APP controls the formation of PI(3,5)P2 vesicles through its binding of the PIKfyve complex

Cellular and Molecular Life Sciences

Volumn 73, Issue 2, 2016, Pages 393-408

  Currinn, Heather ^a   Guscott, Benjamin ^a   Balklava, Zita ^a   Rothnie, Alice ^a   Wassmer, Thomas ^a  

^a ASTON UNIVERSITY   (United Kingdom)

Author keywords

Endosomal sorting; ML1Nx2; Mucolipin 1; Neurodegeneration; TRPML1

Indexed keywords

AMYLOID PRECURSOR PROTEIN; GLYCEROPHOSPHOLIPID; PHOSPHATIDYLINOSITOL 3 PHOSPHATE 5 KINASE FAB1 SUBUNIT; PHOSPHATIDYLINOSITOL 3 PHOSPHATE 5 KINASE SAC3 SUBUNIT; PHOSPHATIDYLINOSITOL 3 PHOSPHATE 5 KINASE VAC14 SUBUNIT; PHOSPHATIDYLINOSITOL 3,5 BISPHOSPHATE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; APLP1 PROTEIN, HUMAN; APLP2 PROTEIN, HUMAN; APP PROTEIN, HUMAN; NERVE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,5-DIPHOSPHATE; PIKFYVE PROTEIN, HUMAN; POLYPHOSPHOINOSITIDE; PROTEIN BINDING;

APLP1 GENE; APLP2 GENE; APP GENE; ARTICLE; CELL MIGRATION; CELL SELECTION; CELL VACUOLE; CONTROLLED STUDY; GENE; GENE REPRESSION; HUMAN; HUMAN CELL; PHOSPHOLIPID METABOLISM; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; ENDOSOME; HELA CELL LINE; METABOLISM; MOLECULAR GENETICS; PROTEIN TRANSPORT;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN PRECURSOR; ENDOSOMES; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN BINDING; PROTEIN INTERACTION MAPS; PROTEIN TRANSPORT;

EID: 84954077162     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-1993-0     Document Type: Article

References (53)

1. Cullen PJ (2008) Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 9:574-582. doi: 10.1038/nrm2427
2. Woodman PG, Futter CE (2008) Multivesicular bodies: co-ordinated progression to maturity. Curr Opin Cell Biol 20:408-414. doi: 10.1016/j.ceb.2008.04.001
3. Schink KO, Raiborg C, Stenmark H (2013) Phosphatidylinositol 3-phosphate, a lipid that regulates membrane dynamics, protein sorting and cell signalling. BioEssays 35:900-912. doi: 10.1002/bies.201300064
4. Ellson CD, Gobert-Gosse S, Anderson KE et al (2001) PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40(phox). Nat Cell Biol 3:679-682. doi: 10.1038/35083076
5. Kutateladze TG (2007) Mechanistic similarities in docking of the FYVE and PX domains to phosphatidylinositol 3-phosphate containing membranes. Prog Lipid Res 46:315-327. doi: 10.1016/j.plipres.2007.06.001
6. Burd CG, Emr SD (1998) Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains. Mol Cell 2:157-162
7. Stack JH, DeWald DB, Takegawa K, Emr SD (1995) Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J Cell Biol 129:321-334
8. McCartney AJ, Zhang Y, Weisman LS (2014) Phosphatidylinositol 3,5-bisphosphate: low abundance, high significance. BioEssays News Rev Mol Cell Dev Biol 36:52-64. doi: 10.1002/bies.201300012
9. Shisheva A (2012) PIKfyve and its lipid products in health and in sickness. Curr Top Microbiol Immunol 362:127-162. doi: 10.1007/978-94-007-5025-8-7
10. 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. doi: 10.1074/jbc.274.31.21589
11. Gary JD, Sato TK, Stefan CJ et al (2002) Regulation of Fab1 phosphatidylinositol 3-phosphate 5-kinase pathway by Vac7 protein and Fig4, a polyphosphoinositide phosphatase family member. Mol Biol Cell 13:1238-1251. doi: 10.1091/mbc.01-10-0498
12. Tang Z, Bereczki E, Zhang H et al (2013) Mammalian target of rapamycin (mTor) mediates tau protein dyshomeostasis: implication for Alzheimer disease. J Biol Chem 288:15556-15570. doi: 10.1074/jbc.M112.435123
13. Jin N, Chow CY, Liu L et al (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. doi: 10.1038/emboj.2008.248
14. 2, which serves as both a signaling lipid and the major precursor for PI5P. Proc Natl Acad Sci USA 109:17472-17477. doi: 10.1073/pnas.1203106109
15. Ikonomov OC, Sbrissa D, Mlak K, Shisheva A (2002) Requirement for PIKfyve enzymatic activity in acute and long-term insulin cellular effects. Endocrinology 143:4742-4754. doi: 10.1210/en.2002-220615
16. Rutherford AC, Traer C, Wassmer T et al (2006) The mammalian phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) regulates endosome-to-TGN retrograde transport. J Cell Sci 119:3944-3957. doi: 10.1242/jcs.03153
17. Zhang Y, Zolov SN, Chow CY et al (2007) Loss of Vac14, a regulator of the signaling lipid phosphatidylinositol 3,5-bisphosphate, results in neurodegeneration in mice. Proc Natl Acad Sci USA 104:17518-17523. doi: 10.1073/pnas.0702275104
18. Jefferies HBJ, Cooke FT, Jat P et al (2008) A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep 9:164-170. doi: 10.1038/sj.embor.7401155
19. Dong X, Shen D, Wang X et al (2010) PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun 1:38. doi: 10.1038/ncomms1037
20. De Lartigue J, Polson H, Feldman M et al (2009) PIKfyve regulation of endosome-linked pathways. Traffic 10:883-893. doi: 10.1111/j.1600-0854.2009.00915.x
21. Chow CY, Zhang Y, Dowling JJ et al (2007) Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J. Nature 448:68-72. doi: 10.1038/nature05876
22. Chow CY, Landers JE, Bergren SK et al (2009) Deleterious variants of FIG4, a phosphoinositide phosphatase, in patients with ALS. Am J Hum Genet 84:85-88. doi: 10.1016/j.ajhg.2008.12.010
23. Goate A (2006) Segregation of a missense mutation in the amyloid beta-protein precursor gene with familial Alzheimer's disease. J Alzheimer's Dis JAD 9:341-347
24. Murrell J, Farlow M, Ghetti B, Benson MD (1991) A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease. Science 254:97-99
25. Hardy J, Allsop D (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12:383-388
26. Nicolas M, Hassan BA (2014) Amyloid precursor protein and neural development. Development 141:2543-2548. doi: 10.1242/dev.108712
27. Aydin D, Weyer SW, Müller UC (2012) Functions of the APP gene family in the nervous system: insights from mouse models. Exp Brain Res 217:423-434. doi: 10.1007/s00221-011-2861-2
28. Zhang X, Song W (2013) The role of APP and BACE1 trafficking in APP processing and amyloid beta generation. Alzheimers Res Ther 5:46. doi: 10.1186/alzrt211
29. Burgos PV, Mardones GA, Rojas AL et al (2010) Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev Cell 18:425-436. doi: 10.1016/j.devcel.2010.01.015
30. Bhalla A, Vetanovetz CP, Morel E et al (2012) The location and trafficking routes of the neuronal retromer and its role in amyloid precursor protein transport. Neurobiol Dis 47:126-134. doi: 10.1016/j.nbd.2012.03.030
31. Vieira SI, Rebelo S, Esselmann H et al (2010) Retrieval of the Alzheimer's amyloid precursor protein from the endosome to the TGN is S655 phosphorylation state-dependent and retromer-mediated. Mol Neurodegener 5:40. doi: 10.1186/1750-1326-5-40
32. Arighi CN, Hartnell LM, Aguilar RC et al (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165:123-133. doi: 10.1083/jcb.200312055
33. Seaman MNJ (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165:111-122. doi: 10.1083/jcb.200312034
34. Temkin P, Lauffer B, Jaeger S et al (2011) SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol 13:715-721. doi: 10.1038/ncb2252
35. Pocha SM, Wassmer T, Niehage C et al (2011) Retromer controls epithelial cell polarity by trafficking the apical determinant crumbs. Curr Biol 21:1111-1117
36. Li X, Wang X, Zhang X et al (2013) Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics. Proc Natl Acad Sci USA 110:21165-21170. doi: 10.1073/pnas.1311864110
37. Niehage C, Stange C, Anitei M, Hoflack B (2014) Liposome-based assays to study membrane-associated protein networks. Methods Enzymol 534:223-243. doi: 10.1016/B978-0-12-397926-1.00013-5
38. Wassmer T, Attar N, Harterink M et al (2009) The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev Cell 17:110-122. doi: 10.1016/j.devcel.2009.04.016
39. Wassmer T, Attar N, Bujny MV et al (2007) A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J Cell Sci 120:45-54
40. Rizk A, Paul G, Incardona P et al (2014) Segmentation and quantification of subcellular structures in fluorescence microscopy images using Squassh. Nat Protoc 9:586-596. doi: 10.1038/nprot.2014.037
41. Aridor M, Traub LM (2002) Cargo selection in vesicular transport: the making and breaking of a coat. Traffic 3:537-546. doi: 10.1034/j.1600-0854.2002.30804.x
42. Baust T, Czupalla C, Krause E et al (2006) Proteomic analysis of adaptor protein 1A coats selectively assembled on liposomes. Proc Natl Acad Sci USA 103:3159-3164. doi: 10.1073/pnas.0511062103
43. Lorent K, Overbergh L, Moechars D et al (1995) Expression in mouse embryos and in adult mouse brain of three members of the amyloid precursor protein family, of the alpha-2-macroglobulin receptor/low density lipoprotein receptor-related protein and of its ligands apolipoprotein E, lipoprotein lipase. Neuroscience 65:1009-1025. pii: 0306-4522(94)00555-J
44. 2+-binding FYVE finger-containing phosphoinositide kinase in insulin-sensitive cells. Mol Cell Biol 19:623-634
45. Mccartney AJ, Zolov SN, Kauffman EJ et al (2014) Activity-dependent PI(3,5)P2 synthesis controls AMPA receptor trafficking during synaptic depression. Proc Natl Acad Sci USA 111(45):E4896-E4905. doi: 10.1073/pnas.1411117111
46. 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. doi: 10.1074/jbc.M101722200
47. Cai X, Xu Y, Cheung AK et al (2013) PIKfyve, a class III PI Kinase, is the target of the small molecular IL-12/IL-23 inhibitor apilimod and a player in toll-like receptor signaling. Chem Biol 20:912-921. doi: 10.1016/j.chembiol.2013.05.010
48. Caporaso GL, Takei K, Gandy SE et al (1994) Morphologic and biochemical analysis of the intracellular trafficking of the Alzheimer beta/A4 amyloid precursor protein. J Neurosci Off J Soc Neurosci 14:3122-3138
49. Selkoe DJ, Podlisny MB, Joachim CL et al (1988) Beta-amyloid precursor protein of Alzheimer disease occurs as 110- to 135-kilodalton membrane-associated proteins in neural and nonneural tissues. Proc Natl Acad Sci USA 85:7341-7345
50. Ikonomov OC, Fligger J, Sbrissa D et al (2009) Kinesin adapter JLP links PIKfyve to microtubule-based endosome-to-trans-Golgi network traffic of furin. J Biol Chem 284:3750-3761. doi: 10.1074/jbc.M806539200
51. Ikonomov OC, Sbrissa D, Mlak K et al (2003) Active PIKfyve associates with and promotes the membrane attachment of the late endosome-to-trans-Golgi network transport factor Rab9 effector p40. J Biol Chem 278:50863-50871. doi: 10.1074/jbc.M307260200
52. Burd CG, Emr SD (1998) Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains. Mol Cell 2:157-162. doi: 10.1016/S1097-2765(00)80125-2
53. Nixon RA, Cataldo AM, Mathews PM (2000) The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochem Res 25:1161-1172