Transcriptional analysis of Gli3 mutants identifies Wnt target genes in the developing hippocampus

Cerebral Cortex

Volumn 22, Issue 12, 2012, Pages 2878-2893

  Hasenpusch Theil, Kerstin ^a   Magnani, Dario ^a   Amaniti, Eleni Maria ^a   Han, Lin ^a   Armstrong, Douglas ^a   Theil, Thomas ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Dmrt3; Gli3; hippocampus; ing; Wnt signal; Wnt8b

Indexed keywords

BETA CATENIN; LYMPHOID ENHANCER FACTOR 1; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR GLI3; WNT PROTEIN; WNT8B PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA BINDING; EMBRYO; ENHANCER REGION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; HIPPOCAMPUS; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; TELENCEPHALON; UNINDEXED SEQUENCE; WNT SIGNALING PATHWAY;

ANIMALS; HIPPOCAMPUS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NERVE TISSUE PROTEINS; TISSUE DISTRIBUTION; TRANSCRIPTION FACTORS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84863996715     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr365     Document Type: Article

References (72)

1. Alvarez-Medina R, Cayuso J, Okubo T, Takada S, Marti E. 2008. Wnt canonical pathway restricts graded Shh/Gli patterning activity through the regulation of Gli3 expression. Development. 135:237-247.
2. Blaess S, Stephen D, Joyner AL. 2008. Gli3 coordinates threedimensional patterning and growth of the tectum and cerebellum by integrating Shh and Fgf8 signaling. Development. 135:2093-2103.
3. Bottomly D, Kyler SL, McWeeney SK, Yochum GS. 2010. Identification of {beta}-catenin binding regions in colon cancer cells using ChIPSeq. Nucleic Acids Res. 38:5735-5745.
4. Breitling R, Armengaud P, Amtmann A, Herzyk P. 2004. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 573:83-92.
5. Büscher D, Grotewold L, Rüther U. 1998. The Xt-J allele generates a Gli3 fusion transcript. Mamm Genome. 9:676-678.
6. Chaudhry AZ, Lyons GE, Gronostajski RM. 1997. Expression patterns of the four nuclear factor I genes during mouse embryogenesis indicate a potential role in development. Dev Dyn. 208:313-325.
7. Diep DB, Hoen N, Backman M, Machon O, Krauss S. 2004. Characterisation of the Wnt antagonists and their response to conditionally activated Wnt signalling in the developing mouse forebrain. Brain Res Dev Brain Res. 153:261-270.
8. Flenniken AM, Gale NW, Yancopoulos GD, Wilkinson DG. 1996. Distinct and overlapping expression patterns of ligands for Ephrelated receptor tyrosine kinases during mouse embryogenesis. Dev Biol. 179:382-401.
9. Fotaki V, Larralde O, Zeng S, McLaughlin D, Nichols J, Price DJ, Theil T, Mason JO. 2010. Loss of Wnt8b has no overt effect on hippocampus development but leads to altered Wnt gene expression levels in dorsomedial telencephalon. Dev Dyn. 239:284-296.
10. Fotaki V, Price DJ, Mason JO. 2011. Wnt/beta-catenin signaling is disrupted in the extra-toes (Gli3(Xt/Xt) ) mutant from early stages of forebrain development, concomitant with anterior neural plate patterning defects. J Comp Neurol. 519:1640-1657.
11. Fotaki V, Yu T, Zaki PA, Mason JO, Price DJ. 2006. Abnormal positioning of diencephalic cell types in neocortical tissue in the dorsal telencephalon of mice lacking functional Gli3. J Neurosci. 26: 9282-9292.
12. Frantz GD, Bohner AP, Akers RM, McConnell SK. 1994. Regulation of the POU domain gene SCIP during cerebral cortical development. J Neurosci. 14:472-485.
13. Franz T. 1994. Extra-toes (Xt) homozygous mutant mice demonstrate a role for the Gli-3 gene in the development of the forebrain. Acta Anat (Basel). 150:38-44.
14. Fujimura N, Vacik T, Machon O, Vlcek C, Scalabrin S, Speth M, Diep D, Krauss S, Kozmik Z. 2007. Wnt-mediated down-regulation of Sp1 target genes by a transcriptional repressor Sp5. J Biol Chem. 282:1225-1237.
15. Galceran J, Miyashita-Lin EM, Devaney E, Rubenstein JL, Grosschedl R. 2000. Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development. 127:469-482.
16. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR. 2002. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci. 22: 6309-6314.
17. Gronostajski RM. 2000. Roles of the NFI/CTF gene family in transcription and development. Gene. 249:31-45.
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. Harrison SM, Houzelstein D, Dunwoodie SL, Beddington RS. 2000. Sp5, a new member of the Sp1 family, is dynamically expressed during development and genetically interacts with Brachyury. Dev Biol. 227:358-372.
20. Hong CS, Park BY, Saint-Jeannet JP. 2007. The function of Dmrt genes in vertebrate development: it is not just about sex. Dev Biol. 310:1-9.
21. Hui CC, Slusarski D, Platt KA, Holmgren R, Joyner AL. 1994. Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev Biol. 162:402-413.
22. Iulianella A, Sharma M, Durnin M, Vanden Heuvel GB, Trainor PA. 2008. Cux2 (Cutl2) integrates neural progenitor development with cellcycle progression during spinal cord neurogenesis. Development. 135:729-741.
23. Iulianella A, Sharma M, Vanden Heuvel GB, Trainor PA. 2009. Cux2 functions downstream of Notch signaling to regulate dorsal interneuron formation in the spinal cord. Development. 136:2329-2334.
24. Jho E-h, Zhang T, Domon C, Joo C-K, Freund J-N, Costantini F. 2002. Wnt/b-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 22:1172-1183.
25. Jukkola T, Sinjushina N, Partanen J. 2004. Drapc1 expression during mouse embryonic development. Gene Expr Patterns. 4:755-762.
26. Kimura J, Suda Y, Kurokawa D, Hossain ZM, Nakamura M, Takahashi M, Hara A, Aizawa S. 2005. Emx2 and Pax6 function in cooperation with Otx2 and Otx1 to develop caudal forebrain primordium that includes future archipallium. J Neurosci. 25:5097-5108.
27. Kurokawa D, Kiyonari H, Nakayama R, Kimura-Yoshida C, Matsuo I, Aizawa S. 2004. Regulation of Otx2 expression and its functions in mouse forebrain and midbrain. Development. 131:3319-3331.
28. Lee SM, Tole S, Grove E, McMahon AP. 2000. A local Wnt-3a signal is required for development of the mammalian hippocampus. Development. 127:457-467.
29. Leid M, Ishmael JE, Avram D, Shepherd D, Fraulob V, Dolle P. 2004. CTIP1 and CTIP2 are differentially expressed during mouse embryogenesis. Gene Expr Patterns. 4:733-739.
30. Liem KF Jr, 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.
31. Longo KA, Kennell JA, Ochocinska MJ, Ross SE, Wright WS, MacDougald OA. 2002. Wnt signaling protects 3T3-L1 preadipocytes from apoptosis through induction of insulin-like growth factors. J Biol Chem. 277:38239-38244.
32. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U, van de Wetering M, Clevers H, Schlag PM, Birchmeier W, et al. 2002. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol. 22:1184-1193.
33. Machon O, Backman M, Machonova O, Kozmik Z, Vacik T, Andersen L, Krauss S. 2007. A dynamic gradient of Wnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev Biol. 311:223-237.
34. Magnani D, Hasenpusch-Theil K, Jacobs EC, Campagnoni AT, Price DJ, Theil T. 2010. The Gli3 hypomorphic mutation Pdn causes selective impairment in the growth, patterning, and axon guidance capability of the lateral ganglionic eminence. J Neurosci. 30:13883-13894.
35. Mangale VS, Hirokawa KE, Satyaki PR, Gokulchandran N, Chikbire S, Subramanian L, Shetty AS, Martynoga B, Paul J, Mai MV, et al. 2008. Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science. 319:304-309.
36. Mao B, Niehrs C. 2003. Kremen2 modulates Dickkopf2 activity during Wnt/LRP6 signaling. Gene. 302:179-183.
37. Mao B, Wu W, Davidson G, Marhold J, Li M, Mechler BM, Delius H, Hoppe D, Stannek P, Walter C, et al. 2002. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature. 417:664-667.
38. Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, Volpin D, Bressan GM, Piccolo S. 2003. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A. 100:3299-3304.
39. Maynard TM, Jain MD, Balmer CW, LaMantia AS. 2002. High-resolution mapping of the Gli3 mutation extra-toes reveals a 51.5-kb deletion. Mamm Genome. 13:58-61.
40. Muzio L, Soria JM, Pannese M, Piccolo S, Mallamaci A. 2005. A mutually stimulating loop involving emx2 and canonical wnt signalling specifically promotes expansion of occipital cortex and hippocampus. Cereb Cortex. 15:2021-2028.
41. Okada T, Okumura Y, Motoyama J, Ogawa M. 2008. FGF8 signaling patterns the telencephalic midline by regulating putative key factors of midline development. Dev Biol. 320:92-101.
42. Oldekamp J, Kraemer N, Alvarez-Bolado G, Skutella T. 2004. bHLH gene expression in the Emx2-deficient dentate gyrus reveals defective granule cells and absence of migrating precursors. Cereb Cortex. 14:1045-1058.
43. Oliver G, Sosa-Pineda B, Geisendorf S, Spana EP, Doe CQ, Gruss P. 1993. Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech Dev. 44:3-16.
44. Paparidis Z, Abbasi AA, Malik S, Goode DK, Callaway H, Elgar G, deGraaff E, Lopez-Rios J, Zeller R, Grzeschik KH. 2007. Ultraconserved non-coding sequence element controls a subset of spatiotemporal GLI3 expression. Dev Growth Differ. 49:543-553.
45. Parr BA, Shea MJ, Vassileva G, McMahon AP. 1993. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development. 119:247-261.
46. Pellegrini M, Mansouri A, Simeone A, Boncinelli E, Gruss P. 1996. Dentate gyrus formation requires Emx2. Development. 122:3893-3898.
47. Pispa J, Mikkola ML, Mustonen T, Thesleff I. 2003. Ectodysplasin, Edar and TNFRSF19 are expressed in complementary and overlapping patterns during mouse embryogenesis. Gene Expr Patterns. 3:675-679.
48. Qiu W, Hu Y, Andersen TE, Jafari A, Li N, Chen W, Kassem M. 2010. Tumor necrosis factor receptor superfamily member 19 (TNFRSF19) regulates differentiation fate of human mesenchymal (stromal) stem cells through canonical Wnt signaling and C/EBP. J Biol Chem. 285:14438-14449.
49. Quinn JC, Molinek M, Mason JO, Price DJ. 2009. Gli3 is required autonomously for dorsal telencephalic cells to adopt appropriate fates during embryonic forebrain development. Dev Biol. 327:204-215.
50. Quina LA, Wang S, Ng L, Turner EE. 2009. Brn3a and Nurr1 mediate a gene regulatory pathway for habenula development. J Neurosci. 29:14309-14322.
51. Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D. 1999. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol. 215:208-220.
52. Ring DB, Johnson KW, Henriksen EJ, Nuss JM, Goff D, Kinnick TR, Ma ST, Reeder JW, Samuels I, Slabiak T, et al. 2003. Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes. 52:588-595.
53. Shimomura Y, Agalliu D, Vonica A, Luria V, Wajid M, Baumer A, Belli S, Petukhova L, Schinzel A, Brivanlou AH, et al. 2010. APCDD1 is a novel Wnt inhibitor mutated in hereditary hypotrichosis simplex. Nature. 464:1043-1047.
54. Smith CA, Hurley TM, McClive PJ, Sinclair AH. 2002. Restricted expression of DMRT3 in chicken and mouse embryos. Gene Expr Patterns. 2:69-72.
55. Suda Y, Kokura K, Kimura J, Kajikawa E, Inoue F, Aizawa S. 2010. The same enhancer regulates the earliest Emx2 expression in caudal forebrain primordium, subsequent expression in dorsal telencephalon and later expression in the cortical ventricular zone. Development. 137:2939-2949.
56. Summerhurst K, Stark M, Sharpe J, Davidson D, Murphy P. 2008. 3D representation of Wnt and Frizzled gene expression patterns in the mouse embryo at embryonic day 11.5 (Ts19). Gene Expr Patterns. 8:331-348.
57. Tang BL, Zhang T, Low DY, Wong ET, Horstmann H, Hong W. 2000. Mammalian homologues of yeast sec31p. An ubiquitously expressed form is localized to endoplasmic reticulum (ER) exit sites and is essential for ER-Golgi transport. J Biol Chem. 275:13597-13604.
58. Tetsu O, McCormick F. 1999. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 398:422-426.
59. Theil T. 2005. Gli3 is required for the specification and differentiation of preplate neurons. Dev Biol. 286:559-571.
60. Theil T, Alvarez-Bolado G, Walter A, Rüther U. 1999. Gli3 is required for Emx gene expression during dorsal telencephalon development. Development. 126:3561-3571.
61. Theil T, Aydin S, Koch S, Grotewold L, Rüther U. 2002. Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development. 129:3045-3054.
62. Theil T, Frain M, Gilardi-Hebenstreit P, Flenniken A, Charnay P, Wilkinson DG. 1998. Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20. Development. 125:443-452.
63. Tole S, Grove EA. 2001. Detailed field pattern is intrinsic to the embryonic mouse hippocampus early in neurogenesis. J Neurosci. 21:1580-1589.
64. Tole S, Ragsdale CW, Grove EA. 2000. Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes(J). Dev Biol. 217:254-265.
65. Ulloa F, Briscoe J. 2007. Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle. 6:2640-2649.
66. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD, Holt A, Plajzer- Frick I, Afzal V, Rubin EM, Pennacchio LA. 2008. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat Genet. 40:158-160.
67. Williamson I, Hill RE, Bickmore WA. 2011. Enhancers: from developmental genetics to the genetics of common human disease. Dev Cell. 21:17-19.
68. Yee SP, Rigby PW. 1993. The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 7:1277-1289.
69. Yi W, Ross JM, Zarkower D. 2000. Mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior. Development. 127:4469-4480.
70. Yoshida M, Suda Y, Matsuo I, Miyamoto N, Takeda N, Kuratani S, Aizawa S. 1997. Emx1 and Emx2 functions in development of dorsal telencephalon. Development. 124:101-111.
71. Yu X, Riese J, Eresh S, Bienz M. 1998. Transcriptional repression due to high levels of Wingless signalling. EMBO J. 17:7021-7032.
72. Zimmer C, Tiveron MC, Bodmer R, Cremer H. 2004. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex. 14:1408-1420.