Modelling of amino acid turnover in the horse during training and racing: A basis for developing a novel supplementation strategy


Autoři: R. Hugh Dunstan aff001;  Margaret M. Macdonald aff001;  Brittany Thorn aff001;  David Wood aff002;  Timothy K. Roberts aff001
Působiště autorů: School of Environmental and Life Sciences, University of Newcastle, Callaghan, Australia aff001;  Horsepower Pty Ltd, Windsor, NSW, Australia aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0226988

Souhrn

Horses in heavy training in preparation for racing and competition have increased metabolic demands to support the more intensive levels of exercise and recovery. However, little is known at the metabolic level about amino acid turnover and the specific alterations of demand caused by high intensity exercise. During exercise, certain amino acids are required in greater quantities due to disproportionate losses via excretory systems and usage in biosynthetic pathways. This investigation has built a theoretical computer model in an attempt to bring together the published rates of protein intake and utilisation to try to understand how some amino acids might be in higher demand than others. The model indicated that after evaluation of the daily amino acid turnover, glutamine/glutamic acid (Glx), serine and ornithine were in negative nitrogen balance which identified these amino acids as critical limiting factors for anabolism. Adjustment of the modelling conditions to cater for high intensity training indicated that an additional demand was placed on eight amino acids, including GLx, valine, lysine, histidine and phenylalanine which could thus become limiting under these conditions. The modelling results indicated that an amino acid supplement with the correct amino acids to match demand could theoretically be beneficial to a 500Kg horse in quantities of 20-80g/day. These results open new avenues of research for specifically tailoring amino acid supplementation to meet demands for sports horses in heavy training and improving general well-being, especially in hotter climates.

Klíčová slova:

Amino acid metabolism – Excretion – Histidine – Horses – Protein metabolism – Serine – Sweat – Urine


Zdroje

1. Dunstan R.H.; Macdonald M.M.; Murphy G.R.; Thorn B.; Roberts T.K. Modelling of protein turnover provides insight for metabolic demands on those specific amino acids utilised at disproportionately faster rates than other amino acids. Amino Acids 2019, 10.1007/s00726-019-02734-1, doi: 10.1007/s00726-019-02734-1 31028564

2. Tessari P. Nitrogen balance and protein requirements: definition and measurements. In Cachexia and wasting: a modern approach., Mantovani G., Ed. Springer: New York, 2006; pp. 73–80.

3. Poortmans J.R.; Carpentier A.; Pereira-Lancha L.O.; Lancha A. Jr Protein turnover, amino acid requirements and recommendations for athletes and active populations. Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas 2012, 45, 875–890. doi: 10.1590/S0100-879X2012007500096 22666780

4. Wickens C.L.; Moore J.E.; Shelle J.; Skelly C.; Trottier N.L. Effect of exercise on dietary protein requirement of the Arabian horse. Proc. 18th Equine Nutrition Physiology Society 2003, 129–131.

5. Freeman D.W.; Potter G.D.; Schelling G.T.; Kreider J.L. Nitrogen metabolism in mature horses at varying levels of work. Journal of animal science 1988, 66, 407–412. doi: 10.2527/jas1988.662407x 3372384

6. NRC. Nutrient Requirements of Horses: Sixth Revised Edition; The National Academies Press: Washington, DC, 2007; doi: 10.17226/11653pp 360.

7. Graham-Thiers P.M.; Kronfeld D.S. Amino acid supplementation improves muscle mass in aged and young horses. Journal of animal science 2005, 83, 2783–2788, doi: 10.2527/2005.83122783x 16282616

8. Rasmussen B.B.; Tipton K.D.; Miller S.L.; Wolf S.E.; Wolfe R.R. An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. Journal of applied physiology (Bethesda, Md.: 1985) 2000, 88, 386–392.

9. Martin-Rosset W. Protein requirements and allowances of the exercising horse. In Nutrition of the exercising horse, Saastamoinen M.T., Martin-Rosset W., Eds. Wageningen Academic Publishers: The Netherlands., 2008; https://doi.org/10.3920/978-90-8686-644-1pp. 183–204.

10. Dunstan R.H.; Sparkes D.L.; Dascombe B.J.; Evans C.A.; Macdonald M.M.; Crompton M.; et al. Sweat facilitated losses of amino acids in Standardbred horses and the application of supplementation strategies to maintain condition during training. Comp Exerc Physiol 2015, 11, 201–212, doi: 10.3920/Cep150027

11. Evans D.L. Physiology of equine performance and associated tests of function. Equine Vet J 2007, 39, 373–383. doi: 10.2746/042516407x206418 17722733

12. Manohar M. Regional distribution of brain blood flow during maximal exertion in splenectomized ponies. Respiration physiology 1987, 68, 77–84. doi: 10.1016/0034-5687(87)90078-8 3602613

13. Poole D.C.; Erikson H.H. Heart and Vessels: function during exercise and response to training. In Equine Sports. Cardiac responses to exercise and training., Hinchcliff K.W., Kaneps A.J., Goer R.J., Eds. Medicine and Surgery: Elsevier Science: Oxford, 2004; pp. 699–727.

14. van Wijck K.; Pennings B.; van Bijnen A.A.; Senden J.M.G.; Buurman W.A.; Dejong C.H.C.; et al. Dietary protein digestion and absorption are impaired during acute postexercise recovery in young men. American journal of physiology. Regulatory, integrative and comparative physiology 2013, 304, R356–R361, doi: 10.1152/ajpregu.00294.2012 23283940

15. Butterfield G.E. Whole-body protein utilisation in humans. Med Sci Sports Exerc 1987, 19, S157–S165. 3316915

16. Williams B.D.; Robert R.W.; Bracy D.P.; Wasserman D.H. Gut proteolysis contributes essential amino acids during exercise. American journal of physiology. Endocrinology and metabolism 1996, 270, E85–E90.

17. Burton D.A.; Stokes K.; Hall G.M. Physiological effects of exercise. BJA Educ 2004, 4.

18. Brouns F.; Saris W.H.; Rehrer N.J. Abdominal complaints and gastrointestinal function during long-lasting exercise. International journal of sports medicine 1987, 8, 175–189, doi: 10.1055/s-2008-1025653 3305389

19. de Koning T.J.; Snell K.; Duran M.; Berger R.; Poll-The B.-T.; Surtees R. L-serine in disease and development. Biochemical Journal 2003, 371, 653–661, doi: 10.1042/BJ20021785 12534373

20. Pratt-Phillips S.E.; Lawrence L.M. Nutrition of the performance horse. In The Athletic Horse, 2nd ed.; Hodgson D.R., McKeever K.H., McGowan C.M., Eds. W.B. Saunders: 2014; doi: 10.1016/b978-0-7216-0075-8.00013-7pp. 34–55.

21. Geor R.; Harris P.; Coenen M. Equine applied and clinical nutrition; Saunders Elsevier: 2013; pp. 696.

22. Millward D.J.; Bates P.C.; de Benoist B.; Brown J.G.; Cox M.; Halliday D.; et al. Protein turnover: the nature of the phenomenon and its physiological regulation [degradation of specific proteins, non specific degradation; protein and energy requirements]. Colloques de l'INRA (France) 1983, 1, 69–96.

23. Reeds P.J.; Harris C.l. Protein turnover in animals: man in his context. In Nitrogen metabolism in man, Waterlow J.C., Stephen J.M.L., Eds. Applied Science Publishers: London, 1981; pp. 391–408.

24. Ricard-Blum S. The collagen family. Cold Spring Harb Perspect Biol. 2011, 3, a004978, doi: 10.1101/cshperspect.a004978 21421911

25. Gunn H.M. Muscle, bone and fat proportions and muscle distribution of Thoroughbreds and other horses. In Equine Exercise Physiology 2, Gillespie J.R., Robinson N.E., Eds. ICEEP Publications: Davis, CA, 1987; pp. 253–264.

26. Waterlow J.C. Protein turnover with special reference to man. Quarterly journal of experimental physiology (Cambridge, England) 1984, 69, 409–438.

27. Waterlow J.C.; Jackson A.A. Nutrition and protein turnover in man. British Medical Bulletin 1981, 37, 5–10. doi: 10.1093/oxfordjournals.bmb.a071676 7020867

28. Montero D.; Cathomen A.; Jacobs R.A.; Fluck D.; de Leur J.; Keiser S.; et al. Haematological rather than skeletal muscle adaptations contribute to the increase in peak oxygen uptake induced by moderate endurance training. The Journal of physiology 2015, 593, 4677–4688, doi: 10.1113/JP270250 26282186

29. McGowan C.M.; Hodgson D.R. Hematology and biochemistry. In The Athletic Horse: Principles and Practice of Equine Sports Medicine, SECOND EDITION ed.; W.B. Saunders: 2014; https://doi.org/10.1016/B978-0-7216-0075-8.00014-9pp. 56–68.

30. Knottenbelt D.C.; Malalana F. Part 1—Vital signs, normal values. In Saunders Equine Formulary (Second Edition), W.B. Saunders: 2015; https://doi.org/10.1016/B978-0-7020-5109-8.00001-8pp. 1–37.

31. Boldt J. Use of albumin: an update. British journal of anaesthesia 2010, 104, 276–284, doi: 10.1093/bja/aep393 20100698

32. Tokita N.; Shimojo M.; Masuda Y. Amino Acid Profiles of Tropical Legumes, Cooper (Glycine wightii), Tinaroo (Neonotonia wightii) and Siratro (Macroptilium atropurpureum), at Pre-blooming and Blooming Stages. Asian-Australasian Journal of Animal Sciences 2006, 19, 651–654.

33. al-Gaby A.M. Amino acid composition and biological effects of supplementing broad bean and corn proteins with Nigella sativa (black cumin) cake protein. Die Nahrung 1998, 42, 290–294. doi: 10.1002/(sici)1521-3803(199810)42:05<290::aid-food290>3.0.co;2-y 9882224

34. Pomeranz Y.; Robbins G.S.; Briggle L.W. Amino acid composition of oat groats. Journal of agricultural and food chemistry 1971, 19, 536–539, doi: 10.1021/jf60175a016

35. Babinec J.; Kozová Z.; Straková E.; Suchy P. The variance of the amino acids in some lucerne (Medicago sativa L.) populations. In Quality in lucerne and medics for animal production, Delgado I., Lloveras J., Eds. Zaragoza: CIHEAM: 2001; Vol. 45, pp. 235–239.

36. Folkes B.F.; Yemm E.W. The amino acid content of the proteins of barley grains. Biochemical Journal 1956, 62, 4–11. doi: 10.1042/bj0620004 13293145

37. Chen C.H.; Bushuk W. Nature of proteins in Triticale and its parental species: 1. Solubility characteristics and amino acid composition of endosperm proteins. Canadian Journal of Plant Science 1970, 50, 9–14, doi: 10.4141/cjps70-002

38. Chung E.; Miller E.J. Collagen polymorphism: characterization of molecules with the chain composition (alpha 1 (3)03 in human tissues. Science 1974, 183, 1200–1201. doi: 10.1126/science.183.4130.1200 4812351

39. Spahr P.F.; Edsall J.T. Amino acid composition of human and bovine serum mercaptalbumins. J Biol Chem 1964, 239, 850–854. 14154465

40. Stein W.H.; Kunkel H.G.; Cole R.D.; Spackman D.H.; Moore S. Observation on the amino acid composition of human hemoglobins. Biochim Biophys Acta 1957, 24, 640–642. doi: 10.1016/0006-3002(57)90261-5 13436493

41. Stein, W.H. Observations of the amino acid composition of human hemoglobins. In Proceedings of National Academy of Sciences (US) and National Research Council (US) Division of Medical Sciences. Conference on Hemoglobin: 2–3 May 1957., Washington (DC), 1958.

42. Carsten M.E. Actin, its amino acid composition and its reaction with iodoacetate. Biochemistry 1963, 2, 32–34. doi: 10.1021/bi00901a007 14018933

43. Raszkowski R.R.; Welty J.D.; Peterson M.B. The amino acid composition of actin and myosin and Ca2+-activated myosin adenosine triphosphatase in chronic canine congestive heart failure. Circulation research 1977, 40, 191–198. doi: 10.1161/01.res.40.2.191 139212

44. Martin-Rosset W.; Vermorel M.; Doreau M.; Tisserand J.L.; Andrieu J. The French horse feed evaluation systems and recommended allowances for energy and protein. Livestock Production Science 1994, 40, 37–56, https://doi.org/10.1016/0301-6226(94)90264-X.

45. Hodgson D.R.; McKeever K.H.; McGowan C.M. The Athletic Horse. Principles and Practice of Equine Sports Medicine, 2nd ed.; Hodgson D.R., McKeever K.H., McGowan C.M., Eds.; Elsevier Health Sciences; W.B. Saunders: London, 2014; https://doi.org/10.1016/C2009-0-46058-6pp. 408.

46. Beeley J.R.; Eason R.; Snow D.H. Isolation and characterization of latherin, a surface-active protein from horse sweat. Biochem. J. 1986, 235, 645–650. doi: 10.1042/bj2350645 3753435

47. Winkel C. Untersuchungen uber Schweissmenge und zusammensetzung des Pferdes unter besonderer Berucksichtigung der Eiweissversorgung. Vet. Diss. Hanover 1977.

48. Dunstan R.H.; Sparkes D.L.; Macdonald M.M.; Janse De Jonge X.; Dascombe B.J.; Gottfries J.; et al. Diverse characteristics of the urinary excretion of amino acids in humans and the use of amino acid supplementation to reduce fatigue and sub-health in adults. Nutr J 2017, 16, 19, doi: 10.1186/s12937-017-0240-y 28330481

49. Bauchart C.; Savary-Auzeloux I.; Patureau Mirand P.; Thomas E.; Morzel M.; Remond D. Carnosine concentration of ingested meat affects carnosine net release into the portal vein of minipigs. J Nutr 2007, 137, 589–593. doi: 10.1093/jn/137.3.589 17311945

50. Tamaki N.; Funatsuka A.; Fujimoto S.; Hama T. The utilization of carnosine in rats fed on a histidine-free diet and its effect on the levels of tissue histidine and carnosine. Journal of nutritional science and vitaminology 1984, 30, 541–551. doi: 10.3177/jnsv.30.541 6533273

51. Snell K.; Natsumeda Y.; Weber G. The modulation of serine metabolism in hepatoma 3924A during different phases of cellular proliferation in culture. The Biochemical journal 1987, 245, 609–612. doi: 10.1042/bj2450609 3117048

52. de Paz-Lugo P.; Lupianez J.A.; Melendez-Hevia E. High glycine concentration increases collagen synthesis by articular chondrocytes in vitro: acute glycine deficiency could be an important cause of osteoarthritis. Amino Acids 2018, 50, 1357–1365, doi: 10.1007/s00726-018-2611-x 30006659

53. Eagle H. Amino acid metabolism in mammalian cell cultures. Science 1959, 130, 432–437. doi: 10.1126/science.130.3373.432 13675766

54. Darling P.B.; Dunn M.; Sarwar G.; Brookes S.; Ball R.O.; Pencharz P.B. Threonine kinetics in preterm infants fed their mothers' milk or formula with various ratios of whey to casein. Am J Clin Nutr 1999, 69, 105–114, doi: 10.1093/ajcn/69.1.105 9925131

55. Wu G. Functional amino acids in growth, reproduction, and health. Advances in nutrition (Bethesda, Md.) 2010, 1, 31–37, doi: 10.3945/an.110.1008 22043449

56. Jackson A.A. The glycine story. European journal of clinical nutrition 1991, 45, 59–65. 2050089

57. Wu G. Recent advances in swine amino acid nutrition. Journal of Animal Science and Biotechnology 2010, 1, 118–130.

58. Meléndez-Hevia E.; de Paz-Lugo P.; Cornish-Bowden A.; Cárdenas M.L. A weak link in metabolism: the metabolic capacity for glycine biosynthesis does not satisfy the need for collagen synthesis. J Biosci 2009, 34, 853–872. doi: 10.1007/s12038-009-0100-9 20093739

59. Rezaei R.; Wang W.; Wu Z.; Dai Z.; Wang J.; Wu G. Biochemical and physiological bases for utilization of dietary amino acids by young Pigs. Journal of animal science and biotechnology 2013, 4, 7, doi: 10.1186/2049-1891-4-7 23445937

60. Wang W.; Wu Z.; Dai Z.; Yang Y.; Wang J.; Wu G. Glycine metabolism in animals and humans: implications for nutrition and health. Amino Acids 2013, 45, 463–477, doi: 10.1007/s00726-013-1493-1 23615880

61. Stover P.J.; Chen L.H.; Suh J.R.; Stover D.M.; Keyomarsi K.; Shane B. Molecular Cloning, Characterization, and Regulation of the Human Mitochondrial Serine Hydroxymethyltransferase Gene. J Biol Chem 1997, 272, 1842–1848. doi: 10.1074/jbc.272.3.1842 8999870

62. Sugino T.; Shirai T.; Kajimoto Y.; Kajimoto O. L-ornithine supplementation attenuates physical fatigue in healthy volunteers by modulating lipid and amino acid metabolism. Nutrition research (New York, N.Y.) 2008, 28, 738–743, doi: 10.1016/j.nutres.2008.08.008 19083482

63. Rodwell V.W. Conversion of amino acids to specialized products. In Harper's biochemistry., 25th ed ed.; Murray R.K., Granner D.K., Mayes P.A., Rodwell P.W., Eds. Appleton & Lange: New York, 2000.

64. Briggs S.; Freedland R.A. Effect of ornithine and lactate on urea synthesis in isolated hepatocytes. The Biochemical journal 1976, 160, 205–209. doi: 10.1042/bj1600205 1008850

65. Pokrovskiy M.V.; Korokin M.V.; Tsepeleva S.A.; Pokrovskaya T.G.; Gureev V.V.; Konovalova E.A.; et al. Arginase inhibitor in the pharmacological correction of endothelial dysfunction. International journal of hypertension 2011, 2011, 515047, doi: 10.4061/2011/515047 21747978

66. Lawrence L. Nutrient needs of performance horses. Revista Brasileira de Zootecnia 2008, 37, 206–210.

67. Knowles A.M.; Herbert P.; Easton C.; Sculthorpe N.; Grace F.M. Impact of low-volume, high-intensity interval training on maximal aerobic capacity, health-related quality of life and motivation to exercise in ageing men. Age (Dordrecht, Netherlands) 2015, 37, 25, doi: 10.1007/s11357-015-9763-3 25773069

68. Imayama I.; Alfano C.M.; Mason C.E.; Wang C.; Xiao L.; Duggan C.; et al. Exercise adherence, cardiopulmonary fitness and anthropometric changes improve exercise self-efficacy and health-related quality of life. Journal of physical activity & health 2013, 10, 676–689.

69. Kopple J.D.; Swendseid M.E. Evidence that histidine is an essential amino acid in normal and chronically uremic man. J Clin Invest 1975, 55, 881–891, doi: 10.1172/JCI108016 1123426

70. Clemens R.A.; Kopple J.D.; Swendseid M.E. Metabolic effects of histidine-deficient diets fed to growing rats by gastric tube. J Nutr 1984, 114, 2138–2146. doi: 10.1093/jn/114.11.2138 6491766

71. Cooperman J.M.; Lopez R. The role of histidine in the anemia of folate deficiency. Experimental Biology and Medicine 2002, 227, 998–1000. doi: 10.1177/153537020222701107 12486209

72. Maxwell M.; McCoy T.A.; Neuman R.E. The amino acid requirements of the Walker carcinosarcoma 256 in vitro. Cancer research 1956, 16, 979–984. 13374708


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