Rab11 activation by Ik2 kinase is required for dendrite pruning in Drosophila sensory neurons
Autoři:
Tzu Lin aff001; Hao-Hsiang Kao aff001; Che-Hsuan Chou aff001; Chih-Yu Chou aff001; Yu-Ching Liao aff001; Hsiu-Hsiang Lee aff001
Působiště autorů:
Institute of Molecular Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan
aff001
Vyšlo v časopise:
Rab11 activation by Ik2 kinase is required for dendrite pruning in Drosophila sensory neurons. PLoS Genet 16(2): e1008626. doi:10.1371/journal.pgen.1008626
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008626
Souhrn
Neuronal pruning is a commonly observed phenomenon for the developing nervous systems to ensure precise wiring of neural circuits. The function of Ik2 kinase and its downstream mediator, Spindle-F (Spn-F), are essential for dendrite pruning of Drosophila sensory neurons during development. However, little is known about how Ik2/Spn-F signaling is transduced in neurons and ultimately results in dendrite pruning. Our genetic analyses and rescue experiments demonstrated that the small GTPase Rab11, especially the active GTP-bound form, is required for dendrite pruning. We also found that Rab11 shows genetic interactions with spn-F and ik2 on pruning. Live imaging of single neurons and antibody staining reveal normal Ik2 kinase activation in Rab11 mutant neurons, suggesting that Rab11 could have a functional connection downstream of and/or parallel to the Ik2 kinase signaling. Moreover, we provide biochemical evidence that both the Ik2 kinase activity and the formation of Ik2/Spn-F/Rab11 complexes are central to promote Rab11 activation in cells. Together, our studies reveal that a critical role of Ik2/Spn-F signaling in neuronal pruning is to promote Rab11 activation, which is crucial for dendrite pruning in neurons.
Klíčová slova:
Cloning – Drosophila melanogaster – Neuronal dendrites – Neuronal morphology – Neurons – Protein interactions – RNA interference – Guanosine triphosphatase
Zdroje
1. Luo L, O'Leary DD. Axon retraction and degeneration in development and disease. Annu Rev Neurosci. 2005;28:127–156. doi: 10.1146/annurev.neuro.28.061604.135632 16022592
2. Riccomagno MM1, Kolodkin AL. Sculpting neural circuits by axon and dendrite pruning. Annu Rev Cell Dev Biol. 2015;31:779–805. doi: 10.1146/annurev-cellbio-100913-013038 26436703
3. Hayashi Y, Hirotsu T, Iwata R, Kage-Nakadai E, Kunitomo H, Ishihara T, et al. A trophic role for Wnt-Ror kinase signaling during developmental pruning in Caenorhabditis elegans. Nat Neurosci. 2009;12(8):981–987. doi: 10.1038/nn.2347 19561603
4. Mayseless O, Berns DS, Yu XM, Riemensperger T, Fiala A, Schuldiner O. Developmental coordination during olfactory circuit remodeling in Drosophila. Neuron. 2018;99(6):1–12.
5. Redt-Clouet C, Trannoy S, Boulanger A, Tokmatcheva E, Savvateeva-Popova E, Parmentier ML, et al. Mushroom body neuronal remodelling is necessary for short-term but not for long-term courtship memory in Drosophila. Eur J Neurosci. 2012;35(11):1684–1691. doi: 10.1111/j.1460-9568.2012.08103.x 22571719
6. 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(18):4065–4076. 10457015
7. Williams DW, Truman JW. Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons. Development. 2005;132(16):3631–3642. doi: 10.1242/dev.01928 16033801
8. Kuo CT, Jan LY, Jan YN. Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc Natl Acad Sci U S A. 2005;102(42):15230–15235. doi: 10.1073/pnas.0507393102 16210248
9. Yu F, Schuldiner O. Axon and dendrite pruning in Drosophila. Curr Opin Neurobiol. 2014;27:192–198. doi: 10.1016/j.conb.2014.04.005 24793180
10. Kanamori T, Togashi K, Koizumi H, Emoto K. Dendritic remodeling: lessons from invertebrate model systems. Int Rev Cell Mol Biol. 2015;318:1–25. doi: 10.1016/bs.ircmb.2015.05.001 26315882
11. Lee HH, Jan LY, Jan YN. 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. 2009;106(15):6363–6368. doi: 10.1073/pnas.0902051106 19329489
12. Han C, Song Y, Xiao H, Wang D, Franc NC, Jan LY, et al. Epidermal cells are the primary phagocytes in the fragmentation and clearance of degenerating dendrites in Drosophila. Neuron. 2014;81(3):544–560. doi: 10.1016/j.neuron.2013.11.021 24412417
13. Kirilly D, Gu Y, Huang Y, Wu Z, Bashirullah A, Low BC, et al. A genetic pathway composed of Sox14 and Mical governs severing of dendrites during pruning. Nat Neurosci. 2009;12(12):1497–1505. doi: 10.1038/nn.2415 19881505
14. Wong JJ, Li S, Lim EK, Wang Y, Wang C, Zhang H, et al. A cullin1-based SCF E3 ubiquitin ligase targets the InR/PI3K/TOR pathway to regulate neuronal pruning. PLoS Biol. 2013;11(9):e1001657. doi: 10.1371/journal.pbio.1001657 24068890
15. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW. Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci. 2006;9(10):1234–1236. doi: 10.1038/nn1774 16980964
16. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN. Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron. 2006;51(3):283–290. doi: 10.1016/j.neuron.2006.07.014 16880123
17. Herzmann S, Krumkamp R, Rode S, Kintrup C, Rumpf S. PAR-1 promotes microtubule breakdown during dendrite pruning in Drosophila. EMBO J. 2017;36(13):1981–1991. doi: 10.15252/embj.201695890 28554895
18. Wang Y, Rui M, Tang Q, Bu S, Yu F. Patronin governs minus-end-out orientation of dendritic microtubules to promote dendrite pruning in Drosophila. Elife. 2019;8:e39964. doi: 10.7554/eLife.39964 30920370
19. Kanamori T, Kanai MI, Dairyo Y, Yasunaga K, Morikawa RK, Emoto K. Compartmentalized calcium transients trigger dendrite pruning in Drosophila sensory neurons. Science. 2013;340(6139):1475–1478. doi: 10.1126/science.1234879 23722427
20. Issman-Zecharya N, Schuldiner O. The PI3K class III complex promotes axon pruning by downregulating a Ptc-derived signal via endosome-lysosomal degradation. Dev Cell. 2014;31(4):461–473. doi: 10.1016/j.devcel.2014.10.013 25458013
21. Zhang H, Wang Y, Wong JJL, Lim KL, Liou YC, Wang H, et al. Endocytic pathways downregulate the L1-type cell adhesion molecule Neuroglian to promote dendrite pruning in Drosophila. Dev Cell. 2014;30(4):463–478. doi: 10.1016/j.devcel.2014.06.014 25158855
22. Kanamori T, Yoshino J, Yasunaga K, Dairyo Y, Emoto K. Local endocytosis triggers dendritic thinning and pruning in Drosophila sensory neurons. Nat Commun. 2015;6:6515. doi: 10.1038/ncomms7515 25761586
23. Welz T, Wellbourne-Wood J, Kerkhoff E. Orchestration of cell surface proteins by Rab11. Trends Cell Biol. 2014;24(7):407–415. doi: 10.1016/j.tcb.2014.02.004 24675420
24. Lin T, Pan PY, Lai YT, Chiang KW, Hsieh HL, Wu YP, et al. Spindle F Is the central mediator of Ik2 kinase-dependent dendrite pruning in Drosophila sensory neurons. PLoS Genet. 2015;11(11):e1005642. doi: 10.1371/journal.pgen.1005642 26540204
25. Kramer R, Rode S, Rumpf S. Rab11 is required for neurite pruning and developmental membrane protein degradation in Drosophila sensory neurons. Dev Biol. 2019;451(1):68–78. doi: 10.1016/j.ydbio.2019.03.003 30871987
26. Bogard N, Lan L, Xu J, Cohen RS. Rab11 maintains connections between germline stem cells and niche cells in the Drosophila ovary. Development. 2007;134(19):3413–3418. doi: 10.1242/dev.008466 17715175
27. Lee T, Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 1999;22(3):451–461. doi: 10.1016/s0896-6273(00)80701-1 10197526
28. Zhang J, Schulze KL, Hiesinger PR, Suyama K, Wang S, Fish M, et al. Thirty-one flavors of Drosophila Rab proteins. Genetics. 2007;176(2):1307–1322. doi: 10.1534/genetics.106.066761 17409086
29. Roman G, Davis RL. Conditional expression of UAS-transgenes in the adult eye with a new gene-switch vector system. Genesis. 2002;34(1–2):127–131. doi: 10.1002/gene.10133 12324966
30. Abdu U, Bar D, Schupbach T. spn-F encodes a novel protein that affects oocyte patterning and bristle morphology in Drosophila. Development. 2006;133(8):1477–1488. doi: 10.1242/dev.02319 16540510
31. Kuranaga E, Kanuka H, Tonoki A, Takemoto K, Tomioka T, Kobayashi M, et al. Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell. 2006;126(3):583–596. doi: 10.1016/j.cell.2006.05.048 16887178
32. Otani T, Oshima K, Onishi S, Takeda M, Shinmyozu K, Yonemura S, et al. IKKε regulates cell elongation through recycling endosome shuttling. Dev Cell. 2011;20(2):219–232. doi: 10.1016/j.devcel.2011.02.001 21316589
33. Parkinson K, Baines AE, Keller T, Gruenheit N, Bragg L, North RA, et al. Calcium-dependent regulation of Rab activation and vesicle fusion by an intracellular P2X ion channel. Nat Cell Biol. 2014;16(1):87–98. doi: 10.1038/ncb2887 24335649
34. Raff MC, Whitmore AV, Finn JT. Axonal self-destruction and neurodegeneration. Science. 2002;296(5569):868–871. doi: 10.1126/science.1068613 11988563
35. Shirane M, Nakayama KI. Protrudin induces neurite formation by directional membrane trafficking. Science. 2006;314(5800):818–821. doi: 10.1126/science.1134027 17082457
36. Barr F, Lambright DG. Rab GEFs and GAPs. Curr Opin Cell Biol. 2010;22(4):461–470. doi: 10.1016/j.ceb.2010.04.007 20466531
37. Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev. 2011;91(1):119–149. doi: 10.1152/physrev.00059.2009 21248164
38. Wandinger-Ness A, Zerial M. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol. 2014;6(11):a022616. doi: 10.1101/cshperspect.a022616 25341920
39. Umaer K, Bush PJ, Bangs JD. Rab11 mediates selective recycling and endocytic trafficking in Trypanosoma brucei. Traffic. 2018;19(6):406–420. doi: 10.1111/tra.12565 29582527
40. De Antoni A, Schmitzova J, Trepte HH, Gallwitz D, Albert S. Significance of GTP hydrolysis in Ypt1p-regulated endoplasmic reticulum to Golgi transport revealed by the analysis of two novel Ypt1-GAPs. J Biol Chem. 2002;277(43):41023–41031. doi: 10.1074/jbc.M205783200 12189143
41. Pan X, Eathiraj S, Munson M, Lambright DG. TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism. Nature. 2006;442(7100):303–306. doi: 10.1038/nature04847 16855591
42. Langemeyer L, Bastos RN, Cai Y, Itzen A, Reinisch KM, Barr FA. Diversity and plasticity in Rab GTPase nucleotide release mechanism has consequences for Rab activation and inactivation. Elife. 2014;3:e01623. doi: 10.7554/eLife.01623 24520163
43. Otani T, Oshima K, Kimpara A, Takeda M, Abdu U, Hayashi S. A transport and retention mechanism for the sustained distal localization of Spn-F–IKKε during Drosophila bristle elongation. Development. 2015;142(13):2338–2351. doi: 10.1242/dev.121863 26092846
44. Dubin-Bar D, Bitan A, Bakhrat A, Kaiden-Hasson R, Etzion S, Shaanan B, et al. The Drosophila IKK-related kinase (Ik2) and Spindle-F proteins are part of a complex that regulates cytoskeleton organization during oogenesis. BMC Cell Biol. 2008;9:51. doi: 10.1186/1471-2121-9-51 18796167
45. Bitan A, Guild GM, Bar-Dubin D, Abdu U. Asymmetric microtubule function is an essential requirement for polarized organization of the Drosophila bristle. Mol Cell Biol. 2010;30(2):496–507. doi: 10.1128/MCB.00861-09 19917727
46. Amsalem S, Bakrhat A, Otani T, Hayashi S, Goldstein B, Abdu U. Drosophila oocyte polarity and cytoskeleton organization require regulation of Ik2 activity by Spn-F and Javelin-like. Mol Cell Biol. 2013;33(22):4371–4380. doi: 10.1128/MCB.00713-13 24019068
47. Grueber WB, Ye B, Moore AW, Jan LY, Jan YN. Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr Biol. 2003;13(8):618–626. doi: 10.1016/s0960-9822(03)00207-0 12699617
48. Grueber WB, Ye B, Yang CH, Younger S, Borden K, Jan LY, et al. Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development. 2007;134(1):55–64. doi: 10.1242/dev.02666 17164414
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