Point mutation in trkB causes loss of NT4-dependent neurons without major effects on diverse BDNF responses

Neuron

Volumn 21, Issue 2, 1998, Pages 335-345

  Minichiello, Liliana ^a   Casagranda, Franca ^a,d   Tatche, Rosa Soler ^b,e   Stucky, Cheryl L ^c   Postigo, Antonio ^a   Lewin, Gary R ^c   Davies, Alun M ^b   Klein, Rüdiger ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d ROYAL MELBOURNE HOSPITAL   (Australia)

^e Universitat de Lleida Facultat de Medicina Sabadell   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIN 4; TYROSINE KINASE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

EID: 0032143555     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80543-7     Document Type: Article

References (64)

1. Abercrombie, M. (1946). Estimation of nuclear populations from microtome sections. Anat. Rec. 94, 239-247.
2. Airaksinen, M.S., Koltzenburg, M., Lewin, G.R., Masu, Y., Helbig, C., Wolf, E., Brem, G., Toyka, K.V., Thoenen, H., and Meyer, M. (1996). Specific subsets of cutaneous mechanoreceptors require neurotrophin-3 after peripheral target innervation. Neuron 16, 287-295.
3. Alcantara, S., Frisen, J., del Rio, J.A., Soriano, E., Barbacid, M., and Silos-Santiago, I. (1997). TrkB signaling is required for postnatal survival of CNS neurons and protects hippocampal and motor neurons from axotomy-induced cell death. J. Neurosci. 17, 3623-3633.
4. Altar, C.A., Cai, N., Bliven, T., Juhuasz, M., Conner, J.M., Acheson, A.L., Lindsay, R.M., and Wiegand, S.J. (1997). Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389, 856-860.
5. Barbacid, M. (1995). Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 7, 148-155.
6. Baxter, R.M., Cohen, P., Obermeier, A., Ullrich, A., Downes, C.P., and Doza, Y.N. (1995). Phosphotyrosine residues in the nerve growth factor receptor (Trk-A). Eur. J. Biochem. 234, 84-91.
7. Cabelli, R.J., Shelton, D.L., Segal, R.A., and Shatz, C.J. (1997). Blockade of endogenous ligands of TrkB inhibits formation of ocular dominance columns. Neuron 19, 63-76.
8. Carroll, P., Lewin, G.R., Koltzenburg, M., Toyka, K.V., and Thoenen, H. (1998). A role for BDNF in mechanosensation. Nat. Neurosci. 1, 42-46.
9. Carter, B.D., and Lewin, G.R. (1997). Neurotrophins live or let die: does p75NTR decide? Neuron 18, 187-190.
10. Cohen-Cory, S., and Fraser, S.E. (1995). Effects of brain-derived neurotrophic factor on optic axon branching and remodeling in vivo. Nature 378, 192-196.
11. Collazo, D., Takahashi, H., and McKay, R.D. (1992). Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron 9, 643-656.
12. Davies, A.M. (1997a). Neurotrophin switching: where does it stand? Curr. Opin. Neurobiol. 7, 110-118.
13. Davies, A.M. (1997b). Neurotrophins: the yin and yang of nerve growth factor. Curr. Biol. 7, R38-R40.
14. Davies, A.M., Horton, A., Burton, L.E., Schmelzer, C., Vandlen, R., and Rosenthal, A. (1993a). NT-4/5 is a mammalian-specific survival factor for distinct populations of sensory neurons. J. Neurosci. 13, 4961-4967.
15. Davies, A.M., Lee, K.F., and Jaenisch, R. (1993b). p75-deficent trigeminal neurons have an altered response to NGF but not to other neurotrophins. Neuron 11, 565-574.
16. Davies, A.M., Minichiello, L., and Klein, R. (1995). Developmental changes in NTS signaling via TrkA and TrkB in embryonic neurons. EMBO J. 14, 4482-4489.
17. de Hoop, M.J., Meyn, L., and Dotti, C.G. (1998). Culturing hippocampal neurons and astrocytes from fetal rodent brain. In Cell Biology, 2nd edition, J.E.Celis, ed. (Denmark: University of Aahus), pp. 154-163.
18. Dymecki, S. (1996). Flp recombinase promotes site-specific DNA recombination in embryonic stem cells and transgenic mice. Proc. Natl. Acad. Sci. USA 93, 6191-6196.
19. Dymecki, S.M., and Tomasiewicz, H., (1998). Using Flp-recombinase to characterize expansion of Wnt1-expressing neural progenitors in the mouse. Dev. Biol., in press.
20. ElShamy, W.M., and Ernfors, P. (1997). Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 complement and cooperate with each other sequentially during visceral neuron development. J. Neurosci. 17, 8667-8675.
21. Erickson, J.T., Conover, J.C., Borday, V., Champagnat, J., Barbacid, M., Yancopoulos, G., and Katz, D.M. (1996). Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron loss distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing. J. Neurosci. 16, 5361-5371.
22. Finkbeiner, S., Tavazoie, S.F., Maloratsky, A., Jacobs, K.M., Harris, K.M., and Greenberg, M.E. (1997). CREB: a major mediator of neuronal neurotrophin responses. Neuron 19, 1031-1047.
23. Fischer, W., Sirevaag, A., Wiegand, S.J., Lindsay, R.M., and Björklund, A. (1994). Reversal of spatial memory impairments in aged rats by nerve growth factor and neurotrophins 3 and 4/5 but not by brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 91, 8607-8611.
24. Frank, D.A., and Greenberg, M.E. (1994). CREB: a mediator of long-term memory from mollusks to mammals. Cell 79, 5-8.
25. Franke, T.F., Kaplan, D.R., and Cantley, L.C. (1997). Pl3K: downstream AKTion blocks apoptosis. Cell 88, 435-437.
26. Fritzsch, B., Silos-Santiago, I., Bianchi, L.M., and Farinas, I. (1997). The role of neurotrophic factors in regulating the development of inner ear innervation. Trends Neurosci. 20, 159-164.
27. Greene, L.A., and Kaplan, D.R. (1995). Early events in neurotrophin signaling via Trk and p75 receptors. Curr. Opin. Neurobiol. 5, 579-587.
28. Guiton, M., Gunn-Moore, F.J., Stitt, T.N., Yancopoulos, G.D., and Tavare, J.M. (1994). Identification of in vivo brain-derived neurotrophic factor-stimulated autophosphorylation sites on the TrkB receptor tyrosine kinase by site-directed mutagenesis. J. Biol. Chem. 269, 30370-30377.
29. Henderson, C.E. (1996). Role of neurotrophic factors in neuronal development. Curr. Opin. Neurobiol. 6, 64-70.
30. Hyman, C., Juhasz, M., Jackson, C., Wright, P., Ip, N.Y., and Lindsay, R.M. (1994). Overlapping and distinct actions of the neurotrophins BDNF, NT-3, and NT-4/5 on cultured dopaminergic and GABAergic neurons of the ventral mesencephalon. J. Neurosci. 14, 335-347.
31. Inoue, A., and Sanes, J.R. (1997). Lamina-specific connectivity in the brain: regulation by N-cadherin, neurotrophins, and glycoconjugates. Science 276, 1428-1431.
32. Jones, K.R., Farinas, I., Backus, C., and Reichardt, L.F. (1994). Targeted disruption of the BDNF gene perturbs brain and sensory neuron develoment but not motor neuron development. Cell 76, 989-999.
33. Kaplan, D.R., and Miller, F.D. (1997). Signal transduction by the neurotrophin receptors. Curr. Opin. Cell Biol. 9, 213-221.
34. Kavanaugh, W.M., and Williams, L.T. (1994). An alternative to SH2 domains for binding tyrosine-phosphorylated proteins. Science 266, 1862-1865.
35. Klein, R., Parada, L.F., Coulier, F., and Barbacid, M. (1989). trkB, a novel tyrosine protein kinase receptor expressed during mouse neural development. EMBO J. 8, 3701-3709.
36. 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.
37. Koltzenburg, M., Stucky, C.L., and Lewin, G.R. (1997). Receptive properties of mouse cutaneous sensory neurons. J. Neurophysiol. 78, 1841-1850.
38. Kouhara, H., Hadari, Y.R., Spivak-Kroizman, T., Schilling, J., Bar-Sagi, D., Lax, I., and Schlessinger, J. (1997). A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89, 693-702.
39. Lewin, G.R., and Barde, Y.-A. (1996). Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
40. Lindvall, O., Kokaia, Z., Bengzon, J., Elmer, E., and Kokaia, M. (1994). Neurotrophins and brain insults. Trends Neurosci. 17, 490-496.
41. Marshall, C.J. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
42. Marty, S., Berninger, B., Carroll, P., and Thoenen, H. (1996). GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 16, 565-570.
43. Minichiello, L., and Klein, R. (1996). TrkB and TrkC neurotrophin receptors cooperate in promoting survival of hippocampal and cerebellar granule neurons. Genes Dev. 10, 2849-2858.
44. Minichiello, L., Piehl, F., Vazquez, E., Schimmang, T., Hökfelt, T., Represa, J., and Klein, R. (1995). Differential effects of combined trk receptor mutations on dorsal root ganglion and inner ear sensory neurons. Development 121, 4067-4075.
45. Nakamura, T., Sanokawa, R., Sasaki, Y., Ayusawa, D., Oishi, M., and Mori, N. (1996). N-Shc: a neural-specific adapter molecule that mediates signaling from neurotrophin/Trk to Ras/MAPK pathway. Oncogene 13, 1111-1121.
46. O'Bryan, J.P., Songyang, Z., Cantley, L., Der, C.J., and Pawson, T. (1996). A mammalian adaptor protein with conserved Src homology 2 and phosphotyrosine-binding domains is related to Shc and is specifically expressed in the brain. Proc. Natl. Acad. Sci. USA 93, 2729-2734.
47. Obermeier, A., Lammers, R., Wiesmüller, K.-H., Jung, G., Schlessinger, J., and Ullrich, A. (1993). Identification of Trk binding sites for SHC and phosphatidylinositol 3′-kinase and formation of a multimeric signaling complex. J. Biol. Chem. 268, 22963-22966.
48. Obermeier, A., Bradshaw, R.A., Seedorf, K., Choidas, A., Schlessinger, J., and Ullrich, A. (1994). Neuronal differentiation signals are controlled by nerve growth factor receptor/Trk binding sites for SHC and PLCγ. EMBO J. 13, 1585-1590.
49. Ponzetto, C., Bardelli, A., Zhen, Z., Maina, F., dalla Zonca, P., Giordano, S., Graziani, A., Panayotou, G., and Comoglio, P.M. (1994). A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 77, 261-271.
50. Riddle, D.R., Lo, D.C., and Katz, L.C. (1995). NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature 378, 189-191.
51. Schnell, L., Schneider, R., Kolbeck, R., Barde, Y.A., and Schwab, M.E. (1994). Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-173.
52. -/- mice reveals a role for neurotrophins in CNS patterning. Neuron 19, 269-281.
53. Segal, R.A., and Greenberg, M.E. (1996). Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19, 463-489.
54. Shieh, P.B., and Ghosh, A. (1997). Neurotrophins: new roles for a seasoned cast. Curr. Biol. 7, R627-R630.
55. Smeyne, R.J., Klein, R., Schnapp, A., Long, L.K., Bryant, S., Lewin, A., Lira, S.A., and Barbacid, M. (1994). Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368, 246-249.
56. Stephens, R.M., Loeb, D.M., Copeland, T.D., Pawson, T., Greene, L.A., and Kaplan, D.R. (1994). Trk receptors use redundant signal transduction pathways involving SHC and PLC-γ1 to mediate NGF responses. Neuron 12, 691-705.
57. Stucky, C.L., Koltzenburg, M., DeChiara, T., Lindsay, R., and Yancopoulos, G.D. (1998). Neurotrophin-4 (NT-4) is required for the survival of a subclass of hair follicle receptors. J. Neurosci., in press.
58. Teng, K.K., Courtney, J.C., van Bergen en Henegouwen, P., Birge, R.B., and Hempstead, B.L. (1996). Dissociation of NGF induced signal transduction from neurite elongation by expression of a mutant adaptor protein v-Crk in PC12 cells. Mol. Cell. Neurosci. 8, 157-170.
59. Thoenen, H. (1995). Neurotrophins and neuronal plasticity. Science 270, 593-598.
60. Vaillancourt, R.R., Heasley, L.E., Zamarripa, J., Storey, B., Valius, M., Kazlauskas, A., and Johnson, G.L. (1995). Mitogen-activated protein kinase activation is insufficient for growth factor receptor-mediated PC12 cell differentiation. Mol. Cell. Biol. 15, 3644-3653.
61. van der Geer, P., Wiley, S., Lai, V.K., Olivier, J.P., Gish, G.D., Stephen, R., Kaplan, D., Shoelson, S., and Pawson, T. (1995). A conserved amino-terminal Shc domain binds to phosphotyrosine motifs in activated receptors and phosphopeptides. Curr. Biol. 5, 404-412.
62. Vicario-Abejon, C., Johe, K.K., Hazel, T.G., Collazo, D., and McKay, R.D.G. (1995). Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15, 105-114.
63. Yamada, M., Ohnishi, H., Sano, S., Nakatani, A., Ikeuchi, T., and Hatanaka, H. (1997). Insulin receptor substrate (IRS)-1 and IRS-2 are tyrosine-phosphorylated and associated with phosphatidylinositol 3-kinase in response to brain-derived neurotrophic factor in cultured cerebral cortical neurons. J. Biol. Chem. 272, 30334-30339.
64. York, R.D., Yao, H., Dillon, T., Ellig, C.L., Eckert, S.P., McCleskey, E.W., and Stork, P.J.S. (1998). Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392, 622-626.