Linkage of aerobic glycolysis to sodium-potassium transport in rat skeletal muscle: Implications for increased muscle lactate production in sepsis

Journal of Clinical Investigation

Volumn 98, Issue 10, 1996, Pages 2388-2397

  James, J Howard ^a,c   Fang, Cheng Hui ^b   Schrantz, Stephen J ^a   Hasselgren, Per Olof ^a   Paul, Richard J ^a   Fischer, Josef E ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN   (United States)

^c UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

Author keywords

glycolysis; monensin; muscle, skeletal; Na+, K+ ATPase; sepsis syndrome

Indexed keywords

ENDOTOXIN; GLUCOSE; LACTIC ACID; MONENSIN; OUABAIN; POTASSIUM ION; PYRUVIC ACID; SODIUM ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; GLYCOLYSIS; INHIBITION KINETICS; LACTIC ACIDOSIS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SEPSIS; SKELETAL MUSCLE; SODIUM TRANSPORT; VASCULAR SMOOTH MUSCLE; WEIGHT GAIN;

EID: 0029849945     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119052     Document Type: Article

References (55)

1. Parrillo, J.E., M.M. Parker, C. Natanson, A.F. Suffredini, R.L. Danner, R.E. Cunnion, and F.P. Ognibene. 1990. Septic shock in humans. Advances in the understanding of pathogenesis, cardiovascular dysfunction, and therapy. Ann. Intern. Med. 113:227-242.
2. Hotchkiss, R.S., and I.E. Karl. 1992. Reevaluation of the role of cellular hypoxia and bioenergetic failure in sepsis. JAMA (J. Am. Med. Assoc.). 267: 1503-1510.
3. Hotchkiss, R.S., R.S. Rust, C.S. Dence, T.H. Wasserman, S.K. Song, D.R. Hwang, I.E. Karl, and M.J. Welch. 1991. Evaluation of the role of cellular hypoxia in sepsis by the hypoxic marker [18F]fluoromisonidazole. Am. J. Physiol. 261:R965-972.
4. Hotchkiss, R.S., S.K. Song, J.J. Neil, R.D. Chen, J. K. Manchester, I.E. Karl, O.H. Lowry, and J.J. Ackerman. 1991. Sepsis does not impair tricarboxylic acid cycle in the heart. Am. J. Physiol. 260:C50-C57.
5. Gore, D.C., F. Jahoor, J.M. Hibbert, and E.J. DcMaria. 1996. Lactic acidosis during sepsis is related to increased pyruvate production, not deficits in tissue oxygen availability. Ann. Surg. 224:97-102.
6. Gibson, W.H., J.J. Cook, G. Gatipon, and M.E. Moses. 1977. Effect of endotoxin shock on skeletal muscle cell membrane potential. Surgery (St. Louis). 81:571-577.
7. Trunkey, D.D., H. Illner, I.Y. Wagner, and G.T. Shires. 1979. The effect of septic shock on skeletal muscle action potentials in the primate. Surgery (St. Louis). 85:638-643.
8. Illner, H.P., and G.T. Shires. 1981. Membrane defect and energy status of rabbit skeletal muscle cells in sepsis and septic shock. Arch. Surg. 116:1302-1305.
9. Shiono, S., G.A. Fantini, J.P. Roberts, J. Chiao, and G.T. Shires. 1989. Assessment of the early cellular membrane response to live Escherichia coli bacteremia. J. Surg. Res. 46:9-15.
10. Minei, J.P., G.A. Fantini, D.G. Hesse, S. Shiono, K.J. Tracey, Y. Fong, S.F. Lowry, and G.T. Shires. 1987. Endotoxin infusion in human volunteers: assessment of the early cellular membrane response. Surg. Forum. 38:102-104.
11. Tracey, K.J., S.F. Lowry, T.J. Fahey, J.D. Albert, Y. Fong, D. Hesse, B. Beutler, K.R. Manogue, S. Calvano, H. Wei, A. Cerami, and G.T. Shires, 1987. Cachectin/tumor necrosis factor induces lethal shock and stress hormone responses in the dog. Surg. Gynecol. Obstet. 164:415-422.
12. Chiao, J.J., W.G. Jones, 2d, G.T. Shires, 3d, A.E. Barber, and G.T. Shires. 1992. Effect of sepsis on intracellular sodium activity, sodium concentration, and water content in thermal injured rat. Circ. Shock. 38:42-49.
13. Hannon, R.J., and V.E. Boston. 1990. Fluid and ion redistribution in skeletal muscle in an animal sepsis model. J. Ped. Surg. 25:599-603.
14. Jennische, E., E. Enger. A. Medegard, L. Appelgren, and H. Haljamae. 1978. Correlation between tissue pH, cellular transmembrane potentials, and cellular energy metabolism during shock and during ischemia. Circ. Shock. 5: 251-260.
15. Peitzman, A.B., W.A. Corbett, G.T. Shires, 3d, H. Illner, G.T. Shires, and R. Inamdar. 1985. Cellular function in liver and muscle during hemorrhagic shock in primates. Surg. Gynecol. Obstet. 161:419-424.
16. Liaw, K.Y., J. Askanazi, C.B. Michelson, L.R. Kantrowitz, P. Furst, and J.M. Kinney. 1980. Effect of injury and sepsis on high-energy phosphates in muscle and red cells. J. Trauma. 20:755-759.
17. Jacobs, D.O., J. Maris, R. Fried, R.G. Settle, R.R. Rolandelli, M.J. Koruda, B. Chance, and J.L. Rombeau. 1988. In vivo phosphorus 31 magnetic resonance spectroscopy of rat hind limb skeletal muscle during sepsis. Arch. Surg. 123:1425-1428.
18. Jacobs, D.O., T. Kobayashi, J. Imagire, C. Grant, B. Kesselly, and D.W. Wilmore. 1991. Sepsis alters skeletal muscle energetics and membrane function. Surgery (St. Louis). 110:318-326.
19. Mizobata, Y., D. Prechek, J.D. Rounds, V. Robinson, D.W. Wilmore, and D.O. Jacobs. 1995. The duration of infection modifies mitochondrial oxidative capacity in rat skeletal muscle. J. Surg. Res. 59:165-173.
20. Clausen, T. 1965. The relationship between the transport of glucose and cations across cell membranes in isolated tissues. I. Stimulation of glycogen deposition and inhibition of lactic acid production in diaphragm, induced by ouabain. Biochim. Biophys. Acta. 109:164-171.
21. +-free medium, ouabain and insulin upon the fate of glucose in rat diaphragm. Biochim. Biophys. Acta. 120:361-368.
22. Parker, J.C., and J.F. Hoffman. 1967. The role of membrane phosphoglycerate kinase in the control of glycolytic rate by active cation transport in human red blood cells. J. Gen. Physiol. 50:893-916.
23. Paul, R.J., M. Bauer, and W. Pease. 1979. Vascular smooth muscle: aerobic glycolysis linked to sodium and potassium transport processes. Science (Wash. DC). 206:1414-1416.
24. +]o stimulation of protein synthesis and K+ uptake require glycolysis. Fed. Proc. 42:2875-2880.
25. +-ATPase in renal cell line MDCK. Am. J. Physiol. 253:C269-276.
26. Lynch, R.M., and R.S. Balaban. 1987. Energy metabolism of renal cell lines, A6 and MDCK: regulation by Na-K-ATPase. Am. J. Physiol. 252:C225-31.
27. Erecinska, M., F. Dagani, D. Nelson, J. Deas, and I.A. Silver. 1991. Relations between intracellular ions and energy metabolism: a study with monensin in synaptosomes, neurons, and C6 glioma cells. J. Neurosci. 11:2410-2421.
28. Pellerin, L., and P.J. Magistretti. 1994. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. USA. 91:10625-10629.
29. Lynch, R.M., and R.J. Paul. 1983. Compartmentation of glycolytic and glycogenolytic metabolism in vascular smooth muscle. Science (Wash. DC). 222: 1344-1346.
30. Paul, R.J. 1983. Functional compartmentalization of oxidative and glycolytic metabolism in vascular smooth muscle. Am. J. Physiol. 244:C399-409.
31. + transport. Am. J. Physiol. 247: C433-440.
32. +-ATPase in porcine vascular smooth muscle. J. Physiol. (Lond.). 447: 67-82.
33. 2+ uptake in smooth muscle plasma membrane vesicles by an endogenous glycolytic cascade. FASEB J. 3:2298-2301.
34. Maltin, C.A., M.I. Delday, A.G.S. Baillie, D.A. Grubb, and P.J. Garlick. 1989. Fiber type composition in nine rat muscles. I. Changes during the first year of life. Am. J. Physiol. 257:E823-E832.
35. Everts, M.E., and T. Clausen. 1992. Activation of the Na-K pump by intracellular Na in rat slow- and fast-twitch muscle. Acta Physiol. Scand. 145:353-362.
36. Lowry, O.H., and J.V. Passonneau. 1972. A Flexible System of Enzymatic Analyses. Anonymous Academic Press, Orlando, FL. 199-201.
37. Lee, P.L., and R.H. Slocum. 1988. A high-resolution method for amino acid analysis of physiological fluids containing mixed disulfides. Clin. Chem. 34: 719-723.
38. Graser, T.A., H.A. Godel, S. Albers, P. Földi, and P. Fürst. 1985. An ultra-rapid and sensitive HPLC method for determination of tissue and plasma free amino acids. Anal. Biochem. 151:142-151.
39. James, J.H., P.O. Hasselgren, J.K. King, L.E. James, and J.E. Fischer. 1993. Intracellular glutamine concentration does not decrease in all muscles during sepsis. J. Surg. Res. 54:558-564.
40. 2+]i in porcine coronary artery smooth muscle. Circ. Res. 75:990-998.
41. Wichterman, K.A., A.E. Baue, and I.H. Chaudry. 1980. Sepsis and septic shock-a review of laboratory models and a proposal. J. Surg. Res. 29:189-201.
42. Fagan, J.M., and M.E. Tischler. 1989. Effects of oxygen deprivation on incubated rat soleus muscle. Life Sci. 44:677-681.
43. Bihler, I., P.C. Sawh, and P. Charles. 1985. Stimulation of glucose transport in skeletal muscle by the sodium ionophore monensin. Biochim. Biophys. Acta. 821:30-36.
44. Hoya, A., and R.A. Venosa. 1992. Ionic movements mediated by monensin in frog skeletal muscle. Biochim. Biophys. Acta. 1104:123-131.
45. + influx? Eur. J. Pharmacol. 129:77-85.
46. Trivedi, B., and W.H. Danforth. 1966. Effect of pH on the kinetics of frog muscle phosphofructokinase. J. Biol. Chem. 241:4110-4112.
47. Clausen, T. and J.A. Flatman. 1977. The effect of catecholamines on Na-K transport and membrane potential in rat soleus muscle. J. Physiol. 270:383-414.
48. Borst, C., R. Hempelmann, S. Herzig, and K. Mohr. 1991. Modulation of ouabain binding in heating ventricular myocardium from guinea-pigs: effects of lidocaine and monensin. Pharmacol. Toxicol. 68:243-248.
49. Angeras, U., M. Hall-Angeras, K.R. Wagner, J.H. James, P.O. Hasselgren, and J.E. Fischer. 1991. Tissue metabolite levels in different types of skeletal muscle during sepsis. Metab. Clin. Exp. 40:1147-1151.
50. Mizock, B.A., and J.L. Falk. 1992. Lactic acidosis in critical illness. Crit. Care Med. 20:80-93.
51. Kagan, B.L., R.L. Baldwin, D. Munoz, and B.J. Wisnieski. 1992. Formation of ion-permeable channels by tumor necrosis factor-alpha. Science (Wash. DC). 255:1427-1430.
52. Tracey, K.J., S.F. Lowry, B. Beutler, A. Cerami, J.D. Albert, and G.T. Shires. 1986. Cachectin/tumor necrosis factor mediates changes of skeletal muscle plasma membrane potential. J. Exp. Med. 164:1368-1373.
53. Zentella, A., K. Manogue, and A. Cerami. 1993. Cachectin/TNF-mediated lactate production in cultured myocytes is linked to activation of a futile substrate cycle. Cytokine. 5:436-447.
54. Karlstad, M.D., and M.M. Sayeed. 1992. Effect of endotoxic shock on basal and insulin-mediated Na+/K+-pump activity in rat solcus muscle. Circ. Shock. 38:222-227.
55. O'Brien, W.J., J.B. Lingrel, J.E. Fischer, and P.O. Hasselgren. 1996. Sepsis increases skeletal muscle sodium, potassium-ATPase activity without affecting mRNA or protein levels. J. Am. Coll. Surg. In press.