Neurobiology of Aging
Volume 28, Issue 8 , Pages 1148-1162 , August 2007

Trophic factors counteract elevated FGF-2-induced inhibition of adult neurogenesis

  • Honghui Chen

      Affiliations

    • Present address: Wuhan Psychiatric Hospital/Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, PR China.
  • ,
  • Yunn-Chyn Tung
  • ,
  • Bin Li
  • ,
  • Khalid Iqbal
  • ,
  • Inge Grundke-Iqbal

      Affiliations

    • Corresponding Author InformationCorresponding author at: Neuroimmunology Laboratory, NYS Institute for Basic Research in Developmental Disabilities, 1050 Forest Hill Road, Staten Island, NY 10314-6399, USA. Tel.: +1 718 494 5263; fax: +1 718 494 1080.

Received 7 July 2005 ,Revised 22 May 2006 ,Accepted 24 May 2006.

References 

  1. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS. Peripheral infusion of IGF-1 selectively induces neurogenesis in the adult rat hippocampus. J Neurosci. 2000;20:2896–2903
  2. Albrecht PJ, Dahl JP, Stoltzfus OK, Levenson R, Levison SW. Ciliary neurotrophic factor activates spinal cord astrocytes, stimulating their production and release of fibroblast growth factor-2, to increase motor neuron survival. Exp Neurol. 2002;173:46–62
  3. Alvarez XA, Sampedro C, Perez P, Laredo M, Couceiro V, Hernandez A, et al. Positive effects of Cerebrolysin on electroencephalogram slowing, cognition and clinical outcome in patients with post-acute traumatic brain injury: an exploratory study. Int Clin Psychopharmacol. 2003;18:271–278
  4. Alvarez XA, Cacabelos R, Laredo M, Couceiro V, Sampedro C, Varela M, et al. A 24-week, double-blind, placebo-controlled study of three dosages of Cerebrolysin in patients with mild to moderate Alzheimer's disease. Eur J Neurol. 2006;13:43–54
  5. Anneren G, Tuvemo T, Carlsson-Skwirut C, Lonnerholm T, Bang P, Sara VR, et al. Growth hormone treatment in young children with Down's syndrome: effects on growth and psychomotor development. Arch Dis Child. 1999;80:334–338
  6. Avila J. The influence of aging in one tauopathy: Alzheimer disease. Arch Immunol Ther Exp (Warsz). 2004;52:410–413
  7. Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell. 2005;121:645–657
  8. Bensadoun A, Weinstein D. Assay of proteins in the presence of interfering materials. Anal Biochem. 1976;70:241–250
  9. Betchen SA, Kaplitt M. Future and current surgical therapies in Parkinson's disease. Curr Opin Neurol. 2003;16:487–493
  10. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, et al. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science. 1997;278:477–483
  11. Boucher SE, Hitchcock PF. Insulin-related growth factors stimulate proliferation of retinal progenitors in the goldfish. J Comp Neurol. 1998;394:386–394
  12. Brickman YG, Ford MD, Gallagher JT, Nurcombe V, Bartlett PF, Turnbull JE. Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J Biol Chem. 1998;273:4350–4359
  13. Cameron HA, McKay RD. Restoring production of hippocampal neurons in old age. Nat Neurosci. 1999;2:894–897
  14. Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I. Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat Med. 2002;8:1390–1397
  15. Chen H, Fu YS, Guo JW. Ability of GDNF to diminish free radical production leads to protection against kainite-induced excitotoxicity in hippocampus. Hippocampus. 2004;14:77–86
  16. Cummings BJ, Su JH, Cotman CW. Neuritic involvement within FGF-2 immunopositive plaques of Alzheimer disease. Exp Neurol. 1993;124:315–325
  17. Donovan MH, Yazdani U, Norris RE, Games D, German DC, Eisch AJ. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol. 2006;495:70–83
  18. Durany N, Michel T, Jellinger K, Cruz-Sanchez FF, Cervos-Navarro J, Riederer P. Brain-derived neurotrophic factor and neurotrophin-3 levels in Alzheimer disease brains. Int J Dev Neurosci. 2000;18:807–813
  19. Emerich DF, Thanos CG. Intracompartmental delivery of CNTF as therapy for Huntington's disease and retinitis pigmentosa. Curr Gene Ther. 2006;6:147–159
  20. Emsley JG, Hagg T. Endogenous and exogenous ciliary neurotrophic factor enhances forebrain neurogenesis in adult mice. Exp Neurol. 2003;183:298–310
  21. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Noedborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4:1313–1317
  22. Ford-Perriss M, Turner K, Guimond S, Apedaile A, Haubeck HD, Turnbull J, et al. Localisation of specific heparan sulfate proteoglycans during the proliferative phase of brain development. Dev Dyn. 2003;227:170–184
  23. Frederick TJ, Wood TL. IGF-1 and IGF-2 coordinately enhance cyclin D1 and cyclin E-cdk2 association and activity to promote G1 progression in oligodendrocyte progenitor cells. Mol Cell Neurosci. 2004;25:480–492
  24. Gasparini L, Gouras GK, Wang R, Gross RS, Beal MF, Greengard P, et al. Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. J Neurosci. 2001;21:2561–2570
  25. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci. 1999;2:260–265
  26. Grondin R, Zhang Z, Ai Y, Gash DM, Gerhardt GA. Intracranial delivery of proteins and peptides as a therapy for neurodegenerative diseases. Prog Drug Res. 2003;61:101–123
  27. Ho GJ, Drego R, Hakimian E, Masliah E. Mechanisms of cell signaling and inflammation in Alzheimer's disease. Curr Drug Targets Inflamm Allergy. 2005;4:247–256
  28. Hock C, Heese K, Hulette C, Rosenberg C, Otten U. Region-specific neurotrophin imbalances in Alzheimer disease. Arch Neurol. 2000;57:846–851
  29. Hockfield S, McKay RD. Identification of major cell classes in the developing mammalian nervous system. J Neurosci. 1985;5:3310–3328
  30. Hoffman MC, Braydich-Stolle L, Dym M. Isolation of male germ-line stem cells; influence of GDNF. Dev Biol. 2005;279:114–124
  31. Hong M, Lee VMY. Insulin and insulin-like growth factor-1 regulate tau phosphorylation in cultured human neurons. J Biol Chem. 1997;272:19547–19553
  32. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, et al. Increased hippocampal neurogenesis in Alzheimer disease. Proc Natl Acad Sci USA. 2004;101:343–347
  33. Jin K, Galvan V, Xie L, Mao XO, Gorostiza OF, Bredesen DE, et al. Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSW,Ind) mice. Proc Natl Acad Sci USA. 2004;34:13363–13367
  34. Johe KK, Hazel TG, Muller T, Dugich-Djordjevic MM, McKay RDG. Single factors direct the differentiation of stem cells from fetal and adult central nervous system. Genes Dev. 1996;10:3129–3140
  35. Kaur N, Lu B, Monroe RK, Ward SM, Halvorsen SW. Inducers of oxidative stress block ciliary neurotrophic factor activation of Jak/STAT signaling in neurons. J Neurochem. 2005;92:1521–1530
  36. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature. 1997;386:493–495
  37. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci. 1996;16:2027–2033
  38. Levison SW, Ducceschi MH, Young GM, Wood TL. Acute exposure to CNTF in vivo induces multiple components of reactive gliosis. Exp Neurol. 1996;141:256–268
  39. Lesort M, Johnson GVW. Insulin-like growth factor-1 and insulin mediate transient site-selective increases in tau phosphorylation in primary cortical neurons. Neuroscience. 2000;99:305–316
  40. Lindahl B, Westling C, Gimenez-Gallego G, Lindahl U, Salmivirta M. Common binding sites for β-amyloid fibrils and fibroblast growth factor-2 in heparan sulfate from human cerebral cortex. J Biol Chem. 1999;274:30631–30635
  41. Masliah E, Armasolo F, Veinbergs J, Mallory M, Samuel W. Cerebrolysin ameliorates performance deficits, and neuronal damage in apolipoprotein E-deficient mice. Pharmacol Biochem Behav. 1999;62:239–245
  42. Mittoux V, Joseph JM, Conde F, Palfi S, Dautry C, Poyot T, et al. Restoration of cognitive and motor functions by ciliary neurotrophic factor in a primate model of Huntington's disease. Hum Gene Ther. 2000;11:1177–1187
  43. Morgan D, Gordon MN, Tan J, Wilcock D, Rojiani AM. Dynamic complexity of the microglial activation response in transgenic models of amyloid deposition: implications for Alzheimer therapeutics. J Neuropathol Exp Neurol. 2005;64:743–753
  44. Mustafa A, Lannfelt L, Lilius L, Islam A, Winblad B, Adam A. Decreased plasma insulin-like growth factor-I level in familial Alzheimer disease patients carrying the Swedish APP 670/671 mutation. Dement Geriatr Cogn Disord. 1999;10:446–451
  45. Nakamura Y, Yamamoto M, Oda E, Yamamoto A, Kanemura Y, Hara M, et al. Stem/progenitor cells and radial fibers during human fetal brain development. Lab Invest. 2003;83:479–489
  46. Ohkubo Y, Uchida AO, Shin D, Partanen J, Vaccarino FM. Fibroblast growth factor receptor 1 is required for the proliferation of hippocampal progenitor cells and for hippocampal growth in mouse. J Neurosci. 2004;24:6057–6069
  47. Ostenfeld T, Tai YT, Martin P, Deglon N, Aebischer P, Svendsen CN. Neurospheres modified to produce glial cell line-derived neurotrophic factor increase the survival of transplanted dopamine neurons. J Neurosci Res. 2002;69:955–965
  48. Panisset M, Gauthier S, Moessler H, Windisch M, The Cerebrolysin Study Group . Cerebrolysin in Alzheimer disease: a randomized, double-blind, placebo-controlled trial with a neurotrophic agent. J Neural Transm. 2002;109:1089–1104
  49. Raff MC, Abney ER, Cohen J, Lindsay R, Noble M. Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J Neurosci. 1983;3:1289–1300
  50. Ragusa L, Valetta MR, Proto C, Alberti A, Romano C, Rossodivita A, et al. IGF-I levels in prepubertal and pubertal children with Down syndrome. Minerva Endocrinol. 1998;23:31–36
  51. Rajan P, McKay RD. Multiple routes to astrocytic differentiation in the CNS. J Neurosci. 1998;18:3620–3629
  52. Riikonen R. Neurotrophic factors in the pathogenesis of Rett syndrome. J Child Neurol. 2003;18:693–697
  53. Rockenstein E, Adame A, Mante M, Moessler H, Windisch M, Masliah E. The neuroprotective effects of Cerebrolysin in a transgenic model of Alzheimer disease are associated with improved behavioral performance. J Neural Transm. 2003;110:1313–1327
  54. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, Harrison-Restelli C, et al. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med. 2000;6:271–277
  55. Rűther E, Ritter R, Apecechea M, Freytg S, Gmeinbauer R, Windisch M. Sustained improvements in patients with dementia of Alzheimer type (DAT) 6 months after termination of Cerebrolysin therapy. J Neural Transm. 2000;107:815–829
  56. Shetty AK, Hattiangady B, Shetty GA. Stem/progenitor cell proliferation factors FGF-2, IGF-1 and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia. 2005;51:173–186
  57. Shors TJ. Memory traces of trace memories: neurogenesis, synaptogenesis and awareness. Trends Neurosci. 2004;27:250–256
  58. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM. A role for adult neurogenesis in spatial long-term memory. Neuroscience. 2005;130:843–852
  59. Stopa EG, Gonzalez AM, Chorsky R, Corona RJ, Alzarez J, Bird ED, et al. Basic fibroblast growth factor in Alzheimer disease. Biochem Biophys Res Commun. 1990;171:690–696
  60. Takami K, Matsuo A, Terai K, Walker DG, McGeer EG, McGeer PL. Fibroblast growth factor receptor-1 expression in the cortex and hippocampus in Alzheimer disease. Brain Res. 1998;802:89–97
  61. Tanaka Y, Kawahata K, Nakata T, Hirokawa N. Chronological expression of microtubule-associated proteins (MAPs) in EC cell P19 after neuronal induction by retinoic acid. Brain Res. 1992;596:269–278
  62. Tatebayashi Y, Iqbal K, Grundke-Iqbal I. Dynamic regulation of expression and phosphorylation of tau by fibroblast growth factor-2 in neural progenitor cells from adult rat hippocampus. J Neurosci. 1999;19:5245–5254
  63. Tatebayashi Y, Lee MH, Li L, Iqbal K, Grundke-Iqbal I. The dentate gyrus neurogenesis: a therapeutic target for Alzheimer disease. Acta Neuropathol (Berl). 2003;105:225–232
  64. Tham A, Nordberg A, Grissom FE, Carlsson-Skwirut C, Viitanen M, Sara VR. Insulin-like growth factors and insulin-like growth factor binding proteins in cerebrospinal fluid and serum of patients with dementia of the Alzheimer type. J Neural Transm Park Dis Dement Sect. 1993;5:165–176
  65. Vanhala R, Turpeinen U, Riikonen R. Low levels of insulin-like growth factor-I in cerebrospinal fluid in children with autism. Dev Med Child Neurol. 2001;43:614–616
  66. Yasuhara T, Shingo T, Muraoka K, Kobayashi K, Takeuchi A, Yano A, et al. Early transplantation of an encapsulated glial cell line-derived neurotrophic factor-producing cell demonstrating strong neuroprotective effects in a rat model of Parkinsonism disease. J Neurosurg. 2005;102:80–89
  67. Ye J, Cao L, Cui R, Huang A, Yan Z, Lu C, et al. The effects of ciliary neurotrophic factor on neurological function and glial activity following contusive spinal cord injury in rats. Brain Res. 2004;997:30–39
  68. Zala D, Bensadoun J-C, de Almeida LP, Leavitt BR, Gutekunst CA, Aebischer P, et al. Long-term lentiviral-mediated expression of ciliary neurotrophic factor in the striatum of Huntington's disease transgenic mice. Exp Neurol. 2004;185:26–35

PII: S0197-4580(06)00188-6

doi: 10.1016/j.neurobiolaging.2006.05.036

Neurobiology of Aging
Volume 28, Issue 8 , Pages 1148-1162 , August 2007