The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring

Journal of Neuroscience

Volumn 24, Issue 40, 2004, Pages 8641-8650

  Van Epps, Heather A ^a   Hayashi, Mitsuko ^b   Lucast, Louise ^b   Stearns, George W ^a   Hurley, James B ^a   De Camilli, Pietro ^b   Brockerhoff, Susan E ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cone photoreceptor; Retina; Ribbon synapse; Sensory neurons; Synaptojanin; Zebrafish

Indexed keywords

POLYPHOSPHOINOSITIDE; POLYPHOSPHOINOSITIDE PHOSPHATASE; SYNAPTOJANIN; UNCLASSIFIED DRUG;

ARTICLE; AUDITORY NERVOUS SYSTEM; CYTOARCHITECTURE; CYTOSKELETON; ENDOCYTOSIS; ENZYME ANALYSIS; GENE; GENE MUTATION; MOLECULAR MECHANICS; NONHUMAN; NRC GENE; PHENOTYPE; PHOSPHOINOSITIDE METABOLISM; PHOTORECEPTOR; PRIORITY JOURNAL; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; SYNJ1 GENE; VESTIBULAR NERVOUS SYSTEM; VISUAL NERVOUS SYSTEM; ZEBRA FISH;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; CONES (RETINA); LARVA; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; PHENOTYPE; PHOSPHORIC MONOESTER HYDROLASES; RETINA; SYNAPTIC VESICLES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 5444268144     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2892-04.2004     Document Type: Article

References (56)

1. Allwardt BA, Lall AB, Brockerhoff SE, Dowling JE (2001) Synapse formation is arrested in retinal photoreceptors of the zebrafish nrc mutant. J Neurosci 21:2330-2342.
2. Balkema G, Jones N, Chalifoux J, Mayer J (2003) Co-localization of focal adhesion proteins with the synaptic ribbon in the photoreceptor terminal. Soc Neurosci Abstr 29:475.13.
3. Ball SL, Powers PA, Shin HS, Morgans CW, Peachey NS, Gregg RG (2002) Role of the beta(2) subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Invest Ophthalmol Vis Sci 43:1595-1603.
4. Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, Dowling JE (1995) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci USA 92:10545-10549.
5. Brockerhoff SE, Hurley JB, Niemi GA, Dowling JE (1997) A new form of inherited red-blindness identified in zebrafish. J Neurosci 17:4236-4242.
6. 2+ and suppression of current in cones from the zebrafish mutant nof. J Neurosci 23:470-480.
7. Calderwood DA, Ginsberg MH (2003) Talin forges the links between integrins and actin. Nat Cell Biol 5:694-697.
8. Cestra G, Castagnoli L, Dente L, Minenkova O, Petrelli A, Migone N, Hoffmuller U, Schneider-Mergener J, Cesareni G (1999) The SH3 domains of endophilin and amphiphysin bind to the proline-rich region of synaptojanin 1 at distinct sites that display an unconventional binding specificity. J Biol Chem 274:32001-32007.
9. Chen Y, Deng L, Maeno-Hikichi Y, Lai M, Chang S, Chen G, Zhang JF (2003) Formation of an endophilin-Ca2+ channel complex is critical for clathrin-mediated synaptic vesicle endocytosis. Cell 115:37-48.
10. Corey DR, Abrams JM (2001) Morpholino antisense oligonucleotides: tools for investigating vertebrate development. Genome Biol 2:REVIEWS1015.1-1015.3.
11. Cremona O, Di Paolo G, Wenk MR, Luthi A, Kim WT, Takei K, Daniell L, Nemoto Y, Shears SB, Flavell RA, McCormick DA, De Camilli P (1999) Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99:179-188.
12. De Camilli P, Cameron R, Greengard P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J Cell Biol 96:1337-1354.
13. Derbin C (1970) Effects de la section du nerve lateral sur les jonctions sensorineurales des ampuoules de Lorenzini de la Torpille Torpedo marmorata. J Microsc (Paris) 9:119-126.
14. Dick O, tom Dieck S, Altrock WD, Ammermuller J, Weiler R, Garner CC, Gundelfinger ED, Brandstatter JH (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775-786.
15. Di Paolo G, Pellegrini L, Letinic K, Cestra G, Zoncu R, Voronov S, Chang S, Guo J, Wenk MR, De Camilli P (2002) Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the PERM domain of talin. Nature 420:85-89.
16. Gad H, Ringstad N, Low P, Kjaerulff O, Gustafsson J, Wenk M, Di Paolo G, Nemoto Y, Crun J, Ellisman MH, De Camilli P, Shupliakov O, Brodin L (2000) Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27:301-312.
17. Guo S, Stolz LE, Lemrow SM, York JD (1999) SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases. J Biol Chem 274:12990-12995.
18. Ha SA, Torabinejad J, DeWald DB, Wenk MR, Lucast L, De Camilli P, Newitt RA, Aebersold R, Nothwehr SF (2003) The synaptojanin-like protein Inp53/Sj13 functions with clathrin in a yeast TGN-to-endosome pathway distinct from the GGA protein-dependent pathway. Mol Biol Cell 14:1319-1333.
19. Haffner C, Di Paolo G, Rosenthal JA, de Camilli P (2000) Direct interaction of the 170 kDa isoform of synaptojanin 1 with clathrin and with the clathrin adaptor AP-2. Curr Biol 10:471-474.
20. Harder KW, Owen P, Wong LK, Aebersold R, Clark-Lewis I, Jirik FR (1994) Characterization and kinetic analysis of the intracellular domain of human protein tyrosine phosphatase beta (HPTP beta) using synthetic phosphopeptides. Biochem J 298:395-401.
21. Harris TW, Hartwieg E, Horvitz HR, Jorgensen EM (2000) Mutations in synaptojanin disrupt synaptic vesicle recycling. J Cell Biol 150:589-600.
22. Holt M, Cooke A, Wu MM, Lagnado L (2003) Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. J Neurosci 23:1329-1339.
23. Holt M, Cooke A, Neef A, Lagnado L (2004) High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Curr Biol 14:173-183.
24. Hukriede NA, Joly L, Tsang M, Miles J, Tellis P, Epstein JA, Barbazuk WB, Li FN, Paw B, Postlethwait JH, Hudson TJ, Zon LI, McPherson JD, Chevrette M, Dawid IB, Johnson SL, Ekker M (1999) Radiation hybrid mapping of the zebrafish genome. Proc Natl Acad Sci USA 96:9745-9750.
25. Kim WT, Chang S, Daniell L, Cremona O, Di Paolo G, De Camilli P (2002) Delayed reentry of recycling vesicles into the fusion-competent synaptic vesicle pool in synaptojanin 1 knockout mice. Proc Natl Acad Sci USA 99:17143-17148.
26. Ladman AJ (1958) The fine structure of the rod-bipolar cell synapse in the retina of the albino rat. J Biophys Biochem Cytol 4:459-466.
27. Lenzi D, Crum J, Ellisman MH, Roberts WM (2002) Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron 36:649-659.
28. Libby RT, Lavallee CR, Balkema GW, Brunken WJ, Hunter DD (1999) Disruption of laminin beta2 chain production causes alterations in morphology and function in the CNS. J Neurosci 19:9399-9411.
29. Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA (2002) Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420:89-93.
30. Luthi A, Di Paolo G, Cremona O, Daniell L, De Camilli P, McCormick DA (2001) Synaptojanin 1 contributes to maintaining the stability of GABAergic transmission in primary cultures of cortical neurons. J Neurosci 21:9101-9111.
31. McPherson PS, Garcia EP, Slepnev VI, David C, Zhang X, Grabs D, Sossin WS, Bauerfeind R, Nemoto Y, De Camilli P (1996) A presynaptic inositol-5-phosphatase. Nature 379:353-357.
32. Meng A, Jessen JR, Lin S (1999) Transgenesis. In: Methods in cell biology: the zebrafish: genetics and genomics (William H, Detrich I, Westerfield M, Zon LI, eds), pp 133-147. San Diego: Academic.
33. Nemoto Y, Wenk MR, Watanabe M, Daniell L, Murakami T, Ringstad N, Yamada H, Takei K, De Camilli P (2001) Identification and characterization of a synaptojanin 2 splice isoform predominantly expressed in nerve terminals. J Biol Chem 276:41133-41142.
34. Paillart C, Li J, Matthews G, Sterling P (2003) Endocytosis and vesicle recycling at a ribbon synapse. J Neurosci 23:4092-4099.
35. Parsons TD, Lenzi D, Almers W, Roberts WM (1994) Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron 13:875-883.
36. Postlethwait JH, Johnson SL, Midson CN, Talbot WS, Gates M, Ballinger EW, Africa D, Andrews R, Carl T, Eisen JS, Horne S, Kimmel CB, Hutchinson M, Johnson M, Rodriguez A (1994) A genetic linkage map for the zebrafish. Science 264:699-703.
37. Raucher D, Stauffer T, Chen W, Shen K, Guo S, York JD, Sheetz MP, Meyer T (2000) Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100:221-228.
38. Rea R, Li J, Dharia A, Levitan ES, Sterling P, Kramer RH (2004) Streamlined synaptic vesicle cycle in cone photoreceptor terminals. Neuron 41:755-766.
39. Reme CE, Young RW (1977) The effects of hibernation on cone visual cells in the ground squirrel. Invest Ophthalmol Vis Sci 16:815-840.
40. Rieke F, Schwartz EA (1996) Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. J Physiol (Lond) 493:1-8.
41. Ringstad N, Nemoto Y, De Camilli P (1997) The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc Natl Acad Sci USA 94:8569-8574.
42. Ringstad N, Gad H, Low P, Di Paolo G, Brodin L, Shupliakov O, De Camilli P (1999) Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24:143-154.
43. Ringstad N, Nemoto Y, De Camilli P (2001) Differential expression of endophilin 1 and 2 dimers at central nervous system synapses. J Biol Chem 276:40424-40430.
44. Sakisaka T, Itoh T, Miura K, Takenawa T (1997) Phosphatidylinositol 4,5-bisphosphate phosphatase regulates the rearrangement of actin filaments. Mol Cell Biol 17:3841-3849.
45. Schmilz F, Drenckhahn D (1993) Li(+)-induced structural changes of synaptic ribbons are related to the phosphoinositide metabolism in photoreceptor synapses. Brain Res 604:142-148.
46. Schuske KR, Richmond JE, Matthies DS, Davis WS, Runz S, Rube DA, van der Bliek AM, Jorgensen EM (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40:749-762.
47. Shimoda N, Knapik EW, Ziniti J, Sim C, Yamada E, Kaplan S, Jackson D, de Sauvage F, Jacob H, Fishman MC (1999) Zebrafish genetic map with 2000 microsatellite markers. Genomics 58:219-232.
48. Singer-Kruger B, Nemoto Y, Daniell L, Ferro-Novick S, De Camilli P (1998) Synaptojanin family members are implicated in endocytic membrane traffic in yeast. J Cell Sci 111:3347-3356.
49. Stefan CJ, Audhya A, Emr SD (2002) The yeast synaptojanin-like proteins control the cellular distribution of phosphatidylinositol (4,5)-bisphosphate. Mol Biol Cell 13:542-557.
50. Takenawa T, Itoh T (2001) Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim Biophys Acta 1533:190-206.
51. Takenawa T, Itoh T, Fukami K (1999) Regulation of phosphatidylinositol 4,5-bisphosphate levels and its roles in cytoskeletal re-organization and malignant transformation. Chem Phys Lipids 98:13-22.
52. Van Epps HA, Yim CM, Hurley JB, Brockerhoff SE (2001) Investigations of photoreceptor synaptic transmission and light adaptation in the zebrafish visual mutant nrc. Invest Ophthalmol Vis Sci 42:868-874.
53. Verstreken P, Koh TW, Schulze KL, Zhai RG, Hiesinger PR, Zhou Y, Mehta SQ, Cao Y, Roos J, Bellen HJ (2003) Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40:733-748.
54. 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.
55. Westerfield M (1994) The zebrafish book: a guide for laboratory use of zebrafish (Brachydanio rerio), Ed 2.1. Eugene, OR: University of Oregon.
56. Yarfitz S, Hurley JB (1994) Transduction mechanisms of vertebrate and invertebrate photoreceptors. J Biol Chem 269:14329-14332.