Top

Published in:

01-09-2008 | Original Paper

Hypothyroidism induces selective oxidative stress in amygdala and hippocampus of rat

Authors: Edgar Cano-Europa, Francisca Pérez-Severiano, Paula Vergara, Rocío Ortiz-Butrón, Camilo Ríos, José Segovia, Jorge Pacheco-Rosado

Published in: Metabolic Brain Disease | Issue 3/2008

Abstract

The effects of hypothyroidism on lipid peroxidation (LP), reactive oxygen species (ROS), and nitric oxide synthase (NOS), levels and expression, in rat brain were examined. Hypothyroidism was induced by administering methimazole in drinking water (60 mg/kg/day). In striatum, motor cortex and cerebellum of hypothyroid rats LP was not modified, whereas LP and ROS increased in amygdala and hippocampus of hypothyroid rats at the third week of treatment with methimazole as compared to euthyroid group values. Regarding NOS participation, only hippocampal constitutive-NOS activity was increased, accompanied by an augmentation in nNOS expression. Results show that hypothyroidism induces selective oxidative stress in both the hippocampus and amygdala, where the nitrergic system is involved.

Alevizaki M, Synetou M, Xynos K, Alevizaki CC, Vemmos KN (2006) Hypothyroidism as a protective factor in acute stroke patients. Clin Endocrinol (Oxf) 65:369–372CrossRef

Alva-Sánchez C, Ortiz-Butrón R, Cuellar-García M, Hernández-García A, Pacheco-Rosado J (2002) Anatomical changes in CA3 hippocampal region by hypothyroidism in rats. Proc West Pharmacol Soc 45:125–126PubMed

Alva-Sánchez C, Ortiz-Butrón R, Pacheco-Rosado J (2004) Kainic acid does no affect CA3 hippocampal region pyramidal cells in hypothyroid rats. Brain Res Bull 63:167–171PubMedCrossRef

Amato A, Barbour B, Szatkowski M, Attwell D (1994) Counter-transport of potassium by glutamate uptake carrier in glial cell isolated from the tiger salamander retina. J Physiol (Lond) 479:371–390

Ambrogini P, Cuppini R, Ferri P, Manzini C, Ciaroni S, Voci A, Gerdoni E, Gallo G (2005) Thyroid hormona affect neurogenesis in the dentate gyrus of adult rat. Neuroendocrinol 81:244–253CrossRef

Aniello F, Couchie A, Bidox A, Gripois D, Nunez J (1991) Splicing of juvenile and adult tau mRNA variants is regulated by thyroid hormone. Proc Natl Acad Sci U S A 88:4035–4039PubMedCrossRef

Arrica M, Bissonnette B (2007) Therapeutic hypothermia. Semen Cardiothorac Vasc Anesth 11:6–15CrossRef

Boelaert K, Franklyn JA (2005) Thyroid hormone in health and disease. J Endocrinol 187:1–15PubMedCrossRef

Bradford MM (1976) A rapid and sensitive method for the quantification of micrograms quantities of protein utilizing the principle of protein-dye binding. Annal Biochem 72:248–254CrossRef

Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase. A cadmodulin-requiring enzyme. Proc Natl Acad Sci U S A 87:682–685PubMedCrossRef

Brown LA, Key BJ, Lovick TA (1999) Bio-imaging of nitric oxide-producing neurones in slices of rat brain using 4,5-diaminofluorescein. J Neurosci Methods 92:101–110PubMedCrossRef

Carageorgiou H, Pantos C, Zarros A, Stolakis V, Mourouzis I, Cokkinos D, Tsakiris S (2007) Changes in acetylcholinesterase, Na⁺, K⁺-ATPase, and Mg²⁺-ATPase activities in the frontal cortex and the hippocampus of hyper- and hypothyroid adult rats. Metab Clin Exp 56:1104–1110PubMed

Carreras MC, Peralta JG, Converso DP, Finocchietto PV, Rebagliati I, Zaninovich AA, Poderoso JJ (2001) Modulation of liver mitochondrial NOS is implicated in thyroid-dependent regulation of O₂ uptake. Am J Physiol Heart Circ Physiol 281:H2282–H2288PubMed

Constantinou C, Margarity M, Valcana T (2005) Region-specific effects of hypothyroidism on the relative expression of thyroid hormone receptors in adult rat brain. Mol Cell Biochem 278:93–100PubMedCrossRef

Cooper DS (2001) Clinical practice. Subclinical hypothyroidism. N Engl J Med 345:260–265PubMedCrossRef

Das K, Chainy GBN (2001) Modulation of rat liver mitochondrial antioxidant defence system by thyroid hormone. Biochim Biophys Acta 1537:1–13PubMed

Davis FB, Cody V, Davis PJ, Borzynski LJ, Blas SD (1983) Stimulation by thyroid hormone analogues of red blood cell Ca²⁺-ATPase activity in vitro. Correlations between hormone structure and biological activity in a human cell system. J Biol Chem 258:12373–12377PubMed

Desouza LA, Ladiwala U, Daniel SM, Agashe S, Vahadilla RA, Vahadilla VA (2005) Thyroid hormone regulates hippocampal neurogenesis in the adult rat brain. Mol Cel Neurosci 29:414–426CrossRef

Doyle KP, Suchland KL, Ciesielski TM, Lessov NS, Grandy DK, Scanlan TS, Stenzel-Poore MP (2007) Novel thyroxine derivatives, thyronamine and 3-iodothyronamine, induce transient hypothermia and marked neuroprotection against stroke injury. Stroke 38:2569–2576PubMedCrossRef

Evans PH (1993) Free radicals in brain metabolism and pathology. Br Med Bull 49:577–587PubMed

García-Tovar CG, Pérez A, Luna J, Mena R, Osorio B, Alemán V, Mondragón R, Mornet D, Rendón A, Hernández JM (2001) Biochemical and histochemical analysis of 71 kDa dystrophin isoform (Dp71f) in rat brain. Acta Histochem 103:209–224PubMedCrossRef

Halliwell B, Gutteridge JMC (1999) Free radical in biology and medicine. Claredon, Oxford

Hoch FL (1988) Lipids and thyroid hormones. Prog Lipid Res 27:199–270PubMedCrossRef

Hulbert AJ (2000) Thyroid hormone and their effects: a new perspective. Biol Rev 75:519–631PubMedCrossRef

Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of metabolism. J Theoret Biol 199:257–274CrossRef

Mano T, Sinohara R, Sawai Y, Oda N, Nishida Y, Mokumo T, Asano K, Ito Y, Kotake M, Hamada M (1995) Changes in lipid peroxidation and free radical scavengers in the brain of hyper- and hypothyroid aged rats. J Endocrinol 147:361–365PubMedCrossRef

Matsunaga M, Saotame M, Satoh H, Katoh H, Terrade H, Hayashi H (2005) Different actions of cardioprotective agents on mitochondrial Ca²⁺ paradox-induced Ca²⁺ overload. Circ J 69:1132–1140PubMedCrossRef

Pacheco-Rosado J, Alva-Sánchez C (2007) Thyroid hormone and their possible role as neuron survival factors in the adult rat brain. In: Santamaría A, Jiménez Capdeville ME (eds) New perspectives on brain cell damage, neurodegeneration and neuroprotective strategies. Research Signpost, India, pp 75–93

Pacheco-Rosado J, Quevedo-Corona L, Zamudio-Hernández SR, Chambert G (1997) T3 prolongs convulsion induced by acute pentylentetrazole. Horm Metab Res 29:577–579PubMedCrossRef

Pacheco-Rosado J, Arias-Citalán G, Ortiz-Butrón R, Rodríquez-Páez L (2005) Selective decrease of Na⁺/K⁺-ATPase activity in brain of mild hypothyroid rats. Proc West Pharmacol Soc 48:52–54PubMed

Packer MA, Stasiv Y, Benraiss A, Chmielnicki E, Grinberg A, Westphal H, Goldman SA, Enikolopou G (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci U S A 100:9566–9571PubMedCrossRef

Pamplona R, Portero-Otin M, Ruiz C, Bellmunt MF, Requena JR, Thorpe SR, Baynes JW, Romero M, López-Torres M, Barja G (1999) Thyroid status modulates glycoxidative and lipoxidative modification of tissue proteins. Free Radic Biol Med 27:901–910PubMedCrossRef

Paul S, Das S, Sarkar PK (1992) Effect of hypothyroidism on different forms of actin in rat cerebral neuronal cultures studied by an improved DNAase I inhibition assay. J Neurochem 59:701–706PubMedCrossRef

Pérez-Severiano F, Escalante B, Vergara P, Rios C, Segovia J (2002) Age-dependent changes in nitric oxide synthase activity and protein expression in striata of mice transgenic for the Huntington’s disease mutation. Brain Res 951:36–42PubMedCrossRef

Pérez-Severiano F, Santamaría A, Pedraza-Caverri J, Medina-Campos ON, Rios C, Segovia J (2004) Increased formation of reactive oxygen species, but no changes in glutathione preoxidase activity, in striata of mice transgenic for the Huntington’s disease mutation. Neurochem Res 29:729–733PubMedCrossRef

Psarra AM, Solakidi S, Sekeris CE (2006) The mitochondrion as a primary site of action of steroid and thyroid hormones: presence and action of steroid and thyroid hormone receptors in mitochondria of animal cells. Mol Cell Endocrinol 246:21–33PubMedCrossRef

Puymirat J (1992) Thyroid receptors in the rat brain. Prog Neurobiol 39:281–294PubMedCrossRef

Quesada A, Sainz J, Wangensteen R, Rodríguez-Gomez I, Vargas F, Osuna A (2002) Nitric oxide synthase activity in hyperthyroid and hypothyroid rats. Eur J Endocrinol 147:117–122PubMedCrossRef

Rahaman SO, Ghosh S, Mohanakumar KP, Das S, Sarkar PK (2001) Hypothyroidism in the developing rat brain is associated with marked oxidative stress and aberrant intraneuronal accumulation of neurofilaments. Neurosci Res 40:273–279PubMedCrossRef

Rami A, Krieglstein J (1992) Thyroxine attenuates hippocampal neuronal damage caused by ischemia in the rat. Life Sci 50:645–650PubMedCrossRef

Rivas M, Naranjo JR (2007) Thyroid hormones, learning and memory. Genes Brain Behav 6:40–44PubMedCrossRef

Rossi DJ, Oshima T, Attwell D (2000) Glutamate release in sever brain ischaemia is mainly by reversed uptake. Nature 403:316–321PubMedCrossRef

Ruiz-Marcos A, Sánchez-Toscano F, Obregón MJ, Escobar del Rey F, Morreale de Escobar G (1982) Thyroxine treatment and recovery of hypothyroidism induced pyramidal cell damage. Brain Res 239:559–574PubMedCrossRef

Sarkar PK (2002) In quest of thyroid hormone function in mature mammalian brain. Ind J Exp Biol 40:865–873

Scmitt KR, Diestel A, Lehnardt S, Schwartlander R, Lange PE, Berger F, Ullrich O, Abdul-Khaliq H (2007) Hypothermia suppress inflammation via ERK signaling pathway in stimulated microglial cells. J Neuroimmunol 189:7–16CrossRef

Segovia J, Vergara P, Brenner M (1998) Differentiation-dependent expression of transgenes in engineered astrocyte cell lines. Neurosci Lett 242:172–176PubMedCrossRef

Shuaib A, Ijaz S, Hemmings S, Galazka P, Ishaqzay R, Liu L, Ravindran J, Miyashita H (1994) Decreased glutamate release during hypothyroidism may contribute to protection in cerebral ischemia. Exp Neurol 128:260–265PubMedCrossRef

Simonian NA, Coyle JT (1996) Oxidative stress in neurodegenerative diseases. Annu Rev Pharmacol Toxicol 36:83–106PubMedCrossRef

Simonides WS, Brent GA, Thelen MHM, van der Linden CG, Larsen PR, van Hardeveld C (1996) Characterization of the promoter of the rat sarcoplasmic endoplasmic reticulum Ca²⁺-ATPase 1 gene and analysis of thyroid hormone responsiveness. J Biol Chem 271:32048–32056PubMedCrossRef

Singh R, Upadhyay G, Kumar S, Kapoor A, Kumar A, Tiwari M, Godbole MM (2003) Hypothyroidism alters the expression of Bcl-2 family genes to induce enhanced apoptosis I the developing cerebellum. J Edocrinol 176:39–46CrossRef

Venditti P, Balestrieri M, Di Meo S, De Leo T (1997) Effect of thyroid state on lipid peroxidation, antioxidant defences and susceptibility to oxidative stress in rat tissues. J Endocrinol 155:151–157PubMedCrossRef

Title: Hypothyroidism induces selective oxidative stress in amygdala and hippocampus of rat
Authors: Edgar Cano-Europa
Francisca Pérez-Severiano
Paula Vergara
Rocío Ortiz-Butrón
Camilo Ríos
José Segovia
Jorge Pacheco-Rosado
Publication date: 01-09-2008
Publisher: Springer US
Published in: Metabolic Brain Disease / Issue 3/2008
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI: https://doi.org/10.1007/s11011-008-9099-0

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Hypothyroidism induces selective oxidative stress in amygdala and hippocampus of rat

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2008

Equilibrated diet restores the effects of early age choline-deficient feeding on rat brain antioxidant status and enzyme activities: the role of homocysteine, l-phenylalanine and l-alanine

Selective alterations of brain dopamine D2 receptor binding in cirrhotic patients: results of a 11C-N-methylspiperone PET study

Effects of fulminant hepatic encephalopathy on the adult rat brain antioxidant status and the activities of acetylcholinesterase, (Na+,K+)- and Mg2+-ATPase: comparison of the enzymes’ response to in vitro treatment with ammonia

Methylphenidate does not increase ethanol consumption in a rat model for attention-deficit hyperactivity disorder—the spontaneously hypertensive rat

Risk for metabolic syndrome predisposes to alterations in the thalamic metabolism

Newly observed thalamic involvement and mutations of the HEXA gene in a Korean patient with juvenile GM2 gangliosidosis