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Department of Anesthesiology and Department of Physiology and Biophysics, Mayo Clinic and Foundation, Rochester, Minnesota 55905
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Perkins, William J., Young-Soo Han, and Gary C. Sieck.
Skeletal muscle force and actomyosin ATPase activity reduced by
nitric oxide donor. J. Appl. Physiol.
83(4): 1326-1332, 1997.
Nitric oxide (NO) may exert direct
effects on actin-myosin cross-bridge cycling by modulating critical
thiols on the myosin head. In the present study, the effects of the NO
donor sodium nitroprusside (SNP; 100 µM to 10 mM) on mechanical
properties and actomyosin adenosinetriphosphatase (ATPase) activity of
single permeabilized muscle fibers from the rabbit psoas muscle were
determined. The effects of
N-ethylmaleimide (NEM; 5-250
µM), a thiol-specific alkylating reagent, on mechanical properties of
single fibers were also evaluated. Both NEM (
25 µM) and SNP (1
mM) significantly inhibited isometric force and actomyosin ATPase
activity. The unloaded shortening velocity of SNP-treated single fibers
was decreased, but to a lesser extent, suggesting that SNP effects on
isometric force and actomyosin ATPase were largely due to decreased cross-bridge recruitment. The calcium sensitivity of SNP-treated single
fibers was also decreased. The effects of SNP, but not NEM, on force
and actomyosin ATPase activity were reversed by treatment with 10 mM
DL-dithiothreitol, a
thiol-reducing agent. We conclude that the NO donor SNP inhibits
contractile function caused by reversible oxidation of contractile
protein thiols.
rabbit psoas; pharmacology; sodium nitroprusside; sulfhydryl
reagents; ethylmaleimide; dithiothreitol; adenosinetriphosphatase
INTRODUCTION NITRIC OXIDE (NO) is a relatively nonpolar solute
species that is implicated in a wide variety of tissue functions,
including relaxation of smooth muscle (27). In most NO-regulated
tissues, the enzyme responsible for NO synthesis [nitric oxide
synthase (NOS)] is present in the tissue itself or in a proximate
tissue, and there are NO-responsive targets present in the tissue. One such target is soluble guanylate cyclase, which is activated by NO (2)
to increase production of guanosine 3 Recently, it was demonstrated that skeletal muscle contains neuronal
and endothelial NOS isoforms (21, 22). Skeletal muscle also contains
critical thiols that, when oxidized or covalently modified, decrease
contractile function. Reactive oxidant species other than NO have been
shown to be generated by skeletal muscle (3, 7) and can modulate
skeletal muscle contractile function (8, 29). Although it remains
possible that NO modulates skeletal muscle function in part via cGMP
and changes in Ca2+ processing
(21), the purpose of the present study was to determine the direct
effects of a NO donor on permeabilized skeletal muscle fibers devoid of
these second messengers. Accordingly, the sensitivity of permeabilized
rabbit psoas fibers to the thiol-specific alkylating agent
N-ethylmaleimide (NEM) and the NO
donor sodium nitroprusside (SNP) was examined. It was hypothesized that
NO-related thiol modification inhibits actin-myosin cross-bridge
cycling and actomyosin adenosinetriphosphatase (ATPase) activity.
METHODS
,5-cyclic
monophosphate (cGMP). The tissue then is responsive to cGMP via
cGMP-dependent protein kinase. In addition to this second-messenger
pathway, NO may directly modulate tissue function by protein
modification, via transnitrosylation or oxidation of cysteine thiol
residues (33).
-aminoethyl
ether)-N,N,N,N-tetraacetic acid, 1.0 free Mg2+, 2 MgATP2
, 20.0 imidazole, 15 creatine phosphate, 1 mg/ml creatine phosphokinase, and sufficient KCl
to adjust the ionic strength to 150 mM. The pH was adjusted to 7.0 with
KOH. The negative log free Ca2+
concentration (pCa) of the relaxing solution was 9. Single
fibers were then dissected with fine forceps under a microscope and
immersed for 25 min in a skinning solution that was of the same
composition as the relaxing solution except that 1% Triton X-100 and
10 mM DL-dithiothreitol (DTT)
were added. The skinning solution was kept at 15°C to
thermoequilibrate the fibers before mechanical measurements. DTT was
added to the skinning solution to prevent oxidation of cysteine thiols
on contractile proteins.
,
Vo was determined
by using the "slack" test (10), in which the muscle was quickly
released after developing maximal force and shortened to different
fractions of Lm
(8, 10, 12, and 14% of
Lm). The time required to redevelop force was measured, and the slope of the line
relating this time to the change in length was calculated as a measure
of Vo and
expressed as muscle fiber length per second (Lm/s).
Measurement of actomyosin ATPase activity.
Isometric actomyosin ATPase activity was measured at 15°C by using
a fluorescence-coupled enzyme assay (14). The ATPase assay
solution contained relaxing solution, plus 5 mM
phospho(enol)- pyruvate (PEP),
0.2 mM reduced -nicotinamide adenine dinucleotide (NADH), 100 U/ml
pyruvate kinase (PK), and 140 U/ml lactate dehydrogenase (LDH). The fluorescence-coupled enzyme assay involves the following reactions
|
(1) |
|
(2) |
|
(3) |
on actomyosin ATPase
activity. Calibration involved photometric measurements of fluorescence
in the presence of known amounts of NADH. Previous work on
permeabilized single fibers has shown that mitochondrial ATPases and
sarcoplasmic reticulum ATPase make no detectable contribution to the
observed ATPase activity (19). The light source was a mercury lamp, and
excitation and emission wavelengths were set by using a 340-nm
band-pass filter and 450-nm interference cutoff filter, respectively.
The photomultiplier was positioned perpendicular to the axis of
excitation, and the gain was fixed during the actomyosin ATPase
measurements. In control experiments, we found that exposure to 50 µM
NEM or 10 mM SNP did not interfere with NADH fluorescence.
Isometric actomyosin ATPase activity was determined at a pCa of 9 (relaxing conditions) and 4 (maximal activating condition). During the
actomyosin ATPase measurements, flow through the cuvette was stopped
for 15 s, and the rate of extinction of the NADH fluorescence signal
was recorded. Thereafter, flow through the cuvette was reinitiated, and
the activating solution was exchanged. This cycling of flow every 15 s
through the cuvette was regulated by using a computer-controlled
peristaltic pump.
Sensitivity of permeabilized fibers to thiol modification.
Single fibers were initially perfused with relaxing solution (pCa 9) to
establish baseline force. The fibers were then perfused with pCa 4 activating solution, and maximum isometric force was measured once a
stable plateau was reached and maintained for 5 min. This was taken as
the reference or initial force. The muscle fiber was then reperfused
with relaxing solution until the force returned to baseline. After ~1
min, the fiber was perfused for 20 min with NEM (5-250 µM) in
the relaxing solution. Thereafter, the fiber was once again perfused
with the pCa 4 activating solution, and the force response was
remeasured. Finally, after perfusing the fiber for another 20 min with
relaxing solution containing DTT, force responses to the pCa 4 activating solution were measured again. Rundown in the contractile
response was assessed in separate fibers in which the same sequence of
events was followed except that the fibers were not exposed to NEM or
DTT.
The effect of exposing fibers to 50 µM NEM on actomyosin ATPase
activity was also evaluated. The same protocol was followed as
described above for determining the effect of NEM on isometric force.
Effects of SNP on permeabilized fibers.
The effect of SNP (100 µM to 10 mM) on maximum isometric force and
Vo of single
psoas fibers was determined by using the same protocol as described
above for determining the effects of NEM. In addition, the effect of
varying concentrations of SNP on isometric actomyosin ATPase activity
of fibers was measured. In separate fibers, the effect of 5 mM SNP on
the force-pCa relationship of permeabilized fibers was also determined.
The reversibility of the effects of SNP on force, actomyosin ATPase,
and Vo by DTT was
also evaluated. In each experiment, rundown in the force and actomyosin
ATPase responses were evaluated in separate fibers by using the same
sequence of events except that the fibers were not exposed to SNP.
Data acquisition and statistical analysis.
Force, length, and photometric data were digitally acquired at a 1-kHz
sampling rate with the use of a Pentium personal computer equipped with
a National Instruments AT-MIO-16 digital acquisition board and LabView
software. In addition, the Güth Scientific Instruments Muscle
Research System was computer controlled. The 50% effective
concentration of pCa
(pCa50) of the
force pCa relationship was determined by using a sigmoid regression
analysis in SigmaPlot. An analysis of variance for repeated measures
was used to compare forces in control and agent-treated fibers. When
appropriate, an unpaired Student's
t-test was used for post hoc analysis
of significance between groups. A difference was considered significant at P < 0.05. Values are reported as
means ± SE.
RESULTS
3 · s1,
whereas resting ATPase activity at pCa 9 was 0.60 ± 0.13 nmol · mm3 · s1.
Isometric actomyosin ATPase activity at pCa 4 decreased significantly over 20 min from 2.14 ± 0.11 to 1.81 ± 0.18 nmol · mm3 · s1
(P < 0.05; see Fig. 4). Addition of
10 mM DTT to the skinned fiber perfusate had no significant effect on
either initial or subsequent maximal force and actomyosin ATPase
activity.
significantly different from timed control
(P < 0.01).
NEM effects on force and actomyosin ATPase activity. The isometric force generated during maximal activation at pCa 4 was significantly reduced, in a concentration-dependent fashion, by exposure to NEM for 20 min (Table 1). This effect of NEM on maximal isometric force was not reversed by 20-min exposure to DTT. Exposing the permeabilized fiber to DTT alone had no effect on either the initial maximum force or the NEM related reduction in force (Table 1).
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(0.54 ± 0.16 and
2.09 ± 0.19 nmol · mm3 · s1,
respectively) was not different from that obtained at pCa 9 and pCa 4 in the presence of 2 mM
MgATP2 (0.60 ± 0.13 and
2.14 ± 0.11 nmol · mm3 · s1,
respectively).
SNP effects on force, actomyosin ATPase activity, and
Vo.
The maximal isometric force generated at pCa 4 was significantly
reduced, in a concentration-dependent fashion, by 20-min exposure to
SNP but only at concentrations >0.5 mM (Figs.
1 and 2).
Exposing fibers to SNP for times >20 min did not affect the extent of
force reduction. At 5 mM SNP, there was a 35% reduction in isometric
force at pCa 4, which was significantly less
(P < 0.001) than the 15%
reduction observed in control fibers.
Addition of CN
(10 mM), a
breakdown product of SNP, or NO2 (5 mM), the product of NO autoxidation, resulted in no significant
reduction in force. The SNP effect on force reduction at pCa 4 was
reversible after exposure of the SNP-treated fiber with DTT (Fig.
3). Treatment of fibers with DTT in the
absence of SNP and/or after rundown resulted in no significant
change in force at pCa 4.
significantly
different from timed control, P
<0.01.
The actomyosin ATPase activity at pCa 4 was decreased 35% after exposure to 5 mM SNP (see Figs. 1 and 4). A significant reduction in the pCa 9 actomyosin ATPase was not observed. The reduction in the pCa 4 actomyosin ATPase activity was fully reversed by exposure of SNP-exposed skinned single fibers to 10 mM DTT for 20 min. The effects of 5 mM SNP on the isometric force-pCa relation were determined (Fig. 5). Both the maximal force and Ca2+ sensitivity were decreased by SNP. The pCa50 values for initial, timed-control, and SNP-treated fibers were 5.42, 5.27, and 5.1, respectively. The pCa50 for SNP-treated fibers was significantly lower than that in both initial and timed-control fibers.
significantly different from initial value
(P < 0.01).
The Vo for the rabbit psoas skinned single fibers treated with 25 µM NEM for 20 min was decreased 43% from 1.29 ± 0.16 to 0.74 ± 0.09 Lm/s (P = 0.0004). Exposure of the skinned single fiber to 5 mM SNP for 20 min resulted in a smaller (17%) but significant reduction in Vo (1.14 ± 0.09 vs. 0.95 ± 0.09 Lm/s, P = 0.002; Fig. 6). There was no significant change in Vo in 20-min timed controls (1.26 ± 0.15 vs. 1.38 ± 0.17 ml/s; P = 0.15). Treatment of the 20-min control and NEM-treated fibers with DTT for 20 min resulted in no significant change in Vo. There was no significant difference between Vo in control vs. SNP-treated fibers after 20 min exposure to DTT.
significantly different from timed control
(P < 0.01).
DISCUSSION
In single permeabilized rabbit psoas muscle fibers, exposure to the NO donor SNP inhibited isometric force, Ca2+ sensitivity, and actomyosin ATPase activity. Similarly, exposure of permeabilized fibers to NEM, which selectively modifies thiols, reduced both isometric force and actomyosin ATPase in a concentration-dependent manner.
The NEM-mediated reduction in force is consistent with previous work in
which a maleimide spin label (6, 31) and the thiol-specific reagent
5,5-dithiobis(2-nitrobenzoic acid) (DTNB; Ref. 36) were found to
decrease force and stiffness in permeabilized single fibers. In these
previous studies (6, 36), it was concluded that inhibition of fiber
contractile properties was the result of direct modification of
cysteine residues on contractile proteins. In rabbit psoas muscle
fibers, two highly reactive and ATPase-critical thiols, SH-1 and SH-2,
are present on the myosin head (30, 32). In the present
study, permeabilized fibers were exposed to thiol-modifying reagents
under relaxing conditions because this increases the reactivity of
cysteine thiols on the myosin head, particularly SH-1, relative to the
cysteine thiols of other contractile proteins (9, 35). The specificity
of SH-1 modification has been verified by extraction of the myosin from
treated single fibers and subsequent determination of ATPase activities, thiol titrations, and radiolabeling experiments (6, 31). We
suggest that the effect of the NO donor SNP in reducing isometric force
in permeabilized fibers was also mediated by reversible oxidation of
critical thiols on the myosin head.
SNP was selected as the NO donor in the present study for several reasons. It is a widely used NO donor in biological studies and is also used in the medical treatment of hypertension. It is also relatively stable in aqueous solution. Although it is typically thought to work by releasing NO and activating soluble guanylate cyclase (16), SNP also reacts with biological thiols and formed the basis of one of the earliest assays for the detection of thiols in tissue extracts. SNP reacts with free thiols to give rise to a compound with a red color and an absorption maximum at 510 nm (18), in all likelihood an S-nitrosothiol or protein. The efficiency and speed with which SNP participates in S-nitrosylation reactions (33) with protein thiols, however, is unknown.
After NEM treatment, actomyosin ATPase was reduced in parallel with the reduction in maximal isometric force at pCa 4. The basal ATPase activity of permeabilized fibers under relaxing conditions (pCa 9) was also reduced. Although there is a possibility that there is some loss of myofibrillar Ca2+ regulation in this preparation, the fourfold increase (pCa 9 to pCa 4) in actomyosin ATPase activity is in agreement with previous reports (19). Because the ATPase activity measured under relaxing conditions is that of the myosin head while either not bound to or weakly associated with actin, this result implies that NEM treatment affects the intrinsic ATPase activity of the myosin head. It is, therefore, likely that the effects of NEM on actomyosin ATPase activity and force production observed at pCa 4 are also due to modifications of the myosin head rather than due to an effect on other proteins involved in the activation process, such as troponin C or tropomyosin. To our knowledge, this is the first demonstration that contractile protein thiol modification causes a reduction in actomyosin ATPase activity in single permeabilized fibers. However, these observations are consistent with previous results obtained by using purified actin and myosin (26).
Whereas NEM irreversibly modifies protein thiols, the NO-donor compound SNP may reversibly modify protein thiols by transnitrosylation (34). Transnitrosylation involves transfer of NO+ from a NO donor to a protein thiol and results in the formation of a stable S-nitrosoprotein. Functionally significant S-nitrosylation of proteins has been demonstrated both in purified proteins (1, 33) and in vivo (17). In the present study, it was observed that SNP decreased isometric force of permeabilized psoas fibers in a concentration-dependent manner, with no effects observed at SNP concentrations <0.5 mM. Thus permeabilized fibers were sensitive to SNP but to a much lesser extent than to NEM, which significantly decreased force and actomyosin ATPase activity at concentrations more than an order of magnitude lower. SNP also significantly decreased actomyosin ATPase in parallel with the reduction in maximal force produced at pCa 4. While the effective concentrations of SNP were very high, the SNP-mediated reduction in force and actomyosin ATPase activity at pCa 4 and Vo were reversed by treatment with the thiol-reducing agent DTT. This indicates that the SNP-mediated changes in force and actomyosin ATPase activity were related to modification of functionally significant contractile protein thiols. These results do not permit determination of which contractile proteins were affected by SNP-mediated thiol modification or whether more than one protein was modified. However the most reactive thiols in this system are the myosin head SH-1 and SH-2 thiols (6, 36), although other potential target proteins include tropomyosin, troponin T (9), troponin C (13, 28), and F-actin (24).
The relationship between force, actomyosin ATPase activity, and
Vo may be
analyzed by using Brenner's analytic model (4), which is based on the
Huxley two-state model of cross bridge cycling (15). The steady-state
fraction of cycling cross-bridges
(
fs) in the force-generating
state is given by Eq. 4
|
(4) |
|
(5) |
These results are consistent with earlier results in which force and stiffness were decreased after treatment with maleimide adducts (6, 31) or DTNB (36). When DTNB was used as the thiol-modifying reagent in permeabilized fast- and slow-twitch single fibers, the effects on force and stiffness were reversible (36). The relationship between degree of thiol modification on the myosin head, particularly of SH-1, force and stiffness reduction, and actomyosin ATPase activity is unclear in permeabilized single fibers (31). Actomyosin ATPase activity may be either increased or decreased depending on the degree of SH-1 and SH-2 modification. Force and stiffness, however, are consistently reduced by modification of the myosin head critical thiols. Further studies are required to clarify these relationships.
The force-pCa relationship of permeabilized fibers is also altered by treatment with a thiol-modifying reagent such as DTNB (36). The slope of the force-pCa relationship and the pCa50 were decreased in both fast-twitch (extensor digitorum longus) and slow-twitch (soleus) rat skeletal muscle single fibers (36). This work suggests that thiol modification of the myosin head may modulate the Ca2+-activation mechanism in permeabilized fibers, independent of any modification of other contractile proteins involved in Ca2+ regulation. In the present study, exposing permeabilized fibers to SNP also decreased both force at maximum [Ca2+] and the pCa50. The possibility that this result is due to local changes in fiber core Ca2+ buffering and pH reductions that are proportional to the actomyosin ATPase cannot be ruled out in this study (25).
Although the effective concentration of SNP required to appreciably decrease maximal force and actomyosin ATPase activity in permeabilized fibers was in the millimolar rather than the micromolar range, this does not necessarily exclude the possibility that S-nitrosylation reactions with contractile proteins occur in vivo and may be functionally significant. Hemoglobin, which is reportedly S-nitrosylated in vivo, requires millimolar concentrations of a NO donor over a 30-min period to achieve appreciable S-nitrosylation in vitro (17). Similarly, the ras oncogene product p21 is modified at Cys 113 and regulated by micromolar concentrations of NO in vivo, but it requires 0.3 mM and 1 mM concentrations of the NO donors S-nitroso-N-penicillamine and SNP, respectively, to achieve a similar extent of modification (23). This underscores the fact that not all NO donors or sources are equal but that effects observed at high concentrations with one, such as SNP, may mimic modifications that occur physiologically at much lower concentrations of NO. It was not feasible to examine the effects of NO itself in this system, since doing so would require exclusion of oxygen from the perfusion system. NO is unstable in O2-containing aqueous solutions, giving rise, ultimately, to nitrous acid, which would result in an uncontrolled pH effect on the perfusion buffers. In addition, NO is unable to participate in S-nitrosylation reactions in the absence of O2 (20). The effects of SNP on the contractile properties of permeabilized rabbit psoas fibers were, however, reversible with DTT, indicating that the reaction is, in part, thiol selective and that reversible thiol oxidation and possibly S-nitrosylation of contractile proteins had taken place.
In conclusion, the present results indicate that exposing permeabilized fibers to the NO donor SNP inhibits force, Ca2+ sensitivity, actomyosin ATPase activity and, to a lesser extent, decreases Vo. These inhibitory effects of SNP are reversed by DTT, indicating that the SNP-mediated reduction in force, Ca2+ sensitivity, actomyosin ATPase activity, and Vo are due to reversible oxidation of thiols on the contractile proteins. The results suggest the possibility of a cGMP-independent mechanism by which NO or NO donors may modulate skeletal muscle function under either normal or pathophysiological conditions, particularly those, such as sepsis, in which NO production is markedly increased.
ACKNOWLEDGEMENTS
This work was supported by National Heart, Lung, and Blood Institute Grants HL-34817 and HL-37680 (to G. C. Sieck).
FOOTNOTES
Address for reprint requests: W. J. Perkins, Dept. of Anesthesiology, Mayo Clinic, Rochester, MN 55905.
Received 12 August 1996; accepted in final form 22 May 1997.
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