Over-expression of hNGF in adult human olfactory bulb neural stem cells promotes cell growth and oligodendrocytic differentiation

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Marei, Hany E S ^a   Althani, Asmaa ^b   Afifi, Nahla ^c   Abd Elmaksoud, Ahmed ^a   Bernardini, Camilla ^d   Michetti, Fabrizio ^d   Barba, Marta ^d   Pescatori, Mario ^e   Maira, Giulio ^d   Paldino, Emanuela ^f   Manni, Luigi ^g   Casalbore, Patrizia ^f   Cenciarelli, Carlo ^g  

^a Mansoura University   (Egypt)

^b Qatar University   (Qatar)

^c AIN SHAMS UNIVERSITY   (Egypt)

^d CATHOLIC UNIVERSITY   (Italy)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f CNR   (Italy)

^g INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; BIOINFORMATICS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CNPASE GENE; CONTROLLED STUDY; DNA MICROARRAY; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENE ONTOLOGY; GENE OVEREXPRESSION; GENE TARGETING; GENETIC MARKER; GFP GENE; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; IN VITRO STUDY; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NEURAL STEM CELL; NG2 GENE; NGF GENE; OLFACTORY BULB; OLIGODENDROGLIA; PDGFRALPHA GENE; PROTEIN PROTEIN INTERACTION; REPORTER GENE; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

ALGORITHMS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; NERVE GROWTH FACTOR; NEURAL STEM CELLS; OLFACTORY BULB; OLIGODENDROGLIA;

EID: 84893198150     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082206     Document Type: Article

References (104)

1. Fischer W, Wictorin K, Bjorklund A, Williams LR, Varon S et al. (1987) Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329: 65-68. doi:10.1038/329065a0. PubMed: 3627243. (Pubitemid 17125895)
2. Hefti F (1986) Nerve growth factor (NGF) promotes survival of septal cholinergic neurons after fimbrial transection. J Neurosci 6: 2155-2162. PubMed: 3746405.
3. Kromer LF (1987) Nerve growth factor treatment after brain injury prevents neuronal death. Science 235: 214-216. doi:10.1126/science.3798108. PubMed: 3798108.
4. Koliatsos VE, Nauta HJ, Clatterbuck RE, knusel B, Burton DI et al. (1991) Human nerve growth factor prevent Mouse nerve growth factorprevents degeneration of basal forebrain cholinergic neurons in primates. Ann Neurol 30: 831-840. doi:10.1002/ana.410300613. PubMed: 1789695.
5. Kordower JH, Winn SR, Liu SR, Mufson EJ, Sladek JR et al. (1994) The aged monkey basal forebrain: Rescue and sprouting of axotomized basal forebrain neurons after grafts of encapsulated cells secreting human nerve growth factor. Proc Natl Acad Sci U S A 91: 10898-10902. doi:10.1073/pnas.91.23.10898. PubMed: 7971980. (Pubitemid 24349592)
6. Tuszynski MH, Roberts J, Senut MC, Gage FH (1996) Gene therapy in the adult primate brain: Intraparenchymal grafts of cells genetically modified to produce nerve growth factor prevent cholinergic neuronal degeneration. Gene Ther 3: 305-314. PubMed: 8732162.
7. Tuszynski MH, Amaral DG, Gage FH (1990) Nerve growth factor infusion in primate brain reduces lesion-induced cholinergic neuronal degenemouseion. J Neurosci 10: 3604-3614. PubMed: 2230949.
8. Tuszynski MH, Thal L, Pay M et al. (2005) A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 11: 551-555. doi:10.1038/nm1239. PubMed: 15852017. (Pubitemid 40691288)
9. Bradbury J (2005) Hope for AD with NGF gene therapy trial. Lancet Neurol 4: 335. doi:10.1016/S1474-4422(05)70086-7. PubMed: 15931729.
10. Begley David J (2004) Delivery of therapeutic agents to the central nervous system: the problems and the possibilities. Pharmacol Therapeutics 104: 29-45. doi:10.1016/j.pharmthera.2004.08.001.
11. Rosenberg MB, Friedmann T, Robertson RC, Tuszynski M, Wolff et al. (1988) Grafting genetically modified cells to the damaged brain: Restorative effects of NGF expression. Science 242: 1575-1578. doi:10.1126/science.3201248. PubMed: 3201248. (Pubitemid 19023703)
12. Winkler J, Ramirez GA, Kuhn HG, Peterson DA, Day-Lollini PA et al. (1996) Reversible induction of Schwann cell hyperplasia and sprouting of sensory and sympathetic neurites in vivo after continuous intracerebroventricular administration of nerve growth factor. Ann Neurol 40: 128-139. doi:10.1002/ana.410400123.
13. Bishop KM, Hoefer EK, Mehta A, Ramirez A, Sun L et al. (2008) Therapeutic potential of CERE-110 (AAV2-NGF): targeted, stable, and sustained NGF delivery and trophic activity on rodent basal forebrain cholinergic neurons. Exp Neurol 211: 574-584. doi:10.1016/j.expneurol.2008.03.004. PubMed: 18439998.
14. Marks WJ Jr, Bartus RT, Siffert J, Davis CS, Lozano A, Boulis N, Vitek J et al. (2010) Gene delivery of AAV2-neurturin for Parkinson's disease: a double-blind, randomized, controlled trial. Lancet Neurol 9: 1164-1172. doi:10.1016/S1474-4422(10)70254-4. PubMed: 20970382.
15. Tannermaat MR, Eggers R, Hendriks WT, de Ruiter GC, van Heerikhuize JJ et al. (2008) Differential effects of lentiviral vector-mediated overexpression of nerve growth factor and glial cell line-derived neurotrophic factor on regenerating sensory and motor axons in the transected peripheral nerve. Eur J Neurosci 28: 1467-1479. doi:10.1111/j.1460-9568.2008.06452.x. PubMed: 18973572.
16. Schumacher JM, Short MP, Hyman BT et al. (1991) Intracerebral implantation of nerve growth factor-producing fibroblasts protects striatum against neurotoxic levels of excitatory amino acids. Neuroscience 45: 561-570. doi:10.1016/0306-4522(91)90271-O. PubMed: 1837849.
17. Martinez-Serrano A, Fischer W, Bjorklund A (1995) Reversal of age-dependent cognitive impairments and cholinergic neuron atrophy by NGF-secreting neural progenitors grafted to the basal forebrain. Neuron 15: 473-484. doi:10.1016/0896-6273(95)90051-9. PubMed: 7646899.
18. Nagahara AH, Bernot T, Moseanko R, Brignolo L, Blesch A et al. (2009) Long term reversal of cholinergic neuronal decline in aged non-human primates by lentiviral NGF gene delivery. Exp Neurol 215: 153-159. doi:10.1016/j.expneurol. 2008.10.004. PubMed: 19013154.
19. Cattaneo A, Capsoni S, Paoletti F (2008) Towards noninvasive nerve growth factor therapies for Alzheimer's disease. J Alzheimers Dis 15: 255-283. PubMed: 18953113.
20. Tuszynski MH, Roberts J, Senut MC, HS U, Gage FH (1996) Gene therapy in the adult primates brain: intraparanchymal grafts of cells genetically modified to produce nerve growth factor prevent cholinergic neuronal degeneration. Gene Ther 2:305-14.21
21. Zhang X, Klueber KM, Guo Z, Roisen FJ (2004) Adult human olfactory neural progenitors cultured in defined medium. Exp Neurol 186: 112-123. doi:10.1016/j.expneurol.2003.10.022. PubMed: 15026250. (Pubitemid 38333187)
22. Baker H, Liu N, Chun HS, Saino S, Berlin R et al. (2001) Phenotipic differentiation during migration of dopaminergic progenitor cells to the olfactory bulb. J Neurosci 21: 8505-8513. PubMed: 11606639. (Pubitemid 33051449)
23. Calza L, Giuliani A, Fernandez M et al. (2003) Neural stem cells and cholinergic neurons: regulation by immunolesion and treatment with mitogens, retinoic acid, and nerve growth factor. Proc Natl Acad Sci U S A 100: 7325-7330. doi:10.1073/pnas.1132092100. PubMed: 12777625. (Pubitemid 36706437)
24. Curtis MA, Kam M, Nannmark U, Andreson MF, Axel MZ, Willelso C et al. (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243-1249. doi:10.1126/science.1136281. PubMed: 17303719. (Pubitemid 46364256)
25. Crigler L, Robey RC, Asawachaicharn A et al. (2006) Human mesenchymal stem cell subpopulations express a variety of neuroregulatory molecules and promote neuronal cell survival and neuritogenesis. Exp Neurol 198: 54-64. doi:10.1016/j.expneurol.2005.10.029. PubMed: 16336965. (Pubitemid 43243744)
26. Gascon E, Vutskits L, Zhang H et al. (2005) Sequential activation of p75 and TrkB is involved in dendritic development of subventricular zone-derived neuronal progenitors in vitro. Eur J Neurosci 21: 69-80. doi:10.1111/j.1460- 9568.2004.03849.x. PubMed: 15654844. (Pubitemid 40193876)
27. Ip NY (1998) The neurotrophins and neuropoietic cytokines: two families of growth factors acting on neural and hematopoietic cells. Ann N Y Acad Sci 840: 97-106. doi:10.1111/j.1749-6632.1998.tb09553.x. PubMed: 9629241.
28. Dechant G, Neumann H (2002) Neurotrophins. Adv Exp Med Biol 513: 303-334. PubMed: 12575826. (Pubitemid 36332412)
29. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24: 677-736. doi:10.1146/annurev. neuro.24.1.677. PubMed: 11520916. (Pubitemid 32695243)
30. Huang EJ, Reichardt LF (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642. doi:10.1146/annurev.biochem.72. 121801.161629. PubMed: 12676795. (Pubitemid 36930455)
31. Hwang DH, Kim HM, Kang YM, Joo IS, Cho CS et al. (2011) Combination of multifaceted strategies to maximize the therapeutic benefits of neural stem cell transplantation for spinal cord repair. Cell Transplant 20: 1361-1379. doi:10.3727/096368910X557155. PubMed: 21396156.
32. Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M et al. (2004) Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 101: 18117-18122. doi:10.1073/pnas.0408258102. PubMed: 15608062. (Pubitemid 40054083)
33. Kim SU, Park IH, Kim TH (2006) Brain transplantation of human neural stem cells transduced with tyrosine hydroxylase and GTP cyclohydrolase 1 provides functional improvement in animal models of Parkinson disease. Neuropathology 26: 129-140. doi:10.1111/j.1440-1789.2006.00688.x. PubMed: 16708545.
34. Lee HJ, Kim KS, Kim EJ (2007) Brain transplantation of immortalized human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 25: 1204-1212. doi:10.1634/stemcells.2006- 0409. PubMed: 17218400. (Pubitemid 46684880)
35. Lee HJ, Kim KS, Kim EJ (2007) Human neural stem cells overexpressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLOS ONE 1: e156.
36. Lee HJ, Lim IJ, Lee MC, Kim SU (2010) Human neural stem cells genetically modified to overexpress BDNF promote functional recovery and neuroprotection in mouse stroke model. J Neurosci Res 88: 3282-3294. doi:10.1002/jnr.22474. PubMed: 20818776.
37. Lee HJ, Park IH, Kim HJ (2009) Human neural stem cells overexpressing glial cell line derived neurotrophic factor (GDNF) promote functional recovery and neuroprotection in experimental cerebral hemorrhage. Gene The 16:1066-1076.
38. Lee ST, Chu K, Jung KH (2008) Antiinflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 131: 616-629. doi:10.1093/brain/awm306. PubMed: 18156155. (Pubitemid 351294711)
39. Park D, Lee HJ, Joo SS, Bae DK, Yang G et al. (2012) Human neural stem cells overexpressing choline acetyltransferase restore cognition in mouse model of cognitive dysfunction. Exp Neurol 234: 521-526. doi:10.1016/j.expneurol.2011. 12.040. PubMed: 22245157.
40. Ryu JK, Kim J, Cho SJ, Hatori K, Nagai A et al. (2004) Proactive transplantation of human neural stem cells blocks neuronal cell death in mouse model of Huntington disease. Neurobiol Dis 16: 68-77. doi:10.1016/j.nbd.2004.01. 016. PubMed: 15207263. (Pubitemid 38569797)
41. Marei HES, Althani A, Afifi N, Michetti F, Pescatori M et al. (2011) Gene Expression Profiling of Embryonic Human Neural Stem Cells and Dopaminergic Neurons from Adult Human Substantia Nigra. PLoS ONE 6(12): e28420.
42. Marei HES, Ahmed AE, Michetti F, Pescatori M, Pallini R, et al. (2012) Gene Expression Profile of Adult Human Olfactory Bulb and Embryonic Neural Stem Cell Suggests Distinct Signaling Pathways and Epigenetic Control. PLOS ONE 7(4): e33542. doi:10.1371/journal.pone.0033542. PubMed: 22485144. Available online at: PubMed: 22485144
43. Cenciarelli C, Budoni M, Mercanti D, Fernandez E, Pallini R et al. (2006) In vitro analysis of mouse neural stem cells genetically modified to stably express human NGF by a novel multigenic viral expression system. Neurol Res 28: 505-512. PubMed: 16808880. (Pubitemid 44141318)
44. Pagani L, Cenciarelli C, Casalbore P, Budoni M, Sposato V et al. (2008) Identification and early characterization of genetically modified NGF-producing neural stem cells grafted into the injured adult rat brain. Neurol Res 3: 244-250. PubMed: 17915045. (Pubitemid 351769416)
45. Leng SL, Fan WG, Qu HG, Xu SC, Zhong WY et al. (2009) Transplantation of bone mesenchymal stem cells containing the nerve growth factor gene in adult rat brain with fimbria fornix lesion. Brain Res. PubMed: 19401170
46. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284. PubMed: 11682119. (Pubitemid 33000466)
47. Wright GW, Simon R (2003) A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics 19: 2448-2455. PubMed: 14668230. (Pubitemid 38016644)
48. Simon R, Lam A BRB-ArrayTools User Guide, version 3.2. Biometric Research Branch, National Cancer Institute. Available: http://linus.nci.nih.gov/brb. Accessed 2013 anuary 3.)
49. Pavlidis P, Qin J, Arango V, Mann JJ, Sibille E (2004) Using the Gene Ontology for microarray data mining: A comparison of methods and application to age effects in human prefrontal cortex. Neurochem Res 29: 1213-1222. PubMed: 15176478. (Pubitemid 39023495)
50. Shamir R, Maron-Katz A, Tanay A, Linhart C, Steinfeld I (2005) EXPANDER-an integrative program suite for microarray data analysis. BMC Bioinformatics 6: 232. PubMed: 16176576.
51. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C (2009) STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 37: 412-416.
52. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504. PubMed: 14597658. (Pubitemid 37428274)
53. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449. PubMed: 15972284. (Pubitemid 41222459)
54. Irizarry RA, Hobbs B, Collin F (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264. PubMed: 12925520.
55. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc 4: 44-57. PubMed: 19131956.
56. Nomura T, Göritz C, Catchpole T, Henkemeyer M, Frisén J (2010) EphB signaling controls lineage plasticity of adult neural stem cell niche cells. Cell Stem Cell 7: 730-743. PubMed: 21112567.
57. Vergaño-Vera E, Méndez-Gómez HR, Hurtado-Chong A, Cigudosa JC, Vicario-Abejón C (2009) Fibroblast growth factor-2 increases the expression of neurogenic genes and promotes the migration and differentiation of neurons derived from transplanted neural stem/progenitor cells. Neuroscience 162: 39-54. PubMed: 19318120.
58. Genini D, Garcia-Escudero R, Carbone GM, Catapano CV (2012) Transcriptional and Non-Transcriptional Functions of PPARβ/δ in Non-Small Cell Lung Cancer. PLOS ONE. 7(9): e46009. PubMed: 23049921.
59. Manuel MN, Martynoga B, Molinek MD, Quinn JC, Kroemmer C et al. (2011) The transcription factor Foxg1 regulates telencephalic progenitor proliferation cell autonomously, in part by controlling Pax6 expression levels. Neural Dev 18: 6:9
60. Louhivuori V, Vicario A, Uutela M, Rantamäki T, Louhivuori LM et al. (2011) BDNF and TrkB in neuronal differentiation of Fmr1-knockout mouse. Neurobiol Dis: F41:469-80.
61. Martin I, Andres CR, Védrine S, Tabagh R, Michelle C et al. (2009) Effect of the oligodendrocyte myelin glycoprotein (OMgp) on the expansion and neuronal differentiation of ratneural stem cells. Brain Res 1284: 22-30. PubMed: 19501059.
62. Redmond L, Hockfield S, Morabito MA (1996) The divergent homeobox gene PBX1 is expressed in the postnatal subventricular zone and interneurons of the olfactory bulb. J Neurosci 9: 2972-2982. (Pubitemid 26121840)
63. Fan XY, Mothe AJ, Tator CH (2013) Ephrin-B3 decreases the survival of adult rat spinal cord-derived neural stem/progenitor cells in vitro and after transplantation into the injured rat spinal cord. Stem Cells Dev 22: 359-373. PubMed: 22900481.
64. Barlow A, de Graaff E, Pachnis V (2003) Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET. Neuron 40: 905-916. PubMed: 14659090. (Pubitemid 37522049)
65. Kang E, Burdick KE, Kim JY, Duan X, Guo JU et al. (2011) Interaction between FEZ1 and DISC1 in regulation of neuronal development and risk for schizophrenia. Neuron 72: 559-571. PubMed: 22099459.
66. Jacquet BV, Salinas-Mondragon R, Liang H, Therit B, Buie JD et al. (2009) FoxJ1-dependent gene expression is required for differentiation of radial glia into ependymal cells and a subset of astrocytes in the postnatal brain. Development 136: 4021-4031. PubMed: 19906869.
67. Liu H, Jia D, Li A, Chau J, He D et al. (2013) p53 regulates neural stem cell proliferation and differentiation via BMP-Smad1 signaling and Id1. Stem Cells Dev 22: 913-927. PubMed: 23199293.
68. Zeng L, Zhang P, Shi L, Yamamoto V, Lu W et al. (2013) Functional impacts of NRXN1 knockdown on neurodevelopment in stem cell models. PLOS ONE. 8(3): e59685. PubMed: 23536886.
69. Sánchez-Sánchez R, Morales-Lázaro SL, Baizabal JM, Sunkara M, Morris AJ et al. (2012) Lack of lipid phosphate phosphatase-3 in embryonic stem cells compromises neuronal differentiation and neurite outgrowth. Dev Dyn 241: 953-964. PubMed: 22434721.
70. Lin CW, Huang TN, Wang GS, Kuo TY, Yen TY et al. (2006) Neural activity- and development-dependent expression and distribution of CASK interacting nucleosome assembly protein in mouse brain. J Comp Neurol 494: 606-619. PubMed: 16374801.
71. Schecterson LC, Sanchez JT, Rubel EW, Bothwell M (2012) TrkB down regulation is required for dendrite retraction in developing neurons of chicken nucleus magnocellularis. J Neurosci 32: 14000-14009. PubMed: 23035107.
72. Nieto-Estévez V, Pignatelli J, Araúzo-Bravo MJ, Hurtado-Chong A, Vicario-Abejón C (2013) A global transcriptome analysis reveals molecular hallmarks of neural stem cell death, survival, and differentiation in response to partial FGF-2 and EGF deprivation. PLOS ONE 8(1): e53594. PubMed: 23308259.
73. Majumder A, Banerjee S, Harrill JA, Machacek DW, Mohamad O et al. (2012) Neurotrophic effects of leukemia inhibitory factor on neural cells derived from human embryonic stem cells. Stem Cells 30: 2387-2399. PubMed: 22899336.
74. Kawahara H, Okada Y, Imai T, Iwanami A, Mischel PS et al. (2011) Musashi1 cooperates in abnormal cell lineage protein 28 (Lin28)-mediated let-7 family microRNA biogenesis in early neural differentiation. J Biol Chem 286: 16121-16130. PubMed: 21378162.
75. Khodosevich K, Watanabe Y, Monyer H (2011) EphA4 preserves postnatal and adult neural stem cells in an undifferentiated state in vivo. J Cell Sci 124: 1268-1279. doi:10.1242/jcs.076059. PubMed: 21444754.
76. Huang Y, Xu Z, Cao J, Cao H, Zhang S (2013) The Expression of FOXJ1 in Neurogenesis after Transient Focal Cerebral Ischemia. Can J Neurol Sci 40: 403-409. PubMed: 23603178.
77. Takarada T, Tamaki K, Takumi T, Ogura M, Ito Y et al. (2009) A protein-protein interaction of stress-responsive myosin VI endowed to inhibit neural progenitor self-replication with RNA binding protein, TLS, in murine hippocampus. J Neurochem 110: 1457-1468. PubMed: 19558455.
78. Zeng L, Zhang P, Shi L, Yamamoto V, Lu W et al. (2013) Functional impacts of NRXN1 knockdown on neurodevelopment in stem cell models. PLOS ONE. 8(3): e59685. PubMed: 23536886.
79. Ohishi K, Varnum-Finney B, Bernstein ID (2002) The notch pathway: modulation of cell fate decisions in hematopoiesis. Int J Hematol 75: 449-459. doi:10.1007/BF02982106. PubMed: 12095143.
80. Ohishi K, Katayama N, Shiku H, Varnum-Finney B, Bernstein ID (2003) Notch signalling in hematopoiesis. Semin Cell Dev Biol 14: 143-150. PubMed: 12651098. (Pubitemid 36315881)
81. van de Wetering M, de Lau W, Clevers H (2002) WNT signaling and lymphocyte development. Cell 109(Suppl): S13-S19. PubMed: 11983149.
82. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL et al. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423: 448-452. PubMed: 12717451. (Pubitemid 36626997)
83. Tago K, Nakamura T, Nishita M, Hyodo J, Nagai S et al. (2000) Inhibition of Wnt signaling by ICAT, a novel beta-catenin-interacting protein. Genes Dev 14: 1741-1749. PubMed: 10898789. (Pubitemid 30602993)
84. Kawasoe T, Furukawa Y, Daigo Y, Nishiwaki T, Ishiguro H et al. (2000) Isolation and characterization of a novel human gene, DRCTNNB1A, the expression of which is down-regulated by beta catenin. Cancer Res 60: 3354-3358. PubMed: 10910037. (Pubitemid 30482145)
85. Raff MC, Miller RH, Noble M (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303: 390-396. PubMed: 6304520. (Pubitemid 13094875)
86. Butt AM, Duncan A, Hornby MF, Kirvell SL, Hunter A et al. (1999) Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26: 84-91. PubMed: 10088675. (Pubitemid 29103171)
87. Lomoio S, Necchi D, Scherini E (2012) Uneven distribution of NG2 cells in the rat cerebellar vermis and changes in aging. Eur J Histochem 29;56(3):e27.
88. Raff MC, Miller RH, Noble M (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium". Nature 303: 390-396. . (Pubitemid 13094875)
89. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): Multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9-22. PubMed: 19096367.
90. Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE (2007) Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10: 321-330. PubMed: 17293857.
91. Casalbore P, Barone I, Felsani A, D'Agnano I, Maira G et al. (2010) Neural stem cells modified to express BDNF antagonize trimethyltin-induced neurotoxicity through PI3K/AKT and MAP kinase pathways. J Chem Phys 224: 710-721. PubMed: 20432466.
92. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at Serine 133. Cell 59: 675-680. PubMed: 2573431. (Pubitemid 19282874)
93. Sheng M, McFadden G, Greenberg ME (1990) Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 4: 571-582. PubMed: 2157471. (Pubitemid 20160846)
94. Ginty DD, Bonni A, Greenberg ME (1994) Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77: 713-725. PubMed: 8205620. (Pubitemid 24175607)
95. Deisseroth K, Bito H, Tsien R (1996) Signaling from synapse to nucleus: post-synaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16: 89-101. PubMed: 8562094. (Pubitemid 26044732)
96. Kim JB, Zaehres H, Wu G, Gentile L, Ko K et al. (2008) Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454: 646-650. PubMed: 18594515.
97. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-765. PubMed: 12948443. (Pubitemid 37088088)
98. Murray AW (2004) Recycling the cell cycle: cyclins revisited. Cell 23: 221-234. PubMed: 14744433.
99. Holmes JK, Solomon MJ (1996) A predictive scale for evaluating cyclin-dependent kinase substrates. A Comparison P 34cdc2 and p33cdk2. J Biol Chem. 271:25240-6 (Pubitemid 26337889)
100. Sun P, Watanabe H, Takano K, Yokoyama T, Fujisawa J et al. (2006) Sustained activation ofM-Ras induced by nerve growth factor is essential for neuronal differentiation of PC12 cells. Genes Cells. 11: 1097-1113. PubMed: 16923128. (Pubitemid 44256387)
101. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB (1996) Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitorcells in the developing rat brain. J Neurosci Res 43: 299-314. PubMed: 8714519. (Pubitemid 26054018)
102. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB (1996) Interaction between NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells is required for optimal response to PDGF. J Neurosci Res 43: 315-330. PubMed: 8714520. (Pubitemid 26054019)
103. Oumesmar BN, Vignais L, Baron Vanevercooren A (1997) Developmental expression of platelet-derived growth factor alpha-receptor in neurons and glial cells of the mouse CNS. J Neurosci 17: 125-139. PubMed: 8987742. (Pubitemid 27008856)
104. Vignais L, Oumesmar BN, Baron Vanevercooren A (1995) PDGF-alpha receptor is expressed by mature neurones of the central nervous system. Neuroreport 6: 1993-1996. PubMed: 8580425.