Thermodynamic and solution state NMR characterization of the binding of secondary and conjugated bile acids to STARD5

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1831, Issue 11, 2013, Pages 1589-1599

  Létourneau, Danny ^a   Lorin, Aurélien ^a   Lefebvre, Andrée ^a   Cabana, Jérôme ^a   Lavigne, Pierre ^a   Lehoux, Jean Guy ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Bile acid; Cholesterol metabolism; Circular dichroism; Isothermal titration calorimetry; NMR spectroscopy; Steroidogenic acute regulatory protein (StAR)

Indexed keywords

BILE ACID CONJUGATE; CHENODEOXYCHOLIC ACID; CHOLIC ACID; DEOXYCHOLIC ACID; GLYCOCHOLIC ACID; GLYCODEOXYCHOLIC ACID; HYDROXYL GROUP; LITHOCHOLIC ACID; STARD5 PROTEIN; STEROID; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TAUROCHOLIC ACID; TAURODEOXYCHOLIC ACID; UNCLASSIFIED DRUG; URSODEOXYCHOLIC ACID;

ARTICLE; BINDING AFFINITY; CHEMICAL PHENOMENA; CHEMICAL SHIFT DISPLACEMENT; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EPIMERIZATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; THERMODYNAMICS; TITRIMETRY;

BILE ACID; CA; CD; CDCA; CHEMICAL SHIFT DISPLACEMENT; CHENODEOXYCHOLIC ACID; CHOLESTEROL METABOLISM; CHOLIC ACID; CIRCULAR DICHROISM; CSD; DCA; DEOXYCHOLIC ACID; GCA; GDCA; GLYCOCHOLIC ACID; GLYCODEOXYCHOLIC ACID; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HSQC; ISOTHERMAL TITRATION CALORIMETRY; ITC; LCA; LITHOCHOLIC ACID; NMR; NMR SPECTROSCOPY; NUCLEAR MAGNETIC RESONANCE; STEROIDOGENIC ACUTE REGULATORY PROTEIN (STAR); TAUROCHOLIC ACID; TAURODEOXYCHOLIC ACID; TCA; TDCA; UDCA; URSODEOXYCHOLIC ACID;

BILE ACIDS AND SALTS; CARRIER PROTEINS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; THERMODYNAMICS;

EID: 84883717177     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.07.005     Document Type: Article

References (69)

1. M.J. Monte, J.J. Marin, A. Antelo, and J. Vazquez-Tato Bile acids: chemistry, physiology, and pathophysiology World J. Gastroenterol. 15 2009 804 816
2. S.M. Houten, and J. Auwerx The enterohepatic nuclear receptors are major regulators of the enterohepatic circulation of bile salts Ann. Med. 36 2004 482 491 (Pubitemid 39490958)
3. O. Bortolini, A. Medici, and S. Poli Biotransformations on steroid nucleus of bile acids Steroids 62 1997 564 577 (Pubitemid 27381668)
4. K.D. Setchell, A.M. Lawson, N. Tanida, and J. Sjovall General methods for the analysis of metabolic profiles of bile acids and related compounds in feces J. Lipid Res. 24 1983 1085 1100 (Pubitemid 13002347)
5. C. Fang, F.V. Filipp, and J.W. Smith Unusual binding of ursodeoxycholic acid to ileal bile acid binding protein: role in activation of FXRalpha J. Lipid Res. 53 2012 664 673
6. P. Lefebvre, B. Cariou, F. Lien, F. Kuipers, and B. Staels Role of bile acids and bile acid receptors in metabolic regulation Physiol. Rev. 89 2009 147 191
7. J.Y. Chiang Bile acid regulation of gene expression: roles of nuclear hormone receptors Endocr. Rev. 23 2002 443 463 (Pubitemid 34925641)
8. J.J. Eloranta, P.J. Meier, and G.A. Kullak-Ublick Coordinate transcriptional regulation of transport and metabolism Methods Enzymol. 400 2005 511 530 (Pubitemid 43052437)
9. A. Geier, M. Wagner, C.G. Dietrich, and M. Trauner Principles of hepatic organic anion transporter regulation during cholestasis, inflammation and liver regeneration Biochim. Biophys. Acta (BBA) - Mol. Cell Res. 1773 2007 283 308 (Pubitemid 46275063)
10. B. Hagenbuch, and P.J. Meier Molecular cloning, chromosomal localization, and functional characterization of a human liver Na +/bile acid cotransporter J. Clin. Invest. 93 1994 1326 1331 (Pubitemid 24087193)
11. G.A. Kullak-Ublick, M.G. Ismair, B. Stieger, L. Landmann, R. Huber, F. Pizzagalli, K. Fattinger, P.J. Meier, and B. Hagenbuch Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver Gastroenterology 120 2001 525 533 (Pubitemid 32147650)
12. T. Gerloff, B. Stieger, B. Hagenbuch, J. Madon, L. Landmann, J. Roth, A.F. Hofmann, and P.J. Meier The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver J. Biol. Chem. 273 1998 10046 10050 (Pubitemid 28183107)
13. H. Akita, H. Suzuki, K. Ito, S. Kinoshita, N. Sato, H. Takikawa, and Y. Sugiyama Characterization of bile acid transport mediated by multidrug resistance associated protein 2 and bile salt export pump Biochim. Biophys. Acta 1511 2001 7 16 (Pubitemid 32206667)
14. A.L. Craddock, M.W. Love, R.W. Daniel, L.C. Kirby, H.C. Walters, M.H. Wong, and P.A. Dawson Expression and transport properties of the human ileal and renal sodium-dependent bile acid transporter Am. J. Physiol. 274 1998 G157 G169
15. P.A. Dawson, M. Hubbert, J. Haywood, A.L. Craddock, N. Zerangue, W.V. Christian, and N. Ballatori The heteromeric organic solute transporter alpha-beta, Ostalpha-Ostbeta, is an ileal basolateral bile acid transporter J. Biol. Chem. 280 2005 6960 6968 (Pubitemid 40341252)
16. N. Ballatori, W.V. Christian, J.Y. Lee, P.A. Dawson, C.J. Soroka, J.L. Boyer, M.S. Madejczyk, and N. Li OSTalpha-OSTbeta: a major basolateral bile acid and steroid transporter in human intestinal, renal, and biliary epithelia Hepatology 42 2005 1270 1279 (Pubitemid 43260029)
17. J.F. Landrier, J. Grober, I. Zaghini, and P. Besnard Regulation of the ileal bile acid-binding protein gene: an approach to determine its physiological function(s) Mol. Cell. Biochem. 239 2002 149 155 (Pubitemid 35385805)
18. J. Grober, I. Zaghini, H. Fujii, S.A. Jones, S.A. Kliewer, T.M. Willson, T. Ono, and P. Besnard Identification of a bile acid-responsive element in the human ileal bile acid-binding protein gene. Involvement of the farnesoid X receptor/9-cis-retinoic acid receptor heterodimer J. Biol. Chem. 274 1999 29749 29754
19. L. Ragona, M. Catalano, M. Luppi, D. Cicero, T. Eliseo, J. Foote, F. Fogolari, L. Zetta, and H. Molinari NMR dynamic studies suggest that allosteric activation regulates ligand binding in chicken liver bile acid-binding protein J. Biol. Chem. 281 2006 9697 9709 (Pubitemid 43864688)
20. H.L. Monaco Review: the liver bile acid-binding proteins Biopolymers 91 2009 1196 1202
21. B. Stieger, and A. Geier Genetic variations of bile salt transporters as predisposing factors for drug-induced cholestasis, intrahepatic cholestasis of pregnancy and therapeutic response of viral hepatitis Expert Opin. Drug Metab. Toxicol. 7 2011 411 425
22. L.B. Agellon, and E.C. Torchia Intracellular transport of bile acids Biochim. Biophys. Acta 1486 2000 198 209 (Pubitemid 30336801)
23. F. Alpy, and C. Tomasetto Give lipids a START: the StAR-related lipid transfer (START) domain in mammals J. Cell Sci. 118 2005 2791 2801 (Pubitemid 41136357)
24. C.P. Ponting, and L. Aravind START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins Trends Biochem. Sci. 24 1999 130 132 (Pubitemid 29222709)
25. D. Rodriguez-Agudo, S. Ren, P.B. Hylemon, K. Redford, R. Natarajan, A. Del Castillo, G. Gil, and W.M. Pandak Human StarD5, a cytosolic StAR-related lipid binding protein J. Lipid Res. 46 2005 1615 1623 (Pubitemid 41099328)
26. J.F. Strauss III, T. Kishida, L.K. Christenson, T. Fujimoto, and H. Hiroi START domain proteins and the intracellular trafficking of cholesterol in steroidogenic cells Mol. Cell. Endocrinol. 202 2003 59 65 (Pubitemid 36603365)
27. Y.C. Chen, R.K. Meier, S. Zheng, S.J. Khundmiri, M.T. Tseng, E.D. Lederer, P.N. Epstein, and B.J. Clark Steroidogenic acute regulatory-related lipid transfer domain protein 5 localization and regulation in renal tubules Am. J. Physiol. Renal Physiol. 297 2009 F380 F388
28. D. Rodriguez-Agudo, S. Ren, P.B. Hylemon, R. Montanez, K. Redford, R. Natarajan, M.A. Medina, G. Gil, and W.M. Pandak Localization of StarD5 cholesterol binding protein J. Lipid Res. 47 2006 1168 1175 (Pubitemid 43830708)
29. R.E. Soccio, R.M. Adams, M.J. Romanowski, E. Sehayek, S.K. Burley, and J.L. Breslow The cholesterol-regulated StarD4 gene encodes a StAR-related lipid transfer protein with two closely related homologues, StarD5 and StarD6 Proc. Natl. Acad. Sci. U. S. A. 99 2002 6943 6948 (Pubitemid 34526237)
30. J.H. Miyake, S.L. Wang, and R.A. Davis Bile acid induction of cytokine expression by macrophages correlates with repression of hepatic cholesterol 7alpha-hydroxylase J. Biol. Chem. 275 2000 21805 21808 (Pubitemid 30621747)
31. R.A. Davis Resolving the mechanism of bile acid negative-feedback regulation, a Journal of Lipid Research tradition J. Lipid Res. 49 2008 2 3
32. A. Mencarelli, B. Renga, E. Distrutti, and S. Fiorucci Antiatherosclerotic effect of farnesoid X receptor Am. J. Physiol. Heart Circ. Physiol. 296 2009 H272 H281
33. T.W. Pols, M. Nomura, T. Harach, G. Lo Sasso, M.H. Oosterveer, C. Thomas, G. Rizzo, A. Gioiello, L. Adorini, R. Pellicciari, J. Auwerx, and K. Schoonjans TGR5 activation inhibits atherosclerosis by reducing macrophage inflammation and lipid loading Cell Metab. 14 2011 747 757
34. H. Lee, Y. Zhang, F.Y. Lee, S.F. Nelson, F.J. Gonzalez, and P.A. Edwards FXR regulates organic solute transporters alpha and beta in the adrenal gland, kidney, and intestine J. Lipid Res. 47 2006 201 214 (Pubitemid 43107463)
35. L.M. Iyer, E.V. Koonin, and L. Aravind Adaptations of the helix-grip fold for ligand binding and catalysis in the START domain superfamily Proteins 43 2001 134 144
36. N. Kudo, K. Kumagai, R. Matsubara, S. Kobayashi, K. Hanada, S. Wakatsuki, and R. Kato Crystal structures of the CERT START domain with inhibitors provide insights into the mechanism of ceramide transfer J. Mol. Biol. 396 2010 245 251
37. N. Kudo, K. Kumagai, N. Tomishige, T. Yamaji, S. Wakatsuki, M. Nishijima, K. Hanada, and R. Kato Structural basis for specific lipid recognition by CERT responsible for nonvesicular trafficking of ceramide Proc. Natl. Acad. Sci. U. S. A. 105 2008 488 493 (Pubitemid 351171735)
38. P. Lavigne, R. Najmanivich, and J.G. Lehoux Mammalian StAR-related lipid transfer (START) domains with specificity for cholesterol: structural conservation and mechanism of reversible binding Subcell. Biochem. 51 2010 425 437
39. A.P. Mathieu, P. Lavigne, and J.G. LeHoux Molecular modeling and structure-based thermodynamic analysis of the StAR protein Endocr. Res. 28 2002 419 423 (Pubitemid 36042495)
40. S.L. Roderick, W.W. Chan, D.S. Agate, L.R. Olsen, M.W. Vetting, K.R. Rajashankar, and D.E. Cohen Structure of human phosphatidylcholine transfer protein in complex with its ligand Nat. Struct. Biol. 9 2002 507 511 (Pubitemid 34693804)
41. M.J. Romanowski, R.E. Soccio, J.L. Breslow, and S.K. Burley Crystal structure of the Mus musculus cholesterol-regulated START protein 4 (StarD4) containing a StAR-related lipid transfer domain Proc. Natl. Acad. Sci. U. S. A. 99 2002 6949 6954 (Pubitemid 34526238)
42. A.G. Thorsell, W.H. Lee, C. Persson, M.I. Siponen, M. Nilsson, R.D. Busam, T. Kotenyova, H. Schuler, and L. Lehtio Comparative structural analysis of lipid binding START domains PLoS One 6 2011 e19521
43. Y. Tsujishita, and J.H. Hurley Structure and lipid transport mechanism of a StAR-related domain Nat. Struct. Biol. 7 2000 408 414 (Pubitemid 30250006)
44. D. Rodriguez-Agudo, M. Calderon-Dominguez, M.A. Medina, S. Ren, G. Gil, and W.M. Pandak ER stress increases StarD5 expression by stabilizing its mRNA and leads to relocalization of its protein from the nucleus to the membranes J. Lipid Res. 53 2012 2708 2715
45. B.J. Clark The mammalian START domain protein family in lipid transport in health and disease J. Endocrinol. 212 2012 257 275
46. D. Letourneau, A. Lorin, A. Lefebvre, V. Frappier, F. Gaudreault, R. Najmanovich, P. Lavigne, and J.G. Lehoux StAR-related lipid transfer domain protein 5 binds primary bile acids J. Lipid Res. 53 2012 2677 2689
47. A. Roostaee, E. Barbar, J.G. Lehoux, and P. Lavigne Cholesterol binding is a prerequisite for the activity of the steroidogenic acute regulatory protein (StAR) Biochem. J. 412 2008 553 562 (Pubitemid 351846421)
48. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
49. W.F. Vranken, W. Boucher, T.J. Stevens, R.H. Fogh, A. Pajon, M. Llinas, E.L. Ulrich, J.L. Markley, J. Ionides, and E.D. Laue The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins 59 2005 687 696 (Pubitemid 40695845)
50. 15N chemical shift referencing in biomolecular NMR J. Biomol. NMR 6 1995 135 140
51. K.H. Gardner, M.K. Rosen, and L.E. Kay Global folds of highly deuterated, methyl-protonated proteins by multidimensional NMR Biochemistry 36 1997 1389 1401 (Pubitemid 27074963)
52. A. Lorin, D. Letourneau, A. Lefebvre, J.G. Lehoux, and P. Lavigne (1)H, (13)C, and (15)N backbone chemical shift assignments of StAR-related lipid transfer domain protein 5 (STARD5) Biomol. NMR 7 1 Apr 2013 21 24
53. H.J.C. Berendsen, D. van der Spoel, and R. van Drunen GROMACS: a message-passing parallel molecular dynamics implementation Comput. Phys. Commun. 91 1995 43 56
54. D. Van Der Spoel, E. Lindahl, B. Hess, G. Groenhof, A.E. Mark, and H.J. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718 (Pubitemid 43076182)
55. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
56. D. Van Der Spoel, and B. Hess GROMACS - the road ahead WIREs Comput. Mol. Sci. 1 2011 710 715
57. C.D. Berweger, W.F. van Gunsteren, and F. Müller-Plathe Force field parametrization by weak coupling. Re-engineering SPC water Chem. Phys. Lett. 232 1995 429 436
58. C. Oostenbrink, A. Villa, A.E. Mark, and W.F. van Gunsteren A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6 J. Comput. Chem. 25 2004 1656 1676
59. C. Oostenbrink, T.A. Soares, N.F. van der Vegt, and W.F. van Gunsteren Validation of the 53A6 GROMOS force field Eur. Biophys. J. 34 2005 273 284 (Pubitemid 40884072)
60. A.K. Malde, L. Zuo, M. Breeze, M. Stroet, D. Poger, P.C. Nair, C. Oostenbrink, and A.E. Mark An automated force field topology builder (ATB) and repository: version 1.0 J. Chem. Theory Comput. 7 2011 4026 4037
61. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity rescaling J. Chem. Phys. 126 2007 014101 014107
62. D.S. Wishart, and B.D. Sykes Chemical shifts as a tool for structure determination Methods Enzymol. 239 1994 363 392
63. C.J. Layton, and H.W. Hellinga Thermodynamic analysis of ligand-induced changes in protein thermal unfolding applied to high-throughput determination of ligand affinities with extrinsic fluorescent dyes Biochemistry 49 2010 10831 10841
64. A.F. Hofmann The continuing importance of bile acids in liver and intestinal disease Arch. Intern. Med. 159 1999 2647 2658
65. H. Sato, A. Macchiarulo, C. Thomas, A. Gioiello, M. Une, A.F. Hofmann, R. Saladin, K. Schoonjans, R. Pellicciari, and J. Auwerx Novel potent and selective bile acid derivatives as TGR5 agonists: biological screening, structure-activity relationships, and molecular modeling studies J. Med. Chem. 51 2008 1831 1841 (Pubitemid 351438866)
66. G.P. Tochtrop, J.L. Bruns, C. Tang, D.F. Covey, and D.P. Cistola Steroid ring hydroxylation patterns govern cooperativity in human bile acid binding protein Biochemistry 42 2003 11561 11567 (Pubitemid 37243615)
67. O. Toke, J.D. Monsey, G.T. DeKoster, G.P. Tochtrop, C. Tang, and D.P. Cistola Determinants of cooperativity and site selectivity in human ileal bile acid binding protein Biochemistry 45 2006 727 737 (Pubitemid 43122237)
68. G.P. Tochtrop, G.T. DeKoster, D.F. Covey, and D.P. Cistola A single hydroxyl group governs ligand site selectivity in human ileal bile acid binding protein J. Am. Chem. Soc. 126 2004 11024 11029 (Pubitemid 39180587)
69. V. Kolhatkar, and J.E. Polli Structural requirements of bile acid transporters: C-3 and C-7 modifications of steroidal hydroxyl groups Eur. J. Pharm. Sci. 46 2012 86 99