Fibroblast growth factors in neurodevelopment and psychopathology

Neuroscientist

Volumn 19, Issue 5, 2013, Pages 479-494

  Terwisscha Van Scheltinga, Afke F ^a   Bakker, Steven C ^a   Kahn, René S ^a   Kas, Martien J H ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

behavior; brain; development; gliogenesis; growth factor; mood disorder; neurogenesis; neurotrophic; psychopathology; schizophrenia

Indexed keywords

ANTIDEPRESSANT AGENT; DOPAMINE 2 RECEPTOR; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; NEUROLEPTIC AGENT;

ANXIETY; BEHAVIOR; BRAIN DEVELOPMENT; BRAIN SIZE; CHRONIC STRESS; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; ENTORHINAL CORTEX; ENVIRONMENTAL FACTOR; FRONTAL CORTEX; GLIA; HIPPOCAMPUS; HUMAN; HYPERACTIVITY; MENTAL DISEASE; NERVE CELL DIFFERENTIATION; NONHUMAN; PARKINSON DISEASE; PREFRONTAL CORTEX; PRENATAL STRESS; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SCHIZOPHRENIA; SLEEP TIME; SOCIAL BEHAVIOR; TELENCEPHALON; TREATMENT RESPONSE; VENTRAL TEGMENTUM; WORKING MEMORY;

BEHAVIOR; BRAIN; DEVELOPMENT; GLIOGENESIS; GROWTH FACTOR; MOOD DISORDER; NEUROGENESIS; NEUROTROPHIC; PSYCHOPATHOLOGY; SCHIZOPHRENIA;

ANIMALS; BRAIN; ENVIRONMENT; FIBROBLAST GROWTH FACTORS; HUMANS; NEUROGLIA; NEURONS; PSYCHOPATHOLOGY;

EID: 84883711580     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858412472399     Document Type: Review

References (97)

1. Aguilar LC, Islas A, Rosique P, Hernandez B, Portillo E, Herrera JM. Psychometric analysis in children with mental retardation due to perinatal hypoxia treated with fibroblast growth factor (FGF) and showing improvement in mental development. J Intellect Disabil Res. 1993 ; 37 (1). 507-20
2. Bansal R. Fibroblast growth factors and their receptors in oligodendrocyte development: implications for demyelination and remyelination. Dev Neurosci. 2002 ; 24 (1). 35-46
3. Beenken A, Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov. 2009 ; 8 (3). 235-53
4. Bellon A, Krebs MO, Jay TM. Factoring neurotrophins into a neurite-based pathophysiological model of schizophrenia. Prog Neurobiol. 2011 ; 94 (1). 77-90
5. Bernstein HG, Steiner J, Bogerts B. Glial cells in schizophrenia: pathophysiological significance and possible consequences for therapy. Expert Rev Neurother. 2009 ; 9 (7). 1059-71
6. Bland ST, Tamlyn JP, Barrientos RM, Greenwood BN, Watkins LR, Campeau S. Expression of fibroblast growth factor-2 and brain-derived neurotrophic factor mRNA in the medial prefrontal cortex and hippocampus after uncontrollable or controllable stress. Neuroscience. 2007 ; 144 (4). 1219-28
7. Borroto-Escuela DO, Romero-Fernandez W, Mudo G, Perez-Alea M, Ciruela F, Tarakanov AO. Fibroblast growth factor receptor 1- 5-hydroxytryptamine 1A heteroreceptor complexes and their enhancement of hippocampal plasticity. Biol Psychiatry. 2012 ; 71 (1). 84-91
8. Brandon NJ, Sawa A. Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci. 2011 ; 12 (12). 707-22
9. Brown RE, Stevens DR, Haas HL. The physiology of brain histamine. Prog Neurobiol. 2001 ; 63 (6). 637-72
10. Brunskill EW, Ehrman LA, Williams MT, Klanke J, Hammer D, Schaefer TL. Abnormal neurodevelopment, neurosignaling and behaviour in Npas3-deficient mice. Eur J Neurosci. 2005 ; 22 (6). 1265-76
11. Cannon M, Jones PB, Murray RM. Obstetric complications and schizophrenia: historical and meta-analytic review. Am J Psychiatry. 2002 ; 159 (7). 1080-92
12. Carlsson A, Waters N, Holm-Waters S, Tedroff J, Nilsson M, Carlsson ML. Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annu Rev Pharmacol Toxicol. 2001 ; 41: 237-60
13. Cholfin JA, Rubenstein JL. Patterning of frontal cortex subdivisions by Fgf17. Proc Natl Acad Sci U S A. 2007 ; 104 (18). 7652-7
14. Clinton SM, Turner CA, Flagel SB, Simpson DN, Watson SJ, Akil H. Neonatal fibroblast growth factor treatment enhances cocaine sensitization. Pharmacol Biochem Behav. 2012 ; 103 (1). 6-17
15. Comeau WL, Hastings E, Kolb B. Pre- and postnatal FGF-2 both facilitate recovery and alter cortical morphology following early medial prefrontal cortical injury. Behav Brain Res. 2007 ; 180 (1). 18-27
16. Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, Hallet MJ. Neuron number and size in prefrontal cortex of children with autism. JAMA. 2011 ; 306 (18). 2001-10
17. Dono R. Fibroblast growth factors as regulators of central nervous system development and function. Am J Physiol Regul Integr Comp Physiol. 2003 ; 284 (4). R867-81
18. Dono R, Texido G, Dussel R, Ehmke H, Zeller R. Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J. 1998 ; 17 (15). 4213-25
19. Eisch AJ, Petrik D. Depression and hippocampal neurogenesis: a road to remission?. Science. 2012 ; 338 (6103). 72-5
20. Elsayed M, Banasr M, Duric V, Fournier NM, Licznerski P, Duman RS. Antidepressant effects of fibroblast growth factor-2 in behavioral and cellular models of depression. Biol Psychiatry. 2012 ; 72 (4). 258-65
21. Eren-Kocak E, Turner CA, Watson SJ, Akil H. Short-hairpin RNA silencing of endogenous fibroblast growth factor 2 in rat hippocampus increases anxiety behavior. Biol Psychiatry. 2011 ; 69 (6). 534-40
22. Fadda P, Bedogni F, Fresu A, Collu M, Racagni G, Riva MA. Reduction of corticostriatal glutamatergic fibers in basic fibroblast growth factor deficient mice is associated with hyperactivity and enhanced dopaminergic transmission. Biol Psychiatry. 2007 ; 62 (3). 235-42
23. Fagel DM, Ganat Y, Cheng E, Silbereis J, Ohkubo Y, Ment LR. Fgfr1 is required for cortical regeneration and repair after perinatal hypoxia. J Neurosci. 2009 ; 29 (4). 1202-11
24. Favalli G, Li J, Belmonte-de-Abreu P, Wong AH, Daskalakis ZJ. The role of BDNF in the pathophysiology and treatment of schizophrenia. J Psychiatr Res. 2012 ; 46 (1). 1-11
25. Ferrada C, Ferre S, Casado V, Cortes A, Justinova Z, Barnes C. Interactions between histamine H3 and dopamine D2 receptors and the implications for striatal function. Neuropharmacology. 2008 ; 55 (2). 190-7
26. Flajolet M, Wang Z, Futter M, Shen W, Nuangchamnong N, Bendor J. FGF acts as a co-transmitter through adenosine A(2A) receptor to regulate synaptic plasticity. Nat Neurosci. 2008 ; 11 (12). 1402-9
27. Flores C, Stewart J. Changes in astrocytic basic fibroblast growth factor expression during and after prolonged exposure to escalating doses of amphetamine. Neuroscience. 2000 ; 98 (2). 287-93
28. Fortin D, Rom E, Sun H, Yayon A, Bansal R. Distinct fibroblast growth factor (FGF)/FGF receptor signaling pairs initiate diverse cellular responses in the oligodendrocyte lineage. J Neurosci. 2005 ; 25 (32). 7470-9
29. Frank MG, Der-Avakian A, Bland ST, Watkins LR, Maier SF. Stress-induced glucocorticoids suppress the antisense molecular regulation of FGF-2 expression. Psychoneuroendocrinology. 2007 ; 32 (4). 376-384
30. Fumagalli F, Bedogni F, Slotkin TA, Racagni G, Riva MA. Prenatal stress elicits regionally selective changes in basal FGF-2 gene expression in adulthood and alters the adult response to acute or chronic stress. Neurobiol Dis. 2005 ; 20 (3). 731-7
31. Ganat Y, Soni S, Chacon M, Schwartz ML, Vaccarino FM. Chronic hypoxia up-regulates fibroblast growth factor ligands in the perinatal brain and induces fibroblast growth factor-responsive radial glial cells in the subependymal zone. Neuroscience. 2002 ; 112 (4). 977-991
32. Gaughran F, Payne J, Sedgwick PM, Cotter D, Berry M. Hippocampal FGF-2 and FGFR1 mRNA expression in major depression, schizophrenia and bipolar disorder. Brain Res Bull. 2006 ; 70 (3). 221-7
33. Grothe C, Timmer M. The physiological and pharmacological role of basic fibroblast growth factor in the dopaminergic nigrostriatal system. Brain Res Rev. 2007 ; 54 (1). 80-91
34. Haijma SV, Van Haren N, Cahn W, Koolschijn PC, Hulshoff Pol HE, Kahn RS. Brain volumes in schizophrenia: a meta-analysis in over 18 000 subjects. Schizophr Bull Oct 5. 2012 ;:
35. Hansen SM, Berezin V, Bock E. Signaling mechanisms of neurite outgrowth induced by the cell adhesion molecules NCAM and N-cadherin. Cell Mol Life Sci. 2008 ; 65 (23). 3809-21
36. Hashimoto K, Shimizu E, Komatsu N, Nakazato M, Okamura N, Watanabe H. Increased levels of serum basic fibroblast growth factor in schizophrenia. Psychiatry Res. 2003 ; 120 (3). 211-8
37. Itoh N, Ornitz DM. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem. 2011 ; 149 (2). 121-30
38. Iwata T, Hevner RF. Fibroblast growth factor signaling in development of the cerebral cortex. Dev Growth Differ. 2009 ; 51 (3). 299-323
39. Jarosik J, Legutko B, Werner S, Unsicker K, von Bohlen Und Halbach O. Roles of exogenous and endogenous FGF-2 in animal models of depression. Restor Neurol Neurosci. 2011 ; 29 (3). 153-65
40. Kaga Y, Shoemaker WJ, Furusho M, Bryant M, Rosenbluth J, Pfeiffer SE. Mice with conditional inactivation of fibroblast growth factor receptor-2 signaling in oligodendrocytes have normal myelin but display dramatic hyperactivity when combined with Cnp1 inactivation. J Neurosci. 2006 ; 26 (47). 12339-50
41. Kamnasaran D, Muir WJ, Ferguson-Smith MA, Cox DW. Disruption of the neuronal PAS3 gene in a family affected with schizophrenia. J Med Genet. 2003 ; 40 (5). 325-32
42. Kan SH, Elanko N, Johnson D, Cornejo-Roldan L, Cook J, Reich EW. Genomic screening of fibroblast growth-factor receptor 2 reveals a wide spectrum of mutations in patients with syndromic craniosynostosis. Am J Hum Genet. 2002 ; 70 (2). 472-86
43. Kato M, Okugawa G, Wakeno M, Takekita Y, Nonen S, Tetsuo S. Effect of basic fibroblast growth factor (FGF2) gene polymorphisms on SSRIs treatment response and side effects. Eur Neuropsychopharmacol. 2009 ; 19 (10). 718-25
44. Katsel P, Davis KL, Gorman JM, Haroutunian V. Variations in differential gene expression patterns across multiple brain regions in schizophrenia. Schizophr Res. 2005 ; 77 (2-3). 241-52
45. Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008 ; 65 (2). 146-52
46. Kiyota T, Ingraham KL, Jacobsen MT, Xiong H, Ikezu T. FGF2 gene transfer restores hippocampal functions in mouse models of Alzheimer's disease and has therapeutic implications for neurocognitive disorders. Proc Natl Acad Sci U S A. 2011 ; 108 (49). E1339-48
47. Klejbor I, Kucinski A, Wersinger SR, Corso T, Spodnik JH, Dziewiatkowski J. Serotonergic hyperinnervation and effective serotonin blockade in an FGF receptor developmental model of psychosis. Schizophr Res. 2009 ; 113 (2-3). 308-21
48. Klejbor I, Myers JM, Hausknecht K, Corso TD, Gambino AS, Morys J. Fibroblast growth factor receptor signaling affects development and function of dopamine neurons - inhibition results in a schizophrenia-like syndrome in transgenic mice. J Neurochem. 2006 ; 97 (5). 1243-58
49. Korada S, Zheng W, Basilico C, Schwartz ML, Vaccarino FM. Fibroblast growth factor 2 is necessary for the growth of glutamate projection neurons in the anterior neocortex. J Neurosci. 2002 ; 22 (3). 863-75
50. Krejci P, Prochazkova J, Bryja V, Kozubik A, Wilcox WR. Molecular pathology of the fibroblast growth factor family. Hum Mutat. 2009 ; 30 (9). 1245-55
51. Li AJ, Suzuki S, Suzuki M, Mizukoshi E, Imamura T. Fibroblast growth factor-2 increases functional excitatory synapses on hippocampal neurons. Eur J Neurosci. 2002 ; 16 (7). 1313-24
52. Ma YP, Ma MM, Cheng SM, Ma HH, Yi XM, Xu GL. Intranasal bFGF-induced progenitor cell proliferation and neuroprotection after transient focal cerebral ischemia. Neurosci Lett. 2008 ; 437 (2). 93-7
53. MacDonald AW, Schulz SC. What we know: findings that every theory of schizophrenia should explain. Schizophr Bull. 2009 ; 35 (3). 493-508
54. Marin O. Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci. 2012 ; 13 (2). 107-20
55. Mason I. Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat Rev Neurosci. 2007 ; 8 (8). 583-96
56. Minassian A, Henry BL, Geyer MA, Paulus MP, Young JW, Perry W. The quantitative assessment of motor activity in mania and schizophrenia. J Affect Disord. 2010 ; 120 (1-3). 200-6
57. Moises HW, Zoega T, Gottesman II. The glial growth factors deficiency and synaptic destabilization hypothesis of schizophrenia. BMC Psychiatry. 2002 ; 2 (8). 1-14
58. Molteni R, Fumagalli F, Magnaghi V, Roceri M, Gennarelli M, Racagni G. Modulation of fibroblast growth factor-2 by stress and corticosteroids: from developmental events to adult brain plasticity. Brain Res Brain Res Rev. 2001 ; 37 (1-3). 249-58
59. Muller Smith K, Fagel DM, Stevens HE, Rabenstein RL, Maragnoli ME, Ohkubo Y. Deficiency in inhibitory cortical interneurons associates with hyperactivity in fibroblast growth factor receptor 1 mutant mice. Biol Psychiatry. 2008 ; 63 (10). 953-62
60. Norton WH, Stumpenhorst K, Faus-Kessler T, Folchert A, Rohner N, Harris MP. Modulation of Fgfr1a signaling in zebrafish reveals a genetic basis for the aggression-boldness syndrome. J Neurosci. 2011 ; 31 (39). 13796-807
61. O'Donovan MC, Norton N, Williams H, Peirce T, Moskvina V, Nikolov I. Analysis of 10 independent samples provides evidence for association between schizophrenia and a SNP flanking fibroblast growth factor receptor 2. Mol Psychiatry. 2009 ; 14 (1). 30-6
62. 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 (27). 6057-69
63. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C. Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci U S A. 1998 ; 95 (10). 5672-7
64. Perez JA, Clinton SM, Turner CA, Watson SJ, Akil H. A new role for FGF2 as an endogenous inhibitor of anxiety. J Neurosci. 2009 ; 29 (19). 6379-87
65. Pieper AA, Wu X, Han TW, Estill SJ, Dang Q, Wu LC. The neuronal PAS domain protein 3 transcription factor controls FGF-mediated adult hippocampal neurogenesis in mice. Proc Natl Acad Sci U S A. 2005 ; 102 (39). 14052-7
66. Polanska UM, Fernig DG, Kinnunen T. Extracellular interactome of the FGF receptor-ligand system: complexities and the relative simplicity of the worm. Dev Dyn. 2009 ; 238 (2). 277-93
67. Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM. Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci. 2000 ; 20 (13). 5012-23
68. Ratzka A, Baron O, Grothe C. FGF-2 deficiency does not influence FGF ligand and receptor expression during development of the nigrostriatal system. PLoS One. 2011 ; 6 (8). e23564
69. Ratzka A, Baron O, Stachowiak MK, Grothe C. Fibroblast growth factor 2 regulates dopaminergic neuron development in vivo. J Neurochem. 2012 ; 122 (1). 94-105
70. Reuss B, von Bohlen und Halbach O. Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res. 2003 ; 313 (2). 139-57
71. Riva MA, Molteni R, Bedogni F, Racagni G, Fumagalli F. Emerging role of the FGF system in psychiatric disorders. Trends Pharmacol Sci. 2005 ; 26 (5). 228-31
72. Scearce-Levie K, Roberson ED, Gerstein H, Cholfin JA, Mandiyan VS, Shah NM. Abnormal social behaviors in mice lacking Fgf17. Genes Brain Behav. 2008 ; 7 (3). 344-54
73. Shamir A, Kwon OB, Karavanova I, Vullhorst D, Leiva-Salcedo E, Janssen MJ. The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J Neurosci. 2012 ; 32 (9). 2988-97
74. Shi Y, Li Z, Xu Q, Wang T, Li T, Shen J. Common variants on 8p12 and 1q24.2 confer risk of schizophrenia. ; 2011 ; 2011. 1224.
75. Shin DM, Korada S, Raballo R, Shashikant CS, Simeone A, Taylor JT. Loss of glutamatergic pyramidal neurons in frontal and temporal cortex resulting from attenuation of FGFR1 signaling is associated with spontaneous hyperactivity in mice. J Neurosci. 2004 ; 24 (9). 2247-58
76. Smith KM, Maragnoli ME, Phull PM, Tran KM, Vaccarino FM. Fibroblast growth factor receptor 1 (FGFR1) participates in post-natal interneuron development. Int J Dev Neurosci. 2010 ; 28: 698
77. Stevens HE, Jiang GY, Schwartz ML, Vaccarino FM. Learning and memory depend on fibroblast growth factor receptor 2 functioning in hippocampus. Biol Psychiatry. 2012 ; 71 (12). 1090-8
78. Stevens HE, Smith KM, Maragnoli ME, Fagel D, Borok E, Shanabrough M. Fgfr2 is required for the development of the medial prefrontal cortex and its connections with limbic circuits. J Neurosci. 2010a ; 30 (16). 5590-602
79. Stevens HE, Smith KM, Rash BG, Vaccarino FM. Neural stem cell regulation, fibroblast growth factors, and the developmental origins of neuropsychiatric disorders. Front Neurosci. 2010b ;: 4
80. Szebenyi G, Fallon JF. Fibroblast growth factors as multifunctional signaling factors. Int Rev Cytol. 1999 ; 185: 45-106
81. Terwisscha van Scheltinga AF, Bakker SC, Kahn RS. Fibroblast growth factors in schizophrenia. Schizophr Bull. 2009 ; 36 (6). 1157-66
82. Timmer M, Cesnulevicius K, Winkler C, Kolb J, Lipokatic-Takacs E, Jungnickel J. Fibroblast growth factor (FGF)-2 and FGF receptor 3 are required for the development of the substantia nigra, and FGF-2 plays a crucial role for the rescue of dopaminergic neurons after 6-hydroxydopamine lesion. J Neurosci. 2007 ; 27 (3). 459-71
83. Turner CA, Akil H, Watson SJ, Evans SJ. The fibroblast growth factor system and mood disorders. Biol Psychiatry. 2006 ; 59 (12). 1128-35
84. Turner CA, Calvo N, Frost DO, Akil H, Watson SJ. The fibroblast growth factor system is downregulated following social defeat. Neurosci Lett. 2008a ; 430 (2). 147-50
85. Turner CA, Capriles N, Flagel SB, Perez JA, Clinton SM, Watson SJ. Neonatal FGF2 alters cocaine self-administration in the adult rat. Pharmacol Biochem Behav. 2009 ; 92 (1). 100-4
86. Turner CA, Clinton SM, Thompson RC, Watson SJ, Akil H. Fibroblast growth factor-2 (FGF2) augmentation early in life alters hippocampal development and rescues the anxiety phenotype in vulnerable animals. Proc Natl Acad Sci U S A. 2011 ; 108 (19). 8021-5
87. Turner CA, Gula EL, Taylor LP, Watson SJ, Akil H. Antidepressant-like effects of intracerebroventricular FGF2 in rats. Brain Res. 2008b ; 1224 (1). 63-8
88. Turner CA, Watson SJ, Akil H. The fibroblast growth factor family: neuromodulation of affective behavior. Neuron. 2012 ; 76 (1). 160-74
89. Vaccarino FM, Grigorenko EL, Smith KM, Stevens HE. Regulation of cerebral cortical size and neuron number by fibroblast growth factors: implications for autism. J Autism Dev Disord. 2008 ; 39 (3). 511-20
90. Volk DW, Lewis DA. Prefrontal cortical circuits in schizophrenia. Curr Top Behav Neurosci. 2010 ; 4 (1). 485-508
91. Wang T, Zeng Z, Hu Z, Zheng L, Li T, Li Y. FGFR2 is associated with bipolar disorder: a large-scale case-control study of three psychiatric disorders in the Chinese Han population. World J Biol Psychiatry. 2012 ; 13 (8). 599-604
92. Wu D. Neuroprotection in experimental stroke with targeted neurotrophins. NeuroRx. 2005 ; 2 (1). 120-8
93. Yamaguchi Y. Heparan sulfate proteoglycans in the nervous system: their diverse roles in neurogenesis, axon guidance, and synaptogenesis. Semin Cell Dev Biol. 2001 ; 12 (2). 99-106
94. Zechel S, Jarosik J, Kiprianova I, Schober A, Unsicker K, von Bohlen und Halbach O. FGF-2 deficiency does not alter vulnerability of the dopaminergic nigrostriatal system towards MPTP intoxication in mice. Eur J Neurosci. 2006 ; 23 (6). 1671-5
95. Zechel S, Werner S, Unsicker K, von Bohlen und Halbach O. Expression and functions of fibroblast growth factor 2 (FGF-2) in hippocampal formation. Neuroscientist. 2010 ; 16 (4). 357-73
96. Zhao M, Li D, Shimazu K, Zhou YX, Lu B, Deng CX. Fibroblast growth factor receptor-1 is required for long-term potentiation, memory consolidation, and neurogenesis. Biol Psychiatry. 2007 ; 62 (5). 381-90
97. Zhou M, Sutliff RL, Paul RJ, Lorenz JN, Hoying JB, Haudenschild CC. Fibroblast growth factor 2 control of vascular tone. Nat Med. 1998 ; 4 (2). 201-7