Fibroblast Growth Factor 2 Modulates Hypothalamic Pituitary Axis Activity and Anxiety Behavior Through Glucocorticoid Receptors

Biological Psychiatry

Volumn 80, Issue 6, 2016, Pages 479-489

  Salmaso, Natalina ^a,e   Stevens, Hanna E ^a   McNeill, Jessica ^e   ElSayed, Maha ^b   Ren, Qiuyin ^a   Maragnoli, Maria E ^a   Schwartz, Michael L ^b   Tomasi, Simone ^a   Sapolsky, Robert M ^d   Duman, Ronald ^b   Vaccarino, Flora M ^a,b,c  

^a Department of Pediatrics   (United States)

^b Department of Psychiatry ^*  (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d STANFORD UNIVERSITY   (United States)

^e CARLETON UNIVERSITY   (Canada)

Author keywords

Anxiety; FGF receptors; FGF2; Glucocorticoids; Hippocampus; Mouse; Stress

Indexed keywords

ANXIOLYTIC AGENT; EARLY GROWTH RESPONSE FACTOR 1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GLUCOCORTICOID RECEPTOR; TRANSCRIPTION FACTOR EGR 1; EGR1 PROTEIN, MOUSE; FIBROBLAST GROWTH FACTOR RECEPTOR; MIFEPRISTONE;

ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEPRESSION; GENE EXPRESSION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LOCOMOTION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; TRANQUILIZING ACTIVITY; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; ANXIETY; BIOSYNTHESIS; DRUG EFFECTS; GENETICS; HIPPOCAMPUS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; PSYCHOLOGY;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 1; FIBROBLAST GROWTH FACTOR 2; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MICE; MICE, KNOCKOUT; MIFEPRISTONE; PITUITARY-ADRENAL SYSTEM; RECEPTORS, FIBROBLAST GROWTH FACTOR; RECEPTORS, GLUCOCORTICOID;

EID: 84964584354     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2016.02.026     Document Type: Article

References (49)

1. 1 Woodbury, M.E., Ikezu, T., Fibroblast growth factor-2 signaling in neurogenesis and neurodegeneration. J Neuroimmune Pharmacol 9 (2014), 92–101.
2. 2 Vaccarino, F.M., Grigorenko, E.L., Smith, K.M., Stevens, H.E., Regulation of cerebral cortical size and neuron number by fibroblast growth factors: Implications for autism. J Autism Dev Disord 39 (2009), 511–520.
3. 3 Vaccarino, F.M., Schwartz, M.L., Raballo, R., Nilsen, J., Rhee, J., Zhou, M., et al. Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2 (1999), 246–253.
4. 4 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 20 (2000), 5012–5023.
5. 5 Korada, S., Zheng, W., Basilico, C., Schwartz, M.L., Vaccarino, F.M., Fgf2 is necessary for the growth of glutamate projection neurons in the anterior neocortex. J Neurosci 22 (2002), 863–875.
6. 6 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 26 (2004), 181–196.
7. 7 Flores, C., Stewart, J., Salmaso, N., Zhang, Y., Boksa, P., Astrocytic basic fibroblast growth factor expression in dopaminergic regions after perinatal anoxia. Biol Psychiatry, 52, 2002, 362.
8. 8 Ganat, Y., Soni, S., Chacon, M., Schwartz, M.L., Vaccarino, F.M., Chronic hypoxia up-regulates fibroblast growth factor ligands in the perinatal brain and induces fibroblast growth factor -responsive radial glial cells in the sub-ependymal zone. Neuroscience 112 (2002), 977–991.
9. 9 Rai, K.S., Hattiangady, B., Shetty, A.K., Enhanced production and dendritic growth of new dentate granule cells in the middle-aged hippocampus following intracerebroventricular FGF-2 infusions. Eur J Neurosci 26 (2007), 1765–1779.
10. 10 Akil, H., Evans, S.J., Turner, C.A., Perez, J., Myers, R.M., Bunney, W.E., et al. The fibroblast growth factor family and mood disorders. Novartis Found Symp 289 (2008), 94–96 discussion 97–100, 193–105.
11. 11 Eren-Kocak, 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 69 (2011), 534–540.
12. 12 Evans, S.J., Choudary, P.V., Neal, C.R., Li, J.Z., Vawter, M.P., Tomita, H., et al. Dysregulation of the fibroblast growth factor system in major depression. Proc Natl Acad Sci U S A 101 (2004), 15506–15511.
13. 13 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 29 (2009), 6379–6387.
14. 14 Turner, C.A., Gula, E.L., Taylor, L.P., Watson, S.J., Akil, H., Antidepressant-like effects of intracerebroventricular FGF2 in rats. Brain Res 1224 (2008), 63–68.
15. 15 Salmaso, N., Vaccarino, F.M., Toward a novel endogenous anxiolytic factor, fibroblast growth factor 2. Biol Psychiatry 69 (2011), 508–509.
16. 16 Bachis, A., Mallei, A., Cruz, M.I., Wellstein, A., Mocchetti, I., Chronic antidepressant treatments increase basic fibroblast growth factor and fibroblast growth factor-binding protein in neurons. Neuropharmacology 55 (2008), 1114–1120.
17. 17 Zhou, M., Sutliff, R.L., Paul, R.J., Lorenz, J.N., Hoying, J.B., Haudenschild, C.C., et al. Fibroblast growth factor 2 controls vascular tone. Nat Med 4 (1998), 201–207.
18. 18 Stevens, H.E., Smith, K.M., Maragnoli, M.E., Fagel, D., Borok, E., Shanabrough, M., et al. Fgfr2 is required for the development of the medial prefrontal cortex and its connections with limbic circuits. J Neurosci 30 (2010), 5590–5602.
19. 19 Deng, C., Wynshaw-Boris, A., Zhou, F., Kuo, A., Leder, P., Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 84 (1996), 911–921.
20. 20 Rash, B.G., Lim, H.D., Breunig, J.J., Vaccarino, F.M., FGF signaling expands embryonic cortical surface area by regulating notch-dependent neurogenesis. J Neurosci 31 (2011), 15604–15617.
21. 21 Comeau, W., Gibb, R., Hastings, E., Cioe, J., Kolb, B., Therapeutic effects of complex rearing or bFGF after perinatal frontal lesions. Dev Psychobiol 50 (2008), 134–146.
22. 22 Wagner, J.P., Black, I.B., DiCicco-Bloom, E., Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci 19 (1999), 6006–6016.
23. 23 de Kloet, E.R., Oitzl, M.S., Joels, M., Functional implications of brain corticosteroid receptor diversity. Cell Mol Neurobiol 13 (1993), 433–455.
24. 24 De Kloet, E.R., Vreugdenhil, E., Oitzl, M.S., Joels, M., Brain corticosteroid receptor balance in health and disease. Endocr Rev 19 (1998), 269–301.
25. 25 Sapolsky, R.M., Krey, L.C., McEwen, B.S., Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci U S A 81 (1984), 6174–6177.
26. 26 McEwen, B.S., Plasticity of the hippocampus: Adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 933 (2001), 265–277.
27. 27 Sapolsky, R.M., Krey, L.C., McEwen, B.S., The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis. Endocr Rev 7 (1986), 284–301.
28. 28 Garcia, A., Steiner, B., Kronenberg, G., Bick-Sander, A., Kempermann, G., Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 3 (2004), 363–371.
29. 29 Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277 (1997), 1659–1662.
30. 30 Weaver, I.C., Cervoni, N., Champagne, F.A., D'Alessio, A.C., Sharma, S., Seckl, J.R., et al. Epigenetic programming by maternal behavior. Nat Neurosci 7 (2004), 847–854.
31. 31 Jiang, C., Salton, S.R., The role of neurotrophins in major depressive disorder. Transl Neurosci 4 (2013), 46–58.
32. 32 Sapolsky, R.M., Meaney, M.J., McEwen, B.S., The development of the glucocorticoid receptor system in the rat limbic brain. III. Negative-feedback regulation. Brain Res 350 (1985), 169–173.
33. 33 Ridder, S., Chourbaji, S., Hellweg, R., Urani, A., Zacher, C., Schmid, W., et al. Mice with genetically altered glucocorticoid receptor expression show altered sensitivity for stress-induced depressive reactions. J Neurosci 25 (2005), 6243–6250.
34. 34 Brown, E.S., Rush, A.J., McEwen, B.S., Hippocampal remodeling and damage by corticosteroids: Implications for mood disorders. Neuropsychopharmacology 21 (1999), 474–484.
35. 35 Calvo, N., Volosin, M., Glucocorticoid and mineralocorticoid receptors are involved in the facilitation of anxiety-like response induced by restraint. Neuroendocrinology 73 (2001), 261–271.
36. 36 Korte, S.M., de Boer, S.F., de Kloet, E.R., Bohus, B., Anxiolytic-like effects of selective mineralocorticoid and glucocorticoid antagonists on fear-enhanced behavior in the elevated plus-maze. Psychoneuroendocrinology 20 (1995), 385–394.
37. 37 Gonzalez, A.-M., Berry, M., Maher, P.A., Logan, A., Baird, A., A comprehensive analysis of the distribution of FGF-2 and FGF-1 in the rat brain. Brain Res 701 (1995), 201–226.
38. 38 Belluardo, N., Wu, G.-Y., Mudo, G., Hansson, A.C., Petterson, R., Fuxe, K., Comparative localization of fibroblast growth factor receptor-1, -2, and -3 mRNAs in the rat brain: In situ hybridization analysis. J Comp Neurol 379 (1997), 226–246.
39. 39 McCormick, J.A., Lyons, V., Jacobson, M.D., Noble, J., Diorio, J., Nyirenda, M., et al. 5’-heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: Differential regulation of variant transcripts by early-life events. Mol Endocrinol 14 (2000), 506–517.
40. 40 Zhang, T.Y., Labonte, B., Wen, X.L., Turecki, G., Meaney, M.J., Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans. Neuropsychopharmacology 38 (2013), 111–123.
41. 41 Anisman, H., Zaharia, M.D., Meaney, M.J., Merali, Z., Do early-life events permanently alter behavioral and hormonal responses to stressors?. Int J Dev Neurosci 16 (1998), 149–164.
42. 42 Francis, D.D., Meaney, M.J., Maternal care and the development of stress responses. Curr Opin Neurobiol 9 (1999), 128–134.
43. 43 Hellstrom, I.C., Dhir, S.K., Diorio, J.C., Meaney, M.J., Maternal licking regulates hippocampal glucocorticoid receptor transcription through a thyroid hormone-serotonin-NGFI-A signalling cascade. Philos Trans R Soc Lond B Biol Sci 367 (2012), 2495–2510.
44. 44 Bredy, T.W., Humpartzoomian, R.A., Cain, D.P., Meaney, M.J., Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neuroscience 118 (2003), 571–576.
45. 45 Muller Smith, K., Fagel, D.M., Stevens, H.E., Rabenstein, R.L., Maragnoli, M.E., Ohkubo, Y., et al. Deficiency in inhibitory cortical interneurons associates with hyperactivity in fibroblast growth factor receptor 1 mutant mice. Biol Psychiatry 63 (2008), 953–962.
46. 46 Smith, K.M., Williamson, T.L., Schwartz, M.L., Vaccarino, F.M., Impaired motor coordination and disrupted cerebellar architecture in Fgfr1 and Fgfr2 double knockout mice. Brain Res 1460 (2012), 12–24.
47. 47 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 71 (2012), 1090–1098.
48. 48 Aurbach, E.L., Inui, E.G., Turner, C.A., Hagenauer, M.H., Prater, K.E., Li, J.Z., et al. Fibroblast growth factor 9 is a novel modulator of negative affect. Proc Natl Acad Sci U S A 112 (2015), 11953–11958.
49. 49 Kessler, R.C., Chiu, W.T., Demler, O., Merikangas, K.R., Walters, E.E., Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62 (2005), 617–627.