Structures suggest a mechanism for energy coupling by a family of organic anion transporters

Jonathan B. Leano; Samir Batarni; Jacob Eriksen; Narinobu Juge; John E. Pak; Tomomi Kimura-Someya; Yaneth Robles-Colmenares; Yoshinori Moriyama; Robert M. Stroud; Robert H. Edwards

doi:10.1371/journal.pbio.3000260

Structures suggest a mechanism for energy coupling by a family of organic anion transporters

Jonathan B. Leano, Samir Batarni, Jacob Eriksen, Narinobu Juge, John E. Pak, Tomomi Kimura-Someya, Yaneth Robles-Colmenares, Yoshinori Moriyama, Robert M. Stroud, Robert H. Edwards

Research output: Contribution to journal › Article › peer-review

23 Citations (Scopus)

Abstract

Members of the solute carrier 17 (SLC17) family use divergent mechanisms to concentrate organic anions. Membrane potential drives uptake of the principal excitatory neurotransmitter glutamate into synaptic vesicles, whereas closely related proteins use proton cotransport to drive efflux from the lysosome. To delineate the divergent features of ionic coupling by the SLC17 family, we determined the structure of Escherichia coli D-galactonate/H⁺ symporter D-galactonate transporter (DgoT) in 2 states: One open to the cytoplasmic side and the other open to the periplasmic side with substrate bound. The structures suggest a mechanism that couples H⁺ flux to substrate recognition. A transition in the role of H⁺ from flux coupling to allostery may confer regulation by trafficking to and from the plasma membrane.

Original language	English
Article number	e3000260
Journal	PLoS biology
Volume	17
Issue number	5
DOIs	https://doi.org/10.1371/journal.pbio.3000260
Publication status	Published - May 2019
Externally published	Yes

ASJC Scopus subject areas

Neuroscience(all)
Biochemistry, Genetics and Molecular Biology(all)
Immunology and Microbiology(all)
Agricultural and Biological Sciences(all)

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abstract = "Members of the solute carrier 17 (SLC17) family use divergent mechanisms to concentrate organic anions. Membrane potential drives uptake of the principal excitatory neurotransmitter glutamate into synaptic vesicles, whereas closely related proteins use proton cotransport to drive efflux from the lysosome. To delineate the divergent features of ionic coupling by the SLC17 family, we determined the structure of Escherichia coli D-galactonate/H+ symporter D-galactonate transporter (DgoT) in 2 states: One open to the cytoplasmic side and the other open to the periplasmic side with substrate bound. The structures suggest a mechanism that couples H+ flux to substrate recognition. A transition in the role of H+ from flux coupling to allostery may confer regulation by trafficking to and from the plasma membrane.",

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note = "Funding Information: National Institutes of Health: R37 MH50712 to RHE and GM24485 to RMS; R01 NS089713 to RHE and RMS; R37 GM024485-37S1 supplement to JBL. JE was supported by a postdoctoral fellowship from the Lundbeck Foundation (R77-A6780). Beamline 8.3.1 at the Advanced Light Source is operated by the University of California Office of the President, Multicampus Research Programs and Initiatives grant MR-15-328599. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: {\textcopyright} 2019, Public Library of Science. All rights reserved.",

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AU - Batarni, Samir

AU - Eriksen, Jacob

AU - Juge, Narinobu

AU - Pak, John E.

AU - Kimura-Someya, Tomomi

AU - Robles-Colmenares, Yaneth

AU - Moriyama, Yoshinori

AU - Stroud, Robert M.

AU - Edwards, Robert H.

N1 - Funding Information: National Institutes of Health: R37 MH50712 to RHE and GM24485 to RMS; R01 NS089713 to RHE and RMS; R37 GM024485-37S1 supplement to JBL. JE was supported by a postdoctoral fellowship from the Lundbeck Foundation (R77-A6780). Beamline 8.3.1 at the Advanced Light Source is operated by the University of California Office of the President, Multicampus Research Programs and Initiatives grant MR-15-328599. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: © 2019, Public Library of Science. All rights reserved.

PY - 2019/5

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Structures suggest a mechanism for energy coupling by a family of organic anion transporters

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