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1 School of Nursing2 Department of Molecular and Integrative Physiology3 School of Allied Health, Nurse Anaesthesia4Department of Preventive Medicine and Public Health5 Department of Molecular and Integrative Physiology, University of Kansas Medical Center, 3901 Rainbow Blvd, Kansas City, KS 66160-7504, USA
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Abstract |
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(Received 25 January 2006;
accepted after revision 25 March 2006; first published online 27 April 2006)
Corresponding author J. D. Pierce: University of Kansas Medical Center, School of Nursing, 3901 Rainbow Blvd, Mail stop no. 4043, Kansas City, KS 66160, USA. Email: jpierce{at}kumc.edu
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Introduction |
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Dopamine (DA) is a drug commonly used intravenously in the ICU to treat haemodynamic imbalances in shock due to myocardial infarction, trauma, septicemia, open heart surgery, renal failure and congestive heart failure. Often the most critically ill ICU patients on MV also receive intravenous DA. Previously, we found in an animal model that low-dose DA (2 µg/kg/min) prevented and treated diaphragmatic contractile dysfunction during inspiratory resistance loading (Pierce et al. 2002). This finding has potential clinical significance for patients on MV because it provides a possible intervention to prevent diaphragmatic dysfunction and to assist patients with weaning from MV.
Muscle fibres continually produce both reactive oxygen species (ROS) and nitric oxide (NO). Both of these types of free radicals play critical roles in contractile regulation. Muscle dysfunction occurs when there is an increase in ROS or NO levels resulting in muscle fatigue (Smith & Reid, 2006). Free radicals, specifically ROS, have been shown to be generated during strenuous contractions of the diaphragm (Kolbeck et al. 1997; Supinski, 1998; Nethery et al. 2000). There are several mechanisms and pathways in which free radicals may produce diaphragm dysfunction (Supinski, 1998). It has also been demonstrated that administration of free radical scavengers, e.g. N-acetylcysteine (Supinski et al. 1997; Travaline et al. 1997), catalase (Fujimura et al. 2000), dimethyl sulphoxide (Fujimura et al. 2000) and superoxide dismutase (Callahan et al. 2001), prevents diaphragm dysfunction. Thus it may be possible, to prevent diaphragm dysfunction pharmacologically through the administration of free radical scavengers.
Apoptosis (programmed cell death) can be induced by ROS-induced mitochondrial release of proapoptotic factors such as cytochrome c and apoptosis-inducing factor (AIF; Adhihetty et al. 2005). In addition, ROS can act as a signal for regulation of gene transcription (Palmer & Paulson, 1997; Simon et al. 2000) and activation of caspase 3 that can result in apoptosis (Powers et al. 2005). Although apoptosis may occur via several mechanisms, mitochondria have recently been implicated as major regulatory centres for apoptosis (Cai et al. 1998; Green & Kroemer, 1998; Green & Reed, 1998). It has been suggested that cellular stimuli, such as high levels of calcium or reactive oxygen intermediates, may trigger apoptosis by the cytochrome c-dependent pathway (Adhihetty et al. 2005).
Dopamine has been shown to be an effective scavenger of superoxide (·O2–) and hydroxyl radicals (·HO; Yen & Hsieh, 1997). One possible explanation is that DA is an uncomplexed catecholamine which has been demonstrated to be a superoxide scavenger (Siraki et al. 2000). The ability of the catechol ring to scavenge free radicals is attributed to the ability of the structure to donate electrons (Yen & Hsieh, 1997). In addition, several investigators have found that using DA receptor agonists, such as bromocriptine (Yoshikawa et al. 1994), lisuride, pergolide and R-apomorphine, exerts a neuroprotective action and acts as a potent antioxidant (Youdim et al. 2000). However, others have demonstrated that DA also can increase oxidative stress in neurones (Spencer et al. 1996; Mazzio & Soliman, 2004). Thus, it appears that DA can either be a free radical scavenger or a free radical generator, which may depend on the DA concentration or the type of tissue.
The data from our previous in vivo experiments (Pierce et al. 2002) suggest that the increase in diaphragmatic blood flow from DA administration resulted in an increase in diaphragm O2 availability that may have decreased free radical formation, thereby attenuating diaphragm dysfunction. Subsequently, in vivo experiments in our laboratory demonstrated a significant reduction in the number of apoptotic nuclei in the diaphragm with the administration of low-dose DA (Pierce et al. 2004b). This effect of DA on apoptosis is probably due to increased diaphragmatic blood flow preventing a cascade of intricate molecular pathways that stimulate apoptosis and/or DA acting as a scavenger of free radicals. In the present in vitro study, we hypothesized that under conditions of constant O2 availability (no diaphragmatic blood flow), DA would decrease apoptosis. In addition, we hypothesized that DA would attenuate the decrease in diaphragmatic contractile performance associated with repetitive isometric contractions.
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Methods |
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The study was conducted according to procedures approved by the University of Kansas Medical Center Institutional Animal Use and Care Committee and followed the guidelines for animal experiments in accordance with the Guide for the Care and Use of Laboratory Animals. Experiments were performed using adult male Sprague–Dawley rats (330–450 g). Animals were individually housed, maintained on a 12 h–12 h light–dark cycle with free access to water and rat chow.
Animals were anaesthetized by intraperitoneal injection of sodium pentobarbitone (70 mg kg–1). When a surgical plane of anaesthesia was achieved, the trachea was exposed and cannulated. The animal was placed on controlled mechanical ventilation (Harvard Apparatus, Hollister, MI, USA), the diaphragm excised, and the animal was killed with a lethal overdose of sodium pentobarbitone.
The diaphragm was then placed in a continuously oxygenated dissecting dish containing Krebs–Ringer solution (KR): pH 7.4, 120 mM NaCl, 5 mM KCl, 2.5 mM CaCl2, 0.2 mM MgCl, 1.3 mM NaH2PO4, 0.7 mM Na2H2PO4, 24 mM NaHCO3, 8.9 mM glucose, 40 U l–1 insulin and 16 mg l–1 racemic tubocurarine chloride (Sigma, St Louis, MO, USA). The KR solution was equilibrated with 5% CO2 and varying O2 concentrations (10, 21 or 95%), with the balance being nitrogen. The diaphragm was divided along the central tendon, and a longitudinal portion of the costal diaphragm (approximately 4 mm x 10 mm) was dissected from each hemidiaphragm. Clamps were applied to the ends of two muscle strips, which were suspended vertically in separate 30 ml water-jacketed organ baths (Schuler Organ Bath, Harvard Apparatus) and maintained at 30°C. One end of the muscle was attached to a rigid support and the other to an isometric force transducer (Hugo Sachs Electronic (HSE) Force Transducers F30, type 372, March-Hugstetter, Germany). One diaphragm strip was placed in KR only (KR group) and the other in KR plus 100 µM DA (DA group). The organ bath solutions were continuously equilibrated with 10, 21 or 95% O2 throughout the duration of the experiment. In preliminary experiments, 1 or 10 µM DA had no effect on diaphragm performance when equilibrated with 10 or 21% O2.
The HSE F30 is a sensitive and reliable isometric force transducer suitable for use with very small muscle specimens. The ultra-low vertical displacement of the transducer means that we were able to obtain true isometric measurements. The Programmable Stimulator Module (PSM) for PLUSYS System (HSE) is a combination of stimulator and measurement system in one mainframe. The PSM sets and produces a constant current with alternating polarity output.
After mounting the muscle, muscle contraction was produced using electrical field stimulation provided by two platinum electrodes adjacent to the muscle strip. A constant current intensity of 200 mA and 2 ms duration was used throughout the experiment. The pulse generator provided reverse polarity. This stimulus was twice that was required to elicit maximum contraction. The optimal length (L0) was determined by incrementally increasing the resting force (preload) until peak isometric twitch force was obtained. This resting force was maintained throughout the experiment. The isometric force signals were digitized by HSE DAQ software package ACAD and stored for later analysis. Twitch contractions were produced at a frequency of 0.5 Hz (30 min–1). In experiments using subtetanic stimulation, 30 Hz stimuli of 250 ms duration were applied every 2 s.
At the end of the experiment, diaphragm strip lengths were measured and weighed, enabling us to calculate the cross-sectional area (CSA) in centimetres squared (Nethery et al. 1999). The two muscle performance indices measured throughout the experiments were: isometric developed force (DF; in N cm–2) and maximum rate of isometric force development (dF/dtmax; in N cm–2 s–1).
Each diaphragm strip was homogenized for apoptosis analysis. Although the homogenate contained cell types other than myofibres, the predominance of the skeletal muscle fibres, coupled with these cells being multinucleated, resulted in a high probability that the nuclei examined originated from diaphragm skeletal muscle fibres. The muscle strips were minced and suspended in 2.5 ml KR with 200 µl of antioxidant and 300 µl each of trypsin (15 mg) and collagenase (0.3 mg). The antioxidant consisted of 45 mg of L-ascorbate (Fisher Scientific, Pittsburgh, PA, USA), 75 mg L-glutathione (Sigma), 4.5 mg butylated hyroxyanisole (Sigma), 2.25 ml phosphate-buffered saline (Sigma) and 0.25 ml dimethyl sulphoxide (Fisher Scientific). The minced diaphragms were vortexed and incubated at 37°C for 30 min. The supernatant was transferred to another tube and centrifuged at 3600g for 30 min. The pellet was resuspended in 2 ml of KR. A 250 µl aliquot was added to a 1 ml microcentrifuge tube containing 2 µl (0.2 ng) of ethidium bromide (EB) and 2 µl (0.2 ng) Acridine Orange (AO; Sigma-Aldrich, St Louis, MO, USA). The sample was vortexed and 20 µl placed on a microscope slide and mounted on the fluorescence microscope (Nikon Eclipse TE 2000S, Melville, NY, USA) platform.
Acridine Orange stained viable nuclei green, while EB stained only apoptotic nuclei orange. Thus, when both dyes were added, viable nuclei appeared green while apoptotic nuclei appeared orange (McGahon et al. 1995). Both EB and AO images were captured at x400, merged, stored, and analysed using the Boyce software program (Boyce Scientific Digitive 3c Analysis System, St Louis, MO, USA; Fig. 1). The software program provided an interpretation of colour images based on hue number. For instance, a normal undamaged nucleus visually appeared green in colour and, when selected by the reader, the software program assigned a hue value between 90 and 120. However, an apoptotic nucleus appeared visually orange in colour, the hue value ranging from 25 to 89. Necrotic nuclei were red in colour and had a hue value ranging from 0 to 24. The software automatically provided a database with all hue values for nuclei classification. A total nuclei count of 300 was used for all diaphragm samples. This technique for quantifying the nuclear images using an automated visual count versus human visual identification was validated in a previous study (Goodyear-Bruch et al. 2005).
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Six diaphragm muscle strips from three animals were incubated in muscle baths for 65 min in 95% O2 with minimal stimulation (five subtetanic stimulations during each the four time periods). We also evaluated muscle performance in 95% O2 with 10 min of continuous subtetanic isometric contractions (n = 8).
Twelve muscle strips from six animals were equilibrated in 21% O2 with minimal stimulation (five subtetanic stimulations at each the four time periods) in muscle baths for 65 min. Experiments using single-twitch stimulations (n = 6) and subtetanic stimulation (n = 6) were performed with the diaphragm in 21% O2. The durations of the stimulation during the various time periods were the same as previously noted.
To evaluate diaphragm muscle contractility and apoptosis in a hypoxic environment, we used 10% O2 in the tissue baths (n = 8). The experimental time periods and the subtetanic stimulation parameters were the same as in the 21% O2 experiments.
Statistical analysis
Non-parametric statistics were used because the sample size was small and data were not always normally distributed. Statistical comparisons for within-group percentage of control DF and dF/dtmax were performed using the Wilcoxon rank sum non-parametric test. The Mann–Whitney U test was used to determine the differences of the percentage control DF and dF/dtmax between the KR and DA groups during each of the four time periods. For both tests, significance was set at the level of P < 0.05.
The same two non-parametric tests (Wilcoxon rank sum and Mann–Whitney U) were used for within- and between-group comparisons of normal, apoptotic and necrotic nuclei. Measurements were expressed as means of the percentage for nuclei types ± S.D. All results were considered statistically significant at P < 0.05.
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Results |
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There were no statistically significant differences for absolute values in period 1 in diaphragm subtetanic DF and dF/dtmax between the KR and DA groups at each O2 concentration (10 and 21%; Table 2). Thus, muscle performance parameters were calculated as a percentage of control values. To examine the stability of the preparation in 21% O2, we measured muscle parameters using only five subtetanic stimulations during each of the four experimental time periods. These results are summarized in Table 3A. Following 40 min recovery (period 4), both muscle performance indices were significantly decreased with respect to period 1. It is noteworthy, with the exception of DF during period 4, that DF and dF/dtmax in the DA group were significantly greater than in the KR group. Apoptosis in the 21% O2 non-stressed diaphragms is summarized in Fig. 2A (N = 6). The KR group had 89.5 ± 7.3% normal nuclei and 10.4 ± 7.1% apoptotic nuclei. There were 95.6 ± 4.1% normal nuclei and 4.2 ± 3.7% apoptotic nuclei in the DA group. The differences between the two groups were not statistically different (P = 0.180 for normal nuclei and P = 0.132 for apoptotic nuclei).
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In Fig. 2B (21% O2 twitch stimulation), there were significantly higher numbers of normal nuclei (96.1 ± 3.2%) in the DA group than in the KR group (72.7 ± 9.0%, n = 6, P = 0.002). Corresponding, the percentages of apoptotic and necrotic nuclei in the DA group were statistically less than in the KR group (P = 0.002 and P = 0.015, respectively).
In Table 3C (21% O2, subtetanic stimulation), muscle performance in the DA group during period 2 was significantly greater than in the KR group, again suggesting a positive inotropic effect of DA (P < 0.05). Subtetanic stimulation resulted in highly significantly decreases in muscle performance in both groups (period 3). Muscle performance following 40 min of rest (period 4) was significantly increased in both groups with respect to period 3 (P < 0.05).
In the 21% O2 subtetanic stimulation experiments, DA markedly decreased the extent of apoptosis (Fig. 2C). There were significantly greater percentages of normal nuclei (P = 0.002) and significantly less apoptotic (P = 0.002) and necrotic nuclei (P = 0.015) in the DA group versus the KR group (n = 6).
In the KR group, DF and dF/dtmax during period 2 were significantly less than during period 1 (Table 4, 10% O2, subtetanic stimulation), whereas in the DA group these indices were slightly increased at this time, resulting in muscle contractility being significantly greater than in the KR group (P = 0.028). In both groups, all muscle performance indices following 10 min of stimulation and 40 min recovery were statistically significantly less than in period 1. There were no statistically significant differences in diaphragm performance between the two groups following subtetanic stimulation (period 3) and 40 min recovery (period 4).
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Discussion |
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In these experiments, we did not explicitly measure free radical generation. Free radicals may have their deleterious effects on the diaphragm through numerous intracellular processes. Oxidants can often alter Ca2+ release from the sarcoplasmic reticulum and can compromise excitation–contraction coupling in the diaphragm (Darnley et al. 2001). Several investigators have demonstrated that apoptosis can be evoked when ROS-induced mitochondria initiate the release of oxidants from the cells (Adhihetty et al. 2005; Pletjushkina et al. 2006; Valencia & Kochevar, 2006). In addition, other investigators have found that low intracellular partial pressure of O2 induces a burst of oxidants, and that antioxidants have a protective influence on muscle function (Wright et al. 2005; Zuo & Clanton, 2005). In this in vitro preparation, there was no diaphragmatic blood flow, so O2 delivery was determined by the O2 concentration of the bath solution, resulting in a constant O2 availability throughout the experiment. In the 10% and 21% O2 experiments, we believe free radicals were generated during muscle contraction and thereby promoting stimulation of apoptotic pathways. Future experimentation will be directed at measuring, in the diaphragm the type and amount of free radicals under low O2 concentrations.
Using isolated diaphragm muscle strips superfused with 95% O2, there was less than 5% apoptosis accompanying subtetanic stimulation, suggesting that this O2 concentration was sufficient to circumvent an O2 deficit. In contrast, superfusion with 21 or 10% O2 resulted in significant diaphragmatic apoptosis with either twitch or subtetanic stimulation. This may be a result of limited O2 availability resulting in free radical formation. Administration of 100 µM DA markedly attenuated diaphragmatic apoptosis. This suggests that DA may indirectly or directly effect different cellular processes that prevent apoptosis by interrupting ROS-induced mitochondrial release of the apoptotic factors such as cytochrome c and apoptosis-inducing factor (AIF).
Stimulation of ß2-adrenoreceptors produces antiapoptotic signals in cardiac myocytes (Communal et al. 1999; Patterson et al. 2004) via the inhibitory G-protein (Communal et al. 1999). Thus, stimulation of ß2-adrenoreceptors in myocytes protects against apoptosis (Chesley et al. 2000) and may impact mortality (Patterson et al. 2004). ß2-Adrenoreceptors have been identified in diaphragm skeletal muscle (Collet et al. 1998). It is well established that high concentrations of DA activate ß2-adrenoreceptors (Service, 2001). Thus, our results of decreased apoptosis in 100 µM DA may be caused by DA binding to ß2-adrenoreceptors, resulting in activation of an antiapoptotic pathway (Patterson et al. 2004).
Other investigators have observed that DA scavenges free radicals in systems devoid of ß2-adrenoreceptors (Yen & Hsieh, 1997; Kang et al. 1998; Gassen, 1999). The scavenging activity of DA is attributed to the 1,2-hydroxyl group positions on the phenolic ring and the amine side-chain being electron donors (Yen & Hsieh, 1997). However, there are studies indicating that DA produces free radicals (Spencer et al. 1996; Mazzio & Soliman, 2004). Whether DA is a scavenger or generator of free radicals may be dependent upon the administered concentration. Our observation of a reduction in apoptosis indicates that 100 µM DA may act as a free radical scavenger in low-oxygen conditions. During exposure to hypoxia both intracellular and extracellular antioxidants improved muscle function and protected cell function (Mohanraj et al. 1998). Future studies should be directed at determining whether the antiapoptotic effect of 100 µM DA is via ß2-adrenoreceptor activation, scavenging of free radicals and/or non-specific binding.
After 15 min of DA equilibration (period 2) in 10 or 21% O2, muscle performance was greater than in KR-only groups. To our knowledge, there are no published studies indicating this DA effect on muscle performance is mediated through diaphragm muscle DA adrenoreceptors. Dopamine only attenuated the decline in diaphragm contractility between periods 1 and 2 at a dose of 100 µM DA, which may be a result of DA binding to ß2-adrenoreceptors (Collet et al. 1998). In addition, the tendency for muscle performance following 10 min of stimulation (period 3) and 40 min recovery (period 4) to be greater in the DA groups than the KR groups also may be attributable to ß2-adrenoreceptor activation. Our data are in agreement with van der Heijden et al. (1999), who found that the ß2-agonist salbutamol increased diaphragm force development in hypoxic conditions.
Following 15 min of equilibration with 10% O2 (period 2), there was a significant decline in DF and dF/dtmax in the KR group (Table 4). This decrease in muscle performance may have occurred owing to decreased O2 availability resulting in changes in the cytoplasmic environment. In addition, the reduced O2 supply may have resulted in increased free radical formation, thus contributing to the decline in diaphragm contractility. In contrast, administration of DA during this time resulted in no decline in muscle performance. The difference in muscle performance parameters between the two groups could be a result of DA activating adrenoreceptors and/or scavenging free radicals.
Following 40 min of rest in 21% O2 (Table 3B), twitch DF and dF/dtmax in the KR group were 49% of control values (period 1). These results are similar to the finding of van der Heijden et al. (1999) that after 60 min of isometric twitch contraction, muscle performance parameters decreased to 40–54% of control values.
Dopamine had no effect on diaphragm DF and dF/dtmax following 10 min of stimulation or following 40 min of recovery at the stimulation frequencies of 0.5 (twitch) and 30 Hz (subtetanic). It seems likely that similar relative force productions with and without DA would occur at higher stimulation frequencies, including maximal tetanic stimulation.
In previous in vivo studies in our laboratory, DA prevented and treated diaphragm fatigue (Pierce et al. 2002) and decreased apoptosis (Pierce et al. 2004a,b). During the in vivo experiments, diaphragm blood flow increased, thus increasing O2 availability to the muscle during increased inspiratory resistance loading. However, in this in vitro study there was no blood flow and O2 (21 and 10%) was varied based on the concentration available within the isolated tissue bath. We found that DA did not prevent diaphragm muscle decline, as we found in the in vivo studies. However, diaphragm apoptosis was prevented when the muscle was superfused with 95% O2 or when it was superfused with 21 or 10% O2 with the administration of DA. These data suggest that when the muscle is stimulated and there is lower O2 availability to the diaphragm, apoptosis occurs. Thus, without diaphragmatic blood flow, DA may inhibit complex apoptotic mechanisms, stimulate antiapoptotic pathways and/or act as a free radical scavenger.
In summary, we observed that in 10 and 21% O2, DA decreased diaphragmatic apoptosis, perhaps by directly scavenging free radicals, inhibiting apoptotic pathways and/or activating the ß2-adrenoreceptor antiapoptotic pathway. Dopamine prevented a decline in muscle function in the resting diaphragm (periods 1 and 2), possibly by activating ß2-adrenoreceptors. The observation that DA markedly attenuated diaphragmatic apoptosis but did not prevent the decline in muscle performance accompanying isometric contractions indicates a lack of correlation between muscle performance and apoptosis. This dissociation is in agreement with Jiang et al. (2001), who reported that free radical scavengers (superoxide dismutase (SOD) and N-acetylcysteine (NAC)) prevented diaphragm injury while only partly preserving muscle performance. Further studies are needed to delineate the mechanism(s) by which DA attenuates diaphragm apoptosis.
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References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Cai J, Yang J & Jones DP (1998). Mitochondrial control of apoptosis: the role of cytochrome c. Biochim Biophys Acta 1366, 139–149.[Medline]
Callahan
LA, Nethery
D, Stofan
D, DiMarco
A
&
Supinski
G (2001). Free radical-induced contractile protein dysfunction in endotoxin-induced sepsis. Am J Respir Cell Mol Biol
24, 210–217.
Chesley
A, Lundberg
MS, Asai
T, Xiao
RP, Ohtani
S, Lakatta
EG
&
Crow
MT (2000). The beta(2)-adrenergic receptor delivers an antiapoptotic signal to cardiac myocytes through Gi-dependent coupling to phosphatidylinositol 3'-kinase. Circ Res
87, 1172–1179.
Collet F, Feve B, Frisdal E, Pavoine C, Pecker F & Atlan G (1998). Pharmacological and molecular characterisation of beta-adrenoceptors in adult rat diaphragm muscle. Respir Physiol 112, 1–12.[CrossRef][Medline]
Communal
C, Singh
K, Sawyer
DB
&
Colucci
WS (1999). Opposing effects of beta(1)- and beta(2)-adrenergic receptors on cardiac myocyte apoptosis: role of a pertussis toxin-sensitive G protein. Circulation
100, 2210–2212.
Darnley GM, Duke AM, Steele DS & MacFarlane NG (2001). Effects of reactive oxygen species on aspects of excitation–contraction coupling in chemically skinned rabbit diaphragm muscle fibres. Exp Physiol 86, 161–168.[Abstract]
Fujimura
N, Sumita
S, Aimono
M, Masuda
Y, Shichinohe
Y, Narimatsu
E
&
Namiki
A (2000). Effect of free radical scavengers on diaphragmatic contractility in septic peritonitis. Am J Respir Crit Care Med
162, 2159–2165.
Gassen MYM (1999). Free radical scavengers: chemical concepts and clinical relevance. J Neural Transm Suppl 56, 193–210.[Medline]
Gayan-Ramirez
G
&
Decramer
M (2002). Effects of mechanical ventilation on diaphragm function and biology. Eur Respir J
20, 1579–1586.
Goodyear-Bruch C, Simon K, Hall S, Mayo MS & Pierce JD (2005). Comparison of a visual to a computer-assisted technique for detecting apoptosis. Biol Res Nurs 6, 180–186.[Abstract]
Green D & Kroemer G (1998). The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol 8, 267–271.[CrossRef][Medline]
Green
DR
&
Reed
JC (1998). Mitochondria and apoptosis. Science
281, 1309–1312.
Guide for the Care and Use of Laboratory Animals (1996). Washington D.C., U S A. National Academy of Sciences.
Jiang
TX, Reid
WD
&
Road
JD (2001). Free radical scavengers and diaphragm injury following inspiratory resistive loading. Am J Respir Crit Care Med
164, 1288–1294.
Kang MY, Tsuchiya M, Packer L & Manabe M (1998). In vitro study on antioxidant potential of various drugs used in the perioperative period. Acta Anaesthesiol Scand 42, 4–12.[Medline]
Kolbeck
RC, She
ZW, Callahan
LA
&
Nosek
TM (1997). Increased superoxide production during fatigue in the perfused rat diaphragm. Am J Respir Crit Care Med
156, 140–145.
McGahon AJ, Martin SJ, Bissonnette RP, Mahboubi A, Shi Y, Mogil RJ, Nishioka WK & Green DR (1995). The end of the (cell) line: methods for the study of apoptosis in vitro. Meth Cell Biol 46, 153–185.[Medline]
Mazzio EA & Soliman KF (2004). Glioma cell antioxidant capacity relative to reactive oxygen species produced by dopamine. J Appl Toxicol 24, 99–106.[Medline]
Mohanraj
P, Merola
AJ, Wright
VP
&
Clanton
TL (1998). Antioxidants protect rat diaphragmatic muscle function under hypoxic conditions. J Appl Physiol
84, 1960–1966.
Nethery
D, Callahan
LA, Stofan
D, Mattera
R, DiMarco
A
&
Supinski
G (2000). PLA2 dependence of diaphragm mitochondrial formation of reactive oxygen species. J Appl Physiol
89, 72–80.
Nethery
D, DiMarco
A, Stofan
D
&
Supinski
G (1999). Sepsis increases contraction-related generation of reactive oxygen species in the diaphragm. J Appl Physiol
87, 1279–1286.
Palmer HJ & Paulson KE (1997). Reactive oxygen species and antioxidants in signal transduction and gene expression. Nutr Rev 55, 353–361.[Medline]
Patterson AJ, Zhu W, Chow A, Agrawal R, Kosek J, Xiao RP & Kobilka B (2004). Protecting the myocardium: a role for the beta(2) adrenergic receptor in the heart. Crit Care Med 32, 1041–1048.[CrossRef][Medline]
Pierce
JD, Clancy
RL, Smith-Blair
N
&
Kraft
R (2002). Treatment and prevention of diaphragm fatigue using low-dose dopamine. Biol Res Nurs
3, 140–149.
Pierce JD, Goodyear-Bruch C, Jegathesan J & Clancy R (2004a). Diaphragm apoptosis: alleviation by dopamine. Crit Care Med 32, A121.
Pierce JD, Jegathesan J, Arnett MD, Reed GD, Masure RD & Clancy RD (2004b). Dopamine alleviation of reactive oxygen species mediated diaphragm fatigue. 2004 Experimental Biology meeting abstract [accessed at http://select.biosis.org/faseb]. FASEB Journal 18, abstract no. 702.702.
Pletjushkina OY, Fetisova EK, Lyamzaev KG, Ivanova OY, Domnina LV, Vyssokikh MY, Pustovidko AV, Alexeevski AV, Alexeevski DA, Vasiliev JM, Murphy MP, Chernyak BV & Skulachev VP (2006). Hydrogen peroxide produced inside mitochondria takes part in cell-to-cell transmission of apoptotic signal. Biochemistry (Mosc) 71, 60–67.[CrossRef][Medline]
Powers
SK, Kavazis
AN
&
DeRuisseau
KC (2005). Mechanisms of disuse muscle atrophy: role of oxidative stress. Am J Physiol Regul Integr Comp Physiol
288, R337–R344.
Service AHF (2001). Dopamine. In American Hospital Formulary Service, pp. 1227–1229. American Society of Health-System Pharmacist, Bethesda, MD, USA.
Shanely
RA, Coombes
JS, Zergeroglu
AM, Webb
AI, Powers
SK (2003). Short-duration mechanical ventilation enhances diaphragmatic fatigue resistance but impairs force production. Chest, 123(1), 195–201.
Simon HU, Haj-Yehia A & Levi-Schaffer F (2000). Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415–418.[CrossRef][Medline]
Siraki AG, Smythies J & O'Brien PJ (2000). Superoxide radical scavenging and attenuation of hypoxia-reoxygenation injury by neurotransmitter ferric complexes in isolated rat hepatocytes. Neurosci Lett 296, 37–40.[CrossRef][Medline]
Smith MA & Reid MB (2006). Redox modulation of contractile function in respiratory and limb skeletal muscle. Respir Physiol Neurobiol 151, 229–241.[CrossRef][Medline]
Spencer JP, Jenner A, Butler J, Aruoma OI, Dexter DT, Jenner P & Halliwell B (1996). Evaluation of the pro-oxidant and antioxidant actions of L-DOPA and dopamine in vitro: implications for Parkinson's disease. Free Radic Res 24, 95–105.[Medline]
Supinski G (1998). Free radical induced respiratory muscle dysfunction. Mol Cell Biochem 179, 99–110.[CrossRef][Medline]
Supinski
G, Stofan
D, Ciufo
R
&
DiMarco
A (1997). N-Acetylcysteine administration alters the response to inspiratory loading in oxygen-supplemented rats. J Appl Physiol
82, 1119–1125.
Tobin
MJ, Jubran
A
&
Laghi
F (2001). Patient–ventilator interaction. Am J Respir Crit Care Med
163, 1059–1063.
Travaline
JM, Sudarshan
S, Roy
BG, Cordova
F, Leyenson
V
&
Criner
GJ (1997). Effect of N-acetylcysteine on human diaphragm strength and fatigability. Am J Respir Crit Care Med
156, 1567–1571.
Valencia A & Kochevar IE (2006). Ultraviolet A induces apoptosis via reactive oxygen species in a model for Smith–Lemli–Opitz syndrome. Free Radic Biol Med 40, 641–650.[CrossRef][Medline]
van der Heijden
HFM, Heunks
LMA, Folgering
H, van Herwaarden
CLA
&
Dekhuijzen
PNR (1999). beta2-Adrenoceptor agonists reduce the decline of rat diaphragm twitch force during severe hypoxia. Am J Physiol Lung Cell Mol Physiol
276, L474–L480.
Vassilakopoulos
T
&
Petrof
BJ (2004). Ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med
169, 336–341.
Wright
VP, Klawitter
PF, Iscru
DF, Merola
AJ
&
Clanton
TL (2005). Superoxide scavengers augment contractile but not energetic responses to hypoxia in rat diaphragm. J Appl Physiol
98, 1753–1760.
Yen GC & Hsieh CL (1997). Antioxidant effects of dopamine and related compounds. Biosci Biotechnol Biochem 61, 1646–1649.[Medline]
Yoshikawa T, Minamiyama Y, Naito Y & Kondo M (1994). Antioxidant properties of bromocriptine, a dopamine agonist. J Neurochem 62, 1034–1038.[Medline]
Youdim MB, Gassen M, Gross A, Mandel S & Grunblatt E (2000). Iron chelating, antioxidant and cytoprotective properties of dopamine receptor agonist; apomorphine. J Neural Transm Suppl 58, 83–96.
Zuo
L
&
Clanton
TL (2005). Reactive oxygen species formation in the transition to hypoxia in skeletal muscle. Am J Physiol Cell Physiol
289, C207–C216.
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