Doxycycline counteracts neuroinflammation restoring memory in Alzheimer's disease mouse models

Neurobiology of Aging - Tập 70 - Trang 128-139 - 2018
Claudia Balducci1, Giulia Santamaria1, Pietro La Vitola1, Edoardo Brandi1, Federica Grandi1, Arturo Roberto Viscomi2, Marten Beeg3, Marco Gobbi3, Mario Salmona3, Simone Ottonello2, Gianluigi Forloni1
1Department of Neuroscience, IRCCS, Istituto di Ricerhe Farmacologiche Mario Negri, Milano, Italy
2Department of Biochemistry and Molecular Biology, University of Parma, Parma, Italy
3Department of Biochemistry, IRCCS, Istituto di Ricerhe Farmacologiche Mario Negri, Milano, Italy

Tài liệu tham khảo

Airoldi, 2011, Tetracycline prevents Abeta oligomer toxicity through an atypical supramolecular interaction, Org. Biomol. Chem., 9, 463, 10.1039/C0OB00303D Aronson, 1980, Pharmacotherapeutics of the newer tetracyclines, J. Am. Vet. Med. Assoc., 176, 1061 Assar, 2015, A case of variably protease-sensitive prionopathy treated with doxycyclin, J. Neurol. Neurosurg. Psychiatry, 86, 816, 10.1136/jnnp-2014-309871 Baazaoui, 2017, Prevention of amyloid-β and tau pathologies, associated neurodegeneration, and cognitive deficit by early treatment with a neurotrophic compound, J. Alzheimers Dis., 58, 215, 10.3233/JAD-170075 Balducci, 2010, Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein, Proc. Natl. Acad. Sci. U. S. A., 107, 2295, 10.1073/pnas.0911829107 Balducci, 2014, In vivo application of beta amyloid oligomers: a simple tool to evaluate mechanisms of action and new therapeutic approaches, Curr. Pharm. Des., 20, 2491, 10.2174/13816128113199990497 Balducci, 2017, 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., 60, 188, 10.1016/j.bbi.2016.10.012 Balducci, 2014, Multifunctional liposomes reduce brain β-amyloid burden and ameliorate memory impairment in Alzheimer's disease mouse models, J. Neurosci., 34, 14022, 10.1523/JNEUROSCI.0284-14.2014 Balducci, 2011, The gamma-secretase modulator CHF5074 restores memory and hippocampal synaptic plasticity in plaque-free Tg2576 mice, J. Alzheimers Dis., 24, 799, 10.3233/JAD-2011-101839 Bengoetxea, 2015, Object recognition test for studying cognitive impairments in animal models of Alzheimer’s disease, Front. Biosci. (Schol Ed), 7, 10, 10.2741/s421 Benilova, 2012, The toxic Abeta oligomer and Alzheimer’s disease: an emperor in need of clothes, Nat. Neurosci., 15, 349, 10.1038/nn.3028 Callaway, 2012, Alzheimer’s drugs take a new tack, Nature, 489, 13, 10.1038/489013a Coleman, 2003, Synaptic slaughter in Alzheimer’s disease, Neurobiol. Aging, 24, 1023, 10.1016/j.neurobiolaging.2003.09.001 De Luigi, 2008, The efficacy of tetracyclines in peripheral and intracerebral prion infection, PLoS One, 3, e1888, 10.1371/journal.pone.0001888 DeKosky, 1990, Synapse loss in frontal cortex biopsies in Alzheimer’s disease: correlation with cognitive severity, Ann. Neurol., 27, 457, 10.1002/ana.410270502 Diomede, 2010, Tetracycline and its analogues protect Caenorhabditis elegans from beta amyloid-induced toxicity by targeting oligomers, Neurobiol. Dis., 40, 424, 10.1016/j.nbd.2010.07.002 Fluharty, 2013, An N-terminal fragment of the prion protein binds to amyloid-beta oligomers and inhibits their neurotoxicity in vivo, J. Biol. Chem., 288, 7857, 10.1074/jbc.M112.423954 Forloni, 2016, Oligomeropathies and pathogenesis of Alzheimer and Parkinson’s diseases, Mov. Disord., 31, 771, 10.1002/mds.26624 Forloni, 2001, Anti-amyloidogenic activity of tetracyclines: studies in vitro, FEBS Lett., 487, 404, 10.1016/S0014-5793(00)02380-2 Forloni, 2002, Tetracyclines affect prion infectivity, Proc. Natl. Acad. Sci. U. S. A., 99, 10849, 10.1073/pnas.162195499 Forloni, 2009, Tetracyclines and prion infectivity, Infect Disord. Drug Targets, 9, 23, 10.2174/1871526510909010023 Frid, 2007, Congo red and protein aggregation in neurodegenerative diseases, Brain Res. Rev., 53, 135, 10.1016/j.brainresrev.2006.08.001 Gandy, 2017, Lifelong management of amyloid-beta metabolism to prevent Alzheimer’s disease, N. Engl. J. Med., 367, 864, 10.1056/NEJMe1207995 Grayson, 2015, Assessment of disease-related cognitive impairments using the novel object recognition (NOR) task in rodents, Behav. Brain Res., 285, 176, 10.1016/j.bbr.2014.10.025 Griffin, 2010, Tetracyclines: a pleitropic family of compounds with promising therapeutic properties. Review of the literature, Am. J. Physiol. Cell Physiol., 299, C539, 10.1152/ajpcell.00047.2010 Guerriero, 2017, Neuroinflammation, immune system and Alzheimer disease: searching for the missing link, Aging Clin. Exp. Res., 29, 821, 10.1007/s40520-016-0637-z Haik, 2014, Doxycycline in Creutzfeldt-Jakob disease: a phase 2, randomised, double-blind, placebo-controlled trial, Lancet Neurol., 13, 150, 10.1016/S1474-4422(13)70307-7 Hammond, 2004, On the delay-dependent involvement of the hippocampus in object recognition memory, Neurobiol. Learn Mem., 82, 26, 10.1016/j.nlm.2004.03.005 Heneka, 2015, Neuroinflammation in Alzheimer’s disease, Lancet Neurol., 14, 388, 10.1016/S1474-4422(15)70016-5 Hong, 2016, Complement and microglia mediate early synapse loss in Alzheimer mouse models, Science, 352, 712, 10.1126/science.aad8373 Huang, 2012, Alzheimer mechanisms and therapeutic strategies, Cell, 148, 1204, 10.1016/j.cell.2012.02.040 Jankowsky, 2001, Co-expression of multiple transgenes in mouse CNS: a comparison of strategies, Biomol. Eng., 17, 157, 10.1016/S1389-0344(01)00067-3 Kayed, 2013, Molecular mechanisms of amyloid oligomers toxicity, J. Alzheimers Dis., 33, S67 Kincheski, 2017, Chronic sleep restriction promotes brain inflammation and synapse loss, and potentiates memory impairment induced by amyloid-β oligomers in mice, Brain Behav. Immun., 64, 140, 10.1016/j.bbi.2017.04.007 Klein, 1995, Tetracyclines, Med. Clin. North Am., 79, 789, 10.1016/S0025-7125(16)30039-6 Krakauer, 2003, Doxycycline is anti-inflammatory and inhibits staphylococcal exotoxin-induced cytokines and chemokines, Antimicrob. Agents Chemother., 47, 3630, 10.1128/AAC.47.11.3630-3633.2003 Kumar, 2012, Specific soluble oligomers of amyloid-β peptide undergo replication and form non-fibrillar aggregates in interfacial environments, J. Biol. Chem., 287, 21253, 10.1074/jbc.M112.355156 Lee, 2012, Human umbilical cord blood-derived mesenchymal stem cells improve neuropathology and cognitive impairment in an Alzheimer’s disease mouse model through modulation of neuroinflammation, Neurobiol. Aging, 33, 588, 10.1016/j.neurobiolaging.2010.03.024 Lendel, 2014, A hexameric peptide barrel as building block of amyloid-β protofibrils, Angew. Chem. Int. Ed. Engl., 53, 12756, 10.1002/anie.201406357 Lesné, 2006, A specific amyloid-beta protein assembly in the brain impairs memory, Nature, 440, 352, 10.1038/nature04533 Liddelow, 2017, Neurotoxic reactive astrocytes are induced by activated microglia, Nature, 541, 481, 10.1038/nature21029 Loeb, 2004, A randomized, controlled trial of doxycycline and rifampin for patients with Alzheimer’s disease, J. Am. Geriatr. Soc., 52, 381, 10.1111/j.1532-5415.2004.52109.x Lue, 1999, Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer’s disease, Am. J. Pathol., 155, 853, 10.1016/S0002-9440(10)65184-X Mancini, 2017, Multifunctional liposomes delay phenotype progression and prevent memory impairment in a presymptomatic stage mouse model of Alzheimer disease, J. Control. Release, 258, 121, 10.1016/j.jconrel.2017.05.013 Mc Donald, 2010, The presence of sodium dodecyl sulphate-stable Abeta dimers is strongly associated with Alzheimer-type dementia, Brain, 133, 1328, 10.1093/brain/awq065 McLean, 1999, Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer’s disease, Ann. Neurol., 46, 860, 10.1002/1531-8249(199912)46:6<860::AID-ANA8>3.0.CO;2-M Molloy, 2013, A multicenter, blinded, randomized, factorial controlled trial of doxycycline and rifampin for treatment of Alzheimer’s disease: the DARAD trial, Int. J. Geriatr. Psychiatry, 28, 463, 10.1002/gps.3846 Morris, 2013, Microglia: a new frontier for synaptic plasticity, learning and memory, and neurodegenerative disease research, Neurobiol. Learn. Mem., 105, 40, 10.1016/j.nlm.2013.07.002 Mucke, 2012, Neurotoxicity of amyloid beta-protein: synaptic and network dysfunction, Cold Spring Harb. Perspect. Med., 2, a006338, 10.1101/cshperspect.a006338 Pocchiari, 2015, Rethinking of doxycycline therapy in Creutzfeldt-Jakob disease, J. Neurol. Neurosurg. Psychiatry, 86, 705, 10.1136/jnnp-2014-310127 Porat, 2006, Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism, Chem. Biol. Drug Des., 67, 27, 10.1111/j.1747-0285.2005.00318.x Rachal Pugh, 2001, The immune system and memory consolidation: a role for the cytokine IL-1beta, Neurosci. Biobehav. Rev., 25, 29, 10.1016/S0149-7634(00)00048-8 Reed, 1997, Impaired recognition memory in patients with lesions limited to the hippocampal formation, Behav. Neurosci., 111, 667, 10.1037/0735-7044.111.4.667 Santos, 2017, Acyl ghrelin improves cognition, synaptic plasticity deficits and neuroinflammation following amyloid beta (Aβ1-40) administration in mice, J. Neuroendocrinol., 29, 1, 10.1111/jne.12476 Sengupta, 2016, The role of amyloid-β oligomers in toxicity, propagation, and immunotherapy, EBioMedicine, 6, 42, 10.1016/j.ebiom.2016.03.035 Squire, 2007, Recognition memory and the medial temporal lobe: a new perspective, Nat. Rev. Neurosci., 8, 872, 10.1038/nrn2154 Stoilova, 2013, A new face for old antibiotics: tetracyclines in treatment of amyloidoses, J. Med. Chem., 56, 5987, 10.1021/jm400161p Sutton, 2006, Dendritic protein synthesis, synaptic plasticity, and memory, Cell, 127, 49, 10.1016/j.cell.2006.09.014 Tagliavini, 2000, Tetracycline affects abnormal properties of synthetic PrP peptides and PrP(Sc) in vitro, J. Mol. Biol., 300, 1309, 10.1006/jmbi.2000.3840 Tarr, 2011, The effects of age on lipopolysaccharide-induced cognitive deficits and interleukin-1beta expression, Behav. Brain Res., 217, 481, 10.1016/j.bbr.2010.10.036 Terry, 1991, Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment, Ann. Neurol., 30, 572, 10.1002/ana.410300410 Varges, 2017, Doxycycline in early CJD: a double-blinded randomised phase II and observational study, J. Neurol. Neurosurg. Psychiatry, 88, 119, 10.1136/jnnp-2016-313541 Vasconcelos, 2014, Intermittent fasting attenuates lipopolysaccharide-induced neuroinflammation and memory impairment, J. Neuroinflammation, 11, 85, 10.1186/1742-2094-11-85 Wang, 1999, The levels of soluble versus insoluble brain Abeta distinguish Alzheimer’s disease from normal and pathologic aging, Exp. Neurol., 158, 328, 10.1006/exnr.1999.7085 Wolff, 2015, Amyloid β oligomeric species present in the lag phase of amyloid formation, PLoS One, 10, e0127865, 10.1371/journal.pone.0127865 Yrjanheikki, 1998, Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia, Proc. Natl. Acad. Sci. U. S. A., 95, 15769, 10.1073/pnas.95.26.15769