A Bimodal Influence of Thyroid Hormone on Cerebellum Oligodendrocyte Differentiation

Overview

Journal Mol Endocrinol

Specialties Endocrinology
Molecular Biology

Date 2012 Feb 25

PMID 22361821

Citations 27

Authors

Frederic Picou

Teddy Fauquier

Fabrice Chatonnet

Frederic Flamant

Affiliations

Soon will be listed here.

Abstract

Thyroid hormone (T(3)) can trigger a massive differentiation of cultured oligodendrocytes precursor cells (OPC) by binding the nuclear T(3) receptor α1 (TRα1). Whether this reflects a physiological function of TRα1 remains uncertain. Using a recently generated mouse model, in which CRE/loxP recombination is used to block its function, we show that TRα1 acts at two levels for the in vivo differentiation of OPC in mouse cerebellum. At the early postnatal stage, it promotes the secretion of several neurotrophic factors by acting in Purkinje neurons and astrocytes, defining an environment suitable for OPC differentiation. At later stages, TRα1 acts in a cell-autonomous manner to ensure the complete arrest of OPC proliferation. These data explain contradictory observations made on various models and outline the importance of T(3) signaling both for synchronizing postnatal neurodevelopment and restraining OPC proliferation in adult brain.

Citing Articles

Impaired T3 uptake and action in MCT8-deficient cerebral organoids underlie Allan-Herndon-Dudley syndrome.

Salas-Lucia F, Escamilla S, Bianco A, Dumitrescu A, Refetoff S JCI Insight. 2024; 9(7).

PMID: 38376950 PMC: 11128209. DOI: 10.1172/jci.insight.174645.

Thyroid hormone action during GABAergic neuron maturation: The quest for mechanisms.

Richard S, Ren J, Flamant F Front Endocrinol (Lausanne). 2023; 14:1256877.

PMID: 37854197 PMC: 10579935. DOI: 10.3389/fendo.2023.1256877.

International Union of Basic and Clinical Pharmacology CXIII: Nuclear Receptor Superfamily-Update 2023.

Burris T, de Vera I, Cote I, Flaveny C, Wanninayake U, Chatterjee A Pharmacol Rev. 2023; 75(6):1233-1318.

PMID: 37586884 PMC: 10595025. DOI: 10.1124/pharmrev.121.000436.

Thyroid hormone as a temporal switch in mouse development.

Ren J, Flamant F Eur Thyroid J. 2023; 12(2).

PMID: 36715693 PMC: 10083660. DOI: 10.1530/ETJ-22-0225.

Single-cell RNA-based phenotyping reveals a pivotal role of thyroid hormone receptor alpha for hypothalamic development.

Sreenivasan V, Dore R, Resch J, Maier J, Dietrich C, Henck J Development. 2023; 150(3).

PMID: 36715020 PMC: 10110490. DOI: 10.1242/dev.201228.

References

Mecklenburg N, Garcia-Lopez R, Puelles E, Sotelo C, Martinez S . Cerebellar oligodendroglial cells have a mesencephalic origin. Glia. 2011; 59(12):1946-57. DOI: 10.1002/glia.21236. View

Mittag J, Wallis K, Vennstrom B . Physiological consequences of the TRalpha1 aporeceptor state. Heart Fail Rev. 2008; 15(2):111-5. DOI: 10.1007/s10741-008-9119-5. View

Grimaldi P, Parras C, Guillemot F, Rossi F, Wassef M . Origins and control of the differentiation of inhibitory interneurons and glia in the cerebellum. Dev Biol. 2009; 328(2):422-33. DOI: 10.1016/j.ydbio.2009.02.008. View

Guo F, Ma J, McCauley E, Bannerman P, Pleasure D . Early postnatal proteolipid promoter-expressing progenitors produce multilineage cells in vivo. J Neurosci. 2009; 29(22):7256-70. PMC: 2717630. DOI: 10.1523/JNEUROSCI.5653-08.2009. View

Fauquier T, Romero E, Picou F, Chatonnet F, Nguyen X, Quignodon L . Severe impairment of cerebellum development in mice expressing a dominant-negative mutation inactivating thyroid hormone receptor alpha1 isoform. Dev Biol. 2011; 356(2):350-8. DOI: 10.1016/j.ydbio.2011.05.657. View

Boukhtouche F, Janmaat S, Vodjdani G, Gautheron V, Mallet J, Dusart I . Retinoid-related orphan receptor alpha controls the early steps of Purkinje cell dendritic differentiation. J Neurosci. 2006; 26(5):1531-8. PMC: 6675487. DOI: 10.1523/JNEUROSCI.4636-05.2006. View

Slezak M, Goritz C, Niemiec A, Frisen J, Chambon P, Metzger D . Transgenic mice for conditional gene manipulation in astroglial cells. Glia. 2007; 55(15):1565-76. DOI: 10.1002/glia.20570. View

Zhu X, Hill R, Dietrich D, Komitova M, Suzuki R, Nishiyama A . Age-dependent fate and lineage restriction of single NG2 cells. Development. 2011; 138(4):745-53. PMC: 3026417. DOI: 10.1242/dev.047951. View

Rodriguez-Pena A, Ibarrola N, Iniguez M, Munoz A, Bernal J . Neonatal hypothyroidism affects the timely expression of myelin-associated glycoprotein in the rat brain. J Clin Invest. 1993; 91(3):812-8. PMC: 288032. DOI: 10.1172/JCI116301. View

10.

Baas D, Legrand C, Samarut J, Flamant F . Persistence of oligodendrocyte precursor cells and altered myelination in optic nerve associated to retina degeneration in mice devoid of all thyroid hormone receptors. Proc Natl Acad Sci U S A. 2002; 99(5):2907-11. PMC: 122446. DOI: 10.1073/pnas.052482299. View

11.

Tang D, Tokumoto Y, Apperly J, Lloyd A, Raff M . Lack of replicative senescence in cultured rat oligodendrocyte precursor cells. Science. 2001; 291(5505):868-71. DOI: 10.1126/science.1056780. View

12.

Delaney C, Brenner M, Messing A . Conditional ablation of cerebellar astrocytes in postnatal transgenic mice. J Neurosci. 1996; 16(21):6908-18. PMC: 6579279. View

13.

Bouslama-Oueghlani L, Wehrle R, Sotelo C, Dusart I . Heterogeneity of NG2-expressing cells in the newborn mouse cerebellum. Dev Biol. 2005; 285(2):409-21. DOI: 10.1016/j.ydbio.2005.07.003. View

14.

Lin S, Huck J, Roberts J, Macklin W, Somogyi P, Bergles D . Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron. 2005; 46(5):773-85. DOI: 10.1016/j.neuron.2005.04.025. View

15.

Rivers L, Young K, Rizzi M, Jamen F, Psachoulia K, Wade A . PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci. 2008; 11(12):1392-401. PMC: 3842596. DOI: 10.1038/nn.2220. View

16.

Morte B, Manzano J, Scanlan T, Vennstrom B, Bernal J . Aberrant maturation of astrocytes in thyroid hormone receptor alpha 1 knockout mice reveals an interplay between thyroid hormone receptor isoforms. Endocrinology. 2003; 145(3):1386-91. DOI: 10.1210/en.2003-1123. View

17.

Heuer H, Mason C . Thyroid hormone induces cerebellar Purkinje cell dendritic development via the thyroid hormone receptor alpha1. J Neurosci. 2003; 23(33):10604-12. PMC: 6740935. View

18.

Du Y, Dreyfus C . Oligodendrocytes as providers of growth factors. J Neurosci Res. 2002; 68(6):647-54. DOI: 10.1002/jnr.10245. View

19.

Goodman J, Gilbert M . Modest thyroid hormone insufficiency during development induces a cellular malformation in the corpus callosum: a model of cortical dysplasia. Endocrinology. 2007; 148(6):2593-7. DOI: 10.1210/en.2006-1276. View

20.

Quignodon L, Vincent S, Winter H, Samarut J, Flamant F . A point mutation in the activation function 2 domain of thyroid hormone receptor alpha1 expressed after CRE-mediated recombination partially recapitulates hypothyroidism. Mol Endocrinol. 2007; 21(10):2350-60. DOI: 10.1210/me.2007-0176. View