Thyroid Hormone Insufficiency Alters the Expression of Psychiatric Disorder-related Molecules in the Hypothyroid Mouse Brain During the Early Postnatal Period

Overview

Journal Sci Rep

Specialty Science

Date 2021 Mar 25

PMID 33762687

Citations 8

Authors

Katsuya Uchida

Kentaro Hasuoka

Toshimitsu Fuse

Kenichi Kobayashi

Takahiro Moriya

Mao Suzuki

Norihiro Katayama

Keiichi Itoi

Affiliations

Soon will be listed here.

Abstract

The functional role of thyroid hormone (TH) in the cortex and hippocampus of mouse during neuronal development was investigated in this study. TH insufficiency showed a decrease in the expression of parvalbumin (PV) in the cortex and hippocampus of pups at postnatal day (PD) 14, while treatment with thyroxine from PD 0 to PD 14 ameliorated the PV loss. On the other hand, treatment with antithyroid agents in adulthood did not result in a decrease in the expression of PV in these areas. These results indicate the existence of a critical period of TH action during the early postnatal period. A decrease in MeCP2-positive neuronal nuclei was also observed in the cortical layers II-IV of the cerebral cortex. The brains were then stained with CUX1, a marker for cortical layers II-IV. In comparison with normal mice, CUX1 signals were decreased in the somatosensory cortex of the hypothyroid mice, and the total thickness of cortical layers II-IV of the mice was lower than that of normal mice. These results suggest that TH insufficiency during the perinatal period strongly and broadly affects neuronal development.

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References

Liu X, Shimada T, Otowa T, Wu Y, Kawamura Y, Tochigi M . Genome-wide Association Study of Autism Spectrum Disorder in the East Asian Populations. Autism Res. 2015; 9(3):340-9. DOI: 10.1002/aur.1536. View

Stagi S, Cavalli L, Congiu L, Scusa M, Ferlini A, Bigoni S . Thyroid function in Rett syndrome. Horm Res Paediatr. 2015; 83(2):118-25. DOI: 10.1159/000370066. View

Soghomonian J, Zhang K, Reprakash S, Blatt G . Decreased parvalbumin mRNA levels in cerebellar Purkinje cells in autism. Autism Res. 2017; 10(11):1787-1796. DOI: 10.1002/aur.1835. View

Lawrence Y, Kemper T, Bauman M, Blatt G . Parvalbumin-, calbindin-, and calretinin-immunoreactive hippocampal interneuron density in autism. Acta Neurol Scand. 2009; 121(2):99-108. DOI: 10.1111/j.1600-0404.2009.01234.x. View

Nagarajan R, Hogart A, Gwye Y, Martin M, LaSalle J . Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics. 2007; 1(4):e1-11. PMC: 1866172. DOI: 10.4161/epi.1.4.3514. View

Percy A . Rett syndrome: exploring the autism link. Arch Neurol. 2011; 68(8):985-9. PMC: 3674963. DOI: 10.1001/archneurol.2011.149. View

Prange Jr A, Breese G, Cott J, Martin B, Cooper B, Wilson I . Thydrotropin releasing hormone: antagonism of pentobarbital in rodents. Life Sci. 1974; 14(3):447-55. DOI: 10.1016/0024-3205(74)90359-2. View

Tamamaki N, Fujimori K, Takauji R . Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci. 1997; 17(21):8313-23. PMC: 6573720. View

Chai X, Fan L, Shao H, Lu X, Zhang W, Li J . Reelin Induces Branching of Neurons and Radial Glial Cells during Corticogenesis. Cereb Cortex. 2014; 25(10):3640-53. DOI: 10.1093/cercor/bhu216. View

10.

Gilbert M, Sui L, Walker M, Anderson W, Thomas S, Smoller S . Thyroid hormone insufficiency during brain development reduces parvalbumin immunoreactivity and inhibitory function in the hippocampus. Endocrinology. 2006; 148(1):92-102. DOI: 10.1210/en.2006-0164. View

11.

Lischinsky J, Skocic J, Clairman H, Rovet J . Preliminary Findings Show Maternal Hypothyroidism May Contribute to Abnormal Cortical Morphology in Offspring. Front Endocrinol (Lausanne). 2016; 7:16. PMC: 4766309. DOI: 10.3389/fendo.2016.00016. View

12.

Mohan V, Sinha R, Pathak A, Rastogi L, Kumar P, Pal A . Maternal thyroid hormone deficiency affects the fetal neocorticogenesis by reducing the proliferating pool, rate of neurogenesis and indirect neurogenesis. Exp Neurol. 2012; 237(2):477-88. DOI: 10.1016/j.expneurol.2012.07.019. View

13.

Madeira M, Azevedo F, Paula-Barbosa M . Effects of long-term hypothyroidism in the morphology and synaptic organization of cerebellar ectopic granule cells. Histol Histopathol. 1988; 3(4):351-9. View

14.

Bunker S, Dandapat J, Chainy G, Sahoo S, Nayak P . Neonatal Exposure to 6-n-Propyl-Thiouracil, an Anti-Thyroid Drug, Alters Expression of Hepatic DNA Methyltransferases, Methyl CpG-Binding Proteins, Gadd45a, p53, and PCNA in Adult Male Rats. Eur Thyroid J. 2017; 6(6):281-291. PMC: 5704726. DOI: 10.1159/000479681. View

15.

Hashemi E, Ariza J, Rogers H, Noctor S, Martinez-Cerdeno V . The Number of Parvalbumin-Expressing Interneurons Is Decreased in the Prefrontal Cortex in Autism. Cereb Cortex. 2017; 28(2):690. PMC: 6790539. DOI: 10.1093/cercor/bhx063. View

16.

MOSIER Jr H, Dearden L, Jansons R, HILL R . Growth hormone, somatomedin and cartilage sulfation in failure of catch-up growth after propylthiouracil-induced hypothyroidism in the rat. Endocrinology. 1977; 100(6):1644-51. DOI: 10.1210/endo-100-6-1644. View

17.

Lavado-Autric R, Auso E, Garcia-Velasco J, Arufe M, del Rey F, Berbel P . Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest. 2003; 111(7):1073-82. PMC: 152582. DOI: 10.1172/JCI16262. View

18.

Fishman R, Gaathon A, Yanai J . Early barbiturate treatment eliminates peak serum thyroxine levels in neonatal mice and produces ultrastructural damage in the brains of adults. Brain Res. 1982; 281(2):202-5. DOI: 10.1016/0165-3806(82)90158-4. View

19.

Li N, Zhao C, Wang Y, Yuan X . The transcription factor Cux1 regulates dendritic morphology of cortical pyramidal neurons. PLoS One. 2010; 5(5):e10596. PMC: 2868054. DOI: 10.1371/journal.pone.0010596. View

20.

Uchida K, Yonezawa M, Nakamura S, Kobayashi T, Machida T . Impaired neurogenesis in the growth-retarded mouse is reversed by T3 treatment. Neuroreport. 2005; 16(2):103-6. DOI: 10.1097/00001756-200502080-00005. View