Lactate transport by rainbow trout white muscle: Kinetic characteristics and sensitivity to inhibitors

Yuxiang Wang, Pamela M. Wright, George J F Heigenhauser, Chris M. Wood

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

This study used an isolated-perfused tail-trunk preparation of rainbow trout to examine the uptake and release of lactate (Lac) and metabolic protons (ΔH(m)/+) in resting and exercised fish white muscle. In exercised muscle, L(+)-Lac efflux was inhibited (~40%) by 5 mM α-cyano-4- hydroxycinnamate (CIN), but not by 0.5 mM 4-acetamido-4'- isothiocyanostilbene-2,2'-disulfonic acid (SITS) or 0.1 mM amiloride. These results suggest that Lac release occurs through a Lac--H+ symport and the free diffusion of lactic acid (HLac) or Lac, but not via the Lac-/HCO3- Cl- antiporter. Lac efflux was accompanied by AH(m)/+ influx in all treatments, and increased ΔH(m)/+ influx occurred after SITS treatment. In resting muscle, Lac uptake rates were greater than Lac efflux rates in the postexercise preparation. L-Lac influx exhibited partial saturation kinetics, whereas D(-)-Lac influx was linearly related to its extracellular concentration (0-32 mM). At 16 mM extracellular L-Lac, with a negligible transmembrane L-HLac gradient and an outwardly directed net driving force on L-Lac, CIN, and SITS reduced net L-Lac uptake by 75 and 45%, respectively. At 16 mM extracellular concentration, D-Lac influx was 64% of the net L-Lac influx. These results suggest that in trout muscle at 16 mM extracellular L- Lac, the Lac--H+ symport accounts for 30-36%, the Lac-/HCO3-Cl- antiport for 39-45%, and diffusion for 19-25% of uptake, although the latter is probably overestimated and the former underestimated for methodological reasons. Net L-Lac efflux was not affected by extracellular D-Lac concentration and/or D-Lac influx, implying the existence of a concurrent L- Lac efflux during L-Lac influx. The D-Lac influx kinetics data indicated that the Lac-/HCO3/- antiport was not saturable in the extracellular D-Lac concentration range of 0-32 mM. This study clearly demonstrates the involvement of carrier-mediated transport in transmembrane Lac movement in fish muscle and supports the 'active lactate retention' mechanism proposed by Turner and Wood (J. Exp. Biol. 105: 395-401, 1983).

Original languageEnglish
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume272
Issue number5 41-5
StatePublished - Jun 19 1997

Fingerprint

Oncorhynchus mykiss
Lactic Acid
Muscles
Ion Transport
4-Acetamido-4'-isothiocyanatostilbene-2,2'-disulfonic Acid

Keywords

  • α-cyano-4- hydroxycinnamate
  • 4-acetamido-4'- isothiocyanostilbene-2,2'-disulfonic acid
  • Amiloride
  • Exercise
  • Kinetics
  • Metabolic hydrogen ion
  • Perfusion

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Lactate transport by rainbow trout white muscle : Kinetic characteristics and sensitivity to inhibitors. / Wang, Yuxiang; Wright, Pamela M.; Heigenhauser, George J F; Wood, Chris M.

In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology, Vol. 272, No. 5 41-5, 19.06.1997.

Research output: Contribution to journalArticle

@article{739e7982711f4e0884bc0dbc4127449c,
title = "Lactate transport by rainbow trout white muscle: Kinetic characteristics and sensitivity to inhibitors",
abstract = "This study used an isolated-perfused tail-trunk preparation of rainbow trout to examine the uptake and release of lactate (Lac) and metabolic protons (ΔH(m)/+) in resting and exercised fish white muscle. In exercised muscle, L(+)-Lac efflux was inhibited (~40{\%}) by 5 mM α-cyano-4- hydroxycinnamate (CIN), but not by 0.5 mM 4-acetamido-4'- isothiocyanostilbene-2,2'-disulfonic acid (SITS) or 0.1 mM amiloride. These results suggest that Lac release occurs through a Lac--H+ symport and the free diffusion of lactic acid (HLac) or Lac, but not via the Lac-/HCO3- Cl- antiporter. Lac efflux was accompanied by AH(m)/+ influx in all treatments, and increased ΔH(m)/+ influx occurred after SITS treatment. In resting muscle, Lac uptake rates were greater than Lac efflux rates in the postexercise preparation. L-Lac influx exhibited partial saturation kinetics, whereas D(-)-Lac influx was linearly related to its extracellular concentration (0-32 mM). At 16 mM extracellular L-Lac, with a negligible transmembrane L-HLac gradient and an outwardly directed net driving force on L-Lac, CIN, and SITS reduced net L-Lac uptake by 75 and 45{\%}, respectively. At 16 mM extracellular concentration, D-Lac influx was 64{\%} of the net L-Lac influx. These results suggest that in trout muscle at 16 mM extracellular L- Lac, the Lac--H+ symport accounts for 30-36{\%}, the Lac-/HCO3-Cl- antiport for 39-45{\%}, and diffusion for 19-25{\%} of uptake, although the latter is probably overestimated and the former underestimated for methodological reasons. Net L-Lac efflux was not affected by extracellular D-Lac concentration and/or D-Lac influx, implying the existence of a concurrent L- Lac efflux during L-Lac influx. The D-Lac influx kinetics data indicated that the Lac-/HCO3/- antiport was not saturable in the extracellular D-Lac concentration range of 0-32 mM. This study clearly demonstrates the involvement of carrier-mediated transport in transmembrane Lac movement in fish muscle and supports the 'active lactate retention' mechanism proposed by Turner and Wood (J. Exp. Biol. 105: 395-401, 1983).",
keywords = "α-cyano-4- hydroxycinnamate, 4-acetamido-4'- isothiocyanostilbene-2,2'-disulfonic acid, Amiloride, Exercise, Kinetics, Metabolic hydrogen ion, Perfusion",
author = "Yuxiang Wang and Wright, {Pamela M.} and Heigenhauser, {George J F} and Wood, {Chris M.}",
year = "1997",
month = "6",
day = "19",
language = "English",
volume = "272",
journal = "American Journal of Physiology - Cell Physiology",
issn = "0363-6143",
publisher = "American Physiological Society",
number = "5 41-5",

}

TY - JOUR

T1 - Lactate transport by rainbow trout white muscle

T2 - Kinetic characteristics and sensitivity to inhibitors

AU - Wang, Yuxiang

AU - Wright, Pamela M.

AU - Heigenhauser, George J F

AU - Wood, Chris M.

PY - 1997/6/19

Y1 - 1997/6/19

N2 - This study used an isolated-perfused tail-trunk preparation of rainbow trout to examine the uptake and release of lactate (Lac) and metabolic protons (ΔH(m)/+) in resting and exercised fish white muscle. In exercised muscle, L(+)-Lac efflux was inhibited (~40%) by 5 mM α-cyano-4- hydroxycinnamate (CIN), but not by 0.5 mM 4-acetamido-4'- isothiocyanostilbene-2,2'-disulfonic acid (SITS) or 0.1 mM amiloride. These results suggest that Lac release occurs through a Lac--H+ symport and the free diffusion of lactic acid (HLac) or Lac, but not via the Lac-/HCO3- Cl- antiporter. Lac efflux was accompanied by AH(m)/+ influx in all treatments, and increased ΔH(m)/+ influx occurred after SITS treatment. In resting muscle, Lac uptake rates were greater than Lac efflux rates in the postexercise preparation. L-Lac influx exhibited partial saturation kinetics, whereas D(-)-Lac influx was linearly related to its extracellular concentration (0-32 mM). At 16 mM extracellular L-Lac, with a negligible transmembrane L-HLac gradient and an outwardly directed net driving force on L-Lac, CIN, and SITS reduced net L-Lac uptake by 75 and 45%, respectively. At 16 mM extracellular concentration, D-Lac influx was 64% of the net L-Lac influx. These results suggest that in trout muscle at 16 mM extracellular L- Lac, the Lac--H+ symport accounts for 30-36%, the Lac-/HCO3-Cl- antiport for 39-45%, and diffusion for 19-25% of uptake, although the latter is probably overestimated and the former underestimated for methodological reasons. Net L-Lac efflux was not affected by extracellular D-Lac concentration and/or D-Lac influx, implying the existence of a concurrent L- Lac efflux during L-Lac influx. The D-Lac influx kinetics data indicated that the Lac-/HCO3/- antiport was not saturable in the extracellular D-Lac concentration range of 0-32 mM. This study clearly demonstrates the involvement of carrier-mediated transport in transmembrane Lac movement in fish muscle and supports the 'active lactate retention' mechanism proposed by Turner and Wood (J. Exp. Biol. 105: 395-401, 1983).

AB - This study used an isolated-perfused tail-trunk preparation of rainbow trout to examine the uptake and release of lactate (Lac) and metabolic protons (ΔH(m)/+) in resting and exercised fish white muscle. In exercised muscle, L(+)-Lac efflux was inhibited (~40%) by 5 mM α-cyano-4- hydroxycinnamate (CIN), but not by 0.5 mM 4-acetamido-4'- isothiocyanostilbene-2,2'-disulfonic acid (SITS) or 0.1 mM amiloride. These results suggest that Lac release occurs through a Lac--H+ symport and the free diffusion of lactic acid (HLac) or Lac, but not via the Lac-/HCO3- Cl- antiporter. Lac efflux was accompanied by AH(m)/+ influx in all treatments, and increased ΔH(m)/+ influx occurred after SITS treatment. In resting muscle, Lac uptake rates were greater than Lac efflux rates in the postexercise preparation. L-Lac influx exhibited partial saturation kinetics, whereas D(-)-Lac influx was linearly related to its extracellular concentration (0-32 mM). At 16 mM extracellular L-Lac, with a negligible transmembrane L-HLac gradient and an outwardly directed net driving force on L-Lac, CIN, and SITS reduced net L-Lac uptake by 75 and 45%, respectively. At 16 mM extracellular concentration, D-Lac influx was 64% of the net L-Lac influx. These results suggest that in trout muscle at 16 mM extracellular L- Lac, the Lac--H+ symport accounts for 30-36%, the Lac-/HCO3-Cl- antiport for 39-45%, and diffusion for 19-25% of uptake, although the latter is probably overestimated and the former underestimated for methodological reasons. Net L-Lac efflux was not affected by extracellular D-Lac concentration and/or D-Lac influx, implying the existence of a concurrent L- Lac efflux during L-Lac influx. The D-Lac influx kinetics data indicated that the Lac-/HCO3/- antiport was not saturable in the extracellular D-Lac concentration range of 0-32 mM. This study clearly demonstrates the involvement of carrier-mediated transport in transmembrane Lac movement in fish muscle and supports the 'active lactate retention' mechanism proposed by Turner and Wood (J. Exp. Biol. 105: 395-401, 1983).

KW - α-cyano-4- hydroxycinnamate

KW - 4-acetamido-4'- isothiocyanostilbene-2,2'-disulfonic acid

KW - Amiloride

KW - Exercise

KW - Kinetics

KW - Metabolic hydrogen ion

KW - Perfusion

UR - http://www.scopus.com/inward/record.url?scp=0030961506&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0030961506&partnerID=8YFLogxK

M3 - Article

C2 - 9176350

AN - SCOPUS:0030961506

VL - 272

JO - American Journal of Physiology - Cell Physiology

JF - American Journal of Physiology - Cell Physiology

SN - 0363-6143

IS - 5 41-5

ER -