Neurogenin2 expression together with NeuroM regulates GDNF family neurotrophic factor receptor α1 (GFRα1) expression in the embryonic spinal cord

Developmental Biology

Volumn 370, Issue 2, 2012, Pages 250-263

  Shimada, Takako ^a   Yaginuma, Hiroyuki ^a   Sato, Noboru ^b   Homma, Shunsaku ^a  

^a FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

Author keywords

Cash1; Chick; Electroporation; In situ hybridization; Math3; NeuroD4; P27; Ptf1a

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR FAMILY NEUROTROPHIC FACTOR RECEPTOR ALPHA1; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; MESSENGER RNA; NEUROGENIN 2; NEUROM PROTEIN; TRANSCRIPTION FACTOR MASH1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHICK EMBRYO; ELECTROPORATION; EMBRYO; GENE; GENE EXPRESSION; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR FAMILY NEUROTROPHIC FACTOR RECEPTOR ALPHA1 GENE; NERVE CELL DIFFERENTIATION; NEUROGENIN 2 GENE; NEUROM GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; SPINAL CORD NERVE CELL;

SPONDIAS PURPUREA;

EID: 84866256314     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.08.002     Document Type: Article

References (62)

1. Aaker J.D., Patineau A.L., Yang H.J., Ewart D.T., Gong W., Li T., Nakagawa Y., McLoon S.C., Koyano-Nakagawa N. Feedback regulation of NEUROG2 activity by MTGR1 is required for progression of neurogenesis. Mol. Cell Neurosci. 2009, 42:267-277.
2. Airaksinen M.S., Titievsky A., Saarma M. GDNF family neurotrophic factor signaling: four masters, one servant? Molecular and Cellular Neuroscience 1999, 13:313-325.
3. Airaksinen M.S., Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 2002, 3:383-394.
4. Akagi T., Inoue T., Miyoshi G., Bessho Y., Takahashi M., Lee J.E., Guillemot F., Kageyama R. Requirement of multiple basic helix-loop-helix genes for retinal neuronal subtype specification. J. Biol. Chem. 2004, 279:28492-28498.
5. Backman M., Machon O., Mygland L., van den Bout C.J., Zhong W., Taketo M.M., Krauss S. Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev. Biol. 2005, 279:155-168.
6. Bertrand N., Castro D.S., Guillemot F. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 2002, 3:517-530.
7. Bessho Y., Sakata R., Komatsu S., Shiota K., Yamada S., Kageyama R. Dynamic expression and essential functions of Hes7 in somite segmentation. Genes Dev. 2001, 15:2642-2647.
8. Boger H.A., Middaugh L.D., Zaman V., Hoffer B., Granholm A.C. Differential effects of the dopamine neurotoxin MPTP in animals with a partial deletion of the GDNF receptor, GFR alpha1, gene. Brain Res. 2008, 1241:18-28.
9. Bylund M., Andersson E., Novitch B.G., Muhr J. Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci. 2003, 6:1162-1168.
10. Caspary T., Anderson K.V. Patterning cell types in the dorsal spinal cord: what the mouse mutants say. Nat. Rev. Neurosci. 2003, 4:289-297.
11. Canty A.J., Dietze J., Harvey M., Enomoto H., Milbrandt J., Ibáñez C.F. Regionalized loss of parvalbumin interneurons in the cerebral cortex of mice with deficits in GFRα1 signaling. J. Neurosci. 2009, 29:10695-10705.
12. Deng H., Yang H., Le W., Deng X., Xu H., Xiong W., Zhu S., Xie W., Song Z., Jankovic J. Examination of the MASH1 gene in patients with Parkinson's disease. Biochem. Biophys. Res. Commun. 2010, 392:548-550.
13. Dubrulle J., Pourquié O. Coupling segmentation to axis formation. Development 2004, 131:5783-5793.
14. Fode C., Gradwohl G., Morin X., Dierich A., LeMeur M., Goridis C., Guillemot F. The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron 1998, 20:483-494.
15. Fode C., Ma Q., Casarosa S., Ang S.L., Anderson D.J., Guillemot F. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 2000, 14:67-80.
16. Garcès A., Haase G., Airaksinen M.S., Livet J., Filippi P., deLapeyrière O. GFRα1 is required for development of distinct subpopulations of motoneuron. J. Neurosci. 2000, 20:4992-5000.
17. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 1992, 119:493-501.
18. Gould T.W., Yonemura S., Oppenheim R.W., Ohmori S., Enomoto H. The neurotrophic effects of glial cell line-derived neurotrophic factor on spinal motoneurons are restricted to fusimotor subtypes. J. Neurosci. 2008, 28:2131-2146.
19. Gelman D.M., Marín O. Generation of interneuron diversity in the mouse cerebral cortex. Eur. J. Neurosci. 2010, 31:2136-2141.
20. Guillemot F. Spatial and temporal specification of neural fates by transcription factor codes. Development 2007, 134:3771-3780.
21. Haase G., Dessaud E., Garcès A., de Bovis B., Birling M., Filippi P., Schmalbruch H., Arber S., deLapeyrière O. GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron 2002, 35:893-905.
22. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morph. 1951, 88:49-92.
23. Henke R.M., Savage T.K., Meredith D.M., Glasgow S.M., Hori K., Dumas J., MacDonald R.J., Johnson J.E. Neurog2 is a direct downstream target of the Ptf1a-Rbpj transcription complex in dorsal spinal cord. Development 2009, 136:2945-2954.
24. Hirabayashi Y., Itoh Y., Tabata H., Nakajima K., Akiyama T., Masuyama N., Gotoh Y. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 2004, 131:2791-2801.
25. Hirata H., Bessho Y., Kokubu H., Masamizu Y., Yamada S., Lewis J., Kageyama R. Instability of Hes7 protein is crucial for the somite segmentation clock. Nat. Genet. 2004, 36:750-754.
26. Hollenbeck P.J., Fekete D.M. Expression of transgenes in primary neurons from chick peripheral and central nervous systems by retroviral infection of early embryos. Methods Cell Biol. 2003, 71:369-386.
27. Homma S., Yaginuma H., Vinsant S., Seino M., Kawata M., Gould T., Shimada T., Kobayashi N., Oppenheim R.W. Differential expression of the GDNF family receptors RET and GFRαlpha1, 2, and 4 in subsets of motoneurons: a relationship between motoneuron birthdate and receptor expression. J. Comp. Neurol. 2003, 456:245-259.
28. Hoshino M., Nakamura S., Mori K., Kawauchi T., Terao M., Nishimura Y.V., Fukuda A., Fuse T., Matsuo N., Sone M., Watanabe M., Bito H., Terashima T., Wright C.V., Kawaguchi Y., Nakao K., Nabeshima Y. Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 2005, 47:201-213.
29. Ide M., Yamada K., Toyota T., Iwayama Y., Ishitsuka Y., Minabe Y., Nakamura K., Hattori N., Asada T., Mizuno Y., Mori N., Yoshikawa T. Genetic association analyses of PHOX2B and ASCL1 in neuropsychiatric disorders: evidence for association of ASCL1 with Parkinson's disease. Hum. Genet. 2005, 117:520-527.
30. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 2000, 1:20-29.
31. Kageyama R., Ohtsuka T., Kobayashi T. The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 2007, 134:1243-1251.
32. Kageyama R., Ohtsuka T., Shimojo H., Imayoshi I. Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat. Neurosci. 2008, 11:1247-1251.
33. Lee S.K., Pfaff S.L. Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 2003, 38:731-745.
34. Lin L.F., Doherty D.H., Lile J.D., Bektesh S., Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993, 260:1130-1132.
35. Lo L., Tiveron M.C., Anderson D.J. MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development 1998, 125:609-620.
36. Ma Q. Transcriptional regulation of neuronal phenotype in mammals. J. Physiol. 2006, 575-2:379-387.
37. Mao W., Yan R.T., Wang S.Z. Proneural gene ash1 promotes amacrine cell production in the chick retina. Dev. Neurobiol. 2009, 69:88-104.
38. Machon O., Backman M., Machonova O., Kozmik Z., Vacik T., Andersen L., Krauss S. A dynamic gradient of Wnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev. Biol. 2007, 311:223-237.
39. Mattar P., Langevin L.M., Markham K., Klenin N., Shivji S., Zinyk D., Schuurmans C. Basic helix-loop-helix transcription factors cooperate to specify a cortical projection neuron identity. Mol. Cell. Biol. 2008, 28:1456-1469.
40. Mizuguchi R., Sugimori M., Takebayashi H., Kosako H., Nagao M., Yoshida S., Nabeshima Y., Shimamura K., Nakafuku M. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 2001, 31:757-771.
41. Niwa H., Yamamura K., Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 1991, 108:193-199.
42. Novitch B.G., Chen A.I., Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 2001, 31:773-789.
43. Parras C.M., Schuurmans C., Scardigli R., Kim J., Anderson D.J., Guillemot F. Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev. 2002, 16:324-338.
44. Pascual A., Hidalgo-Figueroa M., Piruat J.I., Pintado C.O., Gómez-Díaz R., López-Barneo J. Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat. Neurosci. 2008, 11:755-761.
45. Perez S.E., Rebelo S., Anderson D.J. Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 1999, 126:1715-1728.
46. Pleasure S.J., Collins A.E., Lowenstein D.H. Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J. Neurosci. 2000, 20:6095-6105.
47. Pozas E., Ibáñez C.F. GDNF and GFRα1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 2005, 45:701-713.
48. Puelles L., Rubenstein J.L. Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci. 2003, 26:469-476.
49. Roybon L., Mastracci T.L., Ribeiro D., Sussel L., Brundin P., Li J.Y. GABAergic differentiation induced by Mash1 is compromised by the bHLH proteins Neurogenin2, NeuroD1, and NeuroD2. Cereb. Cortex 2010, 20:1234-1244.
50. Roztocil T., Matter-Sadzinski L., Alliod C., Ballivet M., Matter J.M. NeuroM, a neural helix-loop-helix transcription factor, defines a new transition stage in neurogenesis. Development 1997, 124:3263-3272.
51. Shimojo H., Ohtsuka T., Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 2008, 58:52-64.
52. Schuchardt A., Srinivas S., Pachnis V., Costantini F. Isolation and characterization of a chicken homolog of the c-ret proto-oncogene. Oncogene 1995, 10:641-649.
53. Schuurmans C., Armant O., Nieto M., Stenman J.M., Britz O., Klenin N., Brown C., Langevin L.M., Seibt J., Tang H., Cunningham J.M., Dyck R., Walsh C., Campbell K., Polleux F., Guillemot F. Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. EMBO J. 2004, 23:2892-2902.
54. Snider W.D. Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 1994, 77:627-638.
55. Sugimori M., Nagao M., Bertrand N., Parras C.M., Guillemot F., Nakafuku M. Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development 2007, 134:1617-1629.
56. Sussel L., Marin O., Kimura S., Rubenstein J.L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 1999, 126:3359-3370.
57. Tomita K., Moriyoshi K., Nakanishi S., Guillemot F., Kageyama R. Mammalian achaete-scute and atonal homologs regulate neuronal versus glial fate determination in the central nervous system. EMBO J. 2000, 19:5460-5472.
58. Vrieseling E., Arber S. Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 2006, 127:1439-1452.
59. Wildner H., Müller T., Cho S.H., Bröhl D., Cepko C.L., Guillemot F., Birchmeier C. dILA neurons in the dorsal spinal cord are the product of terminal and non-terminal asymmetric progenitor cell divisions, and require Mash1 for their development. Development 2006, 133:2105-2113.
60. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.
61. Yoon K., Gaiano N. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat. Neurosci. 2005, 8:709-715.
62. Zaman V., Boger H.A., Granholm A.C., Rohrer B., Moore A., Buhusi M., Gerhardt G.A., Hoffer B.J., Middaugh L.D. The nigrostriatal dopamine system of aging GFRalpha-1 heterozygous mice: neurochemistry, morphology and behavior. Eur. J. Neurosci. 2008, 28:1557-1568.