Effect of thyroid hormone T3 on Myosin-Va expression in the central nervous system

Brain Research

Volumn 1275, Issue , 2009, Pages 1-9

  de Souza Martins, Sheila Cristina ^a,b   Romão, Luciana Ferreira ^a   Faria, Jane Cristina ^a   de Holanda Afonso, Rosenilde Carvalho ^a   Murray, Samantha Angel ^c   Pellizzon, Claudia Helena ^d   Mercer, John A ^e   Cameron, Luiz Claudio ^b,f,g   Moura Neto, Vivaldo ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF THE STATE OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^d SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^e MCLAUGHLIN RESEARCH INSTITUTE   (United States)

^f Universidade Castelo Branco   (Brazil)

^g FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

Author keywords

Astrocyte; Astroglioma; Hypothyroidism; Myosin Va; Neuron; T3

Indexed keywords

LIOTHYRONINE; MYOSIN VA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN; CANCER CELL CULTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EUTHYROIDISM; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; HYPOTHYROIDISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SYNAPTOSOME;

ANIMALS; ANIMALS, NEWBORN; CELL LINE, TUMOR; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, KNOCKOUT; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PREGNANCY; RATS; TRIIODOTHYRONINE;

ANIMALIA; RATTUS;

EID: 67349092506     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.03.070     Document Type: Article

References (68)

1. Abu-Hamdah R., Cho W.J., Horber J.K., and Jena B.P. Secretory vesicles in live cells are not free-floating but tethered to filamentous structures, a study using photonic force microscopy. Ultramicroscopy 106 8-9 (2006) 670-673
2. Ahmed O.M., El-Gareib A.W., El-Bakry A.M., Abd El-Tawab S.M., and Ahmed R.G. Thyroid hormones states and brain development interactions. Int. J. Dev. Neurosci. 26 2 (2008) 147-209
3. Alavez S., Moran J., Franco-Cea A., Ortega-Gomez A., Casaletti L., and Cameron L.C. Myosin Va is proteolysed in rat cerebellar granule neurons after excitotoxic injury. Neurosci. Lett. 367 3 (2004) 404-409
4. Bernal J., Guadano-Ferraz A., and Morte B. Perspectives in the study of thyroid hormone action on brain development and function. Thyroid 13 11 (2003) 1005-1012
5. Bianco A.C., and Kim B.W. Deiodinases: implications of the local control of thyroid hormone action. J. Clin. Invest. 116 10 (2006) 2571-2579
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
7. Bremel R.D., and Weber A. Calcium binding to rabbit skeletal myosin under physiological conditions. Biochim. Biophys. Acta. 376 2 (1975) 366-374
8. Bruno A.N., Ricachenevsky F.K., Pochmann D., Bonan C.D., Battastini A.M., Barreto-Chaves M.L., and Sarkis J.J. Hypothyroidism changes adenine nucleotide hydrolysis in synaptosomes from hippocampus and cerebral cortex of rats in different phases of development. Int. J. Dev. Neurosci. 23 1 (2005) 37-44
9. Calliari A., Sotelo-Silveira J., Costa M.C., Nogueira J., Cameron L.C., Kun A., Benech J., and Sotelo J.R. Myosin Va is locally synthesized following nerve injury. Cell. Motil. Cytoskeleton 51 4 (2002) 169-176
10. Calloni G.W., Alvarez-Silva M., Vituri C., and Trentin A.G. Thyroid hormone deficiency alters extracellular matrix protein expression in rat brain. Brain Res. Dev. Brain Res. 126 1 (2001) 121-124
11. Carlson D.J., Strait K.A., Schwartz H.L., and Oppenheimer J.H. Immunofluorescent localization of thyroid hormone receptor isoforms in glial cells of rat brain. Endocrinology 135 5 (1994) 1831-1836
12. Carlson D.J., Strait K.A., Schwartz H.L., and Oppenheimer J.H. Thyroid hormone receptor isoform content in cultured type 1 and type 2 astrocytes. Endocrinology 137 3 (1996) 911-917
13. Carre J.L., Demerens C., Rodriguez-Pena A., Floch H.H., Vincendon G., and Sarlieve L.L. Thyroid hormone receptor isoforms are sequentially expressed in oligodendrocyte lineage cells during rat cerebral development. J. Neurosci. Res. 54 5 (1998) 584-594
14. Casaletti L., Tauhata S.B., Moreira J.E., and Larson R.E. Myosin-Va proteolysis by Ca2+/calpain in depolarized nerve endings from rat brain. Biochem. Biophys. Res. Commun. 308 1 (2003) 159-164
15. Clos J., Legrand C., Legrand J., Ghandour M.S., Labourdette G., Vincendon G., and Gombos G. Effects of thyroid state and undernutrition on S100 protein and astroglia development in rat cerebellum. Dev. Neurosci. 5 2-3 (1982) 285-292
16. de Escobar G.M., Obregón M.J., and del Rey F.E. Iodine deficiency and brain development in the first half of pregnancy. Public Health Nutr. 10 12A (2007) 1554-1570
17. Dent E.W., and Kalil K. Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 21 24 (2001) 9757-9769
18. Desnos C., Huet S., Fanget I., Chapuis C., Böttiger C., Racine V., Sibarita J.B., Henry J.P., and Darchen F. Myosin va mediates docking of secretory granules at the plasma membrane. J. Neurosci. 27 39 (2007) 10636-10645
19. Dunkley P.R., Jarvie P.E., Heath J.W., Kidd G.J., and Rostas J.A. A rapid method for isolation of synaptosomes on Percoll gradients. Brain Res. 372 1 (1986) 115-129
20. Dunkley P.R., Heath J.W., Harrison S.M., Jarvie P.E., Glenfield P.J., and Rostas J.A. A rapid Percoll gradient procedure for isolation of synaptosomes directly from an S1 fraction: homogeneity and morphology of subcellular fractions. Brain Res. 441 1-2 (1988) 59-71
21. Dussault J.H., and Ruel J. Thyroid hormones and brain development. Annu. Rev. Physiol. 49 (1987) 321-334
22. Espreafico E.M., Cheney R.E., Matteoli M., Nascimento A.A., De Camilli P.V., Larson R.E., and Mooseker M.S. Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains. J. Cell. Biol. 119 6 (1992) 1541-1557
23. Evans L.L., Hammer J., and Bridgman P.C. Subcellular localization of myosin V in nerve growth cones and outgrowth from dilute-lethal neurons. J. Cell. Sci. 110 Pt 4 (1997) 439-449
24. Evans L.L., Lee A.J., Bridgman P.C., and Mooseker M.S. Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. J. Cell. Sci. 111 Pt 14 (1998) 2055-2066
25. Faria J., Romao L., Martins S., Alves T., Mendes F.A., de Faria G.P., Hollanda R., Takiya C., Chimelli L., Morandi V., de Souza J.M., Abreu J.G., and Moura Neto V. Interactive properties of human glioblastoma cells with brain neurons in culture and neuronal modulation of glial laminin organization. Differentiation 74 9-10 (2006) 562-572
26. Gilbert M.E., Sui L., Walker M.J., Anderson W., Thomas S., Smoller S.N., Schon J.P., Phani S., and Goodman J.H. Thyroid hormone insufficiency during brain development reduces parvalbumin immunoreactivity and inhibitory function in the hippocampus. Endocrinology 148 1 (2007) 92-102
27. Gomes F.C., Maia C.G., de Menezes J.R., and Neto V.M. Cerebellar astrocytes treated by thyroid hormone modulate neuronal proliferation. Glia 25 3 (1999) 247-255
28. Gomes F.C., Garcia-Abreu J., Galou M., Paulin D., and Moura Neto V. Neurons induce GFAP gene promoter of cultured astrocytes from transgenic mice. Glia 26 2 (1999) 97-108
29. Gomes F.C., Lima F.R., Trentin A.G., and Moura Neto V. Thyroid hormone role in nervous system morphogenesis. Prog. Brain Res. 132 (2001) 41-50
30. Goodman J.H., and Gilbert M.E. Modest thyroid hormone insufficiency during development induces a cellular malformation in the corpus callosum: a model of cortical dysplasia. Endocrinology 148 6 (2007) 2593-2597
31. Konig S., and Moura Neto V. Thyroid hormone actions on neural cells. Cell Mol. Neurobiol. 22 5-6 (2002) 517-544
32. Legrand C., Ghandour M.S., and Clos J. Histochemical and biochemical studies of butyrylcholinesterase activity in adult and developing cerebellum. Effects of abnormal thyroid state and undernutrition. Neuropathol. Appl. Neurobiol. 9 6 (1983) 433-453
33. Lima F.R., Trentin A.G., Rosenthal D., Chagas C., and Moura Neto V. Thyroid hormone induces protein secretion and morphological changes in astroglial cells with an increase in expression of glial fibrillary acidic protein. J. Endocrinol. 154 1 (1997) 167-175
34. Lima F.R., Goncalves N., Gomes F.C., de Freitas M.S., and Moura Neto V. Thyroid hormone action on astroglial cells from distinct brain regions during development. Int. J. Dev. Neurosci. 16 1 (1998) 19-27
35. Lima F.R., 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 6 (2001) 2028-2038
36. Martinez R., and Gomes F.C. Neuritogenesis induced by thyroid hormone-treated astrocytes is mediated by epidermal growth factor/mitogen-activated protein kinase-phosphatidylinositol 3-kinase pathways and involves modulation of extracellular matrix proteins. J. Biol. Chem. 277 51 (2002) 49311-49318
37. Martinez 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 3 (2005) 341-349
38. Mehta A.D., Rock R.S., Rief M., Spudich J.A., Mooseker M.S., and Cheney R.E. Myosin-V is a processive actin-based motor. Nature 400 6744 (1999) 590-593
39. Mellstrom B., Naranjo J.R., Santos A., Gonzalez A.M., and Bernal J. Independent expression of the alpha and beta c-erbA genes in developing rat brain. Mol. Endocrinol. 5 9 (1991) 1339-1350
40. Mercer J.A., Seperack P.K., Strobel M.C., Copeland N.G., and Jenkins N.A. Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349 6311 (1991) 709-713
41. Milankov K., and De Boni U. Cytochemical localization of actin and myosin aggregates in interphase nuclei in situ. Exp. Cell. Res. 209 2 (1993) 189-199
42. Miller K.E., and Sheetz M.P. Characterization of myosin V binding to brain vesicles. J. Biol. Chem. 275 4 (2000) 2598-2606
43. Moore K.J., Seperack P.K., Strobel M.C., Swing D.A., Copeland N.G., and Jenkins N.A. Dilute suppressor dsu acts semidominantly to suppress the coat color phenotype of a deletion mutation, dl20J, of the murine dilute locus. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 8131-8135
44. Ohashi S., Koike K., Omori A., Ichinose S., Ohara S., Kobayashi S., Sato T.A., and Anzai K. Identification of mRNA/protein (mRNP) complexes containing Puralpha, mStaufen, fragile X protein, and myosin Va and their association with rough endoplasmic reticulum equipped with a kinesin motor. J. Biol. Chem. 277 40 (2002) 37804-37810
45. Ohyama A., Komiya Y., and Igarashi M. Globular tail of myosin-V is bound to vamp/synaptobrevin. Biochem. Biophys. Res. Commun. 280 4 (2001) 988-991
46. Ortiga-Carvalho T.M., Hashimoto K., Pazos-Moura C.C., Geenen D., Cohen R., Lang R.M., and Wondisford F.E. Thyroid hormone resistance in the heart: role of the thyroid hormone receptor beta isoform. Endocrinology 145 4 (2004) 1625-1633
47. Ortiga-Carvalho T.M., Shibusawa N., Nikrodhanond A., Oliveira K.J., Machado D.S., Liao X.H., Cohen R.N., Refetoff S., and Wondisford F.E. Negative regulation by thyroid hormone receptor requires an intact coactivator-binding surface. J. Clin. Invest. 115 9 (2005) 2517-2523
48. Pestic-Dragovich L., Stojiljkovic L., Philimonenko A.A., Nowak G., Ke Y., Settlage R.E., Shabanowitz J., Hunt D.F., Hozak P., and de Lanerolle P. A myosin I isoform in the nucleus. Science 290 5490 (2000) 337-341
49. 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
50. Prekeris R., and Terrian D.M. Brain myosin V is a synaptic vesicle-associated motor protein: evidence for a Ca2+-dependent interaction with the synaptobrevin-synaptophysin complex. J. Cell. Biol. 137 7 (1997) 1589-1601
51. Provance D.W., James T.L., and Mercer J.A. Melanophilin, the product of the leaden locus, is required for targeting of myosin-Va to melanosomes. Traffic 3 2 (2002) 124-132
52. Puymirat J. Thyroid receptors in the rat brain. Prog. Neurobiol. 39 3 (1992) 281-294
53. Rudolf R., Kögel T., Kuznetsov S.A., Salm T., Schlicker O., Hellwig A., Hammer III J.A., and Gerdes H.H. Myosin Va facilitates the distribution of secretory granules in the F-actin rich cortex of PC12 cells. J. Cell Sci. 116 Pt 7 (2003) 1339-1348
54. Sakamoto T., Amitani I., Yokota E., and Ando T. Direct observation of processive movement by individual myosin V molecules. Biochem. Biophys. Res. Commun. 272 2 (2000) 586-590
55. Salerno V.P., Calliari A., Provance Jr. D.W., Sotelo-Silveira J.R., Sotelo J.R., and Mercer J.A. Myosin-Va mediates RNA distribution in primary fibroblasts from multiple organs. Cell. Motil. Cytoskeleton 65 5 (2008) 422-433
56. Sarkar P.K. L-triiodothyronine differentially and nongenomically regulates synaptosomal protein phosphorylation in adult rat brain cerebral cortex: role of calcium and calmodulin. Life Sci. 82 17-18 (2008) 920-927
57. Schumm M.A., Castellanos D.A., Frydel B.R., and Sagen J. Enhanced viability and neuronal differentiation of neural progenitors by chromaffin cell co-culture. Brain Res. Dev. Brain Res. 137 2 (2002) 115-125
58. Sotelo-Silveira J.R., Calliari A., Cardenas M., Koenig E., and Sotelo J.R. Myosin Va and kinesin II motor proteins are concentrated in ribosomal domains (periaxoplasmic ribosomal plaques) of myelinated axons. J. Neurobiol. 60 2 (2004) 187-196
59. Stachelek S.J., Kowalik T.F., Farwell A.P., and Leonard J.L. Myosin V plays an essential role in the thyroid hormone-dependent endocytosis of type II iodothyronine 5′-deiodinase. J. Biol. Chem. 275 41 (2000) 31701-31707
60. Strait K.A., Schwartz H.L., Seybold V.S., Ling N.C., and Oppenheimer J.H. Immunofluorescence localization of thyroid hormone receptor protein beta 1 and variant alpha 2 in selected tissues: cerebellar Purkinje cells as a model for beta 1 receptor-mediated developmental effects of thyroid hormone in brain. Proc. Natl. Acad. Sci. U. S. A. 88 9 (1991) 3887-3891
61. Takagishi Y., Hashimoto K., Kayahara T., Watanabe M., Otsuka H., Mizoguchi A., Kano M., and Murata Y. Diminished climbing fiber innervation of Purkinje cells in the cerebellum of myosin Va mutant mice and rats. Dev. Neurobiol. 67 7 (2007) 909-923
62. Tilelli C.Q., Martins A.R., Larson R.E., and Garcia-Cairasco N. Immunohistochemical localization of myosin Va in the adult rat brain. Neuroscience 121 3 (2003) 573-586
63. Trentin A.G. Thyroid hormone and astrocyte morphogenesis. J. Endocrinol. 189 2 (2006) 189-197
64. Trentin A.G., and Moura Neto V. T3 affects cerebellar astrocyte proliferation, GFAP and fibronectin organization. Neuroreport 6 2 (1995) 293-296
65. Trentin A.G., Rosenthal D., and Moura Neto V. Thyroid hormone and conditioned medium effects on astroglial cells from hypothyroid and normal rat brain: factor secretion, cell differentiation, and proliferation. J. Neurosci. Res. 41 3 (1995) 409-417
66. 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 5 (2001) E1088-1094
67. Yoshimura A., Fujii R., Watanabe Y., Okabe S., Fukui K., and Takumi T. Myosin-Va facilitates the accumulation of mRNA/protein complex in dendritic spines. Curr. Biol. 16 23 (2006) 2345-2351
68. Zoeller R.T., and Rovet J. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J. Neuroendocrinol. 16 10 (2004) 809-818