The bidirectional effects of hypothyroidism and hyperthyroidism on anxiety- and depression-like behaviors in rats

Hormones and Behavior

Volumn 69, Issue , 2015, Pages 106-115

  Yu, Dafu ^a,c,d   Zhou, Heng ^b,c   Yang, Yuan ^a,c,e   Jiang, Yong ^d   Wang, Tianchao ^d   Lv, Liang ^d   Zhou, Qixin ^c   Yang, Yuexiong ^c   Dong, Xuexian ^d   He, Jianfeng ^d   Huang, Xiaoyan ^f   Chen, Jijun ^f   Wu, Kunhua ^d   Xu, Lin ^a,b,c   Mao, Rongrong ^c  

^a YUNNAN UNIVERSITY   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c KUNMING INSTITUTE OF ZOOLOGY   (China)

^d KUNMING UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^e KUNMING MEDICAL UNIVERSITY   (China)

^f KUNMING INSTITUTE OF BOTANY   (China)

Author keywords

Anxiety; Brain derived neurotrophic factor; Depression; Hyperthyroidism; Hypothyroidism

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; IMIPRAMINE; IODINE 131; LEVOTHYROXINE; LIOTHYRONINE; SEROTONIN; THYROXINE; THYROID HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CONTROLLED STUDY; DEPRESSION; ELEVATED PLUS MAZE TEST; FORCED SWIM TEST; HIPPOCAMPUS; HYPERTHYROIDISM; HYPOTHYROIDISM; LIOTHYRONINE BLOOD LEVEL; MALE; NEUROMODULATION; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SEROTONIN BLOOD LEVEL; SUCROSE PREFERENCE TEST; THYROXINE BLOOD LEVEL; ANIMAL; ANIMAL BEHAVIOR; BLOOD; BRAIN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DEPRESSION; HIPPOCAMPUS; HYPERTHYROIDISM; HYPOTHYROIDISM; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; THYROID HORMONES;

EID: 84921818438     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.01.003     Document Type: Article

References (83)

1. Ara I., Bano S. Citalopram decreases tryptophan 2,3-dioxygenase activity and brain 5-HT turnover in swim stressed rats. Pharmacol. Rep. 2012, 64:558-566.
2. Aronson R., Offman H.J., Joffe R.T., Naylor C.D. Triiodothyronine augmentation in the treatment of refractory depression. A meta-analysis. Arch. Gen. Psychiatry 1996, 53:842-848.
3. Ayala C., Valdez S.R., Morero M.L., Soaje M., Carreno N.B., Sanchez M.S., Bittencourt J.C., Jahn G.A., Celis M.E. Hypo- and hyperthyroidism affect NEI concentration in discrete brain areas of adult male rats. Peptides 2011, 32:1249-1254.
4. Bakos B., Takacs I., Nagy Z., Kosa J.P., Balla B., Tobias B., Halaszlaki C., Szili B., Lakatos P. Long term efficacy of radioiodine treatment in hyperthyroidism. Exp. Clin. Endocrinol. Diabetes 2013, 121:494-497.
5. Bartalena L., Bogazzi F., Brogioni S., Burelli A., Scarcello G., Martino E. Measurement of serum free thyroid hormone concentrations: an essential tool for the diagnosis of thyroid dysfunction. Horm. Res. 1996, 45:142-147.
6. Bauer M., Heinz A., Whybrow P.C. Thyroid hormones, serotonin and mood: of synergy and significance in the adult brain. Mol. Psychiatry 2002, 7:140-156.
7. Baumann M.H., Clark R.D., Rothman R.B. Locomotor stimulation produced by 3,4-methylenedioxymethamphetamine (MDMA) is correlated with dialysate levels of serotonin and dopamine in rat brain. Pharmacol. Biochem. Behav. 2008, 90:208-217.
8. Berent D., Zboralski K., Orzechowska A., Galecki P. Thyroid hormones association with depression severity and clinical outcome in patients with major depressive disorder. Mol. Biol. Rep. 2014, 41:2419-2425.
9. Cardenas-Aguayo Mdel C., Kazim S.F., Grundke-Iqbal I., Iqbal K. Neurogenic and neurotrophic effects of BDNF peptides in mouse hippocampal primary neuronal cell cultures. PLoS One 2013, 8:e53596.
10. Carvalho S.C.B.a.G.A.D. The relation between thyroid function and depression: a review. Rev. Bras. Psiquiatr. 2004, 26:8.
11. Casimiro-Lopes G., Alves S.B., Salerno V.P., Passos M.C., Lisboa P.C., Moura E.G. Maximum acute exercise tolerance in hyperthyroid and hypothyroid rats subjected to forced swimming. Horm. Metab. Res. 2008, 40:276-280.
12. Castren E., Rantamaki T. The role of BDNF and its receptors in depression and antidepressant drug action: reactivation of developmental plasticity. Dev. Neurobiol. 2010, 70:289-297.
13. Ceretta L.B., Reus G.Z., Stringari R.B., Ribeiro K.F., Zappellini G., Aguiar B.W., Pfaffenseller B., Lersh C., Kapczinski F., Quevedo J. Imipramine treatment reverses depressive-like behavior in alloxan-diabetic rats. Diabetes Metab. Res. Rev. 2012, 28:139-144.
14. Chang C.M., Sato S., Han C. Evidence for the benefits of nonantipsychotic pharmacological augmentation in the treatment of depression. CNS Drugs 2013, 27(Suppl. 1):S21-S27.
15. Chiu K., Lau W.M., Lau H.T., So K.F., Chang R.C. Micro-dissection of rat brain for RNA or protein extraction from specific brain region. J. Vis. Exp. 2007, 269.
16. Cortes C., Eugenin E., Aliaga E., Carreno L.J., Bueno S.M., Gonzalez P.A., Gayol S., Naranjo D., Noches V., Marassi M.P., Rosenthal D., Jadue C., Ibarra P., Keitel C., Wohllk N., Court F., Kalergis A.M., Riedel C.A. Hypothyroidism in the adult rat causes incremental changes in brain-derived neurotrophic factor, neuronal and astrocyte apoptosis, gliosis, and deterioration of postsynaptic density. Thyroid 2012, 22:951-963.
17. Dalili S., Rezvany S.M., Dadashi A., Medghalchi A., Mohammadi H., Dalili H., Mirzanejad M., Gholamnezhad H., Amirhakimi A. Congenital hypothyroidism: a review of the risk factors. Acta Med. Iran. 2012, 50:735-739.
18. Demet M.M., Ozmen B., Deveci A., Boyvada S., Adiguzel H., Aydemir O. Depression and anxiety in hyperthyroidism. Arch. Med. Res. 2002, 33:552-556.
19. Dhawan D., Singh Baweja M., Dani V. Zinc sulphate following the administration of iodine-131 on the regulation of thyroid function, in rats. Hell. J. Nucl. Med. 2007, 10:167-171.
20. Dias G.R., Vieira F.A., Dobrachinski F., Bridi J.C., Balk Rde S., Soares F.A., Nogueira C.W., Barbosa N.B. Diphenyl diselenide diet intake improves spatial learning and memory deficits in hypothyroid female rats. Int. J. Dev. Neurosci. 2012, 30:83-89.
21. Duntas L.H., Maillis A. Hypothyroidism and depression: salient aspects of pathogenesis and management. Minerva Endocrinol. 2013, 38:365-377.
22. Engum A., Bjoro T., Mykletun A., Dahl A.A. An association between depression, anxiety and thyroid function - a clinical fact or an artefact?. Acta Psychiatr. Scand. 2002, 106:27-34.
23. Feldman A.Z., Shrestha R.T., Hennessey J.V. Neuropsychiatric manifestations of thyroid disease. Endocrinol. Metab. Clin. N. Am. 2013, 42:453-476.
24. First M., Gil-Ad I., Taler M., Tarasenko I., Novak N., Weizman A. The effects of reboxetine treatment on depression-like behavior, brain neurotrophins, and ERK expression in rats exposed to chronic mild stress. J. Mol. Neurosci. 2013, 50:88-97.
25. Fjalling M., Dackenberg A., Hedman I., Tisell L.E. An evaluation of the risk of developing hyperparathyroidism after 131I treatment for thyrotoxicosis. Acta Chir. Scand. 1983, 149:681-686.
26. Freeman S.A. Radioactive iodine-induced psychosis. Am. J. Psychiatry 2009, 166:1067-1068.
27. Fregly M.J. Increased water exchange in rats treated with antithyroid drugs. J. Pharmacol. Exp. Ther. 1961, 134:69-76.
28. Fukao A., Takamatsu J., Kubota S., Miyauchi A., Hanafusa T. The thyroid function of Graves' disease patients is aggravated by depressive personality during antithyroid drug treatment. BioPsychoSocial Med. 2011, 5:9.
29. Ginsberg J. Diagnosis and management of Graves' disease. CMAJ 2003, 168:575-585.
30. Gold M.S., Pottash A.L., Extein I. Hypothyroidism and depression. Evidence from complete thyroid function evaluation. JAMA 1981, 245:1919-1922.
31. Gonzalez C.R., Martinez de Morentin P.B., Martinez-Sanchez N., Gomez-Diaz C., Lage R., Varela L., Dieguez C., Nogueiras R., Castano J.P., Lopez M. Hyperthyroidism differentially regulates neuropeptide S system in the rat brain. Brain Res. 2012, 1450:40-48.
32. Goodwin F.K., Prange A.J., Post R.M., Muscettola G., Lipton M.A. Potentiation of anti-depressant effects by L-triiodothyronine in tricyclic non-responders. Am. J. Psychiatry 1982, 139:34-38.
33. Hage M.P.A., Sami T. The link between thyroid function and depression. J. Thyroid. Res. 2012, 2012:8.
34. Harbert J. Nuclear Medicine Therapy 1987, Thieme Medical Publisher Inc., New York.
35. Heal D.J., Smith S.L. The effects of acute and repeated administration of T3 to mice on 5-Ht1 and 5-Ht2 function in the brain and its influence on the actions of repeated electroconvulsive shock. Neuropharmacology 1988, 27:1239-1248.
36. Hillert M., Zimmermann M., Klein J. Uptake of lithium into rat brain after acute and chronic administration. Neurosci. Lett. 2012, 521:62-66.
37. Homberg J.R., Molteni R., Calabrese F., Riva M.A. The serotonin-BDNF duo: developmental implications for the vulnerability to psychopathology. Neurosci. Biobehav. Rev. 2014, 43C:35-47.
38. Hyams C., Joshi P., Foster P., Katz J. Acute psychosis caused by hypothyroidism following radioactive iodine treatment of Graves' disease. JRSM Short Rep. 2013, 4:26.
39. Iglesias R., Llobera M., Montoya E. Long-term effects of TRH administration on food intake and body weight in the rat. Pharmacol. Biochem. Behav. 1986, 24:1817-1819.
40. Ito J.M., Valcana T., Timiras P.S. Effect of hypo- and hyperthyroidism on regional monoamine metabolism in the adult rat brain. Neuroendocrinology 1977, 24:55-64.
41. Jackson I.M. The thyroid axis and depression. Thyroid 1998, 8:951-956.
42. Jacobsen J.P., Medvedev I.O., Caron M.G. The 5-HT deficiency theory of depression: perspectives from a naturalistic 5-HT deficiency model, the tryptophan hydroxylase 2Arg439His knockin mouse. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367:2444-2459.
43. Jacoby J.H., Mueller G., Wurtman R.J. Thyroid state and brain monoamine metabolism. Endocrinology 1975, 97:1332-1335.
44. Jonklaas J., Nsouli-Maktabi H. Weight changes in euthyroid patients undergoing thyroidectomy. Thyroid 2011, 21:1343-1351.
45. Kamble M.T., Nandedkar P.D., Dharme P.V., L.L.S., Bhosale P.G. Thyroid function and mental disorders: an insight into the complex interaction. J. Clin. Diagn. Res. 2013, 7:11-14.
46. Karras S., Memi E., Kintiraki E., Krassas G.E. Pathogenesis of propylthiouracil-related hepatotoxicity in children: present concepts. J. Pediatr. Endocrinol. Metab. 2012, 25:623-630.
47. Kennedy J.A., Jarrett D.B., Wellby M.L. Influence of imipramine on the hypothalamic/pituitary/thyroid axis of the rat. Metab. Clin. Exp. 1997, 46:1429-1434.
48. Kong W.M., Martin N.M., Smith K.L., Gardiner J.V., Connoley I.P., Stephens D.A., Dhillo W.S., Ghatei M.A., Small C.J., Bloom S.R. Triiodothyronine stimulates food intake via the hypothalamic ventromedial nucleus independent of changes in energy expenditure. Endocrinology 2004, 145:5252-5258.
49. Kulikov A., Torresani J., Jeanningros R. Experimental hypothyroidism increases immobility in rats in the forced swim paradigm. Neurosci. Lett. 1997, 234:111-114.
50. Lee I.T., Sheu W.H., Liau Y.J., Lin S.Y., Lee W.J., Lin C.C. Relationship of stressful life events, anxiety and depression to hyperthyroidism in an Asian population. Horm. Res. 2003, 60:247-251.
51. Li W., Changsheng C., Jiangfang F., Bin G., Nanyan Z., Xiaomiao L., Deqiang L., Ying X., Wensong Z., Qiuhe J. Effects of sex steroid hormones, thyroid hormone levels, and insulin regulation on thyrotoxic periodic paralysis in Chinese men. Endocrine 2010, 38:386-390.
52. Lifschytz T., Shalom G., Lerer B., Newman M.E. Sex-dependent effects of fluoxetine and triiodothyronine in the forced swim test in rats. Eur. Neuropsychopharmacol. 2006, 16:115-121.
53. Lifschytz T., Zozulinsky P., Eitan R., Landshut G., Ohayon S., Lerer B. Effect of triiodothyronine on antidepressant screening tests in mice and on presynaptic 5-HT1A receptors: mediation by thyroid hormone alpha receptors. J. Pharmacol. Exp. Ther. 2011, 337:494-502.
54. Lin Z., Chen L., Fang Y., Cai A., Zhang T., Wu V.W. Longitudinal study on the correlations of thyroid antibody and thyroid hormone levels after radiotherapy in patients with nasopharyngeal carcinoma with radiation-induced hypothyroidism. Head Neck 2014, 36:171-175.
55. Lorenzetti V., Allen N.B., Fornito A., Yucel M. Structural brain abnormalities in major depressive disorder: a selective review of recent MRI studies. J. Affect. Disord. 2009, 117:1-17.
56. McLelland A.E., Martin-Iverson M.T., Beninger R.J. The effect of quetiapine (Seroquel) on conditioned place preference and elevated plus maze tests in rats when administered alone and in combination with (+)-amphetamine. Psychopharmacology 2014, 231:4349-4359.
57. Menconi F., Marcocci C., Marino M. Diagnosis and classification of Graves' disease. Autoimmun. Rev. 2014, 13:398-402.
58. Montero-Pedrazuela A., Venero C., Lavado-Autric R., Fernandez-Lamo I., Garcia-Verdugo J.M., Bernal J., Guadano-Ferraz A. Modulation of adult hippocampal neurogenesis by thyroid hormones: implications in depressive-like behavior. Mol. Psychiatry 2006, 11:361-371.
59. Nambiar P.R., Palanisamy G.S., Okerberg C., Wolford A., Walters K., Buckbinder L., Reagan W.J. Toxicities associated with 1-month treatment with propylthiouracil (PTU) and methimazole (MMI) in male rats. Toxicol. Pathol. 2013, 42:970-983.
60. Ni G.X., Liu S.Y., Lei L., Li Z., Zhou Y.Z., Zhan L.Q. Intensity-dependent effect of treadmill running on knee articular cartilage in a rat model. BioMed Res. Int. 2013, 2013:172392.
61. Olivares E.L., Silva-Almeida C., Pestana F.M., Sonoda-Cortes R., Araujo I.G., Rodrigues N.C., Mecawi A.S., Cortes W.S., Marassi M.P., Reis L.C., Rocha F.F. Social stress-induced hypothyroidism is attenuated by antidepressant treatment in rats. Neuropharmacology 2012, 62:446-456.
62. Page M.E., Detke M.J., Dalvi A., Kirby L.G., Lucki I. Serotonergic mediation of the effects of fluoxetine, but not desipramine, in the rat forced swimming test. Psychopharmacology 1999, 147:162-167.
63. Palizgir M., Bakhtiari M., Esteghamati A. Association of depression and anxiety with diabetes mellitus type 2 concerning some sociological factors. Iran. Red Crescent Med. J. 2013, 15:644-648.
64. Paulson M.L., R.L., Pekary E., Sattin A. Double dissociation of antidepressant and endocrine effects of thyrotropin - releasing hormone analogues in the Porsolt animal model of depression. Society for Neuroscience Abstract Viewer and Itinerary Planner 2003, Abstract No. 344.311 2003.
65. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur. J. Pharmacol. 1978, 47:379-391.
66. Redei E.E., Solberg L.C., Kluczynski J.M., Pare W.P. Paradoxical hormonal and behavioral responses to hypothyroid and hyperthyroid states in the Wistar-Kyoto rat. Neuropsychopharmacology 2001, 24:632-639.
67. Reus G.Z., Dos Santos M.A., Abelaira H.M., Ribeiro K.F., Petronilho F., Vuolo F., Colpo G.D., Pfaffenseller B., Kapczinski F., Dal-Pizzol F., Quevedo J. Imipramine reverses alterations in cytokines and BDNF levels induced by maternal deprivation in adult rats. Behav. Brain Res. 2013, 242:40-46.
68. Rivkees S.A., Szarfman A. Dissimilar hepatotoxicity profiles of propylthiouracil and methimazole in children. J. Clin. Endocrinol. Metab. 2010, 95:3260-3267.
69. Rizvi I., Ansari N.A., Beg M., Shamim M.D. Widespread intracranial calcification, seizures and extrapyramidal manifestations in a case of hypoparathyroidism. N. Am. J. Med. Sci. 2012, 4:369-372.
70. Sala-Roca J., Marti-Carbonell M.A., Garau A., Darbra S., Balada F. Effects of dysthyroidism in plus maze and social interaction tests. Pharmacol. Biochem. Behav. 2002, 72:643-650.
71. Sandrini M., Vitale G., Vergoni A.V., Ottani A., Bertolini A. Effect of acute and chronic treatment with triiodothyronine on serotonin levels and serotonergic receptor subtypes in the rat brain. Life Sci. 1996, 58:1551-1559.
72. Schmidt H.D., Duman R.S. The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav. Pharmacol. 2007, 18:391-418.
73. Shiovitz T., Greenberg W.M., Chen C., Forero G., Gommoll C.P. A randomized, double-blind, placebo-controlled trial of the efficacy and safety of levomilnacipran ER 40-120mg/day for prevention of relapse in patients with major depressive disorder. Innov. Clin. Neurosci. 2014, 11:10-22.
74. Sinha R.A., Pathak A., Kumar A., Tiwari M., Shrivastava A., Godbole M.M. Enhanced neuronal loss under perinatal hypothyroidism involves impaired neurotrophic signaling and increased proteolysis of p75(NTR). Mol. Cell. Neurosci. 2009, 40:354-364.
75. Streetman D.D., Khanderia U. Diagnosis and treatment of Graves disease. Ann. Pharmacother. 2003, 37:1100-1109.
76. Tian M., Mao R.R., Wang L.P., Zhou Q.X., Cao J., Xu L. Interaction between behavioral despair and addictive behaviors in rats. Physiol. Behav. 2011, 102:7-12.
77. Torlak V., Zemunik T., Modun D., Capkun V., Pesutic-Pisac V., Markotic A., Pavela-Vrancic M., Stanicic A. 131 I-induced changes in rat thyroid gland function. Braz. J. Med. Biol. Res. 2007, 40:1087-1094.
78. Tousson E., Ibrahim W., Arafa N., Akela M.A. Monoamine concentrations changes in the PTU-induced hypothyroid rat brain and the ameliorating role of folic acid. Hum. Exp. Toxicol. 2012, 31:282-289.
79. Tsuru J., Ishitobi Y., Ninomiya T., Kanehisa M., Imanaga J., Inoue A., Okamoto S., Maruyama Y., Higuma H., Tanaka Y., Hanada H., Isogawa K., Akiyoshi J. The thyrotropin-releasing hormone test may predict recurrence of clinical depression within ten years after discharge. Neuroendocrinol. Lett. 2013, 34:409-417.
80. Vaidya V.A., Castro M.E., Pei Q., Sprakes M.E., Grahame-Smith D.G. Influence of thyroid hormone on 5-HT1A and 5-HT2A receptor-mediated regulation of hippocampal BDNF mRNA expression. Neuropharmacology 2001, 40:48-56.
81. van Oers H.A., Haverman L., Limperg P.F., van Dijk-Lokkart E.M., Maurice-Stam H., Grootenhuis M.A. Anxiety and depression in mothers and fathers of a chronically ill child. Matern. Child Health J. 2014, 18:1993-2002.
82. Vega-Rivera N.M., Lopez-Rubalcava C., Estrada-Camarena E. The antidepressant-like effect of ethynyl estradiol is mediated by both serotonergic and noradrenergic systems in the forced swimming test. Neuroscience 2013, 250:102-111.
83. Williams G.R. Neurodevelopmental and neurophysiological actions of thyroid hormone. J. Neuroendocrinol. 2008, 20:784-794.