Resilience to Alzheimer’s disease: The role of physical activity

Current Alzheimer Research

Volumn 14, Issue 5, 2017, Pages 546-553

  Pedrinolla, Anna ^a   Schen, Federico ^b   Venturelli, Massimo ^b  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

Author keywords

Alzheimer's disease; Brain resilience; Cardiovascular resilience; Exercise; Mitochondrial resilience; Neuroendocrine resilience

Indexed keywords

ALZHEIMER DISEASE; BRAIN; CARDIOVASCULAR SYSTEM; EXERCISE; HUMAN; MEDLINE; MITOCHONDRION; NEUROENDOCRINE SYSTEM; NEUROLOGIC DISEASE ASSESSMENT; OUTCOMES RESEARCH; PATHOLOGY; PHYSICAL ACTIVITY; PRIORITY JOURNAL; REVIEW;

EID: 85019709323     PISSN: 15672050     EISSN: 18755828     Source Type: Journal    
DOI: 10.2174/1567205014666170111145817     Document Type: Review

References (76)

1. Feldman HH, Haas M, Gandy S, Schoepp DD, Cross AJ, Mayeux R, et al. Alzheimer's disease research and development: a call for a new research roadmap. Ann NY Acad Sci 1313: 1-16 (2014).
2. Pistollato F, Ohayn EL, Lam A, Langley GR, Novak TJ, Pamies D, et al. Alzheimer disease research in the 21st century: past and current failures, new perspectives and funding priorities. Oncotarget 7(26): 18 (2016).
3. De-Paula VJ, Radanovic M, Diniz BS, Forlenza OV. Alzheimer's disease. Sub-cell Biochem 65: 329-52 (2012).
4. Mayeux R, Stern Y. Epidemiology of Alzheimer disease. Cold Spring Harb Perspect Med 2(8): pii: a006239 (2012).
5. Dede DS, Yavuz B, Yavuz BB, Cankurtaran M, Halil M, Ulger Z, et al. Assessment of endothelial function in Alzheimer's disease: is Alzheimer's disease a vascular disease? J Am Geriatr Soc 55(10): 1613-7 (2007).
6. Geerlings MI, Sigurdsson S, Eiriksdottir G, Garcia M, Launer L. Salivary cortisol, brain volumes, and cognition in communitydwelling elderly without dementia. Am Acad Neurol 85(15): 973-83 (2015).
7. Popa-Wagner A, Mitran S, Sivanesan S, Chang E, Buga AM. ROS and brain diseases: the good, the bad, and the ugly. Oxid Med Cell Longev 2013: 963520 (2013).
8. Jelliger KA, Attems JA. Neuropathological approaches to cerebral aging and neuroplasticity. Dialogues Clin Neurosci 15(1): 29-43 (2013).
9. Whitson HE, Duan-Porter WD, Schmader KE, Morey MC, Cohen HJ, Colon-Emeric CS. Physical resilience in older adults: systematic review and development of an emerging construct. J Gerontol A Biol Sci Med Sci 71(4): 489-95 (2016).
10. Negash S, Xie S, Davatzikos C, Clark CM, Trojanowski JQ, Shaw LM, et al. Cognitive and functional resilience despite molecular evidence of Alzheimer's disease pathology. Alzheimer's Dement 9(3): e89-95 (2013).
11. Forbes D, Thiessen EJ, Blake CM, Forbes SC, Forbes S. Exercise programs for people with dementia. Cochrane Database Syst Rev (12): CD006489 (2013).
12. Venturelli M, Lanza M, Muti E, Schena F. Positive effects of physical training in activity of daily living-dependent older adults. Exp Aging Res 36(2): 190-205 (2010).
13. Venturelli M, Scarsini R, Schena F. Six-month walking program changes cognitive and ADL performance in patients with Alzheimer. Am J Alzheimers Dis Other Demen 26(5): 381-8 (2011).
14. Santos-Lozano A, Pareja-Galeano H, Sanchis-Gomar F, Quindos-Rubial M, Fiuza-Luces C, Cristi-Montero C, et al. Physical activity and alzheimer disease: a protective association. Mayo Clin Proc 91(8): 12 (2016).
15. Reitz C, Brayne C, Mayeux R. Epidemiology of Alzheimer disease. Nat Rev Neurol 7(3): 137-52 (2011).
16. Reitz C, Mayeux R. Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem Pharmacol 88(4): 640-51 (2014).
17. Groot C, Hooghiemstra AM, Raijmakers PG, van Berckel BN, Scheltens P, Scherder EJ, et al. The effect of physical activity on cognitive function in patients with dementia: A meta-analysis of randomized control trials. Ageing Res Rev 25: 13-23 (2016).
18. Lange-Asschenfeldt C, Kojda G. Alzheimer's disease, cerebrovascular dysfunction and the benefits of exercise: from vessels to neurons. Exp Gerontol 43(6): 499-504 (2008).
19. Marques-Aleixo I, Oliveira PJ, Moreira PI, Magalhaes J, Ascensao A. Physical exercise as a possible strategy for brain protection: evidence from mitochondrial-mediated mechanisms. Prog Neurobiol 99(2): 149-62 (2012).
20. Schultz SA, Boots EA, Almeida RP, Oh JM, Einerson J, Korcarz CE, et al. Cardiorespiratory fitness attenuates the influence of amyloid on cognition. J Intern Neuropsychol Soc 21(10): 841-50 (2015).
21. Souza LC, Filho CB, Goes AT, Fabbro LD, de Gomes MG, Savegnago L, et al. Neuroprotective effect of physical exercise in a mouse model of Alzheimer's disease induced by beta-amyloid(1)(-)(4)(0) peptide. Neurotox Res 24(2): 148-63 (2013).
22. Hare BD, Beierle JA, Toufexis DJ, Hammack SE, Falls WA. Exercise-associated changes in the corticosterone response to acute restraint stress: evidence for increased adrenal sensitivity and reduced corticosterone response duration. Neuropsychopharmacology 39(5): 1262-9 (2014).
23. Alleman RJ, Stewart LM, Tsang AM, Brown DA. Why does exercise "trigger" adaptive protective responses in the heart? Dose-Response 13(1): Pii (2015).
24. Geary K, Knaub LA, Schauer IE, Keller AC, Watson PA, Miller MW, et al. Targeting mitochondria to restore failed adaptation to exercise in diabetes. Biochem Soc Trans 42(2): 231-8 (2014).
25. Park SY, Rossman MJ, Gifford JR, Bharath LP, Bauersachs J, Richardson RS, et al. Exercise training improves vascular mitochondrial function. Am J Physiol Heart Circ Physiol 310(7): H821-9 (2016).
26. Ristow M, Zarse K. How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 45(6): 410-8 (2010).
27. Gerecke KM, Kolobova A, Allen S, Fawer JL. Exercise protects against chronic restraint stress-induced oxidative stress in the cortex and hippocampus. Brain Res 1509: 66-78 (2013).
28. Radak Z, Chung HY, Goto S. Systemic adaptation to oxidative challenge induced by regular exercise. Free Rad Biol Med 44(2): 153-9 (2008).
29. Radak Z, Suzuki K, Higuchi M, Balogh L, Boldogh I, Koltai E. Physical exercise, reactive oxygen species and neuroprotection. Free Radic Biol Med 98: 187-96 (2016).
30. Stranahn AM, Martin B, Maudsley S. Anti-inflammatory effects of physical activity in relationship to improved cognitive status in humans and mouse models of alzheimer's disease. Curr Alzheimer Res 9: 86-92 (2012).
31. Burns JM, Swerdlow RH. Effect of high-intensity exercise on aged mouse brain mitochondria, neurogenesis, and inflammation. Neurobiol Aging 35(11): 2574-83 (2014).
32. Silverman MN, Deuster PA. Biological mechanisms underlying the role of physical fitness in health and resilience. Interface Focus 4(5): 20140040 (2014).
33. Bozzali M, Dowling C, Serra L, Spanò B, Torso M, Marra C, et al. The impact of cognitive reserve on brain functional connectivity in Alzheimer's disease. J Alzheimer's Dis 44: 243-50 (2015).
34. Wook Yoo S, Han CE, Shin JS, Won Seo S, Na DL, Kaiser M, et al. A network flow-based analysis of cognitive reserve in normal ageing and Alzheimer's disease. Sci Rep 5: 10057 (2015).
35. Cavedo E, Galluzzi S, Pievani M, Boccardi M, Frisoni GB. Norms for imaging makers of brain reserve. J Alzheimer Dis 31: 623-33 (2012).
36. Isacson O. On neuronal health. Trends Nanosci 16(8): 306-8 (1993).
37. Rothman SM, Mattson MP. Activity-dependent, stress-responsive BDNF signaling and the quest for optimal brain health and resilience throughout the lifespan. Neuroscience 239: 228-40 (2013).
38. Bramham CR, Messaoudi E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76(2): 99-125 (2005).
39. Karatsoreos IN, McEwen BS. Resilience and vulnerability: a neurobiological perspective. F1000 Prime Rep 5: 13 (2013).
40. McEwen BS, Bowles NP, Gray JD, Hill MN, Hunter RG, Karatsoreos IN, et al. Mechanisms of stress in the brain. Nat Neurosci 18(10): 1353-63 (2015).
41. Mang CS, Campbell KL, Ross CJ, Boyd LA. Promoting neuroplasticity for motor rehabilitation after stroke: considering the effects of aerobic exercise and genetic variation on brain-derived neurotrophic factor. Phy Ther 93(12): 1707-16 (2013).
42. Kaliman P, Parrizas M, Lalanza JF, Camins A, Escorihuela RM, Pallas M. Neurophysiological and epigenetic effects of physical exercise on the aging process. Ageing Res Rev 10(4): 475-86 (2011).
43. Tortosa-Martinez J, Clow A. Does physical activity reduce risk for Alzheimer's disease through interaction with the stress neuroendocrine system? Stress 15(3): 243-61 (2012).
44. Nation DA, Hong S, Jak AJ, Delano-Wood L, Mills PJ, Bondi MW, et al. Stress, exercise, and Alzheimer's disease: a neurovascular pathway. Med Hypotheses 76(6): 847-54 (2011).
45. Lehallier B, Essioux L, Gayan J, Alexandridis R, Nikolcheva T, Wyss-Coray T, et al. Combined plasma and cerebrospinal fluid signature for the prediction of midterm progression from mild cognitive impairment to Alzheimer disease. JAMA Neurol 1-10 (2015).
46. Venturelli M, Scarsini R, Salvagno GL, Schena F. Sundowning syndrome and hypotalamic-pituitary-adrenal axis dysregulation in individual with alzheimer's disease: is there an association? J Am Geriatr Soc 61(11): 2055-6 (2013).
47. Venturelli M, Cè E, Limonta E, Muti E, Scarsini R, Brasioli A, et al. Possible predictors of involuntary weight loss in patients with Alzheimer’s disease. PLoS One 11(6): e0157384 (2016).
48. Yau SY, Li A, Zhang ED, Christie BR, Xu A, Lee TM, et al. 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 Trans 23(4-5): 481-92 (2014).
49. Lucertini F, Ponzio E, Di Palma M, Galati C, Federici A, Barbadoro P, et al. High cardiorespiratory fitness is negatively associated with daily cortisol output in healthy aging men. PloS one 10(11): e0141970 (2015).
50. Venturelli M, Sollima A, Cè E, Limonta E, Bisconti AV, Brasioli A, et al. Effectiveness of exercise-and cognitive-based treatments on salivary cortisol levels and sundowning syndrome symptoms in patients with Alzheimer’s disease. J Alzheimers Dis 53(4): 1631-40 (2016).
51. Lakatta EG. So! What's aging? Is cardiovascular aging a disease? J Mol Cell Cardiol 83: 1-13 (2015).
52. Picano E, Bruno RM, Ferrari GF, Bonuccelli U. Cognitive impairment and cardiovascular disease: so near, so far. Intern J Cardiol 175(1): 21-9 (2014).
53. de la Torre JC. The vascula hypothesis of Alzheimer's Disease: bench to bedside and beyond. Neurodegenerative Dis 7: 116-21 (2010).
54. de la Torre JC. Alzheimer's disease is a vasocognopathy: a new term to describe its nature. Neurol Res 26: 517-24 (2004).
55. Popa-Wagner A, Buga AM, Popescu B, Muresanu D. Vascular cognitive impairment, dementia, aging and energy demand. A vicious cycle. J Neural Transm 122(1): S47-54 (2015).
56. Di Marco LY, Farkas E, Martin C, Venneri A, Frangi AF. Is vasomotion in cerebral arteries impaired in Alzheimer's disease? J Alzheimer's Dis 46(1): 35-53 (2015).
57. Carmichael O. Preventing vascular effects on brain injury and cognition late in life: knowns and unknowns. Neuropsychol Rev 24(3): 371-87 (2014).
58. Katusic ZS, Austin SA. Endothelial nitric oxide: protector of a healthy mind. Eur Heart J 35(14): 888-94 (2014).
59. Seals DR, Jablonski KL, Donato AJ. Aging and vascular endothelial function in humans. Clin Sci 120(9): 357-75 (2011).
60. Aliyev A, Seyidova D, Rzayev N, Obrenovich ME, Lamb BT, Chen SG, et al. Is nitric oxide a key target in the pathogenesis of brain lesions during the development of Alzheimer's disease? Neurol Res 26: 547-53 (2004).
61. Seifert T, Secher NH. Sympathetic influence on cerebral blood flow and metabolism during exercise in humans. Prog Neurobiol 95(3): 406-26 (2011).
62. Ramos ES, Larsson NG, Mourier A. Bioenergetic roles of mitochondrial fusion. Biochimica et Biophysica Acta 1857(8): 1277-83 (2016).
63. Bhat AH, Dar KB, Anees S, Zargar MA, Masood A, Sofi MA, et al. Oxidative stress, mitochondrial dysfunction and neurodegenerative diseases; a mechanistic insight. Biomed Pharmacother 74: 101-10 (2015).
64. Demetrius LA, Driver J. Alzheimer's as a metabolic disease. Biogerontology 14(6): 641-9 (2013).
65. Morris JK, Honea RA, Vidoni ED, Swerdlow RH, Burns JM. Is Alzheimer's disease a systemic disease? Biochimica et Biophysica Acta 1842(9): 1340-9 (2014).
66. Swerdlow RH, Burns JM, Khan SM. The Alzheimer's disease mitochondrial cascade hypothesis. J Alzheimer's Dis 20(2): S265-79 (2010).
67. Navarro A, Boveris A. The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol 292(2): C670-86 (2007).
68. Venturelli M, Morgan GR, Donato AJ, Reese V, Bottura R, Tarperi C, et al. Cellular aging of skeletal muscle: telomeric and free radical evidence that physical inactivity is responsible and not age. Clin Sci 127(6): 415-21 (2014).
69. Cadonic C, Sabbir MG, Albensi BC. Mechanisms of mitochondrial dysfunction in Alzheimer's disease. Mol Neurobiol 53(9): 6078-6090 (2016).
70. Dai DF, Rabinovitch PS, Ungvari Z. Mitochondria and cardiovascular aging. Circ Res 110(8): 1109-24 (2012).
71. El Assar M, Angulo J, Rodriguez-Manas L. Oxidative stress and vascular inflammation in aging. Free Rad Biol Med 65: 380-401 (2013).
72. Swerdlow RH. Brain aging, Alzheimer's disease, and mitochondria. Biochimica et Biophysica Acta 1812(12): 1630-9 (2011).
73. Navarro A, Boveris A. Rat brain and liver mitochondria develop oxidative stress and lose enzymatic activities on aging. Am J Physiol Regul Integr Comp Physiol 287(5): R1244-9 (2004).
74. Gerhart-Hines Z, Rodgers T, Bare O, Lerin C, Kim SH, Mostoslavsky R, et al. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1a. EMBO J 26: 1913-23 (2007).
75. Bayod S, Del Valle J, Canudas AM, Lalanza JF, Sanchez-Roige S, Camins A, et al. Long-term treadmill exercise induces neuroprotective molecular changes in rat brain. J Appl Physiol 111(5): 1380-90 (2011).
76. Steiner JL, Murphy EA, McClellan JL, Carmichael MD, Davis JM. Exercise training increases mitochondrial biogenesis in the brain. J Appl Physiol 111(4): 1066-71 (2011).