| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
LETTERS TO THE EDITOR
35% of maximal isometric force; 2–10 s continuous contractions). We suggested that ion pumps, primarily Ca2+-ATPase, accounted for the remaining ATP utilization, although this was not directly measured. We provided calculations based on stated assumptions, as well as other evidence from the literature in support of this explanation. Barclay and Loiselle (2) express skepticism regarding our suggested high relative contribution of Ca2+-pumping based on: i) heat measurements in fatigued muscles and muscles exposed to dantrolene (to inhibit SR Ca2+ release); ii) estimates of Ca2+ release per stimulus pulse; and iii) belief that our ATP splitting per cross bridge would be only one-quarter the value previously assumed. We address each of these points.
i) Heat production occurs in proportion to the amount of ATP split, and when heat measurements are used in combination with the stretch technique, extrapolation to zero force allows for the partitioning of heat into tension-dependent (cross bridges) and tension-independent (primarily SR Ca2+-ATPase) components. Barclay (1) and Wendt and Barclay (9) used the stretch technique to study mouse extensor digitorum longus (EDL) muscles and demonstrated that the heat associated with the tension-independent component amounted to 35% of total in fatigued muscles and 42% in dantrolene-treated muscles (control = 33%), respectively. These findings appear to be in disagreement with our estimate of Ca2+ pumping during submaximal contractions. It should be noted, however, that the heat measurements were performed during short contraction intervals (0.2–0.5 s), whereas our measurements (using BTS) were performed during longer periods (2–10 s). Earlier studies have shown that the percent contribution of the non-tension-dependent components to ATP splitting increases as contraction duration is prolonged in mouse EDL muscles (4). Another potential factor to consider is that we used BTS, whereas the cited studies employed the stretch technique. However, why BTS and stretch would yield fairly concordant results during conditions of maximal force, but not during submaximal force, is unclear.
ii) Barclay and Loiselle (2) suggest that the amount of Ca2+ released per pulse (action potential) would result in a much lower Ca2+ pumping rate than we estimate. The actual amount of total Ca2+ released and the activity of the Ca2+ pump cannot be directly measured in intact muscle fibers. Estimates of these parameters generally depend on modeling. Based on the Ca2+ release values given in the cited study (at 16°C), one can calculate that ATP splitting by the Ca2+ pump would range from 1.6 to 17.3 mM ATP during the submaximal 2-s contraction (we estimate 21.4 mM). Clearly, the estimated Ca2+ release (and hence Ca2+ pump) values will depend on the model employed with its inherent assumptions.
iii) Barclay and Loiselle (2) suggest that if cross bridges account for only 20% of energy use, then the rate of ATP splitting per cross bridge must be one-quarter the value previously assumed. However, they do not state what the assumed value is. Indeed, the value varies markedly depending on the conditions studied (e.g., contraction duration, type of contraction, temperature, fiber type, etc.). If we assume that at 35% of maximal isometric force only 35% of the cross bridges are functioning and a myosin subfragment I concentration of 150 µM (7), then ATP splitting per cross bridge would amount to 65, 34, and 21 s–1 during the 2-, 5-, and 10-s contractions, respectively, at 30°C. These values are similar to or higher than those reported in the literature for isometric contractions after adjusting for temperature (assuming a Q10 of 2.5 for myosin ATPase) (3, 5, 6, 8, 10).
We find the skepticism expressed by Barclay and Loiselle and the exchange of views in these letters to be refreshing and hope that this exchange will stimulate physiologists to take a more active interest in the field of muscle energetics. Ultimately, however, independent verification in the form of hard data collected during relevantly designed experiments will be required to settle the issue.
FOOTNOTES
Address for reprint requests and other correspondence: A. Katz, Dept. of Physiology and Pharmacology, Karolinska Institutet, Von Eulers väg 8, 171 77 Stockholm, Sweden (e-mail: abram.katz{at}ki.se)
REFERENCES
1. Barclay CJ. Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J Physiol 497: 781–794, 1996.[ISI][Medline]
2. Barclay CJ, Loiselle DS. Can activation account for 80% of skeletal muscle energy use during isometric contraction? Am J Physiol Cell Physiol 292: C612, 2007.
3. Crow MT, Kushmerick MJ. Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol 79: 147–166, 1982.
4. Crow MT, Kushmerick MJ. Correlated reduction of velocity of shortening and the rate of energy utilization in mouse fast-twitch muscle during a continuous tetanus. J Gen Physiol 82: 703–720, 1983.
5. Elzinga G, Lannergren J, Stienen GJ. Stable maintenance heat rate and contractile properties of different single muscle fibres from Xenopus laevis at 20 degrees C. J Physiol 393: 399–412, 1987.
6. He Z, Stienen GJ, Barends JP, Ferenczi MA. Rate of phosphate release after photoliberation of adenosine 5'-triphosphate in slow and fast skeletal muscle fibers. Biophys J 75: 2389–2401, 1998.
7. He ZH, Chillingworth RK, Brune M, Corrie JE, Trentham DR, Webb MR, Ferenczi MA. ATPase kinetics on activation of rabbit and frog permeabilized isometric muscle fibres: a real time phosphate assay. J Physiol 501: 125–148, 1997.[CrossRef][ISI][Medline]
8. Potma EJ, van Graas IA, Stienen GJ. Influence of inorganic phosphate and pH on ATP utilization in fast and slow skeletal muscle fibers. Biophys J 69: 2580–2589, 1995.
9. Wendt IR, Barclay JK. Effects of dantrolene on the energetics of fast- and slow-twitch muscles of the mouse. Am J Physiol Cell Physiol 238: C56–C61, 1980.
10. West TG, Curtin NA, Ferenczi MA, He ZH, Sun YB, Irving M, Woledge RC. Actomyosin energy turnover declines while force remains constant during isometric muscle contraction. J Physiol 555: 27–43, 2004.
11. Zhang SJ, Andersson DC, Sandstrom ME, Westerblad H, Katz A. Cross bridges account for only 20% of total ATP consumption during submaximal isometric contraction in mouse fast-twitch skeletal muscle. Am J Physiol Cell Physiol 291: C147–C154, 2006. First published February 15, 2006; doi:10.1152/ajpcell.00578.2005.
Shi-Jin Zhang
Daniel C. Andersson
Marie E. Sandström
Håkan Westerblad
Abram Katz
Karolinska Institutet
Department of Physiology and Pharmacology
Stockholm
Sweden
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
