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

Keller, Rebecca, Ziegler, Christine, Schneider, Dirk·2014·Biological Chemistry
DOI 10.1515/hsz-2014-0224
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Abstract

The recently increasing number of atomic structures for active transporters has not only revealed strong conservation in the architecture of sequence-unrelated transporter families, but also identified a unifying element called the ‘inverted repeat topology,’ which is found in nearly all transporter folds to date. Indeed, most membrane transporters consist of two or more domains with similar structure, so-called repeats. It is tempting to speculate that transporters have evolved by duplication of one repeat followed by gene fusion and modification events. An intriguing question is, whether recent genes encoding such a ‘half-transporter’ still exist as independent folding units. Although it seems likely that the evolution of membrane transport proteins, which harbor internal repeats, is linked to these minimal structural building blocks, their identification in the absence of structural data represents a major challenge, as sequence homology is not an issue. In this review we discuss two protein families, the DedA family and the SWEET family, being potential half-transporters and putative ancestors for two of the most abundant secondary transporter families, the MFS family and the LeuT-fold family.

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Research works printed but not linked: 154

  1. Shaffer, 2009, Structure and mechanism of a Na - independent amino acid transporter, Science, 325
  2. Ressl, 2009, van Molecular basis of transport and regulation in the Na betaine symporter, Nature, 458
  3. Nikaido, 2002, How are the ABC transporters energized, Proc Natl Acad Sci USA, 99
  4. Madej, 2013, Evolutionary mix match with MFS transporters, Proc Natl Acad Sci USA, 110
  5. Forrest, 2009, The rocking bundle : a mechanism for ion - coupled solute flux by symmetrical transporters Bethesda, Physiology, 24, 377, 10.1152/physiol.00030.2009 · DOI
  6. Wisedchaisri, 2014, Proton - coupled sugar transport in the prototypical major facilitator superfamily protein, Nat Commun, 4521, 10.1038/ncomms5521 · DOI
  7. Sun, 2012, structure of a bacterial homologue of glucose transporters GLUT, Nature, 1
  8. Chen, 2007, ray structure of EmrE supports dual topology model, Proc Natl Acad Sci USA, 18999, 10.1073/pnas.0709387104 · DOI
  9. Fang, 2009, Structure of a prokaryotic virtual proton pump at resolution, Nature, 3, 460
  10. McLachlan, 1972, Gene duplication in carp muscle calcium binding protein, Nat New Biol, 240
  11. Rapp, 2006, von Identification and evolution of dual topology membrane proteins, Nat Struct Mol Biol, 13, 112, 10.1038/nsmb1057 · DOI
  12. Fang, 2009, Structure of a prokaryotic virtual proton pump at resolution, Nature, 3, 460
  13. Sun, 2012, structure of a bacterial homologue of glucose transporters GLUT, Nature, 1
  14. Guan, 2006, Lessons from lactose permease, Annu Rev Biophys Biomol, 35
  15. Madej, 2013, Evolutionary mix and match with MFS transporters II, Proc Natl Acad Sci USA, 110
  16. Horio, 1988, dependent transport of vinblastine in vesicles from human multidrug - resistant cells, Proc Natl Acad Sci USA, 85
  17. Boughner, 2012, Multiple deletions reveal the essentiality of the DedA membrane protein family in Escherichia coli, Microbiology, 158
  18. Faham, 2008, The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na sugar symport, Science, 321
  19. Screpanti, 2007, Discontinuous membrane helices in transport proteins and their correlation with function, Struct Biol, 159
  20. Chardon, 2013, fructose content is controlled by the vacuolar transporter SWEET in, Curr Biol, 17, 697, 10.1016/j.cub.2013.03.021 · DOI
  21. Perez, 2014, Substrate - bound outward - open state of the betaine transporter BetP provides insights into Na coupling, Nat Commun, 4231, 10.1038/ncomms5231 · DOI
  22. Chen, 2007, ray structure of EmrE supports dual topology model, Proc Natl Acad Sci USA, 18999, 10.1073/pnas.0709387104 · DOI
  23. Mirza, 2006, Structural evidence for induced fit and a mechanism for sugar symport in LacY, EMBO J, 25, 1177, 10.1038/sj.emboj.7601028 · DOI
  24. Weyand, 2008, Structure and molecular mechanism of a nucleobase - cation - symport family transporter, Science, 1
  25. Kallberg, 2012, Template - based protein structure modeling using the RaptorX web server, Nat Protoc, 1511, 10.1038/nprot.2012.085 · DOI
  26. Henderson, 2012, Structural biology Bundles of insights into sugar transporters, Nature, 490
  27. Yamashita, 2005, structure of a bacterial homologue of Na - dependent neurotransmitter transporters, Nature, 437
  28. Lloris, 2014, von Why have small multidrug resistance proteins not evolved into fused internally duplicated structures, Mol Biol, 426
  29. Perez, 2014, Substrate - bound outward - open state of the betaine transporter BetP provides insights into Na coupling, Nat Commun, 4231, 10.1038/ncomms5231 · DOI
  30. Madej, 2014, Functional architecture of MFS glucose transporters, Proc Natl Acad Sci USA, 111
  31. Chen, 2010, Sugar transporters for intercellular exchange and nutrition of pathogens, Nature, 468
  32. Oldham, 2008, Structural insights into ABC transporter mechanism, Biol, 18, 726
  33. Perez, 2013, Mechanistic aspects of sodium - binding sites in LeuT - like fold symporters, Biol Chem, 394
  34. Madej, 2013, Evolutionary mix and match with MFS transporters II, Proc Natl Acad Sci USA, 110
  35. Screpanti, 2007, Discontinuous membrane helices in transport proteins and their correlation with function, Struct Biol, 159
  36. Nikaido, 2002, How are the ABC transporters energized, Proc Natl Acad Sci USA, 99
  37. Pebay, 2003, Structure of mitochondrial carrier in complex with carboxyatractyloside, Nature, 426
  38. Forrest, 2009, The rocking bundle : a mechanism for ion - coupled solute flux by symmetrical transporters Bethesda, Physiology, 24, 377, 10.1152/physiol.00030.2009 · DOI
  39. Yuan, 2010, The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution, Plant Cell, 22, 3164, 10.1105/tpc.110.078022 · DOI
  40. Khafizov, 2010, study of the evolution of inverted - topology repeats from LeuT - fold transporters using, Biochemistry, 49
  41. Singh, 2007, Antidepressant binding site in a bacterial homologue of neurotransmitter transporters, Nature, 448
  42. Koshy, 2013, Structural evidence for functional lipid interactions in the betaine transporter, EMBO J, 3096, 10.1038/emboj.2013.226 · DOI
  43. Perez, 2012, Alternating - access mechanism in conformationally asymmetric trimers of the betaine transporter, Nature, 490
  44. Boughner, 2012, Multiple deletions reveal the essentiality of the DedA membrane protein family in Escherichia coli, Microbiology, 158
  45. Kallberg, 2012, Template - based protein structure modeling using the RaptorX web server, Nat Protoc, 1511, 10.1038/nprot.2012.085 · DOI
  46. Kumar, 2014, Structure of sugar - bound, Proc Natl Acad Sci USA, 111
  47. Holland, 1999, Blight ABC adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans, Mol Biol, 293
  48. Bordignon, 2010, The maltose ATP - binding cassette transporter in the st century towards a structural dynamic perspective on its mode of action, Mol Microbiol, 21, 77
  49. Schmitt, 2002, Structure and mechanism of ABC transporters, Biol, 12, 754
  50. Tzeng, 2010, Structural and functional analysis of transmembrane segment VI of the isoform of the Na exchanger, Biol Chem, 1
  51. Baker, 2012, Breaker Widespread genetic switches and toxicity resistance proteins for fluoride, Science, 335
  52. Yuan, 2014, Rice saliva gene family expression profiling sugar transport, Evolution J Integr Plant Biol, 559, 10.1111/jipb.12173 · DOI
  53. Tsai, 2011, Structural asymmetry in a trimeric Na betaine symporter from Corynebacterium glutamicum, Mol Biol, 407
  54. Faham, 2008, The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na sugar symport, Science, 321
  55. Yamashita, 2005, structure of a bacterial homologue of Na - dependent neurotransmitter transporters, Nature, 437
  56. Shaffer, 2009, Structure and mechanism of a Na - independent amino acid transporter, Science, 325
  57. Jardetzky, 1966, Simple allosteric model for membrane pumps, Nature, 211
  58. Chen, 2010, Sugar transporters for intercellular exchange and nutrition of pathogens, Nature, 468
  59. Marger, 1993, major superfamily of transmembrane facilitators that catalyse uniport symport antiport, Trends Biochem Sci, 18, 13, 10.1016/0968-0004(93)90081-W · DOI
  60. McLachlan, 1972, Gene duplication in carp muscle calcium binding protein, Nat New Biol, 240
  61. Ames, 1989, Reconstitution of periplasmic transport in inside - out membrane vesicles by, Biol Chem, 264
  62. Quistgaard, 2013, Low Metal - mediated crystallization of the xylose transporter XylE from Escherichia coli in three different crystal forms, Struct Biol, 184
  63. Morrison, 2011, Antiparallel EmrE exports drugs by exchanging between asymmetric structures, Nature, 481
  64. Hirai, 2003, Structural model for helix transporters belonging to the major facilitator superfamily, Bacteriol, 12, 185
  65. Lloris, 2014, von Why have small multidrug resistance proteins not evolved into fused internally duplicated structures, Mol Biol, 426
  66. Liu, 1998, In vitro disassembly and reassembly of an ABC transporter the histidine permease, Proc Natl Acad Sci USA, 95
  67. Gouaux, 2009, The molecular logic of sodium - coupled neurotransmitter transporters, Review Philos Trans Soc Lond Biol Sci, 364
  68. Mirza, 2006, Structural evidence for induced fit and a mechanism for sugar symport in LacY, EMBO J, 25, 1177, 10.1038/sj.emboj.7601028 · DOI
  69. Weber, 2013, Bräutigam The role of membrane transport in metabolic engineering of plant primary metabolism, Curr Opin Biotechnol, 24, 256, 10.1016/j.copbio.2012.09.010 · DOI
  70. Li, 2013, Eukaryotic resistance to fluoride toxicity mediated by a widespread family of fluoride export proteins, Proc Natl Acad Sci USA, 110
  71. Abramson, 2003, Structure and mechanism of the lactose permease of Escherichia coli, Science, 301
  72. Sand, 2003, Phenotypic characterization of overexpression or deletion of the Escherichia coli crcA cspE and crcB genes, Microbiology, 149
  73. 2013, Common folds and transport mechanisms of secondary active transporters, Annu Rev Biophys, 42
  74. Guan, 2007, Structural determination of wild - type lactose permease, Proc Natl Acad Sci USA, 15294, 10.1073/pnas.0707688104 · DOI
  75. Oldham, 2008, Structural insights into ABC transporter mechanism, Biol, 18, 726
  76. Perez, 2012, Alternating - access mechanism in conformationally asymmetric trimers of the betaine transporter, Nature, 490
  77. Madej, 2014, Functional architecture of MFS glucose transporters, Proc Natl Acad Sci USA, 111
  78. Ames, 1989, Reconstitution of periplasmic transport in inside - out membrane vesicles by, Biol Chem, 264
  79. Pebay, 2003, Structure of mitochondrial carrier in complex with carboxyatractyloside, Nature, 426
  80. Rapp, 2006, von Identification and evolution of dual topology membrane proteins, Nat Struct Mol Biol, 13, 112, 10.1038/nsmb1057 · DOI
  81. Schmitt, 2002, Structure and mechanism of ABC transporters, Biol, 12, 754
  82. Rapp, 2007, von Emulating membrane protein evolution by rational design, Science, 315
  83. Krishnamurthy, 2012, ray structures of LeuT in substrate - free outward - open and apo inward - open states, Nature, 481
  84. Liu, 1998, In vitro disassembly and reassembly of an ABC transporter the histidine permease, Proc Natl Acad Sci USA, 95
  85. Smirnova, 2009, Residues in the translocation site define the pKa for sugar binding to, Biochemistry, 8852, 10.1021/bi9011918 · DOI
  86. Madej, 2013, Evolutionary mix match with MFS transporters, Proc Natl Acad Sci USA, 110
  87. Tsai, 2011, Structural asymmetry in a trimeric Na betaine symporter from Corynebacterium glutamicum, Mol Biol, 407
  88. Sand, 2003, Phenotypic characterization of overexpression or deletion of the Escherichia coli crcA cspE and crcB genes, Microbiology, 149
  89. Yan, 2013, Structural advances for the major facilitator superfamily MFS transporters, Trends Biochem Sci, 151, 10.1016/j.tibs.2013.01.003 · DOI
  90. Kumar, 2014, Structure of sugar - bound, Proc Natl Acad Sci USA, 111
  91. Tanford, 1982, Simple model for the chemical potential change of a transported ion in active transport, Proc Natl Acad Sci USA, 2882, 10.1073/pnas.79.9.2882 · DOI
  92. Weber, 2013, Bräutigam The role of membrane transport in metabolic engineering of plant primary metabolism, Curr Opin Biotechnol, 24, 256, 10.1016/j.copbio.2012.09.010 · DOI
  93. Gouaux, 2009, The molecular logic of sodium - coupled neurotransmitter transporters, Review Philos Trans Soc Lond Biol Sci, 364
  94. Tanford, 1982, Simple model for the chemical potential change of a transported ion in active transport, Proc Natl Acad Sci USA, 2882, 10.1073/pnas.79.9.2882 · DOI
  95. Weyand, 2008, Structure and molecular mechanism of a nucleobase - cation - symport family transporter, Science, 1
  96. Yuan, 2013, Rice saliva SWEET family genes and their homologs in cellular organisms, Mol Plant, 665, 10.1093/mp/sst035 · DOI
  97. Mourez, 1998, In vitro interaction between components of the inner membrane complex of the maltose ABC transporter of Escherichia coli : modulation by, Mol Microbiol, 30, 353, 10.1046/j.1365-2958.1998.01070.x · DOI
  98. Xuan, 2013, Frommer Functional role of oligomerization for bacterial and plant SWEET sugar transporter family, Proc Natl Acad Sci USA, 110
  99. Kaback, 2011, The alternating access transport mechanism in, Biol, 239
  100. Yuan, 2010, The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution, Plant Cell, 22, 3164, 10.1105/tpc.110.078022 · DOI
  101. Smirnova, 2009, Residues in the translocation site define the pKa for sugar binding to, Biochemistry, 8852, 10.1021/bi9011918 · DOI
  102. Rapp, 2007, von Emulating membrane protein evolution by rational design, Science, 315
  103. Quistgaard, 2013, Low Metal - mediated crystallization of the xylose transporter XylE from Escherichia coli in three different crystal forms, Struct Biol, 184
  104. Duran, 2013, Meiler Inverted topologies in membrane proteins a mini, review Comput Struct Biotechnol
  105. Tzeng, 2010, Structural and functional analysis of transmembrane segment VI of the isoform of the Na exchanger, Biol Chem, 1
  106. Holland, 1999, Blight ABC adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans, Mol Biol, 293
  107. Xu, 2014, Structures of bacterial homologues of SWEET transporters in two distinct conformations, Nature nature, 10.1038/13670 · DOI
  108. Keller, 2013, Homologs of the yeast vesicle - associated protein are conserved in chloroplasts and cyanobacteria Front Plant, Sci, 467
  109. Tang, 2010, structure of the carnitine transporter and insights into the antiport mechanism, Nat Struct Mol Biol, 17, 492, 10.1038/nsmb.1788 · DOI
  110. Li, 2013, Eukaryotic resistance to fluoride toxicity mediated by a widespread family of fluoride export proteins, Proc Natl Acad Sci USA, 110
  111. Doerrler, 2013, New functions for the ancient DedA membrane protein family, Bacteriol, 195
  112. 2013, Common folds and transport mechanisms of secondary active transporters, Annu Rev Biophys, 42
  113. Hirai, 2003, Structural model for helix transporters belonging to the major facilitator superfamily, Bacteriol, 12, 185
  114. Yan, 2013, Structural advances for the major facilitator superfamily MFS transporters, Trends Biochem Sci, 151, 10.1016/j.tibs.2013.01.003 · DOI
  115. Tang, 2010, structure of the carnitine transporter and insights into the antiport mechanism, Nat Struct Mol Biol, 17, 492, 10.1038/nsmb.1788 · DOI
  116. Guan, 2006, Lessons from lactose permease, Annu Rev Biophys Biomol, 35
  117. Xu, 2014, Structures of bacterial homologues of SWEET transporters in two distinct conformations, Nature nature, 10.1038/13670 · DOI
  118. Chardon, 2013, fructose content is controlled by the vacuolar transporter SWEET in, Curr Biol, 17, 697, 10.1016/j.cub.2013.03.021 · DOI
  119. Chaptal, 2011, structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition, Proc Natl Acad Sci USA, 108
  120. Singh, 2007, Antidepressant binding site in a bacterial homologue of neurotransmitter transporters, Nature, 448
  121. Ressl, 2009, van Molecular basis of transport and regulation in the Na betaine symporter, Nature, 458
  122. Xuan, 2013, Frommer Functional role of oligomerization for bacterial and plant SWEET sugar transporter family, Proc Natl Acad Sci USA, 110
  123. Bordignon, 2010, The maltose ATP - binding cassette transporter in the st century towards a structural dynamic perspective on its mode of action, Mol Microbiol, 21, 77
  124. Cohn, 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, 10.1094/MPMI-06-14-0161-R · DOI
  125. Doerrler, 2013, New functions for the ancient DedA membrane protein family, Bacteriol, 195
  126. Kaback, 2011, The alternating access transport mechanism in, Biol, 239
  127. Marger, 1993, major superfamily of transmembrane facilitators that catalyse uniport symport antiport, Trends Biochem Sci, 18, 13, 10.1016/0968-0004(93)90081-W · DOI
  128. Cohn, 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, 10.1094/MPMI-06-14-0161-R · DOI
  129. Perez, 2013, Mechanistic aspects of sodium - binding sites in LeuT - like fold symporters, Biol Chem, 394
  130. Baker, 2012, Breaker Widespread genetic switches and toxicity resistance proteins for fluoride, Science, 335
  131. Yuan, 2014, Rice saliva gene family expression profiling sugar transport, Evolution J Integr Plant Biol, 559, 10.1111/jipb.12173 · DOI
  132. Henderson, 2012, Structural biology Bundles of insights into sugar transporters, Nature, 490
  133. Jardetzky, 1966, Simple allosteric model for membrane pumps, Nature, 211
  134. Wisedchaisri, 2014, Proton - coupled sugar transport in the prototypical major facilitator superfamily protein, Nat Commun, 4521, 10.1038/ncomms5521 · DOI
  135. Mourez, 1998, In vitro interaction between components of the inner membrane complex of the maltose ABC transporter of Escherichia coli : modulation by, Mol Microbiol, 30, 353, 10.1046/j.1365-2958.1998.01070.x · DOI
  136. Smirnova, 2013, replacements for tightly interacting Gly pairs in LacY stabilize an outward - facing conformation, Proc Natl Acad Sci USA, 110
  137. Abramson, 2003, Structure and mechanism of the lactose permease of Escherichia coli, Science, 301
  138. Sikdar, 2013, Multiple envelope stress response pathways are activated in an Escherichia coli strain with mutations in two members of the DedA membrane protein family, Bacteriol, 195
  139. Lee, 2009, Structural and functional analysis of transmembrane XI of the isoform of the Na exchanger, Biol Chem, 1
  140. Guo, 2014, a facilitative transporter mediates fructose transport across the tonoplast of Arabidopsis roots and leaves, Plant Physiol, 17, 164
  141. Sikdar, 2013, Multiple envelope stress response pathways are activated in an Escherichia coli strain with mutations in two members of the DedA membrane protein family, Bacteriol, 195
  142. Guo, 2014, a facilitative transporter mediates fructose transport across the tonoplast of Arabidopsis roots and leaves, Plant Physiol, 17, 164
  143. Lee, 2009, Structural and functional analysis of transmembrane XI of the isoform of the Na exchanger, Biol Chem, 1
  144. Koshy, 2013, Structural evidence for functional lipid interactions in the betaine transporter, EMBO J, 3096, 10.1038/emboj.2013.226 · DOI
  145. Chaptal, 2011, structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition, Proc Natl Acad Sci USA, 108
  146. Khafizov, 2010, study of the evolution of inverted - topology repeats from LeuT - fold transporters using, Biochemistry, 49
  147. Morrison, 2011, Antiparallel EmrE exports drugs by exchanging between asymmetric structures, Nature, 481
  148. Duran, 2013, Meiler Inverted topologies in membrane proteins a mini, review Comput Struct Biotechnol
  149. Smirnova, 2013, replacements for tightly interacting Gly pairs in LacY stabilize an outward - facing conformation, Proc Natl Acad Sci USA, 110
  150. Krishnamurthy, 2012, ray structures of LeuT in substrate - free outward - open and apo inward - open states, Nature, 481
  151. Guan, 2007, Structural determination of wild - type lactose permease, Proc Natl Acad Sci USA, 15294, 10.1073/pnas.0707688104 · DOI
  152. Keller, 2013, Homologs of the yeast vesicle - associated protein are conserved in chloroplasts and cyanobacteria Front Plant, Sci, 467
  153. Yuan, 2013, Rice saliva SWEET family genes and their homologs in cellular organisms, Mol Plant, 665, 10.1093/mp/sst035 · DOI
  154. Horio, 1988, dependent transport of vinblastine in vesicles from human multidrug - resistant cells, Proc Natl Acad Sci USA, 85

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Metadata

Authors
Keller, R., Ziegler, C., & Schneider, D.
Venue
Biological Chemistry
Publisher
Walter de Gruyter GmbH
Published
2014-12-01
Volume
395
Issue
12
Pages
1379-1388
ISSN
  • 1437-4315
  • 1431-6730
DOI
10.1515/hsz-2014-0224
Cited by
42
References
0

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