Autophagy regulates satellite cell ability to regenerate normal and dystrophic muscles

Cell Death and Differentiation

Volumn 23, Issue 11, 2016, Pages 1839-1849

  Fiacco, E ^a,b   Castagnetti, F ^a,b   Bianconi, V ^a   Madaro, L ^a,c   De Bardi, M ^a   Nazio, F ^d,e   D'Amico, A ^e   Bertini, E ^e   Cecconi, F ^d,f   Puri, P L ^a,g   Latella, L ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^c CNR   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

^e BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^f DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^g BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL ACTIVATION; CELL DIFFERENTIATION; CELL REGENERATION; CHILD; CONTROLLED STUDY; DISEASE COURSE; DUCHENNE MUSCULAR DYSTROPHY; HUMAN; HUMAN TISSUE; MALE; MOUSE; MUSCLE BIOPSY; MUSCLE INJURY; MUSCLE REGENERATION; MYOFIBROSIS; NONHUMAN; PRIORITY JOURNAL; SATELLITE CELL; WILD TYPE; ANIMAL; ANIMAL MUSCULAR DYSTROPHY; BIOPSY; C57BL MOUSE; DISEASE EXACERBATION; PATHOLOGY; PATHOPHYSIOLOGY; PRESCHOOL CHILD; REGENERATION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; AUTOPHAGY; BIOPSY; CHILD; CHILD, PRESCHOOL; DISEASE PROGRESSION; HUMANS; MALE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84979266136     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2016.70     Document Type: Article

References (57)

1. Hoffman EP, Brown RH Jr., Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987; 51: 919-928.
2. Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG, Campbell KP. Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 1990; 345: 315-319.
3. Allen DG, Whitehead NP, Froehner SC. Absence of dystrophin disrupts skeletal muscle signaling: roles of Ca2+, reactive oxygen species, and nitric oxide in the development of muscular dystrophy. Physiol Rev 2016; 96: 253-305.
4. Matsumura K, Campbell KP. Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 1994; 17: 2-15.
5. Dumont NA, Wang YX, von Maltzahn J, Pasut A, Bentzinger CF, Brun CE et al. Dystrophin expression in muscle stem cells regulates their polarity and asymmetric division. Nat Med 2015; 21: 1455-1463.
6. Collins CA, Partridge TA. Self-renewal of the adult skeletal muscle satellite cell. Cell Cycle 2005; 4: 1338-1341.
7. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science 2005; 309: 2064-2067.
8. Heslop L, Morgan JE, Partridge TA. Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Sci 2000; 113: 2299-2308.
9. Serrano AL, Mann CJ, Vidal B, Ardite E, Perdiguero E, Munoz-Canoves P. Cellular and molecular mechanisms regulating fibrosis in skeletal muscle repair and disease. Curr Top Dev Biol 2011; 96: 167-201.
10. Chakkalakal JV, Jones KM, Basson MA, Brack AS. The aged niche disrupts muscle stem cell quiescence. Nature 2012; 490: 355-360.
11. Bentzinger CF, Wang YX, Dumont NA, Rudnicki MA. Cellular dynamics in the muscle satellite cell niche. EMBO Rep 2013; 14: 1062-1072.
12. Madaro L, Latella L. Forever young: rejuvenating muscle satellite cells. Front Aging Neurosci 2015; 7: 37.
13. Tierney MT, Aydogdu T, Sala D, Malecova B, Gatto S, Puri PL et al. STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat Med 2014; 20: 1182-1186.
14. Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40: 280-293.
15. Marino G, Madeo F, Kroemer G. Autophagy for tissue homeostasis and neuroprotection. Curr Opin Cell Biol 2011; 23: 198-206.
16. Jiang P, Mizushima N. Autophagy and human diseases. Cell Res 2014; 24: 69-79.
17. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
18. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8: 741-752.
19. Sandri M. Autophagy in skeletal muscle. FEBS Lett 2010; 584: 1411-1416.
20. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M et al. Autophagy is required to maintain muscle mass. Cell Metab 2009; 10: 507-515.
21. Grumati P, Coletto L, Sabatelli P, Cescon M, Angelin A, Bertaggia E et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 2010; 16: 1313-1320.
22. Chrisam M, Pirozzi M, Castagnaro S, Blaauw B, Polishchuck R, Cecconi F et al. Reactivation of autophagy by spermidine ameliorates the myopathic defects of collagen VI-null mice. Autophagy 2015; 11: 2142-2152.
23. Grumati P, Coletto L, Sandri M, Bonaldo P. Autophagy induction rescues muscular dystrophy. Autophagy 2011; 7: 426-428.
24. De Palma C, Morisi F, Cheli S, Pambianco S, Cappello V, Vezzoli M et al. Autophagy as a new therapeutic target in Duchenne muscular dystrophy. Cell Death Dis 2012; 3: e418.
25. Hindi SM, Sato S, Choi Y, Kumar A. Distinct roles of TRAF6 at early and late stages of muscle pathology in the mdx model of Duchenne muscular dystrophy. Hum Mol Genet 2014; 23: 1492-1505.
26. Pauly M, Daussin F, Burelle Y, Li T, Godin R, Fauconnier J et al. AMPK activation stimulates autophagy and ameliorates muscular dystrophy in the mdx mouse diaphragm. Am J Pathol 2012; 181: 583-592.
27. Whitehead NP, Kim MJ, Bible KL, Adams ME, Froehner SC. A new therapeutic effect of simvastatin revealed by functional improvement in muscular dystrophy. Proc Natl Acad Sci USA 2015; 112: 12864-12869.
28. Carnio S, LoVerso F, Baraibar MA, Longa E, Khan MM, Maffei M et al. Autophagy impairment in muscle induces neuromuscular junction degeneration and precocious aging. Cell Rep 2014; 8: 1509-1521.
29. Rubinsztein DC, Marino G, Kroemer G. Autophagy and aging. Cell 2011; 146: 682-695.
30. Sandri M, Coletto L, Grumati P, Bonaldo P. Misregulation of autophagy and protein degradation systems in myopathies and muscular dystrophies. J Cell Sci 2013; 126: 5325-5333.
31. Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE et al. A role for the NADdependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci USA 2008; 105: 3374-3379.
32. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM et al. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 2009; 325: 201-204.
33. Yang L, Licastro D, Cava E, Veronese N, Spelta F, Rizza W et al. Long-term calorie restriction enhances cellular quality-control processes in human skeletal muscle. Cell Rep 2016; 14: 422-428.
34. 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: 515-519.
35. Tang AH, Rando TA. Induction of autophagy supports the bioenergetic demands of quiescent muscle stem cell activation. EMBO J 2014; 33: 2782-2797.
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 Rep 2014; 2: 414-426.
37. Garcia-Prat L, Martinez-Vicente M, Perdiguero E, Ortet L, Rodriguez-Ubreva J, Rebollo E et al. Autophagy maintains stemness by preventing senescence. Nature 2016; 529: 37-42.
38. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282: 24131-24145.
39. Perry CN, Kyoi S, Hariharan N, Takagi H, Sadoshima J, Gottlieb RA. Novel methods for measuring cardiac autophagy in vivo. Methods Enzymol 2009; 453: 325-342.
40. Mosqueira M, Zeiger U, Forderer M, Brinkmeier H, Fink RH. Cardiac and respiratory dysfunction in Duchenne muscular dystrophy and the role of second messengers. Med Res Rev 2013; 33: 1174-1213.
41. Kharraz Y, Guerra J, Pessina P, Serrano AL, Munoz-Canoves P. Understanding the process of fibrosis in Duchenne muscular dystrophy. Biomed Res Int 2014; 2014: 965631.
42. Nazio F, Strappazzon F, Antonioli M, Bielli P, Cianfanelli V, Bordi M et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat Cell Biol 2013; 15: 406-416.
43. Markham LW, Spicer RL, Khoury PR, Wong BL, Mathews KD, Cripe LH. Steroid therapy and cardiac function in Duchenne muscular dystrophy. Pediatr Cardiol 2005; 26: 768-771.
44. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology 2008; 23: 160-170.
45. Bibee KP, Cheng YJ, Ching JK, Marsh JN, Li AJ, Keeling RM et al. Rapamycin nanoparticles target defective autophagy in muscular dystrophy to enhance both strength and cardiac function. FASEB J 2014; 28: 2047-2061.
46. Pal R, Palmieri M, Loehr JA, Li S, Abo-Zahrah R, Monroe TO et al. Src-dependent impairment of autophagy by oxidative stress in a mouse model of Duchenne muscular dystrophy. Nat Commun 2014; 5: 4425.
47. De Palma C, Morisi F, Pambianco S, Assi E, Touvier T, Russo S et al. Deficient nitric oxide signalling impairs skeletal muscle growth and performance: involvement of mitochondrial dysregulation. Skelet Muscle 2014; 4: 22.
48. Brunelli S, Sciorati C, D'Antona G, Innocenzi A, Covarello D, Galvez BG et al. Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy. Proc Natl Acad Sci USA 2007; 104: 264-269.
49. Colussi C, Mozzetta C, Gurtner A, Illi B, Rosati J, Straino S et al. HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc Natl Acad Sci USA 2008; 105: 19183-19187.
50. Minetti GC, Colussi C, Adami R, Serra C, Mozzetta C, Parente V et al. Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors. Nat Med 2006; 12: 1147-1150.
51. Mozzetta C, Consalvi S, Saccone V, Forcales SV, Puri PL, Palacios D. Selective control of Pax7 expression by TNF-activated p38alpha/polycomb repressive complex 2 (PRC2) signaling during muscle satellite cell differentiation. Cell Cycle 2011; 10: 191-198.
52. Saccone V, Consalvi S, Giordani L, Mozzetta C, Barozzi I, Sandona M et al. HDAC-regulated myomiRs control BAF60 variant exchange and direct the functional phenotype of fibroadipogenic progenitors in dystrophic muscles. Genes Dev 2014; 28: 841-857.
53. Consalvi S, Mozzetta C, Bettica P, Germani M, Fiorentini F, Del Bene F et al. Preclinical studies in the mdx mouse model of duchenne muscular dystrophy with the histone deacetylase inhibitor givinostat. Mol Med 2013; 19: 79-87.
54. Mozzetta C, Consalvi S, Saccone V, Tierney M, Diamantini A, Mitchell KJ et al. Fibroadipogenic progenitors mediate the ability of HDAC inhibitors to promote regeneration in dystrophic muscles of young, but not old Mdx mice. EMBO Mol Med 2013; 5: 626-639.
55. Robert T, Vanoli F, Chiolo I, Shubassi G, Bernstein KA, Rothstein R et al. HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature 2011; 471: 74-79.
56. Zhang J, Ng S, Wang J, Zhou J, Tan SH, Yang N et al. Histone deacetylase inhibitors induce autophagy through FOXO1-dependent pathways. Autophagy 2015; 11: 629-642.
57. Krajewska M, Smith LH, Rong J, Huang X, Hyer ML, Zeps N et al. Image analysis algorithms for immunohistochemical assessment of cell death events and fibrosis in tissue sections. J Histochem Cytochem 2009; 57: 649-663.