Reciprocal regulation of the basic helix-loop-helix/Per-Arnt-Sim partner proteins, Arnt and Arnt2, during neuronal differentiation

Nucleic Acids Research

Volumn 41, Issue 11, 2013, Pages 5626-5638

  Hao, Nan ^a   Bhakti, Veronica L D ^a   Peet, Daniel J ^a   Whitelaw, Murray L ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HISTONE H3; HYPOXIA INDUCIBLE FACTOR 1BETA; MESSENGER RNA; PROTEIN ARNT2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; EMBRYO; EMBRYONAL CARCINOMA; EMBRYONIC STEM CELL; GC RICH SEQUENCE; GENE EXPRESSION; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METHYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE, TUMOR; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; MICE; NEUROGENESIS; NEURONS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84878820408     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt206     Document Type: Article

References (49)

1. McIntosh, B.E., Hogenesch, J.B. and Bradfield, C.A. (2010) Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu. Rev. Physiol., 72, 625-645.
2. Furness, S.G., Lees, M.J. and Whitelaw, M.L. (2007) The dioxin (aryl hydrocarbon) receptor as a model for adaptive responses of bHLH/PAS transcription factors. FEBS Lett., 581, 3616-3625.
3. Antonsson, C., Arulampalam, V., Whitelaw, M.L., Pettersson, S. and Poellinger, L. (1995) Constitutive function of the basic helix-loophelix/PAS factor Arnt. Regulation of target promoters via the E box motif. J. Biol. Chem., 270, 13968-13972.
4. Sogawa, K., Nakano, R., Kobayashi, A., Kikuchi, Y., Ohe, N., Matsushita, N. and Fujii-Kuriyama, Y. (1995) Possible function of Ah receptor nuclear translocator (Arnt) homodimer in transcriptional regulation. Proc. Natl Acad. Sci. USA, 92, 1936-1940.
5. Kewley, R.J., Whitelaw, M.L. and Chapman-Smith, A. (2004) The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. Int. J. Biochem. Cell Biol., 36, 189-204.
6. Wang, F., Shi, S., Zhang, R. and Hankinson, O. (2006) Identifying target genes of the aryl hydrocarbon receptor nuclear translocator (Arnt) using DNA microarray analysis. Biol. Chem., 387, 1215-1218.
7. Hirose, K., Morita, M., Ema, M., Mimura, J., Hamada, H., Fujii, H., Saijo, Y., Gotoh, O., Sogawa, K. and Fujii-Kuriyama, Y. (1996) cDNA cloning and tissue-specific expression of a novel basic helix-loop-helix/PAS factor (Arnt2) with close sequence similarity to the aryl hydrocarbon receptor nuclear translocator (Arnt). Mol. Cell. Biol., 16, 1706-1713.
8. Jain, S., Maltepe, E., Lu, M.M., Simon, C. and Bradfield, C.A. (1998) Expression of ARNT, ARNT2, HIF1 alpha, HIF2 alpha and Ah receptor mRNAs in the developing mouse. Mech. Dev., 73, 117-123.
9. Aitola, M.H. and Pelto-Huikko, M.T. (2003) Expression of Arnt and Arnt2 mRNA in developing murine tissues. J. Histochem. Cytochem., 51, 41-54.
10. Dougherty, E.J. and Pollenz, R.S. (2008) Analysis of Ah receptor-ARNT and Ah receptor-ARNT2 complexes in vitro and in cell culture. Toxicol. Sci., 103, 191-206.
11. Freeburg, P.B. and Abrahamson, D.R. (2004) Divergent expression patterns for hypoxia-inducible factor-1beta and aryl hydrocarbon receptor nuclear transporter-2 in developing kidney. J. Am. Soc. Nephrol., 15, 2569-2578.
12. Martinez, V., Kennedy, S., Doolan, P., Gammell, P., Joyce, H., Kenny, E., Prakash Mehta, J., Ryan, E., O'Connor, R., Crown, J. et al. (2008) Drug metabolism-related genes as potential biomarkers: analysis of expression in normal and tumour breast tissue. Breast Cancer Res. Treat., 110, 521-530.
13. Golling, G., Amsterdam, A., Sun, Z., Antonelli, M., Maldonado, E., Chen, W., Burgess, S., Haldi, M., Artzt, K., Farrington, S. et al. (2002) Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat. Genet., 31, 135-140.
14. Hill, A.J., Heiden, T.C., Heideman, W. and Peterson, R.E. (2009) Potential roles of Arnt2 in zebrafish larval development. Zebrafish, 6, 79-91.
15. Hosoya, T., Oda, Y., Takahashi, S., Morita, M., Kawauchi, S., Ema, M., Yamamoto, M. and Fujii-Kuriyama, Y. (2001) Defective development of secretory neurones in the hypothalamus of Arnt2-knockout mice. Genes Cells, 6, 361-374.
16. Keith, B., Adelman, D.M. and Simon, M.C. (2001) Targeted mutation of the murine arylhydrocarbon receptor nuclear translocator 2 (Arnt2) gene reveals partial redundancy with Arnt. Proc. Natl Acad. Sci. USA, 98, 6692-6697.
17. Michaud, J.L., DeRossi, C., May, N.R., Holdener, B.C. and Fan, C.M. (2000) ARNT2 acts as the dimerization partner of SIM1 for the development of the hypothalamus. Mech. Dev., 90, 253-261.
18. Ooe, N., Saito, K., Mikami, N., Nakatuka, I. and Kaneko, H. (2004) Identification of a novel basic helix-loop-helix-PAS factor, NXF, reveals a Sim2 competitive, positive regulatory role in dendriticcytoskeleton modulator drebrin gene expression. Mol. Cell. Biol., 24, 608-616.
19. Ooe, N., Saito, K. and Kaneko, H. (2009) Characterization of functional heterodimer partners in brain for a bHLH-PAS factor NXF. Biochim. Biophys. Acta, 1789, 192-197.
20. Woods, S.L. and Whitelaw, M.L. (2002) Differential activities of murine single minded 1 (SIM1) and SIM2 on a hypoxic response element. Cross-talk between basic helix-loop-helix/per-Arnt-Sim homology transcription factors. J. Biol. Chem., 277, 10236-10243.
21. Maltepe, E., Schmidt, J.V., Baunoch, D., Bradfield, C.A. and Simon, M.C. (1997) Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature, 386, 403-407.
22. Kozak, K.R., Abbott, B. and Hankinson, O. (1997) ARNT-deficient mice and placental differentiation. Dev. Biol., 191, 297-305.
23. Iyer, N.V., Kotch, L.E., Agani, F., Leung, S.W., Laughner, E., Wenger, R.H., Gassmann, M., Gearhart, J.D., Lawler, A.M., Yu, A.Y. et al. (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev., 12, 149-162.
24. Ryan, H.E., Lo, J. and Johnson, R.S. (1998) HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J., 17, 3005-3015.
25. Michaud, J.L., Rosenquist, T., May, N.R. and Fan, C.M. (1998) Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. Genes Dev., 12, 3264-3275.
26. Maltepe, E., Keith, B., Arsham, A.M., Brorson, J.R. and Simon, M.C. (2000) The role of ARNT2 in tumor angiogenesis and the neural response to hypoxia. Biochem. Biophys. Res. Commun., 273, 231-238.
27. Sekine, H., Mimura, J., Yamamoto, M. and Fujii-Kuriyama, Y. (2006) Unique and overlapping transcriptional roles of arylhydrocarbon receptor nuclear translocator (Arnt) and Arnt2 in xenobiotic and hypoxic responses. J. Biol. Chem., 281, 37507-37516.
28. Jones-Villeneuve, E.M., McBurney, M.W., Rogers, K.A. and Kalnins, V.I. (1982) Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J. Cell Biol., 94, 253-262.
29. Ying, Q.L., Stavridis, M., Griffiths, D., Li, M. and Smith, A. (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol., 21, 183-186.
30. Hao, N., Whitelaw, M.L., Shearwin, K.E., Dodd, I.B. and Chapman-Smith, A. (2011) Identification of residues in the N-terminal PAS domains important for dimerization of Arnt and AhR. Nucleic Acids Res., 39, 3695-3709.
31. Clark, S.J., Harrison, J., Paul, C.L. and Frommer, M. (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Res., 22, 2990-2997.
32. Hao, N., Lee, K.L., Furness, S.G., Bosdotter, C., Poellinger, L. and Whitelaw, M.L. (2012) Xenobiotics and loss of cell adhesion drive distinct transcriptional outcomes by aryl hydrocarbon receptor signaling. Molecular pharmacology, 82, 1082-1093.
33. Belsham, D.D., Cai, F., Cui, H., Smukler, S.R., Salapatek, A.M. and Shkreta, L. (2004) Generation of a phenotypic array of hypothalamic neuronal cell models to study complex neuroendocrine disorders. Endocrinology, 145, 393-400.
34. McBurney, M.W., Jones-Villeneuve, E.M., Edwards, M.K. and Anderson, P.J. (1982) Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature, 299, 165-167.
35. Valouev, A., Johnson, D.S., Sundquist, A., Medina, C., Anton, E., Batzoglou, S., Myers, R.M. and Sidow, A. (2008) Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat. Methods, 5, 829-834.
36. Schoenherr, C.J. and Anderson, D.J. (1995) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science, 267, 1360-1363.
37. Chong, J.A., Tapia-Ramirez, J., Kim, S., Toledo-Aral, J.J., Zheng, Y., Boutros, M.C., Altshuller, Y.M., Frohman, M.A., Kraner, S.D. and Mandel, G. (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell, 80, 949-957.
38. Hatada, I., Morita, S., Kimura, M., Horii, T., Yamashita, R. and Nakai, K. (2008) Genome-wide demethylation during neural differentiation of P19 embryonal carcinoma cells. J. Hum. Genet., 53, 185-191.
39. Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 125, 315-326.
40. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jorgensen, H.F., John, R.M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M. et al. (2006) Chromatin signatures of pluripotent cell lines. Nat. Cell Biol., 8, 532-538.
41. Mikkelsen, T.S., Ku, M., Jaffe, D.B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.K., Koche, R.P. et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature, 448, 553-560.
42. Drutel, G., Heron, A., Kathmann, M., Gros, C., Mace, S., Plotkine, M., Schwartz, J.C. and Arrang, J.M. (1999) ARNT2, a transcription factor for brain neuron survival? Eur. J. Neurosci., 11, 1545-1553.
43. Yamakuchi, M., Lotterman, C.D., Bao, C., Hruban, R.H., Karim, B., Mendell, J.T., Huso, D. and Lowenstein, C.J. (2010) P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc. Natl Acad. Sci. USA, 107, 6334-6339.
44. Hoesel, B., Bhujabal, Z., Przemeck, G.K., Kurz-Drexler, A., Weisenhorn, D.M., Angelis, M.H. and Beckers, J. (2010) Combination of in silico and in situ hybridisation approaches to identify potential Dll1 associated miRNAs during mouse embryogenesis. Gene Expr. Patterns, 10, 265-273.
45. Huang, X., Powell-Coffman, J.A. and Jin, Y. (2004) The AHR-1 aryl hydrocarbon receptor and its co-factor the AHA-1 aryl hydrocarbon receptor nuclear translocator specify GABAergic neuron cell fate in C. elegans. Development, 131, 819-828.
46. Kim, M.D., Jan, L.Y. and Jan, Y.N. (2006) The bHLH-PAS protein Spineless is necessary for the diversification of dendrite morphology of Drosophila dendritic arborization neurons. Genes Dev., 20, 2806-2819.
47. Latchney, S.E., Hein, A.M., Kerry O'Banion, M., Dicicco-Bloom, E. and Opanashuk, L.A. (2013) Deletion or activation of the Aryl hydrocarbon receptor (AhR) alters adult hippocampal neurogenesis and contextual fear memory. J Neurochem., 125, 430-445.
48. Hankinson, O. (2008) Why does ARNT2 behave differently from ARNT? Toxicol. Sci., 103, 1-3.
49. Kawajiri, K., Kobayashi, Y., Ohtake, F., Ikuta, T., Matsushima, Y., Mimura, J., Pettersson, S., Pollenz, R.S., Sakaki, T., Hirokawa, T. et al. (2009) Aryl hydrocarbon receptor suppresses intestinal carcinogenesis in ApcMin/+mice with natural ligands. Proc. Natl Acad. Sci. USA, 106, 13481-13486.