CholMine: Determinants and prediction of cholesterol and cholate binding across nonhomologous protein structures

Journal of Chemical Information and Modeling

Volumn 55, Issue 4, 2015, Pages 747-759

  Liu, Nan ^a,b,c   Van Voorst, Jeffrey R ^b,c,d   Johnston, John B ^c   Kuhn, Leslie A ^b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c Michigan State University   (United States)

^d SYMANTEC RESEARCH LABS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CHOLESTEROL; FORECASTING; SOAPS (DETERGENTS);

DIVERSE PROTEINS; FALSE POSITIVE RATES; G PROTEIN COUPLED RECEPTORS; PHYSIOLOGICAL LIGANDS; PROTEIN STRUCTURES; SELECTIVE INHIBITORS; THREE-DIMENSIONAL INTERACTION; TRUE POSITIVE RATES;

PROTEINS;

BACTERIAL PROTEIN; CHOLESTEROL; CHOLIC ACID DERIVATIVE; LIGAND; MEMBRANE PROTEIN; PROTEIN; PROTEIN BINDING;

ANIMAL; BINDING SITE; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; MACHINE LEARNING; METABOLISM; MOUSE; PROCEDURES; PROTEIN MOTIF;

AMINO ACID MOTIFS; ANIMALS; BACTERIAL PROTEINS; BINDING SITES; CHOLATES; CHOLESTEROL; COMPUTATIONAL BIOLOGY; HUMANS; LIGANDS; MACHINE LEARNING; MEMBRANE PROTEINS; MICE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEINS;

EID: 84928658342     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci5006542     Document Type: Article

References (49)

1. 2+-Atpase from Sarcoplasmic Reticulum J. Biol. Chem. 1989, 264, 4907-4915
2. Seddon, A. M.; Curnow, P.; Booth, P. J. Membrane Proteins, Lipids and Detergents: Not Just a Soap Opera Biochim. Biophys. Acta 2004, 1666, 105-117
3. Contreras, F.-X.; Ernst, A. M.; Wieland, F.; Brügger, B. Specificity of Intramembrane Protein-Lipid Interaction Cold Spring Harbor Perspect. Biol. 2011, 3, 1-18
4. Ernst, A. M.; Contreras, F.-X.; Brügger, B.; Wieland, F. Determinants of Specificity at the Protein-Lipid Interface in Membranes FEBS Lett. 2010, 584, 1713-1720
5. Hite, R. K.; Li, Z.; Walz, T. Principles of Membrane Protein Interactions with Annular Lipids Deduced from Aquaporin-0 2D Crystals EMBO J. 2010, 29, 1652-1658
6. Shinzawa-Itoh, K.; Aoyama, H.; Muramoto, K.; Terada, H.; Kurauchi, T.; Tadehara, Y.; Yamasaki, A.; Sugimura, T.; Kurono, S.; Tsujimoto, K.; Mizushima, T.; Yamashita, E.; Tsukihara, T.; Yoshikawa, S. Structures and Physiological Roles of 13 Integral Lipids of Bovine Heart Cytochrome C Oxidase EMBO J. 2007, 26, 1713-1725
7. Qin, L.; Hiser, C.; Mulichak, A.; Garavito, R. M.; Ferguson-Miller, S. Identification of Conserved Lipid Detergent-Binding Sites in a High-Resolution Structure of the Membrane Protein Cytochrome C Oxidase Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 16117-16122
8. Munro, S. Lipid Rafts: Elusive or Illusive? Cell 2003, 115, 377-388
9. Burger, K.; Gimpl, G.; Fahrenholz, F. Regulation of Receptor Function by Cholesterol Cell. Mol. Life Sci. 2000, 57, 1577-1592
10. Schroeder, C. Cholesterol-Binding Viral Proteins in Virus Entry and Morphogenesis. In Cholesterol Binding and Cholesterol Transport Proteins: Structure and Function in Health and Disease; Harris, J. R., Ed.; Springer: Dordrecht, The Netherlands, 2010; Vol. 51, pp 77-108.
11. Huber, T. B.; Schermer, B.; Müeller, R. U.; Höhne, M.; Bartram, M.; Calixto, A.; Hagmann, H.; Reinhardt, C.; Koos, F.; Kunzelmann, K.; Shirokova, E.; Krautwurst, D.; Harteneck, C.; Simons, M.; Pavenstädt, H.; Kerjaschki, D.; Thiele, C.; Walz, G.; Chalfie, M.; Benzing, T. Podocin and MEC-2 Bind Cholesterol to Regulate the Activity of Associated Ion Channels Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 17079-17086
12. Hulce, J. J.; Cognetta, A. B.; Niphakis, M. J.; Tully, S. E.; Cravatt, B. F. Proteome-Wide Mapping of Cholesterol-Interacting Proteins in Mammalian Cells Nat. Methods 2013, 10, 259-264
13. Hanson, M. A.; Cherezov, V.; Griffith, M. T.; Roth, C. B.; Jaakola, V. P.; Chien, E. Y.; Velasquez, J.; Kuhn, P.; Stevens, R. C. A Specific Cholesterol Binding Site is Established by the 2.8 Å Structure of the Human B2-Adrenergic Receptor Structure 2008, 16, 897-905
14. Adamian, L.; Naveed, H.; Liang, J. Lipid-Binding Surface of Membrane Proteins: Evidence from Evolutionary and Structure Analysis Biochim. Biophys. Acta 2011, 1808, 1092-1102
15. Li, H.; Papadopoulos, V. Peripheral-Type Benzodiazepine Receptor Function in Cholesterol Transport. Identification of a Putative Cholesterol Recognition/Interaction Amino Acid Sequence and Consensus Pattern Endocrinology 1998, 139, 4991-4997
16. Takeda, K.; Tonthat, N. K.; Glover, T.; Xu, W.; Koonin, E. V.; Yanagida, M.; Schumacher, M. A. Implications for Proteasome Nuclear Localization Revealed by the Structure of the Nuclear Proteasome Tether Protein Cut8 Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16950-16955
17. Li, F.; Liu, J.; Valls, L.; Ferguson-Miller, S. Identification of a Key Cholesterol Binding Enhancement Motif in Translocator Protein 18 Kda (TSPO) Biochemistry 2015, 54, 1441-1443
18. Baier, C. J.; Fantini, J.; Barrantes, F. J. Disclosure of Cholesterol Recognition Motifs in Transmembrane Domains of the Human Nicoticin Acetylcholine Receptor Sci. Rep. 2011, 1, 1-7
19. Fantini, J.; Yahi, N. Molecular Basis for the Glycosphingolipid-Binding Specificity of α-Synuclein: Key Role of Tyrosine 39 in Membrane Insertion J. Mol. Biol. 2011, 408, 654-669
20. Fantini, J.; Barrantes, F. J. How Cholesterol Interacts With Membrane Proteins: an Exploration of Cholesterol-Binding Sites Including CRAC, CARC, and Tilted Domains Front Physiol. 2013, 4, 1-9
21. Palmer, M. Cholesterol and the Activity of Bacterial Toxins FEMS Microbiol. Lett. 2004, 238, 281-289
22. Barrett, P. J.; Song, Y.; Van Horn, W. D.; Hustedt, E. J.; Schafer, J. M.; Hadziselimovic, A.; Beel, A. J.; Sanders, C. R. The Amyloid Precursor Protein Has a Flexible Transmembrane Domain and Binds Cholesterol Science 2012, 336, 1168-1171
23. Song, Y.; Kenworthy, A. K.; Sanders, C. R. Cholesterol as a Co-Solvent and a Ligand for Membrane Proteins Protein Sci. 2014, 23, 1-22
24. Farrand, A. J.; LaChapelle, S.; Hotze, E. M.; Johnson, A. E.; Tweten, R. K. Only Two Amino Acids are Essential for Cytolytic Toxin Recognition of Cholesterol at the Membrane Surface Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 4341-4346
25. Chiang, J. Y. Bile Acid Regulation of Gene Expression: Roles of Nuclear Hormone Receptors Endocr. Rev. 2001, 23, 443-463
26. Russell, D. W.; Setchell, K. D. R. Bile Acid Biosynthesis Biochemistry 1992, 31, 4737-4749
27. Hofmann, A. F. The Enterohepatic Circulation of Bile Acids in Man Clin. Gastroenterol. 1977, 6, 3-24
28. Maruyama, T.; Miyamoto, Y.; Nakamura, T.; Tamai, Y.; Okada, H.; Sugiyama, E.; Nakamura, T.; Itadani, H.; Tanaka, K. Identification of Membrane-Type Receptor for Bile Acids (M-BAR) Biochem. Biophys. Res. Commun. 2002, 298, 714-719
29. Kawamata, Y.; Fujii, R.; Hosoya, M.; Harada, M.; Yoshida, H.; Miwa, M.; Fukusumi, S.; Habata, Y.; Itoh, T.; Shintani, Y.; Hinuma, S.; Fujisawa, Y.; Fujino, M. A G Protein-Coupled Receptor Responsive to Bile Acids J. Biol. Chem. 2003, 278, 9435-9440
30. Lischka, F.; Kuhn, L. A.; Libants, S.; Wu, H.; Yuan, Q.; Teeter, J.; Li, W. De-Orphanization of Two Vertebrate Pheromone Receptors. In preparation, 2015.
31. Yau, W.-M.; Wimley, W. C.; Gawrisch, K.; White, S. H. The Preference of Tryptophan for Membrane Interfaces Biochemistry 1998, 37, 14713-14718
32. Ballesteros, J. A.; Weinstein, H. Integrated Methods for the Construction of Three-Dimensional Models and Computational Probing of Structure-Function Relations in G Protein-Coupled Receptors Methods Neurosci. 1995, 25, 366-428
33. Hunte, C. Specific Protein-Lipid Interactions in Membrane Proteins Biochem. Soc. Trans. 2005, 33, 938-942
34. Liu, W.; Chun, E.; Thompson, A. A.; Chubukov, P.; Xu, F.; Katritch, V.; Han, G. W.; Roth, C. B.; Heitman, L. H.; IJzerman, A. P.; Cherezov, V.; Stevens, R. C. Structural Basis for Allosteric Regulation of Gpcrs by Sodium Ions Science 2012, 337, 232-236
35. Lin, H. H.; Han, L. Y.; Zhang, H. L.; Zheng, C. J.; Xie, B.; Chen, Y. Z. Prediction of the Functional Class of Lipid Binding Proteins from Sequence-Derived Properties Irrespective of Sequence Similarity J. Lipid Res. 2006, 47, 824-831
36. Xiong, W.; Guo, Y.; Li, M. Prediction of Lipid-Binding Sites Based on Support Vector Machine and Position Specific Scoring Matrix Protein J. 2010, 29, 427-431
37. Scott, D. L.; Diez, G.; Goldmann, W. H. Prediction-Lipid Interactions: Correlation of a Predictive Algorithm for Lipid-Binding Sites with Three-Dimensional Structural Data Theor. Biol. Med. Model. 2006, 3, 1-14
38. Van Voorst, J. R.; Finzel, B. C.; Tonero, M. E.; Rai, B.; Narasimhan, L.; Howe, W. J.; Kuhn, L. A. Screening to Identify Similar Ligand-Binding Pockets in Diverse Proteins. In preparation, 2015.
39. Weill, N.; Rognan, D. Development and Validation of a Novel Protein-Ligand Fingerprint to Mine Chemogenomic Space: Application to G Protein-Coupled Receptors and Their Ligands J. Chem. Inf. Model. 2009, 49, 1049-1062
40. Madala, P. K.; Fairlie, D. P.; Boden, M. Matching Cavities in G Protein-Coupled Receptors to Infer Liand-Binding Sites J. Chem. Inf. Model. 2012, 52, 1401-1410
41. Van Voorst, J. R. Surface Matching and Chemical Scoring to Detect Unrelated Proteins Binding Similar Small Molecules. Ph.D. Thesis, Michigan State University, East Lansing, MI, 2011.
42. Zavodszky, M. I.; Sanschagrin, P. C.; Korde, R. S.; Kuhn, L. A. Distilling the Essential Features of a Protein Surface for Improving Protein-Ligand Docking, Scoring, and Virtual Screening J. Comput.-Aided Mol. Des. 2002, 16, 883-902
43. Wang, G.; Dunbrack, R. L., Jr. PISCES: A Protein Sequence Culling Server Bioinformatics 2003, 19, 1589-1591
44. Tan, P. N.; Steinbach, M.; Kumar, V. Introduction to Data Mining; Addison-Wesley: Boston, MA, 2006; pp 370-386.
45. Craig, L.; Sanschagrin, P. C.; Rozek, A.; Lackie, S.; Kuhn, L. A.; Scott, J. K. The Role of Structure in Antibody Cross-Reactivity between Peptides and Folded Proteins J. Mol. Biol. 1998, 281, 183-201
46. Wallace, A. C.; Laskowski, R. A.; Thornton, J. M. LIGPLOT: a Program to Generate Schematic Diagrams of Protein-Ligand Interactions Protein Eng. 1996, 8, 127-134
47. Laskowski, R. A.; Swindells, M. B. LigPlot+: Multiple Ligand-Protein Interaction Diagrams for Drug Discovery J. Chem. Inf. Model. 2011, 51, 2778-2786
48. Barenholz, Y. Cholesterol and Other Membrane Active Sterols: From Membrane Evolution to Rafts Prog. Lipid Res. 2002, 41, 1-5
49. Majewska, M. D. Steroids and Ion Channels in Evolution: From Bacteria to Synapses and Mind Acta Neurobiol. Exp. 2007, 67, 219-233