Thyroid Hormone Accelerates the Differentiation of Adult Hippocampal Progenitors

Journal of Neuroendocrinology

Volumn 24, Issue 9, 2012, Pages 1259-1271

  Kapoor, R ^a   Desouza, L A ^a   Nanavaty, I N ^a   Kernie, S G ^b   Vaidya, V A ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

Hyperthyroid; Hypothyroid; Neurospheres; Proneural transcription factors

Indexed keywords

DOUBLECORTIN; GREEN FLUORESCENT PROTEIN; LIOTHYRONINE; NESTIN; THYROTROPIN; THYROXINE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; GRANULE CELL; HIPPOCAMPUS; IN VITRO STUDY; MALE; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; STEM CELL; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL;

ANIMALS; CELL COUNT; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; HYPERTHYROIDISM; HYPOTHYROIDISM; MALE; METHIMAZOLE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR IMAGING; NEURAL STEM CELLS; NEUROGENESIS; PROMOTER REGIONS, GENETIC; THYROTROPIN; THYROXINE; TRANSCRIPTION FACTORS; TRIIODOTHYRONINE; UP-REGULATION;

EID: 84865314266     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02329.x     Document Type: Article

References (39)

1. Bernal J. Thyroid hormones and brain development. Vitam Horm 2005; 71: 95-122.
2. Desouza LA, Ladiwala U, Daniel SM, Agashe S, Vaidya RA, Vaidya VA. Thyroid hormone regulates hippocampal neurogenesis in the adult rat brain. Mol Cell Neurosci 2005; 29: 414-426.
3. Ambrogini P, Cuppini R, Ferri P, Mancini C, Ciaroni S, Voci A, Gerdoni E, Gallo G. Thyroid hormones affect neurogenesis in the dentate gyrus of adult rat. Neuroendocrinology 2005; 81: 244-253.
4. Montero-Pedrazuela A, Venero C, Lavado-Autric R, Fernandez-Lamo I, Garcia-Verdugo JM, Bernal J, Guadano-Ferraz A. Modulation of adult hippocampal neurogenesis by thyroid hormones: implications in depressive-like behavior. Mol Psychiatry 2006; 11: 361-371.
5. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004; 27: 447-452.
6. Ming GL, Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011; 70: 687-702.
7. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, von der Behrens W, Kempermann G. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 2003; 24: 603-613.
8. Kronenberg G, Reuter K, Steiner B, Brandt MD, Jessberger S, Yamaguchi M, Kempermann G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 2003; 467: 455-463.
9. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999; 2: 266-270.
10. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999; 2: 260-265.
11. Yu TS, Dandekar M, Monteggia LM, Parada LF, Kernie SG. Temporally regulated expression of Cre recombinase in neural stem cells. Genesis 2005; 41: 147-153.
12. Desouza LA, Sathanoori M, Kapoor R, Rajadhyaksha N, Gonzalez LE, Kottmann AH, Tole S, Vaidya VA. Thyroid hormone regulates the expression of the sonic hedgehog signaling pathway in the embryonic and adult mammalian brain. Endocrinology 2011; 152: 1989-2000.
13. Yamada M, Saga Y, Shibusawa N, Hirato J, Murakami M, Iwasaki T, Hashimoto K, Satoh T, Wakabayashi K, Taketo MM, Mori M. Tertiary hypothyroidism and hyperglycemia in mice with targeted disruption of the thyrotropin-releasing hormone gene. Proc Natl Acad Sci USA 1997; 94: 10862-10867.
14. Jhaveri DJ, Mackay EW, Hamlin AS, Marathe SV, Nandam LS, Vaidya VA, Bartlett PF. Norepinephrine directly activates adult hippocampal precursors via beta3-adrenergic receptors. J Neurosci 2010; 30: 2795-2806.
15. Wang JW, David DJ, Monckton JE, Battaglia F, Hen R. Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J Neurosci 2008; 28: 1374-1384.
16. Benekareddy M, Goodfellow NM, Lambe EK, Vaidya VA. Enhanced function of prefrontal serotonin 5-HT(2) receptors in a rat model of psychiatric vulnerability. J Neurosci 2010; 30: 12138-12150.
17. Denver RJ, Williamson KE. Identification of a thyroid hormone response element in the mouse Kruppel-like factor 9 gene to explain its postnatal expression in the brain. Endocrinology 2009; 150: 3935-3943.
18. Dong H, Yauk CL, Rowan-Carroll A, You SH, Zoeller RT, Lambert I, Wade MG. Identification of thyroid hormone receptor binding sites and target genes using ChIP-on-chip in developing mouse cerebellum. PLoS ONE 2009; 4: e4610.
19. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005; 28: 223-250.
20. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 2005; 21: 1-14.
21. Farioli-Vecchioli S, Saraulli D, Costanzi M, Leonardi L, Cina I, Micheli L, Nutini M, Longone P, Oh SP, Cestari V, Tirone F. Impaired terminal differentiation of hippocampal granule neurons and defective contextual memory in PC3/Tis21 knockout mice. PLoS ONE 2009; 4: e8339.
22. Ding M, Robel L, James AJ, Eisenstat DD, Leckman JF, Rubenstein JL, Vaccarino FM. Dlx-2 homeobox gene controls neuronal differentiation in primary cultures of developing basal ganglia. J Mol Neurosci 1997; 8: 93-113.
23. Elmi M, Matsumoto Y, Zeng ZJ, Lakshminarasimhan P, Yang W, Uemura A, Nishikawa S, Moshiri A, Tajima N, Agren H, Funa K. TLX activates MASH1 for induction of neuronal lineage commitment of adult hippocampal neuroprogenitors. Mol Cell Neurosci 2010; 45: 121-131.
24. Kapoor R, van Hogerlinden M, Wallis K, Ghosh H, Nordstrom K, Vennstrom B, Vaidya VA. Unliganded thyroid hormone receptor {alpha}1 impairs adult hippocampal neurogenesis. FASEB J 2010; 24: 4793-4800.
25. Galli R, Fiocco R, De Filippis L, Muzio L, Gritti A, Mercurio S, Broccoli V, Pellegrini M, Mallamaci A, Vescovi AL. Emx2 regulates the proliferation of stem cells of the adult mammalian central nervous system. Development 2002; 129: 1633-1644.
26. Scobie KN, Hall BJ, Wilke SA, Klemenhagen KC, Fujii-Kuriyama Y, Ghosh A, Hen R, Sahay A. Kruppel-like factor 9 is necessary for late-phase neuronal maturation in the developing dentate gyrus and during adult hippocampal neurogenesis. J Neurosci 2009; 29: 9875-9887.
27. Fernandez M, Paradisi M, Del Vecchio G, Giardino L, Calza L. Thyroid hormone induces glial lineage of primary neurospheres derived from non-pathological and pathological rat brain: implications for remyelination-enhancing therapies. Int J Dev Neurosci 2009; 27: 769-778.
28. Lemkine GF, Raj A, Alfama G, Turque N, Hassani Z, Alegria-Prevot O, Samarut J, Levi G, Demeneix BA. Adult neural stem cell cycling in vivo requires thyroid hormone and its alpha receptor. FASEB J 2005; 19: 863-865.
29. Kelley MW, Turner JK, Reh TA. Ligands of steroid/thyroid receptors induce cone photoreceptors in vertebrate retina. Development 1995; 121: 3777-3785.
30. Wang L, Shao YY, Ballock RT. Thyroid hormone interacts with the Wnt/beta-catenin signaling pathway in the terminal differentiation of growth plate chondrocytes. J Bone Miner Res 2007; 22: 1988-1995.
31. Muscat GE, Mynett-Johnson L, Dowhan D, Downes M, Griggs R. Activation of myoD gene transcription by 3, 5, 3'-triiodo-L-thyronine: a direct role for the thyroid hormone and retinoid X receptors. Nucleic Acids Res 1994; 22: 583-591.
32. Muscat GE, Downes M, Dowhan DH. Regulation of vertebrate muscle differentiation by thyroid hormone: the role of the myoD gene family. BioEssays 1995; 17: 211-218.
33. Barres BA, Lazar MA, Raff MC. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 1994; 120: 1097-1108.
34. Billon N, Jolicoeur C, Tokumoto Y, Vennstrom B, Raff M. Normal timing of oligodendrocyte development depends on thyroid hormone receptor alpha 1 (TRalpha1). EMBO J 2002; 21: 6452-6460.
35. Durand B, Raff M. A cell-intrinsic timer that operates during oligodendrocyte development. BioEssays 2000; 22: 64-71.
36. Attardo A, Fabel K, Krebs J, Haubensak W, Huttner WB, Kempermann G. Tis21 expression marks not only populations of neurogenic precursor cells but also new postmitotic neurons in adult hippocampal neurogenesis. Cereb Cortex 2010; 20: 304-314.
37. Farioli-Vecchioli S, Saraulli D, Costanzi M, Pacioni S, Cina I, Aceti M, Micheli L, Bacci A, Cestari V, Tirone F. The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol 2008; 6: e246.
38. Zhang CL, Zou Y, He W, Gage FH, Evans RM. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 2008; 451: 1004-1007.
39. Hong SM, Liu Z, Fan Y, Neumann M, Won SJ, Lac D, Lum X, Weinstein PR, Liu J. Reduced hippocampal neurogenesis and skill reaching performance in adult Emx1 mutant mice. Exp Neurol 2007; 206: 24-32.