Home LiteratureArticle Details
PMID: 22024752 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Physical exercise stimulates autophagy in normal skeletal muscles but is detrimental for collagen VI-deficient muscles.

Autophagy ·Vol. 7 ·No. 12 ·2011-12-00 ·Pages 1415-23

Grumati P, Coletto L, Schiavinato A, Castagnaro S, Bertaggia E, Sandri M, Bonaldo P

Abstract

Autophagy is a catabolic process that provides the degradation of altered/damaged organelles through the fusion between autophagosomes and lysosomes. Proper regulation of the autophagic flux is fundamental for the homeostasis of skeletal muscles in physiological conditions and in response to stress. Defective as well as excessive autophagy is detrimental for muscle health and has a pathogenic role in several forms of muscle diseases. Recently, we found that defective activation of the autophagic machinery plays a key role in the pathogenesis of muscular dystrophies linked to collagen VI. Impairment of the autophagic flux in collagen VI null (Col6a1–/–) mice causes accumulation of dysfunctional mitochondria and altered sarcoplasmic reticulum, leading to apoptosis and degeneration of muscle fibers. Here we show that physical exercise activates autophagy in skeletal muscles. Notably, physical training exacerbated the dystrophic phenotype of Col6a1–/– mice, where autophagy flux is compromised. Autophagy was not induced in Col6a1–/– muscles after either acute or prolonged exercise, and this led to a marked increase of muscle wasting and apoptosis. These findings indicate that proper activation of autophagy is important for muscle homeostasis during physical activity.

MeSH Terms
Animals Autophagy Collagen Type VI/deficiency,metabolism Mice Mice, Inbred C57BL Muscle, Skeletal/metabolism,pathology,ultrastructure Physical Conditioning, Animal Time Factors Wasting Syndrome/pathology
Chemicals
Col6a1 protein, mouse Collagen Type VI
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Grumati Paolo
Department of Histology, Microbiology and Medical Biotechnology, University of Padova, Padova, Italy.
Coletto Luisa
Schiavinato Alvise
Castagnaro Silvia
Bertaggia Enrico
Sandri Marco
Bonaldo Paolo
References (39)
39 references, click to expand
  1. The role of autophagy in mammalian development: cell makeover rather than cell death.
    Dev Cell. 2008 Sep;15(3):344-357 PMID: 18804433
  2. Autophagy is required to maintain muscle mass.
    Cell Metab. 2009 Dec;10(6):507-15 PMID: 19945408
  3. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver.
    Science. 2003 Jun 6;300(5625):1574-7 PMID: 12791994
  4. Autosomal recessive myosclerosis myopathy is a collagen VI disorder.
    Neurology. 2008 Oct 14;71(16):1245-53 PMID: 18852439
  5. FoxO3 controls autophagy in skeletal muscle in vivo.
    Cell Metab. 2007 Dec;6(6):458-71 PMID: 18054315
  6. Autophagy induction rescues muscular dystrophy.
    Autophagy. 2011 Apr;7(4):426-8 PMID: 21543891
  7. Autophagy in health and disease. 3. Involvement of autophagy in muscle atrophy.
    Am J Physiol Cell Physiol. 2010 Jun;298(6):C1291-7 PMID: 20089936
  8. Autophagy in the pathogenesis of disease.
    Cell. 2008 Jan 11;132(1):27-42 PMID: 18191218
  9. The kinase domain of titin controls muscle gene expression and protein turnover.
    Science. 2005 Jun 10;308(5728):1599-603 PMID: 15802564
  10. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription.
    Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16260-5 PMID: 17053067
  11. Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency.
    Nat Genet. 2003 Dec;35(4):367-71 PMID: 14625552
  12. The sarcomeric cytoskeleton: who picks up the strain?
    Curr Opin Cell Biol. 2011 Feb;23(1):39-46 PMID: 21190822
  13. Mitochondrial dysfunction in the pathogenesis of Ullrich congenital muscular dystrophy and prospective therapy with cyclosporins.
    Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):991-6 PMID: 17215366
  14. Collagen type VI and related disorders: Bethlem myopathy and Ullrich scleroatonic muscular dystrophy.
    Eur J Paediatr Neurol. 2002;6(4):193-8 PMID: 12374585
  15. PI3 kinase regulation of skeletal muscle hypertrophy and atrophy.
    Curr Top Microbiol Immunol. 2010;346:267-78 PMID: 20593312
  16. Dual role of transcription factor FoxO1 in controlling hepatic insulin sensitivity and lipid metabolism.
    J Clin Invest. 2006 Sep;116(9):2464-72 PMID: 16906224
  17. Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging.
    Proc Natl Acad Sci U S A. 2009 Dec 1;106(48):20405-10 PMID: 19918075
  18. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres.
    Nature. 2002 Aug 15;418(6899):797-801 PMID: 12181572
  19. Oxidative stress, chronic disease, and muscle wasting.
    Muscle Nerve. 2007 Apr;35(4):411-29 PMID: 17266144
  20. PGC-1α promotes nitric oxide antioxidant defenses and inhibits FOXO signaling against cardiac cachexia in mice.
    Am J Pathol. 2011 Apr;178(4):1738-48 PMID: 21435455
  21. Autophagy fights disease through cellular self-digestion.
    Nature. 2008 Feb 28;451(7182):1069-75 PMID: 18305538
  22. Mitochondrial biogenesis and fragmentation as regulators of muscle protein degradation.
    Curr Hypertens Rep. 2010 Dec;12(6):433-9 PMID: 20967516
  23. Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals.
    J Biol Chem. 2007 Oct 12;282(41):30014-21 PMID: 17702743
  24. Self-eating and self-killing: crosstalk between autophagy and apoptosis.
    Nat Rev Mol Cell Biol. 2007 Sep;8(9):741-52 PMID: 17717517
  25. Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations.
    Biophys J. 2005 Feb;88(2):790-804 PMID: 15531631
  26. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy.
    Cell. 2004 Apr 30;117(3):399-412 PMID: 15109499
  27. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis.
    Nat Rev Mol Cell Biol. 2011 Jun;12(6):349-61 PMID: 21602905
  28. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker.
    Mol Biol Cell. 2004 Mar;15(3):1101-11 PMID: 14699058
  29. Dysfunction of mitochondria and sarcoplasmic reticulum in the pathogenesis of collagen VI muscular dystrophies.
    Ann N Y Acad Sci. 2008 Dec;1147:303-11 PMID: 19076452
  30. Regulation of autophagy by extracellular matrix glycoproteins in HeLa cells.
    Autophagy. 2011 Jan;7(1):27-39 PMID: 20980830
  31. Collagen VI related muscle disorders.
    J Med Genet. 2005 Sep;42(9):673-85 PMID: 16141002
  32. Contraction regulation of Akt in rat skeletal muscle.
    J Biol Chem. 2002 Apr 5;277(14):11910-7 PMID: 11809761
  33. Signalling and autophagy regulation in health, aging and disease.
    Mol Aspects Med. 2006 Oct-Dec;27(5-6):411-25 PMID: 16973212
  34. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration.
    Nat Med. 2010 Nov;16(11):1313-20 PMID: 21037586
  35. Extracellular matrix regulation of autophagy.
    Curr Opin Cell Biol. 2008 Oct;20(5):583-8 PMID: 18573652
  36. Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation.
    FASEB J. 2009 Nov;23(11):3896-905 PMID: 19661286
  37. From A to Z and back? Multicompartment proteins in the sarcomere.
    Trends Cell Biol. 2006 Jan;16(1):11-8 PMID: 16337382
  38. Interactions with LC3 and polyubiquitin chains link nbr1 to autophagic protein turnover.
    FEBS Lett. 2009 Jun 18;583(12):1846-52 PMID: 19427866
  39. Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy.
    J Biol Chem. 2010 Jun 18;285(25):19460-71 PMID: 20404331
Article Info
Journal
Autophagy
Abbr.
Autophagy
ISSN
1554-8635
Published
2011-12-00
Pages
1415-23
Language
English
Region
United States
NLM ID
101265188
PMCID
PMC3288016
Subset
IM
Grants
Telethon · GGP10225 · Italy
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]