C., Sugii, S., Ohgami, N., Cruz, J. C., and Chang, C. C. (2005) Niemann-Pick type C disease and intracellular cholesterol trafficking J. Biol. Chem. 290, 20917-20920
26. Moles, A., Tarrats, N., Fernández-Checa, J. C., and Mar, M. (2011) Cathepsin B overexpression due to acid sphingomyelinase ablation promotes liver fibrosis in Niemann-Pick disease J. Biol. Chem. 287, 1178-1188
27. Carette, J. E., Raaben, M., Wong, A. C., Herbert, A. S., Obernosterer, G., Mulherkar, N., Kuehne, A. I., Kranzusch, P. J., Griffin, A. M., Ruthel, G., Dal Cin, P., Dye, J. M., Whelan, S. P., Chandran, K., and Brummelkamp, T. R. (2011) Ebola virus entry requires the cholesterol transporter Niemann-Pick C1 Nature 477, 340-343
28. Cote, M., Misasi, J., Ren, T., Bruchez, A., Lee, K., Filone, C. M., Hensley, L., Li, Q., Ory, D., Chandran, K., and Cunningham, J. (2011) Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection Nature 477, 344-348
29. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
30. Case, D. A., Darden, T. A., Cheatham, T. E., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Wang, B., Hayik, S., Roitberg, A., Seabra, G., Kolossváry, I., Wong, K. F., Paesani, F., Vanicek, J., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, X., Wang, J., Hsieh, M., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., and Kollman, P. A. (2010) AMBER11, University of California, San Francisco, CA.
31. Wang, J., Wang, W., Kollman, P. A., and Case, D. A. (2006) Automatic atom type and bond type perception in molecular mechanical calculations J. Mol. Graphics Modell. 25, 247-260
32. Wang, J., Wolf, R. M., Caldwell, J. M., Kollman, P. A., and Case, D. A. (2004) Development and testing of a general Amber force field J. Comput. Chem. 25, 1157-1174
33. Bayly, C. I., Cieplak, P., Cornell, W. D., and Kollman, P. A. (1993) A well-behaved electrostatic potential based method using charge restraints for determining atom-centered charges: the RESP model J. Phys. Chem. 97, 10269-10280
34. Fox, T. and Kollman, P. A. (1998) Application of the RESP methodology in the parametrization of organic solvents J. Phys. Chem. B 102, 8070-8079
35. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23, 327-341
36. Pastor, R. W., Brooks, B. R., and Szabo, A. (1988) An analysis of the accuracy of Langevin and molecular dynamics algorithms Mol. Phys. 65, 1409-1419
37. 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
38. Petersen, H. G. (1995) Accuracy and efficiency of the particle-mesh-ewald method J. Chem. Phys. 103, 3668-3679
39. Hou, T., Wang, J., Li, Y., and W., W. (2011) Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations J. Chem. Inf. Mod. 51, 69-82
40. Wang, J., Hou, T., and Xu, X. (2006) Recent advances in free energy calculations with a combination of molecular mechanics and continuum models Cur. Comput.-Aided Drug Des. 2006, 95-103
41. Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., and Cheatham, T. E. (2000) Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models Acc. Chem. Res. 33, 889-897
42. Zoete, V. and Michielin, O. (2007) Comparison between computational alanine scanning and per-residue binding free energy decomposition for protein-protein association using MM-GBSA: application to the TCR-p-MHC complex Proteins 67, 1026-1047
43. Li, T., Froeyen, M., and Herdewijn, P. (2008) Computational alanine scanning and free energy decomposition for E. coli type I signal peptidase with lipopeptide inhibitor complex J. Mol. Graphics Modell. 26, 813-823
44. Massova, I. and Kollman, P. A. (1999) Computational alanine scanning to probe protein-protein interactions: a novel approach to evaluate binding free energies J. Am. Chem. Soc. 121, 8133-8143
45. Zoete, V., Irving, M. B., and Michielin, O. (2010) MM-GBSA binding free energy decomposition and T cell receptor engineering J. Mol. Recognit. 23, 142-152
46. Gohlke, H., Kiel, C., and Case, D. A. (2003) Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes J. Mol. Biol. 330, 891-913
47. Mathews, D. H. and Case, D. A. (2006) Nudged elastic band calculation of minimal energy paths for the conformational change of a GG non-canonical pair J. Mol. Biol. 357, 1683-1693
48. Tsui, V. and Case, D. A. (2001) Theory and applications of the generalized Born solvation model in macromolecular simulations Biopolymers 56, 275-291
49. Tsui, V. and Case, D. A. (2000) Molecular dynamics simulations of nucleic acids with a generalized born solvation model J. Am. Chem. Soc. 122, 2489-2498
50. Shen, Y., Liu, J., Estiu, G., Isin, B., Lee, D.-S., Barabási, A.-L., Kapatral, V., Wiest, O., and Oltvai, Z. N. (2009) A blueprint for antimicrobial hit discovery targeting metabolic networks Proc. Natl. Acad. Sci. U.S.A. 106, 1082-1087
51. Van Nostrand, K. P., Kennedy, S. D., Turner, D. H., and Mathews, D. H. (2011) Molecular mechanics investigation of an adenine adenine non-canonical pair conformational change J. Chem. Theory Comput. 7, 3779-3792
52. Reblova, K., Strelcova, Z., Kulhanek, P., Besseova, I., Mathews, D. H., Van Nostrand, K. P., YiIildirim, Y., Turner, D. H., and Sponer, J. (2010) An RNA molecular switch: intrinsic flexibility of 23S rRNA helices 40 and 68 5′-UAA/5′-GAN internal loops studied by molecular dynamics methods J. Chem. Theory Comput. 6, 910-929