Activation of the p75 Neurotrophin Receptor through Conformational Rearrangement of Disulphide-Linked Receptor Dimers

Neuron

Volumn 62, Issue 1, 2009, Pages 72-83

  Vilar, Marçal ^a   Charalampopoulos, Ioannis ^a   Kenchappa, Rajappa S ^b   Simi, Anastasia ^a   Karaca, Esra ^a   Reversi, Alessandra ^c   Choi, Soyoung ^d   Bothwell, Mark ^e   Mingarro, Ismael ^f   Friedman, Wilma J ^d   Schiavo, Giampietro ^c   Bastiaens, Philippe I H ^g   Verveer, Peter J ^g   Carter, Bruce D ^b   Ibáñez, Carlos F ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d RUTGERS UNIVERSITY   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f UNIVERSITY OF VALENCIA   (Spain)

^g MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

MOLNEURO; PROTEINS; SIGNALING

Indexed keywords

CYSTEINE; DISULFIDE; NEUROTROPHIN RECEPTOR P75;

ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; LIGAND BINDING; MUTATIONAL ANALYSIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; RAT;

ANIMALS; ANIMALS, NEWBORN; BINDING SITES; CELL DEATH; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CYSTEINE; GREEN FLUORESCENT PROTEINS; HUMANS; MEMBRANE PROTEINS; MICE; MUTATION; NERVE GROWTH FACTOR; NERVE TISSUE PROTEINS; NEURONS; NF-KAPPA B; OLIGOPEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RATS; RECEPTOR, NERVE GROWTH FACTOR; RECEPTORS, NERVE GROWTH FACTOR; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUPERIOR CERVICAL GANGLION; TRANSFECTION;

EID: 64149116399     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.02.020     Document Type: Article

References (52)

1. Ashkenazi A., and Dixit V.M. Apoptosis control by death and decoy receptors. Curr. Opin. Cell Biol. 11 (1999) 255-260
2. Barker P.A. p75NTR is positively promiscuous: novel partners and new insights. Neuron 42 (2004) 529-533
3. Bibel M., and Barde Y.A. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev. 14 (2000) 2919-2937
4. Bothwell M. Evolution of the neurotrophin signaling system in invertebrates. Brain Behav. Evol. 68 (2006) 124-132
5. Bronfman F.C., and Fainzilber M. Multi-tasking by the p75 neurotrophin receptor: sortilin things out?. EMBO Rep. 5 (2004) 867-871
6. Bronfman F.C., Tcherpakov M., Jovin T.M., and Fainzilber M. Ligand-induced internalization of the p75 neurotrophin receptor: a slow route to the signaling endosome. J. Neurosci. 23 (2003) 3209-3220
7. Carter B.D., Kaltschmidt C., Kaltschmidt B., Offenhäuser N., Böhm-Matthaei R., Baeuerle P.A., and Barde Y.A. Selective activation of NF-kappa B by nerve growth factor through the neurotrophin receptor p75. Science 272 (1996) 542-545
8. Constantinescu S.N., Ghaffari S., and Lodish H.F. The erythropoietin receptor: Structure, activation and intracellular signal transduction. Trends Endocrinol. Metab. 10 (1999) 18-23
9. Dechant G., and Barde Y.A. The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat. Neurosci. 5 (2002) 1131-1136
10. Eketjäll S., Fainzilber M., Murray-Rust J., and Ibáñez C.F. Distinct structural elements in GDNF mediate binding to GFRa1 and activation of the GFRa1-c-Ret receptor complex. EMBO J. 18 (1999) 5901-5910
11. Esposito D., Patel P., Stephens R.M., Perez P., Chao M.V., Kaplan D.R., and Hempstead B.L. The cytoplasmic and transmembrane domains of the p75 and Trk A receptors regulate high affinity binding to nerve growth factor. J. Biol. Chem. 276 (2001) 32687-32695
12. Fournier A.E., GrandPre T., and Strittmatter S.M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409 (2001) 341-346
13. Friedman W.J. Neurotrophins induce death of hippocampal neurons via the p75 receptor. J. Neurosci. 20 (2000) 6340-6346
14. Friedman W.J., and Greene L.A. Neurotrophin signaling via Trks and p75. Exp. Cell Res. 253 (1999) 131-142
15. Gong Y., Cao P., Yu H.J., and Jiang T. Crystal structure of the neurotrophin-3 and p75NTR symmetrical complex. Nature 454 (2008) 789-793
16. Grob P.M., Ross A.H., Koprowski H., and Bothwell M. Characterization of the human melanoma nerve growth factor receptor. J. Biol. Chem. 260 (1985) 8044-8049
17. He X.L., and Garcia K.C. Structure of nerve growth factor complexed with the shared neurotrophin receptor p75. Science 304 (2004) 870-875
18. Hempstead B.L., Martin-Zanca D., Kaplan D.R., Parada L.F., and Chao M.V. High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350 (1991) 678-683
19. Jiang G., and Hunter T. Receptor signaling: when dimerization is not enough. Curr. Biol. 9 (1999) R568-R571
20. Jung K.M., Tan S., Landman N., Petrova K., Murray S., Lewis R., Kim P.K., Kim D.S., Ryu S.H., Chao M.V., and Kim T.W. Regulated intramembrane proteolysis of the p75 neurotrophin receptor modulates its association with the TrkA receptor. J. Biol. Chem. 278 (2003) 42161-42169
21. Kanning K.C., Hudson M., Amieux P.S., Wiley J.C., Bothwell M., and Schecterson L.C. Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J. Neurosci. 23 (2003) 5425-5436
22. Kaplan D.R., and Miller F.D. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10 (2000) 381-391
23. Kenchappa R.S., Zampieri N., Chao M.V., Barker P.A., Teng H.K., Hempstead B.L., and Carter B.D. Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 50 (2006) 219-232
24. Kubatzky K.F., Ruan W., Gurezka R., Cohen J., Ketteler R., Watowich S.S., Neumann D., Langosch D., and Klingmuller U. Self assembly of the transmembrane domain promotes signal transduction through the erythropoietin receptor. Curr. Biol. 11 (2001) 110-115
25. Lee K.F., Davies A.M., and Jaenisch R. p75-deficient embryonic dorsal root sensory and neonatal sympathetic neurons display a decreased sensitivity to NGF. Development 120 (1994) 1027-1033
26. Lee F.S., Kim A.H., Khursigara G., and Chao M.V. The uniqueness of being a neurotrophin receptor. Curr. Opin. Neurobiol. 11 (2001) 281-286
27. Lee R., Kermani P., Teng K.K., and Hempstead B.L. Regulation of cell survival by secreted proneurotrophins. Science 294 (2001) 1945-1948
28. Li R., Gorelik R., Nanda V., Law P.B., Lear J.D., DeGrado W.F., and Bennett J.S. Dimerization of the transmembrane domain of Integrin alphaIIb subunit in cell membranes. J. Biol. Chem. 279 (2004) 26666-26673
29. Liepinsh E., Ilag L.L., Otting G., and Ibañez C.F. NMR structure of the death domain of the p75 neurotrophin receptor. EMBO J. 16 (1997) 4999-5005
30. Mahadeo D., Kaplan L., Chao M.V., and Hempstead B.L. High affinity nerve growth factor binding displays a faster rate of association than p140trk binding. Implications for multi-subunit polypeptide receptors. J. Biol. Chem. 269 (1994) 6884-6891
31. McClain M.S., Iwamoto H., Cao P., Vinion-Dubiel A.D., Li Y., Szabo G., Shao Z., and Cover T.L. Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J. Biol. Chem. 278 (2003) 12101-12108
32. Mendrola J.M., Berger M.B., King M.C., and Lemmon M.A. The single transmembrane domains of ErbB receptors self-associate in cell membranes. J. Biol. Chem. 277 (2002) 4704-4712
33. Mi S., Lee X., Shao Z., Thill G., Ji B., Relton J., Levesque M., Allaire N., Perrin S., Sands B., et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 7 (2004) 221-228
34. Moriki T., Maruyama H., and Maruyama I.N. Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain. J. Mol. Biol. 311 (2001) 1011-1026
35. Nykjaer A., Lee R., Teng K.K., Jansen P., Madsen P., Nielsen M.S., Jacobsen C., Kliemannel M., Schwarz E., Willnow T.E., et al. Sortilin is essential for proNGF-induced neuronal cell death. Nature 427 (2004) 843-848
36. Palmada M., Kanwal S., Rutkoski N.J., Gustafson-Brown C., Johnson R.S., Wisdom R., and Carter B.D. c-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation. J. Cell Biol. 158 (2002) 453-461
37. Patapoutian A., and Reichardt L.F. Trk receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 11 (2001) 272-280
38. Roux P.P., and Barker P.A. Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol. 67 (2002) 203-233
39. Russ W.P., and Engelman D.M. TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. USA 96 (1999) 863-868
40. Rydén M., Hempstead B., and Ibáñez C.F. Differential modulation of neuron survival during development by nerve growth factor binding to the p75 neurotrophin receptor. J. Biol. Chem. 272 (1997) 16322-16328
41. Schlessinger J. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell 110 (2002) 669-672
42. Seubert N., Royer Y., Staerk J., Kubatzky K.F., Moucadel V., Krishnakumar S., Smith S.O., and Constantinescu S.N. Active and inactive orientations of the transmembrane and cytosolic domains of the erythropoietin receptor dimer. Mol. Cell 12 (2003) 1239-1250
43. Squire A., Verveer P.J., Rocks O., and Bastiaens P.I. Red-edge anisotropy microscopy enables dynamic imaging of homo-FRET between green fluorescent proteins in cells. J. Struct. Biol. 147 (2004) 62-69
44. Troy C.M., Friedman J.E., and Friedman W.J. Mechanisms of p75-mediated death of hippocampal neurons. Role of caspases. J. Biol. Chem. 277 (2002) 34295-34302
45. Wang J.J., Rabizadeh S., Tasinato A., Sperandio S., Ye X., Green M., Assa-Munt N., Spencer D., and Bredesen D.E. Dimerization-dependent block of the proapoptotic effect of p75(NTR). J. Neurosci. Res. 60 (2000) 587-593
46. Wang K.C., Kim J.A., Sivasankaran R., Segal R.A., and He Z. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420 (2002) 74-78
47. Wehrman T., He X., Raab B., Dukipatti A., Blau H., and Garcia K.C. Structural and mechanistic insights into nerve growth factor interactions with the TrkA and p75 receptors. Neuron 53 (2007) 25-38
48. Wong S.T., Henley J.R., Kanning K.C., Huang K.H., Bothwell M., and Poo M.M. A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci. 5 (2002) 1302-1308
49. Yamashita T., Tucker K.L., and Barde Y.A. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron 24 (1999) 585-593
50. Yamashita T., Higuchi H., and Tohyama M. The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J. Cell Biol. 157 (2002) 565-570
51. Yohannan S., Faham S., Yang D., Whitelegge J.P., and Bowie J.U. The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors. Proc. Natl. Acad. Sci. USA 101 (2004) 959-963
52. Yoon S.O., Casaccia-Bonnefil P., Carter B., and Chao M.V. Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J. Neurosci. 18 (1998) 3273-3281