Publications

2024

Rosenzweig N, Kleemann KL, Rust T, Carpenter M, Grucci M, Aronchik M, Brouwer N, Valenbreder I, Cooper-Hohn J, Iyer M, Krishnan RK, Sivanathan KN, Brandão W, Yahya T, Durao A, Yin Z, Chadarevian JP, Properzi MJ, Nowarski R, Davtyan H, Weiner HL, Blurton-Jones M, Yang HS, Eggen BJL, Sperling RA, Butovsky O. “Sex-dependent APOE4 neutrophil-microglia interactions drive cognitive impairment in Alzheimer’s disease.” Nat Med. Oct 2024. DOI: 10.1038/s41591-024-03122-3

Kaiser T, Dattero J, Li L, Chen M, Jiang M, Harrahill A, Butovsky O, Feng G. “Transgenic Targeting of Fcrls Creates a Highly Efficient Constitutively Active Microglia Cre Line with Differentiated Specificity.” eNeuro. Jul 2024. DOI: 10.1523/ENEURO.0549-23.2024

Wasén C, Beauchamp LC, Vincentini J, Li S, LeServe DS, Gauthier C, Lopes JR, Moreira TG, Ekwudo MN, Yin Z, da Silva P, Krishnan RK, Butovsky O, Cox LM, Weiner HL. “Bacteroidota inhibit microglia clearance of amyloid-beta and promote plaque deposition in Alzheimer’s disease mouse models.” Nat Commun. May 2024. DOI: 10.1038/s41467-024-47683-w

Bosch ME, Dodiya HB, Michalkiewicz J, Lee C, Shaik SM, Weigle IQ, Zhang C, Osborn J, Nambiar A, Patel P, Parhizkar S, Zhang X, Laury ML, Mondal P, Gomm A, Schipma MJ, Mallah D, Butovsky O, Chang EB, Tanzi RE, Gilbert JA, Holtzman DM, Sisodia SS. “Sodium oligomannate alters gut microbiota, reduces cerebral amyloidosis and reactive microglia in a sex-specific manner.” Mol Neurodegener. Feb 2024. DOI: 10.1186/s13024-024-00764-2

2023

Yin Z, Rosenzweig N, Kleemann KL, Zhang X, Brandão W, Margeta MA, Schroeder C, Sivanathan KN, Silveira S, Gauthier C, Mallah D, Pitts KM, Durao A, Herron S, Shorey H, Cheng Y, Barry JL, Krishnan RK, Wakelin S, Rhee J, Yung A, Aronchik M, Wang C, Jain N, Bao X, Gerrits E, Brouwer N, Deik A, Tenen DG, Ikezu T, Santander NG, McKinsey GL, Baufeld C, Sheppard D, Krasemann S, Nowarski R, Eggen BJL, Clish C, Tanzi RE, Madore C, Arnold TD, Holtzman DM, Butovsky O. “APOE4 impairs the microglial response in Alzheimer’s disease by inducing TGFβ-mediated checkpoints.” Nat Immunol. Nov 2023. DOI: 10.1038/s41590-023-01627-6

McKinsey GL, Santander N, Zhang X, Kleemann K, Tran L, Katewa A, Conant K, Barraza M, Waddell K, Lizama C, La Russa M, Koo HJ, Lee H, Mukherjee D, Paidassi H, Anton ES, Atabai K, Sheppard D, Butovsky O, Arnold TD. “Radial glia promote microglial development through integrin αVβ8 -TGFβ1 signaling.” bioRxiv [Preprint]. Sep 2023. DOI: 10.1101/2023.07.13.548459

Abou-El-Hassan H, Rezende RM, Izzy S, Gabriely G, Yahya T, Tatematsu BK, Habashy KJ, Lopes JR, de Oliveira GLV, Maghzi AH, Yin Z, Cox LM, Krishnan R, Butovsky O, Weiner HL. “Vγ1 and Vγ4 gamma-delta T cells play opposing roles in the immunopathology of traumatic brain injury in males.” Nat Commun. Jul 2023. DOI: 10.1038/s41467-023-39857-9

Yin Z, Herron S, Silveira S, Kleemann K, Gauthier C, Mallah D, Cheng Y, Margeta MA, Pitts KM, Barry J-L, Subramanian A, Shorey H, Brandao W, Durao A, Delpech J-C, Madore C, Jedrychowski M, Ajay AK, Murugaiyan G, Hersh SW, Ikezu S, Ikezu T, Butovsky O. “Identification of a protective microglial state mediated by miR-155 and interferon-γ signaling in a mouse model of Alzheimer’s disease.” Nat Neurosci. Jul 2023. DOI: 1038/s41593-023-01355-y

Guneykaya D, Ugursu B, Logiacco F, Popp O, Feiks MA, Meyer N, Wendt S, Semtner M, Cherif F, Gauthier C, Madore C, Yin Z, Çınar Ö, Arslan T, Gerevich Z, Mertins P, Butovsky O, Kettenmann H, Wolf SA. “Sex-specific microglia state in the Neuroligin-4 knock-out mouse model of autism spectrum disorder.” Brain Behav Immun. Mar 2023. DOI: 1016/j.bbi.2023.03.023

2022

Paolicelli RC, Sierra A, Stevens B, Tremblay ME, Aguzzi A, Ajami B, Amit I, Audinat E, Bechmann I, Bennett M, Bennett F, Bessis A, Biber K, Bilbo S, Blurton-Jones M, Boddeke E, Brites D, Brône B, Brown GC, Butovsky O, Carson MJ, Castellano B, Colonna M, Cowley SA, Cunningham C, Davalos D, De Jager PL, de Strooper B, Denes A, Eggen BJL, Eyo U, Galea E, Garel S, Ginhoux F, Glass CK, Gokce O, Gomez-Nicola D, González B, Gordon S, Graeber MB, Greenhalgh AD, Gressens P, Greter M, Gutmann DH, Haass C, Heneka MT, Heppner FL, Hong S, Hume DA, Jung S, Kettenmann H, Kipnis J, Koyama R, Lemke G, Lynch M, Majewska A, Malcangio M, Malm T, Mancuso R, Masuda T, Matteoli M, McColl BW, Miron VE, Molofsky AV, Monje M, Mracsko E, Nadjar A, Neher JJ, Neniskyte U, Neumann H, Noda M, Peng B, Peri F, Perry VH, Popovich PG, Pridans C, Priller J, Prinz M, Ragozzino D, Ransohoff RM, Salter MW, Schaefer A, Schafer DP, Schwartz M, Simons M, Smith CJ, Streit WJ, Tay TL, Tsai LH, Verkhratsky A, von Bernhardi R, Wake H, Wittamer V, Wolf SA, Wu LJ, Wyss-Coray T. “Microglia states and nomenclature: A field at its crossroads.” Neuron. 2022 Nov 2;110(21):3458-3483. DOI: 1016/j.neuron.2022.10.020

Cappelli S, Spalloni A, Feiguin F, Visani G, Šušnjar U, Brown AL; NYGC ALS Consortium; De Bardi M, Borsellino G, Secrier M, Phatnani H, Romano M, Fratta P, Longone P, Buratti E. “NOS1AP is a novel molecular target and critical factor in TDP-43 pathology.” Brain Commun. 2022 Sep 23;4(5):fcac242. DOI: 1093/braincomms/fcac242

Shi H, Yin Z, Koronyo Y, Fuchs DT, Sheyn J, Davis MR, Wilson JW, Margeta MA, Pitts KM, Herron S, Ikezu S, Ikezu T, Graham SL, Gupta VK, Black KL, Mirzaei M, Butovsky O, Koronyo-Hamaoui M. “Regulating microglial miR-155 transcriptional phenotype alleviates Alzheimer’s-induced retinal vasculopathy by limiting Clec7a/Galectin-3(+) neurodegenerative microglia.” Acta Neuropathol Commun. 2022 Sep 8;10(1):136. DOI: 1186/s40478-022-01439-z

Margeta MA, Yin Z, Madore C, Pitts KM, Letcher SM, Tang J, Jiang S, Gauthier CD, Silveira SR, Schroeder CM, Lad EM, Proia AD, Tanzi RE, Holtzman DM, Krasemann S, Chen DF, Butovsky O. “Apolipoprotein E4 impairs the response of neurodegenerative retinal microglia and prevents neuronal loss in glaucoma.” Immunity. 2022 Sep 13;55(9):1627-1644.e7. DOI: 1016/j.immuni.2022.07.014

West PK, McCorkindale AN, Guennewig B, Ashhurst TM, Viengkhou B, Hayashida E, Jung SR, Butovsky O, Campbell IL, Hofer MJ. “The cytokines interleukin-6 and interferon-α induce distinct microglia phenotypes.” J Neuroinflammation. 2022 Apr 16;19(1):96. DOI: 1186/s12974-022-02441-x

Šušnjar U, Škrabar N, Brown AL, Abbassi Y, Phatnani H; NYGC ALS Consortium; Cortese A, Cereda C, Bugiardini E, Cardani R, Meola G, Ripolone M, Moggio M, Romano M, Secrier M, Fratta P, Buratti E. “Cell environment shapes TDP-43 function with implications in neuronal and muscle disease.” Commun Biol. 2022 Apr 5;5(1):314. DOI: 1038/s42003-022-03253-8

Cox LM, Calcagno N, Gauthier C, Madore C, Butovsky O, Weiner HL. “The microbiota restrains neurodegenerative microglia in a model of amyotrophic lateral sclerosis.” Microbiome. 2022 Mar 11;10(1):47. DOI: 1186/s40168-022-01232-z

Brown AL, Wilkins OG, Keuss MJ, Hill SE, Zanovello M, Lee WC, Bampton A, Lee FCY, Masino L, Qi YA, Bryce-Smith S, Gatt A, Hallegger M, Fagegaltier D, Phatnani H; NYGC ALS Consortium; Newcombe J, Gustavsson EK, Seddighi S, Reyes JF, Coon SL, Ramos D, Schiavo G, Fisher EMC, Raj T, Secrier M, Lashley T, Ule J, Buratti E, Humphrey J, Ward ME, Fratta P. “TDP-43 loss and ALS-risk SNPs drive mis-splicing and depletion of UNC13A.” Nature. 2022 Mar;603(7899):131-137. DOI: 1038/s41586-022-04436-3 (Epub 2022 Feb 23)

Fiore NT, Yin Z, Guneykaya D, Gauthier CD, Hayes JP, D’Hary A, Butovsky O, Moalem-Taylor G. “Sex-specific transcriptome of spinal microglia in neuropathic pain due to peripheral nerve injury.” Glia. 2022 Apr;70(4):675-696. DOI: 1002/glia.24133 (Epub 2022 Jan 20)

2021

NeuroLINCS Consortium; Li J, Lim RG, Kaye JA, Dardov V, Coyne AN, Wu J, Milani P, Cheng A, Thompson TG, Ornelas L, Frank A, Adam M, Banuelos MG, Casale M, Cox V, Escalante-Chong R, Daigle JG, Gomez E, Hayes L, Holewenski R, Lei S, Lenail A, Lima L, Mandefro B, Matlock A, Panther L, Patel-Murray NL, Pham J, Ramamoorthy D, Sachs K, Shelley B, Stocksdale J, Trost H, Wilhelm M, Venkatraman V, Wassie BT, Wyman S, Yang S; NYGC ALS Consortium; Van Eyk JE, Lloyd TE, Finkbeiner S, Fraenkel E, Rothstein JD, Sareen D, Svendsen CN, Thompson LM. “An integrated multi-omic analysis of iPSC-derived motor neurons from C9ORF72 ALS patients.” iScience. 2021 Oct 12;24(11):103221. DOI: 1016/j.isci.2021.103221

Moreira TG, Mangani D, Cox LM, Leibowitz J, Lobo ELC, Oliveira MA, Gauthier CD, Nakagaki BN, Willocq V, Song A, Guo L, Lima DCA, Murugaiyan G, Butovsky O, Gabriely G, Anderson AC, Rezende RM, Faria AMC, Weiner HL. “PD-L1(+) and XCR1(+) dendritic cells are region-specific regulators of gut homeostasis.” Nat Commun. 2021 Aug 13;12(1):4907. DOI: 1038/s41467-021-25115-3

Wang C, Xiong M, Gratuze M, Bao X, Shi Y, Andhey PS, Manis M, Schroeder C, Yin Z, Madore C, Butovsky O, Artyomov M, Ulrich JD, Holtzman DM. “Selective removal of astrocytic APOE4 strongly protects against tau-mediated neurodegeneration and decreases synaptic phagocytosis by microglia.” Neuron. 2021 May 19;109(10):1657-1674.e7. DOI: 1016/j.neuron.2021.03.024

Zrzavy T, Schwaiger C, Wimmer I, Berger T, Bauer J, Butovsky O, Schwab JM, Lassmann H, Höftberger R. “Acute and non-resolving inflammation associate with oxidative injury after human spinal cord injury.” Brain. 2021 Feb 12;144(1):144-161. DOI: 1093/brain/awaa360

Dewan R, Chia R, Ding J, Hickman RA, Stein TD, Abramzon Y, Ahmed S, Sabir MS, Portley MK, Tucci A, Ibáñez K, Shankaracharya FNU, Keagle P, Rossi G, Caroppo P, Tagliavini F, Waldo ML, Johansson PM, Nilsson CF; American Genome Center (TAGC); FALS Sequencing Consortium; Genomics England Research Consortium; International ALS/FTD Genomics Consortium (iAFGC); International FTD Genetics Consortium (IFGC); International LBD Genomics Consortium (iLBDGC); NYGC ALS Consortium; PROSPECT Consortium; Rowe JB, Benussi L, Binetti G, Ghidoni R, Jabbari E, Viollet C, Glass JD, Singleton AB, Silani V, Ross OA, Ryten M, Torkamani A, Tanaka T, Ferrucci L, Resnick SM, Pickering-Brown S, Brady CB, Kowal N, Hardy JA, Van Deerlin V, Vonsattel JP, Harms MB, Morris HR, Ferrari R, Landers JE, Chiò A, Gibbs JR, Dalgard CL, Scholz SW, Traynor BJ. “Pathogenic Huntingtin Repeat Expansions in Patients with Frontotemporal Dementia and Amyotrophic Lateral Sclerosis.” Neuron. 2021 Feb 3;109(3):448-460.e4. DOI: 1016/j.neuron.2020.11.005

2020

Madore C, Leyrolle Q, Morel L, Rossitto M, Greenhalgh AD, Delpech JC, Martinat M, Bosch-Bouju C, Bourel J, Rani B, Lacabanne C, Thomazeau A, Hopperton KE, Beccari S, Sere A, Aubert A, De Smedt-Peyrusse V, Lecours C, Bisht K, Fourgeaud L, Gregoire S, Bretillon L, Acar N, Grant NJ, Badaut J, Gressens P, Sierra A, Butovsky O, Tremblay ME, Bazinet RP, Joffre C, Nadjar A, Layé S. Essential omega-3 fatty acids tune microglial phagocytosis of synaptic elements in the mouse developing brain. Nat Commun. 2020 Nov 30;11(1):6133. doi: 1038/s41467-020-19861-z.

Hagan N, Kane JL, Grover D, Woodworth L, Madore C, Saleh J, Sancho J, Liu J, Li Y, Proto J, Zelic M, Mahan A, Kothe M, Scholte AA, Fitzgerald M, Gisevius B, Haghikia A, Butovsky O, Ofengeim D. CSF1R signaling is a regulator of pathogenesis in progressive MS. Cell Death Dis. 2020 Oct 23;11(10):904. doi: 1038/s41419-020-03084-7.

Margeta MA, Letcher SM, Igo RP Jr, Cooke Bailey JN, Pasquale LR, Haines JL, Butovsky O, Wiggs JL; NEIGHBORHOOD consortium. Association of APOE With Primary Open-Angle Glaucoma Suggests a Protective Effect for APOE ε4. Invest Ophthalmol Vis Sci. 2020 Jul 1;61(8):3. doi: 1167/iovs.61.8.3.

Kempthorne L, Yoon H, Madore C, Smith S, Wszolek ZK, Rademakers R, Kim J, Butovsky O, Dickson DW. Correction to: Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy. Acta Neuropathol Commun. 2020 Jun 24;8(1):90. doi: 1186/s40478-020-00970-1.

Clarke J, Yaqubi M, Futhey NC, Sedaghat S, Baufeld C, Blain M, Baranzini S, Butovsky O, Antel J, White JH, Healy LM. Vitamin D Regulates MerTK-Dependent Phagocytosis in Human Myeloid Cells. J Immunol. 2020 Jul 15;205(2):398-406. doi: 4049/jimmunol.2000129.

Kempthorne L, Yoon H, Madore C, Smith S, Wszolek ZK, Rademakers R, Kim J, Butovsky O, Dickson DW. Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy. Acta Neuropathol Commun. 2020 May 19;8(1):72. doi: 1186/s40478-020-00947-0.

Ikezu S, Yeh H, Delpech JC, Woodbury ME, Van Enoo AA, Ruan Z, Sivakumaran S, You Y, Holland C, Guillamon-Vivancos T, Yoshii-Kitahara A, Botros MB, Madore C, Chao PH, Desani A, Manimaran S, Kalavai SV, Johnson WE, Butovsky O, Medalla M, Luebke JI, Ikezu T. Inhibition of colony stimulating factor 1 receptor corrects maternal inflammation-induced microglial and synaptic dysfunction and behavioral abnormalities. Mol Psychiatry. 2021 Jun;26(6):1808-1831. doi: 1038/s41380-020-0671-2.

Madore C, Yin Z, Leibowitz J, Butovsky O. Microglia, Lifestyle Stress, and Neurodegeneration. Immunity. 2020 Feb 18;52(2):222-240. doi: 1016/j.immuni.2019.12.003.

Roy ER, Wang B, Wan YW, Chiu G, Cole A, Yin Z, Propson NE, Xu Y, Jankowsky JL, Liu Z, Lee VM, Trojanowski JQ, Ginsberg SD, Butovsky O, Zheng H, Cao W. Type I interferon response drives neuroinflammation and synapse loss in Alzheimer disease. J Clin Invest. 2020 Apr 1;130(4):1912-1930. doi: 1172/JCI133737.

2019

Okunuki Y, Mukai R, Nakao T, Tabor SJ, Butovsky O, Dana R, Ksander BR, Connor KM. Retinal Microglia Initiate Neuroinflammation in Ocular Autoimmunity. Proc Natl Acad Sci U S A. 2019 May 14;116(20):9989-98. doi: 1073/pnas.1820663116.

Zrzavy T, Höftberger R, Berger T, Rauschka H, Butovsky O, Weiner H, Lassmann H. Pro‐Inflammatory Activation of Microglia in the Brain of Patients With Sepsis. Neuropathology and Applied Neurobiology. 2019;45(3):278-90. doi: 1111/nan.12523.

Duffy SS, Keating BA, Perera CJ, Lees JG, Tonkin RS, Makker PGS, Carrive P, Butovsky O, Moalem-Taylor G. Regulatory T Cells and Their Derived Cytokine, Interleukin-35, Reduce Pain in Experimental Autoimmune Encephalomyelitis. Journal of Neuroscience. 2019;39(12):2326-46. doi: 1523/JNEUROSCI.1866-18.2018.

Götzl JK, Brendel M, Werner G, Parhizkar S, Sebastian Monasor L, Kleinberger G, Colombo AV, Deussing M, Wagner M, Winkelmann J, Diehl-Schmid J, Levin J, Fellerer K, Reifschneider A, Bultmann S, Bartenstein P, Rominger A, Tahirovic S, Smith ST, Madore C, Butovsky O, Capell A, Haass C. Opposite Microglial Phenotypes Upon Loss of PGRN or TREM2 Result in Reduced Cerebral Glucose Metabolism. EMBO Mol Med. 2019 Jun;11(6):e9711. doi: 15252/emmm.201809999.

Parhizkar S, Arzberger T, Brendel M, Kleinberger G, Deussing M, Focke C, Nuscher B, Xiong M, Ghasemigharagoz A, Katzmarski N, Krasemann S, Lichtenthaler SF, Müller SA, Colombo A, Monasor LS, Tahirovic S, Herms J, Willem M, Pettkus N, Butovsky O, Bartenstein P, Edbauer D, Rominger A, Ertürk A, Grathwohl SA, NeherJJ, Holtzman DM, Meyer-Luehmann M, Haass C. Loss of TREM2 Function Increases Amyloid Seeding but Reduces Plaque-Associated ApoE. Nature Neuroscience. 2019;22(2):191. doi: 1038/s41593-018-0296-9.

Faustino J, Chip S, Derugin N, Jullienne A, Hamer M, Haddad E, Butovsky O, Obenaus A, Vexler ZS. CX3CR1-CCR2-Dependent Monocyte-Microglial Signaling Modulates Neurovascular Leakage and Acute Injury in a Mouse Model of Childhood Stroke. Journal of Cerebral Blood Flow Metabolism. 2019 Oct;39(10):1919-35. doi: 1177/0271678X19869908.

2018

Katsumoto A, Miranda AS, Butovsky O, Teixeira AL, Ransohoff RM, Lamb BT. Laquinimod Attenuates Inflammation by Modulating Macrophage Functions in Traumatic Brain Injury Mouse Model. J Neuroinflammation. 2018 Jan 30;15(1):26. doi: 1186/s12974-018-1069-6.

Lund H, Pieber M, Parsa R, Han J, Grommisch D, Ewing E, Kular L, Needhamsen M, Espinosa A, Nilsson E, Överby AK, Butovsky O, Jagodic M, Zhang XM, Harris RA. Competitive Repopulation of an Empty Microglial Niche Yields Functionally Distinct Subsets of Microglia-Like Cells. Nat Commun. 2018;9(1):4845. doi: 1038/s41467-018-07296-8.

Rubino SJ, Mayo L, Wimmer I, Siedler V, Brunner F, Hametner S, Madi A, Lanser A, Moreira T, Donnelly D, Cox L, Rezende RM, Butovsky O, Lassmann H, Weiner HL. Acute Microglia Ablation Induces Neurodegeneration in the Somatosensory System. Nat Commun. 2018;9(1):4578. doi: 1038/s41467-018-06898-4.

Zrzavy T, Machado-Santos J, Christine S, Baumgartner C, Weiner HL, Butovsky O, Lassmann H. Dominant Role of Microglial and Macrophage Innate Immune Responses in Human Ischemic Infarcts. Brain Pathol. 2018;28(6):791-805. doi: 1111/bpa.12644.

Butovsky O, Weiner HL. Microglial Signatures and Their Role in Health and Disease. Nat Rev Neurosci. 2018 Oct;19(10):622-35. doi: 1038/s41583-018-0057-5.

Okunuki Y, Mukai R, Pearsall EA, Klokman G, Husain D, Park DH, Korobkina E, Weiner HL, Butovsky O, Ksander BR, Miller JW, Connor KM. Microglia Inhibit Photoreceptor Cell Death and Regulate Immune Cell Infiltration in Response to Retinal Detachment. Proc Natl Acad Sci U S A. 2018 Jul 3;115(27):E6264-E6273. doi: 1073/pnas.1722115115.

Calcagno N, Baufeld C, Madore C, Butovsky O. TREMendous 2 Be Social. Immunity. 2018;48(5):842-3. doi: 1016/j.immuni.2018.04.032.

Lund H, Pieber M, Parsa R, Grommisch D, Ewing E, Kular L, Han J, Zhu K, Nijssen J, Hedlund E, Needhamsen M, Ruhrmann S, Guerreiro-Cacais AO, Berglund R, Forteza MJ, Ketelhuth DFJ, Butovsky O, Jagodic M, Zhang XM, Harris RA. Fatal Demyelinating Disease Is Induced by Monocyte-Derived Macrophages in the Absence of TGF-Β Signaling. Nat Immunol. 2018 May;19(5):1-7. doi: 1038/s41590-018-0108-z.

Baufeld C, O’Loughlin E, Calcagno N, Madore C, Butovsky O. Differential Contribution of Microglia and Monocytes in Neurodegenerative Diseases. J Neural Transm. 2018;125(5):809-26. doi: 1007/s00702-018-1901-0.

O’Loughlin E, Madore C, Lassmann H, Butovsky O. Microglial Phenotypes and Functions in Multiple Sclerosis. Cold Spring Harb Perspect Med. 2018 Feb 1;8(2):a028993. doi: 1101/cshperspect.a028993.

2017

Drokhlyansky E, Göz Aytürk D, Soh TK, Chrenek R, O’Loughlin E, Madore C, Butovsky O, Cepko CL. The Brain Parenchyma Has a Type I Interferon Response That Can Limit Virus Spread. Proc Natl Acad Sci USA. 2017 Jan 3;114(1):E95-E104. doi: 1073/pnas.1617461114.

Makker PG, Duffy SS, Lees JG, Perera CJ, Tonkin RS, Butovsky O, Park SB, Goldstein D, Moalem-Taylor G. Characterisation of Immune and Neuroinflammatory Changes Associated With Chemotherapy-Induced Peripheral Neuropathy. PLoS One. 2017 Jan 26;12(1):e0170814. doi: 1371/journal.pone.0170814.

Mazaheri F, Snaidero N, Kleinberger G, Madore C, Daria A, Werner G, Krasemann S, Capell A, Trümbach D, Wurst W, Brunner B, Bultmann S, Tahirovic S, Kerschensteiner M, Misgeld T, Butovsky O, Haass C. TREM2 Deficiency Impairs Chemotaxis and Microglial Responses to Neuronal Injury. EMBO Rep. 2017 Jul;18(7):1186-1198. doi: 15252/embr.201743922.

Zrzavy T, Hametner S, Wimmer I, Butovsky O, Weiner HL, Lassmann H. Loss of ‘Homeostatic’ Microglia and Patterns of Their Activation in Active Multiple Sclerosis. Brain. 2017 Jul 1;140(7):1900-1913. doi: 1093/brain/awx113.

2016

Bisht K, Sharma KP, Lecours C, Sánchez MG, El Hajj H, Milior G, Olmos-Alonso A, Gómez-Nicola D, Luheshi G, Vallières L, Branchi I, Maggi L, Limatola C, Butovsky O, Tremblay MÈ. Dark Microglia: A New Phenotype Predominantly Associated With Pathological States. Glia. 2016 May;64(5):826-839. doi: 1002/glia.22966.

Delpech JC, Wei L, Hao J, Yu X, Madore C, Butovsky O, Kaffman A. Early Life Stress Perturbs the Maturation of Microglia in the Developing Hippocampus. Brain Behav Immun. 2016 Oct;57:79-93. doi: 1016/j.bbi.2016.03.024.

Muth C, Schröck K, Madore C, Hartmann K, Fanek Z, Butovsky O, Glatzel M, Krasemann S. Activation of Microglia by Retroviral Infection Correlates With Transient Clearance of Prions From the Brain but Does Not Change Incubation Time. Brain Pathol. 2017 Sep;27(5):590-602. doi: 1111/bpa.12477.

2015

Jay TR, Miller CM, Cheng PJ, Graham LC, Bemiller S, Broihier ML, Xu G, Margevicius D, Karlo JC, Sousa GL, Cotleur AC, Butovsky O, Bekris L, Staugaitis SM, Leverenz JB, Pimplikar SW, Landreth GE, Howell GR, Ransohoff RM, Lamb BT. TREM2 Deficiency Eliminates TREM2+ Inflammatory Macrophages and Ameliorates Pathology in Alzheimer’s Disease Mouse Models. J Exp Med. 2015 Mar 9;212(3):287-295. doi: 1084/jem.20142322.

Moore CS, Ase AR, Kinsara A, Rao VT, Michell-Robinson M, Leong SY, Butovsky O, Ludwin SK, Séguéla P, Bar-Or A, Antel JP. P2ry12 expression and Function in Alternatively Activated Human Microglia. Neurol Neuroimmunol Neuroinflamm. 2015 Mar 19;2(2):e80. doi: 1212/NXI.0000000000000080.

Verheijden S, Beckers L, Casazza A, Butovsky O, Mazzone M, Baes M. Identification of a Chronic Non-Neurodegenerative Microglia Activation State in a Mouse Model of Peroxisomal Β-Oxidation Deficiency. Glia. 2015 Sep;63(9):1606-1620. doi: 1002/glia.22849.

Asai H, Ikezu S, Tsunoda S, Medalla M, Luebke J, Haydar T, Wolozin B, Butovsky O, Kügler S, Ikezu T. Depletion of Microglia and Inhibition of Exosome Synthesis Halt Tau Propagation. Nat Neurosci. 2015 Nov;18(11):1584-1593. doi: 1038/nn.4132.

2014

Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, et al. Identification of a Unique TGF-Beta-Dependent Molecular and Functional Signature in Microglia. Nat Neurosci. 2014 Feb;17(1):131-143. doi: 1038/nn.3599.

Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, Wu PM, Doykan CE, Lin J, Cotleur AC, et al. Differential Roles of Microglia and Monocytes in the Inflamed CNS: An EAE Study. J Exp Med. 2014 Jul 28;211(8):1533-1549. doi: 1084/jem.20132477.

Butovsky O, Jedrychowski MP, Cialic R, Krasemann S, Murugaiyan G, Fanek Z, Greco DJ, Wu PM, Doykan CE, Kiner O, et al. Targeting miR-155 Restores Abnormal Microglia and Attenuates Disease in SOD1 Mice. Ann Neurol. 2015 Jan;77(1):75-99. doi: 1002/ana.24304.

2000-2012

Butovsky O, Siddiqui S, Gabriely G, Lanser AJ, Dake B, Murugaiyan G, Doykan CE, Wu PM, Gali RR, Iyer LK, Lawson R, Berry J, Krichevsky AM, Cudkowicz ME, Weiner HL. Modulating Inflammatory Monocytes With a Unique microRNA Gene Signature Ameliorates Murine ALS. J Clin Invest. 2012 Sep 4; 122(9):3063-87. doi: 10.1172/JCI62636

Vaknin I, Kunis G, Miller O, Butovsky O, Bukshpan S, Beers DR, Henkel JS, Yoles E, Appel SH, Schwartz M. Excess Circulating Alternatively Activated Myeloid (M2) Cells Accelerate ALS Progression While Inhibiting Experimental Autoimmune Encephalomyelitis. PLoS One. 2011;6(11):e26921. doi: 1371/journal.pone.0026921.

Landa G, Butovsky O, Shoshani J, Schwartz M, Pollack A. Weekly Vaccination With Copaxone (Glatiramer Acetate) as a Potential Therapy for Dry Age-Related Macular Degeneration. Curr Eye Res. 2008;33(11):1011-1013. doi: 1080/02713680802486769.

Butovsky O, Kunis G, Koronyo-Hamaoui M, Schwartz M. Selective Ablation of Bone Marrow-Derived Dendritic Cells Increases Amyloid Plaques in a Mouse Alzheimer’s Disease Model. Eur J Neurosci. 2007 Jan;26(2):413-416. doi: 1111/j.1460-9568.2007.05684.x.

Butovsky O, Bukshpan S, Kunis G, Jung S, Schwartz M. Microglia Can Be Induced by IFN-Gamma or IL-4 to Express Neural or Dendritic-Like Markers. Mol Cell Neurosci. 2007 Nov;35(3):490-500. doi: 1016/j.mcn.2007.04.006.

Butovsky O, Talpalar AE, Ben-Yaakov K, Schwartz M. Activation of Microglia by Aggregated Beta-Amyloid or Lipopolysaccharide Impairs MHC-II Expression and Renders Them Cytotoxic Whereas IFN-Gamma and IL-4 Render Them Protective. Mol Cell Neurosci. 2005 Mar;29(3):381-393. doi: 1016/j.mcn.2005.03.005.

Avidan H, Kipnis J, Butovsky O, Caspi RR, Schwartz M. Vaccination With Autoantigen Protects Against Aggregated Beta-Amyloid and Glutamate Toxicity by Controlling Microglia: Effect of CD4+CD25+ T Cells. Eur J Immunol. 2004 Dec;34(12):3434-3445. doi: 1002/eji.200425405.

Ibarra A, Hauben E, Butovsky O, Schwartz M. The Therapeutic Window After Spinal Cord Injury Can Accommodate T Cell-Based Vaccination and Methylprednisolone in Rats. Eur J Neurosci. 2004 Jun;19(11):2984-2990. doi: 1111/j.1460-9568.2004.03431.x.

Bomstein Y, Marder JB, Vitner K, Smirnov I, Lisaey G, Butovsky O, Fulga V, Yoles E. Features of Skin-Coincubated Macrophages That Promote Recovery From Spinal Cord Injury. J Neuroimmunol. 2003 Jun;142(1-2):10-16. doi: 1016/s0165-5728(03)00230-4.

Hauben E, Gothilf A, Cohen A, Butovsky O, Nevo U, Smirnov I, Yoles E, Akselrod S, Schwartz M. Vaccination With Dendritic Cells Pulsed With Peptides of Myelin Basic Protein Promotes Functional Recovery From Spinal Cord Injury. J Neurosci. 2003 Oct 22;23(29):8808-8819. doi: 1523/jneurosci.23-29-08808.2003.

Fisher J, Levkovitch-Verbin H, Schori H, Yoles E, Butovsky O, Kaye JF, Ben-Nun A, Schwartz M. Vaccination for Neuroprotection in the Mouse Optic Nerve: Implications for Optic Neuropathies. J Neurosci. 2001 Jan 1;21(1):136-142. doi: 1523/jneurosci.21-01-00136.2001.

Butovsky O, Hauben E, Schwartz M. Morphological Aspects of Spinal Cord Autoimmune Neuroprotection: Colocalization of T Cells With B7-2 (CD86) and Prevention of Cyst Formation. FASEB J. 2001 May;15(7):1065-1067. doi: 1096/fj.00-0663fje.

Hauben E, Butovsky O, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Leibowitz-Amit R, Pevsner E, Akselrod S, Neeman M, Cohen IR, Schwartz M. Passive or Active Immunization With Myelin Basic Protein Promotes Recovery From Spinal Cord Contusion. Neurosci. 2000 Sep 1;20(17):6421-6430. doi: 1523/jneurosci.20-17-06421.2000.

2023

Guneykaya D, Ugursu B, Logiacco F, Popp O, Feiks MA, Meyer N, Wendt S, Semtner M, Cherif F, Gauthier C, Madore C, Yin Z, Çınar Ö, Arslan T, Gerevich Z, Mertins P, Butovsky O, Kettenmann H, Wolf SA. “Sex-specific microglia state in the Neuroligin-4 knock-out mouse model of autism spectrum disorder.” Brain Behav Immun. March 2023. DOI: 1016/j.bbi.2023.03.023

Yin Z, Herron S, Silveira S, Kleemann K, Gauthier C, Mallah D, Cheng Y, Margeta MA, Pitts KM, Barry J-L, Subramanian A, Shorey H, Brandao W, Durao A, Delpech J-C, Madore C, Jedrychowski M, Ajay AK, Murugaiyan G, Hersh SW, Ikezu S, Ikezu T, Butovsky O. “Identification of a protective microglial state mediated by miR-155 and interferon-γ signaling in a mouse model of Alzheimer’s disease.” Nat Neurosci. 2023. DOI: 1038/s41593-023-01355-y

2022

Paolicelli RC, Sierra A, Stevens B, Tremblay ME, Aguzzi A, Ajami B, Amit I, Audinat E, Bechmann I, Bennett M, Bennett F, Bessis A, Biber K, Bilbo S, Blurton-Jones M, Boddeke E, Brites D, Brône B, Brown GC, Butovsky O, Carson MJ, Castellano B, Colonna M, Cowley SA, Cunningham C, Davalos D, De Jager PL, de Strooper B, Denes A, Eggen BJL, Eyo U, Galea E, Garel S, Ginhoux F, Glass CK, Gokce O, Gomez-Nicola D, González B, Gordon S, Graeber MB, Greenhalgh AD, Gressens P, Greter M, Gutmann DH, Haass C, Heneka MT, Heppner FL, Hong S, Hume DA, Jung S, Kettenmann H, Kipnis J, Koyama R, Lemke G, Lynch M, Majewska A, Malcangio M, Malm T, Mancuso R, Masuda T, Matteoli M, McColl BW, Miron VE, Molofsky AV, Monje M, Mracsko E, Nadjar A, Neher JJ, Neniskyte U, Neumann H, Noda M, Peng B, Peri F, Perry VH, Popovich PG, Pridans C, Priller J, Prinz M, Ragozzino D, Ransohoff RM, Salter MW, Schaefer A, Schafer DP, Schwartz M, Simons M, Smith CJ, Streit WJ, Tay TL, Tsai LH, Verkhratsky A, von Bernhardi R, Wake H, Wittamer V, Wolf SA, Wu LJ, Wyss-Coray T. “Microglia states and nomenclature: A field at its crossroads.” Neuron. 2022 Nov 2;110(21):3458-3483. DOI: 1016/j.neuron.2022.10.020

Cappelli S, Spalloni A, Feiguin F, Visani G, Šušnjar U, Brown AL; NYGC ALS Consortium; De Bardi M, Borsellino G, Secrier M, Phatnani H, Romano M, Fratta P, Longone P, Buratti E. “NOS1AP is a novel molecular target and critical factor in TDP-43 pathology.” Brain Commun. 2022 Sep 23;4(5):fcac242. DOI: 1093/braincomms/fcac242

Shi H, Yin Z, Koronyo Y, Fuchs DT, Sheyn J, Davis MR, Wilson JW, Margeta MA, Pitts KM, Herron S, Ikezu S, Ikezu T, Graham SL, Gupta VK, Black KL, Mirzaei M, Butovsky O, Koronyo-Hamaoui M. “Regulating microglial miR-155 transcriptional phenotype alleviates Alzheimer’s-induced retinal vasculopathy by limiting Clec7a/Galectin-3(+) neurodegenerative microglia.” Acta Neuropathol Commun. 2022 Sep 8;10(1):136. DOI: 1186/s40478-022-01439-z

Margeta MA, Yin Z, Madore C, Pitts KM, Letcher SM, Tang J, Jiang S, Gauthier CD, Silveira SR, Schroeder CM, Lad EM, Proia AD, Tanzi RE, Holtzman DM, Krasemann S, Chen DF, Butovsky O. “Apolipoprotein E4 impairs the response of neurodegenerative retinal microglia and prevents neuronal loss in glaucoma.” Immunity. 2022 Sep 13;55(9):1627-1644.e7. DOI: 1016/j.immuni.2022.07.014

West PK, McCorkindale AN, Guennewig B, Ashhurst TM, Viengkhou B, Hayashida E, Jung SR, Butovsky O, Campbell IL, Hofer MJ. “The cytokines interleukin-6 and interferon-α induce distinct microglia phenotypes.” J Neuroinflammation. 2022 Apr 16;19(1):96. DOI: 1186/s12974-022-02441-x

Šušnjar U, Škrabar N, Brown AL, Abbassi Y, Phatnani H; NYGC ALS Consortium; Cortese A, Cereda C, Bugiardini E, Cardani R, Meola G, Ripolone M, Moggio M, Romano M, Secrier M, Fratta P, Buratti E. “Cell environment shapes TDP-43 function with implications in neuronal and muscle disease.” Commun Biol. 2022 Apr 5;5(1):314. DOI: 1038/s42003-022-03253-8

Cox LM, Calcagno N, Gauthier C, Madore C, Butovsky O, Weiner HL. “The microbiota restrains neurodegenerative microglia in a model of amyotrophic lateral sclerosis.” Microbiome. 2022 Mar 11;10(1):47. DOI: 1186/s40168-022-01232-z

Brown AL, Wilkins OG, Keuss MJ, Hill SE, Zanovello M, Lee WC, Bampton A, Lee FCY, Masino L, Qi YA, Bryce-Smith S, Gatt A, Hallegger M, Fagegaltier D, Phatnani H; NYGC ALS Consortium; Newcombe J, Gustavsson EK, Seddighi S, Reyes JF, Coon SL, Ramos D, Schiavo G, Fisher EMC, Raj T, Secrier M, Lashley T, Ule J, Buratti E, Humphrey J, Ward ME, Fratta P. “TDP-43 loss and ALS-risk SNPs drive mis-splicing and depletion of UNC13A.” Nature. 2022 Mar;603(7899):131-137. DOI: 1038/s41586-022-04436-3 (Epub 2022 Feb 23)

Fiore NT, Yin Z, Guneykaya D, Gauthier CD, Hayes JP, D’Hary A, Butovsky O, Moalem-Taylor G. “Sex-specific transcriptome of spinal microglia in neuropathic pain due to peripheral nerve injury.” Glia. 2022 Apr;70(4):675-696. DOI: 1002/glia.24133 (Epub 2022 Jan 20)

2021

NeuroLINCS Consortium; Li J, Lim RG, Kaye JA, Dardov V, Coyne AN, Wu J, Milani P, Cheng A, Thompson TG, Ornelas L, Frank A, Adam M, Banuelos MG, Casale M, Cox V, Escalante-Chong R, Daigle JG, Gomez E, Hayes L, Holewenski R, Lei S, Lenail A, Lima L, Mandefro B, Matlock A, Panther L, Patel-Murray NL, Pham J, Ramamoorthy D, Sachs K, Shelley B, Stocksdale J, Trost H, Wilhelm M, Venkatraman V, Wassie BT, Wyman S, Yang S; NYGC ALS Consortium; Van Eyk JE, Lloyd TE, Finkbeiner S, Fraenkel E, Rothstein JD, Sareen D, Svendsen CN, Thompson LM. “An integrated multi-omic analysis of iPSC-derived motor neurons from C9ORF72 ALS patients.” iScience. 2021 Oct 12;24(11):103221. DOI: 1016/j.isci.2021.103221

Moreira TG, Mangani D, Cox LM, Leibowitz J, Lobo ELC, Oliveira MA, Gauthier CD, Nakagaki BN, Willocq V, Song A, Guo L, Lima DCA, Murugaiyan G, Butovsky O, Gabriely G, Anderson AC, Rezende RM, Faria AMC, Weiner HL. “PD-L1(+) and XCR1(+) dendritic cells are region-specific regulators of gut homeostasis.” Nat Commun. 2021 Aug 13;12(1):4907. DOI: 1038/s41467-021-25115-3

Wang C, Xiong M, Gratuze M, Bao X, Shi Y, Andhey PS, Manis M, Schroeder C, Yin Z, Madore C, Butovsky O, Artyomov M, Ulrich JD, Holtzman DM. “Selective removal of astrocytic APOE4 strongly protects against tau-mediated neurodegeneration and decreases synaptic phagocytosis by microglia.” Neuron. 2021 May 19;109(10):1657-1674.e7. DOI: 1016/j.neuron.2021.03.024

Zrzavy T, Schwaiger C, Wimmer I, Berger T, Bauer J, Butovsky O, Schwab JM, Lassmann H, Höftberger R. “Acute and non-resolving inflammation associate with oxidative injury after human spinal cord injury.” Brain. 2021 Feb 12;144(1):144-161. DOI: 1093/brain/awaa360

Dewan R, Chia R, Ding J, Hickman RA, Stein TD, Abramzon Y, Ahmed S, Sabir MS, Portley MK, Tucci A, Ibáñez K, Shankaracharya FNU, Keagle P, Rossi G, Caroppo P, Tagliavini F, Waldo ML, Johansson PM, Nilsson CF; American Genome Center (TAGC); FALS Sequencing Consortium; Genomics England Research Consortium; International ALS/FTD Genomics Consortium (iAFGC); International FTD Genetics Consortium (IFGC); International LBD Genomics Consortium (iLBDGC); NYGC ALS Consortium; PROSPECT Consortium; Rowe JB, Benussi L, Binetti G, Ghidoni R, Jabbari E, Viollet C, Glass JD, Singleton AB, Silani V, Ross OA, Ryten M, Torkamani A, Tanaka T, Ferrucci L, Resnick SM, Pickering-Brown S, Brady CB, Kowal N, Hardy JA, Van Deerlin V, Vonsattel JP, Harms MB, Morris HR, Ferrari R, Landers JE, Chiò A, Gibbs JR, Dalgard CL, Scholz SW, Traynor BJ. “Pathogenic Huntingtin Repeat Expansions in Patients with Frontotemporal Dementia and Amyotrophic Lateral Sclerosis.” Neuron. 2021 Feb 3;109(3):448-460.e4. DOI: 1016/j.neuron.2020.11.005

2020

Madore C, Leyrolle Q, Morel L, Rossitto M, Greenhalgh AD, Delpech JC, Martinat M, Bosch-Bouju C, Bourel J, Rani B, Lacabanne C, Thomazeau A, Hopperton KE, Beccari S, Sere A, Aubert A, De Smedt-Peyrusse V, Lecours C, Bisht K, Fourgeaud L, Gregoire S, Bretillon L, Acar N, Grant NJ, Badaut J, Gressens P, Sierra A, Butovsky O, Tremblay ME, Bazinet RP, Joffre C, Nadjar A, Layé S. Essential omega-3 fatty acids tune microglial phagocytosis of synaptic elements in the mouse developing brain. Nat Commun. 2020 Nov 30;11(1):6133. doi: 1038/s41467-020-19861-z.

Hagan N, Kane JL, Grover D, Woodworth L, Madore C, Saleh J, Sancho J, Liu J, Li Y, Proto J, Zelic M, Mahan A, Kothe M, Scholte AA, Fitzgerald M, Gisevius B, Haghikia A, Butovsky O, Ofengeim D. CSF1R signaling is a regulator of pathogenesis in progressive MS. Cell Death Dis. 2020 Oct 23;11(10):904. doi: 1038/s41419-020-03084-7.

Margeta MA, Letcher SM, Igo RP Jr, Cooke Bailey JN, Pasquale LR, Haines JL, Butovsky O, Wiggs JL; NEIGHBORHOOD consortium. Association of APOE With Primary Open-Angle Glaucoma Suggests a Protective Effect for APOE ε4. Invest Ophthalmol Vis Sci. 2020 Jul 1;61(8):3. doi: 1167/iovs.61.8.3.

Kempthorne L, Yoon H, Madore C, Smith S, Wszolek ZK, Rademakers R, Kim J, Butovsky O, Dickson DW. Correction to: Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy. Acta Neuropathol Commun. 2020 Jun 24;8(1):90. doi: 1186/s40478-020-00970-1.

Clarke J, Yaqubi M, Futhey NC, Sedaghat S, Baufeld C, Blain M, Baranzini S, Butovsky O, Antel J, White JH, Healy LM. Vitamin D Regulates MerTK-Dependent Phagocytosis in Human Myeloid Cells. J Immunol. 2020 Jul 15;205(2):398-406. doi: 4049/jimmunol.2000129.

Kempthorne L, Yoon H, Madore C, Smith S, Wszolek ZK, Rademakers R, Kim J, Butovsky O, Dickson DW. Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy. Acta Neuropathol Commun. 2020 May 19;8(1):72. doi: 1186/s40478-020-00947-0.

Ikezu S, Yeh H, Delpech JC, Woodbury ME, Van Enoo AA, Ruan Z, Sivakumaran S, You Y, Holland C, Guillamon-Vivancos T, Yoshii-Kitahara A, Botros MB, Madore C, Chao PH, Desani A, Manimaran S, Kalavai SV, Johnson WE, Butovsky O, Medalla M, Luebke JI, Ikezu T. Inhibition of colony stimulating factor 1 receptor corrects maternal inflammation-induced microglial and synaptic dysfunction and behavioral abnormalities. Mol Psychiatry. 2021 Jun;26(6):1808-1831. doi: 1038/s41380-020-0671-2.

Madore C, Yin Z, Leibowitz J, Butovsky O. Microglia, Lifestyle Stress, and Neurodegeneration. Immunity. 2020 Feb 18;52(2):222-240. doi: 1016/j.immuni.2019.12.003.

Roy ER, Wang B, Wan YW, Chiu G, Cole A, Yin Z, Propson NE, Xu Y, Jankowsky JL, Liu Z, Lee VM, Trojanowski JQ, Ginsberg SD, Butovsky O, Zheng H, Cao W. Type I interferon response drives neuroinflammation and synapse loss in Alzheimer disease. J Clin Invest. 2020 Apr 1;130(4):1912-1930. doi: 1172/JCI133737.

2019

Okunuki Y, Mukai R, Nakao T, Tabor SJ, Butovsky O, Dana R, Ksander BR, Connor KM. Retinal Microglia Initiate Neuroinflammation in Ocular Autoimmunity. Proc Natl Acad Sci U S A. 2019 May 14;116(20):9989-98. doi: 1073/pnas.1820663116.

Zrzavy T, Höftberger R, Berger T, Rauschka H, Butovsky O, Weiner H, Lassmann H. Pro‐Inflammatory Activation of Microglia in the Brain of Patients With Sepsis. Neuropathology and Applied Neurobiology. 2019;45(3):278-90. doi: 1111/nan.12523.

Duffy SS, Keating BA, Perera CJ, Lees JG, Tonkin RS, Makker PGS, Carrive P, Butovsky O, Moalem-Taylor G. Regulatory T Cells and Their Derived Cytokine, Interleukin-35, Reduce Pain in Experimental Autoimmune Encephalomyelitis. Journal of Neuroscience. 2019;39(12):2326-46. doi: 1523/JNEUROSCI.1866-18.2018.

Götzl JK, Brendel M, Werner G, Parhizkar S, Sebastian Monasor L, Kleinberger G, Colombo AV, Deussing M, Wagner M, Winkelmann J, Diehl-Schmid J, Levin J, Fellerer K, Reifschneider A, Bultmann S, Bartenstein P, Rominger A, Tahirovic S, Smith ST, Madore C, Butovsky O, Capell A, Haass C. Opposite Microglial Phenotypes Upon Loss of PGRN or TREM2 Result in Reduced Cerebral Glucose Metabolism. EMBO Mol Med. 2019 Jun;11(6):e9711. doi: 15252/emmm.201809999.

Parhizkar S, Arzberger T, Brendel M, Kleinberger G, Deussing M, Focke C, Nuscher B, Xiong M, Ghasemigharagoz A, Katzmarski N, Krasemann S, Lichtenthaler SF, Müller SA, Colombo A, Monasor LS, Tahirovic S, Herms J, Willem M, Pettkus N, Butovsky O, Bartenstein P, Edbauer D, Rominger A, Ertürk A, Grathwohl SA, NeherJJ, Holtzman DM, Meyer-Luehmann M, Haass C. Loss of TREM2 Function Increases Amyloid Seeding but Reduces Plaque-Associated ApoE. Nature Neuroscience. 2019;22(2):191. doi: 1038/s41593-018-0296-9.

Faustino J, Chip S, Derugin N, Jullienne A, Hamer M, Haddad E, Butovsky O, Obenaus A, Vexler ZS. CX3CR1-CCR2-Dependent Monocyte-Microglial Signaling Modulates Neurovascular Leakage and Acute Injury in a Mouse Model of Childhood Stroke. Journal of Cerebral Blood Flow Metabolism. 2019 Oct;39(10):1919-35. doi: 1177/0271678X19869908.

2018

Katsumoto A, Miranda AS, Butovsky O, Teixeira AL, Ransohoff RM, Lamb BT. Laquinimod Attenuates Inflammation by Modulating Macrophage Functions in Traumatic Brain Injury Mouse Model. J Neuroinflammation. 2018 Jan 30;15(1):26. doi: 1186/s12974-018-1069-6.

Lund H, Pieber M, Parsa R, Han J, Grommisch D, Ewing E, Kular L, Needhamsen M, Espinosa A, Nilsson E, Överby AK, Butovsky O, Jagodic M, Zhang XM, Harris RA. Competitive Repopulation of an Empty Microglial Niche Yields Functionally Distinct Subsets of Microglia-Like Cells. Nat Commun. 2018;9(1):4845. doi: 1038/s41467-018-07296-8.

Rubino SJ, Mayo L, Wimmer I, Siedler V, Brunner F, Hametner S, Madi A, Lanser A, Moreira T, Donnelly D, Cox L, Rezende RM, Butovsky O, Lassmann H, Weiner HL. Acute Microglia Ablation Induces Neurodegeneration in the Somatosensory System. Nat Commun. 2018;9(1):4578. doi: 1038/s41467-018-06898-4.

Zrzavy T, Machado-Santos J, Christine S, Baumgartner C, Weiner HL, Butovsky O, Lassmann H. Dominant Role of Microglial and Macrophage Innate Immune Responses in Human Ischemic Infarcts. Brain Pathol. 2018;28(6):791-805. doi: 1111/bpa.12644.

Butovsky O, Weiner HL. Microglial Signatures and Their Role in Health and Disease. Nat Rev Neurosci. 2018 Oct;19(10):622-35. doi: 1038/s41583-018-0057-5.

Okunuki Y, Mukai R, Pearsall EA, Klokman G, Husain D, Park DH, Korobkina E, Weiner HL, Butovsky O, Ksander BR, Miller JW, Connor KM. Microglia Inhibit Photoreceptor Cell Death and Regulate Immune Cell Infiltration in Response to Retinal Detachment. Proc Natl Acad Sci U S A. 2018 Jul 3;115(27):E6264-E6273. doi: 1073/pnas.1722115115.

Calcagno N, Baufeld C, Madore C, Butovsky O. TREMendous 2 Be Social. Immunity. 2018;48(5):842-3. doi: 1016/j.immuni.2018.04.032.

Lund H, Pieber M, Parsa R, Grommisch D, Ewing E, Kular L, Han J, Zhu K, Nijssen J, Hedlund E, Needhamsen M, Ruhrmann S, Guerreiro-Cacais AO, Berglund R, Forteza MJ, Ketelhuth DFJ, Butovsky O, Jagodic M, Zhang XM, Harris RA. Fatal Demyelinating Disease Is Induced by Monocyte-Derived Macrophages in the Absence of TGF-Β Signaling. Nat Immunol. 2018 May;19(5):1-7. doi: 1038/s41590-018-0108-z.

Baufeld C, O’Loughlin E, Calcagno N, Madore C, Butovsky O. Differential Contribution of Microglia and Monocytes in Neurodegenerative Diseases. J Neural Transm. 2018;125(5):809-26. doi: 1007/s00702-018-1901-0.

O’Loughlin E, Madore C, Lassmann H, Butovsky O. Microglial Phenotypes and Functions in Multiple Sclerosis. Cold Spring Harb Perspect Med. 2018 Feb 1;8(2):a028993. doi: 1101/cshperspect.a028993.

2017

Drokhlyansky E, Göz Aytürk D, Soh TK, Chrenek R, O’Loughlin E, Madore C, Butovsky O, Cepko CL. The Brain Parenchyma Has a Type I Interferon Response That Can Limit Virus Spread. Proc Natl Acad Sci USA. 2017 Jan 3;114(1):E95-E104. doi: 1073/pnas.1617461114.

Makker PG, Duffy SS, Lees JG, Perera CJ, Tonkin RS, Butovsky O, Park SB, Goldstein D, Moalem-Taylor G. Characterisation of Immune and Neuroinflammatory Changes Associated With Chemotherapy-Induced Peripheral Neuropathy. PLoS One. 2017 Jan 26;12(1):e0170814. doi: 1371/journal.pone.0170814.

Mazaheri F, Snaidero N, Kleinberger G, Madore C, Daria A, Werner G, Krasemann S, Capell A, Trümbach D, Wurst W, Brunner B, Bultmann S, Tahirovic S, Kerschensteiner M, Misgeld T, Butovsky O, Haass C. TREM2 Deficiency Impairs Chemotaxis and Microglial Responses to Neuronal Injury. EMBO Rep. 2017 Jul;18(7):1186-1198. doi: 15252/embr.201743922.

Zrzavy T, Hametner S, Wimmer I, Butovsky O, Weiner HL, Lassmann H. Loss of ‘Homeostatic’ Microglia and Patterns of Their Activation in Active Multiple Sclerosis. Brain. 2017 Jul 1;140(7):1900-1913. doi: 1093/brain/awx113.

2016

Bisht K, Sharma KP, Lecours C, Sánchez MG, El Hajj H, Milior G, Olmos-Alonso A, Gómez-Nicola D, Luheshi G, Vallières L, Branchi I, Maggi L, Limatola C, Butovsky O, Tremblay MÈ. Dark Microglia: A New Phenotype Predominantly Associated With Pathological States. Glia. 2016 May;64(5):826-839. doi: 1002/glia.22966.

Delpech JC, Wei L, Hao J, Yu X, Madore C, Butovsky O, Kaffman A. Early Life Stress Perturbs the Maturation of Microglia in the Developing Hippocampus. Brain Behav Immun. 2016 Oct;57:79-93. doi: 1016/j.bbi.2016.03.024.

Muth C, Schröck K, Madore C, Hartmann K, Fanek Z, Butovsky O, Glatzel M, Krasemann S. Activation of Microglia by Retroviral Infection Correlates With Transient Clearance of Prions From the Brain but Does Not Change Incubation Time. Brain Pathol. 2017 Sep;27(5):590-602. doi: 1111/bpa.12477.

2015

Jay TR, Miller CM, Cheng PJ, Graham LC, Bemiller S, Broihier ML, Xu G, Margevicius D, Karlo JC, Sousa GL, Cotleur AC, Butovsky O, Bekris L, Staugaitis SM, Leverenz JB, Pimplikar SW, Landreth GE, Howell GR, Ransohoff RM, Lamb BT. TREM2 Deficiency Eliminates TREM2+ Inflammatory Macrophages and Ameliorates Pathology in Alzheimer’s Disease Mouse Models. J Exp Med. 2015 Mar 9;212(3):287-295. doi: 1084/jem.20142322.

Moore CS, Ase AR, Kinsara A, Rao VT, Michell-Robinson M, Leong SY, Butovsky O, Ludwin SK, Séguéla P, Bar-Or A, Antel JP. P2ry12 expression and Function in Alternatively Activated Human Microglia. Neurol Neuroimmunol Neuroinflamm. 2015 Mar 19;2(2):e80. doi: 1212/NXI.0000000000000080.

Verheijden S, Beckers L, Casazza A, Butovsky O, Mazzone M, Baes M. Identification of a Chronic Non-Neurodegenerative Microglia Activation State in a Mouse Model of Peroxisomal Β-Oxidation Deficiency. Glia. 2015 Sep;63(9):1606-1620. doi: 1002/glia.22849.

Asai H, Ikezu S, Tsunoda S, Medalla M, Luebke J, Haydar T, Wolozin B, Butovsky O, Kügler S, Ikezu T. Depletion of Microglia and Inhibition of Exosome Synthesis Halt Tau Propagation. Nat Neurosci. 2015 Nov;18(11):1584-1593. doi: 1038/nn.4132.

2014

Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, et al. Identification of a Unique TGF-Beta-Dependent Molecular and Functional Signature in Microglia. Nat Neurosci. 2014 Feb;17(1):131-143. doi: 1038/nn.3599.

Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, Wu PM, Doykan CE, Lin J, Cotleur AC, et al. Differential Roles of Microglia and Monocytes in the Inflamed CNS: An EAE Study. J Exp Med. 2014 Jul 28;211(8):1533-1549. doi: 1084/jem.20132477.

Butovsky O, Jedrychowski MP, Cialic R, Krasemann S, Murugaiyan G, Fanek Z, Greco DJ, Wu PM, Doykan CE, Kiner O, et al. Targeting miR-155 Restores Abnormal Microglia and Attenuates Disease in SOD1 Mice. Ann Neurol. 2015 Jan;77(1):75-99. doi: 1002/ana.24304.

2000-2012

Butovsky O, Siddiqui S, Gabriely G, Lanser AJ, Dake B, Murugaiyan G, Doykan CE, Wu PM, Gali RR, Iyer LK, Lawson R, Berry J, Krichevsky AM, Cudkowicz ME, Weiner HL. Modulating Inflammatory Monocytes With a Unique microRNA Gene Signature Ameliorates Murine ALS. J Clin Invest. 2012 Sep 4; 122(9):3063-87. doi: 10.1172/JCI62636

Vaknin I, Kunis G, Miller O, Butovsky O, Bukshpan S, Beers DR, Henkel JS, Yoles E, Appel SH, Schwartz M. Excess Circulating Alternatively Activated Myeloid (M2) Cells Accelerate ALS Progression While Inhibiting Experimental Autoimmune Encephalomyelitis. PLoS One. 2011;6(11):e26921. doi: 1371/journal.pone.0026921.

Landa G, Butovsky O, Shoshani J, Schwartz M, Pollack A. Weekly Vaccination With Copaxone (Glatiramer Acetate) as a Potential Therapy for Dry Age-Related Macular Degeneration. Curr Eye Res. 2008;33(11):1011-1013. doi: 1080/02713680802486769.

Butovsky O, Kunis G, Koronyo-Hamaoui M, Schwartz M. Selective Ablation of Bone Marrow-Derived Dendritic Cells Increases Amyloid Plaques in a Mouse Alzheimer’s Disease Model. Eur J Neurosci. 2007 Jan;26(2):413-416. doi: 1111/j.1460-9568.2007.05684.x.

Butovsky O, Bukshpan S, Kunis G, Jung S, Schwartz M. Microglia Can Be Induced by IFN-Gamma or IL-4 to Express Neural or Dendritic-Like Markers. Mol Cell Neurosci. 2007 Nov;35(3):490-500. doi: 1016/j.mcn.2007.04.006.

Butovsky O, Talpalar AE, Ben-Yaakov K, Schwartz M. Activation of Microglia by Aggregated Beta-Amyloid or Lipopolysaccharide Impairs MHC-II Expression and Renders Them Cytotoxic Whereas IFN-Gamma and IL-4 Render Them Protective. Mol Cell Neurosci. 2005 Mar;29(3):381-393. doi: 1016/j.mcn.2005.03.005.

Avidan H, Kipnis J, Butovsky O, Caspi RR, Schwartz M. Vaccination With Autoantigen Protects Against Aggregated Beta-Amyloid and Glutamate Toxicity by Controlling Microglia: Effect of CD4+CD25+ T Cells. Eur J Immunol. 2004 Dec;34(12):3434-3445. doi: 1002/eji.200425405.

Ibarra A, Hauben E, Butovsky O, Schwartz M. The Therapeutic Window After Spinal Cord Injury Can Accommodate T Cell-Based Vaccination and Methylprednisolone in Rats. Eur J Neurosci. 2004 Jun;19(11):2984-2990. doi: 1111/j.1460-9568.2004.03431.x.

Bomstein Y, Marder JB, Vitner K, Smirnov I, Lisaey G, Butovsky O, Fulga V, Yoles E. Features of Skin-Coincubated Macrophages That Promote Recovery From Spinal Cord Injury. J Neuroimmunol. 2003 Jun;142(1-2):10-16. doi: 1016/s0165-5728(03)00230-4.

Hauben E, Gothilf A, Cohen A, Butovsky O, Nevo U, Smirnov I, Yoles E, Akselrod S, Schwartz M. Vaccination With Dendritic Cells Pulsed With Peptides of Myelin Basic Protein Promotes Functional Recovery From Spinal Cord Injury. J Neurosci. 2003 Oct 22;23(29):8808-8819. doi: 1523/jneurosci.23-29-08808.2003.

Fisher J, Levkovitch-Verbin H, Schori H, Yoles E, Butovsky O, Kaye JF, Ben-Nun A, Schwartz M. Vaccination for Neuroprotection in the Mouse Optic Nerve: Implications for Optic Neuropathies. J Neurosci. 2001 Jan 1;21(1):136-142. doi: 1523/jneurosci.21-01-00136.2001.

Butovsky O, Hauben E, Schwartz M. Morphological Aspects of Spinal Cord Autoimmune Neuroprotection: Colocalization of T Cells With B7-2 (CD86) and Prevention of Cyst Formation. FASEB J. 2001 May;15(7):1065-1067. doi: 1096/fj.00-0663fje.

Hauben E, Butovsky O, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Leibowitz-Amit R, Pevsner E, Akselrod S, Neeman M, Cohen IR, Schwartz M. Passive or Active Immunization With Myelin Basic Protein Promotes Recovery From Spinal Cord Contusion. Neurosci. 2000 Sep 1;20(17):6421-6430. doi: 1523/jneurosci.20-17-06421.2000.

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