Local caspase activation interacts with Slit-Robo signaling to restrict axonal arborization

Journal of Cell Biology

Volumn 203, Issue 4, 2013, Pages 657-672

  Campbell, Douglas S ^a,b   Okamoto, Hitoshi ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; MEMBRANE PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; ROUNDABOUT RECEPTOR; SLIT1A PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC ANALYSIS; IN SITU HYBRIDIZATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RETINA GANGLION CELL; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION; SYNAPTOGENESIS; TIME LAPSE IMAGING; WILD TYPE; ZEBRA FISH;

EID: 84890173854     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201303072     Document Type: Article

References (78)

1. Alsina, B., T. Vu, and S. Cohen-Cory. 2001. Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat. Neurosci. 4:1093-1101. http://dx.doi.org/10.1038/nn735
2. Barresi, M.J., L.D. Hutson, C.B. Chien, and R.O. Karlstrom. 2005. Hedgehog regulated Slit expression determines commissure and glial cell position in the zebrafish forebrain. Development. 132:3643-3656. http://dx.doi.org/10.1242/dev.01929
3. Bashaw, G.J., and R. Klein. 2010. Signaling from axon guidance receptors. Cold Spring Harb. Perspect. Biol. 2:a001941. http://dx.doi.org/10.1101/cshperspect. a001941
4. Biehlmaier, O., S.C. Neuhauss, and K. Kohler. 2001. Onset and time course of apoptosis in the developing zebrafish retina. Cell Tissue Res. 306:199-207. http://dx.doi.org/10.1007/s004410100447
5. Bingol, B., and M. Sheng. 2011. Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron. 69:22-32. http://dx.doi.org/10.1016/j.neuron.2010.11.006
6. Cajigas, I.J., T. Will, and E.M. Schuman. 2010. Protein homeostasis and synaptic plasticity. EMBO J. 29:2746-2752. http://dx.doi.org/10.1038/emboj.2010.173
7. Campbell, D.S., and C.E. Holt. 2001. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron. 32:1013-1026. http://dx.doi.org/10.1016/S0896-6273(01)00551-7
8. Campbell, D.S., and C.E. Holt. 2003. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron. 37:939-952. http://dx.doi.org/10.1016/S0896-6273(03)00158-2
9. Campbell, D.S., A.G. Regan, J.S. Lopez, D. Tannahill, W.A. Harris, and C.E. Holt. 2001. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21:8538-8547.
10. Campbell, D.S., S.A. Stringham, A. Timm, T. Xiao, M.Y. Law, H. Baier, M.L. Nonet, and C.B. Chien. 2007. Slit1a inhibits retinal ganglion cell arborization and synaptogenesis via Robo2-dependent and-independent pathways. Neuron. 55:231-245. http://dx.doi.org/10.1016/j.neuron.2007.06.034
11. Carson, C., M. Saleh, F.W. Fung, D.W. Nicholson, and A.J. Roskams. 2005. Axonal dynactin p150Glued transports caspase-8 to drive retrograde olfactory receptor neuron apoptosis. J. Neurosci. 25:6092-6104. http://dx.doi.org/10.1523/JNEUROSCI.0707-05.2005
12. Cohen-Cory, S. 2007. Imaging retinotectal synaptic connectivity. CSH Protoc. 2007:pdb.prot4782. http://dx.doi.org/10.1101/pdb.prot4782
13. Cohen-Cory, S., and S.E. Fraser. 1995. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature. 378:192-196. http://dx.doi.org/10.1038/378192a0
14. Crawford, E.D., and J.A. Wells. 2011. Caspase substrates and cellular remodeling. Annu. Rev. Biochem. 80:1055-1087. http://dx.doi.org/10.1146/annurev-biochem-061809-121639
15. Creagh, E.M., and S.J. Martin. 2001. Caspases: cellular demolition experts. Biochem. Soc. Trans. 29:696-702. http://dx.doi.org/10.1042/BST0290696
16. D'Amelio, M., V. Cavallucci, S. Middei, C. Marchetti, S. Pacioni, A. Ferri, A. Diamantini, D. De Zio, P. Carrara, L. Battistini, et al. 2011. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat. Neurosci. 14:69-76. http://dx.doi.org/10.1038/nn.2709
17. D'Amelio, M., M. Sheng, and F. Cecconi. 2012. Caspase-3 in the central nervous system: beyond apoptosis. Trends Neurosci. 35:700-709. http://dx.doi.org/10.1016/j.tins.2012.06.004
18. Dingwell, K.S., C.E. Holt, and W.A. Harris. 2000. The multiple decisions made by growth cones of RGCs as they navigate from the retina to the tectum in Xenopus embryos. J. Neurobiol. 44:246-259. http://dx.doi.org/10.1002/1097-4695(200008)44:2<246::AID-NEU13>3.0.CO;2-K
19. Eimon, P.M., E. Kratz, E. Varfolomeev, S.G. Hymowitz, H. Stern, J. Zha, and A. Ashkenazi. 2006. Delineation of the cell-extrinsic apoptosis pathway in the zebrafish. Cell Death Differ. 13:1619-1630. http://dx.doi.org/10.1038/sj.cdd.4402015
20. Fischer, U., R.U. Jänicke, and K. Schulze-Osthoff. 2003. Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ. 10:76-100. http://dx.doi.org/10.1038/sj.cdd.4401160
21. Gallo, G. 2011. The cytoskeletal and signaling mechanisms of axon collateral branching. Dev. Neurobiol. 71:201-220. http://dx.doi.org/10.1002/dneu.20852
22. Gibson, D.A., and L. Ma. 2011. Developmental regulation of axon branching in the vertebrate nervous system. Development. 138:183-195. http://dx.doi.org/10.1242/dev.046441
23. Harris, W.A., C.E. Holt, and F. Bonhoeffer. 1987. Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. Development. 101:123-133.
24. Hsu, R.J., C.C. Lin, Y.F. Su, and H.J. Tsai. 2011. dickkopf-3-related gene regulates the expression of zebrafish myf5 gene through phosphorylated p38adependent Smad4 activity. J. Biol. Chem. 286:6855-6864. http://dx.doi.org/10.1074/jbc.M110.161638
25. Huesmann, G.R., and D.F. Clayton. 2006. Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song-response habituation. Neuron. 52:1061-1072. http://dx.doi.org/10.1016/j.neuron.2006.10.033
26. Hutson, L.D., D.S. Campbell, and C.B. Chien. 2004. Analyzing axon guidance in the zebrafish retinotectal system. Methods Cell Biol. 76:13-35. http://dx.doi.org/10.1016/S0091-679X(04)76002-1
27. Hyman, B.T., and J. Yuan. 2012. Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat. Rev. Neurosci. 13:395-406. http://dx.doi.org/10.1038/nrn3228
28. Jiao, S., and Z. Li. 2011. Nonapoptotic function of BAD and BAX in long-term depression of synaptic transmission. Neuron. 70:758-772. http://dx.doi.org/10.1016/j.neuron.2011.04.004
29. Jin, Y., and C.C. Garner. 2008. Molecular mechanisms of presynaptic differentiation. Annu. Rev. Cell Dev. Biol. 24:237-262. http://dx.doi.org/10.1146/annurev.cellbio.23.090506.123417
30. Jung, H., C.M. O'Hare, and C.E. Holt. 2011. Translational regulation in growth cones. Curr. Opin. Genet. Dev. 21:458-464. http://dx.doi.org/10.1016/j.gde.2011.04.004
31. Kimmel, C.B., W.W. Ballard, S.R. Kimmel, B. Ullmann, and T.F. Schilling. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:253-310. http://dx.doi.org/10.1002/aja.1002030302
32. Kothakota, S., T. Azuma, C. Reinhard, A. Klippel, J. Tang, K. Chu, T.J. McGarry, M.W. Kirschner, K. Koths, D.J. Kwiatkowski, and L.T. Williams. 1997. Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science. 278:294-298. http://dx.doi.org/10.1126/science.278.5336.294
33. Krens, S.F., S. He, H.P. Spaink, and B.E. Snaar-Jagalska. 2006. Characterization and expression patterns of the MAPK family in zebrafish. Gene Expr. Patterns. 6:1019-1026. http://dx.doi.org/10.1016/j.modgep.2006.04.008
34. Kulkarni, R.P., M. Bak-Maier, and S.E. Fraser. 2007. Differences in protein mobility between pioneer versus follower growth cones. Proc. Natl. Acad. Sci. USA. 104:1207-1212. http://dx.doi.org/10.1073/pnas.0610142104
35. Kuo, C.T., S. Zhu, S. Younger, L.Y. Jan, and Y.N. Jan. 2006. Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron. 51:283-290. http://dx.doi.org/10.1016/j.neuron.2006.07.014
36. Kuranaga, E., and M. Miura. 2007. Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol. 17:135-144. http://dx.doi.org/10.1016/j.tcb.2007.01.001
37. Kuranaga, E., H. Kanuka, A. Tonoki, K. Takemoto, T. Tomioka, M. Kobayashi, S. Hayashi, and M. Miura. 2006. Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell. 126:583-596. http://dx.doi.org/10.1016/j.cell.2006.05.048
38. Lee, J.S., R. Ray, and C.B. Chien. 2001. Cloning and expression of three zebrafish roundabout homologs suggest roles in axon guidance and cell migration. Dev. Dyn. 221:216-230. http://dx.doi.org/10.1002/dvdy.1136
39. Leu, B.H., and J.T. Schmidt. 2008. Arachidonic acid as a retrograde signal controlling growth and dynamics of retinotectal arbors. Dev. Neurobiol. 68:18-30. http://dx.doi.org/10.1002/dneu.20561
40. Li, Z., J. Jo, J.M. Jia, S.C. Lo, D.J. Whitcomb, S. Jiao, K. Cho, and M. Sheng. 2010. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell. 141:859-871. http://dx.doi.org/10.1016/j.cell.2010.03.053
41. Lin, Y.C., and A.J. Koleske. 2010. Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu. Rev. Neurosci. 33:349-378. http://dx.doi.org/10.1146/annurevneuro-060909-153204
42. Lu, M., W. Witke, D.J. Kwiatkowski, and K.S. Kosik. 1997. Delayed retraction of filopodia in gelsolin null mice. J. Cell Biol. 138:1279-1287. http://dx.doi.org/10.1083/jcb.138.6.1279
43. Manitt, C., A.M. Nikolakopoulou, D.R. Almario, S.A. Nguyen, and S. Cohen-Cory. 2009. Netrin participates in the development of retinotectal synaptic connectivity by modulating axon arborization and synapse formation in the developing brain. J. Neurosci. 29:11065-11077. http://dx.doi.org/10.1523/JNEUROSCI.0947-09.2009
44. Meyer, M.P., and S.J. Smith. 2006. Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J. Neurosci. 26:3604-3614. http://dx.doi.org/10.1523/JNEUROSCI.0223-06.2006
45. Ming, G.L., S.T. Wong, J. Henley, X.B. Yuan, H.J. Song, N.C. Spitzer, and M.M. Poo. 2002. Adaptation in the chemotactic guidance of nerve growth cones. Nature. 417:411-418. http://dx.doi.org/10.1038/nature745
46. Ndozangue-Touriguine, O., J. Hamelin, and J. Bréard. 2008. Cytoskeleton and apoptosis. Biochem. Pharmacol. 76:11-18. http://dx.doi.org/10.1016/j.bcp.2008.03.016
47. Nikolaev, A., T. McLaughlin, D.D. O'Leary, and M. Tessier-Lavigne. 2009. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature. 457:981-989. http://dx.doi.org/10.1038/nature07767
48. O'Donnell, M., R.K. Chance, and G.J. Bashaw. 2009. Axon growth and guidance: receptor regulation and signal transduction. Annu. Rev. Neurosci. 32:383-412. http://dx.doi.org/10.1146/annurev.neuro.051508.135614
49. Ohsawa, S., S. Hamada, K. Kuida, H. Yoshida, T. Igaki, and M. Miura. 2010. Maturation of the olfactory sensory neurons by Apaf-1/caspase-9-mediated caspase activity. Proc. Natl. Acad. Sci. USA. 107:13366-13371. http://dx.doi.org/10.1073/pnas.0910488107
50. Oshima, K., M. Takeda, E. Kuranaga, R. Ueda, T. Aigaki, M. Miura, and S. Hayashi. 2006. IKK epsilon regulates F actin assembly and interacts with Drosophila IAP1 in cellular morphogenesis. Curr. Biol. 16:1531-1537. http://dx.doi.org/10.1016/j.cub.2006.06.032
51. Pittman, A.J., M.Y. Law, and C.B. Chien. 2008. Pathfinding in a large vertebrate axon tract: isotypic interactions guide retinotectal axons at multiple choice points. Development. 135:2865-2871. http://dx.doi.org/10.1242/dev.025049
52. Poulain, F.E., J.A. Gaynes, C. Stacher Hörndli, M.Y. Law, and C.B. Chien. 2010. Analyzing retinal axon guidance in zebrafish. Methods Cell Biol. 100:3-26.
53. Putt, K.S., G.W. Chen, J.M. Pearson, J.S. Sandhorst, M.S. Hoagland, J.T. Kwon, S.K. Hwang, H. Jin, M.I. Churchwell, M.H. Cho, et al. 2006. Smallmolecule activation of procaspase-3 to caspase-3 as a personalized anticancer strategy. Nat. Chem. Biol. 2:543-550. http://dx.doi.org/10.1038/nchembio814
54. Ruthazer, E.S., J. Li, and H.T. Cline. 2006. Stabilization of axon branch dynamics by synaptic maturation. J. Neurosci. 26:3594-3603. http://dx.doi.org/10.1523/JNEUROSCI.0069-06.2006
55. Sato, T., T. Hamaoka, H. Aizawa, T. Hosoya, and H. Okamoto. 2007. Genetic single-cell mosaic analysis implicates ephrinB2 reverse signaling in projections from the posterior tectum to the hindbrain in zebrafish. J. Neurosci. 27:5271-5279. http://dx.doi.org/10.1523/JNEUROSCI.0883-07.2007
56. Saxena, S., and P. Caroni. 2007. Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 83:174-191. http://dx.doi.org/10.1016/j.pneurobio.2007.07.007
57. Schoenmann, Z., E. Assa-Kunik, S. Tiomny, A. Minis, L. Haklai-Topper, E. Arama, and A. Yaron. 2010. Axonal degeneration is regulated by the apoptotic machinery or a NAD+-sensitive pathway in insects and mammals. J. Neurosci. 30:6375-6386. http://dx.doi.org/10.1523/JNEUROSCI.0922-10.2010
58. Schulte-Merker, S., R.K. Ho, B.G. Herrmann, and C. Nüsslein-Volhard. 1992. The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development. 116:1021-1032.
59. Shirvan, A., I. Ziv, G. Fleminger, R. Shina, Z. He, I. Brudo, E. Melamed, and A. Barzilai. 1999. Semaphorins as mediators of neuronal apoptosis. J. Neurochem. 73:961-971. http://dx.doi.org/10.1046/j.1471-4159.1999.0730961.x
60. Sidi, S., T. Sanda, R.D. Kennedy, A.T. Hagen, C.A. Jette, R. Hoffmans, J. Pascual, S. Imamura, S. Kishi, J.F. Amatruda, et al. 2008. Chk1 suppresses a caspase-2 apoptotic response to DNA damage that bypasses p53, Bcl-2, and caspase-3. Cell. 133:864-877. http://dx.doi.org/10.1016/j.cell.2008.03.037
61. Simon, D.J., R.M. Weimer, T. McLaughlin, D. Kallop, K. Stanger, J. Yang, D.D. O'Leary, R.N. Hannoush, and M. Tessier-Lavigne. 2012. A caspase cascade regulating developmental axon degeneration. J. Neurosci. 32:17540-17553. http://dx.doi.org/10.1523/JNEUROSCI.3012-12.2012
62. Smear, M.C., H.W. Tao, W. Staub, M.B. Orger, N.J. Gosse, Y. Liu, K. Takahashi, M.M. Poo, and H. Baier. 2007. Vesicular glutamate transport at a central synapse limits the acuity of visual perception in zebrafish. Neuron. 53:65-77. http://dx.doi.org/10.1016/j.neuron.2006.12.013
63. Steiner, M.R., F.W. Holtsberg, J.N. Keller, M.P. Mattson, and S.M. Steiner. 2000. Lysophosphatidic acid induction of neuronal apoptosis and necrosis. Ann. NY Acad. Sci. 905:132-141. http://dx.doi.org/10.1111/j.1749-6632.2000.tb06545.x
64. Steward, O., and E.M. Schuman. 2003. Compartmentalized synthesis and degradation of proteins in neurons. Neuron. 40:347-359. http://dx.doi.org/10.1016/S0896-6273(03)00635-4
65. Stuermer, C.A. 1988. Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J. Neurosci. 8:4513-4530.
66. Takemoto, K., T. Nagai, A. Miyawaki, and M. Miura. 2003. Spatio-temporal activation of caspase revealed by indicator that is insensitive to environmental effects. J. Cell Biol. 160:235-243. http://dx.doi.org/10.1083/jcb.200207111
67. Takemoto, K., E. Kuranaga, A. Tonoki, T. Nagai, A. Miyawaki, and M. Miura. 2007. Local initiation of caspase activation in Drosophila salivary gland programmed cell death in vivo. Proc. Natl. Acad. Sci. USA. 104:13367-13372. http://dx.doi.org/10.1073/pnas.0702733104
68. Timmer, J.C., and G.S. Salvesen. 2007. Caspase substrates. Cell Death Differ. 14:66-72. http://dx.doi.org/10.1038/sj.cdd.4402059
69. Ulukaya, E., C. Acilan, and Y. Yilmaz. 2011. Apoptosis: why and how does it occur in biology? Cell Biochem. Funct. 29:468-480. http://dx.doi.org/10.1002/cbf.1774
70. Waites, C.L., A.M. Craig, and C.C. Garner. 2005. Mechanisms of vertebrate synaptogenesis. Annu. Rev. Neurosci. 28:251-274. http://dx.doi.org/10.1146/annurev.neuro.27.070203.144336
71. Williams, D.W., S. Kondo, A. Krzyzanowska, Y. Hiromi, and J.W. Truman. 2006. Local caspase activity directs engulfment of dendrites during pruning. Nat. Neurosci. 9:1234-1236. http://dx.doi.org/10.1038/nn1774
72. Wishart, T.M., S.H. Parson, and T.H. Gillingwater. 2006. Synaptic vulnerability in neurodegenerative disease. J. Neuropathol. Exp. Neurol. 65:733-739. http://dx.doi.org/10.1097/01.jnen.0000228202.35163.c4
73. Wong, M. 2008. Stabilizing dendritic structure as a novel therapeutic approach for epilepsy. Expert Rev. Neurother. 8:907-915. http://dx.doi.org/10.1586/14737175.8.6.907
74. Wyatt, C., A. Ebert, M.M. Reimer, K. Rasband, M. Hardy, C.B. Chien, T. Becker, and C.G. Becker. 2010. Analysis of the astray/robo2 zebrafish mutant reveals that degenerating tracts do not provide strong guidance cues for regenerating optic axons. J. Neurosci. 30:13838-13849. http://dx.doi.org/10.1523/JNEUROSCI.3846-10.2010
75. Xiao, T., W. Staub, E. Robles, N.J. Gosse, G.J. Cole, and H. Baier. 2011. Assembly of lamina-specific neuronal connections by slit bound to type IV collagen. Cell. 146:164-176. http://dx.doi.org/10.1016/j.cell.2011.06.016
76. Yabu, T., S. Kishi, T. Okazaki, and M. Yamashita. 2001. Characterization of zebrafish caspase-3 and induction of apoptosis through ceramide generation in fish fathead minnow tailbud cells and zebrafish embryo. Biochem. J. 360:39-47. http://dx.doi.org/10.1042/0264-6021:3600039
77. Yamashita, M., N. Mizusawa, M. Hojo, and T. Yabu. 2008. Extensive apoptosis and abnormal morphogenesis in pro-caspase-3 transgenic zebrafish during development. J. Exp. Biol. 211:1874-1881. http://dx.doi.org/10.1242/jeb.012690
78. Zinsmaier, K.E., M. Babic, and G.J. Russo. 2009. Mitochondrial transport dynamics in axons and dendrites. Results Probl. Cell Differ. 48:107-139.