Neuronal basic helix-loop-helix proteins neurod2/6 regulate cortical commissure formation before midline interactions

Journal of Neuroscience

Volumn 33, Issue 2, 2013, Pages 641-651

  Bormuth, Ingo ^a,b   Yan, Kuo ^b   Yonemasu, Tomoko ^a   Gummert, Maike ^a   Zhang, Mingyue ^c   Wichert, Sven ^a   Grishina, Olga ^b   Pieper, Alexander ^a   Zhang, Weiqi ^c   Goebbels, Sandra ^a   Tarabykin, Victor ^b   Nave, Klaus Armin ^a   Schwab, Markus H ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4', 6 DIAMIDINO 2 PHENYLINDOLE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CONTACTIN; DNA BINDING PROTEIN; EOMESODERMIN; F ACTIN; HU ANTIGEN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NERVE CELL ADHESION MOLECULE L1; NESTIN; NEUROFILAMENT PROTEIN; NEUROGENIC DIFFERENTIATION FACTOR; NEUROGENIC DIFFERENTIATION FACTOR 2; NEUROGENIC DIFFERENTIATION FACTOR 6; PROTEIN FNP7; PROTEIN SATB2; ROUNDABOUT RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BRN2; TRANSCRIPTION FACTOR CTIP2; TRANSCRIPTION FACTOR CUX2; TRANSCRIPTION FACTOR LMO4; TRANSCRIPTION FACTOR SOX5; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTROPORATION; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; GENOTYPE; GLIA; HIPPOCAMPAL CA1 REGION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LASER CAPTURE MICRODISSECTION; MOUSE; NERVE FIBER; NERVE FIBER GROWTH; NEUROMODULIN; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REAL TIME POLYMERASE CHAIN REACTION; SYNAPTOGENESIS; THALAMOCORTICAL TRACT;

ANIMALS; ANIMALS, NEWBORN; AXONS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CEREBRAL CORTEX; CONTACTIN 2; CORPUS CALLOSUM; ELECTROPORATION; EMBRYO, MAMMALIAN; GENOTYPE; GLUTAMATES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LASER CAPTURE MICRODISSECTION; MICE; NERVE FIBERS; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; POLYMERASE CHAIN REACTION; RECEPTORS, IMMUNOLOGIC; SYNAPSES;

EID: 84872072593     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0899-12.2013     Document Type: Article

References (66)

1. Agarwal A, Dibaj P, Kassmann CM, Goebbels S, Nave KA, Schwab MH (2012) In vivo imaging and noninvasive ablation of pyramidal neurons in adult NEX-CreERT2 mice. Cereb Cortex 22:1473-1486. CrossRef Medline
2. Alcamo EA, Chirivella L, Dautzenberg M, Dobreva G, Fariñas I, Grosschedl R, McConnell SK (2008) Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57:364-377. CrossRef Medline
3. Andrews WD, Barber M, Parnavelas JG (2007) Slit-Robo interactions during cortical development. J Anat 211:188-198. CrossRef Medline
4. Angevine JB Jr, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766-768. CrossRef Medline
5. Arimura N, Kaibuchi K (2007) Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8:194-205. CrossRef Medline
6. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45:207-221. CrossRef Medline
7. Armentano M, Filosa A, Andolfi G, Studer M (2006) COUP-TFI is required for the formation of commissural projections in the forebrain by regulating axonal growth. Development 133:4151-4162. CrossRef Medline
8. Bagri A, Marín O, Plump AS, Mak J, Pleasure SJ, Rubenstein JL, Tessier-Lavigne M (2002) Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33:233-248. CrossRef Medline
9. Barnes AP, Polleux F (2009) Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci 32:347-381. CrossRef Medline
10. Bartholomä A, Nave KA (1994) NEX-1: a novel brain-specific helix-loophelix protein with autoregulation and sustained expression in mature cortical neurons. Mech Dev 48:217-228. CrossRef Medline
11. Berkes CA, Tapscott SJ (2005) MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 16:585-595. CrossRef Medline
12. Britanova O, de Juan Romero C, Cheung A, Kwan KY, Schwark M, Gyorgy A, Vogel T, Akopov S, Mitkovski M, Agoston D, Sestan N, Molnár Z, Tarabykin V (2008) Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57:378-392. CrossRef Medline
13. Brzózka MM, Radyushkin K, Wichert SP, Ehrenreich H, Rossner MJ (2010) Cognitive and sensorimotor gating impairments in transgenic mice overexpressing the schizophrenia susceptibility gene Tcf4 in the brain. Biol Psychiatry 68:33-40. CrossRef Medline
14. Burbach JP, van der Zwaag B (2009) Contact in the genetics of autism and schizophrenia. Trends Neurosci 32:69-72. CrossRef Medline
15. Cherry TJ, Wang S, Bormuth I, Schwab M, Olson J, Cepko CL (2011) NeuroD factors regulate cell fate and neurite stratification in the developing retina. J Neurosci 31:7365-7379. CrossRef Medline
16. Demyanenko GP, Tsai AY, Maness PF (1999) Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knock-out mice. J Neurosci 19:4907-4920. Medline
17. Dickson BJ, Gilestro GF (2006) Regulation of commissural axon pathfinding by Slit and its Robo receptors. Annu Rev Cell Dev Biol 22:651-675. CrossRef Medline
18. Donahoo AL, Richards LJ (2009) Understanding the mechanisms of callosal development through the use of transgenic mouse models. Semin Pediatr Neurol 16:127-142. CrossRef Medline
19. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, Stoeckli ET, Keino-Masu K, Masu M, Rayburn H, Simons J, Bronson RT, Gordon JI, Tessier-Lavigne M, Weinberg RA (1997) Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386: 796-804. CrossRef Medline
20. Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14:67-80. CrossRef Medline
21. Fukamauchi F, Aihara O, Wang YJ, Akasaka K, Takeda Y, Horie M, Kawano H, Sudo K, Asano M, Watanabe K, Iwakura Y (2001) TAG-1-deficient mice have marked elevation of adenosine A1 receptors in the hippocampus. Biochem Biophys Res Commun 281:220-226. CrossRef Medline
22. Goebbels S, Bormuth I, Bode U, Hermanson O, Schwab MH, Nave KA (2006) Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44:611-621. CrossRef Medline
23. Hand R, Polleux F (2011) Neurogenin2 regulates the initial axon guidance of cortical pyramidal neurons projecting medially to the corpus callosum. Neural Dev 6:30. CrossRef Medline
24. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29:353-366. CrossRef Medline
25. Huang HP, Chu K, Nemoz-Gaillard E, Elberg D, Tsai MJ (2002) Neogenesis of +-cells in adult BETA2/NeuroD-deficient mice. Mol Endocrinol 16: 541-551. CrossRef Medline
26. Ince-Dunn G, Hall BJ, Hu SC, Ripley B, Huganir RL, Olson JM, Tapscott SJ, Ghosh A (2006) Regulation of thalamocortical patterning and synaptic maturation by NeuroD2. Neuron 49:683-695. CrossRef Medline
27. Innocenti GM, Price DJ (2005) Exuberance in the development of cortical networks. Nat Rev Neurosci 6:955-965. CrossRef Medline
28. Inoue C, Bae SK, Takatsuka K, Inoue T, Bessho Y, Kageyama R (2001) Math6, a bHLH gene expressed in the developing nervous system, regulates neuronal versus glial differentiation. Genes Cells 6:977-986. CrossRef Medline
29. Jones L, López-Bendito G, Gruss P, Stoykova A, Molnár Z (2002) Pax6 is required for the normal development of the forebrain axonal connections. Development 129:5041-5052. Medline
30. Katidou M, Vidaki M, Strigini M, Karagogeos D (2008) The immunoglobulin superfamily of neuronal cell adhesion molecules: lessons from animal models and correlation with human disease. Biotechnol J 3:1564-1580. CrossRef Medline
31. Kay JN, Voinescu PE, Chu MW, Sanes JR (2011) Neurod6 expression defines new retinal amacrine cell subtypes and regulates their fate. Nat Neurosci 14:965-972. CrossRef Medline
32. Kume H, Maruyama K, Tomita T, Iwatsubo T, Saido TC, Obata K (1996) Molecular cloning of a novel basic helix-loop-helix protein from the rat brain. Biochem Biophys Res Commun 219:526-530. CrossRef Medline
33. Lin CH, Stoeck J, Ravanpay AC, Guillemot F, Tapscott SJ, Olson JM (2004) Regulation of neuroD2 expression in mouse brain. Dev Biol 265:234-245. CrossRef Medline
34. Lin CH, Hansen S, Wang Z, Storm DR, Tapscott SJ, Olson JM (2005) The dosage of the neuroD2 transcription factor regulates amygdala development and emotional learning. Proc Natl Acad Sci U S A 102:14877-14882. CrossRef Medline
35. Lindwall C, Fothergill T, Richards LJ (2007) Commissure formation in the mammalian forebrain. Curr Opin Neurobiol 17:3-14. CrossRef Medline
36. Liu M, Pleasure SJ, Collins AE, Noebels JL, Naya FJ, Tsai MJ, Lowenstein DH (2000) Loss of BETA2/NeuroD leads to malformation of the dentate gyrus and epilepsy. Proc Natl Acad Sci U S A 97:865-870. CrossRef Medline
37. López-Bendito G, Flames N, Ma L, Fouquet C, Di Meglio T, Chedotal A, Tessier-Lavigne M, Marín O (2007) Robo1 and Robo2 cooperate to control the guidance of major axonal tracts in the mammalian forebrain. J Neurosci 27:3395-3407. CrossRef Medline
38. Ma Q, Kintner C, Anderson DJ (1996) Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87:43-52. CrossRef Medline
39. Malhotra JD, Tsiotra P, Karagogeos D, Hortsch M (1998) Cis-activation of L1-mediated ankyrin recruitment by TAG-1 homophilic cell adhesion. J Biol Chem 273:33354-33359. CrossRef Medline
40. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26. CrossRef Medline
41. Mihrshahi R (2006) The corpus callosum as an evolutionary innovation. J Exp Zool B Mol Dev Evol 306:8-17. CrossRef Medline
42. Mikami T, Yasunaga D, Kitagawa H (2009) Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E. J Biol Chem 284: 4494-4499. CrossRef Medline
43. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427-437. CrossRef Medline
44. O'Donnell M, Chance RK, Bashaw GJ (2009) Axon growth and guidance: receptor regulation and signal transduction. Annu Rev Neurosci 32:383-412. CrossRef Medline
45. Olson JM, Asakura A, Snider L, Hawkes R, Strand A, Stoeck J, Hallahan A, Pritchard J, Tapscott SJ (2001) NeuroD2 is necessary for development and survival of central nervous system neurons. Dev Biol 234:174-187. CrossRef Medline
46. Parrish JZ, Emoto K, Kim MD, Jan YN (2007) Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci 30:399-423. CrossRef Medline
47. Paul LK, Brown WS, Adolphs R, Tyszka JM, Richards LJ, Mukherjee P, Sherr EH (2007) Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat Rev Neurosci 8:287-299. CrossRef Medline
48. Pavlou O, Theodorakis K, Falk J, Kutsche M, Schachner M, Faivre-Sarrailh C, Karagogeos D (2002) Analysis of interactions of the adhesion molecule TAG-1 and its domains with other immunoglobulin superfamily members. Mol Cell Neurosci 20:367-381. CrossRef Medline
49. Richards LJ, Plachez C, Ren T (2004) Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin Genet 66:276-289. CrossRef Medline
50. Ross SE, Greenberg ME, Stiles CD (2003) Basic helix-loop-helix factors in cortical development. Neuron 39:13-25. CrossRef Medline
51. Rudnicki MA, Braun T, Hinuma S, Jaenisch R (1992) Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71:383-390. CrossRef Medline
52. Saito T (2006) In vivo electroporation in the embryonic mouse central nervous system. Nat Protoc 1:1552-1558. CrossRef Medline
53. Sansom SN, Livesey FJ (2009) Gradients in the brain: the control of the development of form and function in the cerebral cortex. Cold Spring Harb Perspect Biol 1:a002519. CrossRef Medline
54. Savvaki M, Panagiotaropoulos T, Stamatakis A, Sargiannidou I, Karatzioula P, Watanabe K, Stylianopoulou F, Karagogeos D, Kleopa KA (2008) Impairment of learning and memory in TAG-1 deficient mice associated with shorter CNS internodes and disrupted juxtaparanodes. Mol Cell Neurosci 39:478-490. CrossRef Medline
55. Schuurmans C, Armant O, Nieto M, Stenman JM, Britz O, Klenin N, Brown C, Langevin LM, Seibt J, Tang H, Cunningham JM, Dyck R, Walsh C, Campbell K, Polleux F, Guillemot F (2004) Sequential phases of cortical specification involve Neurogenin-dependent and-independent pathways. EMBO J 23:2892-2902. CrossRef Medline
56. Schwab MH, Druffel-Augustin S, Gass P, Jung M, Klugmann M, Bartholomae A, Rossner MJ, Nave KA (1998) Neuronal basic helix-loop-helix proteins (NEX, neuro D, NDRF): spatiotemporal expression and targeted disruption of the NEX gene in transgenic mice. J Neurosci 18:1408-1418. Medline
57. Schwab MH, Bartholomae A, Heimrich B, Feldmeyer D, Druffel-Augustin S, Goebbels S, Naya FJ, Zhao S, Frotscher M, Tsai MJ, Nave KA (2000) Neuronal basic helix-loop-helix proteins (NEX and BETA2/Neuro D) regulate terminal granule cell differentiation in the hippocampus. J Neurosci 20:3714-3724. Medline
58. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, Tessier-Lavigne M (1996) Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014. CrossRef Medline
59. Shen Y, Mani S, Donovan SL, Schwob JE, Meiri KF (2002) Growthassociated protein-43 is required for commissural axon guidance in the developing vertebrate nervous system. J Neurosci 22:239-247. Medline
60. Sommer L, Ma Q, Anderson DJ (1996) Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol Cell Neurosci 8:221-241. CrossRef Medline
61. Stefansson H, Ophoff RA, Steinberg S, Andreassen OA, Cichon S, Rujescu D, Werge T, Pietiläinen OP, Mors O, Mortensen PB, Sigurdsson E, Gustafsson O, Nyegaard M, Tuulio-Henriksson A, Ingason A, Hansen T, Suvisaari J, Lonnqvist J, Paunio T, Børglum AD, et al. (2009) Common variants conferring risk of schizophrenia. Nature 460:744-747. CrossRef Medline
62. Vernes SC, Newbury DF, Abrahams BS, Winchester L, Nicod J, Groszer M, Alarcón M, Oliver PL, Davies KE, Geschwind DH, Monaco AP, Fisher SE (2008) A functional genetic link between distinct developmental language disorders. N Engl J Med 359:2337-2345. CrossRef Medline
63. Wilke SA, Hall BJ, Antonios JK, Denardo LA, Otto S, Yuan B, Chen F, Robbins EM, Tiglio K, Williams ME, Qiu Z, Biederer T, Ghosh A (2012) NeuroD2 regulates the development of hippocampal mossy fiber synapses. Neural Dev 7:9. CrossRef Medline
64. Wu SX, Goebbels S, Nakamura K, Nakamura K, Kometani K, Minato N, Kaneko T, Nave KA, Tamamaki N (2005) Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc Natl Acad Sci U S A 102:17172-17177. CrossRef Medline
65. Yang Y, Kim AH, Yamada T, Wu B, Bilimoria PM, Ikeuchi Y, de la Iglesia N, Shen J, Bonni A (2009) A Cdc20-APC ubiquitin signaling pathway regulates presynaptic differentiation. Science 326:575-578. CrossRef Medline
66. Yasunami M, Suzuki K, Maruyama H, Kawakami H, Nagai Y, Hagiwara M, Ohkubo H (1996) Molecular cloning and characterization of a cDNA encoding a novel basic helix-loop-helix protein structurally related to Neuro-D/BHF1. Biochem Biophys Res Commun 220:754-758. CrossRef Medline