The E3 ligase mind bomb-1 (Mib1) modulates delta-notch signaling to control neurogenesis and gliogenesis in the developing spinal cord

Journal of Biological Chemistry

Volumn 288, Issue 4, 2013, Pages 2580-2592

  Kang, Kyungjoon ^a   Lee, Donghoon ^a   Hong, Seulgi ^a   Park, Sung Gyoo ^a   Song, Mi Ryoung ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

DELETION MUTANTS; E3 LIGASE; KNOCK OUTS; NEUROGENESIS; NOTCH SIGNALING PATHWAYS; OLIGODENDROCYTES; SPINAL CORDS; UBIQUITIN LIGASES;

BOMBS (ORDNANCE); LIGANDS; MOLECULAR BIOLOGY; SPECIFICATIONS;

NEURONS;

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; CELL PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR 3; JAGGED1; JAGGED2; JAGGED3; KI 67 ANTIGEN; MESSENGER RNA; MIND BOMB 1 PROTEIN; NESTIN; NEUROGENIN 1; NEUROGENIN 2; NEURON SPECIFIC NUCLEAR PROTEIN; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; PRESENILIN 1; PROTEIN DLL1; PROTEIN DLL4; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE LOCATION; HES5 GENE; IN SITU HYBRIDIZATION; INTERNEURON; INTRACELLULAR SIGNALING; MASH1 GENE; MOUSE; MUTANT; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROGENIN 1 GENE; NEUROGENIN 2 GENE; NEUROMODULATION; NONHUMAN; NOTCH1 GENE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SPINAL CORD; UBIQUITINATION; UPREGULATION;

ALLELES; ANIMALS; ASTROCYTES; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; INTERNEURONS; LIGANDS; MICE; MICE, KNOCKOUT; NEUROGENESIS; NEUROGLIA; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; SPINAL CORD; STEM CELLS; UBIQUITIN-PROTEIN LIGASES;

EID: 84873870968     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.398263     Document Type: Article

References (59)

1. Artavanis-Tsakonas, S., Matsuno, K., and Fortini, M. E. (1995) Notch signaling. Science 268, 225-232
2. Park, H. C., and Appel, B. (2003) Delta-Notch signaling regulates oligodendrocyte specification. Development 130, 3747-3755
3. Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D., and Kintner, C. (1995) Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761-766
4. Haddon, C., Smithers, L., Schneider-Maunoury, S., Coche, T., Henrique, D., and Lewis, J. (1998) Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development 125, 359-370
5. Jessell, T. M. (2000) Neuronal specification in the spinal cord. Inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29
6. Mizuguchi, R., Kriks, S., Cordes, R., Gossler, A., Ma, Q., and Goulding, M. (2006) Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat. Neurosci. 9, 770-778
7. Peng, C. Y., Yajima, H., Burns, C. E., Zon, L. I., Sisodia, S. S., Pfaff, S. L., and Sharma, K. (2007) Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord. Neuron 53, 813-827
8. Yang, X., Tomita, T., Wines-Samuelson, M., Beglopoulos, V., Tansey, M. G., Kopan, R., and Shen, J. (2006) Notch1 signaling influences v2 interneuron and motor neuron development in the spinal cord. Dev. Neurosci. 28, 102-117
9. Kriegstein, A., and Alvarez-Buylla, A. (2009) The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184
10. Gaiano, N., Nye, J. S., and Fishell, G. (2000) Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26, 395-404
11. Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., and Kriegstein, A. R. (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714-720
12. Yoon, K. J., Koo, B. K., Im, S. K., Jeong, H. W., Ghim, J., Kwon, M. C., Moon, J. S., Miyata, T., and Kong, Y. Y. (2008) Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 58, 519-531
13. Bernardos, R. L., Lentz, S. I., Wolfe, M. S., and Raymond, P. A. (2005) Notch-Delta signaling is required for spatial patterning and Müller glia differentiation in the zebrafish retina. Dev. Biol. 278, 381-395
14. Eiraku, M., Tohgo, A., Ono, K., Kaneko, M., Fujishima, K., Hirano, T., and Kengaku, M. (2005) DNER acts as a neuron-specific Notch ligand during Bergmann glial development. Nat. Neurosci. 8, 873-880
15. Taylor, M. K., Yeager, K., and Morrison, S. J. (2007) Physiological Notch signaling promotes gliogenesis in the developing peripheral and central nervous systems. Development 134, 2435-2447
16. Wang, S., Sdrulla, A. D., diSibio, G., Bush, G., Nofziger, D., Hicks, C., Weinmaster, G., and Barres, B. A. (1998) Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21, 63-75
17. Kim, H., Shin, J., Kim, S., Poling, J., Park, H. C., and Appel, B. (2008) Notch-regulated oligodendrocyte specification from radial glia in the spinal cord of zebrafish embryos. Dev. Dyn. 237, 2081-2089
18. Pierfelice, T., Alberi, L., and Gaiano, N. (2011) Notch in the vertebrate nervous system. An old dog with new tricks. Neuron 69, 840-855
19. Seugnet, L., Simpson, P., and Haenlin, M. (1997) Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev. Biol. 192, 585-598
20. Yeh, E., Zhou, L., Rudzik, N., and Boulianne, G. L. (2000) Neuralized functions cell autonomously to regulate Drosophila sense organ development. EMBO J. 19, 4827-4837
21. Itoh, M., Kim, C. H., Palardy, G., Oda, T., Jiang, Y. J., Maust, D., Yeo, S. Y., Lorick, K., Wright, G. J., Ariza-McNaughton, L., Weissman, A. M., Lewis, J., Chandrasekharappa, S. C., and Chitnis, A. B. (2003) Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67-82
22. Weinmaster, G., and Fischer, J. A. (2011) Notch ligand ubiquitylation. What is it good for? Dev. Cell 21, 134-144
23. Chitnis, A. (2006) Why is delta endocytosis required for effective activation of notch? Dev. Dyn. 235, 886-894
24. Koo, B. K., Yoon, M. J., Yoon, K. J., Im, S. K., Kim, Y. Y., Kim, C. H., Suh, P. G., Jan, Y. N., and Kong, Y. Y. (2007) An obligatory role of mind bomb-1 in notch signaling of mammalian development. PLoS ONE 2, e1221
25. Imayoshi, I., Ohtsuka, T., Metzger, D., Chambon, P., and Kageyama, R. (2006) Temporal regulation of Cre recombinase activity in neural stem cells. Genesis 44, 233-238
26. Thaler, J. P., Koo, S. J., Kania, A., Lettieri, K., Andrews, S., Cox, C., Jessell, T. M., and Pfaff, S. L. (2004) A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41, 337-350
27. Thaler, J., Harrison, K., Sharma, K., Lettieri, K., Kehrl, J., and Pfaff, S. L. (1999) Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 23, 675-687
28. Thaler, J. P., Lee, S.-K., Jurata, L. W., Gill, G. N., and Pfaff, S. L. (2002) LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 110, 237-249
29. Kawaguchi, D., Yoshimatsu, T., Hozumi, K., and Gotoh, Y. (2008) Selection of differentiating cells by different levels of delta-like 1 among neural precursor cells in the developing mouse telencephalon. Development 135, 3849-3858
30. Koo, B. K., Lim, H. S., Song, R., Yoon, M. J., Yoon, K. J., Moon, J. S., Kim, Y. W., Kwon, M. C., Yoo, K. W., Kong, M. P., Lee, J., Chitnis, A. B., Kim, C. H., and Kong, Y. Y. (2005) Mind bomb 1 is essential for generating functional Notch ligands to activate Notch. Development 132, 3459-3470
31. Lindsell, C. E., Boulter, J., diSibio, G., Gossler, A., and Weinmaster, G. (1996) Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol. Cell. Neurosci. 8, 14-27
32. Caprioli, A., Goitsuka, R., Pouget, C., Dunon, D., and Jaffredo, T. (2002) Expression of Notch genes and their ligands during gastrulation in the chicken embryo. Mech. Dev. 116, 161-164
33. Panayi, H., Panayiotou, E., Orford, M., Genethliou, N., Mean, R., Lapathitis, G., Li, S., Xiang, M., Kessaris, N., Richardson, W. D., and Malas, S. (2010) Sox1 is required for the specification of a novel p2-derived interneuron subtype in the mouse ventral spinal cord. J. Neurosci. 30, 12274-12280
34. Deneen, B., Ho, R., Lukaszewicz, A., Hochstim, C. J., Gronostajski, R. M., and Anderson, D. J. (2006) The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52, 953-968
35. Pringle, N. P., Yu, W. P., Howell, M., Colvin, J. S., Ornitz, D. M., and Richardson, W. D. (2003) Fgfr3 expression by astrocytes and their precursors. Evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 130, 93-102
36. Bani-Yaghoub, M., Tremblay, R. G., Lei, J. X., Zhang, D., Zurakowski, B., Sandhu, J. K., Smith, B., Ribecco-Lutkiewicz, M., Kennedy, J., Walker, P. R., and Sikorska, M. (2006) Role of Sox2 in the development of the mouse neocortex. Dev. Biol. 295, 52-66
37. Cahoy, J. D., Emery, B., Kaushal, A., Foo, L. C., Zamanian, J. L., Christopherson, K. S., Xing, Y., Lubischer, J. L., Krieg, P. A., Krupenko, S. A., Thompson, W. J., and Barres, B. A. (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264-278
38. Alberi, L., Liu, S., Wang, Y., Badie, R., Smith-Hicks, C., Wu, J., Pierfelice, T. J., Abazyan, B., Mattson, M. P., Kuhl, D., Pletnikov, M., Worley, P. F., and Gaiano, N. (2011) Activity-induced Notch signaling in neurons requires Arc/Arg3.1 and is essential for synaptic plasticity in hippocampal networks. Neuron 69, 437-444
39. Shimada, I. S., Borders, A., Aronshtam, A., and Spees, J. L. (2011) Proliferating reactive astrocytes are regulated by Notch-1 in the peri-infarct area after stroke. Stroke 42, 3231-3237
40. Berndt, J. D., Aoyagi, A., Yang, P., Anastas, J. N., Tang, L., and Moon, R. T. (2011) Mindbomb 1, an E3 ubiquitin ligase, forms a complex with RYK to activate Wnt/α-catenin signaling. J. Cell Biol. 194, 737-750
41. Givogri, M. I., de Planell, M., Galbiati, F., Superchi, D., Gritti, A., Vescovi, A., de Vellis, J., and Bongarzone, E. R. (2006) Notch signaling in astrocytes and neuroblasts of the adult subventricular zone in health and after cortical injury. Dev. Neurosci. 28, 81-91
42. de la Pompa, J. L., Wakeham, A., Correia, K. M., Samper, E., Brown, S., Aguilera, R. J., Nakano, T., Honjo, T., Mak, T. W., Rossant, J., and Conlon, R. A. (1997) Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124, 1139-1148
43. Jin, Y., Blue, E. K., and Gallagher, P. J. (2006) Control of death-associated protein kinase (DAPK) activity by phosphorylation and proteasomal degradation. J. Biol. Chem. 281, 39033-39040
44. Barsi, J. C., Rajendra, R., Wu, J. I., and Artzt, K. (2005) Mind bomb1 is a ubiquitin ligase essential for mouse embryonic development and Notch signaling. Mech. Dev. 122, 1106-1117
45. Del Barrio, M. G., Taveira-Marques, R., Muroyama, Y., Yuk, D. I., Li, S., Wines-Samuelson, M., Shen, J., Smith, H. K., Xiang, M., Rowitch, D., and Richardson, W. D. (2007) A regulatory network involving Foxn4, Mash1, and delta-like 4/Notch1 generates V2a and V2b spinal interneurons from a common progenitor pool. Development 134, 3427-3436
46. Li, S., Misra, K., and Xiang, M. (2010)ACre transgenic line for studying V2 neuronal lineages and functions in the spinal cord. Genesis 48, 667-672
47. Yeo, S. Y., and Chitnis, A. B. (2007) Jagged-mediated Notch signaling maintains proliferating neural progenitors and regulates cell diversity in the ventral spinal cord. Proc. Natl. Acad. Sci. U.S.A. 104, 5913-5918
48. Rabadán, M. A., Cayuso, J., Le Dréau, G., Cruz, C., Barzi, M., Pons, S., Briscoe, J., and Martí, E. (2012) Jagged2 controls the generation of motor neuron and oligodendrocyte progenitors in the ventral spinal cord. Cell Death Differ. 19, 209-219
49. Rowitch, D. H. (2004) Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 5, 409-419
50. Grandbarbe, L., Bouissac, J., Rand, M., Hrabé de Angelis, M., Artavanis- Tsakonas, S., and Mohier, E. (2003) Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process. Development 130, 1391-1402
51. del Álamo, D., Rouault, H., and Schweisguth, F. (2011) Mechanism and significance of cis-inhibition in Notch signalling. Curr. Biol. 21, R40-R47
52. de Celis, J. F., and Bray, S. (1997) Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124, 3241-3251
53. Klein, T., Brennan, K., and Arias, A. M. (1997) An intrinsic dominant negative activity of serrate that is modulated during wing development in Drosophila. Dev. Biol. 189, 123-134
54. Micchelli, C. A., Rulifson, E. J., and Blair, S. S. (1997) The function and regulation of cut expression on the wing margin of Drosophila. Notch, Wingless, and a dominant negative role for Delta and Serrate. Development 124, 1485-1495
55. Schweisguth, F. (2004) Regulation of notch signaling activity. Curr. Biol. 14, R129-R138
56. Ladi, E., Nichols, J. T., Ge, W., Miyamoto, A., Yao, C., Yang, L. T., Boulter, J., Sun, Y. E., Kintner, C., and Weinmaster, G. (2005) The divergent DSL ligand Dll3 does not activate Notch signaling but cell autonomously attenuates signaling induced by other DSL ligands. J. Cell Biol. 170, 983-992
57. Glittenberg, M., Pitsouli, C., Garvey, C., Delidakis, C., and Bray, S. (2006) Role of conserved intracellular motifs in Serrate signalling, cis-inhibition, and endocytosis. EMBO J. 25, 4697-4706
58. Nishimura, T., Yamaguchi, T., Tokunaga, A., Hara, A., Hamaguchi, T., Kato, K., Iwamatsu, A., Okano, H., and Kaibuchi, K. (2006) Role of numb in dendritic spine development with a Cdc42 GEF intersectin and EphB2. Mol. Biol. Cell 17, 1273-1285
59. Giniger, E. (1998) A role for Abl in Notch signaling. Neuron 20, 667-681