The nuclear protein Waharan is required for endosomal-lysosomal trafficking in Drosophila

Journal of Cell Science

Volumn 123, Issue 14, 2010, Pages 2369-2374

  Lone, Mohiddin ^a,e   Kungl, Theresa ^a   Koper, Andre ^a   Bottenberg, Wolfgang ^a,f   Kammerer, Richard ^a   Klein, Melanie ^a   Sweeney, Sean T ^b   Auburn, Richard P ^c,d   O'Kane, Cahir J ^c   Prokop, Andreas ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f R Biopharm AG Rhome Ltd Scotland   (Germany)

Author keywords

Drosophila; Endosome; Muscle; Nuclear proteins; Ubiquitin

Indexed keywords

NUCLEAR PROTEIN; PROTEIN WAHARAN; UNCLASSIFIED DRUG;

ACIDITY; ARTICLE; BIOACCUMULATION; CELL COMPARTMENTALIZATION; DROSOPHILA; ENDOSOME; LYSOSOME; MORPHOLOGY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES POMBE; UBIQUITINATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA; DROSOPHILA PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; GENE KNOCKDOWN TECHNIQUES; HUMANS; LYSOSOMES; MUSCLES; NUCLEAR PROTEINS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES; UBIQUITINATION; VESICULAR TRANSPORT PROTEINS;

SCHIZOSACCHAROMYCES POMBE;

EID: 77954915703     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.060582     Document Type: Article

References (41)

1. Arents, G. and Moudrianakis, E. N. (1995). The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. USA 92, 11170-11174.
2. Askree, S. H., Yehuda, T., Smolikov, S., Gurevich, R., Hawk, J., Coker, C., Krauskopf, A., Kupiec, M. and McEachern, M. J. (2004). A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl. Acad. Sci. USA 101, 8658-8663.
3. Bate, M. (1993). The mesoderm and its derivatives. In The development of Drosophila melanogaster, vol. 2 (eds M. Bate and A. Martínez Arias), pp. 1013-1090. Cold Spring Harbor: CSH Laboratory Press.
4. Baudhuin, P., Beaufay, H. and De Duve, C. (1965). Combined biochemical and morphological study of particulate fractions from rat liver. Analysis of preparations enriched in lysosomes or in particles containing urate oxidase, D-amino acid oxidase, and catalase. J. Cell Biol. 26, 219-243.
5. Berndsen, C. E., Tsubota, T., Lindner, S. E., Lee, S., Holton, J. M., Kaufman, P. D., Keck, J. L. and Denu, J. M. (2008). Molecular functions of the histone acetyltransferase chaperone complex Rtt109-Vps75. Nat. Struct. Mol. Biol. 15, 948-956.
6. Bottenberg, W. (2004). Neuronal differentiation and epithelial integrity: The role of Drosophila Short stop. In Inst. Genetics, pp. 166. Mainz: Johannes Gutenberg-University.
7. Budnik, V., Koh, Y. H., Guan, B., Hartmann, B., Hough, C., Woods, D. and Gorczyca, M. (1996). Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 17, 627-40. (Pubitemid 26365343)
8. Budnik, V., Gorczyca, M. and Prokop, A. (2006). Selected methods for the anatomical study of Drosophila embryonic and larval neuromuscular junctions. Int. Rev. Neurobiol. 75, 323-365. (Pubitemid 44809149)
9. Cornell, M., Evans, D. A., Mann, R., Fostier, M., Flasza, M., Monthatong, M., Artavanis-Tsakonas, S. and Baron, M. (1999). The Drosophila melanogaster Suppressor of deltex gene, a regulator of the Notch receptor signaling pathway, is an E3 class ubiquitin ligase. Genetics 152, 567-576.
10. Deák, P., Omar, M. M., Saunders, R. D., Pal, M., Komonyi, O., Szidonya, J., Maroy, P., Zhang, Y., Ashburner, M., Benos, P. et al. (1997). P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: correlation of physical and cytogenetic maps in chromosomal region 86E-87F. Genetics 147, 1697-1722.
11. Dudu, V., Bittig, T., Entchev, E., Kicheva, A., Julicher, F. and González-Gaitán, M. (2006). Postsynaptic mad signaling at the Drosophila neuromuscular junction. Curr. Biol. 16, 625-635.
12. Entchev, E. V., Schwabedissen, A. and González-Gaitán, M. (2000). Gradient formation of the TGF-beta homolog Dpp. Cell 103, 981-991.
13. Kegel, K. B., Kim, M., Sapp, E., McIntyre, C., Castano, J. G., Aronin, N. and DiFiglia, M. (2000). Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J. Neurosci. 20, 7268-7278.
14. Landgraf, M., Sánchez-Soriano, N., Technau, G. M., Urban, J. and Prokop, A. (2003). Charting the Drosophila neuropile: a strategy for the standardised characterisation of genetically amenable neurites. Dev. Biol. 260, 207-225. (Pubitemid 36900345)
15. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461. (Pubitemid 29159845)
16. Lloyd, T. E., Atkinson, R., Wu, M. N., Zhou, Y., Pennetta, G. and Bellen, H. J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269. (Pubitemid 34161145)
17. Marin, I. (2003). Evolution of chromatin-remodeling complexes: comparative genomics reveals the ancient origin of "novel" compensasome genes. J. Mol. Evol. 56, 527-539.
18. Mendjan, S., Taipale, M., Kind, J., Holz, H., Gebhardt, P., Schelder, M., Vermeulen, M., Buscaino, A., Duncan, K., Mueller, J. et al. (2006). Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol. Cell 21, 811-823.
19. Mudher, A., Shepherd, D., Newman, T. A., Mildren, P., Jukes, J. P., Squire, A., Mears, A., Berg, S., MacKay, D., Asuni, A. A. et al. (2004). GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol. Psychiatry 9, 522-530.
20. Nakano, Y., Fujitani, K., Kurihara, J., Ragan, J., Usui-Aoki, K., Shimoda, L., Lukacsovich, T., Suzuki, K., Sezaki, M., Sano, Y. et al. (2001). Mutations in the novel membrane protein spinster interfere with programmed cell death and cause neural degeneration in Drosophila melanogaster. Mol. Cell. Biol. 21, 3775-3788.
21. Oliveira, S. A., Scott, W. K., Zhang, F., Stajich, J. M., Fujiwara, K., Hauser, M., Scott, B. L., Pericak-Vance, M. A., Vance, J. M. and Martin, E. R. (2004). Linkage disequilibrium and haplotype tagging polymorphisms in the Tau H1 haplotype. Neurogenetics 5, 147-155. (Pubitemid 39361967)
22. Pilecka, I., Banach-Orlowska, M. and Miaczynska, M. (2007). Nuclear functions of endocytic proteins. Eur. J. Cell Biol. 86, 533-547.
23. Plickert, G., Gajewski, M., Gehrke, G., Gausepohl, H., Schlossherr, J. and Ibrahim, H. (1997). Automated in situ detection (AISD) of biomolecules. Dev. Genes Evol. 207, 362-367. (Pubitemid 27497062)
24. Pulipparacharuvil, S., Akbar, M. A., Ray, S., Sevrioukov, E. A., Haberman, A. S., Rohrer, J. and Kramer, H. (2005). Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J. Cell Sci. 118, 3663-3673. (Pubitemid 41309413)
25. Razi, M. and Futter, C. E. (2006). Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. Mol. Biol. Cell 17, 3469-3483. (Pubitemid 44156441)
26. Schweisguth, F. (1999). Dominant-negative mutation in the beta2 and beta6 proteasome subunit genes affect alternative cell fate decisions in the Drosophila sense organ lineage. Proc. Natl. Acad. Sci. USA 96, 11382-11386.
27. Sorkin, A. and von Zastrow, M. (2009). Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622.
28. Spradling, A. C., Stern, D., Beaton, A., Rhem, E. J., Laverty, T., Mozden, N., Misra, S. and Rubin, G. M. (1999). The Berkeley Drosophila genome project gene disruption project. Single P-element insertions mutating 25% of vital Drosophila genes. Genetics 153, 135-177. (Pubitemid 29434774)
29. Stauffer, D. R., Howard, T. L., Nyun, T. and Hollenberg, S. M. (2001). CHMP1 is a novel nuclear matrix protein affecting chromatin structure and cell-cycle progression. J. Cell Sci. 114, 2383-2393. (Pubitemid 32684794)
30. Sutherland, D. J., Li, M., Liu, X. Q., Stefancsik, R. and Raftery, L. A. (2003). Stepwise formation of a SMAD activity gradient during dorsal-ventral patterning of the Drosophila embryo. Development 130, 5705-5716. (Pubitemid 37540845)
31. Sweeney, N. T., Brenman, J. E., Jan, Y. N. and Gao, F. B. (2006). The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila. Curr. Biol. 16, 1006-1011.
32. Sweeney, S. T. and Davis, G. W. (2002). Unrestricted synaptic growth in spinster-a late endosomal protein implicated in TGF-beta-mediated synaptic growth regulation. Neuron 36, 403-416.
33. Tanimoto, H., Itoh, S., ten Dijke, P. and Tabata, T. (2000). Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol. Cell 5, 59-71.
34. Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81-85. (Pubitemid 19205971)
35. Thor, S., Andersson, S. G., Tomlinson, A. and Thomas, J. B. (1999). A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature 397, 76-80. (Pubitemid 29038252)
36. Vogler, G. and Urban, J. (2008). The transcription factor Zfh1 is involved in the regulation of neuropeptide expression and growth of larval neuromuscular junctions in Drosophila melanogaster. Dev. Biol. 319, 78-85.
37. Weiss, P., Huppert, S. and Kolling, R. (2008). ESCRT-III protein Snf7 mediates high-level expression of the SUC2 gene via the Rim101 pathway. Eukaryotic Cell 7, 1888-1894.
38. Wu, W. H., Alami, S., Luk, E., Wu, C. H., Sen, S., Mizuguchi, G., Wei, D. and Wu, C. (2005). Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat. Struct. Mol. Biol. 12, 1064-1071. (Pubitemid 41746776)
39. Wucherpfennig, T., Wilsch-Brauninger, M. and González- Gaitán, M. (2003). Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161, 609-624.
40. Xu, Z., Gong, Q., Xia, B., Groves, B., Zimmermann, M., Mugler, C., Mu, D., Matsumoto, B., Seaman, M. and Ma, D. (2009). A role of histone H3 lysine 4 methyltransferase components in endosomal trafficking. J. Cell Biol. 186, 343-353.
41. Yeghiayan, P., Tu, J., Vallier, L. G. and Carlson, M. (1995). Molecular analysis of the SNF8 gene of Saccharomyces cerevisiae. Yeast 11, 219-224.