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Oxygen-dependence of metabolic rate in the muscles of craniates
Authors:Leonard G Forgan  Malcolm E Forster
Institution:(1) New Zealand Institute for Plant and Food Research, P.O. Box 5114, Port Nelson, Nelson, 7043, New Zealand;(2) School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, 8140, New Zealand
Abstract:We present evidence that oxygen consumption (V\textO2 ) (V_{{{\text{O}}_{2} }} ) is oxygen partial pressure (P\textO2 ) (P_{{{\text{O}}_{2} }} ) dependent in striated muscles and P\textO2 P_{{{\text{O}}_{2} }} -independent in the vasculature in representatives of three craniate taxa: two teleost fish, a hagfish and a rat. Blood vessel V\textO2 V_{{{\text{O}}_{2} }} displayed varying degrees of independence in a P\textO2 P_{{{\text{O}}_{2} }} range of 15–95 mmHg, while V\textO2 V_{{{\text{O}}_{2} }} by striated muscle tissue slices from all species related linearly to P\textO2 P_{{{\text{O}}_{2} }} between 0 and 125 mmHg, despite V\textO2 V_{{{\text{O}}_{2} }} rates varying greatly between species and muscle type. In salmon red muscle, lactate concentrations fell in slices incubated at a P\textO2 P_{{{\text{O}}_{2} }} of either 30 or 100 mmHg, suggesting aerobic rather than anaerobic metabolism. Consistent with this finding, potential energy, a proxy of ATP turnover, was P\textO2 P_{{{\text{O}}_{2} }} -dependent. Our data suggest that the reduction in V\textO2 V_{{{\text{O}}_{2} }} with falling P\textO2 P_{{{\text{O}}_{2} }} results in a decrease in ATP demand, suggesting that the hypoxic signal is sensed and cellular changes effected. Viability and diffusion limitation of the preparations were investigated using salmon cardiac and skeletal muscles. Following the initial P\textO2 P_{{{\text{O}}_{2} }} depletion, reoxygenation of the Ringer bathing salmon cardiac muscle resulted in V\textO2 \texts V_{{{\text{O}}_{2} }} {\text{s}} that was unchanged from the first run. V\textO2 V_{{{\text{O}}_{2} }} increased in all muscles uncoupled with p-trifluoromethoxylphenyl-hydrazone (FCCP) and 2,4-dinitrophenol (DNP). Mitochondrial succinate dehydrogenase activity, quantified by reduction of 3-(4,5-dimethylthiazol)-2,5-diphenyl-2H-tetrazolium bromide (MTT) to formazan, was constant over the course of the experiment. These three findings indicate that the tissues remained viable over time and ruled out diffusion-limitation as a constraint on V\textO2 V_{{{\text{O}}_{2} }} .
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