The doublesex homolog Dmrt5 is required for the development of the caudomedial cerebral cortex in mammals

Cerebral Cortex

Volumn 23, Issue 11, 2013, Pages 2552-2567

  Saulnier, Amandine ^a   Keruzore, Marc ^a   De Clercq, Sarah ^a   Bar, Isabelle ^a   Moers, Virginie ^a   Magnani, Dario ^b   Walcher, Tessa ^c   Filippis, Carol ^d   Kricha, Sadia ^a   Parlier, Damien ^a   Viviani, Laurène ^a   Matson, Clinton K ^e   Nakagawa, Yasushi ^f   Theil, Thomas ^b   Götz, Magdalena ^c   Mallamaci, Antonello ^d   Marine, Jean Christophe ^g   Zarkower, David ^e   Bellefroid, Eric J ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d SISSA   (Italy)

^e Department of Genetics Cell Biology and Development   (Italy)

^f UNIVERSITY OF MINNESOTA   (United States)

^g UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

choroid plexus; cortical hem; Emx2; telencephalon; Wnt Bmp

Indexed keywords

DOUBLESEX AND MAB 3 RELATED TRANSCRIPTION FACTOR 5; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN MALFORMATION; CHOROID PLEXUS; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; GENE DELETION; GENE EXPRESSION; HIPPOCAMPUS; MAMMAL; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; THALAMOCORTICAL TRACT;

CHOROID PLEXUS; CORTICAL HEM; EMX2; TELENCEPHALON; WNT/BMP;

ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS; CEREBRAL CORTEX; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 84880772628     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs234     Document Type: Article

References (83)

1. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: Its role in the development of connections between thalamus and cortex. Annu Rev Neurosci. 17:185-218. (Pubitemid 24117029)
2. Aoto K, Nishimura T, Eto K, Motoyama J. 2002. Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev Biol. 251:320-332. (Pubitemid 35373752)
3. Armentano M, Chou SJ, Tomassy GS, Leingärtner A, O'Leary DD, Studer M. 2007. COUP-TF1 regulates the balance of cortical patterning between frontal/motor and sensory areas. Nat Neurosci. 10:1277-1286. (Pubitemid 47480291)
4. Balciuniene J, Bardwell VJ, Zarkower D. 2006. Mice mutant in the DM domain gene Dmrt4 are viable and fertile but have polyovular follicles. Mol Cell Biol. 26:8984-8991. (Pubitemid 44851955)
5. Bedogni F, Hodge RD, Elsen GE, Nelson BR, Daza RA, Beyer RP, Bammler TK, Rubenstein JL, Hevner RF. 2010. Tbr1 regulates regional and laminar identity of postmitotic neurons in developing neocortex. Proc Natl Acad Sci USA. 107:13129-13134.
6. Benadiba C, Magnani D, Niquille M, Morlé L, Valloton D, Nawabi H, Ait-Lounis A, Otsmane B, Reith W, Theil T et al. 2012. The ciliogenic transcription factor RFX3 regulates early midline distribution of guidepost neurons required for corpus callosum development. PLoS Genet. 8:e1002606.
7. Bielle F, Griveau A, Narboux-Nême N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A. 2005. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci. 8:1002-1012. (Pubitemid 41061510)
8. Bishop KM, Garel S, Nakagawa Y, Rubenstein JL, O'Leary DD. 2003. Emx1 and Emx2 cooperate to regulate cortical size, lamination, neuronal differentiation, development of cortical efferents, and thalamocortical pathfinding. J Comp Neurol. 457:345-360. (Pubitemid 36255332)
9. Bishop KM, Goudreau G, O'Leary DD. 2000. Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science. 288:344-349. (Pubitemid 30226197)
10. Bishop KM, Rubenstein JL, O'Leary DD. 2002. Distinct actions of Emx1, Emx2, and Pax6 in regulating the specification of areas in the developing neocortex. J Neurosci. 22:7627-7638. (Pubitemid 35386363)
11. Bluske KK, Kawakami Y, Koyano-Nakagawa N, Nakagawa Y. 2009. Differential activity of Wnt/b-catenin signaling in the embryonic mouse thalamus. Dev Dyn. 238:3297-3309.
12. Borello U, Pierani A. 2010. Patterning the cerebral cortex: Traveling with morphogens. Curr Opin Genet Dev. 20:408-415.
13. Bulchand S, Grove EA, Porter FD, Tole S. 2001. LIM-homeodomain gene Lhx2 regulates the formation of the cortical hem. Mech Dev. 100:165-175. (Pubitemid 32109327)
14. Causeret F, Ensini M, Teissier A, Kessaris N, Richardson WD, de Couville T Lucas, Pierani A. 2011. Dbx1-expressing cells are necessary for the survival of the mammalian anterior neural and craniofacial structures. PloS One. 6:e19367.
15. Cheng X, Hsu CM, Currle DS, Hu JS, Barkovich AJ, Monuki ES. 2006. Central roles of the roof plate in telencephalic development and holoprosencephaly. J Neurosci. 26:7640-7649. (Pubitemid 44315183)
16. Cholfin JA, Rubenstein JL. 2008. Frontal cortex subdivision patterning is coordinately regulated by Fgf8, Fgf17 and Emx2. J Comp Neurol. 509:144-155. (Pubitemid 351960779)
17. Chou SJ, Perez-Garcia CG, Kroll TT, O'Leary DD. 2009. Lhx2 specifies regional fate in Emx1 lineage of telencephalic progenitors generating cerebral cortex. Nat Neurosci. 12:1381-1389.
18. 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. (Pubitemid 41246128)
19. Fernandes M, Gutin G, Alcorn H, McConnell S, Hébert JM. 2007. Mutations in the BMP pathway in mice support the existence of two molecular classes of holoprosencephaly. Development. 134:3789-3794. (Pubitemid 350187338)
20. Fotaki V, Price DJ, Mason JO. 2011. Wnt/?-catenin is disrupted in the extra-toes (Gli3xt/xt) mutant from early stages of forebrain development, concomitant with anterior neural plate patterning defects. J Comp Neurol. 519:1640-1657.
21. 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. (Pubitemid 44359854)
22. Friedrichs M, Larralde O, Skutella T, Theil T. 2008. Lamination of the cerebral cortex is disturbed in Gli3 mutant mice. Dev Biol. 318:203-214.
23. Fukuchi-Shimogori T, Grove EA. 2003. Emx2 patterns the neocortex by regulating FGF positional signaling. Nat Neurosci. 6:825-831. (Pubitemid 36929703)
24. Furuta Y, Piston DW, Hogan LM. 1997. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development. 124:2203-2212. (Pubitemid 27283241)
25. Gennet N, Gale E, Nan X, Farley E, Takacs K, Oberwallner B, Chambers D, Li M. 2011. Doublesex and Mab-3-related transcription factor 5 promotes midbrain dopaminergic identity in pluripotent stem cells by enforcing a ventral-medial progenitor fate. Proc Natl Acad Sci USA. 108:9131-9136.
26. 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. (Pubitemid 28336391)
27. Hamasaki T, Leingärtner A, Ringstedt T, O'Leary DD. 2004. EMX2 regulates sizes and positioning of the primary and motor areas in neocortex by direct specification of cortical progenitors. Neuron. 43:359-372. (Pubitemid 39061128)
28. Hasenpusch-Theil K, Magnani D, Amaniti EM, Han L, Amstrong D, Theil T. 2012. Transcriptional analysis of Gli3 mutants identifies Wnt target genes in the developing hippocampus. Cereb Cortex. (Epub ahead of print).
29. Hauptmann G, Gerster T. 1994. Two-color whole-mount in situ hybridization to vertebrate and drosolphilia embryos. Trends Genet. 10:266. (Pubitemid 24238896)
30. Hébert JM, Fishell G. 2008. The genetics of early telencephalon patterning: Some assembly required. Nat Rev Neurosci. 9:678-685.
31. Heins N, Cremisi F, Malatesta P, Gangemi RM, Corte G, Price J, Goudreau G, Gruss P, Gotz M. 2001. Emx2 promotes symmetrical cell divisions and a multipotential fate in precursors from the cerebral cortex. Mol Cell Neurosci. 18:485-502. (Pubitemid 34008389)
32. 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.
33. Imayoshi I, Shimogori T, Ohtsuka T, Kageyama R. 2008. Hes genes and neurogenin regulate non-neural versus neural fate specification in the dorsal telencephalic midline. Development. 135:2531-2541.
34. Ivaniutsin U, Chen Y, Mason JO, Price DJ, Pratt T. 2009. Adenomatous polyposis coli is required for early events in the normal growth and differentiation of the developing cerebral cortex. Neural Dev. 4:3.
35. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. 2002. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 22:1172-1183. (Pubitemid 34094853)
36. Kanold PO, Luhmann HJ. 2010. The subplate and early cortical circuits. Annu Rev Neurosci. 33:23-48.
37. Kimura K, Hachiya T, Koganezawa M, Tazawa T, Yamamoto D. 2008. Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron. 59:759-769.
38. Kuschel S, Rüther U, Theil T. 2003. A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of Gli3 mutant telencephalon. Dev Biol. 260:484-495. (Pubitemid 36960093)
39. Lee SM, Tole S, Grove S, McMahon A. 2000. A local Wnt-3a signal is required for development of the mammalian hippocampus. Development. 127:457-467. (Pubitemid 30093394)
40. Lindwall C, Fothergill T, Richards LJ. 2007. Commissure formation in the mammalian forebrain. Curr Opin Neurobiol. 17:3-14. (Pubitemid 46227983)
41. 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. (Pubitemid 47588241)
42. 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.
43. Mallamaci A. 2011. Molecular bases of cortico-cerebral regionalization. Prog Brain Res. 189:37-64.
44. Mallamaci A, Mercurio S, Muzio L, Cecchi C, Pardini CL, Gruss P, Boncinelli E. 2000. The lack of Emx2 causes impairment of Reelin signaling and defects of neuronal migration in the developing cerebral cortex. J Neurosci. 20:1109-1118. (Pubitemid 30220468)
45. Mangale VS, Hirokawa KE, Satyaki PR, Gokulchandran N, Chikbire S, Subranian L, Shetty A, Martynoga B, Paul J, Mai MV et al. 2008. Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science. 319:304-309.
46. Manuel M, Georgala PA, Carr CB, Chanas S, Kleinjan DA, Martynoga B, Mason JO, Molinek M, Pinson J, Pratt T et al. 2007. Controlled overexpression of Pax6 in vivo negatively autoregulates the Pax6 locus, causing cell-autonomous defects of late cortical progenitor proliferation with little effects on cortical arealization. Development. 134:545-555. (Pubitemid 46332491)
47. Martoriati A, Doumont G, Alcalay M, Bellefroid E, Pelicci PG, Marine JC. 2005. dapk1, encoding an activator of a p19ARF-p53-mediated apoptotic checkpoint, is a transcription target of p53. Oncogene. 24:1461-1466. (Pubitemid 40343126)
48. Matson CK, Murphy MW, Griswold MD, Yoshida S, Bardwell VJ, Zarkower D. 2010. The mammalian doublesex homolog DMRT1 is a transcriptional gatekeeper that controls the mitosis versus meiosis decision in male germ cells. Dev Cell. 19:612-624.
49. Miquelajauregui A, Vareal-Echavarria A, Ceci ML, Garcia F, Ricano I, Hoang K, Frade-Perez D, Portera-Cailliau C, Tamariz E, De Carlos JA et al. 2010. LIM-homeobox gene Lhx5 is required for normal development of Cajal-Retzius cells. J Neurosci. 30: 10551-10562.
50. 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. (Pubitemid 33145194)
51. Muzio L, DiBenedetto B, Stoykova A, Boncinelli E, Gruss P, Mallamaci A. 2002. Emx2 and Pax6 control regionalization of the preneurogenic cortical primordium. Cereb Cortex. 12:129-139. (Pubitemid 34052969)
52. Muzio L, Mallamaci A. 2005. FoxG1 confines Cajal-Retzius neurogenesis and hippocampal morphogenesis to the dorsomedial pallium. J Neurosci. 25:4435-4441. (Pubitemid 40628787)
53. 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. (Pubitemid 41628340)
54. Naruse I, Kato K, Asano T, Suzuki F, Kameyama Y. 1990. Developmental brain abnormalities accompanied with the retarded production of S-100 beta protein in genetic polydactyly mice. Brain Res Dev Brain Res. 51:253-258. (Pubitemid 20056165)
55. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaba K, Yamamoto H, Mikoshiba K. 1995. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron. 14:899-912.
56. O'Leary DD, Sahara S. 2008. Genetic regulation of arealization of the neocortex. Curr Opin Neurobiol. 18:90-100.
57. Piper M, Moldrich RX, Lindwall C, Little E, Barry G, Mason S, Sunn N, Kurniawan ND, Gronostajski RM, Richards LJ. 2009. Multiple non-cell-autonomous defects underlie neocortical callosal dysgenesis in Nfib-deficient mice. Neural Dev. 4:43.
58. Rakic P. 2009. Evolution of the neocortex: A perspective from developmental biology. Nat Rev Neurosci. 10:724-735.
59. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D. 1998. Evidence for evolutionary conservation of sexdertermining genes. Nature. 391:691-695. (Pubitemid 28113214)
60. Ross JM, Kalis AK, Murphy MW, Zarkower D. 2005. The DM domain protein MAB-3 promotes sex-specific neurogenesis in C. elegans by regulating bHLH proteins. Dev Cell. 8:881-892. (Pubitemid 40754059)
61. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 132:365-386.
62. Sahara S, Kawakami Y, Izpisua Belmonte JC, O'Leary DD. 2007. Sp8 exhibits reciprocal induction with Fgf8 but has an opposing effect on anterior-posterior cortical area patterning. Neural Dev. 2:10.
63. Sánchez-Camacho C, Ortega JA, Ocaña I, Alcántara S, Bovolenta P. 2011. Appropriate Bmp7 levels are required for the differentiation of midline guidepost cells involved in corpus callosum formation. Dev Neurobiol. 71:337-350.
64. Scardigli R, Baumer N, Gruss P, Guillemot F, Le Roux I. 2003. Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6. Development. 130:3269-3281. (Pubitemid 36926963)
65. Schuurmans C, Armant O, Nieto M, Stenman JM, Britz O, Klenin N, Brown C, Langevin LM, Seibt J, Tang H et al. 2004. Sequential phases of cortical specification involve Neurogenin-dependent and-independent pathways. EMBO J. 23:2892-2902. (Pubitemid 39013561)
66. Shinozaki K, Miyagi T, Yoshida M, Miyata T, Ogawa M, Aizawa S, Suda Y. 2002. Absence of Cajal-Retzius cells and subplate neurons associated with defects of tangential migration from ganglionic eminence in Emx1/2 double mutant cerebral cortex. Development. 129:3479-3492.
67. Shinozaki K, Yoshida M, Nakamura M, Aizawa S, Suda Y. 2004. Emx1 and Emx2 cooperate in initial phase of archipallium development. Mech Dev. 121:475-489. (Pubitemid 38624542)
68. Smith CA, Hurley TM, McClive PJ, Sinclair AH. 2002. Restricted expression of DMRT3 in chicken and mouse embryos. Mech Dev. 119(Suppl 1):S73-S76. (Pubitemid 39658688)
69. Spandidos A, Wang X, Wang H, Seed B. 2010. PrimerBank: A resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res. 38: D792-D799.
70. 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.
71. 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. (Pubitemid 29419513)
72. 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. (Pubitemid 34874280)
73. 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. (Pubitemid 30220349)
74. Tresser J, Chiba S, Veeman M, El-Nachef D, Newman-Smith E, Horie T, Tsuda M, Smith WC. 2010. Doublesex/mab3 related-1 (dmrt1) is essential for development of anterior neural plate derivatives in Ciona. Development. 137:2197-2203.
75. Wang Y, Zhang J, Mori S, Nathans J. 2006. Axonal growth and guidance defects in Frizzled3 knock-out mice: A comparison of diffusion tensor magnetic resonance imaging, neurofilament staining, and genetically directed cell labeling. J Neurosci. 26:355-364. (Pubitemid 43237097)
76. Wilkinson DG, Nieto MA. 1993. Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 225:361-373.
77. Xie Z, Ma X, Ji W, Zhou G, Lu Y, Xiang Z, Wang YX, Zhang L, Hu Y, Ding YQ et al. 2010. Zbtb20 is essential for the specification of CA1 field identity in the developing hippocampus. Proc Natl Acad Sci USA. 107:6510-6515.
78. Yoshida M, Assimacopoulos S, Jones K, Grove E. 2006. Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development. 133:537-545. (Pubitemid 43273839)
79. 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. (Pubitemid 27053010)
80. Yoshizawa A, Nakahara Y, Izawa T, Ishitani T, Tsutsumi M, Kuroiwa A, Itoh M, Kikuchi Y. 2011. Zebrafish Dmrta2 regulates neurogenesis in the telencephalon. Genes Cells. 16:1097-1109.
81. Zembrzycki A, Griesel G, Stoykova A, Mansouri A. 2007. Genetic interplay between the transcription factors Sp8 and Emx2 in the patterning of the forebrain. Neural Dev. 2:8.
82. Zhou C, Qiu Y, Pereira FA, Crair MC, Tsai SY, Tsai MJ. 1999. The nuclear orphan receptor COUP-TFI is required for differentiation of subplate neurons and guidance of thalamocortical axons. Neuron. 24:847-859. (Pubitemid 30017664)
83. Zhou C, Tsai SY, Tsai MJ. 2001. COUP-TF1: An intrinsic factor for early regionalization of the neocortex. Genes Dev. 15:2054-2059. (Pubitemid 32762049)