Structure of a prokaryotic fumarate transporter reveals the architecture of the SLC26 family

Nature Structural and Molecular Biology

Volumn 22, Issue 10, 2015, Pages 803-808

  Geertsma, Eric R ^a,b   Chang, Yung Ning ^a,b   Shaik, Farooque R ^a,e   Neldner, Yvonne ^a   Pardon, Els ^c,d   Steyaert, Jan ^c,d   Dutzler, Raimund ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b GOETHE UNIVERSITY   (Germany)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^e PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FUMARIC ACID; MEMBRANE PROTEIN; SLC26 PROTEIN; UNCLASSIFIED DRUG; ANION TRANSPORT PROTEIN; FUMARIC ACID DERIVATIVE; PRIMER DNA; SELENOMETHIONINE;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DEINOCOCCUS; DEINOCOCCUS GEOTHERMALIS; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; INVERTED REPEAT; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROKARYOTIC CELL; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; DNA SEQUENCE; ESCHERICHIA COLI; FLUORESCENCE; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; SIZE EXCLUSION CHROMATOGRAPHY;

ANION TRANSPORT PROTEINS; BASE SEQUENCE; CHROMATOGRAPHY, GEL; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; DEINOCOCCUS; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; FLUORESCENCE; FUMARATES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OPEN READING FRAMES; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; SELENOMETHIONINE; SEQUENCE ANALYSIS, DNA;

EID: 84943390515     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3091     Document Type: Article

References (49)

1. Alper, S.L. &Sharma, A.K. The SLC26 gene family of anion transporters and channels. Mol. Aspects Med. 34, 494-515 (2013).
2. Dorwart, M.R., Shcheynikov, N., Yang, D. &Muallem, S. The solute carrier 26 family of proteins in epithelial ion transport. Physiology (Bethesda) 23, 104-114 (2008).
3. Price, G.D. &Howitt, S.M. The cyanobacterial bicarbonate transporter BicA: its physiological role and the implications of structural similarities with human SLC26 transporters. Biochem. Cell Biol. 89, 178-188 (2011).
4. Ohana, E., Yang, D., Shcheynikov, N. &Muallem, S. Diverse transport modes by the solute carrier 26 family of anion transporters. J. Physiol. (Lond.) 587, 2179-2185 (2009).
5. Oliver, D. et al. Intracellular anions as the voltage sensor of prestin, the outer hair cell motor protein. Science 292, 2340-2343 (2001).
6. Dallos, P. &Fakler, B. Prestin, a new type of motor protein. Nat. Rev. Mol. Cell Biol. 3, 104-111 (2002).
7. Price, G.D., Woodger, F.J., Badger, M.R., Howitt, S.M. &Tucker, L. Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc. Natl. Acad. Sci. USA 101, 18228-18233 (2004).
8. Karinou, E., Compton, E.L., Morel, M. &Javelle, A. The Escherichia coli SLC26 homologue YchM (DauA) is a C4-dicarboxylic acid transporter. Mol. Microbiol. 87, 623-640 (2013).
9. Sharma, A.K., Rigby, A.C. &Alper, S.L. STAS domain structure and function. Cell. Physiol. Biochem. 28, 407-422 (2011).
10. Sharma, A.K. et al. Solution structure of the guanine nucleotide-binding STAS domain of SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis. J. Biol. Chem. 286, 8534-8544 (2011).
11. Babu, M. et al. Structure of a SLC26 anion transporter STAS domain in complex with acyl carrier protein: implications for E. coli YchM in fatty acid metabolism. Structure 18, 1450-1462 (2010).
12. Pasqualetto, E. et al. Structure of the cytosolic portion of the motor protein prestin and functional role of the STAS domain in SLC26/SulP anion transporters. J. Mol. Biol. 400, 448-462 (2010).
13. Geertsma, E.R. &Dutzler, R. A versatile and efficient high-throughput cloning tool for structural biology. Biochemistry 50, 3272-3278 (2011).
14. Kawate, T. &Gouaux, E. Fluorescence-detection size-exclusion chromatography for precrystallization screening of integral membrane proteins. Structure 14, 673-681 (2006).
15. Geertsma, E.R., Groeneveld, M., Slotboom, D.J. &Poolman, B. Quality control of overexpressed membrane proteins. Proc. Natl. Acad. Sci. USA 105, 5722-5727 (2008).
16. Detro-Dassen, S. et al. Conserved dimeric subunit stoichiometry of SLC26 multifunctional anion exchangers. J. Biol. Chem. 283, 4177-4188 (2008).
17. Compton, E.L. et al. Conserved structure and domain organization among bacterial Slc26 transporters. Biochem. J. 463, 297-307 (2014).
18. Shibagaki, N. &Grossman, A.R. The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. J. Biol. Chem. 281, 22964-22973 (2006).
19. Chernova, M.N. et al. Acute regulation of the SLC26A3 congenital chloride diarrhoea anion exchanger (DRA) expressed in Xenopus oocytes. J. Physiol. (Lond.) 549, 3-19 (2003).
20. Pardon, E. et al. A general protocol for the generation of Nanobodies for structural biology. Nat. Protoc. 9, 674-693 (2014).
21. Compton, E.L., Karinou, E., Naismith, J.H., Gabel, F. &Javelle, A. Low resolution structure of a bacterial SLC26 transporter reveals dimeric stoichiometry and mobile intracellular domains. J. Biol. Chem. 286, 27058-27067 (2011).
22. Forrest, L.R., Kramer, R. &Ziegler, C. The structural basis of secondary active transport mechanisms. Biochim. Biophys. Acta 1807, 167-188 (2011).
23. Lu, F. et al. Structure and mechanism of the uracil transporter UraA. Nature 472, 243-246 (2011).
24. Wong, F.H. et al. The amino acid-polyamine-organocation superfamily. J. Mol. Microbiol. Biotechnol. 22, 105-113 (2012).
25. Västermark, A. &Saier, M.H. Jr. Evolutionary relationship between 5+5 and 7+7 inverted repeat folds within the amino acid-polyamine-organocation superfamily. Proteins 82, 336-346 (2014).
26. Gorbunov, D. et al. Molecular architecture and the structural basis for anion interaction in prestin and SLC26 transporters. Nat. Commun. 5, 3622 (2014).
27. Barneaud-Rocca, D., Etchebest, C. &Guizouarn, H. Structural model of the anion exchanger 1 (SLC4A1) and identification of transmembrane segments forming the transport site. J. Biol. Chem. 288, 26372-26384 (2013).
28. Cordat, E. &Reithmeier, R.A. Structure, function, and trafficking of SLC4 and SLC26 anion transporters. Curr. Top. Membr. 73, 1-67 (2014).
29. He, J.J. &Quiocho, F.A. Dominant role of local dipoles in stabilizing uncompensated charges on a sulfate sequestered in a periplasmic active transport protein. Protein Sci. 2, 1643-1647 (1993).
30. Dutzler, R., Campbell, E.B. &MacKinnon, R. Gating the selectivity filter in ClC chloride channels. Science 300, 108-112 (2003).
31. Lobet, S. &Dutzler, R. Ion-binding properties of the ClC chloride selectivity filter. EMBO J. 25, 24-33 (2006).
32. Kalli, A.C., Sansom, M.S. &Reithmeier, R.A. Molecular dynamics simulations of the bacterial UraA H+-uracil symporter in lipid bilayers reveal a closed state and a selective interaction with cardiolipin. PLOS Comput. Biol. 11, e1004123 (2015).
33. Lee, C. et al. A two-domain elevator mechanism for sodium/proton antiport. Nature 501, 573-577 (2013).
34. Paulino, C., Wohlert, D., Kapotova, E., Yildiz, O. &Kuhlbrandt, W. Structure and transport mechanism of the sodium/proton antiporter MjNhaP1. eLife 3, e03583 (2014).
35. Landau, M. et al. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299-W302 (2005).
36. Casadaban, M.J. &Cohen, S.N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138, 179-207 (1980).
37. Ehrnstorfer, I.A., Geertsma, E.R., Pardon, E., Steyaert, J. &Dutzler, R. Crystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transport. Nat. Struct. Mol. Biol. 21, 990-996 (2014).
38. Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L. &Clardy, J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229, 105-124 (1993).
39. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800 (1993).
40. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
41. Schneider, T.R. &Sheldrick, G.M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (2002).
42. Pape, T. &Schneider, T.R. HKL2MAP: a graphical user interface for phasing with SHELX programs. J. Appl. Crystallogr. 37, 843-844 (2004).
43. de La Fortelle, E. &Bricogne, G. in Methods in Enzymology (eds. Carter, C.W. &Sweet, R.M.) 492-494 (Academic, New York, 1997).
44. Abrahams, J.P. &Leslie, A.G. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D Biol. Crystallogr. 52, 30-42 (1996).
45. Jones, T.A., Zou, J.Y., Cowan, S.W. &Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
46. Emsley, P. &Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
47. Adams, P.D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (2002).
48. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
49. Geertsma, E.R., Nik Mahmood, N.A., Schuurman-Wolters, G.K. &Poolman, B. Membrane reconstitution of ABC transporters and assays of translocator function. Nat. Protoc. 3, 256-266 (2008).