Artículo

Pietrelli, A.; Di Nardo, M.; Masucci, A.; Brusco, A.; Basso, N.; Matkovic, L. "Lifelong Aerobic Exercise Reduces the Stress Response in Rats" (2018) Neuroscience. 376:94-107
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Abstract:

The aim of this study was to analyze the effects of lifelong aerobic exercise (AE) on the adaptive response of the stress system in rats. It is well known that hypothalamic–pituitary–adrenal axis (HPA) activity differs when triggered by voluntary or forced exercise models. Male Wistar rats belonging to exercise (E) or control (C) groups were subjected to chronic AE, and two cutoff points were established at 8 (middle age) and 18 months (old age). Behavioral, biochemical and histopathological studies were performed on the main components/targets of the stress system. AE increased adrenal sensitivity (AS), brain corticosterone (CORT) and corticotropin-releasing factor (CRF), but had no effect on the thymus, adrenal glands (AGs) weight or plasma CORT. In addition, AE exerted no effect on the sympathetic tone, but significantly reduced anxiety-related behavior and emotionality. Aging decreased AS and deregulated neuroendocrine feedback, leading to an anxiogenic state which was mitigated by AE. Histopathological and morphometric analysis of AGs showed no alterations in middle-aged rats but adrenal vacuolization in approximately 20% old rats. In conclusion, lifelong AE did not produce adverse effects related to a chronic stress state. On the contrary, while AE upregulated some components of the HPA axis, it generated an adaptive response to cumulative changes, possibly through different compensatory and/or super compensatory mechanisms, modulated by age. The long-term practice of AE had a strong positive impact on stress resilience so that it could be recommended as a complementary therapy in stress and depression disease. © 2018 IBRO

Registro:

Documento: Artículo
Título:Lifelong Aerobic Exercise Reduces the Stress Response in Rats
Autor:Pietrelli, A.; Di Nardo, M.; Masucci, A.; Brusco, A.; Basso, N.; Matkovic, L.
Filiación:Department of Basic Sciences Research, School of Health Sciences, University of Business and Social Sciences (UCES), Buenos Aires, Argentina
CONICET-Universidad de Buenos Aires, Instituto de Biología Celular y Neurociencia (IBCN), Buenos Aires, Argentina
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Biología Celular y Molecular, Buenos Aires, Argentina
Children's Hospital “Dr. Ricardo Gutierrez”, Department of Pathology, Buenos Aires, Argentina
Universidad de Buenos Aires, Facultad de Medicina, Departamento de Biología Celular, Histología, Embriología y Genética, Buenos Aires, Argentina
CONICET-Universidad de Buenos Aires, Instituto de Fisiopatología Cardiovascular (INFICA), Buenos Aires, Argentina
Palabras clave:aging; anxiety; exercise; HPA axis; stress; treadmill running; catecholamine; corticosterone; corticotropin releasing factor; catecholamine; corticosterone; adaptive behavior; adrenal gland; adrenal sensitivity; adult; aerobic exercise; age; aged; aging; animal cell; animal experiment; animal tissue; anxiety; anxiogenic state; Article; behavior; behavior assessment; biochemical analysis; brain function; cell vacuole; controlled study; corticosterone blood level; emotionality; histopathology; male; middle aged; neurofeedback; nonhuman; priority journal; psychological resilience; rat; stress; sympathetic tone; thymus; upregulation; animal; brain; mental stress; metabolism; pathology; pathophysiology; physiology; prevention and control; psychological resilience; psychology; randomization; running; Wistar rat; Adrenal Glands; Aging; Animals; Anxiety; Brain; Catecholamines; Corticosterone; Male; Random Allocation; Rats, Wistar; Resilience, Psychological; Running; Stress, Psychological
Año:2018
Volumen:376
Página de inicio:94
Página de fin:107
DOI: http://dx.doi.org/10.1016/j.neuroscience.2018.02.019
Título revista:Neuroscience
Título revista abreviado:Neuroscience
ISSN:03064522
CODEN:NRSCD
CAS:corticosterone, 50-22-6; corticotropin releasing factor, 9015-71-8, 178359-01-8, 79804-71-0, 86297-72-5, 86784-80-7; Catecholamines; Corticosterone
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03064522_v376_n_p94_Pietrelli

Referencias:

  • Beery, A.K., Kaufer, D., Stress, social behavior, and resilience: Insights from rodents (2015) Neurobiol Stress, 21, pp. 16-127
  • Belloni, A.S., Rebuffat, P., Malendowicz, L.K., Mazzocchi, G., Rocco, S., Nussdorfer, G.G., Age-related changes in the morphology and function of the zona glomerulosa of the rat adrenal cortex (1992) Tissue Cell, 24, pp. 835-842
  • Bompa, T.O., Haff, G., Periodization: theory and methodology of training (2009), 5th ed. Human Kinetics Champaign, IL, USA; Calabrese, E.J., Hormesis: a revolution in toxicology, risk assessment and medicine (2004) Embo Rep, 5, pp. 37-40
  • Campbell, J.E., Rakhshani, N., Fediuc, S., Bruni, S., Riddell, M.C., Voluntary wheel running initially increases adrenal sensitivity to adrenocorticotrophic hormone, which is attenuated with long-term training (2009) J Appl Physiol, 106, pp. 66-72
  • Campeau, S., Nyhuis, T.J., Sasse, S.K., Kryskow, E.M., Herlihy, L., Masini, C.V., Babb, J.A., Day, H.E., Hypothalamic–Pituitary–Adrenal Axis responses to low-Intensity stressors are reduced after voluntary wheel running in rats (2010) J Neuroendocrinol, 22, pp. 872-888
  • Campeau, S., Liberzon, I., Morilak, D., Ressler, K., Stress modulation of cognitive and affective processes (2011) Stress, 5, pp. 503-519
  • Costa, M.S., Ardais, A.P., Fioreze, G.T., Mioranzza, S., Botton, P.H., Portela, L.V., Souza, D.O., Porciúncula, L.O., Treadmill running frequency on anxiety and hippocampal adenosine receptors density in adult and middle-aged rats (2012) Prog Neuropsychoph, 36, pp. 198-204
  • Crawford, T.B., Law, W., The urinary excretion of adrenaline and noradrenaline by rats under various experimental conditions (1958) Br J Pharmacol Chemother, 1, pp. 35-43
  • Droste, S.K., Gensing, A., Ulbricht, S., Muller, M.B., Linthorst, A.C., Reul, J.M., Effects of long-term voluntary exercise on the mouse Hypothalamic-Pituitary-Adrenocortical Axis (2003) Neuroendocrinology, 77, pp. 388-405
  • Droste, S.K., Chandramohan, Y., Hill, L.E., Linthorst, A., Reul, J., Voluntary exercise impacts on the rat Hypothalamic-Pituitary-Adrenocortical Axis mainly at the adrenal level (2007) Neuroendocrinology, 86, pp. 26-37
  • Franklin, K.B.J., Paxinos, G., The mouse brain in stereotaxic coordinates (2007), 3rd. ed. Academic Press, Elsevier NY, USA; Fulford, A.J., Harbuz, M.S., An introduction to the HPA axis (2005) Handbook of stress and the brain, Chapter 1.3, 15, pp. 43-66. , Elsevier BV Oxford, UK
  • Fulk, L.J., Stock, H.S., Lynn, A., Marshall, J., Wilson, M.A., Hand, G.A., Chronic physical exercise reduces anxiety-like behavior in rats (2004) Int J Sports Med, 25, pp. 78-82
  • Garrido, P., Aging and Stress: Past hypotheses, present approaches and perspectives (2011) Aging Dis, 2, pp. 80-99
  • Gomez-Sanchez, C.E., Murry, B.A., Kem, D.C., Kaplan, N.M., Método de RIA (1975) Endocrinology, 96, pp. 796-798
  • Goosens, K.A., Sapolsky, R.M., Stress and glucocorticoid contributions to normal and pathological aging in brain aging: models, methods, and mechanisms, chapter 13 (2007), CRC Press Boca Raton,FL, USA; Gradari, S., Pallé, A., McGreevy, K.R., Fontán-Lozano, A., Trejo, J.L., Can exercise make you smarter, happier, and have more neurons? A Hormetic Perspective (2016) Front Neurosci, 10, pp. 1-16
  • Haak, D., Luu, H., Cho, J., Chen, M.J., Russo-Neustadt, A., Exercise reverses chronic stress-induced Bax oligomer formation in the cerebral cortex (2008) Neurosci Lett, 438, pp. 290-294
  • Heijnen, S., Hommel, B., Kibele, A., Colzato, L.S., Neuromodulation of aerobic exercise. A review (2016) Front Psychol, 6, pp. 1-6
  • Heinrichs, S.C., Behavioral consequences of altered corticotropin-releasing factor activation in brain: a functionalist view of affective neuroscience in Handbook of Stress and the Brain, vol. 15, part II, Chapter 2.3 (2005), pp. 155-178. , Elsevier BV Oxford, UK; Homberg, J.R., Molteni, R., Calabrese, F., Riva, M.A., The serotonin–BDNF duo: Developmental implications for the vulnerability to psychopathology (2014) Neurosci Biobehav Rev, 43, pp. 35-47
  • Janjua, M.Z., Khan, M.Y., Age related changes in the rat adrenal cortex (1992) J Pak Med Assoc, 42, pp. 89-94
  • Kaliman, P., Párrizas, M., Lalanza, J.F., Camins, A., Escorihuela, R.M., Pallàs, M., Neurophysiological and epigenetic effects of physical exercise on the aging process (2011) Ageing Res Rev, 10, pp. 475-486
  • Kenney, W.L., Wilmore, J.H., Costill, D.L., (2012), Fisiología del Deporte y el Ejercicio, 5ta. ed, Ed. Médica Panamericana. Madrid, España; Kosti, O., Raven, P.W., Renshaw, D., Hinson, J.P., Intra-adrenal mechanisms in the response to chronic stress: Investigation in a rat model of emotionality (2006) J Endocrinol, 189, pp. 211-218
  • Kulesskaya, N., Voikar, V., Assessment of mouse anxiety like behavior in the light-dark box and open-field arena: role of equipment and procedure (2014) Physiol Behav, 133, pp. 30-38
  • Leasure, J.L., Jones, M., Forced and voluntary exercise differentially affect brain and behavior (2008) Neuroscience, 156, pp. 456-465
  • Lepschy, M., Rettenbacher, S., Touma, C., Palme, R.G., Excretion of catecholamines in rats, mice and chicken (2008) J Comp Physiol B, 178, pp. 629-636
  • Levone, B.R., Cryan, J.F., O'Leary, O.F., Role of adult hippocampal neurogenesis in stress resilience (2015) Neurobiol Stress, 1, pp. 147-155
  • Lowry, C.A., Moore, F.L., Regulation of behavioral responses by corticotropin-releasing factor (2006) Gen Comp Endocrinol, 146, pp. 19-27
  • Lowry, C.A., Fox, J.H., Corticotropin-releasing factor-related peptides, serotonergic systems, and emotional behavior (2013) Front Neurosci, 7, pp. 1-16
  • Mammarella, N., Di Domenico, A., Palumbo, R., Fairfield, B., Noradrenergic modulation of emotional memory in aging (2016) Ageing Res Rev, 27, pp. 61-66
  • Martinowich, K., Lu, B., Interaction between BDNF and Serotonin: Role in Mood Disorders (2008) Neuropsychopharmacol, 33, pp. 73-83
  • Mattson, M.P., Hormesis and disease resistance: Activation of cellular stress response pathways (2007) Hum Exp Toxicol, 27, pp. 155-162
  • Mattson, M.P., Awareness of hormesis will enhance future research in basic and applied neuroscience (2008) Crit Rev Toxicol, 7, pp. 633-639
  • McEwen, B., Physiology and neurobiology of stress and adaptation: central role of the brain (2007) Physiol Rev, 87, pp. 873-904
  • McEwen, B., Gray, D.J., Nasca, C., Recognizing resilience: Learning from the effects of stress on the brain (2015) Neurobiol Stress, 1, pp. 1-11
  • Myers, B., McKlyeen, J.M., Herman, J.P., Neural regulation of the stress response: The many faces of feedback (2012) Cell Mol Neurobiol, 32, pp. 683-694
  • Nicolaides, N.C., Kyratzi, E., Lamprokostopoulou, A., Chrousos, G.P., Charmandari, E., Stress, the stress system and the role of glucocorticoids (2015) Neuroimmunomodulation, 22, pp. 6-19
  • Oliveira, L.C., Gomes, M.Z., Brandao, M.L., Influence of age on reactivity to diverse emotional challenges in low-and high-anxiety rats (2010) Int J Dev Neurosci, 1, pp. 77-83
  • Park, E., Chan, O., Li, Q., Kiraly, M., Matthews, S.G., Vranic, M., Riddell, M.C., Changes in basal hypothalamo- pituitary-adrenal activity during exercise training are centrally mediated (2005) Am J Physiol Regul Integr Comp Physiol, 289, pp. 1360-1371
  • Patki, G., Li, L., Allam, F., Solanki, N., Dao, A.T., Alkhadhi, K., Salim, S., Moderate treadmill exercise rescues anxiety and depression-like behavior as well as memory impairment in a rat model of posttraumatic stress disorder (2014) Physiol Behav, 130, pp. 47-53
  • Pietrelli, A., López-Costa, J.J., Goñi, R., Brusco, A., Basso, N., Aerobic exercise prevents age-dependent cognitive decline and reduces anxiety-related behaviors in middle-aged and old rats (2012) Neuroscience, 202, pp. 252-266
  • Pietrelli, A., López-Costa, J.J., Goñi, R., López, M.E., Brusco, A., Basso, N., Effects of moderate and chronic exercise on the nitrergic system and behavioral parameters in rats (2011) Brain Res, 1389, pp. 71-82
  • Rebuffat, P., Belloni, A.S., Rocco, S., Andreis, P.G., Neri, G., Malendowicz, L.K., Gottardo, G., Nussdorfer, G.G., The effects of ageing on the morphology and function of the zonae fasciculata and reticularis of the rat adrenal cortex (1992) Cell Tissue Res, 270, pp. 265-272
  • Sanchis-Gomar, F., García-Gimenez, J.L., Perez-Quilis, C., Gomez-Cabrera, M.C., Pallardo, F.V., Lippi, G., Physical exercise as an epigenetic modulator: Eustress, “the positive stress” as an effector of gene expression (2012) J Strength Cond Res, 26, pp. 3469-3472
  • Segar, T.M., Kasckow, J.W., Welge, J.A., Herman, J.P., Heterogeneity of neuroendocrine stress responses in aging rat strains (2009) Physiol Behav, 96, pp. 6-11
  • Soya, H., Mukai, A., Deocaris, C.C., Ohiwa, N., Chang, H., Nishijima, T., Fujikawa, T., Saito, T., Threshold-like pattern of neuronal activation in the hypothalamus during treadmill running: Establishment of a minimum running stress (MRS) rat model (2007) Neurosci Res, 58, pp. 341-348
  • Stanford, S.C., Adrenaline and noradrenaline: introduction (2013), John Wiley & Sons, Ltd Chichester; Stranahan, A.M., Lee, K., Mattson, M.P., Central mechanisms of HPA axis regulation by voluntary exercise (2008) Neuromol Med, 10, pp. 118-127
  • Stranahan, A.M., Zhou, Y., Martin, B., Maudsley, S., Pharmacomimetics of exercise: novel approaches for hippocampally-targeted neuroprotective agents (2010) Curr Med Chem, 16, pp. 4635-4668
  • Stranahan, A.M., Mattson, M.P., Recruiting adaptive cellular stress responses for successful brain aging (2014) Nat Rev Neurosci, 13, pp. 209-216
  • Taliaz, D., Loya, A., Gersner, R., Haramati, S., Chen, A., Zangen, A., Resilience to chronic stress is mediated by hippocampal brain-derived neurotrophic factor (2011) J Neurosci, 31, pp. 4475-4483
  • Ulrich-Lai, Y.M., Engeland, W.C., Sympatho-adrenal activity and hypothalamic-pituitary-adrenal axis regulation (2005) Handbook of stress and the brain, chapter 4.2, 15, pp. 419-435. , Elsevier BV Oxford, UK
  • Westermann, J., Hubl, W., Kaiser, N., Salewski, L., Simple, rapid and sensitive determination of epinephrine and norepinephrine in urine and plasma by non-competitive enzyme immunoassay, compared with HPLC method (2002) Clin Lab, 48, pp. 61-71
  • Yanagita, S., Amemiya, S., Suzuki, S., Kita, I., Effects of spontaneous and forced running on activation of hypothalamic corticotropin-releasing hormone neurons in rats (2007) Life Sci, 80, pp. 356-363
  • Zhou, J., Li, L., Tang, S., Cao, X., Li, Z., Li, W., Li, C., Zhang, X., Effects of serotonin depletion on the hippocampal GR/MR and BDNF expression during the stress adaptation (2008) Behav Brain Res, 195, pp. 129-138

Citas:

---------- APA ----------
Pietrelli, A., Di Nardo, M., Masucci, A., Brusco, A., Basso, N. & Matkovic, L. (2018) . Lifelong Aerobic Exercise Reduces the Stress Response in Rats. Neuroscience, 376, 94-107.
http://dx.doi.org/10.1016/j.neuroscience.2018.02.019
---------- CHICAGO ----------
Pietrelli, A., Di Nardo, M., Masucci, A., Brusco, A., Basso, N., Matkovic, L. "Lifelong Aerobic Exercise Reduces the Stress Response in Rats" . Neuroscience 376 (2018) : 94-107.
http://dx.doi.org/10.1016/j.neuroscience.2018.02.019
---------- MLA ----------
Pietrelli, A., Di Nardo, M., Masucci, A., Brusco, A., Basso, N., Matkovic, L. "Lifelong Aerobic Exercise Reduces the Stress Response in Rats" . Neuroscience, vol. 376, 2018, pp. 94-107.
http://dx.doi.org/10.1016/j.neuroscience.2018.02.019
---------- VANCOUVER ----------
Pietrelli, A., Di Nardo, M., Masucci, A., Brusco, A., Basso, N., Matkovic, L. Lifelong Aerobic Exercise Reduces the Stress Response in Rats. Neuroscience. 2018;376:94-107.
http://dx.doi.org/10.1016/j.neuroscience.2018.02.019