Rabconnectin3α promotes stable activity of the H + pump on synaptic vesicles in hair cells

Journal of Neuroscience

Volumn 32, Issue 32, 2012, Pages 11144-11156

  Einhorn, Zev ^a   Trapani, Josef G ^a   Liu, Qianyong ^a   Nicolson, Teresa ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; NEUROTRANSMITTER; PROTON PUMP; RABCONNECTIN 3 ALPHA; UNCLASSIFIED DRUG;

ACIDIFICATION; ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ESCAPE BEHAVIOR; FEMALE; HAIR CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MECHANICAL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPIKE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; ZEBRA FISH;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ENZYME INHIBITORS; ESCAPE REACTION; GREEN FLUORESCENT PROTEINS; HAIR CELLS, AUDITORY; LARVA; LATERAL LINE SYSTEM; MACROLIDES; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, CONFOCAL; MOLECULAR BIOLOGY; MUTATION; PHYSICAL STIMULATION; PROTON PUMPS; RNA, MESSENGER; SENSATION DISORDERS; SYNAPTIC VESICLES; VACUOLAR PROTON-TRANSLOCATING ATPASES; VIDEO RECORDING; VISION DISORDERS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84864859111     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1705-12.2012     Document Type: Article

References (60)

1. Abreu BJ, Guimarães M, Uliana LC, Vigh J, von Gersdorff H, Prado MA, Guatimosim C (2008) Protein kinase C modulates synaptic vesicle acidification in a ribbon type nerve terminal in the retina. Neurochem Int 53:155-164.
2. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232.
3. Di Giovanni J, Boudkkazi S, Mochida S, Bialowas A, Samari N, Lévêque C, Youssouf F, Brechet A, Iborra C, Maulet Y, Moutot N, Debanne D, Seagar M, El Far O (2010) V-ATPase membrane sector associates with synaptobrevin to modulate neurotransmitter release. Neuron 67:268-279.
4. Dou H, Finberg K, Cardell EL, Lifton R, Choo D (2003) Mice lacking the B1 subunit of H-ATPase have normal hearing. Hear Res 180:76-84.
5. Edwards RH (2007) The neurotransmitter cycle and quantal size. Neuron 55:835-858.
6. Faucherre A, Pujol-Martí J, Kawakami K, López-Schier H (2009) Afferent neurons of the zebrafish lateral line are strict selectors of hair-cell orientation. PLoS One 4:e4477.
7. Finberg KE, Wagner CA, Bailey MA, Paunescu TG, Breton S, Brown D, Giebisch G, Geibel JP, Lifton RP (2005) The B1-subunit of the H() ATPase is required for maximal urinary acidification. Proc Natl Acad Sci U S A 102:13616-13621.
8. Fremeau RT Jr, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci U S A 99:14488-14493.
9. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5:147-154.
10. Goh GY, Huang H, Ullman J, Borre L, Hnasko TS, Trussell LO, Edwards RH (2011) Presynaptic regulation of quantal size: K /H exchange stimulates vesicular glutamate transport. Nat Neurosci 14:1285-1292.
11. Graf ER, Daniels RW, Burgess RW, Schwarz TL, DiAntonio A (2009) Rab3 dynamically controls protein composition at active zones. Neuron 64:663-677.
12. Hiesinger PR, Fayyazuddin A, Mehta SQ, Rosenmund T, Schulze KL, Zhai RG, Verstreken P, Cao Y, Zhou Y, Kunz J, Bellen HJ (2005) The v-ATPase V0 subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell 121:607-620.
13. Horng JL, Lin LY, Hwang PP (2009) Functional regulation of H-ATPase-rich cells in zebrafish embryos acclimated to an acidic environment. Am J Physiol Cell Physiol 296:C682-C692.
14. Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada GH, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V (2006) V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 8:124-136.
15. Karet FE, Finberg KE, Nelson RD, Nayir A, Mocan H, Sanjad SA, RodriguezSoriano J, Santos F, Cremers CW, Di Pietro A, Hoffbrand BI, Winiarski J, Bakkaloglu A, Ozen S, Dusunsel R, Goodyer P, Hulton SA, Wu DK, Skvorak AB, Morton CC, Cunningham MJ, Jha V, Lifton RP (1999) Mutations in the gene encoding B1 subunit of H-ATPase cause renal tubular acidosis with sensorineural deafness. Nat Genet 21:84-90.
16. 2-dependent exocytosis of neurotransmitter. Genes Cells 8:537-546.
17. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236:3088-3099.
18. Leibovici M, Safieddine S, Petit C (2008) Mouse models for human hereditary deafness. Curr Top Dev Biol 84:385-429.
19. Li GL, Keen E, Andor-Ardó D, Hudspeth AJ, von Gersdorff H (2009) The unitary event underlying multiquantal EPSCs at a hair cell's ribbon synapse. J Neurosci 29:7558-7568.
20. Liégeois S, Benedetto A, Garnier JM, Schwab Y, Labouesse M (2006) The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J Cell Biol 173:949-961.
21. Mo W, Nicolson T (2011) Both pre-and postsynaptic activity of Nsf prevents degeneration of hair-cell synapses. PLoS One 6:e27146.
22. Nagano F, Kawabe H, Nakanishi H, Shinohara M, Deguchi-Tawarada M, Takeuchi M, Sasaki T, Takai Y (2002) Rabconnectin-3, a novel protein that binds both GDP/GTP exchange protein and GTPase-activating protein for Rab3 small G protein family. J Biol Chem 277:9629-9632.
23. Nagiel A, Andor-Ardó D, Hudspeth AJ (2008) Specificity of afferent synapses onto plane-polarized hair cells in the posterior lateral line of the zebrafish. J Neurosci 28:8442-8453.
24. Nicolson T, Rusch A, Friedrich RW, Granato M, Ruppersberg JP, NussleinVolhard C (1998) Genetic analysis of vertebrate sensory hair cell mechanosensation: the zebrafish circler mutants. Neuron 20:271-283.
25. Niwa S, Tanaka Y, Hirokawa N (2008) KIF1Bβ-and KIF1A-mediated axonal transport of presynaptic regulator Rab3 occurs in a GTP-dependent manner through DENN/MADD. Nat Cell Biol 10:1269-1279.
26. Nouvian R, Beutner D, Parsons TD, Moser T (2006) Structure and function of the hair cell ribbon synapse. J Membr Biol 209:153-165.
27. Nuckels RJ, Ng A, Darland T, Gross JM (2009) The vacuolar-ATPase complex regulates retinoblast proliferation and survival, photoreceptor morphogenesis, and pigmentation in the zebrafish eye. Invest Ophthalmol Vis Sci 50:893-905.
28. Obholzer N, Wolfson S, Trapani JG, Mo W, Nechiporuk A, Busch-Nentwich E, Seiler C, Sidi S, Söllner C, Duncan RN, Boehland A, Nicolson T (2008) Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28:2110-2118.
29. Oehlke O, Martin HW, Osterberg N, Roussa E (2011) Rab11b and its effector Rip11 regulate the acidosis-induced traffic of V-ATPase in salivary ducts. J Cell Physiol 226:638-651.
30. Peri F, Nusslein-Volhard C (2008) Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell 133:916-927.
31. Ruel J, Emery S, Nouvian R, Bersot T, Amilhon B, Van Rybroek JM, Rebillard G, Lenoir M, Eybalin M, Delprat B, Sivakumaran TA, Giros B, El Mestikawy S, Moser T, Smith RJ, Lesperance MM, Puel JL (2008) Impairment of SLC17A8 encoding vesicular glutamate transporter-3, VGLUT3, underlies nonsyndromic deafness DFNA25 and inner hair cell dysfunction in null mice. Am J Hum Genet 83:278-292.
32. Rutherford MA, Chapochnikov NM, Moser T (2012) Spike encoding of neurotransmitter release timing by spiral ganglion neurons of the cochlea. J Neurosci 32:4773-4789.
33. Sakisaka T, Takai Y (2005) Purification and properties of rabconnectin-3. Methods Enzymol 403:401-407.
34. Sautin YY, Lu M, Gaugler A, Zhang L, Gluck SL (2005) Phosphatidylinositol 3-kinase-mediated effects of glucose on vacuolar H-ATPase assembly, translocation, and acidification of intracellular compartments in renal epithelial cells. Mol Cell Biol 25:575-589.
35. Schenck S, Wojcik SM, Brose N, Takamori S (2009) A chloride conductance in VGLUT1 underlies maximal glutamate loading into synaptic vesicles. Nat Neurosci 12:156-162.
36. Seal RP, Akil O, Yi E, Weber CM, Grant L, Yoo J, Clause A, Kandler K, Noebels JL, Glowatzki E, Lustig LR, Edwards RH (2008) Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 57:263-275.
37. Seol JH, Shevchenko A, Shevchenko A, Deshaies RJ (2001) Skp1 forms multiple protein complexes, including RAVE, a regulator of V-ATPase assembly. Nat Cell Biol 3:384-391.
38. Sethi N, Yan Y, Quek D, Schupbach T, Kang Y (2010) Rabconnectin-3 is a functional regulator of mammalian Notch signaling. J Biol Chem 285:34757-34764.
39. Sheets L, Trapani JG, Mo W, Obholzer N, Nicolson T (2011) Ribeye is required for presynaptic Ca(V)1.3a channel localization and afferent innervation of sensory hair cells. Development 138:1309-1319.
40. Shiao JC, Lin LY, Horng JL, Hwang PP, Kaneko T (2005) How can teleostean inner ear hair cells maintain the proper association with the accreting otolith? J Comp Neurol 488:331-341.
41. Smardon AM, Kane PM (2007) RAVE is essential for the efficient assembly of the C subunit with the vacuolar H()-ATPase. J Biol Chem 282:26185-26194.
42. Smardon AM, Tarsio M, Kane PM (2002) The RAVE complex is essential for stable assembly of the yeast V-ATPase. J Biol Chem 277:13831-13839.
43. Söllner C, Schwarz H, Geisler R, Nicolson T (2004) Mutated otopetrin affects the genesis of otoliths and the localization of Starmaker in zebrafish. Dev Genes Evol 214:582-590.
44. Stover EH, Borthwick KJ, Bavalia C, Eady N, Fritz DM, Rungroj N, Giersch AB, Morton CC, Axon PR, Akil I, Al-Sabban EA, Baguley DM, Bianca S, Bakkaloglu A, Bircan Z, Chauveau D, Clermont MJ, Guala A, Hulton SA, Kroes H, Li Volti G, Mir S, Mocan H, Nayir A, Ozen S, Rodriguez Soriano J, Sanjad SA, Tasic V, Taylor CM, Topaloglu R, Smith AN, Karet FE (2002) Novel ATP6V1B1 and ATP6V0A4 mutations in autosomal recessive distal renal tubular acidosis with new evidence for hearing loss. J Med Genet 39:796-803.
45. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509-547.
46. Sun-Wada GH, Toyomura T, Murata Y, Yamamoto A, Futai M, Wada Y (2006) The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta-cells. J Cell Sci 119:4531-4540.
47. Tanaka M, Miyoshi J, Ishizaki H, Togawa A, Ohnishi K, Endo K, Matsubara K, Mizoguchi A, Nagano T, Sato M, Sasaki T, Takai Y (2001) Role of Rab3 GDP/GTP Exchange Protein in synaptic vesicle trafficking at the mouse neuromuscular junction. Mol Biol Cell 12:1421-1430.
48. Thisse B, Pflumio S, Furthauer M, Loppin B, Heyer V, Degrave A, Woehl R, Lux A, Steffan T, Charbonnier XQ, Thisse C (2001) Expression of the zebrafish genome during embryogenesis. ZFIN Direct Data Submission. Available at http://zfin.org/cgi-bin/webdriver?MIvalaa-pubview2.apg&OIDZDB-PUB010810-1.
49. Toei M, Saum R, Forgac M (2010) Regulation and isoform function of the V-ATPases. Biochemistry 49:4715-4723.
50. Trapani JG, Nicolson T (2011) Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ. J Neurosci 31:1614-1623.
51. Trapani JG, Nicolson T (2010) Physiological recordings from zebrafish lateral-line hair cells and afferent neurons. Methods Cell Biol 100:219-231.
52. Trapani JG, Obholzer N, Mo W, Brockerhoff SE, Nicolson T (2009) Synaptojanin1 is required for temporal fidelity of synaptic transmission in hair cells. PLoS Genet 5: e1000480.
53. Trombetta ES, Ebersold M, Garrett W, Pypaert M, Mellman I (2003) Activation of lysosomal function during dendritic cell maturation. Science 299:1400-1403.
54. Wangemann P (2006) Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J Physiol 576:11-21.
55. Weisz C, Glowatzki E, Fuchs P (2009) The postsynaptic function of type II cochlear afferents. Nature 461:1126-1129.
56. Wittig JH Jr, Parsons TD (2008) Synaptic ribbon enables temporal precision of hair cell afferent synapse by increasing the number of readily releasable vesicles: a modeling study. J Neurophysiol 100:1724-1739.
57. Yan Y, Denef N, Schupbach T (2009) The vacuolar proton pump, V-ATPase, is required for notch signaling and endosomal trafficking in Drosophila. Dev Cell 17:387-402.
58. Yang Q, Li G, Singh SK, Alexander EA, Schwartz JH (2006) Vacuolar H-ATPase B1 subunit mutations that cause inherited distal renal tubular acidosis affect proton pump assembly and trafficking in inner medullary collecting duct cells. J Am Soc Nephrol 17:1858-1866.
59. Zanazzi G, Matthews G (2009) The molecular architecture of ribbon presynaptic terminals. Mol Neurobiol 39:130-148.
60. Zeddies DG, Fay RR (2005) Development of the acoustically evoked behavioral response in zebrafish to pure tones. J Exp Biol 208:1363-1372.