Protective effects of treadmill exercise on apoptotic neuronal damage and astrocyte activation in ovariectomized and/or diabetic rat prefrontal cortex: molecular and histological aspects

References

• Hamed SA. Brain injury with diabetes mellitus: evidence, mechanisms and treatment implications. Expert Rev Clin Pharmacol. 2017;10(4):409–428.
   PubMed Web of Science ®Google Scholar
• Saeedi P, Petersohn I, Salpea P, IDF Diabetes Atlas Committee, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843.
   PubMed Web of Science ®Google Scholar
• Moheet A, Mangia S, Seaquist ER. Impact of diabetes on cognitive function and brain structure. Ann N Y Acad Sci. 2015;1353:60–71.
   PubMed Web of Science ®Google Scholar
• Zilliox LA, Chadrasekaran K, Kwan JY, et al. Diabetes and cognitive impairment. Curr Diab Rep. 2016;16(9):87.
   PubMed Web of Science ®Google Scholar
• Hao J, Rapp PR, Leffler AE, et al. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci. 2006;26(9):2571–2578.
   PubMed Web of Science ®Google Scholar
• Li C, Brake WG, Romeo RD, et al. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc Natl Acad Sci U S A. 2004;101(7):2185–2190.
   PubMed Web of Science ®Google Scholar
• Wise PM. Estrogens and neuroprotection. Trends Endocrinol Metab. 2002;13(6):229–230.
   PubMed Web of Science ®Google Scholar
• Miller NR, Jover T, Cohen HW, et al. Estrogen can act via estrogen receptor alpha and beta to protect hippocampal neurons against global ischemia-induced cell death. Endocrinology. 2005;146(7):3070–3079.
   PubMed Web of Science ®Google Scholar
• Groeneveld ON, van den Berg E, Johansen OE, et al. Oxidative stress and endothelial dysfunction are associated with reduced cognition in type 2 diabetes. Diab Vasc Dis Res. 2019;16(6):577–581.
   PubMed Web of Science ®Google Scholar
• Kong FJ, Ma LL, Guo JJ, et al. Endoplasmic reticulum stress/autophagy pathway is involved in diabetes-induced neuronal apoptosis and cognitive decline in mice. Clin Sci (Lond). 2018;132(1):111–125.
   PubMed Web of Science ®Google Scholar
• Xu L, Zhu J, Yin W, et al. Astaxanthin improves cognitive deficits from oxidative stress, nitric oxide synthase and inflammation through upregulation of PI3K/akt in diabetes rat. Int J Clin Exp Pathol. 2015;8(6):6083–6094.
   PubMed Web of Science ®Google Scholar
• Delrobaei F, Fatemi I, Shamsizadeh A, et al. Ascorbic acid attenuates cognitive impairment and brain oxidative stress in ovariectomized mice. Pharmacol Rep. 2019;71(1):133–138.
   PubMed Web of Science ®Google Scholar
• Kim TW, Kim CS, Kim JY, et al. Combined exercise ameliorates ovariectomy-induced cognitive impairment by enhancing cell proliferation and suppressing apoptosis. Menopause. 2016;23(1):18–26.
   PubMed Web of Science ®Google Scholar
• Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35(4):495–516.
   PubMed Web of Science ®Google Scholar
• Jiang X, Wang X. Cytochrome C-mediated apoptosis. Annu Rev Biochem. 2004;73:87–106.
   PubMed Web of Science ®Google Scholar
• Mohammadi M, Zare Z. Effects of treadmill exercise on cognitive functions and anxiety-related behaviors in ovariectomized diabetic rats. Physiol Behav. 2020;224:113021.
   PubMed Web of Science ®Google Scholar
• Thierry A-M, Gioanni Y, Dégénétais E, et al. Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus. 2000;10(4):411–419.
   PubMed Web of Science ®Google Scholar
• Wood JN. Social cognition and the prefrontal cortex. Behav Cogn Neurosci Rev. 2003;2(2):97–114.
   PubMedGoogle Scholar
• Shah AA, Treit D. Excitotoxic lesions of the medial prefrontal cortex attenuate fear responses in the elevated-plus maze, social interaction and shock probe burying tests. Brain Res. 2003;969(1–2):183–194.
   PubMed Web of Science ®Google Scholar
• Zare Z, Tehrani M, Zarbakhsh S, et al. Effects of paraoxon exposure on expression of apoptosis-related genes, neuronal survival, and astrocyte activation in rat prefrontal cortex. Neurotox Res. 2020;37(2):356–365.
   PubMed Web of Science ®Google Scholar
• Suzuki S, Brown CM, Wise PM. Mechanisms of neuroprotection by estrogen. Endocrine. 2006;29(2):209–215.
   PubMed Web of Science ®Google Scholar
• Lin YY, Cheng YJ, Hu J, et al. The coexistence of hypertension and ovariectomy additively increases cardiac apoptosis. IJMS. 2016;17(12):2036.
   Web of Science ®Google Scholar
• Li ZG, Zhang W, Grunberger G, et al. Hippocampal neuronal apoptosis in type 1 diabetes. Brain Res. 2002;946(2):221–231.
   PubMed Web of Science ®Google Scholar
• Ünver Saraydin S, Özdenoglu Kutlu B, Saraydın D. Effects of diabetes on apoptosis and mitosis in rat hippocampus. Biotech Histochem. 2021;96(6):460–467.
   PubMed Web of Science ®Google Scholar
• Ji ES, Ko IG, Cho JW, et al. Treadmill exercise inhibits apoptotic neuronal cell death with suppressed vascular endothelial growth factor expression in the retinas of the diabetic rats. J Exerc Rehabil. 2013;9(3):348–353.
   PubMedGoogle Scholar
• Ceriello A. Oxidative stress and diabetes-associated complications. Endocr Pract. 2006;12(Suppl 1):60–62.
   PubMedGoogle Scholar
• Redza-Dutordoir M, Averill-Bates DA. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta. 2016;1863(12):2977–2992.
   PubMed Web of Science ®Google Scholar
• Meng Y, Wang W, Kang J, et al. Role of the PI3K/AKT signalling pathway in apoptotic cell death in the cerebral cortex of streptozotocin-induced diabetic rats. Exp Ther Med. 2017;13(5):2417–2422.
   PubMed Web of Science ®Google Scholar
• Habibi P, Alihemmati A, Ahmadiasl N, et al. Exercise training attenuates diabetes-induced cardiac injury through increasing miR-133a and improving pro-apoptosis/anti-apoptosis balance in ovariectomized rats. Iran J Basic Med Sci. 2020;23(1):79–85.
   PubMed Web of Science ®Google Scholar
• Lee MK, Jung CS, Yoon JH, et al. Effects of resistance exercise on antioxidant enzyme activities and apoptosis-related protein expression of hippocampus in OLETF rats. Technol Health Care. 2018;26(3):457–467.
   PubMed Web of Science ®Google Scholar
• Kim DY, Jung SY, Kim CJ, et al. Treadmill exercise ameliorates apoptotic cell death in the retinas of diabetic rats. Mol Med Rep. 2013;7(6):1745–1750.
   PubMed Web of Science ®Google Scholar
• Um HS, Kang EB, Koo JH, et al. Treadmill exercise represses neuronal cell death in an aged transgenic mouse model of Alzheimer’s disease. Neurosci. Res. 2011;69(2):161–173.
   PubMed Web of Science ®Google Scholar
• Mahalakshmi B, Maurya N, Lee SD, et al. Possible neuroprotective mechanisms of physical exercise in neurodegeneration. IJMS. 2020;21(16):5895.
   Web of Science ®Google Scholar
• Wrann CD, White JP, Salogiannnis J, et al. Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell Metab. 2013;18(5):649–659.
   PubMed Web of Science ®Google Scholar
• Karki P, Smith K, Johnson J, Jr., et al. Astrocyte-derived growth factors and estrogen neuroprotection: role of transforming growth factor-α in estrogen-induced upregulation of glutamate transporters in astrocytes. Mol Cell Endocrinol. 2014;389(1–2):58–64.
   PubMed Web of Science ®Google Scholar
• Sofroniew MV. Reactive astrocytes in neural repair and protection. Neuroscientist. 2005;11(5):400–407.
   PubMed Web of Science ®Google Scholar
• Middeldorp J, Hol EM. GFAP in health and disease. Prog Neurobiol. 2011;93(3):421–443.
   PubMed Web of Science ®Google Scholar
• Baydas G, Nedzvetskii VS, Tuzcu M, et al. Increase of glial fibrillary acidic protein and S-100B in hippocampus and cortex of diabetic rats: effects of vitamin E. Eur J Pharmacol. 2003;462(1–3):67–71.
   PubMed Web of Science ®Google Scholar
• Coleman E, Judd R, Hoe L, et al. Effects of diabetes mellitus on astrocyte GFAP and glutamate transporters in the CNS. Glia. 2004;48(2):166–178.
   PubMed Web of Science ®Google Scholar
• de Senna PN, Ilha J, Baptista PP, et al. Effects of physical exercise on spatial memory and astroglial alterations in the hippocampus of diabetic rats. Metab Brain Dis. 2011;26(4):269–279.
   PubMed Web of Science ®Google Scholar
• Lechuga-Sancho AM, Arroba AI, Frago LM, et al. Activation of the intrinsic cell death pathway, increased apoptosis and modulation of astrocytes in the cerebellum of diabetic rats. Neurobiol Dis. 2006;23(2):290–299.
   PubMed Web of Science ®Google Scholar
• Nardin P, Zanotto C, Hansen F, et al. Peripheral levels of AGEs and astrocyte alterations in the hippocampus of STZ-diabetic rats. Neurochem Res. 2016;41(8):2006–2016.
   PubMed Web of Science ®Google Scholar
• Beauquis J, Roig P, Homo-Delarche F, et al. Reduced hippocampal neurogenesis and number of hilar neurones in streptozotocin-induced diabetic mice: reversion by antidepressant treatment. Eur J Neurosci. 2006;23(6):1539–1546.
   PubMed Web of Science ®Google Scholar
• Saravia FE, Revsin Y, Gonzalez Deniselle MC, et al. Increased astrocyte reactivity in the hippocampus of murine models of type 1 diabetes: the nonobese diabetic (NOD) and streptozotocin-treated mice. Brain Res. 2002;957(2):345–353.
   PubMed Web of Science ®Google Scholar