Microglia states and nomenclature: A field at its crossroads

Rosa C. Paolicelli; Amanda Sierra; Beth Stevens; Marie-Eve Tremblay; Adriano Aguzzi; Bahareh Ajami; Ido Amit; Etienne Audinat; Ingo Bechmann; Mariko Bennett; Frederick Bennett; Alain Bessis; Knut Biber; Staci Bilbo; Mathew Blurton-Jones; Erik Boddeke; Dora Brites; Bert Brône; Guy C. Brown; Oleg Butovsky; Monica J. Carson; Bernardo Castellano; Marco Colonna; Sally A. Cowley; Colm Cunningham; Dimitrios Davalos; Philip L. de Jager; Bart de Strooper; Adam Denes; Bart J. L. Eggen; Ukpong Eyo; Elena Galea; Sonia Garel; Florent Ginhoux; Christopher K. Glass; Ozgun Gokce; Diego Gomez-Nicola; Berta González; Siamon Gordon; Manuel B. Graeber; Andrew D. Greenhalgh; Pierre Gressens; Melanie Greter; David H. Gutmann; Christian Haass; Michael T. Heneka; Frank L. Heppner; Soyon Hong; David A. Hume; Steffen Jung; Helmut Kettenmann; Jonathan Kipnis; Ryuta Koyama; Greg Lemke; Marina Lynch; Ania Majewska; Marzia Malcangio; Tarja Malm; Renzo Mancuso; Takahiro Masuda; Michela Matteoli; Barry W. McColl; Veronique E. Miron; Anna Victoria Molofsky; Michelle Monje; Eva Mracsko; Agnes Nadjar; Jonas J. Neher; Urte Neniskyte; Harald Neumann; Mami Noda; Bo Peng; Francesca Peri; V. Hugh Perry; Phillip G. Popovich; Clare Pridans; Josef Priller; Marco Prinz; Davide Ragozzino; Richard M. Ransohoff; Michael W. Salter; Anne Schaefer; Dorothy P. Schafer; Michal Schwartz; Mikael Simons; Cody J. Smith; Wolfgang J. Streit; Tuan Leng Tay; Li-Huei Tsai; Alexei Verkhratsky; Rommy von Bernhardi; Hiroaki Wake; Valérie Wittamer; Susanne A. Wolf; Long-Jun Wu; Tony Wyss-Coray

doi:10.1016/j.neuron.2022.10.020

Microglia states and nomenclature: A field at its crossroads

Rosa C. Paolicelli^*
, Amanda Sierra^*
, Beth Stevens^*
, Marie-Eve Tremblay^*
, Adriano Aguzzi
, Bahareh Ajami
, Ido Amit
, Etienne Audinat
, Ingo Bechmann
, Mariko Bennett
, Frederick Bennett
, Alain Bessis
, Knut Biber
, Staci Bilbo
, Mathew Blurton-Jones
, Erik Boddeke
, Dora Brites
, Bert Brône
, Guy C. Brown
, Oleg Butovsky

Monica J. Carson, Bernardo Castellano, Marco Colonna, Sally A. Cowley, Colm Cunningham, Dimitrios Davalos, Philip L. de Jager, Bart de Strooper, Adam Denes, Bart J. L. Eggen, Ukpong Eyo, Elena Galea, Sonia Garel, Florent Ginhoux, Christopher K. Glass, Ozgun Gokce, Diego Gomez-Nicola, Berta González, Siamon Gordon, Manuel B. Graeber, Andrew D. Greenhalgh, Pierre Gressens, Melanie Greter, David H. Gutmann, Christian Haass, Michael T. Heneka, Frank L. Heppner, Soyon Hong, David A. Hume, Steffen Jung, Helmut Kettenmann, Jonathan Kipnis, Ryuta Koyama, Greg Lemke, Marina Lynch, Ania Majewska, Marzia Malcangio, Tarja Malm, Renzo Mancuso, Takahiro Masuda, Michela Matteoli, Barry W. McColl, Veronique E. Miron, Anna Victoria Molofsky, Michelle Monje, Eva Mracsko, Agnes Nadjar, Jonas J. Neher, Urte Neniskyte, Harald Neumann, Mami Noda, Bo Peng, Francesca Peri, V. Hugh Perry, Phillip G. Popovich, Clare Pridans, Josef Priller, Marco Prinz, Davide Ragozzino, Richard M. Ransohoff, Michael W. Salter, Anne Schaefer, Dorothy P. Schafer, Michal Schwartz, Mikael Simons, Cody J. Smith, Wolfgang J. Streit, Tuan Leng Tay, Li-Huei Tsai, Alexei Verkhratsky, Rommy von Bernhardi, Hiroaki Wake, Valérie Wittamer, Susanne A. Wolf, Long-Jun Wu, Tony Wyss-Coray

^*Corresponding author for this work

University of Lausanne
Achucarro Basque Center for Neuroscience
University of the Basque Country
Basque Foundation for Science
Broad Institute
Howard Hughes Medical Institute
Harvard University
Université Laval
McGill University
University of Victoria BC
St Paul's Hospital
University of Zurich
Oregon Health and Science University
Weizmann Institute of Science
Université de Montpellier
Leipzig University
Children's Hospital of Philadelphia
University of Pennsylvania
École normale supérieure
AbbVie
Duke University
University California Irvine
University of Groningen
University of Lisbon
Hasselt University
University of Cambridge
Harvard Medical School
University of California at Riverside
Fisiología e Inmunología
Autonomous University of Barcelona
Washington University St. Louis
University of Oxford
Trinity College Dublin
Cleveland Clinic Foundation
Case Western Reserve University
Columbia University Medical Center
University College London
Flanders Institute for Biotechnology
Institute of Experimental Medicine
University of Virginia
ICREA
Collège de France
Agency for Science, Technology and Research, Singapore
University of California at San Diego
Ludwig Maximilian University of Munich
University of Southampton
Chang Gung University
Faculty of Medicine and Health
University of Manchester
Université Paris Cité
German Center for Neurodegenerative Diseases
Munich Cluster for Systems Neurology (SyNergy), Germany
University of Luxembourg
Charité – Universitätsmedizin Berlin
University of Queensland
Max Delbrück Center for Molecular Medicine in the Helmholtz Association
Shenzhen Institute of Advanced Technology
The University of Tokyo
Salk Institute for Biological Studies
University of Rochester
King's College London
University of Eastern Finland
CAPRI-University of Antwerp
Kyushu University
Humanitas University
University of Edinburgh
University of California San Francisco
Stanford University Medical Center
F. Hoffmann-La Roche AG
Neurocentre Magendie
Institut universitaire de France
University of Tübingen
Vilnius University
University Hospital of Bonn
Xi'an Jiaotong University
Fudan University
Ohio State University
Technical University of Munich
University of Freiburg
Albert-Ludwigs-University Freiburg
University of Rome La Sapienza
IRCCS Fondazione Santa Lucia - Roma
Third Rock Ventures
University of Toronto
Icahn School of Medicine at Mount Sinai
Max Planck Institute for Biology of Ageing
University of Massachusetts Medical School
University of Notre Dame
University of Florida
Boston University
Massachusetts Institute of Technology
Universidad San Sebastián
Nagoya University
Université libre de Bruxelles
Mayo Clinic Rochester, MN

Research output: Contribution to journal › Review article › Academic › peer-review

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Abstract

Microglial research has advanced considerably in recent decades yet has been constrained by a rolling series of dichotomies such as “resting versus activated” and “M1 versus M2.” This dualistic classification of good or bad microglia is inconsistent with the wide repertoire of microglial states and functions in development, plasticity, aging, and diseases that were elucidated in recent years. New designations continuously arising in an attempt to describe the different microglial states, notably defined using transcriptomics and proteomics, may easily lead to a misleading, although unintentional, coupling of categories and functions. To address these issues, we assembled a group of multidisciplinary experts to discuss our current understanding of microglial states as a dynamic concept and the importance of addressing microglial function. Here, we provide a conceptual framework and recommendations on the use of microglial nomenclature for researchers, reviewers, and editors, which will serve as the foundations for a future white paper.

Original language	English
Pages (from-to)	3458-3483
Number of pages	26
Journal	Neuron
Volume	110
Issue number	21
DOIs	https://doi.org/10.1016/j.neuron.2022.10.020
Publication status	Published - 2 Nov 2022

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10.1016/j.neuron.2022.10.020

Microglia-states-and-nomenclature.pdfFinal published version, 2.77 MBLicence: CC BY

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Paolicelli, R. C., Sierra, A., Stevens, B., Tremblay, M.-E., 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, G. C., ... Wyss-Coray, T. (2022). Microglia states and nomenclature: A field at its crossroads. Neuron, 110(21), 3458-3483. https://doi.org/10.1016/j.neuron.2022.10.020

@article{49e613ae9d6d4c508dd6c95ee92f0088,

title = "Microglia states and nomenclature: A field at its crossroads",

abstract = "Microglial research has advanced considerably in recent decades yet has been constrained by a rolling series of dichotomies such as “resting versus activated” and “M1 versus M2.” This dualistic classification of good or bad microglia is inconsistent with the wide repertoire of microglial states and functions in development, plasticity, aging, and diseases that were elucidated in recent years. New designations continuously arising in an attempt to describe the different microglial states, notably defined using transcriptomics and proteomics, may easily lead to a misleading, although unintentional, coupling of categories and functions. To address these issues, we assembled a group of multidisciplinary experts to discuss our current understanding of microglial states as a dynamic concept and the importance of addressing microglial function. Here, we provide a conceptual framework and recommendations on the use of microglial nomenclature for researchers, reviewers, and editors, which will serve as the foundations for a future white paper.",

author = "Paolicelli, \{Rosa C.\} and Amanda Sierra and Beth Stevens and Marie-Eve Tremblay and Adriano Aguzzi and Bahareh Ajami and Ido Amit and Etienne Audinat and Ingo Bechmann and Mariko Bennett and Frederick Bennett and Alain Bessis and Knut Biber and Staci Bilbo and Mathew Blurton-Jones and Erik Boddeke and Dora Brites and Bert Br{\^o}ne and Brown, \{Guy C.\} and Oleg Butovsky and Carson, \{Monica J.\} and Bernardo Castellano and Marco Colonna and Cowley, \{Sally A.\} and Colm Cunningham and Dimitrios Davalos and \{de Jager\}, \{Philip L.\} and \{de Strooper\}, Bart and Adam Denes and Eggen, \{Bart J. L.\} and Ukpong Eyo and Elena Galea and Sonia Garel and Florent Ginhoux and Glass, \{Christopher K.\} and Ozgun Gokce and Diego Gomez-Nicola and Berta Gonz{\'a}lez and Siamon Gordon and Graeber, \{Manuel B.\} and Greenhalgh, \{Andrew D.\} and Pierre Gressens and Melanie Greter and Gutmann, \{David H.\} and Christian Haass and Heneka, \{Michael T.\} and Heppner, \{Frank L.\} and Soyon Hong and Hume, \{David A.\} and Steffen Jung and Helmut Kettenmann and Jonathan Kipnis and Ryuta Koyama and Greg Lemke and Marina Lynch and Ania Majewska and Marzia Malcangio and Tarja Malm and Renzo Mancuso and Takahiro Masuda and Michela Matteoli and McColl, \{Barry W.\} and Miron, \{Veronique E.\} and Molofsky, \{Anna Victoria\} and Michelle Monje and Eva Mracsko and Agnes Nadjar and Neher, \{Jonas J.\} and Urte Neniskyte and Harald Neumann and Mami Noda and Bo Peng and Francesca Peri and Perry, \{V. Hugh\} and Popovich, \{Phillip G.\} and Clare Pridans and Josef Priller and Marco Prinz and Davide Ragozzino and Ransohoff, \{Richard M.\} and Salter, \{Michael W.\} and Anne Schaefer and Schafer, \{Dorothy P.\} and Michal Schwartz and Mikael Simons and Smith, \{Cody J.\} and Streit, \{Wolfgang J.\} and Tay, \{Tuan Leng\} and Li-Huei Tsai and Alexei Verkhratsky and \{von Bernhardi\}, Rommy and Hiroaki Wake and Val{\'e}rie Wittamer and Wolf, \{Susanne A.\} and Long-Jun Wu and Tony Wyss-Coray",

note = "Funding Information: All authors in the author list are listed in alphabetical order. This work was supported by grants from the Dementia Research Switzerland – Synapsis Foundation , Swiss National Science Foundation ( SNSF 310030\_197940 ), and European Research Council ( ERC StGrant REMIND 804949 ) to R.C.P.; the Spanish Ministry of Science and Innovation Competitiveness MCIN/AEI/10.13039/501100011033 and FEDER “A way to make Europe” ( RTI2018-099267-B-I00 and RYC-2013-12817 ), a Tatiana Foundation award ( P-048-FTPGB 2018 ), and a Basque Government Department of Education project ( PIBA 2020\_1\_0030 ) to A.S.; Cure Alzheimer{\textquoteright}s Fund and Alzheimer's Association to B.S.; the Canadian Institutes of Health Research (foundation grant 341846 , project grant 461831 ) and Natural Sciences and Engineering Research Council of Canada (discovery grant RGPIN-2014-05308 ) to M.E.T. M.E.T. is a Tier II Canada Research Chair in Neurobiology of Aging and Cognition. This work was also funded by DFG CRC/TRR167 “NeuroMac” to I.A., J.P., M.P., and S.J. and by DFG SFB 1052, Project 209933838 to I.B. Australian Research Council support for project DP150104472 to M.B.G. is gratefully acknowledged. Funding Information: B.A. is the shareholder and member of scientific advisory board of Tranquis Therapeutics. K.B. is an employee and shareholder of AbbVie. M.C. receives research support from Vigil, is a member of the scientific advisory board of Vigil, and has a patent on TREM2. S.C. is a recipient of research funding from Eli Lilly and Company. C.C. is a member of the advisory board of Exalys Therapeutics and is the recipient of a research grant from IONIS therapeutics. B.D.S. is occasionally consulting for different companies. He is founding scientist of Augustin TX and of Muna TX. He is also shareholder of Muna TX. C.H. collaborates with Denali Therapeutics. C.H. is chief advisor of ISAR Bioscience and a member of the advisory board of AviadoBio. J.K. is a scientific advisor and collaborator with PureTech. T.M. is a cofounder of REGAIN Therapeutics, owner of a provisional patent on compositions and methods for treatment and/or prophylaxis of proteinopathies, and owner of a provisional patent on preventing or reverting abnormal amyloid deposition. R.M. has scientific collaborations with Alector, Nodthera, and Alchemab and is a consultant for Sanofi. B.M. has received consultancy fees from AstraZeneca. A. Sierra is a recipient of a research grant from Hoffmann La Roche. Publisher Copyright: {\textcopyright} 2022 Elsevier Inc.",

year = "2022",

month = nov,

day = "2",

doi = "10.1016/j.neuron.2022.10.020",

language = "English",

volume = "110",

pages = "3458--3483",

journal = "Neuron",

issn = "0896-6273",

publisher = "Cell Press",

number = "21",

}

Paolicelli, RC, Sierra, A, Stevens, B, Tremblay, M-E, 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, L-H, Verkhratsky, A, von Bernhardi, R, Wake, H, Wittamer, V, Wolf, SA, Wu, L-J & Wyss-Coray, T 2022, 'Microglia states and nomenclature: A field at its crossroads', Neuron, vol. 110, no. 21, pp. 3458-3483. https://doi.org/10.1016/j.neuron.2022.10.020

TY - JOUR

T1 - Microglia states and nomenclature

T2 - A field at its crossroads

AU - Paolicelli, Rosa C.

AU - Sierra, Amanda

AU - Stevens, Beth

AU - Tremblay, Marie-Eve

AU - Aguzzi, Adriano

AU - Ajami, Bahareh

AU - Amit, Ido

AU - Audinat, Etienne

AU - Bechmann, Ingo

AU - Bennett, Mariko

AU - Bennett, Frederick

AU - Bessis, Alain

AU - Biber, Knut

AU - Bilbo, Staci

AU - Blurton-Jones, Mathew

AU - Boddeke, Erik

AU - Brites, Dora

AU - Brône, Bert

AU - Brown, Guy C.

AU - Butovsky, Oleg

AU - Carson, Monica J.

AU - Castellano, Bernardo

AU - Colonna, Marco

AU - Cowley, Sally A.

AU - Cunningham, Colm

AU - Davalos, Dimitrios

AU - de Jager, Philip L.

AU - de Strooper, Bart

AU - Denes, Adam

AU - Eggen, Bart J. L.

AU - Eyo, Ukpong

AU - Galea, Elena

AU - Garel, Sonia

AU - Ginhoux, Florent

AU - Glass, Christopher K.

AU - Gokce, Ozgun

AU - Gomez-Nicola, Diego

AU - González, Berta

AU - Gordon, Siamon

AU - Graeber, Manuel B.

AU - Greenhalgh, Andrew D.

AU - Gressens, Pierre

AU - Greter, Melanie

AU - Gutmann, David H.

AU - Haass, Christian

AU - Heneka, Michael T.

AU - Heppner, Frank L.

AU - Hong, Soyon

AU - Hume, David A.

AU - Jung, Steffen

AU - Kettenmann, Helmut

AU - Kipnis, Jonathan

AU - Koyama, Ryuta

AU - Lemke, Greg

AU - Lynch, Marina

AU - Majewska, Ania

AU - Malcangio, Marzia

AU - Malm, Tarja

AU - Mancuso, Renzo

AU - Masuda, Takahiro

AU - Matteoli, Michela

AU - McColl, Barry W.

AU - Miron, Veronique E.

AU - Molofsky, Anna Victoria

AU - Monje, Michelle

AU - Mracsko, Eva

AU - Nadjar, Agnes

AU - Neher, Jonas J.

AU - Neniskyte, Urte

AU - Neumann, Harald

AU - Noda, Mami

AU - Peng, Bo

AU - Peri, Francesca

AU - Perry, V. Hugh

AU - Popovich, Phillip G.

AU - Pridans, Clare

AU - Priller, Josef

AU - Prinz, Marco

AU - Ragozzino, Davide

AU - Ransohoff, Richard M.

AU - Salter, Michael W.

AU - Schaefer, Anne

AU - Schafer, Dorothy P.

AU - Schwartz, Michal

AU - Simons, Mikael

AU - Smith, Cody J.

AU - Streit, Wolfgang J.

AU - Tay, Tuan Leng

AU - Tsai, Li-Huei

AU - Verkhratsky, Alexei

AU - von Bernhardi, Rommy

AU - Wake, Hiroaki

AU - Wittamer, Valérie

AU - Wolf, Susanne A.

AU - Wu, Long-Jun

AU - Wyss-Coray, Tony

N1 - Funding Information: All authors in the author list are listed in alphabetical order. This work was supported by grants from the Dementia Research Switzerland – Synapsis Foundation , Swiss National Science Foundation ( SNSF 310030_197940 ), and European Research Council ( ERC StGrant REMIND 804949 ) to R.C.P.; the Spanish Ministry of Science and Innovation Competitiveness MCIN/AEI/10.13039/501100011033 and FEDER “A way to make Europe” ( RTI2018-099267-B-I00 and RYC-2013-12817 ), a Tatiana Foundation award ( P-048-FTPGB 2018 ), and a Basque Government Department of Education project ( PIBA 2020_1_0030 ) to A.S.; Cure Alzheimer’s Fund and Alzheimer's Association to B.S.; the Canadian Institutes of Health Research (foundation grant 341846 , project grant 461831 ) and Natural Sciences and Engineering Research Council of Canada (discovery grant RGPIN-2014-05308 ) to M.E.T. M.E.T. is a Tier II Canada Research Chair in Neurobiology of Aging and Cognition. This work was also funded by DFG CRC/TRR167 “NeuroMac” to I.A., J.P., M.P., and S.J. and by DFG SFB 1052, Project 209933838 to I.B. Australian Research Council support for project DP150104472 to M.B.G. is gratefully acknowledged. Funding Information: B.A. is the shareholder and member of scientific advisory board of Tranquis Therapeutics. K.B. is an employee and shareholder of AbbVie. M.C. receives research support from Vigil, is a member of the scientific advisory board of Vigil, and has a patent on TREM2. S.C. is a recipient of research funding from Eli Lilly and Company. C.C. is a member of the advisory board of Exalys Therapeutics and is the recipient of a research grant from IONIS therapeutics. B.D.S. is occasionally consulting for different companies. He is founding scientist of Augustin TX and of Muna TX. He is also shareholder of Muna TX. C.H. collaborates with Denali Therapeutics. C.H. is chief advisor of ISAR Bioscience and a member of the advisory board of AviadoBio. J.K. is a scientific advisor and collaborator with PureTech. T.M. is a cofounder of REGAIN Therapeutics, owner of a provisional patent on compositions and methods for treatment and/or prophylaxis of proteinopathies, and owner of a provisional patent on preventing or reverting abnormal amyloid deposition. R.M. has scientific collaborations with Alector, Nodthera, and Alchemab and is a consultant for Sanofi. B.M. has received consultancy fees from AstraZeneca. A. Sierra is a recipient of a research grant from Hoffmann La Roche. Publisher Copyright: © 2022 Elsevier Inc.

PY - 2022/11/2

Y1 - 2022/11/2

N2 - Microglial research has advanced considerably in recent decades yet has been constrained by a rolling series of dichotomies such as “resting versus activated” and “M1 versus M2.” This dualistic classification of good or bad microglia is inconsistent with the wide repertoire of microglial states and functions in development, plasticity, aging, and diseases that were elucidated in recent years. New designations continuously arising in an attempt to describe the different microglial states, notably defined using transcriptomics and proteomics, may easily lead to a misleading, although unintentional, coupling of categories and functions. To address these issues, we assembled a group of multidisciplinary experts to discuss our current understanding of microglial states as a dynamic concept and the importance of addressing microglial function. Here, we provide a conceptual framework and recommendations on the use of microglial nomenclature for researchers, reviewers, and editors, which will serve as the foundations for a future white paper.

AB - Microglial research has advanced considerably in recent decades yet has been constrained by a rolling series of dichotomies such as “resting versus activated” and “M1 versus M2.” This dualistic classification of good or bad microglia is inconsistent with the wide repertoire of microglial states and functions in development, plasticity, aging, and diseases that were elucidated in recent years. New designations continuously arising in an attempt to describe the different microglial states, notably defined using transcriptomics and proteomics, may easily lead to a misleading, although unintentional, coupling of categories and functions. To address these issues, we assembled a group of multidisciplinary experts to discuss our current understanding of microglial states as a dynamic concept and the importance of addressing microglial function. Here, we provide a conceptual framework and recommendations on the use of microglial nomenclature for researchers, reviewers, and editors, which will serve as the foundations for a future white paper.

UR - https://www.scopus.com/pages/publications/85140895591

U2 - 10.1016/j.neuron.2022.10.020

DO - 10.1016/j.neuron.2022.10.020

M3 - Review article

C2 - 36327895

SN - 0896-6273

VL - 110

SP - 3458

EP - 3483

JO - Neuron

JF - Neuron

IS - 21

ER -

Microglia states and nomenclature: A field at its crossroads

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