Spatially restricted and developmentally dynamic expression of engrailed genes in multiple cerebellar cell types

Cerebellum

Volumn 10, Issue 3, 2011, Pages 356-372

  Wilson, Sandra L ^a   Kalinovsky, Anna ^a   Orvis, Grant D ^a   Joyner, Alexandra L ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Cerebellum; Compartment; Development; Engrailed; Purkinje cell; Stripe

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; CELL TYPE; CEREBELLUM; CEREBELLUM CELL; CEREBELLUM NUCLEUS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENGRAILED1 GENE; ENGRAILED2 GENE; GENE EXPRESSION; GRANULE CELL; HOMEOBOX; INTERNEURON; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PURKINJE CELL; REGULATORY MECHANISM;

ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BETA-GALACTOSIDASE; CEREBELLUM; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HEAT-SHOCK PROTEINS; HOMEODOMAIN PROTEINS; MICE; MICE, TRANSGENIC; NEOPLASM PROTEINS; NERVE TISSUE PROTEINS; NEURONS; NONLINEAR DYNAMICS; PHOSPHOLIPASE C BETA; RECEPTOR, EPHA4;

EID: 80455177222     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-011-0254-5     Document Type: Article

References (66)

1. Larsell O. The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J Comp Neurol. 1952;97(2):281-356.
2. Ozol K et al. Transverse zones in the vermis of the mouse cerebellum. J Comp Neurol. 1999;412(1):95-111. (Pubitemid 29380327)
3. Sillitoe RV, Joyner AL. Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol. 2007;23:549-77.
4. Joyner AL et al. Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox. Science. 1991;251 (4998):1239-43. (Pubitemid 21926222)
5. Cheng Y et al. The Engrailed homeobox genes determine the different foliation patterns in the vermis and hemispheres of the mammalian cerebellum. Development. 2010;137(3):519-29.
6. Sillitoe RV et al. Engrailed homeobox genes determine the organization of Purkinje cell sagittal stripe gene expression in the adult cerebellum. J Neurosci. 2008;28(47):12150-62.
7. Sillitoe RV, Vogel MW, Joyner AL. Engrailed homeobox genes regulate establishment of the cerebellar afferent circuit map. J Neurosci. 2010;30(30):10015-24.
8. Wurst W, Auerbach AB, Joyner AL. Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development. 1994;120(7):2065-75. (Pubitemid 24209738)
9. Sgaier SK et al. Genetic subdivision of the tectum and cerebellum into functionally related regions based on differential sensitivity to engrailed proteins. Development. 2007;134(12):2325-35. (Pubitemid 47010021)
10. Millen KJ, Hui CC, Joyner AL. A role for En-2 and other murine homologues of Drosophila segment polarity genes in regulating positional information in the developing cerebellum. Development. 1995;121(12):3935-45. (Pubitemid 26007345)
11. Davis CA, Joyner AL. Expression patterns of the homeo boxcontaining genes En-1 and En-2 and the proto-oncogene int-1 diverge during mouse development. Genes Dev. 1988;2(12B):1736-44.
12. Larouche M, Hawkes R. From clusters to stripes: the developmental origins of adult cerebellar compartmentation. Cerebellum. 2006;5(2):77-88. (Pubitemid 44034744)
13. Vandaele S et al. Purkinje cell protein-2 regulatory regions and transgene expression in cerebellar compartments. Genes Dev. 1991;5(7):1136-48. (Pubitemid 21906025)
14. Oberdick J et al. Control of segment-like patterns of gene expression in the mouse cerebellum. Neuron. 1993;10(6):1007-18. (Pubitemid 23194392)
15. Wassef M et al. Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. Dev Biol. 1985;111(1):129-37. (Pubitemid 16246482)
16. Karam SD et al. EphA4 is not required for Purkinje cell compartmentation. Brain Res Dev Brain Res. 2002;135(1-2):29-38. (Pubitemid 34442486)
17. Apps R, Hawkes R. Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci. 2009;10(9):670-81.
18. Ahn AH et al. The cloning of zebrin II reveals its identity with aldolase C. Development. 1994;120(8):2081-90. (Pubitemid 24232276)
19. Brochu G, Maler L, Hawkes R. Zebrin II: a polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J Comp Neurol. 1990;291(4):538-52. (Pubitemid 20047467)
20. Armstrong CL et al. Expression of heat-shock protein Hsp25 in mouse Purkinje cells during development reveals novel features of cerebellar compartmentation. J Comp Neurol. 2001;429(1):7-21.
21. Larouche M, Che PM, Hawkes R. Neurogranin expression identifies a novel array of Purkinje cell parasagittal stripes during mouse cerebellar development. J Comp Neurol. 2006;494(2):215-27. (Pubitemid 41798082)
22. Marzban H et al. Phospholipase Cbeta4 expression reveals the continuity of cerebellar topography through development. J Comp Neurol. 2007;502(5):857-71. (Pubitemid 46732501)
23. Sillitoe RV, Gopal N, Joyner AL. Embryonic origins of ZebrinII parasagittal stripes and establishment of topographic Purkinje cell projections. Neuroscience. 2009;162(3):574-88.
24. Hashimoto M, Mikoshiba K. Mediolateral compartmentalization of the cerebellum is determined on the "birth date" of Purkinje cells. J Neurosci. 2003;23(36):11342-51. (Pubitemid 37549690)
25. Chedotal A, Bloch-Gallego E, Sotelo C. The embryonic cerebellum contains topographic cues that guide developing inferior olivary axons. Development. 1997;124(4):861-70. (Pubitemid 27107434)
26. Chedotal A, Sotelo C. The 'creeper stage' in cerebellar climbing fiber synaptogenesis precedes the 'pericellular nest' - ultrastructural evidence with parvalbumin immunocytochemistry. Brain Res Dev Brain Res. 1993;76(2):207-20. (Pubitemid 24013634)
27. Wassef M et al. Development of the olivocerebellar projection in the rat: II. Matching of the developmental compartmentations of the cerebellum and inferior olive through the projection map. J Comp Neurol. 1992;323(4):537-50.
28. Sudarov A, Joyner AL. Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers. Neural Dev. 2007;2:26.
29. Baader SL et al. Selective disruption of "late onset" sagittal banding patterns by ectopic expression of engrailed-2 in cerebellar Purkinje cells. J Neurosci. 1999;19(13):5370-9. (Pubitemid 29300203)
30. Vogel MW et al. The Engrailed-2 homeobox gene and patterning of spinocerebellar mossy fiber afferents. Brain Res Dev Brain Res. 1996;96(1-2):210-8. (Pubitemid 26348297)
31. Hanks M et al. Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science. 1995;269(5224):679-82.
32. Matei Vet al. Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev Dyn. 2005;234 (3):633-50. (Pubitemid 41532984)
33. Sgaier SK et al. Morphogenetic and cellular movements that shape the mouse cerebellum: insights from genetic fate mapping. Neuron. 2005;45(1):27-40. (Pubitemid 40075347)
34. Kimmel RA et al. Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 2000;14(11):1377-89. (Pubitemid 30397081)
35. Nagy A, Getsenstein M, Vintersten K, Behringer RR. Manipulating the mouse embryo: a laboratory manual. New York: Cold Spring Harbor Laboratory Press; 2003.
36. Davis CA et al. Examining pattern-formation in mouse. Chicken and frog embryos with an en-specific antiserum. Development. 1991;111(2):287-98. (Pubitemid 21920415)
37. Palay SL, Chan-Palay V. Cerebellar cortex: cytology and organization XII. Heidelberg: Springer; 1974. p. 348.
38. Engelkamp D et al. Role of Pax6 in development of the cerebellar system. Development. 1999;126(16):3585-96. (Pubitemid 29419515)
39. Englund C et al. Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci. 2006;26(36):9184-95. (Pubitemid 44359845)
40. Fink AJ et al. Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J Neurosci. 2006;26(11):3066-76.
41. Graham V et al. SOX2 functions to maintain neural progenitor identity. Neuron. 2003;39(5):749-65. (Pubitemid 37088088)
42. Zhao Yet al. LIM-homeodomain proteins Lhx1 and Lhx5, and their cofactor Ldb1, control Purkinje cell differentiation in the developing cerebellum. Proc Natl Acad Sci USA. 2007;104(32):13182-6. (Pubitemid 351737613)
43. Glassmann A et al. Basic molecular fingerprinting of immature cerebellar cortical inhibitory interneurons and their precursors. Neuroscience. 2009;159(1):69-82.
44. Minaki Y et al. Identification of a novel transcriptional corepressor, Corl2, as a cerebellar Purkinje cell-selective marker. Gene Expr Patterns. 2008;8(6):418-23.
45. Nakagawa S, Watanabe M, Inoue Y. Prominent expression of nuclear hormone receptor ROR alpha in Purkinje cells from early development. Neurosci Res. 1997;28(2):177-84. (Pubitemid 27267827)
46. Maricich SM, Herrup K. Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol. 1999;41(2):281-94. (Pubitemid 29494153)
47. Sugitani Y et al. Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. Genes Dev. 2002;16(14):1760-5. (Pubitemid 34803892)
48. Wassef M, Sotelo C. Asynchrony in the expression of guanosine 3':5'-phosphate-dependent protein kinase by clusters of Purkinje cells during the perinatal development of rat cerebellum. Neuroscience. 1984;13(4):1217-41. (Pubitemid 15198967)
49. Smeyne RJ et al. Dynamic organization of developing Purkinje cells revealed by transgene expression. Science. 1991;254(5032):719-21. (Pubitemid 21917396)
50. Karam SD et al. Eph receptors and ephrins in the developing chick cerebellum: relationship to sagittal patterning and granule cell migration. J Neurosci. 2000;20(17):6488-500.
51. Sarna JR et al. Complementary stripes of phospholipase Cbeta3 and Cbeta4 expression by Purkinje cell subsets in the mouse cerebellum. J Comp Neurol. 2006;496(3):303-13.
52. Baader SL et al. Ectopic overexpression of engrailed-2 in cerebellar Purkinje cells causes restricted cell loss and retarded external germinal layer development at lobule junctions. J Neurosci. 1998;18(5):1763-73. (Pubitemid 28103084)
53. Kuemerle B et al. Pattern deformities and cell loss in Engrailed-2 mutant mice suggest two separate patterning events during cerebellar development. J Neurosci. 1997;17(20):7881-9. (Pubitemid 27426225)
54. Lundell MJ et al. The engrailed and huckebein genes are essential for development of serotonin neurons in the Drosophila CNS. Mol Cell Neurosci. 1996;7(1):46-61. (Pubitemid 26088259)
55. Saueressig H, Burrill J, Goulding M. Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development. 1999;126(19):4201-12. (Pubitemid 29509336)
56. Simon HH et al. Fate of midbrain dopaminergic neurons controlled by the engrailed genes. J Neurosci. 2001;21(9):3126-34. (Pubitemid 32323494)
57. Louvi A, Wassef M. Ectopic engrailed 1 expression in the dorsal midline causes cell death, abnormal differentiation of circumventricular organs and errors in axonal pathfinding. Development. 2000;127(18):4061-71.
58. Joly W, Mugat B, Maschat F. Engrailed controls the organization of the ventral nerve cord through frazzled regulation. Dev Biol. 2007;301(2):542-54. (Pubitemid 46073983)
59. Solano PJ et al. Genome-wide identification of in vivo Drosophila Engrailed-binding DNA fragments and related target genes. Development. 2003;130(7):1243-54. (Pubitemid 36410774)
60. Serrano N, Brock HW, Maschat F. beta3-tubulin is directly repressed by the engrailed protein in Drosophila. Development. 1997;124(13):2527-36. (Pubitemid 27341753)
61. Wizenmann A et al. Extracellular Engrailed participates in the topographic guidance of retinal axons in vivo. Neuron. 2009;64 (3):355-66.
62. Brunet I et al. The transcription factor Engrailed-2 guides retinal axons. Nature. 2005;438(7064):94-8. (Pubitemid 41599826)
63. Ashwell KWS, Zhang LL. Ontogeny of afferents to the fetal-rat cerebellum. Acta Anat. 1992;145(1):17-23.
64. Grishkat HL, Eisenman LM. Development of the spinocerebellar projection in the prenatal mouse. J Comp Neurol. 1995;363 (1):93-108.
65. Bourrat F, Sotelo C. Migratory pathways and neuritic differentiation of inferior olivary neurons in the rat embryo - axonal tracing study using the in vitro slab technique. Dev Brain Res. 1988;39(1):19-37. (Pubitemid 18065832)
66. Chedotal A, Sotelo C. Early development of olivocerebellar projections in the fetal rat using CGRP immunocytochemistry. Eur J Neurosci. 1992;4(11):1159-79.