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First published online October 7, 2008
Journal of Experimental Biology 211, 3323-3332 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018887
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Blood flow and metabolic regulation in seal muscle during apnea

Paul J. Ponganis1, Ulrike Kreutzer2, Torre K. Stockard1, Ping-Chang Lin2, Napapon Sailasuta3, Tuan-Khan Tran2, Ralph Hurd3 and Thomas Jue2,*

1 Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093, USA
2 Department of Biochemistry and Molecular Medicine, University of California Davis, Davis, CA 95616, USA
3 GE Medical Systems, Fremont, CA 94539, USA


Figure 1
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  		Fig. 1. Muscle blood flow (MBF) during six long apneas of an elephant seal. Apneic MBF decreases progressively but variably; occasional transient increases occur. At the end of apnea, MBF consistently increases prior to the first breath of eupnea. See Table 1 for a statistical summary. Note that MBF can also begin to decrease prior to the last breath of eupnea (apnea 1). Shaded area corresponds to eupnea period.

 

Figure 2
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  		Fig. 2. 1H NMR spectra of elephant seal muscle in vivo acquired during eupnea and apnea. 1H spectra of the deoxy-Mb proximal histidyl N{delta}H signal were recorded continuously for 25 min. Each spectrum required 1 min of signal averaging. During eupnea, the deoxy-Mb signal is not detected. Once apnea begins, the deoxy-Mb signal rises, indicating oxygen desaturation. As eupnea resumes, the signal decays rapidly, reflecting a restoration of the intracellular oxygen level.

 

Figure 3
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  		Fig. 3. The time course of MbO2 desaturation–resaturation during apnea to eupnea cycles. The oxymyoglobin (MbO2) saturation is derived from the calibrated proximal histidyl N{delta}H signal of deoxy-Mb. MbO2 saturation is plotted against time. Breaths are indicated by marks at the base of the graph. No deoxy-Mb signal is detectable during eupnea. During apnea, the MbO2 desaturates by 20%, as calibrated from the external reference sample. Shaded area corresponds to eupnea period.

 

Figure 4
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  		Fig. 4. Time course of 31P NMR spectra of elephant seal muscle acquired in vivo during an apneic episode. The 31P spectra were recorded continuously, each scan requiring 70 s of signal averaging. The spectra correspond to (a,b) eupneic state, (c–f) apneic state and (g,h) eupneic state. The 31P signals exhibit no change during the eupnea to apnea transition. Peak 1 denotes Pi; peak 2, PCr; and peaks 3, 4 and 5, the {gamma}, {alpha} and β signals of ATP, respectively.

 

Figure 5
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  		Fig. 5. 1H NMR diffusion-weighted spectra of the Val E11 signal of MbO2 from seal muscle at 25°C: A modified pulse PGSTE sequence detects the {gamma} CH3 Val E11 signal at –2.8 p.p.m. The peak intensity decreases as gradient field strength increases in the x direction: (a) 9.5 gauss cm–1 (1 gauss=104 tesla), (b) 23.8 gauss cm–1, (c) 47.5 gauss cm–1 and (d) 71.3 gauss cm–1.

 

Figure 6
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  		Fig. 6. Plots of the natural logarithm of the MbO2 Val E11 peak intensity at 25°C as a function of b where b=–{gamma}2G2{delta}2({Delta}–{delta}/3). The MbO2 signals reveal decreasing intensity with each stepwise increase in gradient field strength applied along the x direction. The natural logarithm plot of signal intensity as a function b yields a linear relationship with a regression coefficient of r2>0.99. Given the linear equation, the analysis has determined the Mb translational diffusion coefficient of 4.5±1.4x10–7 cm2 s–1 at 25°C.

 

Figure 7
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  		Fig. 7. Plots of Mb facilitated O2 diffusion vs free O2 flux as a function of PO2 at 25°C. The equation Formula describes the linear rise of free O2 flux with PO2. Krogh's diffusion coefficient, K0, is the proportionality constant and the slope. The straight line shows the rate of change at a K0 value of 2.52x10–5 ml O2 cm–1 min–1 atm–1 at 23°C. The broken line graphs the equation Formula, the Mb-facilitated O2 diffusion as a function of PO2, P50=1.5 mmHg (1 mmHg=0.133 kPa), CMb=3.8 mmol l–1 and DMb=4.5x10–7 cm2 s–1. The equipoise PO2 67 mmHg corresponds to the intersection of the two curves. Below 67 mmHg, the Mb contribution dominates.

 

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