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Pro-inflammatory interleukin-6 signaling links cognitive impairments and peripheral metabolic alterations in Alzheimer’s disease (2021)

  • Authors:
  • USP affiliated author: DONATO JÚNIOR, JOSÉ - ICB
  • School: ICB
  • DOI: 10.1038/s41398-021-01349-z
  • Subjects: FISIOLOGIA; INTERLEUCINA 6; DOENÇA DE ALZHEIMER; METABOLISMO; MEMÓRIA PROCEDIMENTOS; RESSONÂNCIA MAGNÉTICA; HIPOTÁLAMO; PROCESSOS COGNITIVOS; ASTRÓCITOS; HIPOCAMPU DE ANIMAL; CAMUNDONGOS; MEMÓRIA ANIMAL
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  • Language: Inglês
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    Informações sobre o DOI: 10.1038/s41398-021-01349-z (Fonte: oaDOI API)
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    • ABNT

      SILVA, Natalia M. Lyra e et al. Pro-inflammatory interleukin-6 signaling links cognitive impairments and peripheral metabolic alterations in Alzheimer’s disease. Translational Psychiatry, v. 11, p. 1-15, 2021Tradução . . Disponível em: https://doi.org/10.1038/s41398-021-01349-z. Acesso em: 14 ago. 2022.
    • APA

      Silva, N. M. L. e, Gonçalves, R. A., Pascoal, T. A., Lima Filho, R. A. S., Resende, E. de P. F., Vieira, E. L. M., et al. (2021). Pro-inflammatory interleukin-6 signaling links cognitive impairments and peripheral metabolic alterations in Alzheimer’s disease. Translational Psychiatry, 11, 1-15. doi:10.1038/s41398-021-01349-z
    • NLM

      Silva NML e, Gonçalves RA, Pascoal TA, Lima Filho RAS, Resende E de PF, Vieira ELM, Teixeira AL, Souza LC de, Peny JA, Fortuna JTS, Furigo IC, Hashiguchi D, Coreixas VSM, Clarke JR, Abisambra JF, Longo BM, Donato Junior J, Fraser PE, Rosa Neto P, Caramelli P, Ferreira ST, Felice FGD. Pro-inflammatory interleukin-6 signaling links cognitive impairments and peripheral metabolic alterations in Alzheimer’s disease [Internet]. Translational Psychiatry. 2021 ; 11 1-15.[citado 2022 ago. 14 ] Available from: https://doi.org/10.1038/s41398-021-01349-z
    • Vancouver

      Silva NML e, Gonçalves RA, Pascoal TA, Lima Filho RAS, Resende E de PF, Vieira ELM, Teixeira AL, Souza LC de, Peny JA, Fortuna JTS, Furigo IC, Hashiguchi D, Coreixas VSM, Clarke JR, Abisambra JF, Longo BM, Donato Junior J, Fraser PE, Rosa Neto P, Caramelli P, Ferreira ST, Felice FGD. Pro-inflammatory interleukin-6 signaling links cognitive impairments and peripheral metabolic alterations in Alzheimer’s disease [Internet]. Translational Psychiatry. 2021 ; 11 1-15.[citado 2022 ago. 14 ] Available from: https://doi.org/10.1038/s41398-021-01349-z

    Referências citadas na obra
    Alzheimer’s, A. Alzheimer’s disease facts and figures. Alzheimer’s Dement. J. Alzheimer’s Assoc. 12, 459–509 (2016).
    Clarke, J. R. et al. Alzheimer-associated Abeta oligomers impact the central nervous system to induce peripheral metabolic deregulation. EMBO Mol. Med. 7, 190–210 (2015).
    Craft, S. et al. Cerebrospinal fluid and plasma insulin levels in Alzheimer’s disease: relationship to severity of dementia and apolipoprotein E genotype. Neurology 50, 164–168 (1998).
    Gil-Bea, F. J. et al. Insulin levels are decreased in the cerebrospinal fluid of women with prodomal Alzheimer’s disease. J. Alzheimer’s Dis.: JAD 22, 405–413 (2010).
    Janson, J. et al. Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53, 474–481 (2004).
    Heni, M. et al. Evidence for altered transport of insulin across the blood-brain barrier in insulin-resistant humans. Acta diabetologica 51, 679–681 (2014).
    Takechi, R. et al. Blood-brain barrier dysfunction precedes cognitive decline and neurodegeneration in diabetic insulin resistant mouse model: an implication for causal link. Front. Aging Neurosci. 9, 399 (2017).
    Fakhoury, M. Microglia and astrocytes in Alzheimer’s disease: implications for therapy. Curr. Neuropharmacol. 16, 508–518 (2018).
    Heneka, M. T. et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurol. 14, 388–405 (2015).
    Ferreira, S. T., Clarke, J. R., Bomfim, T. R. & De Felice, F. G. Inflammation, defective insulin signaling, and neuronal dysfunction in Alzheimer’s disease. Alzheimer’s Dement.: J. Alzheimer’s Assoc. 10, S76–S83 (2014).
    Lourenco, M. V. et al. 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, 831–843 (2013).
    Wang, W. Y., Tan, M. S., Yu, J. T. & Tan, L. Role of pro-inflammatory cytokines released from microglia in Alzheimer’s disease. Ann. Transl. Med. 3, 136 (2015).
    Dunn, A. J. Cytokine activation of the HPA axis. Ann. N. Y. Acad. Sci. 917, 608–617 (2000).
    Elwood, E., Lim, Z., Naveed, H. & Galea, I. The effect of systemic inflammation on human brain barrier function. Brain, Behav., Immun. 62, 35–40 (2017).
    Bettcher, B. M. & Kramer, J. H. Longitudinal inflammation, cognitive decline, and Alzheimer’s disease: a mini-review. Clin. Pharmacol. therapeutics 96, 464–469 (2014).
    Fraga, V. G. et al. Inflammatory and pro-resolving mediators in frontotemporal dementia and Alzheimer’s disease. Neuroscience 421, 123–135 (2019).
    Miwa, K., Okazaki, S., Sakaguchi, M., Mochizuki, H. & Kitagawa, K. Interleukin-6, interleukin-6 receptor gene variant, small-vessel disease and incident dementia. Eur. J. Neurol. 23, 656–663 (2016).
    Windham, B. G. et al. Associations between inflammation and cognitive function in African Americans and European Americans. J. Am. Geriatrics Soc. 62, 2303–2310 (2014).
    Huell, M., Strauss, S., Volk, B., Berger, M. & Bauer, J. Interleukin-6 is present in early stages of plaque formation and is restricted to the brains of Alzheimer’s disease patients. Acta Neuropathol. 89, 544–551 (1995).
    Quintanilla, R. A., Orellana, D. I., Gonzalez-Billault, C. & Maccioni, R. B. Interleukin-6 induces Alzheimer-type phosphorylation of tau protein by deregulating the cdk5/p35 pathway. Exp. Cell Res. 295, 245–257 (2004).
    Burton, M. D. & Johnson, R. W. Interleukin-6 trans-signaling in the senescent mouse brain is involved in infection-related deficits in contextual fear conditioning. Brain Behav. Immun. 26, 732–738 (2012).
    Heyser, C. J., Masliah, E., Samimi, A., Campbell, I. L. & Gold, L. H. Progressive decline in avoidance learning paralleled by inflammatory neurodegeneration in transgenic mice expressing interleukin 6 in the brain. Proc. Natl Acad. Sci. USA 94, 1500–1505 (1997).
    Brosseron, F., Krauthausen, M., Kummer, M. & Heneka, M. T. Body fluid cytokine levels in mild cognitive impairment and Alzheimer’s disease: a comparative overview. Mol. Neurobiol. 50, 534–544 (2014).
    Swardfager, W. et al. A meta-analysis of cytokines in Alzheimer’s disease. Biol. Psychiatry 68, 930–941 (2010).
    McKhann, G. M. et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7, 263–269 (2011).
    Brucki, S. M., Nitrini, R., Caramelli, P., Bertolucci, P. H. & Okamoto, I. H. Suggestions for utilization of the mini-mental state examination in Brazil. Arquivos de. neuro-psiquiatria 61, 777–781 (2003).
    Machado, T. H. et al. Normative data for healthy elderly on the phonemic verbal fluency task - FAS. Dement. Neuropsychol. 3, 55–60 (2009).
    Nitrini, R. et al. Performance of illiterate and literate nondemented elderly subjects in two tests of long-term memory. J. Int. Neuropsychol. Soc. 10, 634–638 (2004).
    Beato, R. G., Nitrini, R., Formigoni, A. P. & Caramelli, P. Brazilian version of the Frontal Assessment Battery (FAB): preliminary data on administration to healthy elderly. Dement. Neuropsychologia 1, 59–65 (2007).
    Pauli, W. M., Nili, A. N. & Tyszka, J. M. A high-resolution probabilistic in vivo atlas of human subcortical brain nuclei. Sci. data 5, 180063 (2018).
    Klein, A. & Tourville, J. 101 labeled brain images and a consistent human cortical labeling protocol. Front. Neurosci. 6, 171 (2012).
    Pascoal, T. A. et al. Abeta-induced vulnerability propagates via the brain’s default mode network. Nat. Commun. 10, 2353 (2019).
    Cascino, G. D. Temporal lobe epilepsy: more than hippocampal pathology. Epilepsy Curr. 5, 187–189 (2005).
    Deulofeu Fontanillas, F. et al. Massive hemoptysis secondary to mycotic aortic aneurysm. de. Med. interna 6, 373–375 (1989).
    Pasternak, O., Kubicki, M. & Shenton, M. E. In vivo imaging of neuroinflammation in schizophrenia. Schizophrenia Res 173, 200–212 (2016).
    Souza, P. V. S., Bortholin, T., Naylor, F. G. M., Pinto, W. & Oliveira, A. S. B. Teaching NeuroImages: early-onset dementia and demyelinating neuropathy disclosing cerebrotendinous xanthomatosis. Neurology 89, e134 (2017).
    Virel, A. et al. Magnetic resonance imaging as a tool to image neuroinflammation in a rat model of Parkinson’s disease–phagocyte influx to the brain is promoted by bilberry-enriched diet. Eur. J. Neurosci. 42, 2761–2771 (2015).
    Thaler, J. P. et al. Obesity is associated with hypothalamic injury in rodents and humans. J. Clin. Investig. 122, 153–162 (2012).
    Lambert, M. P. et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95, 6448–6453 (1998).
    Figueiredo, C. P. et al. Memantine rescues transient cognitive impairment caused by high-molecular-weight abeta oligomers but not the persistent impairment induced by low-molecular-weight oligomers. J. Neurosci.: . J. Soc. Neurosci. 33, 9626–9634 (2013).
    Seixas da Silva, G. S. et al. Amyloid-beta oligomers transiently inhibit AMP-activated kinase and cause metabolic defects in hippocampal neurons. J. Biol. Chem. 292, 7395–7406 (2017).
    De Felice, F. G. et al. Protection of synapses against Alzheimer’s-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc. Natl Acad. Sci. USA 106, 1971–1976 (2009).
    Batista, A. F. et al. The diabetes drug liraglutide reverses cognitive impairment in mice and attenuates insulin receptor and synaptic pathology in a non-human primate model of Alzheimer’s disease. J. Pathol. 245, 85–100 (2018).
    Donato, J. Jr., Frazao, R., Fukuda, M., Vianna, C. R. & Elias, C. F. Leptin induces phosphorylation of neuronal nitric oxide synthase in defined hypothalamic neurons. Endocrinology 151, 5415–5427 (2010).
    Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408 (2001).
    Berkseth, K. E. et al. Hypothalamic gliosis associated with high-fat diet feeding is reversible in mice: a combined immunohistochemical and magnetic resonance imaging study. Endocrinology 155, 2858–2867 (2014).
    Briellmann, R. S., Kalnins, R. M., Berkovic, S. F. & Jackson, G. D. Hippocampal pathology in refractory temporal lobe epilepsy: T2-weighted signal change reflects dentate gliosis. Neurology 58, 265–271 (2002).
    Callen, D. J., Black, S. E., Gao, F., Caldwell, C. B. & Szalai, J. P. Beyond the hippocampus: MRI volumetry confirms widespread limbic atrophy in AD. Neurology 57, 1669–1674 (2001).
    Ishii, M. & Iadecola, C. Metabolic and non-cognitive manifestations of Alzheimer’s disease: the hypothalamus as both culprit and target of pathology. Cell Metab. 22, 761–776 (2015).
    Loskutova, N., Honea, R. A., Brooks, W. M. & Burns, J. M. Reduced limbic and hypothalamic volumes correlate with bone density in early Alzheimer’s disease. J. Alzheimer’s Dis. 20, 313–322 (2010).
    Iwahara, N. et al. Role of suppressor of cytokine signaling 3 (SOCS3) in altering activated microglia phenotype in APPswe/PS1dE9 mice. J. Alzheimer’s Dis. 55, 1235–1247 (2017).
    Gjerum, L. et al. A visual rating scale for cingulate island sign on 18F-FDG-PET to differentiate dementia with Lewy bodies and Alzheimer’s disease. J. Neurological Sci. 410, 116645 (2019).
    Wong, D. et al. Reduced hippocampal glutamate and posterior cingulate N-acetyl aspartate in mild cognitive impairment and Alzheimer’s disease is associated with episodic memory performance and white matter integrity in the cingulum: a pilot study. J. Alzheimer’s Dis. 73, 1385–1405 (2020).
    Ferreira, S. T. & Klein, W. L. The Abeta oligomer hypothesis for synapse failure and memory loss in Alzheimer’s disease. Neurobiol. Learn. Mem. 96, 529–543 (2011).
    Hardy, J. & Selkoe, D. J. The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297, 353–356 (2002).
    Sukoff Rizzo, S. J. et al. Evidence for sustained elevation of IL-6 in the CNS as a key contributor of depressive-like phenotypes. Transl. Psychiatry 2, e199 (2012).
    Chiba, T. et al. Amyloid-beta causes memory impairment by disturbing the JAK2/STAT3 axis in hippocampal neurons. Mol. Psychiatry 14, 206–222 (2009).
    Ott, A. et al. Association of diabetes mellitus and dementia: the Rotterdam Study. Diabetologia 39, 1392–1397 (1996).
    Ott, A. et al. Diabetes mellitus and the risk of dementia: the Rotterdam Study. Neurology 53, 1937–1942 (1999).
    Whitmer, R. A. et al. Central obesity and increased risk of dementia more than three decades later. Neurology 71, 1057–1064 (2008).
    Spilt, A. et al. Not all age-related white matter hyperintensities are the same: a magnetization transfer imaging study. AJNR Am. J. Neuroradiol. 27, 1964–1968 (2006).
    Blessing, E. M., Beissner, F., Schumann, A., Brunner, F. & Bar, K. J. A data-driven approach to mapping cortical and subcortical intrinsic functional connectivity along the longitudinal hippocampal axis. Hum. brain Mapp. 37, 462–476 (2016).
    Braak, H. & Braak, E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82, 239–259 (1991).
    Ogomori, K. et al. Beta-protein amyloid is widely distributed in the central nervous system of patients with Alzheimer’s disease. Am. J. Pathol. 134, 243–251 (1989).
    Standaert, D. G., Lee, V. M., Greenberg, B. D., Lowery, D. E. & Trojanowski, J. Q. Molecular features of hypothalamic plaques in Alzheimer’s disease. Am. J. Pathol. 139, 681–691 (1991).
    Fronczek, R. et al. Hypocretin (orexin) loss in Alzheimer’s disease. Neurobiol. aging 33, 1642–1650 (2012).
    Musiek, E. S., Xiong, D. D. & Holtzman, D. M. Sleep, circadian rhythms, and the pathogenesis of Alzheimer disease. Exp. Mol. Med. 47, e148 (2015).
    Kincheski, G. C. et al. Chronic sleep restriction promotes brain inflammation and synapse loss, and potentiates memory impairment induced by amyloid-beta oligomers in mice. Brain, Behav., Immun. 64, 140–151 (2017).
    Balschun, D. et al. Interleukin-6: a cytokine to forget. FASEB J.: . Publ. Federation Am. Societies Exp. Biol. 18, 1788–1790 (2004).
    Song, D. K. et al. Central beta-amyloid peptide-induced peripheral interleukin-6 responses in mice. J. Neurochem 76, 1326–1335 (2001).
    Craft, S., Zallen, G. & Baker, L. D. Glucose and memory in mild senile dementia of the Alzheimer type. J. Clin. Exp. Neuropsychol. 14, 253–267 (1992).
    Wright, C. B. et al. Interleukin-6 is associated with cognitive function: the Northern Manhattan Study. J. Stroke Cerebrovasc. Dis.: . J. Natl Stroke Assoc. 15, 34–38 (2006).
    Pavlov, V. A. & Tracey, K. J. The vagus nerve and the inflammatory reflex–linking immunity and metabolism. Nat. Rev. Endocrinol. 8, 743–754 (2012).
    Gyengesi, E. et al. Chronic microglial activation in the GFAP-IL6 mouse contributes to age-dependent cerebellar volume loss and impairment in motor function. Front. Neurosci. 13, 303 (2019).
    Ledo, J. H. et al. Amyloid-beta oligomers link depressive-like behavior and cognitive deficits in mice. Mol. psychiatry 18, 1053–1054 (2013).
    Chakrabarty, P. et al. Massive gliosis induced by interleukin-6 suppresses Abeta deposition in vivo: evidence against inflammation as a driving force for amyloid deposition. FASEB. J.: . Publ. Federation Am. Societies Exp. Biol. 24, 548–559 (2010).
    Forny-Germano, L. et al. Alzheimer’s disease-like pathology induced by amyloid-beta oligomers in nonhuman primates. J. Neurosci.: . J. Soc. Neurosci. 34, 13629–13643 (2014).
    Bomfim, T. R. et al. An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer’s disease-associated Abeta oligomers. J. Clin. Investig. 122, 1339–1353 (2012).
    Lyra, E. S. N. M. et al. Understanding the link between insulin resistance and Alzheimer’s disease: Insights from animal models. Exp. Neurol. 316, 1–11 (2019).
    Mao, Y. F. et al. Intranasal insulin alleviates cognitive deficits and amyloid pathology in young adult APPswe/PS1dE9 mice. Aging cell 15, 893–902 (2016).
    Talbot, K. et al. Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J. Clin. Investig. 122, 1316–1338 (2012).
    H. H. Ruiz et al. 2016 Increased susceptibility to metabolic dysregulation in a mouse model of Alzheimer’s disease is associated with impaired hypothalamic insulin signaling and elevated BCAA levels Alzheimer’s Dement.: J. Alzheimer’s Assoc. 12 851–861.
    Marciniak, E. et al. Tau deletion promotes brain insulin resistance. J. Exp. Med 214, 2257–2269 (2017).
    Rui, L., Yuan, M., Frantz, D., Shoelson, S. & White, M. F. SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J. Biol. Chem. 277, 42394–42398 (2002).
    Jorgensen, S. B. et al. Deletion of skeletal muscle SOCS3 prevents insulin resistance in obesity. Diabetes 62, 56–64 (2013).
    Pedroso, J. A. et al. Inactivation of SOCS3 in leptin receptor-expressing cells protects mice from diet-induced insulin resistance but does not prevent obesity. Mol. Metab. 3, 608–618 (2014).
    Hashioka, S., Klegeris, A., Qing, H. & McGeer, P. L. STAT3 inhibitors attenuate interferon-gamma-induced neurotoxicity and inflammatory molecule production by human astrocytes. Neurobiol. Dis. 41, 299–307 (2011).
    Reichenbach, N. et al. Inhibition of Stat3-mediated astrogliosis ameliorates pathology in an Alzheimer’s disease model. EMBO Mol. Med. 11, e9665 (2019).
    Nicolas, C. S. et al. The Jak/STAT pathway is involved in synaptic plasticity. Neuron 73, 374–390 (2012).
    Chen, E. et al. A novel role of the STAT3 pathway in brain inflammation-induced human neural progenitor cell differentiation. Curr. Mol. Med 13, 1474–1484 (2013).
    Saxe, M. D. et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl Acad. Sci. USA 103, 17501–17506 (2006).
    Greco, S. J. et al. Leptin reduces pathology and improves memory in a transgenic mouse model of Alzheimer’s disease. J. Alzheimer’s Dis. 19, 1155–1167 (2010).
    Bell, R. D. & Zlokovic, B. V. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer’s disease. Acta Neuropathologica 118, 103–113 (2009).
    Thal, D. R., Griffin, W. S., de Vos, R. A. & Ghebremedhin, E. Cerebral amyloid angiopathy and its relationship to Alzheimer’s disease. Acta Neuropathologica 115, 599–609 (2008).
    Starr, J. M. et al. Increased blood-brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging. J. Neurol. Neurosurg. Psychiatry 74, 70–76 (2003).
    Stevens, M. J., Feldman, E. L. & Greene, D. A. The aetiology of diabetic neuropathy: the combined roles of metabolic and vascular defects. Diabet. Med.: J. Br. Diabet. Assoc. 12, 566–579 (1995).
    Ting, E. Y., Yang, A. C. & Tsai, S. J. Role of Interleukin-6 in depressive disorder. Int. J. Mol. Sci. 21, 2194 (2020).
    Ownby, R. L., Crocco, E., Acevedo, A., John, V. & Loewenstein, D. Depression and risk for Alzheimer disease: systematic review, meta-analysis, and metaregression analysis. Arch. Gen. Psychiatry 63, 530–538 (2006).
    Butchart, J. et al. Etanercept in Alzheimer disease: a randomized, placebo-controlled, double-blind, phase 2 trial. Neurology 84, 2161–2168 (2015).
    Miguel-Alvarez, M. et al. Non-steroidal anti-inflammatory drugs as a treatment for Alzheimer’s disease: a systematic review and meta-analysis of treatment effect. Drugs Aging 32, 139–147 (2015).

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