Optogenetic Probing and Manipulation of the Calyx-Type Presynaptic Terminal in the Embryonic Chick Ciliary Ganglion

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Egawa, Ryo ^a,b   Hososhima, Shoko ^a,b   Hou, Xubin ^a,d   Katow, Hidetaka ^a,b   Ishizuka, Toru ^a,b   Nakamura, Harukazu ^a   Yawo, Hiromu ^a,b,c  

^a TOHOKU UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NIIGATA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CRE RECOMBINASE; CYAN FLUORESCENT PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; RED FLUORESCENT PROTEIN; RHODOPSIN; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL NUCLEUS; CILIARY GANGLION; CONTROLLED STUDY; DNA MODIFICATION; ELECTROPORATION; EMBRYO; EVOKED RESPONSE; EXPRESSION VECTOR; EXTRACELLULAR CALCIUM; FLUORESCENCE ANALYSIS; GENE EXPRESSION; GENETIC VARIABILITY; MOLECULAR PROBE; MOLECULAR SENSOR; NERVE ENDING; NERVE POTENTIAL; NONHUMAN; OPTOGENETICS; PHOTOSTIMULATION; PRESYNAPTIC NERVE; PROTEIN EXPRESSION; STEM CELL;

ACTION POTENTIALS; ANIMALS; AXONS; CALCIUM; CELL NUCLEUS; CHICK EMBRYO; ELECTROPORATION; GANGLIA, PARASYMPATHETIC; GENE EXPRESSION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; ION TRANSPORT; LIGHT; NERVE TISSUE PROTEINS; OPTOGENETICS; PRESYNAPTIC TERMINALS; SYNAPSES; SYNAPTIC TRANSMISSION; TRANSFECTION;

EID: 84875304262     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059179     Document Type: Article

References (72)

1. Jessell TM, Kandel ER, (1993) Synaptic transmission: a bidirectional and self-modifiable form of cell-cell communication. Cell 72Suppl: 1-30.
2. Atwood HL, Karunanithi S, (2002) Diversification of synaptic strength: presynaptic elements. Nat Rev Neurosci 3: 497-516.
3. Reid CA, Bekkers JM, Clements JD, (2003) Presynaptic Ca2+ channels: a functional patchwork. Trends Neurosci 26: 683-687.
4. Schneggenburger R, Neher E, (2005) Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15: 266-274.
5. Jahn R, Fasshauer D, (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490: 201-207.
6. Yamashita T, (2012) Ca2+-dependent regulation of synaptic vesicle endocytosis. Neurosci Res 73: 1-7.
7. Landmesser L, Pilar G, (1972) The onset and development of transmission in the chick ciliary ganglion. J Physiol 222: 691-713.
8. Stanley EF, (1992) The calyx-type synapse of the chick ciliary ganglion as a model of fast cholinergic transmission. Can J Physiol Pharmacol 70Suppl: S73-77.
9. Dryer SE, (1994) Functional development of the parasympathetic neurons of the avian ciliary ganglion: a classic model system for the study of neuronal differentiation and development. Prog Neurobiol 43: 281-322.
10. De Lorenzo AJ, (1960) The fine structure of synapses in the ciliary ganglion of the chick. J Biophys Biochem Cytol 7: 31-36.
11. Takahashi K, Hama K, (1965) Some observations on the fine structure of nerve cell bodies and their satellite cells in the ciliary ganglion of the chick. Z Zellforsch Mikrosk Anat 67: 835-843.
12. Fujiwara T, Nagakuro C, (1989) Three-dimensional structure of the presynaptic nerve ending in the ciliary ganglion of the chick embryo: a scanning electron microscopic study. Neurosci Lett 98: 125-128.
13. Martin AR, Pilar G, (1963) Dual mode of synaptic transmission in the avian ciliary ganglion. J Physiol 168: 443-463.
14. Martin AR, Pilar G, (1964) Quantal components of the synaptic potential in the ciliary ganglion of the chick. J Physiol 175: 1-16.
15. Martin AR, Pilar G, (1964) Presynaptic and post-synaptic events during post-tetanic potentiation and facilitation in the avian ciliary ganglion. J Physiol 175: 17-30.
16. Martin AR, Patel V, Faille L, Mallart A, (1989) Presynaptic calcium currents recorded from calyciform nerve terminals in the lizard ciliary ganglion. Neurosci Lett 105: 14-18.
17. Stanley EF, (1989) Calcium currents in a vertebrate presynaptic nerve terminal: the chick ciliary ganglion calyx. Brain Res 505: 341-345.
18. Stanley EF, Goping G, (1991) Characterization of a calcium current in a vertebrate cholinergic presynaptic nerve terminal. J Neurosci 11: 985-993.
19. Yawo H, Momiyama A, (1993) Re-evaluation of calcium currents in pre- and postsynaptic neurones of the chick ciliary ganglion. J Physiol 460: 153-172.
20. Yawo H, Chuhma N, (1993) Preferential inhibition of ω-conotoxin-sensitive presynaptic Ca2+ channels by adenosine autoreceptors. Nature 365: 256-258.
21. Livet J, Weissman TA, Kang H, Draft RW, Lu J, et al. (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450: 56-62.
22. Lichtman JW, Denk W, (2011) The big and the small: challenges of imaging the brain's circuits. Science 334: 618-623.
23. Miesenböck G, (2004) Genetic methods for illuminating the function of neural circuits. Curr Opin Neurobiol 14: 395-402.
24. Herlitze S, Landmesser LT, (2007) New optical tools for controlling neuronal activity. Curr Opin Neurobiol 17: 87-94.
25. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K, (2011) Optogenetics in neural systems. Neuron 71: 9-34.
26. Momose T, Tonegawa A, Takeuchi J, Ogawa H, Umesono K, et al. (1999) Efficient targeting of gene expression in chick embryos by microelectroporation. Dev Growth Differ 41: 335-344.
27. Odani N, Ito K, Nakamura H, (2008) Electroporation as an efficient method of gene transfer. Dev Growth Differ 50: 443-448.
28. Knöpfel T, Lin MZ, Levskaya A, Tian L, Lin JY, et al. (2010) Toward the second generation of optogenetic tools. J Neurosci 30: 14998-15004.
29. Zhao Y, Araki S, Wu J, Teramoto T, Chang YF, et al. (2011) An expanded palette of genetically encoded Ca2+ indicators. Science 333: 1888-1891.
30. Wang H, Sugiyama Y, Hikima T, Sugano E, Tomita H, et al. (2009) Molecular determinants differentiating photocurrent properties of two channelrhodopsins from chlamydomonas. J Biol Chem 284: 5685-5696.
31. Mattis J, Tye KM, Ferenczi EA, Ramakrishnan C, O'Shea DJ, et al. (2012) Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat Methods 9: 159-172.
32. Lichtman JW, Livet J, Sanes JR, (2008) A technicolour approach to the connectome. Nat Rev Neurosci 9: 417-422.
33. Hampel S, Chung P, McKellar CE, Hall D, Looger LL, et al. (2011) Drosophila Brainbow: a recombinase-based fluorescence labeling technique to subdivide neural expression patterns. Nat Methods 8: 253-259.
34. Hadjieconomou D, Rotkopf S, Alexandre C, Bell DM, Dickson BJ, et al. (2011) Flybow: genetic multicolor cell labeling for neural circuit analysis in Drosophila melanogaster. Nat Methods 8: 260-266.
35. Pan YA, Livet J, Sanes JR, Lichtman JW, Schier AF (2011) Multicolor Brainbow imaging in zebrafish. Cold Spring Harb Protoc 2011: pdb prot5546.
36. Kobiler O, Lipman Y, Therkelsen K, Daubechies I, Enquist LW, (2010) Herpesviruses carrying a Brainbow cassette reveal replication and expression of limited numbers of incoming genomes. Nat Commun 1: 146.
37. Card JP, Kobiler O, Ludmir EB, Desai V, Sved AF, et al. (2011) A dual infection pseudorabies virus conditional reporter approach to identify projections to collateralized neurons in complex neural circuits. PLoS One 6: e21141.
38. Card JP, Kobiler O, McCambridge J, Ebdlahad S, Shan Z, et al. (2011) Microdissection of neural networks by conditional reporter expression from a Brainbow herpesvirus. Proc Natl Acad Sci U S A 108: 3377-3382.
39. Changeux JP, Danchin A, (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264: 705-712.
40. Kasthuri N, Lichtman JW, (2004) Structural dynamics of synapses in living animals. Curr Opin Neurobiol 14: 105-111.
41. Luo L, O'Leary DD, (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28: 127-156.
42. Low LK, Cheng HJ, (2006) Axon pruning: an essential step underlying the developmental plasticity of neuronal connections. Philos Trans R Soc Lond B Biol Sci 361: 1531-1544.
43. Saxena S, Caroni P, (2007) Mechanisms of axon degeneration: from development to disease. Prog Neurobiol 83: 174-191.
44. Bishop DL, Misgeld T, Walsh MK, Gan WB, Lichtman JW, (2004) Axon branch removal at developing synapses by axosome shedding. Neuron 44: 651-661.
45. Song JW, Misgeld T, Kang H, Knecht S, Lu J, et al. (2008) Lysosomal activity associated with developmental axon pruning. J Neurosci 28: 8993-9001.
46. Ekdahl CT, (2012) Microglial activation- tuning and pruning adult neurogenesis. Front Pharmacol 3: 41.
47. Catterall WA, (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16: 521-555.
48. Yawo H, Chuhma N, (1994) ω-Conotoxin-sensitive and-resistant transmitter release from the chick ciliary presynaptic terminal. J Physiol-London 477: 437-448.
49. Stanley EF, Atrakchi AH, (1990) Calcium currents recorded from a vertebrate presynaptic nerve terminal are resistant to the dihydropyridine nifedipine. Proc Natl Acad Sci U S A 87: 9683-9687.
50. Yawo H, (1993) Diversity of calcium channel subtypes in presynaptic terminals of the chick ciliary ganglion. Ann N Y Acad Sci 707: 379-381.
51. Robitaille R, Garcia ML, Kaczorowski GJ, Charlton MP, (1993) Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron 11: 645-655.
52. Haydon PG, Henderson E, Stanley EF, (1994) Localization of individual calcium channels at the release face of a presynaptic nerve terminal. Neuron 13: 1275-1280.
53. Khanna R, Li Q, Bewersdorf J, Stanley EF, (2007) The presynaptic CaV2.2 channel-transmitter release site core complex. Eur J Neurosci 26: 547-559.
54. Llinas R, Sugimori M, Silver RB, (1992) Microdomains of high calcium concentration in a presynaptic terminal. Science 256: 677-679.
55. Wachman ES, Poage RE, Stiles JR, Farkas DL, Meriney SD, (2004) Spatial distribution of calcium entry evoked by single action potentials within the presynaptic active zone. J Neurosci 24: 2877-2885.
56. von Gersdorff H, Borst JGG, (2002) Short-term plasticity at the calyx of Held. Nat Rev Neurosci 3: 53-64.
57. Xu JH, He LM, Wu LG, (2007) Role of Ca2+ channels in short-term synaptic plasticity. Curr Opin Neurobiol 17: 352-359.
58. Catterall WA, Few AP, (2008) Calcium channel regulation and presynaptic plasticity. Neuron 59: 882-901.
59. Neher E, Sakaba T, (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872.
60. Mochida S, (2011) Activity-dependent regulation of synaptic vesicle exocytosis and presynaptic short-term plasticity. Neurosci Res 70: 16-23.
61. Peron S, Svoboda K, (2011) From cudgel to scalpel: toward precise neural control with optogenetics. Nat Methods 8: 30-34.
62. Madisen L, Mao T, Koch H, Zhuo J, Berenyi A, et al. (2012) A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci 15: 793-802.
63. Awatramani GB, Price GD, Trussell LO, (2005) Modulation of transmitter release by presynaptic resting potential and background calcium levels. Neuron 48: 109-121.
64. Schneggenburger R, Sakaba T, Neher E, (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25: 206-212.
65. Borst JGG, van Hoeve JS, (2012) The calyx of held synapse: from model synapse to auditory relay. Annu Rev Physiol 74: 199-224.
66. Kochubey O, Lou XL, Schneggenburger R, (2011) Regulation of transmitter release by Ca2+ and synaptotagmin: insights from a large CNS synapse. Trends Neurosci 34: 237-246.
67. Hamburger V, Hamilton HL, (1951) A series of normal egg stages in the development of the chick embryo. J Morphol 88: 49-92.
68. Hou X, Omi M, Harada H, Ishii S, Takahashi Y, et al. (2011) Conditional knockdown of target gene expression by tetracycline regulated transcription of double strand RNA. Dev Growth Differ 53: 69-75.
69. Yawo H, (1999) Involvement of cGMP-dependent protein kinase in adrenergic potentiation of transmitter release from the calyx-type presynaptic terminal. J Neurosci 19: 5293-5300.
70. Yawo H (2012) Whole-Cell Patch Method. In: Okada Y, editor. Patch-Clamp Techniques: From Beginning to Advanced Protocols. Heidelberg: Springer: 43-69.
71. Wan Y, Otsuna H, Chien CB, Hansen C, (2009) An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research. IEEE Trans Vis Comput Graph 15: 1489-1496.
72. Dehpour AR, Mofakham S, Mahmoudian M, (1982) In vitro binding of dentrolene to sarcoplasmic reticulum of rabbit skeletal muscle. Biochm Pharmacol 31: 965-968.