Hypothyroidsm alters the development of radial glial cells in the term fetal and postnatal neocortex of the rat

Developmental Brain Research

Volumn 153, Issue 1, 2004, Pages 109-114

  Martinez Galan, Juan Ramon ^a   Escobar Del Rey, Francisco ^b   Morreale De Escobar, Gabriela ^b   Santacana, Maria ^c   Ruiz Marcos, Antonio ^c  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b INSTITUTO CAJAL   (Spain)

^c INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

Development; Methylmercaptoimidazole; Neocortex; Nestin; Radial glia; Thyroid hormone

Indexed keywords

NESTIN; ANTITHYROID AGENT; INTERMEDIATE FILAMENT PROTEIN; NERVE PROTEIN; THIAMAZOLE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL MIGRATION; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYO; FETUS DEVELOPMENT; GLIA CELL; HYPOTHYROIDISM; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MENTAL DEFICIENCY; NEOCORTEX; NERVE CELL; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; THYROID FUNCTION; VISUAL CORTEX; ANIMAL; CELL MOTION; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; FEMALE; FETUS; GLIA; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT;

ANIMALIA;

ANIMALS; ANIMALS, NEWBORN; ANTITHYROID AGENTS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; FEMALE; FETUS; HYPOTHYROIDISM; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENT PROTEINS; METHIMAZOLE; NEOCORTEX; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; PREGNANCY; RATS;

EID: 4644253166     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devbrainres.2004.08.002     Document Type: Article

References (42)

1. M. Alvarez-Dolado, M. Ruiz, J.A. Del Rio, S. Alcantara, F. Burgaya, M. Sheldon, K. Nakajima, J. Bernal, B.W. Howell, T. Curran, E. Soriano, and A. Munoz Thyroid hormone regulates reelin and dab1 expression during brain development J. Neurosci. 19 1999 6979 6993
2. S.A. Anderson, D.D. Eisenstat, L. Shi, and J.L. Rubenstein Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes Science 278 1997 474 476
3. J.B. Angevine, and R.L. Sidman Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse Nature 192 1961 766 768
4. E.S. Anton, M.A. Marchionni, K.F. Lee, and P. Rakic Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex Development 124 1997 3501 3510
5. E.S. Anton, J.A. Kreidberg, and P. Rakic Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex Neuron 22 1999 277 289
6. S.A. Bayer, and J. Altman Neocortical Development 1991 Raven Press New York
7. M. Berry, and A.W. Rogers The migration of neuroblasts in the developing cerebral cortex J. Anat. 99 1965 691 709
8. D.J. Bradley, H.C. Towle, and W.S. Young Spatial and temporal expression of alpha- and beta-thyroid hormone receptor mRNAs, including the beta 2-subtype, in the developing mammalian nervous system J. Neurosci. 12 1992 2288 2302
9. R.S. Cameron, and P. Rakic Glial cell lineage in the cerebral cortex: a review and synthesis Glia 4 1991 124 137
10. D.J. Carlson, K.A. Strait, H.L. Schwartz, and J.H. Oppenheimer Immunofluorescent localization of thyroid hormone receptor isoforms in glial cells of rat brain Endocrinology 135 1994 1831 1836
11. D.J. Carlson, K.A. Strait, H.L. Schwartz, and J.H. Oppenheimer Thyroid hormone receptor isoform content in cultured type 1 and type 2 astrocytes Endocrinology 137 1996 911 917
12. G. D'Arcangelo, G.G. Miao, S.C. Chen, H.D. Soares, J.I. Morgan, and T. Curran A protein related to extracellular matrix proteins deleted in the mouse mutant reeler Nature 374 1995 719 723
13. G. D'Arcangelo, K. Nakajima, T. Miyata, M. Ogawa, K. Mikoshiba, and T. Curran Reelin is a secreted glycoprotein recognized by the cr-50 monoclonal antibody J. Neurosci. 17 1997 23 31
14. J.A. De Carlos, L. Lopez-Mascaraque, and F. Valverde Dynamics of cell migration from the lateral ganglionic eminence in the rat J. Neurosci. 16 1996 6146 6156
15. R.M. Evans The steroid and thyroid hormone receptor superfamily Science 240 1988 889 895
16. E. Forster, A. Tielsch, B. Saum, K.H. Weiss, C. Johanssen, D. Graus-Porta, U. Muller, and M. Frotscher Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus Proc. Natl. Acad. Sci. U. S. A. 99 2002 13178 13183
17. W. Halfter, S. Dong, Y.P. Yip, M. Willem, and U. Mayer A critical function of the pial basement membrane in cortical histogenesis J. Neurosci. 22 2002 6029 6040
18. E. Hartfuss, E. Forster, H.H. Bock, M.A. Hack, P. Leprince, J.M. Luque, J. Herz, M. Frotscher, and M. Gotz Reelin signaling directly affects radial glia morphology and biochemical maturation Development 130 2003 4597 4609
19. S.P. Hicks, and C.J. D'Amato Cell migrations to the isocortex in the rat Anat. Rec. 160 1968 619 634
20. S. Hirotsune, T. Takahara, N. Sasaki, K. Hirose, A. Yoshiki, T. Ohashi, M. Kusakabe, Y. Murakami, M. Muramatsu, and S. Watanabe The reeler gene encodes a protein with an EGF-like motif expressed by pioneer neurons Nat. Genet. 10 1995 77 83
21. S. Hockfield, and R.D. McKay Identification of major cell classes in the developing mammalian nervous system J. Neurosci. 5 1985 3310 3328
22. S. Izumo, and V. Madavi Thyroid hormone receptor alpha isoforms generated by alternative splicing differentially activate myosin HC gen transcription Nature 334 1988 539 542
23. R. Lavado-Autric, E. Auso, J.V. Garcia-Velasco, C. Arufe Mdel, F. Escobar del Rey, P. Berbel, and G. Morreale de Escobar Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny J. Clin. Invest. 111 2003 1073 1082
24. A.A. Lavdas, M. Grigoriou, V. Pachnis, and J.G. Parnavelas The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex J. Neurosci. 19 1999 7881 7888
25. M.A. Lazar, R.A. Hodin, D.S. Darling, and W. Chin Identification of a rat c-erbA alpha-related protein which binds deoxyribonucleic acid but does not bind thyroid hormone Mol. Endocrinol. 2 1988 893 901
26. J.L. Leonard, A.P. Farwell, P.M. Yen, W.W. Chin, and M. Stula Differential expression of thyroid hormone receptor isoforms in neurons and astroglial cells Endocrinology 135 1994 548 555
27. R.A. Lucio, J.V. Garcia, J.R. Cerezo, P. Pacheco, G.M. Innocenti, and P. Berbel The development of auditory callosal connections in normal and hypothyroid rats Cereb. Cortex 7 1997 303 316
28. P. Malatesta, E. Hartfuss, and M. Gotz Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage Development 127 2000 5253 5263
29. O. Marin, and J.L. Rubenstein Cell migration in the forebrain Annu. Rev. Neurosci. 26 2003 441 483
30. M. Marin-Padilla Prenatal development of fibrous (white matter), protoplasmic (gray matter), and layer I astrocytes in the human cerebral cortex: a Golgi study J. Comp. Neurol. 357 1995 554 572
31. J.R. Martínez-Galán, P. Pedraza, M. Santacana, F. Escobar del Rey, G. Morreale de Escobar y, and A. Ruiz-Marcos Early effects of iodine deficiency on radial glial cells of the hippocampus of the rat fetus: a model of neurological cretinism J. Clin. Invest. 99 1997 2701 2709
32. G. Morreale de Escobar, R. Pastor, M.J. Obregón, and F. Escobar del Rey Effects of maternal hypothyroidism on the weight and thyroid hormone content of rat embryonic tissues Endocrinology 117 1985 1890 1896
33. B. Nadarajah, and J.G. Parnavelas Modes of neuronal migration in the developing cerebral cortex Nat. Rev., Neurosci. 3 2002 423 432
34. S.C. Noctor, A.C. Flint, T.A. Weissman, R.S. Dammerman, and A.R. Kriegstein Neurons derived from radial glial cells establish radial units in neocortex Nature 409 2001 714 720
35. M. Ogawa, T. Miyata, K. Nakajima, K. Yagyu, M. Seike, K. Ikenaka, H. Yamamoto, and K. Mikoshiba The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons Neuron 14 1995 899 912
36. S.K. Pixley, and J. de Vellis Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin Brain Res. 317 1984 201 209
37. P. Rakic Mode of cell migration to the superficial layers of fetal monkey neocortex J. Comp. Neurol. 145 1972 61 84
38. J. Sap, A. Munoz, K. Damm, Y. Goldberg, J. Ghysdael, A. Leutz, H. Beug, and B. Vennstrom The c-erb-A protein is a high-affinity receptor for thyroid hormone Nature 1986 635 640
39. C.C. Stichel, C.M. Muller, and K. Zilles Distribution of glial fibrillary acidic protein and vimentin immunoreactivity during rat visual cortex development J. Neurocytol. 20 1991 97 108
40. N. Tamamaki, K.E. Fujimori, and R. Takauji Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone J. Neurosci. 17 1997 8313 8323
41. C.C. Thompson, C. Weinberger, R. Lebo, and R.M. Evans Identification of a novel thyroid hormone receptor expressed in the mammalian central nervous system Science 237 1987 1610 1614
42. C. Weinberger, C.C. Thompson, E.S. Ong, R. Lebo, D.J. Grujold, and R.M Evans The c-erb-A gene encodes a thyroid hormone receptor Nature 324 1986 641 646