The Journal of Nutritional Biochemistry
Volume 21, Issue 11 , Pages 1076-1082 , November 2010

The skeletal muscle transcript profile reflects accommodative responses to inadequate protein intake in younger and older males

  • Anna E. Thalacker-Mercer

      Affiliations

    • Department of Foods and Nutrition, Purdue University, West Lafayette, IN 47907, USA
  • ,
  • James C. Fleet

      Affiliations

    • Department of Foods and Nutrition, Purdue University, West Lafayette, IN 47907, USA
  • ,
  • Bruce A. Craig

      Affiliations

    • Department of Statistics, Purdue University, West Lafayette, IN 47907, USA
  • ,
  • Wayne W. Campbell

      Affiliations

    • Department of Foods and Nutrition, Purdue University, West Lafayette, IN 47907, USA
    • Corresponding Author InformationCorresponding author.

Received 25 March 2009 ,Revised 3 August 2009 ,Accepted 11 September 2009.

References 

  1. Swick RW, Benevenga NJ. Labile protein reserves and protein turnover. J Dairy Sci. 1977;60:505–515
  2. Hansen RD, Raja C, Allen BJ. Total body protein in chronic diseases and in aging. Ann N Y Acad Sci. 2000;904:345–352
  3. Young VR, Marchini JS. Mechanisms and nutritional significance of metabolic responses to altered intakes of protein and amino acids, with reference to nutritional adaptation in humans. Am J Clin Nutr. 1990;51:270–289
  4. Waterlow JC. Metabolic adaptation to low intakes of energy and protein. Annu Rev Nutr. 1986;6:495–526
  5. Castaneda C, Charnley JM, Evans WJ, Crim MC. Elderly women accommodate to a low-protein diet with losses of body cell mass, muscle function, and immune response. Am J Clin Nutr. 1995;62:30–39
  6. Castaneda C, Gordon PL, Fielding RA, Evans WJ, Crim MC. Marginal protein intake results in reduced plasma IGF-I levels and skeletal muscle fiber atrophy in elderly women. J Nutr Health Aging. 2000;4:85–90
  7. Campbell WW, Trappe TA, Wolfe RR, Evans WJ. The recommended dietary allowance for protein may not be adequate for older people to maintain skeletal muscle. J Gerontol A Biol Sci Med Sci. 2001;56:M373–380
  8. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids. Washington, DC: The Institute of Medicine of the National Academies; 2002;
  9. Kayo T, Allison DB, Weindruch R, Prolla TA. Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys. Proc Natl Acad Sci U S A. 2001;98:5093–5098
  10. Lee CK, Klopp RG, Weindruch R, Prolla TA. Gene expression profile of aging and its retardation by caloric restriction. Science. 1999;285:1390–1393
  11. Weindruch R, Kayo T, Lee CK, Prolla TA. Microarray profiling of gene expression in aging and its alteration by caloric restriction in mice. J Nutr. 2001;131:918S–923S
  12. Cameron-Smith D, Burke LM, Angus DJ, Tunstall RJ, Cox GR, Bonen A, et al. A short-term, high-fat diet up-regulates lipid metabolism and gene expression in human skeletal muscle. Am J Clin Nutr. 2003;77:313–318
  13. Arkinstall MJ, Tunstall RJ, Cameron-Smith D, Hawley JA. Regulation of metabolic genes in human skeletal muscle by short-term exercise and diet manipulation. Am J Physiol Endocrinol Metab. 2004;287:E25–E31
  14. Thalacker-Mercer AE, Fleet JC, Craig BA, Carnell NS, Campbell WW. Inadequate protein intake affects skeletal muscle transcript profiles in older humans. Am J Clin Nutr. 2007;85:1344–1352
  15. Endo Y, Fu Z, Abe K, Arai S, Kato H. Dietary protein quantity and quality affect rat hepatic gene expression. J Nutr. 2002;132:3632–3637
  16. Campbell WW, Johnson CA, McCabe GP, Carnell NS. Dietary protein requirements of younger and older adults. Am J Clin Nutr. 2008;88:1322–1329
  17. Harris JA, Benedict FG. A biometric study of human basal metabolism. Proc Natl Acad Sci U S A. 1918;4:370–373
  18. Thalacker-Mercer AE, Johnson CA, Yarasheski KE, Carnell NS, Campbell WW. Nutrient ingestion, protein intake, and sex, but not age, affect the albumin synthesis rate in humans. J Nutr. 2007;137:1734–1740
  19. Kruskall LJ, Campbell WW, Evans WJ. The Yale Physical Activity Survey for older adults: predictions in the energy expenditure due to physical activity. J Am Diet Assoc. 2004;104:1251–1257
  20. Evans WJ, Phinney SD, Young VR. Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc. 1982;14:101–102
  21. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402–408
  22. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80
  23. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249–264
  24. R Development Core Team . R: a language and environment for statistical computing. R Foundation for Statistical Computing; 2006;
  25. Davison A, Hinkley D. Bootstrap methods and their applications. Cambridge (UK): Cambridge University Press; 1997;
  26. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57:289–300
  27. Golub TR, Slonim DK, Tamayo P, Huard C, Gaasenbeek M, Mesirov JP, et al Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999;286:531–537
  28. Tamayo P, Slonim D, Mesirov J, Zhu Q, Kitareewan S, Dmitrovsky E, et al. Interpreting patterns of gene expression with self-organizing maps: methods and application to hematopoietic differentiation. Proc Natl Acad Sci U S A. 1999;96:2907–2912
  29. Doniger SW, Salomonis N, Dahlquist KD, Vranizan K, Lawlor SC, Conklin BR. MAPPFinder: using gene ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol. 2003;4:R7
  30. Dahlquist KD, Salomonis N, Vranizan K, Lawlor SC, Conklin BR. GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat Genet. 2002;31:19–20
  31. Campbell WW, Crim MC, Dallal GE, Young VR, Evans WJ. Increased protein requirements in elderly people: new data and retrospective reassessments. Am J Clin Nutr. 1994;60:501–509
  32. Gersovitz M, Motil K, Munro HN, Scrimshaw NS, Young VR. Human protein requirements: assessment of the adequacy of the current recommended dietary allowance for dietary protein in elderly men and women. Am J Clin Nutr. 1982;35:6–14
  33. Uauy R, Scrimshaw NS, Young VR. Human protein requirements: nitrogen balance response to graded levels of egg protein in elderly men and women. Am J Clin Nutr. 1978;31:779–785
  34. Campbell WW, Trappe TA, Jozsi AC, Kruskall LJ, Wolfe RR, Evans WJ. Dietary protein adequacy and lower body versus whole body resistive training in older humans. J Physiol. 2002;542:631–642
  35. Vellas BJ, Hunt WC, Romero LJ, Koehler KM, Baumgartner RN, Garry PJ. Changes in nutritional status and patterns of morbidity among free-living elderly persons: a 10-year longitudinal study. Nutrition. 1997;13:515–519
  36. Campbell WW, Barton ML, Cyr-Campbell D, Davey SL, Beard JL, Parise G, et al. Effects of an omnivorous diet compared with a lactoovovegetarian diet on resistance-training-induced changes in body composition and skeletal muscle in older men. Am J Clin Nutr. 1999;70:1032–1039
  37. Mitch WE, Goldberg AL. Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med. 1996;335:1897–1905
  38. Hasselgren PO, Fischer JE. Muscle cachexia: current concepts of intracellular mechanisms and molecular regulation. Ann Surg. 2001;233:9–17
  39. Combaret L, Dardevet D, Rieu I, Pouch MN, Bechet D, Taillandier D, et al. A leucine-supplemented diet restores the defective postprandial inhibition of proteasome-dependent proteolysis in aged rat skeletal muscle. J Physiol. 2005;569:489–499
  40. Welle S, Brooks AI, Delehanty JM, Needler N, Thornton CA. Gene expression profile of aging in human muscle. Physiol Genomics. 2003;14:149–159
  41. Welle S, Brooks AI, Delehanty JM, Needler N, Bhatt K, Shah B, et al. Skeletal muscle gene expression profiles in 20-29 year old and 65-71 year old women. Exp Gerontol. 2004;39:369–377
  42. Jozsi AC, Dupont-Versteegden EE, Taylor-Jones JM, Evans WJ, Trappe TA, Campbell WW, et al. Aged human muscle demonstrates an altered gene expression profile consistent with an impaired response to exercise. Mech Ageing Dev. 2000;120:45–56
  43. Jozsi AC, Dupont-Versteegden EE, Taylor-Jones JM, Evans WJ, Trappe TA, Campbell WW, et al. Molecular characteristics of aged muscle reflect an altered ability to respond to exercise. Int J Sport Nutr Exerc Metab. 2001;11(Suppl):S9–S15
  44. Giresi PG, Stevenson EJ, Theilhaber J, Koncarevic A, Parkington J, Fielding RA, et al. Identification of a molecular signature of sarcopenia. Physiol Genomics. 2005;21:253–263
  45. Roth SM, Ferrell RE, Peters DG, Metter EJ, Hurley BF, Rogers MA. Influence of age, sex, and strength training on human muscle gene expression determined by microarray. Physiol Genomics. 2002;10:181–190
  46. Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR. Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr. 2005;82:1065–1073
  47. Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR. A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Am J Physiol Endocrinol Metab. 2006;291:E381–E387

 The project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant numbers 03-35200-13779 (to WWC) and 98-35200-6151 (to WWC), NIH R01 AG15750 (to WWC), and a Purdue Research Foundation Research Assistantship.

PII: S0955-2863(09)00204-6

doi: 10.1016/j.jnutbio.2009.09.004

The Journal of Nutritional Biochemistry
Volume 21, Issue 11 , Pages 1076-1082 , November 2010