Cellular mechanisms of dendrite pruning in Drosophila: Insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons

Development

Volumn 132, Issue 16, 2005, Pages 3631-3642

  Williams, Darren W ^a,b   Truman, James W ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

EcR; Local degeneration; Metamorphosis; Pruning

Indexed keywords

STEROID;

ANIMAL CELL; ARTICLE; BLOOD CELL; CYTOSKELETON; DENDRITE; DROSOPHILA; EPIDERMIS; FEMALE; HORMONAL REGULATION; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; LARVAL STAGE; METAMORPHOSIS; MICROTUBULE; NERVE CELL DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHAGOCYTOSIS; PHOTON; PRIORITY JOURNAL; SENSORY NERVE CELL;

ABDOMEN; ANIMALS; CYTOSKELETON; DENDRITES; DROSOPHILA MELANOGASTER; FLUORESCENT DYES; METAMORPHOSIS, BIOLOGICAL; MICROSCOPY, VIDEO; NEURONS, AFFERENT; PHAGOCYTES; RECEPTORS, STEROID;

ANIMALIA;

EID: 24044489758     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01928     Document Type: Article

References (49)

1. Ainsley, J. A., Pettus, J. M., Bosenko, D., Gerstein, C. E., Zinkevich, N., Anderson, M. G., Adams, C. M., Welsh, M. J. and Johnson, W. A. (2003). Enhanced locomotion caused by loss of the Drosophila DEG/ENaC protein Pickpocket1. Curr. Biol. 13, 1557-1563.
2. Awasaki, T. and Ito, K. (2004). Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr. Biol. 14, 668-677.
3. Bagri, A., Cheng, H. J., Yaron, A., Pleasure, S. J. and Tessier-Lavigne, M. (2003). Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113, 285-299.
4. Beirowski, B., Adalbert, R., Wagner, D., Grumme, D. S., Addicks, K., Ribchester, R. R. and Coleman, M. P. (2005). The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci. 6, 6.
5. Bishop, D. L., Misgeld, T., Walsh, M. K., Gan, W. B. and Lichtman, J. W. (2004). Axon branch removal at developing synapses by axosome shedding. Neuron 44, 651-661.
6. Burek, M. J. and Oppenheim, R. W. (1996). Programmed cell death in the developing nervous system. Brain Pathol. 6, 427-446.
7. Bray, D., Thomas, C. and Shaw, G. (1978). Growth cone formation in cultures of sensory neurons. Proc. Natl. Acad. Sci. USA 75, 5226-5229.
8. Cherbas, L., Hu, X., Zhimulev, I., Belyaeva, E. and Cherbas, P. (2003). EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130, 271-284.
9. Clarkson, M. and Saint, R. (1999). A His2AvDGFP fusion gene complements a lethal His2AvD mutant allele and provides an in vivo marker for Drosophila chromosome behavior. DNA Cell Biol. 18, 457-462.
10. Cowan, W. M., Fawcett, J. W., O'Leary, D. D. and Stanfield, B. B. (1984). Regressive events in neurogenesis. Science 225, 1258-1265.
11. Fristrom, D. and Fristrom, J. W. (1993). The metamorphic development of the adult epidermis. In The Development of Drosophila melanogaster. Vol II (ed. M. Bate and A. Martinez), pp. 843-897. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
12. Grieder, N. C., de Cuevas, M., Spradling, A. C. (2000). The fusome organizes the microtubule network during oocyte differentiation in Drosophila. Development 127, 4253-4264.
13. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2002). Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867-2878.
14. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2003). Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112, 805-818.
15. Hartenstein, V. and Posakony, J. W. (1989). Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107, 389-405.
16. He, Y., Yu, W., Baas, P. W. (2002). Microtubule reconfiguration during axonal retraction induced by nitric oxide. J. Neurosci. 22, 5982-5991.
17. Hirata, K. and Kawabuchi, M. (2002). Myelin phagocytosis by macrophages and nonmacrophages during Wallerian degeneration. Microsc. Res. Tech. 57, 541-547.
18. Hummel, T., Krukkert, K., Roos, J., Davis, G. and Klambt, C. (2000). Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26, 357-370.
19. Keller-Peck, C. R., Walsh, M. K., Gan, W. B., Feng, G., Sanes, J. R. and Lichtman, J. W. (2001). Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 31, 381-394.
20. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
21. Lee, T., Marticke, S., Sung, C., Robinow, S. and Luo, L. (2000). Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28, 807-818.
22. Levine, R. B. and Weeks, J. C. (1996). Cell culture approaches to understanding the actions of steroid hormones on the insect nervous system. Dev. Neurosci. 18, 73-86.
23. Luo, L. and O'Leary, D. M. (2005). Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28, 127-156.
24. Madhavan, M. M. and Madhavan, K. (1980). Morphogenesis of the epidermis of adult abdomen of Drosophila. J. Embryol. Exp. Morphol. 60, 1-31.
25. Mallat, M., Marin-Teva, J. L. and Cheret, C. (2005). Phagocytosis in the developing CNS: more than clearing the corpses. Curr. Opin. Neurobiol. 15, 101-107.
26. Marin, E. C., Watts, R. J., Tanaka, N. K., Ito, K. and Luo, L. (2005). Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132, 725-737.
27. Mergliano, J. and Minden, J. S. (2003). Caspase-independent cell engulfment mirrors cell death pattern in Drosophila embryos. Development 130, 5779-5789.
28. Nakamura, H. and O'Leary, D. D. (1989). Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodeling to develop topographic order. J. Neurosci. 9, 3776-3795.
29. O'Leary, D. D. and Koester, S. E. (1993). Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 10, 991-1006.
30. Perry, V. H., Henderson, Z. and Linden, R. (1983). Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat. J. Comp. Neurol. 219, 356-368.
31. Reddien, P. W., Cameron, S. and Horvitz, H. R. (2001). Phagocytosis promotes programmed cell death in C. elegans. Nature 412, 198-202.
32. Reyes, R., Haendel, M., Grant, D., Melancon, E. and Eisen, J. S. (2004). Slow degeneration of zebrafish Rohon-Beard neurons during programmed cell death. Dev. Dyn. 229, 30-41.
33. Savill, J. and Fadok, V. (2000). Corpse clearance defines the meaning of cell death. Nature 407, 784-788.
34. Schubiger, M., Wade, A. A., Carney, G. E., Truman, J. W. and Bender, M. (1998). Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125, 2053-2062.
35. Schubiger, M., Tomita, S., Sung, C., Robinow, S. and Truman, J. W. (2003). Isoform specific control of gene activity in vivo by the Drosophila ecdysone receptor. Mech. Dev. 120, 909-918.
36. Sievers, C., Platt, N., Perry, V. H., Coleman, M. P. and Conforti, L. (2003). Neurites undergoing Wallerian degeneration show an apoptotic-like process with Annexin V positive staining and loss of mitochondrial membrane potential. Neurosci. Res. 46, 161-169.
37. Smith, S. A. and Shepherd, D. (1996). Central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique. J. Comp. Neurol. 364, 311-323.
38. Taylor, B. J. (1989). Sexually dimorphic neurons in the terminalia of Drosophila melanogaster: I. Development of sensory neurons in the genital disc during metamorphosis. J. Neurogenet. 5, 173-192.
39. Truman, J. W. (1996). Steroid receptors and nervous system metamorphosis in insects. Dev. Neurosci. 18, 87-101.
40. Truman, J. W., Schuppe, H., Shepherd, D., Williams, D. W. (2004). Developmental architecture of adult-specific lineages in the ventral CNS of Drosophila. Development 131, 5167-5184.
41. Usui-Ishihara, A., Simpson, P. and Usui, K. (2000). Larval multidendrite neurons survive metamorphosis and participate in the formation of imaginal sensory axonal pathways in the notum of Drosophila. Dev. Biol. 225, 357-369.
42. Waller, A. (1850). Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of primitive fibres. Philos. Trans. R. Soc. London Ser. B 140, 423-429.
43. Watts, R. J., Hoopfer, E. D. and Luo, L. (2003). Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38, 871-885.
44. Watts, R. J., Schuldiner, O., Perrino, J., Larsen, C. and Luo, L. (2004). Glia engulf degenerating axons during developmental axon pruning. Curr. Biol. 14, 678-684.
45. Williams, D. W. and Shepherd, D. (1999). Persistent larval sensory neurons in adult Drosophila melanogaster. J. Neurobiol. 39, 275-286.
46. Williams, D. W. and Shepherd, D. (2002). Persistent larval sensory neurones are required for the normal development of the adult sensory afferent projections in Drosophila. Development 129, 617-624.
47. Williams, D. W. and Truman, J. W. (2004). Mechanisms of dendritic elaboration of sensory neurons in Drosophila: insights from in vivo time lapse. J. Neurosci. 24, 1541-1550.
48. Zhai, Q., Wang, J., Kim, A., Liu, Q., Watts, R., Hoopfer, E., Mitchison, T., Luo, L. and He, Z. (2003). Involvement of the ubiquitin-proteasome system in the early stages of wallerian degeneration. Neuron 39, 217-225.
49. Zheng, X., Wang, J., Haerry, T. E., Wu, A. Y., Martin, J., O'Connor, M. B., Lee, C. H. and Lee, T. (2003). TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 112, 303-315.