Influence of the β2-subunit of L-type voltage-gated Cav channels on the structural and functional development of photoreceptor ribbon synapses

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 4, 2015, Pages 2312-2324

  Katiyar, Rashmi ^a   Weissgerber, Petra ^a   Roth, Elisabeth ^a   Dörr, Janka ^a   Sothilingam, Vithiyanjali ^b   Garrido, Marina Garcia ^b   Beck, Susanne C ^b   Seeliger, Mathias W ^b   Beck, Andreas ^a   Schmitz, Frank ^a   Flockerzi, Veit ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Ca channel; Cavbeta subunit; RIBEYE; Synaptic ribbon

Indexed keywords

MYOSIN HEAVY CHAIN; PEANUT AGGLUTININ; VOLTAGE GATED CALCIUM CHANNEL; CACNB2 PROTEIN, MOUSE; CALCIUM CHANNEL L TYPE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; GENE EXPRESSION; GENOTYPE; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC TRANSMISSION; TRANSGENE; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANIMAL; FEMALE; MALE; METABOLISM; RETINA CONE; RETINA ROD; SYNAPTOSOME; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; BLOTTING, WESTERN; CALCIUM CHANNELS, L-TYPE; ELECTRORETINOGRAPHY; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; PRESYNAPTIC TERMINALS; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84939484121     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-16654     Document Type: Article

References (57)

1. Heidelberger R, Thoreson WB, Witkovsky P. Synaptic transmission at retinal ribbon synapses. Progr Retin Eye Res. 2005; 24:682-720.
2. Matthews G, Fuchs P. The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci. 2010;11:812-822.
3. Schmitz F. The making of synaptic ribbons: how they are built and what they do. Neuroscientist. 2009;15:611-624.
4. Schmitz F. Presynaptic Ca2+ and GCAPs: aspects on the structure and function of photoreceptor ribbon synapses. Front Mol Neurosci. 2014;7:3.
5. Schmitz F, Konigstorfer A, Sudhof TC. RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron. 2000;28:857-872.
6. Chang B, Heckenlively JR, Bayley PR, et al. The nob2 mouse, a null mutation in Cacnalf: anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Vis Neurosci. 2006;23:11-24.
7. Mansergh F, Orton NC, Vessey JP, et al. Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Hum Mol Genet. 2005;14:3035-3046.
8. Strom TM, Nyakatura G, Apfelstedt-Sylla E, et al. An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nat Genet. 1998;19:260-263.
9. Baumann L, Gerstner A, Zong X, Biel M, Wahl-Schott C. Functional characterization of the L-type Ca2+ channel Cav1.4alpha1 from mouse retina. Invest Ophthalmol Vis Sci. 2004;45:708-713.
10. De Sevilla Muller LP, Liu J, Solomon A, Rodriguez A, Brecha NC. Expression of voltage-gated calcium channel alpha2delta4 subunits in the mouse and rat retina. J Comp Neurol. 2013; 521:2486-2501.
11. McRory JE, Hamid J, Doering CJ, et al. The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. J Neurosci. 2004;24:1707-1718.
12. Michalakis S, Shaltiel L, Sothilingam V, et al. Mosaic synaptop-athy and functional defects in Cav1.4 heterozygous mice and human carriers of CSNB2. Hum Mol Genet. 2014;23:1538-1550.
13. Wycisk KA, Budde B, Feil S, et al. Structural and functional abnormalities of retinal ribbon synapses due to Cacna2d4 mutation. Invest Ophthalmol Vis Sci. 2006;47:3523-3530.
14. Wycisk KA, Zeitz C, Feil S, et al. Mutation in the auxiliary calcium-channel subunit CACNA2D4 causes autosomal recessive cone dystrophy. Am JHum Genet. 2006;79:973-977.
15. Bech-Hansen NT, Boycott KM, Gratton KJ, Ross DA, Field LL, Pearce WG. Localization of a gene for incomplete X-linked congenital stationary night blindness to the interval between DXS6849 and DXS8023 in Xp11.23. Hum Genet. 1998;103: 124-130.
16. Boycott KM, Maybaum TA, Naylor MJ, et al. A summary of 20 CACNA1F mutations identified in 36 families with incomplete X-linked congenital stationary night blindness, and characterization of splice variants. Hum Genet. 2001;108:91-97.
17. Wutz K, Sauer C, Zrenner E, et al. Thirty distinct CACNA1F mutations in 33 families with incomplete type of XLCSNB and Cacna1f expression profiling in mouse retina. Eur J Hum Genet. 2002;10:449-456.
18. Ball SL, Powers PA, Shin HS, Morgans CW, Peachey NS, Gregg RG. Role of the beta(2) subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Invest Oph-thalmol Vis Sci. 2002;43:1595-1603.
19. Ball SL, McEnery MW, Yunker AM, Shin HS, Gregg RG. Distribution of voltage gated calcium channel beta subunits in the mouse retina. Brain Res. 2011;1412:1-8.
20. McCall MA, Gregg RG. Comparisons of structural and functional abnormalities in mouse b-wave mutants. JPhysiol. 2008;586:4385-4392.
21. Weissgerber P, Held B, Bloch W, et al. Reduced cardiac L-type Ca2+ current in Cavß2~7~ embryos impairs cardiac development and contraction with secondary defects in vascular maturation. Circ Res. 2006;99:749-757.
22. Link S, Meissner M, Held B, et al. Diversity and developmental expression of L-type calcium channel beta2 proteins and their influence on calcium current in murine heart. J Biol Chem. 2009;284:30129-30137.
23. Gulick J, Robbins J. Cell-type-specific transgenesis in the mouse. Methods Mol Biol. 2009;561:91-104.
24. Meissner M, Weissgerber P, Londono JE, et al. Moderate calcium channel dysfunction in adult mice with inducible cardiomyocyte-specific excision of the cacnb2 gene. J Biol Chem. 2011;286:15875-15882.
25. Alpadi K, Magupalli VG, Kappel S, et al. RIBEYE recruits Munc119, a mammalian ortholog of the Caenorhabditis elegans protein unc119, to synaptic ribbons of photoreceptor synapses. JBiol Chem. 2008;283:26461-26467.
26. Anjum R, Ayoubian H, Schmitz F. Differentialsynaptic distribution of the scaffold proteins Cask and Caskin1 in the bovine retina. Mol Cell Neurosci. 2014;62C:19-29.
27. Schoch S, Mittelstaedt T, Kaeser PS, et al. Redundant functions of RIM1alpha and RIM2alpha in Ca(2+)-triggered neurotrans- mitter release. EMBO J. 2006;25:5852-5863.
28. Bloom FE, Aghajanian GK. Cytochemistry of synapses: selective staining for electron microscopy. Science. 1966; 154:1575-1577.
29. Bloom FE, Aghajanian GK. Fine structural and cytochemical analysis of the staining of synaptic junctions with phospho-tungstic acid. JUltrastruct Res. 1968;22:361-375.
30. Limbach C, Laue MM, Wang X, et al. Molecular in situ topology of Aczonin/Piccolo and associated proteins at the mammalian neurotransmitter release site. Proc Natl Acad Sci U S A. 2011; 108:E392-E401.
31. Tanimoto N, Muehlfriedel RL, Fischer MD, et al. Vision tests in the mouse: functional phenotyping with electroretinography. Front Biosci. 2009;14:2730-2737.
32. Wahl S, Katiyar R, Schmitz F. A local, periactive zone endocytic machinery at photoreceptor synapses in close vicinity to synaptic ribbons. J Neurosci. 2013;33:10278-10300.
33. Hofmann F, Flockerzi V, Kahl S, Wegener JW. L-type CaV1.2 calcium channels: from in vitro findings to in vivo function. Physiol Rev. 2014;94:303-326.
34. Colecraft HM, Alseikhan B, Takahashi SX, et al. Novel functional properties of Ca2+ channel beta subunits revealed by their expression in adult rat heart cells. J Physiol. 2002;541: 435-452.
35. Perez-Reyes E, Castellano A, Kim HS, et al. Cloning and expression of a cardiac/brain beta subunit of the L-type calcium channel. J Biol Chem. 1992;267:1792-1797.
36. Qin N, Olcese R, Bransby M, Lin T, Birnbaumer L. Ca24-induced inhibition of the cardiac Ca2+ channel depends on calmodulin. Proc Natl Acad Sci U S A. 1999;96:2435-2438.
37. Muller B, Butz E, Peichl L, Haverkamp S. The rod pathway of the microbat retina has bistratified rod bipolar cells and tristratified AII amacrine cells. J Neurosci. 2013;33:1014-1023.
38. Schmitz F, Tabares L, Khimich D, et al. CSPalpha-deficiency causes massive and rapid photoreceptor degeneration. Proc Natl Acad Sci USA. 2006;103:2926-2931.
39. Specht D, Tom Dieck S, Ammermuller J, Regus-Leidig H, Gundelfinger ED, Brandstatter JH. 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 JNeurosci. 2007;26:2506-2515.
40. tom Dieck S, Specht D, Strenzke N, et al. Deletion of the presynaptic scaffold CAST reduces active zone size in rod photoreceptors and impairs visual processing. J Neurosci. 2012;32:12192-12203.
41. Koulen P, Fletcher EL, Craven SE, Bredt DS, Wassle H. Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. JNeurosci. 1998;18: 10136-10149.
42. McLaughlin BJ. A fine structural and E-PTA study of photore-ceptor synaptogenesis in the chick retina. J Comp Neurol. 1976;170:347-364.
43. McLaughlin BJ, Boykins L. Ultrastructure of E-PTA stained synaptic ribbons in the chick retina. J Neurobiol. 1977;8:91-96.
44. Couteaux R, Pecot-Dechavassine M. Specialized areas of presynaptic membranes [article in French]. C R Acad Sci Hebd Seances Acad Sci D. 1974;278:291-293.
45. Dyson SE, Jones DG. Synaptic remodelling during development and maturation: junction differentiation and splitting as a mechanism for modifying connectivity. Brain Res. 1984;315: 125-137.
46. Triller A, Cluzeaud F, Pfeiffer F, Betz H, Korn H. Distribution of glycine receptors at central synapses: an immunoelectron microscopy study. J Cell Biol. 1985;101:683-688.
47. Liu X, Kerov V Haeseleer F, et al. Dysregulation of Ca(v)1.4 channels disrupts the maturation of photoreceptor synaptic ribbons in congenital stationary night blindness type 2. Channels. 2013;7:514-523.
48. Neef J, Gehrt A, Bulankina AV, et al. The Ca2+ channel subunit beta2 regulates Ca2+ channel abundance and function in inner hair cells and is required for hearing. J Neurosci. 2009;29: 10730-10740.
49. Zabouri N, Haverkamp S. Calcium channel-dependent molecular maturation of photoreceptor synapses. PLoS One. 2013;8: e63853.
50. Chen J, Billings SE, Nishimune H. Calcium channels link the muscle-derived synapse organizer laminin beta2 to Bassoon and CAST/Erc2 to organize presynaptic active zones. J Neurosci. 2011;31:512-525.
51. Libby RT, Champliaud MF, Claudepierre T, et al. Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J Neurosci. 2000;20:6517-6528.
52. Libby RT, Lavallee CR, Balkema GW, Brunken WJ, Hunter DD. Disruption of laminin beta2 chain production causes alterations in morphology and function in the CNS. J Neurosci. 1999;19:9399-9411.
53. Nishimune H. Transsynaptic channelosomes: non-conducting roles of ion channels in synapse formation. Channels. 2011;5: 432-439.
54. Nishimune H, Sanes JR, Carlson SS. A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature. 2004;432:580-587.
55. Ruth P, Rohrkasten A, Biel M, et al. Primary structure of the beta subunit of the DHP-sensitive calcium channel from skeletal muscle. Science. 1989;245:1115-1118.
56. Muller CS, Haupt A, Bildl W, et al. Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain. Proc Natl Acad Sci USA. 2010;107:14950-14957.
57. Molday RS, MacKenzie D. Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry. 1983;22:653-660.