CSF1R inhibitor JNJ-40346527 attenuates microglial proliferation and neurodegeneration in P301S mice

Renzo Mancuso; Gemma Fryatt; Madeleine Cleal; Juliane Obst; Elena Pipi; Jimena Monzón-Sandoval; Elena Ribe; Laura Winchester; Caleb Webber; Alejo Nevado; Tom Jacobs; Nigel Austin; Clara Theunis; Karolien Grauwen; Eva Daniela Ruiz; Amrit Mudher; Marta Vicente-Rodriguez; Christine A. Parker; Camilla Simmons; Diana Cash; Jill Richardson; Declan N.C. Jones; Simon Lovestone; Diego Gómez-Nicola; V. Hugh Perry; Edward T. Bullmore; Junaid Bhatti; Samuel J. Chamberlain; Marta M. Correia; Anna L. Crofts; Amber Dickinson; Andrew C. Foster; Manfred G. Kitzbichler; Clare Knight; Mary Ellen Lynall; Christina Maurice; Ciara O'Donnell; Linda J. Pointon; Peter St George Hyslop; Lorinda Turner; Petra Vertes; Barry Widmer; Guy B. Williams; B. Paul Morgan; Claire A. Leckey; Angharad R. Morgan; Caroline O'Hagan; Samuel Touchard; Jonathan Cavanagh; Catherine Deith; Scott Farmer; John McClean; Alison McColl; Andrew McPherson; Paul Scouller; Murray Sutherland; H. W.G.M. Boddeke; Jill C. Richardson; Shahid Khan; Phil Murphy; Christine A. Parker; Jai Patel; Declan Jones; Peter De Boer; John Kemp; Wayne C. Drevets; Jeffrey S. Nye; Gayle Wittenberg; John Isaac; Anindya Bhattacharya; Nick Carruthers; Hartmuth Kolb; Carmine M. Pariante; Federico Turkheimer; Gareth J. Barker; Heidi Byrom; Diana Cash; Annamaria Cattaneo; Antony Gee; Caitlin Hastings; Nicole Mariani; Anna McLaughlin; Valeria Mondelli; Maria Nettis; Naghmeh Nikkheslat; Karen Randall; Hannah Sheridan; Camilla Simmons; Nisha Singh; Victoria Van Loo; Marta Vicente-Rodriguez; Tobias C. Wood; Courtney Worrell; Zuzanna Zajkowska; Niels Plath; Jan Egebjerg; Hans Eriksson; Francois Gastambide; Karen Husted Adams; Ross Jeggo; Christian Thomsen; Jan Torleif Pederson; Brian Campbell; Thomas Möller; Bob Nelson; Stevin Zorn; Jason O'Connor; Mary Jane Attenburrow; Alison Baird; Jithen Benjamin; Stuart Clare; Philip Cowen; I. Shu Huang; Samuel Hurley; Helen Jones; Francisca Mada; Alejo Nevado-Holgado; Akintayo Oladejo; Elena Ribe; Katy Smith; Anviti Vyas; Zoe Hughes; Rita Balice-Gordon; James Duerr; Justin R. Piro; Jonathan Sporn; V. Hugh Perry; Madeleine Cleal; Gemma Fryatt; Diego Gomez-Nicola; Renzo Mancuso; Richard Reynolds; Neil A. Harrison; Mara Cercignani; Charlotte L. Clarke; Elizabeth Hoskins; Charmaine Kohn; Rosemary Murray; Lauren Wilcock; Dominika Wlazly; Howard Mount

doi:10.1093/brain/awz241

CSF1R inhibitor JNJ-40346527 attenuates microglial proliferation and neurodegeneration in P301S mice

Renzo Mancuso, Gemma Fryatt, Madeleine Cleal, Juliane Obst, Elena Pipi, Jimena Monzón-Sandoval, Elena Ribe, Laura Winchester, Caleb Webber, Alejo Nevado, Tom Jacobs, Nigel Austin, Clara Theunis, Karolien Grauwen, Eva Daniela Ruiz, Amrit Mudher, Marta Vicente-Rodriguez, Christine A. Parker, Camilla Simmons, Diana CashJill Richardson, Declan N.C. Jones, Simon Lovestone, Diego Gómez-Nicola, V. Hugh Perry, Edward T. Bullmore, Junaid Bhatti, Samuel J. Chamberlain, Marta M. Correia, Anna L. Crofts, Amber Dickinson, Andrew C. Foster, Manfred G. Kitzbichler, Clare Knight, Mary Ellen Lynall, Christina Maurice, Ciara O'Donnell, Linda J. Pointon, Peter St George Hyslop, Lorinda Turner, Petra Vertes, Barry Widmer, Guy B. Williams, B. Paul Morgan, Claire A. Leckey, Angharad R. Morgan, Caroline O'Hagan, Samuel Touchard, Jonathan Cavanagh, Catherine Deith, Scott Farmer, John McClean, Alison McColl, Andrew McPherson, Paul Scouller, Murray Sutherland, H. W.G.M. Boddeke, Jill C. Richardson, Shahid Khan, Phil Murphy, Christine A. Parker, Jai Patel, Declan Jones, Peter De Boer, John Kemp, Wayne C. Drevets, Jeffrey S. Nye, Gayle Wittenberg, John Isaac, Anindya Bhattacharya, Nick Carruthers, Hartmuth Kolb, Carmine M. Pariante, Federico Turkheimer, Gareth J. Barker, Heidi Byrom, Diana Cash, Annamaria Cattaneo, Antony Gee, Caitlin Hastings, Nicole Mariani, Anna McLaughlin, Valeria Mondelli, Maria Nettis, Naghmeh Nikkheslat, Karen Randall, Hannah Sheridan, Camilla Simmons, Nisha Singh, Victoria Van Loo, Marta Vicente-Rodriguez, Tobias C. Wood, Courtney Worrell, Zuzanna Zajkowska, Niels Plath, Jan Egebjerg, Hans Eriksson, Francois Gastambide, Karen Husted Adams, Ross Jeggo, Christian Thomsen, Jan Torleif Pederson, Brian Campbell, Thomas Möller, Bob Nelson, Stevin Zorn, Jason O'Connor, Mary Jane Attenburrow, Alison Baird, Jithen Benjamin, Stuart Clare, Philip Cowen, I. Shu Huang, Samuel Hurley, Helen Jones, Francisca Mada, Alejo Nevado-Holgado, Akintayo Oladejo, Elena Ribe, Katy Smith, Anviti Vyas, Zoe Hughes, Rita Balice-Gordon, James Duerr, Justin R. Piro, Jonathan Sporn, V. Hugh Perry, Madeleine Cleal, Gemma Fryatt, Diego Gomez-Nicola, Renzo Mancuso, Richard Reynolds, Neil A. Harrison, Mara Cercignani, Charlotte L. Clarke, Elizabeth Hoskins, Charmaine Kohn, Rosemary Murray, Lauren Wilcock, Dominika Wlazly, Howard Mount

Department of Pharmacology

Research output: Contribution to journal › Article › peer-review

164 Scopus citations

Abstract

Neuroinflammation and microglial activation are significant processes in Alzheimer's disease pathology. Recent genome-wide association studies have highlighted multiple immune-related genes in association with Alzheimer's disease, and experimental data have demonstrated microglial proliferation as a significant component of the neuropathology. In this study, we tested the efficacy of the selective CSF1R inhibitor JNJ-40346527 (JNJ-527) in the P301S mouse tauopathy model. We first demonstrated the anti-proliferative effects of JNJ-527 on microglia in the ME7 prion model, and its impact on the inflammatory profile, and provided potential CNS biomarkers for clinical investigation with the compound, including pharmacokinetic/pharmacodynamics and efficacy assessment by TSPO autoradiography and CSF proteomics. Then, we showed for the first time that blockade of microglial proliferation and modification of microglial phenotype leads to an attenuation of tau-induced neurodegeneration and results in functional improvement in P301S mice. Overall, this work strongly supports the potential for inhibition of CSF1R as a target for the treatment of Alzheimer's disease and other tau-mediated neurodegenerative diseases.

Original language	English (US)
Pages (from-to)	3243-3264
Number of pages	22
Journal	Brain
Volume	142
Issue number	10
DOIs	https://doi.org/10.1093/brain/awz241
State	Published - Oct 1 2019

Keywords

Alzheimer's disease
CSF1R
Microglia
Neuroinflammation
Tau

ASJC Scopus subject areas

Clinical Neurology

Access to Document

10.1093/brain/awz241

Cite this

Mancuso, R., Fryatt, G., Cleal, M., Obst, J., Pipi, E., Monzón-Sandoval, J., Ribe, E., Winchester, L., Webber, C., Nevado, A., Jacobs, T., Austin, N., Theunis, C., Grauwen, K., Ruiz, E. D., Mudher, A., Vicente-Rodriguez, M., Parker, C. A., Simmons, C., ... Mount, H. (2019). CSF1R inhibitor JNJ-40346527 attenuates microglial proliferation and neurodegeneration in P301S mice. Brain, 142(10), 3243-3264. https://doi.org/10.1093/brain/awz241

Mancuso, R, Fryatt, G, Cleal, M, Obst, J, Pipi, E, Monzón-Sandoval, J, Ribe, E, Winchester, L, Webber, C, Nevado, A, Jacobs, T, Austin, N, Theunis, C, Grauwen, K, Ruiz, ED, Mudher, A, Vicente-Rodriguez, M, Parker, CA, Simmons, C, Cash, D, Richardson, J, Jones, DNC, Lovestone, S, Gómez-Nicola, D, Hugh Perry, V, Bullmore, ET, Bhatti, J, Chamberlain, SJ, Correia, MM, Crofts, AL, Dickinson, A, Foster, AC, Kitzbichler, MG, Knight, C, Lynall, ME, Maurice, C, O'Donnell, C, Pointon, LJ, St George Hyslop, P, Turner, L, Vertes, P, Widmer, B, Williams, GB, Paul Morgan, B, Leckey, CA, Morgan, AR, O'Hagan, C, Touchard, S, Cavanagh, J, Deith, C, Farmer, S, McClean, J, McColl, A, McPherson, A, Scouller, P, Sutherland, M, Boddeke, HWGM, Richardson, JC, Khan, S, Murphy, P, Parker, CA, Patel, J, Jones, D, De Boer, P, Kemp, J, Drevets, WC, Nye, JS, Wittenberg, G, Isaac, J, Bhattacharya, A, Carruthers, N, Kolb, H, Pariante, CM, Turkheimer, F, Barker, GJ, Byrom, H, Cash, D, Cattaneo, A, Gee, A, Hastings, C, Mariani, N, McLaughlin, A, Mondelli, V, Nettis, M, Nikkheslat, N, Randall, K, Sheridan, H, Simmons, C, Singh, N, Van Loo, V, Vicente-Rodriguez, M, Wood, TC, Worrell, C, Zajkowska, Z, Plath, N, Egebjerg, J, Eriksson, H, Gastambide, F, Adams, KH, Jeggo, R, Thomsen, C, Pederson, JT, Campbell, B, Möller, T, Nelson, B, Zorn, S, O'Connor, J, Attenburrow, MJ, Baird, A, Benjamin, J, Clare, S, Cowen, P, Huang, IS, Hurley, S, Jones, H, Mada, F, Nevado-Holgado, A, Oladejo, A, Ribe, E, Smith, K, Vyas, A, Hughes, Z, Balice-Gordon, R, Duerr, J, Piro, JR, Sporn, J, Hugh Perry, V, Cleal, M, Fryatt, G, Gomez-Nicola, D, Mancuso, R, Reynolds, R, Harrison, NA, Cercignani, M, Clarke, CL, Hoskins, E, Kohn, C, Murray, R, Wilcock, L, Wlazly, D & Mount, H 2019, 'CSF1R inhibitor JNJ-40346527 attenuates microglial proliferation and neurodegeneration in P301S mice', Brain, vol. 142, no. 10, pp. 3243-3264. https://doi.org/10.1093/brain/awz241

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title = "CSF1R inhibitor JNJ-40346527 attenuates microglial proliferation and neurodegeneration in P301S mice",

abstract = "Neuroinflammation and microglial activation are significant processes in Alzheimer's disease pathology. Recent genome-wide association studies have highlighted multiple immune-related genes in association with Alzheimer's disease, and experimental data have demonstrated microglial proliferation as a significant component of the neuropathology. In this study, we tested the efficacy of the selective CSF1R inhibitor JNJ-40346527 (JNJ-527) in the P301S mouse tauopathy model. We first demonstrated the anti-proliferative effects of JNJ-527 on microglia in the ME7 prion model, and its impact on the inflammatory profile, and provided potential CNS biomarkers for clinical investigation with the compound, including pharmacokinetic/pharmacodynamics and efficacy assessment by TSPO autoradiography and CSF proteomics. Then, we showed for the first time that blockade of microglial proliferation and modification of microglial phenotype leads to an attenuation of tau-induced neurodegeneration and results in functional improvement in P301S mice. Overall, this work strongly supports the potential for inhibition of CSF1R as a target for the treatment of Alzheimer's disease and other tau-mediated neurodegenerative diseases.",

keywords = "Alzheimer's disease, CSF1R, Microglia, Neuroinflammation, Tau",

author = "Renzo Mancuso and Gemma Fryatt and Madeleine Cleal and Juliane Obst and Elena Pipi and Jimena Monz{\'o}n-Sandoval and Elena Ribe and Laura Winchester and Caleb Webber and Alejo Nevado and Tom Jacobs and Nigel Austin and Clara Theunis and Karolien Grauwen and Ruiz, {Eva Daniela} and Amrit Mudher and Marta Vicente-Rodriguez and Parker, {Christine A.} and Camilla Simmons and Diana Cash and Jill Richardson and Jones, {Declan N.C.} and Simon Lovestone and Diego G{\'o}mez-Nicola and {Hugh Perry}, V. and Bullmore, {Edward T.} and Junaid Bhatti and Chamberlain, {Samuel J.} and Correia, {Marta M.} and Crofts, {Anna L.} and Amber Dickinson and Foster, {Andrew C.} and Kitzbichler, {Manfred G.} and Clare Knight and Lynall, {Mary Ellen} and Christina Maurice and Ciara O'Donnell and Pointon, {Linda J.} and {St George Hyslop}, Peter and Lorinda Turner and Petra Vertes and Barry Widmer and Williams, {Guy B.} and {Paul Morgan}, B. and Leckey, {Claire A.} and Morgan, {Angharad R.} and Caroline O'Hagan and Samuel Touchard and Jonathan Cavanagh and Catherine Deith and Scott Farmer and John McClean and Alison McColl and Andrew McPherson and Paul Scouller and Murray Sutherland and Boddeke, {H. W.G.M.} and Richardson, {Jill C.} and Shahid Khan and Phil Murphy and Parker, {Christine A.} and Jai Patel and Declan Jones and {De Boer}, Peter and John Kemp and Drevets, {Wayne C.} and Nye, {Jeffrey S.} and Gayle Wittenberg and John Isaac and Anindya Bhattacharya and Nick Carruthers and Hartmuth Kolb and Pariante, {Carmine M.} and Federico Turkheimer and Barker, {Gareth J.} and Heidi Byrom and Diana Cash and Annamaria Cattaneo and Antony Gee and Caitlin Hastings and Nicole Mariani and Anna McLaughlin and Valeria Mondelli and Maria Nettis and Naghmeh Nikkheslat and Karen Randall and Hannah Sheridan and Camilla Simmons and Nisha Singh and {Van Loo}, Victoria and Marta Vicente-Rodriguez and Wood, {Tobias C.} and Courtney Worrell and Zuzanna Zajkowska and Niels Plath and Jan Egebjerg and Hans Eriksson and Francois Gastambide and Adams, {Karen Husted} and Ross Jeggo and Christian Thomsen and Pederson, {Jan Torleif} and Brian Campbell and Thomas M{\"o}ller and Bob Nelson and Stevin Zorn and Jason O'Connor and Attenburrow, {Mary Jane} and Alison Baird and Jithen Benjamin and Stuart Clare and Philip Cowen and Huang, {I. Shu} and Samuel Hurley and Helen Jones and Francisca Mada and Alejo Nevado-Holgado and Akintayo Oladejo and Elena Ribe and Katy Smith and Anviti Vyas and Zoe Hughes and Rita Balice-Gordon and James Duerr and Piro, {Justin R.} and Jonathan Sporn and {Hugh Perry}, V. and Madeleine Cleal and Gemma Fryatt and Diego Gomez-Nicola and Renzo Mancuso and Richard Reynolds and Harrison, {Neil A.} and Mara Cercignani and Clarke, {Charlotte L.} and Elizabeth Hoskins and Charmaine Kohn and Rosemary Murray and Lauren Wilcock and Dominika Wlazly and Howard Mount",

note = "Publisher Copyright: {\textcopyright} The Author(s) (2019). Published by Oxford University Press on behalf of the Guarantors of Brain. This is an Open Access article distributed under the terms of the Creative Commons Attribution License",

year = "2019",

month = oct,

day = "1",

doi = "10.1093/brain/awz241",

language = "English (US)",

volume = "142",

pages = "3243--3264",

journal = "Brain",

issn = "0006-8950",

publisher = "Oxford University Press",

number = "10",

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TY - JOUR

T1 - CSF1R inhibitor JNJ-40346527 attenuates microglial proliferation and neurodegeneration in P301S mice

AU - Mancuso, Renzo

AU - Fryatt, Gemma

AU - Cleal, Madeleine

AU - Obst, Juliane

AU - Pipi, Elena

AU - Monzón-Sandoval, Jimena

AU - Ribe, Elena

AU - Winchester, Laura

AU - Webber, Caleb

AU - Nevado, Alejo

AU - Jacobs, Tom

AU - Austin, Nigel

AU - Theunis, Clara

AU - Grauwen, Karolien

AU - Ruiz, Eva Daniela

AU - Mudher, Amrit

AU - Vicente-Rodriguez, Marta

AU - Parker, Christine A.

AU - Simmons, Camilla

AU - Cash, Diana

AU - Richardson, Jill

AU - Jones, Declan N.C.

AU - Lovestone, Simon

AU - Gómez-Nicola, Diego

AU - Hugh Perry, V.

AU - Bullmore, Edward T.

AU - Bhatti, Junaid

AU - Chamberlain, Samuel J.

AU - Correia, Marta M.

AU - Crofts, Anna L.

AU - Dickinson, Amber

AU - Foster, Andrew C.

AU - Kitzbichler, Manfred G.

AU - Knight, Clare

AU - Lynall, Mary Ellen

AU - Maurice, Christina

AU - O'Donnell, Ciara

AU - Pointon, Linda J.

AU - St George Hyslop, Peter

AU - Turner, Lorinda

AU - Vertes, Petra

AU - Widmer, Barry

AU - Williams, Guy B.

AU - Paul Morgan, B.

AU - Leckey, Claire A.

AU - Morgan, Angharad R.

AU - O'Hagan, Caroline

AU - Touchard, Samuel

AU - Cavanagh, Jonathan

AU - Deith, Catherine

AU - Farmer, Scott

AU - McClean, John

AU - McColl, Alison

AU - McPherson, Andrew

AU - Scouller, Paul

AU - Sutherland, Murray

AU - Boddeke, H. W.G.M.

AU - Richardson, Jill C.

AU - Khan, Shahid

AU - Murphy, Phil

AU - Parker, Christine A.

AU - Patel, Jai

AU - Jones, Declan

AU - De Boer, Peter

AU - Kemp, John

AU - Drevets, Wayne C.

AU - Nye, Jeffrey S.

AU - Wittenberg, Gayle

AU - Isaac, John

AU - Bhattacharya, Anindya

AU - Carruthers, Nick

AU - Kolb, Hartmuth

AU - Pariante, Carmine M.

AU - Turkheimer, Federico

AU - Barker, Gareth J.

AU - Byrom, Heidi

AU - Cash, Diana

AU - Cattaneo, Annamaria

AU - Gee, Antony

AU - Hastings, Caitlin

AU - Mariani, Nicole

AU - McLaughlin, Anna

AU - Mondelli, Valeria

AU - Nettis, Maria

AU - Nikkheslat, Naghmeh

AU - Randall, Karen

AU - Sheridan, Hannah

AU - Simmons, Camilla

AU - Singh, Nisha

AU - Van Loo, Victoria

AU - Vicente-Rodriguez, Marta

AU - Wood, Tobias C.

AU - Worrell, Courtney

AU - Zajkowska, Zuzanna

AU - Plath, Niels

AU - Egebjerg, Jan

AU - Eriksson, Hans

AU - Gastambide, Francois

AU - Adams, Karen Husted

AU - Jeggo, Ross

AU - Thomsen, Christian

AU - Pederson, Jan Torleif

AU - Campbell, Brian

AU - Möller, Thomas

AU - Nelson, Bob

AU - Zorn, Stevin

AU - O'Connor, Jason

AU - Attenburrow, Mary Jane

AU - Baird, Alison

AU - Benjamin, Jithen

AU - Clare, Stuart

AU - Cowen, Philip

AU - Huang, I. Shu

AU - Hurley, Samuel

AU - Jones, Helen

AU - Mada, Francisca

AU - Nevado-Holgado, Alejo

AU - Oladejo, Akintayo

AU - Ribe, Elena

AU - Smith, Katy

AU - Vyas, Anviti

AU - Hughes, Zoe

AU - Balice-Gordon, Rita

AU - Duerr, James

AU - Piro, Justin R.

AU - Sporn, Jonathan

AU - Hugh Perry, V.

AU - Cleal, Madeleine

AU - Fryatt, Gemma

AU - Gomez-Nicola, Diego

AU - Mancuso, Renzo

AU - Reynolds, Richard

AU - Harrison, Neil A.

AU - Cercignani, Mara

AU - Clarke, Charlotte L.

AU - Hoskins, Elizabeth

AU - Kohn, Charmaine

AU - Murray, Rosemary

AU - Wilcock, Lauren

AU - Wlazly, Dominika

AU - Mount, Howard

N1 - Publisher Copyright: © The Author(s) (2019). Published by Oxford University Press on behalf of the Guarantors of Brain. This is an Open Access article distributed under the terms of the Creative Commons Attribution License

PY - 2019/10/1

Y1 - 2019/10/1

N2 - Neuroinflammation and microglial activation are significant processes in Alzheimer's disease pathology. Recent genome-wide association studies have highlighted multiple immune-related genes in association with Alzheimer's disease, and experimental data have demonstrated microglial proliferation as a significant component of the neuropathology. In this study, we tested the efficacy of the selective CSF1R inhibitor JNJ-40346527 (JNJ-527) in the P301S mouse tauopathy model. We first demonstrated the anti-proliferative effects of JNJ-527 on microglia in the ME7 prion model, and its impact on the inflammatory profile, and provided potential CNS biomarkers for clinical investigation with the compound, including pharmacokinetic/pharmacodynamics and efficacy assessment by TSPO autoradiography and CSF proteomics. Then, we showed for the first time that blockade of microglial proliferation and modification of microglial phenotype leads to an attenuation of tau-induced neurodegeneration and results in functional improvement in P301S mice. Overall, this work strongly supports the potential for inhibition of CSF1R as a target for the treatment of Alzheimer's disease and other tau-mediated neurodegenerative diseases.

AB - Neuroinflammation and microglial activation are significant processes in Alzheimer's disease pathology. Recent genome-wide association studies have highlighted multiple immune-related genes in association with Alzheimer's disease, and experimental data have demonstrated microglial proliferation as a significant component of the neuropathology. In this study, we tested the efficacy of the selective CSF1R inhibitor JNJ-40346527 (JNJ-527) in the P301S mouse tauopathy model. We first demonstrated the anti-proliferative effects of JNJ-527 on microglia in the ME7 prion model, and its impact on the inflammatory profile, and provided potential CNS biomarkers for clinical investigation with the compound, including pharmacokinetic/pharmacodynamics and efficacy assessment by TSPO autoradiography and CSF proteomics. Then, we showed for the first time that blockade of microglial proliferation and modification of microglial phenotype leads to an attenuation of tau-induced neurodegeneration and results in functional improvement in P301S mice. Overall, this work strongly supports the potential for inhibition of CSF1R as a target for the treatment of Alzheimer's disease and other tau-mediated neurodegenerative diseases.

KW - Alzheimer's disease

KW - CSF1R

KW - Microglia

KW - Neuroinflammation

KW - Tau

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UR - http://www.scopus.com/inward/citedby.url?scp=85072716789&partnerID=8YFLogxK

U2 - 10.1093/brain/awz241

DO - 10.1093/brain/awz241

M3 - Article

C2 - 31504240

AN - SCOPUS:85072716789

SN - 0006-8950

VL - 142

SP - 3243

EP - 3264

JO - Brain

JF - Brain

IS - 10

ER -

CSF1R inhibitor JNJ-40346527 attenuates microglial proliferation and neurodegeneration in P301S mice

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