Role of oxygen in arteriolar functional vasodilation in hamster striated muscle

Gorczynski, Richard J.; Duling, B. R.

doi:10.1152/ajpheart.1978.235.5.h505

Cited by 74 publications

(84 citation statements)

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“…We first compared the contractile properties of EDL at a physiologically extreme bath oxygen tension of 20-21% O 2 (pO 2 Ϸ150 mmHg, ambient pO 2 ), which represents an oxidative stress for peripheral tissue, and at 1-2% O 2 (pO 2 Ϸ10 mmHg), which is characteristic of normal mammalian striated muscle in vivo (8,9). Direct measurement at the muscle core (see Experimental Procedures and Table 1) indicated that mean muscle pO 2 was Ϸ40 mmHg (median 36.7 mmHg) at 20% bath O 2 and Ϸ3.5 mmHg (median 1.75 mmHg) at Ϸ1-2% bath O 2.…”

Section: Resultsmentioning

confidence: 99%

“…Studies of isolated skeletal muscle have generally been carried out at grossly nonphysiological oxygen tension, usually 95% O 2 , whereas skeletal muscle pO 2 is in the range from 4 to 20 mmHg (0.5-2.5% O 2 ), and even lower in working muscle (8,9). Supranormal O 2 concentrations have been shown in vitro to disrupt regulation by NO of the ryanodine receptor͞calcium release channel (RyR1) of skeletal muscle sarcoplasmic reticulum (SR) (10).…”

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confidence: 99%

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Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide

Hare

Hess

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

101

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It is generally accepted that inhibition of nitric oxide synthase (NOS) facilitates, and thus nitric oxide (NO) inhibits, contractility of skeletal muscle. However, standard assessments of contractility are carried out at a nonphysiological oxygen tension [partial pressure of oxygen (pO2)] that can interfere with NO signaling (95% O2). We therefore examined, in normal and neuronal NOS (nNOS)-deficient mice, the influence of pO2 on whole-muscle contractility and on myocyte calcium flux and sarcomere shortening. Here, we demonstrate a significant enhancement of these measures of muscle performance at low physiological pO2 and an inhibitory influence at higher physiological pO2, which depend on endogenous nNOS. At 95% O2 (which produces oxidative stress; muscle core pO2 Ϸ400 mmHg), force production is enhanced but control of contractility by NO͞nitrosylation is greatly attenuated. In addition, responsivity to pO2 is altered significantly in nNOS mutant muscle. These results reveal a fundamental role for the concerted action of NO and O2 in physiological regulation of skeletal muscle contractility, and suggest novel molecular aspects of myopathic disease. They suggest further that the role of NO in some cellular systems may require reexamination. It has recently been recognized that redox-based regulation of protein function serves not only to mediate compensatory responses to oxidative or nitrosative stress but also modulates transduction along basic signaling pathways in mammalian cells (1). Further, accumulating evidence indicates that nitric oxide (NO)-based protein modifications are critical effectors of redox regulation, which may be linked at the molecular level to partial pressure of oxygen (pO 2 ) (1). Accordingly, the functional contribution of redox mechanisms remains, for the most part, untested, and potentially masked in virtually all ex vivo studies, which have been carried out at supranormal oxygen tension (typically 21% O 2 for cells and 95% O 2 for tissue, whereas pO 2 in vivo is much lower).Mammalian skeletal muscle operates over a range of pO 2 , which is determined by local blood flow and muscle activity, and contains endogenous sources of NO. The -isoform of type I or neuronal NO synthase (nNOS) localizes to the plasma membrane (sarcolemma) of skeletal muscle fibers through interaction with the dystrophin complex (2-4). In many mammals, nNOS is either restricted to or particularly abundant in fast-twitch fibers, although, in humans, fast-and slow-twitch fibers are more evenly endowed (2, 5, 6). The loss of nNOS from sarcolemma of mdx mice (whose fast-twitch fibers are disproportionately impaired), and of patients with Duchenne or Becker muscular dystrophy, focused interest on the possibility that NO produced by muscle fibers may play a role in excitation-contraction (E-C) coupling and that NO deficiency may contribute to contractile impairment in muscle disease (2-6). However, although mice deficient in nNOS show subtle abnormalities in muscle blood flow (7), overt alterations in contractile fun...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide

Hare

Hess

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

101

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“…However, the role of H 2 O 2 in this dilation is not diminished by high-salt intake, suggesting that the salt-induced decrease in functional dilation must be due to a reduction in the influence of some other dilator stimulus. A decrease in local oxygen levels can also contribute to arteriolar dilation during muscle contraction (7,17,41), either directly if there is a fall in arteriolar wall PO 2 or indirectly via vasoactive mediators produced when PO 2 declines in nearby parenchymal cells or paired venules (27,43). Because the blunting of functional dilation in salt-fed rats could reflect a reduced arteriolar responsiveness to such changes in PO 2 , one aim of this study was to examine the effects of a high-salt diet on arteriolar responses to oxygen.…”

Section: Discussionmentioning

confidence: 99%

“…We conclude that 20-HETE contributes to oxygen-induced constriction of skeletal muscle arterioles via inhibition of K Ca channels and that a high-salt diet impairs arteriolar responses to increased oxygen availability due to a reduction in vascular smooth muscle responsiveness to 20-HETE. 20-hydroxyeicosatetraenoic acid; vascular control; blood flow; NaCl LOCAL OXYGEN AVAILABILITY is an important determinant of microvascular resistance and tissue blood flow (10,17,22,41), and consumption of a high-salt diet can lead to changes in resistance vessel function that alter the relationship between oxygen and vascular tone. For example, small gracilis muscle feed arteries from rats fed high salt for as little as 3 days consistently show an impaired dilator response to reduced oxygen levels (47,48).…”

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confidence: 99%

High dietary salt reduces the contribution of 20-HETE to arteriolar oxygen responsiveness in skeletal muscle

Marvar

Falck²,

Boegehold

2007

American Journal of Physiology-Heart and Circulatory Physiology

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coupling of tissue blood flow to cellular metabolic demand involves oxygen-dependent adjustments in arteriolar tone, and arteriolar responses to oxygen can be mediated, in part, by changes in local production of 20-HETE. In this study, we examined the long-term effect of dietary salt on arteriolar oxygen responsiveness in the exteriorized, superfused rat spinotrapezius muscle and the role of 20-HETE in this responsiveness. Rats were fed either a normal-salt (NS, 0.45%) or high-salt (HS, 4%) diet for 4 -5 wk. There was no difference in steady-state tissue PO 2 between NS and HS rats, and elevation of superfusate oxygen content from 0% to 10% caused tissue PO 2 to increase by the same amount in both groups. However, the resulting reductions in arteriolar diameter and blood flow were less in HS rats than NS rats. Inhibition of 20-HETE formation with or 17-octadecynoic acid (17-ODYA) attenuated oxygen-induced constriction in NS rats but not HS rats. Exogenous 20-HETE elicited arteriolar constriction that was greatly reduced by the large-conductance Ca 2ϩ -activated potassium (K Ca) channel inhibitors tetraethylammonium chloride (TEA) and iberiotoxin (IbTx) in NS rats and a smaller constriction that was less sensitive to TEA or IbTx in HS rats. Arteriolar responses to exogenous angiotensin II were similar in both groups but more sensitive to inhibition with DDMS in NS rats. Norepinephrine-induced arteriolar constriction was similar and insensitive to DDMS in both groups. We conclude that 20-HETE contributes to oxygen-induced constriction of skeletal muscle arterioles via inhibition of K Ca channels and that a high-salt diet impairs arteriolar responses to increased oxygen availability due to a reduction in vascular smooth muscle responsiveness to 20-HETE. 20-hydroxyeicosatetraenoic acid; vascular control; blood flow; NaCl LOCAL OXYGEN AVAILABILITY is an important determinant of microvascular resistance and tissue blood flow (10,17,22,41), and consumption of a high-salt diet can lead to changes in resistance vessel function that alter the relationship between oxygen and vascular tone. For example, small gracilis muscle feed arteries from rats fed high salt for as little as 3 days consistently show an impaired dilator response to reduced oxygen levels (47, 48). However, the effect of oxygen on the tone of smaller arterioles in rat cremaster muscle is unchanged after 3 days on a high-salt diet (13). This suggests that either a longer period of high-salt intake is required to alter the oxygen responsiveness of these more distal resistance vessels or that there is a fundamental difference between extraparenchymal arteries and intramuscular arterioles in the susceptibility of oxygen-sensitive tone to dietary salt. The first aim of this study was to distinguish between these possibilities by determining whether a prolonged period of high-salt intake can change the relationship between oxygen and vascular tone in the arteriolar network of skeletal muscle.The mechanisms through which oxygen can influence resistance vessel to...

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“…Furthermore, arterial diameter and blood flow can be increased by contracting a subset of muscle fibers (1,12). The exact nature of the dilator factors that are active during exercise is not clear (27).…”

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confidence: 99%

Does arterial myogenic tone determine blood flow distribution in vivo?

Dora¹

2005

American Journal of Physiology-Heart and Circulatory Physiology

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BLOOD FLOW DISTRIBUTION at rest and during exercise is intricately controlled by centrally driven neuroeffector mechanisms and circulating hormones (particularly epinephrine), local autacoids, and metabolites, all superimposed on the inherent or "myogenic" reactivity of the arterial smooth muscle. During exercise, the cardiac output of a trained athlete can increase ϳ5-fold, and these mechanisms serve to coordinate a huge (ϳ20-fold) increase in the amount of blood routed to the exercising muscle (3). The dramatic nature of this increase is illustrated by the fact that the proportion of the cardiac output diverted to skeletal muscle can change from 20% to ϳ80%! Importantly, and to the benefit of the individual, despite this enormous increase in the flow of blood to muscle, brain blood flow is not compromised (3). But to what extent do the inherent characteristics of the arteries of the brain and musculature explain these distinct changes?As cerebral arteries are not particularly responsive to the sympathetic nerves surrounding them, myogenic reactivity is thought to be a fundamental determinant of the constant flow of blood to the brain and, as a consequence, has been extensively studied. The most direct studies have assessed how changes in intraluminal pressure links to smooth muscle contraction/relaxation in isolated arteries, where reflex and most local influences are absent and steady-state conditions can be achieved. It is technically extremely difficult to make intracellular recordings from the very small (Ͻ10 m width) smooth muscle cells, particularly in isolated arteries under physiological pressure. However, a now classic study in 1984 by Harder (13) first showed that increasing pressure alone caused depolarization and as a result stimulated Ca 2ϩ influx and vasoconstriction. Unfortunately, technology at the time did not allow accurate simultaneous measurement of diameter. This was achieved in later studies, notably from Nelson's group (19), as the complexity of the myogenic control mechanism became apparent. It is now known that voltage-activated calcium entry is not the only mechanism responsible for changes in myogenic tone (16) and that the relative contributions from different mechanisms vary between and within vascular beds.In this issue of the American Journal of Physiology-Heart and Circulatory Physiology, Kotecha and Hill (21) are the latest to attempt the extremely difficult task of quantifying the importance of membrane potential for myogenic reactivity, but this time in a resistance artery from a striated muscle bed (the rat cremaster muscle, pressurized arteries with a passive diameter of ϳ140 m at 70 mmHg). This is the first study in a muscle resistance artery that has attempted to assess the effect of a stepwise increase in luminal pressure on smooth muscle membrane potential and arterial diameter. In addition, the authors have compared their data with published data from rat isolated cerebral arteries [distal posterior, passive diameter of ϳ200 m at 70 mmHg (19)] to attempt to reveal how...

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Role of oxygen in arteriolar functional vasodilation in hamster striated muscle

Cited by 74 publications

References 0 publications

Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide

Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide

High dietary salt reduces the contribution of 20-HETE to arteriolar oxygen responsiveness in skeletal muscle

Does arterial myogenic tone determine blood flow distribution in vivo?

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