Synaptojanin 1 is required for endolysosomal trafficking of synaptic proteins in cone photoreceptor inner segments

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  George, Ashley A ^a   Hayden, Sara ^a   Holzhausen, Lars C ^a,c   Ma, Eva Y ^a   Suzuki, Sachihiro C ^b   Brockerhoff, Susan E ^a  

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

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AUTOPHAGY; CILIA; ENDOPLASMIC RETICULUM; ENDOSOMES; GOLGI APPARATUS; LYSOSOMES; NERVE TISSUE PROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN TRANSPORT; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL PHOTORECEPTOR CELL INNER SEGMENT; RETINAL PHOTORECEPTOR CELL OUTER SEGMENT; SYNAPTIC VESICLES; ZEBRAFISH;

EID: 84894229034     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084394     Document Type: Article

References (77)

1. Kolb H (2003) How the retina works - Much of the construction of an image takes place in the retina itself through the use of specialized neural circuits. American Scientist 91: 28-35.
2. Kennedy B, Malicki J (2009) What drives cell morphogenesis: a look inside the vertebrate photoreceptor. Dev Dyn 238: 2115-2138.
3. Young RW (1967) The renewal of photoreceptor cell outer segments. J Cell Biol 33: 61-72.
4. Ramamurthy V, Cayouette M (2009) Development and disease of the photoreceptor cilium. Clin Genet 76: 137-145.
5. Sung CH, Chuang JZ (2010) The cell biology of vision. J Cell Biol 190: 953-963.
6. 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. (Pubitemid 32240531)
7. 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. (Pubitemid 32206933)
8. Van Epps HA, Hayashi M, Lucast L, Stearns GW, Hurley JB, et al. (2004) The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring. J Neurosci 24: 8641-8650. (Pubitemid 39362959)
9. Holzhausen LC, Lewis AA, Cheong KK, Brockerhoff SE (2009) Differential role for synaptojanin 1 in rod and cone photoreceptors. J Comp Neurol 517: 633-644.
10. Cremona O, Di Paolo G, Wenk MR, Luthi A, Kim WT, et al. (1999) Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99: 179-188. (Pubitemid 29491784)
11. McPherson PS, Garcia EP, Slepnev VI, David C, Zhang X, et al. (1996) A presynaptic inositol-5-phosphatase. Nature 379: 353-357. (Pubitemid 26033932)
12. McPherson PS, Takei K, Schmid SL, De Camilli P (1994) p145, a major Grb2-binding protein in brain, is co-localized with dynamin in nerve terminals where it undergoes activity-dependent dephosphorylation. J Biol Chem 269: 30132-30139. (Pubitemid 24376477)
13. Gong LW, De Camilli P (2008) Regulation of postsynaptic AMPA responses by synaptojanin 1. Proc Natl Acad Sci U S A 105: 17561-17566.
14. Cossec JC, Lavaur J, Berman DE, Rivals I, Hoischen A, et al. (2012) Trisomy for synaptojanin1 in Down syndrome is functionally linked to the enlargement of early endosomes. Hum Mol Genet 21: 3156-3172.
15. Wright AF, Chakarova CF, El-Aziz MMA, Bhattacharya SS (2010) Photoreceptor degeneration: genetic and mechanistic dissection of a complex trait. Nature Reviews Genetics 11: 273-284.
16. Insinna C, Besharse JC (2008) Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Dev Dyn 237: 1982-1992.
17. Branchek T (1984) The development of photoreceptors in the zebrafish, brachydanio rerio. II. Function. J Comp Neurol 224: 116-122.
18. Easter SS Jr, Nicola GN (1996) The development of vision in the zebrafish (Danio rerio) . Dev Biol 180: 646-663.
19. Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, et al. (1995) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci U S A 92: 10545-10549.
20. Tsujikawa M, Malicki J (2004) Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron 42: 703-716. (Pubitemid 38748786)
21. Krock BL, Perkins BD (2008) The intraflagellar transport protein IFT57 is required for cilia maintenance and regulates IFT-particle-kinesin-II dissociation in vertebrate photoreceptors. J Cell Sci 121: 1907-1915. (Pubitemid 351943384)
22. Kennedy BN, Alvarez Y, Brockerhoff SE, Stearns GW, Sapetto-Rebow B, et al. (2007) Identification of a zebrafish cone photoreceptor-specific promoter and genetic rescue of achromatopsia in the nof mutant. Invest Ophthalmol Vis Sci 48: 522-529. (Pubitemid 351260680)
23. Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394: 192-195. (Pubitemid 28325974)
24. Wan L, Almers W, Chen W (2005) Two ribeye genes in teleosts: the role of Ribeye in ribbon formation and bipolar cell development. J Neurosci 25: 941-949. (Pubitemid 40171010)
25. Meyer MP, Smith SJ (2006) Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26: 3604-3614.
26. Mazelova J, Ransom N, Astuto-Gribble L, Wilson MC, Deretic D (2009) Syntaxin 3 and SNAP-25 pairing, regulated by omega-3 docosahexaenoic acid, controls the delivery of rhodopsin for the biogenesis of cilia-derived sensory organelles, the rod outer segments. J Cell Sci 122: 2003-2013.
27. 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.
28. Roderick HL, Campbell AK, Llewellyn DH (1997) Nuclear localisation of calreticulin in vivo is enhanced by its interaction with glucocorticoid receptors. FEBS Lett 405: 181-185. (Pubitemid 27136507)
29. Suzuki SC, Bleckert A, Williams PR, Takechi M, Kawamura S, et al. (2013) Cone photoreceptor types in zebrafish are generated by symmetric terminal divisions of dedicated precursors. Proc Natl Acad Sci U S A: 110: 15109-14.
30. Deretic D, Papermaster DS (1991) Polarized sorting of rhodopsin on post-Golgi membranes in frog retinal photoreceptor cells. J Cell Biol 113: 1281-1293. (Pubitemid 21909757)
31. Vicinanza M, D'Angelo G, Di Campli A, De Matteis MA (2008) Function and dysfunction of the PI system in membrane trafficking. EMBO J 27: 2457-2470.
32. He C, Bartholomew CR, Zhou W, Klionsky DJ (2009) Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos. Autophagy 5: 520-526.
33. Vitelli R, Santillo M, Lattero D, Chiariello M, Bifulco M, et al. (1997) Role of the small GTPase Rab7 in the late endocytic pathway. J Biol Chem 272: 4391-4397. (Pubitemid 27078515)
34. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11: 467-480. (Pubitemid 30112158)
35. Jager S, Bucci C, Tanida I, Ueno T, Kominami E, et al. (2004) Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 117: 4837-4848. (Pubitemid 39433449)
36. Bottger G, Nagelkerken B, van der Sluijs P (1996) Rab4 and Rab7 define distinct nonoverlapping endosomal compartments. J Biol Chem 271: 29191-29197. (Pubitemid 26382629)
37. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8: 445-544.
38. Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. Lancet 368: 1795-1809. (Pubitemid 44739028)
39. 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. (Pubitemid 34165082)
40. Bensen ES, Costaguta G, Payne GS (2000) Synthetic genetic interactions with temperature-sensitive clathrin in Saccharomyces cerevisiae . Roles for synaptojanin-like Inp53p and dynamin-related Vps1p in clathrin-dependent protein sorting at the trans-Golgi network. Genetics 154: 83-97. (Pubitemid 30045903)
41. 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. (Pubitemid 28563037)
42. Arshavsky VY (2003) Protein Translocation in Photoreceptor Light Adaptation: A Common Theme in Vertebrate and Invertebrate Vision. Sci STKE 204: pe43.
43. Rajala A, Daly RJ, Tanito M, Allen DT, Holt LJ, et al. (2009) Growth factor receptor-bound protein 14 undergoes light-dependent intracellular translocation in rod photoreceptors: functional role in retinal insulin receptor activation. Biochemistry 48: 5563-5572.
44. Linton JD, Holzhausen LC, Babai N, Song H, Miyagishima KJ, et al. (2010) Flow of energy in the outer retina in darkness and in light. Proc Natl Acad Sci U S A 107: 8599-8604.
45. Schmitt EA, Dowling JE (1999) Early retinal development in the zebrafish, Danio rerio : light and electron microscopic analyses. J Comp Neurol 404: 515-536. (Pubitemid 29084639)
46. Schmied R, Holtzman E (1989) Involvement of the Golgi apparatus in sorting of materials to opposite ends of frog rod retinal photoreceptors. Journal of Neurobiology 20: 115-138.
47. Pfeffer SR (2009) Multiple routes of protein transport from endosomes to the trans Golgi network. FEBS Lett 583: 3811-3816.
48. Ganley IG, Pfeffer SR (2006) Cholesterol accumulation sequesters Rab9 and disrupts late endosome function in NPC1-deficient cells. J Biol Chem 281: 17890-17899. (Pubitemid 44035588)
49. Choudhury A, Dominguez M, Puri V, Sharma DK, Narita K, et al. (2002) Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J Clin Invest 109: 1541-1550. (Pubitemid 34663516)
50. Kirkbride KC, Hong NH, French CL, Clark ES, Jerome WG, et al. (2012) Regulation of late endosomal/lysosomal maturation and trafficking by cortactin. Cytoskeleton (Hoboken) 69: 625-643.
51. Dermaut B, Norga KK, Kania A, Verstreken P, Pan H, et al. (2005) Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurode-generation in Drosophila benchwarmer. J Cell Biol 170: 127-139. (Pubitemid 40994102)
52. Chinchore Y, Mitra A, Dolph PJ (2009) Accumulation of rhodopsin in late endosomes triggers photoreceptor cell degeneration. PLoS Genet 5: e1000377.
53. Nixon RA, Yang DS, Lee JH (2008) Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy 4: 590-599.
54. Dehay B, Martinez-Vicente M, Caldwell GA, Caldwell KA, Yue Z, et al. (2013) Lysosomal impairment in Parkinson's disease. Mov Disord 28: 725-732.
55. Tofaris GK (2012) Lysosome-dependent pathways as a unifying theme in Parkinson's disease. Mov Disord 27: 1364-1369.
56. Nixon RA (2013) The role of autophagy in neurodegenerative disease. Nat Med 19: 983-997.
57. Cook C, Stetler C, Petrucelli L (2012) Disruption of protein quality control in Parkinson's disease. Cold Spring Harb Perspect Med 2: a009423.
58. Krebs CE, Karkheiran S, Powell JC, Cao M, Makarov V, et al. (2013) The Sac1 Domain of SYNJ1 Identified Mutated in a Family with Early-Onset. Hum Mutat 34: 1200-1207.
59. Quadri M, Fang M, Picillo M, Olgiati S, Breedveld GJ, et al. (2013) Mutation in the SYNJ1 Gene Associated with Autosomal Recessive, Early-Onset. Hum Mutat 34: 1208-1215.
60. Wheeler TC, Chin L-S, Li Y, Roudabush FL, Li L (2002) Regulation of Synaptophysin Degradation by Mammalian Homologues of Seven in Absentia. J Biol Chem 277: 10273-10282. (Pubitemid 34968143)
61. Vicinanza M, D'Angelo G, Di Campli A, De Matteis MA (2008) Phosphoinositides as regulators of membrane trafficking in health and disease. Cell Mol Life Sci 65: 2833-2841.
62. Ooms LM, Horan KA, Rahman P, Seaton G, Gurung R, et al. (2009) The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease. Biochem J 419: 29-49.
63. Ikonomov OC, Sbrissa D, Delvecchio K, Xie Y, Jin JP, et al. (2011) The phosphoinositide kinase PIKfyve is vital in early embryonic development: Preimplantation lethality of PIKfyve-/- embryos but normality of PIKfyve+/- mice. J Biol Chem 286: 13404-13413.
64. Chow CY, Zhang Y, Dowling JJ, Jin N, Adamska M, et al. (2007) Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J. Nature 448: 68-72. (Pubitemid 47036999)
65. Ferguson CJ, Lenk GM, Jones JM, Grant AE, Winters JJ, et al. (2012) Neuronal expression of Fig4 is necessary and sufficient to prevent spongiform neurodegeneration. Hum Mol Genet 21: 3525-3534.
66. Zhang Y, Zolov SN, Chow CY, Slutsky SG, Richardson SC, et al. (2007) Loss of Vac14, a regulator of the signalling lipid phosphatidylinositol 3,5-bisphosphate, results in neurodegeneration in mice. Proc Natl Acad Sci U S A 104: 17518-17523. (Pubitemid 350219870)
67. Ferguson CJ, Lenk GM, Meisler MH (2009) Defective autophagy in neurons and astrocytes from mice deficient in PI(3,5)P2. Hum Mol Genet 18: 4868-4878.
68. Vergne I, Deretic V (2010) The role of PI3P phosphatases in the regulation of autophagy. FEBS Lett 584: 1313-1318.
69. 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.
70. Mani M, Lee SY, Lucast L, Cremona O, Di Paolo G, et al. (2007) The dual phosphatase activity of synaptojanin1 is required for both efficient synaptic vesicle endocytosis and reavailability at nerve terminals. Neuron 56: 1004-1018. (Pubitemid 350251112)
71. Insinna C, Baye LM, Amsterdam A, Besharse JC, Link BA (2010) Analysis of a zebrafish dync1h1 mutant reveals multiple functions for cytoplasmic dynein 1 during retinal photoreceptor development. Neural Dev 5: 1-21.
72. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, et al. (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236: 3088-3099. (Pubitemid 350175006)
73. Westerfield M (1995) The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Brachydanio rerio). Eugene: University of Oregon Press.
74. Brockerhoff SE (2006) Measuring the optokinetic response of zebrafish larvae. Nat Protoc 1: 2448-2451.
75. Kikuta H, Kawakami K (2009) Transient and stable transgenesis using tol2 transposon vectors. Methods Mol Biol 546: 69-84.
76. Brockerhoff SE, Hurley JB, Niemi GA, Dowling JE (1997) A new form of inherited red-blindness identified in zebrafish. J Neurosci 20: 1-8.
77. Obholzer N, Wolfson S, Trapani JG, Mo W, Nechiporuk A, et al. (2008) Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28: 2110-2118. (Pubitemid 351317615)