Fibroblast growth factor 8 deficiency compromises the functional response of the serotonergic system to stress

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Brooks, Leah R ^a   Pals, Heide L ^a   Enix, Courtney L ^a   Woolaver, Rachel A ^a   Paul, Evan D ^a   Lowry, Christopher A ^a   Tsai, Pei San ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; FIBROBLAST GROWTH FACTOR 8; SEROTONIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; ELEVATED PLUS MAZE TEST; FGF8 GENE; GENE; IMMUNOHISTOCHEMISTRY; MALE; MOTOR COORDINATION; MOUSE; NONHUMAN; PANIC; PROTEIN DEFICIENCY; ROTAROD TEST; SEROTONINERGIC SYSTEM; STRESS; TISSUE LEVEL; ANIMAL; BRAIN; ELECTROCHEMICAL ANALYSIS; GENETICS; HETEROZYGOTE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; SEROTONINERGIC NERVE CELL; TRANSGENIC MOUSE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROCHEMICAL TECHNIQUES; FIBROBLAST GROWTH FACTOR 8; HETEROZYGOTE; HYDROXYINDOLEACETIC ACID; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; SEROTONERGIC NEURONS; SEROTONIN; STRESS, PHYSIOLOGICAL;

EID: 84903783707     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101420     Document Type: Article

References (63)

1. Leonardo ED, Hen R (2008) Anxiety as a developmental disorder. Neuropsychopharmacology 33: 134-140. (Pubitemid 350191317)
2. Gross C, Zhuang X, Stark K, Ramboz S, Oosting R, et al. (2002) Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature 416: 396-400. (Pubitemid 34272867)
3. Gardner KL, Hale MW, Oldfield S, Lightman SL, Plotsky PM, et al. (2009) Adverse experience during early life and adulthood interact to elevate tph2 mRNA expression in serotonergic neurons within the dorsal raphe nucleus. Neuroscience 163: 991-1001.
4. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature reviews Neuroscience 10: 434-445.
5. Sapolsky R (2003) Taming stress. Scientific American 289: 86-95.
6. Gaspar P, Cases O, Maroteaux L (2003) The developmental role of serotonin: news from mouse molecular genetics. Nature reviews Neuroscience 4: 1002-1012. (Pubitemid 37486676)
7. Hale MW, Shekhar A, Lowry CA (2012) Stress-related serotonergic systems: implications for symptomatology of anxiety and affective disorders. Cellular and molecular neurobiology 32: 695-708.
8. Singewald N, Salchner P, Sharp T (2003) Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol Psychiatry 53: 275-283. (Pubitemid 36175541)
9. Lowry CA, Johnson PL, Hay-Schmidt A, Mikkelsen J, Shekhar A (2005) Modulation of anxiety circuits by serotonergic systems. Stress 8: 233-246. (Pubitemid 43163256)
10. Greenwood BN, Strong PV, Brooks L, Fleshner M (2008) Anxiety-like behaviors produced by acute fluoxetine administration in male Fischer 344 rats are prevented by prior exercise. Psychopharmacology (Berl) 199: 209-222.
11. Sommer W, Moller C, Wiklund L, Thorsell A, Rimondini R, et al. (2001) Local 5,7-dihydroxytryptamine lesions of rat amygdala: release of punished drinking, unaffected plus-maze behavior and ethanol consumption. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology 24: 430-440.
12. Maier SF, Watkins LR (2005) Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev 29: 829-841. (Pubitemid 40762600)
13. Johnson P, Lowry C, Truitt W, Shekhar A (2008) 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 22: 642-652.
14. Johnson PL, Lightman SL, Lowry CA (2004) A functional subset of serotonergic neurons in the rat ventrolateral periaqueductal gray implicated in the inhibition of sympathoexcitation and panic. Annals of the New York Academy of Sciences 1018: 58-64. (Pubitemid 38951390)
15. Partanen J (2007) FGF signalling pathways in development of the midbrain and anterior hindbrain. J Neurochem 101: 1185-1193.
16. Chi CL, Martinez S, Wurst W, Martin GR (2003) The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130: 2633-2644. (Pubitemid 37069580)
17. Saarimaki-Vire J, Peltopuro P, Lahti L, Naserke T, Blak AA, et al. (2007) Fibroblast growth factor receptors cooperate to regulate neural progenitor properties in the developing midbrain and hindbrain. J Neurosci 27: 8581-8592. (Pubitemid 47254256)
18. Jukkola T, Lahti L, Naserke T, Wurst W, Partanen J (2006) FGF regulated gene-expression and neuronal differentiation in the developing midbrain-hindbrain region. Dev Biol 297: 141-157. (Pubitemid 44313909)
19. Ye W, Shimamura K, Rubenstein JL, Hynes MA, Rosenthal A (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93: 755-766. (Pubitemid 28257582)
20. Crossley PH, Martin GR (1995) The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121: 439-451.
21. Meyers EN, Lewandoski M, Martin GR (1998) An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 18: 136-141. (Pubitemid 28082459)
22. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, et al. (2007) Genomewide atlas of gene expression in the adult mouse brain. Nature 445: 168-176. (Pubitemid 46095716)
23. Brooks LR, Enix CL, Rich SC, Magno JA, Lowry CA, et al. (2014) Fibroblast growth factor deficiencies impact anxiety-like behavior and the serotonergic system. Behavioural brain research.
24. Falardeau J, Chung WC, Beenken A, Raivio T, Plummer L, et al. (2008) Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J Clin Invest 118: 2822-2831.
25. Bailey KR, Pavlova MN, Rohde AD, Hohmann JG, Crawley JN (2007) Galanin receptor subtype 2 (GalR2) null mutant mice display an anxiogenic-like phenotype specific to the elevated plus-maze. Pharmacol Biochem Behav 86: 8-20.
26. Voikar V, Vasar E, Rauvala H (2004) Behavioral alterations induced by repeated testing in C57BL/6J and 129S2/Sv mice: implications for phenotyping screens. Genes Brain Behav 3: 27-38. (Pubitemid 38160239)
27. Ferrer I, Olive M, Blanco R, Cinos C, Planas AM (1996) Selective c-Jun overexpression is associated with ionizing radiation-induced apoptosis in the developing cerebellum of the rat. Brain research Molecular brain research 38: 91-100. (Pubitemid 26159197)
28. Bailey JD, Centers A, Jennes L (2006) Expression of AMPA receptor subunits (GluR1-GluR4) in gonadotrophin-releasing hormone neurones of young and middle-aged persistently oestrous rats during the steroid-induced luteinising hormone surge. Journal of neuroendocrinology 18: 1-12.
29. Brooks LR, Chung WC, Tsai PS (2010) Abnormal hypothalamic oxytocin system in fibroblast growth factor 8-deficient mice. Endocrine 38: 174-180.
30. Hale MW, Shekhar A, Lowry CA (2011) Development by environment interactions controlling tryptophan hydroxylase expression. J Chem Neuroanat 41: 219-226.
31. Hale MW, Dady KF, Evans AK, Lowry CA (2011) Evidence for in vivo thermosensitivity of serotonergic neurons in the rat dorsal raphe nucleus and raphe pallidus nucleus implicated in thermoregulatory cooling. Experimental neurology 227: 264-278.
32. Evans AK, Reinders N, Ashford KA, Christie IN, Wakerley JB, et al. (2008) Evidence for serotonin synthesis-dependent regulation of in vitro neuronal firing rates in the midbrain raphe complex. Eur J Pharmacol 590: 136-149.
33. Neufeld-Cohen A, Evans AK, Getselter D, Spyroglou A, Hill A, et al. (2010) Urocortin-1 and -2 double-deficient mice show robust anxiolytic phenotype and modified serotonergic activity in anxiety circuits. Mol Psychiatry 15: 426-441, 339.
34. Paxinos G, Franklin KBJ (2001) The Mouse Brain in Stereotaxic Coordinates. 2nd ed. San Diego: Academic Press.
35. Grubbs FE (1969) Procedures for Detecting Outlying Observations in Samples. Technometrics 11: 1-21.
36. Petersen RG (1985) Design and analysis of experiments. New York: Marcel Dekker, Inc.
37. James MD, Hole DR, Wilson CA (1989) Differential Involvement of 5-Hydroxytryptamine (5HT) in Specific Hypothalamic Areas in the Mediation of Steroid-Induced Changes in Gonadotrophin Release and Sexual Behaviour in Female Rats. Neuroendocrinology 49: 561-569. (Pubitemid 19154605)
38. Kirby LG, Chou-Green JM, Davis K, Lucki I (1997) The effects of different stressors on extracellular 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain research 760: 218-230. (Pubitemid 27304156)
39. Tanaka M, Kohno Y, Nakagawa R, Nishikawa T, Tsuda A, et al. (1983) Immobilization stress increases serotonin turnover in the extended brain regions in the rat. The Kurume medical journal 30: 35-43.
40. Stone EA, Rhee J, Quartermain D (1996) Blockade of effect of stress on risk assessment behavior in mice by a beta-1 adrenoceptor antagonist. Pharmacology, biochemistry, and behavior 55: 215-217. (Pubitemid 26414103)
41. Paul ED, Lowry CA (2013) Functional topography of serotonergic systems supports the Deakin/Graeff hypothesis of anxiety and affective disorders. Journal of psychopharmacology.
42. Heinrichs SC, Menzaghi F, Pich EM, Baldwin HA, Rassnick S, et al. (1994) Anti-stress action of a corticotropin-releasing factor antagonist on behavioral reactivity to stressors of varying type and intensity. Neuropsychopharmacology 11: 179-186. (Pubitemid 24351285)
43. Korte SM, De Boer SF (2003) A robust animal model of state anxiety: fearpotentiated behaviour in the elevated plus-maze. Eur J Pharmacol 463: 163-175. (Pubitemid 36205078)
44. Belzung C, Griebel G (2001) Measuring normal and pathological anxiety-like behaviour in mice: a review. Behavioural brain research 125: 141-149. (Pubitemid 33000452)
45. Lowry CA, Hale MW, Evans AK, Heerkens J, Staub DR, et al. (2008) Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 1148: 86-94.
46. Abrams JK, Johnson PL, Hay-Schmidt A, Mikkelsen JD, Shekhar A, et al. (2005) Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 133: 983-997. (Pubitemid 40814606)
47. Spannuth BM, Hale MW, Evans AK, Lukkes JL, Campeau S, et al. (2011) Investigation of a central nucleus of the amygdala/dorsal raphe nucleus serotonergic circuit implicated in fear-potentiated startle. Neuroscience 179: 104-119.
48. Grahn RE, Will MJ, Hammack SE, Maswood S, McQueen MB, et al. (1999) Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain research 826: 35-43. (Pubitemid 29222957)
49. Spiacci A Jr, Coimbra NC, Zangrossi H Jr (2012) Differential involvement of dorsal raphe subnuclei in the regulation of anxiety- and panic-related defensive behaviors. Neuroscience 227: 350-360.
50. Johnson PL, Hollis JH, Moratalla R, Lightman SL, Lowry CA (2005) Acute hypercarbic gas exposure reveals functionally distinct subpopulations of serotonergic neurons in rats. Journal of psychopharmacology 19: 327-341. (Pubitemid 41003128)
51. Hale MW, Lowry CA (2011) Functional topography of midbrain and pontine serotonergic systems: implications for synaptic regulation of serotonergic circuits. Psychopharmacology 213: 243-264.
52. Boxer AL, Moreno H, Rudy B, Ziff EB (1999) FGF-2 potentiates Ca(2+)- dependent inactivation of NMDA receptor currents in hippocampal neurons. Journal of neurophysiology 82: 3367-3377. (Pubitemid 30017461)
53. Mattson MP, Murrain M, Guthrie PB, Kater SB (1989) Fibroblast growth factor and glutamate: opposing roles in the generation and degeneration of hippocampal neuroarchitecture. The Journal of neuroscience: the official journal of the Society for Neuroscience 9: 3728-3740.
54. Terauchi A, Johnson-Venkatesh EM, Toth AB, Javed D, Sutton MA, et al. (2010) Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature 465: 783-787.
55. Celada P, Puig M, Amargos-Bosch M, Adell A, Artigas F (2004) The therapeutic role of 5-HT1A and 5-HT2A receptors in depression. Journal of psychiatry & neuroscience: JPN 29: 252-265. (Pubitemid 39185866)
56. Jankowski MP, Sesack SR (2004) Prefrontal cortical projections to the rat dorsal raphe nucleus: ultrastructural features and associations with serotonin and gamma-aminobutyric acid neurons. The Journal of comparative neurology 468: 518-529. (Pubitemid 38036693)
57. Wang QP, Ochiai H, Nakai Y (1992) GABAergic innervation of serotonergic neurons in the dorsal raphe nucleus of the rat studied by electron microscopy double immunostaining. Brain research bulletin 29: 943-948.
58. Celada P, Puig MV, Casanovas JM, Guillazo G, Artigas F (2001) Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: Involvement of serotonin-1A, GABA(A), and glutamate receptors. J Neurosci 21: 9917-9929. (Pubitemid 34184076)
59. Iwata T, Hevner RF (2009) Fibroblast growth factor signaling in development of the cerebral cortex. Dev Growth Differ 51: 299-323.
60. Toyoda R, Assimacopoulos S, Wilcoxon J, Taylor A, Feldman P, et al. (2010) FGF8 acts as a classic diffusible morphogen to pattern the neocortex. Development 137: 3439-3448.
61. Storm EE, Garel S, Borello U, Hebert JM, Martinez S, et al. (2006) Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 133: 1831-1844. (Pubitemid 43810989)
62. Huffman KJ, Garel S, Rubenstein JL (2004) Fgf8 regulates the development of intra-neocortical projections. J Neurosci 24: 8917-8923. (Pubitemid 39372236)
63. Forster GL, Pringle RB, Mouw NJ, Vuong SM, Watt MJ, et al. (2008) Corticotropin-releasing factor in the dorsal raphe nucleus increases medial prefrontal cortical serotonin via type 2 receptors and median raphe nucleus activity. Eur J Neurosci 28: 299-310.