Identification of novel glial genes by single-cell transcriptional profiling of Bergmann glial cells from mouse cerebellum

PLoS ONE

Volumn 5, Issue 2, 2010, Pages

  Koirala, Samir ^a,b   Corfas, Gabriel ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; G PROTEIN COUPLED RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GPR126 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN MATURATION; CEREBELLUM CORTEX; CONTROLLED STUDY; DNA FINGERPRINTING; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE PROBE; GENETIC TRANSCRIPTION; GLIA CELL; NONHUMAN; QUALITY CONTROL; SOMATIC CELL GENETICS; SYNAPSE; ANIMAL; ASTROCYTE; CEREBELLUM; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GLIA; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; METABOLISM; MOUSE; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; TIME; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; CEREBELLUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; IN SITU HYBRIDIZATION; METABOLIC NETWORKS AND PATHWAYS; MICE; MICE, TRANSGENIC; NEUROGLIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELLS; TIME FACTORS;

EID: 77949458939     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009198     Document Type: Article

References (92)

1. Hausmann B, Sievers J (1985) Cerebellar external granule cells are attached to the basal lamina from the onset of migration up to the end of their proliferative activity. J Comp Neurol 241: 50-62.
2. Sievers J, Mangold U, Berry M, Allen C, Schlossberger HG (1981) Experimental studies on cerebellar foliation. I. A qualitative morphological analysis of cerebellar fissuration defects after neonatal treatment with 6-OHDA in the rat. J Comp Neurol 203: 751-769.
3. Sievers J, von Knebel Doeberitz C, Pehlemann FW, Berry M (1986) Meningeal cells influence cerebellar development over a critical period. Anat Embryol (Berl) 175: 91-100.
4. Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22: 511-539.
5. Rakic P (1990) Principles of neural cell migration. Experientia 46: 882-891.
6. Belvindrah R, Nalbant P, Ding S, Wu C, Bokoch GM, et al. (2006) Integrin-linked kinase regulates Bergmann glial differentiation during cerebellar development. Mol Cell Neurosci 33: 109-125.
7. Graus-Porta D, Blaess S, Senften M, Littlewood-Evans A, Damsky C, et al. (2001) Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31: 367-379.
8. Lippman JJ, Lordkipanidze T, Buell ME, Yoon SO, Dunaevsky A (2008) Morphogenesis and regulation of Bergmann glial processes during Purkinje cell dendritic spine ensheathment and synaptogenesis. Glia 56: 1463-1477.
9. Yamada K, Fukaya M, Shibata T, Kurihara H, Tanaka K, et al. (2000) Dynamic transformation of Bergmann glial fibers proceeds in correlation with dendritic outgrowth and synapse formation of cerebellar Purkinje cells. J Comp Neurol 418: 106-120.
10. Yamada K, Watanabe M (2002) Cytodifferentiation of Bergmann glia and its relationship with Purkinje cells. Anat Sci Int 77: 94-108.
11. Iino M, Goto K, Kakegawa W, Okado H, Sudo M, et al. (2001) Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia. Science 292: 926-929.
12. Altman J, Bayer SA (1997) Development of the Cerebellar System in Relation to its Evolution, Structure, and Functions. New York: CRC Press.
13. Cui W, Allen ND, Skynner M, Gusterson B, Clark AJ (2001) Inducible ablation of astrocytes shows that these cells are required for neuronal survival in the adult brain. Glia 34: 272-282.
14. Bellamy TC (2006) Interactions between Purkinje neurones and Bergmann glia. Cerebellum 5: 116-126.
15. Lopez-Bayghen E, Rosas S, Castelan F, Ortega A (2007) Cerebellar Bergmann glia: an important model to study neuron-glia interactions. Neuron Glia Biol 3: 155-167.
16. Muller T, Kettenmann H (1995) Physiology of Bergmann glial cells. Int Rev Neurobiol 38: 341-359.
17. Teichberg VI (1991) Glial glutamate receptors: likely actors in brain signaling. Faseb J 5: 3086-3091.
18. Ottersen OP, Chaudhry FA, Danbolt NC, Laake JH, Nagelhus EA, et al. (1997) Molecular organization of cerebellar glutamate synapses. Prog Brain Res 114: 97-107.
19. Ottersen OP, Zhang N, Walberg F (1992) Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience 46: 519-534.
20. Nimmerjahn A, Mukamel EA, Schnitzer MJ (2009) Motor behavior activates Bergmann glial networks. Neuron 62: 400-412.
21. Bordey A, Sontheimer H (2003) Modulation of glutamatergic transmission by bergmann glial cells in rat cerebellum in situ. J Neurophysiol 89: 979-988.
22. Brockhaus J, Deitmer JW (2002) Long-lasting modulation of synaptic input to Purkinje neurons by Bergmann glia stimulation in rat brain slices. J Physiol 545: 581-593.
23. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, 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.
24. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA (2002) "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298: 597-600.
25. Tietjen I, Rihel JM, Cao Y, Koentges G, Zakhary L, et al. (2003) Single-cell transcriptional analysis of neuronal progenitors. Neuron 38: 161-175.
26. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, et al. (1997) Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187: 36-42.
27. Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83: 195-206.
28. Eberwine J, Yeh H, Miyashiro K, Cao Y, Nair S, et al. (1992) Analysis of gene expression in single live neurons. Proc Natl Acad Sci U S A 89: 3010-3014.
29. Mager WH (1988) Control of ribosomal protein gene expression. Biochim Biophys Acta 949: 1-15.
30. Tushinski RJ, Warner JR (1982) Ribosomal proteins are synthesized preferentially in cells commencing growth. J Cell Physiol 112: 128-135.
31. Jimenez-Marin A, Collado-Romero M, Ramirez-Boo M, Arce C, Garrido JJ (2009) Biological pathway analysis by ArrayUnlock and Ingenuity Pathway Analysis. BMC Proc 3 Suppl 4: S6.
32. Eiraku M, Tohgo A, Ono K, Kaneko M, Fujishima K, et al. (2005) DNER acts as a neuron-specific Notch ligand during Bergmann glial development. Nat Neurosci 8: 873-880.
33. Komine O, Nagaoka M, Watase K, Gutmann DH, Tanigaki K, et al. (2007) The monolayer formation of Bergmann glial cells is regulated by Notch/RBP-J signaling. Dev Biol 311: 238-250.
34. Weller M, Krautler N, Mantei N, Suter U, Taylor V (2006) Jagged1 ablation results in cerebellar granule cell migration defects and depletion of Bergmann glia. Dev Neurosci 28: 70-80.
35. Roubelakis MG, Martin-Rendon E, Tsaknakis G, Stavropoulos A, Watt SM (2007) The murine ortholog of the SHP-2 binding molecule, PZR accelerates cell migration on fibronectin and is expressed in early embryo formation. J Cell Biochem 102: 955-969.
36. Bermingham JR Jr, Shearin H, Pennington J, O'Moore J, Jaegle M, et al. (2006) The claw paw mutation reveals a role for Lgi4 in peripheral nerve development. Nat Neurosci 9: 76-84.
37. Tournell CE, Bergstrom RA, Ferreira A (2006) Progesterone-induced agrin expression in astrocytes modulates glia-neuron interactions leading to synapse formation. Neuroscience 141: 1327-1338.
38. Zhao R, Lawler AM, Lee SJ (1999) Characterization of GDF-10 expression patterns and null mice. Dev Biol 212: 68-79.
39. Koirala S, Jin Z, Piao X, Corfas G (2009) GPR56-regulated granule cell adhesion is essential for rostral cerebellar development. J Neurosci 29: 7439-7449.
40. Li S, Jin Z, Koirala S, Bu L, Xu L, et al. (2008) GPR56 regulates pial basement membrane integrity and cortical lamination. J Neurosci 28: 5817-5826.
41. Monk KR, Naylor SG, Glenn TD, Mercurio S, Perlin JR, et al. (2009) A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 325: 1402-1405.
42. Shima Y, Kengaku M, Hirano T, Takeichi M, Uemura T (2004) Regulation of dendritic maintenance and growth by a mammalian 7-pass transmembrane cadherin. Dev Cell 7: 205-216.
43. Tissir F, Bar I, Jossin Y, De Backer O, Goffinet AM (2005) Protocadherin Celsr3 is crucial in axonal tract development. Nat Neurosci 8: 451-457.
44. Alcock J, Scotting P, Sottile V (2007) Bergmann glia as putative stem cells of the mature cerebellum. Med Hypotheses 69: 341-345.
45. Klein C, Butt SJ, Machold RP, Johnson JE, Fishell G (2005) Cerebellum- and forebrain-derived stem cells possess intrinsic regional character. Development 132: 4497-4508.
46. Lee A, Kessler JD, Read TA, Kaiser C, Corbeil D, et al. (2005) Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 8: 723-729.
47. Blackshaw S, Harpavat S, Trimarchi J, Cai L, Huang H, et al. (2004) Genomic analysis of mouse retinal development. PLoS Biol 2: E247.
48. Eichele G (1997) Retinoids: from hindbrain patterning to Parkinson disease. Trends Genet 13: 343-345.
49. Bagri A, Tessier-Lavigne M (2002) Neuropilins as Semaphorin receptors: in vivo functions in neuronal cell migration and axon guidance. Adv Exp Med Biol 515:
50. Paradis S, Harrar DB, Lin Y, Koon AC, Hauser JL, et al. (2007) An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 53: 217-232.
51. Tran TS, Kolodkin AL, Bharadwaj R (2007) Semaphorin regulation of cellular morphology. Annu Rev Cell Dev Biol 23: 263-292.
52. Cunningham NS, Jenkins NA, Gilbert DJ, Copeland NG, Reddi AH, et al. (1995) Growth/differentiation factor-10: a new member of the transforming growth factor-beta superfamily related to bone morphogenetic protein-3. Growth Factors 12: 99-109.
53. Jorgensen JR, Thompson L, Fjord-Larsen L, Krabbe C, Torp M, et al. (2009) Characterization of Meteorin-An Evolutionary Conserved Neurotrophic Factor. J Mol Neurosci.
54. Nishino J, Yamashita K, Hashiguchi H, Fujii H, Shimazaki T, et al. (2004) Meteorin: a secreted protein that regulates glial cell differentiation and promotes axonal extension. Embo J 23: 1998-2008.
55. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43: 647-661.
56. Elias LA, Wang DD, Kriegstein AR (2007) Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448: 901-907.
57. Craig AM, Kang Y (2007) Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17: 43-52.
58. Mustafa AK, Kim PM, Snyder SH (2004) D-Serine as a putative glial neurotransmitter. Neuron Glia Biol 1: 275-281.
59. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, et al. (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125: 775-784.
60. Soto D, Coombs ID, Renzi M, Zonouzi M, Farrant M, et al. (2009) Selective regulation of long-form calcium-permeable AMPA receptors by an atypical TARP, gamma-5. Nat Neurosci 12: 277-285.
61. Schousboe A, Westergaard N, Waagepetersen HS, Larsson OM, Bakken IJ, et al. (1997) Trafficking between glia and neurons of TCA cycle intermediates and related metabolites. Glia 21: 99-105.
62. Magistretti PJ, Pellerin L (1999) Astrocytes Couple Synaptic Activity to Glucose Utilization in the Brain. News Physiol Sci 14: 177-182.
63. Dean C, Dresbach T (2006) Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci 29: 21-29.
64. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, et al. (2003) Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6: 708-716.
65. Taniguchi H, Gollan L, Scholl FG, Mahadomrongkul V, Dobler E, et al. (2007) Silencing of neuroligin function by postsynaptic neurexins. J Neurosci 27: 2815-2824.
66. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897-6906.
67. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, et al. (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369: 744-747.
68. Parpura V, Haydon PG (2000) Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci U S A 97: 8629-8634.
69. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1998) Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur J Neurosci 10: 2129-2142.
70. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, et al. (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43: 729-743.
71. Newman EA (2003) New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci 26: 536-542.
72. Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26: 523-530.
73. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6: 626-640.
74. Pan PY, Tian JH, Sheng ZH (2009) Snapin facilitates the synchronization of synaptic vesicle fusion. Neuron 61: 412-424.
75. Schoch S, Mittelstaedt T, Kaeser PS, Padgett D, Feldmann N, et al. (2006) Redundant functions of RIM1alpha and RIM2alpha in Ca(2+)-triggered neurotransmitter release. Embo J 25: 5852-5863.
76. Park WJ, Lee SE, Kwon NS, Baek KJ, Kim DS, et al. (2008) Leucine-rich glioma inactivated 3 associates with syntaxin 1. Neurosci Lett 444: 240-244.
77. Moore SA, Saito F, Chen J, Michele DE, Henry MD, et al. (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418: 422-425.
78. Ango F, Wu C, Van der Want JJ, Wu P, Schachner M, et al. (2008) Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites. PLoS Biol 6: e103.
79. Sottile V, Li M, Scotting PJ (2006) Stem cell marker expression in the Bergmann glia population of the adult mouse brain. Brain Res 1099: 8-17.
80. Sotelo C, Alvarado-Mallart RM, Frain M, Vernet M (1994) Molecular plasticity of adult Bergmann fibers is associated with radial migration of grafted Purkinje cells. J Neurosci 14: 124-133.
81. Krizhanovsky V, Ben-Arie N (2006) A novel role for the choroid plexus in BMPmediated inhibition of differentiation of cerebellar neural progenitors. Mech Dev 123: 67-75.
82. Dulac C (1998) Cloning of genes from single neurons. Curr Top Dev Biol 36: 245-258.
83. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci U S A 81: 1991-1995.
84. Dolter KE, Braman JC (2001) Small-sample total RNA purification: laser capture microdissection and cultured cell applications. Biotechniques 30: 1358-1361.
85. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
86. Thierry-Mieg D, Thierry-Mieg J (2006) AceView: a comprehensive cDNAsupported gene and transcripts annotation. Genome Biol 7 Suppl 1: S12 11-14.
87. Schaeren-Wiemers N, Gerfin-Moser A (1993) A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100: 431-440.
88. Corfas G, Rosen KM, Aratake H, Krauss R, Fischbach GD (1995) Differential expression of ARIA isoforms in the rat brain. Neuron 14: 103-115.
89. Sassoon D, Rosenthal N (1993) Detection of messenger RNA by in situ hybridization. Methods Enzymol 225: 384-404.
90. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, et al. (2007) Genomewide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.
91. Magdaleno S, Jensen P, Brumwell CL, Seal A, Lehman K, et al. (2006) BGEM: an in situ hybridization database of gene expression in the embryonic and adult mouse nervous system. PLoS Biol 4: e86.
92. Visel A, Thaller C, Eichele G (2004) GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 32: D552-556.