Effects of hypoxia on isolated vessels and perfused gills of rainbow trout

Michael P. Smith, Michael James Russell, Jeffrey T. Wincko, Kenneth R. Olson

Research output: Contribution to journalArticle

30 Citations (Scopus)

Abstract

Local hypoxia dilates systemic and constricts pulmonary blood vessels in mammals without neural or humoral involvement. The direct effects of hypoxia on isolated vessels from bony fish have not been examined. In the present study, isolated vessels (efferent branchial artery, EBA; coeliacomesenteric artery, CMA; ventral aorta, VA; and anterior cardinal vein, ACV) from rainbow or steelhead trout (Oncorhynchus mykiss) were subjected to either passive load (resting tension) or contracted with a ligand or 50 mM KCl and then subjected to 60 min of hypoxia by N2 administration and an additional 30 min of normoxia. All vessels were usually refractory to hypoxia under conditions of resting tension. EBAs, CMAs and VAs pre-contracted with a receptor-mediated ligand were all significantly relaxed by hypoxia and only VAs recovered significantly upon subsequent restoration of normoxia. In contrast, tension in all arteries pre-contracted with 50 mM KCl was elevated further in response to hypoxia. Conversely, ligand-contracted ACVs responded to hypoxia with a further increase in tension, whereas KCl-contracted ACVs relaxed. During apparently random 2-3-week periods EBA and CMA from steelhead and EBA from rainbow trout were hyper-reactive to hypoxia. Steelhead vessels responded to hypoxia with a rapid contraction that increased in magnitude over 3 days. These contractions were independent of pre-stimulation and they were dose-dependent upon Po2. In isolated gills, hypoxic perfusate produced an immediate but transient elevation of resistance (RGILL) in all four gill arches. RGILL increased by as much as 30% of initial values and this response was unaltered upon a second hypoxic exposure. These studies demonstrate that isolated vascular segments of rainbow trout are indeed responsive to hypoxia and that these differential responses are vessel and tone dependent and the overall response may be altered by as yet unknown seasonal or environmental factors. Hypoxia-induced arterial relaxation is blocked by elevated external [K+], implicating alteration of transmembrane K+ conductance and/or membrane potential in this depressor response. K+-channel closure or voltage-gated Ca2+ influx cannot account for arterial vasoconstriction due to hypoxia during KCl contractions. Vascular responses to hypoxia could have a profound impact on local flow in vivo and could mediate ventilation-perfusion matching in the branchial circulation of fish.

Original languageEnglish (US)
Pages (from-to)171-181
Number of pages11
JournalComparative Biochemistry and Physiology - A Molecular and Integrative Physiology
Volume130
Issue number1
DOIs
StatePublished - Aug 21 2001
Externally publishedYes

Fingerprint

Oncorhynchus mykiss
Ligands
Fish
Mammals
Blood vessels
Arches
Refractory materials
Restoration
Ventilation
Membranes
Blood Vessels
Electric potential
Arteries
Hypoxia
Fishes
Trout
Vasoconstriction
Membrane Potentials
Aorta
Veins

Keywords

  • Fish
  • Hypoxic vasoconstriction
  • Hypoxic vasodilation
  • Potassium channels
  • Vascular tone

ASJC Scopus subject areas

  • Biochemistry
  • Physiology
  • Molecular Biology

Cite this

Effects of hypoxia on isolated vessels and perfused gills of rainbow trout. / Smith, Michael P.; Russell, Michael James; Wincko, Jeffrey T.; Olson, Kenneth R.

In: Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology, Vol. 130, No. 1, 21.08.2001, p. 171-181.

Research output: Contribution to journalArticle

Smith, Michael P. ; Russell, Michael James ; Wincko, Jeffrey T. ; Olson, Kenneth R. / Effects of hypoxia on isolated vessels and perfused gills of rainbow trout. In: Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology. 2001 ; Vol. 130, No. 1. pp. 171-181.
@article{b9dfdb5eaa7c4be384eb1902009177fc,
title = "Effects of hypoxia on isolated vessels and perfused gills of rainbow trout",
abstract = "Local hypoxia dilates systemic and constricts pulmonary blood vessels in mammals without neural or humoral involvement. The direct effects of hypoxia on isolated vessels from bony fish have not been examined. In the present study, isolated vessels (efferent branchial artery, EBA; coeliacomesenteric artery, CMA; ventral aorta, VA; and anterior cardinal vein, ACV) from rainbow or steelhead trout (Oncorhynchus mykiss) were subjected to either passive load (resting tension) or contracted with a ligand or 50 mM KCl and then subjected to 60 min of hypoxia by N2 administration and an additional 30 min of normoxia. All vessels were usually refractory to hypoxia under conditions of resting tension. EBAs, CMAs and VAs pre-contracted with a receptor-mediated ligand were all significantly relaxed by hypoxia and only VAs recovered significantly upon subsequent restoration of normoxia. In contrast, tension in all arteries pre-contracted with 50 mM KCl was elevated further in response to hypoxia. Conversely, ligand-contracted ACVs responded to hypoxia with a further increase in tension, whereas KCl-contracted ACVs relaxed. During apparently random 2-3-week periods EBA and CMA from steelhead and EBA from rainbow trout were hyper-reactive to hypoxia. Steelhead vessels responded to hypoxia with a rapid contraction that increased in magnitude over 3 days. These contractions were independent of pre-stimulation and they were dose-dependent upon Po2. In isolated gills, hypoxic perfusate produced an immediate but transient elevation of resistance (RGILL) in all four gill arches. RGILL increased by as much as 30{\%} of initial values and this response was unaltered upon a second hypoxic exposure. These studies demonstrate that isolated vascular segments of rainbow trout are indeed responsive to hypoxia and that these differential responses are vessel and tone dependent and the overall response may be altered by as yet unknown seasonal or environmental factors. Hypoxia-induced arterial relaxation is blocked by elevated external [K+], implicating alteration of transmembrane K+ conductance and/or membrane potential in this depressor response. K+-channel closure or voltage-gated Ca2+ influx cannot account for arterial vasoconstriction due to hypoxia during KCl contractions. Vascular responses to hypoxia could have a profound impact on local flow in vivo and could mediate ventilation-perfusion matching in the branchial circulation of fish.",
keywords = "Fish, Hypoxic vasoconstriction, Hypoxic vasodilation, Potassium channels, Vascular tone",
author = "Smith, {Michael P.} and Russell, {Michael James} and Wincko, {Jeffrey T.} and Olson, {Kenneth R.}",
year = "2001",
month = "8",
day = "21",
doi = "10.1016/S1095-6433(01)00383-X",
language = "English (US)",
volume = "130",
pages = "171--181",
journal = "Comparative biochemistry and physiology. Part A, Molecular & integrative physiology",
issn = "1095-6433",
publisher = "Elsevier Inc.",
number = "1",

}

TY - JOUR

T1 - Effects of hypoxia on isolated vessels and perfused gills of rainbow trout

AU - Smith, Michael P.

AU - Russell, Michael James

AU - Wincko, Jeffrey T.

AU - Olson, Kenneth R.

PY - 2001/8/21

Y1 - 2001/8/21

N2 - Local hypoxia dilates systemic and constricts pulmonary blood vessels in mammals without neural or humoral involvement. The direct effects of hypoxia on isolated vessels from bony fish have not been examined. In the present study, isolated vessels (efferent branchial artery, EBA; coeliacomesenteric artery, CMA; ventral aorta, VA; and anterior cardinal vein, ACV) from rainbow or steelhead trout (Oncorhynchus mykiss) were subjected to either passive load (resting tension) or contracted with a ligand or 50 mM KCl and then subjected to 60 min of hypoxia by N2 administration and an additional 30 min of normoxia. All vessels were usually refractory to hypoxia under conditions of resting tension. EBAs, CMAs and VAs pre-contracted with a receptor-mediated ligand were all significantly relaxed by hypoxia and only VAs recovered significantly upon subsequent restoration of normoxia. In contrast, tension in all arteries pre-contracted with 50 mM KCl was elevated further in response to hypoxia. Conversely, ligand-contracted ACVs responded to hypoxia with a further increase in tension, whereas KCl-contracted ACVs relaxed. During apparently random 2-3-week periods EBA and CMA from steelhead and EBA from rainbow trout were hyper-reactive to hypoxia. Steelhead vessels responded to hypoxia with a rapid contraction that increased in magnitude over 3 days. These contractions were independent of pre-stimulation and they were dose-dependent upon Po2. In isolated gills, hypoxic perfusate produced an immediate but transient elevation of resistance (RGILL) in all four gill arches. RGILL increased by as much as 30% of initial values and this response was unaltered upon a second hypoxic exposure. These studies demonstrate that isolated vascular segments of rainbow trout are indeed responsive to hypoxia and that these differential responses are vessel and tone dependent and the overall response may be altered by as yet unknown seasonal or environmental factors. Hypoxia-induced arterial relaxation is blocked by elevated external [K+], implicating alteration of transmembrane K+ conductance and/or membrane potential in this depressor response. K+-channel closure or voltage-gated Ca2+ influx cannot account for arterial vasoconstriction due to hypoxia during KCl contractions. Vascular responses to hypoxia could have a profound impact on local flow in vivo and could mediate ventilation-perfusion matching in the branchial circulation of fish.

AB - Local hypoxia dilates systemic and constricts pulmonary blood vessels in mammals without neural or humoral involvement. The direct effects of hypoxia on isolated vessels from bony fish have not been examined. In the present study, isolated vessels (efferent branchial artery, EBA; coeliacomesenteric artery, CMA; ventral aorta, VA; and anterior cardinal vein, ACV) from rainbow or steelhead trout (Oncorhynchus mykiss) were subjected to either passive load (resting tension) or contracted with a ligand or 50 mM KCl and then subjected to 60 min of hypoxia by N2 administration and an additional 30 min of normoxia. All vessels were usually refractory to hypoxia under conditions of resting tension. EBAs, CMAs and VAs pre-contracted with a receptor-mediated ligand were all significantly relaxed by hypoxia and only VAs recovered significantly upon subsequent restoration of normoxia. In contrast, tension in all arteries pre-contracted with 50 mM KCl was elevated further in response to hypoxia. Conversely, ligand-contracted ACVs responded to hypoxia with a further increase in tension, whereas KCl-contracted ACVs relaxed. During apparently random 2-3-week periods EBA and CMA from steelhead and EBA from rainbow trout were hyper-reactive to hypoxia. Steelhead vessels responded to hypoxia with a rapid contraction that increased in magnitude over 3 days. These contractions were independent of pre-stimulation and they were dose-dependent upon Po2. In isolated gills, hypoxic perfusate produced an immediate but transient elevation of resistance (RGILL) in all four gill arches. RGILL increased by as much as 30% of initial values and this response was unaltered upon a second hypoxic exposure. These studies demonstrate that isolated vascular segments of rainbow trout are indeed responsive to hypoxia and that these differential responses are vessel and tone dependent and the overall response may be altered by as yet unknown seasonal or environmental factors. Hypoxia-induced arterial relaxation is blocked by elevated external [K+], implicating alteration of transmembrane K+ conductance and/or membrane potential in this depressor response. K+-channel closure or voltage-gated Ca2+ influx cannot account for arterial vasoconstriction due to hypoxia during KCl contractions. Vascular responses to hypoxia could have a profound impact on local flow in vivo and could mediate ventilation-perfusion matching in the branchial circulation of fish.

KW - Fish

KW - Hypoxic vasoconstriction

KW - Hypoxic vasodilation

KW - Potassium channels

KW - Vascular tone

UR - http://www.scopus.com/inward/record.url?scp=0034898267&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0034898267&partnerID=8YFLogxK

U2 - 10.1016/S1095-6433(01)00383-X

DO - 10.1016/S1095-6433(01)00383-X

M3 - Article

VL - 130

SP - 171

EP - 181

JO - Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

JF - Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

SN - 1095-6433

IS - 1

ER -