GDNF and GFRα1 promote formation of neuronal synapses by ligand-induced cell adhesion

Nature Neuroscience

Volumn 10, Issue 3, 2007, Pages 293-300

  Ledda, Fernanda ^a   Paratcha, Gustavo ^a   Sandoval Guzmán, Tatiana ^a   Ibá̃ez, Carlos F ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR ALPHA 1; LIGAND INDUCED CELL ADHESION MOLECULE; UNCLASSIFIED DRUG; GFRA1 PROTEIN, MOUSE; LIGAND; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; NERVE GROWTH FACTOR; PROTEIN RET; RET PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CELL ADHESION; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; HIPPOCAMPUS; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPSE VESICLE; SYNAPTOGENESIS; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; CELL CULTURE; CELL MEMBRANE; CYTOLOGY; EMBRYO; GENE EXPRESSION; METABOLISM; METHODOLOGY; MOUSE MUTANT; NERVE CELL; PHYSIOLOGY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CELL ADHESION; CELL DIFFERENTIATION; CELL MEMBRANE; CELLS, CULTURED; EMBRYO; GENE EXPRESSION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; LIGANDS; MICE; MICE, KNOCKOUT; NERVE GROWTH FACTORS; NEURAL CELL ADHESION MOLECULES; NEURONS; PROTO-ONCOGENE PROTEINS C-RET; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SYNAPSES;

EID: 33847226897     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1855     Document Type: Article

References (45)

1. Scheiffele, P. Cell-cell signaling during synapse formation in the CNS. Annu. Rev. Neurosci. 26, 485-508 (2003).
2. Yamagata, M., Sanes, J.R. & Weiner, J.A. Synaptic adhesion molecules. Curr. Opin. Cell Biol. 15, 621-632 (2003).
3. Scheiffele, P., Fan, J., Choih, J., Fetter, R. & Serafini, T. Neuroligin expressed in non-neuronal cells triggers presynaptic development in contacting axons. Cell 101, 657-669 (2000).
4. Dean, C. et al. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6, 708-716 (2003).
5. Biederer, T. et al. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297, 1525-1531 (2002).
6. Hall, A.C., Lucas, F.R. & Salinas, P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100, 525-535 (2000).
7. Umemori, H., Linhoff, M.W., Ornitz, D.M. & Sanes, J.R. FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118, 257-270 (2004).
8. Christopherson, K.S. et al. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421-433 (2005).
9. Vicario-Abejon, C., Owens, D., McKay, R. & Segal, M. Role of neurotrophins in central synapse formation and stabilization. Nat. Rev. Neurosci. 3, 965-974 (2002).
10. Cohen-Cory, S. The developing synapse: construction and modulation of synaptic structures and circuits. Science 298, 770-776 (2002).
11. Alsina, B., Vu, T. & Cohen-Cory, S. Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat. Neurosci. 4, 1093-1101 (2001).
12. Cohen-Cory, S. & Fraser, S.E. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378, 192-196 (1995).
13. McAllister, A.K., Katz, L.C. & Lo, D.C. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18, 767-778 (1997).
14. Yamada, M.K. et al. Brain-derived neurotrophic factor promotes the maturation of GABAergic mechanisms in cultured hippocampal neurons. J. Neurosci. 22, 7580-7585 (2002).
15. Poo, M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2, 24-32 (2001).
16. Airaksinen, M.S. & Saarma, M. The GDNF family: signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 3, 383-394 (2002).
17. Trupp, M. et al. Functional receptor for glial cell line-derived neurotrophic factor encoded by the c-ret proto-oncogene product. Nature 381, 785-789 (1996).
18. Durbec, P. et al. Glial cell line-derived neurotrophic factor signalling through the Ret receptor tyrosine kinase. Nature 381, 789-792 (1996).
19. Paratcha, G., Ledda, F. & Ibáñez, C.F. The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113, 867-879 (2003).
20. Sariola, H. & Saarma, M. Novel functions and signalling pathways for GDNF. J. Cell Sci. 116, 3855-3862 (2003).
21. Ledda, F., Paratcha, G. & Ibáñez, C.F. Target-derived GFRα1 as an attractive guidance signal for developing sensory and sympathetic axons via activation of Cdk5. Neuron 36, 387-401 (2002).
22. Paratcha, G. et al. Released GFRα1 potentiates downstream signaling, neuronal survival, and differentiation via a novel mechanism of recruitment of c-Ret to lipid rafts. Neuron 29, 171-184 (2001).
23. Bourque, M.J. & Trudeau, L.E. GDNF enhances the synaptic efficacy of dopaminergic neurons in culture. Eur. J. Neurosci. 12, 3172-3180 (2000).
24. Wang, C.Y. et al. Regulation of neuromuscular synapse development by glial cell line-derived neurotrophic factor and neurturin. J. Biol. Chem. 277, 10614-10625 (2002).
25. Scott, R.P. & Ibáñez, C.F. Determinants of ligand binding specificity in the glial cell line-derived neurotrophic factor family receptor alphas. J. Biol. Chem. 276, 1450-1458 (2001).
26. Eigenbrot, C. & Gerber, N. X-ray structure of glial cell-derived neurotrophic factor at 1.9 angstrom resolution and implications for receptor binding. Nat. Struct. Biol. 4, 435-438 (1997).
27. Jing, S. et al. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-α, a novel receptor for GDNF. Cell 85, 1113-1124 (1996).
28. Wiesmann, C., Ultsch, M.H., Bass, S.H. & de Vos, A.M. Crystal structure of nerve growth factor in complex with the ligand-binding domain of the TrkA receptor. Nature 401, 184-188 (1999).
29. Leppanen, V.M. et al. The structure of GFRα1 domain 3 reveals new insights into GDNF binding and RET activation. EMBO J. 23, 1452-1462 (2004).
30. Trupp, M., Raynoschek, C., Belluardo, N. & Ibáñez, C.F. Multiple GPI-anchored receptors control GDNF-dependent and independent activation of the c-Ret receptor tyrosine kinase. Mol. Cell. Neurosci. 11, 47-63 (1998).
31. Trupp, M., Belluardo, N., Funakoshi, H. & Ibáñez, C.F. Complementary and overlapping expression of glial cell line-derived neurotrophic factor (GDNF), c-ret proto-oncogene, and gdnf receptor-α indicates multiple mechanisms of trophic actions in the adult rat CNS. J. Neurosci. 17, 3554-3567 (1997).
32. Pozas, E. & Ibáñez, C.F. GDNF and GFRα1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45, 701-713 (2005).
33. Ziv, N.E. & Garner, C.C. Cellular and molecular mechanisms of presynaptic assembly. Nat. Rev. Neurosci. 5, 385-399 (2004).
34. Pina Serra, M., Quartu, M., Ambu, R., Follesa, P. & Del Fiacco, M. Immunohistochemical localization of GDNF in the human hippocampal formation from prenatal life to adulthood. Brain Res. 928, 138-146 (2002).
35. Miyazaki, H., Nagashima, K., Okuma, Y. & Nomura, Y. Expression of glial cell line-derived neurotrophic factor induced by transient forebrain ischemia in rats. Brain Res. 922, 165-172 (2001).
36. Gerlai, R. et al. Impaired water maze learning performance without altered dopaminergic function in mice heterozygous for the GDNF mutation. Eur. J. Neurosci. 14, 1153-1163 (2001).
37. Voikar, V., Rossi, J., Rauvala, H. & Airaksinen, M.S. Impaired behavioural flexibility and memory in mice lacking GDNF family receptor α2. Eur. J. Neurosci. 20, 308-312 (2004).
38. Cremer, H. et al. Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc. Natl. Acad. Sci. USA 95, 13242-13247 (1998).
39. Dityatev, A., Dityateva, G. & Schachner, M. Synaptic strength as a function of post-versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron 26, 207-217 (2000).
40. Polo-Parada, L., Bose, C.M. & Landmesser, L.T. Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAM-deficient neuromuscular junctions. Neuron 32, 815-828 (2001).
41. Sytnyk, V., Leshchyns'ka, I., Nikonenko, A.G. & Schachner, M. NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. J. Cell Biol. 174, 1071-1085 (2006).
42. Ginsberg, M.H., Partridge, A. & Shattil, S.J. Integrin regulation. Curr. Opin. Cell Biol. 17, 509-516 (2005).
43. Cammarota, M. et al. Cyclic AMP-responsive element binding protein in brain mitochondria. J. Neurochem. 72, 2272-2277 (1999).
44. Matteoli, M., Takei, K., Perin, M.S., Sudhof, T.C. & De Camilli, P. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J. Cell Biol. 117, 849-861 (1992).
45. Maximov, A. & Bezprozvanny, I. Synaptic targeting of N-type calcium channels in hippocampal neurons. J. Neurosci. 22, 6939-6952 (2002).