Abstract
Hevin, also known as SPARC-like 1, is a member of the secreted protein acidic and rich in cysteine family of matricellular proteins, which has been implicated in neuronal migration and synaptogenesis during development. Unlike previously characterized matricellular proteins, hevin remains strongly expressed in the adult brain in both astrocytes and neurons, but its precise pattern of expression is unknown. The present study provides the first systematic description of hevin mRNA distribution in the adult mouse brain. Using isotopic in situ hybridization, we showed that hevin is strongly expressed in the cortex, hippocampus, basal ganglia complex, diverse thalamic nuclei and brainstem motor nuclei. To identify the cellular phenotype of hevin-expressing cells, we used double fluorescent in situ hybridization in mouse and human adult brains. In the mouse, hevin mRNA was found in the majority of astrocytes but also in specific neuronal populations. Hevin was expressed in almost all parvalbumin-positive projection neurons and local interneurons. In addition, hevin mRNA was found in: (1) subsets of other inhibitory GABAergic neuronal subtypes, including calbindin, cholecystokinin, neuropeptide Y, and somatostatin-positive neurons; (2) subsets of glutamatergic neurons, identified by the expression of the vesicular glutamate transporters VGLUT1 and VGLUT2; and (3) the majority of cholinergic neurons from motor nuclei. Hevin mRNA was absent from all monoaminergic neurons and cholinergic neurons of the ascending pathway. A similar cellular profile of expression was observed in human, with expression of hevin in parvalbumin interneurons and astrocytes in the cortex and caudate nucleus as well as in cortical glutamatergic neurons. Furthermore, hevin transcript was enriched in ribosomes of astrocytes and parvalbumin neurons providing a direct evidence of hevin mRNAs translation in these cell types. This study reveals the unique and complex expression profile of the matricellular protein hevin in the adult brain. This distribution is compatible with a role of hevin in astrocytic-mediated adult synaptic plasticity and in the regulation of network activity mediated by parvalbumin-expressing neurons.
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Abbreviations
- 3V:
-
3rd ventricle
- 4V:
-
4th ventricle
- AD:
-
Anterodorsal thalamic nucleus
- ac:
-
Anterior commissure
- AD:
-
Anterodorsal thalamic nucleus
- AM:
-
Anteromedial thalamic nucleus
- Amb:
-
Ambiguus nucleus
- AON:
-
Anterior olfactory nucleus
- APT:
-
Anterior pretectal nucleus
- AVL:
-
Anteroventral thalamic nucleus, lateral part
- AVM:
-
Anteroventral thalamic nucleus, medial part
- Berg.:
-
Bergman glia
- BLA:
-
Basolateral amygdala
- CA1-3:
-
Cornu ammonis
- Cb:
-
Cerebellum
- cc:
-
Corpus callosum
- ChP:
-
Choroid plexus
- Cl:
-
Claustrum
- CPu:
-
Caudate putamen
- Cx:
-
Cortex
- DBB:
-
Diagonal band of Broca
- DG:
-
Dentate gyrus
- DLG:
-
Dorsal lateral geniculate nucleus
- DM:
-
Dorsomedial hypothalamic nucleus
- DRc:
-
Dorsal raphe nucleus caudal part
- GCL:
-
Granule cell layer
- Gl:
-
Glomerular layer
- HDB:
-
Nucleus of the horizontal limb of the diagonal band
- Hipp:
-
Hippocampus
- IC:
-
Inferior colliculus
- ic:
-
Internal capsule
- IPN:
-
Interpeduncular nucleus
- LDDM:
-
Laterodorsal thalamic nucleus, dorsomedial part
- LDTg:
-
Laterodorsal tegmental nucleus
- LGP:
-
Lateral globus pallidus
- LH:
-
Lateral hypothalamic area
- LHb:
-
Lateral habenula nucleus
- LP:
-
Lateral posterior thalamic nucleus
- LS:
-
Lateral septal nucleus
- LSd:
-
Lateral septal nucleus, dorsal part
- LV:
-
Lateral ventricle
- MCPO:
-
Magnocellular preoptic nucleus
- MD:
-
Mediodorsal thalamic nucleus
- MGP:
-
Medial globus pallidus
- Mi:
-
Mitral cell layer of the olfactory bulb
- ML:
-
Molecular layer
- Mol:
-
Molecular layer of the dentate gyrus
- MPO:
-
Medial preoptic nucleus
- MRc:
-
Median raphe nucleus caudal part
- MS:
-
Medial septum
- Mve:
-
Medial vestibular nucleus
- Or:
-
Oriens layer of the hippocampus
- PAG:
-
Periaqueductal gray
- PCL:
-
Purkinje cell layer
- Pn:
-
Pontine nucleus
- Po:
-
Posterior thalamic nuclear group
- PrS:
-
Presubiculum
- PVA:
-
Paraventricular thalamic nucleus, anterior part
- Rad:
-
Stratum radiatum of the hippocampus
- Re:
-
Reuniens thalamic nucleus
- RMC:
-
Red nucleus, magnocellular part
- RN:
-
Red nucleus
- Rt:
-
Reticular thalamic nucleus
- SC:
-
Superior colliculus
- SNc:
-
Substantia nigra pars compacta
- SNr:
-
Substantia nigra pars reticulata
- Sp5:
-
Spinal trigeminal nucleus
- Tg:
-
Tegmental nucleus
- VA:
-
Ventral anterior thalamic nucleus
- Vest:
-
Vestibular nucleus
- VP:
-
Ventral pallidum
- VPM:
-
Ventral posteromedial thalamic nucleus
- VTA:
-
Ventral tegmental area
- ZI:
-
Zona incerta
- III:
-
Oculomotor nucleus
- V:
-
Motor trigeminal nucleus
- VI:
-
Abducens nucleus
- VII:
-
Facial nucleus
- VIII:
-
Cochlear nucleus
- IX:
-
Glossopharyngeal nucleus
- X:
-
Dorsal motor nucleus of vagus
- XII:
-
Hypoglossal nucleus
References
Alberi L, Lintas A, Kretz R, Schwaller B, Villa AE (2013) The calcium-binding protein parvalbumin modulates the firing 1 properties of the reticular thalamic nucleus bursting neurons. J Neurophysiol 109:2827–2841. https://doi.org/10.1152/jn.00375.2012
Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1–14. https://doi.org/10.1002/1098-1136(200010)32:1%3C1::AID-GLIA10%3E3.0.CO;2-W
Apazoglou K, Farley S, Gorgievski V et al (2018) Antidepressive effects of targeting ELK-1 signal transduction. Nat Med 24:591–597. https://doi.org/10.1038/s41591-018-0011-0
Armstrong DM, Saper CB, Levey AI, Wainer BH, Terry RD (1983) Distribution of cholinergic neurons in rat brain: demonstrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 216:53–68. https://doi.org/10.1002/cne.902160106
Bernardinelli Y, Nikonenko I, Muller D (2014) Structural plasticity: mechanisms and contribution to developmental psychiatric disorders. Front Neuroanat 8:123. https://doi.org/10.3389/fnana.2014.00123
Blakely PK, Hussain S, Carlin LE, Irani DN (2015) Astrocyte matricellular proteins that control excitatory synaptogenesis are regulated by inflammatory cytokines and correlate with paralysis severity during experimental autoimmune encephalomyelitis. Front Neurosci 9:344. https://doi.org/10.3389/fnins.2015.00344
Bornstein P (1995) Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 130:503–506. https://doi.org/10.1083/jcb.130.3.503
Braak H, Del Tredici K (2008) Cortico-basal ganglia-cortical circuitry in Parkinson’s disease reconsidered. Exp Neurol 212:226–229. https://doi.org/10.1016/j.expneurol.2008.04.001
Brekken RA, Sage EH (2000) SPARC, a matricellular protein: at the crossroads of cell-matrix. Matrix Biol 19:569–580
Cahoy JD, Emery B, Kaushal A et al (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278. https://doi.org/10.1523/JNEUROSCI.4178-07.2008
Celio MR (1990) Calbindin D-28 k and parvalbumin in the rat nervous system. Neuroscience 35:375–475. https://doi.org/10.1016/0306-4522(90)90091-H
Chazalon M, Dumas S, Bernard JF et al (2018) The GABAergic Gudden’s dorsal tegmental nucleus: a new relay for serotonergic regulation of sleep-wake behavior in the mouse. Neuropharmacology 138:315–330. https://doi.org/10.1016/j.neuropharm.2018.06.014
Christoffel DJ, Golden SA, Dumitriu D et al (2011) IkappaB kinase regulates social defeat stress-induced synaptic and behavioral plasticity. J Neurosci 31:314–321. https://doi.org/10.1523/JNEUROSCI.4763-10.2011
Christoffel DJ, Golden SA, Walsh JJ et al (2015) Excitatory transmission at thalamo-striatal synapses mediates susceptibility to social stress. Nat Neurosci 18:962–964. https://doi.org/10.1038/nn.4034
Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O’Donohue TL (1985) The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15:1159–1181. https://doi.org/10.1016/0306-4522(85)90260-X
Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR, Sudhof TC (2007) Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54:919–931. https://doi.org/10.1016/j.neuron.2007.05.029
Clemente-Perez A, Makinson SR, Higashikubo B et al (2017) Distinct thalamic reticular cell types differentially modulate normal and pathological cortical rhythms. Cell Rep 19:2130–2142. https://doi.org/10.1016/j.celrep.2017.05.044
Cui Q, Pitt JE, Pamukcu A et al (2016) Blunted mGluR activation disinhibits striatopallidal transmission in parkinsonian mice. Cell Rep 17:2431–2444. https://doi.org/10.1016/j.celrep.2016.10.087
Emsley JG, Macklis JD (2006) Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol 2:175–186. https://doi.org/10.1017/S1740925X06000202
Erdozain AM, De Gois S, Bernard V et al (2018) Structural and functional characterization of the interaction of snapin with the dopamine transporter: differential modulation of psychostimulant actions. Neuropsychopharmacology 43:1041–1051. https://doi.org/10.1038/npp.2017.217
Eroglu C (2009) The role of astrocyte-secreted matricellular proteins in central nervous system development and function. J Cell Commun Signal 3:167–176. https://doi.org/10.1007/s12079-009-0078-y
Girard JP, Springer TA (1995) Cloning from purified high endothelial venule cells of hevin, a close relative of the antiadhesive extracellular matrix protein SPARC. Immunity 2:113–123. https://doi.org/10.1016/1074-7613(95)90083-7
Girard JP, Springer TA (1996) Modulation of endothelial cell adhesion by hevin, an acidic protein associated with high endothelial venules. J Biol Chem 271:4511–4517. https://doi.org/10.1074/jbc.271.8.4511
Gongidi V, Ring C, Moody M, Brekken R, Sage EH, Rakic P, Anton ES (2004) SPARC-like 1 regulates the terminal phase of radial glia-guided migration in the cerebral cortex. Neuron 41:57–69
Hambrock HO, Nitsche DP, Hansen U, Bruckner P, Paulsson M, Maurer P, Hartmann U (2003) SC1/hevin. An extracellular calcium-modulated protein that binds collagen I. J Biol Chem 278:11351–11358. https://doi.org/10.1074/jbc.M212291200
Hammack BN, Fung KY, Hunsucker SW, Duncan MW, Burgoon MP, Owens GP, Gilden DH (2004) Proteomic analysis of multiple sclerosis cerebrospinal fluid. Mult Scler 10:245–260. https://doi.org/10.1191/1352458504ms1023oa
Hashimoto N, Sato T, Yajima T et al (2016) SPARCL1-containing neurons in the human brainstem and sensory ganglion. Somatosens Mot Res 33:112–117. https://doi.org/10.1080/08990220.2016.1197115
Herculano-Houzel S (2014) The glia/neuron ratio: how it varies uniformly across brain structures and species and what that means for brain physiology and evolution. Glia 62:1377–1391. https://doi.org/10.1002/glia.22683
Herzog E, Bellenchi GC, Gras C et al (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21:RC181
Huntley GW (2012) Synaptic circuit remodelling by matrix metalloproteinases in health and disease. Nat Rev Neurosci 13:743–757. https://doi.org/10.1038/nrn3320
Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:218–223. https://doi.org/10.1126/science.1168978
Johansson O, Hokfelt T, Elde RP (1984) Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13:265–339. https://doi.org/10.1016/0891-0618(91)90001-S
Johnston IG, Paladino T, Gurd JW, Brown IR (1990) Molecular cloning of SC1: a putative brain extracellular matrix glycoprotein showing partial similarity to osteonectin/BM40/SPARC. Neuron 4:165–176
Jones EV, Bernardinelli Y, Tse YC, Chierzi S, Wong TP, Murai KK (2011) Astrocytes control glutamate receptor levels at developing synapses through SPARC-beta-integrin interactions. J Neurosci 31:4154–4165. https://doi.org/10.1523/JNEUROSCI.4757-10.2011
Kucukdereli H, Allen NJ, Lee AT et al (2011) Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc Natl Acad Sci USA 108:E440–E449. https://doi.org/10.1073/pnas.1104977108
Lively S, Brown IR (2008a) Extracellular matrix protein SC1/hevin in the hippocampus following pilocarpine-induced status epilepticus. J Neurochem 107:1335–1346. https://doi.org/10.1111/j.1471-4159.2008.05696.x
Lively S, Brown IR (2008b) The extracellular matrix protein SC1/hevin localizes to excitatory synapses following status epilepticus in the rat lithium-pilocarpine seizure model. J Neurosci Res 86:2895–2905. https://doi.org/10.1002/jnr.21735
Lively S, Brown IR (2008c) Localization of the extracellular matrix protein SC1 coincides with synaptogenesis during rat postnatal development. Neurochem Res 33:1692–1700. https://doi.org/10.1007/s11064-008-9606-z
Lively S, Moxon-Emre I, Schlichter LC (2011) SC1/hevin and reactive gliosis after transient ischemic stroke in young and aged rats. J Neuropathol Exp Neurol 70:913–929. https://doi.org/10.1097/NEN.0b013e318231151e
Lloyd-Burton S, Roskams AJ (2012) SPARC-like 1 (SC1) is a diversely expressed and developmentally regulated matricellular protein that does not compensate for the absence of SPARC in the CNS. J Comp Neurol 520:2575–2590. https://doi.org/10.1002/cne.23029
Markiewicz I, Lukomska B (2006) The role of astrocytes in the physiology and pathology of the central nervous system. Acta Neurobiol Exp (Wars) 66:343–358
McKinnon PJ, McLaughlin SK, Kapsetaki M, Margolskee RF (2000) Extracellular matrix-associated protein Sc1 is not essential for mouse development. Mol Cell Biol 20:656–660. https://doi.org/10.1128/MCB.20.2.656-660.2000
Mendez P, Bacci A (2011) Assortment of GABAergic plasticity in the cortical interneuron melting pot. Neural Plast 2011:976856. https://doi.org/10.1155/2011/976856
Mendis DB, Malaval L, Brown IR (1995) SPARC, an extracellular matrix glycoprotein containing the follistatin module, is expressed by astrocytes in synaptic enriched regions of the adult brain. Brain Res 676:69–79
Mendis DB, Shahin S, Gurd JW, Brown IR (1996) SC1, a SPARC-related glycoprotein, exhibits features of an ECM component in the developing and adult brain. Brain Res 713:53–63
Mendis DB, Ivy GO, Brown IR (2000) Induction of SC1 mRNA encoding a brain extracellular matrix glycoprotein related to SPARC following lesioning of the adult rat forebrain. Neurochem Res 25:1637–1644
Morel L, Chiang MSR, Higashimori H et al (2017) Molecular and Functional Properties of Regional Astrocytes in the Adult Brain. J Neurosci 37:8706–8717. https://doi.org/10.1523/JNEUROSCI.3956-16.2017
Mothe AJ, Brown IR (2002) Effect of hyperthermia on the transport of mRNA encoding the extracellular matrix glycoprotein SC1 into Bergmann glial cell processes. Brain Res 931:146–158. https://doi.org/10.1016/S0006-8993(02)02270-9
Murphy-Ullrich JE, Sage EH (2014) Revisiting the matricellular concept. Matrix Biol 37:1–14. https://doi.org/10.1016/j.matbio.2014.07.005
Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26:523–530. https://doi.org/10.1016/j.tins.2003.08.008
Nishida H, Okabe S (2007) Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 27:331–340. https://doi.org/10.1523/JNEUROSCI.4466-06.2007
Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SH (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125:775–784. https://doi.org/10.1016/j.cell.2006.02.051
Paxinos G, Franklin KBG (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic, San Diego
Polepalli JS, Wu H, Goswami D, Halpern CH, Sudhof TC, Malenka RC (2017) Modulation of excitation on parvalbumin interneurons by neuroligin-3 regulates the hippocampal network. Nat Neurosci 20:219–229. https://doi.org/10.1038/nn.4471
Risher WC, Patel S, Kim IH et al (2014) Astrocytes refine cortical connectivity at dendritic spines. Elife. https://doi.org/10.7554/eLife.04047
Rossier J, Bernard A, Cabungcal JH et al (2015) Cortical fast-spiking parvalbumin interneurons enwrapped in the perineuronal net express the metallopeptidases Adamts8, Adamts15 and Neprilysin. Mol Psychiatry 20:154–161. https://doi.org/10.1038/mp.2014.162
Sage EH, Bornstein P (1991) Extracellular proteins that modulate cell-matrix interactions—sparc, tenascin, and thrombospondin. J Biol Chem 266:14831–14834
Savasta M, Palacios JM, Mengod G (1988) Regional localization of the mRNA coding for the neuropeptide cholecystokinin in the rat brain studied by in situ hybridization. Neurosci Lett 93:132–138. https://doi.org/10.1016/0169-328X(90)90086-S
Schmitt A, Asan E, Puschel B, Kugler P (1997) Cellular and regional distribution of the glutamate transporter GLAST in the CNS of rats: nonradioactive in situ hybridization and comparative immunocytochemistry. J Neurosci 17:1–10
Schweizer N, Pupe S, Arvidsson E et al (2014) Limiting glutamate transmission in a Vglut2-expressing subpopulation of the subthalamic nucleus is sufficient to cause hyperlocomotion. Proc Natl Acad Sci USA 111:7837–7842. https://doi.org/10.1073/pnas.1323499111
Shigetomi E, Bushong EA, Haustein MD et al (2013) Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J Gen Physiol 141:633–647. https://doi.org/10.1085/jgp.201210949
Singh SK, Stogsdill JA, Pulimood NS et al (2016) Astrocytes assemble thalamocortical synapses by bridging NRX1alpha and NL1 via Hevin. Cell 164:183–196. https://doi.org/10.1016/j.cell.2015.11.034
Soderling JA, Reed MJ, Corsa A, Sage EH (1997) Cloning and expression of murine SC1, a gene product homologous to SPARC. J Histochem Cytochem 45:823–835. https://doi.org/10.1177/002215549704500607
Stobart JL, Ferrari KD, Barrett MJP, Gluck C, Stobart MJ, Zuend M, Weber B (2018) Cortical circuit activity evokes rapid astrocyte calcium signals on a similar timescale to neurons. Neuron 98:726–735 e724. https://doi.org/10.1016/j.neuron.2018.03.050
Sullivan MM, Puolakkainen PA, Barker TH, Funk SE, Sage EH (2008) Altered tissue repair in hevin-null mice: inhibition of fibroblast migration by a matricellular SPARC homolog. Wound Repair Regen 16:310–319. https://doi.org/10.1111/j.1524-475X.2008.00370.x
Tepper JM, Tecuapetla F, Koos T, Ibanez-Sandoval O (2010) Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4:150. https://doi.org/10.3389/fnana.2010.00150
Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19:6897–6906. https://doi.org/10.1523/JNEUROSCI.19-16-06897.1999
Vialou V, Balasse L, Dumas S, Giros B, Gautron S (2007) Neurochemical characterization of pathways expressing plasma membrane monoamine transporter in the rat brain. Neuroscience 144:616–622. https://doi.org/10.1016/j.neuroscience.2006.09.058
Vialou V, Robison AJ, Laplant QC et al (2010) DeltaFosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nat Neurosci 13:745–752. https://doi.org/10.1038/nn.2551
Viereckel T, Dumas S, Smith-Anttila CJ et al (2016) Midbrain gene screening identifies a new mesoaccumbal glutamatergic pathway and a marker for dopamine cells neuroprotected in Parkinson’s disease. Sci Rep 6:35203. https://doi.org/10.1038/srep35203
Vincent AJ, Lau PW, Roskams AJ (2008) SPARC is expressed by macroglia and microglia in the developing and mature nervous system. Dev Dyn 237:1449–1462. https://doi.org/10.1002/dvdy.21495
Weaver MS, Workman G, Cardo-Vila M, Arap W, Pasqualini R, Sage EH (2010) Processing of the matricellular protein hevin in mouse brain is dependent on ADAMTS4. J Biol Chem 285:5868–5877. https://doi.org/10.1074/jbc.M109.070318
Weaver M, Workman G, Schultz CR, Lemke N, Rempel SA, Sage EH (2011) Proteolysis of the matricellular protein hevin by matrix metalloproteinase-3 produces a SPARC-like fragment (SLF) associated with neovasculature in a murine glioma model. J Cell Biochem. https://doi.org/10.1002/jcb.23235
Yin GN, Lee HW, Cho JY, Suk K (2009) Neuronal pentraxin receptor in cerebrospinal fluid as a potential biomarker for neurodegenerative diseases. Brain Res 1265:158–170. https://doi.org/10.1016/j.brainres.2009.01.058
Zeisel A, Munoz-Manchado AB, Codeluppi S et al (2015) Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-sEq. Science 347:1138–1142. https://doi.org/10.1126/science.aaa1934
Zhurov V, Stead JD, Merali Z et al (2012) Molecular pathway reconstruction and analysis of disturbed gene expression in depressed individuals who died by suicide. PLoS One 7:e47581. https://doi.org/10.1371/journal.pone.0047581
Acknowledgements
This work was supported by funds from the Institut National de la Santé et de la Recherche Médicale (INSERM), Centre National de la Recherche Scientifique (CNRS), and Sorbonne Université, and by grants from the Brain & Behavior Research Foundation (NARSAD Young Investigator Award to VV, #17566), FP7 Marie Curie Actions Career Integration Grant (FP7-PEOPLE-2013-CIG #618807 to VV), Promouvoir l’Excellence de la Recherche à Sorbonne Université (PER-SU 2014 to VV), Agence Nationale de la Recherche (ANR JCJC 2015 Hevinsynapse to VV), the Basque Government (IT616/13 to JJM), Fondation pour la Recherche Médicale (DEQ20160334919 to EV), Fundación Vital (2018 to AME) and the European Foundation for Alcohol Research (EA 18 19 to LFC). The authors thank Etienne Audinat for the PV-Cre mice and Glenn Dallerac for the GFAP-CreERT2. EP was a recipient of Marie Curie Intra-European Fellowship (IEF327648). LC has benefited from support by the Labex EpiGenMed (Investissements d’avenir #ANR-10-LABX-12-01). We thank Catalina Betancur for helpful discussions and comments on the manuscript; the staff members of the Basque Institute of Legal Medicine for processing the postmortem human brain samples; Stéphane Fouquet, David Godefroy, and Marie-Laure Niepon of the Imaging Facility at Institut de la Vision; Annick Prigeant of the Histology Facility at Institut du Cerveau et de la Moelle; and Chooyoung Baek and Audrey Pondaven for their help with the FISH experiments.
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Mongrédien, R., Erdozain, A.M., Dumas, S. et al. Cartography of hevin-expressing cells in the adult brain reveals prominent expression in astrocytes and parvalbumin neurons. Brain Struct Funct 224, 1219–1244 (2019). https://doi.org/10.1007/s00429-019-01831-x
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DOI: https://doi.org/10.1007/s00429-019-01831-x