Toll-like receptors in neuroinflammation, neurodegeneration, and alcohol-induced brain damage.


Journal

IUBMB life
ISSN: 1521-6551
Titre abrégé: IUBMB Life
Pays: England
ID NLM: 100888706

Informations de publication

Date de publication:
07 2021
Historique:
revised: 05 05 2021
received: 30 03 2021
accepted: 22 05 2021
pubmed: 26 5 2021
medline: 11 2 2022
entrez: 25 5 2021
Statut: ppublish

Résumé

Toll-like receptors (TLRs) or pattern recognition receptors respond to pathogen-associated molecular patterns (PAMPs) or internal damage-associated molecular patterns (DAMPs). TLRs are integral membrane proteins with both extracellular leucine-rich and cytoplasmic domains that initiate downstream signaling through kinases by activating transcription factors like AP-1 and NF-κB, which lead to the release of various inflammatory cytokines and immune modulators. In the central nervous system, different TLRs are expressed mainly in microglia and astroglial cells, although some TLRs are also expressed in oligodendroglia and neurons. Activation of TLRs triggers signaling cascades by the host as a defense mechanism against invaders to repair damaged tissue. However, overactivation of TLRs disrupts the sustained immune homeostasis-induced production of pro-inflammatory molecules, such as cytokines, miRNAs, and inflammatory components of extracellular vesicles. These inflammatory mediators can, in turn, induce neuroinflammation, and neural tissue damage associated with many neurodegenerative diseases. This review discusses the critical role of TLRs response in Alzheimer's disease, Parkinson's disease, ischemic stroke, amyotrophic lateral sclerosis, and alcohol-induced brain damage and neurodegeneration.

Identifiants

pubmed: 34033211
doi: 10.1002/iub.2510
doi:

Substances chimiques

MicroRNAs 0
Toll-Like Receptors 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

900-915

Subventions

Organisme : GVA
ID : AICO/2019/087
Organisme : Junta de Castilla y Leon
ID : VA294P18
Organisme : Spanish Ministry of Health, Consumption and Social Welfare
ID : PNSD-2018-I003
Organisme : Spanish Ministry of Health, Consumption and Social Welfare
ID : PNSD-2019-I039
Organisme : The Spanish Ministry of Science, Innovation and Universities
ID : RTI2018-099298-B-100

Informations de copyright

© 2021 International Union of Biochemistry and Molecular Biology.

Références

Yirmiya R, Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun. 2011;25:181-213.
Kumar V. Toll-like receptors in the pathogenesis of neuroinflammation. J Neuroimmunol. 2019;332:16-30.
Lanier LL, Sun JC. Do the terms innate and adaptive immunity create conceptual barriers? Nature reviews. Immunology. 2009;9:302-303.
Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124:783-801.
Piccinini AM, Midwood KS. DAMPening inflammation by modulating TLR Signalling. Mediators Inflamm. 2010;2010:1-21.
Casali BT, Reed-Geaghan EG. Microglial function and regulation during development, homeostasis and Alzheimer's disease. Cell. 2021;10:957.
Sabroe I, Whyte MKB. Toll-like receptor (TLR)-based networks regulate neutrophilic inflammation in respiratory disease. Biochem Soc Trans. 2007;35:1492-1495.
Kumar S, Ingle H, Prasad DVR, Kumar H. Recognition of bacterial infection by innate immune sensors. Crit Rev Microbiol. 2013;39:229-246.
Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev. 2009;22:240-273. Table of Contents.
Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: Update on toll-like receptors. Nat Immunol. 2010;11:373-384.
Shukla NM, Mutz CA, Malladi SS, Warshakoon HJ, Balakrishna R, David SA. Toll-like receptor (TLR)-7 and −8 modulatory activities of dimeric imidazoquinolines. J Med Chem. 2012;55:1106-1116.
Gay NJ, Symmons MF, Gangloff M, Bryant CE. Assembly and localization of toll-like receptor signalling complexes. Nat Rev Immunol. 2014;14:546-558.
Arroyo DS, Soria JA, Gaviglio EA, Rodriguez-Galan MC, Iribarren P. Toll-like receptors are key players in neurodegeneration. Int Immunopharmacol. 2011;11:1415-1421.
Okun E, Griffioen KJ, Lathia JD, Tang S-C, Mattson MP, Arumugam TV. Toll-like receptors in neurodegeneration. Brain Res Rev. 2009;59:278-292.
Kaur C, Rathnasamy G, Ling E-A. Biology of microglia in the developing brain. J Neuropathol Exp Neurol. 2017;76:736-753.
Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, et al. Synaptic pruning by microglia is necessary for normal brain development. Science (New York, N.Y.). 2011;333:1456-1458.
Li Q, Barres BA. Microglia and macrophages in brain homeostasis and disease. Nat Rev Immunol. 2018;18:225-242.
Butovsky O, Weiner HL. Microglial signatures and their role in health and disease. Nat Rev Neurosci. 2018;19:622-635.
Bsibsi M, Ravid R, Gveric D, van Noort JM. Broad expression of toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol. 2002;61:1013-1021.
Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol (Baltimore, Md.: 1950). 2004;173:3916-3924.
Block ML, Zecca L, Hong J-S. Microglia-mediated neurotoxicity: Uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8:57-69.
Tahara K, Kim H-D, Jin J-J, Maxwell JA, Li L, Fukuchi KI. Role of toll-like receptor signalling in Abeta uptake and clearance. Brain: J Neurol. 2006;129:3006-3019.
Li L, Acioglu C, Heary RF, Elkabes S. Role of astroglial toll-like receptors (TLRs) in central nervous system infections, injury and neurodegenerative diseases. Brain Behav Immun. 2021;91:740-755.
Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009;32:638-647.
Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, et al. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol (Baltimore, Md.: 1950). 2005;175:4320-4330.
Potokar M, Jorgačevski J, Zorec R. Astrocytes in Flavivirus infections. Int J Mol Sci. 2019;20:691-706.
Bsibsi M, Nomden A, van Noort JM, Baron W. Toll-like receptors 2 and 3 agonists differentially affect oligodendrocyte survival, differentiation, and myelin membrane formation. J Neurosci Res. 2012;90:388-398.
Kigerl KA, Lai W, Rivest S, Hart RP, Satoskar AR, Popovich PG. Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J Neurochem. 2007;102:37-50.
Barak B, Feldman N, Okun E. Toll-like receptors as developmental tools that regulate neurogenesis during development: An update. Front Neurosci. 2014;8:272.
Tang S-C, Arumugam TV, Xu X, et al. Pivotal role for neuronal toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci U S A. 2007;104:13798-13803.
Mishra BB, Mishra PK, Teale JM. Expression and distribution of toll-like receptors in the brain during murine neurocysticercosis. J Neuroimmunol. 2006;181:46-56.
Hardy JA, Higgins GA. Alzheimer's disease: The amyloid cascade hypothesis. Science (New York, N.Y.). 1992;256:184-185.
Calvo-Rodríguez M, García-Durillo M, Villalobos C, Núñez L. Aging enables Ca2+ overload and apoptosis induced by amyloid-β oligomers in rat hippocampal neurons: Neuroprotection by non-steroidal anti-inflammatory drugs and R-Flurbiprofen in aging neurons. J Alzheimer's Dis: JAD. 2016;54:207-221.
Sanz-Blasco S, Calvo-Rodriguez M, Caballero E, Garcia-Durillo M, Nunez L, et al. Is it all said for NSAIDs in Alzheimer's disease? Role of mitochondrial calcium uptake. Curr Alzheimer Res. 2018;15:504-510.
Calvo-Rodriguez M, Hou SS, Snyder AC, et al. Increased mitochondrial calcium levels associated with neuronal death in a mouse model of Alzheimer's disease. Nat Commun. 2020;11:2146.
Kuchibhotla KV, Goldman ST, Lattarulo CR, Wu H-Y, Hyman BT, Bacskai BJ. Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron. 2008;59:214-225.
Karch CM, Goate AM. Alzheimer's disease risk genes and mechanisms of disease pathogenesis. Biol Psychiatry. 2015;77:43-51.
Letiembre M, Liu Y, Walter S, et al. Screening of innate immune receptors in neurodegenerative diseases: A similar pattern. Neurobiol Aging. 2009;30:759-768.
Chakrabarty P, Li A, Ladd TB, et al. TLR5 decoy receptor as a novel anti-amyloid therapeutic for Alzheimer's disease. J Exp Med. 2018;215:2247-2264.
Frank S, Copanaki E, Burbach GJ, Müller UC, Deller T. Differential regulation of toll-like receptor mRNAs in amyloid plaque-associated brain tissue of aged APP23 transgenic mice. Neurosci Lett. 2009;453:41-44.
Kiasalari Z, Heydarifard R, Khalili M, et al. Ellagic acid ameliorates learning and memory deficits in a rat model of Alzheimer's disease: An exploration of underlying mechanisms. Psychopharmacology (Berl). 2017;234:1841-1852.
Calvo-Rodríguez M, de la Fuente C, García-Durillo M, García-Rodríguez C, Villalobos C, Núñez L. Aging and amyloid β oligomers enhance TLR4 expression, LPS-induced Ca2+ responses, and neuron cell death in cultured rat hippocampal neurons. J Neuroinflammation. 2017;14:24.
Caldeira C, Cunha C, Vaz AR, Falcão AS, Barateiro A, et al. Key aging-associated alterations in primary microglia response to Beta-amyloid stimulation. Front Aging Neurosci. 2017;9:277-299.
Song M, Jin J, Lim J-E, et al. TLR4 mutation reduces microglial activation, increases Aβ deposits and exacerbates cognitive deficits in a mouse model of Alzheimer's disease. J Neuroinflammation. 2011;8:92.
Qin Y, Liu Y, Hao W, Decker Y, Tomic I, et al. Stimulation of TLR4 attenuates Alzheimer's disease-related symptoms and pathology in tau-transgenic mice. J Immunol (Baltimore, Md.: 1950). 2016;197:3281-3292.
Walter S, Letiembre M, Liu Y, et al. Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cell Physiol Biochem. 2007;20:947-956.
Balducci C, Frasca A, Zotti M, Vitola PL, Mhillaj E, et al. Toll-like receptor 4-dependent glial cell activation mediates the impairment in memory establishment induced by β-amyloid oligomers in an acute mouse model of Alzheimer's disease. Brain Behav Immun. 2017;60:188-197.
Calvo-Rodriguez M, García-Rodríguez C, Villalobos C, Núñez L. Role of toll like receptor 4 in Alzheimer's disease. Front Immunol. 2020;11:1588-1593.
Richard KL, Filali M, Préfontaine P, Rivest S. Toll-like receptor 2 acts as a natural innate immune receptor to clear amyloid beta 1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. J Neurosci: Off J Soc Neurosci. 2008;28:5784-5793.
Jana M, Palencia CA, Pahan K. Fibrillar amyloid-beta peptides activate microglia via TLR2: Implications for Alzheimer's disease. J Immunol (Baltimore, Md.: 1950). 2008;181:7254-7262.
Rangasamy SB, Jana M, Roy A, et al. Selective disruption of TLR2-MyD88 interaction inhibits inflammation and attenuates Alzheimer's pathology. J Clin Invest. 2018;128:4297-4312.
Zhou C, Sun X, Hu Y, et al. Genomic deletion of TLR2 induces aggravated white matter damage and deteriorated neurobehavioral functions in mouse models of Alzheimer's disease. Aging. 2019;11:7257-7273.
Huang N-Q, Jin H, Zhou S-Y, Shi J-S, Jin F. TLR4 is a link between diabetes and Alzheimer's disease. Behav Brain Res. 2017;316:234-244.
Iribarren P, Chen K, Hu J, et al. CpG-containing oligodeoxynucleotide promotes microglial cell uptake of amyloid beta 1-42 peptide by up-regulating the expression of the G-protein- coupled receptor mFPR2. FASEB J: Off Publ Feder Am Soc Exp Biol. 2005;19:2032-2034.
Scholtzova H, Chianchiano P, Pan J, Sun Y, Goñi F, et al. Amyloid β and tau Alzheimer's disease related pathology is reduced by toll-like receptor 9 stimulation. Acta Neuropathol Commun. 2014;2:101-128.
Kouli A, Camacho M, Allinson K, Williams-Gray CH. Neuroinflammation and protein pathology in Parkinson's disease dementia. Acta Neuropathol Commun. 2020;8:211.
Fellner L, Irschick R, Schanda K, et al. Toll-like receptor 4 is required for α-synuclein dependent activation of microglia and astroglia. Glia. 2013;61:349-360.
Kwon S, Iba M, Masliah E, Kim C. Targeting microglial and neuronal toll-like receptor 2 in Synucleinopathies. Exp Neurobiol. 2019;28:547-553.
Campolo M, Filippone A, Biondo C, Mancuso G, Casili G, et al. TLR7/8 in the pathogenesis of Parkinson's disease. Int J Mol Sci. 2020;21:9384-9404.
Ebrahimi-Fakhari D, Wahlster L, McLean PJ. Protein degradation pathways in Parkinson's disease: Curse or blessing. Acta Neuropathol. 2012;124:153-172.
Gordon R, Albornoz EA, Christie DC, et al. Inflammasome inhibition prevents α-synuclein pathology and dopaminergic neurodegeneration in mice. Sci Transl Med. 2018;10:eaah4066.
Valori CF, Brambilla L, Martorana F, Rossi D. The multifaceted role of glial cells in amyotrophic lateral sclerosis. Cell Mol Life Sci. 2014;71:287-297.
Urushitani M, Sik A, Sakurai T, Nukina N, Takahashi R, Julien JP. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci. 2006;9:108-118.
Casula M, Iyer AM, Spliet WGM, et al. Toll-like receptor signaling in amyotrophic lateral sclerosis spinal cord tissue. Neuroscience. 2011;179:233-243.
Janda E, Boi L, Carta AR. Microglial phagocytosis and its regulation: A therapeutic target in Parkinson's disease? Front Mol Neurosci. 2018;11:144.
Zhao W, Beers DR, Henkel JS, et al. Extracellular mutant SOD1 induces microglial-mediated motoneuron injury. Glia. 2010;58:231-243.
Liu Y, Hao W, Dawson A, Liu S, Fassbender K. Expression of amyotrophic lateral sclerosis-linked SOD1 mutant increases the neurotoxic potential of microglia via TLR2. J Biol Chem. 2009;284:3691-3699.
Fellner A, Barhum Y, Angel A, Perets N, Steiner I, et al. Toll-like Receptor-4 inhibitor TAK-242 attenuates motor dysfunction and spinal cord pathology in an amyotrophic lateral sclerosis mouse model. Int J Mol Sci. 2017;18:1666-1681.
Cassidy JM, Cramer SC. Spontaneous and therapeutic-induced mechanisms of functional recovery after stroke. Transl Stroke Res. 2017;8:33-46.
Tajalli-Nezhad S, Karimian M, Beyer C, Atlasi MA, Azami Tameh A. The regulatory role of toll-like receptors after ischemic stroke: Neurosteroids as TLR modulators with the focus on TLR2/4. Cell Mol Life Sci. 2019;76:523-537.
Xu S, Lu J, Shao A, Zhang JH, Zhang J. Glial cells: Role of the immune response in ischemic stroke. Front Immunol. 2020;11:294.
Ziegler G, Harhausen D, Schepers C, et al. TLR2 has a detrimental role in mouse transient focal cerebral ischemia. Biochem Biophys Res Commun. 2007;359:574-579.
Ziegler G, Freyer D, Harhausen D, Khojasteh U, Nietfeld W, Trendelenburg G. Blocking TLR2 in vivo protects against accumulation of inflammatory cells and neuronal injury in experimental stroke. J Cereb Blood Flow Metab. 2011;31:757-766.
Yang Q, Wang J-Z, Li J-C, Zhou Y, Zhong Q, et al. High-mobility group protein box-1 and its relevance to cerebral ischemia. J Cereb Blood Flow Metab. 2010;30:243-254.
Zhang J, Takahashi HK, Liu K, et al. Anti-high mobility group box-1 monoclonal antibody protects the blood-brain barrier from ischemia-induced disruption in rats. Stroke. 2011;42:1420-1428.
Lin Y-C, Chang Y-M, Yu J-M, Yen J-H, Chang J-G, Hu CJ. Toll-like receptor 4 gene C119A but not Asp299Gly polymorphism is associated with ischemic stroke among ethnic Chinese in Taiwan. Atherosclerosis. 2005;180:305-309.
Yang Q, Li J, Lu F, Wen A, Xiang J, et al. Upregulated expression of toll-like receptor 4 in monocytes correlates with severity of acute cerebral infarction. J Cereb Blood Flow Metab. 2008;28:1588-1596.
Azam S, Jakaria M, Kim I-S, Kim J, Haque ME, Choi DK. Regulation of toll-like receptor (TLR) signaling pathway by polyphenols in the treatment of age-linked neurodegenerative diseases: Focus on TLR4 signaling. Front Immunol. 2019;10:1000.
Powers WJ. Acute ischemic stroke. N Engl J Med. 2020;383:252-260.
Kamal H, Tan GC, Ibrahim SF, et al. Alcohol use disorder, neurodegeneration, Alzheimer's and Parkinson's disease: Interplay between oxidative stress, Neuroimmune response and excitotoxicity. Front Cell Neurosci. 2020;14:282.
He J, Crews FT. Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol. 2008;210:349-358.
Coleman LG, Zou J, Crews FT. Microglial-derived miRNA let-7 and HMGB1 contribute to ethanol-induced neurotoxicity via TLR7. J Neuroinflammation. 2017;14:22.
Vetreno RP, Crews FT. Adolescent binge drinking increases expression of the danger signal receptor agonist HMGB1 and toll-like receptors in the adult prefrontal cortex. Neuroscience. 2012;226:475-488.
Pascual-Lucas M, Viana da Silva S, Di Scala M, Garcia-Barroso C, González-Aseguinolaza G, et al. Insulin-like growth factor 2 reverses memory and synaptic deficits in APP transgenic mice. EMBO Mol Med. 2014;6:1246-1262.
Alfonso-Loeches S, Pascual-Lucas M, Blanco AM, Sanchez-Vera I, Guerri C. Pivotal role of TLR4 receptors in alcohol-induced neuroinflammation and brain damage. J Neurosci: Off J Soc Neurosci. 2010;30:8285-8295.
Fernandez-Lizarbe S, Pascual M, Guerri C. Critical role of TLR4 response in the activation of microglia induced by ethanol. J Immunol (Baltimore, Md.: 1950). 2009;183:4733-4744.
Alfonso-Loeches S, Pascual M, Gómez-Pinedo U, Pascual-Lucas M, Renau-Piqueras J, Guerri C. Toll-like receptor 4 participates in the myelin disruptions associated with chronic alcohol abuse. Glia. 2012;60:948-964.
Montesinos J, Pascual M, Pla A, et al. TLR4 elimination prevents synaptic and myelin alterations and long-term cognitive dysfunctions in adolescent mice with intermittent ethanol treatment. Brain Behav Immun. 2015;45:233-244.
Pascual M, Baliño P, Aragón CMG, Guerri C. Cytokines and chemokines as biomarkers of ethanol-induced neuroinflammation and anxiety-related behavior: Role of TLR4 and TLR2. Neuropharmacology. 2015;89:352-359.
Crews FT, Vetreno RP. Mechanisms of neuroimmune gene induction in alcoholism. Psychopharmacology (Berl). 2016;233:1543-1557.
Pascual M, López-Hidalgo R, Montagud-Romero S, Ureña-Peralta JR, Rodríguez-Arias M, et al. Role of mTOR-regulated autophagy in spine pruning defects and memory impairments induced by binge-like ethanol treatment in adolescent mice. Brain Pathol (Zurich, Switzerland). 2021;31:174-188.
Alfonso-Loeches S, Ureña-Peralta JR, Morillo-Bargues MJ, Oliver-De La Cruz J, Guerri C. Role of mitochondria ROS generation in ethanol-induced NLRP3 inflammasome activation and cell death in astroglial cells. Front Cell Neurosci. 2014;8:216.
Lippai D, Bala S, Petrasek J, et al. Alcohol-induced IL-1β in the brain is mediated by NLRP3/ASC inflammasome activation that amplifies neuroinflammation. J Leukoc Biol. 2013;94:171-182.
Pascual M, Ibáñez F, Guerri C. Exosomes as mediators of neuron-glia communication in neuroinflammation. Neural Regen Res. 2020;15:796-801.
Ibáñez F, Montesinos J, Ureña-Peralta JR, Guerri C, Pascual M. TLR4 participates in the transmission of ethanol-induced neuroinflammation via astrocyte-derived extracellular vesicles. J Neuroinflammation. 2019;16:136.
Eacker SM, Dawson TM, Dawson VL. Understanding microRNAs in neurodegeneration. Nat Rev Neurosci. 2009;10:837-841.
Ibáñez F, Ureña-Peralta JR, Costa-Alba P, Torres J-L, Laso F-J, et al. Circulating MicroRNAs in extracellular vesicles as potential biomarkers of alcohol-induced Neuroinflammation in adolescence: Gender differences. Int J Mol Sci. 2020;21:6730-6745.
Chen J-J, Zhao B, Zhao J, Li S. Potential roles of exosomal MicroRNAs as diagnostic biomarkers and therapeutic application in Alzheimer's disease. Neural Plast. 2017;2017:7027380.
Yao Y-F, Qu M-W, Li G-C, Zhang F-B, Rui H-C. Circulating exosomal miRNAs as diagnostic biomarkers in Parkinson's disease. Eur Rev Med Pharmacol Sci. 2018;22:5278-5283.
Niu M, Li Y, Li G, et al. A longitudinal study on α-synuclein in plasma neuronal exosomes as a biomarker for Parkinson's disease development and progression. Eur J Neurol. 2020;27:967-974.
Sharma S, Lu H-C. microRNAs in neurodegeneration: Current findings and potential impacts. J Alzheimer's Dis Parkin. 2018;8:420-441.
Swarbrick S, Wragg N, Ghosh S, Stolzing A. Systematic review of miRNA as biomarkers in Alzheimer's disease. Mol Neurobiol. 2019;56:6156-6167.
Dong Y, Han L-L, Xu Z-X. Suppressed microRNA-96 inhibits iNOS expression and dopaminergic neuron apoptosis through inactivating the MAPK signaling pathway by targeting CACNG5 in mice with Parkinson's disease. Mol Med (Cambridge, Mass.). 2018;24:61.
Higaki S, Muramatsu M, Matsuda A, et al. Defensive effect of microRNA-200b/c against amyloid-beta peptide-induced toxicity in Alzheimer's disease models. PLoS One. 2018;13:e0196929.
Qin L-X, Tan J-Q, Zhang H-N, et al. Preliminary study of hsa-mir-626 change in the cerebrospinal fluid in Parkinson's disease. Neurol India. 2021;69:115-118.
Ureña-Peralta JR, Alfonso-Loeches S, Cuesta-Diaz CM, García-García F, Guerri C. Deep sequencing and miRNA profiles in alcohol-induced neuroinflammation and the TLR4 response in mice cerebral cortex. Sci Rep. 2018;8:15913.
Vijay K. Toll-like receptors in immunity and inflammatory diseases: Past, present, and future. Int Immunopharmacol. 2018;59:391-412.
Gambuzza ME, Sofo V, Salmeri FM, Soraci L, Marino S, et al. Toll-like receptors in Alzheimer's disease: A therapeutic perspective. CNS Neurol Disord Drug Targets. 2014;13:1542-1558.
Rice TW, Wheeler AP, Bernard GR, et al. A randomized, double-blind, placebo-controlled trial of TAK-242 for the treatment of severe sepsis. Crit Care Med. 2010;38:1685-1694.
Bennett-Guerrero E, Grocott HP, Levy JH, et al. A phase II, double-blind, placebo-controlled, ascending-dose study of Eritoran (E5564), a lipid a antagonist, in patients undergoing cardiac surgery with cardiopulmonary bypass. Anesth Analg. 2007;104:378-383.
Bartels AL, Willemsen ATM, Doorduin J, de Vries EFJ, Dierckx RA, Leenders KL. [11C]-PK11195 PET: Quantification of neuroinflammation and a monitor of anti-inflammatory treatment in Parkinson's disease? Parkinsonism Relat Disord. 2010;16:57-59.
Fattahi MJ, Jamshidi AR, Mahmoudi M, et al. Evaluation of the efficacy and safety of β-d-mannuronic acid in patients with ankylosing spondylitis: A 12-week randomized, placebo-controlled, phase I/II clinical trial. Int Immunopharmacol. 2018;54:112-117.
Lv R, Du L, Liu X, Zhou F, Zhang Z, et al. Rosmarinic acid attenuates inflammatory responses through inhibiting HMGB1/TLR4/NF-κB signaling pathway in a mouse model of Parkinson's disease. Life Sci. 2019;223:158-165.
Feng Y, Zheng C, Zhang Y, Xing C, Cai W, et al. Triptolide inhibits preformed fibril-induced microglial activation by targeting the MicroRNA155-5p/SHIP1 pathway. Oxid Med Cell Longev. 2019;2019:e6527638.
Pascual M, Blanco AM, Cauli O, Miñarro J, Guerri C. Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. Eur J Neurosci. 2007;25:541-550.
Rodriguez-Otormin F, Duro-Castano A, Conejos-Sánchez I, Vicent MJ. Envisioning the future of polymer therapeutics for brain disorders. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2019;11:e1532.
Huang N, Lu S, Liu X-G, Zhu J, Wang Y-J, Liu RT. PLGA nanoparticles modified with a BBB-penetrating peptide co-delivering Aβ generation inhibitor and curcumin attenuate memory deficits and neuropathology in Alzheimer's disease mice. Oncotarget. 2017;8:81001-81013.
Nalamolu KR, Challa SR, Fornal CA, et al. Attenuation of the induction of TLRs 2 and 4 mitigates inflammation and promotes neurological recovery after focal cerebral ischemia. Transl Stroke Res. 2021.
Boozari M, Butler AE, Sahebkar A. Impact of curcumin on toll-like receptors. J Cell Physiol. 2019;234:12471-12482.
Cuesta CM, Ibañez F, Lopez-Hidalgo R, Ureña J, Duro-Castano A, et al. A targeted polypeptide-based nanoconjugate as a nanotherapeutic for alcohol-induced neuroinflammation. Nanomed: Nanotechnol Biol Med. 2021;102376-102385.

Auteurs

María Pascual (M)

Department of Physiology, School of Medicine and Dentistry, University of Valencia, Valencia, Spain.

Maria Calvo-Rodriguez (M)

Alzheimer's Research Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts, USA.

Lucía Núñez (L)

Institute of Biology and Molecular Genetics (IBGM), University of Valladolid and National Research Council (CSIC), Valladolid, Spain.
Department of Biochemistry and Molecular Biology and Physiology, University of Valladolid, Valladolid, Spain.

Carlos Villalobos (C)

Institute of Biology and Molecular Genetics (IBGM), University of Valladolid and National Research Council (CSIC), Valladolid, Spain.

Juan Ureña (J)

Department of Molecular and Cellular Pathology of Alcohol, Príncipe Felipe Research Center, Valencia, Spain.

Consuelo Guerri (C)

Department of Molecular and Cellular Pathology of Alcohol, Príncipe Felipe Research Center, Valencia, Spain.

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