Expression patterns and subcellular localization of the Down syndrome candidate protein MNB/DYRK1A suggest a role in late neuronal differentiation

European Journal of Neuroscience

Volumn 17, Issue 11, 2003, Pages 2277-2286

  Hammerle B ^a   Carnicero, A ^a   Elizalde, C ^a   Ceron, J ^a   Martinez S ^a   Tejedor, F J ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

Brain development; Dendrite; Down syndrome; Dyrk1A; Mnb; Neuronal differentiation

Indexed keywords

PROTEIN DYRK1A; PROTEIN KINASE; PROTEIN MNB; UNCLASSIFIED DRUG;

ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICK EMBRYO; CHROMOSOME 21; CONTROLLED STUDY; DENDRITE; DOWN SYNDROME; DROSOPHILA; EMBRYO; ENZYME SUBSTRATE; GENE EXPRESSION; GENE MAPPING; GENE OVEREXPRESSION; GENETIC CONSERVATION; LEARNING; MEMORY; MINIBRAIN GENE; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBIOLOGY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; STEM CELL; STRUCTURAL GENE; VERTEBRATE;

AGING; ANIMALS; BRAIN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL DIFFERENTIATION; CHICK EMBRYO; DOWN SYNDROME; DYNAMIN I; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; PHALLOIDINE; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RNA, MESSENGER; STEM CELLS; TUBULIN; VIMENTIN;

EID: 0038391317     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02665.x     Document Type: Article

References (71)

1. Altafaj, X., Dierssen, M., Baamonde, C., Marti, E., Visa, J., Guimerá, J., Oset, M., Gonzalez, J.R., Florez, J., Fillat, C. & Estivill, X. (2001) Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum. Mol. Genet., 10, 1915-1923.
2. Altman, J. & Bayer, S.A. (1985) Embryonic development of the rat cerebellum. III. Regional differences in the time of origin, migration, and settling of Purkinje cells. J. Comp. Neurol., 231, 42-65.
3. Antonarakis, S.E. (1998) 10 years of genomics, chromosome 21, and Down syndrome. Genomics, 51, 1-16.
4. Antonarakis, S.E. (2001) Chromosome 21: from sequence to applications. Curr. Opin. Genet. Dev., 11, 241-246.
5. Armengol, J.A. & Sotelo, C. (1991) Early dendritic development of Purkinje cells in the rat cerebellum. A light and electron microscopic study using axonal tracing in 'in vitro' slices. Dev. Brain Res., 64, 95-114.
6. Baptista, C.A., Hatten, M.E., Blazeski, R. & Mason, C.A. (1994) Cell-cell interactions influence survival and differentiation of purified Purkinje cells in vitro. Neuron, 12, 243-260.
7. Bastianelli, E. & Pochet, R. (1993) Transient expression of calretinin during development of chick cerebellum. Comparison with calbindin D28k. Neurosci. Res., 17, 53-61.
8. Becker, W. & Joost, H.G. (1999) Structural and functional characteristics of Dyrk, a novel subfamily of protein kinases with dual specificity. Prog. Nucl. Acid Res. Mol. Biol., 62, 1-17.
9. Becker, L., Mito, T., Takashima, S. & Onodera, K. (1991) Growth and development of the brain in Down Syndrome. In The Morphogenesis of Down Syndrome. Wiley-Liss, New York, USA, pp. 133-152.
10. Becker, W., Weber, Y., Wetzel, K., Eirmbter, K., Tejedor, F.J. & Joost, H.G. (1998) Sequence characteristics, subcellular localization, and substrate specificity of DYRK-related kinases, a novel family of dual specificity protein kinases. J. Biol. Chem., 273, 25,893-25,902.
11. Bertossi, M., Roncali, L., Mancini, L., Ribatti, D. & Nico, B. (1986) Process of differentiation of cerebellar Purkinje neurons in the chick embryo. Anat. Embryol. Berl., 175, 25-34.
12. Bignami, A. & Dahl, D. (1974) Astrocyte-specific protein and neuroglial differentiation. An immunofluorescence study with antibodies to the glial fibrillary acidic protein. J. Comp. Neurol., 153, 27-38.
13. Chedotal, A. & Sotelo, C. (1992) Early development of the olivocerebellar projection in the fetal rat using CGRP immunocytochemistry. Eur. J. Neurosci., 4, 1159-1179.
14. Chen, H. & Antonarakis, S.E. (1997) Localisation of a human homologue of the Drosophila mnb and rat Dyrk genes to chromosome 21q22.2. Hum. Genet., 99, 262-265.
15. Chen-Hwang, M.C., Chen, H.R., Elzinga, M. & Hwang, Y.W. (2002) Dynamin is a minibrain kinase/dual specificity Yak1-related kinase 1A substrate. J. Biol. Chem., 277, 17,597-17,604.
16. Cline, H.T. (2001) Dendritic arbor development and synaptogenesis. Curr. Opin. Neurobiol., 11, 118-126.
17. Coyle, J.T., Oster-Granite, M.L. & Gearhart, J.D. (1986) The neurobiologic consequences of Down syndrome. Brain Res. Bull., 16, 773-87.
18. Dahl, D., Rueger, D.C., Bignami, A., Weber, K. & Osborn, M. (1981) Vimentin, the 57 000 molecular weight protein of fibroblast filaments, is the major cytoskeletal component in immature glia. Eur. J. Cell. Biol., 24, 191-196.
19. Delabar, J.M., Theophile, D., Rahmani, Z., Chettouh, Z., Blouin, J.L., Prieur, M., Noel, B. & Sinet, M. (1993) Molecular mapping of twenty-four features of Down syndrome on chromosome 21. Eur. J. Hum. Genet., 1, 114-124.
20. Foelix, R.F. & Oppenheim, R. (1974) The development of synapses in the cerebellar cortex of the chick embryo. J. Neurocytol., 3, 277-294.
21. Fotaki, V., Dierssen, M., Alcantara, S., Martinez, S., Marti, E., Casas, C., Visa, J., Soriano, E., Estivill, X. & Arbones, M.L. (2002) Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice. Mol. Cell Biol., 22, 6636-6647.
22. Griffin, W.S., Stanley, L.C., Ling, C., White, L., MacLeod, V., Perrot, L.J., White, C.L. 3rd & Araoz, C. (1989) Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl Acad. Sci. USA, 86, 7611-7615.
23. Guimerá, J., Casas, C., Estivill, X. & Pritchard, M. (1999) Human minibrain homologue (MNBH/DYRK1): characterization, alternative splicing, differential tissue expression, and overexpression in Down syndrome. Genomics, 57, 407-418.
24. Guimerá, J., Casas, C., Pucharcos, C., Solans, A., Domenech, A., Planas, A.M., Ashley, J., Lovett, M., Estivill, X. & Pritchard, M.A. (1996) A human homologue of Drosophila minibrain (MNB) is expressed in the neuronal regions affected in Down syndrome and maps to the critical region. Hum. Mol. Genet., 5, 1305-1310.
25. Hamburger, V. & Hamilton, H.L. (1951) A series of normal stages in the development of the chick embryo. J. Morph., 88, 49-92.
26. Hämmerle, B. & Tejedor, F.J. (2002) A method for pulse and chase BrdU-labeling of early chick embryos. J. Neurosci. Meth., 122, 59-64.
27. Hämmerle, B., Vera, E., Spreicher, S., Arencibia, R., Martínez, S. & Tejedor, F.J. (2002) Mnb/Dyrk1A is transiently expressed and asymmetrically segregated in neural progenitor cells at the transition to neurogenic divisions. Dev. Biol., 246, 259-273.
28. Hatten, M.E. & Heintz, N. (1995) Mechanisms of neural patterning and specification in the developing cerebellum. Annu. Rev. Neurosci., 18, 385-408.
29. Heisenberg, M., Borst, A., Wagner, S. & Byers, D. (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet., 2, 1-30.
30. Huber, G. & Matus, A. (1984) Differences in the cellular distributions of two microtubule-associated proteins, MAP1 and MAP2, in rat brain. J. Neurosci., 4, 151-160.
31. Jande, S.S., Tolnai, S. & Lawson, D.E. (1981) Immunohistochemical localization of vitamin D-dependent calcium-binding protein in duodenum, kidney, uterus and cerebellum of chickens. Histochemistry, 71, 99-116.
32. Jeffrey, P.L., Meaney, J., Tolhurst, O. & Weinberger, R.P. (1996) Epigenetic factors controlling the development of avian Purkinje neurons. J. Neurosci. Meth., 67, 163-175.
33. Kanemitsu, A. & Kobayashi, Y. (1988) Time of origin of Purkinje cells and neurons of the deep cerebellar nuclei of the chick embryo examined by 3H-thymidine autoradiography. Anat. Anz., 165, 167-175.
34. Kaufmann, W.E. & Moser, H.W. (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex, 10, 981-991.
35. Kim, Y.T. & Wu, C.F. (1987) Reversible blockage of neurite development and growth cone formation in neuronal cultures of a temperature-sensitive mutant of Drosophila. J. Neurosci., 7, 3245-3255.
36. Kola, I. & Hertzog, P.J. (1998) Down syndrome and mouse models. Curr. Opin. Genet. Dev., 8, 316-321.
37. Korenberg, J.R., Chen, X.N., Schipper, R., Sun, Z., Gonsky, R., Gerwehr, S., Carpenter, N., Daumer, C., Dignan, P. & Disteche, C. (1994) Down syndrome phenotypes: the consequences of chromosomal imbalance. Proc. Natl Acad. Sci. USA, 91, 4997-5001.
38. Lee, M.K., Tuttle, J.B., Rebhun, L.I., Cleveland, D.W. & Frankfurter, A. (1990) The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskeleton, 17, 118-132.
39. Mao, J., Maye, P., Kogerman, P., Tejedor, F.J., Toftgard, R., Xie, W., Wu, G. & Wu, D. (2002) Regulation of Glil transcriptional activity in the nucleus by Dyrkl. J. Biol. Chem. 277, 35,156-35,161.
40. Martinez, S. & Alvarado-Mallart, R.M. (1989) Rostral cerebellum originates from the caudal portion of the so-called 'mesencephalic' vesicle: a study using chick/quail chimeras. Eur. J. Neurosci., 1, 549-560.
41. Mason, C.A., Christakos, S. & Catalano, S.M. (1990) Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J. Comp. Neurol., 297, 77-90.
42. McAllister, A.K. (2000) Cellular and molecular mechanisms of dendrite growth. Cereb. Cortex, 10, 963-973.
43. McCormick, M.K., Schinzel, A., Petersen, M.B., Stetten, G., Driscoll, D.J., Cantu, E.S., Tranebjaerg, L., Mikkelsen, M., Watkins, P.C. & Antonarakis, S.E. (1989) Molecular genetic approach to the characterization of the 'Down syndrome region' of chromosome 21. Genomics, 5, 325-331.
44. Miyata, Y. & Nishida, E. (1999) Distantly related cousins of MAP kinase: biochemical properties and possible physiological functions. Biochem. Biophys. Res. Commun., 266, 291-295.
45. Mundigl, O., Ochoa, G.C., David, C., Slepnev, V.I., Kabanov, A. & De Camilli, P. (1998) Amphiphysin I antisense oligonucleotides inhibit neurite outgrowth in cultured hippocampal neurons. J. Neurosci., 18, 93-103.
46. Obata, K. & Fujita, S.C. (1984) Developmental changes of chick cerebellar cortex revealed by monoclonal antibodies. Neurosci. Res., 1, 117-129.
47. Okui, M., Ide, T., Morita, K., Funakoshi, E., Ito, F., Ogita, K., Yoneda, Y., Kudoh, J. & Shimizu, N. (1999) High-level expression of the Mnb/Dyrk1A gene in brain and heart during rat early development. Genomics, 62, 165-171.
48. Palacios-Pru, E.L., Palacios, L. & Mendoza, R.V. (1981) Synaptogenetic mechanisms during chick cerebellar cortex development. J. Submicrosc. Cytol., 13, 145-167.
49. Perez-Villegas, E.M., Olivier, C., Spassky, N., Poncet, C., Cochard, P., Salc, B., Thomas, J.L. & Martinez, S. (1999) Early specification of oligodendrocytes in the chick embryonic brain. Dev. Biol., 216, 98-113.
50. Rahmani, Z., Blouin, J.L., Creau-Goldberg, N., Watkins, P.C., Mattei, J.F., Poissonnier, M., Prieur, M., Chettouh, Z., Nicole, A., Aurias, A., Sinet, P.M. & Delabar, J.M. (1989) Critical role of the D21S55 region on chromosome 21 in the pathogenesis of Down syndrome. Proc. Natl Acad. Sci. USA, 86, 5958-5962.
51. Rahmani, Z., Lopes, C., Rachidi, M. & Delabar, J.M. (1998) Expression of the mnb (dyrk) protein in adult and embryonic mouse tissues. Biochem. Biophys. Res. Commun., 253, 514-518.
52. Rogero, O. & Tejedor, F.J. (1995) Immunochemical characterization and developmental expression of Shaker potassium channels from the nervous system of Drosophila. J. Biol. Chem., 270, 25,746-25,751.
53. Rogers, J.H. (1989) Immunoreactivity for calretinin and other calcium binding protein in the cerebellum. Neurosci., 31, 711-721.
54. Roth, J., Baetens, D., Norman, A.W. & Garcia-Segura, L.M. (1981) Specific neurons in chick central nervous system stain with an antibody against chick vitamin D-dependent calcium-binding protein. Brain Res., 222, 452-457.
55. Schmid, S.L., McNiven, M.A. & De Camilli, P. (1997) Dynamin and its partners: a progress report. Curr. Opin. Cell Biol., 10, 504-512.
56. Sheppard, A.M., Konopka, M. & Jeffrey, P.L. (1988) The developmental appearance of Thy-1 in the avian cerebellum. Dev. Brain Res., 40, 181-192.
57. Shindoh, N., Kudoh, J., Maeda, H., Yamaki, A., Minoshima, S., Shimizu, Y. & Shimizu, N. (1996) Cloning of a human homolog of the Drosophila minibrain/rat Dyrk gene from 'the Down syndrome critical region' of chromosome 21. Biochem. Biophys. Res. Commun., 225, 92-99.
58. Smith, D.J., Stevens, M.E., Sudanagunta, S.P., Bronson, R.T., Makhinson, M., Watabe, A.M., O'Dell, T.J., Fung, J., Weier, H.U., Cheng, J.F. & Rubin, E.M. (1997) Functional screening of 2 Mb of human chromosome 21q22.2 in transgenic mice implicates minibrain in learning defects associated with Down syndrome. Nat. Genet., 16, 8-9.
59. Song, W.J., Sternberg, L.R., Kasten-Sportes, C., Keuren, M.L., Chung, S.H., Slack, A.C., Miller, D.E., Glover, T.W., Chiang, P.W., Lou, L. & Kurnit, D.M. (1996) Isolation of human and murine homologues of the Drosophila minibrain gene: human homologue maps to 21q22.2 in the Down syndrome 'critical region'. Genomics, 38, 331-339.
60. Sotelo, C. (1980) Mutant mice and the formation of cerebellar circuitry. Trends Neurosci., 3, 33-36.
61. Sotelo, C. & Wassef, M. (1991) Cerebellar development: afferent organization and Purkinje cell heterogeneity. Philos. Trans. R. Soc. Lond. B Biol. Sci., 331, 307-313.
62. Spaltmann, F. & Brummendorf, T. (1996) CEPU-1, a novel immunoglobulin superfamily molecule, is expressed by developing cerebellar Purkinje cells. J. Neurosci., 16, 1770-1779.
63. Takei, K., Slepnev, V.I., Haucke, V. & De Camilli, P. (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nature Cell Biol., 1, 33-39.
64. Tejedor, F., Zhu, X.R., Kaltenbach, E., Ackermann, A., Baumann, A., Canal, I., Heisenberg, M., Fischbach, K.F. & Pongs, O. (1995) Minibrain: a new protein kinase family involved in postembryonic neurogenesis in Drosophila. Neuron, 14, 287-301.
65. Torre, E., McNiven, M.A. & Urrutia, R. (1994) Dynamin 1 antisense oligonucleotide treatment prevents neurite formation in cultured hippocampal neurons. J. Biol. Chem., 269, 32,411-32,417.
66. Wassef, M., Zanetta, J.P., Brehier, A. & Sotelo, C. (1985) Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. Dev. Biol., 111, 129-137.
67. Whitford, K.L., Dijkhuizen, P., Polleux, F. & Ghosh, A. (2002) Molecular control of cortical dendrite development. Annu. Rev. Neurosci., 25, 127-149.
68. Wisniewski, K.E. & Schmidt-Sidor, B. (1989) Postnatal delay of myelin formation in brains from Down syndrome infants and children. Clin. Neuropathol., 8, 55-62.
69. Woods Y.L., Rena G., Morrice N., Barthel A., Becker W., Guo S., Unterman T.G. & Cohen P. (2001). The kinase DYRK1A phosphorylates the transcription factor FKHR at Ser329 in vitro, a novel in vivo phosphorylation site. Biochem. J., 355, 597-607.
70. Yamamura, T., Konola, J.T., Wekerle, H. & Lees, M.B. (1991) Monoclonal antibodies against myelin proteolipid protein: identification and characterization of two major determinants. J. Neurochem., 57: 1671-80.
71. Yang, E.J., Ahn, Y.S. & Chung, K.C. (2001) Protein kinase Dyrk1 activates cAMP response element-binding protein during neuronal differentiation in hippocampal progenitor cells. J. Biol. Chem., 276, 39819-39824.