Regulation of sprouty stability by Mnk1-dependent phosphorylation

Molecular and Cellular Biology

Volumn 26, Issue 5, 2006, Pages 1898-1907

  DaSilva, John ^a   Xu, Lizhong ^a   Kim, Hong Joo ^a   Miller, W Todd ^a   Bar Sagi, Dafna ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CBL PROTEIN; FIBROBLAST GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INTERACTING KINASE 1; PHOSPHATASE; PHOSPHOTRANSFERASE; REGULATOR PROTEIN; SERINE; SPROUTY PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; ENZYME INHIBITION; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; UBIQUITINATION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FIBROBLAST GROWTH FACTORS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; PROTO-ONCOGENE PROTEINS C-CBL; SERINE; TYROSINE;

ANIMALIA; DROSOPHILA MELANOGASTER; MAMMALIA;

EID: 33644521566     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.5.1898-1907.2006     Document Type: Article

References (66)

1. Antoine, M., W. Wirz, C. G. Tag, M. Mavituna, N. Emans, T. Korff, V. Stoldt, A. M. Gressner, and P. Kiefer. 2005. Expression pattern of fibroblast growth factors (FGFs), their receptors and antagonists in primary endothelial cells and vascular smooth muscle cells. Growth Factors 23:87-95.
2. Arquier, N., M. Bourouis, J. Colombani, and P. Leopold. 2005. Drosophila Lk6 kinase controls phosphorylation of eukaryotic translation initiation factor 4E and promotes normal growth and development. Curr. Biol. 15:19-23.
3. MAPK-dependent phosphorylation. Science 286:2514-2517.
4. Buxade, M., J. L. Parra, S. Rousseau, N. Shpiro, R. Marquez, N. Morrice, J. Bain, E. Espel, and C. G. Proud. 2005. The Mnks are novel components in the control of TNFα biosynthesis and phosphorylate and regulate hnRNP A1. Immunity 23:177-189.
5. Casci, T., J. Vinos, and M. Freeman. 1999. Sprouty, an intracellular inhibitor of Ras signaling. Cell 96:655-665.
6. Chi, L., S. Zhang, Y. Lin, R. Prunskaite-Hyyrylainen, R. Vuolteenaho, P. Itaranta, and S. Vainio. 2004. Sprouty proteins regulate ureteric branching by coordinating reciprocal epithelial Wnt11, mesenchymal Gdnf and stromal Fgf7 signalling during kidney development. Development 131:3345-3356.
7. de Alvaro, C., N. Martinez, J. M. Rojas, and M. Lorenzo. 2005. Sprouty-2 overexpression in C2C12 cells confers myogenic differentiation properties in the presence of FGF2. Mol. Biol. Cell 16:4454-4461.
8. de Maximy, A. A., Y. Nakatake, S. Moncada, N. Itoh, J. P. Thiery, and S. Bellusci. 1999. Cloning and expression pattern of a mouse homologue of Drosophila sprouty in the mouse embryo. Mech. Dev. 81:213-216.
9. Egan, J. E., A. B. Hall, B. A. Yatsula, and D. Bar-Sagi. 2002. The bimodal regulation of epidermal growth factor signaling by human Sprouty proteins. Proc. Natl. Acad. Sci. USA 99:6041-6046.
10. Favre, B., P. Turowski, and B. A. Hemmings. 1997. Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin. J. Biol. Chem. 272:13856-13863.
11. Fiorini, M., M. Alimandi, L. Florentino, G. Sala, and O. Segatto. 2001. Negative regulation of receptor tyrosine kinase signals. FEBS Lett. 490:132-141.
12. Fong, C. W., H. F. Leong, E. S. Wong, J. Lim, P. Yusoff, and G. R. Guy. 2003. Tyrosine phosphorylation of Sprouty2 enhances its interaction with c-Cbl and is crucial for its function. J. Biol. Chem. 278:33456-33464.
13. Freeman, M. 2000. Feedback control of intercellular signalling in development. Nature 408:313-319.
14. Fukunaga, R., and T. Hunter. 1997. MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J. 16:1921-1933.
15. Gross, I., B. Bassit, M. Benezra, and J. D. Licht. 2001. Mammalian sprouty proteins inhibit cell growth and differentiation by preventing ras activation. J. Biol. Chem. 276:46460-46468.
16. Guy, G. R., E. S. Wong, P. Yusoff, S. Chandramouli, T. L. Lo, J. Lim, and C. W. Fong. 2003. Sprouty: how does the branch manager work? J. Cell Sci. 116:3061-3068.
17. Hacohen, N., S. Kramer, D. Sutherland, Y. Hiromi, and M. A. Krasnow. 1998. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92:253-263.
18. Hall, A. B., N. Jura, J. DaSilva, Y. J. Jang, D. Gong, and D. Bar-Sagi. 2003. hSpry2 is targeted to the ubiquitin-dependent proteasome pathway by c-Cbl. Curr. Biol. 13:308-314.
19. Hanafusa, H., S. Torii, T. Yasunaga, K. Matsumoto, and E. Nishida. 2004. Shp2, an SH2-containing protein-tyrosine phosphatase, positively regulates receptor tyrosine kinase signaling by dephosphorylating and inactivating the inhibitor Sprouty. J. Biol. Chem. 279:22992-22995.
20. Hanafusa, H., S. Torii, T. Yasunaga, and E. Nishida. 2002. Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4:850-858.
21. Hefner, Y., A. G. Borsch-Haubold, M. Murakami, J. I. Wilde, S. Pasquet, D. Schieltz, F. Ghomashchi, J. R. Yates III, C. G. Armstrong, A. Paterson, P. Cohen, R. Fukunaga, T. Hunter, I. Kudo, S. P. Watson, and M. H. Gelb. 2000. Serine 727 phosphorylation and activation of cytosolic phospholipase A2 by MNK1-related protein kinases. J. Biol. Chem. 275:37542-37551.
22. Huang, A. M., and G. M. Rubin. 2000. A misexpression screen identifies genes that can modulate RAS1 pathway signaling in Drosophila melanogaster. Genetics 156:1219-1230.
23. Impagnatiello, M. A., S. Weitzer, G. Gannon, A. Compagni, M. Cotten, and G. Christofori. 2001. Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J. Cell Biol. 152:1087-1098.
24. Janssens, V., and J. Goris. 2001. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J. 353:417-439.
25. Kidd, D., and J. W. Raff. 1997. LK6, a short lived protein kinase in Drosophila that can associate with microtubules and centrosomes. J. Cell Sci. 110: 209-219.
26. Kim, H. J., and D. Bar-Sagi. 2004. Modulation of signalling by Sprouty: a developing story. Nat. Rev. Mol. Cell. Biol. 5:441-450.
27. Knauf, U., C. Tschopp, and H. Gram. 2001. Negative regulation of protein translation by mitogen-activated protein kinase-interacting kinases 1 and 2. Mol. Cell. Biol. 21:5500-5511.
28. Kramer, S., M. Okabe, N. Hacohen, M. A. Krasnow, and Y. Hiromi. 1999. Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126:2515-2525.
29. Lee, C. C., A. J. Putnam, C. K. Miranti, M. Gustafson, L. M. Wang, G. F. Vande Woude, and C. F. Gao. 2004. Overexpression of sprouty 2 inhibits HGF/SF-mediated cell growth, invasion, migration, and cytokinesis. Oncogene 23:5193-5202.
30. Li, X., V. G. Brunton, H. R. Burgar, L. M. Wheldon, and J. K. Heath. 2004. FRS2-dependent SRC activation is required for fibroblast growth factor receptor-induced phosphorylation of Sprouty and suppression of ERK activity. J. Cell Sci. 117:6007-6017.
31. Cip/WAF1 and promotes cell survival. J. Biol. Chem. 277:11352-11361.
32. Mailleux, A. A., D. Tefft, D. Ndiaye, N. Itoh, J. P. Thiery, D. Warburton, and S. Bellusci. 2001. Evidence that SPROUTY2 functions as an inhibitor of mouse embryonic lung growth and morphogenesis. Mech. Dev. 102:81-94.
33. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
34. Mason, J. M., D. J. Morrison, B. Bassit, M. Dimri, H. Band, J. D. Licht, and I. Gross. 2004. Tyrosine phosphorylation of Sprouty proteins regulates their ability to inhibit growth factor signaling: a dual feedback loop. Mol. Biol. Cell 15:2176-2188.
35. Minowada, G., L. A. Jarvis, C. L. Chi, A. Neubuser, X. Sun, N. Hacohen, M. A. Krasnow, and G. R. Martin. 1999. Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126:4465-4475.
36. Okazaki, K., and N. Sagata. 1995. The Mos/MAP kinase pathway stabilizes c-Fos by phosphorylation and augments its transforming activity in NIH 3T3 cells. EMBO J. 14:5048-5059.
37. Ory, S., M. Zhou, T. P. Conrads, T. D. Veenstra, and D. K. Morrison. 2003. Protein phosphatase 2A positively regulates Ras signaling by dephosphorylating KSR1 and Raf-1 on critical 14-3-3 binding sites. Curr. Biol. 13:1356-1364.
38. Ozaki, K., R. Kadomoto, K. Asato, S. Tanimura, N. Itoh, and M. Kohno. 2001. ERK pathway positively regulates the expression of Sprouty genes. Biochem. Biophys. Res. Commun. 285:1084-1088.
39. Parra-Palau, J. L., G. C. Scheper, D. E. Harper, and C. G. Proud. 2005. The Drosophila protein kinase LK6 is regulated by ERK and phosphorylates the eukaryotic initiation factor eIF4E in vivo. Biochem. J. 385:695-702.
40. Pinna, L. A., and M. Ruzzene. 1996. How do protein kinases recognize their substrates? Biochim. Biophys. Acta 1314:191-225.
41. Pouyssegur, J., V. Volmat, and P. Lenormand. 2002. Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling. Biochem. Pharmacol. 64:755-763.
42. Rebay, I. 2002. Keeping the receptor tyrosine kinase signaling pathway in check: lessons from Drosophila. Dev. Biol. 251:1-17.
43. Reich, A., A. Sapir, and B. Shilo. 1999. Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 126:4139-4147.
44. Reiling, J. H., K. T. Doepfner, E. Hafen, and H. Stocker. 2005. Diet-dependent effects of the Drosophila Mnk1/Mnk2 homolog Lk6 on growth via eIF4E. Curr. Biol. 15:24-30.
45. Roux, P. P., and J. Blenis. 2004. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68:320-344.
46. Rubin, C., G. Gur, and Y. Yarden. 2005. Negative regulation of receptor tyrosine kinases: unexpected links to c-Cbl and receptor ubiquitylation. Cell Res. 15:66-71.
47. Rubin, C., V. Litvak, H. Medvedovsky, Y. Zwang, S. Lev, and Y. Yarden. 2003. Sprouty fine-tunes EGF signaling through interlinked positive and negative feedback loops. Curr. Biol. 13:297-307.
48. Rubin, C., Y. Zwang, N. Vaisman, D. Ron, and Y. Yarden. 2005. Phosphorylation of carboxyl-terminal tyrosines modulates the specificity of Sprouty-2 inhibition of different signaling pathways. J. Biol. Chem. 280:9735-9744.
49. Sasaki, A., T. Taketomi, R. Kato, K. Saeki, A. Nonami, M. Sasaki, M. Kuriyama, N. Saito, M. Shibuya, and A. Yoshimura. 2003. Mammalian Sprouty4 suppresses Ras-independent ERK activation by binding to Raf1. Nat. Cell Biol. 5:427-432.
50. Sasaki, A., T. Taketomi, T. Wakioka, R. Kato, and A. Yoshimura. 2001. Identification of a dominant negative mutant of Sprouty that potentiates fibroblast growth factor- but not epidermal growth factor-induced ERK activation. J. Biol. Chem. 276:36804-36808.
51. Schlessinger, J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103: 211-225.
52. Shilo, B. Z. 2003. Signaling by the Drosophila epidermal growth factor receptor pathway during development. Exp. Cell Res. 284:140-149.
53. Shim, K., G. Minowada, D. E. Coling, and G. R. Martin. 2005. Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev. Cell 8:553-564.
54. Sieburth, D. S., M. Sundaram, R. M. Howard, and M. Han. 1999. A PP2A regulatory subunit positively regulates Ras-mediated signaling during Caenorhabditis elegans vulval induction. Genes Dev. 13:2562-2569.
55. Strutt, H., and D. Strutt. 2003. EGF signaling and ommatidial rotation in the Drosophila eye. Curr. Biol. 13:1451-1457.
56. Sun, H., C. H. Charles, L. F. Lau, and N. K. Tonks. 1993. MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75:487-493.
57. Taketomi, T., D. Yoshiga, K. Taniguchi, T. Kobayashi, A. Nonami, R. Kato, M. Sasaki, A. Sasaki, H. Ishibashi, M. Moriyama, K. I. Nakamura, J. Nishimura, and A. Yoshimura. 2005. Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia. Nat. Neurosci. 8:855-857.
58. Tefft, D., M. Lee, S. Smith, D. L. Crowe, S. Bellusci, and D. Warburton. 2002. mSprouty2 inhibits FGF10-activated MAP kinase by differentially binding to upstream target proteins. Am. J. Physiol. Lung Cell. Mol. Physiol. 283:L700-L706.
59. Tefft, J. D., M. Lee, S. Smith, M. Leinwand, J. Zhao, P. Bringas, Jr., D. L. Crowe, and D. Warburton. 1999. Conserved function of mSpry-2, a murine homolog of Drosophila sprouty, which negatively modulates respiratory organogenesis. Curr. Biol. 9:219-222.
60. Waskiewicz, A. J., A. Flynn, C. G. Proud, and J. A. Cooper. 1997. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J. 16:1909-1920.
61. Waskiewicz, A. J., J. C. Johnson, B. Penn, M. Mahalingam, S. R. Kimball, and J. A. Cooper. 1999. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol. Cell. Biol. 19:1871-1880.
62. Wassarman, D. A., N. M. Solomon, H. C. Chang, F. D. Karim, M. Therrien, and G. M. Rubin. 1996. Protein phosphatase 2A positively and negatively regulates Ras1-mediated photoreceptor development in Drosophila. Genes Dev. 10:272-278.
63. Wong, E. S., C. W. Fong, J. Lim, P. Yusoff, B. C. Low, W. Y. Langdon, and G. R. Guy. 2002. Sprouty2 attenuates epidermal growth factor receptor ubiquitylation and endocytosis, and consequently enhances Ras/ERK signalling. EMBO J. 21:4796-4808.
64. Yamamoto, H., S. Kishida, M. Kishida, S. Ikeda, S. Takada, and A. Kikuchi. 1999. Phosphorylation of axin, a Wnt signal negative regulator, by glycogen synthase kinase-3β regulates its stability. J. Biol. Chem. 274:10681-10684.
65. Yusoff, P., D. H. Lao, S. H. Ong, E. S. Wong, J. Lim, T. L. Lo, H. F. Leong, C. W. Fong, and G. R. Guy. 2002. Sprouty2 inhibits the Ras/MAP kinase pathway by inhibiting the activation of Raf. J. Biol. Chem. 277:3195-3201.
66. Zhang, S., Y. Lin, P. Itaranta, A. Yagi, and S. Vainio. 2001. Expression of Sprouty genes 1, 2 and 4 during mouse organogenesis. Mech. Dev. 109:367-370.