Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Translational Neuroscience

Editor-in-Chief: David, Olivier

IMPACT FACTOR 2018: 2.038

CiteScore 2018: 1.90

SCImago Journal Rank (SJR) 2018: 0.665
Source Normalized Impact per Paper (SNIP) 2018: 0.786

Open Access
See all formats and pricing
More options …

Identification of biological markers for better characterization of older subjects with physical frailty and sarcopenia

Bertrand Fougère
  • Gérontopôle, Centre Hospitalier Universitaire de Toulouse, Toulouse, France
  • Inserm UMR1027, Université de Toulouse III Paul Sabatier, Toulouse, France
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Bruno Vellas
  • Gérontopôle, Centre Hospitalier Universitaire de Toulouse, Toulouse, France
  • Inserm UMR1027, Université de Toulouse III Paul Sabatier, Toulouse, France
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Gabor Abellan van Kan
  • Gérontopôle, Centre Hospitalier Universitaire de Toulouse, Toulouse, France
  • Inserm UMR1027, Université de Toulouse III Paul Sabatier, Toulouse, France
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Matteo Cesari
  • Gérontopôle, Centre Hospitalier Universitaire de Toulouse, Toulouse, France
  • Inserm UMR1027, Université de Toulouse III Paul Sabatier, Toulouse, France
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2015-03-17 | DOI: https://doi.org/10.1515/tnsci-2015-0009


Population aging is rapidly accelerating worldwide; however, longer life expectancy is not the only public health goal. Indeed, extended lifetime involves maintaining function and the capacity of living independently. Sarcopenia and physical frailty are both highly relevant entities with regards to functionality and autonomy of older adults. The concepts and definitions of frailty and sarcopenia have largely been revised over the years. Sarcopenia is an age-related progressive and generalized loss of skeletal muscle mass and strength. On the other hand, frailty is a state of increased vulnerability to stressors, responsible for exposing the older person to enhanced risk of adverse outcomes. Physical frailty and sarcopenia substantially overlap and several adverse outcomes of frailty are likely mediated by sarcopenia. Indeed, the concepts of sarcopenia and physical frailty can be perceived as related to the same target organ (i.e., skeletal muscle) and it may be possible to combine them into a unique definition. The biological background of such a close relationship needs to be explored and clarified as it can potentially provide novel and pivotal insights for the assessment and treatment of these conditions in old age. The aim of this paper is to indicate and discuss possible biological markers to be considered in the framing of physical frailty and sarcopenia.

Keywords: Aging; Elderly; Biomarkers; Physical frailty; Sarcopenia; Skeletal muscle


  • [1] Cesari M., Landi F., Vellas B., Bernabei R., Marzetti E., Sarcopenia and physical frailty: two sides of the same coin, Front. Aging Neurosci., 2014, 6, 192 Google Scholar

  • [2] Wolfe R.R., The underappreciated role of muscle in health and disease, Am. J. Clin. Nutr., 2006, 84, 475-482 Google Scholar

  • [3] Tzankoff S.P., Norris A.H., Longitudinal changes in basal metabolism in man, J. Appl. Physiol., 1978, 45, 536-539 Google Scholar

  • [4] Butler R.N., Did you say “sarcopenia”?, Geriatrics, 1993, 48, 11-12 Google Scholar

  • [5] Cruz-Jentoft A.J., Baeyens J.P., Bauer J.M., Boirie Y., Cederholm T., Landi F., et al., Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People, Age Ageing, 2010, 39, 412-423 Google Scholar

  • [6] Evans W.J., What is sarcopenia?, J. Gerontol. A Biol. Sci. Med Sci., 1995, 50 (SI), 5-8 Google Scholar

  • [7] Evans W.J., Campbell W.W., Sarcopenia and age-related changes in body composition and functional capacity, J. Nutr., 1993, 123 (Suppl. 2), 465-468 Google Scholar

  • [8] Rosenberg I.H., Sarcopenia: origins and clinical relevance, J. Nutr., 1997, 127 (Suppl. 5), 990S- 991S Google Scholar

  • [9] Fielding R.A., Vellas B., Evans W.J., Bhasin S., Morley J.E., Newman A.B., et al., 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 CrossrefGoogle Scholar

  • [10] 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 Google Scholar

  • [11] Lexell J., Human aging, muscle mass, and fiber type composition, J. Gerontol. A Biol. Sci. Med. Sci., 1995, 50 (SI), 11-16 Google Scholar

  • [12] Janssen I., Heymsfield S.B., Ross R., Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability, J. Am. Geriatr. Soc., 2002, 50, 889-896 CrossrefGoogle Scholar

  • [13] Abellan van Kan G., Cameron Chumlea W., Gillette-Guyonet S., Houles M., Dupuy C., Rolland Y., et al., Clinical trials on sarcopenia: methodological issues regarding phase 3 trials, Clin. Geriatr. Med., 2011, 27, 471-482 CrossrefGoogle Scholar

  • [14] Fried L.P., Tangen C.M., Walston J., Newman A.B., Hirsch C., Gottdiener J., et al., Frailty in older adults: evidence for a phenotype, J. Gerontol. A Biol. Sci. Med. Sci., 2001, 56, M146-156 CrossrefGoogle Scholar

  • [15] Mitnitski A.B., Mogilner A.J., MacKnight C., Rockwood K., The mortality rate as a function of accumulated deficits in a frailty index, Mech. Ageing Dev., 2002, 123, 1457-1460 CrossrefGoogle Scholar

  • [16] Rockwood K., Andrew M., Mitnitski A., A comparison of two approaches to measuring frailty in elderly people, J. Gerontol. A Biol. Sci. Med. Sci., 2007, 62, 738-743 CrossrefGoogle Scholar

  • [17] Woo J., Leung J., Morley J.E., Comparison of frailty indicators based on clinical phenotype and the multiple deficit approach in predicting mortality and physical limitation, J. Am. Geriatr. Soc., 2012, 60, 1478-1486 CrossrefGoogle Scholar

  • [18] Abellan van Kan G., Rolland Y., Andrieu S., Bauer J., Beauchet O., Bonnefoy M., et al., Gait speed at usual pace as a predictor of adverse outcomes in community-dwelling older people an International Academy on Nutrition and Aging (IANA) Task Force, J. Nutr. Health Aging, 2009, 13, 881-889 CrossrefGoogle Scholar

  • [19] Daniels R., van Rossum E., de Witte L., Kempen G.I.J.M., van den Heuvel W., Interventions to prevent disability in frail community-dwelling elderly: a systematic review, BMC Health Serv. Res., 2008, 8, 278 CrossrefGoogle Scholar

  • [20] Ferrucci L., Guralnik J.M., Studenski S., Fried L.P., Cutler G.B., Walston J.D., et al., Designing randomized, controlled trials aimed at preventing or delaying functional decline and disability in frail, older persons: a consensus report, J. Am. Geriatr. Soc., 2004, 52, 625-634 CrossrefGoogle Scholar

  • [21] Biomarkers Definitions Working Group. Biomarkers and surrogate endpoints: preferred definitions and conceptual framework, Clin. Pharmacol. Ther., 2001, 69, 89-95 Google Scholar

  • [22] Krabbe K.S., Pedersen M., Bruunsgaard H., Inflammatory mediators in the elderly, Exp. Gerontol., 2004, 39, 687-699 Google Scholar

  • [23] Morley J.E., Baumgartner R.N., Cytokine-related aging process, J. Gerontol. A Biol. Sci. Med. Sci., 2004, 59, M924-929 CrossrefGoogle Scholar

  • [24] Ferrucci L., Corsi A., Lauretani F., Bandinelli S., Bartali B., Taub D.D., et al., The origins of age-related proinflammatory state, Blood, 2005, 105, 2294-2299 CrossrefGoogle Scholar

  • [25] Franceschi C., Campisi J., Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases, J. Gerontol. A Biol. Sci. Med. Sci., 2014, 69 (Suppl. 1), S4-9 CrossrefGoogle Scholar

  • [26] Schaap L.A., Pluijm S.M.F., Deeg D.J.H., Visser M., Inflammatory markers and loss of muscle mass (sarcopenia) and strength, Am. J. Med., 2006, 119, 526.e9-17 Google Scholar

  • [27] Schaap L.A., Pluijm S.M.F., Deeg D.J.H., Harris T.B., Kritchevsky S.B., Newman A.B., et al., Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength, J. Gerontol. A Biol. Sci. Med. Sci., 2009, 64, 1183-1189 Google Scholar

  • [28] Visser M., Pahor M., Taaffe D.R., Goodpaster B.H., Simonsick E.M., Newman A.B., et al. Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study, J. Gerontol. A Biol. Sci. Med. Sci., 2002, 57, M326-332 CrossrefGoogle Scholar

  • [29] Ferrucci L., Penninx B.W.J.H., Volpato S., Harris T.B., Bandeen-Roche K., Balfour J., et al., Change in muscle strength explains accelerated decline of physical function in older women with high interleukin-6 serum levels, J. Am. Geriatr. Soc., 2002, 50, 1947-1954 CrossrefGoogle Scholar

  • [30] Penninx B.W.J.H., Kritchevsky S.B., Newman A.B., Nicklas B.J., Simonsick E.M., Rubin S., et al., Inflammatory markers and incident mobility limitation in the elderly, J. Am. Geriatr. Soc., 2004, 52, 1105-1113 CrossrefGoogle Scholar

  • [31] Gianni P., Jan K.J., Douglas M.J., Stuart P.M., Tarnopolsky M.A., Oxidative stress and the mitochondrial theory of aging in human skeletal muscle, Exp. Gerontol., 2004, 39, 1391-1400 Google Scholar

  • [32] Lim P.-S., Cheng Y.-M., Wei Y.-H., Increase in oxidative damage to lipids and proteins in skeletal muscle of uremic patients, Free Radic. Res., 2002, 36, 295-301 Google Scholar

  • [33] Stadtman E.R., Protein oxidation and aging, Free Radic. Res., 2006, 40, 1250-1258 Google Scholar

  • [34] Fulle S., Protasi F., Di Tano G., Pietrangelo T., Beltramin A., Boncompagni S., et al., The contribution of reactive oxygen species to sarcopenia and muscle ageing, Exp. Gerontol., 2004, 39, 17-24 Google Scholar

  • [35] Howard C., Ferrucci L., Sun K., Fried L.P., Walston J., Varadhan R., et al., Oxidative protein damage is associated with poor grip strength among older women living in the community, J. Appl. Physiol., 2007, 103, 17-20 CrossrefGoogle Scholar

  • [36] Payne G.W., Effect of inflammation on the aging microcirculation: impact on skeletal muscle blood flow control, Microcirculation, 2006, 13, 343-352 CrossrefGoogle Scholar

  • [37] Dalal M., Ferrucci L., Sun K., Beck J., Fried L.P., Semba R.D., Elevated serum advanced glycation end products and poor grip strength in older community-dwelling women, J. Gerontol. A Biol. Sci. Med. Sci., 2009, 64, 132-137 CrossrefGoogle Scholar

  • [38] Wyss M., Kaddurah-Daouk R., Creatine and creatinine metabolism, Physiol. Rev., 2000, 80, 1107-1213 Google Scholar

  • [39] Larsen R.G., Callahan D.M., Foulis S.A., Kent-Braun J.A., Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behavior, Appl. Physiol. Nutr. Metab., 2012, 37, 88-99 CrossrefGoogle Scholar

  • [40] McCully K.K., Fielding R.A., Evans W.J., Leigh J.S., Posner J.D., Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles, J. Appl. Physiol., 1993, 75, 813-819 Google Scholar

  • [41] Möller P., Bergström J., Fürst P., Hellström K., Effect of aging on energy-rich phosphagens in human skeletal muscles, Clin. Sci., 1980, 58, 553-555 CrossrefGoogle Scholar

  • [42] Heymsfield S.B., Arteaga C., McManus C., Smith J., Moffitt S., Measurement of muscle mass in humans: validity of the 24-hour urinary creatinine method, Am. J. Clin. Nutr., 1983, 37, 478-494 Google Scholar

  • [43] Stimpson S.A., Turner S.M., Clifton L.G., Poole J.C., Mohammed H.A., Shearer T.W., et al., Total-body creatine pool size and skeletal muscle mass determination by creatine-(methyl-D3) dilution in rats, J. Appl. Physiol., 2012, 112, 1940-1948 CrossrefGoogle Scholar

  • [44] Bemben M.G., Witten M.S., Carter J.M., Eliot K.A., Knehans A.W., Bemben D.A., The effects of supplementation with creatine and protein on muscle strength following a traditional resistance training program in middle-aged and older men, J. Nutr. Health Aging, 2010, 14, 155-159 CrossrefGoogle Scholar

  • [45] Dalbo V.J., Roberts M.D., Lockwood C.M., Tucker P.S., Kreider R.B., Kerksick C.M., The effects of age on skeletal muscle and the phosphocreatine energy system: can creatine supplementation help older adults, Dyn. Med., 2009, 8, 6 Google Scholar

  • [46] Proctor D.N., Balagopal P., Nair K.S., Age-related sarcopenia in humans is associated with reduced synthetic rates of specific muscle proteins, J. Nutr., 1998, 128 (Suppl. 2), 351S-355S Google Scholar

  • [47] Greenlund L.J., Nair K.S., Sarcopenia - consequences, mechanisms, and potential therapies, Mech. Ageing Dev., 2003, 124, 287-299 CrossrefGoogle Scholar

  • [48] Sakuma K., Yamaguchi A., Sarcopenia and age-related endocrine function, Int. J. Endocrinol., 2012, 127362 Google Scholar

  • [49] Stewart C.E., Pell J.M., IGF is/is not the major physiological regulator of muscle mass. J. Appl. Physiol. 2010, 108, 1820-1821; discussion 1823-1824; author reply 1832 CrossrefGoogle Scholar

  • [50] Serra C., Tangherlini F., Rudy S., Lee D., Toraldo G., Sandor N.L., et al., Testosterone improves the regeneration of old and young mouse skeletal muscle, J. Gerontol. A Biol. Sci. Med. Sci., 2013, 68, 17-26 CrossrefGoogle Scholar

  • [51] Wagers A.J., Conboy I.M., Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis, Cell, 2005, 122, 659-667 CrossrefGoogle Scholar

  • [52] Dubois V., Laurent M., Boonen S., Vanderschueren D., Claessens F., Androgens and skeletal muscle: cellular and molecular action mechanisms underlying the anabolic actions, Cell. Mol. Life Sci., 2012, 69, 1651-1667 CrossrefGoogle Scholar

  • [53] Malkin C.J., Pugh P.J., Jones R.D., Kapoor D., Channer K.S., Jones T.H., The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men, J. Clin. Endocrinol. Metab., 2004, 89, 3313-3318 CrossrefGoogle Scholar

  • [54] Grossmann M., Low testosterone in men with type 2 diabetes: significance and treatment, J. Clin. Endocrinol. Metab., 2011, 96, 2341-2353 CrossrefGoogle Scholar

  • [55] Boland R., Role of vitamin D in skeletal muscle function, Endocr. Rev., 1986, 7, 434-448 Google Scholar

  • [56] Bischoff H.A., Borchers M., Gudat F., Duermueller U., Theiler R., Stähelin H.B., et al., In situ detection of 1,25-dihydroxyvitamin D3 receptor in human skeletal muscle tissue, Histochem. J., 2001, 33, 19-24 Google Scholar

  • [57] Zanello S.B., Collins E.D., Marinissen M.J., Norman A.W., Boland R.L., Vitamin D receptor expression in chicken muscle tissue and cultured myoblasts, Horm. Metab. Res., 1997, 29, 231-236 CrossrefGoogle Scholar

  • [58] Freedman L.P., Transcriptional targets of the vitamin D3 receptor-mediating cell cycle arrest and differentiation, J. Nutr., 1999, 129 (Suppl. 2), 581S-586S Google Scholar

  • [59] McCary L.C., Staun M., DeLuca H.F., A characterization of vitamin D-independent intestinal calcium absorption in the osteopetrotic (op/op) mouse, Arch. Biochem. Biophys., 1999, 15, 368, 249-256 Google Scholar

  • [60] Nader G.A., Esser K.A., Intracellular signaling specificity in skeletal muscle in response to different modes of exercise, J. Appl. Physiol., 2001, 90, 1936-1942 Google Scholar

  • [61] Doherty T.J., Invited review: aging and sarcopenia, J. Appl. Physiol., 2003, 95, 1717-1727 CrossrefGoogle Scholar

  • [62] Barzilay J.I., Blaum C., Moore T., Xue Q.L., Hirsch C.H., Walston J.D., et al., Insulin resistance and inflammation as precursors of frailty: the Cardiovascular Health Study, Arch. Intern. Med., 2007, 167, 635-641 CrossrefGoogle Scholar

  • [63] Trujillo M.E., Scherer P.E., Adipose tissue-derived factors: impact on health and disease, Endocr. Rev., 2006, 27, 762-768 Google Scholar

  • [64] Mulero J., Zafrilla P., Martinez-Cacha A., Oxidative stress, frailty and cognitive decline, J. Nutr. Health Aging, 2011, 15, 756-760 CrossrefGoogle Scholar

  • [65] Adachi J., Kumar C., Zhang Y., Olsen J.V., Mann M., The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins, Genome Biol., 2006, 7, R80 Google Scholar

  • [66] Kentsis A., Monigatti F., Dorff K., Campagne F., Bachur R., Steen H., Urine proteomics for profiling of human disease using high accuracy mass spectrometry, Proteomics Clin. Appl., 2009, 3, 1052-1061 CrossrefGoogle Scholar

  • [67] Li Q.-R., Fan K.-X., Li R.-X., Dai J., Wu C.-C., Zhao S.-L., et al., A comprehensive and non-prefractionation on the protein level approach for the human urinary proteome: touching phosphorylation in urine, Rapid Commun. Mass Spectrom., 2010, 24, 823-832 Google Scholar

  • [68] Marimuthu A., O’Meally R.N., Chaerkady R., Subbannayya Y., Nanjappa V., Kumar P., et al., A comprehensive map of the human urinary proteome, J. Proteome Res., 2011, 10, 2734-2743 CrossrefGoogle Scholar

  • [69] Nagaraj N., Mann M., Quantitative analysis of the intra- and inter-individual variability of the normal urinary proteome, J. Proteome Res., 2011, 10, 637-645 CrossrefGoogle Scholar

  • [70] Niemelä O., Radioimmunoassays for type III procollagen amino-terminal peptides in humans, Clin. Chem., 1985, 31, 1301-1304 Google Scholar

  • [71] Niemelä O., Risteli L., Parkkinen J., Risteli J., Purification and characterization of the N-terminal propeptide of human type III procollagen, Biochem. J., 1985, 232, 145-150 CrossrefGoogle Scholar

  • [72] Prockop D.J., Kivirikko K.I., Tuderman L., Guzman N.A., The biosynthesis of collagen and its disorders (first of two parts), N. Engl. J. Med., 1979, 301, 13-23 Google Scholar

  • [73] Danne T., Grüters A., Schuppan D., Quantas N., Enders I., Weber B., Relationship of procollagen type III propeptide-related antigens in serum to somatic growth in healthy children and patients with growth disorders, J. Pediatr., 1989, 114, 257-260 CrossrefGoogle Scholar

  • [74] Erotokritou-Mulligan I., Bassett E.E., Bartlett C., Cowan D., McHugh C., Seah R., et al., The effect of sports injury on insulin-like growth factor-I and type 3 procollagen: implications for detection of growth hormone abuse in athletes, J. Clin. Endocrinol. Metab., 2008, 93,2760-2763 Google Scholar

  • [75] Nelson A.E., Howe C.J., Nguyen T.V., Leung K.-C., Trout G.J., Seibel M.J., et al., Influence of demographic factors and sport type on growth hormone-responsive markers in elite athletes, J. Clin. Endocrinol. Metab., 2006, 91, 4424-4432 CrossrefGoogle Scholar

  • [76] Nguyen T.V., Nelson A.E., Howe C.J., Seibel M.J., Baxter R.C., Handelsman D.J., et al., Within-subject variability and analytic imprecision of insulinlike growth factor axis and collagen markers: implications for clinical diagnosis and doping tests, Clin. Chem., 2008, 54, 1268-1276 CrossrefGoogle Scholar

  • [77] Verde G.G., Santi I., Chiodini P., Cozzi R., Dallabonzana D., Oppizzi G., et al., Serum type III procollagen propeptide levels in acromegalic patients, J. Clin. Endocrinol. Metab., 1986, 63, 1406-1410 CrossrefGoogle Scholar

  • [78] Erotokritou-Mulligan I., Bassett E.E., Kniess A., Sönksen P.H., Holt R.I., Validation of the growth hormone (GH)-dependent marker method of detecting GH abuse in sport through the use of independent data sets, Growth Horm. IGF Res., 2007, 17, 416-423 CrossrefGoogle Scholar

  • [79] Garma T., Kobayashi C., Haddad F., Adams G.R., Bodell P.W., Baldwin K.M., Similar acute molecular responses to equivalent volumes of isometric, lengthening, or shortening mode resistance exercise, J. Appl. Physiol., 2007, 102, 135-143 Google Scholar

  • [80] Longobardi S., Keay N., Ehrnborg C., Cittadini A., Rosén T., Dall R., et al., Growth hormone (GH) effects on bone and collagen turnover in healthy adults and its potential as a marker of GH abuse in sports: a double blind, placebo-controlled study. The GH-2000 Study Group, J. Clin. Endocrinol. Metab., 2000, 85, 1505-1512 Google Scholar

  • [81] Nelson A.E., Meinhardt U., Hansen J.L., Walker I.H., Stone G., Howe C.J., et al., Pharmacodynamics of growth hormone abuse biomarkers and the influence of gender and testosterone: a randomized double-blind placebo-controlled study in young recreational athletes, J. Clin. Endocrinol. Metab., 2008, 93, 2213-2222 CrossrefGoogle Scholar

  • [82] Wallace J.D., Cuneo R.C., Lundberg P.A., Rosén T., Jørgensen J.O., Longobardi S., et al., Responses of markers of bone and collagen turnover to exercise, growth hormone (GH) administration, and GH withdrawal in trained adult males, J. Clin. Endocrinol. Metab., 2000, 85, 124-133 Google Scholar

  • [83] Erotokritou-Mulligan I., Bassett E.E., Cowan D.A., Bartlett C., McHugh C., Sönksen P.H., et al., Influence of ethnicity on IGF-I and procollagen III peptide (P-III-P) in elite athletes and its effect on the ability to detect GH abuse, Clin. Endocrinol., 2009, 70, 161-168 CrossrefGoogle Scholar

  • [84] McHugh C.M., Park R.T., Sönksen P.H., Holt R.I., Challenges in detecting the abuse of growth hormone in sport, Clin. Chem., 2005, 51, 1587-1593 CrossrefGoogle Scholar

  • [85] Powrie J.K., Bassett E.E., Rosén T., Jørgensen J.O., Napoli R., Saccà L., et al., Detection of growth hormone abuse in sport, Growth Horm. IGF Res., 2007, 17, 220-226 CrossrefGoogle Scholar

  • [86] Bhasin S., He E.J., Kawakubo M., Schroeder E.T., Yarasheski K., Opiteck G.J., et al., N-terminal propeptide of type III procollagen as a biomarker of anabolic response to recombinant human GH and testosterone, J. Clin. Endocrinol. Metab., 2009, 94, 4224-4233 CrossrefGoogle Scholar

  • [87] Langley B., Thomas M., Bishop A., Sharma M., Gilmour S., Kambadur R., Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J. Biol. Chem., 2002, 277, 49831-49840 Google Scholar

  • [88] McPherron A.C., Lawler A.M., Lee S.J., Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member, Nature, 1997, 387, 83-90 Google Scholar

  • [89] Thomas M., Langley B., Berry C., Sharma M., Kirk S., Bass J., et al., Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation, J. Biol. Chem., 2000, 275, 40235-40243 Google Scholar

  • [90] Zimmers T.A., Davies M.V., Koniaris L.G., Haynes P., Esquela A.F., Tomkinson K.N., et al., Induction of cachexia in mice by systemically administered myostatin, Science, 2002, 296, 1486-1488 CrossrefGoogle Scholar

  • [91] Léger B., Derave W., De Bock K., Hespel P., Russell A.P., Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation, Rejuvenation Res., 2008, 11, 163-175B Google Scholar

  • [92] Siriett V., Platt L., Salerno M.S., Ling N., Kambadur R., Sharma M., Prolonged absence of myostatin reduces sarcopenia, J. Cell. Physiol., 2006, 209, 866-873 Google Scholar

  • [93] Siriett V., Salerno M.S., Berry C., Nicholas G., Bower R., Kambadur R., et al., Antagonism of myostatin enhances muscle regeneration during sarcopenia, Mol. Ther., 2007, 15, 1463-1470 CrossrefGoogle Scholar

  • [94] Wagner K.R., Liu X., Chang X., Allen R.E., Muscle regeneration in the prolonged absence of myostatin, Proc. Natl. Acad. Sci. USA, 2005, 102, 2519-2524 CrossrefGoogle Scholar

  • [95] Bogdanovich S., Krag T.O.B., Barton E.R., Morris L.D., Whittemore L.-A., Ahima R.S., et al., Functional improvement of dystrophic muscle by myostatin blockade, Nature, 2002, 420, 418-421 CrossrefGoogle Scholar

  • [96] Whittemore L.-A., Song K., Li X., Aghajanian J., Davies M., Girgenrath S., et al., Inhibition of myostatin in adult mice increases skeletal muscle mass and strength, Biochem. Biophys. Res. Commun., 2003, 300, 965-971 Google Scholar

  • [97] Smith R.C., Lin B.K., Myostatin inhibitors as therapies for muscle wasting associated with cancer and other disorders, Curr. Opin. Support. Palliat. Care, 2013, 7, 352-360 CrossrefGoogle Scholar

  • [98] Wu H., Xiong W.C., Mei L., To build a synapse: signaling pathways in neuromuscular junction assembly, Development, 2010, 137, 1017-1033 Google Scholar

  • [99] Bolliger M.F., Zurlinden A., Lüscher D., Bütikofer L., Shakhova O., Francolini M., et al., Specific proteolytic cleavage of agrin regulates maturation of the neuromuscular junction, J. Cell Sci., 2010, 123, 3944-3955 CrossrefGoogle Scholar

  • [100] Frischknecht R., Fejtova A., Viesti M., Stephan A., Sonderegger P., Activity-induced synaptic capture and exocytosis of the neuronal serine protease neurotrypsin, J. Neurosci., 2008, 28, 1568-1579 CrossrefGoogle Scholar

  • [101] Stephan A., Mateos J.M., Kozlov S.V., Cinelli P., Kistler A.D., Hettwer S., et al., Neurotrypsin cleaves agrin locally at the synapse, FASEB J., 2008, 22, 1861-1873 CrossrefGoogle Scholar

  • [102] Bütikofer L., Zurlinden A., Bolliger M.F., Kunz B., Sonderegger P., Destabilization of the neuromuscular junction by proteolytic cleavage of agrin results in precocious sarcopenia, FASEB J., 2011, 25, 4378-4393 CrossrefGoogle Scholar

  • [103] LIFE Study Investigators, Pahor M., Blair S.N., Espeland M., Fielding R., Gill T.M., et al., Effects of a physical activity intervention on measures of physical performance: results of the lifestyle interventions and independence for Elders Pilot (LIFE-P) study, J. Gerontol. A Biol. Sci. Med. Sci., 2006, 61, 1157-1165 Google Scholar

  • Google Scholar

About the article

Received: 2015-01-07

Accepted: 2015-01-28

Published Online: 2015-03-17

Citation Information: Translational Neuroscience, Volume 6, Issue 1, ISSN (Online) 2081-6936, DOI: https://doi.org/10.1515/tnsci-2015-0009.

Export Citation

©2015 Bertrand Fougère et al.. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Jinjiao Wang, Cathy A. Maxwell, and Fang Yu
Biological Research For Nursing, 2018, Page 109980041879804
Barbara Gazolla de Macedo, Hanna Sette Câmara de Oliveira, Marielle Viotti de Paula, Gisele de Cássia Gomes, and Carlos Maurício de Figueiredo Antunes
Fisioterapia em Movimento, 2018, Volume 31, Number 0
Lourdes Vicent, Helena Martínez-Sellés, Albert Ariza-Solé, Alejandro Lucia, Enzo Emanuele, Antoni Bayés-Genís, Francisco Fernández-Avilés, and Manuel Martínez-Sellés
Maturitas, 2018
Ulrike Junius-Walker, Graziano Onder, Dagmar Soleymani, Birgitt Wiese, Olatz Albaina, Roberto Bernabei, and Emanuele Marzetti
European Journal of Internal Medicine, 2018
Maria Lorenzi, Stefano Bonassi, Teresa Lorenzi, Silvia Giovannini, Roberto Bernabei, and Graziano Onder
Biogerontology, 2018
B. Fougère and John E. Morley
The journal of nutrition, health & aging, 2017
Ifeanyi D. Nwachukwu, Trevor M. Kouritzin, Rotimi E. Aluko, and Semone B. Myrie
Journal of Food Biochemistry, 2017, Page e12435
Mathias Kristiansen, Afshin Samani, Pascal Madeleine, and Ernst A. Hansen
Journal of Strength and Conditioning Research, 2016, Volume 30, Number 7, Page 1948

Comments (0)

Please log in or register to comment.
Log in