Zebrafish Slc5a12 encodes an electroneutral sodium monocarboxylate transporter (SMCTn): A comparison with the electrogenic SMCT (SMCTe/Slc5a8)

Consuelo Plata, Caroline R. Sussman, Aleksandra Sindić, Jennifer O. Liang, David B. Mount, Zara M. Josephs, Min Hwang Chang, Michael F Romero

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Abstract

We have identified and characterized two different sodium-coupled monocarboxylate cotransporters (SMCT) from zebrafish (Danio rerio), electrogenic (zSMCTe) and electroneutral (zSMCTn). zSMCTn is the 12th member of the zebrafish Slc5 gene family (zSlc5a12). Both zSMCT sequences have ∼50% homology to human SLC5A8 (hSMCT). Transport function and kinetics were measured in Xenopus oocytes injected with zSMCT cRNAs by measurement of intracellular Na+ concentration ([Na+]i) and membrane potential. Both zSMCTs oocytes increased [Na+]i with addition of monocarboxylates (MC) such as lactate, pyruvate, nicotinate, and butyrate. By using two electrode voltage clamp experiments, we measured currents elicited from zSMCTe after MC addition. MC-elicited currents from zSMCTe were similar to hSMCT currents. In contrast, we found no significant MC-elicited current in either zSMCTn or control oocytes. Kinetic data show that zSMCTe has a higher affinity for lactate, nicotinate, and pyruvate (Km L-lactate = 0.17 ± 0.02 mM, Km nicotinate = 0.54 ± 0.12 mM at -150 mV) than zSMCTn (Km L-lactate = 1.81 ± 0.19 mM, Km nicotinate = 23.68 ± 4.88 mM). In situ hybridization showed that 1-, 3-, and 5-day-old zebrafish embryos abundantly express both zSMCTs in the brain, eyes, intestine, and kidney. Within the kidney, zSMCTn mRNA is expressed in pronephric tubules, whereas zSMCTe mRNA is more distal in pronephric ducts. zSMCTn is expressed in exocrine pancreas, but zSMCTe is not. Roles for Na +-coupled monocarboxylate cotransporters have not been described for the brain or eye. In summary, zSMCTe is the zebrafish SLC5A8 ortholog, and zSMCTn is a novel, electroneutral SMCT (zSlc5a12). Slc5a12 in higher vertebrates is likely responsible for the electroneutral Na+/lactate cotransport reported in mammalian and amphibian kidneys.

Original languageEnglish (US)
Pages (from-to)11996-12009
Number of pages14
JournalJournal of Biological Chemistry
Volume282
Issue number16
DOIs
StatePublished - Apr 20 2007

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Zebrafish
Lactic Acid
Sodium
Oocytes
Niacin
Pyruvic Acid
Kidney
Brain
Exocrine Pancreas
Complementary RNA
Messenger RNA
Kinetics
Butyrates
Clamping devices
Amphibians
Xenopus
Membrane Potentials
Ducts
Intestines
In Situ Hybridization

ASJC Scopus subject areas

  • Biochemistry

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Zebrafish Slc5a12 encodes an electroneutral sodium monocarboxylate transporter (SMCTn) : A comparison with the electrogenic SMCT (SMCTe/Slc5a8). / Plata, Consuelo; Sussman, Caroline R.; Sindić, Aleksandra; Liang, Jennifer O.; Mount, David B.; Josephs, Zara M.; Chang, Min Hwang; Romero, Michael F.

In: Journal of Biological Chemistry, Vol. 282, No. 16, 20.04.2007, p. 11996-12009.

Research output: Contribution to journalArticle

Plata, Consuelo ; Sussman, Caroline R. ; Sindić, Aleksandra ; Liang, Jennifer O. ; Mount, David B. ; Josephs, Zara M. ; Chang, Min Hwang ; Romero, Michael F. / Zebrafish Slc5a12 encodes an electroneutral sodium monocarboxylate transporter (SMCTn) : A comparison with the electrogenic SMCT (SMCTe/Slc5a8). In: Journal of Biological Chemistry. 2007 ; Vol. 282, No. 16. pp. 11996-12009.
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abstract = "We have identified and characterized two different sodium-coupled monocarboxylate cotransporters (SMCT) from zebrafish (Danio rerio), electrogenic (zSMCTe) and electroneutral (zSMCTn). zSMCTn is the 12th member of the zebrafish Slc5 gene family (zSlc5a12). Both zSMCT sequences have ∼50{\%} homology to human SLC5A8 (hSMCT). Transport function and kinetics were measured in Xenopus oocytes injected with zSMCT cRNAs by measurement of intracellular Na+ concentration ([Na+]i) and membrane potential. Both zSMCTs oocytes increased [Na+]i with addition of monocarboxylates (MC) such as lactate, pyruvate, nicotinate, and butyrate. By using two electrode voltage clamp experiments, we measured currents elicited from zSMCTe after MC addition. MC-elicited currents from zSMCTe were similar to hSMCT currents. In contrast, we found no significant MC-elicited current in either zSMCTn or control oocytes. Kinetic data show that zSMCTe has a higher affinity for lactate, nicotinate, and pyruvate (Km L-lactate = 0.17 ± 0.02 mM, Km nicotinate = 0.54 ± 0.12 mM at -150 mV) than zSMCTn (Km L-lactate = 1.81 ± 0.19 mM, Km nicotinate = 23.68 ± 4.88 mM). In situ hybridization showed that 1-, 3-, and 5-day-old zebrafish embryos abundantly express both zSMCTs in the brain, eyes, intestine, and kidney. Within the kidney, zSMCTn mRNA is expressed in pronephric tubules, whereas zSMCTe mRNA is more distal in pronephric ducts. zSMCTn is expressed in exocrine pancreas, but zSMCTe is not. Roles for Na +-coupled monocarboxylate cotransporters have not been described for the brain or eye. In summary, zSMCTe is the zebrafish SLC5A8 ortholog, and zSMCTn is a novel, electroneutral SMCT (zSlc5a12). Slc5a12 in higher vertebrates is likely responsible for the electroneutral Na+/lactate cotransport reported in mammalian and amphibian kidneys.",
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T1 - Zebrafish Slc5a12 encodes an electroneutral sodium monocarboxylate transporter (SMCTn)

T2 - A comparison with the electrogenic SMCT (SMCTe/Slc5a8)

AU - Plata, Consuelo

AU - Sussman, Caroline R.

AU - Sindić, Aleksandra

AU - Liang, Jennifer O.

AU - Mount, David B.

AU - Josephs, Zara M.

AU - Chang, Min Hwang

AU - Romero, Michael F

PY - 2007/4/20

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N2 - We have identified and characterized two different sodium-coupled monocarboxylate cotransporters (SMCT) from zebrafish (Danio rerio), electrogenic (zSMCTe) and electroneutral (zSMCTn). zSMCTn is the 12th member of the zebrafish Slc5 gene family (zSlc5a12). Both zSMCT sequences have ∼50% homology to human SLC5A8 (hSMCT). Transport function and kinetics were measured in Xenopus oocytes injected with zSMCT cRNAs by measurement of intracellular Na+ concentration ([Na+]i) and membrane potential. Both zSMCTs oocytes increased [Na+]i with addition of monocarboxylates (MC) such as lactate, pyruvate, nicotinate, and butyrate. By using two electrode voltage clamp experiments, we measured currents elicited from zSMCTe after MC addition. MC-elicited currents from zSMCTe were similar to hSMCT currents. In contrast, we found no significant MC-elicited current in either zSMCTn or control oocytes. Kinetic data show that zSMCTe has a higher affinity for lactate, nicotinate, and pyruvate (Km L-lactate = 0.17 ± 0.02 mM, Km nicotinate = 0.54 ± 0.12 mM at -150 mV) than zSMCTn (Km L-lactate = 1.81 ± 0.19 mM, Km nicotinate = 23.68 ± 4.88 mM). In situ hybridization showed that 1-, 3-, and 5-day-old zebrafish embryos abundantly express both zSMCTs in the brain, eyes, intestine, and kidney. Within the kidney, zSMCTn mRNA is expressed in pronephric tubules, whereas zSMCTe mRNA is more distal in pronephric ducts. zSMCTn is expressed in exocrine pancreas, but zSMCTe is not. Roles for Na +-coupled monocarboxylate cotransporters have not been described for the brain or eye. In summary, zSMCTe is the zebrafish SLC5A8 ortholog, and zSMCTn is a novel, electroneutral SMCT (zSlc5a12). Slc5a12 in higher vertebrates is likely responsible for the electroneutral Na+/lactate cotransport reported in mammalian and amphibian kidneys.

AB - We have identified and characterized two different sodium-coupled monocarboxylate cotransporters (SMCT) from zebrafish (Danio rerio), electrogenic (zSMCTe) and electroneutral (zSMCTn). zSMCTn is the 12th member of the zebrafish Slc5 gene family (zSlc5a12). Both zSMCT sequences have ∼50% homology to human SLC5A8 (hSMCT). Transport function and kinetics were measured in Xenopus oocytes injected with zSMCT cRNAs by measurement of intracellular Na+ concentration ([Na+]i) and membrane potential. Both zSMCTs oocytes increased [Na+]i with addition of monocarboxylates (MC) such as lactate, pyruvate, nicotinate, and butyrate. By using two electrode voltage clamp experiments, we measured currents elicited from zSMCTe after MC addition. MC-elicited currents from zSMCTe were similar to hSMCT currents. In contrast, we found no significant MC-elicited current in either zSMCTn or control oocytes. Kinetic data show that zSMCTe has a higher affinity for lactate, nicotinate, and pyruvate (Km L-lactate = 0.17 ± 0.02 mM, Km nicotinate = 0.54 ± 0.12 mM at -150 mV) than zSMCTn (Km L-lactate = 1.81 ± 0.19 mM, Km nicotinate = 23.68 ± 4.88 mM). In situ hybridization showed that 1-, 3-, and 5-day-old zebrafish embryos abundantly express both zSMCTs in the brain, eyes, intestine, and kidney. Within the kidney, zSMCTn mRNA is expressed in pronephric tubules, whereas zSMCTe mRNA is more distal in pronephric ducts. zSMCTn is expressed in exocrine pancreas, but zSMCTe is not. Roles for Na +-coupled monocarboxylate cotransporters have not been described for the brain or eye. In summary, zSMCTe is the zebrafish SLC5A8 ortholog, and zSMCTn is a novel, electroneutral SMCT (zSlc5a12). Slc5a12 in higher vertebrates is likely responsible for the electroneutral Na+/lactate cotransport reported in mammalian and amphibian kidneys.

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