Local Cues Establish and Maintain Region-Specific Phenotypes of Basal Ganglia Microglia

Neuron

Volumn 95, Issue 2, 2017, Pages 341-356.e6

  De Biase, Lindsay M ^a   Schuebel, Kornel E ^b   Fusfeld, Zachary H ^a   Jair, Kamwing ^b   Hawes, Isobel A ^a   Cimbro, Raffaello ^c   Zhang, Hai Ying ^a   Liu, Qing Rong ^a   Shen, Hui ^a   Xi, Zheng Xiong ^a   Goldman, David ^b   Bonci, Antonello ^a,c  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

density; development; electrophysiology; heterogeneity; microglia; morphology; nucleus accumbens; RNA sequencing; substantia nigra; ventral tegmental area

Indexed keywords

TRANSCRIPTOME;

ABLATION THERAPY; ARTICLE; ASSOCIATION; BASAL GANGLION; CELL FUNCTION; CELL MEMBRANE; CELL NUCLEUS; CELL STRUCTURE; LYSOSOME; MICROGLIA; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; TRANSCRIPTOMICS; ANIMAL; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; BASAL GANGLIA; CUES; MICE, TRANSGENIC; MICROGLIA; NEURONS; PHENOTYPE;

EID: 85021832099     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2017.06.020     Document Type: Article

References (64)

1. Albin, R.L., Basal ganglia neurotoxins. Neurol. Clin. 18 (2000), 665–680.
2. Appelqvist, H., Wäster, P., Kågedal, K., Öllinger, K., The lysosome: from waste bag to potential therapeutic target. J. Mol. Cell Biol. 5 (2013), 214–226.
3. Arnoux, I., Hoshiko, M., Mandavy, L., Avignone, E., Yamamoto, N., Audinat, E., Adaptive phenotype of microglial cells during the normal postnatal development of the somatosensory “Barrel” cortex. Glia 61 (2013), 1582–1594.
4. Avignone, E., Ulmann, L., Levavasseur, F., Rassendren, F., Audinat, E., Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J. Neurosci. 28 (2008), 9133–9144.
5. Bayraktar, O.A., Fuentealba, L.C., Alvarez-Buylla, A., Rowitch, D.H., Astrocyte development and heterogeneity. Cold Spring Harb. Perspect. Biol., 7, 2014, a020362.
6. Berger, J.R., Arendt, G., HIV dementia: the role of the basal ganglia and dopaminergic systems. J. Psychopharmacol. (Oxford) 14 (2000), 214–221.
7. Bergles, D.E., Richardson, W.D., Oligodendrocyte Development and Plasticity. Cold Spring Harb. Perspect. Biol., 8, 2015, a020453.
8. Björklund, A., Dunnett, S.B., Dopamine neuron systems in the brain: an update. Trends Neurosci. 30 (2007), 194–202.
9. Boucsein, C., Kettenmann, H., Nolte, C., Electrophysiological properties of microglial cells in normal and pathologic rat brain slices. Eur. J. Neurosci. 12 (2000), 2049–2058.
10. Boucsein, C., Zacharias, R., Färber, K., Pavlovic, S., Hanisch, U.K., Kettenmann, H., Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro. Eur. J. Neurosci. 17 (2003), 2267–2276.
11. Brix, K., Lysosomal Proteases: Revival of the Sleeping Beauty. Saftig, P., (eds.) Lysosomes, 2005, Springer Science + Buisness Media, 50–59.
12. Butovsky, O., Jedrychowski, M.P., Moore, C.S., Cialic, R., Lanser, A.J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P.M., Doykan, C.E., et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 17 (2014), 131–143.
13. Chiu, I.M., Morimoto, E.T., 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.
14. Crawford, A.H., Tripathi, R.B., Richardson, W.D., Franklin, R.J., Developmental origin of oligodendrocyte lineage cells determines response to demyelination and susceptibility to age-associated functional decline. Cell Rep., 2016, 10.1016/j.celrep.2016.03.069 Published online April 13, 2016.
15. Davalos, D., Grutzendler, J., Yang, G., Kim, J.V., Zuo, Y., Jung, S., Littman, D.R., Dustin, M.L., Gan, W.B., ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8 (2005), 752–758.
16. de Haas, A.H., Boddeke, H.W., Biber, K., Region-specific expression of immunoregulatory proteins on microglia in the healthy CNS. Glia 56 (2008), 888–894.
17. Elmore, M.R., Najafi, A.R., Koike, M.A., Dagher, N.N., Spangenberg, E.E., Rice, R.A., Kitazawa, M., Matusow, B., Nguyen, H., West, B.L., Green, K.N., Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82 (2014), 380–397.
18. Elmore, M.R., Lee, R.J., West, B.L., Green, K.N., Characterizing newly repopulated microglia in the adult mouse: impacts on animal behavior, cell morphology, and neuroinflammation. PLoS ONE, 10, 2015, e0122912.
19. Ferguson, S.M., Beyond indigestion: emerging roles for lysosome-based signaling in human disease. Curr. Opin. Cell Biol. 35 (2015), 59–68.
20. − homeostasis. Nat. Neurosci. 16 (2013), 183–192.
21. Garden, G.A., Epigenetics and the modulation of neuroinflammation. Neurotherapeutics 10 (2013), 782–788.
22. Ginhoux, F., Prinz, M., Origin of microglia: current concepts and past controversies. Cold Spring Harb. Perspect. Biol., 7, 2015, a020537.
23. Ginhoux, F., Lim, S., Hoeffel, G., Low, D., Huber, T., Origin and differentiation of microglia. Front. Cell. Neurosci., 7, 2013, 45.
24. González-Hernández, T., Cruz-Muros, I., Afonso-Oramas, D., Salas-Hernandez, J., Castro-Hernandez, J., Vulnerability of mesostriatal dopaminergic neurons in Parkinson's disease. Front. Neuroanat., 4, 2010, 140.
25. Gowrishankar, S., Yuan, P., Wu, Y., Schrag, M., Paradise, S., Grutzendler, J., De Camilli, P., Ferguson, S.M., Massive accumulation of luminal protease-deficient axonal lysosomes at Alzheimer's disease amyloid plaques. Proc. Natl. Acad. Sci. USA 112 (2015), E3699–E3708.
26. Grabert, K., Michoel, T., Karavolos, M.H., Clohisey, S., Baillie, J.K., Stevens, M.P., Freeman, T.C., Summers, K.M., McColl, B.W., Microglial brain region-dependent diversity and selective regional sensitivities to aging. Nat. Neurosci. 19 (2016), 504–516.
27. Graybiel, A.M., Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31 (2008), 359–387.
28. Hanisch, U.K., Kettenmann, H., Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10 (2007), 1387–1394.
29. Hegde, A.N., Mohan, S., Lath, N., Lim, C.C., Differential diagnosis for bilateral abnormalities of the basal ganglia and thalamus. Radiographics 31 (2011), 5–30.
30. 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.
31. Hong, S., Beja-Glasser, V.F., Nfonoyim, B.M., Frouin, A., Li, S., Ramakrishnan, S., Merry, K.M., Shi, Q., Rosenthal, A., Barres, B.A., et al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science 352 (2016), 712–716.
32. Hughes, E.G., Kang, S.H., Fukaya, M., Bergles, D.E., Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 16 (2013), 668–676.
33. Joers, V., Tansey, M.G., Mulas, G., Carta, A.R., Microglial phenotypes in Parkinson's disease and animal models of the disease. Prog. Neurobiol., 2016, 10.1016/j.pneurobio.2016.04.006 Published online April 20, 2016.
34. Johnson, D.E., Ostrowski, P., Jaumouillé, V., Grinstein, S., The position of lysosomes within the cell determines their luminal pH. J. Cell Biol. 212 (2016), 677–692.
35. Kauer, J.A., Malenka, R.C., Synaptic plasticity and addiction. Nat. Rev. Neurosci. 8 (2007), 844–858.
36. Kettenmann, H., Hanisch, U.K., Noda, M., Verkhratsky, A., Physiology of microglia. Physiol. Rev. 91 (2011), 461–553.
37. Lawson, L.J., Perry, V.H., Dri, P., Gordon, S., Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39 (1990), 151–170.
38. Lewitus, G.M., Konefal, S.C., Greenhalgh, A.D., Pribiag, H., Augereau, K., Stellwagen, D., Microglial TNF-α Suppresses Cocaine-Induced Plasticity and Behavioral Sensitization. Neuron 90 (2016), 483–491.
39. 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.
40. Liu, Q.R., Rubio, F.J., Bossert, J.M., Marchant, N.J., Fanous, S., Hou, X., Shaham, Y., Hope, B.T., Detection of molecular alterations in methamphetamine-activated Fos-expressing neurons from a single rat dorsal striatum using fluorescence-activated cell sorting (FACS). J. Neurochem. 128 (2014), 173–185.
41. Long-Smith, C.M., Sullivan, A.M., Nolan, Y.M., The influence of microglia on the pathogenesis of Parkinson's disease. Prog. Neurobiol. 89 (2009), 277–287.
42. Lyons, S.A., Pastor, A., Ohlemeyer, C., Kann, O., Wiegand, F., Prass, K., Knapp, F., Kettenmann, H., Dirnagl, U., Distinct physiologic properties of microglia and blood-borne cells in rat brain slices after permanent middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 20 (2000), 1537–1549.
43. Marín, O., Developmental timing and critical windows for the treatment of psychiatric disorders. Nat. Med. 22 (2016), 1229–1238.
44. Marinov, G.K., Williams, B.A., McCue, K., Schroth, G.P., Gertz, J., Myers, R.M., Wold, B.J., From single-cell to cell-pool transcriptomes: stochasticity in gene expression and RNA splicing. Genome Res. 24 (2014), 496–510.
45. 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.
46. Mattapallil, M.J., Wawrousek, E.F., Chan, C.C., Zhao, H., Roychoudhury, J., Ferguson, T.A., Caspi, R.R., The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Invest. Ophthalmol. Vis. Sci. 53 (2012), 2921–2927.
47. Mufaddel, A.A., Al-Hassani, G.A., Familial idiopathic basal ganglia calcification (Fahr's disease). Neurosciences (Riyadh) 19 (2014), 171–177.
48. Nelson, A.B., Kreitzer, A.C., Reassessing models of basal ganglia function and dysfunction. Annu. Rev. Neurosci. 37 (2014), 117–135.
49. Nimmerjahn, A., Kirchhoff, F., Helmchen, F., Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308 (2005), 1314–1318.
50. Parkhurst, C.N., Yang, G., Ninan, I., Savas, J.N., Yates, J.R. 3rd, Lafaille, J.J., Hempstead, B.L., Littman, D.R., Gan, W.B., Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155 (2013), 1596–1609.
51. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A., Bessis, A., Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. USA 109 (2012), E197–E205.
52. Pribiag, H., Stellwagen, D., Neuroimmune regulation of homeostatic synaptic plasticity. Neuropharmacology 78 (2014), 13–22.
53. Ransohoff, R.M., Perry, V.H., Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27 (2009), 119–145.
54. Reemst, K., Noctor, S.C., Lucassen, P.J., Hol, E.M., The Indispensable Roles of Microglia and Astrocytes during Brain Development. Front. Hum. Neurosci., 10, 2016, 566.
55. 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.
56. Schafer, D.P., Lehrman, E.K., Kautzman, A.G., Koyama, R., Mardinly, A.R., Yamasaki, R., Ransohoff, R.M., Greenberg, M.E., Barres, B.A., Stevens, B., Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74 (2012), 691–705.
57. Sharaf, A., Krieglstein, K., Spittau, B., Distribution of microglia in the postnatal murine nigrostriatal system. Cell Tissue Res. 351 (2013), 373–382.
58. Sipe, G.O., Lowery, R.L., Tremblay, M.E., Kelly, E.A., Lamantia, C.E., Majewska, A.K., Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex. Nat. Commun., 7, 2016, 10905.
59. Tremblay, M.E., Lowery, R.L., Majewska, A.K., Microglial interactions with synapses are modulated by visual experience. PLoS Biol., 8, 2010, e1000527.
60. Wills, T.J., Muessig, L., Cacucci, F., The development of spatial behaviour and the hippocampal neural representation of space. Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 2013, 20130409.
61. Yang, T.T., Lin, C., Hsu, C.T., Wang, T.F., Ke, F.Y., Kuo, Y.M., Differential distribution and activation of microglia in the brain of male C57BL/6J mice. Brain Struct. Funct. 218 (2013), 1051–1060.
62. 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.
63. Zhou, F.M., Lee, C.R., Intrinsic and integrative properties of substantia nigra pars reticulata neurons. Neuroscience 198 (2011), 69–94.
64. Zuchero, J.B., Barres, B.A., Glia in mammalian development and disease. Development 142 (2015), 3805–3809.