Neuronal growth cone retraction relies on proneurotrophin receptor signaling through rac

Science Signaling

Volumn 4, Issue 202, 2011, Pages

  Deinhardt, Katrin ^a   Kim, Taeho ^b,d   Spellman, Daniel S ^a   Mains, Richard E ^c   Eipper, Betty A ^c   Neubert, Thomas A ^a   Chao, Moses V ^a   Hempstead, Barbara L ^b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FASCIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR P75; RAC PROTEIN; SORTILIN; ACTIN; ACTIN BINDING PROTEIN; CARRIER PROTEIN; CELL SURFACE RECEPTOR; NERVE GROWTH FACTOR RECEPTOR; NERVE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INACTIVATION; GROWTH CONE; MOUSE; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL LINE; HUMAN; PHYSIOLOGY; ULTRASTRUCTURE;

ACTINS; ANIMALS; CARRIER PROTEINS; CELL LINE; CELLS, CULTURED; GROWTH CONES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICE; MICROFILAMENT PROTEINS; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; RAC GTP-BINDING PROTEINS; RATS; RECEPTOR, NERVE GROWTH FACTOR; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 83155175604     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002060     Document Type: Article

References (41)

1. D. B. Kantor, A. L. Kolodkin, Curbing the excesses of youth: Molecular insights into axonal pruning. Neuron 38, 849-852 (2003).
2. L. Luo, D. D. O'Leary, Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28, 127-156 (2005).
3. C. S. Cohan, E. A. Welnhofer, L. Zhao, F. Matsumura, S. Yamashiro, Role of the actin bundling protein fascin in growth cone morphogenesis: Localization in filopodia and lamellipodia. Cell Motil. Cytoskeleton 48, 109-120 (2001).
4. T. B. Kuhn, P. J. Meberg, M. D. Brown, B. W. Bernstein, L. S. Minamide, J. R. Jensen, K. Okada, E. A. Soda, J. R. Bamburg, Regulating actin dynamics in neuronal growth cones by ADF/cofilin and Rho family GTPases. J. Neurobiol. 44, 126-144 (2000).
5. R. L. Faulkner, L. K. Low, H. J. Cheng, Axon pruning in the developing vertebrate hippocampus. Dev. Neurosci. 29, 6-13 (2007).
6. N. J. Xu, M. Henkemeyer, Ephrin-B3 reverse signaling through Grb4 and cytoskeletal regulators mediates axon pruning. Nat. Neurosci. 12, 268-276 (2009).
7. S. Cohen-Cory, A. H. Kidane, N. J. Shirkey, S. Marshak, Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev. Neurobiol. 70, 271-288 (2010).
8. A. K. McAllister, D. C. Lo, L. C. Katz, Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15, 791-803 (1995).
9. W. D. Snider, Functions of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77, 627-638 (1994).
10. R. Lee, P. Kermani, K. K. Teng, B. L. Hempstead, Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948 (2001).
11. U. Suter, J. V. Heymach Jr., E. M. Shooter, Two conserved domains in the NGF propeptide are necessary and sufficient for the biosynthesis of correctly processed and biologically active NGF. EMBO J. 10, 2395-2400 (1991).
12. A. Nykjaer, R. Lee, K. K. Teng, P. Jansen, P. Madsen, M. S. Nielsen, C. Jacobsen, M. Kliemannel, E. Schwarz, T. E. Willnow, B. L. Hempstead, C. M. Petersen, Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848 (2004).
13. NTR and sortilin. J. Neurosci. 25, 5455-5463 (2005).
14. R. W. Gundersen, J. N. Barrett, Neuronal chemotaxis: Chick dorsal-root axons turn toward high concentrations of nerve growth factor. Science 206, 1079-1080 (1979).
15. J. Riedl, A. H. Crevenna, K. Kessenbrock, J. H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T. A. Holak, Z. Werb, M. Sixt, R. Wedlich-Soldner, Lifeact: A versatile marker to visualize F-actin. Nat. Methods 5, 605-607 (2008).
16. A. Debant, C. Serra-Pages, K. Seipel, S. O'Brien, M. Tang, S. H. Park, M. Streuli, The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rho-specific guanine nucleotide exchange factor domains. Proc. Natl. Acad. Sci. U.S.A. 93, 5466-5471 (1996).
17. K. Seipel, Q. G. Medley, N. L. Kedersha, X. A. Zhang, S. P. O'Brien, C. Serra-Pages, M. E. Hemler, M. Streuli, Trio amino-terminal guanine nucleotide exchange factor domain expression promotes actin cytoskeleton reorganization, cell migration and anchorage-independent cell growth. J. Cell Sci. 112, 1825-1834 (1999).
18. J. K. Song, E. Giniger, Noncanonical Notch function in motor axon guidance is mediated by Rac GTPase and the GEF1 domain of Trio. Dev. Dyn. 240, 324-332 (2011).
19. V. Benard, G. M. Bokoch, Assay of Cdc42, Rac, and Rho GTPase activation by affinity methods. Methods Enzymol. 345, 349-359 (2002).
20. N. Bouquier, E. Vignal, S. Charrasse, M. Weill, S. Schmidt, J. P. Léonetti, A. Blangy, P. Fort, A cell active chemical GEF inhibitor selectively targets the Trio/RhoG/Rac1 signaling pathway. Chem. Biol. 16, 657-666 (2009).
21. O. Shonukan, I. Bagayogo, P. McCrea, M. Chao, B. Hempstead, Neurotrophin-induced melanoma cell migration is mediated through the actin-bundling protein fascin. Oncogene 22, 3616-3623 (2003).
22. S. Ono, Y. Yamakita, S. Yamashiro, P. T.Matsudaira, J. R. Gnarra, T. Obinata, F. Matsumura, Identification of an actin binding region and a protein kinase C phosphorylation site on human fascin. J. Biol. Chem. 272, 2527-2533 (1997).
23. D. Vignjevic, S. Kojima, Y. Aratyn, O. Danciu, T. Svitkina, G. G. Borisy, Role of fascin in filopodial protrusion. J. Cell Biol. 174, 863-875 (2006).
24. L. C. Schecterson, M. Bothwell, Neurotrophin receptors: Old friends with new partners. Dev. Neurobiol. 70, 332-338 (2010).
25. T. Kim, B. L. Hempstead, NRH2 is a trafficking switch to regulate sortilin localization and permit proneurotrophin-induced cell death. EMBO J. 28, 1612-1623 (2009).
26. A. Briançon-Marjollet, A. Ghogha, H. Nawabi, I. Triki, C. Auziol, S. Fromont, C. Piché, H. Enslen, K. Chebli, J. F. Cloutier, V. Castellani, A. Debant, N. Lamarche-Vane, Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol. Cell. Biol. 28, 2314-2323 (2008).
27. V. E. Neubrand, C. Thomas, S. Schmidt, A. Debant, G. Schiavo, Kidins220/ARMS regulates Rac1-dependent neurite outgrowth by direct interaction with the RhoGEF Trio. J. Cell Sci. 123, 2111-2123 (2010).
28. S. Estrach, S. Schmidt, S. Diriong, A. Penna, A. Blangy, P. Fort, A. Debant, The human Rho-GEF Trio and its target GTPase RhoG are involved in the NGF pathway, leading to neurite outgrowth. Curr. Biol. 12, 307-312 (2002).
29. S. Cheng, J. Mao, V. Rehder, Filopodial behavior is dependent on the phosphorylation state of neuronal growth cones. Cell Motil. Cytoskeleton 47, 337-350 (2000).
30. S. Naska, D. C. Lin, F. D. Miller, D. R. Kaplan, p75NTR is an obligate signaling receptor required for cues that cause sympathetic neuron growth cone collapse. Mol. Cell. Neurosci. 45, 108-120 (2010).
31. A. W. Harrington, B. Leiner, C. Blechschmitt, J. C. Arevalo, R. Lee, K. Morl, M. Meyer, B. L. Hempstead, S. O. Yoon, K. M. Giehl, Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc. Natl. Acad. Sci. U.S.A. 101, 6226-6230 (2004).
32. A. Kichev, E. V. Ilieva, G. Piñol-Ripoll, P. Podlesniy, I. Ferrer, M. Portero-Otín, R. Pamplona, C. Espinet, Cell death and learning impairment in mice caused by in vitro modified pro-NGF can be related to its increased oxidative modifications in Alzheimer disease. Am. J. Pathol. 175, 2574-2585 (2009).
33. NTR-mediated apoptosis via neurotrophin receptor-interacting factor in hippocampal neurons after seizures. J. Neurosci. 28, 9870-9879 (2008).
34. F. Ferraro, X. M. Ma, J. A. Sobota, B. A. Eipper, R. E. Mains, Kalirin/Trio Rho guanine nucleotide exchange factors regulate a novel step in secretory granule maturation. Mol. Biol. Cell 18, 4813-4825 (2007).
35. L. Chen, S. Yang, J. Jakoncic, J. J. Zhang, X. Y. Huang, Migrastatin analogues target fascin to block tumour metastasis. Nature 464, 1062-1066 (2010).
36. L. J. Huber, M. V. Chao, Mesenchymal and neuronal cell expression of the p75 neurotrophin receptor gene occur by different mechanisms. Dev. Biol. 167, 227-238 (1995).
37. C. E. McPherson, B. A. Eipper, R. E. Mains, Multiple novel isoforms of Trio are expressed in the developing rat brain. Gene 347, 125-135 (2005).
38. D. Feng, T. Kim, E. Ozkan, M. Light, R. Torkin, K. K. Teng, B. L. Hempstead, K. C. Garcia, Molecular and structural insight into proNGF engagement of p75NTR and sortilin. J. Mol. Biol. 396, 967-984 (2010).
39. M. Domeniconi, N. Zampieri, T. Spencer, M. Hilaire,W. Mellado, M. V. Chao, M. T. Filbin, MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 46, 849-855 (2005).
40. A. Shutes, C. Onesto, V. Picard, B. Leblond, F. Schweighoffer, C. J. Der, Specificity and mechanism of action of EHT 1864, a novel small molecule inhibitor of Rac family small GTPases. J. Biol. Chem. 282, 35666-35678 (2007).
41. M. Chattopadhyay, M. Mata, D. J. Fink, Continuous d-opioid receptor activation reduces neuronal voltage-gated sodium channel (NaV1.7) levels through activation of protein kinase C in painful diabetic neuropathy. J. Neurosci. 28, 6652-6658 (2008).