Enhancement of Hippocampal Plasticity by Physical Exercise as a Polypill for Stress and Depression: A Review

Author(s): Ang Li , Suk-yu Yau , Sergio Machado , Pingjie Wang , Ti-Fei Yuan* , Kwok-Fai So* .

Journal Name: CNS & Neurological Disorders - Drug Targets

Volume 18 , Issue 4 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Generation of newborn neurons that form functional synaptic connections in the dentate gyrus of adult mammals, known as adult hippocampal neurogenesis, has been suggested to play critical roles in regulating mood, as well as certain forms of hippocampus-dependent learning and memory. Environmental stress suppresses structural plasticity including adult neurogenesis and dendritic remodeling in the hippocampus, whereas physical exercise exerts opposite effects. Here, we review recent discoveries on the potential mechanisms concerning how physical exercise mitigates the stressrelated depressive disorders, with a focus on the perspective of modulation on hippocampal neurogenesis, dendritic remodeling and synaptic plasticity. Unmasking such mechanisms may help devise new drugs in the future for treating neuropsychiatric disorders involving impaired neural plasticity.

Keywords: Physical exercise, stress, depression, hippocampal neurogenesis, dendritic remodeling, synaptic plasticity.

[1]
Altman J. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 1963; 145: 573-91.
[2]
Altman J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 1969; 137(4): 433-57.
[3]
Saxe MD. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 2006; 103(46): 17501-6.
[4]
Deng W. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 2009; 29(43): pp. 13532-.
[5]
Snyder JS. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 2011; 476(7361): 458-61.
[6]
Santarelli L. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301(5634): 805-9.
[7]
Surget A. Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol Psychiatry 2008; 64(4): 293-301.
[8]
Yau SY. Hippocampal neurogenesis and dendritic plasticity support running-improved spatial learning and depression-like behaviour in stressed rats. PLoS One 2011; 6(9)e24263
[9]
Bjornebekk A, Mathe AA, Brene S. The antidepressant effect of running is associated with increased hippocampal cell proliferation. Int J Neuropsychopharmacol 2005; 8(3): 357-68.
[10]
van Praag HG. Kempermann and FH. Gage Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999; 2(3): 266-70.
[11]
Eadie BD, Redila VA, Christie BR. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation dendritic complexity and spine density. J Comp Neurol 2005; 486(1): 39-47.
[12]
Redila VA, Christie BR. Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 2006; 137(4): 1299-307.
[13]
van Praag H. Running enhances neurogenesis learning and long-term potentiation in mice. Proc Natl Acad Sci USA 1999; 96(23): 13427-31.
[14]
Gould E. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 1992; 12(9): 3642-50.
[15]
Pavlides CY, Watanabe B, McEwen S. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 1993; 3(2): 183-92.
[16]
Woolley CSE. Gould and B.S. McEwen Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 1990; 531(1-2): 225-31.
[17]
Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005; 28: p 223-250.
[18]
McKay R. Stem cells in the central nervous system. Science 1997; 276(5309): 66-71.
[19]
Weiner LP. Definitions and criteria for stem cells. Methods Mol Biol 2008; 438: 3-8.
[20]
Lie DC. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 2004; 44: 399-421.
[21]
Andersen P. The hippocampus book 2006 New York: Oxford University Press 832.
[22]
Shepherd GM. The synaptic organization of the brain 5th ed 2004 New York: Oxford University Press 719.
[23]
Schmidt-Hieber CP, Jonas J. Bischofberger enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004; 429(6988): 184-7.
[24]
Dhaliwal J, Lagace DC. Visualization and genetic manipulation of adult neurogenesis using transgenic mice. Eur J Neurosci 2011; 33(6): 1025-36.
[25]
Fukuda S. Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 2003; 23(28): 9357-66.
[26]
Suh H. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 2007; 1(5): 515-28.
[27]
Tozuka Y. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005; 47(6): 803-15.
[28]
Filippov V. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 2003; 23(3): 373-82.
[29]
Bonaguidi MA. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 2011; 145(7): 1142-55.
[30]
Bonaguidi MA. A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus. Curr Opin Neurobiol 2012; 22(5): 754-61.
[31]
Ming GL, Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011; 70(4): 687-702.
[32]
Esposito MS. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 2005; 25(44): 10074-86.
[33]
Hastings NB, Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 1999; 413(1): 146-54.
[34]
van Praag H. Functional neurogenesis in the adult hippocampus. Nature 2002; 415(6875): 1030-4.
[35]
Bhattacharyya BJ. The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. J Neurosci 2008; 28(26): 6720-30.
[36]
Spalding KL. Retrospective birth dating of cells in humans. Cell 2005; 122(1): 133-43.
[37]
Cameron HA, McKay RD. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001; 435(4): 406-17.
[38]
Sierra A. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010; 7(4): 483-95.
[39]
Tashiro A. NMDA-receptor-mediated cell-specific integration of new neurons in adult dentate gyrus. Nature 2006; 442(7105): 929-33.
[40]
Dayer AG. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 2003; 460(4): 563-72.
[41]
Kempermann G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004; 27(8): 447-52.
[42]
Mirescu CE. Gould Stress and adult neurogenesis. Hippocampus 2006; 16(3): 233-8.
[43]
Lu L. Modification of hippocampal neurogenesis and neuroplasticity by social environments. Exp Neurol 2003; 183(2): 600-9.
[44]
Tanapat P. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 2001; 437(4): 496-504.
[45]
Pham K. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 2003; 17(4): 879-86.
[46]
Malberg JE. Duman Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 2003; 28(9): 1562-71.
[47]
Gould E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 1998; 95(6): 3168-71.
[48]
Wong EY. and J. Herbert roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur J Neurosci 2005; 22(4): 785-92.
[49]
Wong EY, Herbert J. Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 2006; 137(1): 83-92.
[50]
Wong EY, Herbert J. The corticoid environment: a determining factor for neural progenitors’ survival in the adult hippocampus. Eur J Neurosci 2004; 20(10): 2491-8.
[51]
McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999; 22: 105-22.
[52]
Garcia A. Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 2004; 3(6): 363-71.
[53]
Kirschbaum C. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci 1996; 58(17): 1475-83.
[54]
Sapolsky RM. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 2000; 57(10): 925-35.
[55]
Gould EC, Woolley S, McEwen BS. Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. J Comp Neurol 1991; 313(3): 479-85.
[56]
Cameron HA, Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994; 61(2): 203-9.
[57]
Alonso R. Blockade of CRF(1) or V(1b) receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression. Mol Psychiatry 2004; 9(3): 278-86.
[58]
Cameron HA, McKay RD. Restoring production of hippocampal neurons in old age. Nat Neurosci 1999; 2(10): 894-7.
[59]
Mirescu CJ, Peters D, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004; 7(8): 841-6.
[60]
Heine VM. Increased P27KIP1 protein expression in the dentate gyrus of chronically stressed rats indicates G1 arrest involvement. Neuroscience 2004; 129(3): 593-601.
[61]
Abraham I. Corticosterone peak is responsible for stress-induced elevation of glutamate in the hippocampus. Stress 1998; 2(3): 171-81.
[62]
Cameron HA, McEwen BS, Gould E. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 1995; 15(6): 4687-92.
[63]
Nacher J. NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol Aging 2003; 24(2): 273-84.
[64]
Adlard PA, Cotman CW. Voluntary exercise protects against stress-induced decreases in brain-derived neurotrophic factor protein expression. Neuroscience 2004; 124(4): 985-92.
[65]
Vaynman SZ, Ying F. Gomez-Pinilla Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004; 20(10): 2580-90.
[66]
Watanabe Y, Gould E, McEwen BS. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 1992; 588(2): 341-5.
[67]
Magarinos AM. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 1996; 16(10): 3534-40.
[68]
McKittrick CR. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 2000; 36(2): 85-94.
[69]
Foy MR. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol 1987; 48(1): 138-49.
[70]
Bodnoff SR. Enduring effects of chronic corticosterone treatment on spatial learning synaptic plasticity and hippocampal neuropathology in young and mid-aged rats. J Neurosci 1995; 15(1 Pt 1): 61-9.
[71]
Alfarez DN, Joels M, Krugers HJ. Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur J Neurosci 2003; 17(9): 1928-34.
[72]
Wang S, Scott BW, Wojtowicz JM. Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 2000; 42(2): 248-57.
[73]
Snyder JS, Kee N, Wojtowicz N. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 2001; 85(6): 2423-31.
[74]
Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997; 386(6624): 493-5.
[75]
Kronenberg G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 2003; 467(4): 455-63.
[76]
Gregoire CA. Untangling the influences of voluntary running environmental complexity social housing and stress on adult hippocampal neurogenesis. PLoS One 2014; 9(1)e86237
[77]
Kempermann G, Gage FH. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition but not probe trial performance in the water maze task. Eur J Neurosci 2002; 16(1): 129-36.
[78]
Snyder JS. The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus 2009; 19(10): 898-906.
[79]
Muotri AR. Environmental influence on L1 retrotransposons in the adult hippocampus. Hippocampus 2009; 19(10): 1002-7.
[80]
van Praag H. Neurogenesis and exercise: past and future directions. Neuromolecular Med 2008; 10(2): 128-40.
[81]
van Praag H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005; 25(38): 8680-5.
[82]
Merkley CM. Homeostatic regulation of adult hippocampal neurogenesis in aging rats: long-term effects of early exercise. Front Neurosci 2014; 8: 174.
[83]
Trejo JL, Llorens-Martin MV, Torres-Aleman I. The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol Cell Neurosci 2008; 37(2): 402-11.
[84]
Anderson BJ. Exercise influences spatial learning in the radial arm maze. Physiol Behav 2000; 70(5): 425-9.
[85]
Fordyce DE, Farrar RP. Physical activity effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behav Brain Res 1991; 43(2): 115-23.
[86]
Bick-Sander A. Running in pregnancy transiently increases postnatal hippocampal neurogenesis in the offspring. Proc Natl Acad Sci USA 2006; 103(10): 3852-7.
[87]
Ma DK. Epigenetic choreographers of neurogenesis in the adult mammalian brain. Nat Neurosci 2010; 13(11): 1338-44.
[88]
Cotman CW, Berchtold N, Christie LA. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 2007; 30(9): 464-72.
[89]
Neeper SA. Exercise and brain neurotrophins. Nature 1995; 373(6510): 109.
[90]
Neeper SA. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 1996; 726(1-2): 49-56.
[91]
Carro E. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 2000; 20(8): 2926-33.
[92]
Fabel K. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 2003; 18(10): 2803-12.
[93]
Trejo JL, Carro E, Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 2001; 21(5): 1628-34.
[94]
Yau SY. Physical exercise-induced hippocampal neurogenesis and antidepressant effects are mediated by the adipocyte hormone adiponectin. Proc Natl Acad Sci USA 2014; 111(44): 15810-5.
[95]
Stranahan AM, Khalil D, Gould E. Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus 2007; 17(11): 1017-22.
[96]
Glasper ER. Blockade of insulin-like growth factor-I has complex effects on structural plasticity in the hippocampus. Hippocampus 2010; 20(6): 706-12.
[97]
Lin TW. Different types of exercise induce differential effects on neuronal adaptations and memory performance. Neurobiol Learn Mem 2012; 97(1): 140-7.
[98]
Zhao C. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006; 26(1): 3-11.
[99]
Choi SH. Regulation of hippocampal progenitor cell survival proliferation and dendritic development by BDNF. Mol Neurodegener 2009; 4: 52.
[100]
Vasuta C. Effects of exercise on NMDA receptor subunit contributions to bidirectional synaptic plasticity in the mouse dentate gyrus. Hippocampus 2007; 17(12): 1201-8.
[101]
Farmer J. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004; 124(1): 71-9.
[102]
O’Callaghan RM, Griffin EW, Kelly AM. Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus 2009; 19(10): 1019-29.
[103]
Ding Q. Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 2006; 140(3): 823-33.
[104]
Meltzer LA, Yabaluri R, Deisseroth K. A role for circuit homeostasis in adult neurogenesis. Trends Neurosci 2005; 28(12): 653-60.
[105]
Campbell S. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am J Psychiatry 2004; 161(4): 598-607.
[106]
Videbech P, Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry 2004; 161(11): 1957-66.
[107]
MacQueen GM. Course of illness hippocampal function and hippocampal volume in major depression. Proc Natl Acad Sci USA 2003; 100(3): 1387-92.
[108]
Malberg JE. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 2000; 20(24): 9104-10.
[109]
Perera TD. Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J Neurosci 2007; 27(18): 4894-901.
[110]
Madsen TM. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 2000; 47(12): 1043-9.
[111]
Ngwenya LB, Peters A, Rosene DL. Maturational sequence of newly generated neurons in the dentate gyrus of the young adult rhesus monkey. J Comp Neurol 2006; 498(2): 204-16.
[112]
Airan RD. High-speed imaging reveals neurophysiological links to behavior in an animal model of depression. Science 2007; 317(5839): 819-23.
[113]
Gould E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997; 17(7): 2492-8.
[114]
Murray F, Smith DW, Hutson E. Chronic low dose corticosterone exposure decreased hippocampal cell proliferation volume and induced anxiety and depression like behaviours in mice. Eur J Pharmacol 2008; 583(1): 115-27.
[115]
Yau SY. Effects of voluntary running on plasma levels of neurotrophins hippocampal cell proliferation and learning and memory in stressed rats. Neuroscience 2012; 222: 289-301.
[116]
Yau SY. Sustained running in rats administered corticosterone prevents the development of depressive behaviors and enhances hippocampal neurogenesis and synaptic plasticity without increasing neurotrophic factor levels. Cell Transplant 2014; 23(4-5): 481-92.
[117]
DeCarolis NA, Eisch AJ. Hippocampal neurogenesis as a target for the treatment of mental illness: a critical evaluation. Neuropharmacology 2010; 58(6): 884-93.
[118]
Droste SK. Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology 2003; 144(7): 3012-23.
[119]
Makatsori A. Voluntary wheel running modulates glutamate receptor subunit gene expression and stress hormone release in Lewis rats. Psychoneuroendocrinology 2003; 28(5): 702-14.
[120]
Stranahan AM, Khalil D, Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 2006; 9(4): 526-33.
[121]
Zheng H. Beneficial effects of exercise and its molecular mechanisms on depression in rats. Behav Brain Res 2006; 168(1): 47-55.
[122]
Fediuc S, Campbell JE, Riddell MC. Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague-Dawley rats. J Appl Physiol 2006; 100(6): 1867-75.
[123]
Chang YT. Glucocorticoid signaling and exercise-induced downregulation of the mineralocorticoid receptor in the induction of adult mouse dentate neurogenesis by treadmill running. Psychoneuroendocrinology 2008; 33(9): 1173-82.
[124]
Morgan WP. Psychological monitoring of overtraining and staleness. Br J Sports Med 1987; 21(3): 107-14.
[125]
McKenzie DC. The effect of repeat exercise on pulmonary diffusing capacity and EIH in trained athletes. Med Sci Sports Exerc 1999; 31(1): 99-104.
[126]
Naylor AS. Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J Neurophysiol 2005; 93(5): 2406-14.
[127]
Shirayama Y. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 2002; 22(8): 3251-61.
[128]
Schaaf MJ. Corticosterone effects on BDNF mRNA expression in the rat hippocampus during morris water maze training. Stress 1999; 3(2): 173-83.
[129]
Vellucci SV, Parrott RF, Mimmack ML. Down-regulation of BDNF mRNA with no effect on trkB or glucocorticoid receptor m RNAs in the porcine hippocampus after acute dexamethasone treatment. Res Vet Sci 2001; 70(2): 157-62.
[130]
Duman CH. Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res 2008; 1199: 148-58.
[131]
Taliaz D. Resilience to chronic stress is mediated by hippocampal brain-derived neurotrophic factor. J Neurosci 2011; 31(12): 4475-83.
[132]
Kiuchi TH, Lee T. Mikami Regular exercise cures depression-like behavior via VEGF-Flk-1 signaling in chronically stressed mice. Neuroscience 2012; 207: 208-17.
[133]
Herskovits AZ, Guarente L. SIRT1 in Neurodevelopment and Brain Senescence. Neuron 2014; 81(3): 471-83.
[134]
Gao J. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 2010; 466: 1105.
[135]
Michán S. SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci 2010; 30(29): 9695.
[136]
Ng FL, Wijaya BL. SIRT1 in the brain—connections with aging-associated disorders and lifespan. Front Cell Neurosci 2015; 9: 64.
[137]
Corpas R. SIRT1 overexpression in mouse hippocampus induces cognitive enhancement through proteostatic and neurotrophic mechanisms. Mol Neurobiol 2017; 54(7): 5604-19.
[138]
Sugino T. Protein deacetylase SIRT1 in the cytoplasm promotes nerve growth factor-induced neurite outgrowth in PC12 cells. FEBS Lett 2010; 584(13): 2821-6.
[139]
Codocedo JF. SIRT1 Regulates dendritic development in hippocampal neurons. PLoS One 2012; 7(10)e47073
[140]
Li XH. Sirt1 promotes axonogenesis by deacetylation of Akt and inactivation of GSK3. Mol Neurobiol 2013; 48(3): 490-9.
[141]
Prozorovski T. Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol 2008; 10: 385.
[142]
Rafalski VA. Expansion of oligodendrocyte progenitor cells following SIRT1 inactivation in the adult brain. Nat Cell Biol 2013; 15: 614.
[143]
Ma CY. SIRT1 suppresses self-renewal of adult hippocampal neural stem cells. Development 2014; 141(24): 4697.
[144]
Asher G. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 2008; 134(2): 317-28.
[145]
Chang HC, Guarente L. SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell 2013; 153(7): 1448-60.
[146]
Jeong H. Sirt1 mediates neuroprotection from mutant huntingtin by activation of the TORC1 and CREB transcriptional pathway. Nat Med 2011; 18: 159.
[147]
Qin W. Neuronal SIRT1 activation as a novel mechanism underlying the prevention of alzheimer disease amyloid neuropathology by calorie restriction. J Biol Chem 2006; 281(31): 21745-54.
[148]
Donmez G. SIRT1 protects against α-Synuclein aggregation by activating molecular chaperones. J Neurosci 2012; 32(1): 124.
[149]
Kim D. SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer’s disease and amyotrophic lateral sclerosis. J EMBO 2007; 26(13): 3169.
[150]
Abe-Higuchi N. Hippocampal sirtuin 1 signaling mediates depression-like behavior. Biol Psychiatry 2016; 80(11): 815-26.
[151]
Futch HS, Croft SL. SIRT1: a novel way to target tau? J Neurosci 2018; 38(36): 7755.
[152]
Cunha-Santos J. Caloric restriction blocks neuropathology and motor deficits in Machado–Joseph disease mouse models through SIRT1 pathway. Nat Commun 2016; 7: 11445.
[153]
Fusco SG. Maulucci and G. Pani Sirt1: Def-eating senescence? Cell Cycle 2012; 11(22): p 4135-4146.
[154]
Cantó C. Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 2010; 11(3): 213-9.
[155]
Cantó C. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009; 458: 1056.
[156]
Thirupathi A, de Souza CT. Multi-regulatory network of ROS: the interconnection of ROS PGC-1 alpha and AMPK-SIRT1 during exercise. J Physiol Biochem 2017; 73(4): 487-94.
[157]
Koo JH, Cho JY. Treadmill exercise attenuates α-Synuclein levels by promoting mitochondrial function and autophagy possibly via sirt1 in the chronic mptp/p-induced mouse model of Parkinson’s disease. Neurotox Res 2017; 32(3): 473-86.
[158]
Huang W. AMPK plays a dual role in regulation of CREB/BDNF pathway in mouse primary hippocampal cells. J Mol Neurosci 2015; 56(4): 782-8.
[159]
Iwabu M. Adiponectin and AdipoR1 regulate PGC-1α and mitochondria by Ca2+ and AMPK/SIRT1. Nature 2010; 464: 1313-9.
[160]
Kadowaki T. Adiponectin adiponectin receptors and epigenetic regulation of adipogenesis. Cold Symp Biol 2011; 76: 257-65.
[161]
Zhang K. Adiponectin suppresses T helper 17 cell differentiation and limits autoimmune cns inflammation via the SIRT1/PPARγ/ RORγt Pathway. Mol Neurobiol 2017; 54(7): 4908-20.
[162]
Jin T, Park KY, Seo SJ. Adiponectin upregulates filaggrin expression via sirt1-mediated signaling in human normal keratinocytes. Ann Dermatol 2017; 29(4): 407-13.
[163]
Wei Q. Adiponectin is required for maintaining normal body temperature in a cold environment. BMC Physiol 2017; 17(1): 8.
[164]
Shah SA. Novel osmotin inhibits SREBP2 via the AdipoR1/AMPK/SIRT1 pathway to improve Alzheimer’s disease neuropathological deficits. Mol Psychiatry 2016; 22: 407.
[165]
Safdar A, Saleem A, Tarnopolsky MA. The potential of endurance exercise-derived exosomes to treat metabolic diseases. Nat Rev Endocrinol 2016; 12: 504-17.
[166]
Safdar A, Tarnopolsky MA. Exosomes as mediators of the systemic adaptations to endurance exercise. Cold Perspective Med 2018; 8(3)
[167]
Dey S, Singh RH, Dey PK. Exercise training: Significance of regional alterations in serotonin metabolism of rat brain in relation to antidepressant effect of exercise. Physiol Behav 1992; 52(6): 1095-9.
[168]
Greenwood BN. Wheel running alters serotonin (5-HT) transporter 5-HT1A 5-HT1B and alpha 1b-adrenergic receptor mRNA in the rat raphe nuclei. Biol Psychiatry 2005; 57(5): 559-68.
[169]
Gomez-Merino D. Site-dependent effects of an acute intensive exercise on extracellular 5-HT and 5-HIAA levels in rat brain. Neurosci Lett 2001; 301(2): 143-6.
[170]
Chaouloff F. Effects of conditioned running on plasma liver and brain tryptophan and on brain 5-hydroxytryptamine metabolism of the rat. Br J Pharmacol 1985; 86(1): 33-41.
[171]
Wilson WM, Marsden CA. In vivo measurement of extracellular serotonin in the ventral hippocampus during treadmill running. Behav Pharmacol 1996; 7(1): 101-4.
[172]
Blomstrand E. Amino acids and central fatigue. Amino Acids 2001; 20(1): 25-34.
[173]
aan het Rot M, Collins KA. Fitterling Physical exercise and depression. Mt Sinai J Med 2009; 76(2): 204-14.
[174]
Barchas JD. Freedman brain amines: Response to physiological stress. Biochem Pharmacol 1963; 12: 1232-5.
[175]
Glavin GB. Stress and brain noradrenaline: A review. Neurosci Biobehav Rev 1985; 9(2): pp 233-243.
[176]
Dishman RK. Brain monoamines exercise and behavioral stress: animal models. Med Sci Sports Exerc 1997; 29(1): 63-74.
[177]
Soares J. Brain noradrenergic responses to footshock after chronic activity-wheel running. Behav Neurosci 1999; 113(3): 558-66.
[178]
Dishman RK. Treadmill exercise training augments brain norepinephrine response to familiar and novel stress. Brain Res Bull 2000; 52(5): 337-42.
[179]
Dishman RK. Neurobiology of exercise. Obesity 2006; 14(3): 345-56.
[180]
Cassilhas RC. Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms. Neuroscience 2012; 202: 309-17.
[181]
Ding QZ, Ying F. Gomez-Pinilla Exercise influences hippocampal plasticity by modulating brain-derived neurotrophic factor processing. Neuroscience 2011; 192: 773-80.
[182]
Erickson KI, Miller DL, Roecklein KA. The aging hippocampus: interactions between exercise depression and BDNF. Neuroscientist 2012; 18(1): 82-97.
[183]
Garcia C. The influence of specific noradrenergic and serotonergic lesions on the expression of hippocampal brain-derived neurotrophic factor transcripts following voluntary physical activity. Neuroscience 2003; 119(3): 721-32.
[184]
Garza AA. Exercise antidepressant treatment and BDNF mRNA expression in the aging brain. Pharmacol Biochem Behav 2004; 77(2): 209-20.
[185]
Heyman E. Intense exercise increases circulating endocannabinoid and BDNF levels in humans-possible implications for reward and depression. Psychoneuroendocrinology 2012; 37(6): 844-51.
[186]
Laske C. Exercise-induced normalization of decreased BDNF serum concentration in elderly women with remitted major depression. Int J Neuropsychopharmacol 2010; 13(5): 595-602.
[187]
Lu J. Exercise ameliorates depression-like behavior and increases hippocampal BDNF level in ovariectomized rats. Neurosci Lett 2014; 573: 13-8.
[188]
Marais L, Stein DJ, Daniels WM. Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis 2009; 24(4): 587-97.
[189]
Russo-Neustadt AA. Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience 2000; 101(2): 305-12.
[190]
Russo-Neustadt AA, Chen MJ. Brain-derived neurotrophic factor and antidepressant activity. Curr Pharm Des 2005; 11(12): 1495-510.
[191]
Sartori CR. The antidepressive effect of the physical exercise correlates with increased levels of mature BDNF and proBDNF proteolytic cleavage-related genes p11 and tPA. Neuroscience 2011; 180: 9-18.
[192]
Seifert T. Endurance training enhances BDNF release from the human brain. Am J Physiol Regul Integr Comp Physiol 2010; 298(2): 372-7.
[193]
Anderson MF. Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res Dev Brain Res 2002; 134(1-2): p. 115-122.
[194]
Cassilhas RC. Mood anxiety and serum IGF-1 in elderly men given 24 weeks of high resistance exercise. Percept Mot Skills 2010; 110(1): 265-76.
[195]
Duman CH. Peripheral insulin-like growth factor-I produces antidepressant-like behavior and contributes to the effect of exercise. Behav Brain Res 2009; 198(2): 366-71.
[196]
Mitschelen M. Long-term deficiency of circulating and hippocampal insulin-like growth factor I induces depressive behavior in adult mice: a potential model of geriatric depression. Neuroscience 2011; 185: 50-60.
[197]
Paslakis G, Blum WF, Deuschle M. Intranasal insulin-like growth factor I (IGF-I) as a plausible future treatment of depression. Med Hypotheses 2012; 79(2): 222-5.
[198]
Cotman CW, Berchtold NC. Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neurosci 2002; 25(6): 295-301.
[199]
Fournier NM, Duman RS. Role of vascular endothelial growth factor in adult hippocampal neurogenesis: Implications for the pathophysiology and treatment of depression. Behav Brain Res 2012; 227(2): 440-9.
[200]
Fournier NM. Vascular endothelial growth factor regulates adult hippocampal cell proliferation through MEK/ERK- and PI3K/Akt-dependent signaling. Neuropharmacology 2012; 63(4): 642-52.
[201]
Tang K. Exercise-induced VEGF transcriptional activation in brain lung and skeletal muscle. Respir Physiol Neurobiol 2010; 170(1): 16-22.
[202]
Gobeske KT. BMP signaling mediates effects of exercise on hippocampal neurogenesis and cognition in mice. PLoS One 2009; 4(10)e7506
[203]
Stranahan AM, Lee K, Mattson MP. Central mechanisms of HPA axis regulation by voluntary exercise. Neuromolecular Med 2008; 10(2): 118-27.
[204]
Eyre H, Baune BT. Neuroimmunological effects of physical exercise in depression. Brain Behav Immun 2012; 26(2): 251-66.
[205]
Morgan WP. Affective beneficence of vigorous physical activity. Med Sci Sports Exerc 1985; 17(1): 94-100.
[206]
Wildmann J. Increase of circulating beta-endorphin-like immunoreactivity correlates with the change in feeling of pleasantness after running. Life Sci 1986; 38(11): 997-1003.
[207]
Hoffmann PL, Terenius TP. Cerebrospinal fluid immunoreactive beta-endorphin concentration is increased by voluntary exercise in the spontaneously hypertensive rat. Regul Pept 1990; 28(2): 233-9.
[208]
Radosevich PM. Effects of low- and high-intensity exercise on plasma and cerebrospinal fluid levels of ir-beta-endorphin ACTH cortisol norepinephrine and glucose in the conscious dog. Brain Res 1989; 498(1): 89-98.
[209]
Boecker H. The runner’s high: opioidergic mechanisms in the human brain. Cereb Cortex 2008; 18(11): 2523-31.
[210]
Grazioli E. Physical activity in the prevention of human diseases: role of epigenetic modifications. BMC Genomics 2017; 18(8): 802.
[211]
Barrès R. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab 2012; 15(3): 405-11.
[212]
Lochmann TL. Epigenetic modifications of the PGC-1α promoter during exercise induced expression in mice. PLoS One 2015; 10(6)e0129647
[213]
Lane SC. Effects of sleeping with reduced carbohydrate availability on acute training responses. J Appl Physiol 2015; 119(6): 643-55.
[214]
Guarente L. Linking DNA damage NAD+/SIRT1 and Aging. Cell Metab 2014; 20(5): 706-7.
[215]
Houtkooper RH, Pirinen E, Auwerx J. Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 2012; 13: 225.
[216]
Voisin S. Exercise training and DNA methylation in humans. Acta Physiol 2015; 213(1): 39-59.
[217]
Denham J. Exercise: putting action into our epigenome. Sports Med 2014; 44(2): 189-209.
[218]
Kashimoto RK. Physical exercise affects the epigenetic programming of rat brain and modulates the adaptive response evoked by repeated restraint stress. Behav Brain Res 2016; 296: 286-9.
[219]
Ieraci A. Physical exercise and acute restraint stress differentially modulate hippocampal brain-derived neurotrophic factor transcripts and epigenetic mechanisms in mice. Hippocampus 2015; 25(11): 1380-92.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 18
ISSUE: 4
Year: 2019
Page: [294 - 306]
Pages: 13
DOI: 10.2174/1871527318666190308102804
Price: $58

Article Metrics

PDF: 33
HTML: 4