The deletion of the microtubule-associated STOP protein affects the serotonergic mouse brain network

Journal of Neurochemistry

Volumn 115, Issue 6, 2010, Pages 1579-1594

  Fournet, Vincent ^a,b   Jany, Marion ^b   Fabre, Véronique ^c   Chali, Farah ^a   Orsal, Didier ^a   Schweitzer, Annie ^b   Andrieux, Annie ^b   Messanvi, Fany ^a   Giros, Bruno ^a   Hamon, Michel ^a   Lanfumey, Laurence ^a   Deloulme, Jean Christophe ^b   Martres, Marie Pascale ^a  

^a INSERM   (France)

^b GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^c INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

Author keywords

anxiety depression; electrophysiology; neurogenesis; schizoaffective disorders; stable tubule only polypeptide; STOP KO mice

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; AUTORECEPTOR; HYDROLASE; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN STABLE TUBULE ONLY PEPTIDE; SEROTONIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANXIETY DISORDER; ARTICLE; BRAIN REGION; BRAIN STEM; CONTROLLED STUDY; DEPRESSION; ENZYME ACTIVITY; FEMALE; FRONTAL CORTEX; GENE DELETION; HIPPOCAMPUS; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PUTAMEN; RAPHE NUCLEUS; SEROTONINERGIC SYSTEM; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

ANIMALS; BRAIN; FEMALE; MALE; MAZE LEARNING; MICE; MICE, 129 STRAIN; MICE, INBRED BALB C; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NERVE NET; SEROTONIN;

MUS;

EID: 78649998201     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07064.x     Document Type: Article

References (68)

1. Aguezzoul M., Andrieux A., and, Denarier E., (2003) Overlap of promoter and coding sequences in the mouse STOP gene (Mtap6). Genomics 81, 623-627.
2. Andrieux A., Salin P. A., Vernet M., et al. (2002) The suppression of brain cold-stable microtubules in mice induces synaptic defects associated with neuroleptic-sensitive behavioral disorders. Genes Dev. 16, 2350-2364.
3. Andrieux A., Salin P., Schweitzer A., et al. (2006) Microtubule stabilizer ameliorates synaptic function and behavior in a mouse model for schizophrenia. Biol. Psychiatry 60, 1224-1230.
4. Antri M., Mouffle C., Orsal D., and, Barthe J. Y., (2003) 5-HT1A receptors are involved in short- and long-term processes responsible for 5-HT-induced locomotor function recovery in chronic spinal rat. Eur. J. Neurosci. 18, 1963-1972.
5. Azmitia E. C., and, Segal M., (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J. Comp. Neurol. 179, 641-667.
6. Baratier J., Peris L., Brocard J., et al. (2006) Phosphorylation of microtubule-associated protein STOP by calmodulin kinase II. J. Biol. Chem. 281, 19561-19569.
7. Bechtholt A. J., Hill T. E., and, Lucki I., (2007) Anxiolytic effect of serotonin depletion in the novelty-induced hypophagia test. Psychopharmacology (Berl) 190, 531-540.
8. Begou M., Brun P., Bertrand J. B., Job D., Schweitzer A., D'Amato T., Saoud M., Andrieux A., and, Suaud-Chagny M. F., (2007) Post-pubertal emergence of alterations in locomotor activity in stop null mice. Synapse 61, 689-697.
9. Begou M., Volle J., Bertrand J. B., et al. (2008) The stop null mice model for schizophrenia displays [corrected] cognitive and social deficits partly alleviated by neuroleptics. Neuroscience 157, 29-39.
10. Bengel D., Murphy D. L., Andrews A. M., Wichems C. H., Feltner D., Heils A., Mossner R., Westphal H., and, Lesch K.-P., (1998) Altered brain serotonin homeostasis and locomotor insensitivity to 3,4-methylenedioxymethamphetamine ("ecstasy") in serotonin transporter-deficient mice. Mol. Pharmacol. 53, 649-655.
11. Bernard J. F., Netzer F., Gau R., Hamon M., Laguzzi R., and, Sevoz-Couche C., (2008) Critical role of B3 serotonergic cells in baroreflex inhibition during the defense reaction triggered by dorsal periaqueductal gray stimulation. J. Comp. Neurol. 506, 108-121.
12. Bianchi M., Hagan J. J., and, Heidbreder C. A., (2005) Neuronal plasticity, stress and depression: involvement of the cytoskeletal microtubular system? Curr. Drug Targets CNS Neurol. Disord. 4, 597-611.
13. Bianchi M., Shah A. J., Fone K. C., Atkins A. R., Dawson L. A., Heidbreder C. A., Hows M. E., Hagan J. J., and, Marsden C. A., (2009) Fluoxetine administration modulates the cytoskeletal microtubular system in the rat hippocampus. Synapse 63, 359-364.
14. Bosc C., Cronk J. D., Pirollet F., Watterson D. M., Haiech J., Job D., and, Margolis R. L., (1996) Cloning, expression, and properties of the microtubule-stabilizing protein STOP. Proc. Natl Acad. Sci. USA 93, 2125-2130.
15. Bouvrais-Veret C., Weiss S., Andrieux A., Schweitzer A., McIntosh J. M., Job D., Giros B., and, Martres M. P., (2007) Sustained increase of alpha7 nicotinic receptors and choline-induced improvement of learning deficit in STOP knock-out mice. Neuropharmacology 52, 1691-1700.
16. Bouvrais-Veret C., Weiss S., Hanoun N., Andrieux A., Schweitzer A., Job D., Hamon M., Giros B., and, Martres M. P., (2008) Microtubule-associated STOP protein deletion triggers restricted changes in dopaminergic neurotransmission. J. Neurochem. 104, 745-756.
17. Brenner E., Sonnewald U., Schweitzer A., Andrieux A., and, Nehlig A., (2007) Hypoglutamatergic activity in the STOP knockout mouse: a potential model for chronic untreated schizophrenia. J. Neurosci. Res. 85, 3487-3493.
18. Brun P., Begou M., Andrieux A., et al. (2005) Dopaminergic transmission in STOP null mice. J. Neurochem. 94, 63-73.
19. Camargo L. M., Collura V., Rain J. C., Mizuguchi K., Hermjakob H., Kerrien S., Bonnert T. P., Whiting P. J., and, Brandon N. J., (2007) Disrupted in Schizophrenia 1 Interactome: evidence for the close connectivity of risk genes and a potential synaptic basis for schizophrenia. Mol. Psychiatry 12, 74-86.
20. Carrel D., Masson J., Al Awabdh S., Capra C. B., Lenkei Z., Hamon M., Emerit M. B., and, Darmon M., (2008) Targeting of the 5-HT1A serotonin receptor to neuronal dendrites is mediated by Yif1B. J. Neurosci. 28, 8063-8073.
21. Caspi A., Sugden K., Moffitt T. E., et al. (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389.
22. Clapcote S. J., Lipina T. V., Millar J. K., et al. (2007) Behavioral phenotypes of Disc1 missense mutations in mice. Neuron 54, 387-402.
23. Cornea-Hébert V., Watkins K. C., Roth B. L., Kroeze W. K., Gaudreau P., Leclerc N., and, Descarries L., (2002) Similar ultrastructural distribution of the 5-HT(2A) serotonin receptor and microtubule-associated protein MAP1A in cortical dendrites of adult rat. Neuroscience 113, 23-35.
24. Cornea-Hébert V., Riad M., Wu C., Singh S. K., and, Descarries L., (1999) Cellular and subcellular distribution of the serotonin 5-HT2A receptor in the central nervous system of adult rat. J. Comp. Neurol. 409, 187-209.
25. Couegnas A., Schweitzer A., Andrieux A., Ghandour M. S., and, Boehm N., (2007) Expression pattern of STOP lacZ reporter gene in adult and developing mouse brain. J. Neurosci. Res. 85, 1515-1527.
26. Craddock N., and, Forty L., (2006) Genetics of affective (mood) disorders. Eur. J. Hum. Genet. 14, 660-668.
27. David D. J., Samuels B. A., Rainer Q., et al. (2009) Neurogenesis- dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479-493.
28. Delotterie D., Ruiz G., Brocard J., Schweitzer A., Roucard C., Roche Y., Suaud-Chagny M. F., Bressand K., and, Andrieux A., (2009) Chronic administration of atypical antipsychotics improves behavioral and synaptic defects of STOP null mice. Psychopharmacology (Berl), 208, 131-141.
29. Denarier E., Aguezzoul M., Jolly C., Vourc'h C., Roure A., Andrieux A., Bosc C., and, Job D., (1998) Genomic structure and chromosomal mapping of the mouse STOP gene (Mtap6). Biochem. Biophys. Res. Commun. 243, 791-796.
30. Desbonnet L., Waddington J. L., and, Tuathaigh C. M., (2009) Mice mutant for genes associated with schizophrenia: common phenotype or distinct endophenotypes? Behav. Brain Res. 204, 258-273.
31. Dranovsky A., and, Hen R., (2006) Hippocampal neurogenesis: regulation by stress and antidepressants. Biol. Psychiatry 59, 1136-1143.
32. Duan X., Chang J. H., Ge S., et al. (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130, 1146-1158. (Pubitemid 47422304)
33. Eastwood S. L., Lyon L., George L., Andrieux A., Job D., and, Harrison P. J., (2007) Altered expression of synaptic protein mRNAs in STOP (MAP6) mutant mice. J. Psychopharmacol. 21, 635-644.
34. Eisch A. J., Cameron H. A., Encinas J. M., Meltzer L. A., Ming G. L., and, Overstreet-Wadiche L. S., (2008) Adult neurogenesis, mental health, and mental illness: hope or hype? J. Neurosci. 28, 11785-11791.
35. Fabre V., Beaufour C., Evrard A., et al. (2000a) Altered expression and functions of serotonin 5-HT1A and 5-HT1B receptors in knock-out mice lacking the 5-HT transporter. Eur. J. Neurosci. 12, 2299-2310.
36. Fabre V., Boutrel B., Hanoun N., Lanfumey L., Fattaccini C. M., Demeneix B., Adrien J., Hamon M., and, Martres M. P., (2000b) Homeostatic regulation of serotonergic function by the serotonin transporter as revealed by nonviral gene transfer. J. Neurosci. 20, 5065-5075.
37. Fradley R. L., O'Meara G. F., Newman R. J., Andrieux A., Job D., and, Reynolds D. S., (2005) STOP knockout and NMDA NR1 hypomorphic mice exhibit deficits in sensorimotor gating. Behav. Brain Res. 163, 257-264.
38. Frankle W. G., Lerma J., and, Laruelle M., (2003) The synaptic hypothesis of schizophrenia. Neuron 39, 205-216.
39. Franklin K. B., and, Paxinos G., (1997) The Mouse Brain in Stereotaxic Coordinates. Academic Press, Inc., San Diego, CA, USA.
40. Galiano M. R., Bosc C., Schweitzer A., Andrieux A., Job D., and, Hallak M. E., (2004) Astrocytes and oligodendrocytes express different STOP protein isoforms. J. Neurosci. Res. 78, 329-337.
41. Gaspar P., Cases O., and, Maroteaux L., (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat. Rev. Neurosci. 4, 1002-1012.
42. Gottesman I. I., Laursen T. M., Bertelsen A., and, Mortensen P. B., (2010) Severe mental disorders in offspring with 2 psychiatrically ill parents. Arch. Gen. Psychiatry 67, 252-257.
43. Guillaud L., Bosc C., Fourest-Lieuvin A., Denarier E., Pirollet F., Lafanechere L., and, Job D., (1998) STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J. Cell Biol. 142, 167-179.
44. Hanaya R., Koning E., Ferrandon A., Schweitzer A., Andrieux A., and, Nehlig A., (2008) Deletion of the STOP gene, a microtubule stabilizing factor, leads only to discrete cerebral metabolic changes in mice. J. Neurosci. Res. 86, 813-820.
45. Jennings K. A., Loder M. K., Sheward W. J., et al. (2006) Increased expression of the 5-HT transporter confers a low-anxiety phenotype linked to decreased 5-HT transmission. J. Neurosci. 26, 8955-8964.
46. Lapointe N. P., Ung R. V., Bergeron M., Cote M., and, Guertin P. A., (2006) Strain-dependent recovery of spontaneous hindlimb movement in spinal cord transected mice (CD1, C57BL/6, BALB/c). Behav. Neurosci. 120, 826-834.
47. Laursen T. M., Labouriau R., Licht R. W., Bertelsen A., Munk-Olsen T., and, Mortensen P. B., (2005) Family history of psychiatric illness as a risk factor for schizoaffective disorder: a Danish register-based cohort study. Arch. Gen. Psychiatry 62, 841-848.
48. Leonardo E. D., and, Hen R., (2006) Genetics of affective and anxiety disorders. Annu. Rev. Psychol. 57, 117-137.
49. Lewis C. M., Levinson D. F., Wise L. H., et al. (2003) Genome scan meta-analysis of schizophrenia and bipolar disorder, part II: Schizophrenia. Am. J. Hum. Genet. 73, 34-48.
50. Lucki I., (1998) The spectrum of behaviors influenced by serotonin. Biol. Psychiatry 44, 151-162.
51. Mannoury la Cour C., Boni C., Hanoun N., Lesch K. P., Hamon M., and, Lanfumey L., (2001) Functional consequences of 5-HT transporter gene disruption on 5-HT(1a) receptor-mediated regulation of dorsal raphe and hippocampal cell activity. J. Neurosci. 21, 2178-2185.
52. Murphy D. L., and, Lesch K. P., (2008) Targeting the murine serotonin transporter: insights into human neurobiology. Nat. Rev. Neurosci. 9, 85-96.
53. Narboux-Neme N., Pavone L. M., Avallone L., Zhuang X., and, Gaspar P., (2008) Serotonin transporter transgenic (SERTcre) mouse line reveals developmental targets of serotonin specific reuptake inhibitors (SSRIs). Neuropharmacology 55, 994-1005.
54. Ozaki N., Goldman D., Kaye W. H., Plotnicov K., Greenberg B. D., Lappalainen J., Rudnick G., and, Murphy D. L., (2003) Serotonin transporter missense mutation associated with a complex neuropsychiatric phenotype. Mol. Psychiatry 8, 933-936. (Pubitemid 37421700)
55. Parras C. M., Galli R., Britz O., et al. (2004) Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23, 4495-4505.
56. Perez J., Mori S., Caivano M., Popoli M., Zanardi R., Smeraldi E., and, Racagni G., (1995) Effects of fluvoxamine on the protein phosphorylation system associated with rat neuronal microtubules. Eur. Neuropsychopharmacol. 5 (Suppl), 65-69.
57. Powell K. J., Hori S. E., Leslie R., Andrieux A., Schellinck H., Thorne M., and, Robertson G. S., (2007) Cognitive impairments in the STOP null mouse model of schizophrenia. Behav. Neurosci. 121, 826-835.
58. Raponi E., Agenes F., Delphin C., Assard N., Baudier J., Legraverend C., and, Deloulme J. C., (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55, 165-177.
59. Robertson G. S., Hori S. E., and, Powell K. J., (2006) Schizophrenia: an integrative approach to modelling a complex disorder. J. Psychiatry Neurosci. 31, 157-167.
60. Ross C. A., Margolis R. L., Reading S. A., Pletnikov M., and, Coyle J. T., (2006) Neurobiology of schizophrenia. Neuron 52, 139-153.
61. Shimizu H., Iwayama Y., Yamada K., et al. (2006) Genetic and expression analyses of the STOP (MAP6) gene in schizophrenia. Schizophr. Res. 84, 244-252.
62. Sun H., Hu X. Q., Emerit M. B., Schoenebeck J. C., Kimmel C. E., Peoples R. W., Miko A., and, Zhang L., (2008) Modulation of 5-HT3 receptor desensitization by the light chain of microtubule-associated protein 1B expressed in HEK293 cells. J. Physiol. 586, 751-762.
63. Talbot K., Cho D. S., Ong W. Y., et al. (2006) Dysbindin-1 is a synaptic and microtubular protein that binds brain snapin. Hum. Mol. Genet. 15, 3041-3054.
64. Tang H., Wang Y., Xie L., Mao X., Won S. J., Galvan V., and, Jin K., (2009) Effect of neural precursor proliferation level on neurogenesis in rat brain during aging and after focal ischemia. Neurobiol. Aging 30, 299-308.
65. Verge D., Daval G., Marcinkiewicz M., Patey A., El Mestikawy S., Gozlan H., and, Hamon M., (1986) Quantitative autoradiography of multiple 5-HT1 receptor subtypes in the brain of control or 5,7-dihydroxytryptamine-treated rats. J. Neurosci. 6, 3474-3482.
66. Vertes R. P., (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J. Comp. Neurol. 313, 643-668.
67. Vertes R. P., Fortin W. J., and, Crane A. M., (1999) Projections of the median raphe nucleus in the rat. J. Comp. Neurol. 407, 555-582.
68. Whitaker-Azmitia P. M., Borella A., and, Raio N., (1995) Serotonin depletion in the adult rat causes loss of the dendritic marker MAP-2. A new animal model of schizophrenia? Neuropsychopharmacology 12, 269-272.