Rab8, POSH, and TAK1 regulate synaptic growth in a Drosophila model of frontotemporal dementia

Journal of Cell Biology

Volumn 208, Issue 7, 2015, Pages 931-947

  West, Ryan J H ^a   Lu, Yubing ^b   Marie, Bruno ^c   Gao, Fen Biao ^b   Sweeney, Sean T ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UBIQUITIN PROTEIN LIGASE E3; CARRIER PROTEIN; CHMP2B PROTEIN, DROSOPHILA; CYTOSKELETON PROTEIN; DROSOPHILA PROTEIN; GUANOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; NERVE PROTEIN; POSH PROTEIN, DROSOPHILA; RAB8 PROTEIN, DROSOPHILA; TAK1 PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR AP 1; VESICULAR TRANSPORT PROTEIN;

ARTICLE; BRAIN DEVELOPMENT; DROSOPHILA MELANOGASTER; DROSOPHILA STRAIN; ENHANCER REGION; FRONTOTEMPORAL DEMENTIA; FRUIT FLY MODEL; GENE EXPRESSION; GENE INTERACTION; GENETIC SCREENING; GROWTH REGULATION; INSECT GENOME; MOTONEURON; NERVE DEGENERATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAB8 GENE; SIGNAL TRANSDUCTION; TIGHT JUNCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; ENDOSOME; GENETICS; METABOLISM; MOUSE; MUTATION; NEUROMUSCULAR JUNCTION; PATHOLOGY; TRANSGENIC ANIMAL;

DROSOPHILA MELANOGASTER;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARRIER PROTEINS; CELLS, CULTURED; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; FRONTOTEMPORAL DEMENTIA; GTP PHOSPHOHYDROLASES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; MUTATION; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSFORMING GROWTH FACTOR BETA; VESICULAR TRANSPORT PROTEINS;

EID: 84928252437     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201404066     Document Type: Article

References (108)

1. Aberle, H., A.P. Haghighi, R.D. Fetter, B.D. McCabe, T.R. Magalhães, and C.S. Goodman. 2002. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron. 33:545-558. http://dx.doi.org/10.1016/S0896-6273(02)00589-5
2. Ahmad, S.T., S.T. Sweeney, J.-A. Lee, N.T. Sweeney, and F.-B. Gao. 2009. Genetic screen identifies serpin5 as a regulator of the toll pathway and CHMP2B toxicity associated with frontotemporal dementia. Proc. Natl. Acad. Sci. USA. 106:12168-12173. http://dx.doi.org/10.1073/pnas .0903134106
3. Ang, A.L., H. Fölsch, U.M. Koivisto, M. Pypaert, and I. Mellman. 2003. The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J. Cell Biol. 163:339-350. http://dx.doi.org/10.1083/jcb.200307046
4. Antoniou, X., and T. Borsello. 2012. The JNK signalling transduction pathway in the brain. Front Biosci (Elite Ed). E4:2110-2120. http://dx.doi .org/10.2741/E528
5. Baines, R.A. 2004. Synaptic strengthening mediated by bone morphogenetic protein-dependent retrograde signaling in the Drosophila CNS. J. Neurosci. 24:6904-6911. http://dx.doi.org/10.1523/JNEUROSCI.1978-04.2004
6. Baker, M., I.R. Mackenzie, S.M. Pickering-Brown, J. Gass, R. Rademakers, C. Lindholm, J. Snowden, J. Adamson, A.D. Sadovnick, S. Rollinson, et al. 2006. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature. 442:916-919. http://dx.doi.org/10.1038/nature05016
7. Berke, B., J. Wittnam, E. McNeill, D.L. Van Vactor, and H. Keshishian. 2013. Retrograde BMP signaling at the synapse: a permissive signal for synapse maturation and activity-dependent plasticity. J. Neurosci. 33:17937-17950. http://dx.doi.org/10.1523/JNEUROSCI.6075-11.2013
8. Borroni, B., C. Bonvicini, A. Alberici, E. Buratti, C. Agosti, S. Archetti, A. Papetti, C. Stuani, M. Di Luca, M. Gennarelli, and A. Padovani. 2009. Mutation within TARDBP leads to frontotemporal dementia without motor neuron disease. Hum. Mutat. 30:E974-E983. http://dx.doi.org/10.1002/humu.21100
9. Brown, T.C., S.S. Correia, C.N. Petrok, and J.A. Esteban. 2007. Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation. J. Neurosci. 27:13311-13315. http://dx.doi.org/10.1523/JNEUROSCI.4258-07.2007
10. Chan, C.-C., S. Scoggin, D. Wang, S. Cherry, T. Dembo, B. Greenberg, E.J. Jin, C. Kuey, A. Lopez, S.Q. Mehta, et al. 2011. Systematic discovery of Rab GTPases with synaptic functions in Drosophila. Curr. Biol. 21:1704-1715. http://dx.doi.org/10.1016/j.cub.2011.08.058
11. Collins, C.A., Y.P. Wairkar, S.L. Johnson, and A. DiAntonio. 2006. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron. 51:57-69. http://dx.doi.org/10.1016/j.neuron.2006.05.026
12. Cox, L.E., L. Ferraiuolo, E.F. Goodall, P.R. Heath, A. Higginbottom, H. Mortiboys, H.C. Hollinger, J.A. Hartley, A. Brockington, C.E. Burness, et al. 2010. Mutations in CHMP2B in lower motor neuron predominant amyotrophic lateral sclerosis (ALS). PLoS ONE. 5:e9872. http://dx.doi.org/10.1371/journal.pone.0009872
13. Cruts, M., I. Gijselinck, J. van der Zee, S. Engelborghs, H. Wils, D. Pirici, R. Rademakers, R. Vandenberghe, B. Dermaut, J.-J. Martin, et al. 2006. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature. 442:920-924. http://dx .doi.org/10.1038/nature05017
14. Davis, G.W., C.M. Schuster, and C.S. Goodman. 1997. Genetic analysis of the mechanisms controlling target selection: target-derived Fasciclin II regulates the pattern of synapse formation. Neuron. 19:561-573. http://dx.doi .org/10.1016/S0896-6273(00)80372-4
15. DeJesus-Hernandez, M., I.R. Mackenzie, B.F. Boeve, A.L. Boxer, M. Baker, N.J. Rutherford, A.M. Nicholson, N.A. Finch, H. Flynn, J. Adamson, et al. 2011. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron. 72:245-256. http://dx.doi.org/10.1016/j.neuron.2011.09.011
16. Delaney, J.R., S. Stöven, H. Uvell, K.V. Anderson, Y. Engström, and M. Mlodzik. 2006. Cooperative control of Drosophila immune responses by the JNK and NF-kappaB signaling pathways. EMBO J. 25:3068-3077. http://dx.doi.org/10.1038/sj.emboj.7601182
17. Derynck, R., and Y.E. Zhang. 2003. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature. 425:577-584. http://dx .doi.org/10.1038/nature02006
18. Engel, M.E., M.A. McDonnell, B.K. Law, and H.L. Moses. 1999. Interdependent SMAD and JNK signaling in transforming growth factor-β-mediated transcription. J. Biol. Chem. 274:37413-37420. http://dx.doi.org/10.1074/jbc.274.52.37413
19. Eresh, S., J. Riese, D.B. Jackson, D. Bohmann, and M. Bienz. 1997. A CREBbinding site as a target for decapentaplegic signalling during Drosophila endoderm induction. EMBO J. 16:2014-2022. http://dx.doi.org/10.1093/emboj/16.8.2014
20. Esseltine, J.L., F.M. Ribeiro, and S.S.G. Ferguson. 2012. Rab8 modulates metabotropic glutamate receptor subtype 1 intracellular trafficking and signaling in a protein kinase C-dependent manner. J. Neurosci. 32:16933-16942. http://dx.doi.org/10.1523/JNEUROSCI.0625-12.2012
21. Filimonenko, M., S. Stuffers, C. Raiborg, A. Yamamoto, L. Malerød, E.M.C. Fisher, A. Isaacs, A. Brech, H. Stenmark, and A. Simonsen. 2007. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J. Cell Biol. 179:485-500. http://dx.doi.org/10.1083/jcb.200702115
22. Freeman, M. 1996. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell. 87:651-660. http://dx.doi .org/10.1016/S0092-8674(00)81385-9
23. Fuentes-Medel, Y., J. Ashley, R. Barria, R. Maloney, M. Freeman, and V. Budnik. 2012. Integration of a retrograde signal during synapse formation by glia-secreted TGF-β ligand. Curr. Biol. 22:1831-1838. http://dx.doi.org/10.1016/j.cub.2012.07.063
24. Fukuda, T., L. Ewan, M. Bauer, R.J. Mattaliano, K. Zaal, E. Ralston, P.H. Plotz, and N. Raben. 2006. Dysfunction of endocytic and autophagic pathways in a lysosomal storage disease. Ann. Neurol. 59:700-708. http://dx.doi.org/10.1002/ana.20807
25. Gascon, E., K. Lynch, H. Ruan, S. Almeida, J.M. Verheyden, W.W. Seeley, D.W. Dickson, L. Petrucelli, D. Sun, J. Jiao, et al. 2014. Alterations in microRNA-124 and AMPA receptors contribute to social behavioral deficits in frontotemporal dementia. Nat. Med. 20:1444-1451. http://dx.doi .org/10.1038/nm.3717
26. Gerges, N.Z., D.S. Backos, and J.A. Esteban. 2004. Local control of AMPA receptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J. Biol. Chem. 279:43870-43878. http://dx.doi.org/10.1074/jbc.M404982200
27. Giagtzoglou, N., S. Yamamoto, D. Zitserman, H.K. Graves, K.L. Schulze, H. Wang, H. Klein, F. Roegiers, and H.J. Bellen. 2012. dEHBP1 controls exocytosis and recycling of Delta during asymmetric divisions. J. Cell Biol. 196:65-83. http://dx.doi.org/10.1083/jcb.201106088
28. Goold, C.P., and G.W. Davis. 2007. The BMP ligand Gbb gates the expression of synaptic homeostasis independent of synaptic growth control. Neuron. 56:109-123. http://dx.doi.org/10.1016/j.neuron.2007.08.006
29. Hardy, J., and E. Rogaeva. 2013. Motor neuron disease and frontotemporal dementia: sometimes related, sometimes not. Exp. Neurol. 262(Pt. B):75-83.
30. Henne, W.M., N.J. Buchkovich, and S.D. Emr. 2011. The ESCRT pathway. Dev. Cell. 21:77-91. http://dx.doi.org/10.1016/j.devcel.2011.05.015
31. Huber, L.A., M.J. de Hoop, P. Dupree, M. Zerial, K. Simons, and C. Dotti. 1993a. Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p. J. Cell Biol. 123:47-55. http://dx.doi.org/10.1083/jcb.123.1.47
32. Huber, L.A., S. Pimplikar, R.G. Parton, H. Virta, M. Zerial, and K. Simons. 1993b. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J. Cell Biol. 123:35-45. http://dx.doi.org/10.1083/jcb.123.1.35
33. Hutton, M., C.L. Lendon, P. Rizzu, M. Baker, S. Froelich, H. Houlden, S. Pickering-Brown, S. Chakraverty, A. Isaacs, A. Grover, et al. 1998. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature. 393:702-705. http://dx.doi.org/10.1038/31508
34. Inoue, H., T. Imamura, Y. Ishidou, M. Takase, Y. Udagawa, Y. Oka, K. Tsuneizumi, T. Tabata, K. Miyazono, and M. Kawabata. 1998. Interplay of signal mediators of decapentaplegic (Dpp): molecular characterization of mothers against dpp, Medea, and daughters against dpp. Mol. Biol. Cell. 9:2145-2156. http://dx.doi.org/10.1091/mbc.9.8.2145
35. Jékely, G., and P. Rørth. 2003. Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep. 4:1163-1168. http://dx.doi .org/10.1038/sj.embor.7400019
36. Kasprowicz, J., S. Kuenen, K. Miskiewicz, R.L.P. Habets, L. Smitz, and P. Verstreken. 2008. Inactivation of clathrin heavy chain inhibits synaptic recycling but allows bulk membrane uptake. J. Cell Biol. 182:1007-1016.
37. Kawasaki, F., J. Iyer, L.L. Posey, C.E. Sun, S.E. Mammen, H. Yan, and R.W. Ordway. 2011. The DISABLED protein functions in CLATHRIN-mediated synaptic vesicle endocytosis and exoendocytic coupling at the active zone. Proc. Natl. Acad. Sci. USA. 108:E222-E229. http://dx.doi.org/10.1073/pnas.1102231108
38. Kim, G.-H., E. Park, Y.-Y. Kong, and J.-K. Han. 2006. Novel function of POSH, a JNK scaffold, as an E3 ubiquitin ligase for the Hrs stability on early endosomes. Cell. Signal. 18:553-563. http://dx.doi.org/10.1016/j.cellsig .2005.05.026
39. Kovacs, G.G., J.R. Murrell, S. Horvath, L. Haraszti, K. Majtenyi, M.J. Molnar, H. Budka, B. Ghetti, and S. Spina. 2009. TARDBP variation associated with frontotemporal dementia, supranuclear gaze palsy, and chorea. Mov.Disord. 24:1843-1847.
40. Kukekov, N.V., Z. Xu, and L.A. Greene. 2006. Direct interaction of the molecular scaffolds POSH and JIP is required for apoptotic activation of JNKs. J. Biol. Chem. 281:15517-15524. http://dx.doi.org/10.1074/jbc .M601056200
41. Lee, J.-A., A. Beigneux, S.T. Ahmad, S.G. Young, and F.-B. Gao. 2007. ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr. Biol. 17:1561-1567. http://dx.doi.org/10.1016/j.cub.2007.07.029
42. Lee, Y.S., and R.W. Carthew. 2003. Making a better RNAi vector for Drosophila: use of intron spacers. Methods. 30:322-329. http://dx.doi.org/10.1016/S1046-2023(03)00051-3
43. Lennox, A.L., and B. Stronach. 2010. POSH misexpression induces caspasedependent cell death in Drosophila. Dev. Dyn. 239:651-664. http://dx .doi.org/10.1002/dvdy.22186
44. Ling, S.-C., M. Polymenidou, and D.W. Cleveland. 2013. Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron. 79:416-438. http://dx.doi.org/10.1016/j.neuron.2013.07.033
45. Lloyd, T.E., R. Atkinson, M.N. Wu, Y. Zhou, G. Pennetta, and H.J. Bellen. 2002. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell. 108:261-269. http://dx.doi .org/10.1016/S0092-8674(02)00611-6
46. Lu, Y., Z. Zhang, D. Sun, S.T. Sweeney, and F.-B. Gao. 2013. Syntaxin 13, a genetic modifier of mutant CHMP2B in frontotemporal dementia, is required for autophagosome maturation. Mol. Cell. 52:264-271. http://dx.doi.org/10.1016/j.molcel.2013.08.041
47. Maldonado, C., D. Alicea, M. Gonzalez, M. Bykhovskaia, and B. Marie. 2013. Adar is essential for optimal presynaptic function. Mol. Cell. Neurosci. 52:173-180. http://dx.doi.org/10.1016/j.mcn.2012.10.009
48. Mao, R., Y. Fan, Y. Mou, H. Zhang, S. Fu, and J. Yang. 2011. TAK1 lysine 158 is required for TGF-β-induced TRAF6-mediated Smad-independent IKK/NF-kB and JNK/AP-1 activation. Cell. Signal. 23:222-227. http://dx.doi.org/10.1016/j.cellsig.2010.09.006
49. Marie, B., S.T. Sweeney, K.E. Poskanzer, J. Roos, R.B. Kelly, and G.W. Davis. 2004. Dap160/intersectin scaffolds the periactive zone to achieve highfidelity endocytosis and normal synaptic growth. Neuron. 43:207-219. http://dx.doi.org/10.1016/j.neuron.2004.07.001
50. Marqués, G. 2005. Morphogens and synaptogenesis in Drosophila. J. Neurobiol. 64:417-434. http://dx.doi.org/10.1002/neu.20165
51. Marqués, G., H. Bao, T.E. Haerry, M.J. Shimell, P. Duchek, B. Zhang, and M.B. O'Connor. 2002. The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron. 33:529-543. http://dx.doi.org/10.1016/S0896-6273(02)00595-0
52. Martín-Blanco, E., A. Gampel, J. Ring, K. Virdee, N. Kirov, A.M. Tolkovsky, and A. Martinez-Arias. 1998. puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12:557-570. http://dx.doi.org/10.1101/gad.12.4.557
53. Massagué, J. 2012. TGFβ signalling in context. Nat. Rev. Mol. Cell Biol. 13:616-630. http://dx.doi.org/10.1038/nrm3434
54. McCabe, B.D., G. Marqués, A.P. Haghighi, R.D. Fetter, M.L. Crotty, T.E. Haerry, C.S. Goodman, and M.B. O'Connor. 2003. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron. 39:241-254. http://dx.doi .org/10.1016/S0896-6273(03)00426-4
55. McCabe, B.D., S. Hom, H. Aberle, R.D. Fetter, G. Marqués, T.E. Haerry, H. Wan, M.B. O'Connor, C.S. Goodman, and A.P. Haghighi. 2004. Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron. 41:891-905. http://dx.doi.org/10.1016/S0896-6273(04)00073-X
56. Mihaly, J., L. Kockel, K. Gaengel, U. Weber, D. Bohmann, and M. Mlodzik. 2001. The role of the Drosophila TAK homologue dTAK during development. Mech. Dev. 102:67-79. http://dx.doi.org/10.1016/S0925-4773(01)00285-4
57. Milton, V.J., H.E. Jarrett, K. Gowers, S. Chalak, L. Briggs, I.M. Robinson, and S.T. Sweeney. 2011. Oxidative stress induces overgrowth of the Drosophila neuromuscular junction. Proc. Natl. Acad. Sci. USA. 108: 17521-17526. http://dx.doi.org/10.1073/pnas.1014511108
58. Moritz, O.L., B.M. Tam, L.L. Hurd, J. Peränen, D. Deretic, and D.S. Papermaster. 2001. Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol. Biol. Cell. 12:2341-2351. http://dx.doi.org/10.1091/mbc.12.8.2341
59. Neubert, M., D.A. Ridder, P. Bargiotas, S. Akira, and M. Schwaninger. 2011. Acute inhibition of TAK1 protects against neuronal death in cerebral ischemia. Cell Death Differ. 18:1521-1530. http://dx.doi.org/10.1038/cdd.2011.29
60. O'Connor-Giles, K.M., L.L. Ho, and B. Ganetzky. 2008. Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron. 58:507-518. http://dx.doi.org/10.1016/j.neuron.2008.03.007
61. Parkinson, N., P.G. Ince, M.O. Smith, R. Highley, G. Skibinski, P.M. Andersen, K.E. Morrison, H.S. Pall, O. Hardiman, J. Collinge, et al. FReJA Consortium. 2006. ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology. 67:1074-1077. http://dx.doi .org/10.1212/01.wnl.0000231510.89311.8b
62. Pauli, A., F. Althoff, R.A. Oliveira, S. Heidmann, O. Schuldiner, C.F. Lehner, B.J. Dickson, and K. Nasmyth. 2008. Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons. Dev. Cell. 14:239-251. http://dx.doi.org/10.1016/j.devcel.2007.12.009
63. Perlman, R., W.P. Schiemann, M.W. Brooks, H.F. Lodish, and R.A. Weinberg. 2001. TGF-β-induced apoptosis is mediated by the adapter protein Daxx that facilitates JNK activation. Nat. Cell Biol. 3:708-714. http://dx.doi .org/10.1038/35087019
64. Persson, U., H. Izumi, S. Souchelnytskyi, S. Itoh, S. Grimsby, U. Engström, C.H. Heldin, K. Funa, and P. ten Dijke. 1998. The L45 loop in type I receptors for TGF-β family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434:83-87. http://dx.doi .org/10.1016/S0014-5793(98)00954-5
65. Pulipparacharuvil, S., M.A. Akbar, S. Ray, E.A. Sevrioukov, A.S. Haberman, J. Rohrer, and H. Krämer. 2005. Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J. Cell Sci. 118:3663-3673. http://dx.doi.org/10.1242/jcs.02502
66. Rawson, J.M., M. Lee, E.L. Kennedy, and S.B. Selleck. 2003. Drosophila neuromuscular synapse assembly and function require the TGF-β type I receptor saxophone and the transcription factor Mad. J. Neurobiol. 55:134-150. http://dx.doi.org/10.1002/neu.10189
67. Renton, A.E., E. Majounie, A. Waite, J. Simón-Sánchez, S. Rollinson, J.R. Gibbs, J.C. Schymick, H. Laaksovirta, J.C. van Swieten, L. Myllykangas, et al. ITALSGEN Consortium. 2011. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron. 72:257-268. http://dx.doi.org/10.1016/j.neuron.2011.09.010
68. Ringholz, G.M., and S.R. Greene. 2006. The relationship between amyotrophic lateral sclerosis and frontotemporal dementia. Curr. Neurol. Neurosci. Rep. 6:387-392. http://dx.doi.org/10.1007/s11910-996-0019-6
69. Robinson, I.M., R. Ranjan, and T.L. Schwarz. 2002. Synaptotagmins I and IV promote transmitter release independently of Ca(2+) binding in the C(2)A domain. Nature. 418:336-340. http://dx.doi.org/10.1038/nature00915
70. Rodal, A.A., A.D. Blunk, Y. Akbergenova, R.A. Jorquera, L.K. Buhl, and J.T. Littleton. 2011. A presynaptic endosomal trafficking pathway controls synaptic growth signaling. J. Cell Biol. 193:201-217. http://dx.doi.org/10.1083/jcb.201009052
71. Rusten, T.E., T. Vaccari, K. Lindmo, L.M.W. Rodahl, I.P. Nezis, C. Sem-Jacobsen, F. Wendler, J.-P. Vincent, A. Brech, D. Bilder, and H. Stenmark. 2007. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr. Biol. 17:1817-1825. http://dx.doi.org/10.1016/j.cub.2007.09.032
72. Ryder, E., M. Ashburner, R. Bautista-Llacer, J. Drummond, J. Webster, G. Johnson, T. Morley, Y.S. Chan, F. Blows, D. Coulson, et al. 2007. The DrosDel deletion collection: a Drosophila genomewide chromosomal deficiency resource. Genetics. 177:615-629. http://dx.doi.org/10.1534/genetics.107.076216
73. Sanyal, S. 2009. Genomic mapping and expression patterns of C380, OK6 and D42 enhancer trap lines in the larval nervous system of Drosophila. Gene Expr. Patterns. 9:371-380. http://dx.doi.org/10.1016/j.gep.2009.01.002
74. Sanyal, S., D.J. Sandstrom, C.A. Hoeffer, and M. Ramaswami. 2002. AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila. Nature. 416:870-874. http://dx.doi.org/10.1038/416870a
75. Sato, T., S. Mushiake, Y. Kato, K. Sato, M. Sato, N. Takeda, K. Ozono, K. Miki, Y. Kubo, A. Tsuji, et al. 2007. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature. 448:366-369. http://dx.doi.org/10.1038/nature05929
76. Sato, T., T. Iwano, M. Kunii, S. Matsuda, R. Mizuguchi, Y. Jung, H. Hagiwara, Y. Yoshihara, M. Yuzaki, R. Harada, and A. Harada. 2014. Rab8a and Rab8b are essential for several apical transport pathways but insufficient for ciliogenesis. J. Cell Sci. 127:422-431. http://dx.doi.org/10.1242/jcs.136903
77. Sekelsky, J.J., S.J. Newfeld, L.A. Raftery, E.H. Chartoff, and W.M. Gelbart. 1995. Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics. 139:1347-1358.
78. Seto, E.S., H.J. Bellen, and T.E. Lloyd. 2002. When cell biology meets development: endocytic regulation of signaling pathways. Genes Dev. 16:1314-1336. http://dx.doi.org/10.1101/gad.989602
79. Shi, W., Y. Chen, G. Gan, D. Wang, J. Ren, Q. Wang, Z. Xu, W. Xie, and Y.Q. Zhang. 2013. Brain tumor regulates neuromuscular synapse growth and endocytosis in Drosophila by suppressing mad expression. J. Neurosci. 33:12352-12363. http://dx.doi.org/10.1523/JNEUROSCI.0386-13.2013
80. Shimizu, H., S. Kawamura, and K. Ozaki. 2003. An essential role of Rab5 in uniformity of synaptic vesicle size. J. Cell Sci. 116:3583-3590. http://dx.doi .org/10.1242/jcs.00676
81. Skibinski, G., N.J. Parkinson, J.M. Brown, L. Chakrabarti, S.L. Lloyd, H. Hummerich, J.E. Nielsen, J.R. Hodges, M.G. Spillantini, T. Thusgaard, et al. 2005. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat. Genet. 37:806-808. http://dx.doi.org/10.1038/ng1609
82. Smith, R.B., J.B. Machamer, N.C. Kim, T.S. Hays, and G. Marqués. 2012. Relay of retrograde synaptogenic signals through axonal transport of BMP receptors. J. Cell Sci. 125:3752-3764. http://dx.doi.org/10.1242/jcs.094292
83. Sorrentino, A., N. Thakur, S. Grimsby, A. Marcusson, V. von Bulow, N. Schuster, S. Zhang, C.-H. Heldin, and M. Landström. 2008. The type I TGF-β receptor engages TRAF6 to activate TAK1 in a receptor kinaseindependent manner. Nat. Cell Biol. 10:1199-1207. http://dx.doi.org/10.1038/ncb1780
84. Sweeney, N.T., J.E. Brenman, Y.N. Jan, and F.B. Gao. 2006. The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila. Curr. Biol. 16:1006-1011. http://dx.doi.org/10.1016/j.cub.2006.03.067
85. Sweeney, S.T., and G.W. Davis. 2002. Unrestricted synaptic growth in spinster-a late endosomal protein implicated in TGF-β-mediated synaptic growth regulation. Neuron. 36:403-416. http://dx.doi.org/10.1016/S0896-6273(02)01014-0
86. Tanaka, T., and A. Nakamura. 2008. The endocytic pathway acts downstream of Oskar in Drosophila germ plasm assembly. Development. 135:1107-1117. http://dx.doi.org/10.1242/dev.017293
87. Tapon, N., K. Nagata, N. Lamarche, and A. Hall. 1998. A new rac target POSH is an SH3-containing scaffold protein involved in the JNK and NF-kappaB signalling pathways. EMBO J. 17:1395-1404. http://dx.doi.org/10.1093/emboj/17.5.1395
88. Tsuda, M., C. Langmann, N. Harden, and T. Aigaki. 2005. The RING-finger scaffold protein Plenty of SH3s targets TAK1 to control immunity signalling in Drosophila. EMBO Rep. 6:1082-1087. http://dx.doi.org/10.1038/sj.embor.7400537
89. Tsuda, M., K.-H. Seong, and T. Aigaki. 2006. POSH, a scaffold protein for JNK signaling, binds to ALG-2 and ALIX in Drosophila. FEBS Lett. 580:3296-3300. http://dx.doi.org/10.1016/j.febslet.2006.05.005
90. Tsuneizumi, K., T. Nakayama, Y. Kamoshida, T.B. Kornberg, J.L. Christian, and T. Tabata. 1997. Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature. 389:627-631. http://dx.doi.org/10.1038/39362
91. Urwin, H., A. Authier, J.E. Nielsen, D. Metcalf, C. Powell, K. Froud, D.S. Malcolm, I. Holm, P. Johannsen, J. Brown, et al. FReJA Consortium. 2010. Disruption of endocytic trafficking in frontotemporal dementia with CHMP2B mutations. Hum. Mol. Genet. 19:2228-2238. http://dx .doi.org/10.1093/hmg/ddq100
92. van Blitterswijk, M., L. Vlam, M.A. van Es, W.L. van der Pol, E.A. Hennekam, D. Dooijes, H.J. Schelhaas, A.J. van der Kooi, M. de Visser, J.H. Veldink, and L.H. van den Berg. 2012. Genetic overlap between apparently sporadic motor neuron diseases. PLoS ONE. 7:e48983. http://dx.doi.org/10.1371/journal.pone.0048983
93. Van Langenhove, T., J. van der Zee, and C. Van Broeckhoven. 2012. The molecular basis of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum. Ann. Med. 44:817-828. http://dx.doi.org/10.3109/07853890.2012.665471
94. Vanlandingham, P.A., T.R. Fore, L.R. Chastain, S.M. Royer, H. Bao, N.E. Reist, and B. Zhang. 2013. Epsin 1 promotes synaptic growth by enhancing BMP signal levels in motoneuron nuclei. PLoS ONE. 8:e65997. http://dx.doi.org/10.1371/journal.pone.0065997
95. Votteler, J., E. Iavnilovitch, O. Fingrut, V. Shemesh, D. Taglicht, O. Erez, S. Sörgel, T. Walther, N. Bannert, U. Schubert, and Y. Reiss. 2009. Exploring the functional interaction between POSH and ALIX and the relevance to HIV-1 release. BMC Biochem. 10:12. http://dx.doi.org/10.1186/1471-2091-10-12
96. Wan, H.I., A. DiAntonio, R.D. Fetter, K. Bergstrom, R. Strauss, and C.S. Goodman. 2000. Highwire regulates synaptic growth in Drosophila. Neuron. 26:313-329. http://dx.doi.org/10.1016/S0896-6273(00)81166-6
97. Wang, X., W.R. Shaw, H.T.H. Tsang, E. Reid, and C.J. O'Kane. 2007. Drosophila spichthyin inhibits BMP signaling and regulates synaptic growth and axonal microtubules. Nat. Neurosci. 10:177-185. http://dx.doi.org/10.1038/nn1841
98. Watts, G.D.J., J. Wymer, M.J. Kovach, S.G. Mehta, S. Mumm, D. Darvish, A. Pestronk, M.P. Whyte, and V.E. Kimonis. 2004. Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36:377-381. http://dx.doi.org/10.1038/ng1332
99. Wheaton, M.W., A.R. Salamone, D.M. Mosnik, R.O. McDonald, S.H. Appel, H.I. Schmolck, G.M. Ringholz, and P.E. Schulz. 2007. Cognitive impairment in familial ALS. Neurology. 69:1411-1417. http://dx.doi.org/ 10.1212/01.wnl.0000277422.11236.2c
100. Winther, A.M.E., W. Jiao, O. Vorontsova, K.A. Rees, T.W. Koh, E. Sopova, K.L. Schulze, H.J. Bellen, and O. Shupliakov. 2013. The dynamin-binding domains of Dap160/intersectin affect bulk membrane retrieval in synapses. J. Cell Sci. 126:1021-1031. http://dx.doi.org/10.1242/jcs.118968
101. Xiao, L., N. Michalski, E. Kronander, E. Gjoni, C. Genoud, G. Knott, and R. Schneggenburger. 2013. BMP signaling specifies the development of a large and fast CNS synapse. Nat. Neurosci. 16:856-864. http://dx.doi .org/10.1038/nn.3414
102. Xu, Z., N.V. Kukekov, and L.A. Greene. 2003. POSH acts as a scaffold for a multiprotein complex that mediates JNK activation in apoptosis. EMBO J.22:252-261. http://dx.doi.org/10.1093/emboj/cdg021
103. Xu, Z., N.V. Kukekov, and L.A. Greene. 2005. Regulation of apoptotic c-Jun N-terminal kinase signaling by a stabilization-based feed-forward loop. Mol. Cell. Biol. 25:9949-9959. http://dx.doi.org/10.1128/MCB.25.22.9949-9959.2005
104. Yamaguchi, K., K. Shirakabe, H. Shibuya, K. Irie, I. Oishi, N. Ueno, T. Taniguchi, E. Nishida, and K. Matsumoto. 1995. Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science. 270:2008-2011. http://dx.doi.org/10.1126/science.270.5244.2008
105. Zhang, B., Y.H. Koh, R.B. Beckstead, V. Budnik, B. Ganetzky, and H.J. Bellen. 1998. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron. 21:1465-1475. http://dx.doi .org/10.1016/S0896-6273(00)80664-9
106. Zhang, J., K.L. Schulze, P.R. Hiesinger, K. Suyama, S. Wang, M. Fish, M. Acar, R.A. Hoskins, H.J. Bellen, and M.P. Scott. 2007. Thirty-one flavors of Drosophila rab proteins. Genetics. 176:1307-1322. http://dx.doi .org/10.1534/genetics.106.066761
107. Zhang, Q.-G., R.-M. Wang, X.-H. Yin, J. Pan, T.-L. Xu, and G.-Y. Zhang. 2005. Knock-down of POSH expression is neuroprotective through downregulating activation of the MLK3-MKK4-JNK pathway following cerebral ischaemia in the rat hippocampal CA1 subfield. J. Neurochem. 95:784-795. http://dx.doi.org/10.1111/j.1471-4159.2005.03435.x
108. Zhang, Q.-G., D. Han, J. Xu, Q. Lv, R. Wang, X.-H. Yin, T.-L. Xu, and G.-Y. Zhang. 2006. Ischemic preconditioning negatively regulates plenty of SH3smixed lineage kinase 3-Rac1 complex and c-Jun N-terminal kinase 3 signaling via activation of Akt. Neuroscience. 143:431-444. http://dx.doi .org/10.1016/j.neuroscience.2006.07.049