Targeted expression of channelrhodopsin-2 to the axon initial segment alters the temporal firing properties of retinal ganglion cells

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Zhang, Zhifei ^a   Feng, Jie ^a,b   Wu, Chaowen ^a   Lu, Qi ^a   Pan, Zhuo Hua ^a,c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^c WAYNE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; MEMBRANE CHANNEL; NERVE FIBER; NONHUMAN; RETINA GANGLION CELL; SPIKE; TRANSIENT EXPRESSION; VISION; ACTION POTENTIAL; ANIMAL; AXON; C57BL MOUSE; CYTOLOGY; DEPENDOPARVOVIRUS; ENZYME IMMUNOASSAY; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY;

CHANNELRHODOPSIN 2, MOUSE; RHODOPSIN; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIALS; ANIMALS; AXONS; DEPENDOVIRUS; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED C57BL; RETINAL GANGLION CELLS; RHODOPSIN; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84951185901     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142052     Document Type: Article

References (26)

1. Rasband MN (2010) The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 11:552-562. doi: 10.1038/nrn2852 PMID: 20631711
2. Gradinaru V, Thompson KR, Zhang F, Mogri M, Kay K, Schneider MB, et al. (2007) Targeting and readout strategies for fast optical neural control in vitro and in vivo. J Neurosci 27:14231-14238. PMID: 18160630
3. Lewis TL, Mao T, Svoboda K, Arnold DB (2009) Myosin-dependent targeting of transmembrane proteins to neuronal dendrites. Nat Neurosci 12:568-576. doi: 10.1038/nn.2318 PMID: 19377470
4. Grubb MS, Burrone J (2010) Channelrhodopsin-2 localised to the axon initial segment. PLoS One 5: e13761. doi: 10.1371/journal.pone.0013761 PMID: 21048938
5. Bi A, Cui J, Ma YP, Olshevskaya E, Pu M, Dizhoor AM, et al. (2006) Ectopic expression of a microbialtype rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50:23-33. PMID: 16600853
6. Tomita H, Sugano E, Yawo H, Ishizuka T, Isago H, Narikawa S, et al. (2007) Restoration of visual response in aged dystrophic RCS rats using AAV-mediated channelopsin-2 gene transfer. Invest Ophthalmol Vis Sci 48:3821-3826. PMID: 17652757
7. Lin B, Koizumi A, Tanaka N, Panda S, Masland RH (2008). Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc Natl Acad Sci USA. 105:16009-16014. doi: 10.1073/pnas.0806114105 PMID: 18836071
8. Boycott B, Wassle H (1999) Parallel processing in the mammalian retina: the Proctor Lecture. Invest Ophthalmol Vis Sci 40:1313-1327. PMID: 10359312
9. Jacobs AL, Werblin FS (1998) Spatiotemporal patterns at the retinal output. J Neurophysiol 80:447-451. PMID: 9658062
10. Naundorf B, Wolf F, Volgushev M (2006) Unique features of action potential initiation in cortical neurons. Nature 440:1060-1063. PMID: 16625198
11. Kole MH, Letzkus JJ, Stuart GJ (2007) Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55:633-647. PMID: 17698015
12. Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ (2008) Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11:178-186. doi: 10.1038/nn2040 PMID: 18204443
13. Zhou D, Lambert S, Malen PL, Carpenter S, Boland LM, Bennett V (1998) AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol 143:1295-1304. PMID: 9832557
14. Jenkins SM, Bennett V (2001) Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol 155:739-746. PMID: 11724816
15. Garrido JJ, Giraud P, Carlier E, Fernandes F, Moussif A, Fache MP, et al. (2003) A targeting motif involved in sodium channel clustering at the axonal initial segment. Science 300:2091-2094. PMID: 12829783
16. Lemaillet G, Walker B, Lambert S (2003) Identification of a conserved ankyrin-binding motif in the family of sodium channel alpha subunits. J Biol Chem 278:27333-27339. PMID: 12716895
17. Wu C, Ivanova E, Cui J, Lu Q, Pan ZH (2011) Action potential generation at an axon initial segment-like process in the axonless retinal AII amacrine cell. J Neurosci 31:14654-14659. doi: 10.1523/JNEUROSCI.1861-11.2011 PMID: 21994381
18. Tian N, Copenhagen DR (2003) Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39:85-96. PMID: 12848934
19. Zhang Y, Ivanova E, Bi A, Pan ZH (2009) Ectopic expression of multiple microbial rhodopsins restores ON and OFF light responses in retinas with photoreceptor degeneration. J Neurosci 29:9186-9196. doi: 10.1523/JNEUROSCI.0184-09.2009 PMID: 19625509
20. Van Wart A, Matthews G (2006) Impaired firing and cell-specific compensation in neurons lacking nav1.6 sodium channels. J Neurosci 26:7172-7180. PMID: 16822974
21. Van Wart A, Trimmer JS, Matthews G (2007) Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol 500:339-352. PMID: 17111377
22. Pan Z, Kao T, Horvath Z, Lemos J, Sul JY, Cranstoun SD, et al. (2006) A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci 26:2599-2613. PMID: 16525039
23. Goldberg EM, Clark BD, Zagha E, Nahmani M, Erisir A, Rudy B (2008) K+ channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 58:387-400. doi: 10.1016/j.neuron.2008.03.003 PMID: 18466749
24. Greenberg KP, Pham A, Werblin FS (2011) Differential targeting of optical neuromodulators to ganglion cell soma and dendrites allows dynamic control of center-surround antagonism. Neuron 69:713-720. doi: 10.1016/j.neuron.2011.01.024 PMID: 21338881
25. Wu C, Ivanova E, Zhang Y, Pan ZH (2013) rAAV-mediated subcellular targeting of optogenetic tools in retinal ganglion cells in vivo. PloS one 8:e66332. doi: 10.1371/journal.pone.0066332 PMID: 23799092
26. Awatramani GB, Slaughter MM. (2000) Origin of transient and sustained responses in ganglion cells of the retina. J Neurosci 20:7087-7095. PMID: 10995856