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1. Microglia states and nomenclature

Author

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, Université de Lausanne = University of Lausanne (UNIL), University of the Basque Country/Euskal Herriko Unibertsitatea (UPV/EHU), Howard Hughes Medical Institute [Boston] (HHMI), Howard Hughes Medical Institute (HHMI)-Harvard Medical School [Boston] (HMS), Boston Children's Hospital, Harvard Medical School [Boston] (HMS), Centre de recherche du CHU de Québec-Université Laval (CRCHUQ), CHU de Québec–Université Laval, Université Laval [Québec] (ULaval)-Université Laval [Québec] (ULaval), McGill University = Université McGill [Montréal, Canada], University of Victoria [Canada] (UVIC), University of British Columbia [Vancouver], Universität Zürich [Zürich] = University of Zurich (UZH), Oregon Health and Science University [Portland] (OHSU), Weizmann Institute of Science [Rehovot, Israël], Institut de Génomique Fonctionnelle (IGF), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Children’s Hospital of Philadelphia (CHOP ), Institut de biologie de l'ENS Paris (IBENS), Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), AbbVie Deutschland GmbH & Co KG, Abbott GmbH & Co KG, Duke University [Durham], University of California [Irvine] (UC Irvine), University of California (UC), Universidade de Lisboa, 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’’ (RTI2018099267-B-I00 and RYC-2013-12817), a Tatiana Foundation award (P-048FTPGB 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., European Project: DP150104472,ARC::Discovery Projects(2015), European Project: 7469381(1974), European Project: 7244968(1972), Brown, Guy [0000-0002-3610-1730], and Apollo - University of Cambridge Repository

Subjects
Neurology & Neurosurgery, [SDV.NEU.NB]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology, General Neuroscience, Neurosciences, Psychology, Cognitive Sciences, ddc:610, Human medicine, Microglia
Abstract

International audience; 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.

Published
2022
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2. A Model-Based Hierarchical Bayesian Approach to Sholl Analysis

Author

Erik Vonkaenel, Alexis Feidler, Rebecca Lowery, Katherine Andersh, Tanzy Love, Ania Majewska, and Matthew N Mccall

Subjects
Article
Abstract

SummaryDue to the link between microglial morphology and function, morphological changes in microglia are frequently used to identify pathological immune responses in the central nervous system. In the absence of pathology, microglia are responsible for maintaining homeostasis, and their morphology can be indicative of how the healthy brain behaves in the presence of external stimuli and genetic differences. Despite recent interest in high throughput methods for morphological analysis, Sholl analysis is still the gold standard for quantifying microglia morphology via imaging data. Often, the raw data are naturally hierarchical, minimally including many cells per image and many images per animal. However, existing methods for performing downstream inference on Sholl data rely on truncating this hierarchy so rudimentary statistical testing procedures can be used. To fill this longstanding gap, we introduce a fully parametric model-based approach for analyzing Sholl data. We generalize our model to a hierarchical Bayesian framework so that inference can be performed without aggressive reduction of otherwise very rich data. We apply our model to three real data examples and perform simulation studies comparing the proposed method with a popular alternative.

Published
2023

3. Movers and shakers: Microglial dynamics and modulation of neural networks

Author

Mark Stoessel, Ania Majewska, and Brendan Whitelaw

Subjects
Cellular and Molecular Neuroscience, Neurology
Abstract

Microglia are multifaceted cells that act as immune sentinels, with important roles in pathological events, but also as integral contributors to the normal development and function of neural circuits. In the last decade, our understanding of the contributions these cells make to synaptic health and dysfunction has expanded at a dizzying pace. Here we review the known mechanisms that govern the dynamics of microglia allowing these motile cells to interact with synapses, and recruit microglia to specific sites on neurons. We then review the molecular signals that may underlie the function of microglia in synaptic remodeling. The emerging picture from the literature suggests that microglia are highly sensitive cells, reacting to neuronal signals with dynamic and specific actions tuned to the need of specific synapses and networks.

Published
2022

5. Repopulated microglia induce expression of Cxcl13 with differential changes in Tau phosphorylation but do not impact amyloid pathology

Author

Berke Karaahmet, M. Kerry O'Banion, Ania Majewska, Linh Le, and Monique Mendes

Subjects
General Neuroscience, Immunology, Amyloidogenic Proteins, Mice, Transgenic, Plaque, Amyloid, tau Proteins, Chemokine CXCL13, Cellular and Molecular Neuroscience, Mice, Neurology, Alzheimer Disease, Animals, Humans, Microglia, Phosphorylation
Abstract

Background Adult microglia rely on self-renewal through division to repopulate and sustain their numbers. However, with aging, microglia display morphological and transcriptional changes that reflect a heightened state of neuroinflammation. This state threatens aging neurons and other cells and can influence the progression of Alzheimer’s disease (AD). In this study, we sought to determine whether renewing microglia through a forced partial depletion/repopulation method could attenuate AD pathology in the 3xTg and APP/PS1 mouse models. Methods We pharmacologically depleted the microglia of two cohorts of 21- to 22-month-old 3xTg mice and one cohort of 14-month-old APP/PS1 mice using PLX5622 formulated in chow for 2 weeks. Following depletion, we returned the mice to standard chow diet for 1 month to allow microglial repopulation. We assessed the effect of depletion and repopulation on AD pathology, microglial gene expression, and surface levels of homeostatic markers on microglia using immunohistochemistry, single-cell RNAseq and flow cytometry. Results Although we did not identify a significant impact of microglial repopulation on amyloid pathology in either of the AD models, we observed differential changes in phosphorylated-Tau epitopes after repopulation in the 3xTg mice. We provide evidence that repopulated microglia in the hippocampal formation exhibited changes in the levels of homeostatic microglial markers. Lastly, we identified novel subpopulations of microglia by performing single-cell RNAseq analysis on CD45int/+ cells from hippocampi of control and repopulated 3xTg mice. In particular, one subpopulation induced after repopulation is characterized by heightened expression of Cxcl13. Conclusion Overall, we found that depleting and repopulating microglia causes overexpression of microglial Cxcl13 with disparate effects on Tau and amyloid pathologies.

Published
2022

6. Defining Microglial States and Nomenclature: A Roadmap to 2030

Author

Rosa 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, Ádám Dénes, 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 Heppner, Soyon Hong, Steffen Jung, Helmut Kettenmann, Jonathan Kipnis, Ryuta Koyama, Greg Lemke, Marina Lynch, Ania Majewska, Marzia Malcangio, Tarja Malm, Renzo Mancuso, Michela Matteoli, Barry 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, Josef Priller, Davide Ragozzino, Richard M. Ransohoff, Michael W. Salter, Anne Schaefer, Dorothy P. Schafer, Michal Schwartz, Mikael Simons, Wolfgang J. Streit, Tuan Leng Tay, Li-Huei Tsai, Alexei Verkhratsky, Rommy von Bernhardi, Hiroaki Wake, Valerie Wittamer, Susanne A. Wolf, Long-Jun Wu, and Tony Wyss-Coray

Subjects
History, Polymers and Plastics, Business and International Management, Industrial and Manufacturing Engineering
Published
2022
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