Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer

Science

Volumn 343, Issue 6177, 2014, Pages

  Cai, Huaqing ^a   Katoh Kurasawa, Mariko ^b   Muramoto, Tetsuya ^c   Santhanam, Balaji ^b   Long, Yu ^a   Li, Lei ^d   Ueda, Masahiro ^c,e   Iglesias, Pablo A ^a,f   Shaulsky, Gad ^b   Devreotes, Peter N ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c RIKEN   (Japan)

^d UNIVERSITY OF VIRGINIA   (United States)

^e OSAKA UNIVERSITY   (Japan)

^f Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; GLYCOGEN SYNTHASE KINASE; GUANINE NUCLEOTIDE BINDING PROTEIN; RESTRICTION ENDONUCLEASE; TRANSCRIPTION FACTOR GATA; G PROTEIN COUPLED RECEPTOR; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PROTOZOAL PROTEIN;

CELL ORGANELLE; GENE EXPRESSION; PROTEIN; PROTOZOAN;

ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL SUSPENSION; DEVELOPMENTAL GENE; DICTYOSTELIUM DISCOIDEUM; GENE DELETION; GENE EXPRESSION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOCYTOPLASMIC TRANSPORT; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR OCCUPANCY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEADY STATE; ZINC FINGER MOTIF; ACTIVE TRANSPORT; CELL NUCLEUS; CHEMISTRY; CYTOPLASM; DICTYOSTELIUM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; CYCLIC AMP; CYTOPLASM; DICTYOSTELIUM; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HETEROTRIMERIC GTP-BINDING PROTEINS; NUCLEAR LOCALIZATION SIGNALS; PHOSPHORYLATION; PROTOZOAN PROTEINS; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84896912620     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1249531     Document Type: Article

References (40)

1. P. E. Belchetz, T. M. Plant, Y. Nakai, E. J. Keogh, E. Knobil, Hypophysial responses to continuous and intermittent delivery of hypopthalamic gonadotropin-releasing hormone. Science 202, 631-633 (1978). doi: 10.1126/science.100883; pmid: 100883
2. H. Shimojo, T. Ohtsuka, R. Kageyama, Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52-64 (2008). doi: 10.1016/j.neuron.2008.02.014; pmid: 18400163
3. J. Mauelshagen, C. M. Sherff, T. J. Carew, Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica. Learn. Mem. 5, 246-256 (1998). pmid: 10454368
4. D. S. Barkley, Adenosine-3′,5′-phosphate: Identification as acrasin in a species of cellular slime mold. Science 165, 1133-1134 (1969). doi: 10.1126/science.165.3898.1133; pmid: 4308325
5. T. M. Konijn, Y. Y. Chang, J. T. Bonner, Synthesis of cyclic AMP in Dictyostelium discoideum and Polysphondylium pallidum. Nature 224, 1211-1212 (1969). doi: 10.1038/2241211a0; pmid: 4311588
6. N. Van Driessche et al., A transcriptional profile of multicellular development in Dictyostelium discoideum. Development 129, 1543-1552 (2002). pmid: 11923193
7. N. Iranfar, D. Fuller, W. F. Loomis, Genome-wide expression analyses of gene regulation during early development of Dictyostelium discoideum. Eukaryot. Cell 2, 664-670 (2003). doi: 10.1128/EC.2.4.664-670.2003; pmid: 12912885
8. G. Gerisch, B. Hess, Cyclic-AMP-controlled oscillations in suspended Dictyostelium cells: Their relation to morphogenetic cell interactions. Proc. Natl. Acad. Sci. U.S.A. 71, 2118-2122 (1974). doi: 10.1073/pnas.71.5.2118; pmid: 4365764
9. C. Rossier, G. Gerisch, D. Malchow, Action of a slowly hydrolysable cyclic AMP analogue on developing cells of Dictyostelium discoideum. J. Cell Sci. 35, 321-338 (1979). pmid: 217886
10. A. Kuspa, Restriction enzyme-mediated integration (REMI) mutagenesis. Methods Mol. Biol. 346, 201-209 (2006). pmid: 16957292
11. H. Otsuka, P. J. Van Haastert, A novel Myb homolog initiates Dictyostelium development by induction of adenylyl cyclase expression. Genes Dev. 12, 1738 -1748 (1998). doi: 10.1101/gad.12.11.1738; pmid: 9620859
12. C. J. Lim, G. B. Spiegelman, G. Weeks, RasC is required for optimal activation of adenylyl cyclase and Akt/PKB during aggregation. EMBO J. 20, 4490-4499 (2001). doi: 10.1093/emboj/20.16.4490; pmid: 11500376
13. K. J. Tomchik, P. N. Devreotes, Adenosine 3′,5′-monophosphate waves in Dictyostelium discoideum: A demonstration by isotope dilution-fluorography. Science 212, 443-446 (1981). doi: 10.1126/science. 6259734; pmid: 6259734
14. P. N. Devreotes, M. J. Potel, S. A. MacKay, Quantitative analysis of cyclic AMP waves mediating aggregation in Dictyostelium discoideum. Dev. Biol. 96, 405 -415 (1983). doi: 10.1016/0012-1606(83)90178-1; pmid: 6299820
15. F. Alcantara, M. Monk, Signal propagation during aggregation in the slime mould Dictyostelium discoideum. J. Gen. Microbiol. 85, 321-334 (1974). doi: 10.1099/00221287-85-2-321; pmid: 4615133
16. B. Wurster, U. Butz, A study on sensing and adaptation in Dictyostelium discoideum: Guanosine 3′,5′-phosphate accumulation and light-scattering responses. J. Cell Biol. 96, 1566-1570 (1900). doi: 10.1083/jcb.96.6.1566; pmid: 6304110
17. G. Lahav et al., Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat. Genet. 36, 147-150 (2004). doi: 10.1038/ng1293; pmid: 14730303
18. D. E. Nelson et al., Oscillations in NF-κB signaling control the dynamics of gene expression. Science 306, 704-708 (2004). doi: 10.1126/science.1099962; pmid: 15499023
19. A. Hoffmann, A. Levchenko, M. L. Scott, D. Baltimore, The IκB-NF-κB signaling module: Temporal control and selective gene activation. Science 298, 1241-1245 (2002). doi: 10.1126/science.1071914; pmid: 12424381
20. H. Hirata et al., Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 298, 840-843 (2002). doi: 10.1126/science.1074560; pmid: 12399594
21. R. Teo et al., Glycogen synthase kinase-3 is required for efficient Dictyostelium chemotaxis. Mol. Biol. Cell 21, 2788-2796 (2010). doi: 10.1091/mbc.E09-10-0891; pmid: 20534815
22. A. Parikh et al., Conserved developmental transcriptomes in evolutionarily divergent species. Genome Biol. 11, R35 (2010). doi: 10.1186/gb-2010-11-3-r35; pmid: 20236529
23. J. R. Chubb, T. Trcek, S. M. Shenoy, R. H. Singer, Transcriptional pulsing of a developmental gene. Curr. Biol. 16, 1018-1025 (2006). doi: 10.1016/j.cub.2006.03.092; pmid: 16713960
24. T. Muramoto et al., Live imaging of nascent RNA dynamics reveals distinct types of transcriptional pulse regulation. Proc. Natl. Acad. Sci. U.S.A. 109, 7350-7355 (2012). doi: 10.1073/pnas.1117603109; pmid: 22529358
25. D. Dormann, G. Weijer, C. A. Parent, P. N. Devreotes, C. J. Weijer, Visualizing PI3 kinase-mediated cell-cell signaling during Dictyostelium development. Curr. Biol. 12, 1178-1188 (2002). doi: 10.1016/S0960-9822(02)00950- 8; pmid: 12176327
26. I. Imayoshi et al., Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342, 1203- 1208 (2013). doi: 10.1126/science.1242366; pmid: 24179156
27. N. Hao, B. A. Budnik, J. Gunawardena, E. K. O'Shea, Tunable signal processing through modular control of transcription factor translocation. Science 339, 460-464 (2013). pmid: 23349292
28. J. E. Purvis et al., p53 dynamics control cell fate. Science 336, 1440-1444 (2012). doi: 10.1126/science.1218351; pmid: 22700930
29. R. E. Dolmetsch, K. L. Xu, R. S. Lewis, Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933 -936 (1998). doi: 10.1038/31960; pmid: 9582075
30. L. Cai, C. K. Dalal, M. B. Elowitz, Frequency-modulated nuclear localization bursts coordinate gene regulation. Nature 455, 485-490 (2008). doi: 10.1038/nature07292; pmid: 18818649
31. D. A. Stavreva et al., Ultradian hormone stimulation induces glucocorticoid receptor-mediated pulses of gene transcription. Nat. Cell Biol. 11, 1093-1102 (2009). doi: 10.1038/ncb1922; pmid: 19684579
32. H. Cai, C. H. Huang, P. N. Devreotes, M. Iijima, Analysis of chemotaxis in Dictyostelium. Methods Mol. Biol. 757, 451-468 (2012). doi: 10.1007/978-1-61779-166-6-26; pmid: 21909927
33. J. Faix, L. Kreppel, G. Shaulsky, M. Schleicher, A. R. Kimmel, A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Res. 32, e143 (2004). doi: 10.1093/nar/gnh136; pmid: 15507682
34. D. M. Veltman, I. Keizer-Gunnink, P. J. Haastert, An extrachromosomal, inducible expression system for Dictyostelium discoideum. Plasmid 61, 119- 125 (2009). doi: 10.1016/j.plasmid.2008.11.003; pmid: 19046986
35. Y. Artemenko, K. F. Swaney, P. N. Devreotes, Assessment of development and chemotaxis in Dictyostelium discoideum mutants. Methods Mol. Biol. 769, 287-309 (2011). doi: 10.1007/978-1-61779-207-6-20; pmid: 21748684
36. H. Cai et al., Ras-mediated activation of the TORC2-PKB pathway is critical for chemotaxis. J. Cell Biol. 190, 233-245 (2010). pmid: 20660630
37. E. Huang et al., BzpF is a CREB-like transcription factor that regulates spore maturation and stability in Dictyostelium . Dev. Biol. 358, 137-146 (2011). doi: 10.1016/j.ydbio.2011.07.017; pmid: 21810415
38. T. J. Hardcastle, K. A. Kelly, baySeq: Empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinformatics 11, 422 (2010). doi: 10.1186/1471-2105-11-422; pmid: 20698981
39. Z. Xiao, Y. Yao, Y. Long, P. Devreotes, Desensitization of G-protein-coupled receptors. agonist-induced phosphorylation of the chemoattractant receptor cAR1 lowers its intrinsic affinity for cAMP. J. Biol. Chem. 274, 1440-1448 (1999). doi: 10.1074/jbc.274.3.1440; pmid: 9880518
40. S. Bader, A. Kortholt, P. J. Van Haastert, Seven Dictyostelium discoideum phosphodiesterases degrade three pools of cAMP and cGMP. Biochem. J. 402, 153-161 (2007). doi: 10.1042/BJ20061153; pmid: 17040207