Identification and Immunocytochemical Characterization of Piccolino, a Novel Piccolo Splice Variant Selectively Expressed at Sensory Ribbon Synapses of the Eye and Ear

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Regus Leidig, Hanna ^a   Ott, Corinna ^a   Löhner, Martina ^a   Atorf, Jenny ^b   Fuchs, Michaela ^a   Sedmak, Tina ^a   Kremers, Jan ^b   Fejtová, Anna ^c,d   Gundelfinger, Eckart D ^c,d   Brandstätter, Johann H ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^d Center for Behavioral Brain Sciences   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BASSOON PROTEIN; CALCIUM CHANNEL L TYPE; MEMBRANE PROTEIN; PICCOLINO PROTEIN; PICCOLO PROTEIN; PROTEIN CAST; PROTEIN ELKS; PROTEIN MUNC13; PROTEIN RIM2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HAIR CELL; IMMUNOCYTOCHEMISTRY; INNER EAR; MOUSE; NONHUMAN; PHOTORECEPTOR CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; RETINA; RETINA BIPOLAR GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBBON SYNAPSE; SYNAPSE; TRANSLATION REGULATION;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; CALCIUM CHANNELS, L-TYPE; CARRIER PROTEINS; CATTLE; CYTOSKELETAL PROTEINS; EAR; EXONS; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; NEUROPEPTIDES; PROTEIN ISOFORMS; RAB3 GTP-BINDING PROTEINS; RATS; RETINA; SENSORY RECEPTOR CELLS; SYNAPSES;

EID: 84881143608     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070373     Document Type: Article

References (39)

1. Gundelfinger ED, Fejtová A, (2012) Molecular organization and plasticity of the cytomatrix at the active zone. Curr Opin Neurobiol 22: 423-30.
2. Südhof TC, (2012) The presynaptic active zone. Neuron 75: 11-25.
3. Zhai RG, Bellen HJ, (2004) The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda) 19: 262-70.
4. tom Dieck S, Brandstätter JH, (2006) Ribbon synapses of the retina. Cell Tissue Res 326: 339-46.
5. Matthews G, Fuchs P, (2010) The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci 11: 812-22.
6. Dick O, tom Dieck S, Altrock WD, Ammermüller J, Weiler R, et al. (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37: 775-86.
7. Schmitz F, (2009) The making of synaptic ribbons: how they are built and what they do. Neuroscientist 15: 611-24.
8. Snellman J, Mehta B, Babai N, Bartoletti TM, Akmentin W, et al. (2011) Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nat Neurosci 14: 1135-41.
9. 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: 825-36.
10. Limbach C, Laue MM, Wang X, Hu B, Thiede N, et al. (2011) Molecular in situ topology of Aczonin/Piccolo and associated proteins at the mammalian neurotransmitter release site. Proc Natl Acad Sci USA 108: E392-401.
11. Deguchi-Tawarada M, Inoue E, Takao-Rikitsu E, Inoue M, Kitajima I, et al. (2006) Active zone protein CAST is a component of conventional and ribbon synapses in mouse retina. J Comp Neurol 495: 480-96.
12. 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: 12192-203.
13. Cooper B, Hemmerlein M, Ammermüller J, Imig C, Reim K, et al. (2012) Munc13-independent vesicle priming at mouse photoreceptor ribbon synapses. J Neurosci 32: 8040-52.
14. Schmitz F, Königstorfer A, Südhof TC, (2000) RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28: 857-72.
15. Muresan V, Lyass A, Schnapp BJ, (1999) The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. J Neurosci 19: 1027-37.
16. Dick O, Hack I, Altrock WD, Garner CC, Gundelfinger ED, et al. (2001) Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: comparison with Bassoon. J Comp Neurol 439: 224-34.
17. Wang X, Hu B, Zieba A, Neumann NG, Kasper-Sonnenberg M, et al. (2009) A protein interaction node at the neurotransmitter release site: domains of Aczonin/Piccolo, Bassoon, CAST, and Rim converge on the N-terminal domain of Munc13-1. J Neurosci 29: 12584-96.
18. Mukherjee K, Yang X, Gerber SH, Kwon HB, Ho A, et al. (2010) Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proc Natl Acad Sci USA 107: 6504-9.
19. Spiwoks-Becker I, Maus C, tom Dieck S, Fejtová A, Engel L, et al. (2008) Active zone proteins are dynamically associated with synaptic ribbons in rat pinealocytes. Cell Tissue Res 333: 185-95.
20. Brandstätter JH, Löhrke S, Morgans CW, Wässle H, (1996) Distributions of two homologous synaptic vesicle proteins, synaptoporin and synaptophysin, in the mammalian retina. J Comp Neurol 370: 1-10.
21. Sedmak T, Sehn E, Wolfrum U (2009) in Methods in Cell Biology, ed Sloboda RD (Academic Press, London), vol. 94, 259-272.
22. Harazny J, Scholz M, Buder T, Lausen B, Kremers J, (2009) Electrophysiological deficits in the retina of the DBA/2J mouse. Doc Ophthalmol 119: 181-97.
23. Cases-Langhoff C, Voss B, Garner AM, Appeltauer U, Takei K, et al. (1996) Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. Eur J Cell Biol 69: 214-23.
24. Wang X, Kibschull M, Laue MM, Lichte B, Petrasch-Parwez E, et al. (1999) Aczonin, a 550-kD putative scaffolding protein of presynaptic active zones, shares homology regions with Rim and Bassoon and binds profilin. J Cell Biol 147: 151-62.
25. Fenster SD, Chung WJ, Zhai R, Cases-Langhoff C, Voss B, et al. (2000) Piccolo, a presynaptic zinc finger protein structurally related to bassoon. Neuron 25: 203-14.
26. Dogan RI, Getoor L, Wilbur WJ, Mount SM (2007) SplicePort- an interactive splice-site analysis tool. Nucleic Acids Res 35 (Web Server issue): W285-91.
27. Cervetto L, Piccolino M, (1974) Synaptic transmission between photoreceptors and horizontal cells in the turtle retina. Science 183(4123): 417-9.
28. Khimich D, Nouvian R, Pujol R, tom Dieck S, Egner A, et al. (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434: 889-94.
29. Lauer AM, Fuchs PA, Ryugo DK, Francis HW, (2012) Efferent synapses return to inner hair cells in the aging cochlea. Neurobiol Aging 33: 2892-902.
30. Bush RA, Sieving PA, (1996) Inner retinal contributions to the primate photopic fast flicker electroretinogram. J Opt Soc Am A Opt Image Sci Vis 13: 557-65.
31. Dong CJ, Hare WA, (2000) Contribution to the kinetics and amplitude of the electroretinogram b-wave by third-order retinal neurons in the rabbit retina. Vision Res 40: 579-89.
32. Viswanathan S, Frishman LJ, Robson JG, (2002) Inner-retinal contributions to the photopic sinusoidal flicker electroretinogram of macaques. Macaque photopic sinusoidal flicker ERG. Doc Ophthalmol 105: 223-42.
33. Fujimoto K, Shibasaki T, Yokoi N, Kashima Y, Matsumoto M, et al. (2002) Piccolo, a Ca2+ sensor in pancreatic beta-cells. Involvement of cAMP-GEFII.Rim2.Piccolo complex in cAMP-dependent exocytosis. J Biol Chem 277: 50497-502.
34. Takao-Rikitsu E, Mochida S, Inoue E, Deguchi-Tawarada M, Inoue M, et al. (2004) Physical and functional interaction of the active zone proteins, CAST, RIM1, and Bassoon, in neurotransmitter release. J Cell Biol 164: 301-11.
35. Shibasaki T, Sunaga Y, Fujimoto K, Kashima Y, Seino S, (2004) Interaction of ATP sensor, cAMP sensor, Ca2+ sensor, and voltage-dependent Ca2+ channel in insulin granule exocytosis. J Biol Chem 279: 7956-61.
36. Gustafsdottir SM, Schallmeiner E, Fredriksson S, Gullberg M, Söderberg O, et al. (2005) Proximity ligation assays for sensitive and specific protein analyses. Anal Biochem 345: 2-9.
37. Venkatesan JK, Natarajan S, Schwarz K, Mayer SI, Alpadi K, et al. (2010) Nicotinamide adenine dinucleotide-dependent binding of the neuronal Ca2+ sensor protein GCAP2 to photoreceptor synaptic ribbons. J Neurosci 30: 6559-76.
38. Fenster SD, Kessels MM, Qualmann B, Chung WJ, Nash J, et al. (2003) Interactions between Piccolo and the actin/dynamin-binding protein Abp1 link vesicle endocytosis to presynaptic active zones. J Biol Chem 278: 20268-77.
39. Kim S, Ko J, Shin H, Lee JR, Lim C, et al. (2003) The GIT family of proteins forms multimers and associates with the presynaptic cytomatrix protein Piccolo. J Biol Chem 278(8): 6291-300.