Antibiotic-induced perturbations in microbial diversity during post-natal development alters amyloid pathology in an aged APPSWE/PS1ΔE9 murine model of Alzheimer’s disease
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Abstract Recent evidence suggests the commensal microbiome regulates host immunity and influences brain function; findings that have ramifications for neurodegenerative diseases. In the context of Alzheimer’s disease (AD), we previously reported that perturbations in microbial diversity induced by life-long combinatorial antibiotic (ABX) selection pressure in the APP SWE /PS1 ΔE9 mouse model of amyloidosis is commensurate with reductions in amyloid-β (Aβ) plaque pathology and plaque-localised gliosis. Considering microbiota-host interactions, specifically during early post-natal development, are critical for immune- and neuro-development we now examine the impact of microbial community perturbations induced by acute ABX exposure exclusively during this period in APP SWE /PS1 ΔE9 mice. We show that early post-natal (P) ABX treatment (P14-P21) results in long-term alterations of gut microbial genera (predominantly Lachnospiraceae and S24-7 ) and reduction in brain Aβ deposition in aged APP SWE /PS1 ΔE9 mice. These mice exhibit elevated levels of blood- and brain-resident Foxp3 + T-regulatory cells and display an alteration in the inflammatory milieu of the serum and cerebrospinal fluid. Finally, we confirm that plaque-localised microglia and astrocytes are reduced in ABX-exposed mice. These findings suggest that ABX-induced microbial diversity perturbations during post-natal stages of development coincide with altered host immunity mechanisms and amyloidosis in a murine model of AD.
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QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00062-07 · Cited by 19,770 · see citing works
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
Price, M. N., Dehal, P. S., & Arkin, A. P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009490 · Cited by 14,894 · see citing works
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
Lozupone, C., & Knight, R. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8228-8235.2005 · Cited by 8,227 · see citing works
Neurotoxic reactive astrocytes are induced by activated microglia
Liddelow, S. A., Guttenplan, K. A., Clarke, L. E., Bennett, F. C., Bohlen, C. J., Schirmer, L., Bennett, M. L., Münch, A. E., Chung, W.-S., Peterson, T. C., et al. (2017) · Nature · doi:10.1038/nature21029 · Cited by 7,971 · see citing works
Macrophage activation and polarization: nomenclature and experimental guidelines
Murray, P. J., Allen, J. E., Biswas, S. K., Fisher, E. A., Gilroy, D. W., Goerdt, S., Gordon, S., Hamilton, J. A., Ivashkiv, L. B., Lawrence, T., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.06.008 · Cited by 6,337 · see citing works
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
Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells
Furusawa, Y., Obata, Y., Fukuda, S., Endo, T. A., Nakato, G., Takahashi, D., Nakanishi, Y., Uetake, C., Kato, K., Kato, T., et al. (2013) · Nature · doi:10.1038/nature12721 · Cited by 5,549 · see citing works
McDonald, D. T., Price, M. N., Goodrich, J. K., Nawrocki, E. P., DeSantis, T. Z., Probst, A. J., Andersen, G. L., Knight, R. D., & Hugenholtz, P. (2011) · The ISME Journal · doi:10.1038/ismej.2011.139 · Cited by 5,010 · see citing works
Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation
Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., deRoos, P., Liu, H., Cross, J. R., Pfeffer, K., Coffer, P. J., et al. (2013) · Nature · doi:10.1038/nature12726 · Cited by 4,838 · see citing works
Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease
Sampson, T. R., Debelius, J. W., Thron, T., Janssen, S., Shastri, G. G., Ilhan, Z. E., Challis, C., Schretter, C. E., Rocha, S., Gradinaru, V., et al. (2016) · Cell · doi:10.1016/j.cell.2016.11.018 · Cited by 3,622 · see citing works
Host microbiota constantly control maturation and function of microglia in the CNS
Erny, D., Hrabě de Angelis, A. L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4030 · Cited by 3,569 · see citing works
PyNAST: a flexible tool for aligning sequences to a template alignment
Caporaso, J. G., Bittinger, K. L., Bushman, F. D., DeSantis, T. Z., Andersen, G. L., & Knight, R. D. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp636 · Cited by 3,374 · see citing works
<i>TREM2</i> Variants in Alzheimer's Disease
Guerreiro, R., Wojtas, A., Bras, J., Carrasquillo, M., Rogaeva, E., Majounie, E., Cruchaga, C., Sassi, C., Kauwe, J. S. K., Younkin, S., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1211851 · Cited by 3,020 · see citing works
Interactions between the microbiota, immune and nervous systems in health and disease
Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4476 · Cited by 1,900 · see citing works
Cox, L. M., Yamanishi, S., Sohn, J., Alekseyenko, A. V., Leung, J. M., Cho, I., Kim, S. G., Li, H., Gao, Z., Mahana, D., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.052 · Cited by 1,859 · see citing works
The ageing systemic milieu negatively regulates neurogenesis and cognitive function
Villeda, S. A., Luo, J., Mosher, K. I., Zou, B., Britschgi, M., Bieri, G., Stan, T. M., Fainberg, N., Ding, Z., Eggel, A., et al. (2011) · Nature · doi:10.1038/nature10357 · Cited by 1,763 · see citing works
A polarizing question: do M1 and M2 microglia exist?
Ransohoff, R. M. (2016) · Nature Neuroscience · doi:10.1038/nn.4338 · Cited by 1,573 · see citing works
Cattaneo, A., Cattane, N., Galluzzi, S., Provasi, S., Lopizzo, N., Festari, C., Ferrari, C., Guerra, U. P., Paghera, B., Muscio, C., et al. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.08.019 · Cited by 1,382 · see citing works
The composition of the gut microbiota throughout life, with an emphasis on early life
Rodríguez, J. M., Murphy, K., Stanton, C., Ross, R. P., Kober, O. I., Juge, N., Avershina, E., Rudi, K., Narbad, A., Jenmalm, M. C., et al. (2015) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v26.26050 · Cited by 1,320 · see citing works
A three-dimensional human neural cell culture model of Alzheimer’s disease
Choi, S. H., Kim, Y. H., Hebisch, M., Sliwinski, C., Lee, S., D’Avanzo, C., Chen, H., Hooli, B., Asselin, C., Muffat, J., et al. (2014) · Nature · doi:10.1038/nature13800 · Cited by 1,195 · see citing works
Self-citationRevealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data
Vital, M., Howe, A. C., & Tiedje, J. M. (2014) · mBio · doi:10.1128/mbio.00889-14 · Cited by 1,189 · see citing works
Commensal microbiota affects ischemic stroke outcome by regulating intestinal γδ T cells
Benakis, C., Brea, D., Caballero, S., Faraco, G., Moore, J., Murphy, M., Sita, G., Racchumi, G., Ling, L., Pamer, E. G., et al. (2016) · Nature Medicine · doi:10.1038/nm.4068 · Cited by 1,114 · see citing works
In-vivo measurement of activated microglia in dementia
Cagnin, A., Brooks, D. J., Kennedy, A. M., Gunn, R. N., Myers, R., Turkheimer, F. E., Jones, T., & Banati, R. B. (2001) · The Lancet · doi:10.1016/s0140-6736(01)05625-2 · Cited by 1,054 · see citing works
Alzheimer’s Disease Risk Gene CD33 Inhibits Microglial Uptake of Amyloid Beta
Griciuc, A., Serrano-Pozo, A., Parrado, A. R., Lesinski, A. N., Asselin, C. N., Mullin, K., Hooli, B., Choi, S. H., Hyman, B. T., & Tanzi, R. E. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.014 · Cited by 1,004 · see citing works
Self-citationLangdon, A. E., Crook, N., & Dantas, G. A. (2016) · Genome Medicine · doi:10.1186/s13073-016-0294-z · Cited by 917 · see citing works
Leone, V., Gibbons, S. M., Martinez, K., Hutchison, A. L., Huang, E. Y., Cham, C. M., Pierre, J. F., Heneghan, A. F., Nadimpalli, A., Hubert, N., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.03.006 · Cited by 908 · see citing works
Self-citationReduction of Abeta amyloid pathology in APPPS1 transgenic mice in the absence of gut microbiota
Harach, T., Marungruang, N., Duthilleul, N., Cheatham, V., Mc Coy, K. D., Frisoni, G., Neher, J. J., Fåk, F., Jucker, M., Lasser, T., et al. (2017) · Scientific Reports · doi:10.1038/srep41802 · Cited by 901 · see citing works
Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Physiology · doi:10.1113/jp273106 · Cited by 813 · see citing works
RAFF, M. C., Fields, K. L., Hakomori, S., Mirsky, R., Pruss, R. M., & Winter, J. (1979) · Brain Research · doi:10.1016/0006-8993(79)90851-5 · Cited by 800 · see citing works
Commensal bacteria protect against food allergen sensitization
Stefka, A. T., Feehley, T., Tripathi, P., Qiu, J., McCoy, K. D., Mazmanian, S. K., Tjota, M. Y., Seo, G., Cao, S. Z., Theriault, B. R., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1412008111 · Cited by 795 · see citing works
Self-citationMining the Human Gut Microbiota for Immunomodulatory Organisms
Geva-Zatorsky, N., Sefik, E., Kua, L., Pasman, L., Tan, T. G., Ortiz-Lopez, A., Yanortsang, T. B., Yang, L., Jupp, R., Mathis, D., et al. (2017) · Cell · doi:10.1016/j.cell.2017.01.022 · Cited by 762 · see citing works
The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms
Engelhardt, B., & Ransohoff, R. M. (2005) · Trends in Immunology · doi:10.1016/j.it.2005.07.004 · Cited by 676 · see citing works
Ormerod, K. L., Wood, D., Lachner, N., Gellatly, S. L., Daly, J. N., Parsons, J. D., Dal’Molin, C. G. D. O., Palfreyman, R. W., Nielsen, L. K., Cooper, M. A., et al. (2016) · Microbiome · doi:10.1186/s40168-016-0181-2 · Cited by 675 · see citing works
The role of peripheral immune cells in the CNS in steady state and disease
Prinz, M., & Priller, J. (2017) · Nature Neuroscience · doi:10.1038/nn.4475 · Cited by 657 · see citing works
Minter, M. R., Zhang, C., Leone, V., Ringus, D. L., Zhang, X., Oyler-Castrillo, P., Musch, M. W., Liao, F., Ward, J. F., Holtzman, D. M., et al. (2016) · Scientific Reports · doi:10.1038/srep30028 · Cited by 655 · see citing works
Self-citationJohnson‐Wood, K., Lee, M., Motter, R. N., Hu, K., Gordon, G., Barbour, R., Khan, K., Gordon, M. N., Tan, H. T., Games, D., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.4.1550 · Cited by 634 · see citing works
Wang, Y., Hoenig, J. D., Malin, K. J., Qamar, S., Petrof, E. O., Sun, J., Antonopoulos, D. A., Chang, E. B., & Claud, E. C. (2009) · The ISME Journal · doi:10.1038/ismej.2009.37 · Cited by 598 · see citing works
Self-citationGury-BenAri, M., Thaiss, C. A., Serafini, N., Winter, D. R., Giladi, A., Lara-Astiaso, D., Levy, M., Salame, T. M., Weiner, A., David, E., et al. (2016) · Cell · doi:10.1016/j.cell.2016.07.043 · Cited by 587 · see citing works
Regulatory T cells promote myelin regeneration in the central nervous system
Dombrowski, Y., O'Hagan, T., Dittmer, M., Penalva, R., Mayoral, S. R., Bankhead, P., Fleville, S., Eleftheriadis, G., Zhao, C., Naughton, M., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4528 · Cited by 533 · see citing works
Inconsistencies and Controversies Surrounding the Amyloid Hypothesis of Alzheimer's Disease
Morris, G. P., Clark, I. A., & Vissel, B. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0135-5 · Cited by 522 · see citing works
Innate lymphoid cells in the initiation, regulation and resolution of inflammation
Sonnenberg, G. F., & Artis, D. (2015) · Nature Medicine · doi:10.1038/nm.3892 · Cited by 503 · see citing works
Baruch, K., Rosenzweig, N., Kertser, A., Deczkowska, A., Sharif, A. M., Spinrad, A., Tsitsou-Kampeli, A., Sarel, A., Cahalon, L., & Schwartz, M. (2015) · Nature Communications · doi:10.1038/ncomms8967 · Cited by 491 · see citing works
The contribution of neuroinflammation to amyloid toxicity in Alzheimer's disease
Minter, M. R., Taylor, J. M., & Crack, P. J. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13411 · Cited by 451 · see citing works
Self-citationBrosseron, F., Krauthausen, M., Kummer, M., & Heneka, M. T. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8657-1 · Cited by 447 · see citing works
Baruch, K., Deczkowska, A., Rosenzweig, N., Tsitsou-Kampeli, A., Sharif, A. M., Matcovitch-Natan, O., Kertser, A., David, E., Amit, I., & Schwartz, M. (2016) · Nature Medicine · doi:10.1038/nm.4022 · Cited by 425 · see citing works
Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment
Nobel, Y. R., Cox, L. M., Kirigin, F. F., Bokulich, N. A., Yamanishi, S., Teitler, I., Chung, J., Sohn, J., Barber, C. M., Goldfarb, D. S., et al. (2015) · Nature Communications · doi:10.1038/ncomms8486 · Cited by 377 · see citing works
Iba1 Is an Actin-Cross-Linking Protein in Macrophages/Microglia
Sasaki, Y., Ohsawa, K., Kanazawa, H., Kohsaka, S., & Imai, Y. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5388 · Cited by 373 · see citing works
Regulatory T cells delay disease progression in Alzheimer-like pathology
Dansokho, C., Ahmed, D. A., Aïd, S., Toly‐Ndour, C., Chaigneau, T., Calle, V., Cagnard, N., Holzenberger, M., Piaggio, E., Aucouturier, P., et al. (2016) · Brain · doi:10.1093/brain/awv408 · Cited by 359 · see citing works
Patterns of Early Gut Colonization Shape Future Immune Responses of the Host
Hansen, C. H. F., Nielsen, D. S., Kverka, M., Zakostelska, Z. J., Kostovcikova, K., Hudcovic, T., Tlaskalová‐Hogenová, H., & Hansen, A. K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034043 · Cited by 310 · see citing works
Laurent, C., Dorothée, G., Hunot, S., Martin, E., Monnet, Y., Duchamp, M., Dong, Y., Légeron, F.-P., Leboucher, A., Burnouf, S., et al. (2016) · Brain · doi:10.1093/brain/aww270 · Cited by 299 · see citing works
Clearance of cerebral Aβ in Alzheimer’s disease: reassessing the role of microglia and monocytes
Zuroff, L. R., Daley, D. A., Black, K. L., & Koronyo‐Hamaoui, M. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2463-7 · Cited by 275 · see citing works
A Technique for Serial Collection of Cerebrospinal Fluid from the Cisterna Magna in Mouse
Liu, L., & Duff, K. (2008) · Journal of Visualized Experiments · doi:10.3791/960 · Cited by 268 · see citing works
Kipnis, J., Mizrahi, T., Hauben, E., Shaked, I., Shevach, E. M., & Schwartz, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.232565399 · Cited by 265 · see citing works
Stem cell factor stimulates neurogenesis in vitro and in vivo
Jin, K., Mao, X. O., Sun, Y., Xie, L., & Greenberg, D. A. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15251 · Cited by 263 · see citing works
Ahmed, Z., Shaw, G., Sharma, V. P., Yang, C., McGowan, E., & Dickson, D. W. (2007) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.6a7156.2007 · Cited by 258 · see citing works
Isolation of murine microglial cells for RNA analysis or flow cytometry
Cardona, A. E., Huang, D., Sasse, M. E., & Ransohoff, R. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.327 · Cited by 236 · see citing works
Zhang, X., Tian, Y., Zhang, C. M., Tian, X., Ross, A., Moir, R. D., Sun, H., Tanzi, R. E., Moore, A. V., & Ran, C. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1505420112 · Cited by 227 · see citing works
Self-citationWang, D., Ho, L., Faith, J. J., Ono, K., Janle, E. M., Lachcik, P. J., Cooper, B. R., Jannasch, A., D’Arcy, B., Williams, B. A., et al. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400544 · Cited by 227 · see citing works
Dissection of Hippocampal Dentate Gyrus from Adult Mouse
Hagihara, H., Toyama, K., Yamasaki, N., & Miyakawa, T. (2009) · Journal of Visualized Experiments · doi:10.3791/1543 · Cited by 203 · see citing works
Stem cell factor stimulates neurogenesis in vitro and in vivo
Jin, K., Mao, X. O., Sun, Y., Xie, L., & Greenberg, D. A. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0215251 · Cited by 200 · see citing works
Naj, A. C., Jun, G., Reitz, C., Kunkle, B. W., Perry, W., Park, Y. S., Beecham, G. W., Rajbhandary, R. A., Hamilton-Nelson, K. L., Wang, L.-S., et al. (2014) · JAMA Neurology · doi:10.1001/jamaneurol.2014.1491 · Cited by 185 · see citing works
Self-citationNeuroprotective effects of CD4+CD25+Foxp3+ regulatory T cells in a 3xTg-AD Alzheimer's disease model
Baek, H., Ye, M., Kang, G., Lee, C., Lee, G., Choi, D. B., Jung, J., Kim, H., Lee, S., Kim, J. S., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.12469 · Cited by 168 · see citing works
Gut microbiota: a potential regulator of neurodevelopment
Tognini, P. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00025 · Cited by 163 · see citing works
CNS Repair Requires Both Effector and Regulatory T Cells with Distinct Temporal and Spatial Profiles
Rapôso, C., Graubardt, N., Cohen, M., Eitan, C., London, A., Berkutzki, T., & Schwartz, M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0076-14.2014 · Cited by 161 · see citing works
Yasuno, F., Kosaka, J., Ota, M., Higuchi, M., Ito, H., Fujimura, Y., Nozaki, S., Takahashi, S., Mizukami, K., Asada, T., et al. (2012) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2011.08.013 · Cited by 148 · see citing works
Type-1 interferon signaling mediates neuro-inflammatory events in models of Alzheimer’s disease
Taylor, J. M., Minter, M. R., Newman, A. G., Zhang, M., Adlard, P. A., & Crack, P. J. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.10.089 · Cited by 145 · see citing works
Self-citationType I/II Interferon Balance in the Regulation of Brain Physiology and Pathology
Deczkowska, A., Baruch, K., & Schwartz, M. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.01.006 · Cited by 125 · see citing works
Erickson, M. A., Morofuji, Y., Owen, J. B., & Banks, W. A. (2014) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.114.213074 · Cited by 110 · see citing works
Study of interleukin-6 production in Alzheimer's disease.
Cojocaru, I. M., Cojocaru, M., Miu, G., & Sapira, V. (2011) · PubMed · Cited by 96 · see citing works
Mode of Delivery Shapes Gut Colonization Pattern and Modulates Regulatory Immunity in Mice
Hansen, C. H. F., Andersen, L. S. F., Krych, Ł., Metzdorff, S. B., Hasselby, J. P., Skov, S., Nielsen, D. S., Buschard, K., Hansen, L. H., & Hansen, A. K. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400085 · Cited by 91 · see citing works
Meisel, M., Mayassi, T., Fehlner-Peach, H., Koval, J., O'Brien, S. L., Hinterleitner, R., Lesko, K., Kim, S. M., Bouziat, R., Chen, L., et al. (2016) · The ISME Journal · doi:10.1038/ismej.2016.114 · Cited by 91 · see citing works
Self-citationKim, Y. S., Lee, K. J., & Kim, H. (2017) · Psychogeriatrics · doi:10.1111/psyg.12218 · Cited by 90 · see citing works
Brain Repair by Hematopoietic Growth Factors in a Rat Model of Stroke
Zhao, L.-R., Singhal, S., Duan, W.-M., Mehta, J., & Kessler, J. A. (2007) · Stroke · doi:10.1161/strokeaha.106.476457 · Cited by 89 · see citing works
Regulatory T Cells in Central Nervous System Injury: A Double-Edged Sword
Walsh, J. T., Zheng, J., Smirnov, I., Lorenz, U. M., Tung, K. S. K., & Kipnis, J. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302401 · Cited by 88 · see citing works
van Rossum, D., Hilbert, S., Straßenburg, S., Hanisch, U., & Brück, W. (2007) · Glia · doi:10.1002/glia.20611 · Cited by 79 · see citing works
Beneficial Effects of Hematopoietic Growth Factor Therapy in Chronic Ischemic Stroke in Rats
Zhao, L., Berra, H. H., Duan, W., Singhal, S., Mehta, J., Apkarian, A. V., & Kessler, J. A. (2007) · Stroke · doi:10.1161/strokeaha.107.486217 · Cited by 79 · see citing works
Minter, M. R., Moore, Z., Zhang, M., Brody, K. M., Jones, N. C., Shultz, S. R., Taylor, J. M., & Crack, P. J. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0341-4 · Cited by 79 · see citing works
Self-citationLalli, M. A., Bettcher, B. M., Arcila, M. L., Garcia, G., Guzman, C., Madrigal, L., Ramirez, L., Acosta-Uribe, J., Baena, A., Wojta, K. J., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.131 · Cited by 73 · see citing works
Microbial Immuno-Communication in Neurodegenerative Diseases
Main, B. S., & Minter, M. R. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00151 · Cited by 68 · see citing works
Self-citationWagner, S. L., Zhang, C. M., Cheng, S., Nguyen, P. A. H., Zhang, X., Rynearson, K. D., Wang, R., Li, Y., Sisodia, S. S., Mobley, W. C., et al. (2014) · Biochemistry · doi:10.1021/bi401537v · Cited by 50 · see citing works
Self-citationLinking T cells to Alzheimer's disease: from neurodegeneration to neurorepair
Bryson, K. J., & Lynch, M. A. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2015.10.003 · Cited by 33 · see citing works
Hansen, C. H. F., Metzdorff, S. B., & Hansen, A. K. (2013) · Gut Microbes · doi:10.4161/gmic.23999 · Cited by 33 · see citing works
Romanian journal of internal medicine = Revue roumaine de médecine interne
Lupu, I. D. M. I. N. G., & Medicale, A. D. Ș. (1991) · Editura Academiei Române eBooks · Cited by 29 · see citing works
Li, B., Gonzalez-Toledo, M. E., Piao, C.-S., Gu, A., Kelley, R. E., & Zhao, L.-R. (2011) · Alzheimer s Research & Therapy · doi:10.1186/alzrt67 · Cited by 26 · see citing works
Laske, C., Sopova, K., Hoffmann, N. A., Stransky, E., Hagen, K., Fallgatter, A. J., Stellos, K., & Leyhe, T. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-110008 · Cited by 6 · see citing works
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Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
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Cryan, J. F., O'Riordan, K. J., Sandhu, K., Peterson, V., & Dinan, T. G. (2020) · The Lancet Neurology · doi:10.1016/s1474-4422(19)30356-4 · Cited by 1,336 · see citing works
MahmoudianDehkordi, S., Arnold, M., Nho, K., Ahmad, S., Jia, W., Xie, G., Louie, G., Kueider‐Paisley, A., Moseley, M. A., Thompson, J. W., et al. (2019) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2018.07.217 · Cited by 706 · see citing works
Sun, J., Xu, J., Ling, Y., Wang, F., Gong, T., Yang, C., Ye, S., Ye, K., Wei, D., Song, Z., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0525-3 · Cited by 532 · see citing works
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Xu, Y., Wang, N., Tan, H.-Y., Li, S., Zhang, C., & Feng, Y. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00219 · Cited by 420 · see citing works
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Colombo, A. V., Sadler, R. K., Llovera, G., Singh, V., Roth, S., Heindl, S., Sebastian Monasor, L., Verhoeven, A., Peters, F., Parhizkar, S., et al. (2021) · eLife · doi:10.7554/elife.59826 · Cited by 354 · see citing works
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Dodiya, H. B., Kuntz, T., Shaik, S. M., Baufeld, C., Leibowitz, J., Zhang, X., Gottel, N., Zhang, X., Butovsky, O., Gilbert, J. A., et al. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20182386 · Cited by 288 · see citing works
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Li, H., Liu, C.-C., Zheng, H., & Huang, T. Y. (2018) · Translational Neurodegeneration · doi:10.1186/s40035-018-0139-3 · Cited by 103 · see citing works
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Ticinesi, A., Tana, C., & Nouvenne, A. (2019) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000521 · Cited by 80 · see citing works
Bosch, M. E., Dodiya, H. B., Michalkiewicz, J., Lee, C., Shaik, S. M., Weigle, I. Q., Zhang, C., Osborn, J., Nambiar, A., Patel, P., et al. (2024) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00700-w · Cited by 70 · see citing works
Self-citationChandra, S., Di Meco, A., Dodiya, H. B., Popovic, J., Cuddy, L. K., Weigle, I. Q., Zhang, X., Sadleir, K., Sisodia, S. S., & Vassar, R. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00635-2 · Cited by 58 · see citing works
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Seo, D.-O., Boros, B. D., & Holtzman, D. M. (2019) · Cell Research · doi:10.1038/s41422-019-0227-7 · Cited by 56 · see citing works
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Cox, L. M., Calcagno, N., Gauthier, C., Madore, C., Butovsky, O., & Weiner, H. L. (2022) · Microbiome · doi:10.1186/s40168-022-01232-z · Cited by 53 · see citing works
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Cook, J., & Prinz, M. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2125739 · Cited by 49 · see citing works
Stanisavljević, S., Čepić, A., Bojić, S., Veljović, K., Mihajlović, S., Đedović, N., Jevtić, B., Momčilović, M., Lazarević, M., Mostarica Stojković, M., et al. (2019) · Scientific Reports · doi:10.1038/s41598-018-37505-7 · Cited by 43 · see citing works
Association of midlife antibiotic use with subsequent cognitive function in women
Mehta, R. S., Lochhead, P., Wang, Y., Ma, W., Nguyen, L. H., Kochar, B., Huttenhower, C., Grodstein, F., & Chan, A. T. (2022) · PLoS ONE · doi:10.1371/journal.pone.0264649 · Cited by 26 · see citing works
Wei, J., Liu, C., Qin, D., Ren, F., Duan, J., Chen, T., & Wu, A. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102544 · Cited by 15 · see citing works
A reappraisal on amyloid cascade hypothesis: The role of chronic infection in Alzheimer’s disease
Phuna, Z. X., & Madhavan, P. (2023) · International Journal of Neuroscience · doi:10.1080/00207454.2022.2045290 · Cited by 12 · see citing works
- Authors
- Minter, M. R., Hinterleitner, R., Meisel, M., Zhang, C., Leone, V., Zhang, X., Oyler-Castrillo, P., Zhang, X., Musch, M. W., Shen, X., Jabri, B., Chang, E. B., Tanzi, R. E., & Sisodia, S. S.
- Affiliations
- University of Chicago (US)
- Massachusetts General Hospital (US)
- Corresponding author
- Sisodia, Sangram S.
- ORCID
- Venue
- Scientific Reports
- Published
- 2017-09-05
- Volume
- 7
- Issue
- 1
- Pages
- 10411-10411
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC5585265
- OpenAlex
- W2753802402
- Cited by
- 292
- References
- 86
- Citations by year
- 2026: 12 · 2025: 31 · 2024: 45 · 2023: 40 · 2022: 44 · 2021: 41 · 2020: 32 · 2019: 27 · 2018: 20
- FWCI
- 15.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Cure Alzheimer's Fund
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK042086)
- Argonne National Laboratory
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Alzheimer's disease, gut microbiota, antibiotic exposure, postnatal development, amyloid plaques, APPswe/PS1ΔE9 mice, Lachnospiraceae, S24-7, regulatory T cells, Foxp3, neuroinflammation, cerebrospinal fluid, microglia, astrocytes, gliosis, microbiota-host interactions, brain development
- MeSH terms
- Gastrointestinal Microbiome, Alzheimer Disease, Amyloidosis, Animals, Anti-Bacterial Agents, Brain, Disease Models, Animal, Male, Mice, Transgenic, RNA, Ribosomal, 16S, Neuroimmunomodulation, Biomarkers, Amyloid beta-Protein Precursor, Inflammation Mediators, Biodiversity, Mice, Metagenome, Metagenomics, Plaque, Amyloid, Microbiota
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