The PI3K class III complex promotes axon pruning by downregulating a ptc-derived signal via endosome-lysosomal degradation

Developmental Cell

Volumn 31, Issue 4, 2014, Pages 461-473

  Issman Zecharya, Noa ^a   Schuldiner, Oren ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN PATCHED; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; CELL SURFACE RECEPTOR; DROSOPHILA PROTEIN; PROTEIN BINDING; PTC PROTEIN, DROSOPHILA;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; GENE FUNCTION; IN VIVO STUDY; LYSOSOME; MUSHROOM BODY; NERVE FIBER; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; ULTRAVIOLET RADIATION; ANIMAL; DROSOPHILA MELANOGASTER; EMBRYOLOGY; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; SIGNAL TRANSDUCTION;

BASIDIOMYCOTA; ERINACEIDAE;

ANIMALS; AXONS; DOWN-REGULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCYTOSIS; ENDOSOMES; LYSOSOMES; MUSHROOM BODIES; NEUROGENESIS; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BINDING; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 84921268569     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.10.013     Document Type: Article

References (44)

1. Boulanger A., Clouet-Redt C., Farge M., Flandre A., Guignard T., Fernando C., Juge F., Dura J.M. ftz-f1 and Hr39 opposing roles on EcR expression during Drosophila mushroom body neuron remodeling. Nat. Neurosci. 2011, 14:37-44.
2. Briscoe J., Thérond P.P. The mechanisms of Hedgehog signalling and its roles in development and disease. Nat. Rev. Mol. Cell Biol. 2013, 14:416-429.
3. Briscoe J., Chen Y., Jessell T.M., Struhl G. A hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of sonic hedgehog in the neural tube. Mol. Cell 2001, 7:1279-1291.
4. Burman C., Ktistakis N.T. Regulation of autophagy by phosphatidylinositol 3-phosphate. FEBS Lett. 2010, 584:1302-1312.
5. Callejo A., Culi J., Guerrero I. Patched, the receptor of Hedgehog, is a lipoprotein receptor. Proc. Natl. Acad. Sci. USA 2008, 105:912-917.
6. Chen Y., Struhl G. Dual roles for patched in sequestering and transducing Hedgehog. Cell 1996, 87:553-563.
7. Funderburk S.F., Wang Q.J., Yue Z. The Beclin 1-VPS34 complex-at the crossroads of autophagy and beyond. Trends Cell Biol. 2010, 20:355-362.
8. Gillooly D.J., Morrow I.C., Lindsay M., Gould R., Bryant N.J., Gaullier J.M., Parton R.G., Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 2000, 19:4577-4588.
9. Guichet A., Wucherpfennig T., Dudu V., Etter S., Wilsch-Bräuniger M., Hellwig A., González-Gaitán M., Huttner W.B., Schmidt A.A. Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J. 2002, 21:1661-1672.
10. He S., O'Connell D., Zhang X., Yang Y., Liang C. The intersection of Golgi-ER retrograde and autophagic trafficking. Autophagy 2014, 10:180-181.
11. Incardona J.P., Gruenberg J., Roelink H. Sonic hedgehog induces the segregation of patched and smoothened in endosomes. Curr. Biol. 2002, 12:983-995.
12. Ionov Y., Nowak N., Perucho M., Markowitz S., Cowell J.K. Manipulation of nonsense mediated decay identifies gene mutations in colon cancer cells with microsatellite instability. Oncogene 2004, 23:639-645.
13. Itakura E., Mizushima N. Atg14 and UVRAG: mutually exclusive subunits of mammalian Beclin 1-PI3K complexes. Autophagy 2009, 5:534-536.
14. Itoh F., Divecha N., Brocks L., Oomen L., Janssen H., Calafat J., Itoh S., Dijke Pt P. The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-beta/Smad signalling. Genes Cells 2002, 7:321-331.
15. Jaber N., Dou Z., Chen J.S., Catanzaro J., Jiang Y.P., Ballou L.M., Selinger E., Ouyang X., Lin R.Z., Zhang J., Zong W.X. Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc. Natl. Acad. Sci. USA 2012, 109:2003-2008.
16. Juhász G., Hill J.H., Yan Y., Sass M., Baehrecke E.H., Backer J.M., Neufeld T.P. The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J.Cell Biol. 2008, 181:655-666.
17. Kim M.S., Jeong E.G., Ahn C.H., Kim S.S., Lee S.H., Yoo N.J. Frameshift mutation of UVRAG, an autophagy-related gene, in gastric carcinomas with microsatellite instability. Hum. Pathol. 2008, 39:1059-1063.
18. Kitamoto T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J.Neurobiol. 2001, 47:81-92.
19. Knævelsrud H., Ahlquist T., Merok M.A., Nesbakken A., Stenmark H., Lothe R.A., Simonsen A. UVRAG mutations associated with microsatellite unstable colon cancer do not affect autophagy. Autophagy 2010, 6:863-870.
20. Kutateladze T.G. Translation of the phosphoinositide code by PI effectors. Nat. Chem. Biol. 2010, 6:507-513.
21. Lee T., Lee A., Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999, 126:4065-4076.
22. Lee T., Marticke S., Sung C., Robinow S., Luo L. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 2000, 28:807-818.
23. Lee G., Liang C., Park G., Jang C., Jung J.U., Chung J. UVRAG is required for organ rotation by regulating Notch endocytosis in Drosophila. Dev. Biol. 2011, 356:588-597.
24. Liang C., Feng P., Ku B., Dotan I., Canaani D., Oh B.H., Jung J.U. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat. Cell Biol. 2006, 8:688-699.
25. Low L.K., Cheng H.J. Axon pruning: an essential step underlying the developmental plasticity of neuronal connections. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:1531-1544.
26. Luo L., O'Leary D.D.M. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 2005, 28:127-156.
27. Peplowska K., Cabrera M., Ungermann C. UVRAG reveals its second nature. Nat. Cell Biol. 2008, 10:759-761.
28. Perelman B., Dafni N., Naiman T., Eli D., Yaakov M., Feng T.L., Sinha S., Weber G., Khodaei S., Sancar A., et al. Molecular cloning of a novel human gene encoding a 63-kDa protein and its sublocalization within the 11q13 locus. Genomics 1997, 41:397-405.
29. Pfeiffer B.D., Truman J.W., Rubin G.M. Using translational enhancers to increase transgene expression in Drosophila. Proc. Natl. Acad. Sci. USA 2012, 109:6626-6631.
30. Portera-Cailliau C., Weimer R.M., De Paola V., Caroni P., Svoboda K. Diverse modes of axon elaboration in the developing neocortex. PLoS Biol. 2005, 3:e272.
31. Robbins D.J., Fei D.L., Riobo N.A. The Hedgehog signal transduction network. Sci. Signal. 2012, 5:re6.
32. Rodal A.A., Blunk A.D., Akbergenova Y., Jorquera R.A., Buhl L.K., Littleton J.T. A presynaptic endosomal trafficking pathway controls synaptic growth signaling. J.Cell Biol. 2011, 193:201-217.
33. Schuldiner O., Berdnik D., Levy J.M., Wu J.S., Luginbuhl D., Gontang A.C., Luo L. piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev. Cell 2008, 14:227-238.
34. Shravage B.V., Hill J.H., Powers C.M., Wu L., Baehrecke E.H. Atg6 is required for multiple vesicle trafficking pathways and hematopoiesis in Drosophila. Development 2013, 140:1321-1329.
35. Thoresen S.B., Pedersen N.M., Liestøl K., Stenmark H. A phosphatidylinositol 3-kinase class III sub-complex containing VPS15, VPS34, Beclin 1, UVRAG and BIF-1 regulates cytokinesis and degradative endocytic traffic. Exp. Cell Res. 2010, 316:3368-3378.
36. Tsukazaki T., Chiang T.A., Davison A.F., Attisano L., Wrana J.L. SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell 1998, 95:779-791.
37. Watts R.J., Hoopfer E.D., Luo L. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 2003, 38:871-885.
38. Watts R.J., Schuldiner O., Perrino J., Larsen C., Luo L. Glia engulf degenerating axons during developmental axon pruning. Curr. Biol. 2004, 14:678-684.
39. Yaniv S.P., Issman-Zecharya N., Oren-Suissa M., Podbilewicz B., Schuldiner O. Axon Regrowth during Development and Regeneration Following Injury Share Molecular Mechanisms. Current biology: CB 2012, 22:1774-1782.
40. Yu X.M., Gutman I., Mosca T.J., Iram T., Özkan E., Garcia K.C., Luo L., Schuldiner O. Plum, an immunoglobulin superfamily protein, regulates axon pruning by facilitating TGF-β signaling. Neuron 2013, 78:456-468.
41. Zhang H., Wang Y., Wong J.J., Lim K.L., Liou Y.C., Wang H., Yu F. Endocytic pathways downregulate the L1-type cell adhesion molecule neuroglian to promote dendrite pruning in Drosophila. Dev. Cell 2014, 30:463-478.
42. Zhao Z., Oh S., Li D., Ni D., Pirooz S.D., Lee J.H., Yang S., Lee J.Y., Ghozalli I., Costanzo V., et al. A dual role for UVRAG in maintaining chromosomal stability independent of autophagy. Dev. Cell 2012, 22:1001-1016.
43. Zheng X., Wang J., Haerry T.E., Wu A.Y., Martin J., O'Connor M.B., Lee C.H., Lee T. TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 2003, 112:303-315.
44. Zhou X., Wang L., Hasegawa H., Amin P., Han B.X., Kaneko S., He Y., Wang F. Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway. Proc. Natl. Acad. Sci. USA 2010, 107:9424-9429.