The ins and outs of muscle stem cell aging

Skeletal Muscle

Volumn 6, Issue 1, 2016, Pages

  Brack, Andrew S ^a   Muñoz Cánoves, Pura ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; HUMAN; METABOLISM; PHENOTYPE; PHYSIOLOGY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; STEM CELL NICHE;

ANIMALS; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; MUSCLE, SKELETAL; PHENOTYPE; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; STEM CELL NICHE;

EID: 84954348838     PISSN: None     EISSN: 20445040     Source Type: Journal    
DOI: 10.1186/s13395-016-0072-z     Document Type: Review

References (75)

1. Jung Y, Brack AS. Cellular mechanisms of somatic stem cell aging. Curr Top Dev Biol. 2014;107:405-38. doi: 10.1016/B978-0-12-416022-4.00014-7.
2. Cheung TH, Rando TA. Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol. 2013;14(6):329-40. doi: 10.1038/nrm3591.
3. Oh J, Lee YD, Wagers AJ. Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nat Med. 2014;20(8):870-80. doi: 10.1038/nm.3651.
4. 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(7027):760-4. doi: 10.1038/nature03260.
5. Conboy MJ, Conboy IM, Rando TA. Heterochronic parabiosis: historical perspective and methodological considerations for studies of aging and longevity. Aging cell. 2013;12(3):525-30. doi: 10.1111/acel.12065.
6. Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M, Ottaviani E, et al. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci. 2000;908:244-54.
7. Shavlakadze T, McGeachie J, Grounds MD. Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice. Biogerontology. 2010;11(3):363-76. doi: 10.1007/s10522-009-9260-0.
8. 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(6):550-62. doi: 10.1016/j.exger.2008.02.005.
9. Lepper C, Partridge TA, Fan CM. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development. 2011;138(17):3639-46. doi: 10.1242/dev.067595.
10. Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, Gayraud-Morel B, et al. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development. 2011;138(17):3647-56. doi: 10.1242/dev.067587.
11. 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(41):16474-9. doi: 10.1073/pnas.1307680110.
12. Brack AS, Rando TA. Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell. 2012;10(5):504-14. doi: 10.1016/j.stem.2012.04.001.
13. Chakkalakal JV, Jones KM, Basson MA, Brack AS. The aged niche disrupts muscle stem cell quiescence. Nature. 2012;490(7420):355-60. doi: 10.1038/nature11438.
14. Sousa-Victor P, Gutarra S, Garcia-Prat L, Rodriguez-Ubreva J, Ortet L, Ruiz-Bonilla V, et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature. 2014;506(7488):316-21. doi: 10.1038/nature13013.
15. 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(3):265-71. doi: 10.1038/nm.3465.
16. Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP, Corbel SY, et al. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med. 2014;20(3):255-64. doi: 10.1038/nm.3464.
17. Price FD, von Maltzahn J, Bentzinger CF, Dumont NA, Yin H, Chang NC et al. Inhibition of JAK-STAT signaling stimulates adult satellite cell function. Nature medicine. 2014. doi: 10.1038/nm.3655.
18. Tierney MT, Aydogdu T, Sala D, Malecova B, Gatto S, Puri PL et al. STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nature medicine. 2014. doi: 10.1038/nm.3656.
19. Fry CS, Lee JD, Mula J, Kirby TJ, Jackson JR, Liu F, et al. Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat Med. 2015;21(1):76-80. doi: 10.1038/nm.3710.
20. 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(Pt 20):4813-21. doi: 10.1242/jcs.02602.
21. Harrison DE. Long-term erythropoietic repopulating ability of old, young, and fetal stem cells. The Journal of experimental medicine. 1983;157(5):1496-504.
22. Carlson BM, Faulkner JA. The regeneration of skeletal muscle fibers following injury: a review. MedSciSports Exercise. 1983;15:187.
23. Brack AS, Rando TA. Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev. 2007;3(3):226-37.
24. Carlson BM, Faulkner JA. Muscle transplantation between young and old rats: age of host determines recovery. The American journal of physiology. 1989;256(6 Pt 1):C1262-6.
25. 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):78-91.
26. Lee AS, Anderson JE, Joya JE, Head SI, Pather N, Kee AJ, et al. Aged skeletal muscle retains the ability to fully regenerate functional architecture. Biogeosciences. 2013;3(2):25-37. doi: 10.4161/bioa.24966.
27. Carlson ME, Hsu M, Conboy IM. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature. 2008;454(7203):528-32. doi: 10.1038/nature07034.
28. Elabd C, Cousin W, Upadhyayula P, Chen RY, Chooljian MS, Li J, et al. Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration. Nat Commun. 2014;5:4082. doi: 10.1038/ncomms5082.
29. Naito AT, Sumida T, Nomura S, Liu ML, Higo T, Nakagawa A, et al. Complement C1q activates canonical Wnt signaling and promotes aging-related phenotypes. Cell. 2012;149(6):1298-313. doi: 10.1016/j.cell.2012.03.047.
30. Paliwal P, Pishesha N, Wijaya D, Conboy IM. Age dependent increase in the levels of osteopontin inhibits skeletal muscle regeneration. Aging (Albany NY). 2012;4(8):553-66.
31. Yousef H, Conboy MJ, Morgenthaler A, Schlesinger C, Bugaj L, Paliwal P, et al. Systemic attenuation of the TGF-beta pathway by a single drug simultaneously rejuvenates hippocampal neurogenesis and myogenesis in the same old mammal. Oncotarget. 2015;6(14):11959-78.
32. Egerman MA, Cadena SM, Gilbert JA, Meyer A, Nelson HN, Swalley SE, et al. GDF11 increases with age and inhibits skeletal muscle regeneration. Cell Metab. 2015;22(1):164-74. doi: 10.1016/j.cmet.2015.05.010.
33. Sinha M, Jang YC, Oh J, Khong D, Wu EY, Manohar R, et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science. 2014;344(6184):649-52. doi: 10.1126/science.1251152.
34. Brun CE, Rudnicki MA. GDF11 and the mythical fountain of youth. Cell Metab. 2015;22(1):54-6. doi: 10.1016/j.cmet.2015.05.009.
35. Kharraz Y, Guerra J, Pessina P, Serrano AL, Munoz-Canoves P. Understanding the process of fibrosis in Duchenne muscular dystrophy. BioMed research international. 2014;2014:965631. doi: 10.1155/2014/965631.
36. Tidball JG, Dorshkind K, Wehling-Henricks M. Shared signaling systems in myeloid cell-mediated muscle regeneration. Development. 2014;141(6):1184-96. doi: 10.1242/dev.098285.
37. Salminen A, Kaarniranta K, Kauppinen A. Inflammaging: disturbed interplay between autophagy and inflammasomes. Aging (Albany NY). 2012;4(3):166-75.
38. Lemos DR, Babaeijandaghi F, Low M, Chang CK, Lee ST, Fiore D, et al. Nilotinib reduces muscle fibrosis in chronic muscle injury by promoting TNF-mediated apoptosis of fibro/adipogenic progenitors. Nat Med. 2015;21(7):786-94. doi: 10.1038/nm.3869.
39. McCulloch EA, Till JE. The radiation sensitivity of normal mouse bone marrow cells, determined by quantitative marrow transplantation into irradiated mice. Radiat Res. 1960;13:115-25.
40. Till JE, Mc CE. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res. 1961;14:213-22.
41. Collins CA, Zammit PS, Ruiz AP, Morgan JE, Partridge TA. A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells. 2007;25(4):885-94. doi: 10.1634/stemcells.2006-0372.
42. Garcia-Prat L, Sousa-Victor P, Munoz-Canoves P. Functional dysregulation of stem cells during aging: a focus on skeletal muscle stem cells. The FEBS journal. 2013;280(17):4051-62. doi: 10.1111/febs.12221.
43. Sousa-Victor P, Garcia-Prat L, Serrano AL, Perdiguero E, Munoz-Canoves P. Muscle stem cell aging: regulation and rejuvenation. Trends in endocrinology and metabolism: TEM. 2015;26(6):287-96. doi: 10.1016/j.tem.2015.03.006.
44. Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007;129(5):999-1010. doi: 10.1016/j.cell.2007.03.044.
45. 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(1-2):112-25. doi: 10.1016/j.cell.2011.11.049.
46. 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(5), e102. doi: 10.1371/journal.pbio.0050102.
47. Zeng W, Lu YH, Lee J, Friedman JM. Reanalysis of parabiosis of obesity mutants in the age of leptin. Proc Natl Acad Sci U S A. 2015;112(29):E3874-82. doi: 10.1073/pnas.1510378112.
48. Sun J, Ramos A, Chapman B, Johnnidis JB, Le L, Ho YJ, et al. Clonal dynamics of native haematopoiesis. Nature. 2014;514(7522):322-7. doi: 10.1038/nature13824.
49. Hall JK, Banks GB, Chamberlain JS, Olwin BB. Prevention of muscle aging by myofiber-associated satellite cell transplantation. Science translational medicine. 2010;2(57):57ra83. doi: 10.1126/scitranslmed.3001081.
50. Vahidi Ferdousi L, Rocheteau P, Chayot R, Montagne B, Chaker Z, Flamant P, et al. More efficient repair of DNA double-strand breaks in skeletal muscle stem cells compared to their committed progeny. Stem Cell Res. 2014;13(3 Pt A):492-507. doi: 10.1016/j.scr.2014.08.005.
51. Fulle S, Di Donna S, Puglielli C, Pietrangelo T, Beccafico S, Bellomo R, et al. Age-dependent imbalance of the antioxidative system in human satellite cells. Exp Gerontol. 2005;40(3):189-97. doi: 10.1016/j.exger.2004.11.006.
52. Didier N, Hourde C, Amthor H, Marazzi G, Sassoon D. Loss of a single allele for Ku80 leads to progenitor dysfunction and accelerated aging in skeletal muscle. EMBO Mol Med. 2012;4(9):910-23. doi: 10.1002/emmm.201101075.
53. Baj A, Bettaccini AA, Casalone R, Sala A, Cherubino P, Toniolo AQ. Culture of skeletal myoblasts from human donors aged over 40 years: dynamics of cell growth and expression of differentiation markers. J Transl Med. 2005;3(1):21. doi: 10.1186/1479-5876-3-21.
54. Bortoli S, Renault V, Eveno E, Auffray C, Butler-Browne G, Pietu G. Gene expression profiling of human satellite cells during muscular aging using cDNA arrays. Gene. 2003;321:145-54.
55. Charge SB, Brack AS, Hughes SM. Aging-related satellite cell differentiation defect occurs prematurely after Ski-induced muscle hypertrophy. Am J Physiol Cell Physiol. 2002;283(4):C1228-41. doi: 10.1152/ajpcell.00206.2002.
56. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science. 2003;302(5650):1575-7. doi: 10.1126/science.1087573.
57. Day K, Shefer G, Shearer A, Yablonka-Reuveni Z. The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev Biol. 2010;340(2):330-43. doi: 10.1016/j.ydbio.2010.01.006.
58. Liu L, Cheung TH, Charville GW, Hurgo BM, Leavitt T, Shih J, et al. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell reports. 2013;4(1):189-204. doi: 10.1016/j.celrep.2013.05.043.
59. Pietrangelo T, Puglielli C, Mancinelli R, Beccafico S, Fano G, Fulle S. Molecular basis of the myogenic profile of aged human skeletal muscle satellite cells during differentiation. Exp Gerontol. 2009;44(8):523-31. doi: 10.1016/j.exger.2009.05.002.
60. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, et al. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature. 2011;479(7372):232-6. doi: 10.1038/nature10600.
61. Sousa-Victor P, Perdiguero E, Munoz-Canoves P. Geroconversion of aged muscle stem cells under regenerative pressure. Cell Cycle. 2014;13(20):3183-90. doi: 10.4161/15384101.2014.965072.
62. Juan AH, Derfoul A, Feng X, Ryall JG, Dell'Orso S, Pasut A, et al. Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes Dev. 2011;25(8):789-94. doi: 10.1101/gad.2027911.
63. Le Roux I, Konge J, Le Cam L, Flamant P, Tajbakhsh S. Numb is required to prevent p53-dependent senescence following skeletal muscle injury. Nat Commun. 2015;6:8528. doi: 10.1038/ncomms9528.
64. Chakkalakal JV, Christensen J, Xiang W, Tierney MT, Boscolo FS, Sacco A, et al. Early forming label-retaining muscle stem cells require p27kip1 for maintenance of the primitive state. Development. 2014;141(8):1649-59. doi: 10.1242/dev.100842.
65. Shea KL, Xiang W, LaPorta VS, Licht JD, Keller C, Basson MA, et al. Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell. 2010;6(2):117-29. doi: 10.1016/j.stem.2009.12.015.
66. Bigot A, Duddy WJ, Ouandaogo ZG, Negroni E, Mariot V, Ghimbovschi S, et al. Age-associated methylation suppresses SPRY1, leading to a failure of re-quiescence and loss of the reserve stem cell pool in elderly muscle. Cell reports. 2015. doi: 10.1016/j.celrep.2015.09.067.
67. Goh LK, Sorkin A. Endocytosis of receptor tyrosine kinases. Cold Spring Harbor perspectives in biology. 2013;5(5):a017459. doi: 10.1101/cshperspect.a017459.
68. Franceschi C, Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol Ser A Biol Med Sci. 2014;69 Suppl 1:S4-9. doi: 10.1093/gerona/glu057.
69. Kodama R, Kato M, Furuta S, Ueno S, Zhang Y, Matsuno K, et al. ROS-generating oxidases Nox1 and Nox4 contribute to oncogenic Ras-induced premature senescence. Genes to cells: devoted to molecular & cellular mechanisms. 2013;18(1):32-41. doi: 10.1111/gtc.12015.
70. Lee AC, Fenster BE, Ito H, Takeda K, Bae NS, Hirai T, et al. Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. The Journal of biological chemistry. 1999;274(12):7936-40.
71. Mandal PK, Blanpain C, Rossi DJ. DNA damage response in adult stem cells: pathways and consequences. Nat Rev Mol Cell Biol. 2011;12(3):198-202. doi: 10.1038/nrm3060.
72. Ramsey MR, Sharpless NE. ROS as a tumour suppressor? Nat Cell Biol. 2006;8(11):1213-5. doi: 10.1038/ncb1106-1213.
73. Shao L, Li H, Pazhanisamy SK, Meng A, Wang Y, Zhou D. Reactive oxygen species and hematopoietic stem cell senescence. Int J Hematol. 2011;94(1):24-32. doi: 10.1007/s12185-011-0872-1.
74. 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(5):515-9. doi: 10.1016/j.stem.2012.04.002.
75. Charville GW, Cheung TH, Yoo B, Santos PJ, Lee GK, Shrager JB, et al. Ex vivo expansion and in vivo self-renewal of human muscle stem cells. Stem cell reports. 2015;5(4):621-32. doi: 10.1016/j.stemcr.2015.08.004.