Behavioral inhibition and impaired spatial learning and memory in hypothyroid mice lacking thyroid hormone receptor α

Behavioural Brain Research

Volumn 177, Issue 1, 2007, Pages 109-116

  Wilcoxon, Jennifer Slone ^a   Nadolski, Gregory J ^a   Samarut, Jacques ^b   Chassande, Olivier ^c   Redei, Eva E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITÉ DE LYON   (France)

^c INSERM   (France)

Author keywords

Forced swim test; GAP 43; Glucocorticoid receptor; Morris water maze; Neurogranin; Open field test; PTU; T4

Indexed keywords

GLUCOCORTICOID RECEPTOR; NEUROGRANIN; NEUROMODULIN; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA; THYROXINE;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR DISORDER; BRAIN REGION; COGNITIVE DEFECT; CONTROLLED STUDY; EUTHYROIDISM; FEAR; FORCED SWIMMING TEST; GENE CONTROL; GENE EXPRESSION; GENE INTERACTION; HIPPOCAMPUS; HORMONAL REGULATION; HYPERTHYROIDISM; HYPOTHYROIDISM; IMMOBILIZATION; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; MOUSE; NONHUMAN; OPEN FIELD TEST; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RECALL; SPATIAL MEMORY; TISSUE DISTRIBUTION;

EID: 33846144179     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2006.10.030     Document Type: Article

References (61)

1. Adams P.M., Stein S.A., Palnitkar M., Anthony A., Gerrity L., and Shanklin D.R. Evaluation and characterization of the hypothyroid hyt/hyt mouse. I. Somatic and behavioral studies. Neuroendocrinology 49 (1989) 138-143
2. Akaike M., Kato N., Ohno H., and Kobayashi T. Hyperactivity and spatial maze learning impairment of adult rats with temporary neonatal hypothyroidism. Neurotoxicol Teratol 13 (1991) 317-322
3. Anthony A., Adams P.M., and Stein S.A. The effects of congenital hypothyroidism using the hyt/hyt mouse on locomotor activity and learned behavior. Horm Behav 27 (1993) 418-433
4. Aronsson M., Fuxe K., Dong Y., Agnati L.F., Okret S., and Gustafsson J.A. Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridisation. Proc Natl Acad Sci USA 85 (1988) 9331-9335
5. Auso E., Lavado-Autric R., Cuevas E., Del Rey F.E., Morreale De Escobar G., and Berbel P. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 145 (2004) 4037-4047
6. Bachmann C.G., Bilang-Bleuel A., De Carli S., Linthorst A.C., and Reul J.M. The selective glucocorticoid receptor antagonist ORG 34116 decreases immobility time in the forced swim test and affects cAMP-responsive element-binding protein phosphorylation in rat brain. Neuroendocrinology 81 (2005) 129-136
7. Bast T., Zhang W.N., and Feldon J. Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABA(A) receptor antagonist picrotoxin. Psychopharmacology (Berl) 156 (2001) 225-233
8. Baxter M.G., and Murray E.A. The amygdala and reward. Nat Rev Neurosci 3 (2002) 563-573
9. Borsini F., and Meli A. Is the forced swimming test a suitable model for revealing antidepressant activity?. Psychopharmacology (Berl) 94 (1988) 147-160
10. Burgos-Trinidad M., and Koenig R.J. Dominant negative activity of thyroid hormone receptor variant alpha2 and interaction with nuclear corepressors. Mol Cell Endocrinol 149 (1999) 107-114
11. de Escobar G.M., Obregon M.J., and del Rey F.E. Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract Res Clin Endocrinol Metab 18 (2004) 225-248
12. Forrest D. The developing brain and maternal thyroid hormone: finding the links. Endocrinology 145 (2004) 4034-4036
13. Forrest D., Golarai G., Connor J., and Curran T. Genetic analysis of thyroid hormone receptors in development and disease. Recent Prog Horm Res 51 (1996) 1-22
14. Forrest D., Hanebuth E., Smeyne R.J., Everds N., Stewart C.L., Wehner J.M., et al. Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor beta: evidence for tissue-specific modulation of receptor function. EMBO J 15 (1996) 3006-3015
15. Fraichard A., Chassande O., Plateroti M., Roux J.P., Trouillas J., Dehay C., et al. The T3R alpha gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production. EMBO J 16 (1997) 4412-4420
16. Gauthier K., Plateroti M., Harvey C.B., Williams G.R., Weiss R.E., Refetoff S., et al. Genetic analysis reveals different functions for the products of the thyroid hormone receptor alpha locus. Mol Cell Biol 21 (2001) 4748-4760
17. Gerendasy D.D., and Sutcliffe J.G. RC3/neurogranin, a postsynaptic calpacitin for setting the response threshold to calcium influxes. Mol Neurobiol 15 (1997) 131-163
18. Gothe S., Wang Z., Ng L., Kindblom J.M., Barros A.C., Ohlsson C., et al. Mice devoid of all known thyroid hormone receptors are viable but exhibit disorders of the pituitary-thyroid axis, growth, and bone maturation. Genes Dev 13 (1999) 1329-1341
19. Guadano-Ferraz A., Benavides-Piccione R., Venero C., Lancha C., Vennstrom B., Sandi C., et al. Lack of thyroid hormone receptor alpha1 is associated with selective alterations in behavior and hippocampal circuits. Mol Psychiatr 8 (2003) 30-38
20. Haddow J.E., Palomaki G.E., Allan W.C., Williams J.R., Knight G.J., Gagnon J., et al. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N Engl J Med 341 (1999) 549-555
21. Hashimoto K., Curty F.H., Borges P.P., Lee C.E., Abel E.D., Elmquist J.K., et al. An unliganded thyroid hormone receptor causes severe neurological dysfunction. Proc Natl Acad Sci USA 98 (2001) 3998-4003
22. Hsu J.-H., and Brent G.A. Thyroid hormone receptor gene knockouts. Trends Endocrinol Metab (1998) 103-112
23. Iniguez M.A., Rodriguez-Pena A., Ibarrola N., Aguilera M., Munoz A., and Bernal J. Thyroid hormone regulation of RC3, a brain-specific gene encoding a protein kinase-C substrate. Endocrinology 133 (1993) 467-473
24. Jefferys D., Copolov D., Irby D., and Funder J. Behavioural effect of adrenalectomy: reversal by glucocorticoids or [D-Ala2,Met5]enkephalinamide. Eur J Pharmacol 92 (1983) 99-103
25. Kulikov A., Torresani J., and Jenningros R. Experimental hypothyroidism increases immobility in rats in the forced swim paradigm. Neurosci Lett 234 (1997) 111-114
26. Lacroix L., Spinelli S., Heidbreder C.A., and Feldon J. Differential role of the medial and lateral prefrontal cortices in fear and anxiety. Behav Neurosci 114 (2000) 1119-1130
27. Lafranchi S.H., Haddow J.E., and Hollowell J.G. Is thyroid inadequacy during gestation a risk factor for adverse pregnancy and developmental outcomes?. Thyroid 15 (2005) 60-71
28. Lavado-Autric R., Auso E., Garcia-Velasco J.V., Arufe Mdel C., Escobar del Rey F., Berbel P., et al. Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 111 (2003) 1073-1082
29. Lazar M.A., Hodin R.A., Darling D.S., and Chin W.W. Identification of a rat c-erbA alpha-related protein which binds deoxyribonucleic acid but does not bind thyroid hormone. Mol Endocrinol 2 (1988) 893-901
30. Lee I., and Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J Neurosci 23 (2003) 1517-1523
31. Macchia P.E., Takeuchi Y., Kawai T., Cua K., Gauthier K., Chassande O., et al. Increased sensitivity to thyroid hormone in mice with complete deficiency of thyroid hormone receptor alpha. Proc Natl Acad Sci USA 98 (2001) 349-354
32. MacNabb C., O'Hare E., Cleary J., and Georgopoulos A.P. Congenital hypothyroidism impairs response alternation discrimination behavior. Brain Res 847 (1999) 231-239
33. Miyakawa T., Yared E., Pak J.H., Huang F.L., Huang K.P., and Crawley J.N. Neurogranin null mutant mice display performance deficits on spatial learning tasks with anxiety related components. Hippocampus 11 (2001) 763-775
34. Mons N., Enderlin V., Jaffard R., and Higueret P. Selective age-related changes in the PKC-sensitive, calmodulin-binding protein, neurogranin, in the mouse brain. J Neurochem 79 (2001) 859-867
35. Morte B., Manzano J., Scanlan T., Vennstrom B., and Bernal J. Deletion of the thyroid hormone receptor alpha 1 prevents the structural alterations of the cerebellum induced by hypothyroidism. Proc Natl Acad Sci USA 99 (2002) 3985-3989
36. Munoz A., Rodriguez-Pena A., Perez-Castillo A., Ferreiro B., Sutcliffe J.G., and Bernal J. Effects of neonatal hypothyroidism on rat brain gene expression. Mol Endocrinol 5 (1991) 273-280
37. Namgung U., and Routtenberg A. Transcriptional and post-transcriptional regulation of a brain growth protein: regional differentiation and regeneration induction of GAP-43. Eur J Neurosci 12 (2000) 3124-3136
38. Oitzl M.S., Fluttert M., Sutanto W., and de Kloet E.R. Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. Eur J Neurosci 10 (1998) 3759-3766
39. Oppenheimer J.H., and Schwartz H.L. Molecular basis of thyroid hormone-dependent brain. Endocr Rev 18 (1997) 462-475
40. Pascale A., Gusev P.A., Amadio M., Dottorini T., Govoni S., Alkon D.L., et al. Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc Natl Acad Sci USA 101 (2004) 1217-1222
41. Paxinos G, Franklin KBJ. The mouse brain in stereotaxic coordinates; Compact second edition, 2003.
42. Pop V.J., Kuijpens J.L., van Baar A.L., Verkerk G., van Son M.M., de Vijlder J.J., et al. Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin Endocrinol 50 (1999) 155-159
43. Porsolt R.D., Bertin A., and Jalfre M. Behavioral despair in mice: a primary screening test for anitdepressants. Archives Internationales de Pharmacodynamie et de Therapie 229 (1977) 327-336
44. Prange Jr. A.J., Lara P.P., Wilson I.C., Alltop L.B., and Breese G.R. Effects of thyrotropin-releasing hormone in depression. Lancet 2 (1972) 999-1002
45. Redei E., Halasz I., Li L.F., Prystowsky M.B., and Aird F. Maternal adrenalectomy alters the immune and endocrine functions of fetal alcohol-exposed male offspring. Endocrinology 133 (1993) 452-460
46. Redei E.E., Solberg L.C., Kluczynski J.M., and Pare W.P. Paradoxical hormonal and behavioral responses to hypothyroid and hyperthyroid states in the Wistar-Kyoto rat. Neuropsychopharmacology 24 (2001) 632-639
47. Rittenhouse P.A., and Redei E. Thyroxine administration prevents streptococcal cell wall-induced inflammatory responses. Endocrinology 138 (1997) 1434-1439
48. Routtenberg A., Cantallops I., Zaffuto S., Serrano P., and Namgung U. Enhanced learning after genetic overexpression of a brain growth protein. Proc Natl Acad Sci USA 97 (2000) 7657-7662
49. Sadow P.M., Koo E., Chassande O., Gauthier K., Samarut J., Xu J., et al. Thyroid hormone receptor-specific interactions with steroid receptor coactivator-1 in the pituitary. Mol Endocrinol 17 (2003) 882-894
50. Sala-Roca J., Marti-Carbonell M.A., Garau A., Darbra S., and Balada F. Effects of dysthyroidism in plus maze and social interaction tests. Pharmacol Biochem Behav 72 (2002) 643-650
51. Salto C., Kindblom J.M., Johansson C., Wang Z., Gullberg H., Nordstrom K., et al. Ablation of TRalpha2 and a concomitant overexpression of alpha1 yields a mixed hypo- and hyperthyroid phenotype in mice. Mol Endocrinol 15 (2001) 2115-2128
52. Sap J., Munoz A., Damm K., Goldberg Y., Ghysdael J., Leutz A., et al. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature 324 (1986) 635-640
53. Slone J.L., and Redei E.E. Maternal alcohol and adrenalectomy: asynchrony of stress response and forced swim behavior. Neurotoxicol Teratol 24 (2002) 173-178
54. Tagami T., Kopp P., Johnson W., Arseven O.K., and Jameson J.L. The thyroid hormone receptor variant alpha2 is a weak antagonist because it is deficient in interactions with nuclear receptor corepressors. Endocrinology 139 (1998) 2535-2544
55. van Boxtel M.P., Menheere P.P., Bekers O., Hogervorst E., and Jolles J. Thyroid function, depressed mood, and cognitive performance in older individuals: the Maastricht Aging Study. Psychoneuroendocrinology 29 (2004) 891-898
56. Vasudevan N., Morgan M., Brewer C., Forrest D., Vennstrom B., Pfaff D.W., and Ogawa S. Distinct behavioral phenotypes in male mice lacking the thyroid hormone receptor (TR)α1 versus the TRβ gene isoforms. Soc Neurosci Abstr (2001) 955.10
57. Versloot P.M., van der Heide D., Schroder-van der Elst J.P., and Boogerd L. Maternal thyroxine and 3,5,3′-tri-iodothyronine kinetics in near-term pregnant rats at two different levels of hypothyroidism. Eur J Endocrinol 138 (1998) 113-119
58. Weinberger C., Thompson C.C., Ong E.S., Lebo R., Gruol D.J., and Evans R.M. The c-erb-A gene encodes a thyroid hormone receptor. Nature 324 (1986) 641-646
59. Wikstrom L., Johansson C., Salto C., Barlow C., Campos Barros A., Baas F., et al. Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor alpha 1. EMBO J 17 (1998) 455-461
60. Young E.A., Owen E.H., Meiri K.F., and Wehner J.M. Alterations in hippocampal GAP-43 phosphorylation and protein level following contextual fear conditioning. Brain Res 860 (2000) 95-103
61. Zoeller R.T. Transplacental thyroxine and fetal brain development. J Clin Invest 111 (2003) 954-957