Disrupted brain thyroid hormone homeostasis and altered thyroid hormone-dependent brain gene expression in autism spectrum disorders

Journal of Physiology and Pharmacology

Volumn 65, Issue 2, 2014, Pages 257-272

  Khan, A ^a   Harney, J W ^a   Zavacki, A M ^a   Sajdel Sulkowska, Elizabeth M ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

3',3,5 triiodothyronine; Autism spectrum disorders; Brain region dependent; Deiodinase; Oxidative stress marker 3 nitrotrosine; Sex dependent; Type

Indexed keywords

3 NITROTYROSINE; CYCLOPHILIN A; IODOTHYRONINE; IODOTHYRONINE DEIODINASE TYPE 2; IODOTHYRONINE DEIODINASE TYPE 3; LIOTHYRONINE; MERCURY; THYROID HORMONE; UNCLASSIFIED DRUG; 3,3',5' TRIIODOTHYRONINE; 3-NITROTYROSINE; IODIDE PEROXIDASE; IODOTHYRONINE DEIODINASE TYPE II; IODOTHYRONINE DEIODINASE TYPE III; TYROSINE;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN STEM; CEREBELLUM; CHILD; CINGULATE GYRUS; CONTROLLED STUDY; ELISA KIT; ENZYME ACTIVITY; FEMALE; GENDER; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORBITAL CORTEX; OXIDATIVE STRESS; PRESCHOOL CHILD; PROTEIN HOMEOSTASIS; PUTAMEN; RAT; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; WERNICKE AREA; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; GENETICS; HOMEOSTASIS; METABOLISM; SPRAGUE DAWLEY RAT;

ADOLESCENT; ANIMALS; BRAIN; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CHILD, PRESCHOOL; FEMALE; GENE EXPRESSION; HOMEOSTASIS; HUMANS; IODIDE PEROXIDASE; MALE; MERCURY; RATS, SPRAGUE-DAWLEY; THYROID HORMONES; TRIIODOTHYRONINE, REVERSE; TYROSINE;

EID: 84899655170     PISSN: 08675910     EISSN: 18991505     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Schantz SL, Widholm JJ. Cognitive effects of endocrinedisrupting chemicals in animals. Environ Health Perspect 2001; 109: 1197-1206.
2. Sulkowski ZL, Chen T, Midha S, Zavacki AM, Sajdel-Sulkowska EM. Maternal thimerosal exposure results In aberrant cerebellar oxidative stress, thyroid hormone metabolism, and motor behavior In rat pups; sex-and straindependent effect. Cerebellum 2012; 11: 575-586.
3. Abbassi V, Linscheid T, Coleman M. Triiodothyronine (T3) concentration and therapy in autistic children. J Autism Child Schizophr 1978; 8: 383-387.
4. Cohen DJ, Young JG, Lowe TL, Harcheric D. Thyroid hormone in autistic children. J Autism Dev Disord 1980; 10: 445-450.
5. Soldin OP, O'Mara DM, Escher M. Thyroid hormones and methylmercury toxicity. Biol Trace Elem Res 2008; 126: 1-12.
6. Leonard JL. Regulation of T3 production in the brain. Acta Med Austriaca 1992; 19(Suppl 1): 5-8.
7. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronone selenodeiodinase. Endocr Rev 2002; 23: 38-89.
8. Crantz FR, Silva JE, Larsen PR. An analysis of the sources and quantity of 3,5,3',-triiodothyronine specifically bound to nuclear receptors in rat cerebral cortex and cerebellum. Endocrinology 1982; 110: 367-375.
9. Silva JE, Larsen PR. Comparison of iodothyronine 5'-deiodinase and other thyroid-hormone-dependent enzyme activities in the cerebral cortex of hypothyroid neonatal rat. Evidence for adaptation to hypothyroidism. J Clin Invest 1982; 70: 1110-1123.
10. Khan A, Sulkowski ZL, Chen T, Zavacki AM, Sajdel-Sulkowska EM. Sex-dependent changes in cerebellar thyroid hormone-dependent gene expression following perinatal exposure to thimerosal in rats. J Physiol Pharmacol 2012; 63: 277-283.
11. Cuadrado A, Bernal J, Munoz A. Identification of the mammalian homolog of the splicing regulator Suppressorof-white-apricot as a thyroid hormone regulated gene. Brain Res Mol Brain Res 1999; 71: 332-340.
12. Alkemade A, Friesema EC, Unmehopa UA, et al. Neuroanatomical pathways for thyroid hormone feedback in the human hypothalamus. J Clin Endocrinol Metab 2005; 90: 4322-4334.
13. Matsunami N, Hadley D, Hensel CH, et al. Identification of rare recurrent copy number variants in high-risk autism families and their prevalence in a large ASD population. PLoS One 2013; 8: e52239. doi: 10.1371/journal.pone.0052239
14. Tunc-Ozcan E, Ullmann TM, Shukla PK, Redel EE. Low-dose thyroxine attenuates autism-associated adverse effects of fetal alcohol in male offspring's social behavior and hippocampal gene expression. Alcohol Clin Exp Res 2013; 37: 1986-1995.
15. Sajdel-Sulkowska EM. Oxidative stress in autism: expression of oxidative stress markers in a rat model of the human postmortem process. Abstract 2524, Internationl Meeting for Autism Research, London, 2008.
16. Sajdel-Sulkowska EM, Lipinski B, Windom H, Audhya T, McGinnis W. Oxidative stress in autism: cerebellar 3-nitrotyrosine levels. Am J Biochem Biotechnol 2008; 4: 73-84.
17. Zavacki AM, Ying H, Christoffolete MA. Type 1 iodothyronine deiodinase is a sensitive marker of peripheral thyroid status in the mouse. Endocrinology 2005; 146: 1568-1575.
18. Pachucki J, Hopkins J, Peeters, et al. R. Type 2 iodothyronine deiodinase transgene expression in the mouse heart causes cardiac-specific thyrotoxicosis. Endocrinology 2001; 142: 13-20.
19. Galton VA, Wood ET, St Germain EA, et al. Thyroid hormone homeostasis and action in the type 2 deiodinasedeficient rodent brain during development. Endocrinology 2007; 148: 3080-3088.
20. Gahete MD, Cordoba-Chacon J, Salvatori R, Castano JP, Kineman RD, Luque RM. Metabolic regulation of ghrelin O-acyl transferase (GOAT) expression in the mouse hypothalamus, pituitary, and stomach. Mol Cell Endocrinol 2010; 317: 154-160.
21. Guan J, Luo Y, Denker BM. Purkinje cell protein-2 (Pcp2) stimulates differentiation in PC12 cells by G-betagammamediated activation of Ras and p38 MAPK. Biochem J 2005; 392: 389-397.
22. Bangalore S, Messerli FH. Of statistical significance: "trends" toward significance and optimism bias. J Am Coll Cardiol 2006; 48: 1471.
23. Padhi BK, Pelletier G, Williams A. Gene expression profiling in rat cerebellum following in utero and lactational exposure to mixtures of methylmercury, polychlorinated biphenyls and organochlorine pesticides. Toxicol Lett 2008; 176: 93-103.
24. Morte B, Ceballos A, Diez D, et al. Thyroid hormoneregulated mouse cerebral cortex genes are differentially dependent on the source of the hormone: a study in monocarboxylate transporter-8-and deiodinase-2-deficient mice. Endocrinology 2010; 151: 2381-2387.
25. Faustino LC, Almeida NA, Pereira GF, et al. Thyroid hormone and estradiol have overlapping effects on kidney glutathione S-transferase-gene expression. Am J Physiol Endocrinol Metab 2012; 303: E787-E797.
26. Benvenuti S, Luciani P, Cellai I, et al. Thyroid hormone promote cell differentiation and up-regulate the expression of seladin-1 gene in in vitro models of human neuronal precursors. J Endocrinol 2008; 197: 437-446.
27. Kanner L. Autistic disturbance of affective contact. Nervous Child 1943; 2: 217-250.
28. Anney R, Klei L, Pinto D, et al. A genome-wide scan for common alleles affecting risk for autism. Hum Mol Genet 2010; 19: 4072-4082.
29. Rosenberg RE, Law JK, Yenokyan G, McGready J, Kaufman WE, Law PA. Characteristics and concordance of autism spectrum disorders among 277 twin pairs. Arch Pediatr Adolesc Med 2009; 163: 907-914.
30. Oppenheimer JH, Schwartz HL. Molecular basis of thyroid hormone-dependent brain development. Endocr Rev 1997; 18: 462-475.
31. Vermiglio F, Lo Presti VO, Scaffidi Argentina G, et al. Maternal hypothyroxemia during the first half of gestation in an iodine deficient area with endemic cretinism and related disorders. Clin Endocr (Oxf) 1995; 42: 409-415.
32. Sajdel-Sulkowska EM. Oxidative stress and neurotrophin signaling in autism. In: Autism: Oxidative Stress, Inflammation and Immune Abnormalities, A. Chauhan, V. Chauhan, W.T. Brown (eds). CRC Press, 2010, pp. 47-60.
33. Sajdel-Sulkowska EM, Xu M, McGinnis W, Koibuchi N. Brain region-specific changes in oxidative stress and neurotrophin levels in autism spectrum disorders (ASD). Cerebellum 2011; 10: 43-48.
34. Hua X, Thompson PM, Leow AD, et al. Brain growth rate abnormalities visualized in adolescents with autism. Hum Brain Mapp 2013; 34: 425-436.
35. Kawakami Y, Monobe M, Kuwabara K, et al. A comparative study of nitric oxide, glutathione, and glutathione peroxidase activities in cerebrospinal fluid from children with convulsive diseases/children with aseptic meningitis. Brain Dev 2006; 28: 243-246.
36. Pecanha FM, Wiggers GA, Briones AM, et al. The role of cyclooxygenase (COX)-2 derived prostanoids on vasoconstrictor responses to phenylephrine is increased by exposure to low mercury concentration. J Physiol Pharmacol 2010; 61: 29-36.
37. Hallene KL, Oby E, Lee BJ, et al. Prenatal exposure to thalidomide, altered vasculogenesis, and CNS malformations. Neuroscience 2006; 142: 267-283.
38. Bates JM, St. Germain DL, Galton VA. Expression profiles of the three deiodinases, D1, D2, and D3, in the developing rat. Endocrinology 1999; 140: 844-851.
39. Harish G, Venkateshappa C, Mahadevan A, Pruthin N, Srinivas Bharath MM, Shankar SS. Glutathione metabolism is modulated by postmortem interval, gender difference and agonal state in postmortem human brains. Neurochem Int 2011; 59: 1029-1042.
40. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadian EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDAWork Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984; 34: 939-944.
41. Davis JD, Podolanczuk A, Donahue JE, et al. Thyroid hormone levels in the prefrontal cortex of post-mortem brains of Alzheimer's disease patients. Curr Aging Sci 2008; 1: 175-181.
42. Hornig M, Chian D, Lipkin WI. Neurotoxic effects of postnatal thimerosal are mouse strain dependent. Mol Psychiatry 2004; 9: 1-13.
43. Lamirand A, Ramauge M, Pierre M, Courtin F. Bacterial lipopolysaccharide induced type 2deiodinase in cultured rat astrocytes. J Endocrinol 2011; 208: 183-192.
44. Wajner SM, Goemann IM, Bueno AL, Larsen PR, Maia AL. IL-6 promotes nonthyroidal illness syndrome by blocking thyroxine activation while promoting thyroid hormone inactivation in human cells. J Clin Invest 2011; 121: 1834-1845.
45. Dasgupta A, Das S, Sarkar PK. Thyroid hormone promotes glutathione synthesis in astrocytes by up regulation of glutamate cysteine ligase through differential stimulation of its catalytic and modular subunit mRNAs. Free Radic Biol Med 2007; 42: 617-626.
46. Tagami M, Madison LD, Nagaya T, Jameson JL. Nuclear receptor corepressors activate rather than suppress basal transcription of genes that are negatively regulated by thyroid hormone. Mol Cell Biol 1997; 17: 2642-2648.
47. Sousa JC, de Escobar GM, Oliveira P, Saraivo MJ, Palha JA. Transthyretin is not necessary for thyroid hormone metabolism in conditions of increased hormone demand. J Endocrinol 2005; 187: 257-266.
48. Richardson SJ. Cell and molecular biology of transthyretin and thyroid hormones. Int Rev Cytol 2007; 258: 137-193.
49. Tu HM, Legradi G, Bartha T, Salvatore D, Lechan RM, Larsen PR. Regional expression of the 3 iodothyronine deiodinase messenger ribonucleic acid in the rat central nervous system and its regulation by thyroid hormone. Endocrinology 1999; 140: 784-790.
50. Koibuchi N, Yamaoka S, Chin WW. Effect of altered thyroid status on neurotrophin gene expression during postnatal development of mouse cerebellum. Thyroid 2001; 11: 205-2010.
51. Camboni D, Roskoden T, Schwegler H. Effect of early thyroxine on brain-derived neurotrophic factor mRNA expression and protein amount in the rat medial septum/diagonal band of Brocca. Neurosci Lett 2003; 350: 141-144.
52. Zoladz JA, Pilc A. The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. J Physiol Pharmacol 2010; 61: 533-541.
53. Bernhardt BC, Valk SL, Silani G, Bird G, Frith U, Singer T. Selective disruption of sociocognitive structural brain networks in autism and alexithymia. Cereb Cortex 2013; Jul 17 (epub ahead of print). doi: 10.1093/cercor/bht182
54. Pathak A, Sinha RA, Mohan V, Mitra K, Godbole MM. Maternal thyroid hormone before the onset of fetal thyroid function regulated reelin and downstream signaling affecting neocortical neuronal migration. Cereb Cortex 2011; 21: 11-21.
55. Folsom TD, Fatemi SH. The involvement of reelin in neurodevelopmental disorders. Neuropharmacology 2013; 68: 122-135.
56. Schweizer U, Kohrle J. Function of thyroid hormone transporters in the central nervous system. Biochim Biophys Acta 2013; 1830: 3965-3973.
57. Tonduti D, Vanderver A, Berardinelli A. MCT8 deficiency: extrapyramidal symptoms and delayed myelination as prominent features. J Child Neurol 2013; 28: 792-797.
58. des Portes V. X-linked mental deficiency. Handb Clin Neurol 2013; 111: 297-306.
59. Fatemi SH, Folsom TD, Kneeland RE, Liesh SB. Metabotropic glutamate receptor 5 up regulation in children with autism is associated with under expression of both Fragile X mental retardation protein and GABAA receptor beta 3 in adults with autism. Anat Rec (Hoboken) 2011; 294: 1635-1645.
60. Orekhova EV, Tsetlin MM, Butorina AV, et al. Auditory cortex responses to clicks and sensory modulation difficulties in children with autism spectrum disorders (ASD). PLoS One 2012; 7: e39906. doi:10.1371/journal.pone.0039906.
61. Carreon-Rodriguez A, Perez-Martinez L. Clinical implications of thyroid hormones effects on nervous system development. Pediatr Endocrinol Rev 2012; 9: 644-649.
62. Mohan V, Sinha RA, Pathak A, et al. Maternal thyroid hormone deficiency affects the fetal neocorticogenesis by reducing the proliferating pool, rate of neurogenesis and indirect neurogenesis. Exp Neurol 2012; 237: 477-488.
63. Rabie A, Favre C, Clavel MC, Legrand J. Sequential effects of thyroxine on the developing cerebellum of rats made hypothyroid by propylthiouracil. Brain Res 1979; 161: 469-479.
64. Sendin G, Bulankhina AV, Riedel D, Moser T. Maturation of ribbon synapses in hair cells is driven by thyroid hormone. J Neurosci 2007; 27: 3163-3173.