Calcium Channel-Dependent Molecular Maturation of Photoreceptor Synapses

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Zabouri, Nawal ^a   Haverkamp, Silke ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN BASSOON; PROTEIN RIM2; PROTEIN VELI3; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL VACUOLE; CONTROLLED STUDY; EYE MOVEMENT; KNOCKOUT MOUSE; MORPHOLOGY; MOUSE; NERVE SPROUTING; NONHUMAN; PHOTORECEPTOR; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RETINA CONE; RETINA DEVELOPMENT; SYNAPSE; SYNAPTOGENESIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGING; ANIMALS; ANIMALS, NEWBORN; CALCIUM CHANNELS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GUANYLATE KINASE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE TISSUE PROTEINS; RAB3 GTP-BINDING PROTEINS; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; SYNAPSES;

EID: 84877674003     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063853     Document Type: Article

References (71)

1. Mercer AJ, Thoreson WB, (2011) The dynamic architecture of photoreceptor ribbon synapses: cytoskeletal, extracellular matrix, and intramembrane proteins. Vis Neurosci 28: 453-471.
2. Nachman-Clewner M, St Jules R, Townes-Anderson E, (1999) L-type calcium channels in the photoreceptor ribbon synapse: localization and role in plasticity. J Comp Neurol 415: 1-16.
3. Morgans CW, (2001) Localization of the alpha(1F) calcium channel subunit in the rat retina. Invest Ophthalmol Vis Sci 42: 2414-2418.
4. Xiao H, Chen X, Steele EC Jr, (2007) Abundant L-type calcium channel Ca(v)1.3 (alpha1D) subunit mRNA is detected in rod photoreceptors of the mouse retina via in situ hybridization. Mol Vis 13: 764-771.
5. Kersten FF, van Wijk E, van Reeuwijk J, van der Zwaag B, Marker T, et al. (2010) Association of whirlin with Cav1.3 (alpha1D) channels in photoreceptors, defining a novel member of the usher protein network. Invest Ophthalmol Vis Sci 51: 2338-2346.
6. Bech-Hansen NT, Naylor MJ, Maybaum TA, Pearce WG, Koop B, et al. (1998) Loss-of-function mutations in a calcium-channel alpha1-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nat Genet 19: 264-267.
7. Platzer J, Engel J, Schrott-Fischer A, Stephan K, Bova S, et al. (2000) Congenital deafness and sinoatrial node dysfunction in mice lacking class D L-type Ca2+ channels. Cell 102: 89-97.
8. Mansergh F, Orton NC, Vessey JP, Lalonde MR, Stell WK, et al. (2005) Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Hum Mol Genet 14: 3035-3046.
9. Wu J, Marmorstein AD, Striessnig J, Peachey NS, (2007) Voltage-dependent calcium channel CaV1.3 subunits regulate the light peak of the electroretinogram. J Neurophysiol 97: 3731-3735.
10. Specht D, Wu SB, Turner P, Dearden P, Koentgen F, et al. (2009) Effects of presynaptic mutations on a postsynaptic Cacna1s calcium channel colocalized with mGluR6 at mouse photoreceptor ribbon synapses. Invest Ophthalmol Vis Sci 50: 505-515.
11. Chang B, Heckenlively JR, Bayley PR, Brecha NC, Davisson MT, et al. (2006) The nob2 mouse, a null mutation in Cacna1f: anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Vis Neurosci 23: 11-24.
12. Sheets L, Kindt KS, Nicolson T, (2012) Presynaptic CaV1.3 Channels Regulate Synaptic Ribbon Size and Are Required for Synaptic Maintenance in Sensory Hair Cells. J Neurosci 32: 17273-17286.
13. Strom TM, Nyakatura G, Apfelstedt-Sylla E, Hellebrand H, Lorenz B, et al. (1998) An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nat Genet 19: 260-263.
14. Doering CJ, Rehak R, Bonfield S, Peloquin JB, Stell WK, et al. (2008) Modified Ca(v)1.4 expression in the Cacna1f(nob2) mouse due to alternative splicing of an ETn inserted in exon 2. PLoS One 3: e2538.
15. Lodha N, Bonfield S, Orton NC, Doering CJ, McRory JE, et al. (2010) Congenital stationary night blindness in mice- a tale of two Cacna1f mutants. Adv Exp Med Biol 664: 549-558.
16. Bayley PR, Morgans CW, (2007) Rod bipolar cells and horizontal cells form displaced synaptic contacts with rods in the outer nuclear layer of the nob2 retina. J Comp Neurol 500: 286-298.
17. Raven MA, Orton NC, Nassar H, Williams GA, Stell WK, et al. (2008) Early afferent signaling in the outer plexiform layer regulates development of horizontal cell morphology. J Comp Neurol 506: 745-758.
18. Regus-Leidig H, Tom Dieck S, Specht D, Meyer L, Brandstatter JH, (2009) Early steps in the assembly of photoreceptor ribbon synapses in the mouse retina: the involvement of precursor spheres. J Comp Neurol 512: 814-824.
19. Wei T, Schubert T, Paquet-Durand F, Tanimoto N, Chang L, et al. (2012) Light-driven calcium signals in mouse cone photoreceptors. J Neurosci 32: 6981-6994.
20. D'Ascenzo M, Piacentini R, Casalbore P, Budoni M, Pallini R, et al. (2006) Role of L-type Ca2+ channels in neural stem/progenitor cell differentiation. Eur J Neurosci 23: 935-944.
21. Kulbatski I, Cook DJ, Tator CH, (2004) Calcium entry through L-type calcium channels is essential for neurite regeneration in cultured sympathetic neurons. J Neurotrauma 21: 357-374.
22. Heck N, Golbs A, Riedemann T, Sun JJ, Lessmann V, et al. (2008) Activity-dependent regulation of neuronal apoptosis in neonatal mouse cerebral cortex. Cereb Cortex 18: 1335-1349.
23. McRory JE, Hamid J, Doering CJ, Garcia E, Parker R, et al. (2004) The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. J Neurosci 24: 1707-1718.
24. Pfeiffer-Guglielmi B, Fleckenstein B, Jung G, Hamprecht B, (2003) Immunocytochemical localization of glycogen phosphorylase isozymes in rat nervous tissues by using isozyme-specific antibodies. J Neurochem 85: 73-81.
25. Zhang H, Cuenca N, Ivanova T, Church-Kopish J, Frederick JM, et al. (2003) Identification and light-dependent translocation of a cone-specific antigen, cone arrestin, recognized by monoclonal antibody 7G6. Invest Ophthalmol Vis Sci 44: 2858-2867.
26. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, et al. (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.
27. Brandstatter JH, Fletcher EL, Garner CC, Gundelfinger ED, Wassle H, (1999) Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina. Eur J Neurosci 11: 3683-3693.
28. Dick O, tom Dieck S, Altrock WD, Ammermuller J, Weiler R, et al. (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37: 775-786.
29. Stohr H, Molday LL, Molday RS, Weber BH, Biedermann B, et al. (2005) Membrane-associated guanylate kinase proteins MPP4 and MPP5 associate with Veli3 at distinct intercellular junctions of the neurosensory retina. J Comp Neurol 481: 31-41.
30. Koulen P, Fletcher EL, Craven SE, Bredt DS, Wassle H, (1998) Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J Neurosci 18: 10136-10149.
31. Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, et al. (2003) Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J Neurosci 23: 518-529.
32. von Kriegstein K, Schmitz F, (2003) The expression pattern and assembly profile of synaptic membrane proteins in ribbon synapses of the developing mouse retina. Cell Tissue Res 311: 159-173.
33. Wang Y, Okamoto M, Schmitz F, Hofmann K, Sudhof TC, (1997) Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388: 593-598.
34. Bello OD, Zanetti MN, Mayorga LS, Michaut MA, (2012) RIM, Munc13, and Rab3A interplay in acrosomal exocytosis. Exp Cell Res 318: 478-488.
35. Landgraf I, Muhlhans J, Dedek K, Reim K, Brandstatter JH, et al. (2012) The absence of Complexin 3 and Complexin 4 differentially impacts the ON and OFF pathways in mouse retina. Eur J Neurosci.
36. Reim K, Wegmeyer H, Brandstatter JH, Xue M, Rosenmund C, et al. (2005) Structurally and functionally unique complexins at retinal ribbon synapses. J Cell Biol 169: 669-680.
37. Reim K, Regus-Leidig H, Ammermuller J, El-Kordi A, Radyushkin K, et al. (2009) Aberrant function and structure of retinal ribbon synapses in the absence of complexin 3 and complexin 4. J Cell Sci 122: 1352-1361.
38. Von Kriegstein K, Schmitz F, Link E, Sudhof TC, (1999) Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur J Neurosci 11: 1335-1348.
39. Schiviz AN, Ruf T, Kuebber-Heiss A, Schubert C, Ahnelt PK, (2008) Retinal cone topography of artiodactyl mammals: influence of body height and habitat. J Comp Neurol 507: 1336-1350.
40. Haverkamp S, Wassle H, Duebel J, Kuner T, Augustine GJ, et al. (2005) The primordial, blue-cone color system of the mouse retina. J Neurosci 25: 5438-5445.
41. Wassle H, Regus-Leidig H, Haverkamp S, (2006) Expression of the vesicular glutamate transporter vGluT2 in a subset of cones of the mouse retina. J Comp Neurol 496: 544-555.
42. Hombrebueno JR, Tsai MM, Kim HL, De Juan J, Grzywacz NM, et al. (2010) Morphological changes of short-wavelength cones in the developing S334ter-3 transgenic rat. Brain Res 1321: 60-66.
43. Puller C, Haverkamp S, (2011) Cell-type-specific localization of protocadherin beta16 at AMPA and AMPA/Kainate receptor-containing synapses in the primate retina. J Comp Neurol 519: 467-479.
44. Haverkamp S, Wassle H, (2000) Immunocytochemical analysis of the mouse retina. J Comp Neurol 424: 1-23.
45. Negishi K, Kato S, Teranishi T, (1988) Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neurosci Lett 94: 247-252.
46. Hu SS, Arnold A, Hutchens JM, Radicke J, Cravatt BF, et al. (2010) Architecture of cannabinoid signaling in mouse retina. J Comp Neurol 518: 3848-3866.
47. Sherry DM, Wang MM, Bates J, Frishman LJ, (2003) Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465: 480-498.
48. Specht D, Tom Dieck S, Ammermuller J, Regus-Leidig H, Gundelfinger ED, et al. (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.
49. Michalakis S, Schaferhoff K, Spiwoks-Becker I, Zabouri N, Koch S, et al. (2012) Characterization of neurite outgrowth and ectopic synaptogenesis in response to photoreceptor dysfunction. Cell Mol Life Sci.
50. Regus-Leidig H, tom Dieck S, Brandstatter JH, (2010) Absence of functional active zone protein Bassoon affects assembly and transport of ribbon precursors during early steps of photoreceptor synaptogenesis. Eur J Cell Biol 89: 468-475.
51. Lv C, Gould TJ, Bewersdorf J, Zenisek D, (2012) High-Resolution Optical Imaging of Zebrafish Larval Ribbon Synapse Protein RIBEYE, RIM2, and CaV 1.4 by Stimulation Emission Depletion Microscopy. Microsc Microanal 18: 745-752.
52. Elferink LA, Scheller RH, (1995) Synaptic vesicle proteins and regulated exocytosis. Prog Brain Res 105: 79-85.
53. Santos MS, Li H, Voglmaier SM, (2009) Synaptic vesicle protein trafficking at the glutamate synapse. Neuroscience 158: 189-203.
54. Cote PD, De Repentigny Y, Coupland SG, Schwab Y, Roux MJ, et al. (2005) Physiological maturation of photoreceptors depends on the voltage-gated sodium channel NaV1.6 (Scn8a). J Neurosci 25: 5046-5050.
55. Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD, et al. (2000) The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27: 513-523.
56. Olney JW, (1968) An electron microscopic study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina. Invest Ophthalmol 7: 250-268.
57. Blanks JC, Adinolfi AM, Lolley RN, (1974) Synaptogenesis in the photoreceptor terminal of the mouse retina. J Comp Neurol 156: 81-93.
58. Rich KA, Zhan Y, Blanks JC, (1997) Migration and synaptogenesis of cone photoreceptors in the developing mouse retina. J Comp Neurol 388: 47-63.
59. Omori Y, Araki F, Chaya T, Kajimura N, Irie S, et al. (2012) Presynaptic Dystroglycan-Pikachurin Complex Regulates the Proper Synaptic Connection between Retinal Photoreceptor and Bipolar Cells. J Neurosci 32: 6126-6137.
60. Nishimune H, Numata T, Chen J, Aoki Y, Wang Y, et al. (2012) Active zone protein bassoon co-localizes with presynaptic calcium channel, modifies channel function, and recovers from aging related loss by exercise. PLoS One 7: e38029.
61. Frank T, Rutherford MA, Strenzke N, Neef A, Pangrsic T, et al. (2010) Bassoon and the synaptic ribbon organize Ca(2)+ channels and vesicles to add release sites and promote refilling. Neuron 68: 724-738.
62. Xing W, Akopian A, Krizaj D, (2012) Trafficking of presynaptic PMCA signaling complexes in mouse photoreceptors requires Cav1.4 alpha1 subunits. Adv Exp Med Biol 723: 739-744.
63. Aartsen WM, Arsanto JP, Chauvin JP, Vos RM, Versteeg I, et al. (2009) PSD95beta regulates plasma membrane Ca2+ pump localization at the photoreceptor synapse. Mol Cell Neurosci 41: 156-165.
64. Aartsen WM, Kantardzhieva A, Klooster J, van Rossum AG, van de Pavert SA, et al. (2006) Mpp4 recruits Psd95 and Veli3 towards the photoreceptor synapse. Hum Mol Genet 15: 1291-1302.
65. tom Dieck S, Specht D, Strenzke N, Hida Y, Krishnamoorthy V, et al. (2012) Deletion of the Presynaptic Scaffold CAST Reduces Active Zone Size in Rod Photoreceptors and Impairs Visual Processing. J Neurosci 32: 12192-12203.
66. Haeseleer F, Imanishi Y, Maeda T, Possin DE, Maeda A, et al. (2004) Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci 7: 1079-1087.
67. Haverkamp S, Michalakis S, Claes E, Seeliger MW, Humphries P, et al. (2006) Synaptic plasticity in CNGA3(-/-) mice: cone bipolar cells react on the missing cone input and form ectopic synapses with rods. J Neurosci 26: 5248-5255.
68. Peng YW, Hao Y, Petters RM, Wong F, (2000) Ectopic synaptogenesis in the mammalian retina caused by rod photoreceptor-specific mutations. Nat Neurosci 3: 1121-1127.
69. Fei Y, (2002) Cone neurite sprouting: an early onset abnormality of the cone photoreceptors in the retinal degeneration mouse. Mol Vis 8: 306-314.
70. Lin B, Masland RH, Strettoi E, (2009) Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp Eye Res 88: 589-599.
71. Beutner D, Moser T, (2001) The presynaptic function of mouse cochlear inner hair cells during development of hearing. J Neurosci 21: 4593-4599.