Exercise-mediated reinnervation of skeletal muscle in elderly people: An update

Published: 28 February 2022
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Sarcopenia is defined by the loss of muscle mass and function. In aging sarcopenia is due to mild chronic inflammation but also to fiber-intrinsic defects, such as mitochondrial dysfunction. Age-related sarcopenia is associated with physical disability and lowered quality of life. In addition to skeletal muscle, the nervous tissue is also affected in elderly people. With aging, type 2 fast fibers preferentially undergo denervation and are reinnervated by slow-twitch motor neurons. They spread forming new neuro-muscular junctions with the denervated fibers: the result is an increased proportion of slow fibers that group together since they are associated in the same motor unit. Grouping and fiber type shifting are indeed major histological features of aging skeletal muscle. Exercise has been proposed as an intervention for age-related sarcopenia due to its numerous beneficial effects on muscle mechanical and biochemical features. In 2013, a precursor study in humans was published in the European Journal of Translation Myology (formerly known as Basic and Applied Myology), highlighting the occurrence of reinnervation in the musculature of aged, exercise-trained individuals as compared to the matching control. This paper, entitled «Reinnervation of Vastus lateralis is increased significantly in seniors (70-years old) with a lifelong history of high-level exercise», is now being reprinted for the second issue of the «Ejtm Seminal Paper Series». In this short review we discuss those results in the light of the most recent advances confirming the occurrence of exercise-mediated reinnervation, ultimately preserving muscle structure and function in elderly people who exercise.

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Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M; European Working Group on Sarcopenia in Older People. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010 Jul;39(4):412-23. Epub 2010 Apr 13. DOI: https://doi.org/10.1093/ageing/afq034
Berardi E, Madaro L, Lozanoska-Ochser B, Adamo S, Thorrez L, Bouche M, Coletti D. A Pound of Flesh: What Cachexia Is and What It Is Not. Diagnostics (Basel). 2021 Jan 12;11(1):116. DOI: https://doi.org/10.3390/diagnostics11010116
Larsson L, Degens H, Li M, Salviati L, Lee YI, Thompson W, Kirkland JL, Sandri M. Sarcopenia: Aging-Related Loss of Muscle Mass and Function. Physiol Rev. 2019 Jan 1;99(1):427-511. DOI: https://doi.org/10.1152/physrev.00061.2017
Dodds RM, Roberts HC, Cooper C, Sayer AA. The Epidemiology of Sarcopenia. J Clin Densitom. 2015 Oct-Dec;18(4):461-6. Epub 2015 Jun 12. DOI: https://doi.org/10.1016/j.jocd.2015.04.012
Mosole S, Rossini K, Kern H, Löfler S, Simone Fruhmann H, Vogelauer M, Burggraf S, Grim-Stieger M, Cvečka J, Hamar D, Sedliak M, Šarabon N, Pond A, Biral D, Carraro U, Zampieri S. Reinnervation of Vastus lateralis is increased significantly in seniors (70-years old) with a lifelong history of high-level exercise. Eur J Transl Myol Basic Appl Myol. 2013;23 (4):205–10. DOI: https://doi.org/10.4081/bam.2013.4.205
Power GA, Dalton BH, Gilmore KJ, Allen MD, Doherty TJ, Rice CL. Maintaining Motor Units into Old Age: Running the Final Common Pathway. Eur J Transl Myol. 2017 Mar 24;27(1):6597. DOI: https://doi.org/10.4081/ejtm.2017.6597
Zampieri S, Mosole S, Löfler S, Fruhmann H, Burggraf S, Cvečka J, Hamar D, Sedliak M, Tirptakova V, Šarabon N, Mayr W, Kern H. Physical Exercise in Aging: Nine Weeks of Leg Press or Electrical Stimulation Training in 70 Years Old Sedentary Elderly People. Eur J Transl Myol. 2015 Aug 25;25(4):237-42. DOI: https://doi.org/10.4081/ejtm.2015.5374
Mosole S, Carraro U, Kern H, Loefler S, Zampieri S. Use it or Lose It: Tonic Activity of Slow Motoneurons Promotes Their Survival and Preferentially Increases Slow Fiber-Type Groupings in Muscles of Old Lifelong Recreational Sportsmen. Eur J Transl Myol. 2016 Nov 25;26(4):5972. eCollection 2016 Sep 15. DOI: https://doi.org/10.4081/ejtm.2016.5972
Galloza J, Castillo B, Micheo W. Benefits of Exercise in the Older Population. Phys Med Rehabil Clin N Am. 2017 Nov;28(4):659-669. DOI: https://doi.org/10.1016/j.pmr.2017.06.001
Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev. 2011 Oct;91(4):1447-531. DOI: https://doi.org/10.1152/physrev.00031.2010
Larsson L, Edström L, Lindegren B, Gorza L, Schiaffino S. MHC composition and enzyme-histochemical and physiological properties of a novel fast-twitch motor unit type. Am J Physiol. 1991 Jul;261(1 Pt 1):C93-101. DOI: https://doi.org/10.1152/ajpcell.1991.261.1.C93
Esser K, Gunning P, Hardeman E. Nerve-dependent and -independent patterns of mRNA expression in regenerating skeletal muscle. Dev Biol. 1993 Sep;159(1):173-83. DOI: https://doi.org/10.1006/dbio.1993.1231
Coletti D, Daou N, Hassani M, Li Z, Parlakian A. Serum Response Factor in Muscle Tissues: From Development to Ageing. Eur J Transl Myol. 2016 Jun 22;26(2):6008. DOI: https://doi.org/10.4081/ejtm.2016.6008
Coletti D, Teodori L, Lin Z, Beranudin JF, Adamo S. Restoration versus reconstruction: cellular mechanisms of skin, nerve and muscle regeneration compared. Regen Med Res. 2013 Oct 1;1(1):4. DOI: https://doi.org/10.1186/2050-490X-1-4
Daou N, Hassani M, Matos E, De Castro GS, Costa RGF, Seelaender M, Moresi V, Rocchi M, Adamo S, Li Z, Agbulut O, Coletti D. Displaced Myonuclei in Cancer Cachexia Suggest Altered Innervation. Int J Mol Sci. 2020 Feb 6;21(3):1092. DOI: https://doi.org/10.3390/ijms21031092
Grifone R, Saquet A, Desgres M, Sangiorgi C, Gargano C, Li Z, Coletti D, Shi DL. Rbm24 displays dynamic functions required for myogenic differentiation during muscle regeneration. Sci Rep. 2021 May 3;11(1):9423. DOI: https://doi.org/10.1038/s41598-021-88563-3
Mazzotti AL, Coletti D. The Need for a Consensus on the Locution "Central Nuclei" in Striated Muscle Myopathies. Front Physiol. 2016 Nov 23;7:577. DOI: https://doi.org/10.3389/fphys.2016.00577
Blaauw B, Schiaffino S, Reggiani C. Mechanisms modulating skeletal muscle phenotype. Compr Physiol. 2013 Oct;3(4):1645-87. DOI: https://doi.org/10.1002/cphy.c130009
Punkt K, Krug H, Huse J, Punkt J. Age-dependent changes of enzyme activities in the different fibre types of rat extensor digitorum longus and gastrocnemius muscles. Acta Histochem. 1993 Sep;95(1):97-110. DOI: https://doi.org/10.1016/S0065-1281(11)80395-8
Marcucci L, Reggiani C. Increase of resting muscle stiffness, a less considered component of age-related skeletal muscle impairment. Eur J Transl Myol. 2020 Jun 17;30(2):8982. DOI: https://doi.org/10.4081/ejtm.2020.8982
Wilkinson DJ, Piasecki M, Atherton PJ. The age-related loss of skeletal muscle mass and function: Measurement and physiology of muscle fibre atrophy and muscle fibre loss in humans. Ageing Res Rev. 2018 Nov;47:123-132. Epub 2018 Jul 23. DOI: https://doi.org/10.1016/j.arr.2018.07.005
Klein CS, Marsh GD, Petrella RJ, Rice CL. Muscle fiber number in the biceps brachii muscle of young and old men. Muscle Nerve. 2003 Jul;28(1):62-8. DOI: https://doi.org/10.1002/mus.10386
Nilwik R, Snijders T, Leenders M, Groen BB, van Kranenburg J, Verdijk LB, van Loon LJ. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol. 2013 May;48(5):492-8. Epub 2013 Feb 17. DOI: https://doi.org/10.1016/j.exger.2013.02.012
Messa GAM, Piasecki M, Rittweger J, McPhee JS, Koltai E, Radak Z, Simunic B, Heinonen A, Suominen H, Korhonen MT, Degens H. Absence of an aging-related increase in fiber type grouping in athletes and non-athletes. Scand J Med Sci Sports. 2020 Nov;30(11):2057-2069. Epub 2020 Aug 28. DOI: https://doi.org/10.1111/sms.13778
Kelly NA, Hammond KG, Stec MJ, Bickel CS, Windham ST, Tuggle SC, Bamman MM. Quantification and characterization of grouped type I myofibers in human aging. Muscle Nerve. 2018 Jan;57(1):E52-E59. Epub 2017 Sep 7. DOI: https://doi.org/10.1002/mus.25711
Jerkovic R, Argentini C, Serrano-Sanchez A, Cordonnier C, Schiaffino S. Early myosin switching induced by nerve activity in regenerating slow skeletal muscle. Cell Struct Funct. 1997 Feb;22(1):147-53. DOI: https://doi.org/10.1247/csf.22.147
Murgia M, Serrano AL, Calabria E, Pallafacchina G, Lomo T, Schiaffino S. Ras is involved in nerve-activity-dependent regulation of muscle genes. Nat Cell Biol. 2000 Mar;2(3):142-7. DOI: https://doi.org/10.1038/35004013
Larsson L, Ansved T. Effects of ageing on the motor unit. Prog Neurobiol. 1995 Apr;45(5):397-458. DOI: https://doi.org/10.1016/0301-0082(95)98601-Z
Piasecki M, Ireland A, Jones DA, McPhee JS. Age-dependent motor unit remodelling in human limb muscles. Biogerontology. 2016 Jun;17(3):485-96. Epub 2015 Dec 14. DOI: https://doi.org/10.1007/s10522-015-9627-3
Demontis F, Piccirillo R, Goldberg AL, Perrimon N. Mechanisms of skeletal muscle aging: insights from Drosophila and mammalian models. Dis Model Mech. 2013 Nov;6(6):1339-52. Epub 2013 Oct 2. DOI: https://doi.org/10.1242/dmm.012559
Naro F, De Arcangelis V, Coletti D, Molinaro M, Zani B, Vassanelli S, Reggiani C, Teti A, Adamo S. Increase in cytosolic Ca2+ induced by elevation of extracellular Ca2+ in skeletal myogenic cells. Am J Physiol Cell Physiol. 2003 Apr;284(4):C969-76. Epub 2002 Dec 18. DOI: https://doi.org/10.1152/ajpcell.00237.2002
De Arcangelis V, Coletti D, Canato M, Molinaro M, Adamo S, Reggiani C, Naro F. Hypertrophy and transcriptional regulation induced in myogenic cell line L6-C5 by an increase of extracellular calcium. J Cell Physiol. 2005 Mar;202(3):787-95. DOI: https://doi.org/10.1002/jcp.20174
Lamboley CR, Wyckelsma VL, McKenna MJ, Murphy RM, Lamb GD. Ca(2+) leakage out of the sarcoplasmic reticulum is increased in type I skeletal muscle fibres in aged humans. J Physiol. 2016 Jan 15;594(2):469-81. Epub 2015 Dec 14. DOI: https://doi.org/10.1113/JP271382
Westerterp KR. Daily physical activity and ageing. Curr Opin Clin Nutr Metab Care. 2000 Nov;3(6):485-8. DOI: https://doi.org/10.1097/00075197-200011000-00011
Meijer EP, Westerterp KR, Verstappen FT. Effect of exercise training on physical activity and substrate utilization in the elderly. Int J Sports Med. 2000 Oct;21(7):499-504. DOI: https://doi.org/10.1055/s-2000-7419
Mosole S, Carraro U, Kern H, Loefler S, Fruhmann H, Vogelauer M, Burggraf S, Mayr W, Krenn M, Paternostro-Sluga T, Hamar D, Cvecka J, Sedliak M, Tirpakova V, Sarabon N, Musarò A, Sandri M, Protasi F, Nori A, Pond A, Zampieri S. Long-term high-level exercise promotes muscle reinnervation with age. J Neuropathol Exp Neurol. 2014 Apr;73(4):284-94. DOI: https://doi.org/10.1097/NEN.0000000000000032
Drey M, Sieber CC, Degens H, McPhee J, Korhonen MT, Müller K, Ganse B, Rittweger J. Relation between muscle mass, motor units and type of training in master athletes. Clin Physiol Funct Imaging. 2016 Jan;36(1):70-6. Epub 2014 Oct 24. DOI: https://doi.org/10.1111/cpf.12195
Bechshøft RL, Malmgaard-Clausen NM, Gliese B, Beyer N, Mackey AL, Andersen JL, Kjær M, Holm L. Improved skeletal muscle mass and strength after heavy strength training in very old individuals. Exp Gerontol. 2017 Jun;92:96-105. Epub 2017 Mar 28. DOI: https://doi.org/10.1016/j.exger.2017.03.014
Batsis JA, Villareal DT. Sarcopenic obesity in older adults: aetiology, epidemiology and treatment strategies. Nat Rev Endocrinol. 2018 Sep;14 (9):513-537. DOI: https://doi.org/10.1038/s41574-018-0062-9
Messi ML, Li T, Wang ZM, Marsh AP, Nicklas B, Delbono O. Resistance Training Enhances Skeletal Muscle Innervation Without Modifying the Number of Satellite Cells or their Myofiber Association in Obese Older Adults. J Gerontol A Biol Sci Med Sci. 2016 Oct;71(10):1273-80. Epub 2015 Oct 7. DOI: https://doi.org/10.1093/gerona/glv176
Kletzien H, Russell JA, Connor NP. The effects of treadmill running on aging laryngeal muscle structure. Laryngoscope. 2016 Mar;126(3):672-7. Epub 2015 Aug 8. DOI: https://doi.org/10.1002/lary.25520
Bathgate KE, Bagley JR, Jo E, Talmadge RJ, Tobias IS, Brown LE, Coburn JW, Arevalo JA, Segal NL, Galpin AJ. Muscle health and performance in monozygotic twins with 30 years of discordant exercise habits. Eur J Appl Physiol. 2018 Oct;118(10):2097-2110. Epub 2018 Jul 14. DOI: https://doi.org/10.1007/s00421-018-3943-7
Carraro U, Kern H, Gava P, Hofer C, Loefler S, Gargiulo P, Mosole S, Zampieri S, Gobbo V, Ravara B, Piccione F, Marcante A, Baba A, Schils S, Pond A, Gava F. Biology of Muscle Atrophy and of its Recovery by FES in Aging and Mobility Impairments: Roots and By-Products. Eur J Transl Myol. 2015 Aug 25;25(4):221-30. DOI: https://doi.org/10.4081/ejtm.2015.5272
Carraro U, Kern H, Gava P, Hofer C, Loefler S, Gargiulo P, Edmunds K, Árnadóttir ÍD, Zampieri S, Ravara B, Gava F, Nori A, Gobbo V, Masiero S, Marcante A, Baba A, Piccione F, Schils S, Pond A, Mosole S. Recovery from muscle weakness by exercise and FES: lessons from Masters, active or sedentary seniors and SCI patients. Aging Clin Exp Res. 2017 Aug;29(4):579-590. ep 3. DOI: https://doi.org/10.1007/s40520-016-0619-1
Carraro U, Coletti D, Kern H. The Ejtm Specials "The Long-Term Denervated Muscle". Eur J Transl Myol. 2014 Mar 27;24(1):3292. DOI: https://doi.org/10.4081/bam.2014.1.3
Kern H, Hofer C, Loefler S, Zampieri S, Gargiulo P, Baba A, Marcante A, Piccione F, Pond A, Carraro U. Atrophy, ultra-structural disorders, severe atrophy and degeneration of denervated human muscle in SCI and Aging. Implications for their recovery by Functional Electrical Stimulation, updated 2017. Neurol Res. 2017 Jul;39(7):660-666. Epub 2017 Apr 13. DOI: https://doi.org/10.1080/01616412.2017.1314906
Kern H, Hofer C, Loefler S, Zampieri S, Gargiulo P, Baba A, Marcante A, Piccione F, Pond A, Carraro U. Atrophy, ultra-structural disorders, severe atrophy and degeneration of denervated human muscle in SCI and Aging. Implications for their recovery by Functional Electrical Stimulation, updated 2017. Neurol Res. 2017 Jul;39(7):660-666. d Epub 2017 Apr 13. DOI: https://doi.org/10.1080/01616412.2017.1314906
Wang P, Li Y, Zhang Z, Lin Y, Jiang Z, Ding X, Yang L. Effects of functional electrical stimulation on neuromuscular function after targeted muscle reinnervation surgery in rats. Annu Int Conf IEEE Eng Med Biol Soc. 2020 Jul;2020:3823-3826. DOI: https://doi.org/10.1109/EMBC44109.2020.9175836
Mense S. Muscle Nociceptors, Neurochemistry. In: Gebhart GF, Schmidt RF, editors. Encyclopedia of Pain. Berlin, Heidelberg: Springer Berlin Heidelberg; 2013. p. 1944–50. DOI: https://doi.org/10.1007/978-3-642-28753-4_2529
Giuriati W, Ravara B, Porzionato A, Albertin G, Stecco C, Macchi V, De Caro R, Martinello T, Gomiero C, Patruno M, Coletti D, Zampieri S, Nori A. Muscle spindles of the rat sternomastoid muscle. Eur J Transl Myol. 2018 Dec 13;28(4):7904. DOI: https://doi.org/10.4081/ejtm.2018.7904
Ravara B, Gobbo V, Incendi D, Porzionato A, Macchi V, Caro R, Coletti D, Martinello T, Patruno M. Revisiting the peculiar regional distribution of muscle fiber types in rat Sternomastoid Muscle. Eur J Transl Myol. 2018 Mar 1;28(1):7302. DOI: https://doi.org/10.4081/ejtm.2018.7302
Konrad HR, Girardi M, Helfert R. Balance and aging. Laryngoscope. 1999 Sep;109(9):1454-60. DOI: https://doi.org/10.1097/00005537-199909000-00019
Piitulainen H, Seipäjärvi S, Avela J, Parviainen T, Walker S. Cortical Proprioceptive Processing Is Altered by Aging. Front Aging Neurosci. 2018 Jun 14;10:147. DOI: https://doi.org/10.3389/fnagi.2018.00147
Henry M, Baudry S. Age-related changes in leg proprioception: implications for postural control. J Neurophysiol. 2019 Aug 1;122(2):525-538. Epub 2019 Jun 5. DOI: https://doi.org/10.1152/jn.00067.2019
Rosant C, Nagel MD, Pérot C. Aging affects passive stiffness and spindle function of the rat soleus muscle. Exp Gerontol. 2007 Apr;42(4):301-8. Epub 2006 Nov 21. DOI: https://doi.org/10.1016/j.exger.2006.10.007
Desaki J, Nishida N. A further observation of muscle spindles in the extensor digitorum longus muscle of the aged rat. J Electron Microsc (Tokyo). 2010;59(1):79-86. Epub 2009 Jul 31. PMID: 19648233. DOI: https://doi.org/10.1093/jmicro/dfp038
Chartier SR, Mitchell SAT, Majuta LA, Mantyh PW. The Changing Sensory and Sympathetic Innervation of the Young, Adult and Aging Mouse Femur. Neuroscience. 2018 Sep 1;387:178-190. Epub 2018 Feb 10. DOI: https://doi.org/10.1016/j.neuroscience.2018.01.047
Vaughan SK, Stanley OL, Valdez G. Impact of Aging on Proprioceptive Sensory Neurons and Intrafusal Muscle Fibers in Mice. J Gerontol A Biol Sci Med Sci. 2017 Jun 1;72(6):771-779.
Miwa T, Miwa Y, Kanda K. Dynamic and static sensitivities of muscle spindle primary endings in aged rats to ramp stretch. Neurosci Lett. 1995 Dec 8;201(2):179-82. DOI: https://doi.org/10.1016/0304-3940(95)12165-X
Kim GH, Suzuki S, Kanda K. Age-related physiological and morphological changes of muscle spindles in rats. J Physiol. 2007 Jul 15;582(Pt 2):525-38. Epub 2007 May 10. DOI: https://doi.org/10.1113/jphysiol.2007.130120
Fortier S, Basset FA. The effects of exercise on limb proprioceptive signals. J Electromyogr Kinesiol. 2012 Dec;22(6):795-802. Epub 2012 May 11. DOI: https://doi.org/10.1016/j.jelekin.2012.04.001
Nascimento CM, Ingles M, Salvador-Pascual A, Cominetti MR, Gomez-Cabrera MC, Viña J. Sarcopenia, frailty and their prevention by exercise. Free Radic Biol Med. 2019 Feb 20;132:42-49. Epub 2018 Aug 31. DOI: https://doi.org/10.1016/j.freeradbiomed.2018.08.035
Wilke J, Mohr L, Tenforde AS, Edouard P, Fossati C, González-Gross M, Sánchez Ramírez C, Laiño F, Tan B, Pillay JD, Pigozzi F, Jimenez-Pavon D, Novak B, Jaunig J, Zhang M, van Poppel M, Heidt C, Willwacher S, Yuki G, Lieberman DE, Vogt L, Verhagen E, Hespanhol L, Hollander K. A Pandemic within the Pandemic? Physical Activity Levels Substantially Decreased in Countries Affected by COVID-19. Int J Environ Res Public Health. 2021 Feb 24;18(5):2235. DOI: https://doi.org/10.3390/ijerph18052235
Denison HJ, Cooper C, Sayer AA, Robinson SM. Prevention and optimal management of sarcopenia: a review of combined exercise and nutrition interventions to improve muscle outcomes in older people. Clin Interv Aging. 2015 May 11;10:859-69. DOI: https://doi.org/10.2147/CIA.S55842
Phu S, Boersma D, Duque G. Exercise and Sarcopenia. J Clin Densitom. 2015 Oct-Dec;18(4):488-92. Epub 2015 Jun 10. DOI: https://doi.org/10.1016/j.jocd.2015.04.011
Papadopoulou SK. Sarcopenia: A Contemporary Health Problem among Older Adult Populations. Nutrients. 2020 May 1;12(5):1293. DOI: https://doi.org/10.3390/nu12051293
Giallauria F, Cittadini A, Smart NA, Vigorito C. Resistance training and sarcopenia. Monaldi Arch Chest Dis. 2016 Jun 22;84(1-2):738. DOI: https://doi.org/10.4081/monaldi.2015.738
Lichtenberg T, von Stengel S, Sieber C, Kemmler W. The Favorable Effects of a High-Intensity Resistance Training on Sarcopenia in Older Community-Dwelling Men with Osteosarcopenia: The Randomized Controlled FrOST Study. Clin Interv Aging. 2019 Dec 16;14:2173-2186. d DOI: https://doi.org/10.2147/CIA.S225618
Freiberger E, Sieber C, Pfeifer K. Physical activity, exercise, and sarcopenia - future challenges. Wien Med Wochenschr. 2011 Sep;161(17-18):416-25. Epub 2011 Jul 29 DOI: https://doi.org/10.1007/s10354-011-0001-z
Carraro U. Thirty years of translational research in Mobility Medicine: Collection of abstracts of the 2020 Padua Muscle Days. Eur J Transl Myol. 2020 Apr 1;30(1):8826. DOI: https://doi.org/10.4081/ejtm.2019.8826
Furst T, Massaro A, Miller C, Williams BT, LaMacchia ZM, Horvath PJ. β-Alanine supplementation increased physical performance and improved executive function following endurance exercise in middle aged individuals. J Int Soc Sports Nutr. 2018 Jul 11;15(1):32. DOI: https://doi.org/10.1186/s12970-018-0238-7
Moreillon M, Conde Alonso S, Broskey NT, Greggio C, Besson C, Rousson V, Amati F. Hybrid fiber alterations in exercising seniors suggest contribution to fast-to-slow muscle fiber shift. J Cachexia Sarcopenia Muscle. 2019 Jun;10(3):687-695. Epub 2019 Mar 25. DOI: https://doi.org/10.1002/jcsm.12410
Garcia M, Seelaender M, Sotiropoulos A, Coletti D, Lancha AH Jr. Vitamin D, muscle recovery, sarcopenia, cachexia, and muscle atrophy. Nutrition. 2019 Apr;60:66-69. Epub 2018 Oct 7. DOI: https://doi.org/10.1016/j.nut.2018.09.031
Barbieri E, Agostini D, Polidori E, Potenza L, Guescini M, Lucertini F, Annibalini G, Stocchi L, De Santi M, Stocchi V. The pleiotropic effect of physical exercise on mitochondrial dynamics in aging skeletal muscle. Oxid Med Cell Longev. 2015;2015:917085. Epub 2015 Apr 5 DOI: https://doi.org/10.1155/2015/917085
Di Felice V, Coletti D, Seelaender M. Editorial: Myokines, Adipokines, Cytokines in Muscle Pathophysiology. Front Physiol. 2020 Oct 23;11:592856. DOI: https://doi.org/10.3389/fphys.2020.592856
Coletti D, Aulino P, Pigna E, Barteri F, Moresi V, Annibali D, Adamo S, Berardi E. Spontaneous Physical Activity Downregulates Pax7 in Cancer Cachexia. Stem Cells Int. 2016; 2016: 6729268. Published online 2015 Dec 20. DOI: https://doi.org/10.1155/2016/6729268
Alves de Lima E Jr, Teixeira AAS, Biondo LA, Diniz TA, Silveira LS, Coletti D, Busquets Rius S, Rosa Neto JC. Exercise Reduces the Resumption of Tumor Growth and Proteolytic Pathways in the Skeletal Muscle of Mice Following Chemotherapy. Cancers (Basel). 2020 Nov 20;12(11):3466. DOI: https://doi.org/10.3390/cancers12113466
Consitt LA, Dudley C, Saxena G. Impact of Endurance and Resistance Training on Skeletal Muscle Glucose Metabolism in Older Adults. Nutrients. 2019 Nov 3;11(11):2636. DOI: https://doi.org/10.3390/nu11112636
Partridge L, Deelen J, Slagboom PE. Facing up to the global challenges of ageing. Nature. 2018 Sep;561(7721):45-56. Epub 2018 Sep 5. DOI: https://doi.org/10.1038/s41586-018-0457-8
de Castro GS, Simoes E, Lima JDCC, Ortiz-Silva M, Festuccia WT, Tokeshi F, Alcântara PS, Otoch JP, Coletti D, Seelaender M. Human Cachexia Induces Changes in Mitochondria, Autophagy and Apoptosis in the Skeletal Muscle. Cancers (Basel). 2019 Aug 28;11(9):1264. DOI: https://doi.org/10.3390/cancers11091264
Pigna E, Berardi E, Aulino P, Rizzuto E, Zampieri S, Carraro U, Kern H, Merigliano S, Gruppo M, Mericskay M, Li Z, Rocchi M, Barone R, Macaluso F, Di Felice V, Adamo S, Coletti D, Moresi V. Aerobic Exercise and Pharmacological Treatments Counteract Cachexia by Modulating Autophagy in Colon Cancer. Sci Rep. 2016 May 31;6:26991. DOI: https://doi.org/10.1038/srep26991
Brunjes DL, Kennel PJ, Christian Schulze P. Exercise capacity, physical activity, and morbidity. Heart Fail Rev. 2017 Mar;22(2):133-139. DOI: https://doi.org/10.1007/s10741-016-9592-1
Sartori R, Hagg A, Zampieri S, Armani A, Winbanks CE, Viana LR, Haidar M, Watt KI, Qian H, Pezzini C, Zanganeh P, Turner BJ, Larsson A, Zanchettin G, Pierobon ES, Moletta L, Valmasoni M, Ponzoni A, Attar S, Da Dalt G, Sperti C, Kustermann M, Thomson RE, Larsson L, Loveland KL, Costelli P, Megighian A, Merigliano S, Penna F, Gregorevic P, Sandri M. Perturbed BMP signaling and denervation promote muscle wasting in cancer cachexia. Sci Transl Med. 2021 Aug 4;13(605):eaay9592. DOI: https://doi.org/10.1126/scitranslmed.aay9592
Huot JR, Pin F, Bonetto A. Muscle weakness caused by cancer and chemotherapy is associated with loss of motor unit connectivity. Am J Cancer Res. 2021 Jun 15;11(6):2990-3001
Bouché M, Muñoz-Cánoves P, Rossi F, Coletti D. Inflammation in muscle repair, aging, and myopathies. Biomed Res Int. 2014;2014:821950. Epub 2014 Aug 4. DOI: https://doi.org/10.1155/2014/821950
Beckwée D, Delaere A, Aelbrecht S, Baert V, Beaudart C, Bruyere O, de Saint-Hubert M, Bautmans I. Exercise Interventions for the Prevention and Treatment of Sarcopenia. A Systematic Umbrella Review. J Nutr Health Aging. 2019;23(6):494-502. DOI: https://doi.org/10.1007/s12603-019-1196-8
Racca AW, Beck AE, Rao VS, Flint GV, Lundy SD, Born DE, Bamshad MJ, Regnier M. Contractility and kinetics of human fetal and human adult skeletal muscle. J Physiol. 2013 Jun 15;591(12):3049-61. Epub 2013 Apr 29. DOI: https://doi.org/10.1113/jphysiol.2013.252650
Wall CE, Holmes M, Soderblom EJ, Taylor AB. Proteomics and immunohistochemistry identify the expression of α-cardiac myosin heavy chain in the jaw-closing muscles of sooty mangabeys (order Primates). Arch Oral Biol. 2018 Jul;91:103-108. Epub 2018 Feb 3. DOI: https://doi.org/10.1016/j.archoralbio.2018.01.019
Briggs MM, Schachat F. The superfast extraocular myosin (MYH13) is localized to the innervation zone in both the global and orbital layers of rabbit extraocular muscle. J Exp Biol. 2002 Oct;205(Pt 20):3133-42. DOI: https://doi.org/10.1242/jeb.205.20.3133
Rossi AC, Mammucari C, Argentini C, Reggiani C, Schiaffino S. Two novel/ancient myosins in mammalian skeletal muscles: MYH14/7b and MYH15 are expressed in extraocular muscles and muscle spindles. J Physiol. 2010 Jan 15;588(Pt 2):353-64. Epub 2009 Nov 30. DOI: https://doi.org/10.1113/jphysiol.2009.181008
Mosole S, Rossini K, Kern H, Löfler S, Simone Fruhmann H, Vogelauer M, Burggraf S, Grim-Stieger M, Cvečka J, Hamar D, Sedliak M, Šarabon N, Pond A, Biral D, Carraro U, Zampieri S. Reinnervation of Vastus lateralis is increased significantly in seniors (70-years old) with a lifelong history of high-level exercise (2013, revisited here in 2022). Eur J Transl Myol. 32 (1): 10420, 2022. DOI: https://doi.org/10.4081/bam.2013.4.205

How to Cite

Coletti, C., Acosta, G. F., Keslacy, S., & Coletti, D. (2022). Exercise-mediated reinnervation of skeletal muscle in elderly people: An update. European Journal of Translational Myology, 32(1). https://doi.org/10.4081/ejtm.2022.10416

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