Distinctive behavioral and cellular responses to fluoxetine in the mouse model for Fragile X syndrome

Frontiers in Cellular Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Uutela, Marko ^a   Lindholm, Jesse ^a   Rantamäki, Tomi ^a   Umemori, Juzoh ^a   Hunter, Kerri ^a   Võikar, Vootele ^a   Castrén, Maija L ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Autism; BDNF; Behavior; Neurogenesis; TrkB receptors

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FLUOXETINE; MESSENGER RNA; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ANXIETY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL BEHAVIORAL TEST; EXPLORATORY BEHAVIOR; FORCED SWIM TEST; FRAGILE X SYNDROME; HIPPOCAMPUS; HYPERACTIVITY; IN SITU HYBRIDIZATION; KNOCKOUT MOUSE; LATENT PERIOD; MOUSE; NEURAL STEM CELL; NONHUMAN; OPEN FIELD TEST; PROTEIN EXPRESSION; STEM CELL CULTURE; THALAMUS NUCLEUS; WESTERN BLOTTING;

EID: 84901639525     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00150     Document Type: Article

References (74)

1. Aman, M. G., Lam, K. S., and Van Bourgondien, M. E. (2005). Medication patterns in patients with autism: temporal, regional, and demographic influences. J. Child Adolesc. Psychopharmacol. 15, 116-126. doi: 10.1089/cap.2005.15.116
2. Bakker, C. E., Verheij, C., Willemsen, R., Vanderhelm, R., Oerlemans, F., Vermey, M., et al. (1994). Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 78, 23-33. doi: 10.1016/0092-8674(94)90569-X
3. Banasr, M., Hery, M., Printemps, R., and Daszuta, A. (2004). Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 29, 450-460. doi: 10.1038/sj.npp.1300320
4. Bassel, G. J., and Warren, S. T. (2008). Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60, 201-214. doi: 10.1016/j.neuron.2008.10.004
5. Bernardet, M., and Crusio, W. E. (2006). Fmr1 KO mice as a possible model of autistic features. Sci. World J. 6, 1164-1176.
6. Berton, O., Mcclung, C. A., Dileone, R. J., Krishnan, V., Renthal, W., Russo, S. J., et al. (2006). Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868. doi: 10.1126/science.1120972
7. Brown, W. T., Jenkins, E. C., Cohen, I. L., Fisch, G. S., Wolf-Schein, E. G., Gross, A., et al. (1986). Fragile X and autism: a multicenter survey. Am. J. Med. Genet. 23, 341-352. doi: 10.1002/ajmg.1320230126
8. Brune, C., Kim, S., Salt, J., Leventhal, B., Lord, C., and Cook, E. J. (2006). 5-HTTLPR genotype-specific phenotype in children and adolescents with autism. Am. J. Psychiatry 163, 2148-2156. doi: 10.1176/appi.ajp.163.12.2148
9. Buchsbaum, M. S., Hollander, E., Haznedar, M. M., Tang, C., Spiegel-Cohen, J., Wei, T. C., et al. (2001). Effect of fluoxetine on regional cerebral metabolism in autistic spectrum disorders: a pilot study. Int. J. Neuropsychopharmacol. 4, 119-125. doi: 10.1017/S1461145701002280
10. Castrén, M., Lampinen, K. E., Miettinen, R., Koponen, E., Sipola, I., Bakker, C. E., et al. (2002). BDNF regulates the expression of fragile X mental retardation protein mRNA in the hippocampus. Neurobiol. Dis. 11, 221-229. doi: 10.1006/nbdi.2002.0544
11. Castrén, M., Tervonen T., Kärkkäinen V., Heinonen S., Castrén E., Larsson K., et al. (2005). Altered neuronal differentiation of neural stem cells in fragile X syndrome. Proc. Natl. Acad. Sci. U.S.A. 102, 17408-17449. doi: 10.1073/pnas.0508995102
12. Castrén, M. L., and Castrén, E. (2014). BDNF in fragile X syndrome. Neuropharmacology 76, 729-736. doi: 10.1016/j.neuropharm.2013.05.018
13. Chen, Z. Y., Jing, D., Bath, K. G., Ieraci, A., Khan, T., Siao, C. J., et al. (2006). Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314, 140-143. doi: 10.1126/science.1129663
14. Connolly, A., Chez, M., Streif, E. M., Keeling, R. M., Golumbek, P. T., Kwon, J. M., et al. (2006). Brain-derived neurotrophic factor and autoantibodies to neural antigens in sera of children with autistic spectrum disorders, Landau-Kleffner syndrome, and epilepsy. Biol. Psychiatry 59, 354-363. doi: 10.1016/j.biopsych.2005.07.004
15. Correia, C. T., Coutinho, A. M., Sequeira, A. F., Sousa, I. G., Venda, L. L., Almeida, J. P., et al. (2011). Increased BDNF levels and NTRK2 gene association suggest a disruption of BDNF/TRKB signaling in autism. Genes Brain Behav. 9, 841-848. doi: 10.1111/j.1601-183X.2010.00627.x
16. Cryan, J. F., Markou, A., and Lucki, I. (2002). Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol. Sci. 23, 238-245. doi: 10.1016/S0165-6147(02)02017-5
17. Darnell, J. C., Van Driesche, S. J., Zhang, C., Hung, K. Y., Mele, A., Fraser, C. E., et al. (2011). FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146, 247-261. doi: 10.1016/j.cell.2011.06.013
18. DeLong, G. R., Ritch, C. R., and Burch, S. (2002). Fluoxetine response in children with autistic spectrum disorders: correlation with familial major affective disorder and intellectual achievement. Dev. Med. Child Neurol. 44, 652-659. doi: 10.1111/j.1469-8749.2002.tb00266.x
19. DeLong, G. R., Teague, L. A., and Mcswain Kamran, M. (1998). Effects of fluoxetine treatment in young children with idiopathic autism. Dev. Med. Child Neurol. 40, 551-562. doi: 10.1111/j.1469-8749.1998.tb15414.x
20. Devlin, B., Cook, E. J., Coon, H., Dawson, G., Grigorenko, E., Mcmahon, W., et al. (2005). Autism and the serotonin transporter: the long and short of it. Mol. Psychiatry 10, 1110-1116. doi: 10.1038/sj.mp.4001724
21. Dolen, G., Osterweil, E., Rao, B. S. S, Smith, G. B., Auerbach, B. D., Chattarji, S., et al. (2007). Correction of fragile X syndrome in mice. Neuron 56, 955-962. doi: 10.1016/j.neuron.2007.12.001
22. Duman, R. S., and Monteggia, L. M. (2006). A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59, 1116-1127. doi: 10.1016/j.biopsych.2006.02.013
23. Dölen, G., and Bear, M. F. (2009). Fragile X syndrome and autism: from disease model to therapeutic targets. J. Neurodevelop. Disord. 1, 133-140. doi: 10.1007/s11689-009-9015-x
24. Garcia, K., Yu, G., Nicolini, C., Michalski, B., Garzon, D., Chiu, V. S., et al. (2012). Altered balance of proteolytic isoforms of pro-brain-derived neurotrophic factor in autism. J. Neuropathol. Exp. Neurol. 71, 289-297. doi: 10.1097/NEN.0b013e31824b27e4
25. Gibson, J. R., Bartley, A. F., Hays, S. A., and Huber, K. M. (2008). Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J. Neurophysiol. 100, 2615-2626. doi: 10.1152/jn.90752.2008
26. Hagerman, R., Berry-Kravis, E., Kaufmann, W., Ono, M., Tartaglia, N., Lachiewicz, A., et al. (2009). Advances in the treatment of fragile X syndrome. Pediatrics 123, 378-390. doi: 10.1542/peds.2008-0317
27. Hagerman, R., Fulton, M. J., Leaman, A., Riddle, J., Hagerman, K., and Sobesky, W. (1994). A survey of fluoxetine therapy in fragile syndrome. Dev. Brain Dysfunct. 7, 155-164.
28. Hagerman, R., Hoem, G., and Hagerman, P. (2010). Fragile X and autism: intertwined at the molecular level leading to targeted treatments. Mol. Autism 1, 1-14. doi: 10.1186/2040-2392-1-12
29. Hernandez, R. N., Feinberg, R. L., Vaurio, R., Passanante, N. M., Thompson, R. E., and Kaufmann, W. E. (2009). Autism spectrum disorder in fragile X syndrome: a longitudinal evaluation. Am. J. Med. Genet. 149A, 1125-1137. doi: 10.1002/ajmg.a.32848
30. Hollander, E., Soorya, L., Chaplin, W., Anagnostou, E., Taylor, B. P., Ferretti, C. J., et al. (2012). A double-blind placebo-controlled trial of fluoxetine for repetitive behaviors and global severity in adult autism spectrum disorders. Am. J. Psychiatry 169, 292-299. doi: 10.1176/appi.ajp.2011.10050764
31. Hughes, J. (2009). Update on autism: a review of 1300 reports published in 2008. Epilepsy Behav. 16, 569-589. doi: 10.1016/j.yebeh.2009.09.023
32. Ibarguen-Vargas, Y., Surget, A., Vourc'h, P., Leman, S., Andres, C. R., Gardier, A. M., et al. (2009). Deficit in BDNF does not increase vulnerability to stress but dampens antidepressant-like effects in the unpredictable chronic mild stress. Behav. Brain Res. 202, 245-251. doi: 10.1016/j.bbr.2009.03.040
33. Iughetti, L., Casarosa, E., Predieri, B., Patianna, V., and Luisi, S. (2011). Plasma brain-derived neurotrophic factor concentrations in children and adolescents. Neuropeptides 45, 205-211. doi: 10.1016/j.npep.2011.02.002
34. Karpova, N., Lindholm, J., Pruunsild, P., Timmusk, T., and Castrén, E. (2009). Long-lasting behavioural and molecular alterations induced by early postnatal fluoxetine exposure are restored by chronic fluoxetine treatment in adult mice. Eur. Neuropsychopharmacol. 19, 97-108. doi: 10.1016/j.euroneuro.2008.09.002
35. Kernie, S., Liebl, D. J., and Parada, F. B. (2000). BDNF regulates eating behavior and locomotor activity in mice. EMBO J. 19, 1290-1300. doi: 10.1093/emboj/19.6.1290
36. Kim, H., Gibboni, R., Kirkhart, C., and Bao, S. (2013a). Impaired critical period plasticity in primary auditory cortex of fragile X model mice. J. Neurosci. 33, 15686-15692. doi: 10.1523/JNEUROSCI.3246-12.2013
37. +]i spikes and excitotoxicity in cultured rat hippocampal neurons. Brain Res. 1490, 23-34. doi: 10.1016/j.brainres.2012.10.062
38. Kiryanova, V., McAllister, B., and Dyck, R. (2013). Long-term outcomes of developmental exposure to fluoxetine: a review of the animal literature. Dev. Neurosci. 35, 437-439. doi: 10.1159/000355709
39. Koponen, E., Rantamäki, T., Voikar, V., Saarelainen, T., MacDonald, E., and Castrén, E. (2005). Enhanced BDNF signaling is associated with an antidepressant-like behavioral response and changes in brain monoamines. Cell. Mol. Neurobiol. 25, 973-980. doi: 10.1007/s10571-005-8468-z
40. Lebrand, C., Cases, O., Adelbrecht, C., Doye, A., Alvarez, C., El Mestikawy, S., et al. (1996). Transient uptake and storage of serotonin in developing thalamic neurons. Neuron 17, 823-835. doi: 10.1016/S0896-6273(00)80215-9
41. Louhivuori, V., Vicario, A., Uutela, M., Rantamäki, T., Louhivuori, L. M., Castrén, E., et al. (2011). BDNF and TrkB in neuronal differentiation of Fmr1-knockout mouse. Neurobiol. Dis. 41, 469-480. doi: 10.1016/j.nbd.2010.10.018
42. Luo, Y., Shan, G., Guo, W., Smrt, R. D., Johnson, E. B., Li, X., et al. (2010). Fragile x mental retardation protein regulates proliferation and differentiation of adult neural stem/progenitor cells. PLoS Genet. 6:e1000898. doi: 10.1371/journal.pgen.1000898
43. Lyons, W. E., Maumonas, L. A., Ricaurte, G. A., Coppola, V., Reid, S. W., Bora, S. H., et al. (1999). Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc. Natl. Acad. Sci. U.S.A. 96, 15239-15244. doi: 10.1073/pnas.96.26.15239
44. MacQueen, G., Ramakrishnan, K., Croll, S. D., Siuciak, J. A., Yu, G., Young, L. T., et al. (2001). Performance of heterozygous brain-derived neurotrophic factor knockout mice on behavioral analogues of anxiety, nociception, and depression. Behav. Neurosci. 115, 1145-1153. doi: 10.1037/0735-7044.115.5.1145
45. Makkonen, I., Riikonen, R., Kuikka, J. T., Kokki, H., Bressler, J., Marshall, C., et al. (2011). Brain derived neurotrophic factor and serotonin transporter binding as markers of clinical response to fluoxetine therapy in children with autism. J. Pediatr. Neurol. 9, 1-8. doi: 10.3233/JPN-2010-0446
46. Maya-Vetencourt, J., Sale, A., Viegi, A., Baroncelli, L., De Pasquale, R., O'Leary, O., et al. (2008). The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320, 385-388. doi: 10.1126/science.1150516
47. Mineur, Y. S., Huynh, L. X., and Crusio, W. E. (2006). Social behavior deficits in the Fmr1 mutant mouse. Behav. Brain Res. 168, 172-175. doi: 10.1016/j.bbr.2005.11.004
48. Mineur, Y. S., Sluyter, F., De Wit, S., Oostra, B. A., and Crusio, W. E. (2002). Behavioral and neuroanatomical characterization of the Fmr1 knockout mouse. Hippocampus 12, 39-46. doi: 10.1002/hipo.10005
49. Miyazaki, K., Narita, N., Sakuta, R., Miyahara, T., Naruse, H., Okado, N., et al. (2004). Serum neurotrophin concentrations in autism and mental retardation: a pilot study. Brain Dev. 26, 292-295. doi: 10.1016/S0387-7604(03)00168-2
50. Monteggia, L. M., Luikart, B., Barrot, M., Theobold, D., Malkovska, I., Nef, S., et al. (2007). Brain-derived neurotrophic factor conditional knockouts show gender differences in depression-related behaviors. Biol. Psychiatry 15, 187-197. doi: 10.1016/j.biopsych.2006.03.021
51. Nelson, K., Grether, J. K., Croen, L. A., Dambrosia, J. M., Dickens, B. F., Jelliffe, L. L., et al. (2001). Neuropeptides and neurotrophins in neonatal blood of children with autism or mental retardation. Ann. Neurol. 49, 597-606. doi: 10.1002/ana.1024
52. Nibuya, M., Morinobu, S., and Duman, R. S. (1995). Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci. 15, 7539-7547.
53. Nielsen, D. M., Derber, W. J., McClellan, D. A., and Crnic, L. S. (2002). Alterations in the auditory startle response in Fmr1 targeted mutant mouse models of fragile X syndrome. Brain Res. 927. 8-17. doi: 10.1016/S0006-8993(01)03309-1
54. Oswald, D. P., and Sonenklar, N. A. (2007). Medication use among children with autism spectrum disorders. J. Child Adolesc. Psychopharmacol. 17, 348-355. doi: 10.1089/cap.2006.17303
55. Peier, A. M., McIlwain, K. L., Kenneson, A., Warren, S. T., Paylor, R., and Nelson, D. L. (2000). (Over)correction of FMR1 deficiency with YAC transgenics: behavioral and physical features. Hum. Mol. Genet. 9, 1145-1159. doi: 10.1093/hmg/9.8.1145
56. Perry, E. K., Lee, M. L. W., Martin-Ruiz, C. M., Court, J. A., Volsen, S. G., Merrit, J., et al. (2001). Cholinergic activity in autism: abnormalities in the cerebral cortex and basal forebrain. Am. J. Psychiatry 158, 1058-1066. doi: 10.1176/appi.ajp.158.7.1058
57. Piven, J., Tsai, G., Nehme, E., Coyle, J., Chase, G., and Folstein, S. (1991). Platelet serotonin, a possible marker for familial autism. J. Autism Dev. Disord. 21, 51-59. doi: 10.1007/BF02206997
58. Porsolt, R. D., Le Pichon, M., and Jalfre, M. (1977). Depression: a new animal model sensitive to antidepressant treatments. Nature 266, 730-732. doi: 10.1038/266730a0
59. Prut, L., and Belzung, C. (2003). The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463, 3-33. doi: 10.1016/S0014-2999(03)01272-X
60. Rattiner, L. M., Davis, M., French, C. T., and Ressler, K. J. (2004). Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. J. Neurosci. 19, 4796-4806. doi: 10.1523/JNEUROSCI.5654-03.2004
61. Rios, M., Fan, G., Fekete, C., Kelly, J., Bates, B., Kuehn, R., et al. (2001). Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol. Endocrinol. 15, 1748-1757. doi: 10.1210/mend.15.10.0706
62. Saarelainen, T., Hendolin, P., Lucas, G., Koponen, E., Sairanen, M., MacDonald, E., et al. (2003). Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioural effects. J. Neurosci. 23, 349-357.
63. Sairanen, M., Lucas, G., Ernfors, P., Castrén, M., and Castrén, E. (2005). BDNF signaling and antidepressant drugs differentially but coordinatedly regulate neurogenesis, survival and turnover of new-born neurons in the adult dentate gyrus. J. Neurosci. 25, 1089-1094. doi: 10.1523/JNEUROSCI.3741-04.2005
64. Spencer, C. M., Alekseyenko, O., Serysheva, E., Yuva-Paylor, L. A., and Paylor, R. (2005). Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav. 4, 420-430. doi: 10.1111/j.1601-183X.2005.00123.x
65. Uutela, M., Lindholm, J., Louhivuori, V., Wei, H., Louhivuori, L. M., Pertovaara, A., et al. (2012). Reduction of BDNF expression in Fmr1 knockout mice worsens cognitive deficits but improves hyperactivity and sensorimotor deficits. Genes Brain Behav. 5, 513-523. doi: 10.1111/j.1601-183X.2012.00784.x
66. Van Dam, D., D'Hooge, R., Hauben, E., Reyniers, E., Gantois, I., Bakker, C. E., et al. (2000). Spatial learning, contextual fear conditioning and conditioned emotional response in Fmr1 knockout mice. Behav. Brain Res. 117, 127-136. doi: 10.1016/S0166-4328(00)00296-5
67. Warner-Schmidt, J. L., and Duman, R. S. (2006). Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 16, 239-249. doi: 10.1002/hipo.20156
68. Williams, K., Brignell, A., Randall, M., Silove, N., and Hazell, P. (2013). Selective serotonin reuptake inhibitors (SSRIs) for autism spectrum disorders (ASD). Cochrane Database. Syst. Rev. 20, CD004677. doi: 10.1002/14651858.CD004677.pub3
69. Wisden, W., and Morris, B. (1994). "In situ hybridization with synthetic oligonucleotide probes, " in In Situ Protocols for Neurobiology, eds W. Wisden and B. Morris (London: Academic Press), 1-34.
70. Vitalis, T., and Parnavelas, J. G. (2003). The role of serotonin in early cortical development. Dev. Neurosci. 25, 245-256. doi: 10.1159/000072272
71. Wong, D. T., Horng, J. S., Bymaster, F. P., Hauser, K. L., and Molloy, B. B. (1974). A selective inhibitor of serotonin uptake: Lilly 110140, 3-(p-trifluoromethylphenoxy)-N-methyl-3 phenylpropylamine. Life Sci. 15, 471-479. doi: 10.1016/0024-3205(74)90345-2
72. Wu, X., and Castrén, E. (2009). Co-treatment with diazepam prevents the effects of fluoxetine on the proliferation and survival of hippocampal dentate granule cells. Biol. Psychiatry 66, 5-8. doi: 10.1016/j.biopsych.2009.01.023
73. Xu, Z., Yang, Q., Ma, L., Liu, S., Chen, G., Wu, Y., et al. (2012). Deficits in LTP induction by 5-HT2A receptor antagonist in a mouse model for fragile X syndrome. PLoS ONE 7:e48741. doi: 10.1371/journal.pone.0048741
74. Zhao, M. G., Toyoda, H., Ko, S. W., Ding, H. K., Wu, L. J., and Zhuo, M. (2005). Deficits in trace fear memory and long-term potentiation in a mouse model for Fragile X syndrome. J. Neurosci. 25, 7385-7392. doi: 10.1523/JNEUROSCI.1520-05.2005