Presynaptic partner selection during retinal circuit reassembly varies with timing of neuronal regeneration in vivo

Nature Communications

Volumn 7, Issue , 2016, Pages

  Yoshimatsu, Takeshi ^a   D'Orazi, Florence D ^a   Gamlin, Clare R ^a   Suzuki, Sachihiro C ^a   Suli, Arminda ^a,b   Kimelman, David ^c   Raible, David W ^a   Wong, Rachel O ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b BRIGHAM YOUNG UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABLATION; CELLS AND CELL COMPONENTS; CONNECTIVITY; CYPRINID; EYE; ULTRAVIOLET RADIATION;

DENDRITE; NERVE REGENERATION; RETINA; SYNAPSE; SYNAPTOGENESIS; ULTRAVIOLET RADIATION; ZEBRA FISH; ANIMAL; ASSOCIATION; CONFOCAL MICROSCOPY; FLUORESCENCE IMAGING; IMMUNOHISTOCHEMISTRY; PHYSIOLOGY; REGENERATION; RETINA CONE; RETINA HORIZONTAL NERVE CELL; RETINA NERVE CELL;

DANIO RERIO;

ANIMALS; CUES; DENDRITES; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; OPTICAL IMAGING; REGENERATION; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL HORIZONTAL CELLS; RETINAL NEURONS; SYNAPSES; ULTRAVIOLET RAYS; ZEBRAFISH;

EID: 84957598061     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10590     Document Type: Article

References (50)

1. Christensen, R., Shao, Z. & Colón-Ramos, D. A. The cell biology of synaptic specificity during development. Curr. Opin. Neurobiol. 23, 1018-1026 (2013).
2. Sanes, J. R. & Yamagata, M. Many paths to synaptic specificity. Annu. Rev. Cell Dev. Biol. 25, 161-195 (2009).
3. Yogev, S. & Shen, K. Cellular and molecular mechanisms of synaptic specificity. Annu. Rev. Cell Dev. Biol. 30, 417-437 (2014).
4. Liu, X., Hirano, A. A., Sun, X., Brecha, N. C. & Barnes, S. Calcium channels in rat horizontal cells regulate feedback inhibition of photoreceptors through an unconventional GABA- and pH-sensitive mechanism. J. Physiol. 591, 3309-3324 (2013).
5. Thoreson, W. B. & Mangel, S. C. Lateral interactions in the outer retina. Prog. Retin. Eye Res. 31, 407-441 (2012).
6. Vroman, R., Klaassen, L. J. & Kamermans, M. Ephaptic communication in the vertebrate retina. Front. Hum. Neurosci. 7, 612 (2013).
7. Li, Y. N., Matsui, J. I. & Dowling, J. E. Specificity of the horizontal cellphotoreceptor connections in the zebrafish (Danio rerio) retina. J. Comp. Neurol. 516, 442-453 (2009).
8. Yoshimatsu, T. et al. Transmission from the dominant input shapes the stereotypic ratio of photoreceptor inputs onto horizontal cells. Nat. Commun. 5, 3699 (2014).
9. Lenkowski, J. R. & Raymond, P. A. Müller glia: Stem cells for generation and regeneration of retinal neurons in teleost fish. Prog. Retin. Eye Res. 40, 94-123 (2014).
10. Takechi, M., Hamaoka, T. & Kawamura, S. Fluorescence visualization of ultraviolet-sensitive cone photoreceptor development in living zebrafish. FEBS Lett. 553, 90-94 (2003).
11. Davison, J. M. et al. Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Dev. Biol. 304, 811-824 (2007).
12. Pisharath, H., Rhee, J. M., Swanson, M. A., Leach, S. D. & Parsons, M. J. Targeted ablation of beta cells in the embryonic zebrafish pancreas using E. coli nitroreductase. Mech. Dev. 124, 218-229 (2007).
13. Vihtelic, T. S. & Hyde, D. R. Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J. Neurobiol. 44, 289-307 (2000).
14. Johns, P. R. & Fernald, R. D. Genesis of rods in teleost fish retina. Nature 293, 141-142 (1981).
15. Cuenca, N. et al. Cellular responses following retinal injuries and therapeutic approaches for neurodegenerative diseases. Prog. Retin. Eye Res. 43, 17-75 (2014).
16. D'Orazi, F. D., Suzuki, S. C. & Wong, R. O. Neuronal remodeling in retinal circuit assembly, disassembly, and reassembly. Trends Neurosci. 37, 594-603 (2014).
17. Jones, B. W. & Marc, R. E. Retinal remodeling during retinal degeneration. Exp. Eye Res. 81, 123-137 (2005).
18. Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A. & Lledo, P.-M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6, 507-518 (2003).
19. Christian, K. M., Song, H. & Ming, G. Functions and dysfunctions of adult hippocampal neurogenesis. Annu. Rev. Neurosci. 37, 243-262 (2014).
20. Laplagne, D. A. et al. Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur. J. Neurosci. 25, 2973-2981 (2007).
21. Nissant, A. & Pallotto, M. Integration and maturation of newborn neurons in the adult olfactory bulb-from synapses to function. Eur. J. Neurosci. 33, 1069-1077 (2011).
22. Toni, N. et al. Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat. Neurosci. 11, 901-907 (2008).
23. Barber, A. C. et al. Repair of the degenerate retina by photoreceptor transplantation. Proc. Natl Acad. Sci. USA 110, 354-359 (2013).
24. MacLaren, R. E. et al. Retinal repair by transplantation of photoreceptor precursors. Nature 444, 203-207 (2006).
25. Magavi, S. S. P. & Lois, C. Transplanted neurons form both normal and ectopic projections in the adult brain. Dev. Neurobiol. 68, 1527-1537 (2008).
26. Michelsen, K. A. et al. Area-specific reestablishment of damaged circuits in the adult cerebral cortex by cortical neurons derived from mouse embryonic stem cells. Neuron 85, 982-997 (2015).
27. Singh, M. S. et al. Reversal of end-stage retinal degeneration and restoration of visual function by photoreceptor transplantation. Proc. Natl Acad. Sci. USA 110, 1101-1106 (2013).
28. Cline, H. T. Dendritic arbor development and synaptogenesis. Curr. Opin. Neurobiol. 11, 118-126 (2001).
29. Parrish, J. Z., Emoto, K., Kim, M. D. & Jan, Y. N. Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu. Rev. Neurosci. 30, 399-423 (2007).
30. Raven, M. A., Oh, E. C. T., Swaroop, A. & Reese, B. E. Afferent control of horizontal cell morphology revealed by genetic respecification of rods and cones. J. Neurosci. 27, 3540-3547 (2007).
31. Reese, B. E., Raven, M. A. & Stagg, S. B. Afferents and homotypic neighbors regulate horizontal cell morphology, connectivity, and retinal coverage. J. Neurosci. 25, 2167-2175 (2005).
32. Eliasieh, K., Liets, L. C. & Chalupa, L. M. Cellular reorganization in the human retina during normal aging. Invest. Ophthalmol. Vis. Sci. 48, 2824-2830 (2007).
33. Michalakis, S. et al. Characterization of neurite outgrowth and ectopic synaptogenesis in response to photoreceptor dysfunction. Cell. Mol. Life Sci. 70, 1831-1847 (2013).
34. Phillips, M. J., Otteson, D. C. & Sherry, D. M. Progression of neuronal and synaptic remodeling in the rd10 mouse model of retinitis pigmentosa. J. Comp. Neurol. 518, 2071-2089 (2010).
35. Poché, R. A. et al. Somal positioning and dendritic growth of horizontal cells are regulated by interactions with homotypic neighbors. Eur. J. Neurosci. 27, 1607-1614 (2008).
36. Samuel, M. A. et al. LKB1 and AMPK regulate synaptic remodeling in old age. Nat. Neurosci. 17, 1190-1197 (2014).
37. Haq, W., Arango-Gonzalez, B., Zrenner, E., Euler, T. & Schubert, T. Synaptic remodeling generates synchronous oscillations in the degenerated outer mouse retina. Front. Neural Circuits 8, 108 (2014).
38. Peng, Y. W., Hao, Y., Petters, R. M. & Wong, F. Ectopic synaptogenesis in the mammalian retina caused by rod photoreceptor-specific mutations. Nat. Neurosci. 3, 1121-1127 (2000).
39. Puthussery, T., Gayet-Primo, J., Pandey, S., Duvoisin, R. M. & Taylor, W. R. Differential loss and preservation of glutamate receptor function in bipolar cells in the rd10 mouse model of retinitis pigmentosa. Eur. J. Neurosci. 29, 1533-1542 (2009).
40. Strettoi, E., Mears, A. J. & Swaroop, A. Recruitment of the rod pathway by cones in the absence of rods. J. Neurosci. 24, 7576-7582 (2004).
41. Rossi, F., van der Want, J. J., Wiklund, L. & Strata, P. Reinnervation of cerebellar Purkinje cells by climbing fibres surviving a subtotal lesion of the inferior olive in the adult rat. II. Synaptic organization on reinnervated Purkinje cells. J. Comp. Neurol. 308, 536-554 (1991).
42. Ueki, Y. et al. Transgenic expression of the proneural transcription factor Ascl1 in Müller glia stimulates retinal regeneration in young mice. Proc. Natl Acad. Sci. USA 112, 13717-13722 (2015).
43. Takechi, M., Seno, S. & Kawamura, S. Identification of cis-acting elements repressing blue opsin expression in zebrafish UV cones and pineal cells. J. Biol. Chem. 283, 31625-31632 (2008).
44. Salbreux, G., Barthel, L. K., Raymond, P. A. & Lubensky, D. K. Coupling mechanical deformations and planar cell polarity to create regular patterns in the zebrafish retina. PLoS Comput. Biol. 8, e1002618 (2012).
45. Kwan, K. M. et al. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099 (2007).
46. Suli, A., Guler, A. D., Raible, D. W. & Kimelman, D. A targeted gene expression system using the tryptophan repressor in zebrafish shows no silencing in subsequent generations. Development 141, 1167-1174 (2014).
47. Shields, C. R. et al. Retinal horizontal cell-specific promoter activity and protein expression of zebrafish connexin 52.6 and connexin 55.5. J. Comp. Neurol. 501, 765-779 (2007).
48. Suzuki, S. C. et al. Cone photoreceptor types in zebrafish are generated by symmetric terminal divisions of dedicated precursors. Proc. Natl Acad. Sci. USA 110, 15109-15114 (2013).
49. Neef, A. B. & Luedtke, N. W. Dynamic metabolic labeling of DNA in vivo with arabinosyl nucleosides. Proc. Natl Acad. Sci. USA 108, 20404-20409 (2011).
50. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).