The Fibroblast Growth Factor Family: Neuromodulation of Affective Behavior

Neuron

Volumn 76, Issue 1, 2012, Pages 160-174

  Turner, Cortney A ^a   Watson, Stanley J ^a,b   Akil, Huda ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3;

ADULTHOOD; AFFECT; ANXIETY; BRAIN FUNCTION; CONDITIONING; DEPRESSION; DRUG DEPENDENCE; EMOTIONALITY; FEAR; GENE EXPRESSION; GENE SWITCHING; GENETIC PREDISPOSITION; HUMAN; LIFESPAN; LIGAND BINDING; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; MOOD DISORDER; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REGULATOR GENE; REVIEW; SIGNAL TRANSDUCTION; STRESS;

ANIMALS; BRAIN; FIBROBLAST GROWTH FACTORS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MOOD DISORDERS; NEUROTRANSMITTER AGENTS;

EID: 84867136639     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.08.037     Document Type: Review

References (155)

1. Akil H. Stressed and depressed. Nat. Med. 2005, 11:116-118.
2. Alam K.Y., Frostholm A., Hackshaw K.V., Evans J.E., Rotter A., Chiu I.M. Characterization of the 1B promoter of fibroblast growth factor 1 and its expression in the adult and developing mouse brain. J. Biol. Chem. 1996, 271:30263-30271.
3. Anderson M.F., Aberg M.A., Nilsson M., Eriksson P.S. Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res. Dev. Brain Res. 2002, 134:115-122.
4. Aonurm-Helm A., Jurgenson M., Zharkovsky T., Sonn K., Berezin V., Bock E., Zharkovsky A. Depression-like behaviour in neural cell adhesion molecule (NCAM)-deficient mice and its reversal by an NCAM-derived peptide, FGL. Eur. J. Neurosci. 2008, 28:1618-1628.
5. Aonurm-Helm A., Berezin V., Bock E., Zharkovsky A. NCAM-mimetic, FGL peptide, restores disrupted fibroblast growth factor receptor (FGFR) phosphorylation and FGFR mediated signaling in neural cell adhesion molecule (NCAM)-deficient mice. Brain Res. 2010, 1309:1-8.
6. Aston C., Jiang L., Sokolov B.P. Transcriptional profiling reveals evidence for signaling and oligodendroglial abnormalities in the temporal cortex from patients with major depressive disorder. Mol. Psychiatry 2005, 10:309-322.
7. Atz M.E., Rollins B., Vawter M.P. NCAM1 association study of bipolar disorder and schizophrenia: polymorphisms and alternatively spliced isoforms lead to similarities and differences. Psychiatr. Genet. 2007, 17:55-67.
8. Audigier S., Guiramand J., Prado-Lourenco L., Conte C., Gonzalez-Herrera I.G., Cohen-Solal C., Récasens M., Prats A.C. Potent activation of FGF-2 IRES-dependent mechanism of translation during brain development. RNA 2008, 14:1852-1864.
9. Bartlett P.F., Dutton R., Likiardopoulos V., Brooker G. Regulation of neurogenesis in the embryonic and adult brain by fibroblast growth factors. Alcohol Alcohol. Suppl. 1994, 2:387-394.
10. Bernard R., Kerman I.A., Thompson R.C., Jones E.G., Bunney W.E., Barchas J.D., Schatzberg A.F., Myers R.M., Akil H., Watson S.J. Altered expression of glutamate signaling, growth factor, and glia genes in the locus coeruleus of patients with major depression. Mol. Psychiatry 2011, 16:634-646.
11. Berton O., McClung C.A., Dileone R.J., Krishnan V., Renthal W., Russo S.J., Graham D., Tsankova N.M., Bolanos C.A., Rios M., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006, 311:864-868.
12. Bisaz R., Schachner M., Sandi C. Causal evidence for the involvement of the neural cell adhesion molecule, NCAM, in chronic stress-induced cognitive impairments. Hippocampus 2011, 21:56-71.
13. Bland S.T., Schmid M.J., Greenwood B.N., Watkins L.R., Maier S.F. Behavioral control of the stressor modulates stress-induced changes in neurogenesis and fibroblast growth factor-2. Neuroreport 2006, 17:593-597.
14. Bland S.T., Tamlyn J.P., Barrientos R.M., Greenwood B.N., Watkins L.R., Campeau S., Day H.E., Maier S.F. 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, 144:1219-1228.
15. Blier P., Abbott F.V. Putative mechanisms of action of antidepressant drugs in affective and anxiety disorders and pain. J. Psychiatry Neurosci. 2001, 26:37-43.
16. Blier P., Ward N.M. Is there a role for 5-HT1A agonists in the treatment of depression?. Biol. Psychiatry 2003, 53:193-203.
17. Borcel E., Perez-Alvarez L., Herrero A.I., Brionne T., Varea E., Berezin V., Bock E., Sandi C., Venero C. Chronic stress in adulthood followed by intermittent stress impairs spatial memory and the survival of newborn hippocampal cells in aging animals: prevention by FGL, a peptide mimetic of neural cell adhesion molecule. Behav. Pharmacol. 2008, 19:41-49.
18. Borroto-Escuela D.O., Romero-Fernandez W., Mudó G., Pérez-Alea M., Ciruela F., Tarakanov A.O., Narvaez M., Di Liberto V., Agnati L.F., Belluardo N., Fuxe K. Fibroblast growth factor receptor 1- 5-hydroxytryptamine 1A heteroreceptor complexes and their enhancement of hippocampal plasticity. Biol. Psychiatry 2012, 71:84-91.
19. Borroto-Escuela D.O., Romero-Fernandez W., Pérez-Alea M., Narvaez M., Tarakanov A.O., Mudó G., Agnati L.F., Ciruela F., Belluardo N., Fuxe K. The existence of FGFR1-5-HT1A receptor heterocomplexes in midbrain 5-HT neurons of the rat: relevance for neuroplasticity. J. Neurosci. 2012, 32:6295-6303.
20. Cambon K., Hansen S.M., Venero C., Herrero A.I., Skibo G., Berezin V., Bock E., Sandi C. A synthetic neural cell adhesion molecule mimetic peptide promotes synaptogenesis, enhances presynaptic function, and facilitates memory consolidation. J. Neurosci. 2004, 24:4197-4204.
21. Campbell S., Marriott M., Nahmias C., MacQueen G.M. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am. J. Psychiatry 2004, 161:598-607.
22. Carafoli F., Saffell J.L., Hohenester E. Structure of the tandem fibronectin type 3 domains of neural cell adhesion molecule. J. Mol. Biol. 2008, 377:524-534.
23. Chadi G., Rosén L., Cintra A., Tinner B., Zoli M., Pettersson R.F., Fuxe K. Corticosterone increases FGF-2 (bFGF) immunoreactivity in the substantia nigra of the rat. Neuroreport 1993, 4:783-786.
24. Cheng Y., Tao Y., Black I.B., DiCicco-Bloom E. A single peripheral injection of basic fibroblast growth factor (bFGF) stimulates granule cell production and increases cerebellar growth in newborn rats. J. Neurobiol. 2001, 46:220-229.
25. Choudary P.V., Molnar M., Evans S.J., Tomita H., Li J.Z., Vawter M.P., Myers R.M., Bunney W.E., Akil H., Watson S.J., Jones E.G. Altered cortical glutamatergic and GABAergic signal transmission with glial involvement in depression. Proc. Natl. Acad. Sci. USA 2005, 102:15653-15658.
26. Christensen C., Lauridsen J.B., Berezin V., Bock E., Kiselyov V.V. The neural cell adhesion molecule binds to fibroblast growth factor receptor 2. FEBS Lett. 2006, 580:3386-3390.
27. Cinaroglu A., Ozmen Y., Ozdemir A., Ozcan F., Ergorul C., Cayirlioglu P., Hicks D., Bugra K. Expression and possible function of fibroblast growth factor 9 (FGF9) and its cognate receptors FGFR2 and FGFR3 in postnatal and adult retina. J. Neurosci. Res. 2005, 79:329-339.
28. Clinton S.M., Turner C.A., Flagel S.B., Simpson D.N., Watson S.J., Akil H. Neonatal fibroblast growth factor treatment enhances cocaine sensitization. Pharmacol. Biochem. Behav. 2012, 103:6-17.
29. Conboy L., Bisaz R., Markram K., Sandi C. Role of NCAM in emotion and learning. Adv. Exp. Med. Biol. 2010, 663:271-296.
30. Cordero M.I., Rodríguez J.J., Davies H.A., Peddie C.J., Sandi C., Stewart M.G. Chronic restraint stress down-regulates amygdaloid expression of polysialylated neural cell adhesion molecule. Neuroscience 2005, 133:903-910.
31. Ditlevsen D.K., Owczarek S., Berezin V., Bock E. Relative role of upstream regulators of Akt, ERK and CREB in NCAM- and FGF2-mediated signalling. Neurochem. Int. 2008, 53:137-147.
32. 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, 17:4213-4225.
33. Duman R.S. Novel therapeutic approaches beyond the serotonin receptor. Biol. Psychiatry 1998, 44:324-335.
34. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 2006, 59:1116-1127.
35. Duman R.S., Heninger G.R., Nestler E.J. A molecular and cellular theory of depression. Arch. Gen. Psychiatry 1997, 54:597-606.
36. Elde R., Cao Y.H., Cintra A., Brelje T.C., Pelto-Huikko M., Junttila T., Fuxe K., Pettersson R.F., Hökfelt T. Prominent expression of acidic fibroblast growth factor in motor and sensory neurons. Neuron 1991, 7:349-364.
37. Elsayed M., Banasr M., Duric V., Fournier N.M., Licznerski P., Duman R.S. Antidepressant effects of fibroblast growth factor-2 in behavioral and cellular models of depression. Biol. Psychiatry 2012, 72:258-265.
38. Erabi K., Morinobu S., Kawano K., Tsuji S., Yamawaki S. Neonatal isolation changes the expression of IGF-IR and IGFBP-2 in the hippocampus in response to adulthood restraint stress. Int. J. Neuropsychopharmacol. 2007, 10:369-381.
39. Eren-Koçak E., Turner C.A., Watson S.J., Akil H. Short-hairpin RNA silencing of endogenous fibroblast growth factor 2 in rat hippocampus increases anxiety behavior. Biol. Psychiatry 2011, 69:534-540.
40. Evans S.J., Choudary P.V., Neal C.R., Li J.Z., Vawter M.P., Tomita H., Lopez J.F., Thompson R.C., Meng F., Stead J.D., et al. Dysregulation of the fibroblast growth factor system in major depression. Proc. Natl. Acad. Sci. USA 2004, 101:15506-15511.
41. Flagel S.B., Watson S.J., Akil H., Robinson T.E. Individual differences in the attribution of incentive salience to a reward-related cue: influence on cocaine sensitization. Behav. Brain Res. 2008, 186:48-56.
42. Flagel S.B., Akil H., Robinson T.E. Individual differences in the attribution of incentive salience to reward-related cues: Implications for addiction. Neuropharmacology 2009, 56(Suppl 1):139-148.
43. Flagel S.B., Robinson T.E., Clark J.J., Clinton S.M., Watson S.J., Seeman P., Phillips P.E., Akil H. An animal model of genetic vulnerability to behavioral disinhibition and responsiveness to reward-related cues: implications for addiction. Neuropsychopharmacology 2010, 35:388-400.
44. Flajolet M., Wang Z., Futter M., Shen W., Nuangchamnong N., Bendor J., Wallach I., Nairn A.C., Surmeier D.J., Greengard P. FGF acts as a co-transmitter through adenosine A(2A) receptor to regulate synaptic plasticity. Nat. Neurosci. 2008, 11:1402-1409.
45. Flores C., Stewart J. Changes in astrocytic basic fibroblast growth factor expression during and after prolonged exposure to escalating doses of amphetamine. Neuroscience 2000, 98:287-293.
46. Flores C., Rodaros D., Stewart J. Long-lasting induction of astrocytic basic fibroblast growth factor by repeated injections of amphetamine: blockade by concurrent treatment with a glutamate antagonist. J. Neurosci. 1998, 18:9547-9555.
47. Flores C., Samaha A.N., Stewart J. Requirement of endogenous basic fibroblast growth factor for sensitization to amphetamine. J. Neurosci. 2000, 20:RC55.
48. Flores C., Stewart J., Salmaso N., Zhang Y., Boksa P. Astrocytic basic fibroblast growth factor expression in dopaminergic regions after perinatal anoxia. Biol. Psychiatry 2002, 52:362-370.
49. Ford-Perriss M., Abud H., Murphy M. Fibroblast growth factors in the developing central nervous system. Clin. Exp. Pharmacol. Physiol. 2001, 28:493-503.
50. Forget C., Stewart J., Trudeau L.E. Impact of basic FGF expression in astrocytes on dopamine neuron synaptic function and development. Eur. J. Neurosci. 2006, 23:608-616.
51. Frank M.G., Der-Avakian A., Bland S.T., Watkins L.R., Maier S.F. Stress-induced glucocorticoids suppress the antisense molecular regulation of FGF-2 expression. Psychoneuroendocrinology 2007, 32:376-384.
52. Frinchi M., Bonomo A., Trovato-Salinaro A., Condorelli D.F., Fuxe K., Spampinato M.G., Mudò G. Fibroblast growth factor-2 and its receptor expression in proliferating precursor cells of the subventricular zone in the adult rat brain. Neurosci. Lett. 2008, 447:20-25.
53. Fuchs E., Flügge G. Stress, glucocorticoids and structural plasticity of the hippocampus. Neurosci. Biobehav. Rev. 1998, 23:295-300.
54. Fumagalli F., Bedogni F., Maragnoli M.E., Gennarelli M., Perez J., Racagni G., Riva M.A. Dopaminergic D2 receptor activation modulates FGF-2 gene expression in rat prefrontal cortex and hippocampus. J. Neurosci. Res. 2003, 74:74-80.
55. Fumagalli F., Bedogni F., Slotkin T.A., Racagni G., Riva M.A. 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, 20:731-737.
56. Fumagalli F., Pasquale L., Racagni G., Riva M.A. Dynamic regulation of fibroblast growth factor 2 (FGF-2) gene expression in the rat brain following single and repeated cocaine administration. J. Neurochem. 2006, 96:996-1004.
57. Fumagalli F., Di Pasquale L., Caffino L., Racagni G., Riva M.A. Stress and cocaine interact to modulate basic fibroblast growth factor (FGF-2) expression in rat brain. Psychopharmacology (Berl.) 2008, 196:357-364.
58. Gaughran F., Payne J., Sedgwick P.M., Cotter D., Berry M. Hippocampal FGF-2 and FGFR1 mRNA expression in major depression, schizophrenia and bipolar disorder. Brain Res. Bull. 2006, 70:221-227.
59. Gilbertson M.W., Shenton M.E., Ciszewski A., Kasai K., Lasko N.B., Orr S.P., Pitman R.K. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat. Neurosci. 2002, 5:1242-1247.
60. Goetz R., Dover K., Laezza F., Shtraizent N., Huang X., Tchetchik D., Eliseenkova A.V., Xu C.F., Neubert T.A., Ornitz D.M., et al. Crystal structure of a fibroblast growth factor homologous factor (FHF) defines a conserved surface on FHFs for binding and modulation of voltage-gated sodium channels. J. Biol. Chem. 2009, 284:17883-17896.
61. Goldfarb M., Schoorlemmer J., Williams A., Diwakar S., Wang Q., Huang X., Giza J., Tchetchik D., Kelley K., Vega A., et al. Fibroblast growth factor homologous factors control neuronal excitability through modulation of voltage-gated sodium channels. Neuron 2007, 55:449-463.
62. Gómez-Pinilla F., Lee J.W., Cotman C.W. Distribution of basic fibroblast growth factor in the developing rat brain. Neuroscience 1994, 61:911-923.
63. Gómez-Pinilla F., Dao L., Choi J., Ryba E.A. Diazepam induces FGF-2 mRNA in the hippocampus and striatum. Brain Res. Bull. 2000, 53:283-289.
64. Gonzalez A.M., Berry M., Maher P.A., Logan A., Baird A. A comprehensive analysis of the distribution of FGF-2 and FGFR1 in the rat brain. Brain Res. 1995, 701:201-226.
65. Goodrich S.P., Yan G.C., Bahrenburg K., Mansson P.E. The nucleotide sequence of rat heparin binding growth factor 1 (HBGF-1). Nucleic Acids Res. 1989, 17:2867.
66. Graham B.M., Richardson R. Acute systemic fibroblast growth factor-2 enhances long-term memory in developing rats. Neurobiol. Learn. Mem. 2009, 91:424-430.
67. Graham B.M., Richardson R. Acute systemic fibroblast growth factor-2 enhances long-term extinction of fear and reduces reinstatement in rats. Neuropsychopharmacology 2009, 34:1875-1882.
68. Graham B.M., Richardson R. Early-life exposure to fibroblast growth factor-2 facilitates context-dependent long-term memory in developing rats. Behav. Neurosci. 2010, 124:337-345.
69. Graham B.M., Richardson R. Fibroblast growth factor-2 enhances extinction and reduces renewal of conditioned fear. Neuropsychopharmacology 2010, 35:1348-1355.
70. Graham B.M., Richardson R. Fibroblast growth factor-2 alters the nature of extinction. Learn. Mem. 2011, 18:80-84.
71. Graham B.M., Richardson R. Memory of fearful events: the role of fibroblast growth factor-2 in fear acquisition and extinction. Neuroscience 2011, 189:156-169.
72. Guillemot F., Zimmer C. From cradle to grave: the multiple roles of fibroblast growth factors in neural development. Neuron 2011, 71:574-588.
73. Hanneken A., Ying W., Ling N., Baird A. Identification of soluble forms of the fibroblast growth factor receptor in blood. Proc. Natl. Acad. Sci. USA 1994, 91:9170-9174.
74. Hannon J., Hoyer D. Molecular biology of 5-HT receptors. Behav. Brain Res. 2008, 195:198-213.
75. Hansen S.M., Berezin V., Bock E. Signaling mechanisms of neurite outgrowth induced by the cell adhesion molecules NCAM and N-cadherin. Cell. Mol. Life Sci. 2008, 65:3809-3821.
76. Hoshaw B.A., Malberg J.E., Lucki I. Central administration of IGF-I and BDNF leads to long-lasting antidepressant-like effects. Brain Res. 2005, 1037:204-208.
77. Huang J.Y., Hong Y.T., Chuang J.I. Fibroblast growth factor 9 prevents MPP+-induced death of dopaminergic neurons and is involved in melatonin neuroprotection in vivo and in vitro. J. Neurochem. 2009, 109:1400-1412.
78. Kahl K.G., Bens S., Ziegler K., Rudolf S., Kordon A., Dibbelt L., Schweiger U. Angiogenic factors in patients with current major depressive disorder comorbid with borderline personality disorder. Psychoneuroendocrinology 2009, 34:353-357.
79. Kang H.J., Adams D.H., Simen A., Simen B.B., Rajkowska G., Stockmeier C.A., Overholser J.C., Meltzer H.Y., Jurjus G.J., Konick L.C., et al. Gene expression profiling in postmortem prefrontal cortex of major depressive disorder. J. Neurosci. 2007, 27:13329-13340.
80. Kato M., Okugawa G., Wakeno M., Takekita Y., Nonen S., Tetsuo S., Nishida K., Azuma J., Kinoshita T., Serretti A. Effect of basic fibroblast growth factor (FGF2) gene polymorphisms on SSRIs treatment response and side effects. Eur. Neuropsychopharmacol. 2009, 19:718-725.
81. Kessler R.C., McGonagle K.A., Zhao S., Nelson C.B., Hughes M., Eshleman S., Wittchen H.U., Kendler K.S. Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch. Gen. Psychiatry 1994, 51:8-19.
82. Kiselyov V.V., Soroka V., Berezin V., Bock E. Structural biology of NCAM homophilic binding and activation of FGFR. J. Neurochem. 2005, 94:1169-1179.
83. Knee R., Li A.W., Murphy P.R. Characterization and tissue-specific expression of the rat basic fibroblast growth factor antisense mRNA and protein. Proc. Natl. Acad. Sci. USA 1997, 94:4943-4947.
84. Knüsel B., Hefti F. Multiple and interactive responses of central neurons to neurotrophic factors. Semin. Neurosci. 1993, 5:259-267.
85. Køhler L.B., Christensen C., Rossetti C., Fantin M., Sandi C., Bock E., Berezin V. Dennexin peptides modeled after the homophilic binding sites of the neural cell adhesion molecule (NCAM) promote neuronal survival, modify cell adhesion and impair spatial learning. Eur. J. Cell Biol. 2010, 89:817-827.
86. Kollack-Walker S., Watson S.J., Akil H. Social stress in hamsters: defeat activates specific neurocircuits within the brain. J. Neurosci. 1997, 17:8842-8855.
87. Kollack-Walker S., Don C., Watson S.J., Akil H. Differential expression of c-fos mRNA within neurocircuits of male hamsters exposed to acute or chronic defeat. J. Neuroendocrinol. 1999, 11:547-559.
88. Kraev I., Henneberger C., Rossetti C., Conboy L., Kohler L.B., Fantin M., Jennings A., Venero C., Popov V., Rusakov D., et al. A peptide mimetic targeting trans-homophilic NCAM binding sites promotes spatial learning and neural plasticity in the hippocampus. PLoS ONE 2011, 6:e23433.
89. Krishnan V., Han M.H., Graham D.L., Berton O., Renthal W., Russo S.J., Laplant Q., Graham A., Lutter M., Lagace D.C., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131:391-404.
90. Kurokawa T., Seno M., Igarashi K. Nucleotide sequence of rat basic fibroblast growth factor cDNA. Nucleic Acids Res. 1988, 16:5201.
91. Laezza F., Lampert A., Kozel M.A., Gerber B.R., Rush A.M., Nerbonne J.M., Waxman S.G., Dib-Hajj S.D., Ornitz D.M. FGF14 N-terminal splice variants differentially modulate Nav1.2 and Nav1.6-encoded sodium channels. Mol. Cell. Neurosci. 2009, 42:90-101.
92. Levi-Montalcini R. The nerve growth factor 35 years later. Science 1987, 237:1154-1162.
93. Levi-Montalcini R., Dal Toso R., della Valle F., Skaper S.D., Leon A. Update of the NGF saga. J. Neurol. Sci. 1995, 130:119-127.
94. Li J.Z., Vawter M.P., Walsh D.M., Tomita H., Evans S.J., Choudary P.V., Lopez J.F., Avelar A., Shokoohi V., Chung T., et al. Systematic changes in gene expression in postmortem human brains associated with tissue pH and terminal medical conditions. Hum. Mol. Genet. 2004, 13:609-616.
95. Lu B., Figurov A. Role of neurotrophins in synapse development and plasticity. Rev. Neurosci. 1997, 8:1-12.
96. MacFarlane L.A., Murphy P.R. Regulation of FGF-2 by an endogenous antisense RNA: effects on cell adhesion and cell-cycle progression. Mol. Carcinog. 2010, 49:1031-1044.
97. MacFarlane L.A., Gu Y., Casson A.G., Murphy P.R. Regulation of fibroblast growth factor-2 by an endogenous antisense RNA and by argonaute-2. Mol. Endocrinol. 2010, 24:800-812.
98. Magariños A.M., Verdugo J.M., McEwen B.S. Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl. Acad. Sci. USA 1997, 94:14002-14008.
99. Mallei A., Shi B., Mocchetti I. Antidepressant treatments induce the expression of basic fibroblast growth factor in cortical and hippocampal neurons. Mol. Pharmacol. 2002, 61:1017-1024.
100. Mark R.J., Keller J.N., Kruman I., Mattson M.P. Basic FGF attenuates amyloid beta-peptide-induced oxidative stress, mitochondrial dysfunction, and impairment of Na+/K+-ATPase activity in hippocampal neurons. Brain Res. 1997, 756:205-214.
101. McEwen B.S., Magarinos A.M. Stress effects on morphology and function of the hippocampus. Ann. N Y Acad. Sci. 1997, 821:271-284.
102. Miller D.L., Ortega S., Bashayan O., Basch R., Basilico C. Compensation by fibroblast growth factor 1 (FGF1) does not account for the mild phenotypic defects observed in FGF2 null mice. Mol. Cell. Biol. 2000, 20:2260-2268.
103. Moldrich R.X., Mezzera C., Holmes W.M., Goda S., Brookfield S.J., Rankin A.J., Barr E., Kurniawan N., Dewar D., Richards L.J., et al. Fgfr3 regulates development of the caudal telencephalon. Dev. Dyn. 2011, 240:1586-1599.
104. Molteni R., Fumagalli F., Magnaghi V., Roceri M., Gennarelli M., Racagni G., Melcangi R.C., Riva M.A. Modulation of fibroblast growth factor-2 by stress and corticosteroids: from developmental events to adult brain plasticity. Brain Res. Brain Res. Rev. 2001, 37:249-258.
105. Monteggia L.M., Barrot M., Powell C.M., Berton O., Galanis V., Gemelli T., Meuth S., Nagy A., Greene R.W., Nestler E.J. Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc. Natl. Acad. Sci. USA 2004, 101:10827-10832.
106. Mueller D., Chapman C.A., Stewart J. Amphetamine induces dendritic growth in ventral tegmental area dopaminergic neurons in vivo via basic fibroblast growth factor. Neuroscience 2006, 137:727-735.
107. Nibuya M., Morinobu S., Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci. 1995, 15:7539-7547.
108. Numakawa T., Yamamoto N., Chiba S., Richards M., Ooshima Y., Kishi S., Hashido K., Adachi N., Kunugi H. Growth factors stimulate expression of neuronal and glial miR-132. Neurosci. Lett. 2011, 505:242-247.
109. Ohkubo Y., Uchida A.O., Shin D., Partanen J., Vaccarino F.M. 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.
110. Olsen S.K., Garbi M., Zampieri N., Eliseenkova A.V., Ornitz D.M., Goldfarb M., Mohammadi M. Fibroblast growth factor (FGF) homologous factors share structural but not functional homology with FGFs. J. Biol. Chem. 2003, 278:34226-34236.
111. Palmer T.D., Markakis E.A., Willhoite A.R., Safar F., Gage F.H. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci. 1999, 19:8487-8497.
112. Peeters P.J., Fierens F.L., van den Wyngaert I., Goehlmann H.W., Swagemakers S.M., Kass S.U., Langlois X., Pullan S., Stenzel-Poore M.P., Steckler T. Gene expression profiles highlight adaptive brain mechanisms in corticotropin releasing factor overexpressing mice. Brain Res. Mol. Brain Res. 2004, 129:135-150.
113. Perez J.A., Clinton S.M., Turner C.A., Watson S.J., Akil H. A new role for FGF2 as an endogenous inhibitor of anxiety. J. Neurosci. 2009, 29:6379-6387.
114. Pizarro J.M., Lumley L.A., Medina W., Robison C.L., Chang W.E., Alagappan A., Bah M.J., Dawood M.Y., Shah J.D., Mark B., et al. Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice. Brain Res. 2004, 1025:10-20.
115. Plotnikov A.N., Eliseenkova A.V., Ibrahimi O.A., Shriver Z., Sasisekharan R., Lemmon M.A., Mohammadi M. Crystal structure of fibroblast growth factor 9 reveals regions implicated in dimerization and autoinhibition. J. Biol. Chem. 2001, 276:4322-4329.
116. Raballo R., Rhee J., Lyn-Cook R., Leckman J.F., Schwartz M.L., Vaccarino F.M. Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J. Neurosci. 2000, 20:5012-5023.
117. Reuss B., von Bohlen und Halbach O. Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res. 2003, 313:139-157.
118. Riedel B., Friauf E., Grothe C., Unsicker K. Fibroblast growth factor-2-like immunoreactivity in auditory brainstem nuclei of the developing and adult rat: correlation with onset and loss of hearing. J. Comp. Neurol. 1995, 354:353-360.
119. Robins L.N., Regier D.A. In Psychiatric Disorders in America: the Epidemiologic Catchment Area Study 1991, The Free Press, New York.
120. Roceri M., Molteni R., Fumagalli F., Racagni G., Gennarelli M., Corsini G., Maggio R., Riva M. Stimulatory role of dopamine on fibroblast growth factor-2 expression in rat striatum. J. Neurochem. 2001, 76:990-997.
121. Romero-Fernandez W., Borroto-Escuela D.O., Tarakanov A.O., Mudó G., Narvaez M., Pérez-Alea M., Agnati L.F., Ciruela F., Belluardo N., Fuxe K. Agonist-induced formation of FGFR1 homodimers and signaling differ among members of the FGF family. Biochem. Biophys. Res. Commun. 2011, 409:764-768.
122. Salaria S., Chana G., Caldara F., Feltrin E., Altieri M., Faggioni F., Domenici E., Merlo-Pich E., Everall I.P. Microarray analysis of cultured human brain aggregates following cortisol exposure: implications for cellular functions relevant to mood disorders. Neurobiol. Dis. 2006, 23:630-636.
123. Salmaso N., Vaccarino F.M. Toward a novel endogenous anxiolytic factor, fibroblast growth factor 2. Biol. Psychiatry 2011, 69:508-509.
124. Sanchez-Heras E., Howell F.V., Williams G., Doherty P. The fibroblast growth factor receptor acid box is essential for interactions with N-cadherin and all of the major isoforms of neural cell adhesion molecule. J. Biol. Chem. 2006, 281:35208-35216.
125. Sandi C., Loscertales M. Opposite effects on NCAM expression in the rat frontal cortex induced by acute vs. chronic corticosterone treatments. Brain Res. 1999, 828:127-134.
126. Sandi C., Bisaz R. A model for the involvement of neural cell adhesion molecules in stress-related mood disorders. Neuroendocrinology 2007, 85:158-176.
127. Sandi C., Woodson J.C., Haynes V.F., Park C.R., Touyarot K., Lopez-Fernandez M.A., Venero C., Diamond D.M. Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex. Biol. Psychiatry 2005, 57:856-864.
128. Schmidt H.D., Duman R.S. Peripheral BDNF produces antidepressant-like effects in cellular and behavioral models. Neuropsychopharmacology 2010, 35:2378-2391.
129. Shah C.A., Bei L., Wang H., Platanias L.C., Eklund E.A. HoxA10 protein regulates transcription of gene encoding fibroblast growth factor 2 (FGF2) in myeloid cells. J. Biol. Chem. 2012, 287:18230-18248.
130. Sharp T., Cowen P.J. 5-HT and depression: is the glass half-full?. Curr. Opin. Pharmacol. 2011, 11:45-51.
131. Shibata F., Baird A., Florkiewicz R.Z. Functional characterization of the human basic fibroblast growth factor gene promoter. Growth Factors 1991, 4:277-287.
132. Shin D.M., Korada S., Raballo R., Shashikant C.S., Simeone A., Taylor J.R., Vaccarino F. 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, 24:2247-2258.
133. Snider W.D., Johnson E.M. Neurotrophic molecules. Ann. Neurol. 1989, 26:489-506.
134. Spugnini E.P., Citro G., Fais S. Proton pump inhibitors as anti vacuolar-ATPases drugs: a novel anticancer strategy. J. Exp. Clin. Cancer Res. 2010, 29:44.
135. Stead J.D., Clinton S., Neal C., Schneider J., Jama A., Miller S., Vazquez D.M., Watson S.J., Akil H. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 2006, 36:697-712.
136. Stevens H.E., Smith K.M., Maragnoli M.E., Fagel D., Borok E., Shanabrough M., Horvath T.L., Vaccarino F.M. Fgfr2 is required for the development of the medial prefrontal cortex and its connections with limbic circuits. J. Neurosci. 2010, 30:5590-5602.
137. Stevens H.E., Jiang G.Y., Schwartz M.L., Vaccarino F.M. Learning and memory depend on fibroblast growth factor receptor 2 functioning in hippocampus. Biol. Psychiatry 2012, 71:1090-1098.
138. Tao Y., Black I.B., DiCicco-Bloom E. Neurogenesis in neonatal rat brain is regulated by peripheral injection of basic fibroblast growth factor (bFGF). J. Comp. Neurol. 1996, 376:653-663.
139. Temple S., Qian X. bFGF, neurotrophins, and the control or cortical neurogenesis. Neuron 1995, 15:249-252.
140. Thoenen H. The changing scene of neurotrophic factors. Trends Neurosci. 1991, 14:165-170.
141. Tochigi M., Iwamoto K., Bundo M., Sasaki T., Kato N., Kato T. Gene expression profiling of major depression and suicide in the prefrontal cortex of postmortem brains. Neurosci. Res. 2008, 60:184-191.
142. Turner C.A., Akil H., Watson S.J., Evans S.J. The fibroblast growth factor system and mood disorders. Biol. Psychiatry 2006, 59:1128-1135.
143. Turner C.A., Calvo N., Frost D.O., Akil H., Watson S.J. The fibroblast growth factor system is downregulated following social defeat. Neurosci. Lett. 2008, 430:147-150.
144. Turner C.A., Flagel S.B., Clinton S.M., Akil H., Watson S.J. Cocaine interacts with the novelty-seeking trait to modulate FGFR1 gene expression in the rat. Neurosci. Lett. 2008, 446:105-107.
145. Turner C.A., Gula E.L., Taylor L.P., Watson S.J., Akil H. Antidepressant-like effects of intracerebroventricular FGF2 in rats. Brain Res. 2008, 1224:63-68.
146. Turner C.A., Capriles N., Flagel S.B., Perez J.A., Clinton S.M., Watson S.J., Akil H. Neonatal FGF2 alters cocaine self-administration in the adult rat. Pharmacol. Biochem. Behav. 2009, 92:100-104.
147. Turner C.A., Clinton S.M., Thompson R.C., Watson S.J., 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. USA 2011, 108:8021-8025.
148. Vaccarino F.M., Schwartz M.L., Raballo R., Nilsen J., Rhee J., Zhou M., Doetschman T., Coffin J.D., Wyland J.J., Hung Y.T. Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat. Neurosci. 1999, 2:848.
149. Vawter M.P. Dysregulation of the neural cell adhesion molecule and neuropsychiatric disorders. Eur. J. Pharmacol. 2000, 405:385-395.
150. Williams E.J., Furness J., Walsh F.S., Doherty P. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin. Neuron 1994, 13:583-594.
151. Williams G., Williams E.J., Doherty P. Dimeric versions of two short N-cadherin binding motifs (HAVDI and INPISG) function as N-cadherin agonists. J. Biol. Chem. 2002, 277:4361-4367.
152. Yamanaka Y., Kitano A., Takao K., Prasansuklab A., Mushiroda T., Yamazaki K., Kumada T., Shibata M., Takaoka Y., Awaya T., et al. Inactivation of fibroblast growth factor binding protein 3 causes anxiety-related behaviors. Mol. Cell. Neurosci. 2011, 46:200-212.
153. Zhang X., Ibrahimi O.A., Olsen S.K., Umemori H., Mohammadi M., Ornitz D.M. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 2006, 281:15694-15700.
154. Zhao M., Li D., Shimazu K., Zhou Y.X., Lu B., Deng C.X. Fibroblast growth factor receptor-1 is required for long-term potentiation, memory consolidation, and neurogenesis. Biol. Psychiatry 2007, 62:381-390.
155. Zheng W., Nowakowski R.S., Vaccarino F.M. Fibroblast growth factor 2 is required for maintaining the neural stem cell pool in the mouse brain subventricular zone. Dev. Neurosci. 2004, 26:181-196.