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Published in: NeuroMolecular Medicine 4/2019

Open Access 01-12-2019 | Stroke | Original Paper

A Short Bout of Exercise Prior to Stroke Improves Functional Outcomes by Enhancing Angiogenesis

Authors: Stefano Pianta, Jea Young Lee, Julian P. Tuazon, Vanessa Castelli, Leigh Monica Mantohac, Naoki Tajiri, Cesar V. Borlongan

Published in: NeuroMolecular Medicine | Issue 4/2019

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Abstract

Stroke remains a significant unmet clinical need with limited therapeutic options. The peculiar feature of ischemic stroke is the interruption in brain circulation, resulting in a cascade of detrimental cerebrovasculature alterations. Treatment strategies designed to maintain potency of the cerebrovasculature may protect against stroke. The present study assessed the effects of short bouts of exercise prior to stroke induction and characterized cerebral blood flow and motor functions in vivo. Adult Sprague–Dawley rats were exposed to a single short bout of exercise (30-min or 60-min forced running wheel) then subjected to transient middle cerebral artery occlusion (MCAO). Non-exercise stroke rats served as controls while non-stroke rats represented shams. Cerebral blood flow (CBF) was evaluated by laser Doppler at baseline (prior to MCAO), during MCAO, and during reperfusion. Behavioral tests using the elevated body swing test was conducted at baseline, day 0 (day of stroke), and at days 1 and 3 after stroke. Animals that received exercise displayed typical alterations in CBF after stroke, but exhibited improved motor performance compared to non-exercise rats. Exercised stroke rats showed a reduction in infarct size and an increased number of surviving cells in the peri-infarct area, with a trend towards prolonged duration of the exercise. Immunofluorescence staining and Western blot analysis of the peri-infarct area revealed increased levels of endothelial markers/angiogenesis markers, VEGF, VEGFR-2, and Ang-2, and endothelial progenitor cell marker CD34+ in exercise groups compared with the controls. These results demonstrated that prophylactic exercise affords neuroprotection possibly by improving cerebrovascular potency.
Literature
go back to reference Acosta, S. A., Tajiri, N., Hoover, J., Kaneko, Y., & Borlongan, C. V. (2015). Intravenous bone marrow stem cell grafts preferentially migrate to spleen and abrogate chronic inflammation in stroke. Stroke, 46(9), 2616–2627.PubMedPubMedCentral Acosta, S. A., Tajiri, N., Hoover, J., Kaneko, Y., & Borlongan, C. V. (2015). Intravenous bone marrow stem cell grafts preferentially migrate to spleen and abrogate chronic inflammation in stroke. Stroke, 46(9), 2616–2627.PubMedPubMedCentral
go back to reference Arrick, D. M., Yang, S., Li, C., Cananzi, S., & Mayhan, W. G. (2014). Vigorous exercise training improves reactivity of cerebral arterioles and reduces brain injury following transient focal ischemia. Microcirculation, 21(6), 516–523.PubMed Arrick, D. M., Yang, S., Li, C., Cananzi, S., & Mayhan, W. G. (2014). Vigorous exercise training improves reactivity of cerebral arterioles and reduces brain injury following transient focal ischemia. Microcirculation, 21(6), 516–523.PubMed
go back to reference Arumugam, T. V., Gleichmann, M., Tang, S. C., & Mattson, M. P. (2006). Hormesis/preconditioning mechanisms, the nervous system and aging. Ageing Research Reviews, 5(2), 165–178.PubMed Arumugam, T. V., Gleichmann, M., Tang, S. C., & Mattson, M. P. (2006). Hormesis/preconditioning mechanisms, the nervous system and aging. Ageing Research Reviews, 5(2), 165–178.PubMed
go back to reference Barrientos, R. M., Frank, M. G., Crysdale, N. Y., Chapman, T. R., Ahrendsen, J. T., Day, H. E., et al. (2011). Little exercise, big effects: Reversing aging and infection-induced memory deficits, and underlying processes. The Journal of Neuroscience, 31(32), 11578–11586.PubMedPubMedCentral Barrientos, R. M., Frank, M. G., Crysdale, N. Y., Chapman, T. R., Ahrendsen, J. T., Day, H. E., et al. (2011). Little exercise, big effects: Reversing aging and infection-induced memory deficits, and underlying processes. The Journal of Neuroscience, 31(32), 11578–11586.PubMedPubMedCentral
go back to reference Belfiore, P., Miele, A., Galle, F., & Liguori, G. (2018). Adapted physical activity and stroke: A systematic review. The Journal of Sports Medicine and Physical Fitness, 58(12), 1867–1875.PubMed Belfiore, P., Miele, A., Galle, F., & Liguori, G. (2018). Adapted physical activity and stroke: A systematic review. The Journal of Sports Medicine and Physical Fitness, 58(12), 1867–1875.PubMed
go back to reference Benjamin, E. J., Blaha, M. J., Chiuve, S. E., Cushman, M., Das, S. R., Deo, R., et al. (2017). Heart disease and stroke statistics-2017 update: A report from the American Heart Association. Circulation, 135(10), e146–e603.PubMedPubMedCentral Benjamin, E. J., Blaha, M. J., Chiuve, S. E., Cushman, M., Das, S. R., Deo, R., et al. (2017). Heart disease and stroke statistics-2017 update: A report from the American Heart Association. Circulation, 135(10), e146–e603.PubMedPubMedCentral
go back to reference Billinger, S. A., Arena, R., Bernhardt, J., Eng, J. J., Franklin, B. A., Johnson, C. M., et al. (2014). Physical activity and exercise recommendations for stroke survivors: A statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 45(8), 2532–2553.PubMed Billinger, S. A., Arena, R., Bernhardt, J., Eng, J. J., Franklin, B. A., Johnson, C. M., et al. (2014). Physical activity and exercise recommendations for stroke survivors: A statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 45(8), 2532–2553.PubMed
go back to reference Borlongan, C. V., Hida, H., & Nishino, H. (1998). Early assessment of motor dysfunctions aids in successful occlusion of the middle cerebral artery. Neuroreport, 9(16), 3615–3621.PubMed Borlongan, C. V., Hida, H., & Nishino, H. (1998). Early assessment of motor dysfunctions aids in successful occlusion of the middle cerebral artery. Neuroreport, 9(16), 3615–3621.PubMed
go back to reference Borlongan, C. V., & Sanberg, P. R. (1995). Elevated body swing test: A new behavioral parameter for rats with 6-hydroxydopamine-induced hemiparkinsonism. The Journal of Neuroscience, 15(7 Pt 2), 5372–5378.PubMedPubMedCentral Borlongan, C. V., & Sanberg, P. R. (1995). Elevated body swing test: A new behavioral parameter for rats with 6-hydroxydopamine-induced hemiparkinsonism. The Journal of Neuroscience, 15(7 Pt 2), 5372–5378.PubMedPubMedCentral
go back to reference Brandt, M. D., Maass, A., Kempermann, G., & Storch, A. (2010). Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis. European Journal of Neuroscience, 32(8), 1256–1264. Brandt, M. D., Maass, A., Kempermann, G., & Storch, A. (2010). Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis. European Journal of Neuroscience, 32(8), 1256–1264.
go back to reference Cai, W., Zhang, K., Li, P., Zhu, L., Xu, J., Yang, B., et al. (2017). Dysfunction of the neurovascular unit in ischemic stroke and neurodegenerative diseases: An aging effect. Ageing Research Reviews, 34, 77–87.PubMed Cai, W., Zhang, K., Li, P., Zhu, L., Xu, J., Yang, B., et al. (2017). Dysfunction of the neurovascular unit in ischemic stroke and neurodegenerative diseases: An aging effect. Ageing Research Reviews, 34, 77–87.PubMed
go back to reference Campbell, B. C. V., Donnan, G. A., Lees, K. R., Hacke, W., Khatri, P., Hill, M. D., et al. (2015). Endovascular stent thrombectomy: The new standard of care for large vessel ischaemic stroke. The Lancet Neurology, 14(8), 846–854.PubMed Campbell, B. C. V., Donnan, G. A., Lees, K. R., Hacke, W., Khatri, P., Hill, M. D., et al. (2015). Endovascular stent thrombectomy: The new standard of care for large vessel ischaemic stroke. The Lancet Neurology, 14(8), 846–854.PubMed
go back to reference Carro, E., Nunez, A., Busiguina, S., & Torres-Aleman, I. (2000). Circulating insulin-like growth factor I mediates effects of exercise on the brain. The Journal of Neuroscience, 20(8), 2926–2933.PubMedPubMedCentral Carro, E., Nunez, A., Busiguina, S., & Torres-Aleman, I. (2000). Circulating insulin-like growth factor I mediates effects of exercise on the brain. The Journal of Neuroscience, 20(8), 2926–2933.PubMedPubMedCentral
go back to reference Cohen, D. L., Kearney, R., Griffiths, M., Nadesalingam, V., & Bathula, R. (2015). Around 9% of patients with ischaemic stroke are suitable for thrombectomy. BMJ, 351, h4607.PubMed Cohen, D. L., Kearney, R., Griffiths, M., Nadesalingam, V., & Bathula, R. (2015). Around 9% of patients with ischaemic stroke are suitable for thrombectomy. BMJ, 351, h4607.PubMed
go back to reference Cotman, C. W., Berchtold, N. C., & Christie, L. A. (2007). Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends in Neurosciences, 30(9), 464–472.PubMed Cotman, C. W., Berchtold, N. C., & Christie, L. A. (2007). Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends in Neurosciences, 30(9), 464–472.PubMed
go back to reference Deplanque, D., Masse, I., Lefebvre, C., Libersa, C., Leys, D., & Bordet, R. (2006). Prior TIA, lipid-lowering drug use, and physical activity decrease ischemic stroke severity. Neurology, 67(8), 1403–1410.PubMed Deplanque, D., Masse, I., Lefebvre, C., Libersa, C., Leys, D., & Bordet, R. (2006). Prior TIA, lipid-lowering drug use, and physical activity decrease ischemic stroke severity. Neurology, 67(8), 1403–1410.PubMed
go back to reference Deplanque, D., Masse, I., Libersa, C., Leys, D., & Bordet, R. (2012). Previous leisure-time physical activity dose dependently decreases ischemic stroke severity. Stroke Research and Treatment, 2012, 614925.PubMed Deplanque, D., Masse, I., Libersa, C., Leys, D., & Bordet, R. (2012). Previous leisure-time physical activity dose dependently decreases ischemic stroke severity. Stroke Research and Treatment, 2012, 614925.PubMed
go back to reference Ding, Y. H., Li, J., Yao, W. X., Rafols, J. A., Clark, J. C., & Ding, Y. (2006). Exercise preconditioning upregulates cerebral integrins and enhances cerebrovascular integrity in ischemic rats. Acta Neuropathologica, 112(1), 74–84.PubMed Ding, Y. H., Li, J., Yao, W. X., Rafols, J. A., Clark, J. C., & Ding, Y. (2006). Exercise preconditioning upregulates cerebral integrins and enhances cerebrovascular integrity in ischemic rats. Acta Neuropathologica, 112(1), 74–84.PubMed
go back to reference Ding, Y. H., Young, C. N., Luan, X., Li, J., Rafols, J. A., Clark, J. C., et al. (2005). Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathologica, 109(3), 237–246.PubMed Ding, Y. H., Young, C. N., Luan, X., Li, J., Rafols, J. A., Clark, J. C., et al. (2005). Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathologica, 109(3), 237–246.PubMed
go back to reference Dornbos, D. III, Zwagerman, N., Guo, M., Ding, J. Y., Peng, C., Esmail, F., et al. (2013). Preischemic exercise reduces brain damage by ameliorating metabolic disorder in ischemia/reperfusion injury. Journal of Neuroscience Research, 91(6), 818–827.PubMed Dornbos, D. III, Zwagerman, N., Guo, M., Ding, J. Y., Peng, C., Esmail, F., et al. (2013). Preischemic exercise reduces brain damage by ameliorating metabolic disorder in ischemia/reperfusion injury. Journal of Neuroscience Research, 91(6), 818–827.PubMed
go back to reference Emberson, J., Lees, K. R., Lyden, P., Blackwell, L., Albers, G., Bluhmki, E., et al. (2014). Effect of treatment delay, age, and stroke severity on the effects of intravenous thrombolysis with alteplase for acute ischaemic stroke: A meta-analysis of individual patient data from randomised trials. Lancet, 384(9958), 1929–1935.PubMedPubMedCentral Emberson, J., Lees, K. R., Lyden, P., Blackwell, L., Albers, G., Bluhmki, E., et al. (2014). Effect of treatment delay, age, and stroke severity on the effects of intravenous thrombolysis with alteplase for acute ischaemic stroke: A meta-analysis of individual patient data from randomised trials. Lancet, 384(9958), 1929–1935.PubMedPubMedCentral
go back to reference Furlan, A. J. (2015). Endovascular therapy for stroke—It’s about time. The New England Journal of Medicine, 372(24), 2347–2349.PubMed Furlan, A. J. (2015). Endovascular therapy for stroke—It’s about time. The New England Journal of Medicine, 372(24), 2347–2349.PubMed
go back to reference Gao, Y., Zhao, Y., Pan, J., Yang, L., Huang, T., Feng, X., et al. (2014). Treadmill exercise promotes angiogenesis in the ischemic penumbra of rat brains through caveolin-1/VEGF signaling pathways. Brain Research, 1585, 83–90.PubMed Gao, Y., Zhao, Y., Pan, J., Yang, L., Huang, T., Feng, X., et al. (2014). Treadmill exercise promotes angiogenesis in the ischemic penumbra of rat brains through caveolin-1/VEGF signaling pathways. Brain Research, 1585, 83–90.PubMed
go back to reference Gheysen, F., Poppe, L., DeSmet, A., Swinnen, S., Cardon, G., De Bourdeaudhuij, I., et al. (2018). Physical activity to improve cognition in older adults: Can physical activity programs enriched with cognitive challenges enhance the effects? A systematic review and meta-analysis. International Journal of Behavioral Nutrition and Physical Activity, 15(1), 63. Gheysen, F., Poppe, L., DeSmet, A., Swinnen, S., Cardon, G., De Bourdeaudhuij, I., et al. (2018). Physical activity to improve cognition in older adults: Can physical activity programs enriched with cognitive challenges enhance the effects? A systematic review and meta-analysis. International Journal of Behavioral Nutrition and Physical Activity, 15(1), 63.
go back to reference Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Blaha, M. J., et al. (2014). Heart disease and stroke statistics—2014 update: A report from the American Heart Association. Circulation, 129(3), e28–e292.PubMed Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Blaha, M. J., et al. (2014). Heart disease and stroke statistics—2014 update: A report from the American Heart Association. Circulation, 129(3), e28–e292.PubMed
go back to reference Hasan, S. M., Rancourt, S. N., Austin, M. W., & Ploughman, M. (2016). Defining optimal aerobic exercise parameters to affect complex motor and cognitive outcomes after stroke: A systematic review and synthesis. Neural Plasticity. 2016, 2961573.PubMedPubMedCentral Hasan, S. M., Rancourt, S. N., Austin, M. W., & Ploughman, M. (2016). Defining optimal aerobic exercise parameters to affect complex motor and cognitive outcomes after stroke: A systematic review and synthesis. Neural Plasticity. 2016, 2961573.PubMedPubMedCentral
go back to reference Howard, V. J., & McDonnell, M. M. (2015). Physical activity in primary stroke prevention: Just do it! Stroke, 46(6), 1735–1739.PubMed Howard, V. J., & McDonnell, M. M. (2015). Physical activity in primary stroke prevention: Just do it! Stroke, 46(6), 1735–1739.PubMed
go back to reference Ibrahim, A. G., Raisman, G., & Li, Y. (2009). Permanent loss of fore-paw grasping requires complete deprivation of afferent input from a minimum of four dorsal roots of the rat brachial plexus. Experimental Neurology, 215(1), 142–145.PubMed Ibrahim, A. G., Raisman, G., & Li, Y. (2009). Permanent loss of fore-paw grasping requires complete deprivation of afferent input from a minimum of four dorsal roots of the rat brachial plexus. Experimental Neurology, 215(1), 142–145.PubMed
go back to reference Ishikawa, H., Tajiri, N., Shinozuka, K., Vasconcellos, J., Kaneko, Y., Lee, H. J., et al. (2013). Vasculogenesis in experimental stroke after human cerebral endothelial cell transplantation. Stroke, 44(12), 3473–3481.PubMedPubMedCentral Ishikawa, H., Tajiri, N., Shinozuka, K., Vasconcellos, J., Kaneko, Y., Lee, H. J., et al. (2013). Vasculogenesis in experimental stroke after human cerebral endothelial cell transplantation. Stroke, 44(12), 3473–3481.PubMedPubMedCentral
go back to reference Josephson, S. A., & Kamel, H. (2018). The acute stroke care revolution: Enhancing access to therapeutic advances. JAMA, 320(12), 1239–1240.PubMed Josephson, S. A., & Kamel, H. (2018). The acute stroke care revolution: Enhancing access to therapeutic advances. JAMA, 320(12), 1239–1240.PubMed
go back to reference Krarup, L. H., Truelsen, T., Gluud, C., Andersen, G., Zeng, X., Korv, J., et al. (2008). Prestroke physical activity is associated with severity and long-term outcome from first-ever stroke. Neurology, 71(17), 1313–1318.PubMed Krarup, L. H., Truelsen, T., Gluud, C., Andersen, G., Zeng, X., Korv, J., et al. (2008). Prestroke physical activity is associated with severity and long-term outcome from first-ever stroke. Neurology, 71(17), 1313–1318.PubMed
go back to reference Li, F., Geng, X., Khan, H., Pendy, J. T. Jr., Peng, C., Li, X., et al. (2017). Exacerbation of brain injury by post-stroke exercise is contingent upon exercise initiation timing. Frontiers in Cellular Neuroscience, 11, 311.PubMedPubMedCentral Li, F., Geng, X., Khan, H., Pendy, J. T. Jr., Peng, C., Li, X., et al. (2017). Exacerbation of brain injury by post-stroke exercise is contingent upon exercise initiation timing. Frontiers in Cellular Neuroscience, 11, 311.PubMedPubMedCentral
go back to reference Liebelt, B., Papapetrou, P., Ali, A., Guo, M., Ji, X., Peng, C., et al. (2010). Exercise preconditioning reduces neuronal apoptosis in stroke by up-regulating heat shock protein-70 (heat shock protein-72) and extracellular-signal-regulated-kinase 1/2. Neuroscience, 166(4), 1091–1100.PubMed Liebelt, B., Papapetrou, P., Ali, A., Guo, M., Ji, X., Peng, C., et al. (2010). Exercise preconditioning reduces neuronal apoptosis in stroke by up-regulating heat shock protein-70 (heat shock protein-72) and extracellular-signal-regulated-kinase 1/2. Neuroscience, 166(4), 1091–1100.PubMed
go back to reference Lo, E. H., Dalkara, T., & Moskowitz, M. A. (2003). Mechanisms, challenges and opportunities in stroke. Nature Reviews Neuroscience, 4(5), 399–415.PubMed Lo, E. H., Dalkara, T., & Moskowitz, M. A. (2003). Mechanisms, challenges and opportunities in stroke. Nature Reviews Neuroscience, 4(5), 399–415.PubMed
go back to reference Mattson, M. P. (2012). Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metabolism, 16(6), 706–722.PubMedPubMedCentral Mattson, M. P. (2012). Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metabolism, 16(6), 706–722.PubMedPubMedCentral
go back to reference Meschia, J. F., & Brott, T. (2018). Ischaemic stroke. European Journal of Neurology, 25(1), 35–40.PubMed Meschia, J. F., & Brott, T. (2018). Ischaemic stroke. European Journal of Neurology, 25(1), 35–40.PubMed
go back to reference Mokin, M., Dumont, T. M., Veznedaroglu, E., Binning, M. J., Liebman, K. M., Fessler, R. D. II, et al (2013). Solitaire flow restoration thrombectomy for acute ischemic stroke: Retrospective multicenter analysis of early postmarket experience after FDA approval. Neurosurgery, 73(1), 19–25.PubMed Mokin, M., Dumont, T. M., Veznedaroglu, E., Binning, M. J., Liebman, K. M., Fessler, R. D. II, et al (2013). Solitaire flow restoration thrombectomy for acute ischemic stroke: Retrospective multicenter analysis of early postmarket experience after FDA approval. Neurosurgery, 73(1), 19–25.PubMed
go back to reference Morton, J. P., Kayani, A. C., McArdle, A., & Drust, B. (2009). The exercise-induced stress response of skeletal muscle, with specific emphasis on humans. Sports Medicine, 39(8), 643–662.PubMed Morton, J. P., Kayani, A. C., McArdle, A., & Drust, B. (2009). The exercise-induced stress response of skeletal muscle, with specific emphasis on humans. Sports Medicine, 39(8), 643–662.PubMed
go back to reference Oberlin, L. E., Waiwood, A. M., Cumming, T. B., Marsland, A. L., Bernhardt, J., & Erickson, K. I. (2017). Effects of physical activity on poststroke cognitive function: A meta-analysis of randomized controlled trials. Stroke, 48(11), 3093–3100.PubMedPubMedCentral Oberlin, L. E., Waiwood, A. M., Cumming, T. B., Marsland, A. L., Bernhardt, J., & Erickson, K. I. (2017). Effects of physical activity on poststroke cognitive function: A meta-analysis of randomized controlled trials. Stroke, 48(11), 3093–3100.PubMedPubMedCentral
go back to reference Otsuka, S., Sakakima, H., Sumizono, M., Takada, S., Terashi, T., & Yoshida, Y. (2016). The neuroprotective effects of preconditioning exercise on brain damage and neurotrophic factors after focal brain ischemia in rats. Behavioural Brain Research, 303, 9–18.PubMed Otsuka, S., Sakakima, H., Sumizono, M., Takada, S., Terashi, T., & Yoshida, Y. (2016). The neuroprotective effects of preconditioning exercise on brain damage and neurotrophic factors after focal brain ischemia in rats. Behavioural Brain Research, 303, 9–18.PubMed
go back to reference Pan, X., Jiang, T., Zhang, L., Zheng, H., Luo, J., & Hu, X. (2017). Physical exercise promotes novel object recognition memory in spontaneously hypertensive rats after ischemic stroke by promoting neural plasticity in the entorhinal cortex. Frontiers in Behavioral Neuroscience, 11, 185.PubMedPubMedCentral Pan, X., Jiang, T., Zhang, L., Zheng, H., Luo, J., & Hu, X. (2017). Physical exercise promotes novel object recognition memory in spontaneously hypertensive rats after ischemic stroke by promoting neural plasticity in the entorhinal cortex. Frontiers in Behavioral Neuroscience, 11, 185.PubMedPubMedCentral
go back to reference Rezaei, R., Nasoohi, S., Haghparast, A., Khodagholi, F., Bigdeli, M. R., & Nourshahi, M. (2018). High intensity exercise preconditioning provides differential protection against brain injury following experimental stroke. Life Sciences, 207, 30–35.PubMed Rezaei, R., Nasoohi, S., Haghparast, A., Khodagholi, F., Bigdeli, M. R., & Nourshahi, M. (2018). High intensity exercise preconditioning provides differential protection against brain injury following experimental stroke. Life Sciences, 207, 30–35.PubMed
go back to reference Robertson, A. D., Marzolini, S., Middleton, L. E., Basile, V. S., Oh, P. I., & MacIntosh, B. J. (2017). Exercise training increases parietal lobe cerebral blood flow in chronic stroke: An observational study. Frontiers in Aging Neuroscience, 9, 318.PubMedPubMedCentral Robertson, A. D., Marzolini, S., Middleton, L. E., Basile, V. S., Oh, P. I., & MacIntosh, B. J. (2017). Exercise training increases parietal lobe cerebral blood flow in chronic stroke: An observational study. Frontiers in Aging Neuroscience, 9, 318.PubMedPubMedCentral
go back to reference Shen, J., Huber, M., Zhao, E. Y., Peng, C., Li, F., Li, X., et al. (2016). Early rehabilitation aggravates brain damage after stroke via enhanced activation of nicotinamide adenine dinucleotide phosphate oxidase (NOX). Brain Research, 1648(Pt A), 266–276.PubMed Shen, J., Huber, M., Zhao, E. Y., Peng, C., Li, F., Li, X., et al. (2016). Early rehabilitation aggravates brain damage after stroke via enhanced activation of nicotinamide adenine dinucleotide phosphate oxidase (NOX). Brain Research, 1648(Pt A), 266–276.PubMed
go back to reference Sheth, S. A., Jahan, R., Gralla, J., Pereira, V. M., Nogueira, R. G., Levy, E. I., et al. (2015). Time to endovascular reperfusion and degree of disability in acute stroke. Annals of Neurology, 78(4), 584–593.PubMedPubMedCentral Sheth, S. A., Jahan, R., Gralla, J., Pereira, V. M., Nogueira, R. G., Levy, E. I., et al. (2015). Time to endovascular reperfusion and degree of disability in acute stroke. Annals of Neurology, 78(4), 584–593.PubMedPubMedCentral
go back to reference Shimada, H., Hamakawa, M., Ishida, A., Tamakoshi, K., Nakashima, H., & Ishida, K. (2013). Low-speed treadmill running exercise improves memory function after transient middle cerebral artery occlusion in rats. Behavioural Brain Research, 243, 21–27.PubMed Shimada, H., Hamakawa, M., Ishida, A., Tamakoshi, K., Nakashima, H., & Ishida, K. (2013). Low-speed treadmill running exercise improves memory function after transient middle cerebral artery occlusion in rats. Behavioural Brain Research, 243, 21–27.PubMed
go back to reference Shinozuka, K., Dailey, T., Tajiri, N., Ishikawa, H., Kaneko, Y., & Borlongan, C. V. (2013). Stem cell transplantation for neuroprotection in stroke. Brain Sciences, 3(1), 239–261.PubMedPubMedCentral Shinozuka, K., Dailey, T., Tajiri, N., Ishikawa, H., Kaneko, Y., & Borlongan, C. V. (2013). Stem cell transplantation for neuroprotection in stroke. Brain Sciences, 3(1), 239–261.PubMedPubMedCentral
go back to reference Stradecki-Cohan, H. M., Youbi, M., Cohan, C. H., Saul, I., Garvin, A. A., Perez, E., et al. (2017). Physical exercise improves cognitive outcomes in 2 models of transient cerebral ischemia. Stroke, 48(8), 2306–2309.PubMedPubMedCentral Stradecki-Cohan, H. M., Youbi, M., Cohan, C. H., Saul, I., Garvin, A. A., Perez, E., et al. (2017). Physical exercise improves cognitive outcomes in 2 models of transient cerebral ischemia. Stroke, 48(8), 2306–2309.PubMedPubMedCentral
go back to reference Tang, K., Xia, F. C., Wagner, P. D., & Breen, E. C. (2010). Exercise-induced VEGF transcriptional activation in brain, lung and skeletal muscle. Respiratory Physiology & Neurobiology, 170(1), 16–22. Tang, K., Xia, F. C., Wagner, P. D., & Breen, E. C. (2010). Exercise-induced VEGF transcriptional activation in brain, lung and skeletal muscle. Respiratory Physiology & Neurobiology, 170(1), 16–22.
go back to reference Tang, Y., Zhang, Y., Zheng, M., Chen, J., Chen, H., & Liu, N. (2018). Effects of treadmill exercise on cerebral angiogenesis and MT1-MMP expression after cerebral ischemia in rats. Brain Behav. 8(8), e01079.PubMedPubMedCentral Tang, Y., Zhang, Y., Zheng, M., Chen, J., Chen, H., & Liu, N. (2018). Effects of treadmill exercise on cerebral angiogenesis and MT1-MMP expression after cerebral ischemia in rats. Brain Behav. 8(8), e01079.PubMedPubMedCentral
go back to reference Vance, D. E., Marson, D. C., Triebel, K. L., Ball, K. K., Wadley, V. G., & Cody, S. L. (2016). Physical activity and cognitive function in older adults: The mediating effect of depressive symptoms. Journal of Neuroscience Nursing, 48(4), E2–E12. Vance, D. E., Marson, D. C., Triebel, K. L., Ball, K. K., Wadley, V. G., & Cody, S. L. (2016). Physical activity and cognitive function in older adults: The mediating effect of depressive symptoms. Journal of Neuroscience Nursing, 48(4), E2–E12.
go back to reference Voss, M. W., Vivar, C., Kramer, A. F., & van Praag, H. (2013). Bridging animal and human models of exercise-induced brain plasticity. Trends in Cognitive Sciences, 17(10), 525–544.PubMedPubMedCentral Voss, M. W., Vivar, C., Kramer, A. F., & van Praag, H. (2013). Bridging animal and human models of exercise-induced brain plasticity. Trends in Cognitive Sciences, 17(10), 525–544.PubMedPubMedCentral
go back to reference Winstein, C. J., Stein, J., Arena, R., Bates, B., Cherney, L. R., Cramer, S. C., et al. (2016). Guidelines for adult stroke rehabilitation and recovery: A guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 47(6), e98–e169.PubMed Winstein, C. J., Stein, J., Arena, R., Bates, B., Cherney, L. R., Cramer, S. C., et al. (2016). Guidelines for adult stroke rehabilitation and recovery: A guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 47(6), e98–e169.PubMed
go back to reference Woitke, F., Ceanga, M., Rudolph, M., Niv, F., Witte, O. W., Redecker, C., et al. (2017). Adult hippocampal neurogenesis poststroke: More new granule cells but aberrant morphology and impaired spatial memory. PLoS ONE, 12(9), e0183463.PubMedPubMedCentral Woitke, F., Ceanga, M., Rudolph, M., Niv, F., Witte, O. W., Redecker, C., et al. (2017). Adult hippocampal neurogenesis poststroke: More new granule cells but aberrant morphology and impaired spatial memory. PLoS ONE, 12(9), e0183463.PubMedPubMedCentral
go back to reference Xie, Q., Cheng, J., Pan, G., Wu, S., Hu, Q., Jiang, H., et al. (2019). Treadmill exercise ameliorates focal cerebral ischemia/reperfusion-induced neurological deficit by promoting dendritic modification and synaptic plasticity via upregulating caveolin-1/VEGF signaling pathways. Experimental Neurology, 313, 60–78.PubMed Xie, Q., Cheng, J., Pan, G., Wu, S., Hu, Q., Jiang, H., et al. (2019). Treadmill exercise ameliorates focal cerebral ischemia/reperfusion-induced neurological deficit by promoting dendritic modification and synaptic plasticity via upregulating caveolin-1/VEGF signaling pathways. Experimental Neurology, 313, 60–78.PubMed
go back to reference Xing, Y., Yang, S. D., Dong, F., Wang, M. M., Feng, Y. S., & Zhang, F. (2018). The beneficial role of early exercise training following stroke and possible mechanisms. Life Sciences, 198, 32–37.PubMed Xing, Y., Yang, S. D., Dong, F., Wang, M. M., Feng, Y. S., & Zhang, F. (2018). The beneficial role of early exercise training following stroke and possible mechanisms. Life Sciences, 198, 32–37.PubMed
go back to reference Zhang, F., Wu, Y., & Jia, J. (2011). Exercise preconditioning and brain ischemic tolerance. Neuroscience, 177, 170–176.PubMed Zhang, F., Wu, Y., & Jia, J. (2011). Exercise preconditioning and brain ischemic tolerance. Neuroscience, 177, 170–176.PubMed
go back to reference Zhang, Q., Zhang, L., Yang, X., Wan, Y., & Jia, J. (2014). The effects of exercise preconditioning on cerebral blood flow change and endothelin-1 expression after cerebral ischemia in rats. Journal of Stroke and Cerebrovascular Diseases, 23(6), 1696–1702.PubMed Zhang, Q., Zhang, L., Yang, X., Wan, Y., & Jia, J. (2014). The effects of exercise preconditioning on cerebral blood flow change and endothelin-1 expression after cerebral ischemia in rats. Journal of Stroke and Cerebrovascular Diseases, 23(6), 1696–1702.PubMed
go back to reference Zhang, Q. W., Deng, X. X., Sun, X., Xu, J. X., & Sun, F. Y. (2013). Exercise promotes axon regeneration of newborn striatonigral and corticonigral projection neurons in rats after ischemic stroke. PLoS ONE, 8(11), e80139.PubMedPubMedCentral Zhang, Q. W., Deng, X. X., Sun, X., Xu, J. X., & Sun, F. Y. (2013). Exercise promotes axon regeneration of newborn striatonigral and corticonigral projection neurons in rats after ischemic stroke. PLoS ONE, 8(11), e80139.PubMedPubMedCentral
go back to reference Zwagerman, N., Sprague, S., Davis, M. D., Daniels, B., Goel, G., & Ding, Y. (2010). Pre-ischemic exercise preserves cerebral blood flow during reperfusion in stroke. Neurological Research, 32(5), 523–529.PubMed Zwagerman, N., Sprague, S., Davis, M. D., Daniels, B., Goel, G., & Ding, Y. (2010). Pre-ischemic exercise preserves cerebral blood flow during reperfusion in stroke. Neurological Research, 32(5), 523–529.PubMed
Metadata
Title
A Short Bout of Exercise Prior to Stroke Improves Functional Outcomes by Enhancing Angiogenesis
Authors
Stefano Pianta
Jea Young Lee
Julian P. Tuazon
Vanessa Castelli
Leigh Monica Mantohac
Naoki Tajiri
Cesar V. Borlongan
Publication date
01-12-2019
Publisher
Springer US
Keyword
Stroke
Published in
NeuroMolecular Medicine / Issue 4/2019
Print ISSN: 1535-1084
Electronic ISSN: 1559-1174
DOI
https://doi.org/10.1007/s12017-019-08533-x

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