Advertisement

Cartography of hevin-expressing cells in the adult brain reveals prominent expression in astrocytes and parvalbumin neurons

  • Raphaële Mongrédien
  • Amaia M. Erdozain
  • Sylvie Dumas
  • Laura Cutando
  • Amaia Nuñez del Moral
  • Emma Puighermanal
  • Sara Rezai Amin
  • Bruno Giros
  • Emmanuel Valjent
  • J. Javier Meana
  • Sophie Gautron
  • Luis F. Callado
  • Véronique Fabre
  • Vincent VialouEmail author
Original Article

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.

Keywords

Hevin Matricellular protein Parvalbumin neurons Astrocytes Glutamatergic neurons In situ hybridization 

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

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. In addition, all applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

No consent is required for using leftover body material for scientific purposes from medico-legal autopsies.

Supplementary material

429_2019_1831_MOESM1_ESM.docx (1.9 mb)
Supplementary material 1 (DOCX 1945 KB)

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. Brekken RA, Sage EH (2000) SPARC, a matricellular protein: at the crossroads of cell-matrix. Matrix Biol 19:569–580CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 41:57–69CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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:RC181CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 4:165–176CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. Markiewicz I, Lukomska B (2006) The role of astrocytes in the physiology and pathology of the central nervous system. Acta Neurobiol Exp (Wars) 66:343–358Google Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 676:69–79CrossRefGoogle Scholar
  45. 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 713:53–63CrossRefGoogle Scholar
  46. 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 25:1637–1644CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. Paxinos G, Franklin KBG (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic, San DiegoGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. Risher WC, Patel S, Kim IH et al (2014) Astrocytes refine cortical connectivity at dendritic spines. Elife.  https://doi.org/10.7554/eLife.04047 Google Scholar
  56. 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 CrossRefGoogle Scholar
  57. Sage EH, Bornstein P (1991) Extracellular proteins that modulate cell-matrix interactions—sparc, tenascin, and thrombospondin. J Biol Chem 266:14831–14834Google Scholar
  58. 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 CrossRefGoogle Scholar
  59. 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 17:1–10CrossRefGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. 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 CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 CrossRefGoogle Scholar
  65. 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 CrossRefGoogle Scholar
  66. 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 CrossRefGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. 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 CrossRefGoogle Scholar
  69. 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 CrossRefGoogle Scholar
  70. 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 CrossRefGoogle Scholar
  71. 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 CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. 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 Google Scholar
  74. 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 CrossRefGoogle Scholar
  75. 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 CrossRefGoogle Scholar
  76. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine, Institut de Biologie Paris SeineParisFrance
  2. 2.Department of PharmacologyUniversity of the Basque Country, UPV/EHUBizkaiaSpain
  3. 3.Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM)MadridSpain
  4. 4.OramacellParisFrance
  5. 5.IGF, CNRS, INSERM, University of MontpellierMontpellierFrance

Personalised recommendations