P75 neurotrophin receptor signaling in nervous system injury and degeneration: paradox and opportunity

Trends in Neurosciences

Volumn 35, Issue 7, 2012, Pages 431-440

  Ibáñez, Carlos F ^a   Simi, Anastasia ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

ALS; Alzheimer's disease; Apoptosis; Degeneration; Injury; Neurotrophin

Indexed keywords

NEUROTROPHIN RECEPTOR P75;

DISEASE SEVERITY; GLIA CELL; HUMAN; INJURY SEVERITY; NERVE CELL LESION; NERVE FIBER DEGENERATION; NERVOUS SYSTEM INJURY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; RECEPTOR, NERVE GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84862775324     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2012.03.007     Document Type: Review

References (123)

1. Chao M.V. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 2003, 4:299-309.
2. Aron L., Klein R. Repairing the parkinsonian brain with neurotrophic factors. Trends Neurosci. 2011, 34:88-100.
3. Dechant G., Barde Y.-A. The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat. Neurosci. 2002, 5:1131-1136.
4. Roux P.P., Barker P.A. Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol. 2002, 67:203-233.
5. Gentry J.J., et al. The p75 neurotrophin receptor: multiple interactors and numerous functions. Prog. Brain Res. 2004, 146:25-39.
6. Underwood C.K., Coulson E.J. The p75 neurotrophin receptor. Int. J. Biochem. Cell Biol. 2008, 40:1664-1668.
7. Reichardt L.F. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2006, 361:1545-1564.
8. Kaplan D.R., Miller F.D. Signal transduction by the neurotrophin receptors. Curr. Opin. Cell Biol. 1997, 9:213-221.
9. Lu B., et al. The yin and yang of neurotrophin action. Nat. Rev. Neurosci. 2005, 6:603-614.
10. Lee R., et al. Regulation of cell survival by secreted proneurotrophins. Science 2001, 294:1945-1948.
11. Nykjaer A., et al. Sortilin is essential for proNGF-induced neuronal cell death. Nature 2004, 427:843-848.
12. Nykjaer A., et al. p75NTR - live or let die. Curr. Opin. Neurobiol. 2005, 15:49-57.
13. Woo N.H., et al. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat. Neurosci. 2005, 8:1069-1077.
14. Yang F., et al. Pro-BDNF-induced synaptic depression and retraction at developing neuromuscular synapses. J. Cell Biol. 2009, 185:727-741.
15. Liepinsh E., et al. NMR structure of the death domain of the p75 neurotrophin receptor. EMBO J. 1997, 16:4999-5005.
16. Carter B.D., et al. Selective activation of NF-kappa B by nerve growth factor through the neurotrophin receptor p75. Science 1996, 272:542-545.
17. Friedman W.J. Neurotrophins induce death of hippocampal neurons via the p75 receptor. J. Neurosci. 2000, 20:6340-6346.
18. Yoon S.O., et al. Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J. Neurosci. 1998, 18:3273-3281.
19. Troy C.M., et al. Mechanisms of p75-mediated death of hippocampal neurons. Role of caspases. J. Biol. Chem. 2002, 277:34295-34302.
20. Yamashita T., et al. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron 1999, 24:585-593.
21. Wang K.C., et al. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 2002, 420:74-78.
22. Wong S.T., et al. A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci. 2002, 5:1302-1308.
23. Yamashita T., et al. The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J. Cell Biol. 2002, 157:565-570.
24. Fournier A.E., et al. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001, 409:341-346.
25. Mi S., et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 2004, 7:221-228.
26. He Z., Koprivica V. The Nogo signaling pathway for regeneration block. Annu. Rev. Neurosci. 2004, 27:341-368.
27. Yamashita T., et al. Enhanced insulin-sensitivity in mice lacking ganglioside GM3. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:3445-3449.
28. Friedman W.J., et al. Temporal and spatial expression of NGF receptor mRNA during postnatal rat brain development analyzed by in situ hybridization. Brain Res. Dev. Brain Res. 1991, 63:43-51.
29. Wyatt S., et al. Expression of the NGF receptor gene in sensory neurons and their cutaneous targets prior to and during innervation. Neuron 1990, 4:421-427.
30. Ernfors P., et al. Expression of nerve growth factor receptor mRNA is developmentally regulated and increased after axotomy in rat spinal cord motoneurons. Neuron 1989, 2:1605-1613.
31. Mobley W.C., et al. Developmental regulation of nerve growth factor and its receptor in the rat caudate-putamen. Neuron 1989, 3:655-664.
32. Cragnolini A.B., et al. Nerve growth factor attenuates proliferation of astrocytes via the p75 neurotrophin receptor. Glia 2009, 57:1386-1392.
33. Ernfors P., et al. Developmental and regional expression of beta-nerve growth factor receptor mRNA in the chick and rat. Neuron 1988, 1:983-996.
34. Verge V.M., et al. Colocalization of NGF binding sites, trk mRNA, and low-affinity NGF receptor mRNA in primary sensory neurons: responses to injury and infusion of NGF. J. Neurosci. 1992, 12:4011-4022.
35. Saika T., et al. Effects of nerve crush and transection on mRNA levels for nerve growth factor receptor in the rat facial motoneurons. Brain Res. Mol. Brain Res. 1991, 9:157-160.
36. Koliatsos V.E., et al. Axotomy induces nerve growth factor receptor immunoreactivity in spinal motor neurons. Brain Res. 1991, 549:297-304.
37. Lowry K.S., et al. A potential role for the p75 low-affinity neurotrophin receptor in spinal motor neuron degeneration in murine and human amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2001, 2:127-134.
38. Taniuchi M., et al. Induction of nerve growth factor receptor in Schwann cells after axotomy. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:4094-4098.
39. Zhou X.F., et al. Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection. J. Neurosci. 1996, 16:2901-2911.
40. Obata K., et al. Suppression of the p75 neurotrophin receptor in uninjured sensory neurons reduces neuropathic pain after nerve injury. J. Neurosci. 2006, 26:11974-11986.
41. Syroid D.E., et al. Induction of postnatal schwann cell death by the low-affinity neurotrophin receptor in vitro and after axotomy. J. Neurosci. 2000, 20:5741-5747.
42. Petratos S., et al. Schwann cell apoptosis in the postnatal axotomized sciatic nerve is mediated via NGF through the low-affinity neurotrophin receptor. J. Neuropathol. Exp. Neurol. 2003, 62:398-411.
43. Hall S.M., et al. Schwann cells responding to primary demyelination in vivo express p75NTR and c-erbB receptors: a light and electron immunohistochemical study. J. Neurocytol. 1997, 26:679-690.
44. Beattie M.S., et al. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 2002, 36:375-386.
45. Dowling P., et al. Up-regulated p75NTR neurotrophin receptor on glial cells in MS plaques. Neurology 1999, 53:1676-1682.
46. Hu B., et al. Localization of p75 neurotrophin receptor in the retina of the adult SD rat: an immunocytochemical study at light and electron microscopic levels. Glia 1998, 24:187-197.
47. Rudzinski M., et al. Changes in retinal expression of neurotrophins and neurotrophin receptors induced by ocular hypertension. J. Neurobiol. 2004, 58:341-354.
48. Lönngren U., et al. The growth factor response in ischemic rat retina and superior colliculus after brimonidine pre-treatment. Brain Res. Bull. 2006, 71:208-218.
49. Giehl K., et al. Endogenous brain-derived neurotrophic factor and neurotrophin-3 antagonistically regulate survival of axotomized corticospinal neurons in vivo. J. Neurosci. 2001, 21:3492-3502.
50. Martínez-Murillo R., et al. Lesion-induced expression of low-affinity nerve growth factor receptor-immunoreactive protein in Purkinje cells of the adult rat. Neuroscience 1993, 52:587-593.
51. Roux P.P., et al. p75 neurotrophin receptor expression is induced in apoptotic neurons after seizure. J. Neurosci. 1999, 19:6887-6896.
52. Oh J.D., et al. Overexpression of neurotrophin receptor p75 contributes to the excitotoxin-induced cholinergic neuronal death in rat basal forebrain. Brain Res. 2000, 853:174-185.
53. Kokaia Z., et al. Focal cerebral ischemia in rats induces expression of P75 neurotrophin receptor in resistant striatal cholinergic neurons. Neuroscience 1998, 84:1113-1125.
54. Kommaddi R.P., et al. Trk-dependent ADAM17 activation facilitates neurotrophin survival signaling. FASEB J. 2011, 25:2061-2070.
55. Ramos A., et al. Hypo-osmolar stress induces p75NTR expression by activating Sp1-dependent transcription. J. Neurosci. 2007, 27:1498-1506.
56. Mufson E.J., Kordower J.H. Cortical neurons express nerve growth factor receptors in advanced age and Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:569-573.
57. Ernfors P., et al. Cholinergic neurons of the nucleus basalis express elevated levels of nerve growth factor receptor mRNA in senile dementia of the Alzheimer type. Dementia 1990, 1:138-145.
58. Rabizadeh S., et al. Induction of apoptosis by the low-affinity NGF receptor. Science 1993, 261:345-348.
59. Barrett G.L., Bartlett P.F. The p75 nerve growth factor receptor mediates survival or death depending on the stage of sensory neuron development. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:6501-6505.
60. Bartheld, von C.S., et al. Positive and negative effects of neurotrophins on the isthmo-optic nucleus in chick embryos. Neuron 1994, 12:639-654.
61. Frade J.M., et al. Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 1996, 383:166-168.
62. Casaccia-Bonnefil P., et al. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 1996, 383:716-719.
63. Bamji S.X., et al. The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuron death. J. Cell Biol. 1998, 140:911-923.
64. Haase G., et al. Signaling by death receptors in the nervous system. Curr. Opin. Neurobiol. 2008, 18:284-291.
65. Raoul C., et al. Active killing of neurons during development and following stress: a role for p75(NTR) and Fas?. Curr. Opin. Neurobiol. 2000, 10:111-117.
66. Cheema S.S., et al. Reducing p75 nerve growth factor receptor levels using antisense oligonucleotides prevents the loss of axotomized sensory neurons in the dorsal root ganglia of newborn rats. J. Neurosci. Res. 1996, 46:239-245.
67. Jansen P., et al. Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat. Neurosci. 2007, 10:1449-1457.
68. Ferri C., et al. Effects of facial nerve injury on mouse motoneurons lacking the p75 low-affinity neurotrophin receptor. J. Neurobiol. 1998, 34:1-9.
69. Wiese S., et al. The role of p75(NTR) in modulating neurotrophin survival effects in developing motoneurons. Eur. J. Neurosci. 1999, 11:1668-1676.
70. Khursigara G., et al. A prosurvival function for the p75 receptor death domain mediated via the caspase recruitment domain receptor-interacting protein 2. J. Neurosci. 2001, 21:5854-5863.
71. Cragnolini A.B., Friedman W.J. The function of p75(NTR) in glia. Trends Neurosci. 2008, 31:99-104.
72. Cosgaya J.M., et al. The neurotrophin receptor p75NTR as a positive modulator of myelination. Science 2002, 298:1245-1248.
73. Tomita K., et al. The neurotrophin receptor p75NTR in Schwann cells is implicated in remyelination and motor recovery after peripheral nerve injury. Glia 2007, 55:1199-1208.
74. Song X.-Y., et al. Knockout of p75(NTR) impairs re-myelination of injured sciatic nerve in mice. J. Neurochem. 2006, 96:833-842.
75. Volosin M., et al. Induction of proneurotrophins and activation of p75(NTR)-mediated apoptosis via neurotrophin receptor-interacting factor in hippocampal neurons after seizures. J. Neurosci. 2008, 28:9870-9879.
76. Domeniconi M., et al. Pro-NGF secreted by astrocytes promotes motor neuron cell death. Mol. Cell. Neurosci. 2007, 34:271-279.
77. Volosin M., et al. Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. J. Neurosci. 2006, 26:7756-7766.
78. Fahnestock M., et al. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol. Cell. Neurosci. 2001, 18:210-220.
79. Podlesniy P., et al. Pro-NGF from Alzheimer's disease and normal human brain displays distinctive abilities to induce processing and nuclear translocation of intracellular domain of p75NTR and apoptosis. Am. J. Pathol. 2006, 169:119-131.
80. Pedraza C.E., et al. Pro-NGF isolated from the human brain affected by Alzheimer's disease induces neuronal apoptosis mediated by p75NTR. Am. J. Pathol. 2005, 166:533-543.
81. Lebrun-Julien F., et al. ProNGF induces TNFalpha-dependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3817-3822.
82. Bai Y., et al. Chronic and acute models of retinal neurodegeneration TrkA activity are neuroprotective whereas p75NTR activity is neurotoxic through a paracrine mechanism. J. Biol. Chem. 2010, 285:39392-39400.
83. Shi Z., et al. Neurotrophic rationale in glaucoma: a TrkA agonist, but not NGF or a p75 antagonist, protects retinal ganglion cells in vivo. Dev. Neurobiol. 2007, 67:884-894.
84. Kohn J., et al. Functionally antagonistic interactions between the TrkA and p75 neurotrophin receptors regulate sympathetic neuron growth and target innervation. J. Neurosci. 1999, 19:5393-5408.
85. Singh K.K., Miller F.D. Activity regulates positive and negative neurotrophin-derived signals to determine axon competition. Neuron 2005, 45:837-845.
86. Singh K.K., et al. Developmental axon pruning mediated by BDNF-p75NTR-dependent axon degeneration. Nat. Neurosci. 2008, 11:649-658.
87. Plachta N., et al. Identification of a lectin causing the degeneration of neuronal processes using engineered embryonic stem cells. Nat. Neurosci. 2007, 10:712-719.
88. Deinhardt K., et al. Neuronal growth cone retraction relies on proneurotrophin receptor signaling through rac. Sci. Signal. 2011, 4:ra82.
89. Park K.J., et al. p75NTR-dependent, myelin-mediated axonal degeneration regulates neural connectivity in the adult brain. Nat. Neurosci. 2010, 13:559-566.
90. Park J.B., et al. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 2005, 45:345-351.
91. Shao Z., et al. TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 2005, 45:353-359.
92. Yamashita T., Tohyama M. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat. Neurosci. 2003, 6:461-467.
93. Nikolaev A., et al. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009, 457:981-989.
94. Scott A.L.M., Ramer M.S. Schwann cell p75NTR prevents spontaneous sensory reinnervation of the adult spinal cord. Brain 2010, 133:421-432.
95. Perini G., et al. Role of p75 neurotrophin receptor in the neurotoxicity by beta-amyloid peptides and synergistic effect of inflammatory cytokines. J. Exp. Med. 2002, 195:907-918.
96. Sotthibundhu A., et al. Beta-amyloid(1-42) induces neuronal death through the p75 neurotrophin receptor. J. Neurosci. 2008, 28:3941-3946.
97. Knowles J.K., et al. The p75 neurotrophin receptor promotes amyloid-beta(1-42)-induced neuritic dystrophy in vitro and in vivo. J. Neurosci. 2009, 29:10627-10637.
98. Pang P.T., et al. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 2004, 306:487-491.
99. Rösch H., et al. The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:7362-7367.
100. Zagrebelsky M., et al. The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons. J. Neurosci. 2005, 25:9989-9999.
101. Copray S., et al. Deficient p75 low-affinity neurotrophin receptor expression exacerbates experimental allergic encephalomyelitis in C57/BL6 mice. J. Neuroimmunol. 2004, 148:41-53.
102. Peter M.E., et al. The CD95 receptor: apoptosis revisited. Cell 2007, 129:447-450.
103. Lee K., et al. Targeted mutation of the gene encoding the low affinity NGF receptor P75 leads to deficits in the peripheral sensory nervous-system. Cell 1992, 69:737-749.
104. Lee K.-F., et al. p75-deficient embryonic dorsal root sensory and neonatal sympathetic neurons display a decreased sensitivity to NGF. Development 1994, 120:1027-1033.
105. Vilar M., et al. Activation of the p75 neurotrophin receptor through conformational rearrangement of disulphide-linked receptor dimers. Neuron 2009, 62:72-83.
106. Vilar M., et al. Ligand-independent signaling by disulfide-crosslinked dimers of the p75 neurotrophin receptor. J. Cell Sci. 2009, 122:3351-3357.
107. Eriksson C., et al. Increased expression of mRNA encoding interleukin-1 beta and caspase-1, and the secreted isoform of interleukin-1 receptor antagonist in the rat brain following systemic kainic acid administration. J. Neurosci. Res. 2000, 60:266-279.
108. Choi S., Friedman W.J. Inflammatory cytokines IL-1β and TNF-α regulate p75NTR expression in CNS neurons and astrocytes by distinct cell-type-specific signalling mechanisms. ASN Neuro 2009, 1:e00010.
109. Ibanez C.F., et al. Disruption of the low affinity receptor-binding site in NGF allows neuronal survival and differentiation by binding to the Trk gene product. Cell 1992, 69:329-341.
110. Rydén M., Ibanez C.F. A second determinant of binding to the p75 neurotrophin receptor revealed by alanine-scanning mutagenesis of a conserved loop in nerve growth factor. J. Biol. Chem. 1997, 272:33085-33091.
111. Rydén M., et al. Functional analysis of mutant neurotrophins deficient in low-affinity binding reveals a role for p75LNGFR in NT-4 signalling. EMBO J. 1995, 14:1979-1990.
112. He X.-L., Garcia K.C. Structure of nerve growth factor complexed with the shared neurotrophin receptor p75. Science 2004, 304:870-875.
113. Gong Y., et al. Crystal structure of the neurotrophin-3 and p75NTR symmetrical complex. Nature 2008, 454:789-793.
114. Longo F., et al. Synthetic NGF peptide derivatives prevent neuronal death via a p75 receptor-dependent mechanism. J. Neurosci. Res. 1997, 48:1-17.
115. Massa S.M., et al. Small, nonpeptide p75NTR ligands induce survival signaling and inhibit proNGF-induced death. J. Neurosci. 2006, 26:5288-5300.
116. Lebrun-Julien F., et al. Inhibition of p75(NTR) in glia potentiates TrkA-mediated survival of injured retinal ganglion cells. Mol. Cell. Neurosci. 2009, 40:410-420.
117. Longo F.M., Massa S.M. Small molecule modulation of p75 neurotrophin receptor functions. CNS Neurol. Disord. Drug Targets 2008, 7:63-70.
118. Esposito D., et al. The cytoplasmic and transmembrane domains of the p75 and TrkA receptors regulate high affinity binding to nerve growth factor. J. Biol. Chem. 2001, 276:32687-32695.
119. Lebrun-Julien F., et al. Excitotoxic death of retinal neurons in vivo occurs via a non-cell-autonomous mechanism. J. Neurosci. 2009, 29:5536-5545.
120. Durany N., et al. Brain-derived neurotrophic factor and neurotrophin-3 levels in Alzheimer's disease brains. Int. J. Dev. Neurosci. 2000, 18:807-813.
121. Gold B., et al. White matter integrity and vulnerability to Alzheimer's disease: preliminary findings and future directions. Biochim. Biophys. Acta 2012, 1822:416-422.
122. DeLacalle S., et al. Reduced retrograde labelling with fluorescent tracer accompanies neuronal atrophy of basal forebrain cholinergic neurons in aged rats. Neuroscience 1996, 75:19-27.
123. Cooper J., et al. Reduced transport of [I-125] nerve growth-factor by cholinergic neurons and down-regulated Trka expression in the medial septum of aged rats. Neuroscience 1994, 62:625-629.