The absence of complexin 3 and complexin 4 differentially impacts the on and off pathways in mouse retina

European Journal of Neuroscience

Volumn 36, Issue 4, 2012, Pages 2470-2481

  Landgraf, Immanuel ^a   Mühlhans, Johanna ^b   Dedek, Karin ^a   Reim, Kerstin ^c   Brandstätter, Johann H ^b   Ammermüller, Josef ^a  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

Amacrine cell; Bipolar cell; Ganglion cell; Photoreceptor; Synapse

Indexed keywords

CELL PROTEIN; COMPLEXIN 3; COMPLEXIN 4; SNARE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTRORETINOGRAM; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL; NONHUMAN; OFF RESPONSE; ON RESPONSE; PHOTOPIC VISION; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA; RETINA AMACRINE CELL; RETINA CONE; RETINA INNER PLEXIFORM LAYER; RETINA ROD; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; STIMULUS RESPONSE; SYNAPSE VESICLE;

ANIMALS; EYE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; RETINAL NEURONS; VISUAL PATHWAYS;

EID: 84865332357     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08149.x     Document Type: Article

References (41)

1. Bolte, S. & Cordelieres, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc., 224, 213-232.
2. Brose, N. (2008) For better or for worse: complexins regulate SNARE function and vesicle fusion. Traffic, 9, 1403-1413.
3. Cho, R.W., Song, Y. & Littleton, J.T. (2010) Comparative analysis of Drosophila and mammalian complexins as fusion clamps and facilitators of neurotransmitter release. Mol. Cell. Neurosci., 45, 389-397.
4. tom Dieck, S., Altrock, W.D., Kessels, M.M., Qualmann, B., Regus, H., Brauner, D., Fejtová, A., Bracko, O., Gundelfinger, E.D. & Brandstätter, J.H. (2005) Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol., 168, 825-836.
5. Engelkamp, D., Rashbass, P., Seawright, A. & van Heyningen, V. (1999) Role of Pax6 in development of the cerebellar system. Development, 126, 3585-3596.
6. von Gersdorff, H., Vardi, E., Matthews, G. & Sterling, P. (1996) Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron, 16, 1221-1227.
7. Giraudo, C.G., Eng, W.S., Melia, T.J. & Rothman, J.E. (2006) A clamping mechanism involved in SNARE-dependent exocytosis. Science, 313, 676-680.
8. Giraudo, C.G., Garcia-Diaz, A., Eng, W.S., Yamamoto, A., Melia, T.J. & Rothman, J.E. (2008) Distinct domains of complexins bind SNARE complexes and clamp fusion in vitro. J. Biol. Chem., 283, 21211-21219.
9. Hasegawa, J., Obara, T., Tanaka, K. & Tachibana, M. (2006) High-density presynaptic transporters are required for glutamate removal from the first visual synapse. Neuron, 50, 63-74.
10. Haverkamp, S. & Wässle, H. (2000) Immunocytochemical analysis of the mouse retina. J. Comp. Neurol., 424, 1-23.
11. Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. (1994) Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature, 371, 513-515.
12. Heidelberger, R., Thoreson, W.B. & Witkovsky, P. (2005) Synaptic transmission at retinal ribbon synapses. Prog. Retin. Eye Res., 24, 682-720.
13. Hilgen, G., von Maltzahn, J., Willecke, K., Weiler, R. & Dedek, K. (2011) Subcellular distribution of connexin45 in OFF bipolar cells of the mouse retina. J. Comp. Neurol., 519, 433-450.
14. Huntwork, S. & Littleton, J.T. (2007) A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat. Neurosci., 10, 1235-1237.
15. Jahn, R. & Scheller, R.H. (2006) SNAREs - engines for membrane fusion. Nat. Rev. Mol. Cell Biol., 7, 631-643.
16. Liang, Z. & Freed, M.A. (2010) The ON pathway rectifies the OFF pathway of the mammalian retina. J. Neurosci., 30, 5533-5543.
17. Manookin, M.B., Beaudoin, D.L., Ernst, Z.R., Flagel, L.J. & Demb, J.B. (2008) Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. J. Neurosci., 28, 4136-4150.
18. Maximov, A., Tang, J., Yang, X., Pang, Z.P. & Südhof, T.C. (2009) Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science, 323, 516-521.
19. Normann, R.A., Warren, D., Ammermüller, J., Fernandez, E. & Guillory, S. (2001) High spatio-temporal mapping of visual pathways using multi-electrode arrays. Vision. Res., 41, 1261-1275.
20. Nusinowitz, S. & Heckenlively, J.R. 2006. Evaluating retinal function in the mouse retina with the electroretinogram. In Heckenlively, J.R. & Arden, G.B. (Eds), Principles and Practice of Clinical Electrophysiology of Vision, 2nd Edn. MIT Press, Cambridge, MA, pp. 899-909.
21. Parsons, T.D. & Sterling, P. (2003) Synaptic ribbon. Conveyor belt or safety belt?. Neuron, 37, 379-382.
22. Peachey, N.S., Alexander, K.R. & Fishman, G.A. (1989) The luminance-response function of the dark-adapted human electroretinogram. Vision. Res., 29, 263-270.
23. Pow, D.V., Wright, L.L. & Vaney, D.I. (1995) The immunocytochemical detection of amino-acid neurotransmitters in paraformaldehyde-fixed tissue. J. Neurosci. Methods, 56, 115-123.
24. 2+-dependent neurotransmitter release. Cell, 104, 71-81.
25. Reim, K., Wegmeyer, H., Brandstätter, J.H., Xue, M., Rosenmund, C., Dresbach, T., Hofmann, K. & Brose, N. (2005) Structurally and functionally unique complexins at retinal ribbon synapses. J. Cell Biol., 169, 669-680.
26. Reim, K., Regus-Leidig, H., Ammermüller, J., El-Kordi, A., Radyushkin, K., Ehrenreich, H., Brandstätter, J.H. & Brose, N. (2009) Aberrant function and structure of retinal ribbon synapses in the absence of complexin 3 and complexin 4. J. Cell Sci., 122, 1352-1361.
27. Rice, D.S. & Curran, T. (2000) Disabled-1 is expressed in type AII amacrine cells in the mouse retina. J. Comp. Neurol., 424, 327-338.
28. Rowan, M.J.M., Ripps, H. & Shen, W. (2010) Fast glutamate uptake via EAAT2 shapes the cone-mediated light offset response in bipolar cells. J. Physiol., 588, 3943-3956.
29. 2+-synaptotagmin I. Nat. Struct. Mol. Biol., 13, 748-750.
30. Schwartz, E.A. (2002) Transport mediated synapses in the retina. Physiol. Rev., 82, 875-891.
31. Specht, D., tom Dieck, S., Ammermüller, J., Regus-Leidig, H., Gundelfinger, E.D. & Brandstätter, J.H. (2007) Structural and functional remodeling in the retina of a mouse with a photoreceptor synaptopathy: plasticity in the rod and degeneration in the cone system. Eur. J. Neurosci., 26, 2506-2515.
32. van Steensel, B., van Binnendijk, E.P., Hornsby, C.D., van der Voort, H.T., Krozowski, Z.S., de Kloet, E.R. & van Driel, R. (1996) Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons. J. Cell Sci., 109, 787-792.
33. Sterling, P. & Matthews, G. (2005) Structure and function of ribbon synapses. Trends Neurosci., 28, 20-29.
34. Strähle, U., Blader, P., Adam, J. & Ingham, P.W. (1994) A simple and efficient procedure for non-isotopic in situ hybridization to sectioned material. Trends Genet., 10, 75-76.
35. Szmajda, B.A. & DeVries, S.H. (2011) Glutamate spillover between mammalian cone photoreceptors. J. Neurosci., 21, 13431-13441.
36. Völgyi, B., Deans, M.R., Paul, D.L. & Bloomfield, S.A. (2004) Convergence and segregation of the multiple rod pathways in mammalian retina. J. Neurosci., 24, 11182-11192.
37. Wachtmeister, L. (1998) Oscillatory potentials in the retina: what do they reveal. Prog. Retin. Eye Res., 17, 485-521.
38. Wersinger, E., Schwab, Y., Sahel, J.-A., Rendon, A., Pow, D.V., Picaud, S. & Roux, M.J. (2006) The glutamate transporter EAAT5 works as a presynaptic receptor in mouse rod bipolar cells. J. Physiol., 577, 221-234.
39. Wojcik, S.M. & Brose, N. (2007) Regulation of membrane fusion in synaptic excitation-secretion coupling: speed and accuracy matter. Neuron, 55, 11-24.
40. Xue, M., Reim, K., Chen, X., Chao, H.-T., Deng, H., Rizo, J., Brose, N. & Rosenmund, C. (2007) Distinct domains of complexin I differentially regulate neurotransmitter release. Nat. Struct. Mol. Biol., 14, 949-958.
41. Xue, M., Lin, Y.Q., Pan, H., Reim, K., Deng, H., Bellen, H.J. & Rosenmund, C. (2009) Tilting the balance between facilitatory and inhibitory functions of mammalian and drosophila complexins orchestrates synaptic vesicle exocytosis. Neuron, 64, 367-380.