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The influence of sex, age and heritability on human skeletal muscle carnosine content

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Abstract

The dipeptide carnosine is found in high concentrations in human skeletal muscle and shows large inter-individual differences. Sex and age are determining factors, however, systematic studies investigating the sex effects on muscle carnosine content throughout the human lifespan are lacking. Despite the large inter-individual variation, the intra-individual variation is limited. The question may be asked whether the carnosine content is a muscle characteristic which may be largely genetically determined. A total of 263 healthy male and female subjects of 9–83 years were divided into five different age groups: prepubertal children (PC), adolescents (A), young adults (YA), middle adults (MA) and elderly (E). We included 25 monozygotic and 22 dizygotic twin pairs among the entire study population to study the heritability. The carnosine content was measured non-invasively in the gastrocnemius medialis and soleus by proton magnetic resonance spectroscopy (1H-MRS). In boys, carnosine content was significantly higher (gastrocnemius 22.9%; soleus 44.6%) in A compared to PC, while it did not differ in girls. A decrease (~16%) was observed both in males and females from YA to MA. However, elderly did not have lower carnosine levels in comparison with MA. Higher correlations were found in monozygotic (r = 0.86) compared to dizygotic (r = 0.51) twins, in soleus muscle, but not in gastrocnemius. In conclusion, this study found an effect of puberty on muscle carnosine content in males, but not in females. Muscle carnosine decreased mainly during early adulthood and hardly from adulthood to elderly. High intra-twin correlations were observed, but muscle-dependent differences preclude clear conclusions toward heritability.

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References

  • Abe (2000) Role of histidine-related compounds as intracellular proton buffering constituents in vertebrate muscle. Biochemistry (Mosc) 65:757–765

  • Baguet A, Reyngoudt H, Pottier A, Everaert I, Callens S, Achten E, Derave W (2009) Carnosine loading and washout in human skeletal muscles. J Appl Physiol 106:837–842

    Article  PubMed  CAS  Google Scholar 

  • Baguet A, Bourgois J, Vanhee L, Achten E, Derave W (2010) Important role of muscle carnosine in rowing performance. J Appl Physiol 109:1096–1101

    Article  PubMed  Google Scholar 

  • Baguet A, Everaert I, De Naeyer H, Reyngoudt H, Stegen S, Beeckman S, Achten E, Vanhee L, Volkaert A, Petrovic M, Taes Y, Derave W (2011a) Effects of sprint training combined with vegetarian or mixed diet on muscle carnosine content and buffering capacity. Eur J Appl Physiol 111:2571–2580

    Article  PubMed  CAS  Google Scholar 

  • Baguet A, Everaert I, Hespel P, Petrovic M, Achten E, Derave W (2011b) A new method for non-invasive estimation of human muscle fiber type composition. PLoS One 6:e21956

    Article  PubMed  CAS  Google Scholar 

  • Bergstrom J, Hermansen L, Hultman E, Saltin B (1967) Diet, muscle glycogen and physical performance. Acta Physiol Scand 71:140–150

    Article  PubMed  CAS  Google Scholar 

  • Bouchard C, Simoneau JA, Lortie G, Boulay MR, Marcotte M, Thibault MC (1986) Genetic effects in human skeletal muscle fiber type distribution and enzyme activities. Can J Physiol Pharmacol 64:1245–1251

    Article  PubMed  CAS  Google Scholar 

  • Derave W, Ozdemir MS, Harris RC, Pottier A, Reyngoudt H, Koppo K, Wise JA, Achten E (2007) Beta-alanine supplementation augments muscle carnosine content and attenuates fatigue during repeated isokinetic contraction bouts in trained sprinters. J Appl Physiol 103:1736–1743

    Article  PubMed  CAS  Google Scholar 

  • Dunnett M, Harris RC, Soliman MZ, Suwar AA (1997) Carnosine, anserine and taurine contents in individual fibres from the middle gluteal muscle of the camel. Res Vet Sci 62:213–216

    Article  PubMed  CAS  Google Scholar 

  • Everaert I, Mooyaart A, Baguet A, Zutinic A, Baelde H, Achten E, Taes Y, De Heer E, Derave W (2010) Vegetarianism, female gender and increasing age, but not CNDP1 genotype, are associated with reduced muscle carnosine levels in humans. Amino Acids 40:1221–1229

    Article  PubMed  Google Scholar 

  • Gallant S, Semyonova M, Yuneva M (2000) Carnosine as a potential anti-senescence drug. Biochemistry (Mosc) 65:866–868

    CAS  Google Scholar 

  • Harris RC, Marlin DJ, Dunnett M, Snow DH, Hultman E (1990) Muscle buffering capacity and dipeptide content in the thoroughbred horse, greyhound dog and man. Comp Biochem Physiol A Comp Physiol 97:249–251

    Article  PubMed  CAS  Google Scholar 

  • Harris RC, Dunnett M, Greenhaff PL (1998) Carnosine and taurine contents in individual fibres of human vastus lateralis muscle. J Sports Sci 16:639–643

    Article  Google Scholar 

  • Harris RC, Tallon MJ, Dunnett M, Boobis L, Coakley J, Kim HJ, Fallowfield JL, Hill CA, Sale C, Wise JA (2006) The absorption of orally supplied beta-alanine and its effect on muscle carnosine synthesis in human vastus lateralis. Amino Acids 30:279–289

    Article  PubMed  CAS  Google Scholar 

  • Hill CA, Harris RC, Kim HJ, Harris BD, Sale C, Boobis LH, Kim CK, Wise JA (2007) Influence of beta-alanine supplementation on skeletal muscle carnosine concentrations and high intensity cycling capacity. Amino Acids 32:225–233

    Article  PubMed  CAS  Google Scholar 

  • Horwill F (2003) Knowing at what age an athlete is likely to achieve peak performance is a big help in planning a training programme. In: Brian MacKenzie’s successful coaching pp. 3–4. ISSN: 1745-7513 /3/ July

  • Janssen B, Hohenadel D, Brinkkoetter P, Peters V, Rind N, Fischer C, Rychlik I, Cerna M, Romzova M, De Heer E, Baelde H, Bakker SJ, Zirie M, Rondeau E, Mathieson P, Saleem MA, Meyer J, Koppel H, Sauerhoefer S, Bartram CR, Nawroth P, Hammes HP, Yard BA, Zschocke J, van der Woude FJ (2005) Carnosine as a protective factor in diabetic nephropathy: association with a leucine repeat of the carnosinase gene CNDP1. Diabetes 54:2320–2327

    Google Scholar 

  • Kaufman JM, Vermeulen A (2005) The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocr Rev 26:833–876

    Article  PubMed  CAS  Google Scholar 

  • Kiens B, Essen-Gustavsson B, Gad P, Lithell H (1987) Lipoprotein lipase activity and intramuscular triglyceride stores after long-term high-fat and high-carbohydrate diets in physically trained men. Clin Physiol 7:1–9

    Article  PubMed  CAS  Google Scholar 

  • Komi PV, Viitasalo JH, Havu M, Thorstensson A, Sjodin B, Karlsson J (1977) Skeletal muscle fibres and muscle enzyme activities in monozygous and dizygous twins of both sexes. Acta Physiol Scand 100:385–392

    PubMed  CAS  Google Scholar 

  • Kostka T, Drygas W, Jegier A, Zaniewicz D (2009) Aerobic and anaerobic power in relation to age and physical activity in 354 men aged 20–88 years. Int J Sports Med 30:225–230

    Article  PubMed  CAS  Google Scholar 

  • Mannion AF, Jakeman PM, Dunnett M, Harris RC, Willan PL (1992) Carnosine and anserine concentrations in the quadriceps femoris muscle of healthy humans. Eur J Appl Physiol Occup Physiol 64:47–50

    Article  PubMed  CAS  Google Scholar 

  • Mannion AF, Jakeman PM, Willan PL (1995) Skeletal muscle buffer value, fibre type distribution and high intensity exercise performance in man. Exp Physiol 80:89–101

    PubMed  CAS  Google Scholar 

  • Missitzi J, Geladas N, Klissouras V (2004) Heritability in neuromuscular coordination: implications for motor control strategies. Med Sci Sports Exerc 36:233–240

    Article  PubMed  Google Scholar 

  • Neale MC, Boker SM, Xie G, Maes HH (2003) Mx: Statistical Modeling, 6th Edn. VCU Box 900126, Richmond, VA 23298: Department of Psychiatry

  • Peeters H, Van Gestel S, Vlietinck R, Derom C, Derom R (1998) Validation of a telephone zygosity questionnaire in twins of known zygosity. Behav Genet 28:159–163

    Article  PubMed  CAS  Google Scholar 

  • Penafiel R, Ruzafa C, Monserrat F, Cremades A (2004) Gender-related differences in carnosine, anserine and lysine content of murine skeletal muscle. Amino Acids 26:53–58

    Article  PubMed  CAS  Google Scholar 

  • Quinn PJ, Boldyrev AA, Formazuyk VE (1992) Carnosine: its properties, functions and potential therapeutic applications. Mol Aspects Med 13:379–444

    Article  PubMed  CAS  Google Scholar 

  • Ramos E, Frontera WR, Llopart A, Feliciano D (1998) Muscle strength and hormonal levels in adolescents: gender related differences. Int J Sports Med 19:526–531

    Article  PubMed  CAS  Google Scholar 

  • Sahlin K, Soderlund K, Tonkonogi M, Hirakoba K (1997) Phosphocreatine content in single fibers of human muscle after sustained submaximal exercise. Am J Physiol 273:C172–C178

    PubMed  CAS  Google Scholar 

  • Sewell DA, Harris RC, Marlin DJ, Dunnett M (1992) Estimation of the carnosine content of different fibre types in the middle gluteal muscle of the thoroughbred horse. J Physiol 455:447–453

    PubMed  CAS  Google Scholar 

  • Simoneau JA, Bouchard C (1995) Genetic determinism of fiber type proportion in human skeletal muscle. FASEB J 9:1091–1095

    PubMed  CAS  Google Scholar 

  • Starka L, Pospisilova H, Hill M (2009) Free testosterone and free dihydrotestosterone throughout the life span of men. J Steroid Biochem Mol Biol 116:118–120

    Article  PubMed  CAS  Google Scholar 

  • Starling RD, Trappe TA, Parcell AC, Kerr CG, Fink WJ, Costill DL (1997) Effects of diet on muscle triglyceride and endurance performance. J Appl Physiol 82:1185–1189

    PubMed  CAS  Google Scholar 

  • Stellingwerff T, Anwander H, Egger A, Buehler T, Kreis R, Decombaz J, Boesch C (2011) Effect of two beta-alanine dosing protocols on muscle carnosine synthesis and washout. Amino Acids (in press)

  • Stout JR, Cramer JT, Zoeller RF, Torok D, Costa P, Hoffman JR, Harris RC, O’Kroy J (2007) Effects of beta-alanine supplementation on the onset of neuromuscular fatigue and ventilatory threshold in women. Amino Acids 32:381–386

    Article  PubMed  CAS  Google Scholar 

  • Stuerenburg HJ, Kunze K (1999) Concentrations of free carnosine (a putative membrane-protective antioxidant) in human muscle biopsies and rat muscles. Arch Gerontol Geriatr 29:107–113

    Article  PubMed  CAS  Google Scholar 

  • Suzuki Y, Ito O, Mukai N, Takahashi H, Takamatsu K (2002) High level of skeletal muscle carnosine contributes to the latter half of exercise performance during 30-s maximal cycle ergometer sprinting. Jpn J Physiol 52:199–205

    Article  PubMed  CAS  Google Scholar 

  • Tallon MJ, Harris RC, Maffulli N, Tarnopolsky MA (2007) Carnosine, taurine and enzyme activities of human skeletal muscle fibres from elderly subjects with osteoarthritis and young moderately active subjects. Biogerontology 8:129–137

    Article  PubMed  CAS  Google Scholar 

  • Thomis MA, Van Leemputte M, Maes HH, Blimkie CJ, Claessens AL, Marchal G, Willems E, Vlietinck RF, Beunen GP (1997) Multivariate genetic analysis of maximal isometric muscle force at different elbow angles. J Appl Physiol 82:959–967

    Google Scholar 

  • Van Thienen R, Van Proeyen K, Vanden Eynde B, Puype J, Lefere T, Hespel P (2009) Beta-alanine improves sprint performance in endurance cycling. Med Sci Sports Exerc 41:898–903

    Article  PubMed  Google Scholar 

  • Vingren JL, Kraemer WJ, Ratamess NA, Anderson JM, Volek JS, Maresh CM (2010) Testosterone physiology in resistance exercise and training: the up-stream regulatory elements. Sports Med 40:1037–1053

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was financially supported by a grant from the Research Foundation-Flanders (FWO 1.5.149.08 and G024311 N). A. Baguet is a recipient of a PhD scholarship from the Research Foundation-Flanders.

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The authors declare that they have no conflict of interest.

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Correspondence to Wim Derave.

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Baguet, A., Everaert, I., Achten, E. et al. The influence of sex, age and heritability on human skeletal muscle carnosine content. Amino Acids 43, 13–20 (2012). https://doi.org/10.1007/s00726-011-1197-3

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