Thyroid hormone triggers the developmental loss of axonal regenerative capacity via thyroid hormone receptor α1 and krüppel-like factor 9 in Purkinje cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 35, 2012, Pages 14206-14211

  Avci, Hasan X ^a,b   Lebrun, Clement ^a,b   Wehrlé, Rosine ^a,b   Doulazmi, Mohamed ^a,b   Chatonnet, Fabrice ^c   Morel, Marie Pierre ^a,b   Ema, Masatsugu ^d   Vodjdani, Guilan ^e   Sotelo, Constantino ^f   Flamant, Frédéric ^c   Dusart, Isabelle ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^f INSTITUTO DE NEUROCIENCIAS   (Spain)

Author keywords

Axon regeneration; Cerebellum; Lentiviral vectors; Neural development

Indexed keywords

KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 9; THYROID HORMONE; THYROID HORMONE RECEPTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXPOSURE; GAIN OF FUNCTION MUTATION; HORMONE ACTION; LOSS OF FUNCTION MUTATION; MOUSE; NERVE FIBER DEGENERATION; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AXONS; AXOTOMY; CEREBELLUM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LENTIVIRUS; MALE; MICE; MICE, KNOCKOUT; NERVE REGENERATION; ORGAN CULTURE TECHNIQUES; PREGNANCY; PURKINJE CELLS; RECEPTORS, THYROID HORMONE; TRIIODOTHYRONINE;

ANIMALIA; MUS; VERTEBRATA;

EID: 84865542307     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1119853109     Document Type: Article

References (41)

1. Schwab ME, Bartholdi D (1996) Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 76:319-370. (Pubitemid 26163712)
2. Schwab ME (2004) Nogo and axon regeneration. Curr Opin Neurobiol 14(1):118-124.
3. He Z, Koprivica V (2004) The Nogo signaling pathway for regeneration block. Annu Rev Neurosci 27:341-368. (Pubitemid 39050407)
4. Cai D, et al. (2001) Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J Neurosci 21:4731-4739. (Pubitemid 32565631)
5. Moore DL, et al. (2009) KLF family members regulate intrinsic axon regeneration ability. Science 326:298-301.
6. Liu K, Tedeschi A, Park KK, He Z (2011) Neuronal intrinsic mechanisms of axon regeneration. Annu Rev Neurosci 34:131-152.
7. Li D, Field PM, Raisman G (1995) Failure of axon regeneration in postnatal rat entorhinohippocampal slice coculture is due to maturation of the axon, not that of the pathway or target. Eur J Neurosci 7:1164-1171.
8. Chen DF, Jhaveri S, Schneider GE (1995) Intrinsic changes in developing retinal neurons result in regenerative failure of their axons. Proc Natl Acad Sci USA 92:7287-7291.
9. Dusart I, Airaksinen MS, Sotelo C (1997) Purkinje cell survival and axonal regeneration are age dependent: an in vitro study. J Neurosci 17:3710-3726. (Pubitemid 27200596)
10. Gianola S, Rossi F (2001) Evolution of the Purkinje cell response to injury and regenerative potential during postnatal development of the rat cerebellum. J Comp Neurol 430(1):101-117.
11. Oishi Y, Baratta J, Robertson RT, Steward O (2004) Assessment of factors regulating axon growth between the cortex and spinal cord in organotypic co-cultures: Effects of age and neurotrophic factors. J Neurotrauma 21:339-356. (Pubitemid 38401755)
12. Morreale de Escobar G, Calvo R, Escobar del Rey F, Obregón MJ (1994) Thyroid hormones in tissues from fetal and adult rats. Endocrinology 134:2410- 2415.
13. Gauthier K, et al. (1999) Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development. EMBO J 18:623-631. (Pubitemid 29057247)
14. Hadj-Sahraoui N, Seugnet I, Ghorbel MT, Demeneix B (2000) Hypothyroidism prolongs mitotic activity in the post-natal mouse brain. Neurosci Lett 280(2):79-82. (Pubitemid 30109137)
15. Kress E, Samarut J, Plateroti M (2009) Thyroid hormones and the control of cell proliferation or cell differentiation: Paradox or duality? Mol Cell Endocrinol 313(1-2):36-49.
16. Martel J, Cayrou C, Puymirat J (2002) Identification of new thyroid hormone-regulated genes in rat brain neuronal cultures. Neuroreport 13:1849-1851. (Pubitemid 35398947)
17. Denver RJ, Williamson KE (2009) Identification of a thyroid hormone response element in the mouse Kruppel-like factor 9 gene to explain its postnatal expression in the brain. Endocrinology 150:3935-3943.
18. Ghoumari AM, Wehrlé R, De Zeeuw CI, Sotelo C, Dusart I (2002) Inhibition of protein kinase C prevents Purkinje cell death but does not affect axonal regeneration. J Neurosci 22:3531-3542.
19. Bouslama-Oueghlani L, Wehrlé R, Sotelo C, Dusart I (2003) The developmental loss of the ability of Purkinje cells to regenerate their axons occurs in the absence of myelin: An in vitro model to prevent myelination. J Neurosci 23:8318-8329.
20. Yen PM (2001) Physiological and molecular basis of thyroid hormone action. Physiol Rev 81:1097-1142.
21. Heuer H, Mason CA (2003) Thyroid hormone induces cerebellar Purkinje cell dendritic development via the thyroid hormone receptor alpha1. J Neurosci 23:10604-10612. (Pubitemid 37485274)
22. Wallis K, et al. (2010) The thyroid hormone receptor alpha1 protein is expressed in embryonic postmitotic neurons and persists in most adult neurons. Mol Endocrinol 24:1904-1916.
23. Bradley DJ, Young, WS, 3rd, Weinberger C (1989) Differential expression of alpha and beta thyroid hormone receptor genes in rat brain and pituitary. Proc Natl Acad Sci USA 86:7250-7254. (Pubitemid 19240904)
24. Quignodon L, Vincent S, Winter H, Samarut J, Flamant F (2007) A point mutation in the activation function 2 domain of thyroid hormone receptor alpha1 expressed after CRE-mediated recombination partially recapitulates hypothyroidism. Mol Endocrinol 21:2350-2360. (Pubitemid 47529350)
25. Panaite P-A, Barakat-Walter I (2010) Thyroid hormone enhances transected axonal regeneration and muscle reinnervation following rat sciatic nerve injury. J Neurosci Res 88:1751-1763.
26. Venero C, et al. (2005) Anxiety, memory impairment, and locomotor dysfunction caused by a mutant thyroid hormone receptor alpha1 can be ameliorated by T3 treatment. Genes Dev 19:2152-2163. (Pubitemid 41330317)
27. Fauquier T, et al. (2011) Severe impairment of cerebellum development in mice expressing a dominant-negative mutation inactivating thyroid hormone receptor alpha1 isoform. Dev Biol 356:350-358.
28. Hashimoto K, et al. (2001) An unliganded thyroid hormone receptor causes severe neurological dysfunction. Proc Natl Acad Sci USA 98:3998-4003. (Pubitemid 32249887)
29. Portella AC, et al. (2010) Thyroid hormone receptor β mutation causes severe impairment of cerebellar development. Mol Cell Neurosci 44(1):68-77.
30. Oppenheimer JH, Schwartz HL (1997) Molecular basis of thyroid hormone-dependent brain development. Endocr Rev 18:462-475. (Pubitemid 27349552)
31. Koibuchi N (2008) The role of thyroid hormone on cerebellar development. Cerebellum 7:530-533.
32. Boukhtouche F, et al. (2010) Induction of early Purkinje cell dendritic differentiation by thyroid hormone requires RORα. Neural Dev 5:18.
33. Barres BA, Lazar MA, Raff MC (1994) A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120:1097-1108. (Pubitemid 24150036)
34. Filbin MT (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 4:703-713.
35. Picou F, Fauquier T, Chatonnet F, Flamant F (2012) A bimodal influence of thyroid hormone on cerebellum oligodendrocyte differentiation. Mol Endocrinol 26:608-618.
36. Beattie MS, Bresnahan JC, Lopate G (1990) Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs. J Neurobiol 21:1108-1122. (Pubitemid 20362731)
37. Gibbs KM, Chittur SV, Szaro BG (2011) Metamorphosis and the regenerative capacity of spinal cord axons in Xenopus laevis. Eur J Neurosci 33:9-25.
38. McNabb FMA (2006) Avian thyroid development and adaptive plasticity. Gen Comp Endocrinol 147(7):93-101.
39. Hasan SJ, Keirstead HS, Muir GD, Steeves JD (1993) Axonal regeneration contributes to repair of injured brainstem-spinal neurons in embryonic chick. J Neurosci 13:492-507. (Pubitemid 23045134)
40. Fisher DA, Polk DH, Wu SY (1994) Fetal thyroid metabolism: A pluralistic system. Thyroid 4:367-371. (Pubitemid 24295438)
41. Meuli-Simmen C, et al. (1996) The fetal spinal cord does not regenerate after in utero transection in a large mammalian model. Neurosurgery 39:555-560, discussion 560-561.