Long term running biphasically improves methylglyoxal-related metabolism, redox homeostasis and neurotrophic support within adult mouse brain cortex

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Falone, Stefano ^a,b   D'Alessandro, Antonella ^a   Mirabilio, Alessandro ^a   Petruccelli, Giacomo ^b   Cacchio, Marisa ^b   Di Ilio, Carmine ^b   Di Loreto, Silvia ^c   Amicarelli, Fernanda ^a  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

^c INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CARBONYL DERIVATIVE; CATALASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYDROXYACYLGLUTATHIONE HYDROLASE; LACTOYLGLUTATHIONE LYASE; METHYLGLYOXAL; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; REACTIVE OXYGEN METABOLITE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN CORTEX; CONTROLLED STUDY; ENZYME ACTIVITY; EXERCISE; FEMALE; FOOD INTAKE; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN CARBONYL CONTENT; PROTEIN CONTENT; PROTEIN EXPRESSION; RECEPTOR AFFINITY; TREADMILL EXERCISE; AGE; ANIMAL; HOMEOSTASIS; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; RUNNING; TIME;

MAMMALIA; MUS;

AGE FACTORS; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; HOMEOSTASIS; MICE; OXIDATION-REDUCTION; PHYSICAL CONDITIONING, ANIMAL; PYRUVALDEHYDE; REACTIVE OXYGEN SPECIES; RUNNING; TIME FACTORS;

EID: 84856719621     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031401     Document Type: Article

References (70)

1. Sohal RS, Weindruch R, (1996) Oxidative stress, caloric restriction, and aging. Science 273: 59-63.
2. Fulle S, Di Donna S, Puglielli C, Pietrangelo T, Beccafico S, et al. (2005) Age-dependent imbalance of the antioxidative system in human satellite cells. Exp Gerontol 40 (3): 189-197.
3. Fanò G, Mecocci P, Vecchiet J, Belia S, Fulle S, et al. (2001) Age and sex influence on oxidative damage and functional status in human skeletal muscle. J Muscle Res Cell Motil 22 (4): 345-351.
4. Frazzini V, Rockabrand E, Mocchegiani E, Sensi SL, (2006) Oxidative stress and brain aging: is zinc the link? Biogerontology 7: 307-314.
5. Sayre LM, Perry G, Smith MA, (2008) Oxidative stress and neurotoxicity. Chem Res Toxicol 21: 172-188.
6. Amicarelli F, Colafarina S, Cesare P, Aimola P, Di Ilio C, et al. (2001) Morphofunctional mitochondrial response to methylglyoxal toxicity in Bufo bufo embryos. Int J Biochem Cell Biol 33: 1129-1139.
7. Lüth HJ, Ogunlade V, Kuhla B, Kientsch-Engel R, Stahl P, et al. (2005) Age- and stage-dependent accumulation of advanced glycation end products in intracellular deposits in normal and Alzheimer's disease brains. Cereb Cortex 15: 211-220.
8. Hipkiss AR, (2006) On the mechanisms of ageing suppression by dietary restriction-is persistent glycolysis the problem? Mech Ageing Dev 127: 8-15.
9. Thornalley PJ, (2008) Protein and nucleotide damage by glyoxal and methylglyoxal in physiological systems-role in ageing and disease. Drug Metabol Drug Interact 23: 125-150.
10. Rabbani N, Thornalley PJ, (2008) The dicarbonyl proteome: proteins susceptible to dicarbonyl glycation at functional sites in health, aging, and disease. Ann N Y Acad Sci 1126: 124-127.
11. Amicarelli F, Colafarina S, Cattani F, Cimini A, Di Ilio C, et al. (2003) Scavenging system efficiency is crucial for cell resistance to ROS-mediated methylglyoxal injury. Free Radic Biol Med 35: 856-871.
12. Desai KM, Wu L, (2008) Free radical generation by methylglyoxal in tissues. Drug Metabol Drug Interact 23: 151-173.
13. Kuhla B, Lüth HJ, Haferburg D, Weick M, Reichenbach A, et al. (2006) Pathological effects of glyoxalase I inhibition in SH-SY5Y neuroblastoma cells. J Neurosci Res 83: 1591-1600.
14. Di Loreto S, Caracciolo V, Colafarina S, Sebastiani P, Gasbarri A, et al. (2004) Methylglyoxal induces oxidative stress-dependent cell injury and up-regulation of interleukin-1beta and nerve growth factor in cultured hippocampal neuronal cells. Brain Res 1006: 157-167.
15. Di Loreto S, Zimmitti V, Sebastiani P, Cervelli C, Falone S, et al. (2008) Methylglyoxal causes strong weakening of detoxifying capacity and apoptotic cell death in rat hippocampal neurons. Int J Biochem Cell Biol 40: 245-257.
16. Viña J, Gomez-Cabrera MC, Lloret A, Marquez R, Miñana JB, et al. (2000) Free radicals in exhaustive physical exercise: mechanism of production, and protection by antioxidants. IUBMB Life 50: 271-277.
17. Williamson J, Pahor M, (2010) Evidence Regarding the Benefits of Physical Exercise. Arch Intern Med 170: 124-125.
18. Gomez-Cabrera MC, Domenech E, Viña J, (2008) Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med 44: 126-131.
19. Berchtold NC, Castello N, Cotman CW, (2010) Exercise and time-dependent benefits to learning and memory. Neuroscience 167: 588-597.
20. Falone S, Mirabilio A, Pennelli A, Cacchio M, Di Baldassarre A, et al. (2010) Differential impact of acute bout of exercise on redox- and oxidative damage-related profiles between untrained subjects and amateur runners. Physiol Res 59: 953-961.
21. O'Callaghan RM, Griffin EW, Kelly AM, (2009) Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus 19: 1019-1029.
22. Muscari A, Giannoni C, Pierpaoli L, Berzigotti A, Maietta P, et al. (2010) Chronic endurance exercise training prevents aging-related cognitive decline in healthy older adults: a randomized controlled trial. Int J Geriatr Psychiatry 25: 1055-1064.
23. Rolland Y, Abellan van Kan G, Vellas B, (2010) Healthy brain aging: role of exercise and physical activity. Clin Geriatr Med 26: 75-87.
24. van Praag H, Shubert T, Zhao C, Gage FH, (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25: 8680-8685.
25. Vaynman SS, Ying Z, Yin D, Gomez-Pinilla F, (2006) Exercise differentially regulates synaptic proteins associated to the function of BDNF. Brain Res 1070: 124-130.
26. Griffin EW, Bechara RG, Birch AM, Kelly AM, (2009) Exercise enhances hippocampal-dependent learning in the rat: evidence for a BDNF-related mechanism. Hippocampus 19: 973-980.
27. Aguiar AS Jr, Castro AA, Moreira EL, Glaser V, Santos AR, et al. (2011) Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: Involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev In press.
28. Fouquet C, Petit GH, Auffret A, Gaillard E, Rovira C, et al. (2011) Early detection of age-related memory deficits in individual mice. Neurobiol Aging 32: 1881-1895.
29. Flurkey K, Currer JM, Harrison DE, (2007) The Mouse in Aging Research. In: Fox JG, Barthold SW, Davisson MT, Newcomer CE, Quimby FW, Smith AL, editors. The Mouse in Biomedical Research 2nd Edition Burlington American College Laboratory Animal Medicine (Elsevier) pp. 637-672.
30. Radak Z, Toldy A, Szabo Z, Siamilis S, Nyakas C, et al. (2006) The effects of training and detraining on memory, neurotrophins and oxidative stress markers in rat brain. Neurochem Int 49: 387-392.
31. Liu YF, Chen HI, Yu L, Kuo YM, Wu FS, et al. (2008) Upregulation of hippocampal TrkB and synaptotagmin is involved in treadmill exercise-enhanced aversive memory in mice. Neurobiol Learn Mem 90: 81-89.
32. Amicarelli F, Di Ilio C, Masciocco L, Bonfigli A, Zarivi O, et al. (1997) Aging and detoxifying enzymes responses to hypoxic or hyperoxic treatment. Mech Ageing Dev 97: 215-226.
33. Amicarelli F, Ragnelli AM, Aimola P, Bonfigli A, Colafarina S, et al. (1999) Age-dependent ultrastructural alterations and biochemical response of rat skeletal muscle after hypoxic or hyperoxic treatments. Biochim Biophys Acta 1453: 105-114.
34. Powers SK, Sen CK, (2000) Physiological antioxidants and exercise training. In: Sen CK, Packer L, Hanninen O, editors. Handbook of oxidants and antioxidants in exercise Amsterdam Elsevier Science B.V.
35. Desai KM, Chang T, Wang H, Banigesh A, Dhar A, et al. (2010) Oxidative stress and aging: is methylglyoxal the hidden enemy? Can J Physiol Pharmacol 88: 273-284.
36. Brownlee M, Vlassara H, Kooney A, Ulrich P, Cerami A, (1986) Aminoguanidine prevents diabetes-induced arterial wall protein cross-linking. Science 232: 1629-1632.
37. Miyata T, Inagi R, Asahi K, Yamada Y, Horie K, et al. (1998) Generation of protein carbonyls by glycoxidation and lipoxidation reactions with autoxidation products of ascorbic acid and polyunsaturated fatty acids. FEBS Lett 437: 24-28.
38. Nicolle MM, Gonzalez J, Sugaya K, Baskerville KA, Bryan D, et al. (2001) Signatures of hippocampal oxidative stress in aged spatial learning-impaired rodents. Neuroscience 107: 415-431.
39. Tongiorgi E, Righi M, Cattaneo A, (1997) Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17: 9492-9505.
40. Hof PR, Morrison JH, (2004) The aging brain: morphomolecular senescence of cortical circuits. Trends Neurosci 27: 607-613.
41. Radak Z, Chung HY, Goto S, (2008) Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 44: 153-159.
42. Somani SM, Ravi R, Rybak LP, (1995) Effect of exercise training on antioxidant system in brain regions of rat. Pharmacol Biochem Behav 50: 635-639.
43. Devi SA, Kiran TR, (2004) Regional responses in antioxidant system to exercise training and dietary vitamin E in aging rat brain. Neurobiol Aging 25: 501-508.
44. Ji LL, (2008) Modulation of skeletal muscle antioxidant defense by exercise: Role of redox signaling. Free Radic Biol Med 44: 142-152.
45. Toldy A, Stadler K, Sasvári M, Jakus J, Jung KJ, et al. (2005) The effect of exercise and nettle supplementation on oxidative stress markers in the rat brain. Brain Res Bull 65: 487-493.
46. Radak Z, Kaneko T, Tahara S, Nakamoto H, Pucsok J, et al. (2001) Regular exercise improves cognitive function and decreases oxidative damage in rat brain. Neurochem Int 38: 17-23.
47. Chao MV, Rajagopal R, Lee FS, (2006) Neurotrophin signaling in health and disease. Clin Sci (Lond) 110: 167-173.
48. Gomez-Pinilla F, (2008) The influences of diet and exercise on mental health through hormesis. Ageing Res Rev 7: 49-62.
49. Greenwood BN, Strong PV, Foley TE, Fleshner M, (2009) A behavioral analysis of the impact of voluntary physical activity on hippocampus-dependent contextual conditioning. Hippocampus 19: 988-1001.
50. Hopkins ME, Bucci DJ, (2010) BDNF expression in perirhinal cortex is associated with exercise-induced improvement in object recognition memory. Neurobiol Learn Mem 94: 278-284.
51. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, et al. (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A; 108: 3017-3022.
52. Mattson MP, Lovell MA, Furukawa K, Markesbery WR, (1995) Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular Ca2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem 65: 1740-1751.
53. Tatone C, Amicarelli F, Carbone MC, Monteleone P, Caserta D, et al. (2008) Cellular and molecular aspects of ovarian follicle ageing. Hum Reprod Update 14: 131-142.
54. Iwata E, Asanuma M, Nishibayashi S, Kondo Y, Ogawa N, (1997) Different effects of oxidative stress on activation of transcription factors in primary cultured rat neuronal and glial cells. Brain Res Mol Brain Res 50: 213-220.
55. Zou J, Crews F, (2006) CREB and NF-kappaB transcription factors regulate sensitivity to excitotoxic and oxidative stress induced neuronal cell death. Cell Mol Neurobiol 26: 385-405.
56. Macri MA, D'Alessandro N, Di Giulio C, Di Iorio P, Di Luzio S, et al. (2010) Region-specific effects on brain metabolites of hypoxia and hyperoxia overlaid on cerebral ischemia in young and old rats: a quantitative proton magnetic resonance spectroscopy study. J Biomed Sci 17: 14.
57. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
58. Sun M, Zigman S, (1978) An improved spectrophotometric assay for superoxide dismutase based on epinephrine autoxidation. Anal Biochem 90: 81-89.
59. Aebi H, (1984) Catalase in vitro. Methods Enzymol 105: 121-126.
60. Paglia DE, Valentine WN, (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70: 158-169.
61. Di Ilio C, Polidoro G, Arduini A, Muccini A, Federici G, (1983) Glutathione peroxidase, glutathione reductase, glutathione S-transferase, and gamma-glutamyltranspeptidase activities in the human early pregnancy placenta. Biochem Med 29: 143-148.
62. Mannervik B, Aronsson AC, Marmstål E, Tibbelin G, (1981) Glyoxalase I (rat liver). Methods Enzymol 77: 297-301.
63. Guha MK, Vander Jagt DL, Creighton DJ, (1988) Diffusion-dependent rates for the hydrolysis reaction catalyzed by glyoxalase II from rat erythrocytes. Biochemistry 27: 8818-8822.
64. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85.
65. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
66. Towbin H, Staehelin T, Gordon J, (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
67. Aldridge GM, Podrebarac DM, Greenough WT, Weiler IJ, (2008) The use of total protein stains as loading controls: an alternative to high-abundance single-protein controls in semi-quantitative immunoblotting. J Neurosci Methods 172: 250-254.
68. Silva-Adaya D, Pérez-De La Cruz V, Herrera-Mundo MN, Mendoza-Macedo K, Villeda-Hernández J, et al. (2008) Excitotoxic damage, disrupted energy metabolism, and oxidative stress in the rat brain: antioxidant and neuroprotective effects of L-carnitine. J Neurochem 105: 677-689.
69. Levine RL, Williams JA, Stadtman ER, Shacter E, (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233: 346-357.
70. Baker MA, Cerniglia GJ, Zaman A, (1990) Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 190: 360-365.