The novel class of seven transmembrane segment inverted repeat carriers

References

Alguel, Y., Amillis, S., Leung, J., Lambrinidis, G., Capaldi, S., Scull, N.J., Craven, G., Iwata, S., Armstrong, A., Mikros, E., et al. (2016). Structure of eukaryotic purine/H⁺ symporter UapA suggests a role for homodimerization in transport activity. Nat. Commun. 7, 11336.10.1038/ncomms11336Search in Google Scholar PubMed PubMed Central

Alper, S.L. and Sharma, A.K. (2013). The SLC26 gene family of anion transporters and channels. Mol. Aspects Med. 34, 494–515.10.1016/j.mam.2012.07.009Search in Google Scholar PubMed PubMed Central

Arakawa, T., Kobayashi-Yurugi, T., Alguel, Y., Iwanari, H., Hatae, H., Iwata, M., Abe, Y., Hino, T., Ikeda-Suno, C., Kuma, H., et al. (2015). Crystal structure of the anion exchanger domain of human erythrocyte band 3. Science 350, 680–684.10.1126/science.aaa4335Search in Google Scholar PubMed

Babu, M., Greenblatt, J.F., Emili, A., Strynadka, N.C., Reithmeier, R.A., and Moraes, T.F. (2010). 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, 1450–1462.10.1016/j.str.2010.08.015Search in Google Scholar PubMed

Brahm, J. and Wieth, J.O. (1977). Separative pathways for urea and water, and for chloride in chicken erythrocytes. J. Physiol. 266, 727–749.10.1113/jphysiol.1977.sp011790Search in Google Scholar PubMed PubMed Central

Bürzle, M., Suzuki, Y., Ackermann, D., Miyazaki, H., Maeda, N., Clemencon, B., Burrier, R., and Hediger, M.A. (2013). The sodium-dependent ascorbic acid transporter family SLC23. Mol Aspects Med 34, 436–454.10.1016/j.mam.2012.12.002Search in Google Scholar PubMed

Casey, J.R. and Reithmeier, R.A. (1991). Analysis of the oligomeric state of Band 3, the anion transport protein of the human erythrocyte membrane, by size exclusion high performance liquid chromatography. Oligomeric stability and origin of heterogeneity. J. Biol. Chem. 266, 15726–15737.10.1016/S0021-9258(18)98470-XSearch in Google Scholar

Chan, R.H., Lewis, J.W., and Bogomolni, R.A. (2013). Photocycle of the LOV-STAS protein from the pathogen Listeria monocytogenes. Photochem. Photobiol. 89, 361–369.10.1111/php.12004Search in Google Scholar PubMed

Chernova, M.N., Jiang, L., Shmukler, B.E., Schweinfest, C.W., Blanco, P., Freedman, S.D., Stewart, A.K., and Alper, S.L. (2003). Acute regulation of the SLC26A3 congenital chloride diarrhoea anion exchanger (DRA) expressed in Xenopus oocytes. J. Physiol. 549, 3–19.10.1113/jphysiol.2003.039818Search in Google Scholar PubMed PubMed Central

Coincon, M., Uzdavinys, P., Nji, E., Dotson, D.L., Winkelmann, I., Abdul-Hussein, S., Cameron, A.D., Beckstein, O., and Drew, D. (2016). Crystal structures reveal the molecular basis of ion translocation in sodium/proton antiporters. Nat. Struct. Mol. Biol. 23, 248–255.10.1038/nsmb.3164Search in Google Scholar PubMed

Compton, E.L., Karinou, E., Naismith, J.H., Gabel, F., and Javelle, A. (2011). Low resolution structure of a bacterial SLC26 transporter reveals dimeric stoichiometry and mobile intracellular domains. J. Biol. Chem. 286, 27058–27067.10.1074/jbc.M111.244533Search in Google Scholar PubMed PubMed Central

Compton, E.L., Page, K., Findlay, H.E., Haertlein, M., Moulin, M., Zachariae, U., Norman, D.G., Gabel, F., and Javelle, A. (2014). Conserved structure and domain organization among bacterial Slc26 transporters. Biochem. J. 463, 297–307.10.1042/BJ20130619Search in Google Scholar PubMed

Crisman, T.J., Qu, S., Kanner, B.I., and Forrest, L.R. (2009). Inward-facing conformation of glutamate transporters as revealed by their inverted-topology structural repeats. Proc. Natl. Acad. Sci. USA 106, 20752–20757.10.1073/pnas.0908570106Search in Google Scholar PubMed PubMed Central

Dahl, N.K., Jiang, L., Chernova, M.N., Stuart-Tilley, A.K., Shmukler, B.E., and Alper, S.L. (2003). Deficient HCO₃⁻ transport in an AE1 mutant with normal Cl⁻ transport can be rescued by carbonic anhydrase II presented on an adjacent AE1 protomer. J. Biol. Chem. 278, 44949–44958.10.1074/jbc.M308660200Search in Google Scholar PubMed

Dallos, P. and Fakler, B. (2002). Prestin, a new type of motor protein. Nat. Rev. Mol. Cell Biol. 3, 104–111.10.1038/nrm730Search in Google Scholar PubMed

Detro-Dassen, S., Schanzler, M., Lauks, H., Martin, I., zu Berstenhorst, S.M., Nothmann, D., Torres-Salazar, D., Hidalgo, P., Schmalzing, G., and Fahlke, C. (2008). Conserved dimeric subunit stoichiometry of SLC26 multifunctional anion exchangers. J. Biol. Chem. 283, 4177–4188.10.1074/jbc.M704924200Search in Google Scholar PubMed

Drew, D. and Boudker, O. (2016). Shared molecular mechanisms of membrane transporters. Annu. Rev. Biochem. 85, 543–572.10.1146/annurev-biochem-060815-014520Search in Google Scholar PubMed

Espiritu, D.J., Bernardo, A.A., and Arruda, J.A. (2006). Role of NH₂ and COOH termini in targeting, stability, and activity of sodium bicarbonate cotransporter 1. Am. J. Physiol. Renal Physiol. 291, F588–596.10.1152/ajprenal.00361.2005Search in Google Scholar PubMed

Forrest, L.R. (2015). Structural symmetry in membrane proteins. Annu. Rev. Biophys. 44, 311–337.10.1146/annurev-biophys-051013-023008Search in Google Scholar PubMed PubMed Central

Forrest, L.R., Zhang, Y.W., Jacobs, M.T., Gesmonde, J., Xie, L., Honig, B.H., and Rudnick, G. (2008). Mechanism for alternating access in neurotransmitter transporters. Proc. Natl. Acad Sci. USA 105, 10338–10343.10.1073/pnas.0804659105Search in Google Scholar PubMed PubMed Central

Geertsma, E.R., Chang, Y.N., Shaik, F.R., Neldner, Y., Pardon, E., Steyaert, J., and Dutzler, R. (2015). Structure of a prokaryotic fumarate transporter reveals the architecture of the SLC26 family. Nat. Struct. Mol. Biol. 22, 803–808.10.1038/nsmb.3091Search in Google Scholar PubMed

Gournas, C., Papageorgiou, I., and Diallinas, G. (2008). The nucleobase-ascorbate transporter (NAT) family: genomics, evolution, structure-function relationships and physiological role. Mol. Biosyst. 4, 404–416.10.1039/b719777bSearch in Google Scholar PubMed

Grinstein, S., Ship, S., and Rothstein, A. (1978). Anion transport in relation to proteolytic dissection of band 3 protein. Biochim. Biophys Acta 507, 294–304.10.1016/0005-2736(78)90424-8Search in Google Scholar PubMed

Hallworth, R., Stark, K., Zholudeva, L., Currall, B.B., and Nichols, M.G. (2013). The conserved tetrameric subunit stoichiometry of Slc26 proteins. Microsc. Microanal. 19, 799–807.10.1017/S1431927613000457Search in Google Scholar PubMed PubMed Central

Hediger, M.A., Romero, M.F., Peng, J.B., Rolfs, A., Takanaga, H., and Bruford, E.A. (2004). The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteins: Introduction. Pflüger’s Arch. 447, 465–468.10.1007/s00424-003-1192-ySearch in Google Scholar PubMed

Heneghan, J.F., Akhavein, A., Salas, M.J., Shmukler, B.E., Karniski, L.P., Vandorpe, D.H., and Alper, S.L. (2010). Regulated transport of sulfate and oxalate by SLC26A2/DTDST. Am. J. Physiol. Cell Physiol. 298, C1363–1375.10.1152/ajpcell.00004.2010Search in Google Scholar PubMed PubMed Central

Jennings, M.L. and Anderson, M.P. (1987). Chemical modification and labeling of glutamate residues at the stilbenedisulfonate site of human red blood cell band 3 protein. J. Biol. Chem. 262, 1691–1697.10.1016/S0021-9258(19)75693-2Search in Google Scholar

Jennings, M.L. and Smith, J.S. (1992). Anion-proton cotransport through the human red blood cell band 3 protein. Role of glutamate 681. J. Biol. Chem. 267, 13964–13971.10.1016/S0021-9258(19)49664-6Search in Google Scholar

Ko, S.B., Zeng, W., Dorwart, M.R., Luo, X., Kim, K.H., Millen, L., Goto, H., Naruse, S., Soyombo, A., Thomas, P.J., et al. (2004). Gating of CFTR by the STAS domain of SLC26 transporters. Nat. Cell Biol. 6, 343–350.10.1038/ncb1115Search in Google Scholar PubMed PubMed Central

Kosti, V., Papageorgiou, I., and Diallinas, G. (2010). Dynamic elements at both cytoplasmically and extracellularly facing sides of the UapA transporter selectively control the accessibility of substrates to their translocation pathway. J. Mol. Biol. 397, 1132–1143.10.1016/j.jmb.2010.02.037Search in Google Scholar PubMed

Lee, C., Kang, H.J., von Ballmoos, C., Newstead, S., Uzdavinys, P., Dotson, D.L., Iwata, S., Beckstein, O., Cameron, A.D., and Drew, D. (2013). A two-domain elevator mechanism for sodium/proton antiport. Nature 501, 573–577.10.1038/nature12484Search in Google Scholar PubMed PubMed Central

Lindenthal, S. and Schubert, D. (1991). Monomeric erythrocyte band 3 protein transports anions. Proc. Natl. Acad. Sci. USA 88, 6540–6544.10.1073/pnas.88.15.6540Search in Google Scholar PubMed PubMed Central

Lolli, G., Pasqualetto, E., Costanzi, E., Bonetto, G., and Battistutta, R. (2016). The STAS domain of mammalian SLC26A5 prestin harbours an anion-binding site. Biochem. J. 473, 365–370.10.1042/BJ20151089Search in Google Scholar PubMed

Low, P.S. (1986). Structure and function of the cytoplasmic domain of band 3: center of erythrocyte membrane-peripheral protein interactions. Biochim. Biophys. Acta 864, 145–167.10.1016/0304-4157(86)90009-2Search in Google Scholar PubMed

Lu, F., Li, S., Jiang, Y., Jiang, J., Fan, H., Lu, G., Deng, D., Dang, S., Zhang, X., Wang, J., et al. (2011). Structure and mechanism of the uracil transporter UraA. Nature 472, 243–246.10.1038/nature09885Search in Google Scholar PubMed

Mancusso, R., Gregorio, G.G., Liu, Q., and Wang, D.N. (2012). Structure and mechanism of a bacterial sodium-dependent dicarboxylate transporter. Nature 491, 622–626.10.1038/nature11542Search in Google Scholar PubMed PubMed Central

Martzoukou, O., Karachaliou, M., Yalelis, V., Leung, J., Byrne, B., Amillis, S., and Diallinas, G. (2015). Oligomerization of the UapA purine transporter is critical for ER-exit, plasma membrane localization and turnover. J. Mol. Biol. 427, 2679–2696.10.1016/j.jmb.2015.05.021Search in Google Scholar PubMed

Masuda, S., Murakami, K.S., Wang, S., Anders Olson, C., Donigian, J., Leon, F., Darst, S.A., and Campbell, E.A. (2004). Crystal structures of the ADP and ATP bound forms of the Bacillus anti-sigma factor SpoIIAB in complex with the anti-anti-sigma SpoIIAA. J. Mol. Biol. 340, 941–956.10.1016/j.jmb.2004.05.040Search in Google Scholar PubMed

Matsuyama, H., Kawano, Y., and Hamasaki, N. (1986). Involvement of a histidine residue in inorganic phosphate and phosphoenolpyruvate transport across the human erythrocyte membrane. J. Biochem. 99, 495–501.10.1093/oxfordjournals.jbchem.a135504Search in Google Scholar PubMed

McAlear, S.D., Liu, X., Williams, J.B., McNicholas-Bevensee, C.M., and Bevensee, M.O. (2006). Electrogenic Na/HCO3 cotransporter (NBCe1) variants expressed in Xenopus oocytes: functional comparison and roles of the amino and carboxy termini. J. Gen. Physiol. 127, 639–658.10.1085/jgp.200609520Search in Google Scholar PubMed PubMed Central

Mio, K., Kubo, Y., Ogura, T., Yamamoto, T., Arisaka, F., and Sato, C. (2008). The motor protein prestin is a bullet-shaped molecule with inner cavities. J. Biol. Chem. 283, 1137–1145.10.1074/jbc.M702681200Search in Google Scholar PubMed

Mulligan, C., Fenollar-Ferrer, C., Fitzgerald, G.A., Vergara-Jaque, A., Kaufmann, D., Li, Y., Forrest, L.R., and Mindell, J.A. (2016). The bacterial dicarboxylate transporter VcINDY uses a two-domain elevator-type mechanism. Nat. Struct. Mol. Biol. 23, 256–263.10.1038/nsmb.3166Search in Google Scholar PubMed PubMed Central

Ohana, E., Yang, D., Shcheynikov, N., and Muallem, S. (2009). Diverse transport modes by the solute carrier 26 family of anion transporters. J. Physiol. 587, 2179–2185.10.1113/jphysiol.2008.164863Search in Google Scholar PubMed PubMed Central

Oliver, D., He, D.Z., Klocker, N., Ludwig, J., Schulte, U., Waldegger, S., Ruppersberg, J.P., Dallos, P., and Fakler, B. (2001). Intracellular anions as the voltage sensor of prestin, the outer hair cell motor protein. Science 292, 2340–2343.10.1126/science.1060939Search in Google Scholar PubMed

Papageorgiou, I., Gournas, C., Vlanti, A., Amillis, S., Pantazopoulou, A., and Diallinas, G. (2008). Specific interdomain synergy in the UapA transporter determines its unique specificity for uric acid among NAT carriers. J. Mol. Biol. 382, 1121–1135.10.1016/j.jmb.2008.08.005Search in Google Scholar PubMed

Parker, M.D. and Boron, W.F. (2013). The divergence, actions, roles, and relatives of sodium-coupled bicarbonate transporters. Physiol. Rev. 93, 803–959.10.1152/physrev.00023.2012Search in Google Scholar PubMed PubMed Central

Pasqualetto, E., Aiello, R., Gesiot, L., Bonetto, G., Bellanda, M., and Battistutta, R. (2010). 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, 448–462.10.1016/j.jmb.2010.05.013Search in Google Scholar PubMed

Passow, H. (1986). Molecular aspects of band 3 protein-mediated anion transport across the red blood cell membrane. Rev. Physiol. Biochem. Pharmacol. 103, 61–203.10.1007/3540153330_2Search in Google Scholar PubMed

Price, G.D., Woodger, F.J., Badger, M.R., Howitt, S.M., and Tucker, L. (2004). Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc. Natl. Acad Sci. USA 101, 18228–18233.10.1073/pnas.0405211101Search in Google Scholar PubMed PubMed Central

Reithmeier, R.A. (1979). Fragmentation of the band 3 polypeptide from human erythrocyte membranes. Size and detergent binding of the membrane-associated domain. J. Biol. Chem. 254, 3054–3060.10.1016/S0021-9258(17)30181-3Search in Google Scholar

Reithmeier, R.A., Casey, J.R., Kalli, A.C., Sansom, M.S., Alguel, Y., and Iwata, S. (2016). Band 3, the human red cell chloride/bicarbonate anion exchanger (AE1, SLC4A1), in a structural context. Biochim. Biophys. Acta 1858, 1507–1532.10.1016/j.bbamem.2016.03.030Search in Google Scholar PubMed

Ressl, S., Terwisscha van Scheltinga, A.C., Vonrhein, C., Ott, V., and Ziegler, C. (2009). Molecular basis of transport and regulation in the Na⁺/betaine symporter BetP. Nature 458, 47–52.10.1038/nature07819Search in Google Scholar PubMed

Reyes, N., Ginter, C., and Boudker, O. (2009). Transport mechanism of a bacterial homologue of glutamate transporters. Nature 462, 880–885.10.1038/nature08616Search in Google Scholar PubMed PubMed Central

Romero, M.F., Chen, A.P., Parker, M.D., and Boron, W.F. (2013). The SLC4 family of bicarbonate HCO₃⁻ transporters. Mol. Aspects Med. 34, 159–182.10.1016/j.mam.2012.10.008Search in Google Scholar PubMed PubMed Central

Rouached, H., Berthomieu, P., El Kassis, E., Cathala, N., Catherinot, V., Labesse, G., Davidian, J.C., and Fourcroy, P. (2005). Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter SULTR1.2. J. Biol. Chem. 280, 15976–15983.10.1074/jbc.M501635200Search in Google Scholar PubMed

Saier, M.H., Jr. (2000). A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64, 354–411.10.1128/MMBR.64.2.354-411.2000Search in Google Scholar PubMed PubMed Central

Schlessinger, A., Matsson, P., Shima, J.E., Pieper, U., Yee, S.W., Kelly, L., Apeltsin, L., Stroud, R.M., Ferrin, T.E., Giacomini, K.M., et al. (2010). Comparison of human solute carriers. Protein Sci. 19, 412–428.10.1002/pro.320Search in Google Scholar PubMed PubMed Central

Sharma, A.K., Rigby, A.C., and Alper, S.L. (2011a). STAS domain structure and function. Cell Physiol. Biochem. 28, 407–422.10.1159/000335104Search in Google Scholar PubMed PubMed Central

Sharma, A.K., Ye, L., Baer, C.E., Shanmugasundaram, K., Alber, T., Alper, S.L., and Rigby, A.C. (2011b). Solution structure of the guanine nucleotide-binding STAS domain of SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis. J. Biol. Chem. 286, 8534–8544.10.1074/jbc.M110.165449Search in Google Scholar PubMed PubMed Central

Shibagaki, N. and Grossman, A.R. (2004). Probing the function of STAS domains of the Arabidopsis sulfate transporters. J. Biol. Chem. 279, 30791–30799.10.1074/jbc.M403248200Search in Google Scholar PubMed

Shibagaki, N. and Grossman, A.R. (2006). The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. J. Biol. Chem. 281, 22964–22973.10.1074/jbc.M603462200Search in Google Scholar PubMed

Shnitsar, V., Li, J., Li, X., Calmettes, C., Basu, A., Casey, J.R., Moraes, T.F., and Reithmeier, R.A. (2013). A substrate access tunnel in the cytosolic domain is not an essential feature of the solute carrier 4 (SLC4) family of bicarbonate transporters. J. Biol. Chem. 288, 33848–33860.10.1074/jbc.M113.511865Search in Google Scholar PubMed PubMed Central

Srinivasan, L., Baars, T.L., Fendler, K., and Michel, H. (2016). Functional characterization of solute carrier (SLC) 26/sulfate permease (SulP) proteins in membrane mimetic systems. Biochim. Biophys. Acta 1858, 698–705.10.1016/j.bbamem.2016.01.006Search in Google Scholar PubMed

Takazaki, S., Abe, Y., Kang, D., Li, C., Jin, X., Ueda, T., and Hamasaki, N. (2006). The functional role of arginine 901 at the C-terminus of the human anion transporter band 3 protein. J. Biochem. 139, 903–912.10.1093/jb/mvj097Search in Google Scholar PubMed

Thurtle-Schmidt, B.H. and Stroud, R.M. (2016). Structure of Bor1 supports an elevator transport mechanism for SLC4 anion exchangers. Proc. Natl. Acad Sci. USA 113, 10542–10546.10.1073/pnas.1612603113Search in Google Scholar PubMed PubMed Central

Van Dort, H.M., Moriyama, R., and Low, P.S. (1998). Effect of band 3 subunit equilibrium on the kinetics and affinity of ankyrin binding to erythrocyte membrane vesicles. J. Biol. Chem. 273, 14819–14826.10.1074/jbc.273.24.14819Search in Google Scholar PubMed

Vastermark, A. and Saier, M.H., Jr. (2014). Evolutionary relationship between 5+5 and 7+7 inverted repeat folds within the amino acid-polyamine-organocation superfamily. Proteins 82, 336–346.10.1002/prot.24401Search in Google Scholar PubMed

Vergara-Jaque, A., Fenollar-Ferrer, C., Kaufmann, D., and Forrest, L.R. (2015). Repeat-swap homology modeling of secondary active transporters: updated protocol and prediction of elevator-type mechanisms. Front Pharmacol. 6, 183.10.3389/fphar.2015.00183Search in Google Scholar PubMed PubMed Central

Vlanti, A., Amillis, S., Koukaki, M., and Diallinas, G. (2006). A novel-type substrate-selectivity filter and ER-exit determinants in the UapA purine transporter. J. Mol. Biol. 357, 808–819.10.1016/j.jmb.2005.12.070Search in Google Scholar PubMed

Wang, D.N., Kuhlbrandt, W., Sarabia, V.E., and Reithmeier, R.A. (1993). Two-dimensional structure of the membrane domain of human band 3, the anion transport protein of the erythrocyte membrane. EMBO J 12, 2233–2239.10.1002/j.1460-2075.1993.tb05876.xSearch in Google Scholar PubMed PubMed Central

Wang, X., Yang, S., Jia, S., and He, D.Z. (2010). Prestin forms oligomer with four mechanically independent subunits. Brain Res 1333, 28–35.10.1016/j.brainres.2010.03.070Search in Google Scholar PubMed PubMed Central

Wohlert, D., Grotzinger, M.J., Kuhlbrandt, W., and Yildiz, O. (2015). Mechanism of Na⁺-dependent citrate transport from the structure of an asymmetrical CitS dimer. eLife 4, e09375.10.7554/eLife.09375Search in Google Scholar PubMed PubMed Central

Zhang, D., Kiyatkin, A., Bolin, J.T., and Low, P.S. (2000). Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood 96, 2925–2933.10.1182/blood.V96.9.2925Search in Google Scholar

Zheng, J., Shen, W., He, D.Z., Long, K.B., Madison, L.D., and Dallos, P. (2000). Prestin is the motor protein of cochlear outer hair cells. Nature 405, 149–155.10.1038/35012009Search in Google Scholar PubMed

Zheng, J., Du, G.G., Anderson, C.T., Keller, J.P., Orem, A., Dallos, P., and Cheatham, M. (2006). Analysis of the oligomeric structure of the motor protein prestin. J. Biol. Chem. 281, 19916–19924.10.1074/jbc.M513854200Search in Google Scholar PubMed