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Effect of chronic exercise on glucose uptake and activities of glycolytic enzymes measured regionally in rat heart

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Summary

Regional glucose uptake in perfused hearts, and the activities of several glycolytic enzymes contributing to the glucose metabolism in perfused and nonperfused hearts were studied in male and female rats after 8–9 weeks of swimming training. The left ventricular glucose uptake showed a transmural gradient in the sedentary animals, the subendocardial uptake being 30% and 12% higher than that of the subepicardial layer in the males and females, respectively. Swimming exercise abolished the left ventricular glucose uptake gradient in male rats, and in female rats an opposite gradient was found, the subepicardial uptake being 23% higher than the subendocardial uptake. The activities of phosphofructokinase and 3-phosphoglyceraldehyde dehydrogenase also showed transmural gradients in the left ventricles. Training did not abolish these gradients. Training-induced changes in the activities of phosphofructokinase, 3-phosphoglyceraldehyde dehydrogenase, pyruvate kinase, lactate dehydrogenase, glucose-6-phosphate dehydrogenase, citrate synthase, and malate dehydrogenase were found in certain sites of the myocardium. Perfusion of isolated hearts for 50 min with insulin-containing Krebs-Ringer buffer especially affected the activities of phosphofructokinase, lactate dehydrogenase, and citrate synthase, increasing these activities in the left ventricles and decreasing them in the atria. These results indicate that there are regional differences between male and female rats in the cardiac glucose uptake rate after swimming training.

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References

  1. Baldwin KM, Cooke DA, Cheadle WG (1977) Time course adaptations in cardiac and skeletal muscle to different running programs. J Appl Physiol 42:267–272

    PubMed  Google Scholar 

  2. Bass A, Brdiczka D, Eyer P, Hofer S, Pette D (1969) Metabolic differentation of distinet muscle types at the level of enzymatic organization. Eur J Biochem 10:198–206

    Article  PubMed  Google Scholar 

  3. Bersohn MM, Scheuer J (1977) Effects of physical training on end-diastolic volume and myocardial performance of isolated rat hearts. Circ Res 40:510–516

    PubMed  Google Scholar 

  4. Breull W, Flohr H, Schuchardt S, Dohm H (1981) Transmural gradients in myocardial metabolic rate. Basic Res Cardiol 76:399–403

    PubMed  Google Scholar 

  5. Czech MP (1977) Molecular basis of insulin action. Ann Rev Biochem 47:359–384

    Article  Google Scholar 

  6. Dowell RT (1978) Transmural citrate synthase and lactate dehydrogenase levels in hypertrophied rat left ventricle. Proc Soc Exp Biol Med 158:599–603

    PubMed  Google Scholar 

  7. Dunaway GA, Kasten TP (1985) Characterization of the rat heart 6-phosphofructo-1-kinase isozymes. J Mol Cell Cardiol 17:947–957

    PubMed  Google Scholar 

  8. Giusti R, Bersohn MM, Malhotra A, Scheuer J (1978) Cardiac function and actomyosin ATPase activity in hearts of conditioned and deconditioned rats. J Appl Physiol 44:171–174

    PubMed  Google Scholar 

  9. Gollnick PD, Struck PJ, Bogyo TP (1967) Lactic dehydrogenase activities of rat heart and skeletal muscle after exercise and training. J Appl Physiol 22:623–627

    PubMed  Google Scholar 

  10. Griggs DM (1979) Blood flow and metabolism in different layers of the left ventricle. Physiologist 22:36–40

    Google Scholar 

  11. Hamilton MJ, Ferguson JH (1972) Effects of exercise and cold acclimation on the ventricular and skeletal muscles of white mice (Mus musculus). I. Succinic dehydrogenase activity. Comp Biochem Physiol (A) 43:815–824

    Article  Google Scholar 

  12. Harpur RP (1980) The rat as a model for physical fitness studies. Comp Biochem Physiol (A) 66:553–574

    Article  Google Scholar 

  13. Hearn GR, Wainio WW (1957) Aldolase activity of the heart and skeletal muscle of exercised rats. Am J Physiol 190:206–208

    PubMed  Google Scholar 

  14. Holsinger JW Jr, Ramey CA, Allison TB (1978) Transmural gradients in ischemic canine left ventricle: effects of blood reflow on glycolytic intermediates. In: Kobayashi T, Ito Y, Rona G (eds) Recent advances in studies on cardiac structure and metabolism, vol 12; University Park Press, Baltimore, pp 579–583

    Google Scholar 

  15. Ichihara K, Abiko Y (1982) Crossover plot study of glycolytic intermediates in the ischemic canine heart. Jpn Heart J 23:817–828

    PubMed  Google Scholar 

  16. Jedeikin LA (1964) Regional distribution of glycogen and phosphorylase in the ventricles of the heart. Circ Res 14:202–211

    PubMed  Google Scholar 

  17. Kainulainen H, Ahomäki E, Vihko V (1984) Selected enzyme activities in mouse cardiac muscle during training and terminated training. Basic Res Cardiol 79:110–123

    Google Scholar 

  18. Kainulainen H, Komulainen J, Takala T, Vihko V (1987) Regional glucose uptake and protein synthesis in isolated perfused rat hearts immediately after training and later. Basic Res Cardiol 82:9–17

    PubMed  Google Scholar 

  19. Kainulainen H, Komulainen J, Vihko V (1985). Regional differences of substrate oxidation in rat hearts. J Mol Cell Cardiol 17 (Suppl 3): abstract no 146

    Google Scholar 

  20. Kainulainen H, Takala TES, Hassinen IE, Vihko V (1985) Redistribution of glucose uptake by chronic exercise, measured in isolated perfused rat hearts. Pflügers Arch 403:296–300

    Article  Google Scholar 

  21. Kainulainen H, Vihko V (1983) Cardiac muscle enzyme activities during the development of exercise-induced hypertrophy in mice. IRCS Med Sci 11:34–35

    Google Scholar 

  22. Kornberg A (1955) Lactic dehydrogenase of muscle. In: Colowick SP, Kaplan NO (eds) Methods in Enzymology, vol 1; Academic Press, New York, pp 441–443

    Google Scholar 

  23. Kraus H, Kirsten R (1970) Die Wirkung von körperlichem Training auf die mitochondriale Energie-Produktion im Herzmuskel und in der Leber. Pflüger Arch 320:334–347

    Article  Google Scholar 

  24. Köhler U, Medugorac I (1980) The behavior of some enzymes of the hypertrophied and postnatally developing myocardium of the rat. Basic Res Cardiol 75:214–220

    PubMed  Google Scholar 

  25. L'Abbate A, Camici B, Trivella MG, Pelosi G (1981) Regional myocardial glucose utilization assessed by (14C)deoxyglucose. Basic Res Cardiol 76:394–398

    PubMed  Google Scholar 

  26. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  Google Scholar 

  27. Lundsgaard-Hansen P, Meyer C, Riedwyll H (1967) Transmural gradients of glycolytic enzyme activities in left ventricular myocardium. I. The normal state. Pflügers Arch 297:89–106

    Article  Google Scholar 

  28. Löhr WG, Waller HD (1974) Glucose-6-phosphate dehydrogenase. In: Bergmeyer HU (ed) Methods of Enzymatic Analysis. vol 2; Academic Press, New York, pp 636–643

    Google Scholar 

  29. Nohara Y, Yamasawa I, Konno S, Shimizu K, Iwane H, Ibukiyama C, Hara A (1978) Experimental study on enzyme distribution and its relation to myocardial ischemic changes following coronary circulatory disturbances. In: Kobayashi T, Ito Y, Rona G (eds) Recent Advances in Studies on Cardiac Structure and Metabolism, vol 12; University Park Press, Baltimore, 391–399

    Google Scholar 

  30. Ochoa S (1955) Malic dehydrogenase from pig heart. In: Colowick SP, Kaplan NO (eds) Methods in Enzymology, vol 1; Academic Press, New York, pp 735–739

    Google Scholar 

  31. Oscai LB, Mole PA, Brei B, Holloszy J (1971) Cardiac growth and respiratory enzyme levels in male rats subjected to a running program. Am J Physiol 220:1238–1241

    PubMed  Google Scholar 

  32. Oscai LB, Mole PA, Holloszy JO (1971) Effects of exercise on cardiac weight and mitochondria in male and female rats. Am J Physiol 220:1944–1948

    PubMed  Google Scholar 

  33. Penney DG, Bugaisky LB, Mieszla JR (1974) Lactate dehydrogenase and pyruvate kinase in rat heart during sideropenic anemia. Biochim Biophys Acta 334:24–30

    Google Scholar 

  34. Penpargkul S, Schwartz A, Scheuer J (1978) Effect of physical conditioning on cardiac mitochondrial function. J Appl Physiol 45:978–986

    PubMed  Google Scholar 

  35. Peterson GL (1977) Simplification of protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346–356

    PubMed  Google Scholar 

  36. Picrce GN, Philipson KD (1985) Binding of glycolytic enzymes to cardiac sarcolemmal and sarcoplasmic reticular membranes. J Biol Chem 260:6862–6870

    PubMed  Google Scholar 

  37. Rider MH, Hue L (1984) Activation of rat heart phosphofructokinase-2 by insulin in vivo. FEBS Letters 176:484–488

    Article  PubMed  Google Scholar 

  38. Sabbah HN, Marzilli M, Stein PD (1981) The relative role of subendocardium and subepicardium in left ventricular mechanics. Am J Physiol 240:H920-H926

    PubMed  Google Scholar 

  39. Schaible TF, Penpargkul S, Scheuer J (1981) Differences in male and female rats in cardiac conditioning. J Appl Physiol 50:112–117

    PubMed  Google Scholar 

  40. Schaible TF, Scheuer J (1979) Effects of physical training by running or swimming on ventricular performance of rat hearts. J Appl Physiol 46:854–860

    PubMed  Google Scholar 

  41. Schaible TF, Scheuer J (1985) Cardiac adaptations to chronic exercise. Progr Cardiovasc Diseases 27:297–324

    Google Scholar 

  42. Scheuer J, Penpargkul S, Bhan AK (1973) Effect of physical conditioning upon metabolism and performance of the rat heart. In: Dhalla NS, Rona G (eds) Recent Advances in Studies on Cardiac Structure and Metabolism, vol 3; University Park Press, Baltimore, pp 145–159

    Google Scholar 

  43. Scheuer J, Penpargkul S, Bhan AK (1974) Experimental observations on the effects of physical training upon intrinsic cardiac physiology and biochemistry. Am J Cardiol 33:745–751

    Article  Google Scholar 

  44. Schmidt E, Schmidt FW (1960) An enzyme model of human tissue. Klin Wochenschr 38:957–962

    Article  PubMed  Google Scholar 

  45. Sokoloff L, Reivich M, Kennedy C, Desrosiers MH, Patlak CS, Pettigren KD, Sakurada D, Sinohara D (1977) The (14C)deoxyglucose method for the measurement of local cerebral glucose utilization: Theory, procedure and normal values in conscious and anesthetized albino rat. J Neurochem 28:897–916

    PubMed  Google Scholar 

  46. Sommercorn J, Steward T, Freedland RA (1984) Activation of phosphofructokinase from rat tissues by 6-phosphogluconate and fructose 2,6-bisphosphate. Arch Biochem Biophys 232:579–584

    Article  PubMed  Google Scholar 

  47. Srere PA (1969) Citrate synthase. In: Colowick SP, Kaplan NO (eds) Methods in Enzymology, vol 13; Academic Press, New York, pp 3–5

    Google Scholar 

  48. Stein PD, Marzilli M, Sabbah HN, Tennyson L (1980) Systolic and diastolic pressure gradients within the left ventricular wall. Am J Physiol 238:H625-H630

    PubMed  Google Scholar 

  49. Stevens EVJ, Husbands DR (1985) Insulin-dependent production of low-molecular-weight compounds that modify key enzymes in metabolism. Comp Biochem Physiol (B) 81:1–8

    Article  Google Scholar 

  50. Taegtmayer H, Hems R, Krebs HA (1980) Utilization of energy-providing substrates in isolated working rat heart. Biochem J 186:701–711

    PubMed  Google Scholar 

  51. Takala T (1981) Protein synthesis in the isolated perfused rat heart. Effects of mechanical work load, diastolic ventricular pressure and coronary pressure on amino acid incorporation and its transmural distribution into left ventricular protein. Basic Res Cardiol 76:44–61

    PubMed  Google Scholar 

  52. Takala TES, Hassinen IE (1981) Effect of mechanical work load on the transmural distribution of glucose uptake in isolated perfused rat heart, studied by regional deoxyglucose trapping. Circ Res 49:62–69

    PubMed  Google Scholar 

  53. Takala TES, Kainulainen H, Vihko V, Hassinen IE (1984) Transmural distribution of glucose uptake in the rat heart: Effects of mechanical work load, substrate supply and exercise. Acta Physiol Scand Suppl 537:17–21

    PubMed  Google Scholar 

  54. Takala T, Pirttisalo J, Hiltunen K, Hassinen IE (1984) Effect of substrate supply and aortic pressure on the transmural distribution of glucose uptake in the isolated perfused rat heart. J Mol Cell Cardiol 16:567–571

    PubMed  Google Scholar 

  55. Takala TES, Ruskoaho HJ, Hassinen IE (1983) Effect of physical exercise on the transmural distribution of cardiac glucose uptake in the rat. Am J Physiol 244:H131-H137

    PubMed  Google Scholar 

  56. Vihko V, Salminen A, Rantamäki J (1978) Oxidative and lysosomal capacity in skeletal muscle of mice after endurance training of different intensities. Acta Physiol Scand 104:74–81

    PubMed  Google Scholar 

  57. Watanabe T, Smith MM, Robinson FW, Kono T (1984) Insulin action on glucose transport in cardiac muscle. J Biol Chem 259:13117–13122

    PubMed  Google Scholar 

  58. Weiss HR, Neubauer JA, Lipp JA, Sinha AK (1978) Quantitative determination of regional oxygen consumption in the dog heart. Circ Res 42:394–401

    PubMed  Google Scholar 

  59. Westrin H, Backman L (1983) Association of rabbit muscle glycolytic enzymes with filamentous actin. A counter-current distribution study at high ionic strength. Eur J Biochem 136:407–411

    Article  PubMed  Google Scholar 

  60. Wu R, Racker E (1959) Regulatory mechanism in carbohydrate metabolism. III. Limiting factors in glycolysis of ascites tumor cells. J Biol Chem 234:1029–1035

    PubMed  Google Scholar 

  61. Yin FCP (1981) Ventricular wall stress. Circ Res 49:829–842

    PubMed  Google Scholar 

  62. York JW, Penney DG, Oscai LB (1975) Effects of physical training on several glycolytic enzymes in rat heart. Biochim Biophys Acta 381:22–27

    PubMed  Google Scholar 

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Author notes

  1. H. Kainulainen

    Present address: Dept. Clinical Sciences, University of Tampere, P.O. Box 607, SF-33101, Tampere, Finland

Authors and Affiliations

  1. Department of Cell Biology, University of Jyväskylä, Jyväskylä, Finland

    H. Kainulainen & J. Komulainen

  2. Department of Sports Medicine, Deaconess Institute of Oulu, Oulu, Finland

    T. Takala

  3. Research Unit for Sport and Physical Fitness, University Campus, Jyväskylä, Finland

    V. Vihko

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Supported by a grant from the Research Council for Physical Education and Sport, Ministry of Education, Finland.

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Kainulainen, H., Komulainen, J., Takala, T. et al. Effect of chronic exercise on glucose uptake and activities of glycolytic enzymes measured regionally in rat heart. Basic Res Cardiol 84, 174–190 (1989). https://doi.org/10.1007/BF01907927

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