Oxidative Stress, Metabolic Syndrome and Alzheimer’s Disease

  • Danira Toral-Rios
  • Karla Carvajal
  • Bryan Phillips-Farfán
  • Luz del Carmen Camacho-Castillo
  • Victoria Campos-PeñaEmail author
Part of the Advances in Biochemistry in Health and Disease book series (ABHD, volume 16)


Oxidative stress, neuroinflammation, insulin signaling deficiency and vascular alterations are common features of many neurodegenerative disorders. Oxidative damage induces chronic inflammation, this condition may lead to insulin resistance and damage to the blood brain barrier (BBB), leading to an exacerbation of central inflammation, causing cognitive dysfunction eventually resulting in dementia. The major cause of dementia affecting the elderly is Alzheimer’s disease, the most common cause of disability characterized by a progressive loss of memory and cognitive function. Neuropathologically, Alzheimer’s disease is characterized by abnormal deposition of the amyloid β (Aβ) peptide and intracellular accumulation of neurofibrillary tangles (NFT) of hyper-phosphorylated tau protein. It has been proposed that Aβ and NFT generate the neuronal damage that leads to cognitive failure, through the generation of reactive oxygen species (ROS). Alternatively, it has been suggested that oxidative damage precedes the accumulation of Aβ, NFTand other alterations such as vascular malfunction and metabolic syndrome. This chapter discusses the main molecular mechanisms associated to oxidative stress, metabolic syndrome and their relationship with Alzheimer’s disease. We also include promising therapeutic strategies.


Alzheimer’s Disease Metabolic syndrome Oxidative stress Insulin resistance Amyloid beta (Aβ) Antioxidant therapies 


  1. 1.
    Luque-Contreras D, Carvajal K, Toral-Rios D et al (2014) Oxidative stress and metabolic syndrome: cause or consequence of Alzheimer’s disease? Oxid Med Cell Longev 2014:497802CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Zhao Y, Zhao B (2013) Oxidative stress and the pathogenesis of Alzheimer’s disease. Oxid Med Cell Longev 2013:316523PubMedPubMedCentralGoogle Scholar
  3. 3.
    Kim GH, Kim JE, Rhie SJ et al (2015) The role of oxidative stress in neurodegenerative diseases. Exp Neurobiol 24:325–340CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Guerrero CA, Acosta O (2016) Inflammatory and oxidative stress in rotavirus infection. World J Virol 5:38–62CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Valko M, Leibfritz D, Moncol J et al (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84CrossRefPubMedGoogle Scholar
  6. 6.
    Sultana R, Perluigi M, Butterfield DA (2006) 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 Analyt Technol Biomed Life Sci 833:3–11CrossRefPubMedGoogle Scholar
  7. 7.
    Bonda DJ, Wang X, Perry G et al (2010) Oxidative stress in Alzheimer disease: a possibility for prevention. Neuropharmacology 59:290–294CrossRefPubMedGoogle Scholar
  8. 8.
    Luca M, Luca A, Calandra C (2015) The role of oxidative damage in the pathogenesis and progression of Alzheimer’s disease and vascular dementia. Oxid Med Cell Longev 2015:504678CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Oyinloye BE, Adenowo AF, Kappo AP (2015) Reactive oxygen species, apoptosis, antimicrobial peptides and human inflammatory diseases. Pharmaceuticals (Basel) 8:151–175CrossRefGoogle Scholar
  10. 10.
    Nordstrom P, Michaelsson K, Gustafson Y et al (2014) Traumatic brain injury and young onset dementia: a nationwide cohort study. Ann Neurol 75:374–381CrossRefPubMedGoogle Scholar
  11. 11.
    Cifuentes D, Poittevin M, Dere E et al (2015) Hypertension accelerates the progression of Alzheimer-like pathology in a mouse model of the disease. Hypertension 65:218–224CrossRefPubMedGoogle Scholar
  12. 12.
    Barbagallo M, Dominguez LJ (2014) Type 2 diabetes mellitus and Alzheimer’s disease. World J Diabetes 5:889–893CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Tangvarasittichai S (2015) Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes 6:456–480CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Meraz-Rios MA, Franco-Bocanegra D, Toral Rios D et al (2014) Early onset Alzheimer’s disease and oxidative stress. Oxid Med Cell Longev 2014:375968CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Goedert M, Spillantini MG, Jakes R et al (1995) Molecular dissection of the paired helical filament. Neurobiol Aging 16:325–334CrossRefPubMedGoogle Scholar
  16. 16.
    Wischik CM, Novak M, Edwards PC et al (1988) Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci U S A 85:4884–4888CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Weingarten MD, Lockwood AH, Hwo SY et al (1975) A protein factor essential for microtubule assembly. Proc Natl Acad Sci U S A 72:1858–1862CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Kolarova M, Garcia-Sierra F, Bartos A et al (2012) Structure and pathology of tau protein in Alzheimer disease. Int J Alzheimers Dis 2012:731526PubMedPubMedCentralGoogle Scholar
  19. 19.
    Goedert M (1999) Filamentous nerve cell inclusions in neurodegenerative diseases: tauopathies and alpha-synucleinopathies. Philos Trans R Soc Lond B Biol Sci 354:1101–1118CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Patterson KR, Remmers C, Fu Y et al (2011) Characterization of prefibrillar Tau oligomers in vitro and in Alzheimer disease. J Biol Chem 286:23063–23076CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Rapoport SI (2003) Coupled reductions in brain oxidative phosphorylation and synaptic function can be quantified and staged in the course of Alzheimer disease. Neurotox Res 5:385–398CrossRefPubMedGoogle Scholar
  22. 22.
    Quintanilla RA, Matthews-Roberson TA, Dolan PJ et al (2009) Caspase-cleaved tau expression induces mitochondrial dysfunction in immortalized cortical neurons: implications for the pathogenesis of Alzheimer disease. J Biol Chem 284:18754–18766CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Su B, Wang X, Lee HG et al (2010) Chronic oxidative stress causes increased tau phosphorylation in M17 neuroblastoma cells. Neurosci Lett 468:267–271CrossRefPubMedGoogle Scholar
  24. 24.
    Feng Y, Xia Y, Yu G et al (2013) Cleavage of GSK-3beta by calpain counteracts the inhibitory effect of Ser9 phosphorylation on GSK-3beta activity induced by H(2)O(2). J Neurochem 126:234–242CrossRefPubMedGoogle Scholar
  25. 25.
    Wakatsuki S, Furuno A, Ohshima M et al (2015) Oxidative stress-dependent phosphorylation activates ZNRF1 to induce neuronal/axonal degeneration. J Cell Biol 211:881–896CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Kamat PK, Kalani A, Rai S et al (2016) Mechanism of oxidative stress and synapse dysfunction in the pathogenesis of Alzheimer’s disease: understanding the therapeutics strategies. Mol Neurobiol 53:648–661CrossRefPubMedGoogle Scholar
  27. 27.
    Jo DG, Arumugam TV, Woo HN et al (2010) Evidence that gamma-secretase mediates oxidative stress-induced beta-secretase expression in Alzheimer’s disease. Neurobiol Aging 31:917–925CrossRefPubMedGoogle Scholar
  28. 28.
    Zhao J, Fu Y, Yasvoina M et al (2007) Beta-site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer’s disease pathogenesis. J Neurosci 27:3639–3649CrossRefPubMedGoogle Scholar
  29. 29.
    Butterfield DA, Swomley AM, Sultana R (2013) Amyloid beta-peptide (1–42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression. Antioxid Redox Signal 19:823–835CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Deibel MA, Ehmann WD, Markesbery WR (1996) Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer’s disease: possible relation to oxidative stress. J Neurol Sci 143:137–142CrossRefPubMedGoogle Scholar
  31. 31.
    Roychaudhuri R, Yang M, Hoshi MM et al (2009) Amyloid beta-protein assembly and Alzheimer disease. J Biol Chem 284:4749–4753CrossRefPubMedGoogle Scholar
  32. 32.
    Yankner BA, Lu T (2009) Amyloid beta-protein toxicity and the pathogenesis of Alzheimer disease. J Biol Chem 284:4755–4759CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Meraz-Rios MA, Toral-Rios D, Franco-Bocanegra D et al (2013) Inflammatory process in Alzheimer’s disease. Front Integr Neurosci 7:1–15CrossRefGoogle Scholar
  34. 34.
    Korczynski W, Ceregrzyn M, Kato I et al (2006) The effect of orexins on intestinal motility in vitro in fed and fasted rats. J Physiol Pharmacol 57:S43–S54Google Scholar
  35. 35.
    Solfrizzi V, Panza F, Colacicco AM et al (2004) Vascular risk factors, incidence of MCI, and rates of progression to dementia. Neurology 63:1882–1891CrossRefPubMedGoogle Scholar
  36. 36.
    Grodstein F, Chen J, Wilson RS et al (2001) Type 2 diabetes and cognitive function in community-dwelling elderly women. Diabetes Care 24:1060–1065CrossRefPubMedGoogle Scholar
  37. 37.
    Siddle K (2011) Signalling by insulin and IGF receptors: supporting acts and new players. J Mol Endocrinol 47:R1–R10CrossRefPubMedGoogle Scholar
  38. 38.
    Bevan P (2001) Insulin signalling. J Cell Sci 114:1429–1430PubMedGoogle Scholar
  39. 39.
    Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7:85–96CrossRefPubMedGoogle Scholar
  40. 40.
    Porte D Jr, Baskin DG, Schwartz MW (2005) Insulin signaling in the central nervous system: a critical role in metabolic homeostasis and disease from C. elegans to humans. Diabetes 54:1264–1276CrossRefPubMedGoogle Scholar
  41. 41.
    Yuan H, Chen R, Wu L et al (2015) The regulatory mechanism of neurogenesis by IGF-1 in adult mice. Mol Neurobiol 51:512–522CrossRefPubMedGoogle Scholar
  42. 42.
    Lee CC, Huang CC, Wu MY et al (2005) Insulin stimulates postsynaptic density-95 protein translation via the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway. J Biol Chem 280:18543–18550CrossRefPubMedGoogle Scholar
  43. 43.
    Chiu SL, Chen CM, Cline HT (2008) Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 58:708–719CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Dou JT, Chen M, Dufour F et al (2005) Insulin receptor signaling in long-term memory consolidation following spatial learning. Learn Mem 12:646–655CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Cheng B, Maffi SK, Martinez AA et al (2011) Insulin-like growth factor-I mediates neuroprotection in proteasome inhibition-induced cytotoxicity in SH-SY5Y cells. Mol Cell Neurosci 47:181–190CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Duarte AI, Santos P, Oliveira CR et al (2008) Insulin neuroprotection against oxidative stress is mediated by Akt and GSK-3beta signaling pathways and changes in protein expression. Biochim Biophys Acta 1783:994–1002CrossRefPubMedGoogle Scholar
  47. 47.
    Hopkins DF, Williams G (1997) Insulin receptors are widely distributed in human brain and bind human and porcine insulin with equal affinity. Diabet Med 14:1044–1050CrossRefPubMedGoogle Scholar
  48. 48.
    Pacold ST, Blackard WG (1979) Central nervous system insulin receptors in normal and diabetic rats. Endocrinology 105:1452–1457CrossRefPubMedGoogle Scholar
  49. 49.
    Blazquez E, Velazquez E, Hurtado-Carneiro V et al (2014) Insulin in the brain: its pathophysiological implications for States related with central insulin resistance, type 2 diabetes and Alzheimer’s disease. Front Endocrinol (Lausanne) 5:1–21Google Scholar
  50. 50.
    Talbot K, Wang HY, Kazi H et al (2012) Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest 122:1316–1338CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Cheng CM, Tseng V, Wang J et al (2005) Tau is hyperphosphorylated in the insulin-like growth factor-I null brain. Endocrinology 146:5086–5091CrossRefPubMedGoogle Scholar
  52. 52.
    Hong M, Lee VM (1997) Insulin and insulin-like growth factor-1 regulate tau phosphorylation in cultured human neurons. J Biol Chem 272:19547–19553CrossRefPubMedGoogle Scholar
  53. 53.
    Adlerz L, Holback S, Multhaup G et al (2007) IGF-1-induced processing of the amyloid precursor protein family is mediated by different signaling pathways. J Biol Chem 282:10203–10209CrossRefPubMedGoogle Scholar
  54. 54.
    Mattson MP (1997) Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol Rev 77:1081–1132PubMedGoogle Scholar
  55. 55.
    Zhao L, Teter B, Morihara T et al (2004) Insulin-degrading enzyme as a downstream target of insulin receptor signaling cascade: implications for Alzheimer’s disease intervention. J Neurosci 24:11120–11126CrossRefPubMedGoogle Scholar
  56. 56.
    Carro E, Spuch C, Trejo JL et al (2005) Choroid plexus megalin is involved in neuroprotection by serum insulin-like growth factor I. J Neurosci 25:10884–10893CrossRefPubMedGoogle Scholar
  57. 57.
    Zhao WQ, De Felice FG, Fernandez S et al (2008) Amyloid beta oligomers induce impairment of neuronal insulin receptors. FASEB J 22:246–260CrossRefPubMedGoogle Scholar
  58. 58.
    Kim B, Feldman EL (2012) Insulin resistance in the nervous system. Trends Endocrinol Metab 23:133–141CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    De Felice FG, Vieira MN, Bomfim TR et al (2009) Protection of synapses against Alzheimer’s-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc Natl Acad Sci U S A 106:1971–1976CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Manolopoulos KN, Klotz LO, Korsten P et al (2010) Linking Alzheimer’s disease to insulin resistance: the FoxO response to oxidative stress. Mol Psychiatry 15:1046–1052CrossRefPubMedGoogle Scholar
  61. 61.
    Bomfim TR, Forny-Germano L, Sathler LB et al (2012) An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer’s disease- associated Abeta oligomers. J Clin Invest 122:1339–1353CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Lourenco MV, Clarke JR, Frozza RL et al (2013) TNF-alpha mediates PKR-dependent memory impairment and brain IRS-1 inhibition induced by Alzheimer’s beta-amyloid oligomers in mice and monkeys. Cell Metab 18:831–843CrossRefPubMedGoogle Scholar
  63. 63.
    Bedse G, Di Domenico F, Serviddio G et al (2015) Aberrant insulin signaling in Alzheimer’s disease: current knowledge. Front Neurosci 9:1–13CrossRefGoogle Scholar
  64. 64.
    Devi L, Alldred MJ, Ginsberg SD et al (2012) Mechanisms underlying insulin deficiency-induced acceleration of beta-amyloidosis in a mouse model of Alzheimer’s disease. PLoS One 7:e32792CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Watts AS, Loskutova N, Burns JM et al (2013) Metabolic syndrome and cognitive decline in early Alzheimer’s disease and healthy older adults. J Alzheimers Dis 35:253–265PubMedPubMedCentralGoogle Scholar
  66. 66.
    Guo S (2014) Insulin signaling, resistance, and the metabolic syndrome: insights from mouse models into disease mechanisms. J Endocrinol 220:T1–T23CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Obici S, Zhang BB, Karkanias G et al (2002) Hypothalamic insulin signaling is required for inhibition of glucose production. Nat Med 8:1376–1382CrossRefPubMedGoogle Scholar
  68. 68.
    Koch L, Wunderlich FT, Seibler J et al (2008) Central insulin action regulates peripheral glucose and fat metabolism in mice. J Clin Invest 118:2132–2147PubMedPubMedCentralGoogle Scholar
  69. 69.
    Ouchi N, Parker JL, Lugus JJ et al (2011) Adipokines in inflammation and metabolic disease. Nat Rev Immunol 11:85–97CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115:1111–1119CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Roberts CK, Hevener AL, Barnard RJ (2013) Metabolic syndrome and insulin resistance: underlying causes and modification by exercise training. Compr Physiol 3:1–58PubMedPubMedCentralGoogle Scholar
  72. 72.
    Baker LD, Cross DJ, Minoshima S et al (2011) Insulin resistance and Alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early type 2 diabetes. Arch Neurol 68:51–57CrossRefPubMedGoogle Scholar
  73. 73.
    Bonomini F, Rodella LF, Rezzani R (2015) Metabolic syndrome, aging and involvement of oxidative stress. Aging Dis 6:109–120CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Kim Y, Park H (2013) Does regular exercise without weight loss reduce insulin resistance in children and adolescents? Int J Endocrinol 2013:402592PubMedPubMedCentralGoogle Scholar
  75. 75.
    Onyango IG, Dennis J, Khan SM (2016) Mitochondrial dysfunction in Alzheimer’s Disease and the rationale for bioenergetics based therapies. Aging Dis 7:201–214CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Galasko D, Montine TJ (2010) Biomarkers of oxidative damage and inflammation in Alzheimer’s disease. Biomark Med 4:27–36CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Di Giacomo G, Rizza S, Montagna C et al (2012) Established principles and emerging concepts on the interplay between mitochondrial physiology and S-(De)nitrosylation: Implications in Cancer and Neurodegeneration. Int J Cell Biol 2012:361872CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Akhtar MW, Sunico CR, Nakamura T et al (2012) Redox regulation of protein function via Cysteine S-Nitrosylation and its relevance to Neurodegenerative Diseases. Int J Cell Biol 2012:463756CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Nakamura T, Tu S, Akhtar MW et al (2013) Aberrant protein s-nitrosylation in neurodegenerative diseases. Neuron 78:596–614CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Nakamura T, Cieplak P, Cho DH et al (2010) S-nitrosylation of Drp1 links excessive mitochondrial fission to neuronal injury in neurodegeneration. Mitochondrion 10:573–578CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Qu J, Nakamura T, Cao G et al (2011) S-Nitrosylation activates Cdk5 and contributes to synaptic spine loss induced by beta-amyloid peptide. Proc Natl Acad Sci U S A 108:14330–14335CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Zhao QF, Yu JT, Tan L (2015) S-Nitrosylation in Alzheimer’s disease. Mol Neurobiol 51:268–280CrossRefPubMedGoogle Scholar
  83. 83.
    Piantadosi CA (2012) Regulation of mitochondrial processes by protein S-nitrosylation. Biochim Biophys Acta 1820:712–721CrossRefPubMedGoogle Scholar
  84. 84.
    Wang X, Su B, Zheng L et al (2009) The role of abnormal mitochondrial dynamics in the pathogenesis of Alzheimer’s disease. J Neurochem 109:S153–S159CrossRefGoogle Scholar
  85. 85.
    Halloran M, Parakh S, Atkin JD (2013) The role of s-nitrosylation and s-glutathionylation of protein disulphide isomerase in protein misfolding and neurodegeneration. Int J Cell Biol 2013:797914CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: A review. Eur J Med Chem 97:55–74CrossRefPubMedGoogle Scholar
  87. 87.
    Rani V, Deep G, Singh RK et al (2016) Oxidative stress and metabolic disorders: Pathogenesis and therapeutic strategies. Life Sci 148:183–193CrossRefPubMedGoogle Scholar
  88. 88.
    Butterfield DA (2004) Proteomics: a new approach to investigate oxidative stress in Alzheimer’s disease brain. Brain Res 1000:1–7CrossRefPubMedGoogle Scholar
  89. 89.
    Drake J, Link CD, Butterfield DA (2003) Oxidative stress precedes fibrillar deposition of Alzheimer’s disease amyloid beta-peptide (1–42) in a transgenic Caenorhabditis elegans model. Neurobiol Aging 24:415–420CrossRefPubMedGoogle Scholar
  90. 90.
    Hills AP, Byrne NM, Lindstrom R et al (2013) ‘Small changes’ to diet and physical activity behaviors for weight management. Obes Facts 6:228–238CrossRefPubMedGoogle Scholar
  91. 91.
    Teixeira J, Silva T, Andrade PB et al (2013) Alzheimer’s disease and antioxidant therapy: how long how far? Curr Med Chem 20:2939–2952CrossRefPubMedGoogle Scholar
  92. 92.
    Feng Y, Wang X (2012) Antioxidant therapies for Alzheimer’s disease. Oxid Med Cell Longev 2012:472932CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Nunes-Souza V, Cesar-Gomes CJ, Da Fonseca LJ et al (2016) Aging increases susceptibility to high fat diet-induced metabolic syndrome in C57BL/6 Mice: Improvement in Glycemic and Lipid Profile after Antioxidant Therapy. Oxid Med Cell Longev 2016:1987960PubMedPubMedCentralGoogle Scholar
  94. 94.
    Strasser B (2013) Physical activity in obesity and metabolic syndrome. Ann NY Acad Sci 1281:141–159CrossRefPubMedGoogle Scholar
  95. 95.
    Gregorio BM, De Souza DB, De Morais Nascimento FA et al (2016) The potential role of antioxidants in metabolic syndrome. Curr Pharm Des 22:859–869CrossRefPubMedGoogle Scholar
  96. 96.
    Di Luccia B, Crescenzo R, Mazzoli A et al (2015) Rescue of fructose-induced metabolic syndrome by antibiotics or faecal transplantation in a rat model of obesity. PLoS One 10:e0134893CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Qiao Y, Sun J, Ding Y et al (2013) Alterations of the gut microbiota in high-fat diet mice is strongly linked to oxidative stress. Appl Microbiol Biotechnol 97:1689–1697CrossRefPubMedGoogle Scholar
  98. 98.
    Qiao Y, Sun J, Xia S et al (2014) Effects of resveratrol on gut microbiota and fat storage in a mouse model with high-fat-induced obesity. Food Funct 5:1241–1249CrossRefPubMedGoogle Scholar
  99. 99.
    Naseer MI, Bibi F, Alqahtani MH et al (2014) Role of gut microbiota in obesity, type 2 diabetes and Alzheimer’s disease. CNS Neurol Disord Drug Targets 13:305–311CrossRefPubMedGoogle Scholar
  100. 100.
    Alam MZ, Alam Q, Kamal MA et al (2014) A possible link of gut microbiota alteration in type 2 diabetes and Alzheimer’s disease pathogenicity: an update. CNS Neurol Disord Drug Targets 13:383–390CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Danira Toral-Rios
    • 1
  • Karla Carvajal
    • 2
  • Bryan Phillips-Farfán
    • 2
  • Luz del Carmen Camacho-Castillo
    • 2
  • Victoria Campos-Peña
    • 3
    Email author
  1. 1.Departamento de Fisiología Biofísica y NeurocienciasCentro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalMexico CityMexico
  2. 2.Laboratorio de Nutrición ExperimentalInstituto Nacional de PediatríaMexico CityMexico
  3. 3.Laboratorio Experimental de Enfermedades NeurodegenerativasInstituto Nacional de Neurología y NeurocirugíaMexico CityMexico

Personalised recommendations