Heterodimerization of p45–p75 Modulates p75 Signaling: Structural Basis and Mechanism of Action

PLoS Biology

Volumn 12, Issue 8, 2014, Pages

  Vilar, Marçal ^a,b   Sung, Tsung Chang ^a   Chen, Zhijiang ^a   García Carpio, Irmina ^b   Fernandez, Eva M ^b   Xu, Jiqing ^a   Riek, Roland ^a,c   Lee, Kuo Fen ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; PROTEIN P45; PROTEIN P75; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; NERVE GROWTH FACTOR RECEPTOR; NRH2 PROTEIN, MOUSE; PROTEIN BINDING; SOLUTION AND SOLUBILITY;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIMERIZATION; IMMUNOPRECIPITATION; MOUSE; NERVE FIBER GROWTH; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STATIC ELECTRICITY; UPREGULATION; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; HEK293 CELL LINE; HUMAN; INJURIES; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN ANALYSIS; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; SCIATIC NERVE; SOLUTION AND SOLUBILITY; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; CYSTEINE; HEK293 CELLS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; RECEPTOR, NERVE GROWTH FACTOR; RECEPTORS, CELL SURFACE; RECEPTORS, NERVE GROWTH FACTOR; SCIATIC NERVE; SIGNAL TRANSDUCTION; SOLUTIONS; STRUCTURE-ACTIVITY RELATIONSHIP; UP-REGULATION;

EID: 84927170517     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001918     Document Type: Article

References (68)

1. Dechant G, Barde YA, (2002) The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat Neurosci5: 1131–1136.
2. Barker PA, (2004) p75NTR is positively promiscuous: novel partners and new insights. Neuron42: 529–533.
3. Gentry JJ, Rutkoski NJ, Burke TL, Carter BD, (2004) A functional interaction between the p75 neurotrophin receptor interacting factors, TRAF6 and NRIF. J Biol Chem279: 16646–16656.
4. Nykjaer A, Willnow TE, Petersen CM, (2005) p75NTR–live or let die. Curr Opin Neurobiol15: 49–57.
5. Yamashita T, Fujitani M, Hata K, Mimura F, Yamagishi S, (2005) Diverse functions of the p75 neurotrophin receptor. Anat Sci Int80: 37–41.
6. Fournier AE, GrandPre T, Strittmatter SM, (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature409: 341–346.
7. Zheng B, Atwal J, Ho C, Case L, He XL, et al. (2005) Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc Natl Acad Sci U S A102: 1205–1210.
8. Benson MD, Romero MI, Lush ME, Lu QR, Henkemeyer M, et al. (2005) Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc Natl Acad Sci U S A102: 10694–10699.
9. Filbin MT, (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci4: 703–713.
10. Schwab ME, (2004) Nogo and axon regeneration. Curr Opin Neurobiol14: 118–124.
11. Fournier AE, Strittmatter SM, (2001) Repulsive factors and axon regeneration in the CNS. Curr Opin Neurobiol11: 89–94.
12. Schweigreiter R, Walmsley AR, Niederost B, Zimmermann DR, Oertle T, et al. (2004) Versican V2 and the central inhibitory domain of Nogo-A inhibit neurite growth via p75NTR/NgR-independent pathways that converge at RhoA. Mol Cell Neurosci27: 163–174.
13. Wong ST, Henley JR, Kanning KC, Huang KH, Bothwell M, et al. (2002) A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat Neurosci5: 1302–1308.
14. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z, (2002) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature420: 74–78.
15. Shao Z, Browning JL, Lee X, Scott ML, Shulga-Morskaya S, et al. (2005) TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron45: 353–359.
16. Park JB, Yiu G, Kaneko S, Wang J, Chang J, et al. (2005) A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron45: 345–351.
17. Mi S, Lee X, Shao Z, Thill G, Ji B, et al. (2004) LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci7: 221–228.
18. Yamashita T, Tucker KL, Barde YA, (1999) Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron24: 585–593.
19. Yamashita T, Tohyama M, (2003) The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci6: 461–467.
20. Yamashita T, Higuchi H, Tohyama M, (2002) The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J Cell Biol157: 565–570.
21. Conrad S, Schluesener HJ, Trautmann K, Joannin N, Meyermann R, et al. (2005) Prolonged lesional expression of RhoA and RhoB following spinal cord injury. J Comp Neurol487: 166–175.
22. Sivasankaran R, Pei J, Wang KC, Zhang YP, Shields CB, et al. (2004) PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci7: 261–268.
23. Frankowski H, Castro-Obregon S, del Rio G, Rao RV, Bredesen DE, (2002) PLAIDD, a type II death domain protein that interacts with p75 neurotrophin receptor. Neuromolecular Med1: 153–170.
24. Wang X, Shao Z, Zetoune FS, Zeidler MG, Gowrishankar K, et al. (2003) NRADD, a novel membrane protein with a death domain involved in mediating apoptosis in response to ER stress. Cell Death Differ10: 580–591.
25. Murray SS, Perez P, Lee R, Hempstead BL, Chao MV, (2004) A novel p75 neurotrophin receptor-related protein, NRH2, regulates nerve growth factor binding to the TrkA receptor. J Neurosci24: 2742–2749.
26. Kanning KC, Hudson M, Amieux PS, Wiley JC, Bothwell M, et al. (2003) Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J Neurosci23: 5425–5436.
27. Kim T, Hempstead BL, (2009) NRH2 is a trafficking switch to regulate sortilin localization and permit proneurotrophin-induced cell death. EMBO J28: 1612–1623.
28. Park HH, Lo YC, Lin SC, Wang L, Yang JK, et al. (2007) The death domain superfamily in intracellular signaling of apoptosis and inflammation. Annu Rev Immunol25: 561–586.
29. Sung TC, Chen Z, Thuret S, Vilar M, Gage FH, et al. (2013) P45 forms a complex with FADD and promotes neuronal cell survival following spinal cord injury. PLoS ONE8: e69286.
30. Vilar M, Charalampopoulos I, Kenchappa RS, Simi A, Karaca E, et al. (2009) Activation of the p75 neurotrophin receptor through conformational rearrangement of disulphide-linked receptor dimers. Neuron62: 72–83.
31. Dubreuil CI, Winton MJ, McKerracher L, (2003) Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. J Cell Biol162: 233–243.
32. Chivatakarn O, Kaneko S, He Z, Tessier-Lavigne M, Giger RJ, (2007) The Nogo-66 receptor NgR1 is required only for the acute growth cone-collapsing but not the chronic growth-inhibitory actions of myelin inhibitors. J Neurosci27: 7117–7124.
33. Lee PS, Yerys BE, Della Rosa A, Foss-Feig J, Barnes KA, et al. (2009) Functional connectivity of the inferior frontal cortex changes with age in children with autism spectrum disorders: a fcMRI study of response inhibition. Cereb Cortex19: 1787–1794.
34. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ, et al. (2010) Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron66: 663–670.
35. Lee JK, Chan AF, Luu SM, Zhu Y, Ho C, et al. (2009) Reassessment of corticospinal tract regeneration in Nogo-deficient mice. J Neurosci29: 8649–8654.
36. Cafferty WB, Kim JE, Lee JK, Strittmatter SM, (2007) Response to correspondence: Kim et al., "axon regeneration in young adult mice lacking Nogo-A/B." Neuron 38, 187–199. Neuron54: 195–199.
37. Sandu C, Morisawa G, Wegorzewska I, Huang T, Arechiga AF, et al. (2006) FADD self-association is required for stable interaction with an activated death receptor. Cell Death Differ13: 2052–2061.
38. Wajant H, (2003) Death receptors. Essays Biochem39: 53–71.
39. Sandu C, Gavathiotis E, Huang T, Wegorzewska I, Werner MH, (2005) A mechanism for death receptor discrimination by death adaptors. J Biol Chem280: 31974–31980.
40. Huang B, Eberstadt M, Olejniczak ET, Meadows RP, Fesik SW, (1996) NMR structure and mutagenesis of the Fas (APO-1/CD95) death domain. Nature384: 638–641.
41. Qu Q, Chen J, Wang Y, Gui W, Wang L, et al. (2013) Structural characterization of the self-association of the death domain of p75(NTR.). PLoS ONE8: e57839.
42. Grzesiek S, Dobeli H, Gentz R, Garotta G, Labhardt AM, et al. (1992) 1H, 13C, and 15N NMR backbone assignments and secondary structure of human interferon-gamma. Biochemistry31: 8180–8190.
43. Pervushin K, Riek R, Wider G, Wuthrich K, (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci U S A94: 12366–12371.
44. Bang S, Jeong EJ, Kim IK, Jung YK, Kim KS, (2000) Fas- and tumor necrosis factor-mediated apoptosis uses the same binding surface of FADD to trigger signal transduction. A typical model for convergent signal transduction. J Biol Chem275: 36217–36222.
45. Liepinsh E, Ilag LL, Otting G, Ibanez CF, (1997) NMR structure of the death domain of the p75 neurotrophin receptor. EMBO J16: 4999–5005.
46. Sykes AM, Palstra N, Abankwa D, Hill JM, Skeldal S, et al. (2012) The effects of transmembrane sequence and dimerization on cleavage of the p75 neurotrophin receptor by gamma-secretase. J Biol Chem287: 43810–43824.
47. Holm L, Rosenstrom P, (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res38: W545–549.
48. Carrington PE, Sandu C, Wei Y, Hill JM, Morisawa G, et al. (2006) The structure of FADD and its mode of interaction with procaspase-8. Mol Cell22: 599–610.
49. Hill JM, Vaidyanathan H, Ramos JW, Ginsberg MH, Werner MH, (2002) Recognition of ERK MAP kinase by PEA-15 reveals a common docking site within the death domain and death effector domain. EMBO J21: 6494–6504.
50. Park HH, (2009) The intracellular domain of the low affinity p75 nerve growth factor receptor is a death effector domain. Mol Med Report2: 539–541.
51. Esposito D, Patel P, Stephens RM, Perez P, Chao MV, et al. (2001) The cytoplasmic and transmembrane domains of the p75 and Trk A receptors regulate high affinity binding to nerve growth factor. J Biol Chem276: 32687–32695.
52. Ferrao R, Wu H, (2012) Helical assembly in the death domain (DD) superfamily. Curr Opin Struct Biol22: 241–247.
53. Xiao T, Towb P, Wasserman SA, Sprang SR, (1999) Three-dimensional structure of a complex between the death domains of Pelle and Tube. Cell99: 545–555.
54. Qin H, Srinivasula SM, Wu G, Fernandes-Alnemri T, Alnemri ES, et al. (1999) Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1. Nature399: 549–557.
55. Wang L, Yang JK, Kabaleeswaran V, Rice AJ, Cruz AC, et al. (2010) The Fas-FADD death domain complex structure reveals the basis of DISC assembly and disease mutations. Nat Struct Mol Biol17: 1324–1329.
56. Lin SC, Lo YC, Wu H, (2010) Helical assembly in the MyD88-IRAK4-IRAK2 complex in TLR/IL-1R signalling. Nature465: 885–890.
57. Park HH, Logette E, Raunser S, Cuenin S, Walz T, et al. (2007) Death domain assembly mechanism revealed by crystal structure of the oligomeric PIDDosome core complex. Cell128: 533–546.
58. Khursigara G, Bertin J, Yano H, Moffett H, DiStefano PS, et al. (2001) A prosurvival function for the p75 receptor death domain mediated via the caspase recruitment domain receptor-interacting protein 2. J Neurosci21: 5854–5863.
59. Charalampopoulos I, Vicario A, Pediaditakis I, Gravanis A, Simi A, et al. (2012) Genetic dissection of neurotrophin signaling through the p75 neurotrophin receptor. Cell Rep2: 1563–1570.
60. Demjen D, Klussmann S, Kleber S, Zuliani C, Stieltjes B, et al. (2004) Neutralization of CD95 ligand promotes regeneration and functional recovery after spinal cord injury. Nat Med10: 389–395.
61. Davis AR, Lotocki G, Marcillo AE, Dietrich WD, Keane RW, (2007) FasL, Fas, and death-inducing signaling complex (DISC) proteins are recruited to membrane rafts after spinal cord injury. J Neurotrauma24: 823–834.
62. Cavanagh. J F, W.J Palmer III, A.G, Mark Rance & N.J. Skelton (2006) Protein NMR spectroscopy: principles & practice (second edition). San Diego, CA: Academic Press.
63. Ritter C, Luhrs T, Kwiatkowski W, Riek R, (2004) 3D TROSY-HNCA(coded)CB and TROSY-HNCA(coded)CO experiments: triple resonance NMR experiments with two sequential connectivity pathways and high sensitivity. J Biomol NMR28: 289–294.
64. Kumar A, Wagner G, Ernst RR, Wuthrich K, (1980) Studies of J-connectives and selective 1H-1H Overhauser effects in H2O solutions of biological macromolecules by two-dimensional NMR experiments. Biochem Biophys Res Commun96: 1156–1163.
65. Fesik SW, Luly JR, Erickson JW, Abad-Zapatero C, (1988) Isotope-edited proton NMR study on the structure of a pepsin/inhibitor complex. Biochemistry27: 8297–8301.
66. Ikura M, Kay LE, Bax A, (1991) Improved three-dimensional 1H-13C-1H correlation spectroscopy of a 13C-labeled protein using constant-time evolution. J Biomol NMR1: 299–304.
67. Guntert P, Mumenthaler C, Wuthrich K, (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol273: 283–298.
68. Guntert P, (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol278: 353–378.