Characterisation of a new regulator of BDNF signalling, Sprouty3, involved in axonal morphogenesis in vivo

Development

Volumn 137, Issue 23, 2010, Pages 4005-4015

  Panagiotaki, Niki ^a   Dajas Bailador, Federico ^a   Amaya, Enrique ^a   Papalopulu, Nancy ^a   Dorey, Karel ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

BDNF; Branching; Motoneuron; Sprouty; TrkB; Xenopus

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM; SPROUTY PROTEIN; SPROUTY PROTEIN 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; MORPHOGENESIS; MOTOR NERVE; MOUSE; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SPINAL CORD; SPINAL CORD MOTONEURON; SPINAL CORD NERVE CELL; TRIGEMINAL NERVE; XENOPUS;

ANIMALS; AXONS; BASE SEQUENCE; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM SIGNALING; CEREBRAL CORTEX; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; PHYLOGENY; PSEUDOPODIA; RECEPTOR, TRKB; SIGNAL TRANSDUCTION; SPINAL CORD; TIME FACTORS; XENOPUS; XENOPUS PROTEINS;

EID: 78649848073     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.053173     Document Type: Article

References (75)

1. Acebes, A. and Ferrus, A. (2000). Cellular and molecular features of axon collaterals and dendrites. Trends Neurosci. 23, 557-565.
2. Akbulut, S., Reddi, A. L., Aggarwal, P., Ambardekar, C., Canciani, B., Kim, M. K. H., Hix, L., Vilimas, T., Mason, J., Basson, M. A. et al. (2010). Sprouty proteins inhibit receptor-mediated activation of phosphatidylinositol- specific phospholipase C. Mol. Biol. Cell 21, 3487-3496.
3. Ayada, T., Taniguchi, K., Okamoto, F., Kato, R., Komune, S., Takaesu, G. and Yoshimura, A. (2009). Sprouty4 negatively regulates protein kinase C activation by inhibiting phosphatidylinositol 4,5-biphosphate hydrolysis. Oncogene 28, 1076-1088.
4. Barde, Y. A., Edgar, D. and Thoenen, H. (1982). Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1, 549-553.
5. Basson, M. A., Akbulut, S., Watson-Johnson, J., Simon, R., Carroll, T. J., Shakya, R., Gross, I., Martin, G. R., Lufkin, T., McMahon, A. P. et al. (2005). Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev. Cell 8, 229-239. (Pubitemid 40197739)
6. Basson, M. A., Watson-Johnson, J., Shakya, R., Akbulut, S., Hyink, D., Costantini, F. D., Wilson, P. D., Mason, I. J. and Licht, J. D. (2006). Branching morphogenesis of the ureteric epithelium during kidney development is coordinated by the opposing functions of GDNF and Sprouty1. Dev. Biol. 299, 466-477.
7. Bronchain, O. J., Hartley, K. O. and Amaya, E. (1999). A gene trap approach in Xenopus. Curr. Biol. 9, 1195-1198.
8. Cabrita, M. A. and Christofori, G. (2008). Sprouty proteins, masterminds of receptor tyrosine kinase signaling. Angiogenesis 11, 53-62.
9. Campbell, D. S., Regan, A. G., Lopez, J. S., Tannahill, D., Harris, W. A. and Holt, C. E. (2001). Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21, 8538-8547.
10. Chen, Y., Costa, R. M., Love, N. R., Soto, X., Roth, M., Paredes, R. and Amaya, E. (2009). C/EBPalpha initiates primitive myelopoiesis in pluripotent embryonic cells. Blood 114, 40-48.
11. Cohen-Cory, S. and Fraser, S. E. (1995). Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378, 192-196.
12. Costa, R. M., Soto, X., Chen, Y., Zorn, A. M. and Amaya, E. (2008). spib is required for primitive myeloid development in Xenopus. Blood 112, 2287-2296.
13. Cunningham, M. E. and Greene, L. A. (1998). A function-structure model for NGF-activated TRK. EMBO J. 17, 7282-7293.
14. Dajas-Bailador, F., Jones, E. V. and Whitmarsh, A. J. (2008). The JIP1 scaffold protein regulates axonal development in cortical neurons. Curr. Biol. 18, 221-226.
15. Davenport, R. W. and Kater, S. B. (1992). Local increases in intracellular calcium elicit local filopodial responses in Helisoma neuronal growth cones. Neuron 9, 405-416.
16. Drinjakovic, J., Jung, H., Campbell, D. S., Strochlic, L., Dwivedy, A. and Holt, C. E. (2010). E3 Ligase Nedd4 Promotes Axon Branching by Downregulating PTEN. Neuron 65, 341-357.
17. Edwards, J. A. and Cline, H. T. (1999). Light-induced calcium influx into retinal axons is regulated by presynaptic nicotinic acetylcholine receptor activity in vivo. J. Neurophysiol. 81, 895-907.
18. Ernfors, P., Lee, K. F. and Jaenisch, R. (1994). Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368, 147-150.
19. Feldner, J., Reimer, M. M., Schweitzer, J., Wendik, B., Meyer, D., Becker, T. and Becker, C. G. (2007). PlexinA3 restricts spinal exit points and branching of trunk motor nerves in embryonic zebrafish. J. Neurosci. 27, 4978-4983.
20. Furthauer, M., Reifers, F., Brand, M., Thisse, B. and Thisse, C. (2001). sprouty4 acts in vivo as a feedback-induced antagonist of FGF signaling in zebrafish. Development 128, 2175-2186.
21. Gibney, J. and Zheng, J. Q. (2003). Cytoskeletal dynamics underlying collateral membrane protrusions induced by neurotrophins in cultured Xenopus embryonic neurons. J. Neurobiol. 54, 393-405.
22. Goldberg, J. L. (2004). Intrinsic neuronal regulation of axon and dendrite growth. Curr. Opin. Neurobiol. 14, 551-557.
23. Gomez, T. M., Harrigan, D., Henley, J. and Robles, E. (2003). Working with Xenopus spinal neurons in live cell culture. Methods Cell Biol. 71, 129-156.
24. Gross, I., Armant, O., Benosman, S., de Aguilar, J. L., Freund, J. N., Kedinger, M., Licht, J. D., Gaiddon, C. and Loeffler, J. P. (2007). Sprouty2 inhibits BDNF-induced signaling and modulates neuronal differentiation and survival. Cell Death Differ. 14, 1802-1812.
25. Hacohen, N., Kramer, S., Sutherland, D., Hiromi, Y. and Krasnow, M. A. (1998). sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92, 253-263.
26. Hanafusa, H., Torii, S., Yasunaga, T. and Nishida, E. (2002). Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4, 850-858.
27. Harland, R. M. (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695.
28. Heasman, J., Kofron, M. and Wylie, C. (2000). Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. Dev. Biol. 222, 124-134.
29. Henderson, C. E., Camu, W., Mettling, C., Gouin, A., Poulsen, K., Karihaloo, M., Rullamas, J., Evans, T., McMahon, S. B., Armanini, M. P. et al. (1993). Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363, 266-270.
30. Horowitz, A. and Simons, M. (2008). Branching morphogenesis. Circ. Res. 103, 784-795.
31. Huang, E. J. and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
32. Huang, J. K., Dorey, K., Ishibashi, S. and Amaya, E. (2007). BDNF promotes target innervation of Xenopus mandibular trigeminal axons in vivo. BMC Dev. Biol. 7, 59.
33. Impagnatiello, M. A., Weitzer, S., Gannon, G., Compagni, A., Cotten, M. and Christofori, G. (2001). Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J. Cell Biol. 152, 1087-1098.
34. Ishida, M., Ichihara, M., Mii, S., Jijiwa, M., Asai, N., Enomoto, A., Kato, T., Majima, A., Ping, J., Murakumo, Y. et al. (2007). Sprouty2 regulates growth and differentiation of human neuroblastoma cells through RET tyrosine kinase. Cancer Sci. 98, 815-821.
35. Islam, N., Gagnon, F. and Moss, T. (1996). Catalytic and non-catalytic forms of the neurotrophin receptor xTrkB mRNA are expressed in a pseudo-segmental manner within the early Xenopus central nervous system. Int. J. Dev. Biol. 40, 973-983.
36. Ji, Y., Lu, Y., Yang, F., Shen, W., Tang, T. T., Feng, L., Duan, S. and Lu, B. (2010). Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat. Neurosci. 13, 302-309.
37. Jones, K. R., Farinas, I., Backus, C. and Reichardt, L. F. (1994). Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76, 989-999.
38. Kawabe, H., Neeb, A., Dimova, K., Young, S. M., Jr, Takeda, M., Katsurabayashi, S., Mitkovski, M., Malakhova, O. A., Zhang, D. E., Umikawa, M. et al. (2010). Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development. Neuron 65, 358-372.
39. Kim, H. J. and Bar-Sagi, D. (2004). Modulation of signalling by Sprouty: a developing story. Nat. Rev. Mol. Cell Biol. 5, 441-450.
40. Klein, O. D., Minowada, G., Peterkova, R., Kangas, A., Yu, B. D., Lesot, H., Peterka, M., Jernvall, J. and Martin, G. R. (2006). Sprouty genes control diastema tooth development via bidirectional antagonism of epithelial- mesenchymal FGF signaling. Dev. Cell 11, 181-190.
41. Klein, R., Smeyne, R. J., Wurst, W., Long, L. K., Auerbach, B. A., Joyner, A. L. and Barbacid, M. (1993). Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75, 113-122.
42. Komisarczuk, A. Z., Topp, S., Stigloher, C., Kapsimali, M., Bally-Cuif, L. and Becker, T. S. (2008). Enhancer detection and developmental expression of zebrafish sprouty1, a member of the fgf8 synexpression group. Dev. Dyn. 237, 2594-2603.
43. Lau, P. M., Zucker, R. S. and Bentley, D. (1999). Induction of filopodia by direct local elevation of intracellular calcium ion concentration. J. Cell Biol. 145, 1265-1275.
44. Lea, R., Papalopulu, N., Amaya, E. and Dorey, K. (2009). Temporal and spatial expression of FGF ligands and receptors during Xenopus development. Dev. Dyn. 238, 1467-1479.
45. Liu, X. and Jaenisch, R. (2000). Severe peripheral sensory neuron loss and modest motor neuron reduction in mice with combined deficiency of brain-derived neurotrophic factor, neurotrophin 3 and neurotrophin 4/5. Dev. Dyn. 218, 94-101.
46. Lohof, A. M., Ip, N. Y. and Poo, M. M. (1993). Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 350-353.
47. Marler, K. J., Becker-Barroso, E., Martinez, A., Llovera, M., Wentzel, C., Poopalasundaram, S., Hindges, R., Soriano, E., Comella, J. and Drescher, U. (2008). A TrkB/EphrinA interaction controls retinal axon branching and synaptogenesis. J. Neurosci. 28, 12700-12712.
48. Mason, J. M., Morrison, D. J., Albert Basson, M. and Licht, J. D. (2006). Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol. 16, 45-54.
49. Ming, G., Lohof, A. M. and Zheng, J. Q. (1997). Acute morphogenic and chemotropic effects of neurotrophins on cultured embryonic Xenopus spinal neurons. J. Neurosci. 17, 7860-7871.
50. Ming, G., Song, H., Berninger, B., Inagaki, N., Tessier-Lavigne, M. and Poo, M. (1999). Phospholipase C-gamma and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 23, 139-148.
51. Mingorance-Le Meur, A. and O'Connor, T. P. (2009). Neurite consolidation is an active process requiring constant repression of protrusive activity. EMBO J. 28, 248-260.
52. Minichiello, L. (2009). TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci. 10, 850-860.
53. Morita, A., Yamashita, N., Sasaki, Y., Uchida, Y., Nakajima, O., Nakamura, F., Yagi, T., Taniguchi, M., Usui, H., Katoh-Semba, R. et al. (2006). Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J. Neurosci. 26, 2971-2980.
54. Musci, T. J., Amaya, E. and Kirschner, M. W. (1990). Regulation of the fibroblast growth factor receptor in early Xenopus embryos. Proc. Natl. Acad. Sci. USA 87, 8365-8369.
55. Navarro, X. (2009). Neural plasticity after nerve injury and regeneration. Int. Rev. Neurobiol. 87, 483-505.
56. Nutt, S. L., Dingwell, K. S., Holt, C. E. and Amaya, E. (2001). Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning. Genes Dev. 15, 1152-1166.
57. O'Donnell, M., Chance, R. K. and Bashaw, G. J. (2009). Axon growth and guidance: receptor regulation and signal transduction. Annu. Rev. Neurosci. 32, 383-412.
58. Patterson, K. D. and Krieg, P. A. (1999). Hox11-family genes XHox11 and XHox11L2 in xenopus: XHox11L2 expression is restricted to a subset of the primary sensory neurons. Dev. Dyn. 214, 34-43.
59. Reichardt, L. F. (2006). Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1545-1564.
60. Robles, E., Huttenlocher, A. and Gomez, T. M. (2003). Filopodial calcium transients regulate growth cone motility and guidance through local activation of calpain. Neuron 38, 597-609.
61. Saha, M. S., Miles, R. R. and Grainger, R. M. (1997). Dorsal-ventral patterning during neural induction in Xenopus: assessment of spinal cord regionalization with xHB9, a marker for the motor neuron region. Dev. Biol. 187, 209-223.
62. Sasaki, A., Taketomi, T., Wakioka, T., Kato, R. and Yoshimura, A. (2001). Identification of a dominant negative mutant of Sprouty that potentiates fibroblast growth factor- but not epidermal growth factor-induced ERK activation. J. Biol. Chem. 276, 36804-36808.
63. Sato, K.-i., Tokmakov, A. A., Iwasaki, T. and Fukami, Y. (2000). Tyrosine kinase-dependent activation of phospholipase C[gamma] is required for calcium transient in Xenopus egg fertilization. Dev. Biol. 224, 453-469.
64. Segal, R. A. (2003). Selectivity in neurotrophin signaling: theme and variations. Annu. Rev. Neurosci. 26, 299-330.
65. Shim, K., Minowada, G., Coling, D. E. and Martin, G. R. (2005). Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev. Cell 8, 553-564.
66. Sivak, J. M., Petersen, L. F. and Amaya, E. (2005). FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. Dev. Cell 8, 689-701.
67. Snider, W. D. (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77, 627-638.
68. Tang, F. and Kalil, K. (2005). Netrin-1 induces axon branching in developing cortical neurons by frequency-dependent calcium signaling pathways. J. Neurosci. 25, 6702-6715.
69. Tang, X. Q., Tanelian, D. L. and Smith, G. M. (2004). Semaphorin3A inhibits nerve growth factor-induced sprouting of nociceptive afferents in adult rat spinal cord. J. Neurosci. 24, 819-827.
70. Taniguchi, K., Ayada, T., Ichiyama, K., Kohno, R., Yonemitsu, Y., Minami, Y., Kikuchi, A., Maehara, Y. and Yoshimura, A. (2007). Sprouty2 and Sprouty4 are essential for embryonic morphogenesis and regulation of FGF signaling. Biochem. Biophys. Res. Commun. 352, 896-902.
71. Taniguchi, K., Ishizaki, T., Ayada, T., Sugiyama, Y., Wakabayashi, Y., Sekiya, T., Nakagawa, R. and Yoshimura, A. (2009a). Sprouty4 deficiency potentiates Ras-independent angiogenic signals and tumor growth. Cancer Sci. 100, 1648-1654.
72. Taniguchi, K., Sasaki, K., Watari, K., Yasukawa, H., Imaizumi, T., Ayada, T., Okamoto, F., Ishizaki, T., Kato, R., Kohno, R. et al. (2009b). Suppression of Sproutys has a therapeutic effect for a mouse model of ischemia by enhancing angiogenesis. PLoS ONE 4, e5467.
73. Tefft, J. D., Lee, M., Smith, S., Leinwand, M., Zhao, J., Bringas, P., Jr, Crowe, D. L. and Warburton, D. (1999). Conserved function of mSpry-2, a murine homolog of Drosophila sprouty, which negatively modulates respiratory organogenesis. Curr. Biol. 9, 219-222.
74. Xu, B., Zang, K., Ruff, N. L., Zhang, Y. A., McConnell, S. K., Stryker, M. P. and Reichardt, L. F. (2000). Cortical degeneration in the absence of neurotrophin signaling: dendritic retraction and neuronal loss after removal of the receptor TrkB. Neuron 26, 233-245.
75. Yoshii, A. and Constantine-Paton, M. (2010). Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev. Neurobiol. 70, 304-322.