Fibroblast growth factor deficiencies impact anxiety-like behavior and the serotonergic system

Behavioural Brain Research

Volumn 264, Issue , 2014, Pages 74-81

  Brooks, Leah R ^a   Enix, Courtney L ^a   Rich, Samuel C ^a   Magno, Jinno A ^a   Lowry, Christopher A ^a   Tsai, Pei San ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Anxiety; Dorsal raphe nucleus; Fibroblast growth factor; Serotonin

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR RECEPTOR 1; TRYPTOPHAN HYDROXYLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; ELEVATED PLUS MAZE TEST; FGFR1 GENE; FGFR8 GENE; FIBROBLAST GROWTH FACTOR DEFICIENCY; GENE MUTATION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NEUROANATOMY; NONHUMAN; OPEN FIELD TEST; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION;

ANXIETY; DORSAL RAPHE NUCLEUS; FIBROBLAST GROWTH FACTOR; SEROTONIN;

ADAPTATION, PSYCHOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; BRAIN; EXPLORATORY BEHAVIOR; FIBROBLAST GROWTH FACTOR 8; GENE EXPRESSION REGULATION; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; MUSCLE STRENGTH; MUTATION; NEURONS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SEROTONIN; TRYPTOPHAN HYDROXYLASE;

EID: 84896735092     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.01.053     Document Type: Article

References (66)

1. Lowry C.A., Johnson P.L., Hay-Schmidt A., Mikkelsen J., Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 2005, 8:233-246.
2. Hale M.W., Lowry C.A. Functional topography of midbrain and pontine serotonergic systems: implications for synaptic regulation of serotonergic circuits. Psychopharmacology 2011, 213:243-264.
3. Calizo L.H., Akanwa A., Ma X., Pan Y.Z., Lemos J.C., Craige C., et al. Raphe serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence. Neuropharmacology 2011, 61:524-543.
4. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol Rev 1992, 72:165-229.
5. Hale M.W., Shekhar A., Lowry C.A. Stress-related serotonergic systems: implications for symptomatology of anxiety and affective disorders. Cell Mol Neurobiol 2012, 32:695-708.
6. Paul E.D., Lowry C.A. Functional topography of serotonergic systems supports the Deakin/Graeff hypothesis of anxiety and affective disorders. J Psychopharmacol 2013.
7. Cordes S.P. Molecular genetics of the early development of hindbrain serotonergic neurons. Clin Genet 2005, 68:487-494.
8. Kiyasova V., Gaspar P. Development of raphe serotonin neurons from specification to guidance. Eur J Neurosci 2011, 34:1553-1562.
9. Deneris E.S., Wyler S.C. Serotonergic transcriptional networks and potential importance to mental health. Nat Neurosci 2012, 15:519-527.
10. Partanen J. FGF signalling pathways in development of the midbrain and anterior hindbrain. J Neurochem 2007, 101:1185-1193.
11. Liu A., Joyner A.L. EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development 2001, 128:181-191.
12. Martinez S., Crossley P.H., Cobos I., Rubenstein J.L., Martin G.R. FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression. Development 1999, 126:1189-1200.
13. Wurst W., Bally-Cuif L. Neural plate patterning: upstream and downstream of the isthmic organizer. Nat Rev Neurosci 2001, 2:99-108.
14. Liu A., Joyner A.L. Early anterior/posterior patterning of the midbrain and cerebellum. Annu Rev Neurosci 2001, 24:869-896.
15. Echevarria D., Vieira C., Gimeno L., Martinez S. Neuroepithelial secondary organizers and cell fate specification in the developing brain. Brain Res Brain Res Rev 2003, 43:179-191.
16. Ye W., Shimamura K., Rubenstein J.L., Hynes M.A., Rosenthal A. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 1998, 93:755-766.
17. Gaspar P., Lillesaar C. Probing the diversity of serotonin neurons. Philos Trans R Soc London, Ser B 2012, 367:2382-2394.
18. Deneris E.S. Molecular genetics of mouse serotonin neurons across the lifespan. Neuroscience 2011, 197:17-27.
19. Hendricks T.J., Fyodorov D.V., Wegman L.J., Lelutiu N.B., Pehek E.A., Yamamoto B., et al. Pet-1 ETS gene plays a critical role in 5-HT neuron development and is required for normal anxiety-like and aggressive behavior. Neuron 2003, 37:233-247.
20. Kiyasova V., Fernandez S.P., Laine J., Stankovski L., Muzerelle A., Doly S., et al. A genetically defined morphologically and functionally unique subset of 5-HT neurons in the mouse raphe nuclei. J Neurosci 2011, 31:2756-2768. Off J Soc Neurosci.
21. Saarimaki-Vire J., Peltopuro P., Lahti L., Naserke T., Blak A.A., Vogt Weisenhorn D.M., et al. Fibroblast growth factor receptors cooperate to regulate neural progenitor properties in the developing midbrain and hindbrain. J Neurosci 2007, 27:8581-8592.
22. Blak A.A., Naserke T., Saarimaki-Vire J., Peltopuro P., Giraldo-Velasquez M., Vogt Weisenhorn D.M., et al. Fgfr2 and Fgfr3 are not required for patterning and maintenance of the midbrain and anterior hindbrain. Dev Biol 2007, 303:231-243.
23. Sato T., Joyner A.L. The duration of Fgf8 isthmic organizer expression is key to patterning different tectal-isthmo-cerebellum structures. Development 2009, 136:3617-3626.
24. Jukkola T., Lahti L., Naserke T., Wurst W., Partanen J. FGF regulated gene-expression and neuronal differentiation in the developing midbrain-hindbrain region. Dev Biol 2006, 297:141-157.
25. Falardeau J., Chung W.C., Beenken A., Raivio T., Plummer L., Sidis Y., et al. Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J Clin Invest 2008, 118:2822-2831.
26. Dode C., Levilliers J., Dupont J.M., De Paepe A., Le Du N., Soussi-Yanicostas N., et al. Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 2003, 33:463-465.
27. Meyers E.N., Lewandoski M., Martin G.R. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 1998, 18:136-141.
28. Partanen J., Schwartz L., Rossant J. Opposite phenotypes of hypomorphic and Y766 phosphorylation site mutations reveal a function for Fgfr1 in anteroposterior patterning of mouse embryos. Genes Dev 1998, 12:2332-2344.
29. Paylor R., Spencer C.M., Yuva-Paylor L.A., Pieke-Dahl S. The use of behavioral test batteries. II: effect of test interval. Physiol Behav 2006, 87:95-102.
30. Voikar V., Vasar E., Rauvala H. Behavioral alterations induced by repeated testing in C57BL/6J and 129S2/Sv mice: implications for phenotyping screens. Genes Brain Behav 2004, 3:27-38.
31. Crawley J.N. Behavioral phenotyping strategies for mutant mice. Neuron 2008, 57:809-818.
32. Bailey K.R., Pavlova M.N., Rohde A.D., Hohmann J.G., Crawley J.N. Galanin receptor subtype 2 (GalR2) null mutant mice display an anxiogenic-like phenotype specific to the elevated plus-maze. Pharmacol Biochem Behav 2007, 86:8-20.
33. McIlwain K.L., Merriweather M.Y., Yuva-Paylor L.A., Paylor R. The use of behavioral test batteries: effects of training history. Physiol Behav 2001, 73:705-717.
34. Crawley J., Goodwin F.K. Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 1980, 13:167-170.
35. Bourin M., Hascoet M. The mouse light/dark box test. Eur J Pharmacol 2003, 463:55-65.
36. Crawley J. What's wrong with my mouse? 2000, Wiley-Liss, New York, NY.
37. Hale M.W., Shekhar A., Lowry C.A. Development by environment interactions controlling tryptophan hydroxylase expression. J Chem Neuroanat 2011, 41:219-226.
38. Hale M.W., Dady K.F., Evans A.K., Lowry C.A. Evidence for in vivo thermosensitivity of serotonergic neurons in the rat dorsal raphe nucleus and raphe pallidus nucleus implicated in thermoregulatory cooling. Exp Neurol 2011, 227:264-278.
39. Brooks L.R., Chung W.C., Tsai P.S. Abnormal hypothalamic oxytocin system in fibroblast growth factor 8-deficient mice. Endocrine 2010, 38:174-180.
40. Grubbs F.E. Procedures for detecting outlying observations in samples. Technometrics 1969, 11:1-21.
41. Chi C.L., Martinez S., Wurst W., Martin G.R. The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 2003, 130:2633-2644.
42. Abrams J.K., Johnson P.L., Hay-Schmidt A., Mikkelsen J.D., Shekhar A., Lowry C.A. Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 2005, 133:983-997.
43. Rozeske R.R., Evans A.K., Frank M.G., Watkins L.R., Lowry C.A., Maier S.F. Uncontrollable, but not controllable, stress desensitizes 5-HT1A receptors in the dorsal raphe nucleus. J Neurosci 2011, 31:14107-14115. Off J Soc Neurosci.
44. Gardner K.L., Thrivikraman K.V., Lightman S.L., Plotsky P.M., Lowry C.A. Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience 2005, 136:181-191.
45. Spannuth B.M., Hale M.W., Evans A.K., Lukkes J.L., Campeau S., Lowry C.A. Investigation of a central nucleus of the amygdala/dorsal raphe nucleus serotonergic circuit implicated in fear-potentiated startle. Neuroscience 2011, 179:104-119.
46. Johnson P., Lowry C., Truitt W., Shekhar A. Disruption of GABAergic tone in the dorsomedial hypothalamus attenuates responses in a subset of serotonergic neurons in the dorsal raphe nucleus following lactate-induced panic. J Psychopharmacol 2008, 22:642-652.
47. Donner N.C., Johnson P.L., Fitz S.D., Kellen K.E., Shekhar A., Lowry C.A. Elevated tph2 mRNA expression in a rat model of chronic anxiety. Depress Anxiety 2012, 29:307-319.
48. Lukkes J.L., Kopelman J.M., Donner N.C., Hale M.W., Lowry C.A. Development×environment interactions control tph2 mRNA expression. Neuroscience 2013, 237:139-150.
49. Brodski C., Weisenhorn D.M., Signore M., Sillaber I., Oesterheld M., Broccoli V., et al. Location and size of dopaminergic and serotonergic cell populations are controlled by the position of the midbrain-hindbrain organizer. J Neurosci 2003, 23:4199-4207.
50. Blaess S., Corrales J.D., Joyner A.L. Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 2006, 133:1799-1809.
51. Crossley P.H., Martin G.R. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 1995, 121:439-451.
52. Xu J., Liu Z., Ornitz D.M. Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 2000, 127:1833-1843.
53. Trokovic R., Jukkola T., Saarimaki J., Peltopuro P., Naserke T., Weisenhorn D.M., et al. Fgfr1-dependent boundary cells between developing mid- and hindbrain. Dev Biol 2005, 278:428-439.
54. Vieira C., Pombero A., Garcia-Lopez R., Gimeno L., Echevarria D., Martinez S. Molecular mechanisms controlling brain development: an overview of neuroepithelial secondary organizers. Int J Dev Biol 2010, 54:7-20.
55. Jensen P., Farago A.F., Awatramani R.B., Scott M.M., Deneris E.S., Dymecki S.M. Redefining the serotonergic system by genetic lineage. Nat Neurosci 2008, 11:417-419.
56. Wallace J.A., Lauder J.M. Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res Bull 1983, 10:459-479.
57. Hawthorne A.L., Wylie C.J., Landmesser L.T., Deneris E.S., Silver J. Serotonergic neurons migrate radially through the neuroepithelium by dynamin-mediated somal translocation. J Neurosci 2010, 30:420-430.
58. Blak A.A., Naserke T., Weisenhorn D.M., Prakash N., Partanen J., Wurst W. Expression of Fgf receptors 1, 2, and 3 in the developing mid- and hindbrain of the mouse. Dev Dyn 2005, 233:1023-1030.
59. Trokovic R., Trokovic N., Hernesniemi S., Pirvola U., Vogt Weisenhorn D.M., Rossant J., et al. FGFR1 is independently required in both developing mid- and hindbrain for sustained response to isthmic signals. EMBO J 2003, 22:1811-1823.
60. Dono R. Fibroblast growth factors as regulators of central nervous system development and function. Am J Physiol Regul Integr Comp Physiol 2003, 284:R867-R881.
61. 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.
62. Olsen S.K., Li J.Y., Bromleigh C., Eliseenkova A.V., Ibrahimi O.A., Lao Z., et al. Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain. Genes Dev 2006, 20:185-198.
63. Wylie C.J., Hendricks T.J., Zhang B., Wang L., Lu P., Leahy P., et al. Distinct transcriptomes define rostral and caudal serotonin neurons. J Neurosci 2010, 30:670-684.
64. Garel S., Huffman K.J., Rubenstein J.L. Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants. Development 2003, 130:1903-1914.
65. 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.
66. Klejbor I., Kucinski A., Wersinger S.R., Corso T., Spodnik J.H., Dziewiatkowski J., et al. Serotonergic hyperinnervation and effective serotonin blockade in an FGF receptor developmental model of psychosis. Schizophr Res 2009, 113:308-321.