Modulation of synaptic function by VAC14, a protein that regulates the phosphoinositides PI(3,5)P 2 and PI(5)P

EMBO Journal

Volumn 31, Issue 16, 2012, Pages 3442-3456

  Zhang, Yanling ^a   McCartney, Amber J ^a,b   Zolov, Sergey N ^a   Ferguson, Cole J ^a,c   Meisler, Miriam H ^c   Sutton, Michael A ^b,c   Weisman, Lois S ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

AMPA receptor; phosphatidylinositol 3,5 bisphosphate; PIKfyve; PtdIns(3,5)P 2; synapse

Indexed keywords

AMPA RECEPTOR; PHOSPHATIDYLINOSITIDE; PROTEIN FIG4; PROTEIN GLUA2; PROTEIN PI(3,5)P2; PROTEIN PI(5)P; PROTEIN VAC14; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOCYTOSIS; FIBROBLAST; HIPPOCAMPUS; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; FIBROBLASTS; GENETIC COMPLEMENTATION TEST; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEURONS; ORGANELLES; PHOSPHATIDYLINOSITOLS; SYNAPSES;

MUS;

EID: 84865273058     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.200     Document Type: Article

References (67)

1. Balla T (2006) Phosphoinositide-derived messengers in endocrine signaling. J Endocrinol 188: 135-153 (Pubitemid 43273804)
2. Beal MF (1992) Mechanisms of excitotoxicity in neurologic diseases. FASEB J 6: 3338-3344 (Pubitemid 23007098)
3. Bonangelino CJ, Catlett NL, Weisman LS (1997) Vac7p, a novel vacuolar protein, is required for normal vacuole inheritance and morphology. Mol Cell Biol 17: 6847-6858 (Pubitemid 27505914)
4. Bonangelino CJ, Nau JJ, Duex JE, Brinkman M, Wurmser AE, Gary JD, Emr SD, Weisman LS (2002) Osmotic stress-induced increase of phosphatidylinositol 3,5-bisphosphate requires Vac14p, an activator of the lipid kinase Fab1p. J Cell Biol 156: 1015-1028 (Pubitemid 34839851)
5. Brown TC, Tran IC, Backos DS, Esteban JA (2005) NMDA receptordependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron 45: 81-94 (Pubitemid 40075351)
6. Brunet A, Datta SR, Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11: 297-305 (Pubitemid 32524094)
7. Bryant NJ, Piper RC, Weisman LS, Stevens TH (1998) Retrograde traffic out of the yeast vacuole to the TGN occurs via the prevacuolar/endosomal compartment. J Cell Biol 142: 651-663 (Pubitemid 28381485)
8. Cabezas A, Pattni K, Stenmark H (2006) Cloning and subcellular localization of a human phosphatidylinositol 3-phosphate 5-kinase, PIKfyve/Fab1. Gene 371: 34-41
9. Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296: 1655-1657 (Pubitemid 34579158)
10. Chow CY, Landers JE, Bergren SK, Sapp PC, Grant AE, Jones JM, Everett L, Lenk GM, McKenna-Yasek DM, Weisman LS, Figlewicz D, Brown RH, Meisler MH (2009) Deleterious variants of FIG4, a phosphoinositide phosphatase, in patients with ALS. Am J Hum Genet 84: 85-88
11. Chow CY, Zhang Y, Dowling JJ, Jin N, Adamska M, Shiga K, Szigeti K, Shy ME, Li J, Zhang X, Lupski JR, Weisman LS, Meisler MH (2007) Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J. Nature 448: 68-72 (Pubitemid 47036999)
12. Corvera S, D'Arrigo A, Stenmark H (1999) Phosphoinositides in membrane traffic. Curr Opin Cell Biol 11: 460-465 (Pubitemid 29396792)
13. de Lartigue J, Polson H, Feldman M, Shokat K, Tooze SA, Urbé S, Clague MJ (2009) PIKfyve regulation of endosome-linked pathways. Traffic 10: 883-893
14. Dittman J, Ryan TA (2009) Molecular circuitry of endocytosis at nerve terminals. Annu Rev Cell Dev Biol 25: 133-160
15. Dong X-p, Shen D, Wang X, Dawson T, Li X, Zhang Q, Cheng X, Zhang Y, Weisman LS, Delling M, Xu H (2010) PI(3,5)P2 controls membrane traffic by direct activation of mucolipin Ca2 release channels in the endolysosome. Nat Commun 1: 38
16. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454-1468
17. Dove SK, Piper RC, McEwen RK, Yu JW, King MC, Hughes DC, Thuring J, Holmes AB, Cooke FT, Michell RH, Parker PJ, Lemmon MA (2004) Svp1p defines a family of phosphatidylinositol 3,5- bisphosphate effectors. EMBO J 23: 1922-1933 (Pubitemid 38902070)
18. Duex JE, Nau JJ, Kauffman EJ, Weisman LS (2006a) Phosphoinositide 5-phosphatase Fig 4p is required for both acute rise and subsequent fall in stress-induced phosphatidylinositol 3,5-bisphosphate levels. Eukaryot Cell 5: 723-731
19. Duex JE, Tang F, Weisman LS (2006b) The Vac14p-Fig4p complex acts independently of Vac7p and couples PI3,5P2 synthesis and turnover. J Cell Biol 172: 693-704
20. Ferguson CJ, Lenk GM, Jones JM, Grant AE, Winters JJ, Dowling JJ, Giger RJ, Meisler MH (2012) Neuronal expression of Fig4 is necessary and sufficient to prevent spongiform neurodegeneration. Hum Mol Genet (advance online publication, 6 June 2012; doi:10.1093/hmg/dds179)
21. 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
22. Gary JD, Wurmser AE, Bonangelino CJ, Weisman LS, Emr SD (1998) Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol 143: 65-79 (Pubitemid 28480518)
23. Gong L-W, De Camilli P (2008) Regulation of postsynaptic AMPA responses by synaptojanin 1. Proc Natl Acad Sci USA 105: 17561-17566
24. Han B-K, Emr SD (2011) Phosphoinositide [PI(3,5)P2] lipid-dependent regulation of the general transcriptional regulator Tupl. Genes Dev 25: 984-995
25. Hirano T, Matsuzawa T, Takegawa K, Sato MH (2011) Loss-offunction and gain-of-function mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in arabidopsis. Plant Physiol 155: 797-807
26. Hirano T, Sato MH (2011) Arabidopsis FAB1A/B is possibly involved in the recycling of auxin transporters. Plant Signal Behav 6: 583-585
27. Horton AC, Rácz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48: 757-771 (Pubitemid 41759427)
28. Huettner JE, Bean BP (1988) Block of N-methyl-D-aspartateactivated current by the anticonvulsant MK-801: selective binding to open channels. Proc Natl Acad Sci USA 85: 1307-1311 (Pubitemid 18073998)
29. Ibáñez CF (2007) Message in a bottle: long-range retrograde signaling in the nervous system. Trends Cell Biol 17: 519-528 (Pubitemid 350087664)
30. Ikonomov OC, Sbrissa D, Delvecchio K, Xie Y, Jin J-P, Rappolee D, Shisheva A (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
31. Ikonomov OC, Sbrissa D, Fenner H, Shisheva A (2009) PIKfyve- ArPIKfyve-Sac3 core complex: contact sites and their consequence for Sac3 phosphatase activity and endocytic membrane homeostasis. J Biol Chem 284: 35794-35806
32. Ikonomov OC, Sbrissa D, Fligger J, Delvecchio K, Shisheva A (2010) ArPIKfyve regulates Sac3 protein abundance and turnover: disruption of the mechanism by Sac3I41T mutation causing Charcot-Marie-Tooth 4J disorder. J Biol Chem 285: 26760-26764
33. Ikonomov OC, Sbrissa D, Foti M, Carpentier J-L, Shisheva A (2003) PIKfyve controls fluid phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. Mol Biol Cell 14: 4581-4591 (Pubitemid 37444657)
34. Ikonomov OC, Sbrissa D, Shisheva A (2001) Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve. J Biol Chem 276: 26141-26147
35. Jefferies HBJ, Cooke FT, Jat P, Boucheron C, Koizumi T, Hayakawa M, Kaizawa H, Ohishi T, Workman P, Waterfield MD, Parker PJ (2008) A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep 9: 164-170 (Pubitemid 351223454)
36. Jin N, Chow CY, Liu L, Zolov SN, Bronson R, Davisson M, Petersen JL, Zhang Y, Park S, Duex JE, Goldowitz D, Meisler MH,Weisman LS (2008) VAC14 nucleates a protein complex essential for the acute interconversion of PI3P and PI(3,5)P(2) in yeast and mouse. EMBO J 27: 3221-3234
37. Katona I, Zhang X, Bai Y, Shy ME, Guo J, Yan Q, Hatfield J, Kupsky WJ, Li J (2011) Distinct pathogenic processes between Fig4-deficient motor and sensory neurons. Eur J Neurosci 33: 1401-1410
38. Kennedy MJ, Ehlers MD (2006) Organelles and trafficking machinery for postsynaptic plasticity. Annu Rev Neurosci 29: 325-362 (Pubitemid 44476849)
39. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26: 2000-2009
40. Lasiecka ZM, Winckler B (2011) Mechanisms of polarized membrane trafficking in neurons - focusing in on endosomes. Mol Cell Neurosci 48: 278-287
41. Lee HW, Kim Y, Han K, Kim H, Kim E (2010) The phosphoinositide 3-phosphatase MTMR2 interacts with PSD-95 and maintains excitatory synapses by modulating endosomal traffic. J Neurosci 30: 5508-5518
42. Lemaire J-F, McPherson PS (2006) Binding of Vac14 to neuronal nitric oxide synthase: Characterisation of a new internal PDZrecognition motif. FEBS Lett 580: 6948-6954 (Pubitemid 44909140)
43. Lenk GM, Ferguson CJ, Chow CY, Jin N, Jones JM, Grant AE, Zolov SN, Winters JJ, Giger RJ, Dowling JJ, Weisman LS, Meisler MH (2011) Pathogenic mechanism of the FIG4 mutation responsible for charcot-marie-tooth disease CMT4J. PLoS Genet 7: e1002104- e1002104
44. LuW, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62: 254-268
45. Martin LJ (2010) Mitochondrial and cell death mechanisms in neurodegenerative diseases. Pharmaceuticals (Basel, Switzerland) 3: 839-915
46. Nicholson G, Lenk GM, Reddel SW, Grant AE, Towne CF, Ferguson CJ, Simpson E, Scheuerle A, Yasick M, Hoffman S, Blouin R, Brandt C, Coppola G, Biesecker LG, Batish SD, Meisler MH (2011) Distinctive genetic and clinical features of CMT4J: a severe neuropathy caused by mutations in the PI(3,5)P2 phosphatase FIG4. Brain 134: 1959-1971
47. Osborne SL, Wen PJ, Boucheron C, Nguyen HN, Hayakawa M, Kaizawa H, Parker PJ, Vitale N, Meunier FA (2008) PIKfyve negatively regulates exocytosis in neurosecretory cells. J Biol Chem 283: 2804-2813
48. Rosenmund C, Clements JD, Westbrook GL (1993) Nonuniform probability of glutamate release at a hippocampal synapse. Science 262: 754-757 (Pubitemid 23350697)
49. Roth MG (2004) Phosphoinositides in constitutive membrane traffic. Physiol Rev 84: 699-730 (Pubitemid 38828280)
50. Rothman SM, Olney JW (1986) Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann Neurol 19: 105-111 (Pubitemid 16114163)
51. Rothstein JD, Martin LJ, Kuncl RW (1992) Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. N Engl J Med 326: 1464-1468
52. Rudge SA, Anderson DM, Emr SD (2004) Vacuole size control: regulation of PtdIns(3,5)P2 levels by the vacuole-associated Vac14-Fig4 complex, a PtdIns(3,5)P2-specific phosphatase. Mol Biol Cell 15: 24-36 (Pubitemid 38044940)
53. Rusten TE, Vaccari T, Lindmo K, Rodahl LMW, Nezis IP, Sem-Jacobsen C, Wendler F, Vincent J-P, Brech A, Bilder D, Stenmark H (2007) ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol 17: 1817-1825 (Pubitemid 47576670)
54. Rutherford AC, Traer C, Wassmer T, Pattni K, Bujny MV, Carlton JG, Stenmark H, Cullen PJ (2006) The mammalian phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) regulates endosome-to-TGN retrograde transport. J Cell Sci 119: 3944-3957 (Pubitemid 44650868)
55. Saksena S, Sun J, Chu T, Emr SD (2007) ESCRTing proteins in the endocytic pathway. Trends Biochem Sci 32: 561-573 (Pubitemid 350123053)
56. Sbrissa D, Ikonomov OC, Filios C, Delvecchio K, Shisheva A (2012) Functional dissociation between PIKfyve-synthesized PtdIns5P and PtdIns(3,5)P2 by means of the PIKfyve inhibitor YM201636. Am J Physiol Cell Physiol (advance online publication, 23 May 2012; doi:10.1152/ajpcell.00105.2012)
57. Sbrissa D, Ikonomov OC, Shisheva A (1999) PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. Effect of insulin. J Biol Chem 274: 21589-21597
58. Shen J, Yu W-M, Brotto M, Scherman JA, Guo C, Stoddard C, Nosek TM, Valdivia HH, Qu C-K (2009) Deficiency of MIP/ MTMR14 phosphatase induces a muscle disorder by disrupting Ca(2) homeostasis. Nat Cell Biol 11: 769-776
59. Sieburth D, Ch'ng Q, Dybbs M, Tavazoie M, Kennedy S, Wang D, Dupuy D, Rual J-F, Hill DE, Vidal M, Ruvkun G, Kaplan JM (2005) Systematic analysis of genes required for synapse structure and function. Nature 436: 510-517
60. Song I, Huganir RL (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25: 578-588 (Pubitemid 35254182)
61. Tochio H, Mok YK, Zhang Q, Kan HM, Bredt DS, Zhang M (2000) Formation of nNOS/PSD-95 PDZ dimer requires a preformed beta-finger structure from the nNOS PDZ domain. J Mol Biol 303: 359-370
62. Tronchère H, Laporte J, Pendaries C, Chaussade C, Liaubet L, Pirola L, Mandel JL, Payrastre B (2004) Production of phosphatidylinositol 5-phosphate by the phosphoinositide 3-phosphatase myotubularin in mammalian cells. J Biol Chem 279: 7304-7312 (Pubitemid 38248880)
63. Tsuruta F, Green EM, Rousset M, Dolmetsch RE (2009) PIKfyve regulates CaV1.2 degradation and prevents excitotoxic cell death. J Cell Biol 187: 279-294
64. Turrigiano GG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135: 422-435
65. Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65: 761-789 (Pubitemid 38249176)
66. Zhang X, Chow CY, Sahenk Z, Shy ME, Meisler MH, Li J (2008) Mutation of FIG4 causes a rapidly progressive, asymmetric neuronal degeneration. Brain 131: 1990-2001
67. Zhang Y, Zolov SN, Chow CY, Slutsky SG, Richardson SC, Piper RC, Yang B, Nau JJ, Westrick RJ, Morrison SJ, Meisler MH, Weisman LS (2007) Loss of Vac14, a regulator of the signalling lipid phosphatidylinositol 3,5-bisphosphate, results in neurodegeneration in mice. Proc Natl Acad Sci USA 104: 17518-17523 (Pubitemid 350219870)