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Resistance wheel exercise from mid-life has minimal effect on sciatic nerves from old mice in which sarcopenia was prevented

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Abstract

The ability of resistance exercise, initiated from mid-life, to prevent age-related changes in old sciatic nerves, was investigated in male and female C57BL/6J mice. Aging is associated with cellular changes in old sciatic nerves and also loss of skeletal muscle mass and function (sarcopenia). Mature adult mice aged 15 months (M) were subjected to increasing voluntary resistance wheel exercise (RWE) over a period of 8 M until 23 M of age. This prevented sarcopenia in the old 23 M aged male and female mice. Nerves of control sedentary (SED) males at 3, 15 and 23 M of age, showed a decrease in the myelinated axon numbers at 15 and 23 M, a decreased g-ratio and a significantly increased proportion of myelinated nerves containing electron-dense aggregates at 23 M. Myelinated axon and nerve diameter, and axonal area, were increased at 15 M compared with 3 and 23 M. Exercise increased myelinated nerve profiles containing aggregates at 23 M. S100 protein, detected with immunoblotting was increased in sciatic nerves of 23 M old SED females, but not males, compared with 15 M, with no effect of exercise. Other neuronal proteins showed no significant alterations with age, gender or exercise. Overall the RWE had no cellular impact on the aging nerves, apart from an increased number of old nerves containing aggregates. Thus the relationship between cellular changes in aging nerves, and their sustained capacity for stimulation of old skeletal muscles to help maintain healthy muscle mass in response to exercise remains unclear.

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References

  • Aagaard P (2003) Training-induced changes in neural function. Exer Sport Sci Rev 31:61–67

    Article  Google Scholar 

  • Aagaard P, Suetta C, Caserotti P, Magnusson SP, Kjaer M (2010) Role of the nervous system in sarcopenia and muscle atrophy with aging: strength training as a countermeasure. Sca J Med Sci Sports 20:49–64

    Article  CAS  Google Scholar 

  • Aldridge GM, Podrebarac DM, Greenough WT, Weiler IJ (2008) The use of total protein stains as loading controls: an alternative to high-abundance single-protein controls in semi-quantitative immunoblotting. J Neurosci Methods 172:250–254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bamman MM, Clarke MS, Feeback DL, Talmadge RJ, Stevens BR, Lieberman SA, Greenisen MC (1998) Impact of resistance exercise during bed rest on skeletal muscle sarcopenia and myosin isoform distribution. J Appl Physiol 84:157–163

    CAS  PubMed  Google Scholar 

  • Barns M, Gondro C, Tellam RL, Radley-Crabb HG, Grounds MD, Shavlakadze T (2014) Molecular analyses provide insight into mechanisms underlying sarcopenia and myofibre denervation in old skeletal muscles of mice. Int J Biochem Cell Biol 53:174–185

    Article  CAS  PubMed  Google Scholar 

  • Berchtold NC, Chinn G, Chou M, Kesslak JP, Cotman CW (2005) Exercise primes a molecular memory for brain-derived neurotrophic factor protein induction in the rat hippocampus. Neuroscience 133:853–861

    Article  CAS  PubMed  Google Scholar 

  • Bjorkoy G et al (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603–614

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bowley MP, Cabral H, Rosene DL, Peters A (2010) Age changes in myelinated nerve fibers of the cingulate bundle and corpus callosum in the rhesus monkey. J Comp Neurol 518:3046–3064

    Article  PubMed  PubMed Central  Google Scholar 

  • Burton LA, Sumukadas D (2010) Optimal management of sarcopenia. Clin Int Aging 5:217–228

    CAS  Google Scholar 

  • Caldwell JH, Klevanski M, Saar M, Muller UC (2013) Roles of the amyloid precursor protein family in the peripheral nervous system. Mech Dev 130:433–446

    Article  CAS  PubMed  Google Scholar 

  • Ceballos D, Cuadras J, Verdu E, Navarro X (1999) Morphometric and ultrastructural changes with ageing in mouse peripheral nerve. J Anat 195(Pt 4):563–576

    Article  PubMed  PubMed Central  Google Scholar 

  • Cederholm T, Cruz-Jentoft AJ, Maggi S (2013) Sarcopenia and fragility fractures. Eur J Phys Rehab Med 49:111–117

    CAS  Google Scholar 

  • Chai RJ, Vukovic J, Dunlop S, Grounds MD, Shavlakadze T (2011) Striking denervation of neuromuscular junctions without lumbar motoneuron loss in geriatric mouse muscle PloS One 6:1–11

    Google Scholar 

  • Cheng A, Morsch M, Murata Y, Ghazanfari N, Reddel SW, Phillips WD (2013) Sequence of age-associated changes to the mouse neuromuscular junction and the protective effects of voluntary exercise. PLoS ONE 8:1–8

    Google Scholar 

  • Chomiak T, Hu B (2009) What is the optimal value of the g-ratio for myelinated fibers in the rat CNS? A theoretical approach. PloS One 4:e7754

    Article  PubMed  CAS  Google Scholar 

  • Cooper C et al (2013) Tools in the assessment of sarcopenia. Calc Tissue Int 93:201–210

    Article  CAS  Google Scholar 

  • Cruz-Jentoft AJ et al (2010) Sarcopenia: European consensus on definition and diagnosis: Report of the european working group on sarcopenia in older people. Age Ageing 39:412–423

    Article  PubMed  PubMed Central  Google Scholar 

  • Denison HJ, Cooper C, Sayer AA, Robinson SM (2015) Prevention and optimal management of sarcopenia: a review of combined exercise and nutrition interventions to improve muscle outcomes in older people. Clin Int Aging 10:859–869

    Google Scholar 

  • Eaton SL, Roche SL, Llavero Hurtado M, Oldknow KJ, Farquharson C, Gillingwater TH, Wishart TM (2013) Total protein analysis as a reliable loading control for quantitative fluorescent western blotting. PLoS ONE 8:1–9

    Google Scholar 

  • Edds MV Jr (1950) Hypertrophy of nerve fibers to functionally overloaded muscles. J Comp Neurol 93:259–275

    Article  PubMed  Google Scholar 

  • English AW, Schwartz G, Meador W, Sabatier MJ, Mulligan A (2007) Electrical stimulation promotes peripheral axon regeneration by enhanced neuronal neurotrophin signaling. Dev Neurobiol 67:158–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • English AW, Wilhelm JC, Sabatier MJ (2011) Enhancing recovery from peripheral nerve injury using treadmill training. Ann Anat 193:354–361

    Article  PubMed  PubMed Central  Google Scholar 

  • Francis P et al (2016) Twelve weeks’ progressive resistance training combined with protein supplementation beyond habitual intakes increases upper leg lean tissue mass, muscle strength and extended gait speed in healthy older women. Biogerontology. doi:10.1007/s10522-016-9671-7

    PubMed  Google Scholar 

  • Franklin RJ, Ffrench-Constant C (2008) Remyelination in the CNS: from biology to therapy Nat Rev Neurosc 9:839–855

    CAS  Google Scholar 

  • Frontera WR, Meredith CN, O’Reilly KP, Knuttgen HG, Evans WJ (1988) Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol 64:1038–1044

    CAS  PubMed  Google Scholar 

  • Gardiner P, Dai Y, Heckman CJ (2006) Effects of exercise training on alpha-motoneurons. J Appl Physiol 101:1228–1236

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Pinilla F, Ying Z, Roy RR, Molteni R, Edgerton VR (2002) Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 88:2187–2195

    Article  CAS  PubMed  Google Scholar 

  • Goncalves AF et al (2010) Gelsolin is required for macrophage recruitment during remyelination of the peripheral nervous system. Glia 58:706–715

    PubMed  Google Scholar 

  • Hairi NN et al (2010) Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: The concord health and ageing in men project. J Am Geriatr Soc 58:2055–2062

    Article  PubMed  Google Scholar 

  • He C et al (2012a) Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 481:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He C, Sumpter R Jr, Levine B (2012b) Exercise induces autophagy in peripheral tissues and in the brain. Autophagy 8:1548–1551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong M, Onyema N, Edeer AO, Olson V (2017) In community dwelling females age 65 or older, gait speed declines as kinesthetic awareness of the lower legs decreases. Adv Aging Res 6:1–13

    Article  Google Scholar 

  • Hunter GR, McCarthy JP, Bamman MM (2004) Effects of resistance training on older adults. Sports Med 34:329–348

    Article  PubMed  Google Scholar 

  • Ibebunjo C et al (2013) Genomic and proteomic profiling reveals reduced mitochondrial function and disruption of the neuromuscular junction driving rat sarcopenia. Mol Cell Biol 33:194–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson JR, Kirby TJ, Fry CS, Cooper RL, McCarthy JJ, Peterson CA, Dupont-Versteegden EE (2015) Reduced voluntary running performance is associated with impaired coordination as a result of muscle satellite cell depletion in adult mice. Skeletal Muscle 5:41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jacobs JM, Love S (1985) Qualitative and quantitative morphology of human sural nerve at different ages. Brain 108(Pt 4):897–924

    Article  PubMed  Google Scholar 

  • Janssen I (2010) Evolution of sarcopenia research. Appl Physiol Nutri Metab 35:707–712

    Article  Google Scholar 

  • Johnson GV, Stoothoff WH (2004) Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 117:5721–5729

    Article  CAS  PubMed  Google Scholar 

  • Jones KJ (1993) Gonadal steroids as promoting factors in axonal regeneration. Brain Res Bull 30:491–498

    Article  CAS  PubMed  Google Scholar 

  • Jones KJ (1994) Androgenic enhancement of motor neuron regeneration. Ann NY Acad Sci 743:141–161

    Article  CAS  PubMed  Google Scholar 

  • Jones KJ, Brown TJ, Damaser M (2001) Neuroprotective effects of gonadal steroids on regenerating peripheral motoneurons. Brain Res Brain Res Rev 37:372–382

    Article  CAS  PubMed  Google Scholar 

  • Kanda K, Hashizume K (1998) Effects of long-term physical exercise on age-related changes of spinal motoneurons and peripheral nerves in rats. Neuroscience Res 31:69–75

    Article  CAS  Google Scholar 

  • Karsenty G, Olson EN (2016) Bone and muscle endocrine functions: Unexpected paradigms of inter-organ communication. Cell 164:1248–1256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawamura Y, Okazaki H, O’Brien PC, Dych PJ (1977) Lumbar motoneurons of man: I) number and diameter histogram of alpha and gamma axons of ventral root. J Neuropathol Exp Neurol 36:853–860

    Article  CAS  PubMed  Google Scholar 

  • Ke Z, Yip SP, Li L, Zheng XX, Tong KY (2011) The effects of voluntary, involuntary, and forced exercises on brain-derived neurotrophic factor and motor function recovery: a rat brain ischemia model. PLoS ONE 6:e16643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Key B, Parker AW, Giorgi PP (1984) Endurance exercise does not modify nerve fibre morphology in the rat soleus nerve. Brain Res 297:137–144

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick LJ, Yablonka-Reuveni Z, Rosser BW (2010) Retention of Pax3 expression in satellite cells of muscle spindles. J Histochem Cytochem 58:317–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krishnan VS et al (2016) A neurogenic perspective of sarcopenia: Time course study of sciatic nerves from aging mice. J Neuropathol Exp Neurol 75:464–478

    Article  PubMed  Google Scholar 

  • Kukuljan S, Nowson CA, Sanders K, Daly RM (2009) Effects of resistance exercise and fortified milk on skeletal muscle mass, muscle size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial. J Appl Physiol 107:1864–1873

    Article  CAS  PubMed  Google Scholar 

  • Kwan P (2013) Sarcopenia: the gliogenic perspective. Mech Ageing Dev 134:349–355

    Article  CAS  PubMed  Google Scholar 

  • Kwon I, Lee Y, Cosio-Lima LM, Cho JY, Yeom DC (2015) Effects of long-term resistance exercise training on autophagy in rat skeletal muscle of chloroquine-induced sporadic inclusion body myositis. J Exerc Nutrition Biochem 19:225–234

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee JS, Auyeung TW, Kwok T, Lau EM, Leung PC, Woo J (2007) Associated factors and health impact of sarcopenia in older chinese men and women: a cross-sectional study. Gerontology 53:404–410

    Article  PubMed  Google Scholar 

  • Legerlotz K, Elliott B, Guillemin B, Smith HK (2008) Voluntary resistance running wheel activity pattern and skeletal muscle growth in rats. Exp Physiol 93:754–762

    Article  PubMed  Google Scholar 

  • Lexell J (1997) Evidence for nervous system degeneration with advancing age. J Nutri 127:1011S–1013S

    CAS  Google Scholar 

  • Li R, Shen Y (2013) An old method facing a new challenge: re-visiting housekeeping proteins as internal reference control for neuroscience research. Life Sci 92:747–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Lee Y, Thompson WJ (2011) Changes in aging mouse neuromuscular junctions are explained by degeneration and regeneration of muscle fiber segments at the synapse. J Neurosc 31:14910–14919

    Article  CAS  Google Scholar 

  • Lira VA et al (2013) Autophagy is required for exercise training-induced skeletal muscle adaptation and improvement of physical performance. FASEB J 27:4184–4193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Ward PJ, English AW (2014) The effects of exercise on synaptic stripping require androgen receptor signaling. PLoS ONE 9:e98633

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Macias M, Dwornik A, Ziemlinska E, Fehr S, Schachner M, Czarkowska-Bauch J, Skup M (2007) Locomotor exercise alters expression of pro-brain-derived neurotrophic factor, brain-derived neurotrophic factor and its receptor TrkB in the spinal cord of adult rats. Eur J Neurosc 25:2425–2444

    Article  Google Scholar 

  • McMahon CD et al (2014) Lifelong exercise and locally produced insulin-like growth factor-1 (IGF-1) have a modest influence on reducing age-related muscle wasting in mice. Sca J Med Sci Sports 24:423–435

    Article  Google Scholar 

  • Misgeld T, Burgess RW, Lewis RM, Cunningham JM, Lichtman JW, Sanes JR (2002) Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36:635–648

    Article  CAS  PubMed  Google Scholar 

  • Mizushima N, Yoshimori T (2007) How to interpret LC3 immunoblotting. Autophagy 3:542–545

    Article  CAS  PubMed  Google Scholar 

  • Molteni R, Zheng JQ, Ying Z, Gomez-Pinilla F, Twiss JL (2004) Voluntary exercise increases axonal regeneration from sensory neurons. Proc Natl Acad Sci 101:8473–8478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan JA, Corrigan F, Baune BT (2015) Effects of physical exercise on central nervous system functions: a review of brain region specific adaptations. J Mol Psychiatry 3:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Myeku N, Metcalfe MJ, Huang Q, Figueiredo-Pereira M (2011) Assessment of proteasome impairment and accumulation/aggregation of ubiquitinated proteins in neuronal cultures. Methods Mol Biol 793:273–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogura Y, Iemitsu M, Naito H, Kakigi R, Kakehashi C, Maeda S, Akema T (2011) Single bout of running exercise changes LC3-II expression in rat cardiac muscle. Biochem Biophys Res Commun 414:756–760

    Article  CAS  PubMed  Google Scholar 

  • Ohia-Nwoko O, Montazari S, Lau YS, Eriksen JL (2014) Long-term treadmill exercise attenuates tau pathology in P301S tau transgenic mice. Mol Neurodegen 9:54

    Article  Google Scholar 

  • Paigen B, Svenson KL, Von Smith R, Marion MA, Stearns T, Peters LL, Smith AL (2012) Physiological effects of housing density on C57BL/6 J mice over a 9-month period. J Anim Sci 90:5182–5192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pannerec A et al (2016) A robust neuromuscular system protects rat and human skeletal muscle from sarcopenia. Aging 8:712–729

    Article  PubMed  PubMed Central  Google Scholar 

  • Payne SC, Bartlett CA, Harvey AR, Dunlop SA, Fitzgerald M (2011) Chronic swelling and abnormal myelination during secondary degeneration after partial injury to a central nervous system tract. J Neurotrauma 28:1077–1088

    Article  PubMed  Google Scholar 

  • Payne SC, Bartlett CA, Harvey AR, Dunlop SA, Fitzgerald M (2012) Myelin sheath decompaction, axon swelling, and functional loss during chronic secondary degeneration in rat optic nerve. Invest Ophthalmol Vis Sci 53:6093–6101

    Article  CAS  PubMed  Google Scholar 

  • Rai M, Demontis F (2016) Systemic nutrient and stress signaling via myokines and myometabolites. Ann Rev Physiol 78:85–107

    Article  CAS  Google Scholar 

  • Robertson A, Day B, Pollock M, Collier P (1993) The neuropathy of elderly mice. Acta Neuropathol 86:163–171

    Article  CAS  PubMed  Google Scholar 

  • Rolland Y et al (2008) Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives. J Nutri 12:433–450

    CAS  Google Scholar 

  • Romero-Calvo I, Ocon B, Martinez-Moya P, Suarez MD, Zarzuelo A, Martinez-Augustin O, de Medina FS (2010) Reversible ponceau staining as a loading control alternative to actin in western blots. Anal Biochem 401:318–320

    Article  CAS  PubMed  Google Scholar 

  • Roy RR, Gilliam TB, Taylor JF, Heusner WW (1983) Activity-induced morphologic changes in rat soleus nerve. Exp Neurol 80:622–632

    Article  CAS  PubMed  Google Scholar 

  • Rushton WA (1951) A theory of the effects of fibre size in medullated nerve. J Physiol 115:101–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabatier MJ, Redmon N, Schwartz G, English AW (2008) Treadmill training promotes axon regeneration in injured peripheral nerves. Exp Neurol 211:489–493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samorajski T (1974) Age differences in the morphology of posterior tibial nerves of mice. J Comp Neurol 157:439–445

    Article  CAS  PubMed  Google Scholar 

  • Samorajski T, Rolsten C (1975) Nerve fiber hypertrophy in posterior tibial nerves of mice in response to voluntary running activity during aging. J Comp Neurol 159:553–558

    Article  CAS  PubMed  Google Scholar 

  • Samorajski T, Ordy JM, Keefe JR (1965) The fine structure of lipofuscin age pigment in the nervous system of aged mice. J Cell Biol 26:779–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sapp RM, Shill DD, Roth SM, Hagberg JM (2017) Circulating microRNAs in acute and chronic exercise: more than mere biomarkers. J Appl Physiol 122:702–717

    Article  PubMed  Google Scholar 

  • Sayer AA, Robinson SM, Patel HP, Shavlakadze T, Cooper C, Grounds MD (2013) New horizons in the pathogenesis, diagnosis and management of sarcopenia. Age Ageing 42:145–150

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma AK, Bajada S, Thomas PK (1980) Age changes in the tibial and plantar nerves of the rat. J Anat 130:417–428

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shavlakadze T, Soffe Z, Anwari T, Cozens G, Grounds MD (2013) Short-term feed deprivation rapidly induces the protein degradation pathway in skeletal muscles of young mice. J Nutri 143:403–409

    Article  CAS  Google Scholar 

  • Sheahan TD, Copits BA, Golden JP, Gereau RW (2015) Voluntary exercise training: analysis of mice in uninjured, inflammatory, and nerve-injured pain states. PLoS ONE 10:e0133191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sheard PW, Anderson RD (2012) Age-related loss of muscle fibres is highly variable amongst mouse skeletal muscles. Biogerontology 13:157–167

    Article  CAS  PubMed  Google Scholar 

  • Sleiman SF et al (2016) Exercise promotes the expression of brain derived neurotrophic factor (BDNF) through the action of the ketone body beta-hydroxybutyrate. Elife 5:e-15092

    Article  Google Scholar 

  • Salzer JL (2012) Axonal regulation of Schwann cell ensheathment and myelination. J Per Nerv Sys 3:14–19

    Article  Google Scholar 

  • Soffe Z, Radley-Crabb HG, McMahon C, Grounds MD, Shavlakadze T (2016) Effects of loaded voluntary wheel exercise on performance and muscle hypertrophy in young and old male C57Bl/6 J mice. Sca J Med Sci Sports 26:172–188

    Article  CAS  Google Scholar 

  • Suetterlin KJ, Sayer AA (2014) Proprioception: where are we now? A commentary on clinical assessment, changes across the life course, functional implications and future interventions. Age Ageing 43:313–318

    Article  PubMed  Google Scholar 

  • Tam BT, Siu PM (2014) Autophagic cellular responses to physical exercise in skeletal muscle. Sports Med 44:625–640

    Article  PubMed  Google Scholar 

  • Thomas PK, King RH, Sharma AK (1980) Changes with age in the peripheral nerves of the rat. An ultrastructural study Acta Neuropathol 52:1–6

    Article  CAS  PubMed  Google Scholar 

  • Tohgi H, Tsukagoshi H, Toyokura Y (1977) Quantitative changes with age in normal sural nerves. Acta Neuropathol 38:213–220

    Article  CAS  PubMed  Google Scholar 

  • Tohma H, Hepworth AR, Shavlakadze T, Grounds MD, Arthur PG (2011) Quantification of ceroid and lipofuscin in skeletal muscle. J Histochem Cytochem 59:769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomanek RJ, Tipton CM (1967) Influence of exercise and tenectomy on the morphology of a muscle nerve. Anat Rec 159:105–113

    Article  CAS  PubMed  Google Scholar 

  • Triolo D et al (2012) Vimentin regulates peripheral nerve myelination. Development 139:1359–1367

    CAS  PubMed  Google Scholar 

  • Udina E, Cobianchi S, Allodi I, Navarro X (2011) Effects of activity-dependent strategies on regeneration and plasticity after peripheral nerve injuries. Ann Anat 193:347–353

    Article  CAS  PubMed  Google Scholar 

  • Ugrenovic S, Jovanovic I, Vasovic L, Kundalic B, Cukuranovic R, Stefanovic V (2016) Morphometric analysis of the diameter and g-ratio of the myelinated nerve fibers of the human sciatic nerve during the aging process. Anat Sci Int 91:238–245

    Article  CAS  PubMed  Google Scholar 

  • Valdez G, Tapia JC, Kang H, Clemenson GD, 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 107:14862–14868

    Article  Google Scholar 

  • van Dellen A, Cordery PM, Spires TL, Blakemore C, Hannan AJ (2008) Wheel running from a juvenile age delays onset of specific motor deficits but does not alter protein aggregate density in a mouse model of Huntington’s disease. BMC Neurosci 9:34

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verdu E, Buti M, Navarro X (1996) Functional changes of the peripheral nervous system with aging in the mouse. Neurobiol Aging 17:73–77

    Article  CAS  PubMed  Google Scholar 

  • Vital A, Meissner WG, Canron MH, Martin-Negrier ML, Bezard E, Tison F, Vital C (2014) Intra-axonal protein aggregation in the peripheral nervous system. J Per Ner Sys 19:44–49

    Article  CAS  Google Scholar 

  • White JP, Gao S, Puppa MJ, Sato S, Welle SL, Carson JA (2013) Testosterone regulation of Akt/mTORC1/FoxO3a signaling in skeletal muscle. Mol Cell Endocrinol 365:174–186

    Article  CAS  PubMed  Google Scholar 

  • White Z, Terrill J, White RB, McMahon C, Sheard P, Grounds MD, Shavlakadze T (2016a) Voluntary resistance wheel exercise from mid-life prevents sarcopenia and increases markers of mitochondrial function and autophagy in muscles of old male and female C57BL/6 J mice. Skeletal Muscle 6:45

    Article  PubMed  PubMed Central  Google Scholar 

  • White Z, White RB, McMahon C, Grounds MD, Shavlakadze T (2016b) High mTORC1 signaling is maintained, while protein degradation pathways are perturbed in old murine skeletal muscles in the fasted state. Int J Biochem Cell Biol 78:10–21

    Article  CAS  PubMed  Google Scholar 

  • Wood K, Wilhelm JC, Sabatier MJ, Liu K, Gu J, English AW (2012) Sex differences in the effectiveness of treadmill training in enhancing axon regeneration in injured peripheral nerves. Dev Neurobiol 72:688–698

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan A, Rao MV, Veeranna Nixon RA (2012) Neurofilaments at a glance. J Cell Sci 125:3257–3263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zampieri S et al (2015) Lifelong physical exercise delays age-associated skeletal muscle decline. J Gerontol A Biol Sci Med Sci 70:163–173

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was made possible by funding from The University of Western Australia (UWA: for MDG), and an International Postgraduate Scholarship and a Postgraduate Scholarship for International Tuition Fees from UWA (for VSK). MF is supported by an NHMRC Career Development Fellowship. ZW was supported by a postgraduate research scholarships from UWA and the Centre for Cell Therapy and Regenerative Medicine Top-up Scholarship, School of Medicine and Pharmacology, UWA and Harry Perkins Institute of Medical Research, Perth, Western Australia. We thank Michael Archer for technical assistance with electron microscopy and the Australian Microscopy and Microanalysis Research Facility at the Centre for Microscopy, Characterization and Analysis, UWA. We also thank Professor John Papadimitriou (UWA) for his insightful comments regarding the precise location of the protein aggregates in the myelinated nerves.

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  1. School of Anatomy, Physiology and Human Biology, The University of Western Australia (UWA), Perth, WA, 6009, Australia

    Vidya S. Krishnan, Zoe White, Jessica R. Terrill, Stuart I. Hodgetts, Tea Shavlakadze, Alan R. Harvey & Miranda D. Grounds

  2. Centre for Cell Therapy and Regenerative Medicine, School of Medicine and Pharmacology, UWA and the Harry Perkins Institute of Medical Research, Perth, WA, 6009, Australia

    Zoe White

  3. School of Chemistry and Biochemistry, The University of Western Australia (UWA), Perth, WA, 6009, Australia

    Jessica R. Terrill

  4. Perron Institute for Neurological and Translational Science, Verdun Street, Nedlands, Perth, WA, 6009, Australia

    Stuart I. Hodgetts, Melinda Fitzgerald & Alan R. Harvey

  5. Experimental and Regenerative Neurosciences, School of Biological Sciences, The University of Western Australia (UWA), Perth, WA, 6009, Australia

    Melinda Fitzgerald

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Correspondence to Miranda D. Grounds.

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10522_2017_9714_MOESM1_ESM.tif

Supplementary Fig. 1: Schematic diagram providing an overview of the study design. Supplementary material 1 (TIFF 1541 kb)

10522_2017_9714_MOESM2_ESM.tif

Supplementary Fig. 2: High magnification (2000X and 8000X) images of aggregates in 23 M SED (A-D) and EXE (E–H) male sciatic nerves. Some of the aggregates (indicated by white arrows) appear to show continuity with the internal surface of myelin sheath (A, B, E, F) suggesting these are probably located within Schwann cell cytoplasm (SC), while some appear to be enclosed within the axoplasm (C), which can be hard to interpret. A shrinkage of axoplasm was observed in some axons (F) indicated by asterisk (*). Two different types of aggregates enclosed in a single axon were occasionally seen (G). Note the presence of double membrane (black arrows) separating an axon from an inclusion in (D, H) indicated by black arrows. Scale bar is 1 µm for A B, C, E, F, G and scale bar is 200 nm for D and H. Supplementary material 2 (TIFF 12094 kb)

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Krishnan, V.S., White, Z., Terrill, J.R. et al. Resistance wheel exercise from mid-life has minimal effect on sciatic nerves from old mice in which sarcopenia was prevented. Biogerontology 18, 769–790 (2017). https://doi.org/10.1007/s10522-017-9714-8

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  • DOI: https://doi.org/10.1007/s10522-017-9714-8

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