Conformational flexibility of helix VI is essential for substrate permeation of the human apical sodium-dependent bile acid transporter

Molecular Pharmacology

Volumn 73, Issue 2, 2008, Pages 305-313

  Hussainzada, Naissan ^a   Khandewal, Akash ^a   Swaan, Peter W ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BILE ACID; BILE ACID TRANSPORTER; CARRIER PROTEINS AND BINDING PROTEINS; MEMBRANE PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; BILE ACID METABOLISM; CONFORMATION; CONTROLLED STUDY; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN SYNTHESIS;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; MOLECULAR SEQUENCE DATA; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY; SYMPORTERS;

EID: 38549107239     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.107.041640     Document Type: Article

References (40)

1. Balakrishnan A and Polli JE (2006) Apical sodium dependent bile acid transporter (ASBT, SLC10A2): a potential prodrug target. Mol Pharm 3:223-230.
2. + and bile acids. Biochem J, in press.
3. Banerjee A, Ray A, Chang C, and Swaan PW (2005) Site-directed mutagenesis and use of bile acid-MTS conjugates to probe the role of cysteines in the human apical sodium-dependent bile acid transporter (SLC10A2). Biochemistry 44:8908-8917.
4. Banerjee A and Swaan PW (2006) Membrane topology of human ASBT (SLC10A2) determined by dual label epitope insertion scanning mutagenesis. New evidence for seven transmembrane domains. Biochemistry 45:943-953.
5. Bright JN, Shrivastava IH, Cordes FS, and Sansom MS (2002) Conformational dynamics of helix S6 from Shaker potassium channel: simulation studies. Biopolymers 64:303-313.
6. Chiang JY, Kimmel R, and Stroup D (2001) Regulation of cholesterol 7alpha-hydroxylase gene (CYP7A1) transcription by the liver orphan receptor (LXRalpha). Gene 262:257-265.
7. Cordes FS, Bright JN, and Sansom MS (2002) Proline-induced distortions of transmembrane helices. J Mol Biol 323:951-960.
8. Deber CM, Glibowicka M, and Woolley GA (1990) Conformations of proline residues in membrane environments. Biopolymers 29:149-157.
9. Geyer J, Wilke T, and Petzinger E (2006) The solute carrier family SLC10: more than a family of bile acid transporters regarding function and phylogenetic relationships. Naunyn Schmiedebergs Arch Pharmacol 372:413-431.
10. Gibbs N, Sessions RB, Williams PB, and Dempsey CE (1997) Helix bending in alamethicin: molecular dynamics simulations and amide hydrogen exchange in methanol. Biophys J 72:2490-2495.
11. Hallén S, Bjorquist A, Ostlund-Lindqvist AM, and Sachs G (2002) Identification of a region of the ileal-type sodium/bile acid cotransporter interacting with a competitive bile acid transport inhibitor. Biochemistry 41:14916-14924.
12. Hallén S, Fryklund J, and Sachs G (2000) Inhibition of the human sodium/bile acid cotransporters by side specific methanethiosulfonate sulphydryl reagents: substrate controlled accessibility of site of activation. Biochemistry 39:6743-6750.
13. Huff MW, Telford DE, Edwards JY, Burnett JR, Barrett PH, Rapp SR, Napawan N, and Keller BT (2002) Inhibition of the apical sodium-dependent bile acid transporter reduces LDL cholesterol and apoB by enhanced plasma clearance of LDL apoB. Arterioscler Thromb Vasc Biol 22:1884-1891.
14. Hussainzada N, Banerjee A, and Swaan PW (2006) Transmembrane domain VII of the human apical sodium-dependent bile acid transporter ASBT (SLC10A2) lines the substrate translocation pathway. Mol Pharmacol 70:1565-1574.
15. Izzat NN, Deshazer ME, and Loose-Mitchell DS (2000) New molecular targets for cholesterol-lowering therapy. J Pharmacol Exp Ther 293:315-320.
16. Javadpour MM, Eilers M, Groesbeek M, and Smith SO (1999) Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys J 77:1609-1618.
17. +/dicarboxylate cotransporter 1, NaDC1. Biochemistry 45:4231-4239.
18. +/solute symport in prokaryotes. Biochim Biophys Acta 1505:131-143.
19. Kaback HR and Wu J (1997) From membrane to molecule to the third amino acid from the left with a membrane transport protein. Q Rev Biophys 30:333-364.
20. +/bile acid cotransporting protein from rabbit ileum. J Biol Chem 276:36020-36027.
21. Labro AJ, Raes AL, Bellens I, Ottschytsch N, and Snyders DJ (2003) Gating of shaker-type channels requires the flexibility of S6 caused by prolines. J Biol Chem 278:50724-50731.
22. Li H, Xu G, Shang Q, Pan L, Shefer S, Batta AK, Bollineni J, Tint GS, Keller BT, and Salen G (2004) Inhibition of ileal bile acid transport lowers plasma cholesterol levels by inactivating hepatic farnesoid X receptor and stimulating cholesterol 7 alpha-hydroxylase. Metabolism 53:927-932.
23. Lin Z, Itokawa M, and Uhl GR (2000) Dopamine transporter proline mutations influence dopamine uptake, cocaine analog recognition, and expression. FASEB J 14:715-728.
24. Lu H, Marti T, and Booth PJ (2001) Proline residues in transmembrane alpha helices affect the folding of bacteriorhodopsin. J Mol Biol 308:437-446.
25. Mitchell SM, Lee E, Garcia ML, and Stephan MM (2004) Structure and function of extracellular loop 4 of the serotonin transporter as revealed by cysteine-scanning mutagenesis. J Biol Chem 279:24089-24099.
26. Oelkers P, Kirby LC, Heubi JE, and Dawson PA (1997) Primary bile acid malabsorption caused by mutations in the ileal sodium-dependent bile acid transporter gene (SLC10A2). J Clin Invest 99:1880-1887.
27. +/dicarboxylate co-transporter. J Biol Chem 280:18728-18735.
28. Pauli-Magnus C, Stieger B, Meier Y, Kullak-Ublick GA, and Meier PJ (2005) Enterohepatic transport of bile salts and genetics of cholestasis. J Hepatol 43:342-357.
29. +-coupled proline uptake. Biochemistry 36:4631-4636.
30. Sansom MS and Weinstein H (2000) Hinges, swivels and switches: the role of prolines in signalling via transmembrane alpha-helices. Trends Pharmacol Sci 21:445-451.
31. Shelden MC, Loughlin P, Tierney ML, and Howitt SM (2001) Proline residues in two tightly coupled helices of the sulphate transporter, SHST1, are important for sulphate transport. Biochem J 356:589-594.
32. + exchanger isoform 1. Biochem J 379:31-38.
33. Swaan PW, Hillgren KM, Szoka FC Jr, and Oie S (1997) Enhanced transepithelial transport of peptides by conjugation to cholic acid. Bioconjug Chem 8:520-525.
34. Tieleman DP, Sansom MS, and Berendsen HJ (1999) Alamethicin helices in a bilayer and in solution: molecular dynamics simulations. Biophys J 76:40-49.
35. Trauner M and Boyer JL (2003) Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev 83:633-671.
36. Weinman SA, Carruth MW, and Dawson PA (1998) Bile acid uptake via the human apical sodium-bile acid cotransporter is electrogenic. J Biol Chem 273:34691-34695.
37. Wong MH, Oelkers P, and Dawson PA (1995) Identification of a mutation in the ileal sodium-dependent bile acid transporter gene that abolishes transport activity. J Biol Chem 270:27228-27234.
38. Woolfson DN and Williams DH (1990) The influence of proline residues on alpha-helical structure. FEBS Lett 277:185-188.
39. Zhang EY, Phelps MA, Banerjee A, Khantwal CM, Chang C, Helsper F, and Swaan PW (2004) Topology scanning and putative three-dimensional structure of the extracellular binding domains of the apical sodium-dependent bile acid transporter (SLC10A2). Biochemistry 43:11380-11392.
40. Zhang YW and Rudnick G (2005) Cysteine-scanning mutagenesis of serotonin transporter intracellular loop 2 suggests an α-helical conformation. J Biol Chem 280:30807-30813.