Multiple developmental programs are altered by loss of Zic1 and Zic4 to cause Dandy-Walker malformation cerebellar pathogenesis

Development

Volumn 138, Issue 6, 2011, Pages 1207-1216

  Blank, Marissa C ^a   Grinberg, Inessa ^a   Aryee, Emmanuel ^a   Laliberte, Christine ^b   Chizhikov, Victor V ^c   Mark Henkelman, R ^b   Millen, Kathleen J ^c,d  

^a UNIVERSITY OF CHICAGO   (United States)

^b The Mouse Imaging Centre (MICE)   (Canada)

^c SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cerbellum; Dandy Walker malformation; Foliation; Proliferation

Indexed keywords

SONIC HEDGEHOG PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; BRAIN DEVELOPMENT; CELL COMPARTMENTALIZATION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; DANDY WALKER SYNDROME; DISEASE SEVERITY; FEMALE; GENE; GRANULE CELL; MOUSE; NONHUMAN; PATHOGENESIS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; STEM CELL; ZIC1 GENE; ZIC4 GENE;

ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; CEREBELLUM; DANDY-WALKER SYNDROME; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; ORGAN SIZE; PREGNANCY; TRANSCRIPTION FACTORS;

MUS;

EID: 79955126771     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.054114     Document Type: Article

References (47)

1. Alcaraz, W. A., Gold, D. A., Raponi, E., Gent, P. M., Concepcion, D. and Hamilton, B. A. (2006). Zfp423 controls proliferation and differentiation of neural precursors in cerebellar vermis formation. Proc. Natl. Acad. Sci. USA 103, 19424-19429.
2. Aldinger, K. A., Lehmann, O. J., Hudgins, L., Chizhikov, V. V., Bassuk, A. G., Ades, L. C., Krantz, I. D., Dobyns, W. B. and Millen, K. J. (2009). FOXC1 is required for normal cerebellar development and is a major contributor to chromosome 6p25.3 Dandy-Walker malformation. Nat. Genet. 41, 1037-1042.
3. Aruga, J., Yokota, N., Hashimoto, M., Furuichi, T., Fukuda, M. and Mikoshiba, K. (1994). A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J. Neurochem. 63, 1880-1890.
4. Aruga, J., Minowa, O., Yaginuma, H., Kuno, J., Nagai, T., Noda, T. and Mikoshiba, K. (1998). Mouse Zic1 is involved in cerebellar development. J. Neurosci. 18, 284-293.
5. Aruga, J., Inoue, T., Hoshino, J. and Mikoshiba, K. (2002a). Zic2 controls cerebellar development in cooperation with Zic1. J. Neurosci. 22, 218-225.
6. Aruga, J., Tohmonda, T., Homma, S. and Mikoshiba, K. (2002b). Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev. Biol. 244, 329-341.
7. Aruga, J., Ogura, H., Shutoh, F., Ogawa, M., Franke, B., Nagao, S. and Mikoshiba, K. (2004). Locomotor and oculomotor impairment associated with cerebellar dysgenesis in Zic3-deficient (Bent tail) mutant mice. Eur. J. Neurosci. 20, 2159-2167.
8. Barkovich, A. J., Millen, K. J. and Dobyns, W. B. (2009). A developmental and genetic classification of mid-hindbrain malformations. Brain 132, 3199-3230.
9. Behesti, H. and Marino, S. (2009). Cerebellar granule cells: insights into proliferation, differentiation, and role in medulloblastoma pathogenesis. Int. J. Biochem. Cell Biol. 41, 435-445.
10. Blanco, M. J., Pena-Melian, A. and Nieto, M. A. (2002). Expression of EphA receptors and ligands during chick cerebellar development. Mech. Dev. 114, 225-229.
11. Borycki, A., Brown, A. M. and Emerson, C. P. (2000). Shh and Wnt signaling pathways converge to control Gli gene activation in avian somites. Development 127, 20755-20787.
12. Cheng, Y., Sudarov, A., Szulc, K. U., Sgaier, S. K., Stephen, D., Turnbull, D. H. and Joyner, A. L. (2010). The Engrailed homeobox genes determine the different foliation patterns in the vermis and hemispheres of the mammalian cerebellum. Development 137, 519-529.
13. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
14. Chizhikov, V. V. and Millen, K. J. (2004). Control of roof plate development and signaling by Lmx1b in the caudal vertebrate CNS. J. Neurosci. 24, 5694-5703.
15. Chizhikov, V. V., Lindgren, A. G., Currle, D. S., Rose, M. F., Monuki, E. S. and Millen, K. J. (2006). The roof plate regulates cerebellar cell-type specification and proliferation. Development 133, 2793-2804.
16. Corrales, J. D., Blaess, S., Mahoney, E. M. and Joyner, A. L. (2006). The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133, 1811-1821.
17. Dipietrantonio, H. J. and Dymecki, S. M. (2009). Zic1 levels regulate mossy fiber neuron position and axon laterality choice in the ventral brain stem. Neuroscience 162, 560-573.
18. Goldowitz, D. and Hamre, K. (1998). The cells and molecules that make a cerebellum. Trends Neurosci. 21, 375-382.
19. Grinberg, I., Northrup, H., Ardinger, H., Prasad, C., Dobyns, W. B. and Millen, K. J. (2004). Heterozygous deletion of the linked genes ZIC1 and ZIC4 is involved in Dandy-Walker malformation. Nat. Genet. 36, 1053-1055.
20. Hashimoto, M. and Mikoshiba, K. (2003). Mediolateral compartmentalization of the cerebellum is determined on the "birth date" of Purkinje cells. J. Neurosci. 23, 11342-11351.
21. Huang, X., Liu, J., Ketova, T., Fleming, J. T., Grover, V. K., Cooper, M. K., Litingtung, Y. and Chiang, C. (2010). Transventricular delivery of Sonic hedgehog is essential to cerebellar ventricular zone development. Proc. Natl. Acad. Sci. USA 107, 8422-8427.
22. Inoue, T., Ogawa, M., Mikoshiba, K. and Aruga, J. (2008). Zic deficiency in the cortical marginal zone and meninges results in cortical lamination defects resembling those in type II lissencephaly. J. Neurosci. 28, 4712-4725.
23. Ishiguro, A., Inoue, T., Mikoshiba, K. and Aruga, J. (2004). Molecular properties of Zic4 and Zic5 proteins: functional diversity within Zic family. Biochem. Biophys. Res. Commun. 324, 302-307.
24. Jalali, A., Aldinger, K. A., Chary, A., McLone, D. G., Bowman, R. M., Le, L. C., Jardine, P., Newbury-Ecob, R., Mallick, A., Jafari, N. et al. (2008). Linkage to chromosome 2q36.1 in autosomal dominant Dandy-Walker malformation with occipital cephalocele and evidence for genetic heterogeneity. Hum. Genet. 123, 237-245.
25. Karam, S. D., Dottori, M., Ogawa, K., Henderson, J. T., Boyd, A. W., Pasquale, E. B. and Bothwell, M. (2002). EphA4 is not required for Purkinje cell compartmentation. Brain Res. Dev. Brain Res. 135, 29-38.
26. Kimmel, R. A., Turnbull, D. H., Blanquet, V., Wurst, W., Loomis, C. A. and Joyner, A. L. (2000). Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 14, 1377-1389.
27. Koyabu, Y., Nakata, K., Mizugishi, K., Aruga, J. and Mikoshiba, K. (2001). Physical and functional interactions between Zic and Gli proteins. J. Biol. Chem. 276, 6889-6892.
28. Larouche, M. and Hawkes, R. (2006). From clusters to stripes: the developmental origins of adult cerebellar compartmentation. Cerebellum 5, 77-88.
29. Lewis, P. M., Gritli-Linde, A., Smeyne, R., Kottmann, A. and McMahon, A. P. (2004). Sonic hedgehog signaling is required for expansion of granule neuron precursors and patterning of the mouse cerebellum. Dev. Biol. 270, 393-410.
30. Li, J. Y., Lao, Z. and Joyner, A. L. (2002). Changing requirements for Gbx2 in development of the cerebellum and maintenance of the mid/hindbrain organizer. Neuron 36, 31-43.
31. Liebl, D. J., Morris, C. J., Henkemeyer, M. and Parada, L. F. (2003). mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system. J. Neurosci. Res. 71, 7-22.
32. McCormack, W. M., Jr, Shen, J. J., Curry, S. M., Berend, S. A., Kashork, C., Pinar, H., Potocki, L. and Bejjani, B. A. (2002). Partial deletions of the long arm of chromosome 13 associated with holoprosencephaly and the Dandy-Walker malformation. Am. J. Med. Genet. 112, 384-389.
33. Merzdorf, C. S. (2007). Emerging roles for zic genes in early development. Dev. Dyn. 236, 922-940.
34. Millen, K. J., Hui, C. C. and Joyner, A. L. (1995). A role for En-2 and other murine homologues of Drosophila segment polarity genes in regulating positional information in the developing cerebellum. Development 121, 3935-3945.
35. Mizugishi, K., Aruga, J., Nakata, K. and Mikoshiba, K. (2001). Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J. Biol. Chem. 276, 2180-2188.
36. Nagai, T., Aruga, J., Takada, S., Gunther, T., Sporle, R., Schughart, K. and Mikoshiba, K. (1997). The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev. Biol. 182, 299-313.
37. Parisi, M. A. and Dobyns, W. B. (2003). Human malformations of the midbrain and hindbrain: review and proposed classification scheme. Mol. Genet. Metab. 80, 36-53.
38. Parr, B. A., Shea, M. J., Vassileva, G. and McMahon, A. P. (1993). Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247-261.
39. Pogoriler, J., Millen, K. J., Utset, M. and Du, W. (2006). Loss of cyclin D1 impairs cerebellar development and suppresses medulloblastoma formation. Development 133, 3929-3937.
40. Ruiz i Altaba, A., Palma, V. and Dahmane, N. (2002). Hedgehog-Gli signalling and the growth of the brain. Nat. Rev. Neurosci. 3, 24-33.
41. Sarna, J. R., Marzban, H., Watanabe, M. and Hawkes, R. (2006). Complementary stripes of phospholipase Cbeta3 and Cbeta4 expression by Purkinje cell subsets in the mouse cerebellum. J. Comp. Neurol. 496, 303-313.
42. Satokata, I., Ma, L., Ohshima, H., Bei, M., Woo, I., Nishizawa, K., Maeda, T., Takano, Y., Uchiyama, M., Heaney, S. et al. (2000). Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat. Genet. 24, 391-395.
43. Sillitoe, R. V. and Hawkes, R. (2002). Whole-mount immunohistochemistry: a high-throughput screen for patterning defects in the mouse cerebellum. J. Histochem. Cytochem. 50, 235-244.
44. Sillitoe, R. V. and Joyner, A. L. (2007). Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu. Rev. Cell Dev. Biol. 23, 549-577.
45. Sillitoe, R. V., Stephen, D., Lao, Z. and Joyner, A. L. (2008). Engrailed homeobox genes determine the organization of Purkinje cell sagittal stripe gene expression in the adult cerebellum. J. Neurosci. 28, 12150-12162.
46. Spring, S., Lerch, J. P. and Henkelman, R. M. (2007). Sexual dimorphism revealed in the structure of the mouse brain using three-dimensional magnetic resonance imaging. Neuroimage 35, 1424-1433.
47. Vaillant, C. and Monard, D. (2009). SHH pathway and cerebellar development. Cerebellum 8, 291-301.