Identification of a Novel Basic Helix-Loop-Helix Gene, Heslike, and Its Role in GABAergic Neurogenesis

Journal of Neuroscience

Volumn 24, Issue 14, 2004, Pages 3672-3682

  Miyoshi, Goichi ^a   Bessho, Yasumasa ^a   Yamada, Shuichi ^a   Kageyama, Ryoichiro ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

bHLH; Diencephalon; GABAergic neuron; Heslike; Mash1; Mesencephalon

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; HELIX LOOP HELIX PROTEIN; PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MASH1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DIENCEPHALON; EMBRYO; EMBRYOLOGY; FEMALE; GENE; HESLIKE GENE; MALE; MESENCEPHALON; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; STEM CELL;

AMINO ACID SEQUENCE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN; CELL LINEAGE; CELLS, CULTURED; DIENCEPHALON; DNA-BINDING PROTEINS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HELIX-LOOP-HELIX MOTIFS; HUMANS; MESENCEPHALON; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NEURONS; RATS; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; STEM CELLS; TAKIFUGU; TRANSCRIPTION FACTORS; ZEBRAFISH;

EID: 1842782799     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5327-03.2004     Document Type: Article

References (57)

1. Anderson SA, Eisenstat DD, Shi L, Rubenstein JLR (1997a) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
2. Anderson SA, Qiu M, Bulfone A, Eisenstat DD, Meneses J, Pedersen R, Rubenstein JLR (1997b) Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19:27-37.
3. Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517-530.
4. Casarosa S, Fode C, Guillemot F (1999) Mash1 regulates neurogenesis in the ventral telencephalon. Development 126:525-534.
5. Caspary T, Anderson KV (2003) Patterning cell types in the dorsal spinal cord: what the mouse mutants say. Nat Rev Neurosci 4:289-297.
6. Chin MT, Maemura K, Fukumoto S, Jain MK, Layne MD, Watanabe M, Hsieh C-M, Lee M-E (2000) Cardiovascular basic helix-loop-helix factor 1, a novel transcriptional repressor expressed preferentially in the developing and adult cardiovascular system. J Biol Chem 275:6381-6387.
7. Corbin JG, Gaiano N, Machold RP, Langston A, Fishell G (2000) The Gsh2 homeodomain gene controls multiple aspects of telencephalic development. Development 127:5007-5020.
8. Corbin JG, Nery S, Fishell G (2001) Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat Neurosci 4:1177-1182.
9. Davis RL, Cheng P-F, Lassar AB, Weintraub H (1990) The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60:733-746.
10. De Carlos JA, López-Mascaraque L, Valverde F (1996) Dynamics of cell migration from the lateral ganglionic eminence in the rat. J Neurosci 16:6146-6156.
11. Fode C, Ma Q, Casarosa S, Ang S-L, Anderson DJ, Guillemot F (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14:67-80.
12. Grbavec D, Stifani S (1996) Molecular interaction between TLE1 and the carboxyl-terminal domain of HES-1 containing the WRPW motif. Biochem Biophys Res Commun 223:701-705.
13. Guillemot F, Lo L-C, Johnson JE, Auerbach A, Anderson DJ, Joyner AL (1993) Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75:463-476.
14. Hatakeyama J, Tomita K, Inoue T, Kageyama R (2001) Roles of homeobox and bHLH genes in specification of a retinal cell type. Development 128:1313-1322.
15. Hirata H, Ohtsuka T, Bessho Y, Kageyama R (2000) Generation of structurally and functionally distinct factors from the basic helix-loop-helix gene Hes3 by alternative first exons. J Biol Chem 275:19083-19089.
16. Hirata H, Tomita K, Bessho Y, Kageyama R (2001) Hes1 and Hes3 regulate maintenance of the isthmic organizer and development of the mid/hindbrain. EMBO J 20:4454-4466.
17. Inoue T, Hojo M, Bessho Y, Tano Y, Lee JE, Kageyama R (2002) Math3 and NeuroD regulate amacrine cell fate specification in the retina. Development 129:831-842.
18. Isaka F, Ishibashi M, Taki W, Hashimoto N, Nakanishi S, Kageyama R (1999) Ectopic expression of the bHLH gene Math1 disturbs neural development. Eur J Neurosci 11:2582-2588.
19. Ishibashi M, Moriyoshi K, Sasai Y, Shiota K, Nakanishi S, Kageyama R (1994) Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 13:1799-1805.
20. Iso T, Sartorelli V, Chung G, Shichinohe T, Kedes L, Hamamori Y (2001) HERP, a new primary target of Notch regulated by ligand binding. Mol Cell Biol 21:6071-6079.
21. Jessell TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1:20-29.
22. Katarova Z, Sekerková G, Prodan S, Mugnaini E, Szabó G (2000) Domain-restricted expression of two glutamic acid decarboxylase genes in midgestation mouse embryos. J Comp Neurol 424:607-627.
23. Kill I (1996) Localisation of the Yi-67 antigen within the nucleolus. J Cell Sci 109:1253-1263.
24. Kokubo H, Lun Y, Johnson RL (1999) Identification and expression of a novel family of bHLH cDNAs related to Drosophila Hairy and Enhancer of split. Biochem Biophys Res Commun 260:459-465.
25. Lee S-K, Pfaff SL (2003) Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 38:731-745.
26. Leimeister C, Externbrink A, Klamt B, Gessler M (1999) Hey genes: a novel subfamily of hairy- and Enhancer of split related genes specifically expressed during mouse embryogenesis. Mech Dev 85:173-177.
27. Lu QR, Cai L, Rowitch D, Cepko CL, Stiles CD (2001) Ectopic expression of Olig1 promotes oligodendrocyte formation and reduces neuronal survival in developing mouse cortex. Nat Neurosci 4:973-974.
28. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109:75-86.
29. Ma Q, Sommer L, Cserjesi P, Anderson DJ (1997) Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing Notch ligands. J Neurosci 17:3644-3652.
30. Marín O, Anderson SA, Rubenstein JLR (2000) Origin and molecular specification of striatal interneurons. J Neurosci 20:6063-6076.
31. Mizuguchi R, Sugimori M, Takebayashi H, Kosako H, Nagao M, Yoshida S, Nabeshima Y, Shimamura K, Nakafuku M (2001) Combinatorial roles of Olig2 and Neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31:757-771.
32. Murray RC, Navi D, Fesenko J, Lander AD, Calof AL (2003) Widespread defects in the primary olfactory pathway caused by loss of Mash1 function. J Neurosci 23:1769-1780.
33. Nakagawa O, Nakagawa M, Richardson JA, Olson EN, Srivastava D (1999) HRT1, HRT2, and HRT3: a new subclass of bHLH transcription factors marking specific cardiac, somitic, and pharyngeal arch segments. Dev Biol 216:72-84.
34. Nakamura Y, Sakakibara S, Miyata T, Ogawa M, Shimazaki T, Weiss S, Kageyama R, Okano H (2000) The bHLH gene Hes1 as a repressor of the neuronal commitment of CNS stem cells. J Neurosci 20:283-293.
35. Nieto M, Schuurmans S, Britz O, Guillemot F (2001) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29:401-413.
36. Novitch BG, Chen AI, Jessell TM (2001) Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31:773-789.
37. Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R (1999) Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO J 18:2196-2207.
38. Ohtsuka T, Sakamoto M, Guillemot F, Kageyama R (2001) Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain. J Biol Chem 276:30467-30474.
39. Paroush Z, Finley Jr RL, Kidd T, Wainwright SM, Ingham PW, Brent R, Ish-Horowictz D (1994) Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell 79:805-815.
40. Parras CM, Schuurmans C, Scardigli R, Kim J, Anderson DJ, Guillemot F (2002) Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev 16:324-338.
41. Poulin G, Lebel M, Chamberland M, Paradis FW, Drouin J (2000) Specific protein-protein interaction between basic helix-loop-helix transcription factors and homeoproteins of the Pitx family. Mol Cell Biol 20:4826-4837.
42. Puelles L, Rubenstein JLR (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469-476.
43. Ross SE, Greenberg ME, Stiles CD (2003) Basic helix-loop-helix factors in cortical development. Neuron 39:13-25.
44. Sasai Y, Kageyama R, Tagawa Y, Shigemoto R, Nakanishi S (1992) Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev 6:2620-2634.
45. Shimamura K, Hartigan DJ, Martinez S, Puelles L, Rubenstein JLR (1995) Longitudinal organization of the anterior neural plate and neural tube. Development 121:3923-3933.
46. Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, Fan G, Greenberg ME (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104:365-376.
47. Sussel L, Marin O, Kimura S, Rubenstein JLR (1999) 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 126:3359-3370.
48. Tamamaki N, Fujimori KE, Takauji R (1997) Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci 17:8313-8323.
49. Tan S-S, Valcanis H, Kalloniatis M, Harvey A (2002) Cellular dispersion patterns and phenotypes in the developing mouse superior colliculus. Dev Biol 241:117-131.
50. Tomita K, Moriyoshi K, Nakanishi S, Guillemot F, Kageyama R (2000) Mammalian achaete-scute and atonal homologs regulate neuronal versus glial fate determination in the central nervous system. EMBO J 19:5460-5472.
51. Toresson H, Potter SS, Campbell K (2000) Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127:4361-4371.
52. Wray S, Fueshko SM, Kusano K, Gainer H (1996) GABAergic neurons in the embryonic olfactory pit/vomeronasal organ: maintenance of functional GABAergic synapses in olfactory explants. Dev Biol 180:631-645.
53. Yun K, Fischman S, Johnson J, Hrabe de Angelis M, Weinmaster G, Rubenstein JLR (2002) Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development 129:5029-5040.
54. Zhong TP, Rosenberg M, Mohideen M-APK, Weinstein B, Fishman MC (2000) gridlock, an HLH gene required for assembly of the aorta in zebrafish. Science 287:1820-1824.
55. Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61-73.
56. Zhou Q, Choi G, Anderson DJ (2001) The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31:791-807.
57. Zimmerman L, Parr B, Lendahl U, Cunningham M, McKay R, Gavin B, Mann J, Vassileva G, McMahon A (1994) Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron 12:11-24.