Internal Gene Duplication in the Evolution of Prokaryotic Transmembrane Proteins

Shimizu, Toshio; Mitsuke, Hironori; Noto, Keisuke; Arai, Masafumi

doi:10.1016/j.jmb.2004.03.048

Cited by 37 publications

(30 citation statements)

References 42 publications

(36 reference statements)

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“…In contrast to highly conserved and clearly orthologous NTTs, NATs changed rapidly during evolution. NAT plasticity and NTT conservation are essential in evolution and imply different selection mechanisms (27). Indeed, the NTT group is stabilized by adaptation to particular substrates (neurotransmitters) and electrochemical homeostasis of the neuronal environ.…”

Section: Discussionmentioning

confidence: 99%

Ancestry and progeny of nutrient amino acid transporters

Boudko

Kohn

Meleshkevitch

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

132

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The biosynthesis of structural and signaling molecules depends on intracellular concentrations of essential amino acids, which are maintained by a specific system of plasma membrane transporters. We identify a unique population of nutrient amino acid transporters (NATs) within the sodium-neurotransmitter symporter family and have characterized a member of the NAT subfamily from the larval midgut of the Yellow Fever vector mosquito, Aedes aegypti (aeAAT1, AAR08269), which primarily supplies phenylalanine, an essential substrate for the synthesis of neuronal and cuticular catecholamines. Further analysis suggests that NATs constitute a comprehensive transport metabolon for the epithelial uptake and redistribution of essential amino acids including precursors of several neurotransmitters. In contrast to the highly conserved subfamily of orthologous neurotransmitter transporters, lineagespecific, paralogous NATs undergo rapid gene multiplication͞ substitution that enables a high degree of evolutionary plasticity of nutrient amino acid uptake mechanisms and facilitates environmental and nutrient adaptations of organisms. These findings provide a unique model for understanding the molecular mechanisms, physiology, and evolution of amino acid and neurotransmitter transport systems and imply that monoamine and GABA transporters evolved by selection and conservation of earlier neuronal NATs.

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Section: Discussionmentioning

confidence: 99%

Ancestry and progeny of nutrient amino acid transporters

Boudko

Kohn

Meleshkevitch

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

132

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“…6D). Therefore, the transport activity of psD and anaD reflecting eight conserved ␤-strands (31) leads to the hypothesis that ␤-barrel proteins, similar to helical proteins (44), have evolved from a minimal structural unit. Such minimal structure might be represented by toxins containing two or four segments and forming a multimeric ␤-barrel channel (45) or by the smallest monomeric ␤-barrel membrane proteins containing eight ␤-strands (45).…”

Section: Fig 5 Analysis Of the C-terminal Region Of The ␤-Barrel Prmentioning

confidence: 99%

The Evolutionarily Related β-Barrel Polypeptide Transporters from Pisum sativum and Nostoc PCC7120 Contain Two Distinct Functional Domains

Ertel

Mirus

Bredemeier

et al. 2005

Journal of Biological Chemistry

118

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Several ␤-barrel-type channels are involved in the translocation or assembly of outer membrane proteins of bacteria or endosymbiotically derived organelles. Here we analyzed the functional units of the ␤-barrel polypeptide transporter Toc75 (translocon in outer envelope of chloroplasts) of the outer envelope of chloroplasts and of a protein, alr2269, from Nostoc PCC7120 with homology to Toc75, both proteins having a similar domain organization. We demonstrated that the N-terminal region functions as a recognition and complex assembly unit, whereas the C terminus forms the ␤-barrel-type pore. The pore region is, in turn, modulated by the N terminus of the proteins. The protein from Nostoc PCC7120, which shares a common ancestor with Toc75, is able to recognize precursor proteins destined for chloroplasts. In contrast, the recognition of peripheral translocon subunits by Toc75 is a novel feature acquired through evolution.␤-barrel-type channels are involved in the translocation of polypeptides (1), the assembly of proteins in the outer membrane of endosymbiotic organelles (2-4), or in the assembly of proteins in the outer membrane of bacteria (5, 6). These proteins belong to one class, which can be termed polypeptide-transporting ␤-barrel channels (2, 4, 7). Four proteins are in the focus of recent investigation, namely the bacterial outer membrane proteins Omp85 and ShlB, the mitochondrial outer membrane protein Tob55/Sam50, and the chloroplast outer envelope protein Toc75.ShlB is an outer membrane protein involved in the secretion of hemolysins or adhesins in various Gram-negative pathogens (8, 9). Omp85 is an essential component for outer membrane biogenesis in Neisseria meningitidis that might have two functions: the assembly of outer membrane proteins (5) and the translocation of lipids (10). Recently, it was discussed that the effect on lipid transfer by Omp85 depletion might be indirect and explained by an assembly defect of the required outer membrane protein, suggesting a function of Omp85 in outer membrane protein assembly only (11). As for ShlB, a ␤-barrel transmembrane structure was suggested for Omp85 (5). Recently, a new polypeptide-transporting protein was identified in the outer membrane of mitochondria and termed Sam50 (3), Tob55 (2), or mitochondrial Omp85 homologue (4). This protein facilitates the assembly of proteins into the outer membrane of mitochondria. Tob55/Sam50 is found in a larger complex with Mas37 (3, 12) and Tob38/Sam35 (13-15).The fourth investigated ␤-barrel-type polypeptide transporter is the 75-kDa subunit of the translocon of the outer envelope of chloroplasts, Toc75. Toc75 forms a complex with Toc34, Toc64, and Toc159 (16). In contrast to the other identified polypeptide transporters, such as Omp85, the translocation of proteins through Toc75 requires the action of assisting proteins, such as Toc159 (17), but still Toc75 seems to contain a preprotein-binding site as determined by electrophysiological measurements (1). Topological modeling of Toc75 from Pisum sativum (18) or T...

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“…The consistency between the structural model and the experimental data supports this conformational switching mechanism of transport. Moreover, because sequence analysis reveals the presence of repeating elements in other transporter families (22,23), the exchange of alternate conformations between internal repeats may well prove to be a transport mechanism of quite general relevance.…”

mentioning

confidence: 99%

Mechanism for alternating access in neurotransmitter transporters

Forrest

Zhang

Jacobs

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

358

483

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Crystal structures of LeuT, a bacterial homologue of mammalian neurotransmitter transporters, show a molecule of bound substrate that is essentially exposed to the extracellular space but occluded from the cytoplasm. Thus, there must exist an alternate conformation for LeuT in which the substrate is accessible to the cytoplasm and a corresponding mechanism that switches accessibility from one side of the membrane to the other. Here, we identify the cytoplasmic accessibility pathway of the alternate conformation in a mammalian serotonin transporter (SERT) (a member of the same transporter family as LeuT). We also propose a model for the cytoplasmic-facing state that exploits the internal pseudosymmetry observed in the crystal structure. LeuT contains two structurally similar repeats (TMs1-5 and TMs 6 -10) that are inverted with respect to the plane of the membrane. The conformational differences between them result in the formation of the extracellular pathway. Our model for the cytoplasm-facing state exchanges the conformations of the two repeats and thus exposes the substrate and ion-binding sites to the cytoplasm. The conformational change that connects the two states primarily involves the tilting of a 4-helix bundle composed of transmembrane helices 1, 2, 6, and 7. Switching the tilt angle of this bundle is essentially equivalent to switching the conformation of the two repeats. Extensive mutagenesis of SERT and accessibility measurements, using cysteine reagents, are accommodated by our model. These observations may be of relevance to other transporter families, many of which contain internal inverted repeats.alternating access mechanism ͉ neurotransmitter:sodium symporters ͉ serotonin ͉ structural modeling ͉ structural repeats

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Internal Gene Duplication in the Evolution of Prokaryotic Transmembrane Proteins

Cited by 37 publications

References 42 publications

Ancestry and progeny of nutrient amino acid transporters

Ancestry and progeny of nutrient amino acid transporters

The Evolutionarily Related β-Barrel Polypeptide Transporters from Pisum sativum and Nostoc PCC7120 Contain Two Distinct Functional Domains

Mechanism for alternating access in neurotransmitter transporters

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