When two turn into one: evolution of membrane transporters from half modules

References

Abramson, J., Smirnova, I., Kasho, V., Verner, G., Kaback, H.R., and Iwata, S. (2003). Structure and mechanism of the lactose permease of Escherichia coli. Science 301, 610–615.Search in Google Scholar

Ames, G.F., Nikaido, K., Groarke, J., and Petithory, J. (1989). Reconstitution of periplasmic transport in inside-out membrane vesicles. Energization by ATP. J. Biol. Chem. 264, 3998–4002.Search in Google Scholar

Andersson, M., Bondar, A.N., Freites, J.A., Tobias, D.J., Kaback, H.R., and White, S.H. (2012). Proton-coupled dynamics in lactose permease. Structure 20, 1893–1904.Search in Google Scholar

Baker, J.L., Sudarsan, N., Weinberg, Z., Roth, A., Stockbridge, R.B., and Breaker, R.R. (2012). Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235.Search in Google Scholar

Bordignon, E., Grote, M., and Schneider, E. (2010). The maltose ATP-binding cassette transporter in the 21st century–towards a structural dynamic perspective on its mode of action. Mol. Microbiol. 77, 1354–1366.Search in Google Scholar

Boughner, L.A. and Doerrler, W.T. (2012). Multiple deletions reveal the essentiality of the DedA membrane protein family in Escherichia coli. Microbiology 158, 1162–1171.Search in Google Scholar

Chaptal, V.K.S., Sawaya, M.R., Guan, L., Kaback, H.R., and Abramson, J. (2011). Crystal structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition. Proc. Natl. Acad. Sci. USA 108, 9361–9366.Search in Google Scholar

Chardon, F., Bedu, M., Calenge, F., Klemens, P.A., Spinner, L., Clement, G., Chietera, G., Leran, S., Ferrand, M., Lacombe, B., et al. (2013). Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr. Biol. 23, 697–702.Search in Google Scholar

Chen, L.Q., Hou, B.H., Lalonde, S., Takanaga, H., Hartung, M.L., Qu, X.Q., Guo, W.J., Kim, J.G., Underwood, W., Chaudhuri, B., et al. (2010). Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532.Search in Google Scholar

Chen, Y.J., Pornillos, O., Lieu, S., Ma, C., Chen, A.P., and Chang, G. (2007). X-ray structure of EmrE supports dual topology model. Proc. Natl. Acad. Sci. USA 104, 18999–19004.Search in Google Scholar

Cohn, M., Bart, R., Shybut, M., Dahlbeck, D., Gomez, M., Morbitzer, R., Hou, B.H., Frommer, W., Lahaye, T., and Staskawicz, B. (2014). Xanthomonas axonopodis virulence is promoted by a transcription activator like (TAL) effector mediated induction of a SWEET sugar transporter in cassava. Mol. Plant. Microbe. Interact. 27, 1186–1198.Search in Google Scholar

Doerrler, W.T., Sikdar, R., Kumar, S., and Boughner, L.A. (2013). New functions for the ancient DedA membrane protein family. J. Bacteriol. 195, 3–11.Search in Google Scholar

Duran, A.M. and Meiler, J. (2013). Inverted topologies in membrane proteins: a mini-review. Comput. Struct. Biotechnol. J. 8, e201308004.Search in Google Scholar

Faham, S., Watanabe, A., Besserer, G.M., Cascio, D., Specht, A., Hirayama, B.A., Wright, E.M., and Abramson, J. (2008). The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na+/sugar symport. Science 321, 810–814.Search in Google Scholar

Fang, Y., Jayaram, H., Shane, T., Kolmakova-Partensky, L., Wu, F., Williams, C., Xiong, Y., and Miller, C. (2009). Structure of a prokaryotic virtual proton pump at 3.2 A resolution. Nature 460, 1040–1043.Search in Google Scholar

Forrest, L.R. and Rudnick, G. (2009). The rocking bundle: a mechanism for ion-coupled solute flux by symmetrical transporters. Physiology (Bethesda) 24, 377–386.Search in Google Scholar

Gouaux, E. (2009). Review. The molecular logic of sodium-coupled neurotransmitter transporters. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364, 149–154.Search in Google Scholar

Guan, L. and Kaback, H.R. (2006). Lessons from lactose permease. Annu. Rev. Biophys. Biomol. Struct. 35, 67–91.Search in Google Scholar

Guan, L., Mirza, O., Verner, G., Iwata, S., and Kaback, H.R. (2007). Structural determination of wild-type lactose permease. Proc. Natl. Acad. Sci. USA 104, 15294–15298.Search in Google Scholar

Guo, W.J., Nagy, R., Chen, H.Y., Pfrunder, S., Yu, Y.C., Santelia, D., Frommer, W.B., and Martinoia, E. (2014). SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol. 164, 777–789.Search in Google Scholar

Henderson, P.J. and Baldwin, S.A. (2012). Structural biology: Bundles of insights into sugar transporters. Nature 490, 348–350.Search in Google Scholar

Higgins, C.F. (1992). ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8, 67–113.Search in Google Scholar

Hirai, T., Heymann, J.A., Maloney, P.C., and Subramaniam, S. (2003). Structural model for 12-helix transporters belonging to the major facilitator superfamily. J. Bacteriol. 185, 1712–1718.Search in Google Scholar

Holland, I.B. and Blight, M.A. (1999). ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol. 293, 381–399.Search in Google Scholar

Horio, M., Gottesman, M.M., and Pastan, I. (1988). ATP-dependent transport of vinblastine in vesicles from human multidrug-resistant cells. Proc. Natl. Acad. Sci. USA 85, 3580–3584.Search in Google Scholar

Jardetzky, O. (1966). Simple allosteric model for membrane pumps. Nature 211, 969–970.Search in Google Scholar

Kaback, H.R., Smirnova, I., Kasho, V., Nie, Y., and Zhou, Y. (2011). The alternating access transport mechanism in LacY. J. Membr. Biol. 239, 85–93.Search in Google Scholar

Kallberg, M., Wang, H., Wang, S., Peng, J., Wang, Z., Lu, H., and Xu, J. (2012). Template-based protein structure modeling using the RaptorX web server. Nat. Protoc. 7, 1511–1522.Search in Google Scholar

Keller, R. and Schneider, D. (2013). Homologs of the yeast Tvp38 vesicle-associated protein are conserved in chloroplasts and cyanobacteria. Front. Plant. Sci. 4, 467.Search in Google Scholar

Khafizov, K., Staritzbichler, R., Stamm, M., and Forrest, L.R. (2010). A study of the evolution of inverted-topology repeats from LeuT-fold transporters using AlignMe. Biochemistry 49, 10702–10713.Search in Google Scholar

Koshy, C., Schweikhard, E.S., Gartner, R.M., Perez, C., Yildiz, O., and Ziegler, C. (2013). Structural evidence for functional lipid interactions in the betaine transporter BetP. EMBO J. 32, 3096–3105.Search in Google Scholar

Krishnamurthy, H. and Gouaux, E. (2012). X-ray structures of LeuT in substrate-free outward-open and apo inward-open states. Nature 481, 469–474.Search in Google Scholar

Kumar, S. and Doerrler, W.T. (2014). Members of the conserved DedA family are likely membrane transporters and are required for drug resistance in Escherichia coli. Antimicrob. Agents. Chemother. 58, 923–930.Search in Google Scholar

Kumar, H., Kasho, V., Smirnova, I., Finer-Moore, J.S., Kaback, H.R., and Stroud, R.M. (2014). Structure of sugar-bound LacY. Proc. Natl. Acad. Sci. USA 111, 1784–1788.Search in Google Scholar

Lee, B.L., Li, X., Liu, Y., Sykes, B.D., and Fliegel, L. (2009). Structural and functional analysis of transmembrane XI of the NHE1 isoform of the Na+/H+ exchanger. J. Biol. Chem. 284, 11546–11556.Search in Google Scholar

Li, S., Smith, K.D., Davis, J.H., Gordon, P.B., Breaker, R.R., and Strobel, S.A. (2013). Eukaryotic resistance to fluoride toxicity mediated by a widespread family of fluoride export proteins. Proc. Natl. Acad. Sci. USA 110, 19018–19023.Search in Google Scholar

Liu, P.Q. and Ames, G.F. (1998). In vitro disassembly and reassembly of an ABC transporter, the histidine permease. Proc. Natl. Acad. Sci. USA 95, 3495–3500.Search in Google Scholar

Lloris-Garcera, P., Seppala, S., Slusky, J.S., Rapp, M., and von Heijne, G. (2014). Why have small multidrug resistance proteins not evolved into fused, internally duplicated structures? J. Mol. Biol. 426, 2246–2254.Search in Google Scholar

Madej, M.G. and Kaback, H.R. (2013). Evolutionary mix-and-match with MFS transporters II. Proc. Natl. Acad. Sci. USA 110, E4831–4838.Search in Google Scholar

Madej, M.G., Dang, S., Yan, N., and Kaback, H.R. (2013). Evolutionary mix-and-match with MFS transporters. Proc. Natl. Acad. Sci. USA 110, 5870–5874.Search in Google Scholar

Madej, M.G., Sun, L., Yan, N., and Kaback, H.R. (2014). Functional architecture of MFS D-glucose transporters. Proc. Natl. Acad. Sci. USA 111, 719–727.Search in Google Scholar

Marger, M.D. and Saier, M.H., Jr. (1993). A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends. Biochem. Sci. 18, 13–20.Search in Google Scholar

McLachlan, A.D. (1972). Gene duplication in carp muscle calcium binding protein. Nat. New Biol. 240, 83–85.Search in Google Scholar

Mirza, O., Guan, L., Verner, G., Iwata, S., and Kaback, H.R. (2006). Structural evidence for induced fit and a mechanism for sugar/H+ symport in LacY. EMBO J. 25, 1177–1183.Search in Google Scholar

Morrison, E.A., DeKoster, G.T., Dutta, S., Vafabakhsh, R., Clarkson, M.W., Bahl, A., Kern, D., Ha, T., and Henzler-Wildman, K.A. (2011). Antiparallel EmrE exports drugs by exchanging between asymmetric structures. Nature 481, 45–50.Search in Google Scholar

Mourez, M., Jehanno, M., Schneider, E., and Dassa, E. (1998). In vitro interaction between components of the inner membrane complex of the maltose ABC transporter of Escherichia coli: modulation by ATP. Mol. Microbiol. 30, 353–363.Search in Google Scholar

Nikaido, H. (2002). How are the ABC transporters energized? Proc. Natl. Acad. Sci. USA 99, 9609–9610.Search in Google Scholar

Oldham, M.L., Davidson, A.L., and Chen, J. (2008). Structural insights into ABC transporter mechanism. Curr. Opin. Struct. Biol. 18, 726–733.Search in Google Scholar

Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trezeguet, V., Lauquin, G.J., and Brandolin, G. (2003). Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39–44.Search in Google Scholar

Perez, C. and Ziegler, C. (2013). Mechanistic aspects of sodium-binding sites in LeuT-like fold symporters. Biol. Chem. 394, 641–648.Search in Google Scholar

Perez, C., Koshy, C., Yildiz, O., and Ziegler, C. (2012). Alternating-access mechanism in conformationally asymmetric trimers of the betaine transporter BetP. Nature 490, 126–130.Search in Google Scholar

Perez, C., Faust, B., Mehdipour, A.R., Francesconi, K.A., Forrest, L.R., and Ziegler, C. (2014). Substrate-bound outward-open state of the betaine transporter BetP provides insights into Na+ coupling. Nat. Commun. 5, 4231.Search in Google Scholar

Quistgaard, E.M., Low, C., Moberg, P., and Nordlund, P. (2013). Metal-mediated crystallization of the xylose transporter XylE from Escherichia coli in three different crystal forms. J. Struct. Biol. 184, 375–378.Search in Google Scholar

Rapp, M., Granseth, E., Seppala, S., and von Heijne, G. (2006). Identification and evolution of dual-topology membrane proteins. Nat. Struct. Mol. Biol. 13, 112–116.Search in Google Scholar

Rapp, M., Seppala, S., Granseth, E., and von Heijne, G. (2007). Emulating membrane protein evolution by rational design. Science 315, 1282–1284.Search in Google Scholar

Rees, D.C., Johnson, E., and Lewinson, O. (2009). ABC transporters: the power to change. Nat Rev Mol. Cell Biol. 10, 218–227.Search in Google Scholar

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.Search in Google Scholar

Sand, O., Gingras, M., Beck, N., Hall, C., and Trun, N. (2003). Phenotypic characterization of overexpression or deletion of the Escherichia coli crcA, cspE and crcB genes. Microbiology 149, 2107–2117.Search in Google Scholar

Schmitt, L. and Tampé, R. (2002). Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol. 12, 754–760.Search in Google Scholar

Screpanti, E. and Hunte, C. (2007). Discontinuous membrane helices in transport proteins and their correlation with function. J. Struct. Biol. 159, 261–267.Search in Google Scholar

Shaffer, P.L., Goehring, A., Shankaranarayanan, A., and Gouaux, E. (2009). Structure and mechanism of a Na+-independent amino acid transporter. Science 325, 1010–1014.Search in Google Scholar

Shi, Y. (2013). Common folds and transport mechanisms of secondary active transporters. Annu. Rev. Biophys 42, 51–72.Search in Google Scholar

Sikdar, R., Simmons, A.R., and Doerrler, W.T. (2013). Multiple envelope stress response pathways are activated in an Escherichia coli strain with mutations in two members of the DedA membrane protein family. J. Bacteriol. 195, 12–24.Search in Google Scholar

Singh, S.K., Yamashita, A., and Gouaux, E. (2007). Antidepressant binding site in a bacterial homologue of neurotransmitter transporters. Nature 448, 952–956.Search in Google Scholar

Smirnova, I., Kasho, V., Sugihara, J., Choe, J.Y., and Kaback, H.R. (2009). Residues in the H+ translocation site define the pKa for sugar binding to LacY. Biochemistry 48, 8852–8860.Search in Google Scholar

Smirnova, I., Kasho, V., Sugihara, J., and Kaback, H.R. (2013). Trp replacements for tightly interacting Gly-Gly pairs in LacY stabilize an outward-facing conformation. Proc. Natl. Acad. Sci. USA 110, 8876–8881.Search in Google Scholar

Stamm, M., Staritzbichler, R., Khafizov, K., and Forrest, L.R. (2013). Alignment of helical membrane protein sequences using AlignMe. PLoS One 8, e57731.Search in Google Scholar

Stockbridge, R.B., Robertson, J.L., Kolmakova-Partensky, L., and Miller, C. (2013). A family of fluoride-specific ion channels with dual-topology architecture. Elife 2, e01084.Search in Google Scholar

Sun, L., Zeng, X., Yan, C., Sun, X., Gong, X., Rao, Y., and Yan, N. (2012). Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature 490, 361–366.Search in Google Scholar

Tanford, C. (1982). Simple model for the chemical potential change of a transported ion in active transport. Proc. Natl. Acad. Sci. USA 79, 2882–2884.Search in Google Scholar

Tang, L., Bai, L., Wang, W.H., and Jiang, T. (2010). Crystal structure of the carnitine transporter and insights into the antiport mechanism. Nat. Struct. Mol. Biol. 17, 492–496.Search in Google Scholar

Tsai, C.J., Khafizov, K., Hakulinen, J., Forrest, L.R., Kramer, R., Kuhlbrandt, W., and Ziegler, C. (2011). Structural asymmetry in a trimeric Na+/betaine symporter, BetP, from Corynebacterium glutamicum. J. Mol. Biol. 407, 368–381.Search in Google Scholar

Tzeng, J., Lee, B.L., Sykes, B.D., and Fliegel, L. (2010). Structural and functional analysis of transmembrane segment VI of the NHE1 isoform of the Na+/H+ exchanger. J. Biol. Chem. 285, 36656–36665.Search in Google Scholar

Weber, A.P. and Bräutigam, A. (2013). The role of membrane transport in metabolic engineering of plant primary metabolism. Curr. Opin. Biotechnol. 24, 256–262.Search in Google Scholar

Weyand, S., Shimamura, T., Yajima, S., Suzuki, S., Mirza, O., Krusong, K., Carpenter, E.P., Rutherford, N.G., Hadden, J.M., O’Reilly, J., et al. (2008). Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322, 709–713.Search in Google Scholar

Wisedchaisri, G., Park, M.S., Iadanza, M.G., Zheng, H., and Gonen, T. (2014). Proton-coupled sugar transport in the prototypical major facilitator superfamily protein XylE. Nat. Commun. 5, 4521.Search in Google Scholar

Xu, Y., Tao, Y., Cheung, L.S., Fan, C., Chen, L.-Q., Xu, S., Perry, K., Frommer, W., and Feng, L. (2014). Structures of bacterial homologues of SWEET transporters in two distinct conformations. Nature doi:10.1038/nature13670.Search in Google Scholar

Xuan, Y.H., Hu, Y.B., Chen, L.Q., Sosso, D., Ducat, D.C., Hou, B.H., and Frommer, W.B. (2013). Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc. Natl. Acad. Sci. USA 110, E3685–3694.Search in Google Scholar

Yamashita, A., Singh, S.K., Kawate, T., Jin, Y., and Gouaux, E. (2005). Crystal structure of a bacterial homologue of Na+/Cl--dependent neurotransmitter transporters. Nature 437, 215–223.Search in Google Scholar

Yan, N. (2013). Structural advances for the major facilitator superfamily (MFS) transporters. Trends. Biochem. Sci. 38, 151–159.Search in Google Scholar

Yuan, M. and Wang, S. (2013). Rice MtN3/saliva/SWEET family genes and their homologs in cellular organisms. Mol. Plant 6, 665–674.Search in Google Scholar

Yuan, M., Chu, Z., Li, X., Xu, C., and Wang, S. (2010). The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution. Plant Cell 22, 3164–3176.Search in Google Scholar

Yuan, M., Zhao, J., Huang, R., Li, X., Xiao, J., and Wang, S. (2014). Rice MtN3/saliva/SWEET gene family: Evolution, expression profiling, and sugar transport. J. Integr. Plant Biol. 56, 559–570.Search in Google Scholar