A small molecule p75NTR ligand protects neurogenesis after traumatic brain injury

Stem Cells

Volumn 31, Issue 11, 2013, Pages 2561-2574

  Shi, Jian ^a   Longo, Frank M ^b   Massa, Stephen M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Hippocampus; Neurogenesis; Neurotrophin; Traumatic brain injury

Indexed keywords

2 AMINO 3 METHYL N [2 (4 MORPHOLINYL)ETHYL]PENTANAMIDE; AMIDE; BROXURIDINE; LM 11A 31; NERVE CELL ADHESION MOLECULE; NEUROPROTECTIVE AGENT; NEUROTROPHIN RECEPTOR P75; PROTEIN TYROSINE KINASE A; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CELL ACTIVATION; CELL LOSS; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MALE; MEMORY DISORDER; MICROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; RAT; SIALYLATION; SIGNAL TRANSDUCTION; SPATIAL MEMORY; STEM CELL CULTURE; TRAUMATIC BRAIN INJURY; WILD TYPE;

HIPPOCAMPUS; NEUROGENESIS; NEUROTROPHIN; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN; BRAIN INJURIES; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; ISOLEUCINE; MALE; MICE; MICE, INBRED C57BL; MORPHOLINES; NEUROGENESIS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, NERVE GROWTH FACTOR;

EID: 84887930062     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1516     Document Type: Article

References (77)

1. Harrington AW, Leiner B, Blechschmitt C et al. Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc Natl Acad Sci USA 2004; 101: 6226-6230. (Pubitemid 38520556)
2. Pehar M, Cassina P, Vargas MR et al. Modulation of p75-dependent motor neuron death by a small non-peptidyl mimetic of the neurotro-phin loop 1 domain. Eur J Neurosci 2006; 24: 1575-1580. (Pubitemid 44427526)
3. Diarra A, Geetha T, Potter P et al. Signaling of the neurotrophin receptor p75 in relation to Alzheimer's disease. Biochem Biophys Res Commun 2009; 390: 352-356.
4. Knowles JK, Rajadas J, Nguyen TV 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.
5. Sotthibundhu A, Li QX, Thangnipon W et al. Abeta(1-42) stimulates adult SVZ neurogenesis through the p75 neurotrophin receptor. Neuro-biol Aging 2009; 30: 1975-1985.
6. Beattie MS, Harrington AW, Lee R et al. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 2002; 36: 375-386. (Pubitemid 35284727)
7. Ibanez CF, Simi A. p75 neurotrophin receptor signaling in nervous system injury and degeneration: Paradox and opportunity. Trends Neurosci 2012; 35: 431-440.
8. Longo FM, Massa SM. Small-molecule modulation of neurotrophin receptors: A strategy for the treatment of neurological disease. Nat Rev Drug Discov 2013; 12: 507-525.
9. Hempstead BL. Dissecting the diverse actions of pro- and mature neu-rotrophins. Curr Alzheimer Res 2006; 3: 19-24.
10. Underwood CK, Coulson EJ. The p75 neurotrophin receptor. Int J Bio-chem Cell Biol 2008; 40: 1664-1668. (Pubitemid 351815186)
11. Longo FM, Massa SM. Small molecule modulation of p75 neurotro-phin receptor functions. CNS Neurol Disord Drug Targets 2008; 7: 63-70. (Pubitemid 351516217)
12. Young KM, Merson TD, Sotthibundhu A et al. p75 neurotrophin receptor expression defines a population of BDNF-responsive neuro-genic precursor cells. J Neurosci 2007; 27: 5146-5155. (Pubitemid 46741778)
13. Catts VS, Al-Menhali N, Burne TH et al. The p75 neurotrophin receptor regulates hippocampal neurogenesis and related behaviours. Eur J Neurosci 2008; 28: 883-892.
14. Colditz MJ, Catts VS, Al-Menhali N et al. p75 neurotrophin receptor regulates basal and fluoxetine-stimulated hippocampal neurogenesis. Exp Brain Res 2010; 200: 161-167.
15. Bernabeu RO, Longo FM. The p75 neurotrophin receptor is expressed by adult mouse dentate progenitor cells and regulates neuronal and non-neuronal cell genesis. BMC Neurosci 2010; 11: 136.
16. Casaccia-Bonnefil P., Carter BD, Dobrowsky RT et al. Death of oligo-dendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 1996; 383: 716-719. (Pubitemid 26360647)
17. von Bohlen Und Halbach O. Immunohistological markers for staging neurogenesis in adult hippocampus. Cell Tissue Res 2007; 329: 409-420. (Pubitemid 47231297)
18. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell 2008; 132: 645-660. (Pubitemid 351253687)
19. Ming GL, Song H. Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron 2011; 70: 687-702.
20. Seki T, Arai Y. Different polysialic acid-neural cell adhesion molecule expression patterns in distinct types of mossy fiber boutons in the adult hippocampus. J Comp Neurol 1999; 410: 115-125. (Pubitemid 29284224)
21. Seki T. Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J Neurosci Res 2002; 70: 327-334. (Pubitemid 35222368)
22. Van der Borght K, Wallinga AE, Luiten PG et al. Morris water maze learning in two rat strains increases the expression of the polysialy-lated form of the neural cell adhesion molecule in the dentate gyrus but has no effect on hippocampal neurogenesis. Behav Neurosci 2005; 119: 926-932. (Pubitemid 41377244)
23. Markram K, Gerardy-Schahn R, Sandi C. Selective learning and memory impairments in mice deficient for polysialylated NCAM in adulthood. Neuroscience 2007; 144: 788-796. (Pubitemid 46013980)
24. Venero C, Herrero AI, Touyarot K et al. Hippocampal up-regulation of NCAM expression and polysialylation plays a key role on spatial memory. Eur J Neurosci 2006; 23: 1585-1595.
25. Lopez-Fernandez M.A., Montaron MF, Varea E et al. Upregulation of polysialylated neural cell adhesion molecule in the dorsal hippocampus after contextual fear conditioning is involved in long-term memory formation. J Neurosci 2007; 27: 4552-4561. (Pubitemid 46663578)
26. Van Hoesen G.W., Augustinack JC, Redman SJ. Ventromedial temporal lobe pathology in dementia, brain trauma, and schizophrenia. Ann N Y Acad Sci 1999; 877: 575-594. (Pubitemid 29351880)
27. Salmond CH, Chatfield DA, Menon DK et al. Cognitive sequelae of head injury: Involvement of basal forebrain and associated structures. Brain 2005; 128: 189-200. (Pubitemid 40070532)
28. Luikart BW, Perederiy JV, Westbrook GL. Dentate gyrus neurogene-sis, integration and microRNAs. Behav Brain Res 2012; 227: 348-355.
29. Blaiss CA, Yu TS, Zhang G et al. Temporally specified genetic ablation of neurogenesis impairs cognitive recovery after traumatic brain injury. J Neurosci 2011; 31: 4906-4916.
30. Gu Y, Arruda-Carvalho M, Wang J et al. Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 2012; 15: 1700-1706.
31. Gu Y, Janoschka S, Ge S. Neurogenesis and hippocampal plasticity in adult brain. Curr Top Behav Neurosci 2013; 15: 31-48.
32. Massa SM, Xie Y, Yang T et al. Small, nonpeptide p75NTR ligands induce survival signaling and inhibit proNGF-induced death. J Neuro-sci 2006; 26: 5288-5300. (Pubitemid 44318381)
33. Yang T, Knowles JK, Lu Q et al. Small molecule, non-peptide p75 ligands inhibit Abeta-induced neurodegeneration and synaptic impairment. PLoS ONE 2008; 3:e3604.
34. James SE, Burden H, Burgess R et al. Anti-cancer drug induced neurotoxicity and identification of Rho pathway signaling modulators as potential neuroprotectants. Neurotoxicology 2008; 29: 605-612.
35. Tep C, Lim TH, Ko PO et al. Oral administration of a small molecule targeted to block proNGF binding to p75 promotes myelin sparing and functional recovery after spinal cord injury. J Neurosci 2013; 33: 397-410.
36. Knowles JK, Simmons DA, Nguyen TV et al. A small molecule p75 ligand prevents cognitive deficits and neurite degeneration in an Alzheimer's mouse model. Neurobiol Aging 2013; 34: 2052-2063.
37. Massa SM, Yang T, Xie Y et al. Small molecule BDNF mimetics activate TrkB signaling and prevent neuronal degeneration in rodents. J Clin Invest 2010; 120: 1774-1785.
38. Ying W, Wei G, Wang D et al. Intranasal administration with NAD1 profoundly decreases brain injury in a rat model of transient focal ischemia. Front Biosci 2007; 12: 2728-2734.
39. Shi J, Miles DK, Orr BA et al. Injury-induced neurogenesis in Bax-deficient mice: Evidence for regulation by voltage-gated potassium channels. Eur J Neurosci 2007; 25: 3499-3512. (Pubitemid 47020462)
40. Lee KF, Li E, Huber LJ 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.
41. Shi J, Parada LF, Kernie SG. Bax limits adult neural stem cell persistence through caspase and IP3 receptor activation. Cell Death Differ 2005; 12: 1601-1612. (Pubitemid 41679165)
42. Zhang J, Pho V, Bonasera SJ et al. Essential function of HIPK2 in TGFbeta-dependent survival of midbrain dopamine neurons. Nat Neu-rosci 2007; 10: 77-86. (Pubitemid 46026530)
43. Storkebaum E, Lambrechts D, Dewerchin M et al. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci 2005; 8: 85-92. (Pubitemid 41236736)
44. d'Avila J.C., Lam TI, Bingham D et al. Microglial activation induced by brain trauma is suppressed by post-injury treatment with a PARP inhibitor. J Neuroinflammation 2012; 9: 31.
45. Maric D, Maric I, Barker JL. Buoyant density gradient fractionation and flow cytometric analysis of embryonic rat cortical neurons and progenitor cells. Methods 1998; 16: 247-259.
46. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984; 11: 47-60. (Pubitemid 14088970)
47. Li Y, Luikart BW, Birnbaum S et al. TrkB regulates hippocampal neu-rogenesis and governs sensitivity to antidepressive treatment. Neuron 2008; 59: 399-412.
48. Dougherty KD, Milner TA. p75NTR immunoreactivity in the rat dentate gyrus is mostly within presynaptic profiles but is also found in some astrocytic and postsynaptic profiles. J Comp Neurol 1999; 407: 77-91. (Pubitemid 29161994)
49. Kaneko N, Okano H, Sawamoto K. Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 2006; 11: 1145-1159. (Pubitemid 44426205)
50. Graham V, Khudyakov J, Ellis P et al. SOX2 functions to maintain neural progenitor identity. Neuron 2003; 39: 749-765. (Pubitemid 37088088)
51. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003; 302: 1760-1765. (Pubitemid 37505739)
52. Ekdahl CT, Claasen JH, Bonde S et al. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 2003; 100: 13632-13637. (Pubitemid 37444791)
53. Acosta SA, Tajiri N, Shinozuka K et al. Long-term upregulation of inflammation and suppression of cell proliferation in the brain of adult rats exposed to traumatic brain injury using the controlled cortical impact model. PLoS One 2013; 8:e53376.
54. Hsieh J, Aimone JB, Kaspar BK et al. IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J Cell Biol 2004; 164: 111-122. (Pubitemid 38082462)
55. Ray J, Gage FH. Differential properties of adult rat and mouse brain-derived neural stem/progenitor cells. Mol Cell Neurosci 2006; 31: 560-573. (Pubitemid 43358027)
56. Nyakas C, Luiten PG, Spencer DG et al. Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus. Brain Res Bull 1987; 18: 533-545.
57. Mrzljak L, Goldman-Rakic PS. Low-affinity nerve growth factor receptor (p75NGFR)- and choline acetyltransferase (ChAT)-immunore-active axons in the cerebral cortex and hippocampus of adult macaque monkeys and humans. Cereb Cortex 1993; 3: 133-147. (Pubitemid 23100837)
58. Neumann H, Misgeld T, Matsumuro K et al. Neurotrophins inhibit major histocompatibility class II inducibility of microglia: Involvement of the p75 neurotrophin receptor. Proc Natl Acad Sci USA 1998; 95: 5779-5784. (Pubitemid 28224173)
59. Zhang J, Geula C, Lu C et al. Neurotrophins regulate proliferation and survival of two microglial cell lines in vitro. Exp Neurol 2003; 183: 469-481. (Pubitemid 37205088)
60. Meeker RB, Poulton W, Feng WH et al. Suppression of immunodeficiency virus-associated neural damage by the p75 neurotrophin receptor ligand, LM11A-31, in an in vitro feline model. J Neuroimmune Pharmacol 2012; 7: 388-400.
61. Rola R, Mizumatsu S, Otsuka S et al. Alterations in hippocampal neu-rogenesis following traumatic brain injury in mice. Exp. Neurol 2006; 202: 189-199. (Pubitemid 44344260)
62. Gao X, Deng-Bryant Y, Cho W et al. Selective death of newborn neurons in hippocampal dentate gyrus following moderate experimental traumatic brain injury. J Neurosci Res 2008; 86: 2258-2270.
63. Kernie SG, Erwin TM, Parada LF. Brain remodeling due to neuronal and astrocytic proliferation after controlled cortical injury in mice. J Neurosci Res 2001; 66: 317-326. (Pubitemid 33027398)
64. Kernie SG, Parent JM. Forebrain neurogenesis after focal Ischemic and traumatic brain injury. Neurobiol Dis 2010; 37: 267-274.
65. Yu TS, Zhang G, Liebl DJ et al. Traumatic brain injury-induced hip-pocampal neurogenesis requires activation of early nestin-expressing progenitors. J Neurosci 2008; 28: 12901-12912.
66. Galvao RP, Garcia-Verdugo JM, Alvarez-Buylla A. Brain-derived neu-rotrophic factor signaling does not stimulate subventricular zone neu-rogenesis in adult mice and rats. J Neurosci 2008; 28: 13368-13383.
67. Colditz MJ, Catts VS, Al-menhali N, et al. p75 neurotrophin receptor regulates basal and fluoxetine-stimulated hippocampal neurogenesis. Exp Brain Res 2010; 200: 161-167.
68. Namba T, Mochizuki H, Suzuki R et al. Time-lapse imaging reveals symmetric neurogenic cell division of GFAP-expressing progenitors for expansion of postnatal dentate granule neurons. PLoS One 2011; 6: e25303.
69. Kaplan GB, Vasterling JJ, Vedak PC. Brain-derived neurotrophic factor in traumatic brain injury, post-traumatic stress disorder, and their comorbid conditions: Role in pathogenesis and treatment. Behav Pharmacol 2010; 21: 427-437.
70. Islam O, Loo TX, Heese K. Brain-derived neurotrophic factor (BDNF) has proliferative effects on neural stem cells through the truncated TRK-B receptor, MAP kinase, AKT, and STAT-3 signaling pathways. Curr Neurovasc Res 2009; 6: 42-53.
71. Waterhouse EG, An JJ, Orefice LL et al. BDNF promotes differentiation and maturation of adult-born neurons through GABAergic transmission. J Neurosci 2012; 32: 14318-14330.
72. Wu H, Lu D, Jiang H et al. Simvastatin-mediated upregulation of VEGF and BDNF, activation of the PI3K/Akt pathway, and increase of neurogenesis are associated with therapeutic improvement after traumatic brain injury. J Neurotrauma 2008; 25: 130-139. (Pubitemid 351252578)
73. Ning R, Xiong Y, Mahmood A et al. Erythropoietin promotes neuro-vascular remodeling and long-term functional recovery in rats following traumatic brain injury. Brain Res 2011; 1384: 140-150.
74. Xiong Y, Lu D, Qu C et al. Effects of erythropoietin on reducing brain damage and improving functional outcome after traumatic brain injury in mice. J Neurosurg 2008; 109: 510-521.
75. Xiong Y, Mahmood A, Meng Y et al. Treatment of traumatic brain injury with thymosin beta(4) in rats. J Neurosurg 2011; 114: 102-115.
76. Zhang Y, Chopp M, Mahmood A et al. Impact of inhibition of eryth-ropoietin treatment-mediated neurogenesis in the dentate gyrus of the hippocampus on restoration of spatial learning after traumatic brain injury. Exp Neurol 2012; 235: 336-344.
77. Gascon E, Vutskits L, Zhang H et al. Sequential activation of p75 and TrkB is involved in dendritic development of subventricular zone-derived neuronal progenitors in vitro. Eur J Neurosci 2005; 21: 69-80. (Pubitemid 40193876)