Inhibition of Microglial Activation Protects Hippocampal Neurogenesis and Improves Cognitive Deficits in a Transgenic Mouse Model for Alzheimer’s Disease
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Background: Activated microglia with macrophage-like functions invade and surround β-amyloid (Aβ) plaques in Alzheimer’s disease (AD), possibly contributing to the turnover of Aβ, but they can also secrete proinflammatory factors that may be involved in the pathogenesis of AD. Microglia are known to modulate adult hippocampal neurogenesis. Objectives/Methods: To determine the role of microglia on neurogenesis in brains with Aβ pathology, we inhibited microglial activation with the tetracycline derivative minocycline in doubly transgenic mice expressing mutant human amyloid precursor protein (APP) and mutant human presenilin-1 (PS1). Results: Minocycline increased the survival of new dentate granule cells in APP/PS1 mice indicated by more BrdU+/NeuN+ cells as compared to vehicle-treated transgenic littermates, accompanied by improved behavioral performance in a hippocampus-dependent learning task. Both brain levels of Aβ and Aβ-related morphological deficits in the new neurons labeled with GFP-expressing retrovirus were unaffected in minocycline-treated mice. Conclusions: These results suggest a role for microglia in Aβ-related functional deficits and in suppressing the survival of new neurons, and show that modulation of microglial function with minocycline can protect hippocampal neurogenesis in the presence of Aβ pathology.
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Treatment with anti-inflammatory medication tends to mitigate cognitive impairment in animal models of amyloid-β injection.
“treatment with antiinflammatory medication tends to mitigate cognitive impairment in animal models of amyloid-β injection [149, 150].”
From Brain-Derived Neurotrophic Factor in Brain Disorders: Focus on Neuroinflammation (2019) · cites this paper as [150]
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Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide
Haass, C., & Selkoe, D. J. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2101 · Cited by 4,744 · see citing works
Correlative Memory Deficits, Aβ Elevation, and Amyloid Plaques in Transgenic Mice
Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F., & Cole, G. (1996) · Science · doi:10.1126/science.274.5284.99 · Cited by 4,210 · see citing works
The efficiency of systematic sampling in stereology and its prediction *
Gundersen, H., & Jensen, E. B. V. (1987) · Journal of Microscopy · doi:10.1111/j.1365-2818.1987.tb02837.x · Cited by 3,586 · see citing works
Mechanisms and Functional Implications of Adult Neurogenesis
Zhao, C., Deng, W., & Gage, F. H. (2008) · Cell · doi:10.1016/j.cell.2008.01.033 · Cited by 3,007 · see citing works
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · see citing works
Functional neurogenesis in the adult hippocampus
van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002) · Nature · doi:10.1038/4151030a · Cited by 2,853 · see citing works
Inflammatory Blockade Restores Adult Hippocampal Neurogenesis
Monje, M. L., Toda, H., & Palmer, T. D. (2003) · Science · doi:10.1126/science.1088417 · Cited by 2,426 · see citing works
ADULT NEUROGENESIS IN THE MAMMALIAN CENTRAL NERVOUS SYSTEM
Ming, G., & Song, H. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.051804.101459 · Cited by 1,829 · see citing works
Amyloid-β–induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks
Palop, J. J., & Mucke, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2583 · Cited by 1,651 · see citing works
Inflammation is detrimental for neurogenesis in adult brain
Ekdahl, C. T., Claasen, J.-H., Bonde, S., Kokaia, Z., & Lindvall, O. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2234031100 · Cited by 1,559 · see citing works
Self-citationHolcomb, L., Gordon, M. N., McGowan, E., Yu, X., Benkovic, S., Jantzen, P., Wright, K., Saad, I., Mueller, R., Morgan, D., et al. (1998) · Nature Medicine · doi:10.1038/nm0198-097 · Cited by 1,386 · see citing works
Wyss-Coray (2006) · doi:10.1038/nm1484 · Cited by 1,284 · see citing works
Bevins, R. A., & Besheer, J. (2006) · Nature Protocols · doi:10.1038/nprot.2006.205 · Cited by 1,278 · see citing works
Ziv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., Cohen, H., Kipnis, J., & Schwartz, M. (2006) · Nature Neuroscience · doi:10.1038/nn1629 · Cited by 1,209 · see citing works
Zhu, S., Stavrovskaya, I. G., Drozda, M., Kim, B. Y. S., Ona, V. O., Li, M., Sarang, S. S., Liu, A. S., Hartley, D. M., Wu, D. C., et al. (2002) · Nature · doi:10.1038/417074a · Cited by 1,071 · see citing works
Bravo, R., & Macdonald-Bravo, H. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.4.1549 · Cited by 928 · see citing works
Kee, N., Teixeira, C. M., Wang, A. H., & Frankland, P. W. (2007) · Nature Neuroscience · doi:10.1038/nn1847 · Cited by 875 · see citing works
Imai, Y., Ibata, I., Ito, D., Ohsawa, K., & Kohsaka, S. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1112 · Cited by 872 · see citing works
A role for adult neurogenesis in spatial long-term memory
Snyder, J. S., Hong, N. S., McDonald, R. J., & Wojtowicz, J. M. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.10.009 · Cited by 854 · see citing works
Brain inflammation and adult neurogenesis: The dual role of microglia
Ekdahl, C. T., Kokaia, Z., & Lindvall, O. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.052 · Cited by 801 · see citing works
Self-citationThe small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines
Peters, A., & Kaiserman‐Abramof, I. R. (1970) · American Journal of Anatomy · doi:10.1002/aja.1001270402 · Cited by 740 · see citing works
Combs, C. K., Karlo, J. C., Kao, S.-C., & Landreth, G. E. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-04-01179.2001 · Cited by 721 · see citing works
Jessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D., Consiglio, A., Lie, D. C., Squire, L. R., & Gage, F. H. (2009) · Learning & Memory · doi:10.1101/lm.1172609 · Cited by 654 · see citing works
Vallières, L., Campbell, I. L., Gage, F. H., & Sawchenko, P. E. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-00486.2002 · Cited by 598 · see citing works
Spatial Relational Memory Requires Hippocampal Adult Neurogenesis
Dupret, D., Revest, J., Koehl, M., Ichas, F., Giorgi, F. D., Costet, P., Abrous, D. N., & Piazza, P. V. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001959 · Cited by 595 · see citing works
Neurogenesis in the Adult Brain: New Strategies for Central Nervous System Diseases
Lie, D. C., Song, H., Colamarino, S. A., Ming, G., & Gage, F. H. (2004) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.44.101802.121631 · Cited by 589 · see citing works
Formation and maintenance of Alzheimer's disease β-amyloid plaques in the absence of microglia
Grathwohl, S. A., Kälin, R. E., Bolmont, T., Prokop, S., Winkelmann, G., Kaeser, S. A., Odenthal, J., Radde, R., Eldh, T., Gandy, S., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2432 · Cited by 401 · see citing works
Microglia and inflammatory mechanisms in the clearance of amyloid β peptide
Rogers, J., Strohmeyer, R., Kovelowski, C. J., & Li, R. (2002) · Glia · doi:10.1002/glia.10153 · Cited by 381 · see citing works
Thored, P., Heldmann, U., Gomes‐Leal, W., Gisler, R., Darsalia, V., Taneera, J., Nygren, J. M., Jacobsen, S. W., Ekdahl, C. T., Kokaia, Z., et al. (2009) · Glia · doi:10.1002/glia.20810 · Cited by 378 · see citing works
Self-citationMechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase
Brown, G. C. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351119 · Cited by 315 · see citing works
Prospects for Minocycline Neuroprotection
Plane, J. M., Shen, Y., Pleasure, D., & Deng, W. (2010) · Archives of Neurology · doi:10.1001/archneurol.2010.191 · Cited by 276 · see citing works
Time Course of the Development of Alzheimer-like Pathology in the Doubly Transgenic PS1+APP Mouse
Gordon, M. N., Holcomb, L. A., Jantzen, P. T., DiCarlo, G., Wilcock, D., Boyett, K. W., Connor, K., Melachrino, J., O'Callaghan, J. P., & Morgan, D. (2002) · Experimental Neurology · doi:10.1006/exnr.2001.7754 · Cited by 247 · see citing works
Minocycline affects microglia activation, Aβ deposition, and behavior in APP‐tg mice
Seabrook, T. J., Jiang, L., Maier, M., & Lemere, C. A. (2006) · Glia · doi:10.1002/glia.20338 · Cited by 223 · see citing works
Kiyota, T., Okuyama, S., Swan, R. J., Jacobsen, M. T., Gendelman, H. E., & Ikezu, T. (2010) · The FASEB Journal · doi:10.1096/fj.10-155317 · Cited by 212 · see citing works
Fan, R., Xu, F., Previti, M. L., Davis, J., Grande, A. V., Robinson, J. K., & Nostrand, W. E. V. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4371-06.2007 · Cited by 195 · see citing works
Morgan, D., Gordon, M. N., Tan, J., Wilcock, D. M., & Rojiani, A. M. (2005) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/01.jnen.0000178444.33972.e0 · Cited by 174 · see citing works
Choi, S. H., Veeraraghavalu, K., Lazarov, O., Marler, S., Ransohoff, R. M., Ramirez, J., & Sisodia, S. S. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.033 · Cited by 171 · see citing works
Inflammation Regulates Functional Integration of Neurons Born in Adult Brain
Jakubs, K., Bonde, S., Iosif, R. E., Ekdahl, C. T., Kokaia, Z., Kokaia, M., & Lindvall, O. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3240-08.2008 · Cited by 148 · see citing works
Self-citationRats with lesions of the hippocampus are impaired on the delayed nonmatching‐to‐sample task†
Clark, R. E., West, A. N., Zola, S. M., & Squire, L. R. (2001) · Hippocampus · doi:10.1002/hipo.1035 · Cited by 135 · see citing works
Liu, Y., Lin, H.-I., & Tzeng, S. (2005) · Brain Research · doi:10.1016/j.brainres.2005.06.085 · Cited by 130 · see citing works
Minocycline reduces the development of abnormal tau species in models of Alzheimer's disease
Noble, W., Garwood, C., Stephenson, J., Kinsey, A. M., Hanger, D., & Anderton, B. (2009) · The FASEB Journal · doi:10.1096/fj.08-113795 · Cited by 123 · see citing works
Minocycline prevents cholinergic loss in a mouse model of Down's syndrome
Hunter, C. L., Bachman, D., & Granholm, A. (2004) · Annals of Neurology · doi:10.1002/ana.20250 · Cited by 120 · see citing works
Schmidt, M. L., Robinson, K. A., Lee, V. M., & Trojanowski, J. Q. (1995) · Europe PMC (PubMed Central) · Cited by 71 · see citing works
Biscaro, B., Lindvall, O., Höck, C., Ekdahl, C. T., & Nitsch, R. M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2055-09.2009 · Cited by 64 · see citing works
Self-citationMarcello, E. E., Epis, R., & Luca, M. D. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.083 · Cited by 61 · see citing works
Quintero, E. M., Willis, L., Singleton, R., Harris, N., Huang, P., Bhat, N., & Granholm, A.-C. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.104 · Cited by 58 · see citing works
Dolbeare, F. A. (1995) · PubMed · Cited by 40 · see citing works
Apoptotic cascades as possible targets for inhibiting cell death in Huntington’s disease
Pattison, L. R., Kotter, M., Fraga, D., & Bonelli, R. M. (2006) · Journal of Neurology · doi:10.1007/s00415-006-0198-8 · Cited by 36 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Marcello E, Epis R, Di Luca M: Amyloid f lir ting w it h sy naptic failure: towards a com- prehensive view of Alzheimer's disease pathogenesis. Eur J Pharmacol 2008; 585: 109-118.
- Seabrook TJ, et al: Minocycline affects mi- croglia activation, Abeta deposition, and be- havior in APP-tg mice. Glia 2006; 53: 776- 782.
- Biscaro /Lindvall /Tesco /Ekdahl /Nitsch Neurodegenerative Dis 2012;9:187-198 198
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Neuroinflammation in Alzheimer's disease
Heneka, M. T., Carson, M. J., Khoury, J. E., Landreth, G. E., Brosseron, F., Feinstein, D. L., Jacobs, A. H., Wyss-Coray, T., Vitorica, J., Ransohoff, R. M., et al. (2015) · The Lancet Neurology · doi:10.1016/s1474-4422(15)70016-5 · Cited by 6,226 · see citing works
Microglia Regulate the Number of Neural Precursor Cells in the Developing Cerebral Cortex
Cunningham, C. L., Martínez-Cerdeño, V., & Noctor, S. C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3441-12.2013 · Cited by 976 · see citing works
Brain-Derived Neurotrophic Factor in Brain Disorders: Focus on Neuroinflammation
Lima Giacobbo, B., Doorduin, J., Klein, H. C., Dierckx, R. A. J. O., Bromberg, E., & de Vries, E. F. J. (2019) · Molecular Neurobiology · doi:10.1007/s12035-018-1283-6 · Cited by 750 · see citing works
An Inflammation-Centric View of Neurological Disease: Beyond the Neuron
Skaper, S. D., Facci, L., Zusso, M., & Giusti, P. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00072 · Cited by 461 · see citing works
The role of pro-inflammatory cytokines in the neuroinflammation and neurogenesis of schizophrenia
Na, K., Jung, H., & Kim, Y. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.10.022 · Cited by 425 · see citing works
Neuroprotective Mechanisms of Resveratrol in Alzheimer’s Disease: Role of SIRT1
Gomes, B. A. Q., Silva, J. P. B., Romeiro, C. F. R., dos Santos, S. M., Rodrigues, C. A., Gonçalves, P. R., Sakai, J. T., Mendes, P. F. S., Varela, E. L. P., & Monteiro, M. C. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/8152373 · Cited by 403 · see citing works
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Kohman, R. A., & Rhodes, J. S. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.09.003 · Cited by 363 · see citing works
Skvarc, D., Berk, M., Byrne, L., Dean, O., Dodd, S., Lewis, M., Marriott, A., Moore, E., Morris, G., Page, R., et al. (2018) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.11.011 · Cited by 301 · see citing works
Oxidative and nitrative stress in neurodegeneration
Cobb, C. A., & Cole, M. P. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.04.020 · Cited by 300 · see citing works
Maurer, S. V., & Williams, C. L. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01489 · Cited by 266 · see citing works
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Sierra, A., Beccari, S., Díaz‐Aparicio, I., Encinas, J. M., Comeau, S., & Tremblay, M. (2014) · Neural Plasticity · doi:10.1155/2014/610343 · Cited by 249 · see citing works
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Bilkei‐Gorzó, A. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.12.009 · Cited by 244 · see citing works
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Hua, Y., Dai, X., Xu, Y., Xing, G., Liu, H., Lu, T., Chen, Y., & Zhang, Y. (2022) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2022.114239 · Cited by 232 · see citing works
Qin, J., Ma, Z., Chen, X., & Shu, S. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1103416 · Cited by 229 · see citing works
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Araki, T., Ikegaya, Y., & Koyama, R. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14969 · Cited by 208 · see citing works
Agis-Torres, A., Sollhuber, M., Fernandez, M., & Sanchez-Montero, J. M. (2014) · Current Neuropharmacology · doi:10.2174/1570159x113116660047 · Cited by 202 · see citing works
Howard, R., Zubko, O., Bradley, R., Harper, E., Pank, L., O’Brien, J., Fox, C., Tabet, N., Livingston, G., Bentham, P., et al. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2019.3762 · Cited by 194 · see citing works
Ryan, S. M., & Nolan, Y. M. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.12.004 · Cited by 191 · see citing works
Mattei, D., Djodari-Irani, A., Hadar, R., Pelz, A., de Cossío, L. F., Goetz, T., Matyash, M., Kettenmann, H., Winter, C., & Wolf, S. A. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.01.019 · Cited by 188 · see citing works
The link between chronic pain and Alzheimer’s disease
Cao, S., Fisher, D. W., Yu, T., & Dong, H. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1608-z · Cited by 183 · see citing works
Scholz, R., Sobotka, M., Caramoy, A., Stempfl, T., Moehle, C., & Langmann, T. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0431-4 · Cited by 177 · see citing works
Skaper, S. D., Facci, L., & Giusti, P. (2015) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527313666141130224206 · Cited by 168 · see citing works
Adult hippocampal neurogenesis in Alzheimer’s disease: A roadmap to clinical relevance
Salta, E., Lazarov, O., Fitzsimons, C. P., Tanzi, R. E., Lucassen, P. J., & Choi, S. H. (2023) · Cell stem cell · doi:10.1016/j.stem.2023.01.002 · Cited by 165 · see citing works
Guadagno, J., Swan, P., Shaikh, R., & Cregan, S. P. (2015) · Cell Death and Disease · doi:10.1038/cddis.2015.151 · Cited by 150 · see citing works
Chen, J.-H., Ke, K.-F., Lu, J.-H., Qiu, Y.-H., & Peng, Y.-P. (2015) · PLOS ONE · doi:10.1371/journal.pone.0116549 · Cited by 151 · see citing works
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The Role of TNF-α in Alzheimer’s Disease: A Narrative Review
Plantone, D., Pardini, M., Righi, D., Manco, C., Colombo, B. M., & Stefano, N. D. (2023) · Cells · doi:10.3390/cells13010054 · Cited by 119 · see citing works
Hu, F., Ku, M., Markovic, D. S., Dzaye, O. D. A., Lehnardt, S., Synowitz, M., Wolf, S. A., & Kettenmann, H. (2014) · International Journal of Cancer · doi:10.1002/ijc.28908 · Cited by 114 · see citing works
Microglia and inflammation: conspiracy, controversy or control?
Fernandes, A. M. A., Miller‐Fleming, L., & Pais, T. F. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1670-8 · Cited by 110 · see citing works
Bernardo, T. C., Marques‐Aleixo, I., Beleza, J., Oliveira, P. J., Ascensão, A., & Magalhães, J. (2016) · Brain Pathology · doi:10.1111/bpa.12403 · Cited by 108 · see citing works
Garcez, M. L., Mina, F., Bellettini-Santos, T., Carneiro, F. G., Luz, A. P., Schiavo, G. L., Andrighetti, M. S., Scheid, M. G., Bolfe, R. P., & Budni, J. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.03.010 · Cited by 102 · see citing works
Ryan, S. M., & Kelly, A. M. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.03.007 · Cited by 104 · see citing works
Hippocampal adult neurogenesis: Does the immune system matter?
de Miranda, A. S., Zhang, C., Katsumoto, A., & Teixeira, A. L. (2016) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2016.10.052 · Cited by 100 · see citing works
Rapamycin‐mediated mouse lifespan extension: Late‐life dosage regimes with sex‐specific effects
Strong, R., Miller, R. A., Bogue, M. A., Fernández, E., Javors, M. A., Libert, S., Martinez, P. A., Murphy, M. P., Musi, N., Nelson, J. F., et al. (2020) · Aging Cell · doi:10.1111/acel.13269 · Cited by 99 · see citing works
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Cankaya, S., Cankaya, B., Kilic, U., Kilic, E., & Yulug, B. (2019) · Drugs in Context · doi:10.7573/dic.212553 · Cited by 93 · see citing works
Minocycline in neurodegenerative and psychiatric diseases: An update
Romero‐Miguel, D., Lamanna‐Rama, N., Casquero‐Veiga, M., Gómez‐Rangel, V., Desco, M., & Soto‐Montenegro, M. L. (2020) · European Journal of Neurology · doi:10.1111/ene.14642 · Cited by 95 · see citing works
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Yang, H., Yang, H., Xie, Z., Wei, L., & Bi, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069129 · Cited by 90 · see citing works
Targeting microglia for the treatment of Alzheimer’s disease
McGeer, P. L., & McGeer, E. G. (2014) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2014.988707 · Cited by 88 · see citing works
Dodiya, H. B., Frith, M., Sidebottom, A. M., Cao, Y., Koval, J., Chang, E. B., & Sisodia, S. S. (2020) · Scientific Reports · doi:10.1038/s41598-020-64797-5 · Cited by 84 · see citing works
D’Mello, C., Riazi, K., Le, T. P., Stevens, K. M., Wang, A., McKay, D. M., Pittman, Q. J., & Swain, M. G. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1329-13.2013 · Cited by 82 · see citing works
Resveratrol Boosts Cognitive Function by Targeting SIRT1
Cao, W., Dou, Y., & Li, A. (2018) · Neurochemical Research · doi:10.1007/s11064-018-2586-8 · Cited by 80 · see citing works
L’Episcopo, F., Tirolo, C., Caniglia, S., Testa, N., Morale, M. C., Serapide, M. F., Pluchino, S., & Marchetti, B. (2014) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjt053 · Cited by 80 · see citing works
Li, Y., Abdourahman, A., Tamm, J. A., Pehrson, A. L., Sánchez, C., & Gulinello, M. (2015) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2015.05.013 · Cited by 79 · see citing works
Discovering New Treatments for Alzheimer's Disease by Repurposing Approved Medications
Appleby, B. S., & Cummings, J. L. (2013) · Current Topics in Medicinal Chemistry · doi:10.2174/15680266113136660162 · Cited by 78 · see citing works
Smith, H. K., Gil, C. D., Oliani, S. M., & Gavins, F. N. E. (2015) · The FASEB Journal · doi:10.1096/fj.14-263160 · Cited by 78 · see citing works
Jiang, Y., Liu, Y., Zhu, C., Ma, X., Ma, L., Zhou, L., Huang, Q., Lei, C., Pi, R., & Chen, X. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.03.003 · Cited by 76 · see citing works
Luo, T., Wu, J., Kabadi, S. V., Sabirzhanov, B. E., Guanciale, K., Hanscom, M., Faden, J., Cardiff, K., Bengson, C. J., & Faden, A. I. (2013) · Anesthesiology · doi:10.1097/aln.0000000000000020 · Cited by 75 · see citing works
Hippocampal Neurogenesis in Alzheimer's Disease: Is There a Role for Dietary Modulation?
Maruszak, A., Pilarski, A. M., Murphy, T., Branch, N., & Thuret, S. (2013) · Journal of Alzheimer s Disease · doi:10.3233/jad-131004 · Cited by 75 · see citing works
Neuroinflammatory Signaling in the Pathogenesis of Alzheimer’s Disease
Uddin, M. S., Kabir, M. T., Jalouli, M., Rahman, M. A., Jeandet, P., Behl, T., Alexiou, A. T., Albadrani, G. M., Abdel‐Daim, M. M., Perveen, A., et al. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210826130210 · Cited by 76 · see citing works
Ma, D.-C., Zhang, N., Zhang, Y., & Chen, D. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113399 · Cited by 72 · see citing works
Linking pathways in the developing and aging brain with neurodegeneration
Kovács, G. G., Adle‐Biassette, H., Milenković, I., Cipriani, S., van Scheppingen, J., & Aronica, E. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.03.045 · Cited by 67 · see citing works
Peña‐Altamira, E., Prati, F., Massenzio, F., Virgili, M., Contestabile, A., Bolognesi, M. L., & Monti, B. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2016.1121237 · Cited by 70 · see citing works
Zhang, Z., Daniels, R., & Schluesener, H. J. (2013) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12124 · Cited by 65 · see citing works
The Ever-Changing Morphology of Hippocampal Granule Neurons in Physiology and Pathology
Llorens-Martı́n, M., Rábano, A., & Ávila, J. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00526 · Cited by 61 · see citing works
Zou, Y., Corniola, R. S., Leu, D., Khan, A., Sahbaie, P., Chakraborti, A., Clark, J. D., Fike, J. R., & Huang, T. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216913110 · Cited by 63 · see citing works
Ahmed, A., Wang, L.-L., Abdel-Maksoud, S. A., Aboelgheit, A., Saeed, S., & Zhang, C. (2017) · Scientific Reports · doi:10.1038/s41598-017-14450-5 · Cited by 64 · see citing works
Isoglutaminyl cyclase contributes to CCL2-driven neuroinflammation in Alzheimer’s disease
Hartlage‐Rübsamen, M., Waniek, A., Meißner, J., Morawski, M., Schilling, S., Jäger, C., Kleinschmidt, M., Cynis, H., Kehlen, A., Arendt, T., et al. (2015) · Acta Neuropathologica · doi:10.1007/s00401-015-1395-2 · Cited by 61 · see citing works
Parul, P., Mishra, A., Singh, S., Singh, S., Tiwari, V., Chaturvedi, S., Wahajuddin, M., Palit, G., & Shukla, S. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.04.017 · Cited by 62 · see citing works
Moore, E., Kooshki, M., Metheny‐Barlow, L. J., Gallagher, P. E., & Robbins, M. E. C. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.08.183 · Cited by 57 · see citing works
The role of glial cells in Alzheimer disease: potential therapeutic implications
Cabezas, I. L., Batista, A. H., & Rol, G. P. (2014) · Neurología (English Edition) · doi:10.1016/j.nrleng.2012.10.009 · Cited by 57 · see citing works
Shamim, D., & Laskowski, M. C. (2017) · Journal of Central Nervous System Disease · doi:10.1177/1179573517722512 · Cited by 56 · see citing works
Zhang, F., Ran, Y., Tahir, M., Li, Z., Wang, J., & Chen, X. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.955222 · Cited by 55 · see citing works
Garcez, M. L., Mina, F., Bellettini‐Santos, T., da Luz, A. P., Schiavo, G. L., Macieski, J. M. C., Medeiros, E. B., Marques, A. O., Magnus, N. Q., & Budni, J. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1211-9 · Cited by 53 · see citing works
Kuo, Y., Chen, C.-L., & Rajesh, R. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.01.065 · Cited by 54 · see citing works
Navakkode, S., Liu, C., & Soong, T. W. (2018) · Ageing Research Reviews · doi:10.1016/j.arr.2018.01.001 · Cited by 53 · see citing works
The role of microglia in Alzheimer's disease and progress of treatment
Guan, Y., Zhang, L., Wang, S., Deng, Y., Zhou, H., Chen, D., & Zhang, L. (2022) · Ibrain · doi:10.1002/ibra.12023 · Cited by 51 · see citing works
Sun, L., Li, X., Wang, F., Zhang, J., Wang, D., Yuan, L., Wu, M., Wang, Z.-J., & Qi, J. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23996 · Cited by 52 · see citing works
Role of Microglia in Modulating Adult Neurogenesis in Health and Neurodegeneration
Al‐Onaizi, M., Al-Khalifah, A., Qasem, D., & ElAli, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186875 · Cited by 53 · see citing works
Alzheimer’s disease pathogenesis: standing at the crossroad of lipid metabolism and immune response
Wang, Z., Zhang, L., & Qin, C. (2025) · Molecular Neurodegeneration · doi:10.1186/s13024-025-00857-6 · Cited by 54 · see citing works
Papel de la glía en la enfermedad de Alzheimer. Futuras implicaciones terapéuticas
Cabezas, I. L., Batista, A. H., & Rol, G. P. (2012) · Neurología · doi:10.1016/j.nrl.2012.10.006 · Cited by 50 · see citing works
Abbaszadeh, A., Darabi, S., Hasanvand, A., Amini-Khoei, H., Abbasnezhad, A., Choghakhori, R., & Aaliehpour, A. (2018) · Europe PMC (PubMed Central) · doi:10.22038/ijbms.2017.24248.6053 · Cited by 50 · see citing works
Minocycline Reduces Spontaneous Hemorrhage in Mouse Models of Cerebral Amyloid Angiopathy
Yan, P., Zhu, A., Liao, F., Xiao, Q.-L., Kraft, A. W., Gonzales, E., Perez, R., Greenberg, S., Holtzman, D., & Lee, J.-M. (2015) · Stroke · doi:10.1161/strokeaha.115.008582 · Cited by 35 · see citing works
Darlington, D., Deng, J., Giunta, B. N., Hou, H., Sanberg, C. D., Kuzmin‐Nichols, N., Zhou, H., Mori, T., Ehrhart, J. C., Sanberg, P. R., et al. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0345 · Cited by 46 · see citing works
Cannabinoid Actions on Neural Stem Cells: Implications for Pathophysiology
Rodrigues, R. S., Lourenço, D. M., Paulo, S. L., Mateus, J. M., Ferreira, M. F., Mouro, F. M., Moreira, J. B., Ribeiro, F. F., Sebastião, A. M., & Xapelli, S. (2019) · Molecules · doi:10.3390/molecules24071350 · Cited by 45 · see citing works
Rahmani, M., Negro, S., & Barcia, E. (2022) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2022.106237 · Cited by 42 · see citing works
Mizuno, Y., Abolhassani, N., Mazzei, G., Sakumi, K., Saito, T., Saido, T. C., Ninomiya, T., Iwaki, T., Yamasaki, R., Kira, J., et al. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/8635088 · Cited by 41 · see citing works
Duan, L., Chen, B., Sun, X., Luo, Z.-J., Rao, Z., Wang, J., & Chen, L.-W. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073768 · Cited by 39 · see citing works
Song, R., Yin, S., Wu, J., & Yan, J. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-24-00025 · Cited by 39 · see citing works
Systemic inflammation as a central player in the initiation and development of Alzheimer’s disease
Bayraktaroğlu, I., Ortí-Casañ, N., Dam, D. V., Deyn, P. P. D., & Eisel, U. L. M. (2025) · Immunity & Ageing · doi:10.1186/s12979-025-00529-5 · Cited by 42 · see citing works
Rao, S. K., Ross, J. M., Harrison, F. E., Bernardo, A., Reiserer, R. S., Reiserer, R. S., Mobley, J. A., & McDonald, M. P. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.03.018 · Cited by 37 · see citing works
Challenges of Repurposing Tetracyclines for the Treatment of Alzheimer’s and Parkinson’s Disease
Markulin, I., Matasin, M., Turk, V. E., & Salković-Petrisic, M. (2022) · Journal of Neural Transmission · doi:10.1007/s00702-021-02457-2 · Cited by 36 · see citing works
Adult neurogenesis in the dentate gyrus
Benarroch, E. E. (2013) · Neurology · doi:10.1212/wnl.0b013e3182a9a156 · Cited by 36 · see citing works
Defining functional changes in the brain caused by targeted stereotaxic radiosurgery.
Parihar, V. K., Acharya, M. M., Roa, D. E., Bosch, O., Christie, L., & Limoli, C. L. (2014) · PubMed · doi:10.3978/j.issn.2218-676x.2013.06.02 · Cited by 34 · see citing works
Impact of hippocampal neuronal ablation on neurogenesis and cognition in the aged brain
Yeung, S. T., Myczek, K., Kang, A., Chabrier, M. A., Baglietto‐Vargas, D., & LaFerla, F. M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.11.054 · Cited by 34 · see citing works
Xie, J., Li, Y., Dai, J., He, Y., Sun, D., Dai, C., Xu, H., & Yin, Z. Q. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00341 · Cited by 35 · see citing works
Insight into the role of adult hippocampal neurogenesis in aging and Alzheimer's disease
Chen, P., Guo, Z., & Zhou, B. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101828 · Cited by 36 · see citing works
Immunomodulatory role of the extracellular matrix protein tenascin-C in neuroinflammation
Wiemann, S., Reinhard, J., & Faissner, A. (2019) · Biochemical Society Transactions · doi:10.1042/bst20190081 · Cited by 33 · see citing works
Vecchioli, S. F., Ricci, V., & Middei, S. (2022) · Neural Plasticity · doi:10.1155/2022/9959044 · Cited by 34 · see citing works
Pluta, R., Bogucka-Kocka, A., Ułamek-Kozioł, M., Furmaga-Jabłońska, W., Januszewski, S., Brzozowska, J., Jabłoński, M., & Kocki, J. (2015) · Folia Neuropathologica · doi:10.5114/fn.2015.52405 · Cited by 34 · see citing works
Boosting mitochondrial health to counteract neurodegeneration
Burtscher, J., Romani, M., Bernardo, G., Popa, T., Ziviani, E., Hummel, F. C., Sorrentino, V., & Millet, G. P. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102289 · Cited by 34 · see citing works
Piazza, F. V., Segabinazi, E., Centenaro, L. A., do Nascimento, P. S., Achaval, M., & Marcuzzo, S. (2013) · Metabolic Brain Disease · doi:10.1007/s11011-013-9467-2 · Cited by 31 · see citing works
Yuan, Z., Chen, X., Yang, W., Lou, B., Ye, N., & Liu, Y. (2019) · PubMed Central · Cited by 31 · see citing works
Gao, H., Li, C., Nabeka, H., Shimokawa, T., Wang, Z., Cao, Y., & Matsuda, S. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160093 · Cited by 31 · see citing works
Corrêa-Velloso, J. C., Gonçalves, M. C., Naaldijk, Y., Oliveira‐Giacomelli, Á., Pillat, M. M., & Ulrich, H. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.04.033 · Cited by 31 · see citing works
LU, K., Zhang, C., Wu, W., Zhou, M., Tang, Y., & Peng, Y. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3693 · Cited by 30 · see citing works
Innate immunity in Alzheimer’s disease: the relevance of animal models?
Franco-Bocanegra, D., Nicoll, J. A. R., & Boche, D. (2017) · Journal of Neural Transmission · doi:10.1007/s00702-017-1729-4 · Cited by 31 · see citing works
Sun, D., Chen, J., Bao, X., Cai, Y., Zhao, J., Huang, J., Huang, W. Y., Fan, X., & Xu, H. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8875-6 · Cited by 29 · see citing works
Prevention of microgliosis halts early memory loss in a mouse model of Alzheimer’s disease
Kater, M. S. J., Huffels, C. F. M., Oshima, T., Renckens, N. S., Middeldorp, J., Boddeke, E., Smit, A. B., Eggen, B. J. L., Hol, E. M., & Verheijen, M. H. G. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.10.009 · Cited by 30 · see citing works
- Authors
- Biscaro, B., Lindvall, O., Tesco, G., Ekdahl, C. T., & Nitsch, R. M.
- Affiliations
- University of Zurich (CH)
- Lund University (SE)
- Tufts University (US)
- Venue
- Neurodegenerative Diseases
- Publisher
- S. Karger AG
- Published
- 2012
- Volume
- 9
- Issue
- 4
- Pages
- 187-198
- ISSN
- 1660-2854 (ISSN-L)
- 1660-2862
- PMC
- PMC7068786
- OpenAlex
- W2003614844
- Cited by
- 164
- References
- 48
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 7 · 2023: 8 · 2022: 14 · 2021: 7 · 2020: 13 · 2019: 14 · 2018: 11 · 2017: 12 · 2016: 7 · 2015: 20 · 2014: 17 · 2013: 16 · 2012: 6
- FWCI
- 9.49
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Neurodegenerative Diseases (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- Lund University Publications (Lund University) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Vetenskapsrådet
- National Institute on Aging (R01AG033016, R01AG025952)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- microglial activation, hippocampal neurogenesis, Alzheimer's disease, minocycline, amyloid-beta, APP/PS1 mice, dentate gyrus granule cells, cognitive impairment, neuroinflammation
- MeSH terms
- Alzheimer Disease, Animals, Anti-Inflammatory Agents, Cognition Disorders, Disease Models, Animal, Female, Hippocampus, Humans, Male, Mice, Inbred C57BL, Mice, Transgenic, Minocycline, Mutation, Amyloid beta-Protein Precursor, Microglia, Mice, Presenilin-1, Neurogenesis
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