Polar residues in a conserved motif spanning helices 1 and 2 are functionally important in the SulP transporter family

International Journal of Biochemistry and Cell Biology

Volumn 40, Issue 11, 2008, Pages 2596-2605

  Leves, Fiona P ^a   Tierney, M Louise ^b   Howitt, Susan M ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b Biology and Environment   (Australia)

Author keywords

Helix packing; Polar amino acids; Site directed mutagenesis; SLC26 family; Sulfate transporter; SulP family

Indexed keywords

ANION TRANSPORT PROTEIN; HYDROXYL GROUP; MUTANT PROTEIN; SULFATE; SULFATE TRANSPORTER SHST1; SULP PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; CELL MEMBRANE; CONTROLLED STUDY; MOLECULAR INTERACTION; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; AMINO ACIDS; ANION TRANSPORT PROTEINS; COMPUTATIONAL BIOLOGY; MOLECULAR SEQUENCE DATA; MUTATION; PLANT PROTEINS; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE; SULFATES;

EID: 48349141803     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2008.05.007     Document Type: Article

References (35)

1. Adamian L., and Liang J. Interhelical hydrogen bonds and spatial motifs in membrane proteins: Polar clamps and serine zippers. Proteins 47 (2002) 209-218
2. Adamian L., and Liang J. Prediction of buried helices in multispan alpha helical membrane proteins. Proteins Structure Function & Bioinformatics 63 (2006) 1-5
3. Adamian L., and Liang J. Prediction of transmembrane helix orientation in polytopic membrane proteins. BMC Structural Biology 6 (2006) 13
4. + channel inactivation. Cell Biochemistry and Biophysics 41 (2004) 25-39
5. Blaber M., Lindstrom J.D., Gassner N., Xu J., Dirk W.H., and Matthews B.W. Energetic cost and structural consequences of burying a hydroxyl group within the core of a protein determined from Ala-]Ser and Val-]Thr substitutions in T4 lysozyme. Biochemistry 32 (1993) 11363-11373
6. Crooks G.E., Hon G., Chandonia J.-M., and Brenner S.E. WebLogo: a sequence logo generator. Genome Research 14 (2004) 1188-1190
7. Curran A.R., and Engelman D.M. Sequence motifs, polar interactions and conformational changes in helical membrane proteins. Current Opinion in Structural Biology 13 (2003) 412-417
8. Dawson J.P., Weinger J.S., and Engelman D.M. Motifs of serine and threonine can drive association of transmembrane helices. Journal of Molecular Biology 316 (2002) 799-805
9. De la Vieja A., Reed M.D., Ginter C.S., and Carrasco N. Amino acid residues in transmembrane segment IX of the Na+/I symporter play a role in its Na+ dependence and are critical for transport activity. Journal of Biological Chemistry 282 (2007) 25290-25298
10. Domene C., Vemparala S., Klein M.L., Venien-Bryan C., and Doyle D.A. Role of aromatic localization in the gating process of a potassium channel. Biophysical Journal 90 (2006) L1-L3
11. Eilers M., Patel A.B., Liu W., and Smith S.O. Comparison of helix interactions in membrane and soluble alpha-bundle proteins. Biophysical Journal 82 (2002) 2720-2736
12. Ellgaard L., Molinari M., and Helenius A. Setting the standards: quality control in the secretory pathway. Science 286 (1999) 1882-1888
13. Gietz R.D., Schiestl R.H., Willems A.R., and Woods R.A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11 (1995) 355-360
14. Hawkesford M.J. Transporter gene families in plants: the sulfate transporter gene family-redundancy or specialization? [Review]. Physiologia Plantarum 117 (2003) 155-163
15. Hong H., Park S., FloresJimenez R.H., Rinehart D., and Tamm L.K. Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins. Journal of the American Chemistry Society 129 (2007) 8320-8327
16. Katzmann D.J., Epping E.A., and Moye-Rowley W.S. Mutational disruption of plasma membrane trafficking of Saccharomyces cerevisiae Yor1p, a homologue of mammalian multidrug resistance protein. Molecular & Cellular Biology 19 (1999) 2998-3009
17. Kere J. Overview of the SLC26 family and associated diseases. Novartis Foundation Symposium, 273 (2006) 2-11
18. Khurana O.K., Coupland L.A., Shelden M.C., and Howitt S.M. Homologous mutations in two diverse sulfate transporters have similar effects. FEBS Letters 477 (2000) 118-122
19. Killian J.A., and von Heijne G. How proteins adapt to a membrane-water interface. Trends in Biochemical Sciences 25 (2000) 429-434
20. Ko S.B.H., Zeng W., Dorwart M.R., Luo X., Kim K.H., Millen L., et al. Gating of CFTR by the STAS domain of SLC26 transporters. Nature Cell Biology 6 (2004) 343-350
21. Loughlin P., Shelden M.C., Tierney M.L., and Howitt S.M. Structure and function of a model member of the SulP transporter family. Cell Biochemistry and Biophysics 36 (2002) 183-190
22. Pflugrath J.W., and Quiocho F.A. The 2 A resolution structure of the sulfate-binding protein involved in active transport in Salmonella typhimurium. Journal of Molecular Biology 200 (1988) 163-180
23. Price G., Woodger F., Badger M., Howitt S., and Tucker L. Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America, vol. 101 (2004) 18228-18233
24. Rajagopalan L., Patel N., Madabushi S., Goddard J.A., Anjan V., Lin F., et al. Essential helix interactions in the anion transporter domain of prestin revealed by evolutionary trace analysis. Journal of Neuroscience 26 (2006) 12727-12734
25. Saier M.H., Eng B.H., Fard S., Garg J., Haggerty D.A., Hutchinson W.J., et al. Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochimica et Biophysica Acta-Reviews on Biomembranes 1422 (1999) 1-56
26. Shelden M.C., Loughlin P., Tierney M.L., and Howitt S.M. Proline residues in two tightly coupled helices of the sulfate transporter, SHST1, are important for sulfate transport. Biochemical Journal 356 (2001) 589-594
27. Shelden M.C., Loughlin P., Tierney M.L., and Howitt S.M. Interactions between charged amino acid residues within transmembrane helices in the sulfate transporter SHST1. Biochemistry 42 (2003) 12941-12949
28. Shibagaki N., and Grossman A.R. The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. Journal of Biological Chemistry 281 (2006) 22964-22973
29. Sindic A., Chang M.-H., Mount D.B., and Romero M.F. Renal physiology of SLC26 anion exchangers. Current Opinion In Nephrology and Hypertension 16 (2007) 484-490
30. Smith F.W., Ealing P.M., Hawkesford M.J., and Clarkson D.T. Plant members of a family of sulfate transporters reveal functional subtypes. Proceedings of the National Academy of Sciences of the United States of America, vol. 92 (1995) 9373-9377
31. Smith F.W., Hawkesford M.J., Prosser I.M., and Clarkson D.T. Isolation of a Cdna from Saccharomyces cerevisiae that encodes a high affinity sulfate transporter at the plasma membrane. Molecular & General Genetics 247 (1995) 709-715
32. Tejada-Jimenez M., Llamas A., Sanz-Luque E., Galvan A., and Fernandez E. A high-affinity molybdate transporter in eukaryotes. Proceedings of the National Academy of Sciences of the United States of America, vol. 104 (2007) 20126-20130
33. Tomatsu H., Takano J., Takahashi H., Watanabe-Takahashi A., Shibagaki N., and Fujiwara T. An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proceedings of the National Academy of Sciences of the United States of America, vol. 104 (2007) 18807-18812
34. Wan W.Y., and Milner-White E.J. A recurring two-hydrogen-bond motif incorporating a serine or threonine residue is found both at alpha-helical N termini and in other situations. Journal of Molecular Biology 286 (1999) 1651-1662
35. Zheng J., Long K.B., Shen W., Madison L.D., and Dallos P. Prestin topology: localization of protein epitopes in relation to the plasma membrane. Neuroreport 12 (2001) 1929-1935