A Combination of Ontogeny and CNS Environment Establishes Microglial Identity

Neuron

Volumn 98, Issue 6, 2018, Pages 1170-1183.e8

  Bennett, F Chris ^a   Bennett, Mariko L ^a   Yaqoob, Fazeela ^a   Mulinyawe, Sara B ^a   Grant, Gerald A ^a   Hayden Gephart, Melanie ^a   Plowey, Edward D ^a   Barres, Ben A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

brain macrophage; Csf1r; glial biology; microglia; neuroimmunity; ontogeny; Tmem119; transplantation

Indexed keywords

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CENTRAL NERVOUS SYSTEM; CHILD; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INFANT; MACROPHAGE; MALE; MICROGLIA; MICROGLIAL CELL CULTURE; MOUSE; NONHUMAN; ONTOGENY; PRESCHOOL CHILD; PRIORITY JOURNAL; YOLK SAC; ANIMAL; BRAIN; CELL LINEAGE; CYTOLOGY; HEMATOPOIETIC STEM CELL; KNOCKOUT MOUSE; METABOLISM;

CSF1R PROTEIN, MOUSE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR;

ANIMALS; BRAIN; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; HEMATOPOIETIC STEM CELLS; HUMANS; MACROPHAGES; MICE; MICE, KNOCKOUT; MICROGLIA; RECEPTORS, GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR;

EID: 85047326041     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2018.05.014     Document Type: Article

References (59)

1. Abud, E.M., Ramirez, R.N., Martinez, E.S., Healy, L.M., Nguyen, C.H.H., Newman, S.A., Yeromin, A.V., Scarfone, V.M., Marsh, S.E., Fimbres, C., et al. iPSC-derived human microglia-like cells to study neurological diseases. Neuron 94 (2017), 278–293.e9.
2. Ajami, B., Bennett, J.L., Krieger, C., Tetzlaff, W., Rossi, F.M.V., Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat. Neurosci. 10 (2007), 1538–1543.
3. Ajami, B., Bennett, J.L., Krieger, C., McNagny, K.M., Rossi, F.M.V., Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat. Neurosci. 14 (2011), 1142–1149.
4. Bain, C.C., Bravo-Blas, A., Scott, C.L., Perdiguero, E.G., Geissmann, F., Henri, S., Malissen, B., Osborne, L.C., Artis, D., Mowat, A.M., Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15 (2014), 929–937.
5. Bardou, P., Mariette, J., Escudié, F., Djemiel, C., Klopp, C., jvenn: an interactive Venn diagram viewer. BMC Bioinformatics, 15, 2014, 293.
6. Bennett, M.L., Bennett, F.C., Liddelow, S.A., Ajami, B., Zamanian, J.L., Fernhoff, N.B., Mulinyawe, S.B., Bohlen, C.J., Adil, A., Tucker, A., et al. New tools for studying microglia in the mouse and human CNS. Proc. Natl. Acad. Sci. USA 113 (2016), E1738–E1746.
7. Biffi, A., Montini, E., Lorioli, L., Cesani, M., Fumagalli, F., Plati, T., Baldoli, C., Martino, S., Calabria, A., Canale, S., et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science, 341, 2013, 1233158.
8. Bohlen, C.J., Bennett, F.C., Tucker, A.F., Collins, H.Y., Mulinyawe, S.B., Barres, B.A., Diverse requirements for microglial survival, specification, and function revealed by defined-medium cultures. Neuron 94 (2017), 759–773.e8.
9. Bruttger, J., Karram, K., Wörtge, S., Regen, T., Marini, F., Hoppmann, N., Klein, M., Blank, T., Yona, S., Wolf, Y., et al. Genetic cell ablation reveals clusters of local self-renewing microglia in the mammalian central nervous system. Immunity 43 (2015), 92–106.
10. Buttgereit, A., Lelios, I., Yu, X., Vrohlings, M., Krakoski, N.R., Gautier, E.L., Nishinakamura, R., Becher, B., Greter, M., Sall1 is a transcriptional regulator defining microglia identity and function. Nat. Immunol. 17 (2016), 1397–1406.
11. Chiu, I.M., Morimoto, E.T.A., Goodarzi, H., Liao, J.T., O'Keeffe, S., Phatnani, H.P., Muratet, M., Carroll, M.C., Levy, S., Tavazoie, S., et al. A neurodegeneration-specific gene-expression signature of acutely isolated microglia from an amyotrophic lateral sclerosis mouse model. Cell Rep. 4 (2013), 385–401.
12. Clarke, L.E., Liddelow, S.A., Chakraborty, C., Münch, A.E., Heiman, M., Barres, B.A., Normal aging induces A1-like astrocyte reactivity. Proc. Natl. Acad. Sci. USA 115 (2018), E1896–E1905.
13. Cronk, J.C., Filiano, A.J., Louveau, A., Marin, I., Marsh, R., Ji, E., Goldman, D.H., Smirnov, I., Geraci, N., Acton, S., et al. Peripherally derived macrophages can engraft the brain independent of irradiation and maintain an identity distinct from microglia. J. Exp. Med. 47 (2018), 1–10.
14. de Chaumont, F., Dallongeville, S., Chenouard, N., Hervé, N., Pop, S., Provoost, T., Meas-Yedid, V., Pankajakshan, P., Lecomte, T., Le Montagner, Y., et al. Icy: an open bioimage informatics platform for extended reproducible research. Nat. Methods 9 (2012), 690–696.
15. Dai, X.-M., Ryan, G.R., Hapel, A.J., Dominguez, M.G., Russell, R.G., Kapp, S., Sylvestre, V., Stanley, E.R., Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99 (2002), 111–120.
16. Dzenko, K.A., Andjelkovic, A.V., Kuziel, W.A., Pachter, J.S., The chemokine receptor CCR2 mediates the binding and internalization of monocyte chemoattractant protein-1 along brain microvessels. J. Neurosci. 21 (2001), 9214–9223.
17. Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M.F., Conway, S.J., Ng, L.G., Stanley, E.R., et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330 (2010), 841–845.
18. Gomez Perdiguero, E., Klapproth, K., Schulz, C., Busch, K., Azzoni, E., Crozet, L., Garner, H., Trouillet, C., de Bruijn, M.F., Geissmann, F., Rodewald, H.R., Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518 (2015), 547–551.
19. Gosselin, D., Link, V.M., Romanoski, C.E., Fonseca, G.J., Eichenfield, D.Z., Spann, N.J., Stender, J.D., Chun, H.B., Garner, H., Geissmann, F., Glass, C.K., Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159 (2014), 1327–1340.
20. Gosselin, D., Skola, D., Coufal, N.G., Holtman, I.R., Schlachetzki, J.C.M., Sajti, E., Jaeger, B.N., O'Connor, C., Fitzpatrick, C., Pasillas, M.P., et al. An environment-dependent transcriptional network specifies human microglia identity. Science 356 (2017), 1–10.
21. Hagemeyer, N., Kierdorf, K., Frenzel, K., Xue, J., Ringelhan, M., Abdullah, Z., Godin, I., Wieghofer, P., Costa Jordão, M.J., Ulas, T., et al. Transcriptome-based profiling of yolk sac-derived macrophages reveals a role for Irf8 in macrophage maturation. EMBO J. 35 (2016), 1730–1744.
22. Haynes, S.E., Hollopeter, G., Yang, G., Kurpius, D., Dailey, M.E., Gan, W.-B., Julius, D., The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 9 (2006), 1512–1519.
23. Heng, T.S.P., Painter, M.W., Immunological Genome Project Consortium. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9 (2008), 1091–1094.
24. Hickman, S.E., Kingery, N.D., Ohsumi, T.K., Borowsky, M.L., Wang, L.-C., Means, T.K., El Khoury, J., The microglial sensome revealed by direct RNA sequencing. Nat. Neurosci. 16 (2013), 1896–1905.
25. Hoeffel, G., Chen, J., Lavin, Y., Low, D., Almeida, F.F., See, P., Beaudin, A.E., Lum, J., Low, I., Forsberg, E.C., et al. C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42 (2015), 665–678.
26. Hollingworth, P., Harold, D., Sims, R., Gerrish, A., Lambert, J.-C., Carrasquillo, M.M., Abraham, R., Hamshere, M.L., Pahwa, J.S., Moskvina, V., et al. Alzheimer's Disease Neuroimaging Initiative CHARGE consortium, EADI1 consortium. Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer's disease. Nat. Genet. 43 (2011), 429–435.
27. Huang, Y., Xu, Z., Xiong, S., Sun, F., Qin, G., Hu, G., Wang, J., Zhao, L., Liang, Y.-X., Wu, T., et al. Repopulated microglia are solely derived from the proliferation of residual microglia after acute depletion. Nat. Neurosci. 21 (2018), 530–540.
28. Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E.G., Wieghofer, P., Heinrich, A., Riemke, P., Hölscher, C., et al. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 16 (2013), 273–280.
29. Krasemann, S., Madore, C., Cialic, R., Baufeld, C., Calcagno, N., El Fatimy, R., Beckers, L., O'Loughlin, E., Xu, Y., Fanek, Z., et al. The TREM2-APOE pathway drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity 47 (2017), 566–581.e9.
30. Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., Amit, I., Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
31. Li, Q., Barres, B.A., Microglia and macrophages in brain homeostasis and disease. Nat. Rev. Immunol. 18 (2018), 225–242.
32. Li, J., Chen, K., Zhu, L., Pollard, J.W., Conditional deletion of the colony stimulating factor-1 receptor (c-fms proto-oncogene) in mice. Genesis 44 (2006), 328–335.
33. Liddelow, S.A., Guttenplan, K.A., Clarke, L.E., Bennett, F.C., Bohlen, C.J., Schirmer, L., Bennett, M.L., Münch, A.E., Chung, W.-S., Peterson, T.C., et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541 (2017), 481–487.
34. Mass, E., Ballesteros, I., Farlik, M., Halbritter, F., Günther, P., Crozet, L., Jacome-Galarza, C.E., Händler, K., Klughammer, J., Kobayashi, Y., et al. Specification of tissue-resident macrophages during organogenesis. Science, 353, 2016, aaf4238.
35. Matcovitch-Natan, O., Winter, D.R., Giladi, A., Vargas Aguilar, S., Spinrad, A., Sarrazin, S., Ben-Yehuda, H., David, E., Zelada González, F., Perrin, P., et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science, 353, 2016, aad8670.
36. Metsalu, T., Vilo, J., ClustVis: a web tool for visualizing clustering of multivariate data using principal component analysis and heatmap. Nucleic Acids Res., 43(W1), 2015 W566–70.
37. Mildner, A., Schmidt, H., Nitsche, M., Merkler, D., Hanisch, U.-K., Mack, M., Heikenwalder, M., Brück, W., Priller, J., Prinz, M., Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat. Neurosci. 10 (2007), 1544–1553.
38. Obermeier, B., Daneman, R., Ransohoff, R.M., Development, maintenance and disruption of the blood-brain barrier. Nat. Med. 19 (2013), 1584–1596.
39. Ohgidani, M., Kato, T.A., Setoyama, D., Sagata, N., Hashimoto, R., Shigenobu, K., Yoshida, T., Hayakawa, K., Shimokawa, N., Miura, D., et al. Direct induction of ramified microglia-like cells from human monocytes: dynamic microglial dysfunction in Nasu-Hakola disease. Sci. Rep., 4, 2014, 4957.
40. Priller, J., Flügel, A., Wehner, T., Boentert, M., Haas, C.A., Prinz, M., Fernández-Klett, F., Prass, K., Bechmann, I., de Boer, B.A., et al. Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat. Med. 7 (2001), 1356–1361.
41. Rathinam, C., Poueymirou, W.T., Rojas, J., Murphy, A.J., Valenzuela, D.M., Yancopoulos, G.D., Rongvaux, A., Eynon, E.E., Manz, M.G., Flavell, R.A., Efficient differentiation and function of human macrophages in humanized CSF-1 mice. Blood 118 (2011), 3119–3128.
42. Robinson, M.D., McCarthy, D.J., Smyth, G.K., edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 (2010), 139–140.
43. Saederup, N., Cardona, A.E., Croft, K., Mizutani, M., Cotleur, A.C., Tsou, C.-L., Ransohoff, R.M., Charo, I.F., Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS ONE, 5, 2010, e13693.
44. Sagar, D., Singh, N.P., Ginwala, R., Huang, X., Philip, R., Nagarkatti, M., Nagarkatti, P., Neumann, K., Ruland, J., Andrews, A.M., et al. Antibody blockade of CLEC12A delays EAE onset and attenuates disease severity by impairing myeloid cell CNS infiltration and restoring positive immunity. Sci. Rep., 7, 2017, 2707.
45. Salter, M.W., Stevens, B., Microglia emerge as central players in brain disease. Nat. Med. 23 (2017), 1018–1027.
46. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
47. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9 (2012), 671–675.
48. Schulz, C., Gomez Perdiguero, E., Chorro, L., Szabo-Rogers, H., Cagnard, N., Kierdorf, K., Prinz, M., Wu, B., Jacobsen, S.E.W., Pollard, J.W., et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336 (2012), 86–90.
49. Scott, C.L., Zheng, F., De Baetselier, P., Martens, L., Saeys, Y., De Prijck, S., Lippens, S., Abels, C., Schoonooghe, S., Raes, G., et al. Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells. Nat. Commun., 7, 2016, 10321.
50. Sellgren, C.M., Sheridan, S.D., Gracias, J., Xuan, D., Fu, T., Perlis, R.H., Patient-specific models of microglia-mediated engulfment of synapses and neural progenitors. Mol. Psychiatry 22 (2017), 170–177.
51. Shi, Y., Yamada, K., Liddelow, S.A., Smith, S.T., Zhao, L., Luo, W., Tsai, R.M., Spina, S., Grinberg, L.T., Rojas, J.C., et al., Alzheimer's Disease Neuroimaging Initiative. ApoE4 markedly exacerbates tau-mediated neurodegeneration in a mouse model of tauopathy. Nature 549 (2017), 523–527.
52. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
53. Suzuki, R., Shimodaira, H., pvclust: hierarchical clustering with p-values via multiscale Bootstrap resampling. R package version 1.2-2, 2014 https://cran.r-project.org/web/packages/pvclust/index.html.
54. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., Pachter, L., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7 (2012), 562–578.
55. van de Laar, L., Saelens, W., De Prijck, S., Martens, L., Scott, C.L., Van Isterdael, G., Hoffmann, E., Beyaert, R., Saeys, Y., Lambrecht, B.N., Guilliams, M., Yolk sac macrophages, fetal liver, and adult monocytes can colonize an empty niche and develop into functional tissue-resident macrophages. Immunity 44 (2016), 755–768.
56. Varvel, N.H., Grathwohl, S.A., Baumann, F., Liebig, C., Bosch, A., Brawek, B., Thal, D.R., Charo, I.F., Heppner, F.L., Aguzzi, A., et al. Microglial repopulation model reveals a robust homeostatic process for replacing CNS myeloid cells. Proc. Natl. Acad. Sci. USA 109 (2012), 18150–18155.
57. Wang, Y., Cella, M., Mallinson, K., Ulrich, J.D., Young, K.L., Robinette, M.L., Gilfillan, S., Krishnan, G.M., Sudhakar, S., Zinselmeyer, B.H., et al. TREM2 lipid sensing sustains the microglial response in an Alzheimer's disease model. Cell 160 (2015), 1061–1071.
58. Wong, K., Noubade, R., Manzanillo, P., Ota, N., Foreman, O., Hackney, J.A., Friedman, B.A., Pappu, R., Scearce-Levie, K., Ouyang, W., Mice deficient in NRROS show abnormal microglial development and neurological disorders. Nat. Immunol. 18 (2017), 633–641.
59. Zhang, Y., Chen, K., Sloan, S.A., Bennett, M.L., Scholze, A.R., O'Keeffe, S., Phatnani, H.P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34 (2014), 11929–11947.