Pre-existing astrocytes form functional perisynaptic processes on neurons generated in the adult hippocampus

Brain Structure and Function

Volumn 220, Issue 4, 2015, Pages 2027-2042

  Krzisch, Marine ^a   Temprana, Silvio G ^b   Mongiat, Lucas A ^b   Armida, Jan ^a   Schmutz, Valentin ^a   Virtanen, Mari A ^c   Kocher Braissant, Jacqueline ^a   Kraftsik, Rudolf ^a   Vutskits, Laszlo ^c,d   Conzelmann, Karl Klaus ^e   Bergami, Matteo ^f   Gage, Fred H ^g   Schinder, Alejandro F ^b   Toni, Nicolas ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b Universidad Nacional de Río Cuarto Consejo Nacional de Investigaciones Científicas y Técnicas   (Argentina)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^e UNIVERSITY OF MUNICH   (Germany)

^f UNIVERSITY OF COLOGNE   (Germany)

^g SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Adult neurogenesis; Astrocytes; Dentate gyrus; Perisynaptic processes; Synaptogenesis

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CELL DENSITY; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC SPINE; ELECTROPHYSIOLOGY; FEMALE; GRANULE CELL; HIPPOCAMPUS; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MOUSE; NEURON PERISYNAPTIC PROCESS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ALDEHYDE DEHYDROGENASE ISOENZYME 1; BROXURIDINE; DIHYDROKAINIC ACID; ENOLASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; ISOENZYME; KAINIC ACID; PROTEIN S100B; RETINAL DEHYDROGENASE;

ANIMALS; ASTROCYTES; BROMODEOXYURIDINE; DENDRITIC SPINES; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; ISOENZYMES; KAINIC ACID; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; NEUROGENESIS; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHOPYRUVATE HYDRATASE; RETINAL DEHYDROGENASE; S100 CALCIUM BINDING PROTEIN BETA SUBUNIT; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84933177806     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0768-y     Document Type: Article

References (67)

1. Allen NJ, Bennett ML, Foo LC, Wang GX, Chakraborty C, Smith SJ, Barres BA (2012) Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 486(7403):410–414. doi:10.1038/nature11059
2. Alonso M, Lepousez G, Sebastien W, Bardy C, Gabellec MM, Torquet N, Lledo PM (2012) Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 15(6):897–904. doi:10.1038/nn.3108
3. Altman J (1962) Are new neurons formed in the brains of adult mammals? Science 135(3509):1127–1128
4. Bergami M, Berninger B (2012) A fight for survival: the challenges faced by a newborn neuron integrating in the adult hippocampus. Dev Neurobiol 72(7):1016–1031. doi:10.1002/dneu.22025
5. Bergami M, Santi S, Formaggio E, Cagnoli C, Verderio C, Blum R, Berninger B, Matteoli M, Canossa M (2008) Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J Cell Biol 183(2):213–221. doi:10.1083/jcb.200806137
6. Bergles DE, Jahr CE (1998) Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J Neurosci 18(19):7709–7716
7. Bruel-Jungerman E, Davis S, Rampon C, Laroche S (2006) Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J Neurosci 26(22):5888–5893. doi:10.1523/JNEUROSCI.0782-06.2006
8. Catalani A, Sabbatini M, Consoli C, Cinque C, Tomassoni D, Azmitia E, Angelucci L, Amenta F (2002) Glial fibrillary acidic protein immunoreactive astrocytes in developing rat hippocampus. Mech Ageing Dev 123(5):481–490
9. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120(3):421–433. doi:10.1016/j.cell.2004.12.020
10. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325(5937):210–213. doi:10.1126/science.1173215
11. Colon-Ramos DA, Margeta MA, Shen K (2007) Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science 318(5847):103–106. doi:10.1126/science.1143762
12. Deshpande A, Bergami M, Ghanem A, Conzelmann KK, Lepier A, Gotz M, Berninger B (2013) Retrograde monosynaptic tracing reveals the temporal evolution of inputs onto new neurons in the adult dentate gyrus and olfactory bulb. Proc Natl Acad Sci USA 110(12):E1152–E1161. doi:10.1073/pnas.1218991110
13. Dietrich D, Beck H, Kral T, Clusmann H, Elger CE, Schramm J (1997) Metabotropic glutamate receptors modulate synaptic transmission in the perforant path: pharmacology and localization of two distinct receptors. Brain Res 767(2):220–227
14. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4(11):1313–1317. doi:10.1038/3305
15. Faissner A, Pyka M, Geissler M, Sobik T, Frischknecht R, Gundelfinger ED, Seidenbecher C (2010) Contributions of astrocytes to synapse formation and maturation—potential functions of the perisynaptic extracellular matrix. Brain Res Rev 63(1–2):26–38. doi:10.1016/j.brainresrev.2010.01.001
16. Finke S, Mueller-Waldeck R, Conzelmann KK (2003) Rabies virus matrix protein regulates the balance of virus transcription and replication. J Gen Virol 84(Pt 6):1613–1621
17. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54(4):559–566. doi:10.1016/j.neuron.2007.05.002
18. Ge WP, Miyawaki A, Gage FH, Jan YN, Jan LY (2012) Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484(7394):376–380. doi:10.1038/nature10959
19. Genoud C, Quairiaux C, Steiner P, Hirling H, Welker E, Knott GW (2006) Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex. PLoS Biol 4(11):e343. doi:10.1371/journal.pbio.0040343
20. Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, Frankland PW, Ge S (2012) Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 15(12):1700–1706. doi:10.1038/nn.3260
21. Haber M, Zhou L, Murai KK (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26(35):8881–8891. doi:10.1523/JNEUROSCI.1302-06.2006
22. Hagemann TL, Paylor R, Messing A (2013) Deficits in adult neurogenesis, contextual fear conditioning, and spatial learning in a Gfap mutant mouse model of Alexander disease. J Neurosci 33(47):18698–18706. doi:10.1523/JNEUROSCI.3693-13.2013
23. Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, Xu Q, Oberheim NA, Bekar L, Betstadt S, Silva AJ, Takano T, Goldman SA, Nedergaard M (2013) Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12(3):342–353. doi:10.1016/j.stem.2012.12.015
24. Hirrlinger J, Hulsmann S, Kirchhoff F (2004) Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur J Neurosci 20(8):2235–2239. doi:10.1111/j.1460-9568.2004.03689.xEJN3689
25. Huang YH, Bergles DE (2004) Glutamate transporters bring competition to the synapse. Curr Opin Neurobiol 14(3):346–352. doi:10.1016/j.conb.2004.05.007
26. Jessberger S, Zhao C, Toni N, Clemenson GD Jr, Li Y, Gage FH (2007) Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J Neurosci 27(35):9400–9407. doi:10.1523/JNEUROSCI.2002-07.2007
27. Kempermann G, Kuhn HG, Gage FH (1997a) Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA 94(19):10409–10414
28. Kempermann G, Kuhn HG, Gage FH (1997b) More hippocampal neurons in adult mice living in an enriched environment. Nature 386(6624):493–495. doi:10.1038/386493a0
29. Krzisch M, Sultan S, Sandell J, Demeter K, Vutskits L, Toni N (2013) Propofol anesthesia impairs the maturation and survival of adult-born hippocampal neurons. Anesthesiology 118(3):602–610. doi:10.1097/ALN.0b013e3182815948
30. Laplagne DA, Esposito MS, Piatti VC, Morgenstern NA, Zhao C, van Praag H, Gage FH, Schinder AF (2006) Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4(12):e409. doi:10.1371/journal.pbio.0040409
31. Macek TA, Winder DG, Gereau RWt, Ladd CO, Conn PJ (1996) Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurophysiol 76(6):3798–3806
32. Maki R, Robinson MB, Dichter MA (1994) The glutamate uptake inhibitor l-trans-pyrrolidine-2,4-dicarboxylate depresses excitatory synaptic transmission via a presynaptic mechanism in cultured hippocampal neurons. J Neurosci 14(11 Pt 1):6754–6762
33. Marin-Burgin A, Mongiat LA, Pardi MB, Schinder AF (2012) Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 335(6073):1238–1242. doi:10.1126/science.1214956
34. Mauch DH, Nagler K, Schumacher S, Goritz C, Muller EC, Otto A, Pfrieger FW (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294(5545):1354–1357. doi:10.1126/science.294.5545.1354
35. Mishchenko Y, Hu T, Spacek J, Mendenhall J, Harris KM, Chklovskii DB (2010) Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67(6):1009–1020. doi:10.1016/j.neuron.2010.08.014
36. Nishida H, Okabe S (2007) Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 27(2):331–340. doi:10.1523/JNEUROSCI.4466-06.2007
37. Nixdorf-Bergweiler BE, Albrecht D, Heinemann U (1994) Developmental changes in the number, size, and orientation of GFAP-positive cells in the CA1 region of rat hippocampus. Glia 12(3):180–195. doi:10.1002/glia.440120304
38. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H (2001) GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33(1):72–86. doi:10.1002/1098-1136(20010101)33:1<72::AID-GLIA1007>3.0.CO;2-A
39. Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292(5518):923–926. doi:10.1126/science.1059162
40. 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(4):775–784. doi:10.1016/j.cell.2006.02.051
41. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310(5745):113–116. doi:10.1126/science.1116916
42. Pfrieger FW, Barres BA (1997) Synaptic efficacy enhanced by glial cells in vitro. Science 277(5332):1684–1687
43. Platel JC, Dave KA, Gordon V, Lacar B, Rubio ME, Bordey A (2010) NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 65(6):859–872. doi:10.1016/j.neuron.2010.03.009
44. Portera-Cailliau C, Pan DT, Yuste R (2003) Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia. J Neurosci 23(18):7129–7142
45. Reye P, Sullivan R, Scott H, Pow DV (2002) Distribution of two splice variants of the glutamate transporter GLT-1 in rat brain and pituitary. Glia 38(3):246–255. doi:10.1002/glia.10059
46. Rollenhagen A, Satzler K, Rodriguez EP, Jonas P, Frotscher M, Lubke JH (2007) Structural determinants of transmission at large hippocampal mossy fiber synapses. J Neurosci 27(39):10434–10444. doi:10.1523/JNEUROSCI.1946-07.2007
47. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16(3):675–686
48. Sahay A, Scobie KN, Hill AS, O’Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472(7344):466–470. doi:10.1038/nature09817
49. Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429(6988):184–187. doi:10.1038/nature02553
50. Spacek J (1985) Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat Embryol (Berl) 171(2):245–252
51. Stone SS, Teixeira CM, Devito LM, Zaslavsky K, Josselyn SA, Lozano AM, Frankland PW (2011) Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory. J Neurosci 31(38):13469–13484. doi:10.1523/JNEUROSCI.3100-11.2011
52. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276(5319):1699–1702
53. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH (2006) NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442(7105):929–933. doi:10.1038/nature05028
54. Toni N, Sultan S (2011) Synapse formation on adult-born hippocampal neurons. Eur J Neurosci 33(6):1062–1068. doi:10.1111/j.1460-9568.2011.07604.x
55. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10(6):727–734. doi:10.1038/nn1908
56. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF (2008) Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11(8):901–907. doi:10.1038/nn.2156
57. Tronel S, Fabre A, Charrier V, Oliet SH, Gage FH, Abrous DN (2010) Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc Natl Acad Sci USA 107(17):7963–7968. doi:10.1073/pnas.0914613107
58. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291(5504):657–661. doi:10.1126/science.291.5504.657291/5504/657
59. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96(23):13427–13431
60. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415(6875):1030–1034. doi:10.1038/4151030a
61. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19(16):6897–6906
62. Vivar C, Potter MC, Choi J, Lee JY, Stringer TP, Callaway EM, Gage FH, Suh H, van Praag H (2012) Monosynaptic inputs to new neurons in the dentate gyrus. Nature Commun 3:1107. doi:10.1038/ncomms2101
63. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6(8):626–640. doi:10.1038/nrn1722
64. Witcher MR, Kirov SA, Harris KM (2007) Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. Glia 55(1):13–23. doi:10.1002/glia.20415
65. Witcher MR, Park YD, Lee MR, Sharma S, Harris KM, Kirov SA (2010) Three-dimensional relationships between perisynaptic astroglia and human hippocampal synapses. Glia 58(5):572–587. doi:10.1002/glia.20946
66. Zhang X, Zhang J, Chen C (2009) Long-term potentiation at hippocampal perforant path-dentate astrocyte synapses. Biochemical and biophysical research communications 383(3):326–330. doi:10.1016/j.bbrc.2009.04.005
67. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26(1):3–11. doi:10.1523/JNEUROSCI.3648-05.2006