The maintenance of hippocampal pyramidal neuron populations is dependent on the modulation of specific cell cycle regulators by thyroid hormones

Brain Research

Volumn 1271, Issue , 2009, Pages 27-35

  Alva Sánchez, Claudia ^a   Sánchez Huerta, Karla ^a   Arroyo Helguera, Omar ^b   Anguiano, Brenda ^b   Aceves, Carmen ^b   Pacheco Rosado, Jorge ^a  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b CENTRO DE FÍSICA APLICADA Y TECNOLOGÍA AVANZADA   (Mexico)

Author keywords

Apoptosis; Bax Bcl 2; Cycline D1; Hypothyroidism; PCNA

Indexed keywords

CYCLIN D1; IODINE 125; LIOTHYRONINE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P21; PROTEIN P53; THIAMAZOLE; THYROXINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE MARKER; DRUG MECHANISM; HIPPOCAMPUS; HISTOPATHOLOGY; HYPOTHYROIDISM; MALE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; ANTITHYROID AGENTS; BCL-2-ASSOCIATED X PROTEIN; CELL CYCLE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HYPOTHYROIDISM; MALE; METHIMAZOLE; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAMIDAL CELLS; RATS; RATS, WISTAR; THYROID GLAND; THYROID HORMONES; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; RATTUS;

EID: 67349142579     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.02.043     Document Type: Article

References (54)

1. Alva-Sánchez C., Ortiz-Butrón R., and Pacheco-Rosado J. Kainic acid does not affect CA3 hippocampal region pyramidal cells in hypothyroid rats. Brain Res. Bull. 63 (2004) 167-171
2. Ambrogini P., Cuppini R., Ferri P., Manzini C., Ciaroni S., Voci A., Gerdoni E., and Gallo G. Thyroid hormones affect neurogenesis in the dentate gryrus of adult rat. Neuroendocrinology 81 (2005) 244-253
3. Anguiano B., Aceves C., Navarro L., Ramírez del Angel A., Luna M., Perera G., and Valverde-R C. Neuroendocrine regulation of adrenal 5′-monodeiodination during acute cold exposure in the rat. I. Effects of hypophysectomy. Endocrinology 128 (1991) 504-508
4. Banks D., Wu M., Higa L.A., Gavrilova N., Quan J., Ye T., Kobayashi R., Sun H., and Zhang H. L2DTL/CDT2 and PCNA interact with p53 and regulate p53 polyubiquitination and protein stability through MDM2 and CUL4A/DDB1 complexes. Cell Cycle 5 (2006) 1719-1729
5. Barrera-Hernández G., Zhan Q., Wong R., and Cheng S.Y. Thyroid hormone receptor is a negative regulator in p53-mediated signaling pathways. DNA Cell Biol. 17 (1998) 743-750
6. Barrera-Hernández G., Park K.S., Dace A., Zhan Q., and Cheng S.Y. Thyroid hormone-induced cell proliferation in GC cells is mediated by changes in G1 cycline/cycline-dependent kinase levels and activity. Endocrinology 140 (1999) 5267-5274
7. Bauer A., Mikulits W., Lagger G., Stengl G., Brosch G., and Beug H. The thyroid hormone receptor functions as a ligand-operated developmental switch between proliferation and differentiation of erythroid progenitors. EMBO J. 17 (1998) 4291-4303
8. Bernal J. Iodine and brain development. Biofactors 10 (1999) 271-276
9. Bernal J. Action of thyroid hormone in brain. J. Endocrinol. Invest. 25 (2002) 268-288
10. Bianco A.C., and Kim B.W. Deiodinases: implications of the local control of thyroid hormone action. J. Clin. Invest. 116 (2006) 2571-2579
11. Cadwell C., and Zambetti G.P. The effects of wild-type p53 tumor suppressor activity and mutant p53 gain-of-function on cell growth. Gene 277 (2001) 15-30
12. Calloni G.W., Penno C.A., Cordova F.M., Trentin A.G., Neto V.M., and Leal R.B. Congenital hypothyroidism alters the phosphorylation of ERK1/2 and p38MAPK in the hippocampus of neonatal rats. Brain Res. Dev. Brain Res. 154 (2005) 141-145
13. Calvo R., Obregón M.J., Ruiz de Ona C., Escobar del Rey F., and Morreale de Escobar G. Congenital hypothyroidism, as studied in rats. Crucial role of maternal thyroxine but not of 3,5,3′-triiodothyronine in the protection of the fetal brain. J. Clin. Invest. 86 (1990) 889-899
14. Calzà L., Aloe L., and Giardino L. Thyroid hormone-induce plasticity in adult rat brain. Brain Res. Bull. 44 (1997) 549-557
15. Cano-Europa E., Pérez-Severiano F., Vergara P., Ortiz-Butrón R., Ríos C., Segovia J., and Pacheco-Rosado J. Hypothyroidism induces selective oxidative stress in amygdala and hippocampus of rat. Metab. Brain Dis. 23 (2008) 275-287
16. Danos P., Frotscher M., and Freund T.F. Non-pyramidal cells in the CA3 region of the rat hippocampus: relationships of fine structure, synaptic input and chemical characteristics. Brain Res. 546 (1991) 195-202
17. Desouza L.A., Ladiwala U., Daniel S.M., Agashe S.S., Vahadilla R.A., and Vaidya V.A. Thyroid hormone regulates hippocampal neurogenesis in the adult rat brain. Mol. Cell. Neurosci. 29 (2005) 414-426
18. Ehninger D., and Kempermann G. Neurogenesis in the adult hippocampus. Cell Tissue Res. 331 (2008) 243-250
19. Escobar-Morreale H.F., Obregón M.J., Hernández A., Escobar del Rey F., and Morreale de Escobar G. Regulation of iodothyronine deiodinase activity as studied in thyroidectomized rats infused with thyroxine or triiodothyronine. Endocrinology 138 (1997) 2559-2568
20. Gali-Muhtasib H., and Bakkar N. Modulating cell cycle: current applications and prospects for future drug development. Curr. Cancer Drug Targets 2 (2002) 309-336
21. Gerges N.Z., and Alkadhi K.A. Hypothyroidism impairs late LTP in CA1 region of the intact rat hippocampus: MAPK involvement. Hippocampus 14 (2004) 40-45
22. Golias C.H., Charalabopoulos A., and Charalabopoulos K. Cell proliferation and cell cycle control: a mini review. Int. J. Clin. Pract. 58 (2004) 1134-1141
23. Gould E., Allan M.D., and McEwen B.S. Dendritic spine density of adult hippocampal pyramidal cells is sensitive to thyroid hormone. Brain Res. 252 (1990) 327-329
24. Harpavat S., and Cepko C.L. Thyroid hormone and retinal development: an emerging field. Thyroid 13 (2003) 1013-1019
25. Herwig S., and Strauss M. The retinoblastoma protein: a master regulator of cell cycle, differentiation and apoptosis. Eur. J. Biochem. 246 (1997) 581-601
26. Huang X.W., Yin H.M., Ji C., Qin Y.F., Yang R.W., and Zhao Z.Y. Effects of perinatal hypothyroidism on rat behavior and its relation with apoptosis of hippocampus neurons. J. Endocrinol. Invest. 31 (2008) 8-15
27. Kundu S., Pramanik M., Roy S., De J., Biswas A., and Ray A.K. Maintenance of brain thyroid hormone level during peripheral hypothyroid condition in adult rat. Life Sci. 79 (2006) 1450-1455
28. Kuribayashi K., and El-Deiry W.S. Regulation of programmed cell death by the p53 pathway. Adv. Exp. Med. Biol. 615 (2008) 201-221
29. Lang J.T., and McCullough L.D. Pathways to ischemic neuronal cell death: are sex differences relevant?. J. Transl. Med. 6 (2008) 33
30. Lemkine G.F., Raj A., Alfama G., Turque N., Hassani Z., Alegria-Prèvot O., Samarut J., Levi G., and Demeneix A. Adult neural stem cell cycling in vivo requires thyroid hormone and its alpha receptor. FASEB J. 19 (2005) 863-865
31. Leonard J.L. Non-genomic actions of thyroid hormone in brain development. Steroids 73 (2008) 1008-1012
32. Lima S.F.S., Gervais A., Colin C., Izembart M., Neto V.M., and Mallat M. Regulation of microglial development: a novel role for thyroid hormone. J. Neurosci. 21 (2001) 2028-2038
33. Lin H.Y., Tang H.Y., Shih A., Keating T., Cao G., Davis P.J., and Davis F.B. Thyroid hormone is a MAPK-dependent growth factor for thyroid cancer cells and is anti-apoptotic. Steroids 72 (2007) 180-187
34. Madeira M.D., Sousa N., Lima-Andrade M.T., Calheiros F., Cadete-Leite A., and Paula-Barbosa M.M. Selective vulnerability of the hippocampal pyramidal neurons to hypothyroidism in male and female rats. J. Comp. Neurol. 322 (1992) 501-518
35. Markakis E.A., and Gage F.H. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J. Comp. Neurol. 406 (1999) 449-460
36. Martínez R., and Gomes F.C. Proliferation of cerebellar neurons induced by astrocytes treated with thyroid hormone is mediated by a cooperation between cell contact and soluble factors and involves the epidermal growth factor-protein kinase a pathway. J. Neurosci. Res. 80 (2005) 341-349
37. Moldovan G.-L., Pfnder B., and Jentsch S. PCNA, the maestro of the replication fork. Cell 129 (2007) 665-679
38. Nicholls D.G., and Budd S.L. Mitochondria and neuronal survival. Physiol. Rev. 80 (2000) 315-360
39. Pacheco-Rosado J., Zamudio-Hernández S., and Chambert G. Thyroid hormones modify susceptibility to lidocaine-kindling in rats. Life Sci. 69 (2001) 2575-2582
40. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, London
41. Porterfield S.P., and Hendrich C.E. The role of thyroid hormones in prenatal and neonatal neurological development - current perspectives. Endocr. Rev. 14 (1993) 94-106
42. Puzianowska-Kuznicka M., Pietrzak M., Turowska O., and Nauman A. Thyroid hormones and their receptors in the regulation of cell proliferation. Acta Biochim. Pol. 53 (2006) 641-650
43. Rami A., and Krieglstein J. Thyroxine attenuates hippocampal neuronal damage caused by ischemia in the rat. Life Sci. 50 (1992) 645-650
44. Richardson S.J., Lemkine G.F., Alfama G., Hassani Z., and Demeneix B.A. Cell division and apoptosis in the adult neural stem cell niche are differentially affected in transthyretin null mice. Neurosci. Lett. 421 (2007) 234-238
45. Rousseau D., Cannella D., Boulaire J., Fitzgerald P., Fotedar A., and Fotedar R. Growth inhibition by CDK-cyclin and PCNA binding domains of p21 occurs by distinct mechanisms and is regulated by ubiquitin-proteasome pathway. Oncogene 18 (1999) 4313-4425
46. Sala-Roca J., Estebanez-Perpina E., Balada F., Garau A., and Martí-Carbonell M.A. Effects of adult dysthyroidism on the morphology of hippocampal neurons. Behav. Brain Res. 188 (2008) 348-354
47. Tatton W.G., and Olanow C.W. Apoptosis in neurodegenerative diseases: the role of mitochondria. Biochim. Biophys. Acta 1410 (1999) 195-213
48. Trentin A.G., Alvarez-Silva M., and Moura Neto V. Thyroid hormone induces cerebellar astrocytes and C6 glioma cells to secrete mitogenic growth factors. Am. J. Physiol: Endocrinol. Metab. 281 (2001) E1088-E1094
49. Toms S.A., Hercbergs A., Liu J., Kondo S., Bernett G.H., Casey G., and Barna B.P. Thyroid hormone depletion inhibits astrocytoma proliferation via a p53-independent induction of p21 (WAF1/CIP1). Anticancer Res. 18 (1998) 289-293
50. Valverde-R C., Aceves C., and Reyes-Z E. Ontogenesis of iodothyronine deiodinase activities in brain and liver of the chick embryo. Endocrinology 132 (1993) 867-872
51. Xiang H., Kinoshita Y., Knudson C.M., Korsmeyer S.J., Schwartzkroin P.A., and Morrison R.S. Bax involvement in p53-mediated neuronal cell death. J. Neurosci. 18 (1998) 1363-1373
52. Yu S.W., Wang H., Dawson T.M., and Dawson V.L. Poly(ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity. Neurobiol. Dis. 14 (2004) 303-317
53. Zamzami N., and Kroemer G. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev., Mol. Cell Biol. 2 (2001) 67-71
54. Zoeller R.T., and Rovet J. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J. Neuroendocrinol. 16 (2004) 809-818