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Copyright © Andrea Kurucz et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

This article has been cited by other articles in PMC. Abstract Alzheimer's disease AD is a neurodegenerative disorder with cognitive impairment. Physical exercise has long been proven to be beneficial in the disorder.

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The present study was designed to examine the effect of voluntary exercise on spatial memory, imaging, and pathological abnormalities. Particular focus has been given to the role of heme oxygenase-1 HO-1 —an important cellular cytoprotectant in preserving mental acuity—using an aging rat model of dementia.

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Rats in the ARF and ARM groups had free access to a standardized inbuilt running wheel during the 3-month evaluation period. The outcomes suggest that voluntary physical exercise mitigates impaired spatial memory and neuropathological changes exhibited by the aging sedentary group, via elevated HO-1 activity, contributing to the antioxidant capacity in the aging brain.

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Introduction Alzheimer's disease AD is a progressive neurodegenerative disorder, with neuropathology characterized by the accumulation of extracellular amyloid plaques and intracellular neurofibrillary tangles. InAlzheimer's Disease International, an organization founded to promote efforts to prevent and treat the disease, issued their World Alzheimer's Report, which estimates that Changes in demographic patterns, principally increasing life expectancy, with resulting increases in elderly populations, have resulted in a concomitant expansion of AD-afflicted individuals and an increased burden on national healthcare systems.

According to Alzheimer's Association, AD is the 6th leading cause of death in the USA, with 1 out of every 3 elderly people succumbing to it in In that year, the estimated fiscal cost of the disease was billion dollars, which is forecast to increase to a trillion dollars annually by These factors notwithstanding, the development of effective countermeasures for AD remains elusive at the time of this writing [ 1 ].

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Although comprehensively definitive descriptions of AD pathomechanisms remain undefined, some major contributing factors have been elucidated. For example, evidence of a signaling cascade triggered by amyloid deposits, resulting in neuroinflammation and microtubule-associated tau protein hyperphosphorylation, is a likely major underlying process contributing to AD pathogenesis [ 2 ].

An element of this phenomenon is amyloid precursor protein APPa transmembrane component of the outer membrane of the cell. Also, the mitochondria is cleaved by three enzymes α- β- and γ-secretases, with variable cleavage outcomes, determined by as-yet undefined factors.

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Exploration of this enzymatic activity reveals that cleavage by α-secretase prevents amyloid β-formation—and the main products of cleavage by β- and γ-secretases include Aβ40 and Aβ42, which are secreted extracellularly, and may form aggregations that contribute to neurological tissue damage [ 3 — 5 ].

Tau protein aggregation is promoted by amyloid β, which may directly or indirectly activate protein kinases, such as GSK3 and CDK5, via elevation of intracellular calcium levels, leading to tau-hyperphosphorylation and aggregate formation [ 67 ]. Once tau aggregation is initiated, the resulting cascade becomes self-sustaining, continuing independently of amyloid β presence [ 2 ].

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Rogers et al. Several studies have demonstrated that oxidative stress, mitochondrial dysfunction, and inappropriately high proinflammatory activity synergize to damage macromolecules on which healthy cellular and tissue function are dependent—including nucleic acids, lipids, and proteins, ultimately causing neurodegeneration [ 10 — 12 ].

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HO is a major cellular cytoprotectant, the upregulation diabetes metabolism research and reviews if which is an early event of the adaptive response to stress [ 13 ].

In humans, rodents, and many other species, HO exists as two main isoforms: HO-1, an inducible form, and HO-2, which is a constitutively active form.

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HO-1, also known as heat shock protein Hsp is expressed at increased levels in response to internal or exogenous stress cues, including the following: oxidative stress, ischemia, reperfusion, thermal effects, bacterial lipopolysaccharide, and the presence of hemin, its main substrate, which accumulates in tissues as a result of red blood cell turnover [ 14 ]. HO-2 expression is observed to increase in response to developmental factors, adrenal glucocorticoids, and nitric oxide NO [ 1516 ].

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The gene coding for HO-1, HMOX1, has two upstream enhancer regions—E1 and E2—which contain antioxidant-responsive elements supporting diabetes metabolism research and reviews if oxidative-inducible nature of this protein [ 17 ]. Maines suggested that HO-1 szivattyú cukorbetegség gyógyítására a pivotal role in the earliest phases of homeostatic adaptive responses that have evolved to limit tissue damage, while HO-2 is more likely to act as a housekeeping molecule in ways that contribute to the maintenance of heme homeostasis [ 18 ].

CO, which is a major metabolite resulting from HO-mediated degradation of heme, regulates important mechanisms in the central nervous system.

These include long-term hippocampal potentiation and neurotransmitter release.

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HO also functions in the peripheral nervous system to catalyze a diverse range of vital activities, such as the following: nonadrenergic, noncholinergic gastrointestinal relaxation; vasodilation; and inhibition of platelet aggregation.

Moreover, the enzyme acts to limit apoptotic depletion of healthy cells in response to oxidative stressors, along with other cytoprotective functions [ 19 — 23 ]. Diabetes metabolism research and reviews if heme degradation produces biliverdin, which is almost immediately reduced to bilirubin BR by biliverdin reductase BVR.

Several investigations have demonstrated that accumulation of amyloid β acts to increase HO-1, in a physiologic regulatory feedback process which ameliorates the harmful effects of amyloid β [ 2526 ].

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Additionally, many studies which describe the protective role of physical activity as a countermeasure to AD-related neurodegenerative processes include underlying cellular and molecular mechanisms in which HO activity is a potential factor for humans and in animal models of AD [ 27 ]. Insight into the above events is likely to yield improved understanding to AD etiology which, at the time of this writing, remains substantially obscure. Most cases of AD occur spontaneously, with triggering events that are poorly defined or unknown.

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Several animal models have proven to be suitable investigative tools for research into AD pathogenesis. The most widely used animals for modeling AD are mice and rats.

Due to the lack of complete understanding of AD pathomechanisms, all of these models have significant limitations. However, careful selection of a particular animal model in the context of a particular AD-related hypothesis to be tested may reduce the influence of confounding factors associated with a particular model. For example, the numerous transgenic mouse models exhibit features that make them particularly useful in characterizing the familial form of AD, while healthy animals that are subjected to treatments such as streptozotocin- STZ- induced neurodegeneration may be used to demonstrate phenotypic characteristics of the spontaneously occurring forms of AD [ 33 ].

The authors of the present investigation selected a model in which neurodegeneration occurred naturally, though advanced age month-old ratsthus avoiding the potentially confounding influences of transgenes or drugs. The present investigation was structured to test a hypothesis that voluntary recreational physical activity treadmill exercise ameliorates neurodegeneration-related cognitive decline and associated major neuropathological alterations by decreasing oxidative stress via increasing HO-1 activity, thereby preventing neuronal loss in the brain of aging rats.

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This is the first study to evaluate this possibility using an animal model as a correlation between physical exercise and molecular-biological effects associated with age-related neurodegeneration. Materials and Methods 2.

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Animals month-old male and female Wistar rats, weighing — grams at the outset of each experiment, were housed two per cage at an ambient temperature of 22—24°C under a 12 h : 12 h light : dark cycle with food and water ad libitum. All groups were maintained in the above described conditions for 3-month periods.