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Age-related loss of muscle fibres is highly variable amongst mouse skeletal muscles

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Abstract

Sarcopenia is the age-related loss of skeletal muscle mass and strength, attributable in part to muscle fibre loss. We are currently unable to prevent fibre loss because we do not know what causes it. To provide a platform from which to better understand the causes of muscle fibre death we have quantified fibre loss in several muscles of aged C57Bl/6J mice. Comparison of muscle fibre numbers on dystrophin-immunostained transverse tissue sections at 6 months of age with those at 24 months shows a significant fibre loss in extensor digitorum longus and soleus, but not in sternomastoid or cleidomastoid muscles. The muscles of the elderly mice were mostly lighter than their younger counterparts, but fibres in the elderly muscles were of about the same cross-sectional area. This study shows that the contribution of fibre death to sarcopenia is highly variable and that there is no consistent pattern of age-related fibre loss between skeletal muscles.

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References

  • Allen DL, Monke SR, Talmadge RJ, Roy RR, Edgerton VR (1995) Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers. J Appl Physiol 78(5):1969–1976

    PubMed  CAS  Google Scholar 

  • Allen DL, Roy RR, Edgerton VR (1999) Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22(10):1350–1360

    Article  PubMed  CAS  Google Scholar 

  • Alnaqeeb MA, Goldspink G (1987) Changes in fibre type, number and diameter in developing and ageing skeletal muscle. J Anat 153:31–45

    PubMed  CAS  Google Scholar 

  • Alway SE, Siu PM (2008) Nuclear apoptosis contributes to sarcopenia. Exerc Sport Sci Rev 36(2):51–57

    Article  PubMed  Google Scholar 

  • Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147(8):755–763

    PubMed  CAS  Google Scholar 

  • Borisov AB, Carlson BM (2000) Cell death in denervated skeletal muscle is distinct from classical apoptosis. Anat Rec 258(3):305–318

    Article  PubMed  CAS  Google Scholar 

  • Brack AS, Bildsoe H, Hughes SM (2005) Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age-related muscle atrophy. J Cell Sci 118(Pt 20):4813–4821

    Article  PubMed  CAS  Google Scholar 

  • Brooks SV, Faulkner JA (1988) Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol 404:71–82

    PubMed  CAS  Google Scholar 

  • Brooks SV, Faulkner JA (1990) Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am J Physiol 258(3 Pt 1):C436–C442

    PubMed  CAS  Google Scholar 

  • Buford TW, Anton SD, Judge AR, Marzetti E, Wohlgemuth SE, Carter CS, Leeuwenburgh C, Pahor M, Manini TM (2010) Models of accelerated sarcopenia: critical pieces for solving the puzzle of age-related muscle atrophy. Age Res Rev 9(4):369–383

    Article  Google Scholar 

  • Campbell MJ, McComas AJ, Petito F (1973) Physiological changes in ageing muscles. J Neurol Neurosurg Psychiatry 36(2):174–182

    Article  PubMed  CAS  Google Scholar 

  • Carlson BM, Faulkner JA (1989) Muscle transplantation between young and old rats: age of host determines recovery. Am J Physiol 256(6 Pt 1):C1262–C1266

    PubMed  CAS  Google Scholar 

  • Carlson BM, Faulkner JA (1996) The regeneration of noninnervated muscle grafts and marcaine-treated muscles in young and old rats. J Gerontol A Biol Sci Med Sci 51(1):B43–B49

    Article  PubMed  CAS  Google Scholar 

  • Daw CK, Starnes JW, White TP (1988) Muscle atrophy and hypoplasia with aging: impact of training and food restriction. J Appl Physiol 64(6):2428–2432

    PubMed  CAS  Google Scholar 

  • Degens H (2007) Age-related skeletal muscle dysfunction: causes and mechanisms. J Musculoskelet Neuronal Interact 7(3):246–252

    PubMed  CAS  Google Scholar 

  • Degens H (2010) The role of systemic inflammation in age-related muscle weakness and wasting. Scand J Med Sci Sports 20(1):28–38

    Article  PubMed  CAS  Google Scholar 

  • Deschenes MR, Roby MA, Eason MK, Harris MB (2010) Remodeling of the neuromuscular junction precedes sarcopenia related alterations in myofibers. Exp Gerontol 45(5):389–393

    Article  PubMed  CAS  Google Scholar 

  • Dirks A, Leeuwenburgh C (2002) Apoptosis in skeletal muscle with aging. Am J Physiol Regul Integr Comp Physiol 282(2):R519–R527

    PubMed  CAS  Google Scholar 

  • Doherty TJ (2003) Invited review: aging and sarcopenia. J Appl Physiol 95(4):1717–1727

    PubMed  CAS  Google Scholar 

  • Dupont-Versteegden EE (2005) Apoptosis in muscle atrophy: relevance to sarcopenia. Exp Gerontol 40(6):473–481

    Article  PubMed  CAS  Google Scholar 

  • Dupont-Versteegden EE (2006) Apoptosis in skeletal muscle and its relevance to atrophy. World J Gastroenterol 12(46):7463–7466

    PubMed  CAS  Google Scholar 

  • Eddinger TJ, Moss RL, Cassens RG (1985) Fiber number and type composition in extensor digitorum longus, soleus, and diaphragm muscles with aging in Fisher 344 rats. J Histochem Cytochem 33(10):1033–1041

    Article  PubMed  CAS  Google Scholar 

  • Edstrom E, Altun M, Bergman E, Johnson H, Kullberg S, Ramirez-Leon V, Ulfhake B (2007) Factors contributing to neuromuscular impairment and sarcopenia during aging. Physiol Behav 92(1–2):129–135

    Article  PubMed  Google Scholar 

  • Eisenberg-Lerner A, Bialik S, Simon HU, Kimchi A (2009) Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 16(7):966–975

    Article  PubMed  CAS  Google Scholar 

  • Evans WJ (1995) What is sarcopenia? J Gerontol A Biol Sci Med Sci 50 Spec No:5–8

  • Faulkner JA, Brooks SV, Zerba E (1995) Muscle atrophy and weakness with aging: contraction-induced injury as an underlying mechanism. J Gerontol A Biol Sci Med Sci 50 Spec No:124–129

  • Faulkner JA, Larkin LM, Claflin DR, Brooks SV (2007) Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharm Physiol 34(11):1091–1096

    Article  CAS  Google Scholar 

  • Gaugler M, Brown A, Merrell E, DiSanto-Rose M, Rathmacher JA, Reynolds TH IV (2011) PKB signaling and atrogene expression in skeletal muscle of aged mice. J Appl Physiol 111(1):192–199

    Article  PubMed  CAS  Google Scholar 

  • Gundersen K, Bruusgaard JC (2008) Nuclear domains during muscle atrophy: nuclei lost or paradigm lost? J Physiol 586(Pt 11):2675–2681

    Article  PubMed  CAS  Google Scholar 

  • Hamrick MW, Ding KH, Pennington C, Chao YJ, Wu YD, Howard B, Immel D, Borlongan C, McNeil PL, Bollag WB, Curl WW, Yu J, Isales CM (2006) Age-related loss of muscle mass and bone strength in mice is associated with a decline in physical activity and serum leptin. Bone 39(4):845–853

    Article  PubMed  CAS  Google Scholar 

  • Harris AJ, Fitzsimons RB, McEwan JC (1989) Neural control of the sequence of expression of myosin heavy chain isoforms in foetal mammalian muscles. Development 107:751–769

    PubMed  CAS  Google Scholar 

  • Hennig R, Lomo T (1985) Firing patterns of motor units in normal rats. Nature 314:164–166

    Article  PubMed  CAS  Google Scholar 

  • Hooper AC (1981) Length, diameter and number of ageing skeletal muscle fibres. Gerontology 27(3):121–126

    Article  PubMed  CAS  Google Scholar 

  • Jang YC, Van Remmen H (2011) Age-associated alterations of the neuromuscular junction. Exp Gerontol 46(2–3):193–198

    Article  PubMed  CAS  Google Scholar 

  • Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol 89(1):81–88

    PubMed  CAS  Google Scholar 

  • Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R (2004) The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52(1):80–85

    Article  PubMed  Google Scholar 

  • Jones TE, Stephenson KW, King JG, Knight KR, Marshall TL, Scott WB (2009) Sarcopenia—mechanisms and treatments. J Geriatr Phys Ther 32(2):39–45

    Article  Google Scholar 

  • Karnovsky MJ, Roots L (1964) A “direct coloring” thiocholine method for cholinesterases. J Histochem Cytochem 12:219–221

    Article  PubMed  CAS  Google Scholar 

  • Kroemer G, Martin SJ (2005) Caspase-independent cell death. Nat Med 11(7):725–730

    Article  PubMed  Google Scholar 

  • Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB (2010) Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporosis Int 21(4):543–559

    Article  CAS  Google Scholar 

  • Lexell J (1995) Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 50 Spec No:11–16

  • Lexell J, Downham DY (1991) The occurrence of fibre-type grouping in healthy human muscle: a quantitative study of cross-sections of whole vastus lateralis from men between 15 and 83 years. Acta Neuropathol 81(4):377–381

    Article  PubMed  CAS  Google Scholar 

  • Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84(2–3):275–294

    Article  PubMed  CAS  Google Scholar 

  • Lionikas A, Blizard DA, Vandenbergh DJ, Stout JT, Vogler GP, McClearn GE, Larsson L (2006) Genetic determinants of weight of fast- and slow-twitch skeletal muscles in old mice. Mamm Genome 17(6):615–628

    Article  PubMed  Google Scholar 

  • Luff AR (1998) Age-associated changes in the innervation of muscle fibers and changes in the mechanical properties of motor units. Ann NY Acad Sci 854:92–101

    Article  PubMed  CAS  Google Scholar 

  • Lynch NA, Metter EJ, Lindle RS, Fozard JL, Tobin JD, Roy TA, Fleg JL, Hurley BF (1999) Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol 86(1):188–194

    PubMed  CAS  Google Scholar 

  • Marcell TJ (2003) Sarcopenia: causes, consequences, and preventions. J Gerontol A Biol Sci Med Sci 58(10):M911–M916

    Article  PubMed  Google Scholar 

  • Marzetti E, Leeuwenburgh C (2006) Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp Gerontol 41(12):1234–1238

    Article  PubMed  CAS  Google Scholar 

  • Marzetti E, Hwang JC, Lees HA, Wohlgemuth SE, Dupont-Versteegden EE, Carter CS, Bernabei R, Leeuwenburgh C (2010) Mitochondrial death effectors: relevance to sarcopenia and disuse muscle atrophy. Biochim Biophysica Acta 1800(3):235–244

    Article  CAS  Google Scholar 

  • Reynolds TH IV, Krajewski KM, Larkin LM, Reid P, Halter JB, Supiano MA, Dengel DR (2002) Effect of age on skeletal muscle proteolysis in extensor digitorum longus muscles of B6C3F1 mice. J Gerontol A Biol Sci Med Sci 57(5):B198–B201

    Article  PubMed  Google Scholar 

  • Rowe RW (1969) The effect of senility on skeletal muscles in the mouse. Exp Gerontol 4(2):119–126

    Article  PubMed  CAS  Google Scholar 

  • Rowlatt C, Chesterman FC, Sheriff MU (1976) Lifespan, age changes and tumour incidence in an ageing C57BL mouse colony. Lab Anim 10(10):419–442

    Article  PubMed  CAS  Google Scholar 

  • Shavlakadze T, McGeachie J, Grounds MD (2010) Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice. Biogerontology 11(3):363–376

    Article  PubMed  Google Scholar 

  • Trachtenberg JT (1998) Fiber apoptosis in developing rat muscles is regulated by activity, neuregulin. Dev Biol 196(2):193–203

    Article  PubMed  CAS  Google Scholar 

  • Valdez G, Tapia JC, Kang H, Clemenson GD Jr, Gage FH, Lichtman JW, Sanes JR (2010) Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc Natl Acad Sci 107(33):14863–14868

    Article  PubMed  CAS  Google Scholar 

  • Wohlgemuth SE, Seo AY, Marzetti E, Lees HA, Leeuwenburgh C (2010) Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Exp Gerontol 45(2):138–148

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Melanie Hutchison and Christopher Simon for their help with the immunohistochemistry and the muscle fibre counting. This work was supported by grants from the Dean of the Otago School of Medical Sciences and the Department of Physiology at the University of Otago. RA was the grateful recipient of a University of Otago Summer Research Scholarship.

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  1. Department of Physiology, University of Otago, P. O. Box 913, Dunedin, New Zealand

    Philip W. Sheard & Ross D. Anderson

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  1. Philip W. Sheard
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Correspondence to Philip W. Sheard.

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Sheard, P.W., Anderson, R.D. Age-related loss of muscle fibres is highly variable amongst mouse skeletal muscles. Biogerontology 13, 157–167 (2012). https://doi.org/10.1007/s10522-011-9365-0

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