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Protective effect of maternal exercise against amyloid-β neurotoxicity in the male rat offspring’s cerebellum

Part of: DOHaD Research in Latin-American

Published online by Cambridge University Press:  23 June 2020

Caroline Peres Klein ,
Juliana Bender Hoppe ,
André Brum Saccomori ,
Bernardo Gindri dos Santos Open the ORCID record for Bernardo Gindri dos Santos [Opens in a new window] ,
Pauline Maciel August ,
Isadora Peres Klein ,
Mariana Scortegagna Crestani ,
Felippo Bifi ,
Régis Mateus Hözer  and
Plácido Navas
...Show all authors
Caroline Peres Klein
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Juliana Bender Hoppe
Affiliation:
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
André Brum Saccomori
Affiliation:
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Bernardo Gindri dos Santos
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Pauline Maciel August
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Isadora Peres Klein
Affiliation:
Programa de Pós-Graduação em Patologia Oral, Faculdade de Odontologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Mariana Scortegagna Crestani
Affiliation:
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Felippo Bifi
Affiliation:
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Régis Mateus Hözer
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Plácido Navas
Affiliation:
Centro Andaluz de Biología del Desarrollo and CIBERER, Instituto de Salud Carlos III, Universidad Pablo de Olavide-CSIC-JA, 41013Sevilla, Spain
Christianne Gazzana Salbego
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Cristiane Matté*
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil Programa de Pós-Graduação em Ciências Biológicas – Fisiologia, Departamento de Fisiologia, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
*
Address for correspondence: Cristiane Matté, Rua Ramiro Barcelos, 2600-Anexo, Porto Alegre Zip Code: 90035-003, RS, Brazil. Email: [email protected]
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Abstract

The Developmental Origins of Health and Disease (DOHaD) states that intrauterine maternal environment influences postnatal life by programming offspring’s metabolism. Intrauterine milieu induced by exercise during pregnancy promotes long-lasting benefits to the offspring’s health and seems to offer some resistance against chronic diseases in adult life. Alzheimer’s disease is a public health concern with limited treatment options. In the present study, we assessed the potential of maternal exercise during pregnancy in long-term programming of young adult male rat offspring’s cerebellar metabolism in conferring neuroprotection against amyloid-β (Aβ) neurotoxicity. Female Wistar rats were submitted to a swimming protocol 1 week prior mating and throughout pregnancy (five sessions/a week lasting 30 min). Aβ oligomers were infused bilaterally in the brain ventricles of 60-day-old male offspring. Fourteen days after surgery, we measured parameters related to redox state, mitochondrial function, and the immunocontent of proteins related to synaptic function. We found that maternal exercise during pregnancy attenuated several parameters in the offspring’s male rat cerebellum, such as the reactive species rise, the increase of inducible nitric oxide synthase immunocontent and tau phosphorylation induced by Aβ oligomers, increased mitochondrial fission indicated by dynamin-related protein 1 (DRP1), and protein oxidation identified by carbonylation. Strikingly, we find that maternal exercise promotes changes in the rat offspring’s cerebellum that are still evident in young adult life. These favorable neurochemical changes in offspring’s cerebellum induced by maternal exercise may contribute to a protective phenotype against Aβ-induced neurotoxicity in young adult male rat offspring.

Keywords

Intrauterine metabolic programmingDOHADexercisebioenergeticsAlzheimer’s disease
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 5 , October 2020 , pp. 521 - 532
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

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References

Hanson, MA, Gluckman, PD.Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev. 2014; 94(4), 1027–1076.CrossRefGoogle ScholarPubMed
Harris, JE, Baer, LA, Stanford, KI.Maternal exercise improves the metabolic health of adult offspring. Trends Endocrinol Metabolism TEM. 2018; 29(3), 164–177.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA, Buklijas, T.A conceptual framework for the developmental origins of health and disease. J Dev Origins Health Disease. 2010; 1(1), 6–18.CrossRefGoogle ScholarPubMed
Bateson, P, Gluckman, P, Hanson, M.The biology of developmental plasticity and the predictive adaptive response hypothesis. J Physiol. 2014; 592(11), 2357–2368.CrossRefGoogle ScholarPubMed
Bale, TL.Epigenetic and transgenerational reprogramming of brain development. Nat Rev Neurosci. 2015; 16(6), 332–344.CrossRefGoogle ScholarPubMed
Barnes, SK, Ozanne, SE.Pathways linking the early environment to long-term health and lifespan. Prog Biophys Mol Biol. 2011; 106(1), 323–336.CrossRefGoogle ScholarPubMed
Marcelino, TB, Longoni, A, Kudo, KY, et al.Evidences that maternal swimming exercise improves antioxidant defenses and induces mitochondrial biogenesis in the brain of young Wistar rats. Neuroscience. 2013; 246, 28–39.CrossRefGoogle ScholarPubMed
Klein, CP, Hoppe, JB, Saccomori, AB, et al.Physical exercise during pregnancy prevents cognitive impairment induced by amyloid-beta in adult offspring rats. Mol Neurobiol. 2018; doi: 10.1007/s12035-018-1210-x.CrossRefGoogle Scholar
Carter, LG, Qi, NR, De Cabo, R, Pearson, KJ.Maternal exercise improves insulin sensitivity in mature rat offspring. Med Sci Sports Exercise. 2013; 45(5), 832–840.CrossRefGoogle ScholarPubMed
Akhavan, MM, Emami-Abarghoie, M, Safari, M, et al.Serotonergic and noradrenergic lesions suppress the enhancing effect of maternal exercise during pregnancy on learning and memory in rat pups. Neuroscience. 2008; 151(4), 1173–1183.CrossRefGoogle ScholarPubMed
Bick-Sander, A, Steiner, B, Wolf, SA, Babu, H, Kempermann, G.Running in pregnancy transiently increases postnatal hippocampal neurogenesis in the offspring. PNAS. 2006; 103(10), 3852–3857.CrossRefGoogle ScholarPubMed
Gomes da Silva, S, de Almeida, AA, Fernandes, J, et al.Maternal exercise during pregnancy increases BDNF levels and cell numbers in the hippocampal formation but not in the cerebral cortex of adult rat offspring. PLoS One 2016; 11(1), e0147200.CrossRefGoogle Scholar
Klein, CP, Dos Santos Rodrigues, K, Hozer, RM, et al.Swimming exercise before and during pregnancy: promising preventive approach to impact offspring s health. Int J Dev Neurosci. 2018; 71, 83–93.CrossRefGoogle Scholar
Herring, A, Donath, A, Yarmolenko, M, et al.Exercise during pregnancy mitigates Alzheimer-like pathology in mouse offspring. FASEB J. 2012; 26(1), 117–128.CrossRefGoogle ScholarPubMed
Stanford, KI, Lee, MY, Getchell, KM, So, K, Hirshman, MF, Goodyear, LJ.Exercise before and during pregnancy prevents the deleterious effects of maternal high-fat feeding on metabolic health of male offspring. Diabetes. 2015; 64(2), 427–433.CrossRefGoogle ScholarPubMed
Wasinski, F, Bacurau, RF, Estrela, GR, et al.Exercise during pregnancy protects adult mouse offspring from diet-induced obesity. Nutrition Metabolism. 2015; 12, 56.CrossRefGoogle ScholarPubMed
Sheldon, RD, Nicole Blaize, A, Fletcher, JA, et al.Gestational exercise protects adult male offspring from high-fat diet-induced hepatic steatosis. J Hepatol. 2016; 64(1), 171–178.CrossRefGoogle ScholarPubMed
Camarillo, IG, Clah, L, Zheng, W, et al.Maternal exercise during pregnancy reduces risk of mammary tumorigenesis in rat offspring. Eur J Cancer Prevention. 2014; 23(6), 502–505.CrossRefGoogle ScholarPubMed
Robinson, AM, Bucci, DJ.Physical exercise during pregnancy improves object recognition memory in adult offspring. Neuroscience. 2014; 256, 53–60.CrossRefGoogle ScholarPubMed
Kim, MJ, Han, CW, Min, KY, et al.Physical exercise with multicomponent cognitive intervention for older adults with Alzheimer’s disease: a 6-month randomized controlled trial. Dementia Geriatric Cognitive Disorders Extra. 2016;6(2), 222–232.CrossRefGoogle ScholarPubMed
Maliszewska-Cyna, E, Lynch, M, Oore, JJ, Nagy, PM, Aubert, I.The benefits of exercise and metabolic interventions for the prevention and early treatment of Alzheimer’s disease. Current Alzheimer Res. 2016.CrossRefGoogle Scholar
Palleschi, L, Vetta, F, De Gennaro, E, et al.Effect of aerobic training on the cognitive performance of elderly patients with senile dementia of Alzheimer type. Arch Gerontol Geriatrics. 1996; 22(Suppl 1), 47–50.CrossRefGoogle ScholarPubMed
Vidoni, ED, Johnson, DK, Morris, JK, et al.Dose-response of aerobic exercise on cognition: a community-based, pilot randomized controlled trial. PLoS One 2015; 10(7), e0131647.CrossRefGoogle Scholar
Labonte-Lemoyne, E, Curnier, D, Ellemberg, D.Exercise during pregnancy enhances cerebral maturation in the newborn: a randomized controlled trial. J Clin Exp Neuropsychol. 2016; 1–8.doi: 10.1080/13803395.2016.1227427.CrossRefGoogle Scholar
Jukic, AM, Lawlor, DA, Juhl, M, et al.Physical activity during pregnancy and language development in the offspring. Paediatric Perinatal Epidemiol. 2013; 27(3), 283–293.CrossRefGoogle ScholarPubMed
Marcelino, TB, de Lemos Rodrigues, PI, Klein, CP, et al.Behavioral benefits of maternal swimming are counteracted by neonatal hypoxia-ischemia in the offspring. Behav Brain Res. 2016; 312, 30–38.CrossRefGoogle ScholarPubMed
Akhavan, MM, Foroutan, T, Safari, M, Sadighi-Moghaddam, B, Emami-Abarghoie, M, Rashidy-Pour, A.Prenatal exposure to maternal voluntary exercise during pregnancy provides protection against mild chronic postnatal hypoxia in rat offspring. Pakistan J. Pharmaceutical Sci. 2012; 25(1), 233–238.Google ScholarPubMed
Kim, H, Lee, SH, Kim, SS, Yoo, JH, Kim, CJ.The influence of maternal treadmill running during pregnancy on short-term memory and hippocampal cell survival in rat pups. Int J Dev Neurosci. 2007; 25(4), 243–249.CrossRefGoogle ScholarPubMed
Reitz, C, Mayeux, R.Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem Pharmacol. 2014; 88(4), 640–651.CrossRefGoogle ScholarPubMed
Dumont, M, Lin, MT, Beal, MF.Mitochondria and antioxidant targeted therapeutic strategies for Alzheimer’s disease. J Alzheimer’s Disease. 2010; 20(Suppl 2), S633–643.CrossRefGoogle ScholarPubMed
Querfurth, HW, LaFerla, FM.Alzheimer’s disease. N Engl J Med. 2010; 362(4), 329–344.CrossRefGoogle ScholarPubMed
Abolhassani, N, Leon, J, Sheng, Z, et al.Molecular pathophysiology of impaired glucose metabolism, mitochondrial dysfunction, and oxidative DNA damage in Alzheimer’s disease brain. Mech Ageing Dev. 2017; 161(Pt A), 95–104.CrossRefGoogle ScholarPubMed
Wojsiat, J, Zoltowska, KM, Laskowska-Kaszub, K, Wojda, U.Oxidant/antioxidant imbalance in Alzheimer’s disease: therapeutic and diagnostic prospects. Oxid Med Cell Longevity 2018; 2018, 6435861.CrossRefGoogle ScholarPubMed
Sultana, R, Perluigi, M, Butterfield, DA.Redox proteomics identification of oxidatively modified proteins in Alzheimer’s disease brain and in vivo and in vitro models of AD centered around Abeta(1-42). J Chromatogr B 2006; 833(1), 3–11.CrossRefGoogle Scholar
Timmann, D, Drepper, J, Frings, M, et al.The human cerebellum contributes to motor, emotional and cognitive associative learning. a review. Cortex. 2010; 46(7), 845–857.CrossRefGoogle ScholarPubMed
Mattson, MP.Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metab. 2012; 16(6), 706–722.CrossRefGoogle Scholar
Klein, WL.Abeta toxicity in Alzheimer’s disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem Int. 2002; 41(5), 345–352.CrossRefGoogle ScholarPubMed
Hoppe, JB, Coradini, K, Frozza, RL, et al.Free and nanoencapsulated curcumin suppress beta-amyloid-induced cognitive impairments in rats: involvement of BDNF and Akt/GSK-3beta signaling pathway. Neurobiol Learn. Memory. 2013; 106, 134–144.CrossRefGoogle ScholarPubMed
Paxinos, G, Watson, C.The Rat Brain in Stereotaxic Coordinates, 2005. Elsevier Academic Press.Google Scholar
Misra, HP, Fridovich, I.The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247(10), 3170–3175.Google Scholar
Aebi, H.Catalase in vitro. Methods Enzymol. 1984; 105, 121–126.CrossRefGoogle ScholarPubMed
Wendel, A.Glutathione peroxidase. Methods Enzymol. 1981; 77, 325–333.CrossRefGoogle ScholarPubMed
Browne, RW, Armstrong, D.Reduced glutathione and glutathione disulfide. Methods Mol Biol. 1998; 108, 347–352.Google ScholarPubMed
Aksenov, MY, Markesbery, WR.Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer’s disease. Neurosci Lett 2001; 302(2–3), 141–145.CrossRefGoogle ScholarPubMed
Reznick, AZ, Packer, L.Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol. 1994; 233, 357–363.CrossRefGoogle ScholarPubMed
Grings, M, Moura, AP, Parmeggiani, B, et al.Higher susceptibility of cerebral cortex and striatum to sulfite neurotoxicity in sulfite oxidase-deficient rats. BBA. 2016; 1862(11), 2063–2074.Google ScholarPubMed
Fischer, JC, Ruitenbeek, W, Berden, JA, et al.Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta. 1985; 153(1), 23–36.CrossRefGoogle ScholarPubMed
Rustin, P, Chretien, D, Bourgeron, T, et al.Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta. 1994; 228(1), 35–51.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL, Randall, RJ.Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1), 265–275.Google ScholarPubMed
Reddy, PH.Amyloid beta-induced glycogen synthase kinase 3beta phosphorylated VDAC1 in Alzheimer’s disease: implications for synaptic dysfunction and neuronal damage. BBA. 2013; 1832(12), 1913–1921.Google ScholarPubMed
Rice, D, Barone, S Jr.Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000; 108(Suppl 3), 511–533.Google ScholarPubMed
Park, JW, Kim, MH, Eo, SJ, et al.Maternal exercise during pregnancy affects mitochondrial enzymatic activity and biogenesis in offspring brain. Int J Neurosci. 2013; 123(4), 253–264.CrossRefGoogle ScholarPubMed
Webb, R, Hughes, MG, Thomas, AW, Morris, K.The ability of exercise-associated oxidative stress to trigger redox-sensitive signalling responses. Antioxidants. 2017; 6(3), 63.CrossRefGoogle ScholarPubMed
Calabrese, EJ, Baldwin, LA.Hormesis: a generalizable and unifying hypothesis. Crit Rev Toxicol. 2001; 31(4–5), 353–424.CrossRefGoogle ScholarPubMed
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. 2012; 99(2), 149–162.CrossRefGoogle ScholarPubMed
Knott, AB, Perkins, G, Schwarzenbacher, R, Bossy-Wetzel, E.Mitochondrial fragmentation in neurodegeneration. Nat Rev Neurosci. 2008; 9(7), 505–518.CrossRefGoogle ScholarPubMed
Chalimoniuk, M, Chrapusta, SJ, Lukacova, N, Langfort, J.Endurance training upregulates the nitric oxide/soluble guanylyl cyclase/cyclic guanosine 3ʹ,5ʹ-monophosphate pathway in the striatum, midbrain and cerebellum of male rats. Brain Res. 2015; 1618, 29–40.CrossRefGoogle ScholarPubMed
Marques-Aleixo, I, Santos-Alves, E, Balca, MM, et al.Physical exercise improves brain cortex and cerebellum mitochondrial bioenergetics and alters apoptotic, dynamic and auto(mito)phagy markers. Neuroscience. 2015; 301, 480–495.CrossRefGoogle ScholarPubMed
Cheng, A, Yang, Y, Zhou, Y, et al.Mitochondrial SIRT3 mediates adaptive responses of neurons to exercise and metabolic and excitatory challenges. Cell Metab. 2016; 23(1), 128–142.CrossRefGoogle ScholarPubMed
Garry, PS, Ezra, M, Rowland, MJ, Westbrook, J, Pattinson, KT.The role of the nitric oxide pathway in brain injury and its treatment—from bench to bedside. Exp Neurol. 2015; 263, 235–243.CrossRefGoogle ScholarPubMed
Furini, CR, Rossato, JI, Bitencourt, LL, Medina, JH, Izquierdo, I, Cammarota, M.Beta-adrenergic receptors link NO/sGC/PKG signaling to BDNF expression during the consolidation of object recognition long-term memory. Hippocampus. 2010;20(5), 672–683.Google ScholarPubMed
Llansola, M, Hernandez-Viadel, M, Erceg, S, Montoliu, C, Felipo, V.Increasing the function of the glutamate-nitric oxide-cyclic guanosine monophosphate pathway increases the ability to learn a Y-maze task. J Neurosci Res. 2009; 87(10), 2351–2355.CrossRefGoogle Scholar
Gertz, K, Priller, J, Kronenberg, G, et al.Physical activity improves long-term stroke outcome via endothelial nitric oxide synthase-dependent augmentation of neovascularization and cerebral blood flow. Circulation Res. 2006; 99(10), 1132–1140.CrossRefGoogle ScholarPubMed
Liu, X, le Yang, J, Fan, SJ, Jiang, H, Pan, F.Swimming exercise effects on the expression of HSP70 and iNOS in hippocampus and prefrontal cortex in combined stress. Neurosci Lett. 2010; 476(2), 99–103.CrossRefGoogle ScholarPubMed
Real, CC, Garcia, PC, Britto, LRG, Pires, RS.Different protocols of treadmill exercise induce distinct neuroplastic effects in rat brain motor areas. Brain Res. 2015; 1624, 188–198.CrossRefGoogle ScholarPubMed
Liu, W, Xue, X, Xia, J, Liu, J, Qi, Z.Swimming exercise reverses CUMS-induced changes in depression-like behaviors and hippocampal plasticity-related proteins. J Affective Disorders. 2018; 227, 126–135.CrossRefGoogle ScholarPubMed
Kuwabara, Y, Ishizeki, M, Watamura, N, et al.Impairments of long-term depression induction and motor coordination precede Abeta accumulation in the cerebellum of APPswe/PS1dE9 double transgenic mice. J Neurochem. 2014; 130(3), 432–443.CrossRefGoogle ScholarPubMed
Lee, JM, Shin, MS, Ji, ES, et al.Treadmill exercise improves motor coordination through ameliorating Purkinje cell loss in amyloid beta23-35-induced Alzheimer’s disease rats. J Exercise Rehab. 2014; 10(5), 258–264.CrossRefGoogle ScholarPubMed
Kozuki, M, Kurata, T, Miyazaki, K, et al.Atorvastatin and pitavastatin protect cerebellar Purkinje cells in AD model mice and preserve the cytokines MCP-1 and TNF-alpha. Brain Res. 2011; 1388, 32–38.CrossRefGoogle ScholarPubMed
Myhre, O, Andersen, JM, Aarnes, H, Fonnum, F.Evaluation of the probes 2ʹ,7ʹ-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation. Biochem Pharmacol. 2003; 65(10), 1575–1582.CrossRefGoogle ScholarPubMed
Kalyanaraman, B, Darley-Usmar, V, Davies, KJ, et al.Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radical Biol Med. 2012; 52(1), 1–6.CrossRefGoogle ScholarPubMed
Manczak, M, Anekonda, TS, Henson, E, Park, BS, Quinn, J, Reddy, PH.Mitochondria are a direct site of A beta accumulation in Alzheimer’s disease neurons: implications for free radical generation and oxidative damage in disease progression. Human Mol Genetics. 2006; 15(9), 1437–1449.CrossRefGoogle ScholarPubMed
Kandimalla, R, Reddy, PH.Multiple faces of dynamin-related protein 1 and its role in Alzheimer’s disease pathogenesis. BBA. 2016; 1862(4), 814–828.Google ScholarPubMed
Manczak, M, Calkins, MJ, Reddy, PH.Impaired mitochondrial dynamics and abnormal interaction of amyloid beta with mitochondrial protein Drp1 in neurons from patients with Alzheimer’s disease: implications for neuronal damage. Human Mol Genetics. 2011; 20(13), 2495–2509.CrossRefGoogle ScholarPubMed
Giralt, A, Villarroya, F.SIRT3, a pivotal actor in mitochondrial functions: metabolism, cell death and aging. Biochem J. 2012; 444(1), 1–10.CrossRefGoogle ScholarPubMed
Palmeira, CM, Teodoro, JS, Amorim, JA, Steegborn, C, Sinclair, DA, Rolo, AP.Mitohormesis and metabolic health: the interplay between ROS, cAMP and sirtuins. Free Radical Biol Med. 2019; 141, 483–491.CrossRefGoogle ScholarPubMed
Demetrius, LA, Magistretti, PJ, Pellerin, L.Alzheimer’s disease: the amyloid hypothesis and the Inverse Warburg effect. Front Physiol. 2014; 5, 522.Google ScholarPubMed
Thal, DR, Rub, U, Orantes, M, Braak, H.Phases of a beta-deposition in the human brain and its relevance for the development of AD. Neurology. 2002; 58(12), 1791–1800.CrossRefGoogle ScholarPubMed