Central roles of the roof plate in telencephalic development and holoprosencephaly

Journal of Neuroscience

Volumn 26, Issue 29, 2006, Pages 7640-7649

  Cheng, Xun ^a   Hsu, Ching Mei ^a   Currle, D Spencer ^a,b   Jia, Sheng Hu ^a,b   Barkovich, A James ^c   Monuki, Edwin S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cerebral cortex; Choroid plexus; Cortical hem; Lhx5; Middle interhemispheric variant; Neural stem cell; Neuropathology; Transgenic mice; Zic2

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL LOSS; CELL MUTANT; CONTROLLED STUDY; DISSOCIATION; EXPLANT; GENE CONTROL; GENE EXPRESSION; HOLOPROSENCEPHALY; HUMAN; MORPHOLOGY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TELENCEPHALON; ANIMAL; DRUG EFFECT; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; MOUSE STRAIN; NERVOUS SYSTEM; NEURAL TUBE DEFECT; PRENATAL DEVELOPMENT; UPREGULATION;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; CEREBRAL CORTEX; EMBRYO; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOLOPROSENCEPHALY; HUMANS; MICE; MICE, INBRED STRAINS; NERVOUS SYSTEM; NEURAL TUBE DEFECTS; PHENOTYPE; TELENCEPHALON; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 33747053414     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0714-06.2006     Document Type: Article

References (48)

1. Anderson RM, Lawrence AR, Stottmann RW, Bachiller D, Klingensmith J (2002) Chordin and noggin promote organizing centers of forebrain development in the mouse. Development 129:4975-4987.
2. Ashe HL, Briscoe J (2006) The interpretation of morphogen gradients. Development 133:385-394.
3. Bachiller D, Klingensmith J, Kemp C, Belo JA, Anderson RM, May SR, McMahon JA, McMahon AP, Harland RM, Rossant J, De Robertis EM (2000) The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 403:658-661.
4. Barkovich AJ, Quint DJ (1993) Middle interhemispheric fusion: an unusual variant of holoprosencephaly. Am J Neuroradiol 14:431-440.
5. Bishop KM, Goudreau G, O'Leary DD (2000) Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 288:344-349.
6. Bourillot PY, Garrett N, Gurdon JB (2002) A changing morphogen gradient is interpreted by continuous transduction flow. Development 129:2167-2180.
7. Brown LY, Odent S, David V, Blayau M, Dubourg C, Apacik C, Delgado MA, Hall BD, Reynolds JF, Sommer A, Wieczorek D, Brown SA, Muenke M (2001) Holoprosencephaly due to mutations in ZIC2: alanine tract expansion mutations may be caused by parental somatic recombination. Hum Mol Genet 10:791-796.
8. Burrows RC, Wancio D, Levitt P, Lillien L (1997) Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19:251-267.
9. Chizhikov VV, Lindgren AG, Currle DS, Rose MF, Monuki ES, Millen KJ (2006) The roof plate regulates cerebellar cell-type specification and proliferation. Development, in press.
10. Currle DS, Cheng X, Hsu CM, Monuki ES (2005) Direct and indirect roles of CNS dorsal midline cells in choroid plexus epithelia formation. Development 132:3549-3559.
11. Feng XH, Derynck R (2005) Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 21:659-693.
12. Flanagan LA, Rebaza LM, Derzic S, Schwartz PH, Monuki ES (2006) Regulation of human neural precursor cells by laminin and integrins. J Neurosci Res 83:845-856.
13. Fukuchi-Shimogori T, Grove EA (2003) Emx2 patterns the neocortex by regulating FGF positional signaling. Nat Neurosci 6:825-831.
14. Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203-2212.
15. Gibson MC, Perrimon N (2005) Extrusion and death of DPP/BMP-compromised epithelial cells in the developing Drosophila wing. Science 307:1785-1789.
16. Golden JA, Bracilovic A, McFadden KA, Beesley JS, Rubenstein JL, Grinspan JB (1999) Ectopic bone morphogenetic proteins 5 and 4 in the chicken forebrain lead to cyclopia and holoprosencephaly. Proc Natl Acad Sci USA 96:2439-2444.
17. Gripp KW, Wotton D, Edwards MC, Roessler E, Ades L, Meinecke P, Richieri-Costa A, Zackai EH, Massague J, Muenke M, Elledge SJ (2000) Mutations in TGIF cause holoprosencephaly and link NODAL signalling to human neural axis determination. Nat Genet 25:205-208.
18. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW (1998) The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125:2315-2325.
19. Hamasaki T, Leingartner A, Ringstedt T, O'Leary DD (2004) EMX2 regulates sizes and positioning of the primary sensory and motor areas in neocortex by direct specification of cortical progenitors. Neuron 43:359-372.
20. Hayhurst M, McConnell SK (2003) Mouse models of holoprosencephaly. Curr Opin Neurol 16:135-141.
21. Hebert JM, Mishina Y, McConnell SK (2002) BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron 35:1029-1041.
22. Hebert JM, Hayhurst M, Marks ME, Kulessa H, Hogan BL, McConnell SK (2003) BMP ligands act redundantly to pattern the dorsal telencephalic midline. Genesis 35:214-219.
23. Lee KJ, Jessell TM (1999) The specification of dorsal cell fates in the vertebrate central nervous system. Annu Rev Neurosci 22:261-294.
24. Lee KJ, Dietrich P, Jessell TM (2000a) Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403:734-740.
25. Lee SM, Tole S, Grove E, McMahon AP (2000b) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127:457-467.
26. Li W, Cogswell CA, LoTurco JJ (1998) Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J Neurosci 18:8853-8862.
27. Liem Jr KF, Tremml G, Jessell TM (1997) A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91:127-138.
28. Mallamaci A, Muzio L, Chan CH, Parnavelas J, Boncinelli E (2000) Area identity shifts in the early cerebral cortex of Emx2-/- mutant mice. Nat Neurosci 3:679-686.
29. Marcorelles P, Loget P, Fallet-Bianco C, Roume J, Encha-Razavi F, Delezoide AL (2002) Unusual variant of holoprosencephaly in monosomy 13q. Pediatr Dev Pathol 5:170-178.
30. Millonig JH, Millen KJ, Hatten ME (2000) The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature 403:764-769.
31. Ming JE, Golden JA (2004) Midline patterning defects. In: Developmental neuropathology (Golden JA, Harding B, eds), p 386. Basel: International Society for Neuropathology.
32. Monuki ES, Walsh CA (2001) Mechanisms of cerebral cortical patterning in mice and humans. Nat Neurosci [Suppl] 4:1199-1206.
33. Monuki ES, Porter FD, Walsh CA (2001) Patterning of the dorsal telencephalon and cerebral cortex by a roof plate-Lhx2 pathway. Neuron 32:591-604.
34. Muenke M, Beachy PA (2000) Genetics of ventral forebrain development and holoprosencephaly. Curr Opin Genet Dev 10:262-269.
35. Nagai T, Aruga J, Takada S, Gunther T, Sporle R, Schughart K, 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.
36. Nagai T, Aruga J, Minowa O, Sugimoto T, Ohno Y, Noda T, Mikoshiba K (2000) Zic2 regulates the kinetics of neurulation. Proc Natl Acad Sci USA 97:1618-1623.
37. Norman MG (1995) Congenital malformations of the brain: pathologic, embryologic, clinical, radiologic, and genetic aspects. New York: Oxford UP.
38. Ohkubo Y, Chiang C, Rubenstein JL (2002) Coordinate regulation and synergistic actions of BMP4, SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111:1-17.
39. Porter FD, Drago J, Xu Y, Cheema SS, Wassif C, Huang SP, Lee E, Grinberg A, Massalas JS, Bodine D, Alt F, Westphal H (1997) Lhx2, a LIM homeobox gene, is required for eye, forebrain, and definitive erythrocyte development. Development 124:2935-2944.
40. Qian X, Goderie SK, Shen Q, Stern JH, Temple S (1998) Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125:3143-3152.
41. Shen J, Dahmann C (2005) Extrusion of cells with inappropriate Dpp signaling from Drosophila wing disc epithelia. Science 307:1789-1790.
42. Shen J, Walsh CA (2005) Targeted disruption of Tgif, the mouse ortholog of a human holoprosencephaly gene, does not result in holoprosencephaly in mice. Mol Cell Biol 25:3639-3647.
43. Simon EM, Hevner RF, Pinter JD, Clegg NJ, Delgado M, Kinsman SL, Hahn JS, Barkovich AJ (2002) The middle interhemispheric variant of holoprosencephaly. Am J Neuroradiol 23:151-156.
44. Solloway MJ, Robertson EJ (1999) Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 126:1753-1768.
45. Takahashi T, Kinsman S, Makris N, Grant E, Haselgrove C, McInerney S, Kennedy DN, Fredrickson K, Mori S, Caviness VS (2003) Semilobar holoprosencephaly with midline "seam": a topologic and morphogenetic model based upon MRI analysis. Cereb Cortex 13:1299-1312.
46. Tole S, Goudreau G, Assimacopoulos S, Grove EA (2000) Emx2 is required for growth of the hippocampus but not for hippocampal field specification. J Neurosci 20:2618-2625.
47. Zhao GQ (2003) Consequences of knocking out BMP signaling in the mouse. Genesis 35:43-56.
48. Zhao Y, Sheng HZ, Amini R, Grinberg A, Lee E, Huang S, Taira M, Westphal H (1999) Control of hippocampal morphogenesis and neuronal differentiation by the LIM homeobox gene Lhx5. Science 284:1155-1158.