The Engrailed homeobox genes determine the different foliation patterns in the vermis and hemispheres of the mammalian cerebellum

Development

Volumn 137, Issue 3, 2010, Pages 519-529

  Cheng, Yulan ^a,c   Sudarov, Anamaria ^a,d   Szulc, Kamila U ^b   Sgaier, Sema K ^a,e   Stephen, Daniel ^a   Turnbull, Daniel H ^b   Joyner, Alexandra L ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Bracco Research USA   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e BILL AND MELINDA GATES FOUNDATION   (United States)

Author keywords

En; Fgf8; Granule cells; Morphogenesis; Mouse; Sonic hedgehog

Indexed keywords

ENGRAILED 1 HOMEODOMAIN PROTEIN; ENGRAILED 2 HOMEODOMAIN PROTEIN; FIBROBLAST GROWTH FACTOR 8; HOMEODOMAIN PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CEREBELLUM; CEREBELLUM DEVELOPMENT; CEREBELLUM FOLIATION PATTERN; CEREBELLUM HEMISPHERE; CEREBELLUM VERMIS; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; GENE EXPRESSION; GRANULE CELL; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ANIMALS; BODY PATTERNING; CEREBELLAR CORTEX; CEREBELLUM; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; MICE; MUTATION; NERVE TISSUE PROTEINS; TRANSCRIPTION FACTORS;

EPICOCCUM; ERINACEIDAE; MAMMALIA;

EID: 74349097700     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.027045     Document Type: Article

References (47)

1. Altman, J. and Bayer, S. A. (1997). Development of the Cerebellar System in Relation to its Evolution, Structure, and Functions. New York: CRC Press.
2. Bai, C. B., Auerbach, W., Lee, J. S., Stephen, D. and Joyner, A. L. (2002). Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129, 4753-4761.
3. Basson, M. A., Echevarria, D., Ahn, C. P., Sudarov, A., Joyner, A. L., Mason, I. J., Martinez, S. and Martin, G. R. (2008). Specific regions within the embryonic midbrain and cerebellum require different levels of FGF signaling during development. Development 135, 889-898.
4. Bilovocky, N. A., Romito-DiGiacomo, R. R., Murcia, C. L., Maricich, S. M. and Herrup, K. (2003). Factors in the genetic background suppress the engrailed-1 cerebellar phenotype. J. Neurosci. 23, 5105-5112.
5. Broccoli, V, Boncinelli, E. and Wurst, W. (1999). The caudal limit of Otx2 expression positions the isthmic organizer. Nature 401, 164-168.
6. Chi, C. L., Martinez, S., Wurst, W. and Martin, G. R. (2003). The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130, 2633-2644.
7. Ciemerych, M. A., Kenney, A. M., Sicinska, E., Kalaszczynska, I., Bronson, R. T., Rowitch, D. H., Gardner, H. and Sicinski, P. (2002). Development of mice expressing a single D-type cyclin. Genes Dev. 16, 3277-3289.
8. Corrales, J. D., Rocco, G. L., Blaess, S., Guo, Q. and Joyner, A. L. (2004). Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131, 5581-5590.
9. 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.
10. Crossley, P. H. and Martin, G. R. (1995). The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439-451.
11. Davis, C. A., Noble-Topham, S. E., Rossant, J. and Joyner, A. L. (1988). Expression of the homeo box-containing gene En-2 delineates a specific region of the developing mouse brain. Genes Dev. 2, 361-371.
12. Davis, C. A., Holmyard, D. P., Millen, K. J. and Joyner, A. L. (1991). Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum. Development 111, 287-298.
13. Engelkamp, D., Rashbass, P., Seawright, A. and van Heyningen, V. (1999). Role of Pax6 in development of the cerebellar system. Development 126, 3585-3596.
14. Feil, R., Wagner, J., Metzger, D. and Chambon, P. (1997). Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 237, 752-757.
15. Frantz, G. D., Weimann, J. M., Levin, M. E. and McConnell, S. K. (1994). Otx1 and Otx2 define layers and regions in developing cerebral cortex and cerebellum. J. Neurosci. 14, 5725-5740.
16. Goldowitz, D. and Hamre, K. (1998). The cells and molecules that make a cerebellum. Trends Neurosci. 21, 375-382.
17. Guillen, I., Mullor, J. L., Capdevila, J., Sanchez-Herrero, E., Morata, G. and Guerrero, I. (1995). The function of engrailed and the specification of Drosophila wing pattern. Development 121, 3447-3456.
18. Hanks, M., Wurst, W., Anson-Cartwright, L., Auerbach, A. B. and Joyner, A. L. (1995). Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science 269, 679-682.
19. Hidalgo, A. (1994). Three distinct roles for the engrailed gene in Drosophila wing development. Curr. Biol. 4, 1087-1098.
20. Indra, A. K., Warot, X., Brocard, J., Bornert, J. M., Xiao, J. H., Chambon, P. and Metzger, D. (1999). Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res. 27, 4324-4327.
21. Inouye, M. and Oda, S. I. (1980). Strain-specific variations in the folial pattern of the mouse cerebellum. J. Comp. Neurol. 190, 357-362.
22. Johnson, G. A., Cofer, G. P., Fubara, B., Gewalt, S. L., Hedlund, L. W. and Maronpot, R. R. (2002). Magnetic resonance histology for morphologic phenotyping. J. Magn. Reson. Imaging 16, 423-429.
23. Joyner, A. L. and Martin, G. R. (1987). En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene: expression during embryogenesis. Genes Dev. 1, 29-38.
24. Joyner, A. L., Herrup, K., Auerbach, B. A., Davis, C. A. and Rossant, J. (1991). Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox. Science 251, 1239-1243.
25. Larsell, O. (1970). The Comparative Anatomy and Histology of the Cerebellum from Monotremes through Apes (ed. J. Jansen), pp. 31-58. Minneapolis, MN: University of Minnesota Press.
26. 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.
27. 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.
28. Liu, A. and Joyner, A. L. (2001). EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development 128, 181-191.
29. Lauder, J. M., Altman, J. and Krebs, H. (1974). Some mechanisms of cerebellar foliation: effects of early hypo- and hyperthyroidism. Brain Res. 76, 33-40.
30. MacLeod, C. E., Zillesb, K., Schleicherb, A., Rillingd, J. K. and Gibson, K. R. (2003). Expansion of the neocerebellum in Hominoidea. J. Hum. Evol. 44, 401-429.
31. Matise, M. P., Auerbach, W. and Joyner, A. L. (2000). Production of targeted embryonic stem cell clones. In Gene Targeting (ed. B. D. Hames), pp. 101-132. Oxford: Oxford University Press.
32. 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.
33. Purves, D., Augustine, G. J., Fitzpatrick, D., Hall, W. C., LaMantia, A., MaNamara, J. O. and Williams, S. M. (eds) (2004). Neuroscience, 3rd edn. Sunderland: Sinauer Associates.
34. Rodriguez, C. I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A. F. and Dymecki, S. M. (2000). High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25, 139-140.
35. Ross, M. E., Fletcher, C., Mason, C. A., Hatten, M. E. and Heintz, N. (1990). Meander tail reveals a discrete developmental unit in the mouse cerebellum. Proc. Natl. Acad. Sci. USA 87, 4189-4192.
36. Sato, T. and Joyner, A. L. (2009). Duration of Fgf8 isthmic organizer expression is key to patterning different tectal-isthmo-cerebellum structures. Development 136, 3617-3626.
37. Sgaier, S. K., Millet, S., Villanueva, M. P., Berenshteyn, F., Song, C. and Joyner, A. L. (2005). Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 45, 27-40.
38. Sgaier, S. K., Lao, Z., Villanueva, M. P., Berenshteyn, F., Stephen, D., Turnbull, R. K. and Joyner, A. L. (2007). Genetic subdivision of the tectum and cerebellum into functionally related regions based on differential sensitivity to engrailed proteins. Development 134, 2325-2335.
39. Shirasawa, S., Arata, A., Onimaru, H., Roth, K. A., Brown, G. A., Horning, S., Arata, S., Okumura, K., Sasazuki, T. and Korsmeyer, S. J. (2000). Rnx deficiency results in congenital central hypoventilation. Nat. Genet. 24, 287-290.
40. 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.
41. 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.
42. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
43. Sudarov, A. and Joyner, A. L. (2007). Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers. Neural Develop. 2, 26.
44. Thomas, K. R., Musci, T. S., Neumann, P. E. and Capecchi, M. R. (1991). Swaying is a mutant allele of the proto-oncogene Wnt-1. Cell 67, 969-976.
45. Wurst, W., Auerbach, A. B. and Joyner, A. L. (1994). Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120, 2065-2075.
46. Xu, J., Liu, Z. and Ornitz, D. M. (2000). Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 127, 1833-1843.
47. Zambrowicz, B. P., Imamoto, A., Fiering, S., Herzenberg, L. A., Kerr, W. G. and Soriano, P. (1997). Disruption of overlapping transcripts in the ROSA beta geo 26 gene trap strain leads to widespread expression of beta-galactosidase in mouse embryos and hematopoietic cells. Proc. Natl. Acad. Sci. USA 94, 3789-3794.