Advertisement

Rejuvenating Stem Cells to Restore Muscle Regeneration in Aging

  • Eyal BengalEmail author
  • Maali Odeh
Chapter

Abstract

Muscle stem cells, also termed satellite cells, are essential to the maintenance and repair of the muscle throughout life. During aging, the muscle tissue loses a significant portion of its mass due to atrophy and degeneration of myofibers. Muscle aging is also characterized by a decline in the repair capacity of satellite cells. A major research effort is devoted in the recent years to deciphering the cause to the decline in satellite cell function and number during aging. Some studies focus at age-associated environmental changes while others emphasize the role of cell-intrinsic mechanisms that reflect accumulation of damage during the life of the stem cell. This chapter focuses on the network of cell-intrinsic and extrinsic factors that contribute to the decline of satellite cells in old animals. We also discuss current ideas on ways to rejuvenate aged satellite cells. Such rejuvenation can potentially improve muscle repair and maintenance in the elderly.

Keywords

Muscle atrophy Sarcopenia Aging Satellite cells Muscle regeneration Stem cell rejuvenation 

References

  1. 1.
    Dutta C, Hadley EC, Lexell J. Sarcopenia and physical performance in old age: overview. Muscle Nerve Suppl. 1997;5:S5–9.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Evans WJ. What is sarcopenia? J Gerontol A Biol Sci Med Sci. 1995;50(Spec No):5–8.Google Scholar
  3. 3.
    Sambasivan R, Tajbakhsh S. Adult skeletal muscle stem cells. Results Probl Cell Differ. 2015;56:191–213.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Scharner J, Zammit PS. The muscle satellite cell at 50: the formative years. Skelet Muscle. 2011;1:28.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Yin H, Price F, Rudnicki MA. Satellite cells and the muscle stem cell niche. Physiol Rev. 2013;93:23–67.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Gunther S, Kim J, Kostin S, Lepper C, Fan CM, Braun T. Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells. Cell Stem Cell. 2013;13:590–601.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Lepper C, Partridge TA, Fan CM. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development. 2011;138:3639–46.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, Gayraud-Morel B, Guenou H, Malissen B, Tajbakhsh S, Galy A. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development. 2011;138:3647–56.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    von Maltzahn J, Jones AE, Parks RJ, Rudnicki MA. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc Natl Acad Sci U S A. 2013;110:16474–9.CrossRefGoogle Scholar
  10. 10.
    Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961;9:493–5.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell. 2005;122:289–301.CrossRefGoogle Scholar
  12. 12.
    Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007;129:999–1010.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Rocheteau P, Gayraud-Morel B, Siegl-Cachedenier I, Blasco MA, Tajbakhsh S. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell. 2012;148:112–25.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM. Self-renewal and expansion of single transplanted muscle stem cells. Nature. 2008;456:502–6.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Bentzinger CF, Wang YX, Rudnicki MA. Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol. 2012;4(2):a008342.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Bober E, Franz T, Arnold HH, Gruss P, Tremblay P. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development. 1994;120:603–12.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Relaix F, Rocancourt D, Mansouri A, Buckingham M. Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev. 2004;18:1088–105.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 2005;19:1426–31.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Kanisicak O, Mendez JJ, Yamamoto S, Yamamoto M, Goldhamer DJ. Progenitors of skeletal muscle satellite cells express the muscle determination gene. MyoD, Dev Biol. 2009;332:131–41.CrossRefGoogle Scholar
  20. 20.
    Chakkalakal JV, Christensen J, Xiang W, Tierney MT, Boscolo FS, Sacco A, Brack AS. Early forming label-retaining muscle stem cells require p27kip1 for maintenance of the primitive state. Development. 2014;141:1649–59.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Ono Y, Masuda S, Nam HS, Benezra R, Miyagoe-Suzuki Y, Takeda S. Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle. J Cell Sci. 2012;125:1309–17.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Schultz E. Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol. 1996;175:84–94.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Gros J, Manceau M, Thome V, Marcelle C. A common somatic origin for embryonic muscle progenitors and satellite cells. Nature. 2005;435:954–8.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Relaix F, Montarras D, Zaffran S, Gayraud-Morel B, Rocancourt D, Tajbakhsh S, Mansouri A, Cumano A, Buckingham M. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol. 2006;l172:91–102.CrossRefGoogle Scholar
  25. 25.
    Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell. 2000;102:777–86.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Fukada S, Ma Y, Ohtani T, Watanabe Y, Murakami S, Yamaguchi M. Isolation, characterization, and molecular regulation of muscle stem cells. Front Physiol. 2013;4:317.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Koopman R, Ly CH, Ryall JG. A metabolic link to skeletal muscle wasting and regeneration. Front Physiol. 2014;5:32.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Pallafacchina G, Francois S, Regnault B, Czarny B, Dive V, Cumano A, Montarras D, Buckingham M. An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res. 2010;4:77–91.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell. 2007;130:77–88.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Liu L, Cheung TH, Charville GW, Hurgo BM, Leavitt T, Shih J, Brunet A, Rando TA. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep. 2013;4:189–204.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Bjornson CR, Cheung TH, Liu L, Tripathi PV, Steeper KM, Rando TA. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells. 2012;30:232–42.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Mourikis P, Sambasivan R, Castel D, Rocheteau P, Bizzarro V, Tajbakhsh S. A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells. 2012;30:243–52.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Olguin HC, Olwin BB. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol. 2004;275:375–88.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Wen Y, Bi P, Liu W, Asakura A, Keller C, Kuang S. Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol Cell Biol. 2012;32:2300–11.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Fukada S, Yamaguchi M, Kokubo H, Ogawa R, Uezumi A, Yoneda T, Matev MM, Motohashi N, Ito T, Zolkiewska A, Johnson RL, Saga Y, Miyagoe-Suzuki Y, Tsujikawa K, Takeda S, Yamamoto H. Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development. 2011;138:4609–19.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Gopinath SD, Webb AE, Brunet A, Rando TA. FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Reports. 2014;2:414–26.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Allen RE, Boxhorn LK. Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol. 1989;138:311–5.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Chen SE, Gerken E, Zhang Y, Zhan M, Mohan RK, Li AS, Reid MB, Li YP. Role of TNF-{alpha} signaling in regeneration of cardiotoxin-injured muscle. Am J Physiol Cell Physiol. 2005;289:C1179–87.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Chen SE, Jin B, Li YP. TNF-alpha regulates myogenesis and muscle regeneration by activating p38 MAPK. Am J Physiol Cell Physiol. 2007;292:C1660–71.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Mourkioti F, Rosenthal N. IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol. 2005;26:535–42.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Sheehan SM, Allen RE. Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J Cell Physiol. 1999;181:499–506.CrossRefGoogle Scholar
  42. 42.
    Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol. 1998;194:114–28.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Bosurgi L, Manfredi AA, Rovere-Querini P. Macrophages in injured skeletal muscle: a perpetuum mobile causing and limiting fibrosis, prompting or restricting resolution and regeneration. Front Immunol. 2011;2:62.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Chazaud B. Macrophages: supportive cells for tissue repair and regeneration. Immunobiology. 2014;219:172–8.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Tidball JG. Mechanisms of muscle injury, repair, and regeneration. Compr Physiol. 2011;1:2029–62.PubMedGoogle Scholar
  46. 46.
    Siegel AL, Kuhlmann PK, Cornelison DD. Muscle satellite cell proliferation and association: new insights from myofiber time-lapse imaging. Skelet Muscle. 2011;1:7.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Blum R, Vethantham V, Bowman C, Rudnicki M, Dynlacht BD. Genome-wide identification of enhancers in skeletal muscle: the role of MyoD1. Genes Dev. 2012;26:2763–79.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Cao Y, Yao Z, Sarkar D, Lawrence M, Sanchez GJ, Parker MH, MacQuarrie KL, Davison J, Morgan MT, Ruzzo WL, Gentleman RC, Tapscott SJ. Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell. 2010;18:662–74.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Cooper RN, Tajbakhsh S, Mouly V, Cossu G, Buckingham M, Butler-Browne GS. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J Cell Sci. 1999;112(Pt 17):2895–901.PubMedGoogle Scholar
  50. 50.
    Boonsanay V, Zhang T, Georgieva A, Kostin S, Qi H, Yuan X, Zhou Y, Braun T. Regulation of skeletal muscle stem cell quiescence by suv4-20h1-dependent facultative heterochromatin formation. Cell Stem Cell. 2016;18:229–42.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Dilworth FJ, Blais A. Epigenetic regulation of satellite cell activation during muscle regeneration. Stem Cell Res Ther. 2011;2:18.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Moresi V, Marroncelli N, Coletti D, Adamo S. Regulation of skeletal muscle development and homeostasis by gene imprinting, histone acetylation and microRNA. Biochim Biophys Acta. 1849;2015:309–16.Google Scholar
  53. 53.
    Segales J, Perdiguero E, Munoz-Canoves P. Epigenetic control of adult skeletal muscle stem cell functions. FEBS J. 2015;282:1571–88.PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Conboy MJ, Karasov AO, Rando TA. High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol. 2007;5:e102.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol. 2006;8:677–87.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Shea KL, Xiang W, LaPorta VS, Licht JD, Keller C, Basson MA, Brack AS. Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell. 2010;6:117–29.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Brohl D, Vasyutina E, Czajkowski MT, Griger J, Rassek C, Rahn HP, Purfurst B, Wende H, Birchmeier C. Colonization of the satellite cell niche by skeletal muscle progenitor cells depends on Notch signals. Dev Cell. 2012;23:469–81.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol (1985). 2000;88:1321–6.CrossRefGoogle Scholar
  59. 59.
    Brack AS, Bildsoe H, Hughes SM. Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age-related muscle atrophy. J Cell Sci. 2005;118:4813–21.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Chakkalakal JV, Jones KM, Basson MA, Brack AS. The aged niche disrupts muscle stem cell quiescence. Nature. 2012;490:355–60.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Sousa-Victor P, Gutarra S, Garcia-Prat L, Rodriguez-Ubreva J, Ortet L, Ruiz-Bonilla V, Jardi M, Ballestar E, Gonzalez S, Serrano AL, Perdiguero E, Munoz-Canoves P. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature. 2014;506:316–21.CrossRefGoogle Scholar
  62. 62.
    Garcia-Prat L, Martinez-Vicente M, Perdiguero E, Ortet L, Rodriguez-Ubreva J, Rebollo E, Ruiz-Bonilla V, Gutarra S, Ballestar E, Serrano AL, Sandri M, Munoz-Canoves P. Autophagy maintains stemness by preventing senescence. Nature. 2016;529:37–42.CrossRefGoogle Scholar
  63. 63.
    Brack AS, Rando TA. Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev. 2007;3:226–37.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Garcia-Prat L, Sousa-Victor P, Munoz-Canoves P. Functional dysregulation of stem cells during aging: a focus on skeletal muscle stem cells. FEBS J. 2013;280:4051–62.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Bernet JD, Doles JD, Hall JK, Kelly Tanaka K, Carter TA, Olwin BB. p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat Med. 2014;20:265–71.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP, Corbel SY, Llewellyn ME, Delp SL, Blau HM. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med. 2014;20:255–64.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Price FD, von Maltzahn J, Bentzinger CF, Dumont NA, Yin H, Chang NC, Wilson DH, Frenette J, Rudnicki MA. Inhibition of JAK-STAT signaling stimulates adult satellite cell function. Nat Med. 2014;20:1174–81.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Vahidi Ferdousi L, Rocheteau P, Chayot R, Montagne B, Chaker Z, Flamant P, Tajbakhsh S, Ricchetti M. More efficient repair of DNA double-strand breaks in skeletal muscle stem cells compared to their committed progeny. Stem Cell Res. 2014;13:492–507.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Fulle S, Di Donna S, Puglielli C, Pietrangelo T, Beccafico S, Bellomo R, Protasi F, Fano G. Age-dependent imbalance of the antioxidative system in human satellite cells. Exp Gerontol. 2005;40:189–97.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, Rando TA. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science. 2007;317:807–10.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Day K, Waite LL, Thalacker-Mercer A, West A, Bamman MM, Brooks JD, Myers RM, Absher D. Differential DNA methylation with age displays both common and dynamic features across human tissues that are influenced by CpG landscape. Genome Biol. 2013;14:R102.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Ong ML, Holbrook JD. Novel region discovery method for Infinium 450K DNA methylation data reveals changes associated with aging in muscle and neuronal pathways. Aging Cell. 2014;13:142–55.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Zykovich A, Hubbard A, Flynn JM, Tarnopolsky M, Fraga MF, Kerksick C, Ogborn D, MacNeil L, Mooney SD, Melov S. Genome-wide DNA methylation changes with age in disease-free human skeletal muscle. Aging Cell. 2014;13:360–6.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Li YP, Niu A, Wen Y. Regulation of myogenic activation of p38 MAPK by TACE-mediated TNFalpha release. Front Cell Dev Biol. 2014;2:21.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Madaro L, Latella L. Forever young: rejuvenating muscle satellite cells. Front Aging Neurosci. 2015;7:37.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Segales J, Perdiguero E, Munoz-Canoves P. Regulation of muscle stem cell functions: a focus on the p38 MAPK signaling pathway. Front Cell Dev Biol. 2016;4:91.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Munoz-Espin D, Serrano M. Cellular senescence: from physiology to pathology. Nat Rev Mol Cell Biol. 2014;15:482–96.CrossRefGoogle Scholar
  78. 78.
    Tierney MT, Aydogdu T, Sala D, Malecova B, Gatto S, Puri PL, Latella L, Sacco A. STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat Med. 2014;20:1182–6.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Zhang H, Ryu D, Wu Y, Gariani K, Wang X, Luan P, D’Amico D, Ropelle ER, Lutolf MP, Aebersold R, Schoonjans K, Menzies KJ, Auwerx J. NAD(+) repletion improves mitochondrial and stem cell function and enhances life span in mice. Science. 2016;352:1436–43.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z. Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol. 2006;294:50–66.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Lefaucheur JP, Sebille A. Basic fibroblastic growth factor promotes in vivo muscle regeneration in murine muscular dystrophy. Neurosci Lett. 1995;202:121–4.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Carlson ME, Hsu M, Conboy IM. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature. 2008;454:528–32.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Biressi S, Miyabara EH, Gopinath SD, Carlig PM, Rando TA. A Wnt-TGFbeta2 axis induces a fibrogenic program in muscle stem cells from dystrophic mice. Sci Transl Med. 2014;6:267ra176.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Pessina P, Kharraz Y, Jardi M, Fukada S, Serrano AL, Perdiguero E, Munoz-Canoves P. Fibrogenic cell plasticity blunts tissue regeneration and aggravates muscular dystrophy. Stem Cell Reports. 2015;4:1046–60.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Phelps M, Stuelsatz P, Yablonka-Reuveni Z. Expression profile and overexpression outcome indicate a role for betaKlotho in skeletal muscle fibro/adipogenesis. FEBS J. 2016;283:1653–68.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science. 2003;302:1575–7.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 2005;433:760–4.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Wagers AJ, Conboy IM. Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell. 2005;122:659–67.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Tierney MT, Gromova A, Sesillo FB, Sala D, Spenle C, Orend G, Sacco A. Autonomous extracellular matrix remodeling controls a progressive adaptation in muscle stem cell regenerative capacity during development. Cell Rep. 2016;14:1940–52.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Tierney MT, Sacco A. The role of muscle stem cell-niche interactions during aging. Nat Med. 2016;22:837–8.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Lukjanenko L, Jung MJ, Hegde N, Perruisseau-Carrier C, Migliavacca E, Rozo M, Karaz S, Jacot G, Schmidt M, Li L, Metairon S, Raymond F, Lee U, Sizzano F, Wilson DH, Dumont NA, Palini A, Fassler R, Steiner P, Descombes P, Rudnicki MA, Fan CM, von Maltzahn J, Feige JN, Bentzinger CF. Loss of fibronectin from the aged stem cell niche affects the regenerative capacity of skeletal muscle in mice. Nat Med. 2016;22:897–905.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Rozo M, Li L, Fan CM. Targeting beta1-integrin signaling enhances regeneration in aged and dystrophic muscle in mice. Nat Med. 2016;22:889–96.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Kragstrup TW, Kjaer M, Mackey AL. Structural, biochemical, cellular, and functional changes in skeletal muscle extracellular matrix with aging. Scand J Med Sci Sports. 2011;21:749–57.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Wood LK, Kayupov E, Gumucio JP, Mendias CL, Claflin DR, Brooks SV. Intrinsic stiffness of extracellular matrix increases with age in skeletal muscles of mice. J Appl Physiol (1985). 2014;117:363–9.PubMedCentralCrossRefGoogle Scholar
  95. 95.
    Trappmann B, Gautrot JE, Connelly JT, Strange DG, Li Y, Oyen ML, Cohen Stuart MA, Boehm H, Li B, Vogel V, Spatz JP, Watt FM, Huck WT. Extracellular-matrix tethering regulates stem-cell fate. Nat Mater. 2012;11:642–9.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Halder G, Dupont S, Piccolo S. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat Rev Mol Cell Biol. 2012;13:591–600.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Carlson BM, Faulkner JA. Muscle transplantation between young and old rats: age of host determines recovery. Am J Physiol. 1989;256:C1262–6.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Grounds MD. Age-associated changes in the response of skeletal muscle cells to exercise and regeneration. Ann N Y Acad Sci. 1998;854:78–91.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Lee AS, Anderson JE, Joya JE, Head SI, Pather N, Kee AJ, Gunning PW, Hardeman EC. Aged skeletal muscle retains the ability to fully regenerate functional architecture. Bioarchitecture. 2013;3:25–37.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Shavlakadze T, McGeachie J, Grounds MD. Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice. Biogerontology. 2010;11:363–76.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Smythe GM, Shavlakadze T, Roberts P, Davies MJ, McGeachie JK, Grounds MD. Age influences the early events of skeletal muscle regeneration: studies of whole muscle grafts transplanted between young (8 weeks) and old (13–21 months) mice. Exp Gerontol. 2008;43:550–62.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, Eggel A, Lucin KM, Czirr E, Park JS, Couillard-Despres S, Aigner L, Li G, Peskind ER, Kaye JA, Quinn JF, Galasko DR, Xie XS, Rando TA, Wyss-Coray T. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature. 2011;477:90–4.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Conboy MJ, Conboy IM, Rando TA. Heterochronic parabiosis: historical perspective and methodological considerations for studies of aging and longevity. Aging Cell. 2013;12:525–30.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Sinha M, Jang YC, Oh J, Khong D, Wu EY, Manohar R, Miller C, Regalado SG, Loffredo FS, Pancoast JR, Hirshman MF, Lebowitz J, Shadrach JL, Cerletti M, Kim MJ, Serwold T, Goodyear LJ, Rosner B, Lee RT, Wagers AJ. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science. 2014;344:649–52.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Elabd C, Cousin W, Upadhyayula P, Chen RY, Chooljian MS, Li J, Kung S, Jiang KP, Conboy IM. Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration. Nat Commun. 2014;5:4082.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    McPherron AC, Huynh TV, Lee SJ. Redundancy of myostatin and growth/differentiation factor 11 function. BMC Dev Biol. 2009;9:24.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Egerman MA, Cadena SM, Gilbert JA, Meyer A, Nelson HN, Swalley SE, Mallozzi C, Jacobi C, Jennings LL, Clay I, Laurent G, Ma S, Brachat S, Lach-Trifilieff E, Shavlakadze T, Trendelenburg AU, Brack AS, Glass DJ. GDF11 increases with age and inhibits skeletal muscle regeneration. Cell Metab. 2015;22:164–74.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Freitas-Rodriguez S, Rodriguez F, Folgueras AR. GDF11 administration does not extend lifespan in a mouse model of premature aging. Oncotarget. 2016;7(35):55951–6.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Hinken AC, Powers JM, Luo G, Holt JA, Billin AN, Russell AJ. Lack of evidence for GDF11 as a rejuvenator of aged skeletal muscle satellite cells. Aging Cell. 2016;15:582–4.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Rinaldi F, Zhang Y, Mondragon-Gonzalez R, Harvey J, Perlingeiro RC. Treatment with rGDF11 does not improve the dystrophic muscle pathology of mdx mice. Skelet Muscle. 2016;6:21.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Rodgers BD, Eldridge JA. Reduced circulating GDF11 is unlikely responsible for age-dependent changes in mouse heart, muscle, and brain. Endocrinology. 2015;156:3885–8.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol. 2010;12:143–52.PubMedCrossRefPubMedCentralGoogle Scholar
  113. 113.
    Joe AW, Yi L, Natarajan A, Le Grand F, So L, Wang J, Rudnicki MA, Rossi FM. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol. 2010;12:153–63.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A, Gherardi RK, Chazaud B. Inflammatory monocytes recruited after skeletal muscle injury switch into anti-inflammatory macrophages to support myogenesis. J Exp Med. 2007;204:1057–69.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Perdiguero E, Sousa-Victor P, Ruiz-Bonilla V, Jardi M, Caelles C, Serrano AL, Munoz-Canoves P. p38/MKP-1-regulated AKT coordinates macrophage transitions and resolution of inflammation during tissue repair. J Cell Biol. 2011;195:307–22.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Heredia JE, Mukundan L, Chen FM, Mueller AA, Deo RC, Locksley RM, Rando TA, Chawla A. Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell. 2013;153:376–88.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Castiglioni A, Corna G, Rigamonti E, Basso V, Vezzoli M, Monno A, Almada AE, Mondino A, Wagers AJ, Manfredi AA, Rovere-Querini P. FOXP3+ T cells recruited to sites of sterile skeletal muscle injury regulate the fate of satellite cells and guide effective tissue regeneration. PLoS One. 2015;10:e0128094.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Zhang J, Xiao Z, Qu C, Cui W, Wang X, Du J. CD8 T cells are involved in skeletal muscle regeneration through facilitating MCP-1 secretion and Gr1(high) macrophage infiltration. J Immunol. 2014;193:5149–60.PubMedCrossRefPubMedCentralGoogle Scholar
  119. 119.
    Burzyn D, Kuswanto W, Kolodin D, Shadrach JL, Cerletti M, Jang Y, Sefik E, Tan TG, Wagers AJ, Benoist C, Mathis D. A special population of regulatory T cells potentiates muscle repair. Cell. 2013;155:1282–95.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Kuswanto W, Burzyn D, Panduro M, Wang KK, Jang YC, Wagers AJ, Benoist C, Mathis D. Poor repair of skeletal muscle in aging mice reflects a defect in local, interleukin-33-dependent accumulation of regulatory T cells. Immunity. 2016;44:355–67.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Villalta SA, Rosenthal W, Martinez L, Kaur A, Sparwasser T, Tidball JG, Margeta M, Spencer MJ, Bluestone JA. Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy. Sci Transl Med. 2014;6:258ra142.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Abou-Khalil R, Mounier R, Chazaud B. Regulation of myogenic stem cell behavior by vessel cells: the “menage a trois” of satellite cells, periendothelial cells and endothelial cells. Cell Cycle. 2010;9:892–6.PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Christov C, Chretien F, Abou-Khalil R, Bassez G, Vallet G, Authier FJ, Bassaglia Y, Shinin V, Tajbakhsh S, Chazaud B, Gherardi RK. Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell. 2007;18:1397–409.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Liu W, Wei-LaPierre L, Klose A, Dirksen RT, Chakkalakal JV. Inducible depletion of adult skeletal muscle stem cells impairs the regeneration of neuromuscular junctions. eLife. 2015;4:e09221.PubMedCentralCrossRefGoogle Scholar
  125. 125.
    Carraro U, Boncompagni S, Gobbo V, Rossini K, Zampieri S, Mosole S, Ravara B, Nori A, Stramare R, Ambrosio F, Piccione F, Masiero S, Vindigni V, Gargiulo P, Protasi F, Kern H, Pond A, Marcante A. Persistent muscle fiber regeneration in long term denervation. past, present, future. Eur J Transl Myol. 2015;25:4832.PubMedPubMedCentralGoogle Scholar
  126. 126.
    Blau HM, Cosgrove BD, Ho AT. The central role of muscle stem cells in regenerative failure with aging. Nat Med. 2015;21:854–62.PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Goodell MA, Nguyen H, Shroyer N. Somatic stem cell heterogeneity: diversity in the blood, skin and intestinal stem cell compartments. Nat Rev Mol Cell Biol. 2015;16:299–309.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, Partridge T, Buckingham M. Direct isolation of satellite cells for skeletal muscle regeneration. Science. 2005;309:2064–7.CrossRefGoogle Scholar
  129. 129.
    Gilbert PM, Havenstrite KL, Magnusson KE, Sacco A, Leonardi NA, Kraft P, Nguyen NK, Thrun S, Lutolf MP, Blau HM. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science. 2010;329:1078–81.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Cerletti M, Jang YC, Finley LW, Haigis MC, Wagers AJ. Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell. 2012;10:515–9.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Shefer G, Rauner G, Stuelsatz P, Benayahu D, Yablonka-Reuveni Z. Moderate-intensity treadmill running promotes expansion of the satellite cell pool in young and old mice. FEBS J. 2013;280:4063–73.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Shefer G, Rauner G, Yablonka-Reuveni Z, Benayahu D. Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS One. 2010;5:e13307.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Joanisse S, Nederveen JP, Baker JM, Snijders T, Iacono C, Parise G. Exercise conditioning in old mice improves skeletal muscle regeneration. FASEB J. 2016;30:3256–68.PubMedCrossRefPubMedCentralGoogle Scholar
  134. 134.
    Pietrangelo T, Di Filippo ES, Mancinelli R, Doria C, Rotini A, Fano-Illic G, Fulle S. Low intensity exercise training improves skeletal muscle regeneration potential. Front Physiol. 2015;6:399.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Biochemistry, The Ruth and Bruce Rappaport Faculty of MedicineTechnion-Israel Institute of TechnologyHaifaIsrael

Personalised recommendations