The CES-2-related transcription factor E4BP4 is an intrinsic regulator of motoneuron growth and survival

Development

Volumn 131, Issue 18, 2004, Pages 4425-4434

  Junghans, Dirk ^a,b   Chauvet, Sophie ^a   Buhler, Emmanuelle ^a   Dudley, Keith ^a   Sykes, Toby ^a   Henderson, Christopher E ^a  

^a INSERM   (France)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

Axon growth; In ovo electroporation; Motoneuron; Survival pathways

Indexed keywords

CELL RECEPTOR; LAMININ; NEUROTROPHIC FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E4BP4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CELL REGENERATION; CELL SIZE; CELL SURVIVAL; CHICK EMBRYO; CHICKEN; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; IN VIVO STUDY; MOTONEURON; MUSCLE DEVELOPMENT; NERVE CELL CULTURE; NERVE CELL GROWTH; NERVE CELL NECROSIS; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURIFICATION; RAT; REGULATORY MECHANISM;

ANIMALS; AXONS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIVISION; CELL SIZE; CELL SURVIVAL; CELLS, CULTURED; CHICKENS; DNA-BINDING PROTEINS; G-BOX BINDING FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MOTOR NEURONS; NERVE GROWTH FACTORS; RATS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ANIMALIA; GALLUS GALLUS; VERTEBRATA;

EID: 6944239882     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01313     Document Type: Article

References (47)

1. Arce, V., Garcès, A., de Bovis, B., Filippi, P., Henderson, C., Pettmann, B. and deLapeyrière, O. (1999). Cardiotrophin-1 requires LIFRbeta to promote survival of mouse motoneurons purified by a novel technique. J. Neurosci. Res. 55 119-126.
2. Backman, S. A., Stambolic, V., Suzuki,,A., Haight, J., Elia, A., Pretorius, J., Tsao, M. S., Shannon, P., Bolon, B., Ivy, G. O. et al. (2001). Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease. Nat. Genet. 29, 396-403.
3. Bloch-Gallego, E., le Roux, I., Joliot, A. H., Volovitch, M., Henderson, C. E. and Prochiantz, A. (1993). Antennapedia homeobox peptide enhances growth and branching of embryonic chicken motoneurons in vitro. J. Cell Biol. 120, 485-492.
4. Brunet, A., Datta, S. R. and Greenberg, M. E. (2001). Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11, 297-305.
5. Chen, W. J., Lewis, K. S., Chandra, G., Cogswell, J. P., Stinnett, S. W., Kadwell, S. H. and Gray, J. G. (1995). Characterization of human E4BP4, a phosphorylated bZIP factor. Biochim. Biophys. Acta 1264, 388-396.
6. Chen, W., Yu, Y. L., Lee, S. F., Chiang, Y. J., Chao, J. R., Huang, J. H., Chiong, J. H., Huang, C. J., Lai, M. Z., Yang-Yen, H. F. et al. (2001). CREB is one component of the binding complex of the Ces-2/E2A-HLF binding element and is an integral part of the interleukin-3 survival signal. Mol. Cell. Biol. 21, 4636-4646.
7. Conlon, I. and Raff, M. (1999). Size control in animal development. Cell 96, 235-244.
8. Coulouarn, Y., Fernex, C., Jegou, S., Henderson, C. E., Vaudry, H. and Lihrmann, I. (2001). Specific expression of the urotensin II gene in sacral motoneurons of developing rat spinal cord. Mech. Dev. 101, 187-190.
9. Cowell, I. G., Skinner, A. and Hurst, H. C. (1992). Transcriptional repression by a novel member of the bZIP family of transcription factors. Mol. Cell. Biol. 12, 3070-3077.
10. Davies, A. M. (1996). The neurotrophic hypothesis: where does it stand? Philos. Trans. R. Soc. London B., Biol. Sci. 351, 389-394.
11. Doi, M., Nakajima, Y., Okano, T. and Fukada, Y. (2001). Light-induced phase-delay of the chicken pineal circadian clock is associated with the induction of cE4BP4, a potential transcriptional repressor of cPer2 gene. Proc. Natl. Acad. Sci. USA 98, 8089-8094.
12. Drolet, D. W., Scully, K. M., Simmons, D. M., Wegner, M., Chu, K. T., Swanson, L. W. and Rosenfeld, M. G. (1991). TEF, a transcription factor expressed specifically in the anterior pituitary during embryogenesis, defines a new class of leucine zipper proteins. Genes Dev. 5, 1739-1753.
13. Ellis, R. E. and Horvitz, H. R. (1991). Two C. elegans genes control the programmed deaths of specific cells in the pharynx. Development 112, 591-603.
14. Falvey, E., Fleury-Olela, F. and Schibler, U. (1995). The rat hepatic leukemia factor (HLF) gene encodes two transcriptional activators with distinct circadian rhythms, tissue distributions and target preferences. EMBO J. 14, 4307-4317.
15. Fonjallaz, P., Ossipow, V., Wanner, G. and Schibler, U. (1996). The two PAR leucine zipper proteins, TEF and DBP, display similar circadian and tissue-specific expression, but have different target promoter preferences. EMBO J. 15, 351-362.
16. Garcès, A., Livet, J., Grillet, N., Henderson, C. E. and deLapeyrière, O. (2001). Responsiveness to neurturin of subpopulations of embryonic rat spinal motoneuron does not correlate with expression of GFR alpha 1 or GFR alpha 2. Dev. Dyn. 220, 189-197.
17. Groszer, M., Erickson, R., Scripture-Adams, D. D., Lesche, R., Trumpp, A., Zack, J. A., Kornblum, H. I., Liu, X. and Wu, H. (2001). Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294, 2186-2189.
18. Haas, N. B., Cantwell, C. A., Johnson, P. F. and Burch, J. B. (1995). DNA-binding specificity of the PAR basic leucine zipper protein VBP partially overlaps those of the C/EBP and CREB/ATF families and is influenced by domains that flank the core basic region. Mol. Cell. Biol. 15, 1923-1932.
19. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Exp. Zool. 88, 49-92.
20. Henderson, C. E., Camu, W., Mettling, C., Gouin, A., Poulsen, K., Karihaloo, M., Rullamas, J., Evans, T., McMahon, S. B., Armanini, M. P. et al. (1993). Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363, 266-270.
21. Henderson, C. E., Phillips, H. S., Pollock, R. A., Davies, A. M., Lemeulle, C., Armanini, M., Simmons, L., Moffet, B., Vandlen, R. A., Simpson, L. C. et al. (1994). GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266 1062-1064.
22. Heumann, R., Goemans, C., Bartsch, D., Lingenhohl, K., Waldmeier, P. C., Hengerer, B., Allegrini, P. R., Schellander, K., Wagner, E. F., Arendt, T. et al. (2000). Transgenic activation of Ras in neurons promotes hypertrophy and protects from lesion-induced degeneration. J. Cell Biol. 151, 1537-1548.
23. Hunger, S. P., Ohyashiki, K., Toyama, K. and Cleary, M. L. (1992). Hlf, a novel hepatic bZIP protein, shows altered DNA-binding properties following fusion to E2A in t(17;19) acute lymphoblastic leukemia. Genes Dev. 6, 1608-1620.
24. Ikushima, S., Inukai, T., Inaba, T., Nimer, S. D., Cleveland, J. L. and Look, A. T. (1997). Pivotal role for the NFIL3/E4BP4 transcription factor in interleukin 3-mediated survival of pro-B lymphocytes. Proc. Natl. Acad. Sci. USA 94, 2609-2614.
25. Inukai, T., Inoue, A., Kurosawa, H., Goi, K., Shinjyo, T., Ozawa, K., Mao, M., Inaba, T. and Look, A. T. (1999). SLUG, a ces-1-related zinc finger transcription factor gene with antiapoptotic activity, is a downstream target of the E2A-HLF oncoprotein. Mol. Cell 4, 343-352.
26. Kuribara, R., Kinoshita, T., Miyajima, A., Shinjyo, T., Yoshihara, T., Inukai, T., Ozawa, K., Look, A. T. and Inaba, T. (1999). Two distinct interleukin-3-mediated signal pathways, Ras-NFIL3 (E4BP4) and Bcl-xL, regulate the survival of murine pro-B lymphocytes. Mol. Cell. Biol. 19, 2754-2762.
27. Kwon, C. H., Zhu, X., Zhang, J., Knoop, L. L., Tharp, R., Smeyne, R. J., Eberhart, C. G., Burger, P. C. and Baker, S. J. (2001 . Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat. Genet. 29, 404-411.
28. Lai, C. K. and Ting, L. P. (1999). Transcriptional repression of human hepatitis B virus genes by a bZIP ANly member, E4BP4. J. Virol. 73, 3197-3209.
29. Lewin, G. R. and Barde, Y. A. (1996). Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
30. Lonze, B. E., Riccio, A., Cohen, S. and Ginty, D. D. (2002). Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34, 371-385.
31. Markus, A., Zhong, J. and Snider, W. D. (2002). Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35 65-76.
32. Metzstein, M. M. and Horvitz, H. R. (1999). The C. elegans cell death specification gene ces-1 encodes a snail family zinc finger protein. Mol. Cell 4, 309-319.
33. Metzstein, M. M., Hengartner, M. O., Tsung, N., Ellis, R. E. and Horvitz, H. R. (1996). Transcriptional regulator of programmed cell death encoded by Caenorhabditis elegans gene ces-2. Nature 382, 545-547.
34. Mitsui, S., Yamaguchi, S., Matsuo, T., Ishida, Y. and Okamura, H. (2001). Antagonistic role of E4BP4 and PAR proteins in the circadian oscillatory mechanism. Genes Dev. 15, 995-1006.
35. Namikawa, K., Honma, M., Abe, K., Takeda, M., Mansur, K., Obata, T., Miwa, A., Okado, H. and Kiyama, H. (2000). Akt/protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration. J. Neurosci. 20, 2875-2886.
36. Nishimune, H., Vasseur, S., Wiese, S., Birling, M. C., Holtmann, B., Sendtner, M., Iovanna, J. L. and Henderson, C. E. (2000). Reg-2 is a motoneuron neurotrophic factor and a signalling intermediate in the CNTF survival pathway. Nat. Cell. Biol. 2 906-914.
37. Oppenheim, R. W. (1991). Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
38. Oppenheim, R. W., Cole, T. and Prevette, D. (1989). Early regional variations in motoneuron numbers arise by differential proliferation in the chick embryo spinal cord. Dev. Biol. 133 468-474.
39. Pettmann, B. and Henderson, C. E. (1998). Neuronal cell death. Neuron 20, 633-647.
40. Raoul, C., Henderson, C. E. and Pettmann, B. (1999). Programmed cell death of embryonic motoneurons triggered through the Fas death receptor. J. Cell Biol. 147, 1049-1062.
41. Raoul, C., Estevez, A. G., Nishimune, H., Cleveland, D. W., deLapeyrière, O., Henderson, C. E., Haase, G. and Pettmann, B. (2002). Motoneuron death triggered by a specific pathway downstream of Fas. potentiation by ALS-linked SOD1 mutations. Neuron 35, 1067-1083.
42. Riccio, A., Ahn, S., Davenport, C. M., Blendy, J. A. and Ginty, D. D. (1999). Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286 2358-2361.
43. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
44. Sulston, J. E. (1983). Neuronal cell lineages in the nematode Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 48, 443-452.
45. Wiese, S., Digby, M. R., Gunnersen, J. M., Gotz, R., Pei, G., Holtmann, B., Lowenthal, J. and Sendtner, M. (1999). The anti-apoptotic protein ITA is essential for NGF-mediated survival of embryonic chick neurons. Nat. Neurosci. 2, 978-983.
46. Yamamoto, Y. and Henderson, C. E. (1999). Patterns of programmed cell death in populations of developing spinal motoneurons in chicken, mouse, and rat. Dev. Biol. 214, 60-71.
47. Zhang, W., Zhang, J., Kornuc, M., Kwan, K., Frank, R. and Nimer, S. D. (1995). Molecular cloning and characterization of NF-IL3A, a transcriptional activator of the human interleukin-3 promoter. Mol. Cell. Biol. 15, 6055-6063.