Skip to main content
Log in

Adenine nucleotide degradation in the thoroughbred horse with increasing exercise duration

  • Published:
European Journal of Applied Physiology and Occupational Physiology Aims and scope Submit manuscript

Summary

Adenine nucleotide (AN) degradation has been shown to occur during intense exercise in the horse and in man, at or close to the point of fatigue. The aim of the study was to compare the concentrations of muscle inosine 5′-monophosphate (IMP) and plasma ammonia (NH3) during intense exercise with the concentrations of muscle and blood lactate. Seven trained thoroughbred horses were used in the study. Each exercised on a treadmill for periods of between 30 s and 150 s, at 11 and/or 12 m · s−1. Blood and muscle samples were taken and analysed for lactate and NH3 and adenosine 5′-triphosphate (ATP), phosphorylcreatine (PCr), IMP, creatine, lactate and glycerol-3-phosphate respectively. Horses showed varying degrees of AN degradation as indicated by plasma [NH3] and muscle [ATP] and [IMP]. Comparisons of [IMP] with muscle [lactate], and plasma [NH3] with that of blood [lactate] indicated a threshold to the start of AN degradation. This threshold corresponded to a lactate content of around 80 mmol · kg−1 dry muscle and 15 mmol · l−1 in blood. We discuss the mechanisms which have been proposed to account for AN degradation and suggest that IMP formation occurs as a result of a sudden rise in the concentration of adenosine 5′-diphosphate (ADP) and consequently the concentration of adenosine 5′-monophosphate. The data suggest a critical pH below which there may be a substantial reduction in the kinetics of ADP rephosphorylation provided by PCr resulting in an increase in [ADP], which is the stimulus to AN degradation during intense exercise.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bergstrom J (1962) Muscle electrolytes in man. Determined by neutron activation analyses on needle biopsy specimens. A study on normal subjects, kidney patients and patients with chronic diarrhoea. Scand J Clin Lab Invest 14 [Suppl] 68:1–110

    Google Scholar 

  • Bessman SP, Savabi F (1990) The role of the phosphocreatine energy shuttle in exercise and muscle hypertrophy. Int Ser Sport Sci 21:167–178

    Google Scholar 

  • Broberg S, Sahlin K (1988) Hyperammoneamia during prolonged repeated submaximal exercise: an effect of glycogen depletion. J Appl Physiol 65:2475–2477

    Google Scholar 

  • Broberg S, Sahlin K (1989) Adenine nucleotide degradation in human skeletal muscle during prolonged exercise. J Appl Physiol 67:116–122

    Google Scholar 

  • Buono MJ, Clancy TR, Cook JR (1984) Blood lactate and ammonium ion accumulation during graded exercise in humans. J Appl Physiol 57:135–139

    Google Scholar 

  • Coakley JH, Wagenmakers AJM, Edwards RHT (1989) Excessive ammonia production during cycle ergometry in McArdle's disease. Clin Sci 76 [Suppl 25]:49

    Google Scholar 

  • Dudley GA, Terjung RL (1985a) Influence of acidosis on AMP deaminase activity in contracting fast-twitch muscle. Am J Physiol 248:C43-C50

    Google Scholar 

  • Dudley GA, Terjung RL (1985b) Influence of aerobic metabolism on IMP accumulation in fast-twitch muscle. Am J Physiol 248:C37-C42

    Google Scholar 

  • Dudley GA, Staron RS, Murray TF, Hagerman FC, Luginbuhl A (1983) Muscle fibre composition and blood ammonia levels after intense exercise in humans. J Appl Physiol 54:582–586

    Google Scholar 

  • Ellington WR (1989) Phosphocreatine represents a thermodynamic and functional improvement over other muscle phosphagens. J Exp Biol 143:177–194

    Google Scholar 

  • Eriksson LS, Broberg S, Bjorkman O, Wahren J (1985) Ammonia metabolism during exercise in man. Clin Physiol 5:325–336

    Google Scholar 

  • Fernandez A, Costas MJ, Gunther Sillero MA, Sillero A (1984) Diadenosine tetraphosphate activates AMP deaminase from rat muscle. Biochem Biophys Res Commun 121:155–161

    Google Scholar 

  • Folley LS, Power SD, Poyton RO (1983) Separation of nucleotides by ion-pair, reversed phase high performance liquid chromatography. J Chromatogr 281:199–207

    Google Scholar 

  • Fonseca-Wollheim F (1990) Pre-analytical increase of ammonia in blood specimens from healthy subjects. Clin Chem 36:1483–1487

    Google Scholar 

  • Funk C, Clark A, Connett RJ (1989) How phosphocreatine buffers cyclic changes in ATP demand in working muscle. In: Rakusan K, Biro GP, Goldstick TK, Turek Z (eds) Oxygen transport to tissue XI. Plenum Press, New York, pp 687–692

    Google Scholar 

  • Greenhaff PL, Harris RC, Snow DH, Sewell DA, Dunnett M (1991a) The influence of metabolic acidosis upon exercise metabolism in the thoroughbred horse. Eur J Appl Physiol 63:129–134

    Google Scholar 

  • Greenhaff PL, Leiper JB, Ball D, Maughan RJ (1991b) The influence of dietary manipulation on plasma ammonia accumulation during incremental exercise in man. Eur J Appl Physiol 63:338–344

    Google Scholar 

  • Harkness RA (1988) Hypoxanthine, xanthine and uridine in body fluids, indicators of ATP depletion. J Chromatogr 429:255–278

    Google Scholar 

  • Harris RC, Hultman E (1985) Adenine nucleotide depletion in human muscle in response to intermittent stimulation in situ. J Physiol (Lond) 365:73P

    Google Scholar 

  • Harris RC, Hultman E, Nordesjo LO (1974) Glycogen, glycolytic intermediates and high energy phosphates in biopsy samples of musculus quadriceps femoris of man at rest. Methods and variance of values. Scand J Clin Lab Invest 33:109–120

    Google Scholar 

  • Harris RC, Marlin DJ, Snow DH (1987) Metabolic response to maximal exercise of 800 m and 2000 m in the thoroughbred horse. J Appl Physiol 63:12–19

    Google Scholar 

  • Harris RC, Snow DH, Katz A, Sahlin K (1989) Effect of freeze-drying on measurements of pH in biopsy samples of the middle gluteal muscle of the horse: comparison of muscle pH to the pyruvate and lactate content. Equine Vet J 21:45–47

    Google Scholar 

  • Harris RC, Marlin DJ, Snow DH, Harkness RA (1991) Muscle ATP loss and lactate accumulation at different work intensities in the exercising thoroughbred horse. Eur J App] Physiol 62:235–244

    Google Scholar 

  • Kammermeier H (1987) Why do cells need phosphocreatine and a phosphocreatine shuttle? J Mol Cell Cardiol 19:115–118

    Google Scholar 

  • Katz A, Sahlin K, Henriksson J (1986) Muscle ammonia metabolism during isometric contraction in humans. Am J Physiol 250:C834-C840

    Google Scholar 

  • Lawson JWR, Veech RL (1979) Effects of pH and free Mg2+ on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transferases. J Biol Chem 254:6528–6537

    Google Scholar 

  • Lowenstein JM (1990) The purine nucleotide cycle revisited. Int J Sports Med 11:S37-S46

    Google Scholar 

  • Meyer RA, Terjung RL (1979) Differences in ammonia and adenylate metabolism in contracting fast and slow muscle. Am J Physiol 237:C111-C118

    Google Scholar 

  • Meyer RA, Terjung RL (1980) AMP deamination and IMP reamination in working skeletal muscle. Am J Physiol 239:C32-C38

    Google Scholar 

  • Meyer RA, Dudley GA, Terjung RL (1980) Ammonia and IMP in different skeletal muscle fibres after exercise in rats. J Appl Physiol 49:1037–1041

    Google Scholar 

  • Norman B, Sollevi A, Jansson E (1988) Increased IMP content in glycogen depleted muscle fibres during submaximal exercise in man. Acta Physiol Scand 133:97–100

    Google Scholar 

  • Raffin JP, Thebault MT (1991) AMP deaminase from equine muscle: purification and determination of regulatory properties. Int J Biochem 23:1069–1078

    Google Scholar 

  • Ranieri-Raggi M, Bergamini C, Raggi A (1980) Effect of pH on the kinetic properties of rat skeletal muscle AMP deaminase. Ital J Biochem 29:238–250

    Google Scholar 

  • Ronca-Testoni S, Raggi A, Ronca G (1970) Muscle AMP aminohydrolase. III. A comparative study on the regulatory properties of skeletal muscle enzyme from various species. Biochim Biophys Acta 198:101–112

    Google Scholar 

  • Sahlin K, Katz A (1988) Purine nucleotide metabolism. In: Poortmans JR (ed) Principles of exercise biochemistry. Karger, Basel, pp 120–139

    Google Scholar 

  • Sahlin K, Palmskog G, Hultman E (1978) Adenine nucleotide and IMP contents of the quadriceps muscle in man after exercise. Pfügers Arch 374:193–198

    Google Scholar 

  • Sahlin K, Edstrom L, Sjoholm H, Hultman E (1981) Effects of lactic acid accumulation and ATP decrease on muscle tension and relaxation. Am J Physiol 240:C121-C126

    Google Scholar 

  • Sahlin K, Broberg S, Ren JM (1989) Formation of inosine monophosphate (IMP) in human skeletal muscle during incremental dynamic exercise. Acta Physiol Scand 136:193–198

    Google Scholar 

  • Setlow B, Lowenstein JM (1967) Adenylate deaminase. Purification and some regulatory properties of the enzyme from calf brain. J Biol Chem 242:607–615

    Google Scholar 

  • Sewell DA, Harris RC (1991) Lactate and ammonia appearance in relation to exercise duration in the thoroughbred horse. J Physiol (Lond) 434:43P

    Google Scholar 

  • Sewell DA, Harris RC, Hanak J, Jahn P (1992) Muscle adenine nucleotide degradation in the thoroughbred horse as a consequence of racing. Comp Biochem Physiol 101B:375–381

    Google Scholar 

  • Siemankowski RF, White HD (1984) Kinetics of the interaction between actin, ADP and cardiac myosins. J Biol Chem 251:5045–5053

    Google Scholar 

  • Snow DH, Harris RC (1985) Thoroughbreds and greyhounds: biochemical adaptations in creatures of nature and of man. In: Gilles R (ed) Circulation, respiration and metabolism. Springer, Berlin Heidelberg New York, pp 227–239

    Google Scholar 

  • Snow DH, Harris RC (1991) Effects of daily exercise on muscle glycogen in the thoroughbred racehorse. In: Persson SG, Lindholm A, Jeffcott LB (eds) Equine exercise physiology 3. ICEEP Publications, Davis, Calif., pp 299–304

    Google Scholar 

  • Snow DH, Harris RC, Gash SP (1985) Metabolic response of equine muscle to intermittent maximal exercise. J Appl Physiol 58:1689–1697

    Google Scholar 

  • Wheeler TJ, Lowenstein JM (1979) Adenylate deaminase from rat muscle. Regulation by purine nucleotides and orthophosphate in the presence of 150 mM KCl. J Biol Chem 254:8994–8999

    Google Scholar 

  • Wilkerson JE, Batterton DL, Horvath SM (1977) Exercise induced changes in blood ammonia levels in humans. Eur J Appl Physiol 37:255–263

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sewell, D.A., Harris, R.C. Adenine nucleotide degradation in the thoroughbred horse with increasing exercise duration. Europ. J. Appl. Physiol. 65, 271–277 (1992). https://doi.org/10.1007/BF00705093

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00705093

Key words

Navigation