Borate Transporters and SLC4 Bicarbonate Transporters Share Key Functional Properties

Borate transporters are membrane transport proteins that regulate intracellular borate levels. In plants, borate is a micronutrient essential for growth but is toxic in excess, while in yeast, borate is unnecessary for growth and borate export confers tolerance. Borate transporters share structural...

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Main Authors: Jean L. Beltran, Lila G. McGrath, Sophia Caruso, Richara K. Bain, Claire E. Hendrix, Hana Kamran, Hartlee G. Johnston, Rebecca M. Collings, Menkara-Chinua N. Henry, Tsega-Ab L. Abera, Valeria A. Donoso, Erin C. Carriker, Bryan H. Thurtle-Schmidt
Format: Article
Language:English
Published: MDPI AG 2023-02-01
Series:Membranes
Subjects:
Online Access:https://www.mdpi.com/2077-0375/13/2/235
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author Jean L. Beltran
Lila G. McGrath
Sophia Caruso
Richara K. Bain
Claire E. Hendrix
Hana Kamran
Hartlee G. Johnston
Rebecca M. Collings
Menkara-Chinua N. Henry
Tsega-Ab L. Abera
Valeria A. Donoso
Erin C. Carriker
Bryan H. Thurtle-Schmidt
author_facet Jean L. Beltran
Lila G. McGrath
Sophia Caruso
Richara K. Bain
Claire E. Hendrix
Hana Kamran
Hartlee G. Johnston
Rebecca M. Collings
Menkara-Chinua N. Henry
Tsega-Ab L. Abera
Valeria A. Donoso
Erin C. Carriker
Bryan H. Thurtle-Schmidt
author_sort Jean L. Beltran
collection DOAJ
description Borate transporters are membrane transport proteins that regulate intracellular borate levels. In plants, borate is a micronutrient essential for growth but is toxic in excess, while in yeast, borate is unnecessary for growth and borate export confers tolerance. Borate transporters share structural homology with human bicarbonate transporters in the SLC4 family despite low sequence identity and differences in transported solutes. Here, we characterize the <i>S. cerevisiae</i> borate transporter Bor1p and examine whether key biochemical features of SLC4 transporters extend to borate transporters. We show that borate transporters and SLC4 transporters share multiple properties, including lipid-promoted dimerization, sensitivity to stilbene disulfonate-derived inhibitors, and a requirement for an acidic residue at the solute binding site. We also identify several amino acids critical for Bor1p function and show that disease-causing mutations in human SLC4A1 will eliminate in vivo function when their homologous mutations are introduced in Bor1p. Our data help elucidate mechanistic features of Bor1p and reveal significant functional properties shared between borate transporters and SLC4 transporters.
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spelling doaj.art-9a4532c27f724cf5aadd6192b2ee41ef2023-11-16T22:03:10ZengMDPI AGMembranes2077-03752023-02-0113223510.3390/membranes13020235Borate Transporters and SLC4 Bicarbonate Transporters Share Key Functional PropertiesJean L. Beltran0Lila G. McGrath1Sophia Caruso2Richara K. Bain3Claire E. Hendrix4Hana Kamran5Hartlee G. Johnston6Rebecca M. Collings7Menkara-Chinua N. Henry8Tsega-Ab L. Abera9Valeria A. Donoso10Erin C. Carriker11Bryan H. Thurtle-Schmidt12Department of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USADepartment of Biology, Davidson College, Davidson, NC 28035, USABorate transporters are membrane transport proteins that regulate intracellular borate levels. In plants, borate is a micronutrient essential for growth but is toxic in excess, while in yeast, borate is unnecessary for growth and borate export confers tolerance. Borate transporters share structural homology with human bicarbonate transporters in the SLC4 family despite low sequence identity and differences in transported solutes. Here, we characterize the <i>S. cerevisiae</i> borate transporter Bor1p and examine whether key biochemical features of SLC4 transporters extend to borate transporters. We show that borate transporters and SLC4 transporters share multiple properties, including lipid-promoted dimerization, sensitivity to stilbene disulfonate-derived inhibitors, and a requirement for an acidic residue at the solute binding site. We also identify several amino acids critical for Bor1p function and show that disease-causing mutations in human SLC4A1 will eliminate in vivo function when their homologous mutations are introduced in Bor1p. Our data help elucidate mechanistic features of Bor1p and reveal significant functional properties shared between borate transporters and SLC4 transporters.https://www.mdpi.com/2077-0375/13/2/235membrane transportersprotein–lipid interactionsBor1SLC4A1yeast
spellingShingle Jean L. Beltran
Lila G. McGrath
Sophia Caruso
Richara K. Bain
Claire E. Hendrix
Hana Kamran
Hartlee G. Johnston
Rebecca M. Collings
Menkara-Chinua N. Henry
Tsega-Ab L. Abera
Valeria A. Donoso
Erin C. Carriker
Bryan H. Thurtle-Schmidt
Borate Transporters and SLC4 Bicarbonate Transporters Share Key Functional Properties
Membranes
membrane transporters
protein–lipid interactions
Bor1
SLC4A1
yeast
title Borate Transporters and SLC4 Bicarbonate Transporters Share Key Functional Properties
title_full Borate Transporters and SLC4 Bicarbonate Transporters Share Key Functional Properties
title_fullStr Borate Transporters and SLC4 Bicarbonate Transporters Share Key Functional Properties
title_full_unstemmed Borate Transporters and SLC4 Bicarbonate Transporters Share Key Functional Properties
title_short Borate Transporters and SLC4 Bicarbonate Transporters Share Key Functional Properties
title_sort borate transporters and slc4 bicarbonate transporters share key functional properties
topic membrane transporters
protein–lipid interactions
Bor1
SLC4A1
yeast
url https://www.mdpi.com/2077-0375/13/2/235
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