Macroautophagic process was differentially modulated by long-term moderate exercise in rat brain and peripheral tissues

Journal of Physiology and Pharmacology

Volumn 65, Issue 2, 2014, Pages 229-239

  Bayod, Sergi ^a,b   Del Valle, J ^a,b,c   Pelegri, C ^a,b   Vilaplana, J ^a,b   Canudas, A M ^a,b   Camins, A ^a,b   Jimenez, A ^a,b   Sanchez Roige, S ^c   Lalanza, J F ^c   Escorihuela, R M ^c   Pallas, M ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Autophagy; Cortex; Heart; Hippocampus; Liver; Long term treadmill exercise; Lysosome; Skeletal muscle

Indexed keywords

BECLIN 1; BETA ACTIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; PROTEIN P62; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, RAT; HEAT SHOCK PROTEIN; LAMP1 PROTEIN, RAT; LC3 PROTEIN, RAT; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MTOR PROTEIN, RAT; SQSTM1 PROTEIN, RAT; TARGET OF RAPAMYCIN KINASE;

ADULT; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN CORTEX; CONTROLLED STUDY; ENDURANCE TRAINING; EXERCISE; HEART; HIPPOCAMPUS; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; LIVER; MACROAUTOPHAGY; MALE; METABOLISM; NERVOUS TISSUE; NONHUMAN; RAT; SITTING; SKELETAL MUSCLE; TREADMILL EXERCISE; WESTERN BLOTTING; ANIMAL; AUTOPHAGY; HEART MUSCLE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CEREBRAL CORTEX; HEAT-SHOCK PROTEINS; HIPPOCAMPUS; LIVER; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MUSCLE, SKELETAL; MYOCARDIUM; PHYSICAL CONDITIONING, ANIMAL; RATS, SPRAGUE-DAWLEY; TOR SERINE-THREONINE KINASES;

EID: 84899657642     PISSN: 08675910     EISSN: 18991505     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Garber CE, Blissmer B, Deschenes MR, et al. American College of Sports Medicine. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc 2011; 43: 1334-1359.
2. Gremeaux V, Gayda M, Lepers R, Sosner P, Juneau M, Nigam A. Exercise and longevity. Maturitas 2012; 73: 312-317.
3. Ahlskog JE, Geda YE, Graff-Radford NR, Petersen RC. Physical exercise as a preventive or disease-modifying treatment of dementia and brain aging. Mayo Clin Proc 2011; 86: 876-884.
4. Griffin EW, Mullally S, Foley C, Warmington SA, O'Mara SM, Kelly AM. Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav 2011; 104: 934-941.
5. Nelson ME, Rejeski WJ, Blair SN, et al. American College of Sports Medicine; American Heart Association. Physical activity and public health in older adults: recommendation from the American College of Sports Medicine and the American Heart Association. Circulation 2007; 116: 1094-1105.
6. van Praag H. Exercise and the brain: something to chew on. Trends Neurosci 2009; 32: 283-290.
7. Boveris A, Navarro A. Systemic and mitochondrial adaptive responses to moderate exercise in rodents. Free Radic Biol Med 2008; 44: 224-229.
8. Salminen A, Kaarniranta K. Regulation of the aging process by autophagy. Trends Mol Med 2009; 15: 217-224.
9. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147: 728-741.
10. Parzych KR, Klionsky DJ. An overview of autophagy: morphology, mechanism, and regulation. Antioxid Redox Signal 2013; 20: 460-473.
11. Korolchuk VI, Menzies FM, Rubinsztein DC. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett 2010; 584: 1393-1398.
12. Komatsu M, Ichimura Y. Selective autophagy regulates various cellular functions. Genes Cells 2010; 15: 923-933.
13. Rezzani R, Stacchiotti A, Rodella LF. Morphological and biochemical studies on aging and autophagy. Ageing Res Rev 2012; 11: 10-31.
14. Choi AM, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med 2013; 368: 651-662.
15. Ravikumar B, Vacher C, Berger Z, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004; 36: 585-595.
16. Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC. Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem 2007; 282: 5641-5652.
17. Dehay B, Bove J, Rodriguez-Muela N, et al. Pathogenic lysosomal depletion in Parkinson's disease. J Neurosci 2010; 30: 12535-12544.
18. Spilman P, Podlutskaya N, Hart MJ, et al. Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One 2010; 5: e9979.
19. Lee IH, Cao L, Mostoslavsky R, et al. A role for the NADdependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci USA 2008; 105: 3374-3379.
20. Wu Y, Li X, Zhu JX, et al. Resveratrol-activated AMPK/SIRT1/autophagy in cellular models of Parkinson's disease. Neurosignals 2011; 19: 163-174.
21. Salminen A, Kaarniranta K. AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res Rev 2012; 11: 230-241.
22. Bayod S, Del Valle J, Canudas AM, et al. Long-term treadmill exercise induces neuroprotective molecular changes in rat brain. J Appl Physiol 2011; 111: 1380-1390.
23. Bayod S, Del Valle J, Lalanza JF, et al. Long-term physical exercise induces changes in sirtuin 1 pathway and oxidative parameters in adult rat tissues. Exp Gerontol 2012; 47: 925-935.
24. He C, Bassik MC, Moresi V, et al. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 2012; 481: 511-515.
25. He C, Sumpter R, Jr, Levine B. Exercise induces autophagy in peripheral tissues and in the brain. Autophagy 2012; 8: 1548-1551.
26. Kim YA, Kim YS, Oh SL, Kim HJ, Song W. Autophagic response to exercise training in skeletal muscle with age. J Physiol Biochem 2013; 69: 697-705.
27. Lira VA, Okutsu M, Zhang M, et al. Autophagy is required for exercise training-induced skeletal muscle adaptation and improvement of physical performance. FASEB J 2013; 27: 4184-4193.
28. Lalanza JF, Sanchez-Roige S, Gagliano H, et al. Physiological and behavioural consequences of long-term moderate treadmill exercise. Psychoneuroendocrinology 2012; 37: 1745-1754.
29. Tanida I. Autophagosome formation and molecular mechanism of autophagy. Antioxid Redox Signal 2011; 14: 2201-2214.
30. Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
31. Huynh KK, Eskelinen EL, Scott CC, Malevanets A, Saftig P, Grinstein S. LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J 2007; 26: 313-324.
32. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011; 7: 279-296.
33. Bjorkoy G, Lamark T, Brech A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005; 171: 603-614.
34. Komatsu M, Waguri S, Koike M, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131: 1149-1163.
35. Ramesh Babu J, Lamar Seibenhener M, Peng J, et al. Genetic inactivation of p62 leads to accumulation of hyperphosphorylated tau and neurodegeneration. J Neurochem 2008; 106: 107-120.
36. Bjorkoy G, Lamark T, Pankiv S, Overvatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009; 452: 181-197.
37. O'Callaghan RM, Griffin EW, Kelly AM. Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus 2009; 19: 1019-1029.
38. Jamart C, Francaux M, Millet GY, Deldicque L, Frere D, Feasson L. Modulation of autophagy and ubiquitinproteasome pathways during ultra-endurance running. J Appl Physiol 2012; 112: 1529-1537.
39. Ghosh HS, McBurney M, Robbins PD. SIRT1 negatively regulates the mammalian target of rapamycin. PLoS One 2010; 5: e9199.
40. Morselli E, Maiuri MC, Markaki M, et al. Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis 2010; 1: e10.
41. Harrison DE, Strong R, Sharp ZD, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 2009; 460: 392-395.
42. Bove J, Martinez-Vicente M, Vila M. Fighting neurodegeneration with rapamycin: mechanistic insights. Nat Rev Neurosci 2011; 12: 437-452.
43. Sardiello M, Palmieri M, di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science 2009; 325: 473-477.
44. Maiuri MC, Criollo A, Tasdemir E, et al. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 2007; 3: 374-376.
45. Wong E, Cuervo AM. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 2010; 13: 805-811.
46. Yamamoto A, Simonsen A. The elimination of accumulated and aggregated proteins: a role for aggrephagy in neurodegeneration. Neurobiol Dis 2011; 43: 17-28.
47. Caballero B, Coto-Montes A. An insight into the role of autophagy in cell responses in the aging and neurodegenerative brain. Histol Histopathol 2012; 27: 263-275.
48. Jamart C, Benoit N, Raymackers JM, Kim HJ, Kim CK, Francaux M. Autophagy-related and autophagy-regulatory genes are induced in human muscle after ultraendurance exercise. Eur J Appl Physiol 2012; 112: 3173-3177.
49. Ogura Y, Iemitsu M, Naito H, et al. Single bout of running exercise changes LC3-II expression in rat cardiac muscle. Biochem Biophys Res Commun 2011; 414: 756-760.
50. Grumati P, Coletto L, Schiavinato A, et al. Physical exercise stimulates autophagy in normal skeletal muscles but is detrimental for collagen VI-deficient muscles. Autophagy 2011; 7: 1415-1423.
51. Rodriguez A, Duran A, Selloum M, et al. Mature-onset obesity and insulin resistance in mice deficient in the signaling adapter p62. Cell Metab 2006; 3: 211-222.
52. Moscat J, Diaz-Meco MT. Feedback on fat: p62-mTORC1-autophagy connections. Cell 2011; 147: 724-727.
53. Yecies JL, Manning BD. Transcriptional control of cellular metabolism by mTOR signaling. Cancer Res 2011; 71: 2815-2820.
54. Geetha T, Zheng C, Vishwaprakash N, Broderick TL, Babu JR. Sequestosome 1/p62, a scaffolding protein, is a newly identified partner of IRS-1 protein. J Biol Chem 2012; 287: 29672-29678.
55. Zoladz JA, Pilc A. The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. J Physiol Pharmacol 2010; 61: 533-541.
56. Sadowska-Krepa E, Klapcinska B, Jagsz S, et al. Diverging oxidative damage and heat shock protein 72 responses to endurance training and chronic testosterone propionate treatment in three striated muscle types of adolescent male rats. J Physiol Pharmacol 2013; 64: 639-647.
57. Sakr HF. Modulation of metabolic and cardiac dysfunctions by swimming in overweight rats on a high cholesterol and fructose diet: possible role of adiponectin. J Physiol Pharmacol 2013; 64: 231-240.