Spindle-F Is the Central Mediator of Ik2 Kinase-Dependent Dendrite Pruning in Sensory Neurons

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In Drosophila, the nervous systems undergo extensive neuronal remodeling during metamorphosis, as many larval neurons die and adult neurons are generated while some larval neurons survive and prune their branches. Pruning that removes specific parts of neuronal branches without causing cell death is a self-destruct process, thus requiring precise regulation to prevent undesired damage to the nervous systems. Certain Drosophila sensory neurons that undergo dendrite pruning, specifically eliminating the dendrites but leaving the axons intact, provide us an opportunity to study the mechanism of how pruning activity is regulated in the dendrites. We reasoned that the distinctive microtubule polarity in dendrites and axons might be involved and factors are required to regulate the pruning activity in the dendrites through their interaction with microtubules. Here, we identified Spindle-F that mediates Ik2-dependent pruning activity in the dendrites by linking Ik2 to the microtubule motor dynein complex. We showed that elevation of Ik2 activity during dendrite pruning promotes Ik2/Spindle-F/dynein complex moving along the microtubules. We also showed that the formation and redistribution of Ik2/Spindle-F/dynein complex are essential for dendrite pruning. Our study reveals a connection between the polarized microtubules of dendrites and the pruning activity through Spindle-F for dendrite pruning.

Vyšlo v časopise: Spindle-F Is the Central Mediator of Ik2 Kinase-Dependent Dendrite Pruning in Sensory Neurons. PLoS Genet 11(11): e32767. doi:10.1371/journal.pgen.1005642
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005642

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Zdroje

1. Kage E, Hayashi Y, Takeuchi H, Hirotsu T, Kunitomo H, et al. (2005) MBR-1, a novel helix-turn-helix transcription factor, is required for pruning excessive neurites in Caenorhabditis elegans. Curr Biol 15: 1554–1559. 16139210

2. Luo L, O'Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28: 127–156. 16022592

3. Hayashi Y, Hirotsu T, Iwata R, Kage-Nakadai E, Kunitomo H, et al. (2009) A trophic role for Wnt-Ror kinase signaling during developmental pruning in Caenorhabditis elegans. Nat Neurosci 12: 981–987. doi: 10.1038/nn.2347 19561603

4. Redt-Clouet C, Trannoy S, Boulanger A, Tokmatcheva E, Savvateeva-Popova E, et al. (2012) Mushroom body neuronal remodelling is necessary for short-term but not for long-term courtship memory in Drosophila. Eur J Neurosci 35: 1684–1691. doi: 10.1111/j.1460-9568.2012.08103.x 22571719

5. Li H, Li SH, Yu ZX, Shelbourne P, Li XJ (2001) Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. J Neurosci 21: 8473–8481. 11606636

6. Tsai J, Grutzendler J, Duff K, Gan WB (2004) Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nat Neurosci 7: 1181–1183. 15475950

7. Watts RJ, Hoopfer ED, Luo L (2003) Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38: 871–885. 12818174

8. Zhai Q, Wang J, Kim A, Liu Q, Watts R, et al. (2003) Involvement of the ubiquitin-proteasome system in the early stages of wallerian degeneration. Neuron 39: 217–225. 12873380

9. Hoopfer ED, McLaughlin T, Watts RJ, Schuldiner O, O'Leary DD, et al. (2006) Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 50: 883–895. 16772170

10. Ciechanover A, Brundin P (2003) The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40: 427–446. 14556719

11. Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126: 4065–4076. 10457015

12. Marin EC, Watts RJ, Tanaka NK, Ito K, Luo L (2005) Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132: 725–737. 15659487

13. Williams DW, Truman JW (2005) Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons. Development 132: 3631–3642. 16033801

14. Kuo CT, Jan LY, Jan YN (2005) Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc Natl Acad Sci U S A 102: 15230–15235. 16210248

15. Lee HH, Jan LY, Jan YN (2009) Drosophila IKK-related kinase Ik2 and Katanin p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc Natl Acad Sci U S A 106: 6363–6368. doi: 10.1073/pnas.0902051106 19329489

16. Han C, Song Y, Xiao H, Wang D, Franc NC, et al. (2014) Epidermal cells are the primary phagocytes in the fragmentation and clearance of degenerating dendrites in Drosophila. Neuron 81: 544–560. doi: 10.1016/j.neuron.2013.11.021 24412417

17. Black MM, Baas PW (1989) The basis of polarity in neurons. Trends Neurosci 12: 211–214. 2473556

18. Stone MC, Roegiers F, Rolls MM (2008) Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol Biol Cell 19: 4122–4129. doi: 10.1091/mbc.E07-10-1079 18667536

19. Ori-McKenney KM, Jan LY, Jan YN (2012) Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76: 921–930. doi: 10.1016/j.neuron.2012.10.008 23217741

20. Kirilly D, Gu Y, Huang Y, Wu Z, Bashirullah A, et al. (2009) A genetic pathway composed of Sox14 and Mical governs severing of dendrites during pruning. Nat Neurosci 12: 1497–1505. doi: 10.1038/nn.2415 19881505

21. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW (2006) Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9: 1234–1236. 16980964

22. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51: 283–290. 16880123

23. Kanamori T, Kanai MI, Dairyo Y, Yasunaga K, Morikawa RK, et al. (2013) Compartmentalized calcium transients trigger dendrite pruning in Drosophila sensory neurons. Science 340: 1475–1478. doi: 10.1126/science.1234879 23722427

24. Abdu U, Bar D, Schupbach T (2006) spn-F encodes a novel protein that affects oocyte patterning and bristle morphology in Drosophila. Development 133: 1477–1484. 16540510

25. Shapiro RS, Anderson KV (2006) Drosophila Ik2, a member of the I kappa B kinase family, is required for mRNA localization during oogenesis. Development 133: 1467–1475. 16540511

26. Dubin-Bar D, Bitan A, Bakhrat A, Kaiden-Hasson R, Etzion S, et al. (2008) The Drosophila IKK-related kinase (Ik2) and Spindle-F proteins are part of a complex that regulates cytoskeleton organization during oogenesis. BMC Cell Biol 9: 51. doi: 10.1186/1471-2121-9-51 18796167

27. Grueber WB, Ye B, Yang CH, Younger S, Borden K, et al. (2007) Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development 134: 55–64. 17164414

28. Kuranaga E, Kanuka H, Tonoki A, Takemoto K, Tomioka T, et al. (2006) Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell 126: 583–596. 16887178

29. Otani T, Oshima K, Onishi S, Takeda M, Shinmyozu K, et al. (2011) IKKepsilon regulates cell elongation through recycling endosome shuttling. Dev Cell 20: 219–232. doi: 10.1016/j.devcel.2011.02.001 21316589

30. Oshima K, Takeda M, Kuranaga E, Ueda R, Aigaki T, et al. (2006) IKK epsilon regulates F actin assembly and interacts with Drosophila IAP1 in cellular morphogenesis. Curr Biol 16: 1531–1537. 16887350

31. Phillis R, Statton D, Caruccio P, Murphey RK (1996) Mutations in the 8 kDa dynein light chain gene disrupt sensory axon projections in the Drosophila imaginal CNS. Development 122: 2955–2963. 8898210

32. Dick T, Ray K, Salz HK, Chia W (1996) Cytoplasmic dynein (ddlc1) mutations cause morphogenetic defects and apoptotic cell death in Drosophila melanogaster. Mol Cell Biol 16: 1966–1977. 8628263

33. Firestone AJ, Weinger JS, Maldonado M, Barlan K, Langston LD, et al. (2012) Small-molecule inhibitors of the AAA+ ATPase motor cytoplasmic dynein. Nature 484: 125–129. doi: 10.1038/nature10936 22425997

34. Rasmusson K, Serr M, Gepner J, Gibbons I, Hays TS (1994) A family of dynein genes in Drosophila melanogaster. Mol Biol Cell 5: 45–55. 8186464

35. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, et al. (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471: 473–479. doi: 10.1038/nature09715 21179090

36. Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, et al. (2008) Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat Cell Biol 10: 1172–1180. doi: 10.1038/ncb1777 18758451

37. Gepner J, Li M, Ludmann S, Kortas C, Boylan K, et al. (1996) Cytoplasmic dynein function is essential in Drosophila melanogaster. Genetics 142: 865–878. 8849893

38. Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252: 1162–1164. 2031185

39. Raff MC, Whitmore AV, Finn JT (2002) Axonal self-destruction and neurodegeneration. Science 296: 868–871. 11988563

40. Hoopfer ED, Penton A, Watts RJ, Luo L (2008) Genomic analysis of Drosophila neuronal remodeling: a role for the RNA-binding protein Boule as a negative regulator of axon pruning. J Neurosci 28: 6092–6103. doi: 10.1523/JNEUROSCI.0677-08.2008 18550751

41. Bitan A, Guild GM, Bar-Dubin D, Abdu U (2010) Asymmetric microtubule function is an essential requirement for polarized organization of the Drosophila bristle. Mol Cell Biol 30: 496–507. doi: 10.1128/MCB.00861-09 19917727

42. Otani T, Oshima K, Kimpara A, Takeda M, Abdu U, Hayashi S (2015) A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation. Development 142:2338–2351. doi: 10.1242/dev.121863 26092846

43. Amsalem S, Bakrhat A, Otani T, Hayashi S, Goldstein B, et al. (2013) Drosophila oocyte polarity and cytoskeleton organization require regulation of Ik2 activity by Spn-F and Javelin-like. Mol Cell Biol 33: 4371–4380. doi: 10.1128/MCB.00713-13 24019068

44. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457: 981–989. doi: 10.1038/nature07767 19225519

45. Simon DJ, Weimer RM, McLaughlin T, Kallop D, Stanger K, et al. (2012) A caspase cascade regulating developmental axon degeneration. J Neurosci 32: 17540–17553. doi: 10.1523/JNEUROSCI.3012-12.2012 23223278

46. Graham RK, Ehrnhoefer DE, Hayden MR (2011) Caspase-6 and neurodegeneration. Trends Neurosci 34: 646–656. doi: 10.1016/j.tins.2011.09.001 22018804

47. Grueber WB, Ye B, Moore AW, Jan LY, Jan YN (2003) Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr Biol 13: 618–626. 12699617