Musculoskeletal system in the old age and the demand for healthy ageing biomarkers

Mechanisms of Ageing and Development

Volumn 134, Issue 11-12, 2013, Pages 541-547

  Collino, Sebastiano ^a   Martin, François Pierre ^a   Karagounis, Leonidas G ^a   Horcajada, Marie Noelle ^a   Moco, Sofia ^b   Franceschi, Claudio ^a   Kussmann, Martin ^a,c,d   Offord, Elizabeth ^a  

^a NESTLÉ RESEARCH CENTER   (Switzerland)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c EPFL   (Switzerland)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

Ageing; Bone; Longevity; Metabolomics; Muscle

Indexed keywords

ACYLCARNITINE; BIOLOGICAL MARKER; CYTOCHROME P450; GLYCEROPHOSPHOLIPID; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; TRANSCRIPTION FACTOR FOXO; TRYPTOPHAN; UBIQUITIN PROTEIN LIGASE E3;

ADAPTATION; AGING; ARTICLE; AWARENESS; BONE DENSITY; BONE METABOLISM; BONE TURNOVER; COMPUTER ASSISTED TOMOGRAPHY; ENZYME ACTIVATION; FRAGILITY FRACTURE; HEALTH CARE SYSTEM; HEALTH PROMOTION; HOMEOSTASIS; HUMAN; INTESTINE FLORA; LIFESTYLE; LONGEVITY; MASS SPECTROMETRY; METABOLOMICS; MOLECULAR DYNAMICS; MORBIDITY; MUSCLE MASS; MUSCULOSKELETAL SYSTEM; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTON NUCLEAR MAGNETIC RESONANCE; QUALITY OF LIFE;

AGEING; BONE; LONGEVITY; METABOLOMICS; MUSCLE;

AGED; AGED, 80 AND OVER; AGING; BIOLOGICAL MARKERS; FEMALE; FRAIL ELDERLY; HUMANS; IMMUNE SYSTEM; INFLAMMATION; LONGEVITY; MALE; METABOLOMICS; MUSCLE, SKELETAL; NUTRITIONAL SCIENCES; OSTEOPOROSIS; PHENOTYPE; RISK FACTORS;

EID: 84891557008     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2013.11.003     Document Type: Article

References (75)

1. Actis G.C., Pazienza P., Rosina F. Mesalamine for inflammatory bowel disease: recent reappraisals. Inflamm. Allergy Drug Targets 2008, 7:1-5.
2. Alonso C., Guilarte M., Vicario M., Ramos L., Rezzi S., Martinez C., Lobo B., Martin F.P., Pigrau M., Gonzalez-Castro A.M., Gallart M., Malagelada J.R., Azpiroz F., Kochhar S., Santos J. Acute experimental stress evokes a differential gender-determined increase in human intestinal macromolecular permeability. Neurogastroenterol. Motil. 2012, 24. 740-e349.
3. Baur P., Martin F.P., Gruber L., Bosco N., Brahmbhatt V., Collino S., Guy P., Montoliu I., Rozman J., Klingenspor M., Tavazzi I., Thorimbert A., Rezzi S., Kochhar S., Benyacoub J., Kollias G., Haller D. Metabolic phenotyping of the Crohn's disease-like IBD etiopathology in the TNF(DeltaARE/WT) mouse model. J. Proteome Res. 2011, 10:5523-5535.
4. Biagi E., Candela M., Turroni S., Garagnani P., Franceschi C., Brigidi P. Ageing and gut microbes: perspectives for health maintenance and longevity. Pharmacol. Res. 2013, 69:11-20.
5. Bodine S.C., Stitt T.N., Gonzalez M., Kline W.O., Stover G.L., Bauerlein R., Zlotchenko E., Scrimgeour A., Lawrence J.C., Glass D.J., Yancopoulos G.D. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 2001, 3:1014-1019.
6. Buescher J.M., Moco S., Sauer U., Zamboni N. Ultrahigh performance liquid chromatography-tandem mass spectrometry method for fast and robust quantification of anionic and aromatic metabolites. Anal. Chem. 2010, 82:4403-4412.
7. Burkle A., Caselli G., Franceschi C., Mariani E., Sansoni P., Santoni A., Vecchio G., Witkowski J.M., Caruso C. Pathophysiology of ageing, longevity and age related diseases. Immun. Ageing 2007, 4:4.
8. Collino S., Martin F.P., Rezzi S. Clinical metabolomics paves the way towards future healthcare strategies. Br. J. Clin. Pharmacol. 2013, 75:619-629.
9. Collino S., Montoliu I., Martin F.P., Scherer M., Mari D., Salvioli S., Bucci L., Ostan R., Monti D., Biagi E., Brigidi P., Franceschi C., Rezzi S. Metabolic signatures of extreme longevity in northern italian centenarians reveal a complex remodeling of lipids, amino acids, and gut microbiota metabolism. PLoS ONE 2013, 8:e56564.
10. Cuthbertson D., Smith K., Babraj J., Leese G., Waddell T., Atherton P., Wackerhage H., Taylor P.M., Rennie M.J. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 2005, 19:422-424.
11. Cuthbertson D.J., Babraj J., Smith K., Wilkes E., Fedele M.J., Esser K., Rennie M. Anabolic signaling and protein synthesis in human skeletal muscle after dynamic shortening or lengthening exercise. Am. J. Physiol. Endocrinol. Metab. 2006, 290:E731-E738.
12. Delmas P.D., Li Z., Cooper C. Relationship between changes in bone mineral density and fracture risk reduction with antiresorptive drugs: some issues with meta-analyses. J. Bone Miner. Res. 2004, 19:330-337.
13. Duncan M., Davison J.S., Sharkey K.A. Review article: endocannabinoids and their receptors in the enteric nervous system. Aliment. Pharmacol. Ther. 2005, 22:667-683.
14. El A.S., Hooiveld G., Tremaroli V., Backhed F., Kleerebezem M. The gut microbiota and mucosal homeostasis: colonized at birth or at adulthood, does it matter?. Gut Microbes 2013, 4:118-124.
15. Fielding R.A., Vellas B., Evans W.J., Bhasin S., Morley J.E., Newman A.B., Abellan van K.G., Andrieu S., Bauer J., Breuille D., Cederholm T., Chandler J., De M.C., Donini L., Harris T., Kannt A., Keime G.F., Onder G., Papanicolaou D., Rolland Y., Rooks D., Sieber C., Souhami E., Verlaan S., Zamboni M. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J. Am. Med. Dir. Assoc. 2011, 12:249-256.
16. Franceschi C. Inflammaging as a major characteristic of old people: can it be prevented or cured. Nutr. Rev. 2007, 65:S173-S176.
17. Franceschi C., Capri M., Monti D., Giunta S., Olivieri F., Sevini F., Panourgia M.P., Invidia L., Celani L., Scurti M., Cevenini E., Castellani G.C., Salvioli S. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech. Ageing Dev. 2007, 128:92-105.
18. Franceschi C., Motta L., Valensin S., Rapisarda R., Franzone A., Berardelli M., Motta M., Monti D., Bonafe M., Ferrucci L., Deiana L., Pes G.M., Carru C., Desole M.S., Barbi C., Sartoni G., Gemelli C., Lescai F., Olivieri F., Marchegiani F., Cardelli M., Cavallone L., Gueresi P., Cossarizza A., Troiano L., Pini G., Sansoni P., Passeri G., Lisa R., Spazzafumo L., Amadio L., Giunta S., Stecconi R., Morresi R., Viticchi C., Mattace R., De B.G., Baggio G. Do men and women follow different trajectories to reach extreme longevity? Italian Multicenter Study on Centenarians (IMUSCE). Aging (Milano) 2000, 12:77-84.
19. Frontera W.R., Hughes V.A., Fielding R.A., Fiatarone M.A., Evans W.J., Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J. Appl. Physiol. 2000, 88:1321-1326.
20. Gonzalez-Covarrubias V., Beekman M., Uh H.W., Dane A., Troost J., Paliukhovich I., van der Kloet F.M., Houwing-Duistermaat J., Vreeken R.J., Hankemeier T., Slagboom E.P. Lipidomics of familial longevity. Aging Cell 2013, 12:426-434.
21. Greenhaff P.L., Karagounis L.G., Peirce N., Simpson E.J., Hazell M., Layfield R., Wackerhage H., Smith K., Atherton P., Selby A., Rennie M.J. Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E595-E604.
22. Guigoz Y., Dore J., Schiffrin E.J. The inflammatory status of old age can be nurtured from the intestinal environment. Curr. Opin. Clin. Nutr. Metab. Care 2008, 11:13-20.
23. Habauzit V., Sacco S.M., Gil-Izquierdo A., Trzeciakiewicz A., Morand C., Barron D., Pinaud S., Offord E., Horcajada M.N. Differential effects of two citrus flavanones on bone quality in senescent male rats in relation to their bioavailability and metabolism. Bone 2011, 49:1108-1116.
24. Hara K., Yonezawa K., Weng Q.P., Kozlowski M.T., Belham C., Avruch J. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J. Biol. Chem. 1998, 273:14484-14494.
25. Harper P.H., Truelove S.C., Lee E.C., Kettlewell M.G., Jewell D.P. Split ileostomy and ileocolostomy for Crohn's disease of the colon and ulcerative colitis: a 20 year survey. Gut 1983, 24:106-113.
26. Heilbronn L.K., Ravussin E. Calorie restriction extends life span - but which calories?. PLoS Med. 2005, 2:e231.
27. Holmes E., Kinross J., Gibson G.R., Burcelin R., Jia W., Pettersson S., Nicholson J.K. Therapeutic modulation of microbiota-host metabolic interactions. Sci. Transl. Med. 2012, 4:137rv6.
28. Horcajada M.N., Habauzit V., Trzeciakiewicz A., Morand C., Gil-Izquierdo A., Mardon J., Lebecque P., Davicco M.J., Chee W.S., Coxam V., Offord E. Hesperidin inhibits ovariectomized-induced osteopenia and shows differential effects on bone mass and strength in young and adult intact rats. J. Appl. Physiol. 2008, 104:648-654.
29. Karagounis L.G., Hawley J.A. Skeletal muscle: increasing the size of the locomotor cell. Int. J. Biochem. Cell Biol. 2010, 42:1376-1379.
30. Keaveny T.M., Kopperdahl D.L., Melton L.J., Hoffmann P.F., Amin S., Riggs B.L., Khosla S. Age-dependence of femoral strength in white women and men. J. Bone Miner. Res. 2010, 25:994-1001.
31. Kirkwood T.B. Understanding the odd science of aging 2005.
32. Lawton K.A., Berger A., Mitchell M., Milgram K.E., Evans A.M., Guo L., Hanson R.W., Kalhan S.C., Ryals J.A., Milburn M.V. Analysis of the adult human plasma metabolome. Pharmacogenomics 2008, 9:383-397.
33. Le G.G., Noor S.O., Ridgway K., Scovell L., Jamieson C., Johnson I.T., Colquhoun I.J., Kemsley E.K., Narbad A. Metabolomics of fecal extracts detects altered metabolic activity of gut microbiota in ulcerative colitis and irritable bowel syndrome. J. Proteome Res. 2011, 10:4208-4218.
34. Lovat L.B. Age related changes in gut physiology and nutritional status. Gut 1996, 38:306-309.
35. Mair W., Piper M.D., Partridge L. Calories do not explain extension of life span by dietary restriction in Drosophila. PLoS Biol. 2005, 3:e223.
36. Marchesi J.R., Holmes E., Khan F., Kochhar S., Scanlan P., Shanahan F., Wilson I.D., Wang Y. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J. Proteome Res. 2007, 6:546-551.
37. Martin F.P., Collino S., Rezzi S. 1H NMR-based metabonomic applications to decipher gut microbial metabolic influence on mammalian health. Magn. Reson. Chem. 2011, 49(Suppl. 1):S47L S54.
38. Martin F.P., Collino S., Rezzi S., Kochhar S. Metabolomic applications to decipher gut microbial metabolic influence in health and disease. Front. Physiol. 2012, 3:113.
39. Martin F.P., Montoliu I., Kochhar S., Rezzi S. Chemometric strategy for modeling metabolic biological space along the gastrointestinal tract and assessing microbial influences. Anal. Chem. 2010, 82:9803-9811.
40. Martin F.P., Wang Y., Sprenger N., Holmes E., Lindon J.C., Kochhar S., Nicholson J.K. Effects of probiotic lactobacillus paracasei treatment on the host gut tissue metabolic profiles probed via magic-angle-spinning NMR spectroscopy. J. Proteome Res. 2007, 6:1471-1481.
41. Martin F.P., Wang Y., Yap I.K., Sprenger N., Lindon J.C., Rezzi S., Kochhar S., Holmes E., Nicholson J.K. Topographical variation in murine intestinal metabolic profiles in relation to microbiome speciation and functional ecological activity. J. Proteome Res. 2009, 8:3464-3474.
42. Milaneschi Y., Tanaka T., Ferrucci L. Nutritional determinants of mobility. Curr. Opin. Clin. Nutr. Metab. Care 2010, 13:625-629.
43. Moco S., Collino S., Rezzi S., Martin F.P. Metabolomics perspectives in pediatric research. Pediatr. Res. 2013, 73:570-576.
44. Morgan S.L., Kitchin B. Osteoporosis: handy tools for detection, helpful tips for treatment. J. Fam. Pract. 2008, 57:311-320.
45. Nagasawa T., Hirano J., Yoshizawa F., Nishizawa N. Myofibrillar protein catabolism is rapidly suppressed following protein feeding. Biosci. Biotechnol. Biochem. 1998, 62:1932-1937.
46. Nicholson J.K., Holmes E., Kinross J., Burcelin R., Gibson G., Jia W., Pettersson S. Host-gut microbiota metabolic interactions. Science 2012, 336:1262-1267.
47. Nicholson J.K., Lindon J.C., Holmes E. 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 1999, 29:1181-1189.
48. Nikkila J., Sysi-Aho M., Ermolov A., Seppanen-Laakso T., Simell O., Kaski S., Oresic M. Gender-dependent progression of systemic metabolic states in early childhood. Mol. Syst. Biol. 2008, 4:197.
49. Nordin B.E. Redefining osteoporosis. Calcif. Tissue Int. 2008, 83:365-367.
50. Piper M.D., Mair W., Partridge L. Counting the calories: the role of specific nutrients in extension of life span by food restriction. J. Gerontol. A Biol. Sci. Med. Sci. 2005, 60:549-555.
51. Qin J., Li R., Raes J., Arumugam M., Burgdorf K.S., Manichanh C., Nielsen T., Pons N., Levenez F., Yamada T., Mende D.R., Li J., Xu J., Li S., Li D., Cao J., Wang B., Liang H., Zheng H., Xie Y., Tap J., Lepage P., Bertalan M., Batto J.M., Hansen T., Le P.D., Linneberg A., Nielsen H.B., Pelletier E., Renault P., Sicheritz-Ponten T., Turner K., Zhu H., Yu C., Li S., Jian M., Zhou Y., Li Y., Zhang X., Li S., Qin N., Yang H., Wang J., Brunak S., Dore J., Guarner F., Kristiansen K., Pedersen O., Parkhill J., Weissenbach J., Bork P., Ehrlich S.D., Wang J. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65.
52. Rayner C.K., Horowitz M. Physiology of the ageing gut. Curr. Opin. Clin. Nutr. Metab. Care 2013, 16:33-38.
53. Rehman T. Role of the gut microbiota in age-related chronic inflammation. Endocr. Metab. Immune Disord. Drug Targets 2012, 12:361-367.
54. Reid G., Jass J., Sebulsky M.T., McCormick J.K. Potential uses of probiotics in clinical practice. Clin. Microbiol. Rev. 2003, 16:658-672.
55. Rennie M.J., Edwards R.H., Halliday D., Matthews D.E., Wolman S.L., Millward D.J. Muscle protein synthesis measured by stable isotope techniques in man: the effects of feeding and fasting. Clin. Sci. (Lond.) 1982, 63:519-523.
56. Rezzi S., Martin F.P., Alonso C., Guilarte M., Vicario M., Ramos L., Martinez C., Lobo B., Saperas E., Malagelada J.R., Santos J., Kochhar S. Metabotyping of biofluids reveals stress-based differences in gut permeability in healthy individuals. J. Proteome Res. 2009, 8:4799-4809.
57. Sacheck J.M., Ohtsuka A., McLary S.C., Goldberg A.L. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am. J. Physiol. Endocrinol. Metab. 2004, 287:E591-E601.
58. Schiaffino S., Dyar K.A., Ciciliot S., Blaauw B., Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 2013.
59. Sinclair D.A. Toward a unified theory of caloric restriction and longevity regulation. Mech. Ageing Dev. 2005, 126:987-1002.
60. Sommer F., Backhed F. The gut microbiota - masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11:227-238.
61. Swann J.R., Spagou K., Lewis M., Nicholson J.K., Glei D.A., Seeman T.E., Coe C.L., Goldman N., Ryff C.D., Weinstein M., Holmes E. Microbial-mammalian cometabolites dominate the age-associated urinary metabolic phenotype in Taiwanese and American populations. J. Proteome Res. 2013, 12:3166-3180.
62. Tiihonen K., Ouwehand A.C., Rautonen N. Human intestinal microbiota and healthy ageing. Ageing Res. Rev. 2010, 9:107-116.
63. Tremaroli V., Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature 2012, 489:242-249.
64. Ueki K., Yamamoto-Honda R., Kaburagi Y., Yamauchi T., Tobe K., Burgering B.M., Coffer P.J., Komuro I., Akanuma Y., Yazaki Y., Kadowaki T. Potential role of protein kinase B in insulin-induced glucose transport, glycogen synthesis, and protein synthesis. J. Biol. Chem. 1998, 273:5315-5322.
65. Vasikaran S.D., Morris H.A., Cooper C., Kanis J.A. Standardising biochemical assessment of bone turnover in osteoporosis. Clin. Biochem. 2011, 44:1033-1034.
66. Volpi E., Kobayashi H., Sheffield-Moore M., Mittendorfer B., Wolfe R.R. Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am. J. Clin. Nutr. 2003, 78:250-258.
67. Volpi E., Mittendorfer B., Wolf S.E., Wolfe R.R. Oral amino acids stimulate muscle protein anabolism in the elderly despite higher first-pass splanchnic extraction. Am. J. Physiol. 1999, 277:E513-E520.
68. Wall B.T., Hamer H.M., de L.A., Kiskini A., Groen B.B., Senden J.M., Gijsen A.P., Verdijk L.B., van Loon L.J. Leucine co-ingestion improves post-prandial muscle protein accretion in elderly men. Clin. Nutr. 2012.
69. Wang Y., Holmes E., Comelli E.M., Fotopoulos G., Dorta G., Tang H., Rantalainen M.J., Lindon J.C., Corthesy-Theulaz I.E., Fay L.B., Kochhar S., Nicholson J.K. Topographical variation in metabolic signatures of human gastrointestinal biopsies revealed by high-resolution magic-angle spinning (1)H NMR spectroscopy. J. Proteome Res. 2007, 6:3944-3951.
70. 1H NMR spectroscopy and multivariate data analysis. J. Proteome Res. 2005, 4:1324-1329.
71. Wenk M.R. The emerging field of lipidomics. Nat. Rev. Drug Discov. 2005, 4:594-610.
72. Winterkamp S., Weidenhiller M., Otte P., Stolper J., Schwab D., Hahn E.G., Raithel M. Urinary excretion of N-methylhistamine as a marker of disease activity in inflammatory bowel disease. Am. J. Gastroenterol. 2002, 97:3071-3077.
73. Yoshizawa F., Nagasawa T., Nishizawa N., Funabiki R. Protein synthesis and degradation change rapidly in response to food intake in muscle of food-deprived mice. J. Nutr. 1997, 127:1156-1159.
74. Yu Z., Zhai G., Singmann P., He Y., Xu T., Prehn C., Romisch-Margl W., Lattka E., Gieger C., Soranzo N., Heinrich J., Standl M., Thiering E., Mittelstrass K., Wichmann H.E., Peters A., Suhre K., Li Y., Adamski J., Spector T.D., Illig T., Wang-Sattler R. Human serum metabolic profiles are age dependent. Aging Cell 2012, 11:960-967.
75. Zhao J., Brault J.J., Schild A., Cao P., Sandri M., Schiaffino S., Lecker S.H., Goldberg A.L. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007, 6:472-483.