Evidence that DIF-1 and hyper-osmotic stress activate a Dictyostelium STAT by inhibiting a specific protein tyrosine phosphatase

Development

Volumn 135, Issue 7, 2008, Pages 1347-1353

  Araki, Tsuyoshi ^a   Langenick, Judith ^a   Gamper, Marianne ^b,c   Firtel, Richard A ^b   Williams, Jeffrey G ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Biomedical Research Foundation (SBF)   (Switzerland)

Author keywords

Dictyostelium; DIF 1; STAT; Stress; Tyrosine phosphatase

Indexed keywords

DIFFERENTIATION INDUCING FACTOR; DIFFERENTIATION INDUCING FACTOR 1; PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE 3; SERINE; STAT PROTEIN; STATC PROTEIN; THREONINE;

ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DICTYOSTELIUM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE OVEREXPRESSION; HYPEROSMOTIC STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL NUCLEUS; DICTYOSTELIUM; HEXANONES; MODELS, BIOLOGICAL; OSMOTIC PRESSURE; OXIDATIVE STRESS; PROTEIN TYROSINE PHOSPHATASES; PROTOZOAN PROTEINS; STAT TRANSCRIPTION FACTORS;

DICTYOSTELIUM;

EID: 43049124400     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.009936     Document Type: Article

References (35)

1. Aoki, N. and Matsuda, T. (2000). A cytosolic protein-tyrosine phosphatase PTP1B specifically dephosphorylates and deactivates prolactin-activated STAT5a and STAT5b. J. Biol. Chem. 275, 39718-39726.
2. Araki, T., Gamper, M., Early, A., Fukuzawa, M., Abe, T., Kawata, T., Kim, E., Firtel, R. A. and Williams, J. G. (1998). Developmentally and spatially regulated activation of a Dictyostelium STAT protein by a serpentine receptor. EMBO J. 17, 4018-4028.
3. Araki, T., Tsujioka, M., Abe, T., Fukuzawa, M., Meima, M., Schaap, P., Morio, T., Urushihara, H., Katoh, M., Maeda, M. et al. (2003). A STAT-regulated, stress-induced signalling pathway in Dictyostelium. J. Cell Sci. 116, 2907-2915.
4. Austin, M. B., Saito, T., Bowman, M. E., Haydock, S., Kato, A., Moore, B. S., Kay, R. R. and Noel, J. P. (2006). Biosynthesis of Dictyostelium discoideum differentiation-inducing factor by a hybrid type I fatty acid-type III polyketide synthase. Nat. Chem. Biol. 2, 494-502.
5. Bloomfield, G. and Pears, C. (2003). Superoxide signalling required for multicellular development of Dictyostelium. J. Cell Sci. 116, 3387-3397.
6. Bromberg, J. and Darnell, J. E., Jr (2000). The role of STATs in transcriptional control and their impact on cellular function. Oncogene 19, 2468-2473.
7. Carballo, M., Conde, M., El Bekay, R., Martin-Nieto, J., Camacho, M. J., Monteseirin, J., Conde, J., Bedoya, F. J. and Sobrino, F. (1999). Oxidative stress triggers STAT3 tyrosine phosphorylation and nuclear translocation in human lymphocytes. J. Biol. Chem. 274, 17580-17586.
8. Early, A., Gamper, M., Moniakis, J., Kim, E., Hunter, T., Williams, J. G. and Firtel, R. A. (2001). Protein tyrosine phosphatase PTP1 negatively regulates Dictyostelium STATa and is required for proper cell-type proportioning. Dev. Biol. 232, 233-245.
9. Flint, A. J., Tiganis, T., Barford, D. and Tonks, N. K. (1997). Development of 'substrate-trapping' mutants to identify physiological substrates of protein tyrosine phosphatases. Proc. Natl. Acad. Sci. USA 94, 1680-1685.
10. Fukuzawa, M. and Williams, J. G. (2000). Analysis of the promoter of the cudA gene reveals novel mechanisms of Dictyostelium cell type differentiation. Development 127, 2705-2713.
11. Fukuzawa, M., Araki, T., Adrian, I. and Williams, J. G. (2001). Tyrosine phosphorylation-independent nuclear translocation of a dictyostelium STAT in response to DIF signaling. Mol. Cell 7, 779-788.
12. Fukuzawa, M., Abe, T. and Williams, J. G. (2003). The Dictyostelium prestalk cell inducer DIF regulates nuclear accumulation of a STAT protein by controlling its rate of export from the nucleus. Development 130, 797-804.
13. Gamper, M., Howard, P. K., Hunter, T. and Firtel, R. A. (1996). Multiple roles of the novel protein tyrosine phosphatase PTP3 during Dictyostelium growth and development. Mol. Cell. Biol. 16, 2431-2444.
14. Gamper, M., Kim, E., Howard, P. K., Ma, H., Hunter, T. and Firtel, R. A. (1999). Regulation of Dictyostelium protein-tyrosine phosphatase-3 (PTP3) through osmotic shock and stress stimulation and identification of pp130 as a PTP3 substrate. J. Biol. Chem. 274, 12129-12138.
15. Garton, A. J. and Tonks, N. K. (1994). PTP-PEST: a protein tyrosine phosphatase regulated by serine phosphorylation. EMBO J. 13, 3763-3771.
16. Gatsios, P., Terstegen, L., Schliess, F., Haussinger, D., Kerr, I. M., Heinrich, P. C. and Graeve, L. (1998). Activation of the Janus kinase/signal transducer and activator of transcription pathway by osmotic shock. J. Biol. Chem. 273, 22962-22968.
17. Goldberg, J. M., Manning, G., Liu, A., Fey, P., Pilcher, K. E., Xu, Y. and Smith, J. L. (2006). The dictyostelium kinome-analysis of the protein kinases from a simple model organism. PLoS Genet. 2, e38.
18. Howard, P. K., Sefton, B. M. and Firtel, R. A. (1992). Analysis of a spatially regulated phosphotyrosine phosphatase identifies tyrosine phosphorylation as a key regulatory pathway in Dictyostelium. Cell 71, 637-647.
19. Howard, P. K., Gamper, M., Hunter, T. and Firtel, R. A. (1994). Regulation by protein-tyrosine phosphatase PTP2 is distinct from that by PTP1 during Dictyostelium growth and development. Mol. Cell. Biol. 14, 5154-5164.
20. Huang, E., Blagg, S. L., Keller, T., Katoh, M., Shaulsky, G. and Thompson, C. R. (2006). bZIP transcription factor interactions regulate DIF responses in Dictyostelium. Development 133, 449-458.
21. Liu, T., Castro, S., Brasier, A. R., Jamaluddin, M., Garofalo, R. P. and Casola, A. (2004). Reactive oxygen species mediate virus-induced STAT activation: role of tyrosine phosphatases. J. Biol. Chem. 279, 2461-2469.
22. Madamanchi, N. R., Li, S., Patterson, C. and Runge, M. S. (2001). Reactive oxygen species regulate heat-shock protein 70 via the JAK/STAT pathway. Arterioscler. Thromb. Vasc. Biol. 21, 321-326.
23. Montalibet, J., Skorey, K. I. and Kennedy, B. P. (2005). Protein tyrosine phosphatase: enzymatic assays. Methods 35, 2-8.
24. Pang, K. M., Lynes, M. A. and Knecht, D. A. (1999). Variables controlling the expression level of exogenous genes in Dictyostelium. Plasmid 41, 187-197.
25. Reich, N. C. and Liu, L. (2006). Tracking STAT nuclear traffic. Nat. Rev. Immunol. 6, 602-612.
26. Simon, A. R., Rai, U., Fanburg, B. L. and Cochran, B. H. (1998). Activation of the JAK-STAT pathway by reactive oxygen species. Am. J. Physiol. 275, C1640-C1652.
27. Tanuma, N., Nakamura, K., Shima, H. and Kikuchi, K. (2000). Protein-tyrosine phosphatase PTPepsilon C inhibits Jak-STAT signaling and differentiation induced by interleukin-6 and leukemia inhibitory factor in M1 leukemia cells. J. Biol. Chem. 275, 28216-28221.
28. ten Hoeve, J., de Jesus Ibarra-Sanchez, M., Fu, Y., Zhu, W., Tremblay, M., David, M. and Shuai, K. (2002). Identification of a nuclear Stat1 protein tyrosine phosphatase. Mol. Cell. Biol. 22, 5662-5668.
29. Thompson, C. R. and Kay, R. R. (2000). The role of DIF-1 signaling in Dictyostelium development. Mol. Cell 6, 1509-1514.
30. Tonks, N. K. (2005). Redox redux: revisiting PTPs and the control of cell signaling. Cell 121, 667-670.
31. Watts, D. J. and Ashworth, J. M. (1970). Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem. J. 119, 171-174.
32. Williams, J. G. (2003). The STAT proteins of Dictyostelium. In Signal Transducers and Activators of Transcription (STATs): Activation and Biology (ed P. B. Sehgal, D. E. Levy and T. Hirano), pp. 105-121. Boston: Kluwer Academic Publishers.
33. Yu, C. L., Jin, Y. J. and Burakoff, S. J. (2000). Cytosolic tyrosine dephosphorylation of STAT5. Potential role of SHP-2 in STAT5 regulation. J. Biol. Chem. 275, 599-604.
34. Yudushkin, I. A., Schleifenbaum, A., Kinkhabwala, A., Neel, B. G., Schultz, C. and Bastiaens, P. I. (2007). Live-cell imaging of enzyme-substrate interaction reveals spatial regulation of PTP1B. Science 315, 115-119.
35. Zhukovskaya, N. V., Fukuzawa, M., Yamada, Y., Araki, T. and Williams, J. G. (2006). The Dictyostelium bZIP transcription factor DimB regulates prestalk-specific gene expression. Development 133, 439-448.