In Vivo development of outer retinal synapses in the absence of glial contact

Journal of Neuroscience

Volumn 30, Issue 36, 2010, Pages 11951-11961

  Williams, Philip R ^a,b   Suzuki, Sachihiro C ^a   Yoshimatsu, Takeshi ^a   Lawrence, Owen T ^a   Waldron, Steven J ^a   Parsons, Michael J ^c   Nonet, Michael L ^b   Wong, Rachel O L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b WASHINGTON UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; PLASMID DNA; AMINO ACID; DOLAISOLEUCINE; GLUTAMATE RECEPTOR; PHOTOPROTEIN; ZEBRAFISH PROTEIN;

ARTICLE; CELL CONTACT; CELL DIFFERENTIATION; CELL INTERACTION; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; EMBRYO; GLIA CELL; IMMUNOFLUORESCENCE; IN VIVO STUDY; MACROGLIA; MOLECULAR CLONING; MUELLER CELL; MULTIPHOTON MICROSCOPY; NONHUMAN; PHOTORECEPTOR; PLASMID; PRIORITY JOURNAL; RETINA; RETINA CONE; RETINA DEVELOPMENT; SYNAPTOGENESIS; TRANSGENIC ANIMAL; TRANSIENT EXPRESSION; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; BLEACHING; CLASSIFICATION; CYTOLOGY; DIAGNOSTIC USE; GENETICS; GLIA; METABOLISM; NERVE CELL; PHYSIOLOGY; PROCEDURES; SYNAPSE; THREE DIMENSIONAL IMAGING; TIME; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AMINO ACIDS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; EMBRYO, NONMAMMALIAN; IMAGING, THREE-DIMENSIONAL; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROGLIA; NEURONS; PHOTOBLEACHING; RECEPTORS, GLUTAMATE; RETINA; SYNAPSES; TIME FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77956588977     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3391-10.2010     Document Type: Article

References (58)

1. Beattie EC, Stellwagen D, Morishita W, Bresnahan JC, Ha BK, Von Zastrow M, Beattie MS, Malenka RC (2002) Control of synaptic strength by glial TNFalpha. Science 295:2282-2285. (Pubitemid 34258846)
2. Bernardos RL, Raymond PA (2006) GFAP transgenic zebrafish. Gene Expr Patterns 6:1007-1013.
3. Blondel O, Collin C, McCarran WJ, Zhu S, Zamostiano R, Gozes I, Brenneman DE, McKay RD (2000) A glia-derived signal regulating neuronal differentiation. J Neurosci 20:8012-8020.
4. Brancheck T (1984) The development of photoreceptors in zebrafish. II. Function. J Comp Neurol 224:116-122.
5. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192.
6. Bushong EA, Martone ME, Ellisman MH (2004) Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22:73-86.
7. 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 120:421-433.
8. Dreher Z, Robinson SR, Distler C (1992) Muller cells in vascular and avascular retinae: a survey of seven mammals. J Comp Neurol 323:59-80.
9. Easter SS Jr, Nicola GN (1996) The development of vision in the zebrafish, Danio rerio. Dev Biol 180:646-663.
10. Elmariah SB, Oh EJ, Hughes EG, Balice-Gordon RJ (2005) Astrocytes regulate inhibitory synapse formation via Trk-mediated modulation of postsynaptic GABAA receptors. J Neurosci 25:3638-3650. (Pubitemid 40503691)
11. Fadool JM (2003) Development of a rod photoreceptor mosaic revealed in transgenic zebrafish. Dev Biol 258:277-290.
12. Feng Z, Ko CP (2008) Schwann cells promote synaptogenesis at the neuromuscular junction via transforming growth factor-β1. J Neurosci 28: 9599-9609.
13. Friauf E, McConnell SK, Shatz CJ (1990) Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J Neurosci 10:2601-2613.
14. Gan WB, Macagno ER (1995) Interactions between segmental homologs and between isoneuronal branches guide the formation of sensory terminal fields. J Neurosci 15:3243-3253.
15. Godinho L, Mumm JS, Williams PR, Schroeter EH, Koerber A, Park SW, Leach SD, Wong RO (2005) Targeting of amacrine cell neurites to appropriate synaptic laminae in the developing zebrafish retina. Development 132:5069-5079.
16. Godinho L, Williams PR, Claassen Y, Provost E, Leach SD, Kamermans M, Wong RO (2007) Nonapical symmetric divisions underlie horizontal cell layer formation in the developing retina in vivo. Neuron 56:597-603.
17. Grosche J, Matyash V, Möller T, Verkhratsky A, Reichenbach A, Kettenmann H (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2:139-143. (Pubitemid 30491313)
18. Grueber WB, Ye B, Moore AW, Jan LY, Jan YN (2003) Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr Biol 13:618-626.
19. Haber M, Zhou L, Murai KK (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26: 8881-8891.
20. Hama H, Hara C, Yamaguchi K, Miyawaki A (2004) PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron 41:405-415.
21. Hirrlinger J, Hülsmann S, Kirchhoff F (2004) Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur J Neurosci 20:2235-2239. (Pubitemid 39331144)
22. Huang CJ, Tu CT, Hsiao CD, Hsieh FJ, Tsai HJ (2003) Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev Dyn 228:30-40.
23. Huckfeldt RM, Schubert T, Morgan JL, Godinho L, Di Cristo G, Huang ZJ, Wong RO (2009) Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat Neurosci 12:35-43.
24. Iino M, Goto K, Kakegawa W, Okado H, Sudo M, Ishiuchi S, Miwa A, Takayasu Y, Saito I, Tsuzuki K, Ozawa S (2001) Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia. Science 292:926-929.
25. Kawakami K (2004) Transgenesis and gene trap methods in zebrafish by using the Tol2 transposable element. Methods Cell Biol 77:201-222. (Pubitemid 44406430)
26. Kawakami K, Shima A (1999) Identification of the Tol2 transposase of the medaka fish Oryzias latipes that catalyzes excision of a nonautonomous Tol2 element in zebrafish Danio rerio. Gene 240:239-244.
27. Kirby BB, Takada N, Latimer AJ, Shin J, Carney TJ, Kelsh RN, Appel B (2006) In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat Neurosci 9:1506-1511.
28. Köster RW, Fraser SE (2001) Tracing transgene expression in living zebrafish embryos. Dev Biol 233:329-346.
29. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236:3088-3099.
30. 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.
31. A current by astrocytes in cultured embryonic rat hippocampal neurons. J Neurosci 16:2912-2923.
32. Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, Sanes JR, Lichtman JW (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450:56-62.
33. Mauch DH, Nägler K, Schumacher S, Göritz C, Müller EC, Otto A, Pfrieger FW (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294:1354-1357. (Pubitemid 33063104)
34. Morest DK (1970) The pattern of neurogenesis in the retina of the rat. Z Anat Entwicklungsgesch 131:45-67.
35. Müller CM (1990) Dark-rearing retards the maturation of astrocytes in restricted layers of cat visual cortex. Glia 3:487-494.
36. Müller CM, Best J (1989) Ocular dominance plasticity in adult cat visual cortex after transplantation of cultured astrocytes. Nature 342:427-430.
37. Nishida H, Okabe S (2007) Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 27:331-340.
38. Obholzer N, Wolfson S, Trapani JG, Mo W, Nechiporuk A, Busch-Nentwich E, Seiler C, Sidi S, Söllner C, Duncan RN, Boehland A, Nicolson T (2008) Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28:2110-2118.
39. Parsons MJ, Pisharath H, Yusuff S, Moore JC, Siekmann AF, Lawson N, Leach SD (2009) Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mech Dev 126:898-912.
40. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248-1251. (Pubitemid 35285495)
41. Prada FA, Quesada A, Dorado ME, Chmielewski C, Prada C (1998) Glutamine synthetase (GS) activity and spatial and temporal patterns of GS expression in the developing chick retina: relationship with synaptogenesis in the outer plexiform layer. Glia 22:221-236.
42. Ramón y Cajal S (1960) Studies on vertebrate neurogenesis. Reprint (Guth L, translator). Springfield, IL: Thomas.
43. Ransom B, Behar T, Nedergaard M (2003) New roles for astrocytes (stars at last). Trends Neurosci 26:520-522. (Pubitemid 37176905)
44. Raymond PA, Barthel LK, Curran GA (1995) Developmental patterning of rod and cone photoreceptors in embryonic zebrafish. J Comp Neurol 359:537-550.
45. Reddy LV, Koirala S, Sugiura Y, Herrera AA, Ko CP (2003) Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron 40:563-580.
46. Ren JQ, McCarthy WR, Zhang H, Adolph AR, Li L (2002) Behavioral visual responses of wild-type and hypopigmented zebrafish. Vision Res 42:293-299.
47. Robinson SR, Dreher Z (1990) Muller cells in adult rabbit retinae: morphology, distribution and implications for function and development. J Comp Neurol 292:178-192.
48. Rochefort N, Quenech'du N, Ezan P, Giaume C, Milleret C (2005) Postnatal development of GFAP, connexin43 and connexin30 in cat visual cortex. Brain Res Dev Brain Res 160:252-264.
49. Sagasti A, Guido MR, Raible DW, Schier AF (2005) Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors. Curr Biol 15:804-814. (Pubitemid 40689398)
50. Schmitt EA, Dowling JE (1999) Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J Comp Neurol 404:515-536.
51. Schroeter EH, Wong RO, Gregg RG (2006) In vivo development of retinal ON-bipolar cell axonal terminals visualized in nyx::MYFP transgenic zebrafish. Vis Neurosci 23:833-843.
52. Stevens B (2008) Neuron-astrocyte signaling in the development and plasticity of neural circuits. Neurosignals 16:278-288.
53. Sugimura K, Yamamoto M, Niwa R, Satoh D, Goto S, Taniguchi M, Hayashi S, Uemura T (2003) Distinct developmental modes and lesion-induced reactions of dendrites of two classes of Drosophila sensory neurons. J Neurosci 23:3752-3760.
54. Takechi M, Hamaoka T, Kawamura S (2003) Fluorescence visualization of ultraviolet-sensitive cone photoreceptor development in living zebrafish. FEBS Lett 553:90-94.
55. Uga S, Smelser GK (1973) Electron microscopic study of the development of retinal Mullerian cells. Invest Ophthalmol 12:295-307.
56. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291:657-661.
57. Ullian EM, Harris BT, Wu A, Chan JR, Barres BA (2004) Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture. Mol Cell Neurosci 25:241-251.
58. Yazulla S, Studholme KM (2001) Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry. J Neurocytol 30:551-592. (Pubitemid 33816124)